Freshwater Snails Of Africa And Their Medical Importance

Freshwater Snails of Africa and their Medical Importance

Second Edition

TO CHRISTOPHER WRIGHT who introduced me to Africa and its snails TO GEORG MANDAHL-BARTH for the pleasures of his friendship and conversation AND TO MY WIFE JULIA for loving encouragement

Freshwater Snails of Africa and their Medical Importance Second Edition

David S.Brown Department of Zoology, The Natural History Museum, London

UK Taylor & Francis Ltd, 4 John St, London WC1N 2ET USA Taylor & Francis Inc., 1900 Frost Road, Suite 101, Bristol PA 19007 Copyright © Taylor & Francis Ltd 1994 First edition 1980 This edition published in the Taylor & Francis e-Library, 2005. “To purchase your own copy of this or any of Taylor & Francis or Routledge’s collection of thousands of eBooks please go to www.eBookstore.tandf.co.uk.” All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, elec trostatic, magnetic tape, mechanical, photocopying, recording or otherwise, with out the prior permission of the copyright owner. British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN 0-203-48144-5 Master e-book ISBN

ISBN 0-203-78968-7 (Adobe eReader Format) ISBN 0 7484 0026 5 (Print Edition) Library of Congress Cataloguing in Publication Data are available Cover design by Amanda Barragry

Contents

Preface

vii

Acknowledgements

ix

Changes in place names and journal titles

xii

1.

Introduction

1

2.

Systematic synopsis: introduction, glossary, identification keys, checklist

7

3.

Systematic synopsis: Prosobranchs

43

Neritidae

43

Hydrocenidae

52

Viviparidae

53

Ampullariidae (Pilidae)

61

Valvatidae

75

Littorinidae

76

Hydrobiidae: Hydrobiinae Cochlipinae

77

Pomatiopsidae

84

Bithyniidae

90

4.

Assimineidae

102

Thiaridae

108

Melanopsidae

152

Systematic synopsis: Pulmonates

162

Ellobiidae

162

Acroloxidae

166

Lymnaeidae

166

vi

Ancylidae

171

Planorbidae:

185

Planorbinae

186

Bulininae

218

Physidae

261

5.

Snails and schistosomes

321

6.

Other snail-transmitted parasitic infections

361

7.

The biology of Bulinus

377

8.

Snail control

420

9.

Local snail faunas

454

10.

Chemical and physical factors

482

11.

Life cycles and populations

515

12.

Regions, lakes and rivers: biogeography

547

Appendix. Selected bibliography: identification and distribution

615

Index to snail names

621

Index to other organism names

639

Subject Index

642

Preface

This edition is extensively revised to take account of advances made since 1980. At first it seemed that new material could be inserted here and there in the text of the 1st Edition, but the outcome is an almost entirely rewritten book. During the last 14 years, new species have been described and changes have been made in classification; much new information has been published about the ecology and distribution of snails and their relationships with trematode parasites. The number of new references added probably exceeds the total cited in the 1st Edition. The arrangement of the book remains much the same; the major changes are the addition of a checklist of species and the replacement of the appendix about techniques by a bibliography of identification and snail distribution. A few years after the publication of the 1st Edition, malacologists and parasitologists suffered a deep shock and loss in the early death of Christopher Wright (1928–1983). To we his remaining colleagues it is a satisfaction that the research group founded by Chris continues to flourish as his memorial; it will soon have completed 40 years of contributing to knowledge of snails and schistosomes. Many people and institutions have contributed, directly or indirectly, to this book. Some are named, but probably not all who deserve to be, in the Acknowledgements below. Looking further back, I was attracted to the study of freshwater biology in the English midlands by the enthusiasm of H.P.Moon of Leicester University. From dissecting the heads of mayfly larvae, I moved in 1959 to unravelling the reproductive organs of planorbid snails, as a result of the Medical Research Council (MRC) seeking to strengthen expertise in the United Kingdom on the taxonomy of the snail hosts of schistosomes in Africa. The MRC sent me to join Chris Wright at the British Museum (Natural History), now named The Natural History Museum, where he was building up the research group that became the Experimental Taxonomy Unit. Here I benefited from the resources of a great museum and the stimulus of colleagues exploring new ways of characterizing species of snails and schistosomes. This laboratory has been my base ever since; its continuity has been invaluable in enabling me to make what I hope has been good use of extensive periods of fieldwork in Africa. It was many years before I began to feel any familiarity with the extensive literature on the freshwater snails of Africa and their parasites. I hope this book

viii

will make it easier for students to find their way. I would like to think too that specialists, whether in applied or academic fields of study, will share my enjoyment in attempting to take a broad view of the freshwater snail fauna of a large continent. David Brown London, January 1994

Acknowledgements

This book is the result of support, help and facilities given by many people and institutions. First I wish to offer my thanks for some outstanding contributions. I am fortunate to have been employed by the Medical Research Council, London, who have given me great freedom to develop my investigations. The Trustees of The Natural History Museum and the British Museum (Natural History) have provided me with working accommodation for 34 years; they have generously permitted the publication in this book of many illustrations. I thank Vaughan Southgate and my other colleagues in the Experimental Taxonomy Division for the daily privilege of a happy working environment. Peter Mordan and John Taylor have kindly allowed me a free run of the museum’s collection of shells. For visits to the hospitable Danish Bilharziasis Laboratory (DBL) during the last decade, I am grateful to Flemming Frandsen, Niels Ørnbjerg Christensen and Thomas Kristensen. To the founder and first director of the DBL, Georg MandahlBarth, I am deeply indebted for numerous visits and conversations and much correspondence, over a period of 30 years; without his friendship the systematic part of this book would probably not have been written. My wife Julia has been closely involved with both editions and I thank her for helping so efficiently with the many tasks that lie between the preparation of a typescript and the production of a book. Chapters and sections of this book have been criticized by the following: D.W.Taylor 4 (Physidae) and 12 (faunal origins), V.R.Southgate 5, D.Rollinson 7, C.C.Appleton 8, J.M.Jewsbury 8 and F.S.McCullough 8. These friends have corrected errors, pointed to things of value that might be included and suggested improvements to clarify the text. I am most grateful to them all. For omissions and mistakes that may remain I am entirely responsible. For accommodating me as a visiting worker in laboratories abroad, I thank the following: Aklilu Lemma (Institute of Pathobiology, University of Addis Ababa), B.A.Curtis (State Museum, Windhoek, Namibia), the late R.Elsdon-Dew (Institute for Parasitology, Durban, South Africa), G.K.Kinoti (Department of Zoology, University of Nairobi), G.Languillat (Centre International de Recherches Médicales de Franceville, Gabon), D.Matovu (East Africa Institute for Medical Research, Mwanza, Tanzania), K.R.McKaye (Fisheries Research Station, Cape Maclear, Malawi), R.J.Pitchford (Bilharzia Research Unit,

x

Nelspruit, South Africa), M.W.Prosser (Biology Department, University of Addis Ababa), S.Tillier (Muséum National d’Histoire Naturelle, Paris), A. Tjønneland (Biology Department, University of Addis Ababa), J.A.Van Eeden (Zoology Department, Potchefstroom University for C.H.E., South Africa). I am indebted to Simon Tillier for making available to me for study the large collection, mostly then unidentified, of the late G.Ranson (Muséum National d’Histoire Naturelle, Paris). To the many people who have worked with me in the field I owe a great debt for practical help and companionship. I hope that all whom I have met in this way will accept this grateful acknowledgement. I would like particularly to thank: Enos Angira, Richard Archer, Barbara Curtis, David Matovu, Gouws Oberholzer, Mick Prosser, Claudine Sarfati and Chris Teesdale. My gratitude is immense to all the people who have taken the trouble to send snails to me in London. Particularly large contributions have been made by: C.C.Appleton, C.Betterton, R.Bills, B.A.Curtis, K.M.Dogba, T.Fison, M.D.Gallagher, P.H.Goll, M.A.Grácio, W.N.Gray, B.Gryseels, R.B.Highton, J.Julvez, G.K.Kinoti, A.Lamboj, E.S.Loker, D.B.Matovu, F.Matthews, F.S. McCullough, F.Mouchet, G.T.Ndifon, P.Obrdlik, F.Starmühlner, C.H. Teesdale, D.J.Thomas and P.T.White. The photographs of shells reproduced in this book, except for Figs 108(a–d), 110(a) and 111b, are copyright The Natural History Museum and I am grateful for permission to use them here. For allowing me to use other copyrighted material, I thank the following: Academic Press Ltd, Fig. 148; Akademie Verlag, Fig. 111b; Annals of Tropical Medicine and Parasitology, Fig. 147; Blackwell Scientific Publications Ltd, Figs 138, 142; Climate Information, Department of Transport, Republic of South Africa, Fig. 146; Editions de l’Office de la Recherche Scientifique et Technique Outre-Mer, Figs 134, 136; Elsevier Science Publishers BV, Fig. 144(a,b); Journal of African Zoology (Revue de Zoologie Africaine), Fig. 141; Dr W.Junk Publishers, Fig. 32; Malacologia, Figs 108(a– d), 110(a), 129(a–f), 131, 139; Onderstepoort Journal of Veterinary Research, Figs 149, 150; Oxford University Press, Figs 85A, 109, 133; Potchefstroom University for C.H.E., Director of Library Services, Fig. 105; South African Journal of Science, Fig. 140; Taylor & Francis Ltd, Fig. 130; Transactions of the Royal Society of Tropical Medicine and Hygiene, Fig. 137; World Health Organisation, Figs 135, 143 and unpublished reports; Zoological Society of London, Figs 107, 108(e), 132. The base maps used to show distributions (Figs 69–74, 116–128, 151) are reproduced by kind permission of Goode Base Map Series, University of Chicago. I would like to express my thanks for the services of colleagues in The Natural History Museum, past and present. Donald Claugher was a perfectionist in making chromosome preparations and in scanning electron microscopy. Fred Naggs is a most helpful guide to the museum’s collection of freshwater shells. I greatly appreciate the careful work of successive photographers: Paul Richens,

xi

Phil Crabb and Harold Taylor. My assistant Neeta Perera has been of great help in searching the library and in checking reference lists. The manuscript benefited greatly from careful copyediting by Dr Ann Lackie.

Changes in place names and journal titles

Names of some countries, towns and lakes used in the literature have been changed in recent decades. Commonly encountered names so affected are listed here. Official recent name States Benin (Republic of) Botswana Burkino Faso Central African Republic Congo (Republic) Equatorial Guinea Ethiopia Ghana Guinea Guinea Bissau Lesotho Malagasy Republic Malawi Mali Namibia Tanzania (mainland) Yemen Arab Republic Yemen, People’s Republic Zaire Zambia Zimbabwe Towns Banjul

Past name, or other name in use Dahomey Bechuanaland Upper Volta Oubangui Chari (part of French Equatorial Africa) Brazzaville Congo (part of French Equatorial Africa) Spanish Guinea Abyssinia Gold Coast French Guinea Portuguese Guinea Basutoland Madagascar Nyasaland French Sudan South West Africa Tanganyika Yemen or North Yemen Democratic South Yemen or Aden Protectorate Belgian Congo (Leopoldville Congo) Northern Rhodesia Southern Rhodesia Bathurst

xiii

Official recent name Chipata Kabwe Kalemié Kinshasa Kisangani Likasi Lubumbashi Maputo Ndjamena Ubundi Lakes Abaya Mobuto Turkana

Past name, or other name in use Fort Jameson Broken Hill Albertville Leopoldville Stanleyville Jadotville Elizabethville Lourenço Marques Fort Lamy Ponthierville Margherita Albert Rudolf

Names of some long-established scientific journals cited in the reference lists in this book have been changed in recent years. Bulletin of Epizootic Diseases in Africa has become Bulletin of Animal Health and Production in Africa. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer (ORSTOM), série Hydrobiologie has become Revue d’Hydrobiologie tropicale. Proceedings of the Malacological Society of London has become Journal of Molluscan Studies. Revue de Zoologie Africaine is also known as Journal of African Zoology. Zeitschrift für Parasitenkunde has become Parasitology Research.

Chapter 1. Introduction

There are about 400 species of freshwater snail (including the limpets) in Africa. Most are known only to specialists, but some are all too familiar to residents and visitors alike, as the source of the ‘peril in the water’—the microscopic cercariae that produce the parasitic infection in man that causes the disease schistosomiasis (bilharzia). To find out more about the species of snail which are the intermediate hosts for schistosomes became a priority about 40 years ago, when the World Health Organisation and some national health authorities began to give serious consideration to the possibility of controlling schistosomiasis. The resulting financial support for malacological studies has advanced knowledge of many species besides those of medical or veterinary importance. Collectors have searched areas where the aquatic molluscan fauna was unknown. Whole animals have been obtained for the study of many species described by earlier taxonomists from only empty shells. Comparative morphology, and the use of biochemical and cytological characters in taxonomy, as well as growing knowledge of distribution and ecology, are all contributing to a better understanding of the species as biological units, and of their histories. Studies focused on the remarkable radiation of prosobranch snails in Lake Tanganyika are providing new insights into the processes of speciation within ancient lakes. The first edition of this book provided the first comprehensive review of freshwater snails for the whole of Africa. During the 14 years since its publication considerable advances have been made in all the main fields of study: taxonomy, ecology, distribution and snail-borne parasitic infections. The catalogue of species is incomplete, but the actual number may be less than 400 and thus is not large compared with some other kinds of invertebrate in Africa, e.g. landsnails and some insect groups. Because the number of species is moderate, it is possible in a volume of reasonable size to review them systematically, and also summarise their ecology, distribution and relationships with parasites. I hope therefore that this book will be useful to a variety of readers: taxonomists, medical malacologists, parasitologists, freshwater biologists in general and biogeographers—indeed all who are interested in the life of the great continent of Africa. Besides the African mainland including the Mediterranean region, this account covers islands in the Atlantic and Indian Oceans, among them the Cape

2 FRESHWATER SNAILS OF AFRICA

Verde Islands, Madagascar and the Mascarene group. Many endemic species and genera live in the tropical area: the fauna of northern Africa is very different, having species that occur also in parts of Europe, the Near East and South West Asia. A few species have been introduced, apparently by man in recent historical time. Africa south of the Sahara, together with Madagascar, was known to early biogeographers as the ‘Ethiopian Region’, but since the name Ethiopia was adopted by the territory formerly called Abyssinia, the replacement term ‘Afrotropical Region’ has come into use (Crosskey & White, 1977). Considerable areas of this region, however, do not experience a tropical climate, notably the highlands of eastern Africa and the temperate zone of South Africa. The Palaearctic Region includes North West Africa: it is not fully understood what factors, past or present, determine the southern limits of palaearctic species, and the northern limits of the afrotropical ones. There appears to be a formidable barrier in the Sahara Desert, but freshwater habitats were widespread in this region less than 10 000 years ago. Yet aquatic molluscs have made remarkably few movements through this apparently broad highway that was available between north and south. The slender thread of the Nile has been the main route taken by snails from tropical Africa to the Mediterranean coast. Since it is difficult to define ecological limits for the freshwater fauna, I include species of brackish/marine affinity which might be encountered in coastal streams, estuaries and lagoons, including the mangrove habitat. Africa has many saline inland waters, but these do not have a specialised snail fauna, except perhaps in North West Africa. Scientific study of African freshwater snails began nearly 250 years ago, in association with the penetration of the continent by European traders and explorers. Full justice cannot be done here to a story that needs a book to itself; our present knowledge owes much to men who suffered great hardships, ill health and risked their lives. Collectors in East Africa are the subjects of a continuing series of most interesting accounts published in The Conchologists’ Newsletter (Verdcourt, 1979–1993). Notable pioneers in this area and elsewhere include M.Adanson (1757; Senegal, 1749–53), F.Krauss (1848; South Africa, 1838–40), G.Tams (Angola, 1841–42; molluscs reported by Dunker, 1853), W.Peters (Mozambique and Zambezi valley, 1843–47; molluscs reported by Martens, 1860, 1879), F.Welwitsch (Angola, 1853–60; molluscs reported by Morelet, 1868), J.Speke (Lake Tanganyika and Lake Victoria, 1858 and 1859; molluscs reported by Woodward, 1859, and Dohrn, 1864), J.Kirk (Lake Nyasa, 1859; molluscs reported by Dohrn, 1865), C.F.Jickeli (1874; north east Africa, 1870–71). In these days of the package tour to game-parks it is startling to read Adanson’s account of his thoughts when setting sail from France in 1749: he would be, he reflected with pleasure, the first naturalist to visit tropical Africa. Then in his early twenties, Adanson spent four years moving from one trading post to another in Senegal, collecting all kinds of biological specimens and especially molluscs. In 1757 was published his Histoire naturelle du Sénégal, a volume devoted entirely to molluscs and now held to be the beginning of their

INTRODUCTION 3

scientific study (Fischer-Piette, 1942). Adanson described shells, anatomy and habitats; he used a binomial system of nomenclature, one year before Linnaeus introduced his own system. From fresh water he described ‘Le Coret’ (now Afrogyrus coretus) and ‘Le Bulin’ (now Bulinus senegalensis), which was to become the type of the genus Bulinus. Nearly 160 years later the discovery in Egypt of the life cycle of Schistosoma haematobium would make Bulinus one of the most intensively studied snails in the world. Unfortunately, some later authors did not share Adanson’s interest in anatomy as well as conchology. During the 19th century numerous species were hastily named according to trivial differences between shells, while important anatomical characteristics went unnoticed, partly because of a want of materials to dissect. Something of the political scramble for Africa can be seen in the promptness with which authors published names for ‘new shells’. A modern student bewildered by long lists of synonyms due to conchologists such as J.R. Bourguignat will be tempted to dismiss this activity as hopelessly unscientific. But some early writers were well aware of the limitations of their materials, often a few shells picked up hurriedly by travellers who were concerned above all with surviving their hazardous daily lives. Shells are still important in molluscan taxonomy, and a knowledge of conchology is usually necessary in order to identify a species, even though its systematic place may depend on the anatomy and bio-chemical properties of the animal within. The first scientific expeditions to study freshwater organisms in tropical Africa were sent by The Royal Society in 1895 and 1899 to Lake Tanganyika, partly to investigate the remarkable prosobranch snails brought to notice by shells that John Speke collected in 1858. But it was the discovery that Bulinus truncatus (=contortus) and Biomphalaria alexandrina (=Planorbis boissyi) are the intermediate hosts for the parasites causing human schistosomiasis in Egypt (Leiper, 1915, 1918), that led to the modern phase in the study of African freshwater snails. For some time though, authorities responsible for health in Africa were preoccupied with other diseases, especially malaria, and there was little progress in knowledge of the intermediate hosts of schistosomes. Nonetheless, professional and amateur malacologists were busy and two outstanding monographs appeared, both still indispensable today, describing the snails of the former Belgian Congo (Pilsbry & Bequaert, 1927) and South Africa (Connolly, 1939). After the 1939– 45 World War interest in African schistosomiasis increased through the influence of the World Health Organisation (Farooq, 1973); growing awareness of an urgent need for improved snail taxonomy led to the meeting in Paris in 1954 of the ‘Study Group on the Identification and Classification of the Bilharzia Snail Vectors (Equatorial and South Africa)’. There was growing interest too in the common parasites of livestock with snail intermediate hosts (schistosomes, amphistomes and liver flukes). Funds were made available by the WHO and national governments for malacological research, and substantial support continues to be given to investigations in the laboratory and the field. Increasing prevalence of

4 FRESHWATER SNAILS OF AFRICA

schistosomiasis continues to be a problem in human populations living nearby man-made lakes, dams and irrigation schemes (Hunter et al., 1993). Studies on snail taxonomy and distribution are major activities of the Experimental Taxonomy Division of The Natural History Museum, London (formerly the British Museum (Natural History)) and the Danish Bilharziasis Laboratory, Copenhagen. An outstanding national survey of snail distribution was carried out in the Republic of South Africa in the Institute for Zoological Research, Potchefstroom University. Today there are staff trained in malacological work in the universities and public health laboratories of many African countries. The first half of this book is mostly a systematic survey of the snails (Chapters 2–4), beginning with glossaries, keys for identification to genera and a checklist of species: there follows a synopsis of species, with brief notes on ecology, distribution and parasites. Relationships are then described between snails and schistosomes (Chapter 5) and with other parasites (Chapter 6). Because the degree of susceptibility to infection with schistosomes varies so greatly among species of Bulinus, from complete resistance to full compatibility, this genus has been much studied in order to improve the definitions of species, and to reach an understanding of variation within them. An account of the still developing species-concepts in Bulinus and a consideration of reasons for the success of this genus occupies Chapter 7. The objective of reducing transmission of schistosomiasis through reducing the numbers of snails has been the motive for many studies of snail ecology and distribution. Whether to rely on molluscicides for controlling snails, or to place more emphasis on non-chemical means (biological control and environmental modifications), has been thoroughly debated; measures that can be sustained by the local community seem to offer the best prospect for successful snail control in Africa (Chapter 8). Local surveys are the essential basis for understanding the ecology and distribution of snails on a larger scale: Chapter 9 describes selected snail faunas in areas of not more than a few hundred square kilometres, and consideration is given to some of the biotic factors that influence occurrence locally (aquatic vegetation, food supply and dispersal). Abiotic factors (physical and chemical) are reviewed in Chapter 10, with particular reference to distribution in the field and experiments in the laboratory. Physicochemical factors are discussed further in relation to growth, life cycles and population dynamics (Chapter 11). My attempt to present the African freshwater snail fauna in a continental perspective (Chapter 12) owes much in its arrangement to the late R.E.Moreau’s The Bird Faunas of Africa and its Islands (1966). By concentrating first on Mediterranean Africa and then southern Africa, we can look at the transition between the snail faunas of the Palaearctic and the Afrotropical regions, and then view the progressive subtraction of tropical species as they reach their various southern limits of penetration into the cooler southern tip of the continent. For other areas it seemed the most effective treatment was to analyse the snail assemblages found in the major lakes and river systems. The Appendix provides a selected bibliography of guides to the identification of freshwater snails and studies of distribution,

INTRODUCTION 5

arranged according to geographical region. In this edition I have not attempted to review methods of study, because of the wide variety of techniques in use, and the difficulty of giving an account of practical value in a limited number of pages. Technical information will be found in many of the references listed, especially in Chapters 5–11. There are good reasons for studying the freshwater snails of Africa, besides the objective of controlling snail-transmitted diseases. Snails are an important part of the freshwater ecosystems on which depend the inland fisheries that are a valuable source of human food. From the purely scientific point of view there is much of interest in the uniquely African events that have occurred in the evolution of many snail lineages. The strange and beautiful snails of Lake Tanganyika are one of the wonders of the living world: may enlightened governments in eastern Africa cooperate to preserve them for the interest and enjoyment of future generations of their people. The well-being of human societies in Africa depends much on conserving water and supplying uncontaminated water to people. Wherever living standards rise and the threat of schistosomiasis recedes, it may be that a rich snail fauna will come to be appreciated as a sign of healthy and sustainable aquatic ecosystems, on which the water supply depends. References Adanson, M. 1757. Histoire Naturelle du Sénégal. Coquillages. Paris. Connolly, M. 1939. A monographic survey of the South African non-marine Mollusca. Annals of the South African Museum, 33:1–660. Crosskey, R.W. & White, G.B. 1977. The Afrotropical Region. A recommended term in zoogeography. Journal of Natural History, 11:541–544. Dohrn, H. 1864. List of shells collected by Capt. Speke during his second journey through Central Africa. Proceedings of the Zoological Society of London, 1864:116–118. Dohrn, H. 1865. List of the land and freshwater shells of the Zambezi and Lake Nyasa, eastern tropical Africa, collected by John Kirk. Proceedings of the Zoological Society of London, 1865:231–234. Dunker, G. 1853. Index Molluscorum quae in Itinere ad Guineam Inferiorum Collegit Georgius Tams. Cassel. Farooq, M. 1973. Historical development. In Epidemiology and Control of Schistosomiasis (Bilharziasis): 1–14. Ansari, N. (Ed.). Basle: Karger. Fischer-Piette, E. 1942. Les mollusques d’Adanson. Journal de Conchyliologie, Paris, 85: 103–374. Hunter, J.M., Rey, L., Chu, K.Y., Adekolu-John, E.O. & Mott, K.E. 1933. Parasitic Diseases and Water Resources Development. Geneva: World Health Organisation. Jickeli, C.F. 1874. Fauna de Land- und Süsswasser Mollusken Nord-Ost-Afrikas. Nova Acta Academiae Caesareae Leopoldino-Carolinae, 37:1–352. Krauss, F. 1848. Die Südafrikanischen Mollusken. Stuttgart: Ebner & Seubert.

6 FRESHWATER SNAILS OF AFRICA

Leiper, R.T. 1915, 1918. Report on the results of the Bilharzia Mission in Egypt, 1915. 1. Transmission. 5. Adults and ova. Journal of the Royal Army Medical Corps, 25: 1–55 and 30:235–260. Martens, E. 1860. Verzeichniss der von Prof. Peters in Mossambique gesammelten Landund Süsswasser-Mollusken. Malakozoologische Blätter, 6:211–221. Martens, E. 1879. Ubersicht der von 1843 bis 1847 in Mossambique gesammelten Mollusca. Monatsberichte der Königlichen Preussischen Akademie der Wissenschaft zu Berlin, 44:727–749. Moreau, R.E. 1966. The Bird Fauna of Africa and its Islands. London and New York: Academic Press. Morelet, A. 1868. Mollusques terrestres et fluviatiles. Voyage du Dr Friedrich Welwitsch. Paris: Ballière. Pilsbry, H.A. & Bequaert, J. 1927. The aquatic mollusks of the Belgian Congo, with a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History, 53:69–602. Verdcourt, B. 1979–93. Collectors in East Africa, Nos 1–18. The Conchologists’ Newsletter (of the Conchological Society of Great Britain and Ireland), 69–124. Woodward, S.P. 1859. On some new freshwater shells from Central Africa. Proceedings of the Zoological Society of London, 1859:348–349.

Chapter 2. Systematic Synopsis: Introduction, Glossary, Identification Keys, Checklist

The synopsis of species to be presented in Chapters 3 and 4 covers Africa, Madagascar and the Mascarene Islands, and includes snails likely to be found in moderately saline coastal habitats such as mangrove swamp. Two families are dominant (Table 2.1), the Thiaridae and the Planorbidae, which together contribute about half of the totals for both genera and species. Few species found in tropical Africa occur also north of the Sahara Desert, and likewise few species of the Mediterranean region extend southwards into the tropics. Faunal composition and biogeography are discussed in Chapter 12; here the contributions of the different families are briefly summarised. Prosobranchs are most varied in the larger lakes and rivers. Neritidae scarcely penetrate the inland waters of Africa apart from the lower Nile and streams in North West Africa. Viviparidae live usually in lakes and rivers; African species belong to either Bellamya or Neothauma, which is confined to Lake Tanganyika. Ampullariids are successful in seasonally flooded habitats, being able to breathe air, while Lanistes also has species adapted to fast-flowing streams and benthic life in Lake Malawi. Many species classified in the Hydrobiidae occur in northern Africa, particularly in the Maghreb area, but the hydrobiid fauna known from the tropical region is comparatively poor. The Pomatiopsidae is represented by a small group of species concentrated in the coastal regions of southern Africa. There is one widespread genus of the Bithyniidae, Gabbiella, which in habitats ranges from rainpools to large lakes; some specialised bithyniids are restricted to rapidly flowing rivers in western Africa. Assimineids are scarce in African inland waters; the few strictly freshwater species are associated with springs in eastern Africa and with rapids of the lower Zaire River. The Thiaridae is well represented in fresh and brackish waters; Melanoides and Cleopatra occur almost throughout tropical Africa. Many thiarids are restricted to the Zaire Basin or to a particular lake, especially Tanganyika (Chapter 12), while Potadoma is characteristic of streams in western forests (Melanatria occupies this niche in Madagascar). Although the Melanopsidae is widespread in the Mediterranean area it is absent from the Nile and further south. The Potamididae is confined to brackish water. Of the pulmonates, ellobiids are confined to brackish coastal waters, while the strictly freshwater groups are most abundant in the smaller waterbodies,

8 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

including seasonal rainpools. Although Lymnaea natalensis is the most widely distributed freshwater snail in Africa, the number of lymnaeid species in the Afrotropical region is surprisingly few. Ancylids occur in most kinds of habitat; clean well-oxygenated waters are suitable for Ancylus (in N Africa) and Burnupia (E and S Africa), while Ferrissia thrives in stagnant conditions. The Planorbidae is well represented in temporary waters, where Bulinus survives in dry mud for Table 2.1. Composition of the gastropod fauna of the fresh and brackish waters of the African continent (according to the checklist at the end of this chapter, and likewise excluding the Hydrobiidae of northern Africa). For each family the number of genera is followed in brackets by the number of species, which is approximate for some genera. Introduced species are included. Prosobranchs Neritidae Viviparidae Ampullariidae Valvatidae Littorinidae Hydrobiidae (tropical region only) Pomatiopsidae Bithyniidae Assimineidae Thiaridae: non-thalassoid thalassoid (of Lake Tanganyika) Melanopsidae Potamididae Total prosobranchs Pulmonates Ellobiidae Lymnaeidae Ancylidae Planorbidae: Planorbinae Bulininae Physidae Total pulmonates Overall totals

4 2 5 1 1 3 1 9 5

(17) (19) (28) (1) (2 plus) (13) (10) (35) (11)

6 17 1 4 59

(78) (31 plus) (1) (4) (250 approximately)

5 1 3

(7 plus) (6) (5 plus)

11 2 2 24 83

(40) (31) (2) (91 approximately) (341 approximately)

many months (Chapters 7, 10). Biomphalaria is rather less successful in seasonal pools and perhaps for this reason is not so well established in the drier parts of

FRESHWATER SNAILS OF AFRICA 9

northern Africa. Few species of Physidae occur in Africa and perhaps all were introduced following European settlement. The introduction by man of exotic freshwater snails into Africa (see Chapter 12) seems to have begun with physids in the nineteenth century and has resulted in the appearance of Lymnaea columella, Helisoma, Amerianna and Indoplanorbis. Deliberate introductions have been made of Helisoma and Marisa for the attempted biological control of snail hosts for schistosomes (Chapter 8). Organisation of systematic synopsis Information is given under species-headings about taxonomy, habitat and ecology, distribution and parasites. Ecology and distribution are considered more fully in Chapters 9–12, and parasites in Chapters 5 and 6. The species are mostly recognisable from the shell; for a few their identification may depend on examination of the radula and soft organs. Cytological and molecular data are available for only a few genera. As knowledge of genetic relationships increases and morphological comparisons are made in more detail, taxonomic changes will be likely. At present evolutionary relationships within the larger families are not clear enough for genera and species to be arranged in a phylogenetic manner with any confidence; use will be made here of geographical distribution and sometimes simply alphabetical order. Taxonomy A type locality given by the original author of a species may be supplemented here by information in brackets. The terms holotype, paratype and syntype are used as defined in the Glossary: General. Commonly used synonyms are mentioned and references are given to publications useful for exploring the taxonomic history of a species; the single most valuable compilation of names is that of Pilsbry & Bequaert (1927), which covers an area far larger than the Congo Basin. Characterisation of species The size given is of a fully grown shell (see Glossary: Shell), but not necessarily the largest known; populations may be found where the maximum is unusually large or small. Attention should be given to scales of magnification in the figures as they may vary within a group. Outstanding characteristics are described as briefly as practicable, with emphasis on the shell and gross anatomical parts wherever possible. References are given also to biochemical and cytological data of current or potential taxonomic application. The institution where particular material is stored may be indicated by an abbreviation listed below.

10 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Habitat and ecology Reference is made to observations in the field and also to studies of ecological factors in the laboratory. Distribution Geographical ranges when extensive are summarised and details may be found in the legends to the distribution maps grouped at the ends of Chapters 3 and 4. Parasites Summaries are given of the medical and veterinary importance of a snail as known from the natural transmission of parasites and of responses to experimental infection in the laboratory. Abbreviations and symbols BMNH BME DBL MNHN E N NW S SE SW ‰ < > ● ○

The Natural History Museum, London: Mollusca Collection. Formerly the British Museum (Natural History). Experimental Taxonomy Division of the Department of Zoology, The Natural History Museum. Danish Bilharziasis Laboratory. Muséum National d’Histoire Naturelle, Paris. East, eastern. North, northern. North-West, north-western. South, southern. South-East, south-eastern. South-West, south-western. Total concentration of dissolved salts (salinity) as parts per thousand. Smaller than. Larger than. A locality for a living population or one believed to have been alive when found. A locality for ‘sub-fossil’ shells, usually of Late PleistoceneHolocene age.

FRESHWATER SNAILS OF AFRICA 11

Glossary (General, Shell, Operculum, Radula) Extensive glossaries of malacological terms are given by Malek (1985) and Burch (1985) and include anatomical terms for which there is not space here. Lincoln et al. (1982) provide a comprehensive dictionary of systematic, ecological and biogeographical terms. General terms allopatric Used of species occupying different geographical areas. Arabia Used here of the Arabian Peninsula southwards from the northern border of Saudi Arabia. Basommatophora A group of pulmonates, possessing one pair of tentacles with eyes at their bases. East Africa Kenya, Uganda and Tanzania. form A minor variant or subset of a species; a morph. holotype The single specimen indicated as the type of a named species by the original author or the single specimen when no type was specified but only one was available. Mascarene islands Mauritius, Réunion and Rodrigues. morph See form. Near East Used here for the area comprising Iraq, Israel, Jordan, Lebanon, Palestine and Syria. North West Africa Morocco, Algeria and Tunisia. paratype Any type specimen there may be additional to the holotype. Prosobranchia, prosobranch A major group of streptoneuran Gastropoda, with gills (branchia or ctenidia) situated in the mantle cavity and anterior to the heart; usually with an operculum. pseudobranch A gill-like respiratory organ developed in some aquatic pulmonates. Pulmonata, pulmonate A major group of euthyneuran Gastropoda, with the mantle cavity serving as a lung; usually lacking an operculum. sympatric Used of species occurring together in the same geographical area. syntype Any of two or more type specimens when a holotype is not established. taxon A taxonomic group of any rank, considered to be sufficiently distinct to be treated as a separate unit. type(s), type specimen(s) Used as neutral terms for specimens without asserting their precise status in taxonomy. type locality The locality of origin for the type(s) of a species. type species The species designated as the type of a genus or subgenus. West Africa The area south of the Sahara and extending westwards from the Cameroon/Nigeria border.

12 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Shell angular Used of the shell surface when it forms an angle rather than an evenly curved contour. aperture The opening or ‘mouth’ of the shell (surrounded by the lip or peristome). apex The tip of the spire. base The part of the shell furthest from the apex. body whorl The last complete whorl of a spired shell. calcareous, calcified Composed of calcium carbonate; of white or chalky appearance. callus A layer of calcareous material; often deposited on the columella and nearby surface (Figs 1a,d). cap-like The limpet form; a shell with little or no coiling, e.g. Ancylidae. carina (plural: carinae) A conspicuous spiral ridge running along an angular contour, like the keel of a boat (Fig. 2b). columella The internal column around which the whorls turn; the axis of a spiral shell, solid or with a cavity that may be open below forming the ‘umbilicus’. columellar Used of those parts of the lip and inner margin of the aperture that lie near the columella; a columellar plate is a well-defined layer of callus (Figs 1a–d, 4b,e). conic, conical Shaped like a cone, tapering from a wide circular base to a point. decollate Used of a shell when the upper whorls are normally detached (Figs 3c, 6f). depressed Used of shells broader than high; spire short (Fig. 3d). dextral Used of a spired shell having its aperture on the observer’s right side when the spire points upwards (Fig. 2a). diameter Maximum distance across a discoid shell. discoid Coiled horizontally, round and flat (Fig. 11b). embryonic whorl See protoconch. fusiform Used of a shell with its sides slightly curved, tapered at both ends (Figs 10a, 49a). globose Used of a shell when its height and width are about equal (Fig. 27c). globosely conic Used of a shell when the height is about 1.20 times the width (Fig. 3e). growth lines or ridges Fine lines on the surface, parallel to the lip, indicating brief phases of growth. height For spired shells the greatest distance between the apex and the base (also termed the length). For discoid shells the height may be measured of the last whorl at the lip. For a cap-like (ancylid) shell the vertical distance between the summit and the base. imperforate Lacking an umbilical opening. inner lip That part of the apertural lip in the columellar-parietal region. lamella (plural: lamellae) See septum.

FRESHWATER SNAILS OF AFRICA 13

length See height. limpet See cap-like. lip The outermost edge of the last whorl surrounding the aperture. malleated Used of a surface when small areas are flattened. microsculpture Fine surface structure seen under magnification. narrowly conic Used of slender spired shells; height about 3 times width (Fig. 6d). neritoid, neritiform Used of shells with a greatly expanded last whorl and of the shape common in the Neritidae (Figs 1a,d). nodule A small rounded projection from the shell surface; described as nodular if many are present. nuclear whorl See protoconch. outer lip That part of the lip opposite to the columellar-parietal region. ovate Egg-shaped in outline; one end narrower than the other. ovately conic Used of spiral shells when the height is about 1.5 times the width (Fig. 5a). parietal Used of the area between the upper attachment of the outer lip and the columella. perforate Used of a spired shell with a narrow umbilical opening. periostracum Thin outer layer of proteinaceous material covering the shell. periphery The outermost edge of a whorl seen in outline. peristome The entire apertural lip. plate see columellar. protoconch The shell formed by a young snail within the egg capsule. punctae Small pits; punctate microsculpture. radial Used of sculptural elements diverging from the apex of a cap-like shell. reflected Used of the apertural lip when it is turned outwards, e.g. the columellar lip reflected over the umbilical area. ribs Conspicuous regularly-spaced transverse ridges. rimate Used of a shell with a narrow, slit-like umbilical opening. sculpture Surface structures; raised (e.g. ribs, nodules) or sunken (e.g. punctae). septum (plural: septa) Elongate projection from the internal shell wall. shoulder A blunt angle in a whorl near the suture. sinistral Used of a spired shell with its aperture on the observer’s left side when the spire points upwards (Fig. 3b). sinuous Used of the outer lip when its margin is wavy (Figs 4a,c). size Measurements given in the text for coiled shells are height followed by width (diameter). For cap-like shells, the dimensions are length and width of the base, followed by height. small: greatest dimension less than 10 mm. medium: greatest dimension 10–30 mm. large: greatest dimension more than 30 mm. spiral Running along the whorl in the direction of growth.

14 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

spire That part of a spired shell rising above the upper attachment of the lip. stepped Used of a spired shell with a succession of shouldered whorls. striae, striation Fine lines on the surface, raised or incised. subfossil Used of shells which are not old enough to be fossilised but come from extinct populations of Late Pleistocene-Holocene age; e.g. in the Saharan area. suture The line of attachment between two whorls. transverse At a right angle to the direction of growth, i.e. parallel to the lip. tubercle A conspicuous blunt projection from the surface. turreted Used of a slender high-spired shell. umbilicate Used of coiled shells with an opening, the ‘umbilicus’, at the base, formed when the inner sides of the coiled whorls do not join (see also perforate). In a discoid shell the umbilicus and underside are taken here to be beneath when the aperture is facing the observer on their righthand side (Figs 11b–d; see also the account of Planorbidae). whorl One complete turn or coil of a spiral shell. width The maximum distance across the shell at a right angle to its height. Operculum apophysis (plural: apophyses) A projection from the internal surface (Figs 8a–d, 15). calcareous, calcified Made partly of calcium carbonate; hard, inflexible, opaque. concentric Growing in a series of zones with the same centre (Fig. 8e). corneous Made partly or entirely of ‘horn-like’ proteinaceous material; flexible and translucent. multispiral Growing spirally with many whorls (more than 3) (Fig. 8g). nucleus The earliest formed part of the operculum. paucispiral Growing spirally with few whorls (up to about 3) (Fig. 9c). subspiral Growing in increments which follow the beginning of a spiral path but turn through less than 180 degrees. Radula basal lobe A projection from the posterior margin on the basal plate of the central tooth (Figs 36c–g). cusps Small pointed cutting blades situated either on the crown of a tooth or below on the basal plate (basal cusps or denticles). central tooth The middle (median or rachidian) tooth in a transverse row. denticles One or more pairs of cusps on the basal plate of the central tooth (Figs 36c–g). ectocone The cusp on the outer (lateral) side of the mesocone. endocone The cusp on the inner (median) side of the mesocone.

FRESHWATER SNAILS OF AFRICA 15

lateral teeth Teeth lying between the central and marginal teeth; there is only a single lateral tooth on each side in the prosobranch taenioglossate radula (Figs 44, 52e), but many in the pulmonate radula. marginal teeth Teeth at the lateral margins of the radula, differing in shape from the central and lateral teeth; there are only two marginal teeth on each side in the taenioglossate radula (Figs 44, 52e), but many in the pulmonate radula. mesocone The middle of the 3 major cusps on the inner lateral teeth of the pulmonate radula (Fig. 105). rhipidoglossate The type of prosobranch radula with many teeth in each transverse row, though only few are conspicuous. taenioglossate The type of prosobranch radula with only 7 teeth in each transverse row: central, one pair lateral and 2 pairs marginals (Figs 44, 52e). Identification keys Keys are given here for identification to family and genus; a series of regional keys for identification to species is published by the Danish Bilharziasis Laboratory (e.g. Brown & Kristensen, 1989). Freshwater snails from our geographical area found with an operculum attached can be identified immediately as members of the subclass Streptoneura (commonly known as prosobranchs); only a single African prosobranch is reported to lack an operculum (Septariellina of the Assimineidae, restricted to the lower Zaire River). All other species lacking an operculum belong to the Pulmonata within the subclass Euthyneura. But the operculum though normally present may be small and inconspicuous (e.g. Septaria of the Neritidae and Soapitia of the Bithyniidae) or deeply withdrawn into the aperture, or it may have been lost from a preserved specimen. Yet whether or not the true condition regarding the operculum is known, the student will soon learn to recognise the limited number of aquatic pulmonate families. An occasional problem may be a landsnail fallen into the water; some are discoid (Fig. 97a) and misleadingly like the Planorbidae (Verdcourt, 1958). The mainly terrestrial family Succineidae includes some species that live on emergent aquatic plants and may turn up in the collecting net; their shells resemble certain lymnaeids, but the tentacles are very different (Figs 12a,b; Key to pulmonate families). Marine shells have sometimes been mistaken for a freshwater species (Brondelia Bourguignat, 1862 and Ancylus turtoni Connolly, 1939), while Afrocanidea of Connolly (1929) was thought to be estuarine but has not been re-discovered in brackish or fresh water. The first key is designed to identify shells as prosobranch or pulmonate using only characters of the empty shell. In later keys to families and genera, use becomes necessary of the operculum, radula and soft organs. Unfortunately there is not space in this book to describe anatomy sufficiently; sources of information include Mandahl-Barth (1958), Brown (1965), Starmühlner, (1969), MeierBrook (1983) and Malek (1985). These simple rules are helpful:

16 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

the only sinistral prosobranch is Lanistes, all strongly sculptured shells are prosobranch, all large shells over 30 mm in height or width are prosobranch, discoid shells are pulmonate except for Marisa (Ampullariidae) and Hadziella (Hydrobiidae). Key to the main gastropod groups: prosobranchs and pulmonates 1 A B 2 A B C 3 A

4

5 6

7

With operculum ................................................................prosobranch Lacking operculum or condition not known ......................................2 Shell cap-like ......................................................................................3 Shell discoid .......................................................................................4 Shell with pointed spire .....................................................................5 Large (reaching over 20 mm); Indo-Pacific coasts ................................ .... .....................................................................Septaria (prosobranch)

B Small (<10 mm long), apex coiled; rapids of lower Zaire River ......... ........ ..........................................................Septariellina (prosobranch) C Small (<10 mm long), apex may be hooked but not coiled; widespread in fresh waters ..........................................ANCYLIDAE (pulmonate) A Large (reaching 50 mm diameter), with light and dark spiral bands; introduced into Sudan ........................................Marisa (prosobranch) B Smaller (rarely 25 mm, usually <10mm) ............................................ ....... .......................PLANORBINAE and Indoplanorbis (pulmonate) A Sinistral ...............................................................................................6 B Dextral ................................................................................................7 A Shell larger (commonly >25 mm high or wide), strongly built, may have spiral bands ..............................................Lanistes (prosobranch) B Smaller (rarely reaching 25 mm high), fragile, without spiral bands. ......... .......................Amerianna, Bulinus, PHYSIDAE (pulmonate) A Shell with lamellae projecting from the inner wall of the aperture; in coastal brackish water. ..............................ELLOBIIDAE (pulmonate) B Shell with sharply pointed spire, thin-walled, smooth, pale-coloured and lacking bands or other pigmented marks ..................................... ........ .......................................................LYMNAEIDAE (pulmonate) C Shell of varied shape from depressed to narrowly conic; often thickwalled, smooth or strongly sculptured; may have pigmented patterns. ...... .............................................................Prosobranch (many genera)

Prosobranch families (excluding Thiaridae endemic to Lake Tanganyika and the discoid Marisa)

FRESHWATER SNAILS OF AFRICA 17

1 A Shell cap-like ....................................................................................2 B Shell not cap-like ..............................................................................3 2 A Large (reaching over 20 mm long); Indo-Pacific coasts ...................... ...... .......................................................NERITIDAE part (Septaria) B Small (<10 mm long), apex coiled; in rapids of the lower Zaire River. ....... ........................................ASSIMINEIDAE part (Septariellina) 3 A Whorls few and rapidly increasing, spire low, aperture ‘D-shaped’ (Figs 1a–d,f); operculum strongly calcified, with one or two internal apophyses (Figs 8a–d). In tropical Africa restricted to coastal areas .. ........ ..............................................................................NERITIDAE B Whorls generally more numerous, spire higher and more conical; operculum calcareous or entirely corneous, without apophyses ........4 4 A Shell globose, up to about 10 mm high; with pigmented markings, bands or entirely dark. Neritoid snails found only in rapidly flowing rivers in Sierra Leone ......................BITHYNIIDAE part (Sierraia) B Shell variously shaped, small to large ...............................................5 5 A Shell ovately conic, smooth reaching about 15 mm high; operculum calcified. In NW Africa only ........BITHYNIIDAE part (Bithynia) B Shell variously shaped, small to large ...............................................6 6 A Shell more than 10 mm high (Figs 2,3,6,7). Central radular tooth without basal denticles (Figs 36a,b; 52) ...........................................7 B Shell <10mm high (Figs 4,5). Central tooth with or without basal denticles (Figs 36c–g; 44) ..............................................................12 7

A Operculum entirely concentric (Figs 8e,f) ........................................8 B Operculum partly concentric with spiral nucleus (e.g. Figs 9a,b) or wholly spiral (Figs 8g; 9c,d,f) ..........................................................9 8 A Shell dextral with conical spire (Fig. 2); Operculum entirely corneous; viviparous .................................................................VIVIPA RIDAE B Dextral or sinistral, depressed to ovate, may be very large (Fig. 3); operculum corneous or calcified; oviparous ......................................... .. .....................................................AMPULLARIIDAE (PILIDAE) 9 A Basal margin of aperture with a notch (Figs 6a; 7a–c) ..................10 B Basal lip without notch ..................................................................11 10 A Operculum multispiral. Restricted to brackish water, usually at the coast .......................................................................POTAMIDIDAE B Operculum paucispiral. Found only in the NW part of Africa ......... ......... ....................................................................MELANOPSIDAE 11 A Spire conical, sharply pointed; rather smooth apart from spiral grooves; pigmented markings may form transverse bands (Fig. 7d). Operculum multispiral. Restricted to coasts, found in mangrove

18 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

B

12 A

B 13 A B 14 A B 15 A B

swamp ............. ...............................................................................LITT ORINIDAE Shell variously shaped, smooth or with strong sculpture (Fig. 6); any dark pattern is spiral rather than transverse. Operculum paucispiral (Figs 9d,f) or concentric with spiral nucleus (Figs 9g,h). In fresh and brackish water ..............................................................THIARIDAE Shell depressed, smooth, aperture circular, umbilicus large. Operculum multispiral (Fig. 8g). Found living only in Egypt and Ethiopia ....... ..................................................................................VAL VATIDAE Commonly ovately conic (Figs 4a,c,f; 5a); if depressed then with notch in lip (Fig. 4d) or spiral ridges (Fig. 5d) ....................................... 13 Operculum calcareous, concentric around a spiral nucleus ................. .... ..........................................BITHYNIIDAE part (e.g. Gabbiella) Operculum entirely corneous ..........................................................14 Operculum small, lacking spiral structure. Found only in river in Guinea ............................................BITHYNIIDAE part (Soapitia) Operculum paucispiral (Fig. 9c) .....................................................15 Radula with accessory plate between the lateral tooth and first marginal tooth (Fig. 44) ..............................................ASSIMINEIDAE Radula without accessory plate ........................................................... .... ..................................HYDROBIIDAE and POMATIOPSIDAE

Prosobranch genera of Africa within families (excluding Thiaridae endemic to Lake Tanganyika) Family NERITIDAE

1 A Shell cap-like (Fig. 1e). Operculum rectangular (Fig. 8a). SE Africa and Indo-Pacific islands .....................................................Septaria (p. 43) B Shell hemispherical. Operculum approximately oval (Fig. 8c) ...........2 2 A Fully grown shell less than 4 mm high (Fig. 1f). Operculum with a single apophysis (Fig. 8b). West Africa and Indo-Pacific islands ................... ..... ..............................................................................Neritilia (p. 45) B Fully grown shell exceeding 6 mm high. Operculum may have rib and peg (Figs 8c,d) ...................................................................................3 3 A Fully grown shell less than 10mm high. NW Africa and Egypt ....... ........... .....................................................................Theodoxus (p. 36) B Fully grown shell commonly more than 10 mm high. Tropical Africa ....... ....................................................................................................4

FRESHWATER SNAILS OF AFRICA 19

Fig. 1. Neritidae. (a) Neritina pulligera (two views), (b) N. oweniana. (c) N. glabrata. (d) N. natalensis. (e) Septaria borbonica (two views), (f) Neritilia manoeli. Scale line: 5 mm (f) or 10 mm (a–e). A guide line indicates the layer of callus on the columellar plate.

4 A Operculum with a low ridge connecting the rib and peg (Fig. 8c). No spines on the shell, which may have wing-like expansions of its aperture (Fig. 1b). Tropical coasts ...........................................Neritina (p. 39) B Operculum with a comparatively high ridge between rib and peg (Fig. 8d). Some species have spines on the shell. Indo-Pacific islands, but not known to occur in Africa .............................................Clithon (p. 43) Family VIVIPARIDAE A Apex sharply pointed and embryonic whorl with spiral ridges (Figs 2a– c). Fully grown shell reaching 50 mm in only one species. Widely distributed, but not known to occur in Lake Tanganyika ................... ................................. .................................................Bellamya (p. 46) B Apex obtuse with smooth embryonic whorl (Fig. 2d). Fully grown shell about 60 mm high. Lives only in Lake Tanganyika ............................ ............. .................................................................Neothauma (p. 53) Family AMPULLARIIDAE (PILIDAE) (see also the discoid Marisa)

20 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Fig. 2. Viviparidae. (a) Bellamya unicolor. (b) B. trochlearis. (c) B. unicolor, apex of juvenile, (d) Neothauma tanganyicense, apex of juvenile. Scale line: 1 mm (c,d) or 10 mm (a,b).

1 A Shell sinistral (Fig. 3b). Operculum entirely corneous Lanistes (p. 57) B Shell dextral. Operculum either corneous or calcareous .....................2 2 A Shell with transverse brown bands (Fig. 3a). Sierra Leone ................... ..... .................................................................................Saulea (p. 66) B Any coloured bands present are spiral ................................................3 3 A Fully grown shell exceeding 40 mm high (Fig. 3e). Operculum calcareous. Rare individuals are sinistral ....................................Pila (p. 54) B Fully grown shell less than 30 mm high (Fig. 3c). Operculum wholly corneous. Sierra Leone and Ivory Coast ..................Afropomus (p. 66) Family HYDROBIIDAE (excluding North Africa) and POMATIOPSIDAE 1 A Outer lip of aperture strongly sinuous, columellar margin heavily thickened (Fig. 4a). SE Zaire and Zambia .......................Lobogenes (p. 74) B Outer lip of aperture nearly straight. Mostly living near coasts ........2 2 A Shell with stout spines. West coast, in brackish water ....................... ........ ..................................................................Potamopyrgus (p. 74) B Shell without spines ...........................................................................3

FRESHWATER SNAILS OF AFRICA 21

Fig. 3. Pilidae. (a) Saulea vitrea. (b) Lanistes purpureus. (c) Afropomus balanoidea. (d) Lanistes carinatus. (e) Pila ovata. Scale line: 10 mm.

3 A Shell varies from depressed to narrowly conical (Figs 32, 33). Central tooth with one basal denticle on each side. West coast, in brackish or fresh waters ...............................................................Hydrobia (p. 70) B Spire ovately to narrowly conic (Figs 37–39). Central tooth (Fig. 36d) with 2 or 3 pairs of basal denticles. In fresh or brackish water near South African coast; also in E Zaire .................................................... ...... .................................................Pomatiopsidae: Tomichia (p. 77) Family BITHYNIIDAE 1 A Neritoid (globose, whorls rapidly increasing, spire low); shell may have pigmented pattern. Operculum nucleus is subspiral. Central tooth without basal denticles. Found only in rivers in Sierra Leone and Guinea. ..................................................................................................... ......2

22 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

B Shell of various other shapes; operculum with definite spiral nucleus; central tooth with basal denticles ......................................................3 2 A Shell may reach 10 mm high; usually with pigmented patches or bands, or evenly dark. Found only in Sierra Leone ...............Sierraia (p. 91) B Reaching only 6 mm high, lip oblique (Fig. 4b). Operculum very small and weakly calcified. Found only in Guinea ..............Soapitia (p. 94) 3 A Shell ovately conic, reaching 15 mm. Found in only the NW part of Africa .........................................................................Bithynia (p. 82) B Smaller (<10 mm); depressed to ovately conic and narrower. In tropical Africa and Egypt .......................................................................... ......4 4 A Shell depressed, very small (<2 mm high), with notch in the basal lip (Fig. 4d). Found only in or near the lower Zaire River ...................... ......... .......................................................................Funduella (p. 91) B Ovate with conical spire; lip without notch. .....................................5

FRESHWATER SNAILS OF AFRICA 23

Fig. 4. Hydrobiidae and Bithyniidae. (a) Lobogenes pusilla. (b) Soapitia dageti (two views), (c) Congodoma zairensis. (d) Funduella incisa (two views), (e) Liminitesta sulcata. (f) Jubaia excentrica. Scale line: 1 mm (a,c,d) or 2 mm (b,e,f).

5 A With strong spiral sculpture and a ridge in the base of the aperture (Fig. 4e) against which the operculum lodges. Found only in the lower Zaire River ............................................................Liminitesta (p. 91) B Shell smooth to the naked eye ...........................................................6 6 A Lip strongly sinuous (Fig. 4c). Found only in the lower Zaire River.. ......... ......................................................................Congodoma (p. 91) B Lip more straight (Fig. 4f). Various habitats including lakes and small pools ...................................................................................................7 7 A Operculum with thin corneous margin (Fig. 9e) and capable of retraction deep within the aperture. Central tooth with only one basal denticle on each side. NE Kenya .................................Incertihydrobia (p. 90) B Operculum calcareous right to its thick margin (Fig. 9b), lodging at or near the apertural lip. Central tooth with 2–5 pairs of basal denticles. ........ ...................................................................................................8

24 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Fig. 5. Assimineidae. (a) Eussoia inopina. (b) Pseudogibbula duponti. (c) Septariellina congolensis. (d) Valvatorbis mauritii. Scale lines: 1 mm (d) or 2 mm (a–c).

8 A Spiral nucleus of operculum central (Fig. 9b). Central tooth with 2–5 pairs of basal denticles. Egypt and tropical Africa ..Gabbiella (p. 82) B Spiral nucleus of operculum nearer the outer margin (Fig. 9a). Central tooth with only 2 pairs of basal denticles. S Somalia and SE Ethiopia. ....... ...............................................................................Jubaia (p. 90) Family ASSIMINEIDAE 1 A Shell ovately conic (Fig. 5a); in fresh or brackish water, usually near coast. ...................................................................................................2 B Shell globose, depressed or cap-like (Figs 5b,c,d); found only in rapids of the lower Zaire River. ....................................................................3 2 A Central tooth with strong basal lobe. Tentacles reduced to short lobes. In brackish water. ....................................................Assiminea (p. 95) B Central tooth with weaker basal lobe; outer marginal tooth with more cusps (Fig. 44). Tentacles longer. In fresh water ........Eussoia (p. 97) 3 A Shell globose with strong spiral ridges (Fig. 5b). Pseudogibbula (p. 98) B Shell depressed or cap-like .................................................................4 4 A Cap-like (Fig. 5c) ................................................Septariellina (p. 99) B Depressed, very small, carinate with spiral ridges. Valvatorbis (p. 99)

FRESHWATER SNAILS OF AFRICA 25

Fig. 6. Thiaridae. (a) Melanopsis praemorsa. (b) Cleopatra ferruginea. (c) Pseudocleopatra bennikei. (d) Melanoides tuberculata. (e) Potadoma freethi. (f) Pachymelania fusca. (g) Thiara amarula. (h) T. scabra. Scale line: 10 mm.

Family THIARIDAE (excluding genera restricted to Lake Tanganyika) 1 A Base of apertural lip narrowed and spout-like (Fig. 6f); sculpture strong. W coast, in brackish water .............................Pachymelania (p. 111) B Basal lip more evenly curved; sculptured to a varying degree or smooth. In fresh water ............................................................................... ......2 2 A Shell with transverse ribs which project as spines near the suture (Figs 6g,h). E coast, in fresh water but near tidal influence.Thiara (p. 100) B Shell otherwise ....................................................................................3 3 A Operculum concentric with spiral nucleus (Figs 9g,h). Shell may have brown spiral bands .............................................................................4 B Operculum entirely paucispiral (Figs 9d,f) ........................................5

26 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

4 A Operculum nucleus small (Fig. 9h). Shell often brown-banded. Widely distributed ..............................................................Cleopatra (p. 120) B Operculum nucleus larger (Fig. 9g). Shell rarely brown-banded. Restricted to Volta Basin and lower Zaire River. Pseudocleopatra (p. 128) 5 A Operculum nucleus near the basal margin (Fig. 9d) ........................... ....... .....................................................................Melanoides (p. 102) B Operculum nucleus near centre (Fig. 9f) ...........................................6 6 A Larger, shell usually >15 mm high even when decollate; may be smooth or with ridges and spines. Radula very long (about half of the shell height); central tooth distinctively quadrangular. Widespread in W and central Africa ..........................................................Potadoma (p. 114) B Smaller, <15 mm high, variously sculptured. Radula shorter, with narrow central tooth. Restricted to E Zaire and Malagarasi Delta of Lake Tanganyika .......................................................Potadomoides (p. 129) Family POTAMIDIDAE 1 A Smaller shell, rarely reaching 20 mm high, with nodular sculpture (Fig. 7a). In brackish water at or near coasts of NE Africa ......................... ................................................................................Pirenella (p. 145) B Larger, >20mm high. Brackish waters in tropical region .................2 2 A Less than 40 mm high, strongly ribbed, decollate (Fig. 7b) ............... ........ ......................................................................Cerithidea (p. 143) B Growing over 50mm high; ribs lacking or only weak .....................3 3 A With strong nodules, tubercles and spines. W coast ........................... ....... ................................................................Tympanotonus (p. 143) B Smoother, spire flat-sided (Fig. 7c). Indo-Pacific coasts .....................4 4 A With low ribs. E coast. ........................................Terebralia (p. 145) B Almost smooth, any sculpture is mainly spiral. In Madagascar but not found in Africa. ...................................................Telescopium (p. 145) Pulmonate families 1 A Shell cap-like (Figs 10d–f) ............................................ANCYLIDAE B Shell spirally coiled ............................................................................2 2 A Spired snails, with a slender aperture having internal lamellae (Figs 10a–c). Confined to brackish water, especially mangrove swamp .... .... ......................................................................................ELLOBIIDAE

FRESHWATER SNAILS OF AFRICA 27

Fig. 7. Potamididae and Littorinidae. (a) Pirenella conica (two views), (b) Cerithidea decollata. (c) Terebralia palustris. (d) Littoraria (Littorinopsis) sp. Scale line: 10 mm (lower part of P. conica twice this magnification). A guide line indicates the columellar notch in (b).

B With spire or discoid. In fresh water .................................................3 3 A Discoid (Figs 11b–g). PLANORBIDAE: subfamily Planorbinae in part and Indoplanorbis of the Bulininae B With distinct spire (Fig. 11a) ............................................................4 4 A Shell dextral. Tentacles broadly triangular (Fig. 12a). LYMNAEIDAE (Shell similar in the landsnail family Succineidae, of which some species live in marshes; these are recognisable by their tentacles (Fig. 12b) with eyes at the tips and narrower bases). B Shell sinistral. Tentacles slender (Figs 12c,d) .....................................5 5 A Shell very smooth (glossy), spire sharply pointed. Without pseudobranch; mantle border with finger-like processes (Fig. 12d); blood colourless; radula teeth in V-shaped rows ........................................ .PHYSIDAE

28 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Fig. 8. Opercula: inner surfaces of (a)–(d) and (f), outer surfaces of (e) and (g). (a) Septaria borbonica. (b) Neritilia manoeli. (c) Neritina natalensis. (d) Clithon longispina. (e) Bellamya trochlearis. (f) Pila wernei. (g) Valvata nilotica. Scale lines: 1 mm (b,g) or 2 mm (a,c,d–f).

B Shell surface comparatively dull; spire may be low and apex obtuse. With pseudobranch, but not mantle processes (Fig. 12c); blood red; tooth rows nearly straight ..................................................................6 6 A Whorls rounded, shouldered or carinate; only few if any spiral ridges. Penis of the ‘ultrapenis’ type, attached at base of preputium (Fig. 14d). Throughout Africa. PLANORBIDAE: subfamily Bulininae in part.. ..... ............................................................................(Bulinus, p. 208) B Whorls sharply shouldered and carinate, flat near the suture; with numerous spiral ridges. Penis of simple type, projecting freely into the sheath. In Africa found only in Nigeria (introduced) .......................... ....... ...PLANORBIDAE: Planorbinae in part (Amerianna, p. 175) Family ELLOBIIDAE 1 A Shell sinistral .........................................................Blauneria (p. 153) B Shell dextral ........................................................................................2

FRESHWATER SNAILS OF AFRICA 29

Fig. 9. Opercula: outer surfaces. (a) Jubaia excentrica. (b) Gabbiella adspersa. (c) Eussoia inopina. (d) Melanoides anomala. (e) Incertihydrobia teesdalei. (f) Potadoma vogeli. (g) Pseudocleopatra togoensis. (h) Cleopatra nsendweensis. Scale line: 1 mm (a– c,e) or 2 mm (d,f–h).

2 A Shell more than twice as high as wide (Fig. 10a). Living subterraneanly. ...........................................Auriculastra and Auriculodes (p. 152–3) B Shell less than twice as high as wide. Surface-dwelling on shaded mud. .......................................................................................................... .3 3 A Outer lip with strong internal rib (Fig. 10b) ........Cassidula (p. 153) B Outer lip without rib, but may have spiral ridges (Fig. 10c) ............. .......... ....................................................................Melampus (p. 155) Family ANCYLIDAE 1 A Apex with radial rows of small pits (Figs 10d; 79e) ........................... ........ .......................................................................Burnupia (p. 163) B Apex with radial ridges ......................................................................2

30 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Fig. 10. Ellobiidae and Ancylidae (viewed from above and side), (a) Auriculastra radiolata. (b) Cassidula labrella. (c) Melampus semiaratus. (d) Burnupia sp. (e) Ferrissia sp. (f) Ancylus fluviatilis. Scale line: 2 mm (d–f) or 4 mm (a–c).

2 A Shell smaller, <5 mm long, apical ridges very fine (Figs 10e; 79f) .... ......... ........................................................................Ferrissia (p. 169) B Larger, reaching 6–10 mm long, apical ridges coarser (Figs 10f; 79c,d). Restricted to NW Africa and Ethiopian highlands ..Ancylus (p. 161) Family PLANORBIDAE: subfamily Planorbinae (excluding the few palaearctic genera reported rarely from NW Africa). This key includes Indoplanorbis of the Bulininae, which has a large discoid shell similar to Biomphalaria and Helisoma. 1

2

A Shell with pointed spire, sinistral; whorls sharply shouldered. In Africa found only in Nigeria ........................................Amerianna (p. 175) B Shell discoid ......................................................................................2 A Shell very small (up to 3 mm diameter); whorls flat, with widelyspaced ribs (Fig. 11f). In Africa found only in Algeria and highland Ethiopia ...................................................................Armiger (p. 179) B Shell may be larger (10–20 mm diameter) or if small then without wide-spaced ribs (Fig. 11g) ..............................................................3

FRESHWATER SNAILS OF AFRICA 31

Fig. 11. Physidae and Planorbidae. (a) Physa acuta. (b) Planorbis planorbis. (c) Biomphalaria angulosa, (d) Helisoma duryi. (e) Segmentorbis angustus (guide line indicates internal lamellae), (f) Armiger crista. (g) Ceratophallus natalensis. Scale lines: 1 mm (e–g) or 2 mm (a–d). A broken line indicates the underside in (c) and the diameter of the umbilicus in (g).

3

4

5 6

A Shell small, <8 mm diameter; distinctly convex on one side (the ‘upper’) and flat on the other (the ‘underside’); whorls rapidly increasing, umbilicus (on underside) very small; internal lamellae may be visible through the shell wall (Fig. 11e) ....................................... ..............4 B Shell larger (10–20 mm diameter) or if small then upper and under sides are more similarly shaped; whorls increase less rapidly, umbilicus larger; without lamellae (Fig. 11g) .......................................... .........5 A Shell usually without lamellae. Copulatory organ without flagellum. ..... .........................................................................Lentorbis (p. 188) B With 3 or more lamellae. Copulatory organ may have a flagellum. .. ....... .................................................................Segmentorbis (p. 190) A Shell large, >2 mm high ..................................................................6 B Shell smaller, <2 mm high ...............................................................9 A Shell up to 3 mm high, usually with carina below (Fig. 11b). In Africa found only in Egypt, Algeria and Morocco ..........Planorbis (p. 176) B Shell >3 mm high, periphery evenly convex although there may be angles on the upper and lower surfaces of the whorls .....................7

32 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

7

A Shell only rarely reaching 7 mm high; whorls not flattened within the umbilicus. Copulatory organ without preputial gland. Prostatic lobes arranged in a row. Widely distributed ..........Biomphalaria (p. 194) B Shell commonly over 7 mm high; whorls may be flat within the umbilicus. Introduced species of restricted occurrence ........................... 8 8 A Whorls commonly angular on the underside and flat within the umbilicus. Copulatory organ with an external preputial gland. Prostatic lobes in a bunch. Many scattered localities ...........Helisoma (p. 205) B Whorls strongly convex above and below, not flat within the umbilicus. Copulatory organ with ‘ultrapenis’ (see Bulininae). Prostatic lobes in a compact organ. In Africa found only in Nigeria and Niger ...... .......................................................................Indoplanor bis (p. 208) 9 A Penis with distal part sclerotised; opening terminal (Fig. 14a) ......... ........ ...............................................................Ceratophallus (p. 180) B Penis tissues not sclerotised, though there is a separate stylet or cuticular cap; opening subterminal .......................................................... ......10 10 A Penis with large dagger-like stylet (Fig. 14b) ......Gyraulus (p. 185) B Penis with small cap-like stylet (Fig. 14c) ...........Afrogyrus (p. 176)

Family PHYSIDAE A Shell broad. Copulatory organ with large preputial gland, visible externally (Fig. 13b). Widely distributed ......................Physa (p. 248) B Shell more slender, fusiform. Copulatory organ without an externally visible gland. W Africa and SE Africa .....................Aplexa (p. 249)

Checklist of gastropod molluscs found in the fresh and brackish waters of the African continent These are species recognised in the present account which can be only provisional. Increases in number of species are likely to arise from further taxonomic study in several groups, especially the endemic prosobranchs of Lake Tanganyika and the hydrobioid snails of northern Africa (the latter excluded entirely from this list because comprehensive revision is needed). Species found only in neighbouring islands are listed separately later. Some authors’ names are abbreviated: Bgt (Bourguignat), Linn. (Linnaeus), M.-B. (Mandahl-Barth), Mor. (Morelet). The order of species is as in the present systematic synopsis. The term ‘aggregate’ is used when it appears likely that a taxon includes more than one

FRESHWATER SNAILS OF AFRICA 33

Figs 12, 13. Fig. 12. (a) Lymnaea natalensis, animal removed from shell to show tentacles, (b) Succinea sp., narcotised whole snail, (c) Bulinus tropicus, narcotised animal, mantle removed, (d) Physa acuta, narcotised animal with copulatory organ everted, mantle removed. Fig. 13. Copulatory organs of (a) Aplexa waterloti and (b) Physa acuta viewed from the left side. An, anus. BW, body wall. Ey, eye. CM, cut edge of mantle. CO, copulatory organ. LT, left tentacle. MP, mantle processes. Pb, pseudobranch. PG, preputial gland. Pr, preputium. PS, penis sheath. Re, rectum. VD, vas deferens. Scale lines: 1 mm.

biologically distinct species. Brackets enclose the names of species believed to have been introduced in recent historical time. CLASS GASTROPODA

34 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Fig. 14. Planorbidae: diagrams of copulatory organs, (a) Ceratophallus. (b) Gyraulus. (c) Afrogyrus. (d) Bulinus. Scale lines: 0.5 mm. BW, position of attachment to body wall. Pe, penis. Pr, preputium. PS, penis sheath. RM, retractor muscle. Sc, sclerotisation. St, stylet. Up, attachment of ‘ultrapenis’ to base of preputium. VD, vas deferens. SUBCLASS STREPTONEURA (PROSOBRANCHS) Family Neritidae

Theodoxus numidicus (Récluz) T. maresi (Bgt) T. meridionalis (Philippi) N. gagates Lamarck N. oweniana (Wood) N. tiassalensis Binder N. rubricata Mor. N. cristata Mor. N. adansoniana (Récluz)

T. niloticus (Reeve) Neritina pulligera (Linn.) N. natalensis Reeve N. glabrata Sowerby N. kuramoensis Yoloye & Adegoke N. afra Sowerby Septaria borbonica (Bory de St Vincent) Neritilia manoeli (Dohrn)

Family Viviparidae Bellamya unicolor (Olivier)

B. crawshayi (Smith)

FRESHWATER SNAILS OF AFRICA 35

B. capillata (Frauenfeld) B. monardi (Haas) B. phthinotropis (Martens) B. costulata (Martens) B. jucunda (Smith) B. constricta (Martens) B. trochlearis (Martens) B. rubicunda (Martens)

B. mweruensis (Smith) B. pagodiformis (Smith) B. ecclesi (Crowley & Pain) B. jeffreysi (Frauenfeld) B. robertsoni (Frauenfeld) B. leopoldvillensis (Putzeys) B. contracta (Haas) (?)B. liberiana (Schepman) Neothauma tanganyicense Smith

Family Ampullariidae Pila ovata (Olivier) P. occidentalis (Mousson) P. africana (Martens) P. speciosa (Philippi) P. wernei (Philippi) Lanistes carinatus (Olivier) L. intortus Martens L. bicarinatus Germain L. neritoides Brown & Berthold L. congicus O.Boettger L. nsendweensis (Dupuis & Putzeys) L. neavei Melvill & Standen L. varicus (Müller) L. libycus (Mor.)

L. ciliatus Martens L. alexandri (Bgt) L. nyassanus Dohrn L. nasutus Mandahl-Barth L. solidus Smith L. ovum Peters L. purpureus (Jonas) L. ellipticus Martens L. farleri Craven L. stuhlmanni Martens L. graueri Thiele Afropomus balanoidea (Gould) Saulea vitrea (Born) (Marisa cornuarietis (Linn.))

Family Valvatidae Valvata nilotica Jickeli Family Littorinidae Littoraria (Littorinopsis) spp. Family Hydrobiidae (of tropical Africa only) Hydrobia accrensis Connolly H. gabonensis Mor. H. guyenoti Binder H. lineata Binder H. luvilana M.-B H. plena Bequaert & Clench

H. schoutedeni Bequaert & Clench (?)H. alabastrina Mor. (?)Potamopyrgus ciliatus (Gould) Lobogenes michaelis Pilsbry & Bequaert L. spiralis Pilsbry & Bequaert L. pusilla M.-B.

36 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

H. rheophila Bequaert & Clench Family Pomatiopsidae Tomichia ventricosa (Reeve) T. zwellendamensis (Küster) T. tristis (Mor.) T. rogersi (Connolly) T. natalensis Connolly

T. differens Connolly T. cawstoni Connolly T. hendrickxi (Verdcourt) T. kivuensis M.-B. (?)T. guillemei Leloup

Family Bithyniidae Bithynia tentaculata (Linn.) Gabbiella humerosa (Martens) G. kichwambae (M.-B.) G. matadina M.-B. G. neothaumaeformis (Germain) G. kisalensis (Pilsbry & Bequaert) G. parva (M.-B.) G. parvipila (Verdcourt) G. verdcourti M.-B. G. spiralis M.-B. G. tchadiensis M.-B. G. stanleyi (Smith) G. neumanni (Martens) G. senaariensis (Küster) G. schweinfurthi (Jickeli) G. africana (Frauenfeld) G. adspersa (Jickeli) G. zambica M.-B.

G. balovalensis M.-B. G. candida M.-B. G. rosea M.-B. G. depressa M.-B. G. barthi Brown G. walleri (Smith) Incertihydrobia teesdalei Verdcourt Jubaia excentrica M.-B. J. aethiopica (Verdcourt) Congodoma zairensis (Bequaert Clench) Funduella incisa M.-B. Liminitesta sulcata M.-B. Sierraia leonensis Connolly S. expansilabrum Brown S. outambensis Brown S. whitei Brown Soapitia dageti Binder

Family Assimineidae Assiminea bifasciata Nevill A. hessei O.Boettger A. keniana Brown Eussoia inopina Preston E. aethiopica (Thiele) E. leptodonta (Connolly) Family Thiaridae

E. oblonga M.-B. Pseudogibbula duponti Dautzenberg (?)P. cara (Pilsbry & Bequaert) Septariellina congolensis Bequaert & Clench Valvatorbis mauritii Bequaert & Clench

&

FRESHWATER SNAILS OF AFRICA 37

Thiara amarula (Linn.) T. scabra (Müller) Melanoides admirabilis (Smith) M. crawshayi (Smith) M. magnifica (Bgt) M. mweruensis (Smith) M. nodicincta (Dohrn) M. nyassana (Smith) M. pergracilis (Martens) M. polymorpha (Smith) M. pupiformis (Smith) M. turritispira (Smith) M. agglutinans (Bequaert & Clench) M. anomala (Dautzenberg & Germain) M. bavayi (Dautzenberg & Germain) M. depravata (Dupuis & Putzeys)

M. dupuisi (Spence) M. kisangani Pilsbry & Bequaert M. kinshassaensis (Dupuis & Putzeys) M. langi Pilsbry & Bequaert M. liebrechtsi (Dautzenberg) M. nsendweensis (Dupuis & Putzeys) M. nyangweensis (Dupuis & Putzeys) M. wagenia Pilsbry & Bequaert M. angolensis M.-B. M. manguensis (Thiele) M. recticosta (Martens) M. tuberculata (Müller) M. victoriae (Dohrn) M. voltae (Thiele) Pachymelania byronensis (Wood) P. aurita (Müller)

P. fusca (Gmelin) Potadoma freethi (Gray) P. schoutedeni Pilsbry & Bequaert P. moerchi (Reeve) P. togoensis Thiele P. vogeli Binder P. liricincta (Smith) P. bicarinata M.-B. P. alutacea Pilsbry & Bequaert P. ignobilis (Thiele) P. wansoni Bequaert & Clench P. liberiensis (Schepman) P. ponthiervillensis (Dupuis & Putzeys) (?)P. buttikoferi (Schepman) P. zenkeri (Martens) P. nyongensis Spence P. trochiformis (Clench) P. angulata Thiele P. kadeii Samé-Ekobo & Kristensen P. riperti Samé-Ekobo & Kristensen

C. obscura M.-B. C. exarata (Martens) C. elata Dautzenberg & Germain C. cridlandi M.-B. C. langi Pilsbry & Bequaert C. johnstoni Smith C. mweruensis Smith C. smithi Ancey C. nsendweensis Dupuis & Putzeys C. pilula M.-B. C. guillemei Bgt C. athiensis Verdcourt C. hemmingi Verdcourt

Cleopatra bulimoides (Olivier) C. ferruginea (I. & H.C.Lea) C. africana (Martens)

C. rugosa Connolly Pseudocleopatra togoensis Thiele P. voltana M.-B. P. dartevellei M.-B. P. bennikei M.-B. Potadomoides pelseneeri Leloup Pot. bequaerti (Dautzenberg & Germain) Pot. hirta (Dautzenberg & Germain) Pot. schoutedeni (Dautzenberg & Germain) (?)Pot. broecki (Putzeys)

38 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Thalassoid prosobranchs of Lake Tanganyika Syrnolopsis lacustris Smith S. minuta Bgt S. gracilis Pilsbry & Bequaert Anceya giraudi Bgt A. terebriformis (Smith) Martelia tanganyicensis Dautzenberg Lavigeria nassa (Woodward) aggregate L. grandis (Smith) Mysorelloides multisulcata (Bgt) Hirthia globosa Ancey H. littorina Ancey Spekia zonata (Woodward) Tanganyicia rufofilosa (Smith) Stanleya neritinoides (Smith) Reymondia horei (Smith) R. pyramidalis Bgt

R. tanganyicensis Smith Bridouxia giraudi Bgt B. praeclara (Bgt) B. leucoraphe (Ancey) B. smithiana (Bgt) B. ponsonbyi (Smith) B. rotundata (Smith) Stormsia minima (Smith) Paramelania damoni (Smith) aggregate P. iridescens (Moore) Bathanalia howesi Moore B. straeleni Leloup Tiphobia horei Smith Limnotrochus thomsoni Smith Chytra kirki (Smith)

Family Melanopsidae Melanopsis praemorsa (Linn.) Family Potamididae Cerithidea decollata (Bruguière) Tympanotonus fuscatus (Linn.)

Terebralia palustris (Linn.) Pirenella conica (de Blainville)

SUBCLASS EUTHYNEURA (INCLUDES THE PULMONATES) Family Ellobiidae

Auriculastra radiolata (Mor.) Auriculodes gaziensis (Preston) Blauneria exsilium Preston Cassidula labrella (Deshayes)

C. mustelina (Deshayes) Melampus semiaratus Connolly M. liberianus H. & A.Adams

Family Lymnaeidae Lymnaea natalensis Krauss (L. columella Say) L. truncatula (Müller)

L. stagnalis (Linn.) L. palustris (Müller) L. peregra (Müller)

FRESHWATER SNAILS OF AFRICA 39

Family Ancylidae Ancylus fluviatilis Müller A. regularis Brown A. ashangiensis Brown

Burnupia caffra (Krauss) aggregate Ferrissia isseli (Bgt) aggregate

Family Planorbidae Subfamily Planorbinae

(Amerianna carinata (H.Adams)) Planorbis planorbis (Linn.) Afrogyrus coretus (de Blainville) Armiger crista (Linn.) Ceratophallus natalensis (Krauss) C. blanfordi Brown C. kigeziensis (Preston) C. kisumiensis (Preston) C. bicarinatus (M.-B.) C. subtilis (M.-B.) C. concavus (M.-B) C. crassus (M.-B.) C. pelecystoma Brown (?)C. apertus (Martens) (?)C. faini (Adam) Gyraulus ehrenbergi (Beck) G. costulatus (Krauss) G. connollyi Brown & Van Eeden Lentorbis benguelensis (Dunker) L. junodi (Connolly)

L. carringtoni (de Azevedo et al.) Segmentorbis angustus (Jickeli) S. planodiscus (Melvill & Ponsonby) S. eussoensis (Preston) S. excavatus M.-B. S. kanisaensis (Preston) Biomphalaria pfeifferi (Krauss) B. rhodesiensis M.-B. B. choanomphala (Martens) B. smithi Preston B. stanleyi (Smith) B. barthi Brown B. alexandrina (Ehrenberg) B. angulosa M.-B. B. tchadiensis (Germain) B. camerunensis (C.R.Boettger) B. salinarum (Mor.) B. sudanica (Martens) (Helisoma duryi (Wetherby)) Planorbarius metidjensis (Forbes)

Subfamily Bulininae (Indoplanorbis exustus (Deshayes)) Bulinus africanus group B. africanus (Krauss) B. nasutus (Martens) B. ugandae M.-B. B. obtusus M.-B.

B. abyssinicus (Martens) B. globosus (Mor.) B. jousseaumei (Dautzenberg) B. umbilicatus M.-B. B. hightoni Brown & Wright

B. truncatus/tropicus complex B. angolensis (Mor.)

B. permembranaceus (Preston)

40 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

B. depressus Haas B. hexaploidus Burch B. natalensis (Küster) B. nyassanus (Smith) B. octoploidus Burch

B. succinoides (Smith) B. transversalis (Martens) B. trigonus (Martens) B. tropicus (Krauss) B. truncatus (Audouin)

B. forskalii group B. forskalii (Ehrenberg) B. scalaris (Dunker) B. canescens (Mor.) B. senegalensis (Müller)

B. camerunensis M.-B. B. crystallinus (Mor.) B. barthi Jelnes B. browni Jelnes

B. reticulatus group B. reticulatus M.-B. B. wrighti M.-B. is closely related but found only in Arabia Family Physidae (Physa acuta Draparnaud)

(Aplexa waterloti (Germain))

Species found in islands of the western Indian Ocean but not in Africa This list is primarily of the freshwater species that seem to be distinct from African species, though probably not all are different. There are likely to be additional brackish-water species not found in Africa, especially in the Neritidae, Assimineidae, Thiaridae, Potamididae and Ellobiidae. Abbreviations: Com. (Comoro Islands), Mad. (Madagascar), Mau. (Mauritius). Family Neritidae Neritilia consimilis (Dohrn) Com., Mad., Clithon spp. Com., Mad., Mau. Mau., Réunion, Seychelles Family Viviparidae Bellamya bengalensis (Lamarck) Mau. Family Ampullariidae Pila cecillei (Philippi) Mad.

Lanistes grasseti (Mor.) Mad.

FRESHWATER SNAILS OF AFRICA 41

Family Thiaridae Thiara datura (Dohrn) Com., Réunion Cleopatra colbeaui (Craven) Mad. Melanoides psorica (Mor.) Mad. C. madagascariensis (Crosse) Mad. Melanatria fluminea (Gmelin) Mad. C. grandidieri (Crosse & Fischer) Mad. M. madagascariensis (Grateloup) Paludomus ajanensis Mor. Seychelles Mad. Family Lymnaeidae Lymnaea mauritiana Mor. Mau.

Lantzia carinata Jousseaume Réunion

Family Ancylidae Ferrissia modesta (Crosse) Mad. Family Planorbidae Afrogyrus rodriguezensis (Crosse) Rodriguez A. starmuehlneri Brown Mad.

G. mauritianus (Mor.) Mau. Bulinus obtusispira (Smith) Mad. A. crassilabrum (Mor.) Mad. B. liratus (Tristram) Mad. (?)Ceratophallus socotrensis (Godwin-Austen) B. cernicus (Mor.) Mau. Socotra B. bavayi (Dautzenberg) Mad., Aldabra Gyraulus cockburni (Godwin-Austen) Socotra References Brown, D.S. 1965. Freshwater Mollusca from Ethiopia. Bulletin of the British Museum (Natural History), Zoology, 12:37–94. Brown, D.S. & Kristensen, T.K. 1989. A Field Guide to African Freshwater Snails. 8. Southern African Species. Charlottenlund: Danish Bilharziasis Laboratory. Burch, J.B. (Ed.), 1985. Handbook on Schistosomiasis and Other Snail-mediated Diseases in Jordan. Ann Arbor, U.S.A.: University of Michigan. Connolly, M. 1929. Notes on African non-marine Mollusca, with descriptions of many new species (concluded). Annals and Magazine of Natural History, 3:165–178. Lincoln, R.J., Boxshall, G.A. & Clark, P.P. 1982. A Dictionary of Ecology, Evolution and Systematics. Cambridge, London: Cambridge University Press. Malek, E.S. 1985. Snail Hosts of Schistosomiasis and Other Snail-transmitted Diseases in Tropical America: a manual. Washington, D.C.: Pan American Health Organisation. Mandahl-Barth, G. 1958. Intermediate Hosts of Schistosoma. African Biomphalaria and Bulinus. Geneva: World Health Organisation, Monograph No. 37.

42 SYSTEMATIC SYNOPSIS: INTRODUCTION, GLOSSARY, IDENTIFICATION KEYS, CHECKLIST

Meier-Brook, C. 1983. Taxonomic studies on Gyraulus (Gastropoda: Planorbidae). Malacologia, 24:1–113. Pilsbry, H.A. & Bequaert, J. 1927. The aquatic mollusks of the Belgian Congo, with a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History, 53:69–602. Starmühlner, F. 1969. Die Gastropoden der Madagassischen Binnengewässer. Malacologia, 8:1–434. Verdcourt, B. 1958. A mystery shell from the Kenya coast. Journal of the East African Natural History Society, 23:99.

Chapter 3. Systematic Synopsis: Prosobranchs

The classification of gastropod molluscs is in a continuing state of revision and it will be some time before a system comes to be generally agreed for the groups of higher rank (Haszprunar, 1988; Ponder, 1988a). Gastropods have been divided commonly into two major groups, the Streptoneura (including those known as the Prosobranchia or prosobranchs) and the Euthyneura (pulmonates and opisthobranchs). The freshwater gastropods of Africa are either prosobranchs (socalled because they have a comb-like gill, the ctenidium, situated within the mantle cavity and in front of the heart) or pulmonates (lacking a gill, the mantle cavity serving as an air-breathing organ; treated in Chapter 4). Almost all African freshwater prosobranchs have an operculum of horny or calcareous material attached to the foot and closing the aperture to a varying degree (the operculum is much reduced in Soapitia and apparently lacking in Valvatorbis). The sexes are separate in all African genera apart from Valvata. The radula is either rhipidoglossate (Neritidae only; many teeth in a transverse row but only few are conspicuous) or taenioglossate (the other families; only 7 teeth per transverse row, all clearly distinct). Of the families considered here the Neritidae have been classified traditionally in the order Archaeogastropoda and the rest in the Mesogastropoda. Family Neritidae Shell small to medium-sized and typically ‘neritiform’; whorls few and rapidly expanding, spire low; lip oblique, aperture D-shaped, its straight side forming a columellar plate, which may be toothed. Shell commonly with a pattern of dark markings on a variously coloured background. Operculum paucispiral, calcified, with one or two internal projections or apophyses (the ‘rib’ and ‘peg’) on its inner columellar side. Radula rhipidoglossate (with many small marginal teeth). Many neritids are marine and various lineages have adapted to brackish and fresh waters, particularly in the tropics; in tropical Africa no species penetrates far above the limit of tidal influence. Because of the obliquity of the neritid apertural lip it is difficult to make standard measurements; those given here are for height or width, according to whichever is the greater.

44 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 15. Neritidae, opercula. (a) Theodoxus fluviatilis (England), (b) T. jordani (Jordan, Azrak). (c) Neritina tiassalensis (shell Fig. 17c). (d) N. oweniana (shell Fig. 17a). (e) N. cristata (syntype, BMNH). Scale lines: 1 mm.

Genus Theodoxus Montfort, 1810 Shell small, neritiform; columellar plate not toothed. Operculum with one or two apophyses (Fig. 15). Two groups of species were recognised (Baker, 1923), section Theodoxus with the peg on the operculum reduced or lacking, and section Neritaea with the peg clearly visible; this division was rejected by Kristensen (1986a) who observed one or two apophyses present in different individuals of the same species. Yet there seems to be a geographical pattern of variation, the single-apophysis form (Fig. 15a) being common in a western area, whereas the double-apophysis form (Fig. 15b) alone is found in the Near East (Dagan, 1971; Roth, 1984; Burch, 1985) and Egypt (my own observations). Further investigation is desirable of variation in the opercular apophyses and their value in taxonomy. In lakes, spring-pools and perennial streams, usually attached to stones; tolerant of low salinity. Europe, North West Africa, Egypt and the Near East (but not found in Sinai or Arabia). Only the one species T. fluviatilis of Europe was recognised to occur in North West Africa by Brown (1980a), but Kristensen (1986a) concluded that this species probably does not occur in the area and recognised the 3 other species that follow. Type species: Nerita fluviatilis Linnaeus, 1758, Europe.

FRESHWATER SNAILS OF AFRICA 45

Theodoxus numidicus (Récluz, 1841, Neritina). Type locality: NW Algeria, Oran. Fig. 16a. 7 mm. Shell small, may be white-spotted though often all black, with flat columellar plate. Operculum with a single apophysis. Central radular tooth with the ‘wings’ narrow and as long as the base; first lateral tooth with the posterior lobe prominent and rounded. DISTRIBUTION. Algeria and Morocco (Kristensen, 1986a). Theodoxus maresi (Bourguignat, 1864, Neritina). Type locality: NE Algeria, Ain Khadra near Zerguin in NE Algeria. 8 mm. Shell dark brown or black, with a convex columellar plate. Operculum commonly with one apophysis, though some individuals have two. Base of central tooth clearly longer than the ‘wings’; first lateral tooth with a weak posterior lobe. DISTRIBUTION. Algeria and Morocco (Kristensen, 1986a). Theodoxus meridionalis (Philippi, 1836, Neritina). Type locality; Sicily, Syracuse. 8 mm. Shell purplish to brown with light spots, last whorl strongly convex. Operculum with two strong apophyses. Central tooth with broad lateral wings; first lateral tooth with a pointed posterior lobe. DISTRIBUTION. Tunisia (Kristensen, 1986a). Theodoxus niloticus (Reeve, 1856, Neritina). Type locality: Egypt, the Nile. Figs 16b,c. 8 mm. Shell may have a prominent spire; colour and patterns highly variable (Gardner, 1932), commonly with purplish-brown zig-zag bands. Operculum with 2 apophyses. T. africanus (Reeve, 1856; of ‘Africa’) is very likely a synonym. T. niloticus is perhaps the same species as T. jordani (Sowerby, 1836) of the Near East (Tchernov, 1975a; Dagan, 1971; Roth, 1984; Burch, 1985); this has a similar Operculum (Fig. 15b). HABITAT. Slowly flowing water in lower Egypt; tolerant of some salinity and abundant in the extinct fauna of aquatic molluscs in the Faiyum Depression (Gardner, 1932). DISTRIBUTION. Egypt; lower Nile and canals. Sudan: ‘modern’ shells below the second Nile Cataract (Martin, 1968). Ethiopia: reports of T. africanus from the Blue Nile below Lake Tana (Bourguignat, 1883) and near Massawa (Bacci, 1951) have not been substantiated. Genus Neritina Lamarck, 1816 Shell small to medium-sized, neritiform, edge of columellar plate smooth or toothed, outer lip smooth (not serrate or toothed as it is in Nerita, a mostly marine genus). Operculum with the rib and peg well separated (compare with Clithon, Figs 8c,d). Egg capsules oval, 1 or 2 mm long, often attached to the shell.

46 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 16. Neritidae. (a) Theodoxus numidicus; Morocco, Ain Fekan. (b) T. niloticus; Egypt, Nile, (c) T. niloticus; Egypt, Maadi, drain, (d–f) Neritina pulligera; Mayotte Island, (g) N. natalensis; South Africa, Durban, (h) N. gagates; Zanzibar. (i) N. natalensis; Kenya, Gazi (range of colour pattern). Scale line: 5 mm (a–c) or 10 mm (d–i).

Neritina was subdivided by Baker (1923) according to radular characters; he

FRESHWATER SNAILS OF AFRICA 47

examined some African species but their shells were not illustrated and the identifications need confirmation. Comments by Binder (1957) on variation in the radulae of West African species add to doubts about the validity of Baker’s groups, which are not employed here. In brackish and fresh water near coasts, circumtropical and subtropical; 13 or more species in Africa and Madagascar, treated here in 3 geographical areas: eastern, Madagascar and western. Type species: Nerita pulligera Linnaeus, 1767. 1) Neritina in eastern Africa Neritina pulligera (Linnaeus, 1767, Nerita). Type locality: not given. Figs 16d–f. 23 mm. Last whorl greatly expanded, almost entirely enclosing the earlier whorls; appearing black, though with a fine reticulate pattern; lip usually orange within. The name N. knorri (Récluz, 1841; Philippine Islands) has been used for African snails but is a synonym of N. pulligera according to Starmühlner (1969). HABITAT. Rivers and streams, near tidal influence; on stones in currents up to 0.5 m sec−1 (Starmühlner, 1969). Found by myself on mud near streams flowing into mangrove swamps in South Africa and Kenya. DISTRIBUTION. Pemba (Mozley, 1939, N. knorri); Kenya (Gazi, BME); Mozambique (Azevedo et al., 1961, N. knorri); South Africa, Durban (Brown, 1967a, N. gagates). Comoro Islands (Starmühlner, 1983; Backeljau et al., 1986); Madagascar, Mascarene Islands and Seychelles (Starmühlner, 1969, 1983; Fischer-Piette & Vukadinovic, 1973); Far East (Brandt, 1974). Neritina natalensis Reeve, 1855. Type locality: South Africa, Umgeni River (near Durban). Figs 16 g,i. 20 mm. Shell with obviously projecting spire; yellowish-brown with variable black bands, sometimes reducing the light areas to small spots (Fig. 16i). HABITAT AND DISTRIBUTION. Mangrove swamp (Brown, 1971). Somalia, Giuba River (Connolly, 1928a) and southwards to Mozambique (Azevedo et al., 1961) and South Africa, Natal: Durban, (Brown, 1971), Umzimkulu River (Connolly, 1939). Neritina gagates Lamarck, 1822. Type locality: not given. Fig. 16h. 22 mm. Like N. natalensis but generally more depressed and darker coloured. HABITAT AND DISTRIBUTION. Streams near tidal influence, on stones in currents up to 0.75 m sec−1 (Starmühlner, 1969, 1983). South Africa: Natal (Connolly, 1939). Comoro Islands, Madagascar, Mascarene Islands and Seychelles (Germain, 1921a; Starmühlner, 1969, 1983; Fischer-Piette & Vukadinovic, 1973; Backeljau et al., 1986). 2) Neritina present in Madagascar but not found in Africa. N. auriculata Lamarck, 1816 (Starmühlner, 1969, 1983) has a rapidly increasing last whorl like N. pulligera, but the lip is distinctively expanded. N. turrita (Chemnitz, 1786) is large and high-spired; reported without precise localities (Fischer-Piette & Vukadinovic, 1973).

48 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

3) Neritina in West Africa. Among the 8 species recognised here, N. oweniana and N. tiassalensis are comparatively large and there is a distinct group of smaller species with strongly patterned shells (adansoniana, glabrata, kuramoensis). Binder (1957) gave a comparative account of 6 species found in Ivory Coast. Neritina oweniana (Wood, 1828, Nerita). Type locality: Africa. Figs 17a,b. 28 mm (including the ‘wings’). Last whorl expanded enclosing earlier whorls almost completely; lip commonly expanded above and below forming two winglike projections; columellar edge smooth in large shells but toothed in some juveniles; highly varied black markings on a yellowish-brown background. Operculum with a well developed peg (Fig. 15d). HABITAT. The wings were most fully developed in nearly fresh water above the mangrove zone (Pilsbry & Bequaert, 1927). Living in a salinity range of 0.3– 1.1‰ (Binder, 1968) and found by myself commonly on Vallisneria plants in apparently fresh water in the lower Volta River. DISTRIBUTION. Liberia to Angola (Pilsbry & Bequaert, 1927); furthest inland at Bator, Volta River (McCullough, 1965a) and Zambi, Zaire River (Pilsbry & Bequaert, 1927). Neritina tiassalensis Binder, 1955, 1957. Type locality: Ivory Coast, rapids of the Bandama River at Tiassalé (80 km inland). Figs 15c, 17c. 26 mm. Like a large darkly-pigmented N. oweniana but lacking the wing-like expansions of the lip (Fig. 17c). Peg of operculum comparatively small (Fig. 15c). Distinguished from N. aequinoxialis (see N. afra) by the smooth columellar edge and the finer microsculpture on the shell (Binder, 1955). HABITAT AND DISTRIBUTION. Rocks in the full current of a river in Ivory Coast. Neritina rubricata Morelet, 1858. Type locality: Senegambia (although syntypes from Morelet’s collection (BMNH) are labelled from Calabar, Gabon and Congo). Figs 17d–f. 13 mm. Spire prominent, columellar edge toothed; similar to N. oweniana in the yellowish-brown colour and dark patterns (Binder, 1957). DISTRIBUTION. Gambia to Cameroon (DBL) and Gabon (BMNH, Fig. 17d). Neritina cristata Morelet, 1864. Type locality: Gabon, Como River. Fig. 17g. 16 mm. Like N. oweniana but spire more prominent and columellar edge always toothed (Binder, 1957). Mature shell usually with an expansion of the upper lip forming a subsutural ridge, to which the species owes its name. Operculum with a large peg (Fig. 15e). DISTRIBUTION. Sierra Leone (DBL), Ivory Coast (Binder, 1957), Cameroon (DBL) and Gabon. Neritina adansoniana (Récluz, 1841, Nerita). Type locality: Senegal River estuary. Fig. 18a. 12 mm (to 16 mm; Binder, 1957). Spire prominent and whorls somewhat angular, being flattened above the periphery; colour ranges from grey to pink with varied markings. It is likely that N. kuramoensis is the same species.

FRESHWATER SNAILS OF AFRICA 49

Fig. 17. Neritina. (a) N. oweniana; Sierra Leone, Kambia. (b) N. oweniana; Ghana, Volta River. (c,c′) N. tiassalensis; Ivory Coast (collected from the type locality in 1964 by E.Binder), (d–f′′) N. rubricata, from the collection of Morelet in BMNH: d,f (same shell), f′ and f′′, all from Gabon; e, from Nigeria, Old Calabar. (g,g′) N. cristata; syntypes (BMNH1893.2.4.1829–34). Scale line: 10 mm.

50 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

HABITAT AND DISTRIBUTION. More tolerant than N. glabrata of varying salinity and strong wave-action according to Pilsbry & Bequaert (1927), although both species were found in a wide salinity range in Ivory Coast (Binder, 1968). Senegal to Angola. Neritina glabrata Sowerby, 1849. Type locality: not given. Figs 18b,c. 8.5 mm. Generally smaller than N. adansoniana, with a smoother and glossy surface; spire lower and last whorl more evenly rounded. The beautiful varied colouration was illustrated in colour by Pilsbry & Bequaert (1927); ground colour commonly yellowish, patterned with black, brown or red. HABITAT AND DISTRIBUTION. Sheltered coves, in brackish water (Pilsbry & Bequaert, 1927); estuaries and lagoons, living usually at depths of less than 1 m, on sand, rocks and vegetation (Binder, 1957). In a moderate range of salinity in Lagos Lagoon (Yoloye & Adegoke, 1977); most common on sand (Ajao & Fagade, 1990a). Gambia to Angola (Pilsbry & Bequaert, 1927). Neritina kuramoensis Yoloye & Adegoke, 1977. Type locality: Nigeria, Kuramo Water (a branch of Lagos Lagoon). 12 (to 15 mm). The authors distinguished this species from N. glabrata by the larger, thicker shell with a higher spire and duller colour; it seems likely to be a synonym of N. adansoniana. HABITAT AND DISTRIBUTION. Nigeria: localities mostly associated with Lagos Lagoon. On mangrove rhizophores, other vegetation and mud, but not sand (Adegoke et al., 1969; Neritina sp.); in a wide range of salinity. Neritina afra Sowerby, 1841. Type locality: Fernando Po. Figs 18d,e. 14 mm. Spire low though distinct, edge of columella with coarse teeth; colour generally dark greenish-brown with yellowish spots; columellar plate white with a faint orange tint towards the outer margin. Placed incorrectly in Theodoxus by Pilsbry & Bequaert (1927) following Baker (1923). N. aequinoxialis Morelet (1848; Ile du Prince) is founded on shells that seem to be large N. afra (Fig. 18d) and resemble N. tiassalensis (see also Binder, 1955). HABITAT. Torrential streams at 200–300 m altitude (Germain, 1912a), but otherwise found only in coastal localities. DISTRIBUTION. Fernando Po, Ile du Prince (Germain, 1912a), São Tomé (Brown, 1991), Cameroon (Germain, 1912a; Victoria, DBL), Angola (Morelet, 1868). Genus Clithon Montfort, 1810 Shell small to medium-sized, neritiform, with spines in some species (Fig. 18g). Operculum with a high ridge between the peg and the rib, unlike Neritina (Figs 8c,d). In the lower courses of rapid streams in the Indo-Pacific region, but not found in Africa. Three species reported from the Comoro Islands (Starmühlner, 1983; Backeljau et al., 1986) and 3 or more found in Madagascar and the Mascarene Islands (Starmühlner, 1969, 1979, 1983; Fischer-Piette & Vukadinovic, 1973), including C. longispina (Récluz, 1841) (Fig. 18g).

FRESHWATER SNAILS OF AFRICA 51

Genus Septaria Ferussac, 1807 Shell medium to large, with its last whorl greatly expanded and cap-like. Operculum reduced to a small angular plate (Fig. 8a). In the lower courses of streams in the Indo-Pacific region, but rarely found in Africa. Type species: Patella borbonica Bory de St Vincent, 1803, Réunion Island. Septaria borbonica (Bory de St Vincent, 1803, Patella). Type locality: Réunion Island. Figs 18h,i. 27 mm long (large South African shell). Taxonomy revised and reproduction described by Haynes (1992); a widespread species, reported under many different names. HABITAT. The only known African localities are streams on the Natal coast (Connolly, 1939); probably now extinct as the result of habitat disturbance. DISTRIBUTION. South Africa, Natal coast (Connolly, 1939, as S. tessellaria) and Indian Ocean Islands (Starmühlner, 1969, 1983; Fischer-Piette & Vukadinovic, 1973, as S. lineata; Backeljau et al., 1986). Genus Neritilia Martens, 1879 Shell small, neritiform, lacking colour and pattern; columellar edge smooth. Operculum with single apophysis (Fig. 8b). Radula lacking central tooth. In fresh water near coasts; West Africa, Caribbean and Indo-Pacific regions. Few species; possible synonymies discussed by Starmühlner (1983). One species in Africa. Type species: Neritina rubida Pease, 1865, Tahiti (Brandt, 1974). Neritilia manoeli (Dohrn, 1866, Neritina). Type locality: Principe Island, in stony streams. Fig. 18f. 4 mm wide. Easily recognised from the small, pale (when clean), unpatterned shell. N. succinea (Récluz, 1841) of the Caribbean region is more depressed with a relatively larger aperture (Brown, 1980b). DISTRIBUTION. Principe Island, São Tomé Island (collected by C.Ripert, 1992) and Cameroon: Bibundi (Boettger, 1905) and Victoria, on aquatic plants (DBL). Neritilia consimilis Martens, 1897a. Type locality: Mauritius, Creole River. 5 mm wide. Shell so like that of N. manoeli that it could be the same species; examples from Mauritius and Anjouan Island described by Brown (1980b), taxonomic relationships discussed by Starmühlner (1983). HABITAT AND DISTRIBUTION. On rocks in streams up to 120 m altitude in Anjouan (Starmühlner, 1976a). Comoro Islands: Anjouan (Starmühlner, 1976a; Backeljau et al., 1986); Madagascar (Fischer-Piette & Vukadinovic, 1973); Mauritius, Réunion and Seychelles (Starmühlner, 1976b, 1983).

52 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 18. Neritidae. (a) Neritina adansoniana; Ivory Coast, lagune d’Ebrié. (b) N. glabrata; Nigeria, Lagos (6 shells), (c) N. glabrata; Lagos. (d,d′) N. afra; Principe Island (syntype of N. aequinoxialis, BMNH1893.2.4.1842–44). (e) N. afra; Cameroon, Victoria (5 shells). (f) Nerititia manoeli; Cameroon, Victoria, (g) Clithon longispina; Mauritius, (h) Septaria borbonica; South Africa, Widenham. (i) S. borbonica; Mauritius. Scale lines: 5 mm.

FRESHWATER SNAILS OF AFRICA 53

Family Hydrocenidae A single genus of small snails, with the operculum bearing an internal apophysis, living on land in moist places in the Indo-Pacific region. Hydrocena noticola Benson is recorded from South Africa (Connolly, 1939) and was classified in Assiminia by Thiele (1927). Three species are listed for Madagascar by Starmühlner (1969); one reported from a freshwater lake (Germain, 1935a). Family Viviparidae Shell medium to large, dextral; spire conical, whorls varying from evenly convex to angular or carinate. Operculum corneous and concentric (Fig. 8e). Viviparous; young develop in the lower oviduct. Male with right tentacle modified as a copulatory organ. Radula taenioglossate; central tooth wide and lacking basal denticles. Nearly cosmopolitan in fresh water, but absent from South America. Two genera in Africa. Genus Bellamya Jousseaume, 1886 Characters as for the family. Distinguished from Viviparus of Europe by anatomical characters including a differently positioned testis (Rohrbach, 1937). Shell apex (Fig. 2c) sharply pointed, with a ridge and bristles (whereas it is blunt and smooth in Neothauma of Lake Tanganyika). In rivers, lakes and smaller permanent waterbodies of Africa and S Asia, but apparently not Arabia or the Near East, although viviparid shells of uncertain generic position are known from Yemen (Ayad, 1956), the Jordan Valley (Tchernov, 1975b) and Syria (Pallary, 1939). In Africa from Egypt southwards into Zululand and N Namibia (Fig. 69). The species were reviewed according to shell characters by Dartevelle (1952a) and taxonomic use of the arrangement of embryos was introduced by Mandahl-Barth (1973a); improved understanding of species is expected from chromosome studies (Kat, 1986). Of the 18 species recognised here, only unicolor and capillata are widely distributed, and most are restricted to large lakes. Species will be treated in 3 groups: those found in smaller habitats, those restricted to lakes and lastly a few of uncertain status. Type species: Vivipara duponti De Rochebrune, 1882, Senegal. 1) Species found in smaller waterbodies Bellamya unicolor (Olivier, 1804, Cyclostoma). Type locality: Egypt, Alexandria. Figs 19a–c. 30×20 mm. Aperture usually about half of the total shell height; last whorl slightly flattened at the periphery, producing two blunt angles; umbilicus narrow or closed; spiral rows of small bristles may occur. Embryos small and numerous (Mandahl-Barth, 1973a). To the same species apparently belong populations living in lakes and having a higher spire; named forms include B. abyssinica

54 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

(Martens, 1866) of Lake Tana, Ethiopia (Fig. 19b), unicolor variety elatior Martens (1897) of Lake Victoria (Fig. 19c) and B. gracilior (Martens, 1903) of Lake Chad. B. duponti (the genus-type) appears to be conspecific, although it is little known. HABITAT. Lakes, rivers and perennial streams. Especially abundant on bottom sediments in Lake Chad (Chapters 10, 11) and Lake Victoria (down to 64 m depth; Mandahl-Barth, 1954a). DISTRIBUTION (Fig. 69). Range large, but localities widely scattered. Lower Egypt, Sudan and southwards into Kenya and perhaps Tanzania; westwards through a narrow zone into Senegambia. Subfossil shells in the Rift Valley of Ethiopia (Brown, 1965); late Pleistocene-Holocene distribution in the Sahara included southern Libya, Chad and Niger (Van Damme, 1984). Doubtful record for Madagascar (Fischer-Piette & Vukadinovic, 1973, Vivipara). Bellamya capillata (Frauenfeld, 1865, Vivipara). Type locality: Lake Nyasa (Malawi). Figs 19d–g. 20×15 mm (syntype); to 35 mm high (Brown et al., 1992). Shell like B. unicolor, although the eggs are larger according to Mandahl-Barth (1973a), variation in shell and embryos described for NE Namibia (Brown et al., 1992). Mandahl-Barth (1968a) treated as two subspecies, B. aethiops (Reeve, 1864; central Africa) and B. kalingwisiensis (Smith, 1908; Kalungwisi River) (Figs 19e,f). B. passargei (Martens, 1904; Botletle area) was named from a subfossil shell found near the south-western limit of distribution. Revision is needed, including chromosome studies, to clarify the taxonomic status of B. capillata and of the many named forms now supposed to be synonyms. HABITAT. Lakes, rivers and smaller waterbodies if permanent. On the coastal plain of Natal, B. capillata lives in shallow pans as well as on the bottom of Lake Sibaya (Appleton, 1977c; Hart, 1979). DISTRIBUTION (Fig. 69). Range large, but localities scattered. From Tanzania southwards into north-eastern Natal; westwards into lower Zaire, Angola and the Okavango River (Brown et al., 1992). Bellamya monardi (Haas, 1934, Viviparus). Type locality: S Angola, Kilui stream, a tributary of the Cunene River. Figs 19g; 21a. 33×27 mm. Last whorl large, shouldered near the suture and rather flattened above the periphery; umbilicus sometimes surrounded by a low angle; surface with many fine spiral ridges, less smooth than in B. capillata and yellowishbrown rather than greenish (Brown et al., 1992). Two earlier named forms seem probably conspecific: Vivipara unicolor variety sambesiensis Sturany, 1898 and V. densestriata Preston, 1905 (Fig. 19g). A shell of B. monardi was illustrated by Connolly (1939) as an example of V. leopoldvillensis (Putzeys) from Namibia. DISTRIBUTION. S Angola and N Namibia; Cunene River and tributaries, Okavango River from Rundu to Popa Falls (Brown et al., 1992). 2) Species restricted to large lakes Bellamya phthinotropis (Martens, 1892, Vivipara). Type locality; SW shore of Lake Victoria at Nyamgotso. Fig. 19h.

FRESHWATER SNAILS OF AFRICA 55

Fig. 19. Viviparidae. (a) Bellamya unicolor; Kenya, Lake Jipe. (b) B. unicolor (form abyssinica); Ethiopia, Lake Tana, (c) B. unicolor (form elatior); Lake Victoria, Kisumu. (d) B. capillata; Lake Malawi (syntype, BMNH). (e,f) B. capillata; Zambia, Kalingwisi River (syntypes) of B. kalingwisiensis, BMNH1907.11.11.56–62). (g) B. densestriata; Zambezi River, above Victoria Falls (syntype, BMNH1905.8.29.2; see under B. monarch), (h) B. phthinotropis; Lake Victoria, Buvuma Channel at 33 m depth, (i–k) B. costulata; Lake Victoria, (i) typical form from Bukoba, (j) form dagusiae from north of Dagusi Island at 9–12 m depth and (k) form ugandae from Jinja Bay. Scale line: 10 mm.

44×30 mm. Large, with a broad body whorl and sharply tapered spire. HABITAT AND DISTRIBUTION. Lake Victoria; in deep water, to 33 m (108 feet) (Mandahl-Barth, 1954a). Bellamya costulata (Martens, 1892, Vivipara). Type locality: Kassarassi Island, SW Lake Victoria. Figs 19i–k.

56 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

19×14 mm. More strongly sculptured than B. unicolor. Mandahl-Barth (1973a) recognised 3 subspecies, differing in the strength of ribs and spiral ridges; costulata (Fig. 19i), dagusiae (Fig. 19j) and ugandae (Fig. 19k). DISTRIBUTION. Lake Victoria: northern shore, Bukoba and Mwanza (Mandahl-Barth, 1954a). Early records for Lake Tanganyika are probably incorrect (Brown & Mandahl-Barth, 1987). Bellamya jucunda (Smith, 1892, Viviparus). Type locality: Lake Victoria. Fig. 20a. 24×16 mm (female); 20.5×15 mm (male). Shell with convex sides forming an obtuse, ‘beehive-shaped’ spire. Two named forms: altior Mandahl-Barth and kisumiensis Preston; Mandahl-Barth (1954a, 1973a). HABITAT AND DISTRIBUTION. Found by myself on mud amongst papyrus near Kisumu, but not on the bottom sediments of the open lake. Lake Victoria and upper Victoria Nile. Bellamya constricta (Martens, 1889, Paludina). Type locality: Lake Victoria. Fig. 22a. 20×13 mm. The smallest species in the genus, with 1–3 carinae. DISTRIBUTION. Lake Victoria and the upper Victoria Nile (Mandahl-Barth, 1954a). Bellamya trochlearis (Martens, 1892, Vivipara). Type locality: Sirwa Island in Lake Victoria (southern shore). Figs 20b,c. 30×19 mm. Like B. constricta but larger, with one or more strong carinae (Mandahl-Barth, 1954a, 1973a). It appears that shells of B. trochlearis from Lake Victoria, mistakenly given the locality Lake Tanganyika, were named Cleopatra trisulcata Germain, 1905 (Brown & Mandahl-Barth, 1987). HABITAT AND DISTRIBUTION. Lake Victoria, living offshore; dredged down to 30 m in Speke Gulf, Mwanza. Bellamya rubicunda (Martens, 1879b, Paludina). Type locality: SW shore of ‘Lake Victoria’ (see below). Fig. 20d. 27×20 mm. Whorls strongly convex; sutures deep, umbilicus open (MandahlBarth, 1973a). The problem of using this name for a species known only from Lake Albert, when the type locality was given as Lake Victoria, was discussed by Mandahl-Barth (1954a) and Verdcourt (1992). The latter found the type specimens to agree closely with the species of Lake Albert, and it therefore seems that a mistake was made in the original locality. HABITAT AND DISTRIBUTION. Lake Albert, to a depth of at least 18 m (60 feet) (Mandahl-Barth, 1954a). Bellamya crawshayi (Smith, 1893, Viviparus). Type locality: Lake Mweru. Fig. 20e. 24×17.5 mm. Shell conical with a single carina. DISTRIBUTION. Lake Mweru (Mandahl-Barth, 1968a). Bellamya mweruensis (Smith, 1893, Viviparus). Type locality: Lake Mweru. Fig. 20f.

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Fig. 20. Viviparidae. (a) Bellamya jucunda; Victoria Nile below Owen Falls dam. (b,c) B. trochlearis; Lake Victoria, (d) B. rubicunda; Lake Albert, (e) B. crawshayi; Lake Mweru (syntype, BMNH1893.8.23.82–4). (f) B. mweruensis; Lake Mweru (syntype, BMNH1893. 8.23.75–7). (g) B. pagodiformis; Lake Mweru (syntype, BMNH1893.8.23.78–81). (h,i) Neothauma tanganyicense; Lake Tanganyika. Scale line: 10 mm.

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Fig. 21. Bellamya of Lake Malawi, (a) B. monardi; Namibia, Cunene River, (b) B. ecclesi; Monkey Bay, about 27 m depth, (c) B. jeffreysi; syntype, BMNH. (d) B. robertsoni; Monkey Bay, about 27 m depth. Scale line: 10 mm.

40×33 mm. Large and broadly conical, with a strong carina and shouldered whorls giving the spire a stepped appearance. DISTRIBUTION. Lake Mweru (Mandahl-Barth, 1968a). Bellamya pagodiformis (Smith, 1893, V. mureruensis variety pagodiformis). Type locality: Lake Mweru. Fig. 20g. 25×19 mm. Shell with a single strong carina; central radular tooth characteristic (Mandahl-Barth, 1968a). DISTRIBUTION. Lake Mweru.

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Fig. 22. Viviparidae. (a) Bellamya constricta; Uganda, Victoria Nile at Jinja. (b) B. leopoldvillensis (after Putzeys, 1898, Fig. 1). (c) B. contracta (after Haas, 1934, Fig. 7). (d) B. liberiana (after Schepman, 1888, Pl. 10). Scale lines: 10 mm.

Bellamya ecclesi (Crowley & Pain, 1964, Neothauma). Type locality: Lake Malawi at Chipoka. Fig. 21b. 54×41 mm. The largest species in this genus; shell fragile, with inflated last whorl and acutely pointed spire. Classified in Bellamya rather than Neothauma because of its pointed, angular embryonic whorl (Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi: down to 80 m (260 feet) (Mandahl-Barth, 1972). Bellamya jeffreysi (Frauenfeld, 1865, Vivipara). Type locality: Lake Malawi. Fig. 21c. 40×30 mm. Shell thick-walled, heavier than any other species in the genus; whorls moderately convex, spire with stepped appearance (Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi: down to 21 m (70 feet). Bellamya robertsoni (Frauenfeld, 1865, Vivipara). Type locality: Lake Malawi. Fig. 21d.

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36×24 mm. Similar to B. jeffreysi; sides flatter and spire more tapered (Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi: down to 87 m (285 feet). 3) Species of uncertain status Bellamya leopoldvillensis (Putzeys, 1898, Paludina). Type locality: Stanley Pool, lower Zaire River near Kinshasa. Fig. 22b. 29×22 mm (apex eroded). Columellar margin straight. Known from only the original description and a few young shells (DBL). The supposed example from Namibia illustrated by Connolly (1939) is B. monardi. DISTRIBUTION. Lower Zaire: type locality and Kinshasa (DBL). Bellamya contracta (Haas, 1934, Viviparus). Type locality: Zaire, upper Katanga, Kiala district in the Luapula area; from an affluent stream of the Mafufya, a tributary of the Dikuluwe. Fig. 22c. 27.5×21 mm. Whorls swollen, sutures sunken, umbilical area with a ridge; shell from near the type locality was illustrated by Mandahl-Barth (1968a). DISTRIBUTION. SE Zaire: type locality; Kiubu Rapids (Dartevelle, 1952a) and Lufira Region (Mandahl-Barth, 1968a). (?)Bellamya liberiana (Schepman, 1888, Paludina). Type locality: Liberia, on rocks in the St Paul’s River near Bavia. Fig. 22d. 24×19 mm (2–3 whorls remaining). From its size and shape, this shell could be taken for a Bellamya, but from the description of the surface as ‘granular’ it might also be a Potadoma. Operculum and anatomy unknown. DISTRIBUTION. Liberia: reported only from the type locality. The Asian species Bellamya bengalensis (Lamarck, 1822) occurs on Mauritius, where it probably has been introduced by man from India (Germain, 1921a; Dartevelle, 1952a; Starmühlner, 1983). It is distinguishable from any African species by the evenly convex whorls, with about 5 spiral brown bands. Genus Neothauma Smith, 1880 Shell larger and heavier than any Bellamya; apex obtuse and smooth (Fig. 2d). Confined to Lake Tanganyika; a record for Lake Malawi is incorrect (see Bellamya ecclesi). Neothauma tanganyicense Smith, 1880a. Type locality: E shore of Lake Tanganyika, at Ujiji. Figs 2d; 20h,i. 60×46 mm. Whorls vary from convex to angular or carinate; variation well illustrated by Leloup (1953). HABITAT AND DISTRIBUTION. On various substrata, of rocks, sand and mud; taken alive down to 65 m (Leloup, 1953). Juveniles burrow beneath sediment, apparently to avoid predators, especially crabs (West et al., 1991). Living today only in Lake Tanganyika, but fossils found in the Albert/Edward Basin (Gautier, 1970).

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Family Ampullariidae (Pilidae) Medium to large, shell dextral or sinistral; depressed to ovate, with strongly rounded whorls, which may be angular or carinate. Operculum (Fig. 25) concentric, either entirely corneous or with calcareous inner layer. There is a tentacle-like process (pseudopodium) on each side of the snout, in addition to the tentacles. Near each tentacle is an epipodial lobe, the left one forming an inhalent siphon and the right one an exhalent siphon. Female oviparous; male with copulatory organ formed by a modified part of the mantle border. Central tooth broad, lacking basal denticles. Some species live in seasonal waterbodies becoming dry for long periods. Tropical regions of America, Asia and Africa, where there are 4 genera. The taxonomic history of this family was reviewed by Pain (1972), and Berthold (1991) carried out a comprehensive revision, based on comparative morphology, of systematics, phylogeny and biogeography. Phylogenetic relationships among genera were reconstructed according to characters of mainly the copulatory organ and shell (Berthold, 1989). According to this scheme, all the African genera are older than the neotropical ones; Pila seems the most advanced African group and Afropomus the most primitive. Genus Pila Röding, 1798 Medium to large, dextral, whorls more or less regularly convex. Operculum with inner calcareous layer. Clusters of eggs, with calcareous capsules, are deposited just above the water surface. Copulatory organ comparatively elaborate (Berthold, 1989). In Africa, Madagascar, S Asia and Indo-Pacific islands. From lower Egypt to northern Mozambique; westwards to Liberia and the Cunene River in the southwest. Five of the 7 African species recognised by Pain (1961) are maintained here. Type species: Helix ampullacea Linnaeus, 1758, Asia. Pila ovata (Olivier, 1804, Ampullaria). Type locality: Egypt, Alexandria. Figs 23a–c,e. 115×108 mm (P. nyanzae; other forms are smaller). Spire generally higher than in P. wernei and P. speciosa. Aperture and operculum (Fig. 25a) are proportionally broader than in P. wernei. Named forms (Mandahl-Barth, 1954a) include: P. adusta (Reeve, 1856, Zanzibar) (Fig. 23c), gradata (Smith, 1881a, Tanzania; see Pain, 1961) (Fig. 23b), nyanzae (Smith, 1892, Lake Victoria) (Fig. 23a) and congoensis Pilsbry & Bequaert, 1927 (Mandahl-Barth et al., 1974). Pain (1963) discussed the position of P. letourneuxi (Bourguignat, 1879, Tanzania, Bagamoyo) as a senior name for P. gradata. HABITAT. Temporary pools, papyrus swamps and, in Lake Victoria, stony beaches. Egg clusters are deposited above the water level amongst stones or in crevices in earth.

62 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

DISTRIBUTION. Lower Nile, Sudan (Brown, Fison et al., 1984) and southwards to N Mozambique (Azevedo et al., 1961; Pain, 1961); westwards to S Nigeria (DBL) and possibly SE Zaire (Mandahl-Barth, 1968a). Isolated northern population in Siwa Oasis, Egypt (Crawford, 1949; Ibrahim, 1975); recent shells in Wadi Howar, W Sudan (Sandford, 1936). Pila occidentalis (Mousson, 1887, Ampullaria). Type locality: Ovamboland, Cunene River. Fig. 24a. 60×59 mm. Globose, with a large umbilicus; hardly distinguishable from some forms of P. ovata. DISTRIBUTION. W Zambia, E Caprivi, Okavango River in Namibia and Botswana, S Angola; the most southerly records are near Maun and at Nyae Nyae Pan, Bushmanland (Brown et al., 1992). Pila africana (Martens, 1886, Ampullaria). Type locality: Ghana, Abetifi and Akra (?Accra). Fig. 23d. 50×45 mm. Like a globose form of P. ovata, but usually smaller and with stronger spiral sculpture (Alderson, 1925; Binder, 1957; Pain, 1961). HABITAT AND DISTRIBUTION. Found by myself in forest streams and on the shore of Lake Volta, under drifted vegetation. West Africa from Liberia to Ghana. Pila speciosa (Philippi, 1849, Ampullaria). Type locality: Somalia, Cape Guardafui. Fig. 24b. 105×100 mm. Globose, whorls strongly convex, sutures sunken; dark bands may be conspicuous. DISTRIBUTION. Somalia; N Kenya, lower Tana River (Pain, 1961; DBL); SE Ethiopia, near Dolo (Brown, 1965). Pila wernei (Philippi, 1851, Ampullaria). Type locality: Sudan, White Nile. Figs 24c,d; 25b. 127×125 mm. The largest African freshwater snail. Spire generally lower than in P. ovata; aperture and operculum comparatively narrow (Fig. 25b). Rare sinistral specimens occur (Fig. 24c). HABITAT. Associated with vegetation in Lake Chad (Lévêque, 1967). Buried aestivating snails in Wadi Howar, Sudan, were dug up and eaten by Jackals (Arkell, 1945). DISTRIBUTION. Scattered records from a large area, but requiring confirmation (Mandahl-Barth, 1954a; Pain, 1961). Late Pleistocene-Holocene distribution was extensive in Sudan and Chad (Van Damme, 1984). Living in S Somalia, Sudan and possibly Kenya; Lake Chad, and westwards to the Niger River in Mali and SW Nigeria (Ndifon & Ukoli, 1989); W Zaire (P. leopoldvillensis; Mandahl-Barth et al., 1974). Reports from further south seem to refer to P. occidentalis. Pila cecillei (Philippi, 1848, 1851, Ampullaria). Type locality: Madagascar, river near Hellville on the island of Nossi Bé. Figs 24e,f. 70×62 mm (or may be broader than high). Whorls almost shouldered near the suture. An extensive synonymy (Starmühlner, 1969) includes the small form P.

FRESHWATER SNAILS OF AFRICA 63

Fig. 23. Pila, (a–c,e) P. ovata: (a) Lake Victoria (possibly from the type series of P. nyanzae (Smith), BMNH); (b) Tanzania (syntype of P. gradata (Smith), BMNH1880.12. 20.120–21); (c) Zanzibar (syntype of P. adusta (Reeve), BMNH); (e) Uganda, Lake Kashiva. (d) P. africana; Ghana, Lake Volta. Scale line: 30 mm.

inops (Morelet, 1851) (Fig. 24e) and P. madagascariensis (Smith, 1882) (Fig. 24f). HABITAT AND DISTRIBUTION. Various muddy substrata, almost throughout Madagascar (Starmühlner, 1969; Fischer-Piette & Vukadinovic, 1973). Genus Lanistes Montfort, 1810 The shell appears sinistral, although the animal is dextral like the rest of the family. Depressed to ovately conic, whorls varying from evenly curved to angular and carinate; umbilicus may be widely open or closed. Operculum

64 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 24. Pila, (a) P. occidentalis; Namibia, Okavango River at Rundu. (b) P. speciosa; Zanzibar, (c) P. wernei; Nigeria, rare sinistral shell, (d) P. wernei; Cameroon, Yargoua (DBL, no. 193). (e) P. cecillei; Madagascar (syntype of P. inops (Morelet), BMNH1893.6. 30.130–32). (f) P. cecillei; Madagascar (syntype of P. madagascariensis Smith), BMNH1882.3.4.53–55). Scale line: 20 mm.

entirely corneous. Gelatinous clusters of eggs are deposited on aquatic vegetation. Madagascar and Africa, from the lower Nile southwards to Zululand and the Okavango Delta (Fig. 70). About 19 species, mostly in central and western Africa. Type species: Cyclostoma carinata Olivier, 1804, Alexandria. The traditional 3 subgenera founded on shell characters are maintained here, but a revised system of classification was proposed by Berthold (1991), to express phylogenetic relationships as indicated by variation in the structure of the mantle cavity diverticulum (Berthold, 1990; Brown & Berthold, 1990). 1) Lanistes sensu stricto. Depressed to ovate; commonly with a large umbilicus, angulations and sometimes carinae. This group is heterogeneous according to variation among species in the mantle cavity diverticulum (Berthold, 1990; Brown & Berthold, 1990; Berthold, 1991). Some species show the most

FRESHWATER SNAILS OF AFRICA 65

Fig. 25. Opercula (inner surfaces) of Pila, (a) P. ovata; W Zaire, Yakubu. (b) P. wernei; Zaire, Kinshasa. Scale line: 10 mm.

primitive state (diverticulum small or lacking), others the most fully developed state. Lanistes carinatus (Olivier, 1804, Cyclostoma). Type locality: Egypt, Kalidje Canal near Alexandria. Fig. 26a. 36×45 mm. Shell depressed, with a large umbilicus, usually brown-banded; angular at the periphery and around the umbilicus. Some authors use the names L. boltenianus (Chemnitz) and L. bolteni Pallary. Genitalia, reproduction and growth described by Aboul-Ela & Beddiny (1970a,b). HABITAT. Standing and slowly flowing waters, with rich vegetation (AboulEla & Beddiny, 1970b; Brown et al., 1984; Madsen et al., 1988). DISTRIBUTION (Fig. 70). Egypt, lower Nile; S Sudan; N Uganda (MandahlBarth, 1954a); SE Ethiopia (Pain, 1956); S Somalia, Giuba and Uebi rivers (Bacci, 1951) and Lake Burra near the Kenyan border (DBL); NE Kenya, Lake Jilore (DBL), Hola (Galole) and Malindi (BME). Late Pleistocene-Holocene sites associated with the Nile (Van Damme, 1984). PARASITE. Angiostrongylus cantonensis; Egypt (Yousif & Ibrahim, 1978). Lanistes intortus Martens, 1877 (see Binder, 1957, for nomenclature). Type locality: Congo (Zaire) River. Fig. 27c. 31×28 mm. Globose, whorls strongly convex. DISTRIBUTION. Lower Zaire River between Zambi and Banana (Pilsbry & Bequaert, 1927, p. 565). Lanistes bicarinatus Germain, 1907. Type locality: Zaire River at Brazzaville. Fig. 27a. 40×40 mm. There are 2 carinae and an angle around the umbilicus; brown banded. This is considered to be a conspecific form of L. varicus by Berthold (1991, p. 14). DISTRIBUTION. Lower Zaire River (Pilsbry & Bequaert, 1927) and near Libenge in Ubangi region (DBL).

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Fig. 26. Lanistes. (a) L. carinatus; Kenya, Hola. (b) L. congicus; Angola, (c) L. congicus; lower Zaire, (d) L. nsendweensis; eastern Zaire (syntype, BMNH1981.148). (e) L. neavei. (f) L. varicus; Nigeria, Epe Lagoon, (g) L. libycus; Ghana, Kumasi. (h) L. libycus; ‘Guinea’ (syntype of L. bernardianus (Morelet), BMNH1893.2.4.1808–9). (i) L. ciliatus; Kenya, Kinango. Scale lines: 15 mm (b–e) or 20 mm (a,f–i).

Lanistes congicus O.Boettger, 1891. Type locality: N Angola, Elau village

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Fig. 27. Lanistes. (a) L. bicarinatus; lower Zaire, Kimbara (DBL). (b) L. stuhlmanni; Tanzania (possible syntype, DBL). (c) L. intortus, lower Zaire (DBL). Scale line: 10 mm.

near San Salvador. Figs 26b,c. 36×42 mm (often smaller). Globose or more depressed, upper whorls strongly carinate; umbilicus large and surrounded by an angulation; dark bands may be present. L. kobelti Pain, 1954 has a strong umbilical carina. The surface of the whorl near the suture is more nearly horizontal than in L. bicarinatus. The spire is lower than in L. libycus. L. congicus is closely related to L. nsendweensis and L. neavei, according to the shell and anatomy (Berthold, 1990). HABITAT. Rivers flowing over sand, gravel or rocks (Mandahl-Barth et al., 1974). DISTRIBUTION. N.Angola (Wright, 1963a, as L. libycus); lower Zaire (Mandahl-Barth et al., 1974); Congo Republic (DBL). Lanistes nsendweensis (Dupuis & Putzeys, 1901, L. libycus variety nsendweensis). Type locality: E Zaire, several localities in the Lualaba River. Fig. 26d. 26×28 mm. Like L. congicus, but the whorls are only bluntly angular rather than carinate. L. gribinguensis Germain, 1905 from Central African Republic seems to be a strongly angular conspecific form. HABITAT. Zaire River near Kisangani (Stanleyville), among rocks below falls and in forest streams (Pilsbry & Bequaert, 1927). DISTRIBUTION. E Zaire: westwards to Ubangi and southwards to Kainana (DBL). Central African Republic (DBL). Lanistes neavei Melvill & Standen, 1907. Type locality: Zambia, Kapopo near Ndola. Fig. 26e. 26×27 mm. Like L. nsendweensis, but whorls evenly curved.

68 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

HABITAT AND DISTRIBUTION. Seasonal pools (Mandahl-Barth et al., 1972). Zambia, Ndola area; SE Zaire, Lubembe Region (Pilsbry & Bequaert, 1927, as L. n. katanganus; Mandahl-Barth, 1968a) and Lac de Retenue (Mandahl-Barth et al., 1972). Lanistes varicus (Müller, 1774, Helix). Type locality: unknown. Fig. 26f. 60×65 mm. A typical shell is approximately globose, with evenly curved whorls, large aperture and wide umbilicus, and usually is brown and unbanded. Some authors use the name L. guinaicus (Lamarck, 1816). L. adansoni Kobelt, 1911 is a higher-spired form, apparently restricted to the region of Senegal. L. millestriatus Pilsbry & Bequaert, 1927, was distinguished for its close-set growth ridges. HABITAT. Irrigation channels, streams and a lake (Madsen et al., 1987). I observed egg-laying beneath Nymphaea leaves in pools near the lower Volta River. DISTRIBUTION. Ghana, widespread; and scattered localities recorded for Senegambia, Mali, Ivory Coast, SW Nigeria, Upper Volta and Niger (DBL). Lanistes libycus (Morelet, 1848, Ampullaria). Type locality: Gabon, in lakes. Figs 26g,h. 52×47 mm; 42×33 mm (form bernardianus). Shell globose to ovately conic; early whorls flat above and carinate; umbilicus large, with strong angle. Surface with fine ridges, both spiral and transverse, which may bear periostracal projections; sometimes finely nodular. Shell usually with many dark bands, but may be uniformly pale brown. Spire highest in L. bernardianus (Morelet, 1860), which possibly is a distinct species. L. sanagaensis Clench, 1929 of Cameroon is founded on a strongly carinate shell with weak spiral sculpture. HABITAT. Common on muddy substrates in marshes, stream sources and shaded woodland streams (Thomas & Tait, 1984); associated with aquatic plants and shade (Ndifon & Ukoli, 1989). DISTRIBUTION. West Africa: coastal region from Ivory Coast to Gabon. Lanistes ciliatus Martens, 1878. Type locality: Kenya, Finboni, between Mombasa and Taita (Martens, 1897; I have failed to locate this place). Fig. 26i. 32×26 mm. Early whorls strongly carinate; lower whorls with transverse ridges and spiral rows of bristles; umbilicus large, surrounded by an angulation (Brown, 1980b). HABITAT AND DISTRIBUTION. Residual pools in drying streambeds; coastal region of SE Kenya (Brown, 1980b). Lanistes alexandri (Bourguignat, 1889a, Meladomus). Type locality: Tanzania, tributaries of the Wami (Vouami) River, above Sadani. 20×18 mm. Like L. ciliatus, but lacking strong spiral ridges; possibly conspecific. Apart from the types (Muséum d’Histoire naturelle, Geneva), I have seen only a single example (DBL). DISTRIBUTION. Tanzania: type locality and Msere (Martens, 1897); near Bagamoyo (DBL).

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Lanistes solidus Smith, 1877. Type locality: Lake Malawi. Fig. 28a. 45×40 mm. Spire higher than in the other species endemic to Lake Malawi (nasutus and nyassanus); umbilicus narrow; thick-walled at all stages of growth; unbanded. HABITAT AND DISTRIBUTION. Lake Malawi: dredged from down to 27 m (90 feet; Mandahl-Barth, 1972), but commonest at about 5 m on sand among weedbeds (Louda et al., 1984). Adaptations to avoiding predatory fishes include burrowing, a daily activity rhythm and the pattern of shell growth (Berthold, 1990). Lanistes nyassanus Dohrn, 1865. Type locality: southern end of Lake Nyassa (Lake Malawi). Fig. 28b. 68×75 mm. Large, low-spired, thick-walled when adult; umbilicus narrow and without angulation; unbanded. Closely related to solidus and nasutus, according to anatomy (Berthold, 1990). HABITAT AND DISTRIBUTION. Lake Malawi: living down to at least 35m, but commonest at 1.5 m on sand, and especially in weedbeds; adaptations to avoiding predatory fishes include burrowing, a daily rhythm of activity and rapid shell growth (Louda & McKaye, 1982; Louda et al., 1984; Berthold, 1990). Lanistes nasutus Mandahl-Barth, 1972. Type locality: Lake Malawi, 8 km (5 miles) E of Monkey Bay, at 82 m (270 feet) depth. Fig. 28c. 32×37 mm. Spire sunken within the greatly expanded last whorl; thin-walled; base of aperture spout-like; umbilicus large, surrounded by an angulation; shell almost colourless. Closely related to the two foregoing species (Berthold, 1990). DISTRIBUTION. Lake Malawi: from depths of 46–82 m (150–270 feet) (Mandahl-Barth, 1972). 2) Lanistes (Meladomus). Spire comparatively high, whorls lacking angulations and umbilicus usually narrow or closed. Lanistes ovum Peters in Troschel, 1845. Type locality: Mozambique, Zambezi River at Tete. Figs 29a,c. 50×43 mm (typical form); 85×53 mm (high-spired form); 105×80 mm (large form; L. magnus Furtado). Highly varied in size and spire height; whorls usually evenly convex, rarely flattened and bluntly angular; coloured a uniform brown; the surface may be flattened in patches (malleated) and sometimes has ribs of periostracum. The name L. olivaceus (Sowerby) was used by some authors (e.g. Leloup, 1953). Species believed to be synonyms include the large, high-spired forms L. procerus Martens, 1866 and L. elatior Martens, 1866. L. ovum bangweolicus Haas, 1936 has bluntly angular whorls. L. connollyi Pain, 1954 (Fig. 29c) from the Zambezi River above Victoria Falls is similar to L. ellipticus (see below), but is apparently a form of L. ovum adapted to flowing water (Brown et al., 1992). HABITAT. Highly varied: standing and slowly flowing waters, with muddy bottoms and vegetation (Mandahl-Barth et al., 1974); seasonal pans (Appleton, 1977c); rainpools (Betterton, 1984a); fishponds (Fashuyi, 1990). An abundant

70 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 28. Lanistes of Lake Malawi, (a) L. solidus (syntype, BMNH1877.9.28.24). (b) L. nyassanus. (c) L. nasutus. Scale line: 20 mm.

population of 75 000 snails per acre caused damage to rice plants (Crossland, 1965). DISTRIBUTION (Fig. 70). Scattered localities over a large area: S Sudan (Brown et al., 1984), S Somalia (Connolly, 1928a; Maffi, 1960), coastal Kenya and southwards to NE Natal (Pretorius et al., 1975); westwards through Chad to SW Nigeria (Ndifon & Ukoli, 1989); southwestwards to Angola (Wright, 1963a) and the Okavango Delta (Brown et al., 1992). PARASITE. The parasitic water-mite Unionicola macani Gledhill lives in the mantle cavity (Fashuyi, 1990). Lanistes purpureus (Jonas, 1839, Ampullaria). Type locality: ‘Swan River Australia’ (in error). Fig. 29b. 50×32 mm. Ovately conic, with a high spire; umbilicus closed; dark brown. Previously treated as a form of L. ovum, but more likely to be distinct (Berthold, 1990, Fig. 36; Brown & Berthold, 1990, Figs 38,39). HABITAT AND DISTRIBUTION. Standing and slowly flowing waters in the coastal region of East Africa, and in Zanzibar (Mozley, 1939, L. olivaceus).

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Lanistes grasseti (Morelet, 1863, Ampullaria). Type locality: Madagascar, no precise details. Fig. 29e. 35×30 mm. Like L. ovum, but commonly with strong ribs overlain by flaps of periostracum. HABITAT AND DISTRIBUTION. Madagascar: irrigation channels in the lower Mangoky region (Degrémont, 1973) and widespread in the south west (Fischer-Piette & Vukadinovic, 1973). Lanistes ellipticus Martens, 1866. Type locality: Zambezi River at Tete. Fig. 29d. 53×44 mm. Columellar margin straighter than in L. ovum; the fine transverse ridges give a silky lustre to the surface. Central tooth of characteristic shape (Mandahl-Barth, 1968a, 1972). Specimens from Lake Malawi were named L. affinis by Smith (1877). Shells from above the Victoria Falls, identified as L. ellipticus by Connolly (1939), were described as the new species L. connollyi by Pain (1954; see L. ovum). HABITAT. Clear streams flowing over gravel (Pilsbry & Bequaert, 1927); marsh beside Lake Malawi, but not found on the open lake shore (Crowley et al., 1964; Mandahl-Barth, 1972). DISTRIBUTION. An area including N Mozambique (Azevedo et al., 1961), SE Zaire (Pilsbry & Bequaert, 1927; Mandahl-Barth, 1968a) and Lake Malawi. 3) Lanistes (Leroya). Comparatively small species, with a strong shell and, typically, with the umbilicus closed. Although it is widely umbilicate, L. neritoides is included because it is closely related to the other species, according to the evidence of its small mantle cavity diverticulum (Brown & Berthold, 1990). Lanistes farleri Craven, 1880. Type locality: NE Tanzania, Magila (in Usambara district). Figs 29A,a. 32×28 mm. Whorls strongly shouldered, with numerous spiral ridges; columellar lip comparatively thin, not entirely fused to the body whorl, truncate at the base and forming an umbilical furrow; many brown bands. The species L. bourguignati and L. charmetanti of Grandidier (1887) are perhaps mature examples of the same species as farleri; their columellar lips are thick (as in L. graueri) and they might be a distinct species. HABITAT AND DISTRIBUTION. NE Tanzania: abundant in a stream (Craven, 1880a); basins of the Kyngani and Vouami (Wami) rivers (Grandidier, 1887); Usambara Mountains and further south, also Zanzibar (Martens, 1897); Muheza (N of Pangani, DBL); a record for the Malagarasi Delta of Lake Tanganyika (Bourguignat, 1889a) seems doubtful. Lanistes stuhlmanni Martens, 1897. Type locality: Tanzania, Dar-es-Salaam, from the market. Figs 29A,b. 28×24 mm. Like L. farleri in shape, but the whorls are less strongly shouldered and lack spiral ridges; columellar lip thick, entirely attached to the body whorl; no umbilical furrow. DISTRIBUTION. E Tanzania: type locality, also Mahenge (Germain, 1916, L. farleri variety alirata) and Ifakara (DBL, BME).

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Fig. 29. (a) L. ovum; Mozambique (syntype BMNH). (b) L. purpureus; Kenya, south coast, (c) L. ovum; Zimbabwe, Zambezi River, Victoria Falls (representing L. connollyi Pain; BMNH, identified as L. ellipticus by M.Connolly). (d) L. ellipticus; Lake Malawi (syntype of L. affinis Smith, BMNH1877.9.28.25). (e) L. grasseti; Madagascar (syntype, BMNH1893.2.4.1810–12). Scale line: 20 mm.

Lanistes graueri Thiele, 1911. Type locality: E Zaire, between Uvira and Kasongo. Figs 29A,c. 26×24 mm. Like L. stuhlmanni in its shape, smooth surface and umbilical area, but the whorls are more strongly shouldered and even carinate. DISTRIBUTION. E Zaire and ?Tanzania (Brown & Mandahl-Barth, 1987).

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Fig. 29A. (a) Lanistes farleri; Tanzania, Magila (syntype, BMNH1891.3.7.36–38). (b) L. stuhlmanni; Tanzania, near Ifakara. (c) L. graueri; Zaire, Nsendwe. (d) L. neritoides; Republic of the Congo (holotype, MNHN). (e) Marisa cornuarietis; Trinidad. Scale lines: 10 mm.

Lanistes neritoides Brown & Berthold, 1990. Type locality: Republic of the Congo, about 85 km NE of Pointe Noire, in a tributary of the Kouilou River. Figs 29A,d,d′. 14×15 mm. Small for the genus, shell globose and thick-walled; whorls expanding rapidly, shouldered and may have strong ribs; lip oblique, columellar margin thick; umbilicus open, with angulation. Animal with a small lung sac, weak jaw and reduced radular denticles. HABITAT AND DISTRIBUTION. Apparently adapted for life at or above the surface of rapidly flowing water, by the compact neritiform shell and anatomical

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specialisations, related to feeding on detritus and breathing atmospheric air. Known from only the type locality in the Republic of the Congo. Genus Afropomus Pilsbry & Bequaert, 1927 Shell ovate, thick-walled, with convex whorls; columellar thick, umbilicus closed; brown with one or more spiral bands; usually decollate when adult. Operculum entirely corneous. Central tooth with long basal lobes (Fig. 36b). According to the anatomy, especially of the copulatory organ, this group is more primitive than other living Ampullariidae (Berthold, 1988, 1989). One known species; in West Africa. Afropomus balanoidea (Gould, 1850, Ampullaria). Type locality: Liberia, Cape Mount. Fig. 30a. 23×20 mm. Characters as for the genus. The subspecies nimbae Binder, 1963 from the highland of Ivory Coast has a comparatively high spire. HABITAT. Ditches, creeks, small rivers (Hubendick, 1977); adapted to an amphibious mode of life and aestivation, according to its anatomy (Berthold, 1988). DISTRIBUTION. Liberia, Ivory Coast, Sierra Leone. Genus Saulea Gray, 1867 Shell ovate, whorls strongly shouldered or carinate; thin-walled, with strong periostracum but a very weak calcareous layer; early whorls with spiral rows of bristles of periostracum; umbilicus narrowly open. The shell colouration of highly varied patterns of brown and yellow is unique among African freshwater snails. The copulatory organ (Berthold, 1989) is little more evolved than that of Afropomus. One known living species, in West Africa; fossil shells identified from East Africa (Verdcourt, 1963; Pain & Beatty, 1964). Saulea vitrea (Born, 1780, Helix). Type locality: not given. Fig. 30b. 45×36 mm. Characters as for the genus. HABITAT. Small streams, pools and swamps (Hubendick, 1977). DISTRIBUTION. Liberia: Sherboro River (Gray, 1867). Sierra Leone: western lowlands (Hubendick, 1977) and in the east near Masingbi (White et al., 1989). Genus Marisa Gray, 1824 Shell large and discoid, whorls rounded; aperture large; colouration yellowish with a few to many dark spiral bands. Operculum concentric, entirely corneous. Copulatory organ more complex than in ampullariid genera native to Africa (Berthold, 1989). Neotropical region (3 species); one species introduced into Africa. Type species: Marisa intermedia Gray, 1824. Marisa cornuarietis (Linnaeus, 1758, Helix). Figs 29A,e,e′.

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Fig. 30. (a) Afropomus balanoidea; Sierra Leone, (b) Saulea vitrea; Sierra Leone, Njala (range of colour pattern). Scale line: 20 mm.

25 mm (aperture height)×50 mm (diameter). Characters as for the genus. HABITAT AND DISTRIBUTION. Standing or slowly flowing water, including irrigation channels. Native to northern S America and the West Indies. Introduced into Africa for the purpose of controlling intermediate hosts for schistosomes; field or semi-field trials conducted in Egypt, Sudan and Tanzania (see Chapter 8: Biological Control). Family Valvatidae Shell small, dextral, discoid to ovate, with a large umbilicus. Operculum circular, corneous and multispiral (Fig. 8g). Hermaphrodite and oviparous. With a feather-like gill and a tentacle-like appendage on the mantle margin, at the

76 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

right side. Central tooth without basal denticles. The systematic position of these unusual prosobranchs is uncertain (Rath, 1988). One genus is widespread in fresh waters of the northern hemisphere. Genus Valvata Müller, 1774 Characters as for the family. In lakes, permanent pools and slowly flowing streams. N America, Europe, Asia, Near East and NE Africa. In Africa, one species now lives in Egypt and Ethiopia: the Late Pleistocene-Holocene distribution was considerably more extensive. Type species: Valvata cristata Müller, 1774, Denmark, Frederiksdal (NW of Copenhagen). Valvata nilotica Jickeli, 1874. Type locality: Egypt, Mahmudi Canal near Alexandria. Fig. 31. 3.3×5.0 mm (Egyptian shell). Shell depressed, with very fine ribs and spiral sculpture; colourless or pale brown. Height of spire and size of umbilicus are highly variable (no less than 12 taxa from Egypt were recognised by Innes, 1884). Ethiopian shells are comparatively large and high-spired (Fig. 31); they have been distinguished as subspecies V. n. scioana Pollonera, 1888 (Bacci, 1940; Brown, 1980a). Gill structure investigated by Rath (1988, Valvata ‘sp. II’ from Cairo). V. nilotica is perhaps the same species as V. saulcyi Bourguignat of the near East (Mienis, 1970, as V. piscinalis; Tchernov, 1971, 1975a; Burch, 1985). HABITAT. Lakes, slowly flowing rivers, streams amd irrigation channels; usually in vegetation, but on coarse sand at 3 m depth in Lake Tana (Brown, 1980a). DISTRIBUTION. Egypt, lower Nile; abundant in drains. Ethiopia: living in the highland area from Akaki (Ayad, 1956) northwards to Lake Tana, common in the Debra Berhan area (Brown, 1965, Valvata sp.); subfossil shells further south near Lake Zwai (Bacci, 1940; Grove et al., 1975). N Sudan: ‘modern’ and fossil shells near the 2nd Nile Cataract (Martin, 1968). The late Pleistocene-Holocene distribution of Valvata was much greater (Van Damme, 1984), extending into Chad, Libya and SE Algeria (V. tilhoi Germain, 1909; Fischer-Piette, 1948, 1949). Confirmation is desirable of other identifications of Valvata from Algeria (Hagenmüller, 1884), Somalia (Bourguignat, 1889a), near Lake Turkana (Rudolf) (Van Damme & Gautier, 1972) and SE Ethiopia (Fischer-Piette & Métivier, 1974). Family Littorinidae Cosmopolitan in marine and brackish habitats; species of Littoraria Griffith & Pidgeon, 1834 occur in mangrove forests and saltmarsh in tropical and subtropical areas (Reid, 1986). Littoraria (Littorinopsis) spp. Fig. 68g. Shell medium to large, with a sharp conical spire and spiral grooves; the varied dark markings of short dashes

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Fig. 31. Valvata nilotica; Ethiopia, Debra Berhan. Scale line: 2 mm.

sometimes form oblique bands. Operculum corneous, paucispiral. L.(L.) scabra (Linnaeus, 1758) and 3 other species occur on the eastern coast of Africa, usually in mangrove habitats and saltmarsh, from the northern Red Sea southwards, nearly to Port Elizabeth (Reid, 1986). On the West coast, L.(L.) angulifera (Lamarck, 1822) is known from similar habitats, in the Zaire estuary (Pilsbry & Bequaert, 1927) and in Sierra Leone and Nigeria (BME). Family Hydrobiidae The definition and relationships of this family have been extensively discussed in recent years (e.g. Davis et al., 1985; Ponder, 1988a; Kabat & Herschler, 1993). A distinction is now made between the Hydrobiidae, narrowly defined according to characters of the female reproductive organs (Davis, 1979), and the Pomatiopsidae (which includes the African genus Tomichia, formerly placed in the Hydrobiidae). For lack of knowledge of anatomy, it is not yet possible to place most of the tropical African ‘hydrobioid’ species in their proper family. Shell small, dextral, discoid to narrowly conic, with a high spire and usually smooth and colourless. Operculum thin, usually entirely corneous, paucispiral to multispiral. Female oviparous or ovoviviparous, with a distinctive anatomy (Davis, 1979). Male with penis attached to the right side of the head-foot, lacking a penial appendage of the bithyniid type. Central radular tooth with one or more pairs of basal denticles. The Hydrobiidae, narrowly defined, is a family characteristic of fresh and brackish water in the northern continents. It seems well-represented in NW Africa, but rare in the tropical region. Two subfamilies are represented in Africa, the Hydrobiinae and the Cochliopinae (Littoridininae). Hydrobiinae. Defined by a combination of character states, which do not allow a concise diagnosis (Davis et al., 1985; Hershler & Thompson, 1992).

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1) Hydrobiinae in North Africa

For NW Africa, the taxonomic picture is complex; the present treatment is restricted to brief notes. Numerous species assigned to Hydrobia Hartmann, 1821 are founded on shells from Algeria and Morocco (Bourguignat, 1864; Morelet, 1880; Backhuys & Boeters, 1974); anatomical studies are needed to determine their true generic positions. Boeters (1976) listed 28 species with type localities in Tunisia alone; some placed in Hydrobia, others in Pseudamnicola Paulucci, 1878 and Mercuria Boeters, 1971. Pseudamnicola is a palaearctic group of globose freshwater snails, including the North African P. dupotetiana (Forbes, 1838) (Fig. 33a). For Morocco and Algeria, Kristensen (1985) distinguished, according to the shell alone, 8 genera: Belgrandia Bourguignat, Bythinella Moquin-Tandon, Hadziella Kuščer, Heideella Backhuys & Boeters, Horatia Bourguignat, Hydrobia, Peringia Paladilhe and Pseudamnicola. Hydrobia apparently is widespread in N Africa. Van Damme (1984) recognised three species, all now living mainly near the coast, though H. aponensis once extended far southwards into the present Sahara. Hydrobia ventrosa (Montagu, 1803). Fig. 32b. Whorls strongly convex. A palaearctic species, known from brackish water in Tunisia and Egypt, at Birket Qarun (Van Damme, 1984). H. musaensis Frauenfeld, 1855. Fig. 32c. Whorls rather flat, sutures shallow. In fresh and brackish waters in lower Egypt and Sinai (Crawford, 1949; Tchernov, 1971; Van Damme, 1984). Possibly the same species as H. lactea (Küster, 1853) of the Near East; relationships between the hydrobiids of this region (Burch, 1985) and of Africa require further investigation. H. aponensis Martens, 1858. Fig. 32a. Shell comparatively large and slender. Fresh and brackish waters in NW Africa and some other Mediterranean countries (Backhuys & Boeters, 1974; Boeters, 1976). This species is known, according to Van Damme (1984), also by the names Hydrobia (or Paludestrina) peraudieri and duveyrieri, both of Bourguignat. Its Late Pleistocene-Holocene distribution is reported to have extended southwards into Mauritania, Niger and Chad. However, revision of this taxon is needed, as some of the forms included were placed in the genus Heleobia by Hershler & Thompson (1992; see under Hydrobiidae: Cochliopinae). 2) Hydrobiinae in tropical Africa and the southern coastal region.

The presence of any true hydrobiid on the eastern coast of Africa remains to be confirmed; a few species are assigned to this family, but are known from only shells, found in Eritrea, Somalia and on Socotra Island (Verdcourt, 1958a). On the southern coast one true species of Hydrobia is reported from brackish water (Davis, 1981, p. 235). None of the tropical species listed below, of Hydrobia or of Potamopyrgus, has been studied in enough anatomical detail to establish clearly its generic position. Species placed in Hydrobia follow in

FRESHWATER SNAILS OF AFRICA 79

Fig. 32. (a) Hydrobia aponensis. (b) H. ventrosa. (c) H. musaensis. From Van Damme (1984, Fig. 21). Scale line: 1 mm.

alphabetical order; by chance the last three are associated with rapidly flowing water in the lower Zaire River. Hydrobia accrensis Connolly, 1929a. Type locality: Ghana, quarry near Accra. Figs 33a,b; 37a. 4.5×2.0 mm. Shell slender when mature, with the spire nearly twice as high as the aperture; whorls regularly increasing; fine spiral ridges may be present; colour reddish-brown (syntypes, BMNH). DISTRIBUTION. Ghana: type locality and Yesor swamp near Ada (McCullough, 1965a). Togo: Lake Togo (DBL). Hydrobia gabonensis Morelet, 1885. Type locality: Gabon, Ogowe River. Fig. 34b. 5.5×3.0 mm. Broader than H. accrensis and whorls more convex. DISTRIBUTION. Gabon: type locality and Lake N’Dogou at Gamba (DBL). Hydrobia guyenoti Binder, 1955. Type locality: Ivory Coast, Toupah Bay in Lagune Ebrié. Fig. 33c. 2.7×1.8 mm. Whorls strongly convex, sutures deep. Central tooth with a single basal denticle on each side and long lateral lobes (Binder, 1955). Female viviparous (Binder, 1957). DISTRIBUTION. Ivory Coast: Lagune Ebrié, in fresh water.

80 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 33. Hydrobia. (a,b) H. accrensis; Ghana (syntypes, BMNH1928.8.1.1–20). (c) H. guyenoti; Ivory Coast (after Binder, 1955, Fig. 6, left), (d) H. lineata; Ivory Coast (holotype after Binder, 1957, Fig. 8). (e) H. schoutedeni; lower Zaire River (holotype after Bequaert & Clench, 1936, Pl. 1). (f) H. luvilana; Congo Republic (holotype after Mandahl-Barth, 1973b, Fig. 1). Scale line: 1 mm.

Hydrobia lineata Binder, 1957. Type locality: Ivory Coast, Bingerville Bay, in fresh water. Fig. 33d. 2.2×1.7 mm. Shell with numerous spiral ridges. Originally described from a globose juvenile (Fig. 33d); larger shells are more narrowly conic (DBL). Central tooth with a single basal denticle on each side and long lateral lobes (Binder, 1957). DISTRIBUTION. Ivory Coast: type locality. Togo: Togoville (DBL). Benin: Lac Toho Todougba (Chippaux et al., 1990, Hydrobia sp.; BME). Hydrobia luvilana Mandahl-Barth, 1973b. Type locality: Congo Republic, stream at Louvila (about 30 km inland from Pointe Noire and south of Loudima). Fig. 33f. 2.8×2.0 mm. Shell smooth. Central tooth with a single basal denticle on each side; copulatory organ attached on the right side (Mandahl-Barth, 1973b).

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Fig. 34. Hydrobiidae. (a) Pseudamnicola dupotetiana; Morocco, Fikh-Ben-Salah (DBL), (b) Hydrobia gabonensis; Gabon (after Morelet, 1885, Pl. 2). (c) H. rheophila; Lower Zaire River (holotype after Bequaert & Clench, 1941, Pl. 2, 4). (d) H. plena; lower Zaire River (holotype after Bequaert & Clench, 1941, Pl. 2, 10). Scale lines: 1 mm.

HABITAT AND DISTRIBUTION. Stream and a river; substrates of gravel with abundant vegetation (Mandahl-Barth et al., 1974). Congo Republic: type locality. W Zaire: river near Kisantu. Hydrobia plena Bequaert & Clench, 1936. Type locality: Zaire, rocks in swiftly flowing water of the Zaire River at Ango Ango (4 km south of Matadi). Fig. 34d. 1.8×2.1 mm. Globose, with open umbilicus. DISTRIBUTION. Zaire River near Matadi (Bequaert & Clench, 1941). Hydrobia rheophila Bequaert & Clench, 1941. Type locality: Zaire, stones in a swift current in the Zaire River at Kala Kala, near Matadi. Fig. 34c. 3.6×1.8 mm. Ovately conic, whorls weakly curved, umbilicus closed. DISTRIBUTION. Zaire River near Matadi; reported from only the type locality. Hydrobia schoutedeni (Bequaert & Clench, 1936, Lobogenes). Type locality: Zaire, same locality as H. plena. Fig. 33e. 2.8×1.8 mm. Like H. rheophila, but with fine spiral ridges. A Hydrobia according to Mandahl-Barth (1973b). DISTRIBUTION. Zaire River: reported from only the type locality.

82 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Genus Potamopyrgus Stimpson This is primarily a genus of fresh and brackish waters in New Zealand. P. antipodarum (Gray, 1843) is believed to have been introduced during the 19th century into Australia (Ponder, 1988b) and Europe, where it is known as P. jenkinsi (Smith) (Winterbourn, 1972). Although the following species was classified in this genus by Pilsbry & Bequaert (1927) and later authors, it has distinctive characters in the banding of the tentacles, presence of only a single pair of basal denticles on the central tooth, and the form of the spines on the shell (which have their bases aligned transversely, rather than longitudinally) (Brown, 1980b). Probably the African species will eventually be placed in a different genus. (?)Potamopyrgus ciliatus (Gould, 1850, Amnicola). Type locality: Liberia, muddy margins of the Deea River. Fig. 35a. 5.8×3.2 mm. Spire high, narrowly conic with shallow sutures, whorls bluntly angular at the periphery and rather flattened above; last whorl with a spiral row of thorn-like spines. Operculum entirely corneous; tentacles with transverse dark bands; central tooth (Fig. 36c) with deep basal projection, slender lateral lobes and a single pair of basal denticles (Brown, 1980b). HABITAT. Burrows made by shipworms (Teredo) in the aerial roots of mangroves (Bequaert & Clench, 1941); found in specimens of the aquatic plant Jussiaea repens sent to a herbarium (Verdcourt, 1976); on moist mud beneath mangrove trees (Brown, 1980b). DISTRIBUTION. Coastal localities from Liberia to Cameroon, and the Zaire River between Malela and Banana. Subfamily Cochliopinae (=Littoridininae). Defined by a combination of anatomical character states; not necessarily a monophyletic group (Davis et al., 1985; Hershler & Thompson, 1992). The genus Heleobia Stimpson, 1865 occurs in S America, Europe, SW Asia and NW Africa, according to Hershler & Thompson (1992), who place in this group both Hydrobia aponensis and H. duveyrieri of Van Damme (1984; see above under Hydrobiinae). Genus Lobogenes Pilsbry & Bequaert, 1927 Small, shell ovately conic, spire slightly higher than aperture; outer lip sinuous (Fig. 35b), columellar lip thickened and usually closing the umbilicus. Operculum entirely corneous, paucispiral. Central tooth with one pair of basal denticles (Mandahl-Barth et al., 1972; Hershler & Thompson, 1992). Female ovoviviparous; genital anatomy of both sexes of L. michaelis described by Hershler & Thompson. Streams in central Africa; 3 species. Type species: Lobogenes michaelis Pilsbry & Bequaert, 1927, Zaire.

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Fig. 35. Hydrobiidae. (a) (?) Potamopyrgus ciliatus; Ghana, Ada. (b) Lobogenes pusilla; SE Zaire (paratype, DBL), (c) L. spiralis; SE Zaire, Likasi (DBL), (d) L. michaelis; SE Zaire, near Lubumbashi (DBL). Scale lines: 1 mm.

Lobogenes michaelis Pilsbry & Bequaert, 1927. Type locality: SE Zaire, source of the Kimililo River, near Elizabethville (Lubumbashi). Fig. 35d. 4.4×3.0 mm. Lip strongly sinuous; spiral sculpture, if present, is fine. HABITAT. Highly varied, including streams flowing over gravel (Pilsbry & Bequaert, 1927), muddy pools beside the Kafue River, and a warm salty spring where snails lived among blue-green algae (P.Obrdlik, unpublished observations, 1985). DISTRIBUTION. SE Zaire: Lubumbashi area (Pilsbry & Bequaert, 1927; Mandahl-Barth, 1968a) and Lake Katebe (Hershler & Thompson, 1992). Zambia: Kafue River, south of Kafue and Moshi Salt Spring in Kafue National Park (BME). Lobogenes spiralis Pilsbry & Bequaert, 1927. Type locality: SE Zaire, source of the Kimililo River near Elizabethville (Lubumbashi). Fig. 35c. 3.7×2.3 mm. Smaller than L. michaelis, more slender, lip less sinuous, spiral sculpture distinct (Hershler & Thompson, 1992, figured a paratype). DISTRIBUTION. SE Zaire: type locality and in affluents of the Lac de Retenue on the Lufira River (Mandahl-Barth et al., 1972).

84 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 36. Central teeth of radula. (a) Lanistes ovum; Kenya, (b) Afropomus balanoidea; Sierra Leone, (c) (?)Potamopyrgus ciliatus; Ghana, (d) Tomichia natalensis; Zululand. (e) Gabbiella humerosa; Lake Victoria, (f) G. walleri; Lake Albert, (g) G. barthi; Kenya. Scale lines: 0.01 mm (c–g) or 0.1 mm (a,b). Guide lines indicate basal denticles in (d) and the basal lobe in (e).

Lobogenes pusilla Mandahl-Barth in Mandahl-Barth et al., 1972. Type locality: SE Zaire, Kibovu River, an affluent of the Lac de Retenue. Fig. 35b. 3.1×2.0 mm. Smallest species in the genus; lacking spiral sculpture. HABITAT AND DISTRIBUTION. Known only from the type locality in SE Zaire; found on decomposing reeds. Family Pomatiopsidae Shell small to medium, discoid to turreted. Operculum thin, corneous, paucispiral. Female oviparous; genital anatomy distinct from that of Hydrobiidae (Davis, 1979, 1981). Male with simple penis, lacking appendages. Central tooth with 2 or more pairs of basal denticles. Two subfamilies. The Triculinae occur in an arc from India to the Philippines and include a remarkable radiation of species, some with strongly ornamented

FRESHWATER SNAILS OF AFRICA 85

shells, especially in the Mekong River. The Pomatiopsinae occur in S America, N America, Asia and Africa (the single genus Tomichia); this group includes the genus Oncomelania Gredler, which transmits Schistosoma japonicum. Genus Tomichia Benson, 1851 Shell small, ovately conical to turreted; spire commonly decollate, smooth or with spiral sculpture. Operculum corneous, paucispiral. Central tooth with 2 or 3 pairs of basal denticles. Distinctive combination of features in the genital anatomy (Davis, 1979). In saline, brackish and fresh water. Seven species in the southern coastal region of Africa (Davis, 1981) and 3 species, though of uncertain generic position, reported from central Africa. Type species: Truncatella ventricosa Reeve, 1842, between Cape Town and Simonstown. Tomichia of South Africa

Tomichia ventricosa (Reeve, 1842, Truncatella). Type locality: South Africa, Lakeside (Muizenberg Vlei), between Cape Town and Simonstown, designated by Connolly (1939). Figs 37c; 38a,b. 8.3×3.2 mm; 10.7×3.0 mm (form producta). Shell narrowly conical (turreted), with convex regularly increasing whorls; sometimes with spiral sculpture. T. producta Connolly (1929b, Eerste River, Cape Flats) is extremely slender, with up to 10 strongly convex whorls (Fig. 37c); it is considered by Davis (1981, p. 230) to be a form of T. ventricosa found mostly in pans. Anatomy described in detail by Davis (1981). HABITAT. Rivers, coastal wetlands and estuaries; also in vleis and pans that dry out seasonally, becoming highly saline (Davis, 1981). DISTRIBUTION. South Africa, south-western coastal area; the habitats for this and other species of Tomichia are vulnerable to destruction by man. Tomichia zwellendamensis (Küster, 1852–3, Paludina). Type locality: South Africa, lakes and streams in the Zoetendal Valley near Agulhas. Fig. 38c. 6.7×2.0 mm. Shell turreted, smooth, fragile with a thin lip. HABITAT AND DISTRIBUTION. South Africa: W Cape, Agulhas area, in fresh water on stems of sedge or bottom of lakes and ponds (Davis, 1981). Tomichia tristis (Morelet, 1889, Hydrobia). Type locality: South Africa, Port Elizabeth. Figs 37b; 39d. 6.0 ¥ 2.7 mm. Shell more broadly turreted than T. ventricosa, transverse and spiral sculpture may be strong, sometimes malleate; colour brownish. Assiminea lirata Turton, 1932 (Port Alfred) (Fig. 39d) {(?)Tomicbia lirata Connolly, 1939 of Brown, 1980a} is a synonym according to Davis (1981, p. 225). HABITAT AND DISTRIBUTION. Amphibious, high on shore of saline lagoon (Davis, 1981). South Africa: type locality, Jeffreys Bay and possibly Port Alfred.

86 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 37. Hydrobiidae, Pomatiopsidae (Tomichia) and Bithyniidae (Soapitia). (a) Hydrobia accrensis; Ghana (syntype, BMNH1929.8.1.1–20). (b) Tomichia tristis; Port Elizabeth (syntype, BMNH1893.2.4.1914–19). (c) T. ventricosa; Cape Flats (syntype of T. producta Connolly, BMNH1937.12.30.6049–54). (d) T. differens; Western Cape (syntype, BMNH1937.12.30.6055– 70). (e) T. cawstoni; Kokstad (syntype, BMNH1937.12.30. 6084–95). (f) T. natalensis; Natal (syntype, 1937.12.30.6071–4). (g) Soapitia dageti; Guinea (paratype, BMNH1967.047). Scale line: 2 mm.

Tomichia rogersi (Connolly, 1929, Hydrobia). Type locality: South Africa, Stinkfontein, Little Namaqualand, W Cape. Figs 38d,e. 6.5×3.0 mm (complete paratype); but the last 3 whorls alone can be 7 mm long (Davis, 1981). Largest species in the genus; shell like T. tristis but smoother; colour dark brown (paratypes, BMNH). HABITAT AND DISTRIBUTION. Seepages from isolated freshwater springs; the snail tends to be amphibious. South Africa: Namaqualand (Connolly, 1939; Davis, 1981). Tomichia natalensis Connolly, 1939. Type locality: South Africa, Natal Province, Lower Umkomaas. Figs 37f; 38f,g. 6×3 mm. Ovately conical with narrowly tapered spire; juveniles bluntly angular at periphery of whorl; lower lip may be somewhat angular; peristome with brown rim. Female anatomy unique (Davis, 1981).

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Fig. 38. Pomatiopsidae. (a,b) Tomichia ventricosa; Western Cape, Simonstown. (c) T. zwellendamensis; Western Cape (after Connolly, 1939, Fig. 47E). (d,e) T. rogersi; Little Namaqualand (syntypes, BMNH1937.12.30.6075–83). (f,g) T. natalensis; Natal, Ibati River. Scale lines: 1 mm.

HABITAT. Freshwater streams with pulmonates (Brown, 1980a); primarily amphibious on mud slopes shaded by vegetation (Davis, 1981). DISTRIBUTION. South Africa, Natal Province: formerly at Umkomaas (type locality) and perhaps Durban (T. ventricosa of Porter, 1938), but more recently found only between Empangeni and Gingindlovu. Tomichia differens Connolly, 1939. Type locality: South Africa, W Cape Province, streams flowing out of limestone cave ‘Die Kelders’. Figs 37d; 39a,b,

88 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 39. Pomatiopsidae. (a,b) Tomichia differens; Western Cape (syntypes, BMNH1937. 12.30.6055–70). (c) ‘Tomichia’ alabastrina; Port Elizabeth (BMNH1911.8.8.56–8). (d) T. tristis; Cape Flats (T. lirata (Turton), after Connolly, 1939, Fig. 47j). (e) T. hendrickxi; E Zaire (syntype, BMNH1951.5.21.85–93). (f) T. kivuensis; E Zaire (paratype, DBL). Scale line: 1 mm.

5.0×2.7 mm. Spire comparatively low, with slightly curved sides and shallow sutures; colour pale brown, glossy (paratypes, BMNH). HABITAT AND DISTRIBUTION. Perennial freshwater streams and small rivers; tolerant of low salinity and brief desiccation (Davis, 1981). South Africa: W Cape Province, De Kelders and eastwards to Stilbaai. Tomichia cawstoni Connolly, 1939. Type locality: South Africa, E Cape Province, Kokstad. Fig. 37e. 4.6×2.5 mm. Spire comparatively short and flat-sided; whorls only weakly convex.

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DISTRIBUTION. South Africa: E Cape Province, known only from the type locality and apparently now extinct (Davis, 1981). (?)Hydrobia alabastrina Morelet, 1889. Type locality: South Africa, Port Elizabeth. Fig. 39c. Although this species was classified as a Tomichia with doubt by Connolly (1939) and with support from Van Bruggen (1970a), the 3 types (BMNH) vary widely (Brown, 1980a) and were found by Davis (1981, pp. 222, 261) to comprise a species of Hydrobia (the holotype) and one of Rissoa. Tomichia in central Africa

It has yet to be shown that these taxa are in fact Tomichia; available morphological data, restricted to shell and radula, are insufficient for assessing relationships (Davis, 1981, p. 234). Tomichia hendrickxi (Verdcourt, 1950, Hydrobia). Type locality: E Zaire, Kakondo, near SW shore of Lake Kivu. Fig. 39e. 5.4×2.7 mm. Spire with slightly curved sides, whorls only weakly convex; last whorl large, contributing nearly three-quarters of the total height; colour pale brown (paratypes, BMNH). Transferred to Tomichia because of the structure of central radular tooth (Verdcourt, 1951). HABITAT. Collected with the pondweed Lemna from a small hot-water pond (35–40°C) in area of volcanic activity (Verdcourt, 1951). DISTRIBUTION. E Zaire: near the SW shore of Lake Kivu (Verdcourt, 1960a). Tomichia kivuensis Mandahl-Barth, 1974. Type locality: E Zaire, Ruzizi Plains, plantation at Lubarika (27 km S of Bukavu). Fig. 39f. 5×2.7 mm. Distinguished from T. hendrickxi by the broader shell, shorter spire and different central tooth (Mandahl-Barth, 1974). HABITAT. Most abundant in the rapidly flowing (0.32–0.37 m sec−1) part of a stream, on a substratum of gravel and pebbles (Baluku et al., 1989). DISTRIBUTION. E Zaire: Ruzizi Plains and Lwiro in the highland W of Lake Kivu (Baluku et al., 1989). (?)Tomichia guillemei Leloup, 1953. Type locality: Lake Tanganyika, W shore, Moba Bay (7°S), dredged from 20 m. 3.4×1.5 mm. Small, with obtuse apex and 4–5 regularly increasing whorls; spire nearly twice height of aperture. Operculum and animal unknown; possibly a terrestrial species. Reported only from type locality. (?)Tomichia n.sp. Reported living on the littoral rocky bottom of Lake Turkana, north of Ferguson’s Gulf, on small cobbles and plants (Cohen, 1986, p. 188). Taxonomic position uncertain; I have not seen a specimen.

90 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Family Bithyniidae Shell small to medium-sized, dextral, depressed to ovately conic and somewhat more slender. Operculum thick and calcareous, with outer concentric area and usually a spiral nucleus. Exhalent siphon (epitaenial fold) usually present on the right side, in connection with the ciliary feeding mechanism. Female oviparous. Penis with accessory appendage and duct (hold-fast organ). Egg capsules (so far as known) with definite exit holes closed by plugs. Central radular tooth usually with basal denticles. Cosmopolitan in fresh waters, apart from the Americas. In Africa 9 genera, of which 8 are endemic. Genus Bithynia Leach, 1818 Shell small to medium, ovately conic. Operculum heavily calcareous, mainly concentric, with a small spiral nucleus. Europe, Near East, Asia and NW Africa. Although no Bithynia is known to occur in Egypt or in Sinai, the genus inhabits Israel (Tchernov, 1975a) and Jordan (Burch, 1985), and a possibly extinct population is known in NW Saudi Arabia (Brown & Wright, 1980). B. tentaculata (Fig. 40a) has been found in Morocco (BMNH) and Algeria (Bourguignat, 1864), but apparently not in recent years. Genus Gabbiella Mandahl-Barth, 1968 Shell small, depressed to ovately conic and somewhat more slender; colourless to pale brown. Operculum with calcareous layer extending to margin, lodging at or near the apertural lip; spiral nucleus occupying 1/6 to 4/5 of diameter. Exhalent siphon varying in size among species and lacking from some (Brown, 1988). Egg capsule contains one egg; capsules laid singly (Mandahl-Barth, 1972, Fig. 2) or in chains (Brown, 1975a, Fig. 5) of 2 to at least 10. Central tooth (Figs 36e–g) with 2–5 pairs of basal denticles. In lakes, rivers and less commonly small waterbodies; rarely in habitats that dry out. Africa: Egypt and southwards to the Okavango Delta (Fig. 71). About 20 species, arranged here in the system of Mandahl-Barth (1968b). Most species are confined to the central tropical region and only 3 are at all widespread (humerosa, kisalensis and senaariensis). Type species: Bithynia stanleyi variety humerosa Martens, 1879, Uganda. Subgenus Gabbiella sensu stricto. Radula comparatively large; base of central tooth with long pointed side lobes. A. The humerosa group. Medium-sized species with the spire less high than the aperture, and a somewhat angular last whorl. Gabbiella humerosa (Martens, 1879, Bithynia stanleyi var. humerosa). Type locality: Uganda, SW shore of Lake Victoria. Fig. 40b. 6.2×5.0 mm. Globose or slightly higher; whorls somewhat shouldered and flattened at the periphery, fine spiral sculpture may be present; umbilicus usually

FRESHWATER SNAILS OF AFRICA 91

open; colour light grey to dark brown. Operculum with large spiral nucleus occupying about 2/3 of total width. Central tooth (Fig. 36e) broader than long, with long lateral lobes and 4 or 5 basal denticles on each side. Mandahl-Barth (1968b) recognised 6 subspecies. HABITAT AND DISTRIBUTION. Mainly large lakes (Mandahl-Barth, 1968b). Lake Victoria, abundant on fine sediment down to at least 12m depth (typical form). Victoria Nile and Lake Kyoga (G. h. kyogae). Lake Albert (G. h. alberti) in shallow water. Lake Edward (G. h. edwardi). Lake Kivu and upper Ruzizi River (G. h. kivuensis). Lake Tanganyika (G. h. tanganyicensis), in tributaries and marshes (Leloup, 1953, as ‘Bithynia alberti’; Brown & MandahlBarth, 1987). Gabbiella kichwambae (Mandahl-Barth, 1954, Gabbia). Type locality: W Uganda, Kichwamba crater lake. Fig. 40c. 7.3×5.7 mm. Similar to the less angular form of G. h. humerosa, but growing larger and with a higher spire (Mandahl-Barth, 1968b). DISTRIBUTION. W Uganda: crater lakes at Kichwamba and Fort Portal, and in Lake Lutoto. Gabbiella matadina Mandahl-Barth, 1968b. Type locality: W Zaire, reservoir at Matadi. Fig. 42a. 4.2×3.7 mm. Small and globose. DISTRIBUTION. W Zaire: known only from the type locality. Gabbiella neothaumaeformis (Germain, 1907; 1908, pl. 5, Bythinia). Type locality: Lake Chad, SE shore. 5×4.5 mm. Known from only the 4 original shells, with shouldered whorls; apparently related to G. humerosa according to Mandahl-Barth (1968b). B. The kisalensis group. Fully grown shell less than 5 mm high; spire shorter than aperture. Gabbiella kisalensis (Pilsbry & Bequaert, 1927, Bulimus). Type locality: SE Zaire, Lake Kisale at Kikondja. Fig. 40e. 4.2×3.7 mm (usually smaller). Small, globose, whorls rapidly increasing. Operculum with spiral part occupying about half the width. HABITAT. Brook with a gravelly bottom (Pilsbry & Bequaert, 1927); on sticks and debris in a river (Wright, 1963a); slowly flowing water and residual pools on flood-plains (Brown et al., 1992). DISTRIBUTION. SE Zaire and Zambia (Mandahl-Barth, 1968b). N Mozambique (Azevedo et al., 1961, as Gabbia humerosa). Gabon: Lambaréné area (BME). Angola: Cuije River (Wright, 1963a). NE Namibia and N Botswana: Okavango Delta (Brown et al., 1992). Gabbiella parva (Mandahl-Barth, 1954, Gabbia). Type locality: W Uganda, small stream below Kichwamba Hotel. Fig. 42b. 2.9×2.5 mm. Very small and globose. Shell like young G. humerosa, but the operculum, radula and copulatory organ are distinctive (Mandahl-Barth, 1968b). DISTRIBUTION. W Uganda: type locality and Lake Bunyoni (MandahlBarth).

92 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 40. Bithyniidae. (a) Bithyia tentaculata; Morocco, Mogador. (b,b′) Gabbiella humerosa; Lake Victoria, Kisumu. (c) G. kichwambae; W Uganda, Lake Kichwamba. (d) G. parvipila; NE Kenya (paratype, BMNH 1968.165). (e) G. kisalensis; Angola, Cuije River, (f) G. verdcourti; Kenya, Taveta. (g) G. tchadiensis; Lake Chad, (h) G. stanleyi; Lake Malawi (syntype, BMNH1887.12.2.10–16). Scale line: 2 mm.

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Gabbiella parvipila (Verdcourt, 1958a, Incertihydrobia). Type locality: NE Kenya, Lake Jilore near Malindi. Fig. 40d. 5×4 mm. Shell globosely conic, apex obtuse. Operculum with very large spiral part occupying 4/5 of its width (Mandahl-Barth, 1968b). HABITAT. Collected from Ceratophyllum plants in Lake Jilore (Verdcourt, 1958a), but I could not find water in that area in December 1975. Ponds, canals and drains in Somalia (Arfaa, 1975). DISTRIBUTION. Kenya: type locality and the nearby Lake Chem Chem. Somalia: Giuba and Webbi Shebelli river valleys. Gabbiella verdcourti Mandahl-Barth, 1968b (Incertihydrobia sp. Verdcourt, 1958a). Type locality: Kenya, Salemba stream near Taveta. Fig. 40f. 4.7×3.8 mm. Like G. parvipila, but apex more pointed and with distinctive reddish-brown colour. Central tooth with only 2 or 3 basal denticles on each side; the smallest number in the genus (Brown, 1975a). HABITAT AND DISTRIBUTION. Stream and a spring-fed pool, on fallen branches and leaves; SE Kenya, Taveta district. Gabbiella spiralis Mandahl-Barth, 1968b. Type locality: Zaire River, just below Kinshasa. Fig. 42c. 4.1×3.2 mm. Shell globosely conic, with strong spiral ridges visible at magnification×6; whorls somewhat shouldered. DISTRIBUTION. Zaire River: numerous localities near Kinshasa (DBL). Gabbiella tchadiensis Mandahl-Barth, 1968b. Type locality: Lake Chad, SE shore at Bol. Fig. 40g. 5×3.5 mm. Shell globosely conic, whorls evenly convex, sutures deep. Although first described from small imperforate shells, larger specimens from Infesafari (BME) have an open umbilicus and fine spiral sculpture. HABITAT. Amongst Vallisneria plants and debris in Lake Léré (Dejoux et al., 1971); abundant in Ceratophyllum beds in Lake Chad (Lévêque, 1975). DISTRIBUTION. Lake Chad and Yobe River at Yo (DBL); Lake Léré (350 km S of Lake Chad). Late Pleistocene-Holocene distribution more extensive in the Chad Basin (Van Damme, 1984). C. The stanleyi group

Gabbiella stanleyi (Smith, 1877, Bythinia). Type locality: Lake Malawi (Nyasa). Fig. 40h. 5.3×3.5 mm. Shell thick-walled and of variable shape (Crowley et al., 1964); like G. kisalensis or with higher spire. Central tooth of characteristic shape (Mandahl-Barth, 1968b). Egg capsule with single egg (Mandahl-Barth, 1972). HABITAT AND DISTRIBUTION. Lake Malawi: commonest in littoral zone down to about 12m, though one specimen was obtained from 95 m (MandahlBarth, 1972). Active at night on leaves of Vallisneria and preyed on by cichlid fishes (Louda et al., 1983; McKaye et al., 1986).

94 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

D. The senaariensis group. Comparatively large species with the spire higher than the aperture and a relatively long central tooth. Gabbiella neumanni (Martens, 1897, Bithynia). Type locality: Tanzania (Tanganyika), pond Monlo-Sakassigan, Masai Steppe. Fig. 42d. 5.7×4.3 mm. Shell similar to G. senaariensis and G. subbadiella (see G. adspersa) according to Verdcourt (1960b) who studied the types. Martens illustrated 3 basal denticles on either side of the central tooth. Later records apparently refer to other species (Mandahl-Barth, 1968b). DISTRIBUTION. Tanzania: type locality and possibly represented by specimens from the Malagarasi River, NE of Kasulu (BME). Gabbiella senaariensis (Küster, 1852, Paludina). Type locality: Sudan, Senaar. Fig. 41b. 8.5×5.5 mm. Shell large for the genus, spire distinctly higher than the aperture, often decollate; 4 whorls completed at about 5 mm height. Subspecies G. s. ugandae was defined by its smaller size and differently-shaped central tooth (Mandahl-Barth, 1968b), but there does not appear to be a clear geographic pattern in size variation (Brown, Fison et al., 1984). ‘Bythinia’ tilhoi Germain, 1912b, 1916, from Niger, known only from the shell, possibly represents an isolated western population (Mandahl-Barth, 1968b). HABITAT. Lakes, rivers, pools and irrigation channels (Brown et al., 1984). DISTRIBUTION. Egypt; Sudan, 2nd Nile Cataract (‘modern’ shells of Bithynia and Gabbia; Martin, 1968) and White Nile (Mandahl-Barth, 1968b; Brown, Fison et al., 1984); Uganda and Chad (Mandahl-Barth, 1968b); Central African Republic, Lake Léré (Dejoux et al., 1971). Gabbiella schweinfurthi (Jickeli, 1874, Hydrobia). Type locality: Sudan, White Nile. 3.3×2.2 mm (shell from Jonglei). Like a juvenile G. senaariensis, but more slender and with the whorls increasing less rapidly, 4 being completed at about 3. 6 mm height. HABITAT AND DISTRIBUTION. Lagoons with Eichhornia plants; S Sudan, Jonglei area (Brown, Fison et al., 1984). Gabbiella africana (Frauenfeld, 1862, Bythinia). Type locality: West Africa (without detail). Fig. 42e. 9×6.6 mm. Largest species in the genus; whorls strongly and evenly convex, smooth or with spiral sculpture; umbilicus narrow to moderately large. Central tooth with 5 or 6 basal denticles on each side. G. tournieri (Binder, 1955) seems conspecific, but possibly more than one species is confused here; Frauenfeld referred to fine spiral lines, whereas Binder described the surface as smooth, although there are strong spiral ridges (about 6 in the last whorl) on shells collected by Binson in 1956 (MNHN). DISTRIBUTION. West Africa: the imprecise type locality; Ivory Coast, Davo River near Gagnoa (B. tournieri), further specimens from near Gagnoa (MNHN) and a few other localities (DBL); Togo (DBL).

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Fig. 41. Bithyniidae. (a) Gabbiella adspersa; Ethiopia, Assaita. (b) G. senaariensis; Egypt, Maadi. (c) G. rosea; Lake Turkana, Central Island, (d) G. barthi; Kenya, Kano Plain (holotype, BMNH1981.153). (e) Incertihydrobia teesdalei; NE Kenya (paratype, BMNH1968.162). (f) Jubaia excentrica; Somalia (paratype, BMNH1993.075). (g) Gabbiella walleri; Lake Albert. Scale line: 3 mm for all but d (2 mm).

Gabbiella adspersa (Jickeli, 1874, Bithynia senaariensis variety adspersa). Type locality: N Ethiopia, Anseba (a watercourse). Fig. 41a. 8.5×5.2 mm. Differing from G. senaariensis mainly in the small spiral nucleus in the operculum and the form of the penis (Mandahl-Barth, 1968b).

96 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 42. Bithyniidae. (a) Gabbiella matadina; W Zaire (holotype, after Mandahl-Barth, 1968b, Pl. 4,5). (b) G. parva; W Uganda (paratype, BMNH 1968.683). (c) G. spiralis; W Zaire (paratype, BMNH1968.692). (d) G. neumanni; Masai Steppe (after Martens, 1897, Pl. 6,33). (e) G. africana; Ivory Coast (syntype of ‘Bithynia’ tournieri, after Binder, 1957, Fig. 9). Scale line: 1 mm (a–d) or 2 mm (e).

HABITAT AND DISTRIBUTION (Fig. 71). Ethiopia: type locality (a seasonal river N of Asmara, but not refound there); lower Awash River, Lake Haussa (Bourguignat, 1885a, Bythinia subbadiella), and in marshes and irrigation channels (Mandahl-Barth, 1968b; BME). Gabbiella zambica Mandahl-Barth, 1968b. Type locality: Zambia, Lundazi Tembwe near Chipata (Fort Jameson). 7.6×5.2 mm. Shell shaped similarly to G. africana, but with flatter whorls; known from a single specimen. DISTRIBUTION. Zambia: reported only from the type locality. E. The candida group. Small species, less than 5 mm high, spire at least as high as the aperture. Central tooth more than twice as wide as long. Gabbiella balovalensis Mandahl-Barth, 1968b. Type locality: Zambia, stream near Mankoyo, Balovale district (upper Zambezi River). Fig. 43a. 4.5×3 mm. Shell with weakly curved whorls and obtuse apex; known from a single specimen.

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Fig. 43. Bithyniidae. (a) Gabbiella balovalensis; Zambia (holotype, after Mandahl-Barth, 1968b, Pl. 3, Fig. 3). (b) G. candida; Lake Albert (paratype, DBL), (c) G. depressa; Cameroon (holotype, DBL), (d) Jubaia aethiopica; SE Ethiopia (paratype, BMNH1968. 163). (e) Funduella incisa; Congo Republic (paratype, DBL). Scale line: 1 mm.

DISTRIBUTION. Zambia: reported only from the type locality. Gabbiella candida Mandahl-Barth, 1968b. Type locality: Uganda, Lake Albert at Butiaba. Fig. 43b. 4.1×2.9 mm. Shell white, translucent; whorls strongly convex. See G. walleri below, a larger species from Lake Albert. DISTRIBUTION. Lake Albert: known only from Butiaba in Uganda. Gabbiella rosea Mandahl-Barth, 1968b. Type locality: W shore of Lake Turkana (Rudolf). Fig. 41c. 4.5×3.1 mm. Whorls strongly convex; sometimes with fine spiral sculpture; colour translucent whitish to rose. Central tooth with 3 basal denticles on either side. HABITAT AND DISTRIBUTION. Lake Turkana, on the littoral rocky bottom and soft muddy substrata below 5 m (Cohen, 1986). Subgenus Omphalogabbia Mandahl-Barth, 1968b. Distinguished from typical Gabbiella by the small depressed shell, widely-open umbilicus and small spiral part of the operculum.

98 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Gabbiella (O.) depressa Mandahl-Barth, 1968b. Type locality: Cameroon, Nyong River. Fig. 43c. 3.2×3.5 mm. Apertural lip expanded below, bluntly angular below columella. Operculum with spiral part less than 1/5 of the width. DISTRIBUTION. Cameroon: type locality and Lake Wum (Wright, 1965, ‘Gabbia’ sp.). Gabbiella (O.) barthi Brown, 1980b. Type locality: W Kenya, Kano Plain, stream 4 km E of Awasi. Fig. 41d. 2.5×3.1 mm. Like G. depressa but smaller and some specimens even more depressed; lip not expanded, almost circular. Operculum with spiral part larger, about 1/3 of width. HABITAT AND DISTRIBUTION. W Kenya: Kano Plain, pools recently filled by rain in seasonal watercourses. Subgenus Conogabbia Mandahl-Barth, 1968. Shell with high spire and strongly convex whorls. Radula smaller than in Gabbiella sensu stricto, central tooth with shorter lateral lobes (Fig. 36f). Gabbiella (C.) walleri (Smith, 1888, Bythinia). Type locality: Uganda, Lake Albert. Fig. 41g. 7.6×4.8 mm. Shell and radula as for the subgenus. Juveniles have fewer whorls than G. candida of the same size. HABITAT AND DISTRIBUTION. Lake Albert: at depths of 8–40 m (Mandahl-Barth, 1968b; Worthington, 1929, p. 118) Genus Incertihydrobia Verdcourt, 1958 Distinguished from Gabbiella by the less calcified operculum, which is corneous and flexible apart from the inner spiral part, and the central tooth where there is only a single basal denticle on either side (Fig. 9e). A single known species; 3 others placed in Incertihydrobia by Verdcourt (1958a) were transferred to other genera by Mandahl-Barth (1968b). Incertihydrobia teesdalei Verdcourt, 1958. Type locality: NE Kenya, Lake Jilore (about 30 km inland from Malindi). Fig. 41e. 5.5×3.7 mm. Spire conical, about as high as aperture; apex obtuse. Operculum and central tooth as for the genus. DISTRIBUTION. NE Kenya: type locality and Takaungu (I. teesdalei variety minor Verdcourt, 1958). Genus Jubaia Mandahl-Barth, 1968 Shell similar to the Gabbiella senaariensis group, but operculum nucleus situated excentrically, towards the outer shell lip, instead of centrally as in Gabbiella. Central tooth with 2 basal denticles on either side. Exhalent siphon lacking (Brown, 1988). Two known species live in NE Africa. Type species: Jubaia excentrica Mandahl-Barth, 1968, Somalia.

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Jubaia excentrica Mandahl-Barth, 1968b. Type locality: Somalia, Far Abis near Mogadiscio. Fig. 41f. 6×4.2 mm. Shell with conical spire, slightly higher than aperture; whitish, with thick lip. Operculum nucleus occupying about 3/4 of the width. DISTRIBUTION. Somalia: Giuba Basin (Mandahl-Barth, 1968b). Ethiopia: shells with opercula (DBL) from Late Pleistocene beds in the lower Omo Basin (Van Damme & Gautier, 1972). Jubaia aethiopica (Verdcourt, 1958a, Incertihydrobia). Type locality: SE Ethiopia, Balleh Mersin, 80 km NW of Wardere, Ogaden Province. Fig. 43d. 4.9×3.6 mm. Smaller than J. excentrica; shell brownish with thin lip. Operculum nucleus occupying only 2/5 of the width. DISTRIBUTION. Ethiopia: reported only from the type locality. Genus Congodoma Mandahl-Barth, 1968 Shell broadly conical, spire less high than aperture; lip strongly sinuous, somewhat expanded below; fine spiral sculpture sometimes present. Operculum nucleus calcified, large, occupying 3/4 of width; outer concentric fringe membraneous. Central tooth with 4 basal denticles on either side. Penial appendage well developed. Exhalent siphon small. The single known species, from the lower Zaire River, is clearly bithyniid (Mandahl-Barth, 1968b; Brown, 1988). Congodoma zairensis (Bequaert & Clench, 1936, Lobogenes). Type locality: lower Zaire River, rocks in swiftly flowing water at Kalawanga islet, opposite Leopold II Point (about 2 km N of Matadi). Figs 4c, 46a. 4.5×3.6 mm. Characters as for the genus. DISTRIBUTION. Zaire River near Matadi, Kinshasa (DBL) and Brazzaville (MNHN). Genus Funduella Mandahl-Barth, 1968 Very small, shell depressed, umbilicus large, aperture sinuous with basal notch. Operculum calcareous, with spiral nucleus. Central tooth with 3 basal denticles on either side. Penial appendage short. A single species known, from W Central Africa. Funduella incisa Mandahl-Barth, 1968b. Type locality: Congo Republic, Fundu-Fundu stream at Dolisie. Figs 4d; 43e. 1.8×2.7 mm. Characters as for genus. DISTRIBUTION. Congo Republic: type locality. W Zaire: source of Madienge River, NE of Kimpese (Mandahl-Barth et al., 1974).

100 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Genus Liminitesta Mandahl-Barth, 1974 Shell globose, thick-walled; whorls rapidly increasing, with strong spiral ridges; lip semicircular with straight thickened columellar margin, closing completely the umbilicus. Operculum lodging within the aperture against a basal ridge; its nucleus completes hardly one spiral turn. Central tooth with 3 basal denticles on either side. Penial appendage well developed. Exhalent siphon present. A single species known, from the lower Zaire River. Liminitesta sulcata Mandahl-Barth, 1974. Type locality: Zaire River, just below Mount Ngaliema (Mount Stanley), Kinshasa. Figs 4e, 45a. 6.3×5.6 mm. Shell colour dark brown; other characters as for genus. HABITAT AND DISTRIBUTION. Apparently adapted for life on stones in rapidly flowing water (Brown, 1988). Lower Zaire River: several localities near Kinshasa (Mandahl-Barth, 1968b). Genus Sierraia Connolly, 1929 Shell small to medium, globose; lip oblique, thickened or expanded according to species; protoconch with spiral ridges, lower whorls smooth or nodular, sometimes with hair-like filaments; variously coloured and patterned. Operculum strongly calcareous when mature, appearing wholly concentric, as the sub-spiral nucleus is usually lost. Central tooth lacking basal denticles. Exhalent siphon present. Penis of one species lacks an accessory appendage. Egg capsule with smooth-edged exit hole, laid singly or in pairs and clusters. Male may mature at a much smaller size than the female. These snails are unique among bithyniids in having colourful patterned shells, and unusual in the operculum nucleus having little spiral structure and the central tooth lacking basal denticles (Brown, 1988). In perennially flowing rivers; beneath stones in rapid runs. Found only in Sierra Leone; 4 species known. Type species: Sierraia leonensis Connolly, 1929, Sierra Leone. Sierraia leonensis Connolly, 1929a. Type locality: Sierra Leone, Mabole River at Batkan. Figs 43A,a–d; 45b. 10×9 mm. Mature aperture oval, lip thick and continuous, neither reflected nor forming the columellar plate present in the 3 other species. Shell surface smooth, colour from greenish-grey to reddish-brown, commonly with dark marks in a broken pattern rather than bands. Operculum broad, flat, lodging at the lip. HABITAT. Rivers: in stony rapids but found most abundantly on tree roots in a slower stretch of the Little Scarcies River. DISTRIBUTION. Sierra Leone: rivers Mabole, Rokel, Jong (Taia), Little Scarcies and possibly the Tabe (Brown, 1988). Sierraia expansilabrum Brown, 1988. Type locality: N Sierra Leone, Little Scarcies River, just below ferry on road from Koto to Outamba National Park. Figs 43A,e–g.

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11×11 mm. Aperture lip thin, expanded and reflected when mature, columellar margin forming a broad plate. Shell surface with numerous nodular spiral ridges; colour commonly dark grey, sometimes with yellowish to orange spiral bands; narrow chequered bands and periostracal filaments may be present. Operculum narrowly ovate, convex, lodging within the aperture. HABITAT AND DISTRIBUTION. Underside of stones in rapidly flowing water. Sierra Leone: Little Scarcies River and Moa River. Sierraia outambensis Brown, 1988. Type locality: N Sierra Leone, Little Scarcies River, just below the ferry on road from Koto to Outamba National Park. Figs 43A,l and m. 5×5 mm. Small, with a columellar plate (unlike S. leonensis) but the outer lip not expanded (unlike S. expansilabrum). Shell surface with only fine spiral ridges; pale yellowish brown with grey spiral bands; narrow chequered bands and periostracal filaments sometimes present. Operculum narrow as in S. expansilabrum. HABITAT AND DISTRIBUTION. Underside of stones in rapidly flowing water. Sierra Leone: Little Scarcies River, type locality and near by. Sierraia whitei Brown, 1988. Type locality: Sierra Leone, Njala, E bank of Jong (Taia) River in Njala University College Campus. Figs 43A,h–k. 8.3×8.0 mm. Shell like S. outambensis, but larger, with stronger spiral ridges; uniformly grey to black or with yellowish to orange spiral bands, sometimes with chequered bands and periostracal filaments. Operculum as in the 2 preceding species. Penis lacks an accessory appendage. HABITAT AND DISTRIBUTION. Underside of stones in rapidly flowing water. Sierra Leone: rivers Jong (Taia), Moa, Rokel and probably Great Scarcies (Brown, 1988); Sewa River (Nagel, 1991). Genus Soapitia Binder, 1961 This apparently is an aberrant bithyniid (Brown, 1988) showing similarities to Sierraia. Shell small, globose, whorls rapidly increasing, with fine spiral ridges, but protoconch smooth; lip strongly oblique, inner margin expanded forming a columellar plate; colour uniform brown, lacking pattern. Operculum small, weakly calcareous, lacking spiral structure. Central tooth lacking basal denticles. Egg capsule with smooth-edged exit holes. A single species, known only from Guinea. Soapitia dageti Binder, 1961. Type locality: Guinea, Konkouré River, above Kaleta Rapids near Soapiti, 10°38′N 13°22′W. Figs 4b, 37g. 5.8×5.4 mm. Characters as for genus. HABITAT AND DISTRIBUTION. Collected from a riverbed drained for engineering works. Guinea: known only from the type locality.

102 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 43A. Bithyniidae. Sierraia from Sierra Leone, (a–d) S. leonensis: (a,b) holotype (BMNH1937.12.30.4937–52); (c,d) banded and blotched examples from the Little Scarcies River. (e–g) S. expansilabrum: (e,f) holotype (BMNH1986.288); (g) banded paratype (BMNH1986.289). (h–k) S. whitei. (h,i) holotype (BMNH1986.294). (j,k) banded paratypes (BMNH1986.295). (l,m) S. outambensis, holotype (BMNH1986.291). Scale line: 6 mm (a–k) or 4 mm (l,m).

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Fig. 44. Radular teeth of Assimineidae. (a) Assiminea bifasciata; Durban, (b) Eussoia inopina; Kenya, Hunter’s Lodge. C, central tooth. L, lateral. AP, accessory plate. M1, first marginal. M2, second marginal. Scale line: 0.01 mm.

Family Assimineidae Belonging to a group of families including the Pomatiopsidae, with a step-like mode of crawling, grooves running from the mantle cavity to the side of the foot and reduced tentacles (Ponder, 1988a). Two subfamilies are recognised. Omphalotropidinae

Habitats almost or entirely terrestrial, in the Indo-Pacific region; marginal teeth of radula deeply divided (pectinate, comb-like). A single species known from Africa, described originally by Preston (1912a) as Assimania {sic} aurifera (type locality: Kenya, Gazi) and placed in Eussoia by Mandahl-Barth (1973b, p. 279). It is known also from Kilifi in Kenya and Zanzibar, Tumbatu Island and appears to be terrestrial (Brown, 1980b). Assimineinae

104 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

African species are small, with dextral shells of varied shapes, including a caplike form. Operculum (Fig. 9c) paucispiral, entirely corneous. Radula with accessory plate between the lateral tooth and first marginal tooth (Fig. 44); central tooth with or without basal denticles. Cosmopolitan; in fresh water and amphibious on the upper seashore. Numerous genera and subgenera (e.g. Brandt, 1974), but a comprehensive revision is needed, not least of the African species. Of 5 genera considered here, 3 are endemic to the lower Zaire River. Genus Assiminea Fleming, 1828 African species small; shell globose to ovately conic. Central tooth lacking basal denticles. Tentacles reduced to lobes containing the eyes. It is not yet clear what is the proper generic or subgeneric position of African species assigned to this genus; most are known from only the shell. Possibly some belong to Paludinella Pfeiffer, which too lacks basal denticles (Brandt, 1974). P. hidalgoi (Gassies) is reported from Réunion (Starmühlner, 1983) and the Comoro Islands (Backeljau et al., 1986). Connolly (1925a) commented that according to differences between their radulae, A. bifasciata and A. leptodonta might be placed in different genera; I follow Mandahl-Barth (1973b) in placing the latter in Eussoia (see below). The nature is obscure of the 11 other species of Assiminea from South Africa listed by Connolly (1939), including A. globulus Connolly reported from brackish water in the Wilderness wetlands (Davies, 1984). Type species: Assiminea grayana Fleming, 1828; England, Greenwich Marshes. Assiminea bifasciata Nevill, 1880. Type locality: South Africa, Durban (Port Natal). Fig. 45e. 7×4 mm. Whorls rather flat, bluntly angular at the periphery and near the suture; chestnut-brown bands, most evident on young shells. Central tooth about as long as broad (Fig. 44a), lateral with large cusps and broad basal plate, outer marginal with about 15 cusps. HABITAT. Moist mud beneath mangrove trees (Brown, 1971). DISTRIBUTION. Mozambique, Komati Estuary and South African coast (Connolly, 1925a, 1939). Assiminea hessei O.Boettger, 1887. Type locality: W Zaire, swamp behind the English trade house at Banana. Fig. 46b. 3.3×2.3. Whorls evenly convex, colour brown. Not refound in Zaire, but some features of the animal were described from Nigerian specimens (Brown, 1980b). Radula like that of A. bifasciata. HABITAT. Mangrove swamp in Nigeria, with Melampus on a sandy substratum near the upper tidal limit. DISTRIBUTION. Zaire: type locality. Nigeria: Port Harcourt (Brown, 1980b). Assiminea keniana Brown, 1980b. Type locality: Kenya, stream at Tiwi, about 20 km S of Mombasa. Fig. 45f. 4.7×2.6 mm. Shell similar in shape to A. bifasciata, but smaller and usually more slender, with 2 spiral ridges on the upper whorls and coloured a uniform

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Fig. 45. Bithyniidae and Assimineidae. (a) Liminitesta sulcata; lower Zaire River, (b) Sierraia leonensis; Sierra Leone (paratype, BMNH1937.12.30). (c) Pseudogibbula duponti; lower Zaire River, Pala Pala. (d) Eussoia aethiopica; ‘Abyssinia’ (syntype BMNH1937.12.30.4980–82). (e) Assiminea bifasciata; Durban, (f) A. keniana; Kenya (holotype, BMNH 1981 155). (g) Eussoia leptodonta; Mozambique (syntype BMNH 1922.11.23.2). (h) E. inopina; Kenya, Hunter’s Lodge. Scale line: 2 mm (d–h) or 5 mm (a– c).

shining brown. Outer marginal tooth of radula with fewer (8–12) cusps than A. bifasciata. HABITAT. In the type locality with Melampus sp. on mud amongst marginal grass in the upper tidal zone of a stream; elsewhere on mud beneath mangrove trees. DISTRIBUTION. Kenya: Mida Creek, Kilifi, Tiwi and Vanga. Genus Eussoia Preston, 1912 Small snails with ovately conical shells, possibly distinguishable as a genus from Assiminea by the less strongly defined basal projection from the central radular tooth, the narrower lateral tooth and the more numerous cusps on the outer marginal tooth (Fig. 45b). Eussoia was described originally from empty shells (Preston, 1912a), treated as a section of Assiminea by Thiele (1927) taking into account radular characters, and regarded as a full genus by Mandahl-Barth (1973b).

106 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 46. Bithyniidae and Assimineidae. (a) Congodoma zairensis; Kinshasa (DBL). (b) Assiminea hessei; Nigeria, Port Harcourt. (c) Eussoia oblonga; Tanzania (paratype. DBL). Scale line: 1 mm.

In fresh and possibly also brackish waters. Eastern Africa: 4 species known, of which one, E. inopina, occurs far inland. Type species: Eussoia inopina Preston, 1912, Kenya. Eussoia inopina Preston, 1912. Type locality: Kenya, banks of the Eusso Nyiro River ‘at least 375 miles’ from the coast (possibly in the Isiolo area). Figs 5a, 45h. 5×3.7 mm. Shell with spire slightly higher than the aperture, whorls regularly increasing, convex; columellar margin of aperture concave, umbilicus narrowly open; lacking spiral sculpture; golden-brown colour. Central tooth as broad or broader than long, according to orientation (Fig. 44b and Brown, 1980b, Fig. 9b). The short tentacles and some other anatomical features described by Brown (1980b). HABITAT. Abundant in very shallow water and on damp mud at a spring shaded by trees, above Hunter’s Lodge dam. DSITRIBUTION. Kenya: type locality, Hunter’s Lodge and Mzima Springs (shells only) (Brown, 1980b). Eussoia aethiopica (Thiele, 1927, Assiminea). Type locality: Abyssinia, Webbi River. Fig. 45d. 6.5×5.0 mm. Like E. inopina, but larger and last whorl somewhat more angular.

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DISTRIBUTION. Somalia: Giuba and Webbi Shebeli river systems (Kristensen, 1987) and in the north-east at Eil (collected by T.Fison from a spring, 1992; BME). Eussoia leptodonta (Connolly, 1922; 1925a, pl. 4, Assiminea). Type locality: Mozambique, Komati River estuary at Rikatla. Fig. 45g. 5.2×3.5 mm. Spire with sides slightly curved, umbilicus completely closed; with groove below the suture and coloured uniform dark brown (a single type in BMNH). DISTRIBUTION. Mozambique: reported only from type locality. Eussoia oblonga Mandahl-Barth, 1973. Type locality: Tanzania, Nianjema Pool, near Bagamoyo. Fig. 46c. 5.5×3.6 mm. Shell ovate, spire obtuse and less conical than in the other species; umbilicus closed. DISTRIBUTION. Tanzania: reported only from the type locality. Genus Pseudogibbula Dautzenberg, 1891 Shell small, globose, with strong spiral ridges. Radula with accessory plate between the bases of the lateral and the first marginal teeth; for this reason the genus apparently belongs in the Assimineidae (Connolly, 1929a; MandahlBarth, 1974). Central tooth lacking basal denticles. River Zaire: one or perhaps two species known. Type species: Pseudogibbula duponti Dautzenberg, 1891, lower Zaire River. Pseudogibbula duponti Dautenberg, 1891. Type locality: lower Zaire River, on rocks at the edge of rapids at Vivi, opposite Matadi. Figs 5b, 45c. 7.5×7.0 mm. Columellar margin of aperture with projecting fold; lip expanded forming well-defined columellar plate, which is white in contrast to the generally reddish-brown shell colour. A pale yellowish form was named subsp. pallidior by Bequaert & Clench (1941). Viviparous and apparently parthenogenetic (Mandahl-Barth, 1974); all of 48 snails dissected were female. DISTRIBUTION. W Zaire: Zaire River in Matadi area. (?)Pseudogibbula cara (Pilsbry & Bequaert, 1927, Cleopatra). Type locality: E Zaire, Stanleyville. 5×4 mm. Smaller than P. duponti, lacking a columellar fold and with stronger spiral ridges. A further difference evident in the paratypes (Academy of Natural Sciences, Philadelphia) is that the columellar margin though thickened lacks a distinct plate. Anatomical study is needed to establish the generic position firmly. DISTRIBUTION. E Zaire: reported only from the type locality.

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Genus Septariellina Bequaert & Clench, 1936 Shell small, cap-like; operculum lacking. The anatomy so far as it is known seems to support classification in the Assimineidae (Bequaert & Clench, 1941). A single known species, from the Zaire River. Septariellina congolensis Bequaert & Clench, 1936. Type locality: Zaire River, rocks in swiftly flowing water at Ango-Ango (4 km S of Matadi). Fig. 5c. 6.8 mm (longest dimension). Central tooth with 2 basal denticles on either side; only a single male among 75 snails dissected (Bequaert & Clench, 1941). DISTRIBUTION. Zaire River near Matadi and Kala Kala (DBL). Genus Valvatorbis Bequaert & Clench, 1936 Shell small, depressed with a sharp carina and numerous spiral ridges. A single known species, from the Zaire River. Valvatorbis mauritii Bequaert & Clench, 1936. Type locality: Zaire River, rocks in swiftly flowing water at Ango-Ango (near Matadi). Fig. 5d. 1.0×2.2 mm. Central tooth with a single pair of basal denticles (Bequaert & Clench, 1941). DISTRIBUTION. Zaire River near Matadi. Family Thiaridae (Melaniidae) Shell small to large, dextral, ovately to narrowly conic (and of various other shapes in Lake Tanganyika); commonly thick-walled and strongly sculptured. Operculum entirely corneous, of varied structure. Mantle edge with or without papillae. Female commonly ovoviviparous, parthenogenetic in some genera, the young developing in a brood pouch. Male lacks a penis (except in Tiphobia) and is rare or unknown for some species. Definitions of subfamilies and even of the family will not be firmly established without further systematic studies (Houbrick, 1988). A narrow definition of the family according to reproductive anatomy (Morrison, 1954), which would exclude many African genera, was not accepted by Binder (1959) or Mandahl-Barth (1967). The Thiaridae is used here in a broad sense and I follow Mandahl-Barth (1954b) by including Syrnolopsis and related genera. In view of the need for fundamental revision I have abandoned the subfamily divisions of the first edition of this book. The order of genera remains the same except that the former Syrnolopsinae have been moved in order to bring together all the ‘thalassoid’ genera of Lake Tanganyika, while Melanopsis is moved into a separate family Melanopsidae. Thiarids live in fresh and slightly brackish waters practically throughout the tropical and subtropical regions. Of the 25 genera found in Africa, 22 are confined to this continent and of these 16 are restricted to Lake Tanganyika.

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Genus Thiara Röding, 1798 Shell medium to large, ovately to almost narrowly conic; with ribs that tend to project as spines from the shoulder of the whorls. Operculum paucispiral with basal nucleus. Mantle border with papillae. Female parthenogenetic, with brood pouch separate from the oviduct; males are rare (Muley, 1977; Starmühlner, 1976c). In fresh and slightly brackish water. Widespread near coasts in the IndoPacific region; 2 species occur uncommonly in Africa. Type species: Helix amarula Linnaeus, 1758, Asia. Thiara amarula (Linnaeus, 1758, Helix). Type locality: Asia, rivers. Figs 47a,b. 33×12.5 mm. Shell large, ovate; upper part of whorls with strong ribs that project as short spines; coloured dark brown. T. vouamica Bourguignat, 1889a, from the Wami River, Tanzania seems conspecific. Anatomy described by Starmühlner (1969; 1976c). HABITAT. Streams just above the limit of tidal influence. DISTRIBUTION. Indo-Pacific coasts, including Madagascar and E Africa from Somalia southwards into Natal (Connolly, 1939, T. vouamica; Starmühlner, 1969); Comoro Islands (Backeljau et al., 1986). Thiara scabra (Müller, 1774, Buccinum). Type locality: India, Coromandel Coast. Fig. 47c. 18×8 mm. Smaller and more slender than T. amarula; sculpture finer, spines less conspicuous; pale with brown transverse markings. Some individuals resemble M. tuberculata, which is even more slender and lacks any spines. Anatomy described by Pace (1973) and Starmühlner (1974; 1976c). Broader snails with long spines identified as T. scabra, from Mauritius and Réunion (Starmühlner, 1983, Figs 35, 36) and Anjouan Island (Backeljau et al., 1986), are a different species (similar snails from Réunion were identified as T. (Plotia) datura Dohrn in Barré et al., 1982). HABITAT. Rivers, streams and ponds, up to 500–600 m in Mauritius (Starmühlner, 1979) and Oman (Brown & Gallagher, 1985), but known only from a few coastal localities near sea-level in Africa. DISTRIBUTION. Indo-Pacific coasts (Starmühlner, 1983) including Madagascar, Zanzibar, Pemba and the Comoro Islands (Backeljau et al., 1986), but uncommon in Africa. Tanzania: Wami and Kingani rivers (Plotia leroyi and P. bloyeti of Bourguignat, 1889a). Kenya: Mambrui (BME). Genus Melanoides Olivier, 1804 Shell medium to large, mostly slender with a high conical spire; transverse and spiral sculpture generally present, commonly producing a tubercular surface. Operculum paucispiral with basal nucleus. Mantle border with papillae. Female with brood pouch in the head-foot separate from the oviduct and perhaps

110 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 47. Thiaridae. (a,b) Thiara amarula; Kenya, Gazi. (c) T. scabra; South Yemen, Wadi Hadhramaut. (d) Melanoides mweruensis; Lake Mweru (syntype, BMNH1893.8.23.85– 91). (e) M. mweruensis; Lake Mweru (syntype of M. imitatrix Smith, BMNH1893.8.23. 92–3). (f) M. crawshayi; Lake Mweru (syntype, BMNH1893.8.23.94). (g) M. admirabilis; Lake Tanganyika (syntype, BMNH1880.12.21.1–4). Scale line: 6 mm (d–f) or 8 mm (a–c,g).

commonly parthenogenetic, since males of M. tuberculata are reported to be lacking or rare in some populations. But no detailed study of reproduction has yet been carried out for any species in Africa.

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In fresh and brackish water (M. tuberculata but not other African species). Indo-Pacific region, southern Asia and much of Africa (Fig. 73); introduced into the West Indies (M. tuberculata). Of about 30 species in Africa, only M. tuberculata is widespread; majority restricted to lakes or the Zaire River. Species will be treated in 3 groups: those endemic to lakes, those restricted to the Zaire Basin and lastly the remainder. Arrangement within groups is alphabetical. Type species: Nerita tuberculata Müller, 1774, India. 1) Species endemic to Lakes Malawi, Mweru and Tanganyika

Melanoides admirabilis (Smith, 1880b, 1881a, Melania). Type locality: Lake Tanganyika. Fig. 47g. 47×14 mm. The largest species in this genus, with strong ribs. HABITAT AND DISTRIBUTION. Organic sediment deposited by the larger tributaries of Lake Tanganyika (Leloup, 1953). Melanoides crawshayi (Smith, 1893, Melania). Type locality: Lake Mweru. Fig. 47f. 19×7.5 mm. A row of outstandingly large tubercles below the suture. DISTRIBUTION. Lake Mweru and the lower Luapula River (Mandahl-Barth, 1968a). Melanoides magnifica (Bourguignat, 1889b, Nyassia). Type locality: Lake Malawi (Nyassa). Fig. 50b. 10×4 mm. Lower whorls almost cylindrical; ribs on upper whorls but not below. Central tooth distinctive (Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi. Melanoides mweruensis (Smith, 1893, Melania; also M. imitatrix). Type locality: Lake Mweru. Figs 47d,e. 22.5×10 mm. Possibly not distinct from M. crawshayi, though the tubercles are more evenly developed. DISTRIBUTION. Lake Mweru and the lower Luapula River (Mandahl-Barth, 1968a). Melanoides nodicincta (Dohrn, 1865, Melania). Type locality: Lake Malawi (Nyassa). Figs 48a–c. 30×10 mm. Similar in shape to M. tuberculata, but with coarser sculpture and fewer (7) cusps on the central tooth (Mandahl-Barth, 1972). Although M. simonsi Smith, 1877, has been regarded as a synonym (Mandahl-Barth, 1972), this may be a distinct species, seeming to have a more acutely-tapered spire (Fig. 48b). DISTRIBUTION. Lake Malawi: at depths down to 27 m (90 feet) (MandahlBarth, 1972). Melanoides nyassana (Smith, 1877, Melania). Type locality: Lake Malawi (Nyassa). Figs 48d,e.

112 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

17×6.5 mm. Shell slender, almost smooth; M. truncatelliformis and other species named by Bourguignat (1889b) may be conspecific (Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi. Melanoides pergracilis (Martens, 1897, Melania). Type locality: Lake Malawi (Nyassa). Fig. 50a. 21×5 mm. Slender, with moderately strong sculpture. DISTRIBUTION. Lake Malawi: down to 27 m (90 feet) (Mandahl-Barth, 1972). Melanoides polymorpha (Smith, 1877, Melania) Type locality: Lake Malawi (Nyassa). Figs 48f,g. 17×6.5 mm. Shell highly varied in shape and sculpture; possibly more than one species is included in this taxon, in which many named by Bourguignat (1889b) have been placed (Crowley et al., 1964; Mandahl-Barth, 1972). A worn shell apparently of this species was described as Melania tanganyicensis by Smith (1880b) (Fig. 48g) under the impression that it was from Lake Tanganyika (see Mandahl-Barth, 1972). DISTRIBUTION. Lake Malawi: found down to 4.5 m (15 feet) depth (Mandahl-Barth, 1972). Melanoides pupiformis (Smith, 1877, Melania). Type locality: Lake Malawi (Nyassa). Fig. 48h. 15.6×4.5 mm. Slender and cylindrical with strong ribs on the upper whorls. DISTRIBUTION. Lake Malawi: down to 21 m (70 feet) (Mandahl-Barth, 1972). Melanoides turritispira (Smith, 1877, Melania). Type locality: Lake Malawi (Nyassa). Figs 48i–k. 19–5×7.2 mm. Shell broad, spire with step-like sides, strongly nodular below the suture. Described originally from a juvenile only 8 mm high; a fully grown shell was later described as M. woodwardi (Smith, 1893). DISTRIBUTION. Lake Malawi: down to 5 m (Mandahl-Barth, 1972). 2) Species endemic to the Zaire Basin

Melanoides agglutinans (Bequaert & Clench, 1941, Potadoma). Type locality: Zaire River, crevices among rocks in swiftly flowing water at Kala Kala near Matadi. Figs 50f,g. 12×7.5 mm. Large shells are deformed by corrosion and contact with other individuals and rocks. The central tooth illustrated by the authors indicates that this curious species belongs in Melanoides rather than Potadoma. DISTRIBUTION. Zaire River: reported only from the type locality. Melanoides anomala (Dautzenberg & Germain, 1914, Melania tuberculata variety anomala). Type locality: SE Zaire, Kabanza on the Lovoi River (selected by Pilsbry & Bequaert, 1927). Figs 51e,i.

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Fig. 48. Thiaridae: Melanoides of Lake Malawi, (a) M. nodicincta (syntype, BMNH1890. 3.22.1– 4). (b,c) M. nodicincta; Nkata Bay (identified by G.Mandahl-Barth). (d,e) M. nyassana; (syntype, BMNH1877.9.28.23). (f) M. polymorpha (syntype, BMNH1877.9.28. 16). (g) M. polymorpha (holotype of M. tanganyicensis Smith, BMNH1880.12.20.55). (h) M. pupiformis (syntype, BMNH1877.9.28.21). (i,j) M. turritispira (syntypes, BMNH1877. 9.28.22). (k) M. turritispira (holotype of M. woodwardi Smith, BMNH1890.3.27.2). Scale line: 5 mm.

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28×11.5 mm. Like M. tuberculata, but sculpture coarser though highly variable and sometimes weak on lower whorls (Pilsbry & Bequaert, 1927; Mandahl-Barth, 1968a); central tooth with fewer cusps on average (maximum 9 rather than 12 in tuberculata; Brown et al., 1992). HABITAT. On gravel or sand where aquatic vegetation was lacking; in rivers, irrigation canals and a lake (Mandahl-Barth et al., 1972). DISTRIBUTION. SE Zaire: Zaire Basin, catchments of the rivers Lualaba, Lufira and Luapula (Mandahl-Barth, 1968a). Melanoides bavayi (Dautzenberg & Germain, 1914, Melania). Type locality: E Zaire, Lualaba River at Kibombo. 14.5×3 mm. Shell slender like M. depravata, but sides regularly tapered; low ribs on only the upper half of the whorls. DISTRIBUTION. E Zaire: reported only from the type locality. Melanoides depravata (Dupuis & Putzeys, 1900, Melania). Type locality: E Zaire, Lualaba River at Nyangwe. Fig. 49a. 19×5 mm. Shell cylindrical, sides slightly curved, somewhat fusiform when large; low ribs below the sutures. DISTRIBUTION. E Zaire: Lualaba River at Nyangwe, Nsendwe and Kibombo (Pilsbry & Bequaert, 1927). Melanoides dupuisi (Spence, 1923, Cleopatra). Type locality: Zaire River, beach at Ngandu (on the W shore about 16 km (10 miles) from Kwamouth on the E shore near the Kasai River). Figs 49b,c. 13×5.6 mm. Whorls with one or 2 rows of large tubercles, developing into spines. DISTRIBUTION. Zaire River: type locality; also Kinshasa and Ubangi River at Banzyville (DBL). Melanoides kisangani Pilsbry & Bequaert, 1927. Type locality: E Zaire, sandbanks in the Tshopo River near Kisangani (Stanleyville). 17×5.5 mm. Slender, rather cylindrical and like M. nsendweensis, but sculpture generally weaker and dominated by a row of tubercles near the suture. DISTRIBUTION. E Zaire: Kisangani district (Pilsbry & Bequaert, 1927). Melanoides kinshassaensis (Dupuis & Putzeys, 1900, Melania). Type locality: Zaire, Kinshasa. Fig. 49d. 15×7 mm. Spire conical, whorls increasing regularly, with flattened sides and weakly sculptured apart from spiral ridges at the base. Embryonic shell distinctive in being smooth (Mandahl-Barth, 1974). DISTRIBUTION. Zaire River, in Stanley Pool (Pilsbry & Bequaert, 1927, p. 560) and other localities near Kinshasa (Mandahl-Barth, 1974). Melanoides langi Pilsbry & Bequaert, 1927. Type locality: E Zaire, sandbanks of the Tshopo River near Kisangani (Stanleyville). 14.5×6 mm (about 3 whorls remaining). Like M. tuberculata in shape, but with stronger spiral ridges, the one below the suture bearing nodules. DISTRIBUTION. Zaire River: type locality and mudbanks between Malela and Zambi (M. langi zambiensis Pilsbry & Bequaert, 1927).

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Fig. 49. Melanoides. (a) M. depravata; E Zaire (syntype, BMNH1901.6.20.140–2). (b,c) M. dupuisi; Congo Republic (syntypes, BMNH1937.12.30.13365–6). (d) M. kinshassaensis; W Zaire (syntypes, BMNH1901.6.20.146–7). (e) M. nsendweensis; E Zaire (syntype of M. consobrina Dupuis & Putzeys, BMNH1901.6.20.143–5). (f) M. nsendweensis; E Zaire (syntype of M. soror Dupuis & Puzeys, BMNH1915.1.5.118–21). (g) M. nyangweensis; (E Zaire (syntype, BMNH1901.6.20.148– 50). (h) M. angolensis; Angola, Lagoa Quilunda. (i) M. recticosta; W Zaire, Mankusa River, (j) M. voltae; Ghana, Apaso. Scale line: 5 mm.

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Melanoides liebrechtsi (Dautzenberg, 1901, Melania). Type locality: Upper Congo (without details). Fig. 50d. 26×11 mm (4.5 whorls remaining). Relatively broad shell with spiny tubercles below the suture. DISTRIBUTION. Zaire: type locality and Kinshasa (Leopoldville) (Pilsbry & Bequaert, 1927). Melanoides nsendweensis (Dupuis & Putzeys, 1900, Melania). Type locality: E Zaire, Lualaba River at Nsendwe. Figs 49e,f. 13.5×4.5 (up to 20 mm high). Shell slender, sides slightly curved, somewhat fusiform like M. depravata, but with strong sculpture all over. The ribs bear strong tubercles in the named forms M. consobrina Dupuis & Putzeys, 1900 (Fig. 49e) and M. soror Dupuis & Putzeys, 1900 (Fig. 49f). DISTRIBUTION. E Zaire: Lualaba River at Nsendwe and other places, and sandbanks in the Tshopo River near Kisangani (Stanleyville; Pilsbry & Bequaert, 1927). Melanoides nyangweensis (Dupuis & Putzeys, 1900, Melania). Type locality: E Zaire. Lualaba River at Nyangwe. Fig. 49g. 18×5.5 mm. Spire high, acutely tapered, with curved sides; lower whorls smooth; colour pale with distinct brown spots. DISTRIBUTION. E Zaire: Lualaba River at Nyangwe and other places (Pilsbry & Bequaert, 1927). Melanoides wagenia Pilsbry & Bequaert, 1927. Type locality: E Zaire, a brook near the falls of the Zaire River at Stanleyville. Fig. 50e. 26×8.5 mm (6 whorls remaining). Spire narrowly conic, whorls increasing regularly, with strong curved ribs above and spiral ridges at the base. DISTRIBUTION. E Zaire: Kisangani (Stanleyville) district (Pilsbry & Bequaert, 1927). 3) Other species

Melanoides angolensis Mandahl-Barth, 1974. Type locality: N Angola, Dande River. Fig. 49h. 24×10 mm. Shell like M. tuberculata in shape, but sculpture much weaker, comprising only fine spiral grooves on the upper whorls and spiral ridges at the base. Similar to M. kinshassaensis, but larger and with more convex whorls (Mandahl-Barth, 1974). DISTRIBUTION. Angola: type locality and other places in the Luanda region (Wright, 1963a, Pl. 16, ‘M. tuberculata’). Melanoides manguensis (Thiele, 1928, Melania). Type locality: E Ghana, Oti River at Mangu (located by Thiele in Togo). Fig. 50c. 21×6 mm. Shell slender, weakly sculptured and without nodules. DISTRIBUTION. Ghana: type locality. Ivory Coast: Comoe River near Adzope (DBL) and Oniassoué (MNHN).

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Fig. 50. Melanoides. (a) M. pergracilis; Lake Malawi (after Mandahl-Barth, 1972, Pl. 6, 26). (b) M. magnifica; Lake Malawi (after Mandahl-Barth, 1972, Pl. 6). (c) M. manguensis; ‘Togo’ (after Thiele, 1928, Pl. 8, Fig. 20). (d) M. liebrechtsi; Congo Republic, Leopoldville (DBL), (e) M. wagenia; Zaire, Stanleyville (DBL). (f,g) M. agglutinans; Zaire River (paratypes, after Bequaert & Clench, 1941, Pl. 1). Scale lines: 2 mm.

Melanoides psorica (Morelet, 1864, Melania). Type locality: Madagascar. Fig. 51d. 17×6 mm (4 whorls remaining). Possibly merely a slender form of M. tuberculata, which is widespread in Madagascar. DISTRIBUTION. Madagascar: apparently no precise locality recorded. Melanoides recticosta (Martens, 1882, Melania). Type locality: Angola, Murie stream, a tributary of the Cuanza River. Fig. 49i.

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20×8.3 mm. Whorls strongly convex, with strong ribs and at the base spiral ridges. HABITAT. Streams with beds of mud or gravel (Mandahl-Barth et al., 1974). DISTRIBUTION. Angola: type locality. Zaire: plain south of the Zaire River below Kinshasa (Mandahl-Barth et al., 1974). Congo Republic: Kouilou River (MNHN). Melanoides tuberculata (Müller, 1774, Nerita). Type locality: India, Coromandel coast. Figs 51a–c. 27×9 mm (complete shell with 11 whorls); some morphs are smaller (less than 20 mm high) or larger (nearly 50 mm high). Shell narrowly conic, whorls regularly increasing, moderately convex, with ribs and spiral ridges forming highly varied sculpture, though commonly tuberculate; colour often pale with reddish-brown patches aligned with the ribs (making flame-like markings), sometimes uniformly brownish. Central tooth (Fig. 52b) with average number of cusps (range 7–12; Brown et al., 1992) greater than in M. anomala or M. victoriae. The shells shown in Figs 51a and b resemble in shape and sculpture the syntypes of M. tuberculata figured by Pointier (1989). To the same species seem to belong many species and varieties named from African specimens (see Pilsbry & Bequaert, 1927; Mandahl-Barth, 1954a). Among them, M. inhambanica (Martens, 1860, Mozambique) is finely sculptured, while M. t. butiabiae Mandahl-Barth (1954a) is a remarkably small and slender form found in Lake Albert (similar shells in Lake Turkana; Brown, 1992). Conchological variation could be due partly to parthenogenetic propagation of clones, as some populations are predominantly or perhaps entirely female. But males occur quite commonly in some localities in Israel and Sinai (Livshits et al., 1984; Heller & Farstey, 1990). Relationships between mode of reproduction and morphological variation have not been investigated in Africa; males may be recognisable from the reddish testis showing as a dark area in the upper whorls (Heller & Farstey, 1989). HABITAT. Various permanent waterbodies including rivers, lakes, shallow seepages and man-made habitats (e.g. Ndifon & Ukoli, 1989), but not found in temporary waters. Very abundant on bottom sediments in lakes (Lévêque, 1972; Hart, 1979) and coarse substrata in eroding streams (Thomas & Tait, 1984). Tolerant of moderate brackishness in coastal localities and abundant in shell deposits representing the last molluscan faunas where inland lakes have entirely evaporated or have become too saline for freshwater organisms. Life cycle and growth studied in Lake Chad (Lévêque, 1972) and SE Transvaal (Appleton, 1974); variation in life history traits among different shell morphs was observed in the West Indies (Pointier et al., 1992). DISTRIBUTION (Fig. 73). Indo-Pacific region, S Asia, Arabia, Near East and much of Africa. Introduced into the Caribbean area (Pointier, 1989). Widespread in tropical Africa but apparently lacking from a large western area, including most of the Zaire Basin. Southern limits lie near Port Elizabeth and in Namibia.

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Fig. 51. Melanoides. (a–c) M. tuberculata: (a) Tanzania, Mbayeni; (b) Kenya, Kisumu; (c) Kenya, Taveta. (d) M. psorica; Madagascar (syntype, BMNH1893.2.4.1272–4). (e) M. anomala; SE Zaire, Kibidwila River, E of Likasi. (f–h) M. victoriae: (f) E Transvaal; (g) Zambezi River above Victoria Falls (syntype BMNH); (h) N Transvaal, Middelburgh (syntype of M. crawfordi Brot, BMNH1902.7.30.2). (i) M. anomala; SE Zaire, Lac de Retenue de la Lufira. Scale line: 5 mm.

Late Pleistocene-Holocene distribution was widespread in the present-day Sahara and isolated populations have been found in Algeria, SW Libya and Chad (Van Damme, 1984). Islands of Socotra (Melania sclateri Godwin-Austen, 1883),

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Pemba (Mozley, 1939), Zanzibar (M. zengana Morelet, 1860) and throughout Madagascar (Fischer-Piette & Vukadinovic, 1973). Melanoides victoriae (Dohrn, 1865, Melania). Type locality: Zimbabwe (Rhodesia), Zambezi River at Victoria Falls. Figs 51f–h. 29×10 mm (9 whorls remaining). Whorls flatter than in M. tuberculata, sculpture weak or almost lacking on the last whorl, though strong ribs and tubercles may be present above. Individuals from Namibia with unusually strong sculpture below, showing similarities to M. anomala, were identified primarily according to the central radular tooth (Fig. 52c), which is smaller in M. victoriae, with fewer cusps (5–7 rather than 7–9; Brown et al., 1992). HABITAT. Rivers with sandy or muddy bottoms in the E Transvaal lowveld; rivers and floodplains in NE Namibia. DISTRIBUTION. N and E Transvaal (Brot, 1894, M. crawfordi: Fig. 51h; Oberholzer & Van Eeden, 1967; BME); Middle Zambezi Basin (type locality and other localities, DBL); NE Namibia (East Caprivi and Okavango River; Brown et al., 1992); Cunene River (Connolly, 1939). Melanoides voltae (Thiele, 1928, Melania). Type locality: Ghana, Volta River at Apaso. Fig. 49j. 18×6 mm (4 whorls remaining). Shell slender, almost cylindrical, with coarse nodules. DISTRIBUTION. E Ghana: tributaries of the Volta River, near Frankadua, Apaso and Balakuna (DBL) and Kpong (BM). Genus Pachymelania Smith, 1893 Shell large, with a high spire (though often decollate) and strong tubercles and ridges; apertural lip expanded at base, spout-like. Operculum paucispiral with basal nucleus. Central tooth with 5–7 cusps (Binder, 1957). Female is both oviparous and ovoviviparous according to various reports (Binder, 1959; Oyenekan, 1984; Ajao & Fagade, 1990b,c). In brackish water on the West African coast: 3 species. Type species: Strombus byronensis Wood, 1828, Upper Guinea. Pachymelania byronensis (Wood, 1828, Strombus). Type locality: coast of Upper Guinea. Fig. 53a. 60×27 mm. Comparatively broad, with 2 or 3 rows of large tubercles. HABITAT. Adapted to low salinity (Oyenekan, 1979). I found it with the 2 following species amongst Vallisneria sp. in the lower Volta River. DISTRIBUTION. Ivory Coast to Nigeria. Pachymelania aurita (Müller, 1774, Nerita). Type locality: not given. Fig. 53b. 55×20 mm. Lower whorls with a single row of very large tubercles, upper whorls with low ribs; colour and banding pattern varied (Binder, 1977). Anatomy described by Binder (1959).

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Fig. 52. Radular teeth of Thiaridae. (a)–(d) Central teeth, (a) Melanoides anomala; SE Zaire (shell 22 mm high), (b) M. tuberculata; Kenya, Lake Jipe (shell 15 mm high), (c) M. victoriae; E Transvaal, Sand River (shell 25 mm high), (d) Spekia zonata; Lake Tanganyika at Kigoma. (e) Lavigeria nassa; Lake Tanganyika at Kigoma. C, central tooth. L, lateral. M1, first marginal. M2, second marginal. Scale lines: 0.01 mm.

DISTRIBUTION. Senegal to Angola, on sandy substrata (Ajao & Fagade, 1990b,c). Pachymelania fusca (Gmelin, 1791, Murex) Type locality: not given. Figs 53c,d. 45×16 mm. Sculpture highly varied, though lacking the strong tubercles of the 2 preceding species. Pilsbry & Bequaert (1927) recognised 3 forms: granulosa (mostly nodular; Fig. 53c), fusca (strong carinae on the lower whorls; Fig. 53d) and mutans (carinate above, nodular below). HABITAT. Shell variation is related to substratum and salinity (Binder, 1957; Plaziat, 1977). In almost fresh water (Binder, 1968) and tolerating salinity of 0. 02–15‰ (Plaziat, 1977). Comparatively tolerant of drying (Oyenekan, 1979). DISTRIBUTION. Senegal to Angola (near Benguela, Wright, 1963a, p. 512); penetrating up the Zaire River to Malela (Pilsbry & Bequaert, 1927). Genus Melanatria Bowdich, 1822 Shell large, with high spire (though often decollate); whorls smooth or strongly sculptured; apertural lip strongly sinuous. Operculum spiral, with up to 5 whorls, nucleus near centre. Radula unusually long (about 20 mm fully grown); central

122 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 53. Thiaridae: Pachymelania from Ghana, (a) P. byronensis. (b) P. aurita. (c,d) P. fusca. Scale line: 10 mm.

tooth approximately rectangular. Mantle border lacking papillae. Both sexes occur; female oviparous (Grossmann, 1967). Anatomy described by Starmühlner (1969). In freshwater streams in Madagascar: 2 species seem recognisable. Type species: Buccinum flumineum Gmelin, 1767, Madagascar. Melanatria fluminea (Gmelin, 1767, Buccinum). Type locality: Madagascar. Figs 54a,b. 70×24 mm (apex missing). Sculpture highly varied; commonly with ribs that may bear spines on the shoulder, sometimes with spiral ridges (M. johnsoni Smith, 1882, Fig. 56b); coloured dark brown. HABITAT AND DISTRIBUTION. NE Madagascar: rivers and streams in primary forest, on hard substrata in currents up to 0.8 m s−1 (Starmühlner, 1969). Melanatria madagascariensis (Grateloup, 1839, Melania). Type locality: Madagascar. 55×18 mm. Comparatively slender; whorls convex, smooth and glossy, sometimes with weak basal ridges (Starmühlner, 1969). HABITAT AND DISTRIBUTION. N Madagascar: rapidly flowing streams in primary forest, and on Nossi Bé Island (Starmühlner, 1969).

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Genus Potadoma Swainson, 1840 Apparently related closely to Melanatria. Shell medium to large, broadly conic to slender or almost cylindrical, though commonly decollate; whorls smooth or variously sculptured, sometimes strongly carinate or ribbed, spiral ridges usually present at the base; apertural lip more or less expanded below; coloured brown, sometimes with spiral bands. Operculum spiral, with up to 4 or 5 whorls; nucleus below and to the left of centre (not basal as in Melanoides and Pachymelania). Radula long; central tooth rectangular (structure discussed by Samé-Ekobo & Kristensen, 1985). Mantle border lacking papillae. Anatomy described by Binder (1959); both sexes occur, but manner of reproduction not reported. In fresh water, especially rivers and streams within forest. Africa: living in two areas (Fig. 72), one including Liberia and lower Zaire in the west, and a separate eastern area in the upper Zaire Basin; further eastwards in Late Cenozoic fossil deposits in the Turkana Basin (Williamson, 1985). About 20 species, mostly reviewed by Mandahl-Barth (1967), whose order of treatment is followed here, with a group of species found only in Cameroon segregated at the end. The genus is suspected to provide the first intermediate host for lung-flukes, Paragonimus spp. in West Africa. Type species: Melania freethi Gray, 1831, Fernando Po. Potadoma freethi (Gray, 1831, Melania). Type locality: Fernando Po. Figs 54c,d. 53×20 mm. Shell usually with only 4–5 whorls remaining; sides slightly curved; fine wavy sculpture may be intersected by growth ridges producing a granular surface; spiral ridges around base. Mandahl-Barth (1967) recognised 5 subspecies, differing in shape and sculpture: P. f. freethi of Fernando Po and Gabon, P. f. dykei Spence, 1925 of SE Nigeria, P. f. guineensis Reeve, 1860 (Fig. 54d) of S Ghana and Ivory Coast, P. f. tigrina Connolly, 1938 (Fig. 54c) of Congo Republic and P. f. graptoconus Pilsbry & Bequaert, 1927 of W Zaire. DISTRIBUTION (Fig. 72). Ivory Coast to lower Zaire. Potadoma schoutedeni Pilsbry & Bequaert, 1927. Type locality: W Zaire, Lukula. Fig. 54g. 28×16 mm. Like P. freethi but smaller and broader, with a different central tooth (Mandahl-Barth, 1967). DISTRIBUTION. W Zaire: tributaries of the Shiloango River (Mandahl-Barth, 1967). Congo Republic: Kouilou River (MNHN). Potadoma moerchi (Reeve, 1859, Melania). Type locality: ‘Guinea danica’ according to Brot (1874) (probably Ghana). Figs 54e,f. 55×18 mm. Shell usually more slender than P. freethi, with whorls more convex and coarser spiral ridges (about 3 per mm). HABITAT AND DISTRIBUTION. Fast flowing rivers and streams, heavily shaded with gravelly or rocky substrates (Ndifon & Ukoli, 1989). Ghana (Volta River system), Togo, Dahomey and SW Nigeria (Mandahl-Barth, 1967).

124 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 54. Thiaridae. (a) Melanatria fluminea; Madagascar, (b) M. fluminea; Madagascar, Mahavavy (form johnsoni Smith), (c) Potadoma freethi; Congo Republic (holotype of P. tigrina Connolly, BMNH). (d) P. freethi; Ghana, Anyinam. (e) P. moerchi; Ghana, Frankadua. (f) P. moerchi (either holotype or a syntype, BMNH 1993.080). (g) P. schoutedeni; W Zaire (paratype, BMNH 1962.528). (h) P. togoensis; Ghana, (i) P. vogelii; Ivory Coast. Scale line: 10 mm (c–i) or 16 mm (a,b).

Potadoma togoensis Thiele, 1928. Type locality: Ghana, White Volta River at Apaso. Fig. 54h. 40×14 mm. Shell slender with basal ridges but elsewhere only few spiral lines; central tooth distinctive (Mandahl-Barth, 1967). DISTRIBUTION (Fig. 72). E Ghana; Togo (Seidl, 1985).

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Fig. 55. Thiaridae: Potadoma. (a) P. liricincta; E Zaire (syntype of variety latior Thiele, BMNH1937.12.30.7058). (b) P. liricincta; E Zaire, Buessa district (paratype of P. tornata Martens, BMNH1893.3.22.1) (c) P. bicarinata; Ghana (paratype, BMNH 1968.699). (d) P. ignobilis; NE Zaire (syntype, BMNH 1937.12.30.7069). (e) P. liberiensis; Liberia, Du River, (f) P. ponthiervillensis; E Zaire (syntype, BMNH 1901.6.20.131–3). (g) P. ponthiervillensis; E Zaire, Lualaba River at Ponthierville (syntype of variety spoliata Dupuis & Putzeys, BMNH1901.6.20.126–7). (h) (?) Potadoma buttikoferi; Liberia (syntype, National Natuurhistorisch Museum, Leiden). Scale line: 6 mm (h) or 10 mm (a– g).

Potadoma vogeli Binder, 1955. Type locality: Ivory Coast, Agnéby (river or stream) at Abgoville. Fig. 54i. 40×11 mm. Slender with coarse spiral ridges on all whorls. DISTRIBUTION (Fig. 72). Ivory Coast: streams and rivers (Mandahl-Barth, 1967). Potadoma liricincta (Smith, 1888, Melania). Type locality: ‘Lake Albert’ (probably incorrect, see Mandahl-Barth, 1967). Figs 55a,b. 40×14 mm. Slender with weakly developed basal ridges and 1–9 strong spiral ridges above. A number of named forms differing widely in degree of

126 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

sculptural development were placed in synonymy by Mandahl-Barth (1967); e.g. variety latior Thiele, 1911 (Fig. 55a) and P. tornata Martens, 1892 (Fig. 55b). DISTRIBUTION (Fig. 72). NE Zaire: Oriental Province, especially Kibale-Ituri district (Mandahl-Barth, 1967). Potadoma bicarinata Mandahl-Barth, 1967. Type locality: Ghana, Volta River at Asikoko village near Frankadua. Fig. 55c. 16.6×9.6 mm. Small, short-spired, with two major carinae and 1–3 basal ridges. Shell like a carinate Cleopatra bulimoides, but operculum different in being entirely paucispiral. DISTRIBUTION. E Ghana: Frankadua area, Otiso River and north-eastern region (Mandahl-Barth, 1967). Potadoma alutacea Pilsbry & Bequaert, 1927. Type locality: E Zaire, Tshope River near Kisangani (Stanleyville). Fig. 57a. 26×11.5 mm. Spire slender; sculpture ‘like pebbled leather’ (original description). DISTRIBUTION. E Zaire: type locality and nearby Lubutu district (MandahlBarth, 1967). Potadoma ignobilis (Thiele, 1911, Melania). Type locality: NE Zaire, Ituri River near Mawambi (NE of Kisangani). Fig. 55d. 32×11.5 mm. Sculpture lacking apart from growth ridges and sometimes fine spiral lines (P. mungwana Pilsbry & Bequaert, 1927); central tooth characteristic (Mandahl-Barth, 1967). HABITAT. Abundant in a highland stream, under varying conditions of substratum, vegetation and shading (Baluku et al., 1989). DISTRIBUTION (Fig. 72). From the area S of Lake Kivu through E Zaire to the SE part of the Central African Republic (Mandahl-Barth, 1967). Potadoma wansoni Bequaert & Clench, 1941. Type locality: Zaire River, rocks in swiftly flowing water near Matadi. Fig. 57b. 12×6 mm (3–5 whorls remaining). The smallest member of this genus, completely lacking spiral sculpture. DISTRIBUTION. W Zaire: reported from only the type locality. Potadoma liberiensis (Schepman, 1888, Melania). Type locality: Liberia, rocks in the St Paul’s River near Bavia. Fig. 55e. 25×9.5 mm. Spiral ridges lacking from the base, but variably developed above, most strongly in the form named P. sancti-pauli (Schepman, 1888) and only weakly in P. bequaerti Binder, 1963 (Ivory Coast, Mount Nimba). DISTRIBUTION (Fig. 72). Liberia and adjacent parts of Ivory Coast and Guinea (Mandahl-Barth, 1967). Potadoma ponthiervillensis (Dupuis & Putzeys, 1900, Melania). Type locality: E Zaire, Lualaba River at Ponthierville. Figs 55f,g. 40×18 mm. Typical form with carinae bearing tubercles (Fig. 55f), while other shells may be almost smooth (form spoliata Dupuis & Putzeys, 1900) (Fig. 55g), or strongly carinate but lacking tubercles (P. superba Pilsbry & Bequaert, 1927).

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DISTRIBUTION. E Zaire: Lualaba River between Ponthierville and Kisangani (Stanleyville), and Tshopo River at Kisangani (P. superba) (Mandahl-Barth, 1967). (?)Potadoma buttikoferi (Schepman, 1888, Melania). Type locality: Liberia, rocks in the St Paul’s River near Bavia. Fig. 55h. 13×8 mm (3 whorls remaining). Shell with strong spiral ridges; broad brown band at the periphery and a weaker one at the base. Soft parts unknown. Generic position uncertain; shell shows some resemblance to Cleopatra. DISTRIBUTION. Reported from only the type locality. (?)Potadoma liberiana (Schepman, 1888, Paludina). See under Bellamya. The Potadoma species of Cameroon

The shells of 6 species found only in Cameroon differ from all the foregoing in varied ways: 1) whorls angular to a varying degree, apertural lip is obviously expanded basally (angulata, kadeii, nyongensis, zenkeri), 2) broadly conical (trochiformis), 3) strongly ribbed (riperti). Potadoma zenkeri (Martens, 1901, Semisinus (Rhinomelania)). Type locality: Cameroon, Lukonje River near Bipindi. Fig. 56a. 40×25 mm (2–3 whorls remaining). Last whorl flattened, bluntly angular; base of aperture spout-like; the shell figured here has fine transverse and spiral sculpture. Rhinomelania africana Clench, 1929 was described from an apparently immature shell with rounded not flattened whorls. DISTRIBUTION. Cameroon: type locality, Kribi (Clench, 1929) and Tchangue River (DBL). Potadoma nyongensis Spence, 1928. Type locality: Cameroon, Nyong River at 10°10′E 3°35′N. Fig. 56b. 29×20 mm (about 2 whorls remaining). Strongly carinate at the periphery and the base. DISTRIBUTION. Cameroon: type locality and Man River at Sakbayeme. Potadoma trochiformis (Clench, 1929, Goodrichia). Type locality: Cameroon, Man River near Sakbayeme (NE of Edea). Fig. 56c. 32×26 mm (2–3 whorls remaining). Strongly carinate like P. nyongensis, but last whorl broader and aperture more oblique; shell more slender and upright in subspecies pilsbryi Clench, 1929. Possibly synonymous with P. nyongensis, as thought by Mandahl-Barth (1967). DISTRIBUTION. Cameroon: reported only from the type locality. Potadoma angulata Thiele, 1928. Type locality: Cameroon, Samanga. Fig. 57c. 32×7 mm (2–3 whorls remaining). Shell slender and angular at the periphery. DISTRIBUTION. Cameroon: type locality and Yaoundé (DBL). Potadoma kadeii Samé-Ekobo & Kristensen, 1985. Type locality: E Cameroon, Kadei River at Pana. Fig. 56d.

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Fig. 56. Thiaridae: Potadoma of Cameroon, (a) P. zenkeri; Kribi. (b) P. nyongensis (paratype, BMNH1937.12.30.13380–81). (c) P. trochiformis (paratype, BMNH1937.12. 30.7070–1). (d) P. kadeii (paratype, BMNH1993.163). (e) P. riperti (paratype, BMNH1993.164). Scale line: 10 mm.

26.8×10 mm (4 whorls remaining). Shell like P. angulata but more cylindrical and less angular; also the radula is different. DISTRIBUTION. Cameroon: reported only from the type locality. Potadoma riperti Samé-Ekobo & Kristensen, 1985. Type locality: E Cameroon, small river at Mikel town. Fig. 56e.

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Fig. 57. Thiaridae: Potadoma. (a) P. alutacea; E Zaire (holotype after Pilsbry & Bequaert, 1927, Pl. 26, Fig. 3a). (b) P. wansoni; lower Zaire River (paratype after Bequaert & Clench, 1941, Pl. 1, Fig. 9). (c) P. angulata; Cameroon (holotype after Thiele, 1928, Pl. 8, Fig. 12). Scale lines: 5 mm.

30×11.5 mm. Shell with high conical spire, strong ribs and spiral ridges all over. DISTRIBUTION. Cameroon: reported from only the type locality. Genus Cleopatra Troschel, 1856 Medium-sized, shell usually ovately or more narrowly conic, rarely low-spired approaching globose (C. pilula); smooth or variously sculptured, sometimes carinate, but not with strong transverse ribs; dark spiral bands present in at least some individuals of most species. In juveniles the lip tends to be more angular below the columella than in adults. Operculum (Fig. 9h) largely concentric with a small spiral nucleus. Radula small, central tooth varied in shape, with about 7 cusps (Hemming & Verdcourt, 1956; Mandahl-Barth, 1968a, 1974). Mantle border lacking papillae, unlike Paludomus, an Asian genus of which some species have a similar shell and operculum. Anatomy described by Binder (1959) and Starmühlner (1969); both sexes known and female supposedly oviparous, but reproduction has not been described. In small, stagnant and slowly flowing waterbodies, some briefly seasonal, also in lakes; especially on muddy substrata. Africa and Madagascar, with a few reports for Arabia and Syria (Fig. 74, 10–12); from lower Egypt to Zululand, and westwards into Senegal and the Okavango Delta. About 20 species, of which C. bulimoides and C. ferruginea are the most widespread. Two taxa treated as Cleopatra in the first edition of this book were

130 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

later found to belong in Paludomus (which follows); they are P. ajanensis Morelet and P. lesnei (Germain). The African localities attributed to both are probably mistaken. Relationships among species can only be guessed at, as the shell and radula are the only sources of comparative characters yet explored. The present arrangement begins with C. bulimoides of northern Africa and apparently related species (bulimoides, ferruginea, africana, obscura and exarata), continues with various forms from the central tropical area, then a group with strongly curved whorls from eastern Africa (guillemei, athiensis, hemmingi and rugosa) and lastly species of Madagascar. Type species: Cyclostoma bulimoides Olivier, 1804, Egypt. Cleopatra bulimoides (Olivier, 1804, Cyclostoma). Type locality: Egypt, Kalidje Canal near Alexandria. Figs 58a–c. 16×9 mm (typical form); 22×9 mm (slender shell). Typical form (Fig. 58a) has lower whorls evenly curved and smooth, carinations confined to the apical whorls; usually with one or more dark brown bands; reported sometimes as C. cyclostomoides (Küster, 1852). C. congener Preston (1913; Kenya, Lake Baringo) is similar. A more slender form with the spire reaching twice the height of the aperture was named C. pauli Bourguignat (1885a; Ethiopia, lower Awash Valley). Some populations have strong spiral ridges; such named forms include C. pirothi Jickeli (1881, ‘Abyssinia’) (Fig. 58b) and C. emini Smith (1888, Lake Albert). C. senegalensis (Morelet, 1860) (Fig. 58c) is small with well-rounded whorls. From the shell it appears that C. bulimoides is a highly varied, polytypic species including many named forms in synonymy (only some mentioned above), but their conspecificity needs to be tested by further evidence, especially genetic. HABITAT. Muddy or sandy substrata, usually with vegetation, in rivers (Longstaff, 1914; Brown, Fison et al., 1984), lakes (Lévêque, 1972) and irrigation channels (Madsen et al., 1988). DISTRIBUTION (Fig. 74). Egypt, Sudan, Somalia (Giuba and Uebi rivers; Brown & Gerlach, 1991), Ethiopia (lower Awash valley and southern lowlands) and westwards to Senegambia. In West Africa the southern limit extends to about latitude 8°N, but in the East the range needs to be more clearly established in comparison with C. ferruginea; the southern limit of bulimoides appears to lie in the lower Tana River basin of Kenya. Late Pleistocene-Holocene distribution includes localities in upper Egypt, Kordofan region of Sudan, central Chad and southern Libya (Van Damme, 1984). Cleopatra ferruginea (I. & H.C.Lea, 1850, Melania). Type locality: Zanzibar, East Africa. Fig. 58d. 30×15 mm. Shell shaped like the typical non-carinate form of C. bulimoides, but commonly more darkly coloured and growing larger. C. ferruginea is not yet adequately characterised as a species. Other early names include Melania amaena Morelet, 1851 (probably from Zanzibar; Brown & Gerlach, 1991, p. 478)

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and M. zanguebarensis Petit, 1851 (from ‘Zanzibar, côte de Zanguebar’). C. dautzenbergi Pilsbry & Bequaert, 1927 (SE Zaire, Lovoi River) is perhaps conspecific. HABITAT. Ponds, streams, swamps and ditches (Mozley, 1939; Azevedo et al., 1961); Pringle & Msangi (1961) described population fluctuations in a fish pond. Muddy residual pools of seasonal streams, and amongst rocks in permanent rivers near the Kenyan coast. DISTRIBUTION (Fig. 74). E Kenya, Zanzibar and mainland Tanzania southwards into N Natal; western limits uncertain. A report for Cape Province (Connolly, 1939) is unconfirmed. Cleopatra africana (Martens, 1878, Paludomus). Type locality: Finboni (probably on the Kenya coast). Fig. 58e. 30×18 mm. Like C. ferruginea, but last whorl flatter near the suture and operculum much thicker (Kristensen, 1987). DISTRIBUTION. Coastal Kenya and Tanzania (DBL). Cleopatra obscura Mandahl-Barth, 1968a. Type locality: SE Zaire, Kimililo River at Keyberg. Fig. 58f. 22×11 mm. Distinguished from C. ferruginea by the smaller size, less convex whorls, darker colour, coarser sculpture and especially the twisted columellar margin. DISTRIBUTION. SE Zaire: reported from only the type locality. Cleopatra exarata (Martens, 1878, figured as Paludomus cingulata). Type locality: Finboni (probably on the coast of Kenya). Fig. 58g. 27×13 mm. Strong and regular spiral grooves and ridges are characteristic. DISTRIBUTION. Kenya: southern coastal region (BME, DBL). Cleopatra elata Dautzenberg & Germain, 1914 (C. pirothi variety elata). Mandahl-Barth, 1974 (C. elata). Type locality: SE Zaire, Lualaba River at Bulongo (Bukama). Figs 58h, 59a. 13×6 mm. Typical shell (Figs 61a,d) slender; spire may reach from 2 to 3 times the height of the aperture; whorls strongly convex, with 3–5 fine spiral ridges; slender brown bands on a yellowish ground colour. Central radular tooth narrow (Mandahl-Barth, 1974). Variation discussed by Brown et al. (1992); the broader shells approach the shape of C. smithi (see below). To C. elata perhaps belong the snails from Chirundu (Figs 58h, 59b) identified previously as C. lesnei (see Brown & Mandahl-Barth, 1989) DISTRIBUTION. SE Zaire: type locality and Kongolo (Mandahl-Barth, 1974). Upper Zambezi River, E Caprivi, Okavango River and Delta (Brown et al., 1992). Possibly also Middle Zambezi Basin: Zimbabwe, Chirundu (DBL, BME). Cleopatra cridlandi Mandahl-Barth, 1954. Type locality: Uganda, Lake Victoria near Dagusi Island, at 6–12 m depth. Fig. 58i. 11×6 mm. Small, slender, whorls strongly convex, with up to 4 spiral ridges. DISTRIBUTION. Lake Victoria: Dagusi Island, Buvuma Channel and Kavirondo (Winam) Gulf.

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Fig. 58. Thiaridae: Cleopatra, (a) C. bulimoides; Ethiopia, lower Awash River, (b) C. bulimoides (form pirothi Jickeli); Ethiopia, lower Awash River, (c) C. bulimoides; Senegal River at Podor (syntype of C. senegalensis (Morelet), BMNH1893.2.4.1900–02). (d) C. ferruginea: NE Tanzania, Mnagaro. (e) C. africana; Tanzania, Bagamoyo (identified by G.Mandahl-Barth), (f) C. obscura; SE Zaire (paratype, BMNH1968.700). (g) C. exarata; Kenya, Maji ya Chumvi. (h) C. elata; Zimbabwe, Chirundu. (i) C. cridlandi; Uganda, Lake Victoria (syntype, BMNH 1968.599). Scale line: 5 mm.

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Fig. 59. Thiaridae: Cleopatra and Paludomus. (a) Cleopatra elata; SE Zaire (syntype, MNHN). (b) C. pilula; Zaire, Kasai region (paratype, DBL). (c,f) C. rugosa from Somalia: (c) syntype, BMNH1937.12.30.4997–8; (f) near Bardera, (d) Paludomus tanschaurica Gmelin; probably from S Asia (holotype of ‘Cleopatra’ lesnei Germain, 1935, MNHN). (e) Paludomus ajanensis; probably from the Seychelles Islands (holotype, BMNH1893.2. 4.1525). (f) see (c). Scale line: 5 mm.

Cleopatra langi Pilsbry & Bequaert, 1927. Type locality: E Zaire, Kisangani (Stanleyville). 8.3×6 mm (3 whorls remaining). Shell relatively broad, the complete spire probably no higher than the aperture, with 1 or 2 strong spiral ridges. DISTRIBUTION. E Zaire: reported from only the type locality. Cleopatra johnstoni Smith, 1893. Type locality: Lake Mweru. Fig. 60a. 15×9.5 mm. Whorls flattened and strongly carinate at the periphery. DISTRIBUTION. Lake Mweru and the Luapula River (Mandahl-Barth, 1968a). Cleopatra mweruensis Smith, 1893. Type locality: Lake Mweru. Fig. 60b. 15.5×9 mm. Whorls convex, carinate, with 1 or 2 basal ridges. DISTRIBUTION. Lake Mweru (Mandahl-Barth, 1968a). Cleopatra smithi Ancey, 1906. Type locality: N Zambia, Chozi River in Upper Chambeshi region. Fig. 60c.

134 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 60. Thiaridae: Cleopatra, (a) C. johnstoni; Lake Mweru (syntype, BMNH1893.8.23. 95–7). (b) C. mweruensis; Lake Mweru (syntype, BMNH1893.8.23–90–4). (c) C. smithi; Zambia, (d) C. nsendweensis; SE Zaire, Kakonde. (e) C. nsendweensis; Zambezi River above Victoria Falls (corresponding to C. morrelli Preston), (f) C. guillemei; W Kenya, Kano Plain, (g) C. athiensis; Kenya, east of Nairobi, (h) C. hemmingi; Somalia (holotype, BMNH 1956.10.31.1–2). Scale line 5 mm.

18×10.5 mm. Like C. mweruensis, but spiral ridges are confined to the early whorls in the typical form (Fig. 60c) or extend only weakly into the last whorl (C. mterizensis Melvill & Standen, 1907 and C. hargeri Smith, 1908); basal ridges lacking. DISTRIBUTION. Zambia: tributaries of rivers near Lake Mweru (C. hargeri and C. mweruensis smithi of Mandahl-Barth, 1968a) and in the south-east near Petauke (C. mterizensis). Cleopatra nsendweensis Dupuis & Putzeys, 1902 (C. bulimoides variety nsendweensis). Type locality: Nsendwe (one of 3 localities given by Dupuis & Putzeys; at 3°05′ S 26°E according to Pilsbry & Bequaert, 1927). Figs 60d,e. 16×10 mm (3 remaining whorls). Lower whorls smooth and somewhat flattened; umbilicus variable and largest in the form C. morelli Preston, 1905. A senior name could be C. welwitschi Martens, 1897 (from Angola). DISTRIBUTION. Zaire: SE region (Mandahl-Barth, 1968a; Mandahl-Barth et al., 1972) also Ubangi and Kinshasa (DBL). Zambia: Zambezi River above

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Victoria Falls (C. morelli) and Kafue River (DBL, BME). Angola (Wright, 1963a, as C. bulimoides). N Namibia (Cunene and Okavango rivers) and N Botswana (Chobe River) (Brown et al., 1992). Cleopatra pilula Mandahl-Barth, 1967. Type locality: S Zaire, Bushimaie River at Lukuta, Kasai region. Fig. 59b. 15×10 mm. Shell broad, spire low, columellar margin of aperture expanded closing the umbilicus. A distinctive species, rather like a young Pila. DISTRIBUTION (Fig. 74). SE Zaire, Kasai region. Cleopatra guillemei Bourguignat, 1885b. Type locality: near the Mission of Nyanza Oukéréwé (S shore of Lake Victoria). Fig. 60f. 15×10 mm. Spire usually less high than aperture, whorls strongly convex; upper whorls with 2 or 3 spiral ridges joined by short ribs; umbilicus open and usually surrounded by a few spiral ridges, but these may not extend to the aperture (C. nyanzae Mandahl-Barth, 1954a). Synonyms include Vivipara brincatiana, V. bridouxiana and probably also C. jouberti, all of Bourguignat, 1888 (see Brown & Mandahl-Barth, 1987, note 25). HABITAT. Small seasonal streams and rainpools in W Kenya near Lake Victoria, but not found within the lake. DISTRIBUTION. NW Tanzania and SW Kenya. Mainly found close to Lake Victoria (Kisumu; Mandahl-Barth, 1954a, and Brown, 1980a) and Lake Tanganyika near the mouth of the Malagarasi River (Bourguignat, 1890) and at Pala (Leloup, 1953); also at Singida (DBL). Cleopatra athiensis Verdcourt, 1957. Type locality: Kenya, Athi Plains (east of Nairobi). Fig. 60g. 14×10 mm. Whorls strongly convex, umbilicus widely open; spiral ridges connected by short ribs, but no basal ridges (unlike C. guillemei). DISTRIBUTION. Kenya: Athi Plains, obtained by myself from a small seasonal stream. Cleopatra hemmingi Verdcourt, 1956, in Hemming & Verdcourt (1956). Type locality: Somalia, 29 km (18 miles) W of Beles Cogani, shallow pool. Fig. 60h. 11.3×8 mm. Like C. athiensis but smoother. A possible synonym is C. convexa Verdcourt, 1957 described from larger, subfossil shells found near Lodwar in Kenya. HABITAT AND DISTRIBUTION. SW Somalia: shallow seasonal pools (Hemming & Verdcourt, 1956). Cleopatra rugosa Connolly, 1925. Type locality: Somalia, Agherrar. Figs 59c,f. 16×10 mm. Whorls strongly convex, with numerous close-set transverse ridges (unlike those of any other Cleopatra); umbilicus large; pale coloured and almost unbanded. Operculum and soft parts unknown to Connolly, but whole animals collected in 1983 by C.F.Hemming (BME, kindly submitted by B.Verdcourt) have a smooth mantle border like Cleopatra. HABITAT. Saline marsh (Connolly, 1928a); semi-permanent pool (Hemming).

136 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

DISTRIBUTION. Somalia: Giuba Basin, type locality and 42 km N of Bardera (BME). Species of Madagascar (see synonymies of Starmühlner, 1969 for names additional to those mentioned below). Cleopatra colbeaui (Craven, 1880b, Paludina). Type locality: Madagascar, island of Nossi-Bé. Fig. 61a. 11×6 mm. Last whorl large and strongly convex; umbilicus narrow; surface appearing smooth, though with fine transverse and spiral sculpture; pale coloured (syntypes, BMNH). HABITAT AND DISTRIBUTION. Sluggish stream (Craven, 1880b), small streams in forest (Starmühlner, 1969), most frequent in central and N Madagascar (Fischer-Piette & Vukadinovic, 1973). Cleopatra madagascariensis (Crosse & Fischer, 1872, Paludina). Type locality: eastern Madagascar. Figs 61b,c. 12.5×6.5 mm. Whorls strongly convex, umbilicus larger than in C. colbeaui; with obvious spiral ridges. Spiral ridges may be few and confined to the upper half of the last whorl (typical form), or run also below the periphery (C. trabonjiensis Smith, 1882) (Fig. 61b); shells with numerous ridges all over seem conspecific (Fig. 61c). HABITAT AND DISTRIBUTION. Small streams and Lake Alaotra (Starmühlner, 1969); irrigation channels and rice fields (Degrémont, 1973, pp. 64, 75; C. carinulata and ‘Bithynia sp.’); throughout Madagascar (Fischer-Piette & Vukadinovic, 1973). Cleopatra grandidieri (Crosse & Fischer, 1872, Paludomus). Type locality: eastern Madagascar. Fig. 61d. 13.5×8.5 mm (about 2 whorls remaining). Last whorl large, strongly convex, umbilicus small; with conspicuous regular spiral ridges; uniformly brown. HABITAT AND DISTRIBUTION. Forest stream (Starmühlner, 1969); E Madagascar and a few localities on the W coast (Fischer-Piette & Vukadinovic, 1973). Genus Paludomus Swainson, 1840 Medium-sized, some species with shells similar to Cleopatra, but differing anatomically and apparently confined to S Asia and the Seychelles Islands. Species of the subgenus Paludomus are particularly like some species of Cleopatra and the opercula have the same structure, but the mantle border of Paludomus has papillae (whereas it is smooth in Cleopatra). Two species believed previously to be Cleopatra of African origin were recently found to belong in Paludomus and it seems likely that African localities were attributed to them in error: P. ajanensis Morelet, 1860 (Fig. 59e) has been regarded as a form of C. bulimoides (Brown, 1980a, Fig. 74, locality 17), but probably is confined to the Seychelles Islands. The supposed type locality (Somalia, Cape Guardafui, Ras Hafun) seems mistaken (Brown & Gerlach, 1991).

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Fig. 61. Thiaridae. (a–d) Cleopatra from Madagascar, (a) C. colbeaui; Nossi-Bé (BMNH1891.3.7.57–63). (b) C. madagascariensis; Trabonji (syntype of C. trabonjiensis Smith, BMNH1882.3.5.8–9). (c) C. madagascariensis; lower Mangoky region, (d) C. grandidieri; NW of Mananjary. (e–g) Pseudocleopatra. (e) P. voltana; Ghana, Apaso. (f) P. togoensis; NE Ghana, Mogeyenga. (g) P. bennikei; lower Zaire River (paratype, BMNH1993.073). Scale line: 5 mm.

‘Cleopatra’ lesnei Germain, 1935 (Fig. 59d), supposedly from the Zambezi River basin, was founded on a shell of Paludomus tanschaurica Gmelin, 1791, which is confined to S Asia (Brown & Mandahl-Barth, 1989). Shells actually from the Zambezi basin and previously identified (Brown, 1980a) as C. lesnei are here placed provisionally under C. elata (Fig. 58h). Genus Pseudocleopatra Thiele, 1928 Small to medium-sized; shell like Cleopatra, but usually lacking dark spiral bands, operculum with larger spiral nucleus (about 2/3 of diameter, Fig. 9g) and central radular tooth with more numerous cusps (about 20; Mandahl-Barth, 1973b). In rivers of western Africa; 4 species. Type species: Pseudocleopatra togoensis Thiele, 1928, Togo. Pseudocleopatra togoensis Thiele, 1928. Type locality: Ghana, Volta River near Apaso (in Togo according to Thiele, but apparently in SE Ghana near Akwamu). Figs 9g; 61f.

138 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

13×9 mm. Shell ovate, last whorl large, rather flattened, smooth; upper whorls with one spiral ridge or more; coloured olive-green. Operculum and radula described by Mandahl-Barth (1973b). DISTRIBUTION. E Ghana: Volta River at Apaso near Akwamu (Thiele, 1928 and collected by M.Odei, 1961, BME); Mogeyenga (DBL), possibly on the Oti River. Pseudocleopatra voltana Mandahl-Barth, 1973b. Type locality: Ghana, Volta River at Daboya. Fig. 61e. 12×6 mm. Shell slender, conical, smooth or with spiral ridges of varying strength, sometimes carinate; yellowish-brown, darker bands may be present. DISTRIBUTION. Ghana: SE region in the Volta River at Daboyu and Apaso (near Akwamu), also in NE region (Mandahl-Barth, 1973b). Pseudocleopatra dartevellei Mandahl-Barth, 1973b. Type locality: Zaire River at Matadi. Fig. 62a. 7.6×5.4 mm (only 3 whorls remaining). Distinguished by Mandahl-Barth from P. togoensis by its smaller size, less angular whorls and thinner shell; operculum and radula similar to that species. DISTRIBUTION. Lower Zaire River: reported from only the type locality. Pseudocleopatra bennikei Mandahl-Barth, 1974. Type locality: Zaire River between Mimosa Island and Monkey Island near Kinshasa. Fig. 61g. 14×12 mm (2 whorls remaining). Last whorl broad and bluntly angular; columellar lip expanded and thickened; coloured pale brown, unbanded. Generic position uncertain as operculum and body are unknown. DISTRIBUTION. Zaire River: type locality and nearby places, also Kala Kala near Matadi (Mandahl-Barth, 1974). Genus Potadomoides Leloup, 1953 Small to medium-sized, shell similar to Cleopatra, smooth or strongly sculptured and may have dark bands; operculum paucispiral, nucleus near centre; central tooth with only 3 cusps (radula like Lavigeria); mantle border smooth. Viviparous with uterine brood pouch (Leloup, 1953). Leloup named this genus because P. pelseneeri resembled Potadoma in its shell and operculum (but differed in its differently-shaped central tooth with fewer cusps). Cleopatra differs too in having more cusps on the central tooth and also in its mostly concentric operculum. Mandahl-Barth (1967) added 4 species previously classified as Cleopatra, having examined the radula of three. All the species seem rare; they are of particular interest in relation to the ancestry of the endemic prosobranch snails of Lake Tanganyika (Chapter 12). Central Africa; 5 species, known only from the Malagarasi Delta in Lake Tanganyika and rivers in E Zaire. Type species: Potadomoides pelseneeri Leloup, 1953, Malagarasi Delta. Potadomides pelseneeri Leloup, 1953. Type locality: Tanzania, Malagarasi River, delta in Lake Tanganyika. Fig. 62b.

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Fig. 62. Thiaridae. (a) Pseudocleopatra dartevellei; lower Zaire River (paratype, DBL). (b) Potadomoides pelseneeri; Malagarasi Delta (after Leloup, 1953, Pl. 3, Fig. 6). (c) P. bequaerti; E Zaire, Lualaba River at Lokandu (DBL). (d) (?) Potadomoides broecki; E Zaire (holotype after Putzeys, 1899, Fig. 16). Scale line: 2 mm.

12×6 mm. Shell ovate, thick-walled with slightly curved sides, lip thickened; last whorl weakly carinate at periphery, with variable spiral ridges, strongest at base. HABITAT AND DISTRIBUTION. Tanzania: shore of Lake Tanganyika, from vegetable debris in a calm bay, at 30–40 cm depth (Leloup). Potadomoides bequaerti (Dautzenberg & Germain, 1914, Cleopatra). Type locality: E Zaire, Lualaba River at Kindu (3°S). Fig. 62c. 8×5 mm. Small, with strong varied sculpture, sometimes forming low spines. DISTRIBUTION. E Zaire: Lualaba River at Kindu and Lokandu. Potadomoides hirta (Dautzenberg & Germain, 1914, Cleopatra). Type locality: E Zaire, Lualaba River at Nyangwe (4°15′S). 14×9 mm. Comparatively large, with strong ridges and spines. DISTRIBUTION. E Zaire: Lualaba River at Nyangwe and Kasongo. Potadomoides schoutedeni (Dautzenberg & Germain, 1914, Cleopatra). Type locality: E Zaire, Lualaba River at Kindu.

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9×6 mm. Shaped like P. bequaerti, but with regular spiral ridges all over. DISTRIBUTION. E Zaire: rivers Luvua and Lualaba. (?)Potadomoides broecki (Putzeys, 1899, Cleopatra). Type locality: E Zaire, Oriental Province, Aruwimi River. Fig. 62d. 10.5×6.5 mm. Thick-walled, weakly angular at periphery, with short transverse ridges on upper whorls. Radula and operculum unknown. DISTRIBUTION. Zaire: reported only from the type locality, found on the bivalve Etheria. The thalassoid snails of Lake Tanganyika

These genera are endemic to Lake Tanganyika and are termed thalassoid (marine-like) because they resemble prosobranchs of the sea-shore rather than the usual run of freshwater kinds (Chapter 12: Lake Tanganyika). This assemblage of species is highly varied, obscure in origins and relationships to living non-lacustrine groups, and it is unlikely that all should be classified in the Thiaridae. Morrison (1954), relying on descriptions of anatomy by Moore (1898, 1899), placed some genera in the Pleuroceridae. All were united in the Thiaridae by Leloup (1953), who studied extensive new materials but provided significant new data for only the operculum and radula. Knowledge of these most interesting snails is being greatly advanced through recent and current studies (Michel et al., 1992) and changes in classification can be expected. Genus Syrnolopsis Smith, 1880 Small slender snails, with the sides of the spire more or less curved, whorls numerous, smooth or with spiral ridges; columella with a fold visible to a varying extent in the aperture, umbilicus closed. Operculum thin, paucispiral; mantle border smooth; central tooth with 7 cusps; female apparently oviparous, as a brood pouch is lacking (Mandahl-Barth, 1954b). Lake Tanganyika: 3 species. Type species: Syrnolopsis lacustris Smith, 1880, Lake Tanganyika. Syrnolopsis lacustris Smith, 1880b; 1881a, Pl. 32. Type locality: Lake Tanganyika. Fig. 63a. 11.5×3.0 mm (usually less than 9 mm high). Typical large shells are smooth (Fig. 63a). The smaller, carinate, shells illustrated by Leloup (1953, Figs 68E– P) seem to be a different species (S. minuta, below). DISTRIBUTION. Lake Tanganyika: on sandy substrata in shallow water (Leloup). Syrnolopsis minuta Bourguignat, 1885b; 1888, Pl. 10. Type locality: Lake Tanganyika at Pambete. Figs 63b,c. 5.8×2.0 mm. Smaller than S. lacustris, whorls smooth or carinate (S. carinifera Smith, 1889); columellar fold emerging strongly into the aperture. Shells identified as S. lacustris by Leloup (1953, Figs 68E–P) seem to include this species.

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Fig. 63. Thiaridae endemic to Lake Tanganyika (see also Figs 64–67). (a) Syrnolopsis lacustris (syntype, BMNH1880.12.20.57–64). (b,c) S. minuta (syntypes of S. carinifera Smith, BMNH1889.6.23.62–72). (d) S. gracilis. (e) Anceya giraudi (holotype of A. rufocincta Smith, BMNH1906.4.5.11). (f) A. terebriformis (syntype, BMNH1890.5.16.9). Scale line: 2 mm.

DISTRIBUTION. Lake Tanganyika: Pambete, Ufipa and Kigoma (Pilsbry & Bequaert, 1927). Syrnolopsis gracilis Pilsbry & Bequaert, 1927. Type locality: Lake Tanganyika. Fig. 63d. 4.3×1.2 mm. Small and slender with up to 9 convex whorls, of which at least the upper ones have spiral ridges; columellar fold weak. DISTRIBUTION. Lake Tanganyika: from 0–116 m (Leloup, 1953).

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Fig. 64. Thiaridae: Martelia tanganyicensis, Lake Tanganyika (after Pilsbry & Bequaert, 1927, Fig. 38). Scale line: 1 mm.

Genus Anceya Bourguignat, 1885 Slender snails, like Syrnolopsis having many whorls and a columellar fold, but with transverse ribs instead of spiral ridges and the upper spire is regularly tapered with straight sides. Like Syrnolopsis in operculum, radula and soft parts (Mandahl-Barth, 1954b). Lake Tanganyika: perhaps only a single species is common. Type species: Anceya giraudi Bourguignat, 1885, Lake Tanganyika. Anceya giraudi Bourguignat, 1885b; 1889a. Type locality: Lake Tanganyika, near Mlilo on the W shore. Fig. 63e. 12×3.3 mm (usually smaller). Ribs present on all whorls, the last may have also a strong carina near the base. Apparently synonyms include A. admirabilis Bourguignat, 1889a (a slender form), A. rufocincta Smith, 1906 (with a brown band below the suture) (Fig. 63e) and A. bella Pilsbry & Bequaert, 1927 (with a weak columellar fold). DISTRIBUTION. Lake Tanganyika: widespread, found alive down to 100 m (Leloup, 1953). Anceya terebriformis (Smith, 1890, Turbonilla; 1904, Fig. 2, Burtonilla). Type locality: Lake Tanganyika (without details). Fig. 63f. 12×2.7 mm. The shell differs from A. giraudi in its proportionally broader whorls and weaker ribs. At least the larger of two syntypes (BMNH, Fig. 63f) seems to be distinct from the range of variation acceptable in A. giraudi, but

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further evidence is needed to support the status of terebriformis as a different species. DISTRIBUTION. Lake Tanganyika: known from only the type specimen. Genus Martelia Dautzenberg, 1908 Very small, slender, strongly ribbed or carinate, with a columellar fold; like Syrnolopsis and Anceya in operculum, radula and soft parts, though differing in apparently minor ways (Bouillon, 1955). Lake Tanganyika: perhaps only one species. Type species: Martelia tanganyicensis Dautzenberg, 1908, Lake Tanganyika. Martelia tanganyicensis Dautzenberg, 1908a. Type locality: Lake Tanganyika at Mpala on the W shore. Fig. 64. 2.3×1.2 mm. Very small, usually strongly ribbed though ribs may fuse at the periphery forming a single carination (M. dautzenbergi Dupuis, 1924). DISTRIBUTION. Lake Tanganyika: many localities (Leloup, 1953). Genus Lavigeria Bourguignat, 1888 Medium to large, shell ovately or more narrowly conic, thick-walled, with varied intersecting sculpture in which ribs usually predominate. Operculum subspiral with nucleus at basal margin (the spiral nucleus shown by Leloup, 1953 for some forms has yet to be confirmed; Brown & Mandahl-Barth, 1987, note 46). Radula (Fig. 52e) like that of Potadomoides. Mantle border smooth. Female viviparous with a uterine brood pouch (Moore, 1899b). Lake Tanganyika: most species live in shallow water, but at least one is found down to 50 m. A large number of species named in the last century were placed in synonymy by later authors, and this lumping culminated in the recognition of only a single species by Leloup (1953) and two by Brown (1980a). Recent studies of morphology, habitat, breeding cycle and protein variation demonstrated much greater speciation, and there apparently are at least ten reproductively isolated forms (Michel et al., 1992). As names have not yet been assigned to the newly recognised species, the classification adopted in the first edition of this book is retained here, and it must be emphasised that certainly L. nassa and probably also L. grandis comprise a number of distinct species. The name Lavigeria has priority for this group over Edgaria employed by Leloup (1953; see Brown & Mandahl-Barth, 1987, note 45). Type species: Melania nassa Woodward variety grandis Smith, 1881b, Lake Tanganyika. Lavigeria nassa (Woodward, 1859, Melania). Leloup, 1953 (Edgaria nassa excluding forms globosa and grandis). Type locality: Lake Tanganyika at Ujiji. Figs 65a,b. 17.5×11 mm (syntype of nassa Woodward). Different ‘morphospecies’ vary in size, shape and sculpture (Johnston & Cohen, 1987; Michel et al., 1992). L.

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nassa as originally described (Fig. 65a) has numerous nodular ribs; ribs are few in the form paucicostata of Smith, 1881b; Leloup, 1953 (Fig. 65b). HABITAT AND DISTRIBUTION. Abundant in the littoral zone of Lake Tanganyika, browsing on algae on wave-beaten rocks (Leloup, 1953); other species are adapted to soft sandy substrata and one lives down to 50 m (Michel et al., 1992). Lavigeria grandis (Smith, 1881b as variety of Melania nassa Woodward). Type locality: Lake Tanganyika, E shore. Fig. 65c. 32×22 mm. Large and broad, whorls somewhat flattened at the suture; dominant sculpture varies from spiral ridges to strongly tuberculate ribs (Leloup, 1953); lower lip bluntly angular below the twisted columella. DISTRIBUTION. Lake Tanganyika: in shallow water (Leloup, 1953). Genus Mysorelloides Leloup, 1953 A single known species.

Mysorelloides multisulcata (Bourguignat, 1888, Bythinia). Type locality: Lake Tanganyika, Ubuari Peninsula on the W shore. Fig. 66a. 10.5×5.0 mm. Shell ovately conic, whorls strongly convex, with strong spiral ridges. Operculum entirely spiral; radular teeth with numerous fine cusps; mantle border smooth (Leloup, 1953, Fig. 41B). Placed incorrectly by Pilsbry & Bequaert (1927) in the Indian genus Mysorella Godwin-Austen. DISTRIBUTION. Lake Tanganyika: all shores, down to 60 m (Leloup). Genus Hirthia Ancey, 1898 Shell medium-sized, sub-globose to ovate, thick-walled with conspicuous sculpture; lip oblique, its columellar margin expanded, closing the umbilicus. Operculum and soft parts unknown. Type species: Hirthia littorina Ancey, 1898, Lake Tanganyika. Hirthia globosa Ancey, 1898. Leloup, 1953 (as form of Edgaria nassa). Type locality: Lake Tanganyika, SE shore in Ufipa district. Fig. 66b. 10×12.5 mm. Depressed, with large last whorl and oblique lip; spiral ridges intersect ribs forming low nodules. DISTRIBUTION. Lake Tanganyika: Ufipa and Pala (Leloup). Hirthia littorina Ancey, 1898. Type locality: Lake Tanganyika, SE shore, Ufipa. 12×9 mm. Like H. globosa, but spire higher and ribs more distinct (Leloup, 1953, Pl. 13,1). DISTRIBUTION. Lake Tanganyika: Ufipa and Mtossi (Leloup).

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Fig. 65. Thiaridae of Lake Tanganyika, (a) Lavigeria nassa (syntype, BMNH1859.12.3. 11). (b) L. nassa (paratype of variety paucicostata Smith, BMNH1880.12.20.53–4). (c) L. grandis (syntype, BMNH1880.12.22.6–8). (d) Spekia zonata (syntype, BMNH1859.12. 23–10). (e) Tanganyicia rufofilosa (syntype, BMNH 1880.12.20.65–8). (f) Stanleya neritinoides. (g) Paramelania damoni (syntype, BMNH1881.4.11.1). (h) P. iridescens. Scale line: 10 mm for all except (f; 7 mm).

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Genus Spekia Bourguignat, 1879 A single known species.

Spekia zonata (Woodward, 1859, Lithoglyphus). Type locality: Lake Tanganyika, E shore at Ujiji. Fig. 65d. 14×14.5 mm. Depressed, with large last whorl and oblique lip; basal area hollowed and surrounded by a carina; smooth and spirally banded with various shades of grey. Operculum concentric with small spiral nucleus. Central tooth (Fig. 52d) without a median cusp. Mantle edge smooth. Genital organs described by Moore (1899a, 1903); oviparous (Michel et al., 1992). HABITAT AND DISTRIBUTION. Lake Tanganyika: browsing algae on rocks on calm and wave-washed shores (Leloup, 1953). Genus Tanganyicia Crosse, 1881 Perhaps no more than one, variable species.

Tanganyicia rufofilosa (Smith, 1880b; 1881a, Pl. 33, Lithoglyphus). Type locality: Lake Tanganyika. Fig. 65e. 17×14 mm. Shell ovately conic; smooth with narrow, brown spiral lines; umbilical area concave and surrounded by a ridge. Operculum concentric with paucispiral nucleus (Smith, 1881a; Leloup, 1953). Radula with long marginal teeth (Pilsbry & Bequaert, 1927; Leloup, 1953). Mantle border smooth; female viviparous, with brood pouch opening on the right side (Moore, 1899a). Smith (1904) and Leloup united many named forms. HABITAT AND DISTRIBUTION. Lake Tanganyika: all shores, on rocks and other firm substrata, from the surface down to 20 m (Leloup). Genus Stanleya Bourguignat, 1885 Perhaps only one species.

Stanleya neritinoides (Smith, 1880b; 1881a, Pl. 33, Lithoglyphus). Type locality: Lake Tanganyika. Fig. 65f. 9.8×8.0 mm. Similar in shape to Tanganyicia and also with brown spiral lines, but more neritoid, with the inner lip broadly expanded and thickened, forming a convex plate over the umbilical area; surface shining. Operculum entirely spiral; mantle border smooth. Some named forms are based on juvenile shells, which are less neritoid, with only thin callus in the umbilical area. DISTRIBUTION. Lake Tanganyika: on all shores, in shallow water (Leloup).

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Genus Reymondia Bourguignat, 1885 Small to medium-sized, shell rather narrowly conic when mature; whorls weakly curved, smooth (sometimes with a few spiral lines in at least R. horei); mature lip thickened, but inner margin not expanded into a columellar plate. Operculum concentric with spiral nucleus; central tooth with large median cusp; mantle border smooth (Leloup, 1953; confirmed by myself in R. horei from Pemba, Zaire). Lake Tanganyika: littoral zone down to about 10 m (Leloup). Type species: Melania(?) horei Smith, 1880b, by designation of Pilsbry & Bequaert (1927). Only one species was recognised by Leloup (1953) and Brown (1980a), but from consideration of the varied relationship between shell size and whorl number, it seems there may be 3 or more species (Brown & Mandahl-Barth, 1987): R. horei (Smith, 1880b; 1881a, Pl. 34, Melania) (Fig. 66c), 16×9 mm; the largest species, distinctively coloured reddish-brown with light band along the suture. R. pyramidalis Bourguignat, 1888 (perhaps the same as R. minor Smith, 1889) (Fig. 66d), 9×4 mm; smaller than R. horei, more slender and paler coloured. R. tanganyicensis Smith, 1889 (Fig. 66e), 3.5×1.7 mm; already with 5 whorls and perhaps mature at this small size. Genus Bridouxia Bourguignat, 1885 Much investigation is still needed to reach an understanding of the many species and groups comprised here in Reymondia and Bridouxia (see Brown & MandahlBarth, 1987, notes 44 and 48). The following description can be only provisional. Small snails, shell differing from Reymondia in their generally broader shape (some species almost globose), and the common expansion of the inner lip into a flat or concave columellar plate. Operculum with paucispiral nucleus and a varying outer zone of concentric growth (see Brown & MandahlBarth, 1987, note 44 on inaccuracies in the figures of Leloup, 1953). Central tooth like that of Spekia (Fig. 52d) in lacking a cusp in the usual median position (Leloup, 1953; confirmed by myself in B. praeclara from Kombe in Zambia). Lake Tanganyika: all shores, on hard substrata in shallow water, though below wave-action (Leloup). Type species: Bridouxia giraudi Bourguignat, 1885, Lake Tanganyika (by designation of Pilsbry & Bequaert, 1927). Leloup (1953) united within Bridouxia the genera Baizea, Coulboisia, Giraudia and Lechaptoisia, recognising only the one species B. giraudi, divided into smooth and spirally ridged forms. The latter were separated as B. ponsonbyi by Brown (1980a), and from further consideration of shell variation it appears that at least the following 6 species may be valid (for further details see Brown & Mandahl-Barth, 1987, note 44):

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Fig. 66. Thiaridae of Lake Tanganyika, (a) Mysorelloides multisulcata. (b) Hirthia globosa; Ufipa. (c–e) Reymondia horei complex: (c) typical large form; (d) R. minor (syntype, BMNH1889.6.23.47– 57); (e) R. tanganyicensis (syntype, BMNH1889.6.23.57– 61). (f) Bridouxia leucoraphe. (g) B. praeclara. (h) B. ponsonbyi (syntype, BMNH1889.6. 23.42–46). (i) Stormsia minima (syntype, BMNH1907.11.11.72–76). Scale lines: 2 mm.

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B. giraudi Bourguignat, 1885b; 1888, Pl. 4; 11×7 mm; Bourguignat figured a smooth shell, broad with a low spire (not slender as shown by Leloup, 1953, Fig. 78E). B. praeclara (Bourguignat, 1885b, Giraudia; 1888, Pl. 11) (Fig. 66g), 5×2.3 mm. A slender brown-banded shell; B. grandidieriana (Bourguignat, 1885b) is similar. B. leucoraphe (Ancey, 1890, Ponsonbya) (Fig. 66f), 4.5×3.3; last whorl broad. B. smithiana (Bourguignat, 1885b, Stanleya; 1888, Pl. 17, Coulboisia), 5×2.5 mm; with fine spiral sculpture on a polished surface (Leloup’s Fig. 79A at left may represent this species, but not Fig. 79A at right, which is B. ponsonbyi). B. ponsonbyi (Smith, 1889, Rissoa; Ancey, 1894, Lechaptoisia) (Fig. 66h), 6. 6 ×4.3; with well-defined spiral and transverse sculpture. B. rotundata (Smith, 1904, Stanleya, for S. neritoides of Bourguignat, 1890), 7×5 mm; last whorl large, globose, with narrow brown spiral lines. Here placed doubtfully in Bridouxia, following Pilsbry & Bequaert (1927); it may well be related more closely to Stanleya. Genus Stormsia Leloup, 1953 A single known species.

Stormsia minima (Smith, 1908a, Giraudia) Type locality: Lake Tanganyika. Fig. 66i. 3.3×1.6 mm. Very small, with smooth whorls. Operculum concentric with spiral nucleus; central tooth saddle-shaped and lacking any pointed cusp (Leloup, 1953; and in my specimens from Kombe, Zambia). HABITAT AND DISTRIBUTION. Lake Tanganyika: browsing algae on rocks in sheltered bays, near or above the water level (Leloup). Genus Paramelania Smith, 1881 Large, shell ovately or more narrowly conic; with strong, highly varied sculpture that may form spines. Operculum concentric with spiral nucleus. Radular teeth (Leloup, 1953) with fine numerous cusps. Mantle border smooth; female perhaps viviparous as the lower oviduct is enlarged (Moore, 1899b). Those shell forms lacking spines resemble Lavigeria, but differ in the generally more slender and more acutely tapered spire, the operculum (not subspiral) and the radula (cusps more numerous and finer than in Lavigeria). Lake Tanganyika: on varied substrata over a wide depth range, 2 or perhaps more species. Type species: Tiphobia (Paramelania) damoni Smith, 1881 (designated by Pilsbry & Bequaert, 1927). Paramelania damoni (Smith, 1881b, Tiphobia (Paramelania)). Type locality: Lake Tanganyika. Fig. 65g.

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37×28 mm. Strong ribs and spiral ridges intersect in highly varied patterns (Leloup, 1953, Pls. 11, 12). There may be a subsutural row of spines, low in the typical form (Fig. 65g) and longer in other named forms, or the surface may be evenly nodular (P. crassigranulata Smith, 1881b). The diversity in shell morphology suggests that more than one species may be confused here. HABITAT AND DISTRIBUTION. Lake Tanganyika: from 1.5–65 m depth, spired forms living on fine sediment, nodular forms on rocky shores or sandy beaches (Leloup). Paramelania iridescens (Moore, 1898b, Bythoceras). Type locality: Lake Tanganyika: S shore near Sumbu, supposedly taken alive at 182–213 m depth. Fig. 65h. 40×19 mm. More slender than P. damoni and with more uniform nodular sculpture; upper and lower lip prolonged when mature into a spine, usually longer above. DISTRIBUTION. Lake Tanganyika: living on muddy substrata, from 10–150 m depth (Leloup, 1953, who doubts reports of greater depths). Genus Bathanalia Moore, 1898 Medium-sized, shell rather narrowly conic, with spiral ridges and an outstanding peripheral carina having spines or tubercles. Operculum entirely paucispiral. Mantle border smooth; anatomy similar to Tiphobia according to Moore (1898a), therefore probably viviparous, and juveniles were found by Leloup (1953) in the mantle cavity of B. straeleni. Lake Tanganyika: in deeper water, 2 species. Type species: Bathanalia howesi Moore, 1898, Lake Tanganyika. Bathanalia howesi Moore, 1898a. Type locality: Lake Tanganyika, S shore near Mleroes, alive at depth of 243 m (800 feet). Fig. 67a. 25×17 mm. Carina with short spines. HABITAT AND DISTRIBUTION. Lake Tanganyika: S shore, few localities, from 45 m depth (Leloup, 1953, who considers the maximum to lie probably between 150 and 200 m rather than the 300 m claimed by Moore). Bathanalia straeleni Leloup, 1953. Type locality: Lake Tanganyika (without detail). 12×6 mm. Smaller than B. howesi and with weaker sculpture, the carina having only blunt tubercles. DISTRIBUTION. Lake Tanganyika: widespread, at 20–80 m depth (Leloup). Genus Tiphobia Smith, 1880 A single known species.

Tiphobia horei Smith, 1880a. Type locality: Lake Tanganyika at Ujiji. Fig. 67b.

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Fig. 67. Thiaridae of Lake Tanganyika, (a) Bathanalia howesi (possible syntype, BMNH1909.5.27.7–9). (b) Tiphobia horei (syntype, BMNH1880.3.5.1–3). (c) Limnotrochus thomsoni (syntype, BMNH1880.12.20.45–8). (d,e) Chytra kirki (syntype, BMNH1880.12.21.11–14). Scale line: 10 mm.

36×26 mm. The large shell, with long spines and lip elongated below is unmistakable. Operculum concentric with large spiral nucleus; central tooth with many fine cusps (Leloup, 1953). Mantle border smooth; female with brood pouch in the lower oviduct, male with mantle lobe perhaps used in copulation (Moore, 1898a). HABITAT AND DISTRIBUTION. Lake Tanganyika: muddy substrata, especially near river mouths, from the water’s edge down to 100–125 m (Leloup). Genus Limnotrochus Smith, 1880 A single known species.

Limnotrochus thomsoni Smith, 1880b; 1881, Pl. 33. Type locality: Lake Tanganyika. Fig. 67c. 19×14 mm. Shell shaped like Bathanalia howesi, but the peripheral carina and other strong spiral ridges bear only nodules (not spines). Mantle border smooth, operculum paucispiral, lateral radular tooth long and deep, with many cusps (Digby, 1902, whose figures were reproduced by Leloup, 1953). These features were confirmed by myself in a specimen from Kombe in Zambia, although in this radula the cusps on all teeth were more numerous and longer. DISTRIBUTION. Lake Tanganyika: many localities, on all shores, down to 70 m (Pilsbry & Bequaert, 1927; Leloup, 1953, locality No. 246).

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Genus Chytra Moore, 1898 A single known species.

Chytra kirki (Smith, 1880b; 1881a, Pl. 33, Limnotrochus). Type locality: Lake Tanganyika. Fig. 67d,e. 15×19 mm. Depressed, lip almost horizontal and umbilicus deep (Fig. 67d′); periphery strongly carinate, spire broadly conic, flat-sided; many spiral rows of nodules. Apparently like Limnotrochus in the operculum, radula and soft parts (Digby, 1902; Leloup, 1953). HABITAT AND DISTRIBUTION. Lake Tanganyika: widespread, on muddy substrata rich in organic matter deposited by rivers, found alive from 10–20 m and possibly down to 80 m (Leloup). Family Melanopsidae Medium to large, shell ovately or more narrowly conic, smooth or strongly sculptured. Operculum paucispiral with basal nucleus. Mantle border smooth. Both sexes occur; oviparous (Morrison, 1954). The essential characteristics of the family lie in the soft parts (Houbrick, 1988). Distribution is remarkably disjunct, in the Mediterranean area and Australian region (New Zealand and New Caledonia). The few genera include Fagotia Bourguignat, 1884 (Europe, lower Danube Basin) and Melanopsis. Genus Melanopsis Ferussac, 1807 Characters as for the family; lip with a notch at the base of the columella (unlike Fagotia of Europe). In rivers, lakes and various smaller habitats; tolerant of high temperature and moderate salinity. NW Africa, Mediterranean region, Near East and Arabia (related snails in New Zealand and New Caledonia). Number of species uncertain; all the many named forms from Africa may belong to a single ‘superspecies’ (Glaubrecht, 1992, 1993). Type species: Buccinum praemorsum Linnaeus, 1758, southern Europe. Melanopsis praemorsa (Linnaeus, 1758, Buccinum). Type locality: S Europe. Fig. 68a. 20×11 mm. Shell smooth or with strong spiral ridges or ribs (Fig. 68a). Four species of Melanopsis were distinguished in NW Africa on shell characters by Chevallier (1969) and 2 by Dupouy et al. (1980). No support for separating different shell forms in Israel was found in the radula (Tchernov, 1975a), but smooth and ribbed forms in Jordan were treated as different subspecies by Burch (1985). Yet there is no direct evidence of genetic differences between these different shell morphs and they all seem to belong to a single, circumMediterranean superspecies (Glaubrecht, 1992, 1993).

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HABITAT. Various waterbodies; the snails tolerate high temperature, desiccation and high dissolved chemical content (Dupouy, 1979; Dupouy et al., 1980; Meier-Brook et al., 1987). DISTRIBUTION. Circum-Mediterranean eastward into Mesopotamia. Morocco, N Algeria and W Tunisia; Late Pleistocene-Holocene distribution similar, extending a little further south in Algeria to Ouallen (Chevallier, 1969; Van Damme, 1984). Absent from Libya and Egypt, but found in Sinai (Tchernov, 1971) and both NW and E Saudi Arabia (Brown & Wright, 1980); widespread in the Near East (Burch, 1985). Family Potamididae Medium to large; shell narrowly conic, sculpture strong in species considered here; lip with deep basal notch below the columella. Operculum multispiral. The family is probably polyphyletic and subdivision has commenced (Houbrick, 1988, 1991). Widespread in brackish coastal waters of the tropics. Genus Cerithidea Swainson, 1840 Shell strongly ribbed. Mantle border smooth with a pallial siphonal eye; this with other morphological features, general biology and oviparous reproduction were described by Houbrick (1984). Especially common on mangrove roots and tree trunks; apparently only one species in Africa, on the E coast. Type species: Cerithium obtusum Lamarck, 1822, Timor. Cerithidea decollata (Linnaeus). Type locality: unknown. Fig. 68b. 32×15 mm (5 whorls remaining). Decollate when adult, strongly ribbed, greyish brown. HABITAT. Dense aggregations of snails occur on mangrove tree trunks; there is a rhythmic movement between the trees and the substrate where feeding occurs, related to tidal flooding (Brown, 1971; Cockcroft & Forbes, 1981a,b). DISTRIBUTION. Indo-Pacific coasts including E Africa: from Port Elizabeth to Kenya, Mida Creek (BME). Genus Tympanotonus Schumacher, 1817 Shell sculpture strong and varied, of ribs, spiral ridges and sharp tubercles. One species occurs on the coast of West Africa. Type species: Murex fuscatus Linnaeus, 1758, ‘M. Mediterraneo’. Tympanotonus fuscatus (Linnaeus, 1758, Murex; Adanson, 1757, Le Popel). Type locality: ‘M. Mediterraneo’ (an incorrect reference to the Mediterranean Sea). Fig. 68c. 80×25 mm. Two main forms of sculpture, small tubercles (form radula) or coarse ribs with short spines (form fuscata); which form develops depends upon

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Fig. 68. (a) Melanopsis praemorsa (form cariosa); Morocco, (b) Cerithidea decollata; South Africa, Durban, (c) Tympanotonus fuscatus; Ghana, (d) Terebralia palustris; Kenya, Mida Creek. (e,f) Pirenella conica; Egypt, (g) Littoraria (Littorinopsis) subvittata Reid, 1986; Kenya, Tiwi. Scale line: 6 mm (a) or 10 mm (b–g).

environmental conditions (Monteillet, 1979). Anatomy described by Johansson

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(1956). HABITAT. Commonly found with Pachymelania fusca (Thiaridae). Occurrence of the different sculptural forms in relation to salinity has been extensively studied (Binder, 1968; Monteillet & Plaziat, 1980, 1981). DISTRIBUTION. Senegal to S Angola, Mossamedes (Pilsbry & Bequaert, 1927). Other Potamididae

Terebralia palustris (Linnaeus). Fig. 68d. Large, 120×44 mm, with 13 whorls; low ribs and spiral grooves. Indo-Pacific coasts including E Africa, living on mud in the lower zone of mangrove swamps. Telescopium telescopium (Linnaeus) is similarly shaped and grows even larger; it is also a mangrove muddweller, but not it seems present in Africa. Morphology described and systematics reviewed by Houbrick (1991). Pirenella conica (de Blainville). Figs 68e,f. Medium-sized, 20×17 mm; with 2–4 spiral rows of nodules; variously coloured with white, grey and brown. Morphology described by Demian et al. (1966); mantle border with papillae. In brackish waters in the Mediterranean region, Red Sea and Arabian Gulf (Plaziat, 1982, Fig. 5); found 200 km inland in Egypt, Birket Qarun (Rose, 1972). Southernmost report is for Somalia (Connolly, 1928a; ‘Laguna di Hordio in Miggiurtina’). First intermediate host for Heterophyes heterophyes, a trematode which can develop in the intestine of man and produces heavy infections in some communities in the Nile Delta (Kuntz & Chandler, 1956; Taraschewski, 1985; see Chapter 6). References See end of Chapter 4. Notes to Figs 69–74 1. The stippled areas are intended to represent approximately the main areas of occurrence; continuity of distribution is not implied and in fact there may be significant discontinuities within stippled areas. 2. The more obviously isolated localities are indicated separately; solid circles (●) for populations living or believed to have been found alive and open circles (○) for records of weathered ‘subfossil’ shells of uncertain age, though in North Africa mostly of the Late Pleistocene-Holocene period (Van Damme, 1984).

156 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 69. Distribution of Bellamya in Africa and Arabia. Isolated or peripheral localities are indicated by numbers. The entire African range corresponds to the combined distributions of the two species B. unicolor and B. capillata. Others are either endemic to lakes or restricted to limited areas. 1. Libya; Tejerhi (Fischer-Piette, 1948). 2,3. Senegambia (Dautzenberg, 1890; Daget, 1961; Malek & Chaine, 1981). 4. Mali; middle Niger River (Daget, 1954; Madsen et al., 1987). 5. Nigeria; Kainji (BME). 6. Lake Chad. 7. Sudan; Khartoum (DBL). 8. Sudan; 2nd Nile Cataract (Martin, 1968). 9. Ethiopia; Lake Tana (Brown, 1965). 10. Ethiopia; Lake Abiata (subfossil, Brown 1965). 11. Kenya; Marsabit (Verdcourt, 1960b). 12. Kenya; Mombasa. 13. Yemen; Ta’iz (Viviparus sp., Ayad, 1956). 14. Central Jordan Valley (subfossil, Tchernov, 1975b). 15. Zaire; Kindu (Pilsbry & Bequaert, 1927). 16. Zaire; Stanley Pool (B. leopoldvillensis). 17. Angola; Cuije River (Wright, 1963a). 18. Angola; lower Cunene River (B. monardi). 19. Botswana; Botletle River district (B. passargei). 20. Zimbabwe; Gwebi River at Nyabira (BME). 21. E Transvaal; Komatipoort district (Schutte & Frank, 1964). 22. Natal; Makatini Flats (Brown, 1967a; Appleton, 1977c). 23. Madagascar; Majunga (Fischer-Piette & Vukadinovic, 1973, Viviparus unicolor; doubtful record). Additional records of Late Pleistocene-Holocene distribution in Niger and Chad reviewed by Van Damme (1984).

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Fig. 70. Distribution of Lanistes. Some peripheral localities are numbered as follows. L. ovum occurs nearly throughout the range and is present in the numbered localities unless indicated otherwise. 1. Senegal/Gambia (Dautzenberg, 1890; Daget, 1961; L. varicus). 2. Mali; Mopti (DBL); L. varicus; 3. Lake Chad (Lévêque, 1967). 4. Sudan; White Nile northwards to AdDuwem (Longstaff, 1914; L. carinatus). 5. Sudan; Wadi Howar (Sandford, 1936; L. carinatus). 6. Sudan; 2nd Nile Cataract (Martin, 1968; L. carinatus, subfossil). 7. Nile Delta (L. carinatus). 8. Sudan; Kassala (Malek, 1958). 9. Ethiopia; Sagan River district (Piersanti, 1941). 10. Kenya; Tana River at Hola (BME, L. ovum and L. carinatus). 11, 12. Somalia; Bardera and Buloburti (Bacci, 1951; L. carinatus). 13. Angola; Lagoa Delagosa (Wright, 1963a). 14. Botswana: Okavango Delta (Brown et al., 1992). 15. Zimbabwe; Chirundu (BME). 16. Mozambique; Tete. 17. Natal; Makatini Flats (Brown, 1967a; Pretorius et al., 1975). 18–20. Madagascar; Tulear, Miandrivaso and Ankasatasa (FischerPiette & Vukadinovic, 1973; L. grasseti). 21. Zanzibar and Pemba (L. purpureus).

158 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 71. Distribution of Gabbiella (Bithyniidae). Peripheral or isolated localities are numbered as follows. 1. Ivory Coast (G. africana). 2. Niger; Bengou (G. tilhoi). 3. Cameroon; Lake Wum (see G. depressa). 4. Lake Chad (G. neothaumaeformis, G. tchadiensis). 5, 6. Sudan; Malakal, Kosti (G. senaariensis). 7. Sudan; 2nd Nile Cataract (Martin, 1968). 8. Egypt; delta southwards to Beni Suef (G. senaariensis). 9. Ethiopia; lower Awash valley (G. adspersa). 10. Kenya; Lake Rudolf (G. rosea). 11. Kenya; Kano Plain (Gabbiella barthi). 12. Kenya; Taveta (G. verdcourti). 13. Somalia; lower Uebi Shebeli and Giuba rivers (G. parvipila). 14. Zaire; Matadi (G. matadina). 15. Angola; Cuije River (G. kisalensis). 16. Okavango Delta (G. kisalensis). 17. Zimbabwe; Chirundu (G. kisalensis). 18. Zambia; Fort Jameson (G. zambica). 19. Lake Malawi (G. stanleyi). 20. ?Zanzibar (see MandahlBarth, 1968b, p. 148). Additional Late Pleistocene-Holocene localities in Chad reviewed by Van Damme (1984).

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Fig. 72. Distribution of Potadoma and Melanatria (Thiaridae). Shaded areas approximate to the ranges of comparatively widespread species; less common species occur within one or other of these areas. Based on localities given by Mandahl-Barth (1967), MandahlBarth et al. (1974) and Fischer-Piette & Vukadinovic (1973). 1. Potadoma liberiensis (Liberia and some adjacent territories but not Sierra Leone). 2. P. vogeli (Ivory Coast). 3. P. togoensis (NE Ghana). 4. P. freethi (Ivory Coast to lower Zaire; P. moerchi is present from SE Ghana to Nigeria). 5. A group of species of which P. ignobilis and P. liricincta are the most widespread, occurring in NE Zaire and part of Central African Republic. 6. Melanatria; M. fluminea is recorded throughout Madagascar, though less frequently in the southwest.

160 SYSTEMATIC SYNOPSIS: PROSOBRANCHS

Fig. 73. Distribution of Melanoides tuberculata in Africa, Near and Middle East. Western limits in Africa between 5° and 25° S require critical determination with regard to possible confusion with M. anomala and M. victoriae. These two and other species occupy much of the area of western central Africa where M. tuberculata appears to be lacking. Some peripheral or isolated localities are numbered as follows. 1, 2. Tunisia/Algeria/Morocco/Mauritania; many scattered localities for Late PleistoceneHolocene shells reviewed by Van Damme (1984). 3. Mauritania; Karakoro River (DBL). 4. Gambia; Kentaur (DBL). 5. Ghana; Accra district (BME). 6. Nigeria; South-west (Ndifon & Ukoli, 1989). 7. Nigeria; Sokoto River (BME). 8. Chad; Lake Léré (Dejoux et al., 1971). 9. Chad; Yebbi Souma (Germain, 1935b) and subfossil sites reviewed by Van Damme (1984). 10. Libya; Tejerhi (Fischer-Piette, 1948), see also Van Damme. 11. Sudan; Bir Natrun (Sandford, 1936). 12. Egypt; Siwa Oasis (Crawford, 1949; Ibrahim, 1975). 13. Sinai (Tchernov, 1971). 14 and 14a. Namibia; Namutoni Spring (Van Bruggen, 1963) and Fish River (Brown et al., 1992). 15. Botswana; Lake Ngami district (Connolly, 1939). 16. Transvaal; ‘far west’ and Johannesburg (Oberholzer & Van Eeden, 1967). 17. E Transvaal and Swaziland lowveld, and eastern Natal (Oberholzer & Van Eeden, 1967; Appleton, 1977c). 18. Natal; Umzimai River (Brown, 1967a). 19. Port Elizabeth (Oberholzer & Van Eeden, 1967). 20. Lake Malawi (Mandahl-Barth, 1972). 21. Lake Kivu (DBL). 22. Lakes Albert and Edward. 23. Sudan; Sudd region (Brown, Fison et al., 1984). 24. Madagascar; widespread (Fischer-Piette & Vukadinovic, 1973). 25. Arabia and Near East; widespread, living and subfossil (Brown & Wright, 1980; Brown & Gallagher, 1985; Burch, 1985).

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Fig. 74. Distribution of Cleopatra. Almost all the range in Africa corresponds to the combined ranges of the two species C. bulimoides and C. ferruginea. One or other of these is recorded, unless indicated otherwise, from the peripheral or isolated localities numbered as follows. 1,2. Senegal and Gambia rivers (Daget, 1961; Malek & Chaine, 1981). 3. Mali; central Niger basin (Daget, 1954; Madsen et al., 1987). 4. Ivory Coast; Mankono (Binder, 1958a). 5. Nigeria; Kainji district (Walsh & Mellink, 1970). 6. Chad; Lake Léré (Dejoux et al., 1971). 7. Sudan; White Nile (Longstaff, 1914; Brown et al., 1984). 8. Egypt; isthmus of Suez (Pallary, 1909). 9. Libya; Tejerhi (Fischer-Piette, 1948; see Van Damme, 1984 for further subfossil sites). 10. Syria (Germain, 1921b; Pallary, 1929). 11. Saudi Arabia; El Sudah (Arfaa, 1976). 12. Yemen; Ta’iz (Ayad, 1956). 13. Sudan; Roseires (Germain, 1918). 14. Ethiopia; Lake Stefanie (BME) and Kenya; Lake Turkana (Cohen, 1986). 15. Ethiopia; Awash basin (BME). 16. Somalia; Agherrar (C. rugosa). 17. Sudan; 2nd Nile cataract (Martin, 1968, modern shells). 18. Zaire; Kisangani (C. langi). 19. Zaire; Kasai Province (C. pilula). 20,21. Angola; Pungo Andongo and Moçamedes district (Wright, 1963a, see C. nsendweensis). 22. Namibia; Omatako River (Connolly, 1939; C. nsendweensis of Brown et al., 1992). 23. Zimbabwe; Chirundu, C. ? elata not Paludomus lesnei (Germain). 24. South Africa; Kruger National Park (Oberholzer & Van Eeden, 1967). 25. South Africa; Tongaland (Brown, 1967a; Appleton, 1977c). 26. Madagascar; widespread endemic species (Fischer-Piette & Vukadinovic, 1973).

Chapter 4. Systematic Synopsis: Pulmonates

Introductory remarks on the higher classification of the African freshwater gastropods are given at the beginning of the first part of this synopsis (Chapter 3). Here we consider the freshwater pulmonates, which often are classified, as in the first edition of this book, in the order Basommatophora (having the eyes situated near the bases of the pair of tentacles, rather than at the ends of the tentacles as in the terrestrial pulmonates). The family Ellobiidae is included here, although these snails are practically restricted to marine and brackish habitats, since some species may be encountered by the freshwater collector working at the coast. As the Basommatophora seems unlikely to be a single evolutionary unit (Hubendick, 1978) and will probably not survive as a group in classification, these snails will be referred to here simply as ‘pulmonates’. All the freshwater pulmonates of Africa lack an operculum. The mantle cavity serves as an air-breathing organ and there is no true gill. However, a secondarilydeveloped respiratory organ, the pseudobranch, is present in the Ancylidae and is particularly well-developed in the Planorbidae. The animal is hermaphrodite, with the lower male and female ducts separate (except in some Ellobiidae); there is a male copulatory organ of varied structure and reproduction is oviparous. The radula has numerous small teeth in each transverse row. Classification in families and subfamilies here follows the first edition of this book. A system that combines the Ancylidae with the Planorbidae (Hubendick, 1978) perhaps reflects phylogeny better, but has not been generally adopted. Family Ellobiidae Small to large, dextral and rarely sinistral (in Blauneria), with lamellae (‘teeth’ or ‘folds’) projecting from the inner margin of the aperture. Pseudobranch lacking. Mostly amphibious, in marine and brackish habitats, especially mangrove swamp. In Africa 4 genera are encountered in coastal habitats where freshwater molluscs may occur nearby. Laemodonta (=Plecotrema) and Pythia also occur on African coasts, but apparently need more saline conditions.

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Genus Auriculastra Martens, 1880 Shell only rarely reaching 15 mm high, slender, tapered above and below (fusiform), nearly smooth; outer lip thin and without teeth; columellar-parietal margin with 2 lamellae. Indo-Pacific range: including the Philippines, N Australia and E Africa. Perhaps only one variable species in Africa. Pilsbry & Bequaert (1927) incorrectly placed in this genus 3 species of Laemodonta from near Massawa (Jickeli, 1874). Type species: Auricula subula Quoy & Gaimard, 1832, New Ireland. Auriculastra radiolata (Morelet, 1860a, Melampus). Type locality: Zanzibar. Fig. 75a. 11×5 mm (about 6 whorls remaining). Shell usually decollate, smooth apart from fine spiral sculpture on upper whorls, almost colourless. Apparently the same species was described later from Natal (Melvill & Ponsonby, 1899, Auricula durbanica and A. catonis), Mozambique (A. acuta Connolly, 1922, 1925a) and Tanzania (Knipper & Meyer, 1956, as A. subula). A slender form, A. nevillei (Morelet, 1882) is reported from Somalia and Mauritius (Connolly, 1928a, p. 150) and the Comoro Islands (Backeljau et al., 1987). HABITAT. Crevices in mud beneath mangrove trees (Brown, 1971). Apparently in association with this subterranean habit, pigment is lacking from the shell and animal apart from the deeply sunken eyes. DISTRIBUTION. E African coast from Somalia to Natal, Zanzibar, Grand Comore and Mauritius (references above). Genus Auriculodes Strand, 1928 Perhaps distinguishable from Auriculastra by the larger and thick-walled shell. Indo-Pacific region. Type species: Auricula gangetica Pfeiffer, 1855. Auriculodes gaziensis (Preston, 1913, Auricula). Type locality: Kenya, Gazi. Fig. 75b. 17.7×7.7 mm (Preston). Aperture with inner lamellae like Auriculastra; upper part of whorls with variable sculpture, sometimes nodular. Paratypes (BMNH) resemble larger shells (up to 24 mm high) from Tanzania (Knipper & Meyer, 1956) and Kenya (Fig. 75b). HABITAT. Mangrove swamp; I found living snails within crevices in the bank of a dry creek near Malindi, Kenya. DISTRIBUTION. Kenya; Gazi and near Malindi. Tanzania; Rufiji estuary (Knipper & Meyer). Genus Blauneria Shuttleworth, 1854 Small (up to about 5 mm high); like a miniature, slender Auriculastra, but sinistral instead of dextral. There is one strong parietal fold and the columella is twisted. Rarely reported, but probably widespread on tropical coasts. B. exsilium

164 SYSTEMATIC SYNOPSIS: PULMONATES

Preston, 1912 is known from Kenya, Gazi and Grand Comore Island (Backeljau et al., 1987). The genus occurs also on Mauritius (Morelet, 1882, p. 103) and in West Africa (Niger Delta; C.B.Powell, 1978, BMNH). Genus Cassidula Férussac, 1821 Shell medium-to-large, with broad conical spire; outer lip with thick internal rib; inner aperture margin with 2 or 3 lamellae. Indo-Pacific; only one species is widespread in Africa. Type species: Bulimus aurisfelis Bruguière, 1789, Bengal. Cassidula labrella (Deshayes, 1830, Auricula). Type locality: Mauritius. Fig. 75c. 12×7.5 mm. Shell coloured reddish-brown; with spiral grooves and sometimes rows of periostracal bristles. HABITAT. Salt marshes and mangrove swamp (Brown, 1971), often with Melampus. DISTRIBUTION. Near Port Elizabeth (Connolly, 1939) and northwards to Massawa and nearby islands (Jickeli, 1874); Grand Comore Island (Backeljau et al., 1987). Cassidula mustelina (Deshayes, 1830). Larger (20 mm high) and pale coloured with spiral bands. Indo-Pacific; found in Africa only near Massawa (Jickeli, 1874, as C. nucleus; Pollonera, 1898). Genus Melampus Montfort, 1810 The larger African species reach about 15 mm high; spire broadly conic; aperture narrow, inner margin with 2–4 lamellae, outer lip often with internal small spiral ridges or tubercles. Circumtropical, in brackish habitats and on more strictly marine shores. Many species and varieties are founded on African shells (Connolly, 1939) and revision is greatly needed. Attention is restricted here to a few species found in brackish water. Type species: Bulimus coniformis Bruguière, 1759. Melampus liberianus H. & A.Adams, 1854. Type locality: Liberia. Fig. 75e. 14×8.3 mm. Shells from Ghana have shallow spiral grooves on the upper and lower parts of the last whorl; the columellar lamella does not reach to aperture margin; about 10 low tubercles within the outer lip; coloured sepia-brown with lighter spiral bands. HABITAT. Abundant under debris in the lower Zaire River near Banana (Pilsbry & Bequaert, 1927); I found specimens on mud beneath mangrove trees at Ada, Ghana. DISTRIBUTION. W Africa from Senegal to the Zaire estuary. Melampus semiaratus Connolly, 1912. Type locality: South Africa, Durban. Fig. 75d. 9.6×5.5 mm. Deep spiral grooves and transverse ridges produce a strong nodular sculpture on the upper part of the whorls; outer lip with only 1 or 2 ridges; coloured uniformly sepia-brown.

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Fig. 75. Ellobiidae. (a) Auriculastra radiolata; South Africa, Durban, (b) Auriculodes gaziensis; Kenya, Gongoni. (c) Cassidula labrella; South Africa; Durban, (d) M. semiaratus; South Africa, Durban, (e) Melampus liberianus; Ghana, Ada. (f) Melampus sp.; Kenya, Kilifi. Scale line: 5 mm.

HABITAT. Mud shaded by mangrove trees (Brown, 1971); living snails found in crevices down to 15 cms.

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DISTRIBUTION. E Africa: Umkomaas River northwards to Giuba River (Connolly, 1928a, 1939); Tanzania (Knipper & Meyer, 1956, as M. semisulcatus Mousson). Grand Comore Island (Backeljau et al., 1987). Melampus spp. One or more other species live in the mangrove swamps of eastern Africa. A small species (Fig. 75f) common in Kenya is nearly smooth, the columellar fold is weak, there are 2–7 ridges within the outer lip, and the colour is usually a uniform purplish-brown. Family Acroloxidae The limpet Acroloxus lacustris (Linnaeus) is stated to occur in Africa (Ellis, 1926; Mienis, 1970), but apparently there are no reliable records. The nearest substantiated localities seem to be in Israel (Mienis, 1970). Family Lymnaeidae Shell small to large, dextral, with pointed spire varying widely in height, thinwalled and fragile. Tentacles flat and triangular (Fig. 12a). Pseudobranch lacking. The two genital openings are situated on the right side. Eggs deposited in an elongated gelatinous capsule. In fresh water worldwide, though with relatively few species in tropical Africa. Hubendick (1951) treated many genera as synonyms of Lymnaea, but it seems justifiable to retain some of these groups, at least as subgenera. Genus Lymnaea Lamarck, 1799 Characters as for the family. Africa has a single widespread species, L. natalensis Krauss, described under many different names. In addition, 3 species widespread in Europe (L. palustris, L. peregra and L. stagnalis) have been found rarely in N Africa, while L. truncatula has an extensive eastern distribution from Egypt to South Africa. L. columella is an introduction of American origin now well-established in southern Africa. Type species: Helix stagnalis Linnaeus, 1758, Europe. Lymnaea (Radix) natalensis Krauss, 1848. Type locality: South Africa, Natal. Figs 76a,b, 79a. 25×14.5 mm. Shell spire generally much less high than the aperture; surface often with spiral rows of short transverse grooves (Fig. 79a), but lacking the spiral ridges characteristic of L. columella. Shape varies widely (Mandahl-Barth, 1954a; Brown, 1965; Pretorius & Van Eeden, 1969; Brown & Gallagher, 1985). The name L. caillaudi Bourguignat, 1883 (Ethiopia, Lake Tana) has often been used for snails from eastern Africa, in the belief that they belonged to a form narrower than typical L. natalensis. But variation in shape appears to be continuous throughout Africa and the number of species falling into the synonymy of L. natalensis is large (Germain, 1920; Pilsbry & Bequaert, 1927;

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Hubendick, 1951). Two extreme forms (Figs 76a,b) were described from Ethiopia, the high-spired L. exserta Martens (1866, Eritrea) and the very depressed L. gravieri Bourguignat (1885a, lower Awash River). Exceptionally slender shells from Arabia are known as L. arabica Smith (1894, Oman) (Brown & Gallagher, 1985). L. natalensis belongs to the L. auricularia ‘superspecies’ of Hubendick (1951), who indicated overlap in Arabia and lower Egypt between the ranges of the African natalensis and the palaearctic auricularia. It still seems uncertain whether or not these species are entirely distinct. There have been further identifications of L. auricularia, according to the large shell aperture, in Saudi Arabia (Brown & Wright, 1980) and Yemen (Al-safadi, 1990); the southern distribution of this species needs to be established by criteria additional to shell characters. L. hovarum Tristram, 1863 of Madagascar has been treated as distinct (Starmühlner, 1969), but seems to be a form of L. natalensis. L. mauritiana Morelet, 1875 of Mauritius, however, appears to be more closely related to the Asian lymnaeids (Hubendick, 1951). HABITAT. L. natalensis is most frequent in permanent streams and impoundments such as small dams; moderate pollution may be favourable (Smith, 1982; Ndifon & Ukoli, 1989). Its abundance in Ghana was much increased by construction of dams (McCullough, 1965b). Found also in very shallow seeping water, but only rarely in seasonal pools (Bitakaramire, 1968). Oxygen requirements are high (Van Someren, 1946). Not particularly tolerant of desiccation (McCullough, 1965b; Cridland, 1967), but capable of surviving drought for several months (Bitakaramire, 1968; Vassiliadès, 1978; Schillhorn van Veen & Usman, 1979). Associations with other snails and water-plants in the Ibadan area were described by Thomas & Tait (1984), and population dynamics in Nigeria by Schillhorn van Veen (1980a). Responses to different temperature regimes (Prinsloo & Van Eeden, 1969, 1973a) suggested that temperature is less important in determining distribution of the snail in South Africa than stable water (De Kock & Van Eeden, 1985; De Kock, 1985). DISTRIBUTION (Fig. 116) In N Africa L. natalensis lives today apparently only in the Nile Basin, but its Late Pleistocene-Holocene distribution was extensive in the present-day Sahara (summarised by Van Damme, 1984). The most northerly living populations in the Sahelian zone (Fig. 116) are known in SW Sudan, Lake Chad, the Niger Basin in Mali (Madsen et al., 1987) and Senegambia (Malek & Chaine, 1981). In the highlands of Ethiopia distribution extends up to about 2440 m (8000 feet) (Brown, 1965). Widespread in tropical Africa, but rare in the north-east coastal area. Probably a combination of low rainfall and cool climate excludes L. natalensis from much of western Cape Province. Found also in Arabia (Brown & Gallagher, 1985; Burch, 1985; Al-safadi, 1990) and Indian Ocean islands: Anjouan (Comores) and Madagascar (Starmühlner, 1983) and Mayotte (Comores; Julvez et al., 1990).

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PARASITES. L. natalensis is the main intermediate host if not the only one in large areas of Africa for Fasciola (e.g. Preston & Castelino, 1977; Schillhorn van Veen, 1980b; see Chapter 6). Loker et al. (1981) reported the prevalences of infections with 6 different trematode species in this snail. Lymnaea (Pseudosuccinea) columella Say, 1817. Type locality North America (apparently near Philadelphia). Figs 76c, 79b. 17×9 mm. Similar in shape to L. natalensis, but usually smaller and more slender, and with characteristic spiral ridges of periostracum (Fig. 79b). HABITAT. Often found with L. natalensis, from which L. columella differs in its habit of crawling out of the water onto vegetation and hard surfaces. DISTRIBUTION (Fig. 150). This American species has been introduced into many areas, including Puerto Rico, Europe (botanical gardens), New Zealand and Africa, where it was found in 1944 on Cape Flats, western Cape Province (Barnard, 1948, in Connolly, 1939). An earlier finding was by J.Omer-Cooper in 1942 near Somerset West (BME). Now widespread in South Africa (Van Eeden & Brown, 1966; De Kock et al., 1974, 1989) and found also in S Mozambique, Zimbabwe, Zambia (Ndola), Kenya (Kitui; Jelnes & Ouma, 1981) and Egypt (DBL, BME). PARASITES. Intermediate host for Fasciola hepatica according to Alicata (1953) and Pullan & Whitten (1972); the introduction of L. columella into South Africa may have increased the prevalence of liver-fluke in livestock (Horak, quoted by Boray, 1974), but recent data apparently are lacking. Lymnaea (Galba) truncatula (Müller, 1774, Buccinum). Type locality: Germany, Thangelstedt in Thuringia (near Weimar). Figs 76d,e. 11×6 mm (often smaller). The smallest African lymnaeid; spire about as high as the aperture, whorls strongly convex; columellar margin straighter and more broadly reflected than in L. natalensis. Copulatory organ described under L. palustris. Synonymous names include L. umlaasiana Küster (1862, Umlaas River, South Africa), L. subtruncatula Boettger (1910, subfossil from Gobabis, Namibia) and L. mweruensis Connolly (1929a, Mweru (Meru) near Mount Kenya). HABITAT. Small streams, seepages and temporary collections of rainwater, particularly in the highlands of Lesotho (Prinsloo & Van Eeden, 1973b, 1974, 1976) and Ethiopia, where snails did not emerge from aestivation until rainfall exceeded 5 mm per day and populations flourished for only about 40 days (Goll & Scott, 1978, 1979). DISTRIBUTION (Fig. 117). The range is mainly holarctic; the extensive though scattered distribution in Africa was attributed by Hubendick (1951) to migratory birds, but it could be long-established as subfossil shells occur in the Sahara (Fig. 117, and Van Damme, 1984). Found alive in Morocco, Algeria and Egypt, and the highlands of Ethiopia, Kenya, E Zaire and SE Tanzania; the most extensive areas of distribution are in the cooler climatic areas of South Africa and Lesotho. Subfossil shells known from 2 localities in Namibia (Fig. 117). Present also in the Near East and SW Arabia (Brown & Wright, 1980). The

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Fig. 76. Lymnaea. (a) L. natalensis; Ethiopia, Jimma. (b) L. natalensis; Ethiopia, lower Awash valley, Assaita (corresponding to L. gravieri Bourguignat). (c) L. columella; South Africa, near Worcester, (d) L. truncatula; Ethiopia, Ambo. (e) L. truncatula; Ethiopia, Debra Berhan. Scale line: 5 mm.

isolated locality reported for Cameroon (Hubendick, 1951, Fig. 307) might have been introduced in error (Hubendick in litt. to Brown, 1977). PARASITES. L. truncatula is well-known as the intermediate host for Fasciola hepatica in Europe. In Africa it is of major importance in transmitting fascioliasis of livestock in Lesotho (Prinsloo & Van Eeden, 1973b) and Ethiopia (Goll & Scott, 1979) (see Chapter 6). The following species are widely distributed in Europe and occur in restricted areas of North Africa. Lymnaea (Lymnaea) stagnalis (Linnaeus). Fig. 77a. 45×25 mm. A large species with a slender and sharply pointed spire. Its extensive range (Hubendick,

170 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 77. Lymnaea of North Africa, (a) L. stagnalis; Morocco, Tangier, (b) L. peregra; Morocco, Ifrane. (c) L. palustris; Morocco, Mago. (d) L. palustris; Algiers. Scale line 6 mm (b–d) or 12 mm (a).

1951) includes N America, Europe, much of Asia, Algeria and Morocco (Khedire and Larache, DBL) and Egypt (Wadi Natroun, DBL). Lymnaea (Stagnicola) palustris (Müller). Figs 77c,d. 16×8 mm. Usually larger and with less convex whorls than L. truncatula; small areas of shell surface are flattened (malleated). Penis sheath about as long as the preputium, whereas it is much shorter in L. truncatula. Shell highly variable, sometimes resembling the extremely slender L. glabra (Müller), but this seems to reach its southern limit in Spain (Sanchez, 1965). Hubendick (1951, p. 148) mentioned L. glabra in the British Museum (Natural History) from the Tangier area of Algeria, but these specimens (apparently shells registered in 1933 and 1937, labelled ‘Mago at 3,600 feet’, Fig. 77c) appear to me to be L. palustris.

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This snail occurs in Europe and much of Asia, and Saudi Arabia (Brown & Wright, 1980). Still found alive in Morocco in the 1970s (Van Damme, 1984); subfossil shells further south in NW Africa and possibly Egypt (Van Damme, 1984). Contrary to Fig. 35 of Van Damme, which is in fact a distribution map for L. truncatula, L. palustris does not seem to have lived in Egypt in recent years. Reported as introduced into a reservoir at Matadi, Zaire (Dartevelle, 1952b); the single shell (Muséum Royale Africaine Centrale, Tervuren, No. 302783) does appear to be this species. Other snails somewhat similar to L. palustris have been obtained recently in NE Zaire near Djugu (DBL; Lymnaea sp. of Chartier et al., 1992). Lymnaea (Radix) peregra (Müller). Fig. 77b. 14×8 mm (reaching over 20 mm high). Shell highly variable; animal can be reliably separated from L. auricularia and L. natalensis by its shorter spermathecal duct (Hubendick, 1951). This is the commonest lymnaeid in Europe; found also in Algeria and Morocco (Van Damme, 1984), but an early report for Ethiopia (Jickeli, 1874, pl. 7) was based on what apparently is L. truncatula. Genus Lantzia Jousseaume, 1872 Shell small (about 6 mm wide), depressed, neritiform and apparently adapted for clinging to rocks. Until recently known from only the original description of L. carinata Jousseaume, 1872 collected on Réunion (Bourbon) Island between 1200 and 1300 m ‘in mosses’. Re-discovered in 1992 by O.Griffiths in a waterfall at or near the type locality. These specimens (BMNH) have flat, triangular lymnaeid-like tentacles as described by Jousseaume. This remarkable neritiform lymnaeid seems likely to have evolved independently of the one that inhabits waterfalls in Hawaii (Erinna; Burch, 1968). Family Ancylidae Freshwater limpets, shell usually less than 10 mm long in Africa, cap-like with the apex obtuse or hooked. Pseudobranch and genital openings on the left side. Eggs arranged spirally in circular dehiscent capsules, with a characteristic outer membrane in at least some genera (Bondesen, 1950). Probably a number of distantly-related stocks have converged in shell form (Hubendick, 1964, 1978). Worldwide distribution in fresh waters of all kinds: the 3 genera found in Africa are Ancylus (mainly palaearctic), Burnupia (Africa only) and Ferrissia (cosmopolitan). Shell measurements given are length (greatest dimension of base), width and, lastly, height. Genus Ancylus Müller, 1774 Comparatively large, may reach 12 mm long; apex (Fig. 79) with coarse radial ridges. Anus situated anteriorly on the folded pseudobranch. Copulatory organ

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with a flagellum. Usually in streams: W Palaearctic region, Canary Islands, Madeira, NW Africa, Ethiopia, SW Arabia. Type species: Ancylus fluviatilis Müller, 1774, Germany. Ancylus fluviatilis Müller, 1774. Type locality: Germany, Ilm River, near Thangelstadt (near Weimar). Fig. 78a. 8×6.6×2 mm (broad form). Basal outline varying from a narrow oval to almost a circle; apex more or less hooked and sometimes overhanging the posterior margin; coarse radial ridges run from the apex (Fig. 79c) to the base. The shell varies widely; two species described from Ethiopia by Jickeli (1874, A. abyssinicus and A. compressus) appear to be synonyms (Brown, 1965). Hubendick (1970) listed a total of 110 synonymous species-names and commented on particularly high variability in NW Africa. However, genetic differences play a part in determining variation of the shell in Britain (Sutcliff & Durrant, 1977), and two or more species may be confused in Africa, as ‘EurasianNorth African’ populations have the high chromosome number n=60, while ‘a species in Ethiopia’ has n=30 (Patterson & Burch, 1978, p. 201). Analysis of this interesting situation is complicated by varied modes of reproduction, perhaps including parthenogenesis (Städler et al., 1992). HABITAT. Common on stones in small streams flowing through grassland on the Ethiopian plateau (Brown, 1965). DISTRIBUTION. Range as for the genus. NW Africa: coastal zone from Morocco to Tunis (Hubendick, 1970); isolated relict populations living in gueltas (streams) in SE Algeria were found in 1961 by J.A.Rioux (MNHN) in the Hoggar (Ahaggar) and in 1978 by H.Dumont in the Tassili N’Ajjar (Van Damme, 1984). Ethiopia: central and N plateau above 2240 m (Brown, 1965, 1973). SW Arabia: streams at high altitude in Yemen Arab Republic (Connolly, 1941, Pseudancylus abyssinicus; Al-safadi, 1990) and South Yemen (P. argenteus Connolly, 1941; Wright, 1963b); western Saudi Arabia (Brown & Wright, 1980). Ancylus regularis Brown, 1973 (1965, Ancylus sp.). Type locality: Ethiopia, Wallaga Province, small stony stream 12 km W of Sire on road to Lekemti. Figs 78b, 79d. 7.3×5.8×3.0 mm. Distinguished from A. fluviatilis by the uniformly broad basal outline and the symmetrical obtuse apex, situated near the middle of the shell and having finer radial ridges (Fig. 79d). HABITAT. Small stony streams flowing through partially cleared forest; upper altitudinal limit of 2130 m, slightly below the lower limit for A. fluviatilis. DISTRIBUTION. SW Ethiopia: common in the districts of Jimma and Lekemti, found also near Dilla and in an eastern tributary of Lake Langano. Ancylus ashangiensis Brown, 1965. Type locality: Ethiopia, Wallo province, E shore of Lake Ashangi. 4.8×2.3×2.2 mm. Small, with very narrow base and sharply pointed apex. Animal unknown. HABITAT and DISTRIBUTION. Their shape suggests that the shells grew upon slender plant-stems. Known only from Lake Ashangi in Ethiopia.

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Fig. 78. Ancylidae. (a) Ancylus fluviatilis; Ethiopia, Debra Berhan. (b) A. regularise Ethiopia, Sire, (c) Burnupia caffra; South Africa, Greytown. (d) B. gordonensis; South Africa (syntype, BMNH1904.4.29.40). Scale line: 5 mm.

‘Ancylus’ turtoni Connolly, 1939, from Port Alfred, does not belong to the freshwater fauna. Two paratypes (BMNH) have the apex distinctly coiled

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(Fig. 80a) and one has a trace of an orange radial band; probably they belong to the marine family Siphonariidae (Brown, 1980b, p. 220; see also Brondelia, below). Genus Brondelia Bourguignat, 1862 Shell broadly oval, about 7.5 mm long, apex turned to the left and coiled. Said in the original description to have been collected from steep humid rocks in the Edough Forest near Bône in Algeria. Hubendick (1970) examined the original shells and commented that the reddish rays visible on some resembled those of the marine genus Williamia (Siphonariidae). This identification was confirmed by Rehder (1984). Type species (by designation of Rehder, 1984): Ancylus drouetianus Bourguignat, 1853. Genus Burnupia Walker, 1912 Shell reaching 10 mm long, apex usually prominent, turned to the right and with radial rows of small pits (Fig. 79e). Anus situated posteriorly on the pseudobranch, which is divided into upper and lower lamellae. Copulatory organ without a flagellum (Oberholzer & Van Eeden, 1969). In well-oxygenated water, especially on stones in streams and at lake edges. Found only in Africa (Fig. 118): highlands of Ethiopia and East Africa, southwards into Zaire, Angola and Zimbabwe, widespread in South Africa. Subfossil shells found in now arid parts of Botswana and Namibia; isolated living population in the Naukluftberge (see B. caffra). Number of species highly uncertain; many founded on shell differences but probably only few are really distinct, for shell shape seems to be affected by current speed and type of substratum. To understand speciation within this group as well as Ancylus it is necessary to investigate the genetic basis of variation among populations and taxa. Pending such revision, species recognised by authorities (principally Walker, 1924, 1926; Pilsbry & Bequaert, 1927; MandahlBarth, 1968a) are listed below, grouped according to geographical region, though details are given for only those with outstanding characteristics or of special taxonomic importance. Type species: Ancylus caffer Krauss, 1848, South Africa. 1) Species described from southern Africa

These commence with the earliest to be described, followed by others in alphabetical order. Burnupia caffra (Krauss, 1848, Ancylus). Type locality: South Africa, Pietermaritzburg, from leaves of plants in mountain streams. Fig. 78c. 5.4×3.8×2.3 mm (type according to Walker, 1924). Krauss described the basal outline as oval and the apex as prominent, so far inclined to the right to reach the basal margin when viewed from above. Some internal organs described from

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Fig. 79. Lymnaeidae and Ancylidae: shell surfaces (scanning electronmicrographs). (a) Lymnaea natalensis; sculpture only of transverse grooves, (b) L. columella; sculpture of spiral ridges of periostracum. (c) Ancylus fluviatilis; apex of shell 5.3 mm long, (d) A. regularise; apex of shell 5.5 mm long, (e) Burnupia sp.; apex of shell 4 mm long, (f) Ferrissia sp.; apex of shell 2.5 mm long. Scale lines: 0.1 mm.

Ethiopian animals by Brown (1961, 1965). B. gaulus (Gould, 1859, Cape of Good Hope) was treated as a synonym by Walker (1924); this taxon is predated otherwise only by B. verreauxi (see below). A number of other named species probably are indistinguishable from B. caffra.

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Fig. 80. Ancylidae. (a) ‘Ancylus’ turtoni; South Africa, Port Alfred (paratype, BMNH1937.12.30.2304–5); apparently a marine siphonariid. (b) Burnupia capensis; South Africa (paratype, BMNH1937.12.30.2317–28). (c) B. farquhari; South Africa (paratype, BMNH1937.12.30.2375–77). (d) B. nana; South Africa (paratype, BMNH1937.12.30.2399–403). Scale line: 2 mm.

HABITAT. Usually found on stones or vegetation in streams. Obtained alive from 70–100 m depth in Lake Tanganyika (Leloup, 1953). DISTRIBUTION. B. caffra probably occupies much of the range known for the genus (Fig. 118). In the Naukluftberge of Namibia an isolated living

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population was found in 1982 by S.Bethune (State Museum, Windhoek, No. 75941). Burnupia brunnea Walker, 1924. Type locality; South Africa, Transvaal, Zoutpansberg. Burnupia capensis (Walker, 1912, Ancylus caffer var. capensis). Type locality: South Africa, Cape Peninsula, Lakeside. Fig. 80b. 7.5×4.5×2.5 mm. Paratypes (BMNH) have strong radial ridges and the apex is more obtuse than in Walker’s figure (1924). Pilsbry (1932) described subspecies B. c. striatissima from Lesotho (Basutoland). Burnupia farquhari (Walker, 1912, A. caffer var. farquhari). Type locality: South Africa, NE Cape, York. Fig. 80c. Burnupia gordonensis (Melvill & Ponsonby, 1903, Ancylus), Type locality: South Africa, Natal, Gordon Falls. Fig. 78d. 6×5×3 mm (holotype); reaching 10 mm (Walker, 1924). Broad, with apex turned less to the right than B. caffra. Burnupia mooiensis (Walker, 1912, Ancylus). Type locality: South Africa, W Transvaal, Mooi River at Potchefstroom. 6.3×4×2.5 mm (Walker, 1924). Oberholzer & Van Eeden (1969) give a detailed account of anatomy and histology for specimens from near the type locality. Burnupia nana (Walker, 1912, Ancylus caffer var. nana). Type locality: South Africa, Natal, Karkloof stream. Fig. 80d. Burnupia obtusata Walker, 1926. Type locality: South Africa, Natal, Pietermaritzburg, Bishopstowe Road. Fig. 82a. Burnupia ponsonbyi Walker, 1924. Type locality: South Africa, Natal, Umgeni River. Fig. 81a. 6.8×5.5×2.5 mm (holotype). Basal outline exceptionally broad; apex obtuse and nearly central. Burnupia stenochorias (Melvill & Ponsonby, 1903, Ancylus). Type locality: South Africa, E Cape, Port Elizabeth, Ebb en Floed. Fig. 81b. 8×4.5×3 mm (Melvill & Ponsonby). The narrow shape suggests that this limpet grew upon a slender plant stem. Burnupia transvaalensis (Craven, 1880c, Ancylus). Type locality: South Africa, Transvaal, Mooi River. Fig. 81c. 7.5×5.3×3.2 mm. A high shell with an obtuse and central apex. Burnupia trapezoidea (Boettger, 1910, Ancylus). Type locality: Botswana, subfossil at Witkop. Fig. 82d. 3.8×2.3×2 mm. Records given by Connolly (1939) include Great Namaqualand and Kamanyab in Namibia, and Ngamiland in Botswana. Burnupia verreauxi (Bourguignat, 1853; 1854, Ancylus). Type locality: South Africa, Cape of Good Hope, Constance. This is perhaps only a smooth form of B. caffra, to which it is next in seniority among the named species of this genus.

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Fig. 81. Ancylidae: Burnupia. (a) B. ponsonbyi; South Africa, Howick Falls, (b) B. stenochorias; South Africa (syntype, BMNH1937.12.30.2409–14). (c) B. transvaalensis; South Africa (syntype, BMNH1891.3.7.19–22). (d) B. crassistriata; Kenya (syntype, BMNH1937.12.30.2290–98). (e,e′) B. stuhlmanni; Kenya, Lake Victoria, Kisumu. Scale line: 5 mm.

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Burnupia vulcanus Walker, 1924. Type locality: South Africa, W Transvaal, Mooi River at Potchefstroom. Possibly a synonym of B. mooiensis. 2) Species described from SE Zaire. In this region Burnupia is probably more abundant than shown by records (Pilsbry & Bequaert, 1927; Mandahl-Barth, 1968a; Mandahl-Barth et al., 1972). Perhaps all the species described by Pilsbry & Bequaert are synonyms of one or other species named earlier from South African shells.

Burnupia alta Pilsbry & Bequaert, 1927. Type locality: SE Zaire, Kisanga River near Lubumbashi (Elizabethville). Fig. 82c. Burnupia kimiloloensis Pilsbry & Bequaert, 1927. Type locality: SE Zaire, Kimilolo River near Lubumbashi (Elizabetheville). Upper Luapula Region (Mandahl-Barth, 1968a). Burnupia walkeri Pilsbry & Bequaert, 1927. Type locality: SE Zaire, Lualaba River at Kalangwe. 3) Species described from East Africa

Burnupia crassistriata (Preston, 1911, Ancylus). Type locality: Kenya, between Rumuruti and Mount Kenya. Fig. 81d. 4.5×3×2 mm (Preston). A high shell was figured by both Preston and Mandahl-Barth (1954), but some syntypes (BMNH) are much lower (Fig. 81d). HABITAT AND DISTRIBUTION. Kenya: stony streams in the highlands, including the Mau, Aberdare and Mount Kenya massifs. Burnupia edwardiana Pilsbry & Bequaert, 1927. Type locality: Zaire, Lake Edward at Kabare. Burnupia kempi (Preston, 1912a, Ancylus). Type locality: SW Uganda, Kigezi at an altitude of 1830 m (6000 feet). Fig. 82b. 4.3×3.3×1.3 mm (Preston); syntypes (BMNH) are more depressed with a small though prominent apex. Reported distribution from Ethiopia to northern Tanzania and Lake Kivu (Kristensen, 1987). Burnupia stuhlmanni (Martens, 1897, Ancylus). Type locality: Lake Victoria at Busisi. Fig. 81e. 2.3×1.5×0.9 mm (Martens); 5.8×4.7×1.8 mm (shell from Kisumu). I follow Mandahl-Barth (1954) in using this name for a Burnupia with a broad base and low profile. The small shell illustrated by Martens could be a Ferrissia. HABITAT AND DISTRIBUTION. Lake Victoria and Victoria Nile (Mandahl-Barth); found by myself commonly on stones at Kisumu. Genus Ferrissia Walker, 1903 Small, rarely reaching 5 mm long, with very fine radial ridges on the apex (Fig. 79f), which is obtuse and never hooked as it may be in Burnupia and Ancylus. A septum partly closing the shell may be formed in association with aestivation through a dry season. When once again active the animal may

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Fig. 82. Ancylidae: Burnupia. (a) B. obtusata; South Africa (holotype, after Walker, 1926, Pl. 1). (b) B. kempi; Uganda (syntype, BMNH1937.12.30.2300–03). (c) B. alta; SE Zaire (holotype, after Pilsbry & Bequaert, 1927, Pl. 12,5). (d) B. trapezoidea; Botswana (holotype, after Boettger, 1910, Fig. 15). Scale lines: 2 mm.

continue growing, producing a curious double shell (Figs 85a,d). Copulatory organ with a flagellum (Brown, 1967b); aphallic individuals are frequent. In varied habitats including streams, lakes, seasonal pools and irrigation channels; often attached to vegetation, especially the underside of lily-leaves. Widespread in the tropical region and probably present throughout Africa, though overlooked because so small (it has been realised only within the last fifty years that the genus is widespread in W Europe). The species of Africa, Asia, Australia and Oceania were placed by Hubendick (1964) with F. wautieri (Mirolli, 1960) of Europe in the subgenus F. pettancylus, having a characteristic structure of the copulatory organ (Brown, 1967b). African

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species with a septate shell have been placed in Gundlachia, but this genus is restricted to the Neotropical Region (Hubendick, 1964). The occasional formation of a septum in Africa seems to have no taxonomic significance. Number of species highly uncertain; many founded on shell differences but probably few are really distinct, for shell shape seems to be related to current speed and type of substratum. As for the other ancylid genera in Africa, genetic investigation is needed for understanding of the true species. Species recognised by authorities (principally Walker, 1924, 1926; Hubendick, 1970) are listed below, grouped according to four geographical regions. Details are given only for those with outstanding characteristics or of special taxonomic importance. Type species: Ancylus regularis Say, 1817, North America. The intermediate host for a small focus of Schistosoma haematobium in W India was claimed to be Ferrissia tenuis (Bourguignat) by Gadgil & Shah (1955), but this is not yet confirmed (Southgate & Agrawal, 1990) and there is no evidence to connect any species of these limpets with transmission of schistosomes in Africa. 1) Species described from North Africa. Egyptian forms were redescribed by Hubendick (1970); probably some species described from tropical Africa will fall within their synonymies.

Ferrissia isseli (Bourguignat, 1866, Ancylus). Type locality: Egypt, Rambe (? Ramleh) district near Alexandria. 3×1.7×1.5 mm (Bourguignat); 3.7×2.4×1.5 mm (Hubendick). Brown (1965) and Hubendick (1970) followed Walker (1914) in regarding this as a comparatively high shell. DISTRIBUTION. Egypt, Ethiopia (Brown, 1965) and perhaps Sudan (Brown, Fison et al., 1984, Ferrissia sp.). Ferrissia clessiniana (Jickeli, 1882, Ancylus). Type locality: Egypt, Alexandria. 4.5×2.5×1.5 mm (Jickeli). Regarded by Walker (1914) as more depressed and longer than F. isseli. Hubendick (1970) included F. wautieri (Mirolli) of Italy amongst possible synonyms. Reported also from Ethiopia (Brown, 1965). Ferrissia l’hotelleriei (Walker, 1914, Gundlachia). Type locality: Egypt, Alexandria. Ferrissia pallaryi Walker, 1914. Type locality: Egypt, Alexandria, Mahmoudich Canal. (?)Ferrissia platyrhynchus Walker, 1914. Type locality: Algeria, Baraki near ‘le Gué de Constantine’. 3.8×2.3×1.3 mm. Described from a single shell, with a hooked apex, appearing from the illustration to be a juvenile Ancylus fluviatilis. Shells of Ferrissia from Libya, Tripoli, collected in 1988 (C.Woods; BME) seem to be the only examples of this genus yet known from North Africa west of Egypt. 2) Species described from eastern Africa

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Fig. 83. Ancylidae: Ferrissia. (a) F. kavirondica; Kenya, Lake Victoria, Kisumu (after Mandahl-Barth, 1954a, Fig. 59c). (b) F. toroensis; Uganda, Fort Portal (after MandahlBarth, 1954a, Fig. 59a). (c) (?)Ferrissia ruandensis; Ruanda (syntype, after Thiele, 1911, Pl. 5, 48). (d) (?)F. vicinus; Ruanda (syntype, after Thiele, 1911, Pl. 5, 49). Scale lines: 2 mm.

Ferrissia kavirondica Mandahl-Barth, 1954. Type locality: Kenya, Winam (Kavirondo) Gulf near Kisumu. Fig. 83a. 2.6×1.5×0.6 mm. Small, with very weak radial ridges on apex. Hardly distinguishable from the range of variation seen in Ferrissia from small waterbodies in Kenya. HABITAT AND DISTRIBUTION. Lake Victoria, Winam Gulf and small pond nearby (Mandahl-Barth); found by myself on stones at the water’s edge in company with Burnupia. Ferrissia toroensis Mandahl-Barth, 1954. Type locality: Uganda, the most westerly of two crater lakes south of Fort Portal. Fig. 83b. (?)Ferrissia ruandensis (Thiele, 1911, Ancylus). Type locality: Ruanda, Lake Luhondo. Fig. 83c. 6.5×4.5×1.8 mm. Large for this genus; depressed and described as having indistinct radial ridges; the generic position needs confirmation. (?)Ferrissia vicinus (Thiele, 1911, Ancylus). Type locality: Ruanda, waterfalls between lakes Bolero and Luhondo. Fig. 83d. 4.3×3×1.8 mm. Less depressed than the foregoing species and with stronger sculpture; generic position needs confirmation.

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Fig. 84. Ancylidae: Ferrissia. (a) F. tanganyicensis; Lake Tanganyika (syntype, BMNH1904.4.6.12–16). (b) F. leonensis; Sierra Leone (syntype, BMNH1937.12.30.2540– 45). (c) F. burnupi; South Africa (paratype, BMNH1937.12.30.2464–5). (d) F. junodi; Mozambique (syntype, BMNH1937.12.30.2516–17). Scale line: 1 mm.

Ferrissia tanganyicensis (Smith, 1906, Ancylus). Type locality: southern Lake Tanganyika at Niamkolo, on a stone dredged from a few fathoms depth. Fig. 84a. 3.4×2.6×1.4 mm (Leloup, 1953). A distinctive form, low and broad with an obtuse apex and strong radial ridges cut by concentric grooves. This is the most senior species described from Africa south of the Sahara. HABITAT AND DISTRIBUTION. Lake Tanganyika: Leloup (1953) gave only the Malagarasi Delta as a definite locality for the living limpet; also Mpulungu, from a rock outcrop at 1–9 m depth (R.Bills, 1992; BME). 3) Species described from West Africa

Ferrissia chudeaui Germain, 1917. Type locality: Bakoy River at Tukoto (SW Mali). 2.5×1.5×1.3 mm. Very small, with a high prominent apex. Ferrissia leonensis Connolly, 1928b. Type locality: Sierra Leone, Regent. Fig. 84b. Ferrissia eburnensis Binder, 1957. Type locality; Ivory Coast, Bingerville. 3.4×2.4×0.9 mm (Binder, Fig. 21b). More depressed than the two preceding species.

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DISTRIBUTION. Ivory Coast, Lake Chad (Brown, 1974), São Tomé Island (Brown, 1991). 4) Species described from southern Africa and Madagascar

Ferrissia burnupi (Walker, 1912, Ancylus). Type locality: South Africa, Natal, Equeefa River. Fig. 84c. 4×2.2×1 mm. Elongate and depressed; anatomy and radula of specimens from near the type locality described by Brown (1967b). Considerable interest attaches to the range of variation, for this species is the most senior of those described from South Africa. Gundlachia equeefensis Walker (1924) has the same type locality and probably is the septate form of F. burnupi. Ferrissia cawstoni Walker, 1924. Type locality: South Africa, Mooi River at Potchefstroom. Ferrissia clifdeni Connolly, 1939 (new name for Gundlachia burnupi Walker, 1926). Type locality: South Africa, Natal, Umtwalumi near Port Shepstone. Fig. 85a. Ferrissia connollyi (Walker, 1912, Ancylus). Type locality: South Africa, W Cape, Black River at Maitland. Fig. 85c. Ferrissia farquhari (Walker, 1924, Gundlachia). Type locality: South Africa, E Cape, Brack Kloof River near Grahamstown. Fig. 85d. Ferrissia fontinalis (Walker, 1912, Ancylus). Type locality: South Africa, Transvaal, Pretoria district, Ranjesfontein. Fig. 85b. Ferrissia junodi Connolly, 1925a. Type locality: Mozambique, Nwambukoto Pool near Rikatla (near Lourenço Marques). Fig. 84d. Ferrissia lacustris Walker, 1924. Type locality: South Africa, E Transvaal, Lake Chrissie. Ferrissia modesta (Crosse, 1880, 1881, Ancylus). Type locality: Madagascar, Nossi Bé Island, Pasandava Stream. 3×2×1 mm. Starmühlner (1969) described some internal organs. Septate specimens found near Tananarive (Richard-Vindard & Badarelli, 1969). DISTRIBUTION. Madagascar: central highlands, Lake Alaotra and Nossi Bé island (Starmühlner, 1969; Fischer-Piette & Vukadinovic, 1973). Ferrissia natalensis Walker, 1924. Type locality: South Africa, Natal, South Coast Junction. Ferrissia victoriensis (Walker, 1912, Ancylus). Type locality: Zimbabwe, Zambezi River near Victoria falls. Fig. 85e. Ferrissia zambesiensis (Walker, 1912, Ancylus). Type locality: Zimbabwe, Zambezi River near Victoria falls. Fig. 85f. Ferrissia zambiensis Mandahl-Barth, 1968a. Type locality: Zambia, Middle Luapula region, Lweba Stream near Matanda. 3.4×2.4×1 mm. Depressed with broadly oval base.

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Fig. 85. Ancylidae: Ferrissia. (a,a′) F. clifdeni; South Africa (holotype and septate paratype after Walker, 1926, Figs 3,4). (b) F. fontinalis; South Africa (paratype, BMNH1937.12.30.2509– 15). (c) F. connollyi; South Africa (paratype, BMNH1937.12. 30.2503–8). (d) F. farquhari; South Africa (holotype after Walker, 1924, Pl. 2, Fig. 30). (e) F. victoriensis; Zambezi River above Victoria Falls (paratype, BMNH1937.12.30. 2526–9). (f) F. zambesiensis; Zambezi River above Victoria Falls (paratype, BMNH1937. 12.30.2530). Scale line: 1.5 mm (a,d) or 2 mm (b,c,e,f).

Family Planorbidae Small to medium-sized snails with long slender tentacles and reddish blood containing haemaglobin. Shell and anatomy are diverse, especially the male copulatory organ and prostate gland. The use of subfamilies here follows Hubendick (1955) as in the first edition of this book; the later classification proposed by Hubendick (1978) places more emphasis on the structures of ovotestis and prostate, and transfers some groups from the Planorbinae to the Bulininae.

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The animals of all planorbid snails are sinistral, coiled to the left in an anticlockwise direction, with the openings of the reproductive organs on the left side. Accordingly the shell is sinistral in the proper morphological sense, but shells of discoidal forms are commonly described and figured, as by MandahlBarth (1957a) and here, as if they were dextral. Consequently the terms ‘underside’ and ‘umbilicus’ used here (Figs 11c,g) refer to what is the morphological upper side. The reverse and strictly correct orientation is employed by some authors (e.g. Meier-Brook, 1983; Burch, 1985). Subfamily Planorbinae Shell usually discoid, with internal septa in some groups, and only rarely with a pointed spire (e.g. Amerianna). The pseudobranch is a simple lobe, sometimes with a ridge. One or more prostatic tubules open either directly into the sperm duct or into a separate prostatic duct. Copulatory organ of varied construction, though not with the ‘ultrapenis’ of the Bulininae. The tip of the penis may be unarmoured, partly sclerotised, or have a cuticular stylet. Normally a spermathecal sac is attached to the lower part of the uterus by a slender duct. Egg capsule nearly circular in outline, with spirally arranged eggs. Radula with 2 cusps on the central tooth and 3 major cusps on the inner lateral teeth. Genera are arranged here in tribes as in the first edition of this book following Hubendick (1955), but some rearrangements may be necessary when evolutionary relationships are better understood (Hubendick, 1978). Amerianna tribe. Shell with a spire. Penis freely pendant, lacking stylet; numerous prostatic tubules arise in a bunch. Genus Amerianna Strand, 1928 Shell similar to some species of Bulinus. Morphology and taxonomy revised by J.C.Walker (1988). Australasian Region and introduced into West Africa. Type species: Physa (Ameria) carinata H.Adams, 1861, Australia. Amerianna carinata (H.Adams, 1861, Physa). Type locality: Australia, Queensland, Boyne River. Figs 85Aa; 102. 7.3×5.2 mm (large Nigerian shell). Shell resembles Bulinus truncatus, but differs in having a carinate shoulder, numerous spiral ridges and a non-punctate protoconch (Fig. 102). Chromosome number, 2n=36 (Jelnes, 1983a). HABITAT AND DISTRIBUTION. In Africa found only in Nigeria; Ibadan, man-made lakes in several localities, including the Botanical Garden (Brown, 1983; Jelnes, 1983a). PARASITES. Not known to be a host for any schistosome parasite of man or livestock.

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Fig. 85A. Planorbidae. (a) Amerianna carinata with (b) Bulinus truncatus for comparison; both from Nigeria (from Brown, 1983, Fig. 1).

Genus Planorbis Geoffroy, 1767 Shell up to 20 mm diameter, with bluntly angular or carinate whorls. Penis sheath short and slender; penis lacking sclerotisation or stylet. N and W Asia, Europe and N Africa. Type species: Helix planorbis Linnaeus, 1758, Europe. Planorbis planorbis (Linnaeus, 1758, Helix). Type locality: Europe, in ponds. Fig. 87a. 2.5×12 mm (large Egyptian shell). Shell usually with a basal carina, but small and only bluntly angular forms occur, e.g. P. philippi de Monterosato and P. planorbis parenzani Bacci, 1940 (subfossil, from Ethiopia). DISTRIBUTION. Europe, SW Asia, Near East (Tchernov, 1975b; Burch, 1985) and N Africa. Morocco and Algeria (Bourguignat, 1864, including P. complanatus and P. subangulatus) southwards to El Golea (DBL). Egypt: delta and Siwa Oasis (Crawford, 1949). Late Pleistocene-Holocene distribution (Van Damme, 1984) extended into Sudan (Martin, 1968) and S Ethiopia (Bacci, 1940; Brown, 1965). Genus Afrogyrus Brown & Mandahl-Barth, 1973 Small, only rarely reaching 5 mm diameter, with slowly increasing whorls. Penis with subterminal opening and a small (less than 10 µm long) cap-like cuticular stylet (Fig. 14c). Most common in streams, small pools and marshes. Africa, Madagascar, Comoro Islands and Rodrigues. Two subgenera were proposed (Brown & Mandahl-Barth, 1973), A. (Afrogyrus) for the small species found in Africa and A. (Hovorbis) for the larger species of Madagascar, which differs anatomically in having fewer prostatic lobes and in lacking a spermatheca. But absence of the spermatheca may be less significant than thought, for it is lacking also in one species of the genus Drepanotrema of the neotropics (Paraense, 1976). Type species: Planorbis coretus de Blainville, 1826, Senegal.

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Fig. 86. Planorbidae: Afrogyrus. (a–c) A. coretus: (a) Ethiopia, Lake Zwai; (b) Angola, Lagoa Panguila, corresponding to A. misellus (Morelet); (c) Egypt, Dakhla Oasis, A. oasiensis (Demian). (d) A. rodriguezensis; Rodriguez Island, St Gabriel. Scale line: 2 mm.

Afrogyrus coretus (de Blainville, 1826, Planorbis coretus for ‘Le Coret’ of Adanson, 1757). Type locality: Senegal, Podor. Figs 86a–c. 0.7×2.5 (small form) to 1.2×5 mm (A. misellus). A fully-grown shell has about 4 whorls, which is about a half-whorl more than a young Ceratophallus natalensis of similar diameter, whose penis is clearly different with its opening at the tip instead of subterminal. Adanson’s ‘Le Coret’ (Dautzenberg, 1890; Fischer-Piette, 1942) belongs to a widespread species that varies considerably in size and shape of the whorls. Although reported under the genera Planorbis, Anisus and Gyraulus, the distinctive structure of the penis was early observed in snails from Ivory Coast (Binder, 1958b), Egypt (Demian, 1962), Angola (Wright, 1963a), Cameroon (Wright, 1965) and Ethiopia (Brown, 1967c). Apparently synonyms, all species of known penial structure, are Planorbis misellus Morelet (1868, Angola; Wright, 1963a, Anisus) (Fig. 86b), Anisus oasiensis Demian (1962, Egypt, Dakhla Oasis) (Fig. 86c) and Planorbis anderssoni Ancey (1890, Ovamboland, Namibia; Brown & Curtis, 1992).

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Probable synonyms based on West African specimens, though the penis is not known for all, are P. chudeaui Germain, 1907 and P. tilhoi Germain, 1911, both of Lake Chad (Brown, 1974), P. fouladougouensis Germain, 1917 and P. toukotoensis Germain, 1917, both from the Bakoy River in Mali, P. dalloni Germain, 1935b, from Brak in Libya (Ranson & Cherbonnier, 1953) and Gyraulus gibbonsi (Nelson) of Binder (1958b) from Ivory Coast. HABITAT. Permanent waters with rich aquatic vegetation; snails commonly found on the underside of floating lily-leaves and amongst leaf litter on the bottom. Habitats in Ibadan described by Thomas & Tait (1984); abundant in small spring-pools in Namibia (Brown & Curtis, 1992). DISTRIBUTION. Widespread in Africa. Recently-living populations in Libya (Ranson & Cherbonnier, 1953; P. dalloni), Egypt (Demian, 1962; Anisus oasiensis) and Mauritania (Van Damme, 1984; who also gives Late PleistoceneHolocene sites). Probably throughout tropical Africa (Brown & Mandahl-Barth, 1973), though records supported by anatomical observations are scattered. Southern limit apparently reached in Namibia (Naukluftberge; Brown & Curtis, 1992) and E Natal (Lake Sibayi, Appleton, 1977c, and Pietermaritzburg, BME). Apparently present in Zanzibar (P. gibbonsi Nelson) and possibly in the Cape Verde Islands (Groh, 1983, shell only) Afrogyrus rodriguezensis (Crosse, 1873, 1874, Planorbis). Type locality: Rodriguez Island, source of the Cocos River. Fig. 86d. 1.4×4 mm. Whorls rounded and rapidly increasing; umbilicus narrow and deeply concave. Penial stylet like that of A. coretus; Brown quoted by Starmühlner (1983). Planorbis mauritianus Morelet has a similar shell but is not closely related (see Gyraulus). DISTRIBUTION. Rodriguez Island: type locality and St Gabriel (Starmühlner, 1983). Afrogyrus starmuehlneri Brown, 1980b (Starmühlner, 1969, Gyraulus apertus). Type locality: Madagascar, Antsirabe district about 150 km S of Tananarive, Amborompotsy Stream in Antsampandrano Forest Station, southern Ankaratra Mountains, at about 2000 m altitude. Fig. 88a. 1.2×2.4 mm (largest paratype; maximum of 1×5 mm reported by Starmühlner, 1969). Whorls increasing even more rapidly than in A. rodriguezensis and the umbilicus is extremely small. This species is not Planorbis apertus Martens of East Africa (see Ceratophallus). HABITAT AND DISTRIBUTION. Madagascar: small streams in the Ankaratra Mountains, between 1800 and 2000 m altitude (Starmühlner, 1969); further possible localities in the north need confirmation (Fischer-Piette & Vukadinovic, 1973, as G. apertus). Afrogyrus crassilabrum (Morelet, 1860, Planorbis). Type locality: Madagascar, Port-Leven on the NW coast. Fig. 87b. 1.8×7 mm (rarely to 9 mm). Up to 5 whorls, varying from bluntly angular to carinate, with fine regular ribs, which may bear membranous crests. The underside of the shell is flat in the form named Planorbis hildebrandti

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Fig. 87. Planorbidae. (a) Planorbis planorbis; Egypt, (b) Afrogyrus crassilabrum; Madagascar (syntype, BMNH1893.2.4.1745–7). Scale lines: 2 mm.

Martens, 1883 (holotype illustrated by Kilias, 1967). Anatomy and histology described by Starmühlner (1969, as Anisus). Some individuals lack a distinct spermatheca, having merely a vaginal swelling (Brown & Mandahl-Barth, 1973, as A. trivialis; Starmühlner, 1983). HABITAT. Various waterbodies in Madagascar, including streams, ricefields, lakes and a thermal spring; cement-walled cistern on Grand Comore. DISTRIBUTION. Madagascar: widespread (Starmühlner, 1969; Fischer-Piette & Vukadinovic, 1973). Comoro Islands: Grand Comore (Starmühlner, 1983), Mayotte (Julvez et al., 1990) and earlier records based on shell only (Backeljau et al., 1986). Genus Armiger Hartmann, 1843 Scarcely 3 mm in diameter, whorls few and rapidly increasing, with widelyspaced ribs, sometimes projecting as spines from the circumference; last whorl not closely embracing the penultimate whorl, so that the inner lip is continuously curved. Penis tip with a small cuticular stylet (Hubendick, 1955; Meier-Brook, 1983). Treated as a subgenus of Gyraulus by Meier-Brook, with probably only one species. Type species: Nautilus crista Linnaeus, 1758, Germany. Armiger crista (Linnaeus, 1758, Nautilus). Type locality: Germany, in marshes. Fig. 88b.

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Fig. 88. Planorbidae. (a,a′) Afrogyrus starmuehlneri; Madagascar (paratype, BMNH1981. 152). (b,b′) Armiger crista; Ethiopia, near Debra Berhan. Scale line: 1 mm.

0.5×3 mm. Characters as for the genus. HABITAT. Amongst vegetation in a small rock-pool beside a rapidly-flowing stream in Ethiopia at 3050 m (9000 feet), with Ceratophallus and other gastropods (Brown, 1967c). DISTRIBUTION. Holarctic: frequent in Europe and N Asia, but scarcer in N America (Clarke, 1973; Meier-Brook, 1983). Southern limits in Africa: recently living in Algeria (Bourguignat, 1864, P. cristatus and P. imbricatus), Morocco (Ifrane, collected in 1971; Van Damme, 1984) and Ethiopia (near Debra Berhan; Brown, 1967c). Shells in Late Pleistocene-Holocene deposits in highlands of S Algeria and N Chad (Sparks & Grove, 1961; Van Damme, 1984). Genus Ceratophallus Brown & Mandahl-Barth, 1973 Usually less than 8 mm diameter; the whorls may be rounded, angular or carinate. Penis (Fig. 14a) with terminal opening and increasingly sclerotised towards the tip, which may bear short spines (whereas Gyraulus and Anisus have a dagger-like stylet). The pseudobranch is a simple lobe lacking the dorsal ridge present in Gyraulus. Numerous prostatic tubules open into a separate prostatic duct. Africa: mainly in the eastern part, with isolated localities near Lake Chad and in Zaire (Fig. 119). About 11 species, mostly confined to lakes, although C.

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Fig. 89. Planorbidae: Ceratophallus. (a) C. natalensis; Kenya, Kano Plain, (b) C. blanfordi; Ethiopia (paratype, BMNH1993.072). Scale line: 2 mm.

natalensis is widespread in small habitats. Type species: Planorbis natalensis Krauss, 1848, Umgeni Valley in Natal. Ceratophallus natalensis (Krauss, 1848, Planorbis). Type locality: South Africa, Natal, Umgeni Valley (near Durban). Fig. 89a. 1×6.7 mm. About 5 slowly increasing and convex whorls which may be bluntly angular near the base; occasionally specimens with a low spire may be found. When small difficult to distinguish from Afrogyrus coretus, which has about a half-whorl more at the same size, but clearly recognisable from the terminal opening and partial sclerotisation of the penis. Variation in shell and penis suggests that different species could be confused here; to this complex apparently belong Planorbis leucochilus Melvill & Ponsonby (1903, Pietermaritzburg) and P. sperabilis Preston (1912; Kenya, Gazi). HABITAT. Marshes, slowly flowing streams and common in rainpools with Bulinus reticulatus in W Kenya. The snail clings to the surface film and propels itself along by rhythmically jerking the shell. DISTRIBUTION (Fig. 119). Eastern Africa from the highlands of Ethiopia southwards into Cape Province, though rarely found near the tropical coast. Scattered localities confirmed by examination of the penis are Lake Chad,

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Banzyville and Katanga in Zaire, and Harare (Salisbury; Brown & MandahlBarth, 1973). Comoro Islands: Anjouan (Starmühlner, 1976a, 1983, Ceratophallus sp.). PARASITES. Loker et al. (1981) obtained 11 species of trematode cercariae from naturally infected snails in NW Tanzania. Ceratophallus blanfordi Brown, 1973. Type locality: Ethiopia, Tigre Province, Lake Ashangi. Fig. 89b. 1.3×5.2 mm. Whorls increasing more rapidly, so that there is about one whorl less than in C. natalensis of similar diameter; underside flatter, periphery more angular. HABITAT AND DISTRIBUTION. Vegetation in shallow water of Lakes Ashangi and Haik in highland Ethiopia. Ceratophallus kigeziensis (Preston, 1912a, Planorbis). Type locality: SW Uganda, Kigezi at 1830 m (6000 feet). Fig. 90a. 0.7×3.0 mm. Shell (3 syntypes, BMNH) with about 3.5 whorls, strongly angular near or below the middle; umbilicus wide and shallow; lacking spiral sculpture but with strong and widely spaced ribs. Mandahl-Barth (1954) proposed the name Gyraulus kigeziensis nyanzae for snails from Lake Victoria having strong spiral sculpture; all such specimens dissected had a Ceratophalluslike penis (Brown & Mandahl-Barth, 1973). Planorbis avakubiensis Pilsbry & Bequaert (1927, E Zaire) is perhaps the same species. DISTRIBUTION. Uganda: type locality and Lake Victoria (Mandahl-Barth, 1954a). Lake Edward (Adam, 1957) and Lake Kivu (DBL). Ceratophallus kisumiensis (Preston, 1912b, Planorbis). Type locality: Kenya, Lake Victoria at Kisumu. Fig. 90d. 1.5×4.5 mm. Umbilicus smaller and deeper than in the preceding species. Shells from Kisumu (BME) have 1 or 2 blunt angulations, a nodular surface due to strong transverse and spiral sculpture, and spiral rows of short bristles. HABITAT AND DISTRIBUTION. Kenya: the stony beaches of Lake Victoria near Kisumu. Ceratophallus bicarinatus (Mandahl-Barth, 1954, Gyraulus). Type locality: Uganda, Lake Albert at Butiaba. Fig. 90b. 1.1×3.7 mm. Whorls rapidly increasing, with two strong carinae. HABITAT. Taken alive at a depth of 18 m in Lake Albert (Mandahl-Barth). Dredged by myself with fine gravel in shallow water in Lakes Awasa and Zwai. DISTRIBUTION. Lake Albert; Lakes Zwai and Awasa in Ethiopia (BME); Lake Chad (Kristensen, 1987). Ceratophallus subtilis (Mandahl-Barth, 1954, Gyraulus costulatus subtilis). Type locality: Uganda, NE side of Dagusi Island in Lake Victoria, at depths of 6– 12 m. Fig. 90e. 1.6×5 mm. Whorls rapidly increasing and depressed, with a peripheral angle. Like G. costulatus but the ribs are finer; examination of penis desirable to confirm identification. DISTRIBUTION. Known with certainty from only northern Lake Victoria.

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Ceratophallus concavus (Mandahl-Barth, 1954, Gyraulus). Type locality: Uganda, Victoria Nile near Bujagali, 11 km (7 miles) N of Jinja. Fig. 90c. 1.2×3.2 mm. Last whorl bluntly angular, flattened beneath and descending to form a small deep umbilicus. HABITAT. Beneath stones with Segmentorbis and Burnupia (MandahlBarth). DISTRIBUTION. Type locality and Lake Victoria; shallow water in Hippo Bay, Entebbe. Ceratophallus crassus (Mandahl-Barth, 1954, Gyraulus). Type locality: Uganda, Lake Victoria, Hippo Bay near Entebbe. Fig. 90g. 2×4.5 mm. Whorls rapidly increasing, high and bluntly angular, with coarse spiral and transverse sculpture. DISTRIBUTION. Northern part of Lake Victoria: Hippo Bay and Buvuma Channel down to depth of 9 m (Mandahl-Barth). Ceratophallus pelecystoma Brown, 1975. Type locality: SE Kenya, Lake Chala near Taveta. Fig. 90f. 1.6×3.4 mm. Shell small and thick-walled, with two strong carinae. Aperture with divergent upper and lower margins, giving it the appearance of an axe-head. HABITAT. Underside of stones in shallow water in a crater lake near Mount Kilimanjaro; no other molluscs were found there. DISTRIBUTION. SE Kenya: Lake Chala near Taveta. (?)Ceratophallus apertus (Martens, 1897, Planorbis). Type locality: NE Zaire, northwest shore of Lake Edward near Kirima. Fig. 91c. 1.5×3 mm. The original figure shows the last whorl as angular beneath and descending to an even greater extent than in C. concavus. Anatomy unknown; generic position needs confirmation. Adam (1957) illustrated as Gyraulus apertus a ‘recent’ shell from Lake Edward near the Kigera River. Other reports are incorrect; specimens illustrated by Leloup (1953) from Lake Tanganyika are Gyraulus costulatus, while those from Madagascar (Starmühlner, 1969) were later described as Afrogyrus starmuehlneri. DISTRIBUTION. Known with certainty only from Lake Edward. (?)Ceratophallus faini (Adam, 1957, Gyraulus). Type locality: Lake Albert, W shore between Kawa and Saliboko. Fig. 91a. 1.2×3.4 mm. Whorls increasing rapidly, with two strong angles. Anatomy unknown: generic position needs confirmation. Larger (2×6 mm) bicarinate shells from Late Pleistocene-early Holocene deposits near Lake Edward were named Gyraulus bequaerti by Adam (1957). (?)Ceratophallus socotrensis (Godwin-Austen, 1883, Planorbis). Type locality: Socotra Island. Fig. 91b. 0.5×3.4 mm. Known from only two shells, with 4 slowly increasing whorls, strongly carinate above and below. Anatomy unknown; generic position needs confirmation. DISTRIBUTION. Socotra Island: known from the type locality only.

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Fig. 90. Planorbidae: Ceratophallus. (a) C. kigeziensis; Uganda (syntype, BMNH1911.11. 2.100– 102). (b) C. bicarinatus; Ethiopia, Lake Awasa. (c) C. concavus; Victoria Nile (syntype, BMNH1968.676). (d) C. kisumiensis; Lake Victoria at Kisumu. (e) C. subtilis; Lake Victoria (syntype, BMNH1993.070). (f) C. pelecystoma; Kenya (paratype, BMNH1973.94.1–4). (g) C. crassus; Lake Victoria (syntype, BMNH1968.600). Scale line: 2 mm.

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Fig. 91. Planorbidae. Species apparently belonging to Ceratophallus, but known only from shells, (a) ?C. faint; Lake Albert (paratype, DBL), (b) ?C. socotrensis; Socotra Island (after Godwin-Austen, 1883, Pl. 1). (c) ?C. apertus; Lake Edward (after Martens, 1897, Pl. 6,17). Scale lines: 2 mm.

Genus Gyraulus Charpentier, 1837 Shell usually less than 7 mm diameter, whorls rounded, angular or carinate, increasing more rapidly than in Anisus (see below). Penis (Fig. 14b) with a subterminal opening and a dagger-like stylet. Pseudobranch with a lamella in its dorsal surface (Brown, 1965, Fig. 30). The taxonomy of mainly Eurasian species was revised according to extensive anatomical studies by Meier-Brook (1983). Distribution worldwide, though occurrence in S America has not yet been confirmed by anatomical observations. Three species on the African mainland and one endemic on each of the islands Socotra and Mauritius. G. laevis (Alder) of Europe is recorded from Algeria and some Mediterranean islands, but such specimens dissected by Meier-Brook (1983) proved to be Planorbis planorbis. Meier-Brook (1983) found the African species G. costulatus and G. connollyi to have distinctive anatomical characteristics that justified segregating them into the subgenus Caillaudia Bourguignat, 1883 (for C. angulata of Ethiopia). Type species (of Gyraulus): Planorbis albus Müller, 1776. Gyraulus species are among the first intermediate hosts of intestinal flukes of the genus Echinostoma which infect man in Asia, but echinostomiasis of man is not known in Africa. Gyraulus ehrenbergi (Beck, 1837, Planorbis). Type locality: Egypt. Fig. 92a. 1.7×6.8 mm (rarely to 10 mm). Periphery rounded or angular (the form known as Planorbis mareoticus Innes), sometimes with a fringe of periostracum; transverse ridges if present are irregularly spaced. Meier-Brook (1983) distinguished this species from G. piscinarum (Bourguignat) of SW Asia by

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characters of the shell and anatomy; further comparison is needed with G. convexiusculus (Hutton) reported from N and S Yemen and Saudi Arabia (Wright, 1963b; Brown & Wright, 1980; Al-safadi, 1990). HABITAT AND DISTRIBUTION. Egypt: especially the delta region, found by myself amongst dense vegetation in drains. Records for Sudan (Pallary, 1909; Longstaff, 1914) probably refer to G. costulatus. In Late Pleistocene-Holocene deposits in Egypt (Gardner, 1932; Van Damme, 1984). Gyraulus costulatus (Krauss, 1848, Planorbis). Type locality: South Africa, Natal, Umgeni River. Figs 92b,c. 1.5×6.6 mm (depressed form). Shell of typical form (Fig. 92b) depressed, whorls rapidly increasing, with strong and regularly-spaced ribs; periphery with a carina near the middle and bearing a fringe of periostracum. Shell and anatomy described for widely scattered populations (e.g. Medeiros, 1964; Wright, 1963a; Brown, 1965; Brown & Van Eeden, 1969; Meier-Brook, 1983). The shape of the whorls is highly varied; they are only bluntly angular in some populations (Fig. 92c), and in South Africa such shells may be confused with G. connollyi (see below). A supposed subspecies, G. c. subtilis Mandahl-Barth, 1954 was transferred to the genus Ceratophallus (Brown & Mandahl-Barth, 1973). G. c. exilis MandahlBarth, 1954, founded on depressed carinate snails from Lake Mutanda, Uganda, seems indistinguishable from the typical form, as does Caillaudia angulata Bourguignat, 1883 of Ethiopia and Planorbis gardei Germain, 1909 of Tchad. HABITAT. Aquatic vegetation, marginal grass and stones in slowly flowing streams and rivers, large dams and lakes. Tolerant of shade and favoured by organic pollution (Ndifon & Ukoli, 1989). Absent from habitats which regularly dry out. Less tolerant of cool climate than G. connollyi, with which it is partly sympatric. G. costulatus seems to be moving northwards in Egypt, probably carried by floating Eichhornia plants (Sattman & Kinzelbach, 1988). DISTRIBUTION. Africa: mainly in the tropical region. Isolated living populations in SE Algeria, Tassili N’Ajjar (P. gardei of Ranson & Cherbonnier, 1953), Libya (Tejerhi in Fezzan, DBL) and Egypt (Asyut and a few localities further south, Sattman & Kinzelbach, 1988). Late Pleistocene-Holocene localities in SE Algeria and Chad (Sparks & Grove, 1961), Sudan (Martin, 1968) and elsewhere in the eastern Sahara (Van Damme, 1984). The main range extends from Ethiopia (Brown, 1965) and S Sudan (Brown, Fison et al., 1984) westwards to the Senegal River (Malek & Chaine, 1981) and southwards to Angola (Wright, 1963a), the Okavango Delta (Brown, Curtis et al., 1992) and eastern South Africa (Brown & Van Eeden, 1969). Absent from the cooler areas of Lesotho and western Cape Province. Gyraulus connollyi Brown & Van Eeden, 1969. Type locality: South Africa, Transvaal, near Vereeniging, dam on farm Witkop. Figs 92d, 93a. 1.6×4.7 mm. Whorls relatively high and strongly angular below; unlike G. costulatus the periphery is never carinate, there is no peripheral fringe of periostracum and the ribs are less regular and closer together. Brown & Van

198 SYSTEMATIC SYNOPSIS: PULMONATES

Eeden gave reasons for rejecting Connolly’s identification of this species as Planorbis lamyi Germain (1905, Lake Tanganyika), which has never been refound (type illustrated by Leloup, 1953) and could be a lacustrine Ceratophallus. HABITAT. Vegetation and stones in rivers and streams in the southern temperate climatic region. DISTRIBUTION (Fig. 148, Chapter 12). South Africa: highveld and escarpments from Pilgrim’s Rest in E Transvaal southwards and found down to sea-level south of latitude 31° S (Brown & Van Eeden). Swaziland: Mbabane (DBL). I failed to find this species in apparently suitable streams in the highlands of E Zimbabwe. Gyraulus cockburni (Godwin-Austen, 1883, Planorbis). Type locality: Socotra Island. Fig. 93c. 1.1×4.3 mm. Whorls increasing slowly and not angular. Copulatory organ examined by Brown & Mandahl-Barth (1973). HABITAT AND DISTRIBUTION. Socotra Island: obtained originally from waterplants with (?)Ceratophallus socotrensis; also from Wadi Erhina (Brown & Mandahl-Barth, 1973). Gyraulus mauritianus (Morelet, 1876, Planorbis). Type locality: Mauritius. Fig. 93b. 1.1×3.6 mm. Whorls bluntly angular, any transverse ridges present are fine. Anatomy described by Starmühlner (1983). HABITAT AND DISTRIBUTION. Mauritius and Seychelles; in slowly flowing rivers and streams, especially where slightly polluted (Starmühlner, 1983). Genus Anisus Studer, 1820 Shell reaching 10 mm diameter, with up to 8 slowly increasing whorls. Penis like that of Gyraulus. In most of the Palaearctic Region and reported from Algeria (Bourguignat, 1864, Planorbis spirorbis L.). Unfortunately no information is available about the anatomy of snails from NW Africa that might be Anisus. Segmentina tribe. Shell small, convex on one side and flat on the other (‘lensshaped’), with a small umbilicus; internal lamellae present in some groups. Segmentina and Hippeutis of the Palaearctic Region have 2 flagella attached to the penis sheath. H. complanatus (L.) possibly occurs in Algeria (Planorbis euphaeus and similar species of Bourguignat, 1864). However, the tropical African species previously placed in these groups were separated into new genera by Mandahl-Barth (1954a), according to the structure of the copulatory organ. Verdcourt (1958b) described an unidentified, possibly planorbid shell from Kenya shaped rather like some members of this tribe. A similar shell from Upper Volta (Fig. 94a) has spiral rows of pits visible at magnification ×50 and probably belongs to the landsnail family Endodontidae.

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Fig. 92. Planorbidae: Gyraulus. (a) G. ehrenbergi; Egypt, (b) G. costulatus; South Africa, Ingwavuma. (c) G. costulatus; South Africa, Klein Jukskei River near Johannesburg, (d) G. connollyi; South Africa (holotype, BMNH1969.4). Scale line: 2 mm.

Genus Lentorbis Mandahl-Barth, 1954 Shell up to 7 mm diameter, lamellae entirely lacking or up to 4 sets present at least

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Fig. 93. Planorbidae. (a) Gyraulus connollyi; South Africa, E Cape, Kentani. (b) G. mauritianus; Mauritius (syntype, BMNH1893.2.4.539–41). (c) G. cockburni; Socotra Island Wadi Erhina. (d) Lentorbis junodi; Mozambique (paratype, BMNH 1937.12.30. 8801–7). Scale line: 2 mm.

as traces. Penis without any flagellum; preputium with a large eversible lobe.

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Widespread in eastern and central Africa (Fig. 120); possibly present in Madagascar. Type species: Planorbis benguelensis Dunker, 1845, Angola. Lentorbis benguelensis (Dunker, 1845, 1853, Planorbis). Type locality: Angola, Benguela. Fig. 94c. 1.5×5 mm (rarely to 7 mm). Non-lamellate or with traces of 1 or 2 sets. Copulatory organ with penis sheath about equal in length to preputium; aphallic individuals occur (Wright, 1963a). HABITAT. Aquatic vegetation in lakes, marshes and slowly flowing rivers. DISTRIBUTION (Fig. 120). Angola: coastal plain (Wright, 1963a). Zaire: Kinshasa (Mandahl-Barth et al., 1974). Lentorbis junodi (Connolly, 1922, 1925, Hippeutis). Type locality: Mozambique, Nwambukoto near Rikatla (near Lourenço Marques). Figs 93d, 94b. 2×5.5 mm. Shell like L. benguelensis but penis sheath longer, as much as twice the length of the preputium (Azevedo et al., 1961; Brown, 1965). HABITAT. Aquatic vegetation in marshes, slowly flowing rivers and streams. DISTRIBUTION (Fig. 120). Tropical Africa: Lake Chad, Ethiopia, S Sudan, eastern Africa including Zanzibar and southwards to near Durban; possibly also Madagascar (DBL, anatomy unknown). Lentorbis carringtoni (Azevedo et al., 1961, Segmentorbis). Type locality: Mozambique, Nacala. Fig. 94d. 1.6×4.7 mm. Commonly with 1–4 sets of lamellae. The very long penis sheath, reaching 3 times the length of the preputium, is distinctive (Oberholzer & Van Eeden, 1967). DISTRIBUTION. Mozambique, SE Transvaal and possibly in the coastal region of Natal (where critical separation from L. junodi is necessary). Genus Segmentorbis Mandahl-Barth, 1954 Shell up to 6 mm diameter, with up to 10 sets of lamellae within the last whorl. Penis sheath either with one flagellum or none (S. kanisaensis). Found from lower Egypt to eastern South Africa and westwards into Gambia; also in Madagascar. Type species: Segmentina angusta Jickeli, 1874, Ethiopia. Segmentorbis angustus (Jickeli, 1874, Segmentina). Type locality: Ethiopia, Hamasen Province, Toquor River at Mekerka (west of Asmara). Fig. 95a. 2×5.5 mm. Fully grown shell about 3 times broader than high, with usually no more than 3 sets of septa. Young shells are relatively higher and apparently these were named Segmentina chevalieri Germain (1904, Lake Chad) and S. kempi Preston (1912a, Kigezi in SW Uganda). Another probable synonym is S. emicans (Melvill & Ponsonby, 1892, South Africa, Port Elizabeth). HABITAT. Vegetation in permanent marshes, on rocks in streams and the stony beaches of Lake Victoria. DISTRIBUTION. Africa: mainly in the tropical region. Isolated living populations found in SE Algeria (Pallary, 1934; collected most recently in 1982

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Fig. 94. (a) Landsnail resembling a small planorbid. (b) Lentorbis junodi; Mozambique (paratype, BMNH1937.12.30.8801–7). (c) L. benguelensis; Angola, Lagoa Lalama. (d) L. carringtoni; Mozambique (syntype, DBL). Scale line: 2 mm.

at Djanet oasis, DBL) and Chad (Tibesti; Germain, 1935b). Late PleistoceneHolocene localities in the present-day desert and Egypt (Van Damme, 1984). The main range includes Ethiopia (Brown, 1965) S Sudan (Brown, Fison et al., 1984), Lake Chad (Lévêque, 1967; Brown, 1974), Nigeria (Kainji district, BME) and extends southwards into the Okavango Delta (Brown, Curtis et al., 1992) and the Natal coast (Brown, 1967a; Appleton, 1977c). Madagascar: widespread in the N and W regions (Fischer-Piette & Vukadinovic, 1973). Segmentorbis planodiscus (Melvill & Ponsonby, 1897, Planorbis). Type locality: South Africa, Natal, Umgeni Valley, Fig. 96a. 1.6×5.8 mm. The numerous lamellae provide the most obvious characteristic; 2 syntypes (BMNH) have 6 and 10 sets in the last whorl. A critical comparison with S. angustus is needed to demonstrate that these species really are different. DISTRIBUTION. Coastal area of SE Africa from Port St Johns (Connolly, 1939) to Mtubatuba (Brown, 1967a). Namibia, Ovamboland according to

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Fig. 95. Planorbidae: Segmentorbis. (a) S. angustus; Ethiopia, near Debra Berhan. (b) S. eussoensis; Kenya (possibly a syntype, BMNH1911.8.22.212). Scale line: 2 mm.

Connolly (1939). Mandahl-Barth (1954a) discussed a doubtful record for Lake Albert. Segmentorbis eussoensis (Preston, 1912a, Segmentina). Type locality: NE Kenya, Chanler Falls on the Eusso Nyiro River. Figs 93b, 96b. 1.5×5.3 mm (Preston); a syntype (BMNH) measures 1.4×4.2 mm and has 5 septa. Shell rather more depressed than S. angustus, with a larger umbilicus (Kristensen, 1987). Further data are needed to confirm that this is a distinct species. DISTRIBUTION. Kenya: type locality and between Eusso Nyiro and Mount Marsabit (BMNH). Sudan (Kristensen, 1987). Segmentorbis excavatus Mandahl-Barth, 1968 (for Segmentina kempi of Pilsbry & Bequaert, 1927 not Preston). Type locality: SE Zaire, Kisanga River, a tributary of the Kafubu River near Elizabethville. Fig. 97b. 1.6×2.7 mm (to 3.3 mm). Comparatively small, with high whorls and deeply concave underside. DISTRIBUTION. SE Zaire: several localities in the Kisanga River (MandahlBarth, 1968a). Segmentorbis kanisaensis (Preston, 1914, Segmentina). Type locality: S Sudan, Nile at Kanisa. Figs 96c,d, 97a. 1.2×4.6 (rarely to 6 mm). Depressed and strongly carinate at the periphery, with stronger spiral sculpture than other species in the genus; up to 4 sets of

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Fig. 96. Planorbidae: Segmentorbis. (a) S. planodiscus; South Africa (syntype, BMNH1902.7.30.12–13). (b) S. eussoensis; Kenya (possibly a syntype, BMNH1911.8.22. 212). (c) S. kanisaensis; Sierra Leone (syntype of S. formosa Connolly, BMNH1937.12. 30.8748–57). (d) S. kanisaensis; Sudan (syntype, BMNH1923.6.8.1224–27). Scale line: 2 mm.

lamellae in the last whorl. Penis sheath lacking any flagellum. This distinctive

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Fig. 97. Planorbidae: Segmentorbis. (a) S. kanisaensis; Sudan (syntype, BMNH1923.6.8. 1224– 27). (b) S. excavatus; SE Zaire (paratype, DBL). Scale line: 2 mm.

species is the type of the subgenus Acutorbis Mandahl-Barth, 1956. S. formosa Connolly, 1928 (Fig. 96c) of Sierra Leone was founded on small shells. HABITAT. Found by myself with S. angustus and Lentorbis in permanent marshes, and also in temporary rainpools where the other two do not occur. DISTRIBUTION (Fig. 121). Africa: mainly in the tropical areas. Ethiopia and S Sudan (Brown, Fison et al., 1984), and westwards through Niger and Mali (Madsen et al., 1987) into Gambia. Southwards to the coastal plain of Angola (Wright, 1963a), Okavango River (Brown, Curtis et al., 1992) and Durban (Brown, 1967a). Liable to be overlooked because small and probably much commoner than appears. Biomphalaria tribe. Distinguished by the structure of the copulatory organ and arrangement of the prostatic tubules (see account of the genus). Genus Biomphalaria Preston, 1910 Medium-sized (rarely reaching 20 mm diameter); whorls evenly convex, angular or carinate; in some species the last whorl descends producing a concave underside. Tooth-like lamellae occur on the inner wall of the shell near the aperture in some individuals of a few species (Mandahl-Barth, 1957a, p. 15). Copulatory organ lacking any accessory glandular structure externally, with a slender penis sheath; penis with terminal pore and without any sclerotisation. Prostatic tubules numerous, arranged in a row, opening directly into the vas deferens without a separate prostatic duct. In varied habitats, including small pools, lakes, streams and irrigation channels. S and central America (several genus-names including Australorbis are synonyms of Biomphalaria), Arabia, Africa and Madagascar (but not other islands).

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About 12 species in Africa, arranged here in the order of Mandahl-Barth (1957a), whose system comprised 4 species groups, typified by B. pfeifferi, B. choanomphala, B. alexandrina and B. sudanica, and distinguished by characters of the shell, copulatory organ and radula. Unfortunately these groups do not seem to be clearly definable, and there has been only limited success in efforts to find further specific characters, whether morphological or biochemical (Mello, 1972; Ukoli, 1974; Wium-Andersen, 1973, 1974; Henriksen & Jelnes, 1980; Jelnes, 1982a; Vollmer, 1992). Type species: Biomphalaria smithi Preston, 1910, Lake Edward. A genus of great medical importance as probably for all species there is at least one compatible strain of S. mansoni. Biomphalaria pfeifferi (Krauss, 1848, Planorbis). Type locality: South Africa, Natal, Umgeni Valley. Figs 98a–c. 5.2×13 mm (to 17 mm). In the typical form (Fig. 98a) the umbilicus occupies about one-third of the shell diameter (Schutte & Van Eeden, 1959; Azevedo et al., 1961) and the whorls are somewhat bluntly angular below. Some individuals in particular populations have shell lamellae within the last quarter-whorl, of various sizes and arrangement (McCullough, 1958). Penis sheath usually shorter than the preputium; the mesocones on the lateral teeth are non-angular (MandahlBarth, 1957a, 1968a; Schutte & Van Eeden, 1959, 1960). Growth of the shell and copulatory organ were analysed by Madsen (1984) for the purpose of discrimination from Helisoma. Six subspecies were recognised by Mandahl-Barth (1957a), but although their total range extends from the Sahara to Natal, no clear pattern of geographical variation could be confirmed (Mandahl-Barth, 1960). Continuous variation (Brown, 1965) links forms distinguished by a narrow umbilicus, e.g. B. adowensis (Bourguignat, 1879) of Ethiopia to those with a wider umbilicus e.g. B. bridouxiana (Bourguignat, 1888) of Lake Tanganyika and B. nairobiensis (Dautzenberg, 1908) from Nairobi. Similarly, populations with high whorls (Fig. 98b) can be linked through intermediates to those with low whorls (Fig. 98c). Names have been given to isolated populations with distinctive shells found in semi-arid areas, e.g. B. hermanni (Boettger, 1910, Namibia), B. germaini (Ranson, 1953, S Algeria) and B. gaudi (Ranson, 1953, Dakar). Beyond Africa, both B. arabica (Melvill & Ponsonby, 1896, Dhofar; Brown & Gallagher, 1985) and B. madagascariensis (Smith, 1892; Starmühlner, 1969) are difficult to distinguish from B. pfeifferi on morphological grounds. The species-name rüppelli (or rueppelli) (Dunker, 1848, from ‘Abyssinia’) is of special interest, being published in the same year as pfeifferi of Krauss. Though rather small, this northern form seems indistinguishable from Krauss’s species (Mandahl-Barth, 1957a, 1960; Brown, 1965). Although taxonomic subdivisions within B. pfeifferi have not been upheld, the variation at some enzyme loci indicates biological differences between populations in Cameroon and Senegal (Mimpfoundi et al., 1986), and also within Cameroon (Mimpfoundi & Greer, 1990a) and in Kenya (Bandoni et al., 1990).

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HABITAT. Various waterbodies including streams, irrigation channels, reservoirs, dams and some seasonal waters, but not briefly-filled rainpools. Factors affecting distribution, life cycle and population dynamics are described in Chapters 10 and 11. Here the space available allows reference to some of only the more recent studies: of streams (Thomas & Tait, 1984; Loreau & Baluku, 1987b; Baluku & Loreau, 1989), a lake (Appleton, 1977c), reservoirs (Dupouy & Mimpfoundi, 1986), irrigated areas (Wibaux-Charlois et al., 1982; Gryseels, 1985, 1991; Betterton, Ndifon et al., 1988; Madsen et al., 1988) and rice-paddies (Dennis et al., 1983). Among factors determining distribution and abundance, climatic temperature is important and can be limiting, both when too cool and too warm (Appleton, 1977a; Appleton & Eriksson, 1984). Clearance of forest seems to have favoured the spread of B. pfeifferi, and shade has been found so unfavourable as to provide a potential means for biological control (Loreau & Baluku, 1991). Moderate pollution can be favourable (Smith, 1982; Ndifon & Ukoli, 1989), and a rich algal flora is beneficial as food (Baluku et al., 1987). The effects of water chemistry have been extensively studied in the field and laboratory (Chapter 10); the decrease in salinity that followed the building of a barrage across the lower Senegal River resulted in greatly increased abundance of this snail (Diaw et al., 1991; Talla et al., 1990). DISTRIBUTION (Fig. 122). Africa, mainly in the tropical region and also SW Arabia (B. arabica) and Madagascar (B. madagascariensis). Late PleistoceneHolocene distribution was extensive in the present Sahara Desert (records summarised by Van Damme, 1984). Living populations have persisted in SE Algeria, Niger and Chad (Fig. 122). The main present-day range lies southwards of a line passing approximately from Asmara in Ethiopia to the lower Senegal River Basin (Fig. 122). In West Africa the distribution is known particularly well for francophone countries (Sellin, 1979; Sellin et al., 1980). Southern limits lie in S Angola, the Okavango Delta, W Transvaal and Transkei, with an isolated and apparently extinct population at Okaputa Pan, Namibia (B. hermanni Boettger). The absence of B. pfeifferi from suitable waterbodies in the Orange Free State, Cape Province and Lesotho seems due to the cool winter climate. On the other hand, it is unfavourable effects of too warm a climate that seem likely to account for the snail’s absence from the eastern coastal region extending from northern Mozambique into Somalia (Sturrock, 1966; Appleton, 1977a; Chapter 10, Temperature). PARASITES. S. mansoni: B. pfeifferi is the most important intermediate host in tropical Africa. Among the more recent field investigations are studies for Burundi (Gryseels, 1985, 1991), Cameroon (Greer et al., 1990), Mali (Madsen et al., 1987; Coulibaly & Madsen, 1990), Niger (Mouchet, Labo et al., 1987), Senegal (Diaw et al., 1991), South Africa (Donnelly & Appleton, 1985), Sudan (Fenwick et al., 1981) and Zimbabwe (Chandiwana et al., 1987). An extensive

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Fig. 98. Planorbidae: Biomphalaria. (a–c) B. pfeifferi: (a) South Africa, Umgeni River; (b) Kenya, Eldoret; (c) Kenya, Nairobi, (d) B. rhodesiensis; Zambia (syntype, BMNH1968.688). (e) B. choanomphala; Kenya, Lake Victoria. Kendu Bay. Scale line: 5 mm.

experimental study (Frandsen, 1979d,f) compared compatibilities among

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different stocks of the snails with parasite isolates from several countries. S. rhodaini: Zaire and Ruanda-Urundi (Schwetz, 1951, 1952), Kenya (Saoud, 1966) and Burundi (Gryseels, 1985). Paramphistomum sukari: Kenya (Dinnik, 1965), Ethiopia (Graber & Daynes, 1974). Echinostoma spp.: Madagascar (Richard & Brygoo, 1978), Togo (Jourdane & Kulo, 1981). Natural infections with 11 species of larval trematode were found in NW Tanzania (Loker et al., 1981). Biomphalaria rhodesiensis Mandahl-Barth, 1957, 1960, 1968a. Type locality: Zambia, Mazabuka, Central Research Station. Fig. 98d. 4×13 mm. Shell flatter than B. pfeifferi, with less rapidly increasing whorls. The mesocones of the lateral teeth are angular. DISTRIBUTION. Zambia: type locality, also Middle Luapula area and Lufubu River (Mandahl-Barth, 1968a). Tanzania: Tunduma (Mandahl-Barth, 1957a). PARASITE. Host for Paramphistomum sukari in Zambia (Dinnik, 1965). Biomphalaria choanomphala (Martens, 1879, 1897, Planorbis). Type locality: Tanzania, SW shore of Lake Victoria (exact location doubtful; see Verdcourt, 1992). Fig. 98e. 4.2×9.7 mm. Comparatively small; whorls nearly as high as wide, strongly angular beneath and sometimes also on the upper surface; umbilicus small. The last whorl descends, though less steeply than in B. smithi of Lake Edward. Holotype illustrated by Kilias (1967). HABITAT. Abundant on gravel and sedimentary rock at depths of 2–3 m, offshore from sandy beaches near Entebbe (Prentice et al., 1970). Commonest on mixed substrata of sand and mud near Mwanza (Magendantz, 1972). Found by myself at Kisumu on stones at the water’s edge. DISTRIBUTION. Lake Victoria, down to depths of about 12m and Victoria Nile; Lake Kyoga (Mandahl-Barth, 1957a); Lake Albert and the Albert Nile (B. elegans Mandahl-Barth, 1954a). PARASITES. S. mansoni: natural transmission at Bukoba and Mwanza (McClelland & Jordan, 1962; Webbe, 1962a; Baalawy, 1971; Magendantz, 1972) and near Entebbe (Prentice et al., 1970). Experimental infections by Cridland (1955) and Frandsen (1979d). Biomphalaria smithi Preston, 1910. Type locality: Lake Edward. Fig. 99a. 5×12 mm. Like B. choanomphala with a small umbilicus and angular underside, but the last whorl more steeply descending. HABITAT. Vegetation growing on sand at depths down to 4 m (Cridland, 1957). DISTRIBUTION. Uganda: Lake Edward and Mirambi crater lake (MandahlBarth, 1957a). PARASITE. S. mansoni: successful experimental infection (Cridland, 1957). Biomphalaria stanleyi (Smith, 1888, Planorbis). Type locality: Lake Albert. Fig. 99b.

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6.5×13 mm. Whorls higher than wide and increasing rapidly; umbilicus only about one-fifth of the shell diameter; last whorl angular on both sides. Mesocone of lateral tooth non-angular in snails from Lake Albert (Mandahl-Barth, 1957a), but strongly angular in those from Lake Chad (Brown, 1974). HABITAT. Vegetation in shallow water (Cridland, 1957; Gryseels et al., 1987). DISTRIBUTION. Lake Albert (Mandahl-Barth, 1954a; Cridland, 1957). Lake Chad (Brown, 1974). Lake Cohoha, Burundi (Gryseels et al., 1987; Kabatereine et al., 1992). PARASITE. S. mansoni: early experimental infection (Cridland, 1957) and recently found natural transmission (Gryseels et al., 1987). Biomphalaria barthi Brown, 1973. Type locality: E Ethiopia, Assaita village, on raised ground beside the lower Awash River. Fig. 99c. 4×11 mm. Whorls flattened above and below, though strongly curved near the suture; last whorl descending, umbilicus small (narrower than in any recognised form of B. pfeifferi). Like B. smithi, but whorls lower and less angular. Animal unknown. HABITAT. The shell shape suggests a lacustrine species, possibly still living in the lower Awash Basin or in the southern Rift Valley of Ethiopia. DISTRIBUTION. Ethiopia: known only from shells obtained near the lower Awash River at Assaita and from a shell deposit near Lake Zwai (BME). Biomphalaria alexandrina (Ehrenberg, 1831, Planorbis). Type locality: Nile Delta between Alexandria and Rosetta. Fig. 99d. 4.8×14.2 mm. The range of shell variation approaches B. pfeifferi at one extreme and B. sudanica at the other; perhaps distinguishable by the long penis sheath and strongly angular mesocone on the lateral teeth (Mandahl-Barth, 1957a). Some enzymes may also be distinctive (Jelnes, 1982a). Known also as B. boissyi (Potiez & Michaud, 1838). HABITAT. Particularly abundant in the water supply and drainage networks of the Nile Delta (Dazo et al., 1966; Doumenge et al., 1987). Found on a restricted part of the Libyan coast at Taourga in springs, streams and muddy edges of swamps, where snails may die due to seasonal increase in salinity (sources in Doumenge et al., 1987). Experimental investigations include studies of responses to temperature and other factors (El-Emam & Madsen, 1982; Madsen, 1987). Populations recently established in southern Egypt showed less genetic diversity than populations near Cairo (Vrijenhoek & Graven, 1992). DISTRIBUTION. North Africa. Egypt: formerly restricted to the Nile Delta, but recently found at increasing distances upstream as far as Lake Nasser at Aswan and Abu Simbel (Sattman & Kinzelbach, 1988; Vrijenhoek & Graven, 1992). NW Libya: Taourga (Doumenge et al., 1987). N Sudan: between Khartoum and Kosti (Williams & Hunter, 1968; Kristensen, 1986b). PARASITES. S. mansoni: in Libya and Egypt, where the endemic area once confined to the delta has spread southwards, establishing isolated foci of

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Fig. 99. Planorbidae: Biomphalaria. (a) B. smithi; Lake Edward (syntype, BMNH1937.12. 30.11416–7). (b) B. stanleyi; Lake Albert, Butiaba. (c) B. barthi; Ethiopia, Bulbulla River near Lake Zwai, subfossil. (d) B. alexandrina; Egypt, Alexandria, (e) B. angulosa; Tanzania, Kalenga swamp. Scale line: 5 mm.

infection in Giza Governorate (Doumenge et al., 1987). For experimental studies

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see Frandsen (1979d,f) and Chapter 5. Echinostoma liei and E. revolutum: B. alexandrina is a first intermediate host (Jeyarasasingam et al., 1972; Moravec et al., 1974a; Christensen et al., 1980). Biomphalaria angulosa Mandahl-Barth, 1957. Type locality: S Tanzania, Lake Ngwasi (near Mufindi). Fig. 99e. 5.5×15 mm. Upper side of whorls with a particularly strong angle, within which the surface is flat and sloping; umbilicus wide; coloured reddish brown. The mesocone of the lateral teeth is angular. A shell (DBL) sent by H.Watson with the locality ‘Durban’ is B. angulosa as reported by Mandahl-Barth (1957a), but the locality may be incorrect since no other specimen has apparently been found in Durban. Four shells (DBL) from Oaklands, Johannesburg, also identified as this species are, in my opinion, B. pfeifferi with unusually high whorls. HABITAT. Found with Bulinus africanus and other gastropods in the Kalenga Swamp, which dried out seasonally, and in the nearby irrigation scheme (Sturrock, 1965b). DISTRIBUTION. Tanzania: type locality, Kalenga and Little Ruaha swamps in Iringa area (DBL). Zambia: Chambezi Wantipa near Mbesuma, and the Chozi River (Mandahl-Barth, 1968a). Malawi: swamps 64 km (40 miles) N of Nkota Kota (BME). Records for South Africa are doubtful (see above). PARASITE. Compatible with S. mansoni from Mwanza (Sturrock, 1965b). Biomphalaria tchadiensis (Germain, 1904, Planorbis). Type locality: Lake Chad, Kouri Archipelago. 3.6×11 mm. Aperture somewhat expanded when mature; copulatory organ and mesocone on the lateral teeth like those of B. pfeifferi, of which tchadiensis is perhaps a lacustrine form. DISTRIBUTION. Lake Chad: type locality and Malamfatori (Brown, 1974). Biomphalaria camerunensis (C.R.Boettger, 1941, Australorbis). Type locality: Cameroon, Mongongo, NW of Mount Cameroon. Fig. 100a. 7×20 mm. Comparatively large, completing about 6 slowly increasing whorls, which are rather flat above and bluntly angular beneath; umbilicus wide and nearly half of the shell diameter. Similar to B. sudanica, but slightly less depressed and with fewer ovotestis diverticula (Vollmer, 1992). Internal shell lamellae present in a few individuals (Wright, 1965; Vollmer, 1992). MandahlBarth (1957a) named specimens from lower Zaire B. camerunensis manzadica; his B. alexandrina wansoni from Banzyville, N Zaire was later identified as B. camerunensis (Wium-Andersen, 1973). Differences from other Biomphalaria species were observed in studies of egg proteins (Wright & Ross, 1965) and enzymes (Wium-Andersen, 1973; Ukoli, 1974; Henriksen & Jelnes, 1980; Jelnes, 1982a). Considerable variation in allozymes was detected in Cameroon (Mimpfoundi & Greer, 1990b). HABITAT. Forty-three sites in Cameroon (Greer et al., 1990) included rivers, streams, lakes and swamps; snails sometimes found in temporary pools (Wright, 1965), but much commoner in permanent waters. In Zaire B. camerunensis

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occupied slowly flowing or stagnant waters where B. pfeifferi was not found (Mandahl-Barth et al., 1974); it was apparently displaced from Kinshasa by B. pfeifferi during the period 1970–1980 (De Clercq, 1987). B. camerunensis was the subject of a series of experiments relating to interspecific competition (e.g. Madsen, 1987, 1991). DISTRIBUTION (Fig. 123). From Ghana eastwards to Central African Republic (DBL) and southwards to lower Zaire. In Cameroon B. camerunensis is confined to the southern equatorial climatic zone (Greer et al., 1990), and it was never found in the same site as B. pfeifferi. PARASITES. S. mansoni: perhaps because of poor compatibility, B. camerunensis plays a minor part in transmission compared with B. pfeifferi (Mandahl-Barth et al., 1974; Ripert et al., 1978; Greer et al., 1990). However, from earlier field studies and the successful results of experimental infections, Frandsen (1979d, p. 344) concluded that in western central Africa there could be a parasite strain no less compatible with camerunensis than with pfeifferi. Biomphalaria salinarum (Morelet, 1868, Planorbis). Type locality: Angola, stream near Dungo (near the Cuije River). Fig. 100b. 4.8×16.3 mm. The original shells (Fig. 100b) resemble B. sudanica, having low and slowly increasing whorls and a wide umbilicus. The status of this species is obscure and further observations are needed on specimens from near the type locality. Mandahl-Barth (1957a) thought that it might be represented by large flat snails from SE Zaire that he identified as B. pfeifferi bridouxiana. Wright (1963a) collected from the district of the type locality snails he believed were juvenile salinarum; the mesocones on their lateral teeth were angular (unlike the non-angular mesocone of B. sudanica). Distinctive digestive gland enzymes were described for snails from Namibia (Wium-Andersen, 1974), but these did not necessarily represent B. salinarum. DISTRIBUTION (Fig. 123). Angola: type locality and near Malange (Wright, 1963a); 6 localities between Cangandala and Vila Artur de Paiva (Morais de Carvalho et al., 1966). Reported also from Namibia, probably Grootfontein, but not identified in recent collections (Brown, Curtis et al., 1992). PARASITES. S. mansoni: compatible in experiments with laboratory-bred snails originating from Namibia, Grootfontein (Pitchford et al., 1969; Frandsen, 1979d). S. edwardiense: compatible with snails of the same stock from Namibia (Pitchford & Visser, 1981). Biomphalaria sudanica (Martens, 1870, Planorbis). Type locality: Sudan, Bahr al Ghazal region (defined by Pilsbry & Bequaert, 1927 as Meshra-el-Req at 8°25′ N, 29°15′ E). Figs 100c,d. 4.2×16 mm (rarely to 22 mm). Shell large and flat, completing about 6 whorls, slowly increasing and flattened above; umbilicus wide, occupying about half of the shell diameter. Copulatory organ and mesocones (non-angular) described by Mandahl-Barth (1957a, 1968a). Shell like B. camerunensis but whorls somewhat lower and ovotestis diverticula more numerous (Vollmer, 1992). Critical

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Fig. 100. Planorbidae: Biomphalaria. (a) B. camerunensis; Cameroon, N’Dop Plain, (b) B. salinarum; Angola (syntype, BMNH1893.2.4.587–591). (c) B. sudanica; Kenya, Kano Plain, (d) B. sudanica; Lake Tanganyika (syntype of B. tanganyicensis (Smith), BMNH1880.12.20.74–77). Scale line: 5 mm.

comparison is needed with B. salinarum, which also has a similar shell. A shell

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from the type series was illustrated by Kilias (1967). The subspecies B. s. rugosa Mandahl-Barth (1960, 1968a; from Zambia, near Kapalala in the upper Luapula region) was differentiated by its coarse growth ridges, very wide umbilicus and the structure of its copulatory organ. A less depressed form with somewhat angular whorls is reported from Lake Chad (Planorbis tetragonostoma Germain, 1904; Mandahl-Barth, 1957a). Another subspecies, B. s. tanganyicensis (Smith, 1881a, Lake Tanganyika) was recognised by Mandahl-Barth (1957a). The original shells (BMNH, Fig. 100d) are strikingly different from typical B. sudanica in having strongly angular whorls, but there is intergradation between this and the typical form in a series (DBL) from a marsh near Albertville. Therefore B. tanganyicensis could be regarded as an angular form of B. sudanica evolved within the Lake Tanganyika basin. But since no similar specimens have been found in the Lake Victoria basin, it would be misleading to follow Mandahl-Barth (1957a) in identifying snails from this region also as B. s. tanganyicensis. HABITAT. Swamps and other habitats associated with lakes and rivers; B. sudanica is one of the few snails that live in papyrus swamp, where the water may lack any dissolved oxygen (Jones, 1964). Although the snail can aestivate (Goll, 1982; Betterton, 1984a) it does not occur in such small waterbodies as B. pfeifferi. Population dynamics were studied in a lake in SE Zaire by Malaisse & Ripert (1977). Distribution in the Sudan apparently increased northwards in association with spread of the water-hyacinth, Eichhornia sp. (Williams & Hunter, 1968). DISTRIBUTION (Fig. 123). North-eastern Africa. Sudan: northwards to Jebel Aulia. Common in Uganda (Mandahl-Barth, 1957a), occurring westwards to Lake Chad. Ethiopia: Lakes Zwai, Awasa and Abaya (Margherita). Kenya: Lakes Victoria, Naivasha and Jipe. Tanzania: Lake Victoria and near Arusha. N Zambia and SE Zaire. Lake Tanganyika basin and Lakes Edward and Kisale (Mandahl-Barth (1957a). Late Pleistocene-Holocene sites in Sudan, Chad and Niger (Van Damme, 1984). PARASITES. S. mansoni: although B. sudanica is commonly named as a host, reports of natural infection are few (Kinoti, 1971b, W Kenya; Magendantz, 1972, NW Tanzania; Goll, 1982, Ethiopia; Gryseels, 1985, Burundi). Laboratorybred snail stocks from Ethiopia and Tanzania showed various degrees of compatibility with parasite strains from 4 different countries (Frandsen, 1979d,f). S. rodhaini: natural infections in E Zaire (Schwetz, 1952), Uganda (Berrie & Goodman, 1962) and Burundi (Gryseels, 1985). Natural infections with 11 species of trematode cercariae found in NW Tanzania (Loker et al., 1981). Biomphalaria glabrata (Say, 1818). The major intermediate host for S. mansoni in the Neotropics. Pflüger (1982) drew attention to its use in laboratories in Africa, reported a possible occurrence in the wild near

216 SYSTEMATIC SYNOPSIS: PULMONATES

Cairo, and warned of possible colonisation of areas free from B. alexandrina. Snails identified as B. cf. glabrata were reported to have a restricted distribution in Durban (Joubert et al., 1986). The shell of B. glabrata is generally widely umbilicate and similar to B. sudanica, though it commonly reaches an even greater size (15–30 mm; Malek, 1985). B. glabrata has a vaginal pouch, not reported for any African species by earlier workers, though one is well developed in at least some species (Mello, 1972) including B. pfeifferi and B. alexandrina. The most reliable character for identification seems to be the presence in B. glabrata of a renal ridge, not observed in any African species. Helisoma tribe. A group of genera displaying high diversity in the copulatory organ, which has various types of external glandular structure. The only indigenous genus in Africa, Planorbarius, is restricted to the north-western extremity of the continent, while Helisoma is introduced. Genus Helisoma Swainson, 1840 Medium-sized discoid snails, reaching 20 mm in diameter, though in some species individuals may have a moderately raised spire; whorls rounded or angular. Prostatic tubules bunched together in a fan-like arrangement; copulatory organ with an accessory preputial organ, connected by a duct to the penis sheath (Hubendick, 1955; 1978, Fig. 205). A North American genus; at least one species has been introduced into Africa. Type species: Planorbis bicarinata Say, North America. The group Planorbella, previously recognised as a subgenus of Helisoma, has been classified as a separate genus including the species duryi by Burch (1978, 1985); I follow Madsen (1992) in maintaining the familiar use of Helisoma duryi. Helisoma duryi (Wetherby, 1879, Planorbis). Type locality: North America, Everglades of Florida. Figs 101a,b. 8×15 mm (typical form); 5×14 mm (flatter, Biomphalaria-like form); Madsen (1984) reports diameters up to 21 mm. Typical form distinguishable from a Biomphalaria by the higher shell, more angular whorls, flat surface within the umbilicus and the deeply concave upper side (Van Bruggen, 1974; Appleton, 1977b). But some specimens resemble Biomphalaria closely and Madsen (1984) found considerable overlap for all measured parameters of the shell. Therefore identification sometimes depends on anatomical characters, especially the presence in Helisoma of a preputial gland, which is obvious even in a juvenile. Some enzymes are also distinctive (Jelnes, 1982b). Helisoma has been reported as Biomphalaria at least twice (Van Bruggen, 1970b; Haller, 1974). Introduction into Africa may have occurred on several occasions and more than one species could be present.

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HABITAT. Cooling ponds of a paper-mill (Brown, 1967a); water storage reservoir (Van Bruggen, 1974); other habitats recorded for Africa are mostly ornamental pools and small dams. The first reported natural site is the Liesbeeck River in Cape Town (Appleton, 1977b). Ecological factors to which responses have been monitored in the laboratory include temperature (Aboul-Ela & Beddiny, 1980; El-Eman & Madsen, 1982), calcium ion concentration (Madsen, 1987) and sodium chloride (Madsen, 1990). There have been trials with H. duryi as a competitor of intermediate hosts for schistosomes in Egypt (reviewed by Frandsen & Madsen, 1979) and Tanzania (Madsen, 1983); for laboratory studies of competitive interactions see Chapter 8. DISTRIBUTION. Scattered localities in Africa from Egypt to Cape Town; also on islands in the Indian Ocean. Lower Egypt (Pflüger & Roushdy, 1980; Roushdy & El-Emam, 1981). Kenya: Mombasa and Nairobi (Frandsen & Madsen, 1979), Malindi (Brown, 1980a). Tanzania: Mwanza and Moshi, Arusha Chini (Frandsen & Madsen, 1979; Madsen, 1983). Further scattered sites (Frandsen & Madsen, 1979; Madsen, 1992, Table 2) in Uganda (Entebbe), Congo (Brazzaville), Zimbabwe (Harare, Chiredzi and Lake Kariba), Malawi and Zambia (Lusaka). South Africa: Natal (Brown, 1967a), Cape Point (Van Bruggen, 1974), Johannesburg and Liesbeeck River, Cape Town (Appleton, 1977b). Namibia: Spitzkoppe (Van Bruggen, 1970b, 1974) and Omaruru area (State Museum, Windhoek; collected by B.Curtis and D.Pittman, 1987). Indian Ocean islands: Zanzibar (Jelnes, 1982b), Mauritius (Frandsen & Madsen, 1979) and Réunion (Barré et al., 1982; Starmühlner, 1983, Planorbella duryi). PARASITES. H. duryi is resistant to infection by schistosomes (experimental studies reviewed by Madsen, 1992). Genus Planorbarius Froriep, 1806 Medium-sized discoid snails reaching 25 mm diameter in Europe, with high and evenly curved whorls. Copulatory organ with a small penis sheath and a large preputium containing two big glandular structures. Prostatic tubules bunched together and opening directly into the vas deferens. Two or more species occur in Europe, of which one extends into NW Africa. Type species: Helix cornea Linnaeus, 1758, Europe. Planorbarius metidjensis (Forbes, 1838, Planorbis). Type locality: Algeria, Mitidjah marsh. Fig. 101c. 7.2×16 mm (large Algerian shell). Last whorl expanding rapidly, lip nearly circular and straight in profile; when viewed from beneath the lower lip is not overlapped by the upper lip (Fig. 101c, above), whereas the upper lip shows extensively in a Biomphalaria. Numerous spiral ridges may be present. Algerian specimens are sometimes identified as P. dufouri (Graells, 1846), and some species named by Bourguignat (1864, including P. aclopus and P. euchelius) appear to differ only in size.

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HABITAT. In Morocco found in small seasonal marshes near Rabat (Gaud, 1958, p. 765) and an irrigation system (Southgate et al., 1984). DISTRIBUTION. Spain, Portugal, Morocco and Algeria (Kechemir, 1986); shells found 600 km from the coast near El Golea (Chevallier, 1969). PARASITES. S. haematobium: despite early reports of transmission by P. metidjensis in Portugal (e.g. Azevedo et al., 1948), later investigators failed to obtain normal development of the parasite in this snail (Oliveira et al., 1974; Kechemir & Combes, 1982; Southgate et al., 1984) and there is no recent evidence of transmission anywhere. S. bovis: natural transmission in Spain (Ramajo-Martin, 1972), compatibility shown experimentally with Spanish parasite isolates (Ramajo-Martin, 1978; Southgate et al., 1984) and to a somewhat lesser degree with an isolate from Sudan (Touassem & Jourdane, 1986). Subfamily Bulininae This subfamily is used here in the sense of Hubendick (1955) and defined according to the structure of the copulatory organ. A different and tentative classification (Hubendick, 1978) placed more emphasis on the structure of the gonad and arrangement of prostatic tubules, resulting in the addition of some groups from the Ancylidae. Shell small to medium-sized, reaching 25 mm in height or diameter, sinistral, either with a spire (Bulinus) or discoid (Indoplanorbis). Pseudobranch large, deeply folded (Fig. 12c) and highly vascularised. The penis (Fig. 14d) does not project freely into the penis sheath, but is a long and coiled eversible tube (the ‘ultra-penis’; Mandahl-Barth, 1957b; Hubendick, 1955, 1978, Fig. 198), attached at both the upper and lower ends of the sheath. Numerous prostatic tubules are concentrated into a compact organ. The spermatheca, egg capsule and radula resemble those of the Planorbinae. Two genera: Bulinus found mainly in Africa and Indoplanorbis of S Asia and SE Arabia (and found recently in Africa). Genus Indoplanorbis Annandale & Prashad, 1920 The single species differs from a Bulinus in its discoid shell and in minor anatomical characters (Hubendick, 1955). Indoplanorbis exustus (Deshayes, 1834, Planorbis). Type locality: marshes on the coast of Malabar (SW India). Fig. 101d. 13×25 mm. Whorls rapidly increasing, higher than wide (proportionally higher than in a Biomphalaria), strongly convex or bluntly angular. Similar to Helisoma in the shell, but lacking the conspicuous preputial gland of that snail. HABITAT. Rice estate in Nigeria and vegetation at margins of artificial lakes in Ivory Coast. DISTRIBUTION. Widespread in S and SE Asia, partly through introduction by man (Brandt, 1974). Muscat in SE Arabia (Wright & Brown, 1980; Brown &

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Fig. 101. Planorbidae. (a) Helisoma duryi; South Africa, Mandini. (b) H. duryi; Kenya, Malindi. (c) Planorbarius metidjensis; Algeria, (d) Indoplanorbis exustus; Socotra Island, West Manuto. Scale line: 5 mm.

Gallagher, 1985) and Socotra Island (Wright, 1971). Recently found, presumably introduced, in Nigeria near Lagos (Kristensen & Ogunnowo, 1987) and Ivory

220 SYSTEMATIC SYNOPSIS: PULMONATES

Coast, Yamoussoukro (Mouchet et al., 1987). PARASITES. Host for some Schistosoma species parasitic in domestic livestock in Asia. Unsuccessful experiments were made to infect a snail stock from Socotra with African schistosomes (Wright, 1971). Genus Bulinus Müller, 1781 Shell sinistral with a spire of highly varied shape and height relative to the aperture, whorls evenly curved or bluntly angular and rarely carinate. Embryonic shell punctate (with spiral rows of small pits) in all subgroups (Walter, 1962). Anatomy as for the subfamily. Highly successful in small seasonal waterbodies, and also abundant in irrigation systems and some lakes. Africa, neighbouring tropical islands, SW Asia, Arabia and Mediterranean region (Fig. 127). About 30 species: the basic revision of Mandahl-Barth (1957b, 1965) is still an essential source of reference for most species. This system was founded on characters of the shell and anatomy, particularly the shape of the mesocone on the lateral radular teeth. Data for chromosome number and molecular properties have resulted in improvements, but few of the species are yet defined entirely satisfactorily. It is convenient to divide the genus into 4 groups, whose tax onomy and biology are described further in Chapter 7. Type species: Bulinus senegalensis Müller, 1781, Senegal. For chromosome number a reference to the earliest determination is given under each species; additional references may be found in Jelnes (1985). Schistosoma haematobium is transmitted probably entirely by snail hosts of this genus. Biocca et al. (1979) subdivided Bulinus into 3 genera and named one of them Mandahlbarthia. The new generic divisions were defined morphologically and with reference to electrophoretic studies of enzymes. Brown (1981) found this classification unacceptable for reasons including the lack of clearly-defined diagnostic genus-characters, the confusion that would be caused to workers in applied malacology by changes of names, and the fact that Mandahlbarthia is a junior synonym of Isidora Ehrenberg, 1831. While accepting the synonymy, Biocca et al. (1981) emphasised their case for separating 3 genera, but this classification has not been generally adopted. 1) B. africanus group (also known as the genus or subgenus Physopsis). The characteristic shell sculpture consists of spirally arranged nodules and corrugations (Fig. 102a). Lower part of columella commonly with an oblique ridge and twisted (‘truncate’), so that the lower columellar lip is expanded at the aperture base. Most species have a renal ridge, along the ventral surface of the kidney, whereas there is no renal ridge in the other 3 species-groups. The last 4 species in the present arrangement do not have all of the group characteristics well developed and their relationships need further investigation. Africa south of the Sahara: it is remarkable that the Late Pleistocene-Holocene distribution known

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for this group (Van Damme, 1984) does not anywhere extend significantly further north than the present range. Chromosome number: 2n=36. Bulinus africanus (Krauss, 1848, Physopsis). Type locality: South Africa, Port Natal (Durban). Fig. 103a. 24.5×13.4 mm. Spire moderately high, with spiral rows of small nodules on the upper whorls; columellar ridge well-developed; lower columellar lip twisted and reflected. Shell and other morphological features of snails from near the type locality described by Van Aardt & Van Eeden (1969). Morphometric analysis of the shell discriminated B. africanus from related species in eastern Africa, though no simply-defined diagnostic character emerged (Kristensen et al., 1987). The separation of a northern subspecies B. a. ovoideus (Bourguignat, 1879; Mandahl-Barth, 1957b, 1965) does not now seem justifiable. B. globosus has a similar shell, but the two species seem to differ in the penis sheath, which in africanus is bigger, being longer and/or thicker than the preputium (Mandahl-Barth, 1957b; Brown, 1966). But intermediate individuals are reported, for Angola (Wright, 1963a) and Zambia (Mandahl-Barth, 1968a; Hira, 1974) and further comparative studies are needed, giving attention to the effects of parasitism and fixation on the copulatory organ. A difference from B. globosus was observed in the perivitelline fluid proteins from the egg (HamiltonAtwell & Van Eeden, 1981a). In some enzymes and in certain geographical areas B. africanus differs from related species (Jelnes, 1979a; Rollinson & Southgate, 1979). Chromosome number: 2n=36 (Burch, 1967a). HABITAT. Common in streams and small dams, where the water is more permanent than in habitats characteristic for B. nasutus (McCullough et al., 1968; Brown, 1975b), yet the 2 species may occur together (Jelnes, 1979a). During drought a natural population declined in relation to increasing salinity (Pretorius et al., 1982). B. africanus was rarely successful in irrigation schemes in Tanzania (Sturrock, 1964, 1965a). Inhabiting cooler climatic areas in southern Africa than B. globosus, which alone occurs in the warmer parts (Brown, 1966; Appleton, 1977c, 1980); reports of B. africanus from such areas (e.g. Pretorius et al., 1975) seem to be based on misidentification. In the laboratory, adequate growth was restricted to the temperature range 20– 26° C (Pretorius et al., 1979); Joubert et al. (1984, 1986) showed that B. africanus could withstand cold better than B. globosus and the latter survived longer at high temperatures. Other laboratory investigations include studies on behaviour rhythms (Morgan & Last, 1982), influence of salinity in coastal lagoons (Donnelly et al., 1983), breeding behaviour (Rudolph & Bailey, 1985), respiration and desiccation (see Chapter 10). DISTRIBUTION (Fig. 124). Eastern and southern Africa; scattered distribution, unclear for many areas, where critical comparison with B. globosus is needed. Ethiopia: Jimma, Lake Tana and NE of Gondar. Kenya: near Lake Victoria (Brown, 1975b) and between Nairobi and Embu (Brown et al., 1981). Uganda: westwards to Arua (Mandahl-Barth, 1954a). Tanzania: Mwanza district

222 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 102. Planorbidae. Apical shell surface, (a) Bulinus nasutus; Kenya, Ramisi (periostracum removed), (b) B. natalensis; South Africa, Pietermaritzburg (periostracum removed), (c) Amerianna carinata; Nigeria, Ibadan (with periostracum). Scale line: 0.1 mm.

(Webbe, 1962b; McCullough et al., 1968) and near Iringa (Sturrock, 1964). E

FRESHWATER SNAILS OF AFRICA 223

Zaire: from Shaba to the Lake Albert region (Danish Bilharziasis Laboratory, 1982). Zambia: Lake Bangweulu region (Mandahl-Barth, 1968a), Lusaka area (Hira, 1974, but needing confirmation) and Lake Kariba (Hira, 1970a, also doubtful). Mozambique; northern provinces (BME). Zimbabwe: near Harare (DBL). South Africa and Swaziland: B. africanus is widespread in Natal except for the northern coastal plain (where B. globosus occurs; Brown, 1966); it is reported from as far south as Humansdorp (Fig. 124); and seems to extend westwards down the Vaal Basin (‘Physopsis’ sp. of Van Eeden et al., 1965; Van Eeden & Combrinck, 1966; B. africanus of Joubert et al., 1984, 1986). Reports for Lesotho (Basutoland) (Connolly, 1939) and Namibia (Connolly, 1939; Doumenge et al., 1987) have not been confirmed. No member of the B. africanus group is found in the Orange River below the Vaal confluence (De Kock et al., 1974). PARASITES. S. haematobium: it is difficult to assess the importance of B. africanus as a host by itself, because it is sometimes sympatric with other potential intermediate hosts. Reported as an actual or likely host in Tanzania (Sturrock, 1964), W Kenya (Kinoti, 1971a), Lake Kariba and Lusaka (Hira, 1970b, 1974; though identification doubtful). B. africanus is undoubtedly responsible for some transmission in Natal, South Africa (Donnelly et al., 1984). Snail stocks from Durban and Tanzania were highly compatible with a parasite isolate from Zambia (Frandsen, 1979c). S. bovis: natural transmission in W Kenya (Southgate & Knowles, 1975a), NW Tanzania (Southgate et al., 1980) and NE Zaire (Chartier et al., 1990). Extensive experimental infections (Kinoti, 1964; Howaldt & Armstrong, 1969; Wright et al., 1972; Southgate et al., 1980; Mutani et al., 1983). S. mattheei: natural transmission in SW Transvaal (Joubert et al., 1987) and successful experimental infection (Kinoti, 1964; Wright et al., 1972). S. intercalatum: experimental infection with the parasite from Zaire (Frandsen, 1979a). S. leiperi: experimental infection (Southgate et al., 1981). Bulinus nasutus (Martens, 1979, Physopsis). Type locality: Tanganyika, Bagamoyo. Figs 103b,c. 25×12 mm. Shell similar to B. africanus, but completing about one whorl more; spire generally higher and more slender; the entire surface may be covered by spiral rows of nodules (Fig. 102a); lip well expanded below the columella and sometimes spout-like. The typical form has the spire only about half as high as the aperture (Fig. 103c); snails with a much taller spire, sometimes more than the height of the aperture (Fig. 103b) were named subspecies B. n. productus by Mandahl-Barth (1960, from Lake Kyogo at Bugondo). Morphometric analysis of the shell discriminated B. nasutus from related species in eastern Africa, and indicated that the form productus might be a distinct species (Kristensen, 1986b; Kristensen et al., 1987). Penis sheath smaller in proportion to the preputium than in B. africanus, but Pringle et al. (1971) found it significantly bigger than in B. globosus of NE Tanzania.

224 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 103. Bulinus. (a) B. africanus; South Africa, Avoca near Durban, (b) B. nasutus (form productus); Kenya, Kano Plain, (c) B. nasutus (typical form); Kenya, Kano Plain, (d) B. ugandae; Kenya, Kisumu. (e) B. jousseaumei; Gambia, Diabugu Bolon. (f) B. abyssinicus; Ethiopia, Assaita. (g) B. globosus; Angola, Rio Lifune in Luanda Province. Scale line: 10 mm.

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Enzyme analyses supported the distinction between nasutus and globosus, and showed differences between productus and the typical form (Rollinson & Southgate, 1979). A difference between nasutus and africanus was observed in W Kenya (Jelnes, 1979a). B. praeclara (Bourguignat, 1879) may have priority as a name for the typical form of B. nasutus (Verdcourt, 1965), but it seems advisable to retain the betterknown name. Chromosome number: 2n=36 (Burch, 1967a). HABITAT. Seasonal waterbodies, some drying out for about 5 months (Webbe & Msangi, 1958; McCullough et al., 1968; Pringle et al., 1971). Uncommon in irrigation schemes (Sturrock, 1965a). Most abundant in ditches and borrow-pits in W Kenya (Brown, 1975b). DISTRIBUTION (Fig. 125). East Africa (Mandahl-Barth, 1965). B. n. nasutus: SE Kenya (Kitui and the coastal area), southwards in coastal Tanzania to Tunduru, and westwards to Mbarali in the southern highlands. B. n. productus: Lango district of Uganda and eastwards in an area extending around the E shore of Lake Victoria to Shinyanga in Tanzania. PARASITES. S. haematobium: B. nasutus is the main intermediate host in NW Tanzania (Webbe, 1962b), though McCullough et al. (1968) found a smaller proportion infected than of the rarer species B. africanus. Similar prevalences of infection in both species were observed near Mwanza (Loker et al., 1981). Natural infections are reported also for Uganda (Cridland, 1955) and W Kenya (Kinoti, 1971a). B. nasutus seems likely to play a part in transmission in the coastal areas of Kenya and Tanzania, but it appeared to be incompatible with a parasite strain borne locally by B. globosus in SE Tanzania (Zumstein, 1983). S. bovis: compatibility is doubtful as natural infection is unknown and experimental infection has proved negative (Kinoti, 1964; Mwambungu, 1988) or positive only for a snail stock of uncertain identification (Southgate & Knowles, 1975a). Echinostome spp.: natural infections observed in NW Tanzania by Loker et al. (1981). Bulinus abyssinicus (Martens, 1866a, Physa). Type locality: ‘southern Abyssinia’. Fig. 103f. 14×9 mm. Whorls with a characteristic shoulder near the suture; aperture narrow; upper whorls with irregular corrugated microsculpture, otherwise smooth. Two names believed to be synonyms were given to shells from the lower Awash River region (Physopsis meneliki and P. soleilleti of Bourguignat, 1885a). Chromosome number: 2n=36 (Jelnes, 1985). HABITAT. Marshes associated with the lower Awash River in Ethiopia, but not the irrigation systems (Brown & Lemma, 1970; Kloos & Lemma, 1974). In irrigation channels of sugar estates in Somalia (Arfaa, 1975), but more frequent in pools and marshes with aquatic plants (Shunzhang & Hongming, 1980;

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Upatham et al., 1981). High capacity for population increase in the laboratory suggested adaptation to unstable environments (Ahmed et al., 1986). DISTRIBUTION (Fig. 124, areas 8 and 9). Somalia: Shebeli and Giuba River basins, and lakes near the Kenyan border (Mandahl-Barth, 1960; Maffi, 1960; Arfaa, 1975; Upatham et al., 1981). Ethiopia: marshes near the Awash River from Assaita upstream to Lake Lyadu (Brown & Lemma, 1970; Kloos et al., 1977). PARASITES. S. haematobium: transmission in Somalia, mainly in the Webbi Shebeli valley and the southern part of the Giuba valley (Arfaa, 1975; Upatham et al., 1981). Bulinus globosus (Morelet, 1866, 1868, Physa). Type locality: Angola, Dande River (Luanda Province). Fig. 103g. 22.5×14 mm. Shell like B. africanus, but copulatory organ with smaller penis sheath, being usually shorter and narrower than the preputium (Mandahl-Barth, 1957b; Brown, 1966). Walter (1968) gave a comprehensive morphological description. In respect of the copulatory organ some populations appear intermediate with B. africanus (see under that species). Morphometric analysis of the shell distinguished a taxon B. globosus from related species in eastern Africa (Kristensen et al., 1987) and W Africa (Kristensen & Christensen, 1989), but we are far from understanding this as a biological species. The existence in W Africa of different forms has long been postulated, with reference to variation in snail size (Hira, 1968a) and radula tooth size (Kuma, 1979). Two populations differing in compatibility with Schistosoma also differed in the form of the copulatory organ (Betterton, 1984a; Fryer et al., 1987). Enzymes vary among populations (Wright & Rollinson, 1979; Dogba & Jelnes, 1985); loci used as genetic markers indicated cross-breeding between two morphologically different populations (Fryer et al., 1987). Enzymic data (Rollinson & Southgate, 1979) supported the discrimination between B. globosus and B. nasutus in NE Tanzania, and between B. globosus and B. umbilicatus in W Africa (Jelnes, 1986). Unfortunately discrepancies have arisen between identifications according to enzymes (Jelnes, 1991) and morphometry (Kristensen & Christensen, 1991). Chromosome number: 2n=36 (Natarajan et al., 1965). HABITAT. Various waterbodies including streams (Paperna, 1968; Kuma, 1979; Marti et al., 1985; Coulibaly & Madsen, 1990), rivers (Mandahl-Barth et al., 1974; Noda et al., 1988; Woolhouse & Chandiwana, 1990a,b), seasonal pools (Betterton, Ndifon et al., 1988), lakes (Cantrell, 1981; Appleton, 1977c), earth dams (Tayo & Jewsbury, 1978; O’Keeffe, 1985a), irrigation systems (Logan, 1983; Betterton, 1984a) and older rice-paddies (Dennis et al., 1983). The snail usually lives in shallow water, where it may occur on bare substrata, but is more common among aquatic plants (Thomas & Tait, 1984). Favoured by moderate organic pollution (Smith, 1982) and tolerant of deep shade (Ndifon & Ukoli, 1989). A wide range of calcium carbonate concentration is tolerated

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(Williams, 1970a). Being so ecologically versatile it is surprising that B. globosus has failed to colonise the man-made Lake Volta (Odei, 1972; Doumenge et al., 1987). Climatic temperature seems to be important among factors influencing distribution. The snail is absent from areas that are too cool (Brown, 1966); optimum temperature is about 25°C (Chapter 10). Temperature above 28°C is also unfavourable (O’Keeffe, 1985a), though B. globosus is better adapted than B. africanus to higher temperature (Joubert et al., 1984, 1986). Other experimental studies have been made of responses to desiccation (Hira & Muller, 1966; Odei, 1967; Cridland, 1967; Diaw et al., 1988; Woolhouse & Taylor, 1990), turbidity (Harrison & Farina, 1965), varying oxygen tension (Van Aardt & Frey, 1979, 1981) and of dispersal by drifting (Marti & Tanner, 1988; Woolhouse, 1988). Field and experimental investigations of growth, life cycle and population dynamics are described in Chapters 10 and 11 (e.g. O’Keeffe, 1985a,b; Marti, 1986; Woolhouse & Chandiwana, 1989, 1990a,b). There have been studies of mating behaviour (Kuma, 1975; Rudolph, 1979, 1983; Rudolph & Bailey, 1985) and self-fertilisation (Jarne, Finot et al., 1991). Mating system (whether selfing or outcrossing; Chapter 7) varies among populations (Njiokou, Bellec et al., 1992); analysis is aided by DNA fingerprinting (Jarne, Delay et al., 1990, 1992). DISTRIBUTION (Fig. 124). B. globosus has the greatest range of any member of its species-group, occupying much of Africa south of the Sahara. Northern limits lie in S Sudan (Brown et al., 1984), Lake Chad (Betterton, 1984a), the middle Niger Basin (Madsen et al., 1987) and the Senegal Basin (Diaw, 1980; Malek & Chaine, 1981). Southern limits are the Okavango Delta (Brown, Curtis et al., 1992) and the warmer part of the coastal plain of eastern South Africa (Brown, 1966). PARASITES. S. haematobium: although an important intermediate host in many areas, the part played by B. globosus locally depends on the presence of a compatible parasite strain. In W Africa the parasite may develop best in either B. globosus or in B. truncatus (=rohlfsi) (McCullough, 1959, and later authors including Betterton et al., 1988). Variation in prevalence of infection in snail populations can be related to nutritional conditions (O’Keeffe, 1985a), snail age (Woolhouse, 1989), season and habitat (Chandiwana et al., 1987; Noda et al., 1988; Woolhouse & Chandiwana, 1989; Okafor, 1990a). Other schistosomes transmitted naturally by B. globosus or which were compatible with the snail in experiments: S. bovis: Southgate & Knowles, 1975a,b; Diaw & Vassiliadès, 1987; Mwambungu, 1988; Ndifon et al., 1988. S. curassoni: Diaw & Vassiliadès, 1987. S. intercalatum: Wright et al., 1972; Frandsen, 1979a; De Clercq, 1987. S. leiperi: Pitchford, 1976, ‘Physopsis’ sp.; Southgate et al., 1981. S. mattheei: Wright et al., 1972; Mahon & Shiff, 1978; Kruger et al., 1990, ‘B. africanus’.

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Natural infections with other trematode species were fewer than in other species of snail in NW Tanzania (Loker et al., 1981). Bulinus jousseaumei (Dautzenberg, 1890, Isidora). Type locality: Senegal River near Medine. Fig. 103e. 11×8 mm. Regarded by Mandahl-Barth (1957b, 1965) as a distinct species, small with both the columellar ridge and microsculpture only weakly developed, but treated by Wright (1957, 1961) as only a form of B. globosus. The question is still open; recently jousseaumei was recognised as distinct according to shell morphometry (Kristensen & Christensen, 1989, 1991), but reduced to a synonym of globosus on the evidence of enzyme analyses (Jelnes, 1986, 1991). Chromosome number: 2n=36 (Jelnes, 1986). HABITAT. Comparatively permanent streams (bolons) in Upper Gambia (Smithers, 1956); absent from the temporary pools where B. senegalensis is abundant. DISTRIBUTION. In the Sahel and dry savanna zone (Sellin et al., 1980) from the lower Senegal River Basin (Diaw, 1980; Malek & Chaine, 1981) eastwards to Niger (Sellin et al., 1980). PARASITES. S. haematobium: natural transmission in the Gambia (Smithers, 1956) and Senegal Delta (Chaine & Malek, 1983), and successful experimental infections (Albaret et al., 1985). S. curassoni: natural transmission in Senegal (Albaret et al., 1985). Bulinus ugandae Mandahl-Barth, 1954 (B. globosus ugandae); 1957b, 1965 (B. ugandae). Type locality: Uganda, Jinja Bay, Lake Victoria. Fig. 103d. 15×11 mm. This species like B. jousseaumei shows only weak development of a columellar ridge and microsculpture, and similarly its separation from B. globosus is questionable. Continuous variation appeared to connect these taxa in southern Sudan (Brown et al., 1984), but B. ugandae from Lake Victoria is smaller and darker than local populations identified as B. globosus. One reason for treating B. ugandae as distinct (Mandahl-Barth, 1957b, 1965) was its resistance to infection by S. haematobium, and further experiments to confirm this are desirable. Little success was achieved in more recent attempts to characterise B. ugandae by means of enzyme analysis (Jelnes, 1979a; Wright & Rollinson, 1979; Archer, 1988) and shell morphometrics (Kristensen, 1986c; Kristensen et al., 1987; Archer, 1988). Chromosome number: 2n=36 (Burch, 1960). HABITAT. Papyrus swamp in or near Lake Victoria (Berrie, 1964); found by myself beneath stones on beaches. DISTRIBUTION. Lake Victoria, Lake Mutanda and other localities in Uganda (Mandahl-Barth, 1957b), S Sudan (Malek, 1958) and Ethiopia (Brown, 1965). PARASITES. S. haematobium: no evidence for natural transmission and snails were resistant to experimental infection (Cridland, 1955; Southgate & Knowles, 1977a). S. bovis: natural transmission in Uganda (Berrie, 1964) and Sudan (Malek, 1969), but apparently not in western Kenya (Southgate & Knowles, 1975b),

FRESHWATER SNAILS OF AFRICA 229

Fig. 104. Bulinus. (a) B. umbilicatus; Sudan, Abu Duloh. (b) B. umbilicatus; Sudan, Zalingei. (c) B. obtusispira; Madagascar, lower Mangoky region, (d) B. obtusus; Chad (paratype, BMNH1993.071). (e) B. hightoni; NE Kenya (holotype, BMNH1978.108). (f) B. hightoni; NE Kenya, Alango Gorani. Scale line: 6.5 mm (d,e) or 10 mm (a–c).

although the snail and parasite were highly compatible in the laboratory (Southgate & Knowles, 1975a, Table 18). Natural infections with 5 other trematode species were observed in NW Tanzania (Loker et al., 1981). Bulinus obtusus Mandahl-Barth, 1973b. Type locality: Chad, Goz Beida. Fig. 104d.

230 SYSTEMATIC SYNOPSIS: PULMONATES

9.2×6.2 mm. Comparatively small with an obtuse apex and a weak columellar ridge; apical whorls with delicate corrugation. Lateral tooth with long slender cusps. Chromosome number unknown. DISTRIBUTION (Fig. 125). Chad: Goz Beida, Fort Lamy, Brumbe, Ouarai, Boum Kabir (Mandahl-Barth, 1973b). Bulinus obtusispira (Smith, 1882, Physa). Type locality: Madagascar, about 32 km from Tananarive. Fig. 104c. 8.8×6.5 mm. Once confused with B. liratus (see B. truncatus/tropicus complex), but differing in the more obtuse apex, more broadly reflected columellar lip and other characters (Wright, 1971; Degrémont, 1973, p. 68). Foot pointed posteriorly rather than rounded (Moyroud et al., 1983). Electrophoretic observations have been reported for egg proteins (Saladin et al., 1976) and enzymes (Jelnes, 1984). Although this snail lacks a columellar ridge, nodular sculpture and a renal ridge, the egg proteins indicated affinity with the B. africanus group (Wright, 1971; Brown & Wright, 1978). The relationships of this interesting species need further investigation. Chromosome number: 2n=36 (Wright, 1971). HABITAT. Common in rice-fields and capable of aestivation for at least 7 months (Degrémont, 1973); ecology reviewed by Moyroud et al. (1983). DISTRIBUTION. Madagascar: widespread in the West (Brygoo, 1968; Wright, 1971; Degrémont, 1973; Moyroud et al., 1983). PARASITES. S. haematobium: the finding of snails naturally infected led to the recognition of B. obtusispira as a distinct species, compatible also with the parasite from Mauritius (Wright, 1971) as well as in Madagascar (Brygoo & Moreau, 1966; Degrémont, 1973; Moyroud et al., 1983). S. bovis: experimental infection was unsuccessful (Southgate & Knowles, 1975b). Bulinus umbilicatus Mandahl-Barth, 1973b. Type locality: W Sudan, Darfur Province, Zalingei. Figs 104a,b. 16×11 mm (to 20 mm high). Whorls convex, sometimes shouldered; columellar lip broadly reflected but umbilicus large; columellar ridge weak and often not extending to the margin of the lip. Renal ridge present in only some individuals (Mandahl-Barth, 1973b). An exceptionally large size is reached by shells from Abu-Duloh in Sudan (BMNH, Fig. 104a) identified as B. truncatus by Connolly (1941). Membership of the B. africanus group is supported by properties of the egg proteins (Wright, 1977; Brown & Wright, 1978) and enzymes (Wright & Rollinson, 1979; Jelnes, 1986). In West Africa there is an intergradation in shell form between B. umbilicatus and B. globosus; electrophoresis of enzymes (Jelnes, 1986) and shell morphometry (Kristensen & Christensen, 1989) produced discrepancies in identification (Jelnes, 1991; Kristensen & Christensen, 1991). Further study of this taxonomic complex is needed. Chromosome number: 2n=36 (Jelnes, 1985).

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HABITAT. Large shells from Abu-Duloh, Sudan (BMNH) are labelled ‘from a rainwater pool’. Albaret et al. (1985) described pools in Senegal, which though extensive were liable to drying; snails can survive dry periods of 6–8 months (Diaw et al., 1988, 1989). DISTRIBUTION (Fig. 125). Sudan, Chad, Nigeria, Mali, Niger and Mauritania (Mandahl-Barth, 1973b; Tager-Kagan, 1977; Brown, 1980a). Further localities in Sudan, Mali, Senegal and possibly Gambia (Jelnes, 1986; Diaw & Vassiliadès, 1987; Kristensen & Christensen, 1989). PARASITES. S. haematobium: natural transmission in Senegal (Albaret et al., 1985). S. curassoni: natural and experimental infections (Albaret et al., 1985; Southgate et al., 1985; Diaw & Vassiliadès, 1987). S. bovis: low compatibility in experiments (Southgate et al., 1985). Bulinus hightoni Brown & Wright, 1978. Type locality: NE Kenya, a seasonal pool (Orma Kote) near Hola, on the western side of the Tana River. Figs 104e,f. 4.8×3.6 mm (holotype); to 9 mm high. Small, columellar lip rather broadly reflected, with or without a low ridge; umbilicus widely open; surface with spiral grooves and wavy ribs, which may bear low lamellae of periostracum (unusual for the B. africanus group). Renal ridge lacking, but immunological reactions of egg proteins (Brown & Wright, 1978) supported classification in the africanus group. B. obtusus is less strongly sculptured and has the columellar margin narrower, while B. umbilicatus grows much larger and has a smoother surface. Chromosome number: 2n=36 (Brown & Wright, 1978). HABITAT. Shallow depressions filled seasonally by rain, with aquatic plants including water-lilies; the only other snail found was B. forskalii. DISTRIBUTION (Fig. 125). NE Kenya: near Hola on the lower Tana River. PARASITES. Compatible in experimental infections with S. haematobium, S. intercalatum and S. leiperi: Brown & Wright (1978), Southgate et al. (1981). 2) B. truncatus/tropicus complex (comprising the B. truncatus and B. tropicus groups of Mandahl-Barth, 1957b; see Chapter 7). Shell lacking nodular or corrugated sculpture (as it is in the B. africanus group) and usually with ribs (Fig. 102b); spiral ridges and grooves only weakly developed; columella lacking a ridge, though the lower columellar lip is twisted and quite broadly reflected in some species (Fig. 109). ‘Mesocone’ refers here to the middle cusp of the first lateral radula tooth; its shape shows continuous variation (Fig. 105) between extreme forms known as ‘angular’ and ‘non-angular’ (or ‘arrowhead’ and ‘triangular’) (Brown, 1982). Renal ridge absent. Aphallic individuals (lacking the copulatory organ) occur in some species. If a genus-name is to be used for this group it should be Isidora Ehrenberg, 1831 (for I. hemprichi), of which Mandahlbarthia Biocca et al., 1979 is a synonym (Brown, 1981). Chromosome numbers: 2n=36 (most species), 72 (permembranaceus, truncatus), 108 (hexaploidus) and 144 (octoploidus).

232 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 105. Bulinus natalensis and B. tropicus. Variation in the mesocone of the first lateral tooth (after Oberholzer et al., 1970, Fig. 14): (a–g) were classified as angular, (h–j) as intermediate and (k–o) as non-angular.

Bulinus angolensis (Morelet, 1866, Physa). Type locality: Angola, district of Duque de Braganza. Figs 106a,b. 14×11 mm. Typical shell (Fig. 106a) low-spired, with strongly convex whorls. Spire more prominent in B. welwitschi (Morelet, 1866) (Fig. 106b), which may be a synonym (Mandahl-Barth, 1957b under B. tropicus and 1965 under B. natalensis; Wright, 1963a). The proper treatment for both of Morelet’s species is unclear, partly because their chromosome number and molecular properties are unknown. Nor is it certain that they were represented by materials studied

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Fig. 106. Bulinus. (a) B. angolensis; Angola (syntype, BMNH1893.2.4.618–20). (b) B. welwitschi; Angola, Benguela, Bumbo River (syntype, BMNH1893.2.4.615–17; see B. angolensis). (c) B. depressus; South Africa, Nylstroom. (d) B. liratus; Madagascar, lower Mangoky region, (e) B. nyassanus; Lake Malawi (syntype, BMNH1877.9.28.27). (f) B. succinoides; Lake Malawi, Monkey Bay. (g) B. truncatus; Senegal, Richard Toll. Scale line: 6.5 mm (c) or 10 mm (a,b,d–g). (a) and (b) from Wright (1963a, Pl. 6).

morphologically (Wright, 1963a; Oberholzer, 1970). Both authors described the mesocone as angular, but while Wright found about one-third of individuals aphallic, none were reported by Oberholzer. B. angolensis of Leloup (1953) from Lake Tanganyika is very likely B. truncatus according to investigation of chromosome number (Brown et al., 1982). Neither of Morelet’s names seems applicable to snails from the Okavango River and East Caprivi (Brown, Curtis et al., 1992). B. parietalis (Mousson, 1887, from Ovamboland) was regarded as a synonym of B. angolensis by Mandahl-Barth (1965), yet a detailed study by Oberholzer (1970) suggests it could be distinct. Chromosome number: unknown.

234 SYSTEMATIC SYNOPSIS: PULMONATES

HABITAT. Streams or pools in streambeds with aquatic vegetation (Wright, 1963a; Oberholzer, 1970). DISTRIBUTION. Angola: N and S plateaux (Wright, 1963a), Mossamedes area (B. welwitschi). Namibia: streams draining into Etosha Pan (Oberholzer, 1970). PARASITES. Not reported to transmit any schistosome. Bulinus coulboisi (Bourguignat, 1888, Physa). Type locality: W shore of Lake Tanganyika, in small pools. Previously kept distinct (Mandahl-Barth, 1965; Brown 1980a) but treated herein under B. truncatus, to which it conforms in its tetraploid chromosome number and other characters (Brown et al., 1982). Bulinus depressus Haas, 1936 (B. hemprichii depressus). Type locality: Zambia, canal flowing from the village of Nsombo to Lake Bangweulu. Fig. 106c. 6.5×5 mm (original description); 11×8 (South African shell). The shells described by Haas were small, low-spired, with a narrowly reflected columellar lip and membranous ribs. Having seen similar snails from Zambia with a nonangular mesocone, Mandahl-Barth (1968a) regarded depressus as a subspecies of B. tropicus. However, South African snails identified as B. depressus by Van Eeden et al. (1965) were found to have a strongly angular mesocone and to be often aphallic (Schutte, 1966; Brown et al., 1967, samples 44, 45; HamiltonAtwell & Van Eeden, 1969). Electrophoresis of proteins from the egg (HamiltonAtwell, 1976) yielded a single-banded main fraction consistent with the diploid chromosome number. B. depressus as known from South Africa is similar to B. natalensis, though more frequently aphallic; whether or not it is correct to use the first name for such snails can only be decided when the nature of Haas’s depressus becomes more fully known from study of representative specimens from the type locality. Chromosome number: 2n=36 (Schutte, 1966; South African snails). HABITAT. Rivers, pools (dembos) and lakes (Mandahl-Barth, 1968a); temporary marsh (Mandahl-Barth et al., 1972). Cement-lined reservoir, earth dams and river (Schutte, 1966; Hamilton-Atwell & Van Eeden, 1969). DISTRIBUTION. Zambia: Lake Bangweulu region (Mandahl-Barth, 1968a). SE Zaire (Mandahl-Barth et al., 1972). South Africa: N Transvaal and westwards down the basins of the Vaal and Orange rivers (De Kock et al., 1974). Namibia: Okavango River and East Caprivi (Brown, Curtis et al., 1992). PARASITES. Snails from N Transvaal were not susceptible to infection with either S. haematobium or S. mattheei from SE Transvaal (Schutte, 1966). Bulinus guernei (Dautzenberg, 1890, Isidora). Type locality: Senegal, marshes near Tuabo. Previously kept distinct (Mandahl-Barth, 1965; Brown, 1980a), but treated herein under B. truncatus, to which it conforms in its tetraploid chromosome number and other characters (Brown, Shaw et al., 1986; Jelnes, 1986).

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Bulinus hexaploidus Burch, 1972. Type locality: Ethiopia, Sululta ‘river’, a small stream about 24 km (15 miles) N of Addis Ababa on the road to Debra Markos. Figs 107d–f. 14.5×9.5 mm. Spire moderately high; columella concave or straight; umbilicus open. Mesocone angular to intermediate shape; not aphallic (Brown & Wright, 1972). Wu (1972) gave a detailed morphological description of snails from one locality. Chromosome number: 2n=108 (Brown & Burch, 1967). HABITAT. Streams flowing through grassland, with abundant aquatic vegetation in the residual pools that persist through the dry season. DISTRIBUTION. Ethiopia: the highland plateau north of Addis Ababa (Brown & Wright, 1972). Bulinus liratus (Tristram, 1863, Physa). Type locality: Madagascar, W of Tananarive. Fig. 106d. 14.6×10.7 mm (to 17 mm high). Formerly confused with B. obtusispira (see B. africanus group), but differing in the more pointed apex and less broadly reflected columellar lip; foot rounded posteriorly rather than pointed (Moyroud et al., 1983). There are further differences from B. obtusispira in enzymes (Jelnes, 1984). The morphological account of B. liratus by Starmühlner (1969) should be treated with caution because the material possibly included B. obtusispira. B. liratus resembles B. tropicus in the shell, lack of aphally, diploid chromosome number and egg proteins (Wright, 1971; Saladin et al., 1976). The later named B. liratus Craven (1880, South Africa) is a form of B. tropicus. Chromosome number: 2n=36 (Wright, 1971). HABITAT. Various waterbodies including irrigation channels and showing a higher tolerance than B. obtusispira of salinity (Degrémont, 1973). DISTRIBUTION. Madagascar: apparently common, particularly in the central and SE regions (Brygoo, 1965, 1968; Starmühlner, 1969) though probably some records refer to B. obtusispira. PARASITES. S. haematobium: B. liratus proved resistant to experimental infection and plays little part if any in natural transmission (Brygoo & Moreau, 1966; Wright, 1971; Degrémont, 1973). Calicophoron (Paramphistomum) microbothrium: natural infection in Madagascar (Prod’hon et al., 1968). Bulinus natalensis (Küster, 1841, Physa). Type locality: South Africa, streams in the Umgeni Valley (Natal Province). Fig. 108. 9.6 ¥ 8.5 mm (depressed form); 9.5 ¥ 6.5 (high-spired form), rarely to 13 mm high. Shell commonly low-spired, though variable, with the columella twisted to some degree; mesocone frequently angular; some individuals aphallic. Distinguished early in modern studies (Mandahl-Barth, 1965) as a southern species with an angular mesocone like the northern B. truncatus, but later found to be diploid rather than tetraploid (as is truncatus). B. natalensis is in fact closely related to B. tropicus in respect of molecular properties (Brown et al.,

236 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 107. Bulinus from Ethiopia, (a–c) B. truncatus: (a) Wonji irrigation scheme; (b) Lake Abaya (Margherita); (c) Lake Tana at Bahr Dahr. (d–f) B. hexaploidus; Sululta, north of Addis Ababa, (g–i) B. octoploidus; Sululta and Ambo districts. Scale line: 5 mm. Shells first figured by Brown & Wright (1972, Pls 2–4).

1971a,b; Brown, Schutte et al., 1967; Burch & Lindsay, 1971; Hamilton-Atwell, 1976; Wright & Rollinson, 1981).

FRESHWATER SNAILS OF AFRICA 237

Shells from populations identified as B. natalensis are highly varied; the form described by Küster has a moderately high spire and slightly twisted columella (Fig. 108a). This form intergrades in one direction with B. tropicus, in which the spire is higher and the columella evenly curved, and in the direction of decreasing spire height and increasing columellar twisting (Figs 108b–d) with B. zuluensis (Melvill & Ponsonby, 1903). The spire is most consistently depressed in lacustrine populations (Figs 108d,e). The mesocone is angular, especially in lacustrine populations, e.g. Lake Sibaya (Oberholzer et al., 1970; Brown, 1982) and mesocone shape provided the basis for distinguishing between natalensis and tropicus in SE Africa (Brown et al., 1971b; Shaw & Brown, 1986). However, variation in mesocone shape is continuous and it was difficult to decide which name to use for some populations in Kenya (Brown et al., 1991). Evidently the status of B. natalensis needs further investigation. Crossfertilisation with B. tropicus was achieved experimentally (Brown & Wright, 1972; Wu, 1972). Although karyotype studies (Goldman et al., 1980, 1984) showed differences from B. tropicus, the B. natalensis stock used was not described morphologically, and being from eastern Transvaal it was not necessarily representative of B. natalensis of Natal. Relationships need to be clarified also between B. natalensis and B. depressus as described from South Africa, which is likewise diploid and similar in morphology, though aphally is much commoner. Chromosome number: n=18–21 (Burch, 1963, 1964); n=18–21, 2n=36 (Brown et al., 1967, 1971a). HABITAT. Various waterbodies including small pools, slowly flowing rivers, lakes and tentatively identified from crater lakes in Cameroon (Mimpfoundi & Greer, 1990c). Living in the weedbed zone of Lake Sibaya down to a depth of 7 m (Boltt, 1969; Appleton, 1977c). B. natalensis is less tolerant of cool climate than B. tropicus according to its more limited distribution in SE Africa (Brown et al., 1971b). DISTRIBUTION. Mainly in eastern Africa (Mandahl-Barth, 1965) from Ethiopia (Lakes Zwai and Awasa; Brown & Wright, 1972) to the coastal region of Natal. Cameroon: diploid populations like B. natalensis found in western crater lakes (Mimpfoundi & Greer, 1990c) are separated by over 2000 km from the main range. PARASITES. S. haematobium: natural transmission by B. natalensis is unknown, but low infection rates were achieved in experiments with snails from Lake Sibaya (Lo et al., 1970). Further, moderate-to-high compatibilities were observed for other diploid snails, possibly B. natalensis, from Zimbabwe (Mandahl-Barth et al., 1976) and Ethiopia, Lake Awasa (Frandsen, 1979a,e, as diploid ‘B. truncatus’). S. bovis: natural infections in Ethiopia of diploid snails possibly B. natalensis (Graber & Daynes, 1974; discussion in Southgate et al., 1989, p. 389).

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Bulinus nyassanus (Smith, 1877, Physa). Type locality: Lake Nyasa (Malawi). Fig. 106e. 13.6×10.8 mm. Shell thick-walled, globose, with the pointed apex scarcely projecting above the last whorl; umbilicus widely open; a comparatively thinshelled form obtained from greater depth deserves consideration as a distinct species (Wright et al., 1967; Mandahl-Barth, 1972). Mesocone of shallow-water form more slender and sharply pointed than mesocone of deep-water form; also differences in enzymes observed (Wright et al., 1967). Chromosome number: 2n=about 36 (Wright et al., 1967, p. 206). HABITAT AND DISTRIBUTION. Lake Malawi: coarse substrata on the SW shore at depths of 1.5–15 m and ‘deep-water form’ dredged from 95 m (52 fathoms; Wright et al., 1967). Open sandy areas (Louda et al., 1983, p. 387). In aquaria B. nyassanus remained buried in sand during daylight; its gelatinous, irregularly-shaped egg masses seemed adapted for laying on loose substrata, while the fine-cusped radular teeth appear suitable for collecting fine detritus (Wright et al., 1967). Bulinus octoploidus Burch, 1972. Type locality: Ethiopia, small body of water 4 km S of Shano, near the road to Debra Berhan, altitude about 2830 m (9285 feet). Figs 107g–i. 14.4×8.5 mm. Shell like B. hexaploidus though generally more slender and sometimes with even higher spire; shape of columella and size of umbilicus widely variable. Mesocone angular to intermediate; not aphallic. No clear characteristic of the octoploid emerged from morphological study of over 30 populations (Brown & Wright, 1972; Wu, 1972). Eggs laid in the laboratory were significantly larger than those of diploid snails and B. truncatus (Brown & Wright, 1972). Egg-laying behaviour was studied by Rudolph & White (1979). Morphological characteristics are summarised in Table 7.1 (Chapter 7). Chromosome number: 2n=144 (Burch, 1964, material from Western Aden Protectorate; Burch, 1967b, and Brown & Burch, 1967, Ethiopian populations). HABITAT. Streams flowing through grassland, with rich aquatic vegetation in the pools which retain water through the dry season. DISTRIBUTION. Ethiopia: on the plateau at altitude 2100–2865 m, between Addis Ababa and Dessie, and north of Gondar (Brown & Wright, 1972). Possibly also in South Yemen (Western Aden Protectorate); octoploid B. sericinus of Burch (1964). PARASITES. S. haematobium: low rates of infection achieved experimentally with parasite from Egypt (Lo, 1972). S. bovis: natural infections in snails from Dessie and Kombolchia (Graber & Daynes, 1974), successful experimental infections (Lo & Lemma, 1975). S. margrebowiei: successful experimental infection (Southgate & Knowles, 1977b). Bulinus permembranaceus (Preston, 1912b, Physa). Type locality: Kenya, Aberdare Range. Figs 109, 111a.

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Fig. 108. Bulinus natalensis. (a–c) Mhlangana River near Durban: (a) resembling ‘Physa’ natalensis Küster; (b) resembling P. natalensis of Krauss; (c) depressed specimen, (d) NE Natal, Lake Umpangazi (resembling P. zuluensis Melvill & Ponsonby). (e) Ethiopia, Lake Awasa. Scale line: 10 mm. Shells (a–d) first figured by Brown et al., 1971b and (e) by Brown & Wright (1972).

19×12 mm. Shell growing large, spire moderately high, whorls evenly curved; columella of widely varying shape (Fig. 109). Mesocone varying from angular to

240 SYSTEMATIC SYNOPSIS: PULMONATES

Fig. 109. Bulinus permembranaceus. Variation in columella shape. Four character states are illustrated: A, concave; B, straight; C, twisted; D, twisted and reflected. Guide lines indicate the positions of the concavity (A), twist (C) and reflection (D). From Brown & Shaw (1989, Fig. 3).

non-angular; not aphallic. This tetraploid species differs from East African populations of the tetraploid B. truncatus in its high acutely-tapered spire, lack of aphally, egg proteins and enzymes (Brown, 1976; Brown & Shaw, 1989). Some populations of the diploid B. tropicus are closely similar but have distinctive enzymes (Jelnes, 1977; Brown et al., 1991). Chromosome number: 2n=72 (Brown, 1976). HABITAT. Earth dams and pools in streams in the altitude range 1940–2760 m; B. truncatus and B. tropicus occur below this zone (Brown & Shaw, 1989). DISTRIBUTION. Kenya: Aberdare Range, Kinangop Plateau and the Mau Escarpment (areas of Mau Narok, Molo and Kipkabus). PARASITES. Experimental infections with schistosomes were all unsuccessful (Southgate & Knowles, 1977b; Frandsen, 1979e). Second intermediate host for Echinostoma in the laboratory (Christensen et al., 1980). Bulinus rohlfsi (Clessin, 1886, Physa). Type locality: Lake Chad at Kuka. Previously kept distinct as a subspecies of B. truncatus by Mandahl-Barth (1965) or as a full species (Brown, 1980a), but treated herein under B. truncatus, to which it conforms in being tetraploid and in its enzymes (Jelnes, 1986). Bulinus succinoides (Smith, 1877, Physa). Type locality: Lake Nyasa (Malawi). Fig. 106f. 6×4.5 mm. Small and slender in comparison with B. nyassanus, with an obtuse spire and closed umbilicus. Mesocone broadly angular, unlike the long slender mesocone of nyassanus; commonly aphallic (Wright et al., 1967). Chromosome number: 2n=36 (Wright et al., 1967). HABITAT. Living upon Vallisneria plants; snails kept in aquaria differed from B. nyassanus in not burrowing into the sand and in laying egg capsules of normal shape; the broad mesocone seemed adapted to browsing epiphytic algae (Wright et al., 1967).

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DISTRIBUTION. Lake Malawi: SW shore in shallow water, down to 4.5 m (15 feet; Mandahl-Barth, 1972). Bulinus transversalis (Martens, 1897, Isidora). Type locality: western Lake Victoria, Ndukali on Bumbide Island (possibly Bumbiri Island, south of Bukoba). Fig. 111c. 6.5×7.5 mm (Martens). Martens’ original figure shows a shell with an unusually large and oblique aperture. Mandahl-Barth (1957b, 1965) identified as this species small dark snails from the lake shore in Uganda, which had angular mesocones and were often aphallic. Similar snails from Kisumu were like B. truncatus in their egg proteins and in being tetraploid (Brown, 1980a); therefore B. transversalis possibly is merely a lacustrine form of B. truncatus. Chromosome number: 2n=72 (Brown, 1980a). HABITAT. Found by myself on stony wave-washed beaches at Kisumu, living with a small dark form of B. ugandae, which was hardly distinguishable in the field. Also present on the same stones was a paler diploid Bulinus (see B. trigonus, below). Bulinus trigonus (Martens, 1892, 1897, Isidora). Type locality: SW Lake Victoria, papyrus thicket at Bukome. Fig. 111b. 11×10.5 mm (Martens). Martens illustrated a shell in which the last whorl increases so rapidly that earlier whorls are invisible and the aperture rises above the flattened top. Mandahl-Barth (1957b, 1965) regarded this as a subspecies of B. truncatus, on the basis of specimens from the lake shore in Uganda, with angular mesocones and mostly aphallic. Snails with similar shells from Kisumu were diploid (Brown, 1980a); thus a relationship with B. natalensis should be considered. A possible synonym is Isidora strigosa Martens (1897, Lake Victoria at Bukoba); this name has been used for shells that appear to be B. truncatus from numerous localities in the Sahara. HABITAT. Besides a papyrus thicket, Martens mentioned a small stream. Obtained by myself on stony beaches down to a depth of about 5 m. DISTRIBUTION. Lake Victoria and Lake Edward (Mandahl-Barth, 1965). Bulinus tropicus (Krauss, 1848, Physa). Type locality: South Africa, Transvaal, Lepenula River, between latitudes 25° and 26° South (exact location unknown). Fig. 110. 12.3×7.8 mm (slender form), 10.6×8.3 mm (more globose form); rarely to 20 mm high. Shell commonly high-spired, columella usually concave to straight; mesocone most frequently non-angular; not aphallic. General morphological accounts are available (e.g. Stiglingh et al., 1962; Wu, 1972) and some organs have been described in detail (Stiglingh & Van Eeden, 1976a,b,c). Early distinguished in modern studies as a diploid species, differing morphologically from the tetraploid B. truncatus in having non-angular or ‘triangular’ mesocones (rather than angular) and lacking aphally (Mandahl-Barth, 1957b, 1965; Burch, 1963). Sperm morphology was described by Brackenbury & Appleton (1991a); comparative data are needed for other species.

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Fig. 110. Bulinus tropicus. (a) South Africa, Avoca near Durban (resembling Physa tropica Krauss). (c) Ethiopia, Tafhi (upper Awash River), (d) Ethiopia, Moggio (resembling Physa rumrutiensis Preston of Kenya), (b) South Africa, Port Elizabeth (syntypes of Physa cornea Morelet, BMNH 1911.8.8.51–2). (e) Uganda, Fort Portal (paratype of B. tropicus toroensis Mandahl-Barth, BMNH 1968.698). Scale line: 8 mm (a,c,d) or 10 mm (b,e).

The shell is highly varied; Krauss described a high-spired form (Fig. 110a, c), which intergrades with a broader, widely umbilicate form (Fig. 110d), while at another extreme are low-spired, narrowly umbilicate populations, found especially in lakes (Fig. 110e). Apparently fully-grown individuals are unusually small in some populations (Fig. 110b). Variation has been described in detail for South Africa (Brown et al., 1971a,b; Stiglingh & Van Eeden, 1977a) and Kenya (Brown et al., 1991). Mesocone shape, though frequently angular, varies widely within and between populations (Oberholzer et al., 1970; Brown et al., 1971a,b; Brown, 1982). An angular frequency of below 50% characterised B. tropicus in SE Africa (Brown et al., 1971b; Shaw & Brown, 1986), but some Kenyan populations considered to be this species had higher frequencies (Brown et al., 1991). Other features of the radular teeth were described by Wu (1972) and Burch & Jeong (1984).

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Close relationship between B. tropicus and B. natalensis was indicated by observations on egg proteins and foot muscle antigens (references under natalensis). Enzyme electrophoresis also failed to separate clearly the two species (Wright & Rollinson, 1981), but differences between B. tropicus and the two tetraploids B. permembranaceus and B. truncatus were clear (Jelnes, 1977; Wright & Rollinson, 1981; Brown et al., 1991). Karyotype studies on B. tropicus were made in comparison with B. natalensis and B. truncatus; studies on more populations and species are needed in order to evaluate the apparent differences (Claugher, 1971; Goldman et al., 1980, 1983, 1984; Goldman & LoVerde, 1983). Among taxa treated as synonyms of B. tropicus one of the most distinctive is B. rumrutiensis (Preston, 1913; Kenya), a plump snail with a large umbilicus and associated with rainpools (Fig. 110d; Brown et al., 1991). B. corneus (Morelet, 1889; Port Elizabeth) is unusually small (Fig. 110b). No reason could be found by Brown et al. (1991) to segregate B. alluaudi (Dautzenberg, 1890; Kenya) or B. zanzebaricus (Clessin, 1886; type locality ‘Zanzibar’, but never re-found on the island). B. tropicus toroensis Mandahl-Barth (1960; Uganda, in a crater lake near Fort Portal) (Fig. 110e) is possibly a lacustrine form of B. truncatus; its chromosome number is unknown. Chromosome number: 2n=36 (Burch, 1963, 1964; Brown et al., 1967). HABITAT. Particularly common in small earth dams and residual pools in seasonally flowing streams in the highlands of eastern Africa and the highveld of southern Africa; found in some lakes, e.g. Naivasha in Kenya (Clark & Baroudy, 1990; Brown et al., 1991, p. 161). B. tropicus is associated with a cooler climatic area than B. natalensis in Natal (Brown et al., 1971b; Shaw & Brown, 1986). It thrives under the extreme conditions of cold dry winters and hot summers on the South African highveld (Stiglingh & Van Eeden, 1977b); experiments showed a high capacity for population increase during brief favourable periods, suited to temporary habitats (Prinsloo & Van Eeden, 1973a; De Kock & Van Eeden, 1985; De Kock, 1985). Yet at controlled temperature the reproductive potential was inferior to that of Physa acuta, a successful invading species (Brackenbury & Appleton, 1991c). Other experimental studies include the topics of ammonia excretion (Mason, 1979), toxicity of copper sulphate (Van Aardt & Coertze, 1981), circadian rhythms (Chaudry & Morgan, 1983) and the effects of laboratory breeding on the performance of snails in experiments on population dynamics (De Kock et al., 1986). DISTRIBUTION (Fig. 126). Eastern and southern Africa from the Ethiopian highlands to W Cape Province and Namibia, but not found in most of the eastern coastal region. Distribution is best known for Ethiopia (Brown & Wright, 1972), Kenya (Brown et al., 1991), South Africa (Van Eeden & Combrinck, 1966; Brown et al., 1971a,b; De Kock et al., 1974), Lesotho (Prinsloo & Van Eeden, 1973b) and Namibia (Brown et al., in prep.). Found up to altitudes of 2700 m in Kenya and 3100 m in Lesotho (Bekong Bogs, R.H.Meakins, 1991; BME).

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PARASITES. S. haematobium: no evidence for natural infection apart from a few unconfirmed reports (e.g. Porter, 1938), and attempted experimental infections were unsuccessful (e.g. Frandsen, 1979b,c). S. bovis: natural transmission in Kenya (Ouma & Waithaka, 1984), in apparently limited areas where concurrent infection with Calicophoron microbothrium is believed to favour infection by the schistosome (Southgate, Brown et al., 1985, 1989). S. margrebowiei: natural transmission in Zambia (Southgate, Howard et al., 1985) and successful experimental infections (Pitchford, 1976; Southgate & Knowles, 1977b). Calicophoron (formerly Paramphistomum) microbothrium: B. tropicus is of veterinary importance as the main intermediate host south of the Sahara (Dinnik, 1965). Echinostoma: second intermediate host in experiments (Christensen et al., 1980). Bulinus truncatus (Audouin, 1827, Physa). Type locality: Egypt. Figs 106g, 107a–c, 111d–i. 9.5×6 mm (slender form); 9.5×7.5 (broad form); sometimes to nearly 20 mm high. Shell widely varied in respect of height of spire, shape of columellar margin and size of umbilicus. A type specimen is small (only 5 mm high), with a depressed spire (Bouchet & Danrigal, 1982, Fig. 29). B. truncatus may be recognised by a combination of characters not easy to define: the uneven curvature of the whorls tends to produce a blunt shoulder, the columellar margin is usually narrow and more or less twisted, and the shell colour is pale. This species was recognised early in modern studies as tetraploid, commonly aphallic (though only rarely in Egypt) and with the mesocone most frequently angular (Mandahl-Barth, 1957b, 1965; Burch, 1960). ‘Egg proteins’ (from the fluid bathing the embryos) give a unique electrophoretic pattern (Wright & Ross, 1965; Hamilton-Atwell, 1976; Brown & Rollinson, 1982). Genital anatomy was described in an outstanding classic account (Larambergue, 1939) and extensive morphological information is available for snails from many countries, e.g. Egypt (Demian, 1960; Walter, 1968; Wu, 1972), Ethiopia (Brown & Wright, 1972; Wu, 1972; Wu & Burch, 1975), Kenya (Brown & Shaw, 1989), Libya (Itagaki & Yasuraoka, 1975) and Senegal (Brown, Shaw et al., 1986). B. truncatus arose as a tetraploid through hybridisation according to karyotype studies (Goldman et al., 1983, 1984; Goldman & LoVerde, 1983). A hybrid origin would be consistent with the considerable amount of genetic variation among populations revealed by enzyme electrophoresis; sampling has extended over large geographical regions (Biocca et al., 1979; Wurzinger, 1979; Wurzinger & Saliba, 1979; Jelnes, 1979b, 1986; Nascetti & Bullini, 1980; Biocca et al., 1981; Wright & Rollinson, 1981) and also concentrated on smaller areas, e.g. in Yemen (Paggi et al., 1978), Sardinia (Arru et al., 1980), Corsica (Orecchia et al., 1981), Senegal (Brown, Shaw et al., 1986), and Cameroon

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Fig. 111. Bulinus. (a) B. permembranaceus; Kenya, Kinangop Plateau, (b) B. trigonus; Uganda (possibly the holotype, from Kilias, 1963, Fig. 8). (c) B. transversalis; Kenya, Lake Victoria at Kisumu. (d–i) B. truncatus: (d) Tanzania, Kigoma (representing Physa coulboisi Bourguignat); (e) Senegal, Tuabo (holotype of Isidora guernei Dautzenberg, Institut Royal des Sciences Naturelles de Belgique); (f) Uganda, Lake Mutanda (representing B. mutandaensis (Preston) of Mandahl-Barth, 1960, 1965); (g) Ghana; (h) Morocco, Bouida; (i) Malawi, near Blantyre, Mpemba Dam. Scale line: 10 mm.

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(Mimpfoundi & Greer, 1990c). Many enzyme loci are in a fixed heterozygous state, and different ‘biotypes’ could be defined according to the number and type of heterozygous loci (Nascetti & Bullini, 1980; Bullini, 1982). Variation was particularly marked in Cameroon, where 4 groups of populations were recognisable (Mimpfoundi & Greer, 1990c). So far it does not appear that any enzymically-defined biotype corresponds to a taxon already named. B. truncatus differs from the only other tetraploid species now recognised, B. permembranaceus, in its lower and more obtuse spire and commonly aphallic condition. No clear morphological differences from either of the higher polyploid species in Ethiopia were found (Brown & Wright, 1972; Wu, 1972). The diploid species belonging to the same species group, including those which are truncatus-like in having angular mesocones and aphally (depressus and natalensis) differ from truncatus in egg proteins and enzymes. From the combination of morphological, cytological and electrophoretic data it appears that many named forms belong to one species: these include names listed under B. t. truncatus by Mandahl-Barth (1957b, 1965) and those treated as other subspecies or full species (Mandahl-Barth, 1965; Jelnes, 1979b; Brown, 1980a). Six names used widely are now considered briefly here. B. contortus (Michaud, 1829; southern France) (Fig. 111h): employed mostly for snails from the western Mediterranean region (Mandahl-Barth, 1965). B. coulboisi (see p. 221): name given to what appear to be populations of B. truncatus in the Lake Tanganyika Basin (Brown, Matovu & Rollinson, 1982). B. guernei (see p. 222) (Figs 106g, 111e): name given to populations in Senegambia and neighbouring territories (Brown, Shaw et al., 1986; Jelnes, 1986). B. mutandaensis (Preston, 1913; Uganda, Lake Mutanda) (Fig. 111f): regarded by Mandahl-Barth (1960, 1965) as a distinct species, with a broad angular mesocone and often aphallic, such snails are tetraploid (Brown & Wright, 1972, Fig. 1, locality 17) and seem to be a lacustrine form of B. truncatus. The shell is closely similar in shape to the species B. ugandae Mandahl-Barth, 1954, which also occurs in Lake Mutanda. Syntypes of mutandaensis (BMNH) belong to that species, but confusion will be avoided by continuing to use the name ugandae for the species belonging to the B. africanus group. B. rohlfsi (see p. 228) (Fig. 111g): name given to populations from Lake Chad and a large area of West Africa (Jelnes, 1986). B. sericinus (Jickeli, 1874; N Ethiopia) (Figs 107a–c): inseparable from Egyptian B. truncatus according to morphology and enzymes (Brown & Wright, 1972; Wu & Burch, 1975; Wurzinger, 1979). Chromosome number: 2n=72 (Burch, 1960). HABITAT. Various waterbodies, flowing and standing, some of which become seasonally dry, but not such briefly-filled pools as are inhabited by B. senegalensis and B. tropicus. Dams were the only kind of habitat occupied by B. truncatus in SW Nigeria, where it was one of the rarest aquatic snails (Ndifon & Ukoli, 1989). Habitats have been described in many publications, among the

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more recent are accounts for Cameroon (Greer et al., 1990), Mali (Madsen et al., 1987), Nigeria (Betterton, 1984a; Betterton, Ndifon et al., 1988; Thomas & Tait, 1984); and Zaire (Mandahl-Barth et al., 1974). B. truncatus is a successful colonist of irrigation systems (Dazo et al., 1966; Kloos & Lemma, 1974; Wibaux-Charlois et al., 1982; Betterton, 1984b; Madsen, Daffalla et al., 1988) and some of the large man-made lakes including Lake Volta, where weedbeds of Ceratophyllum are favourable (Klumpp & Chu, 1977, 1980), and Lake Nasser (Doumenge et al., 1987). The occurrence of the snail was found to be limited by high concentrations of electrolytes, particularly chlorides, in Tunisia (Meier-Brook et al., 1987). Although absent from temporary rainpools, B. truncatus has a considerable capacity for aestivation, studied under tropical conditions in the field (Betterton et al., 1988) and experimentally (Diaw et al., 1988; Oyeyi & Ndifon, 1990). Population fluctuations have been followed in dams (McCullough, 1962b), irrigation channels (Dazo et al., 1966), experimental channels (Demian & Kamel, 1972), a seasonal river (Kechemir, 1987), a reservoir (Betterton et al., 1988) and streams (Coulibaly & Madsen, 1990). An experimental study of population dynamics showed that ‘r’ values were affected adversely by a disturbed muddy substratum amd turbidity (Klumpp et al., 1985). Aspects of the breeding system to receive particular attention are aphally and self-fertilisation in relation to fitness (Jarne, Finot et al., 1992; Njiokou et al., 1993; Schrag et al., 1992; see Chapter 7). DISTRIBUTION (Fig. 127). The northern limit for populations known to be recently living includes Portugal, Sardinia and Corsica, and the Near East. Extensive area of scattered distribution in western Arabia. Many records for whitened shells of Late Pleistocene-Holocene age in the more arid areas of Arabia and northern Africa (reviewed by Van Damme, 1984); a few isolated living populations persist in the Sahara. The main areas of distribution in Africa are in the North-West, lower Egypt, Sudan and westwards into Mauritania. The southern limits lie in Zaire and Malawi. Details of occurrence have been published for many areas, including Algeria (Kechemir, 1986), Cameroon (Greer et al., 1990; Mimpfoundi & Greer, 1990c), Ethiopia (Brown & Wright, 1972), Kenya (Brown & Shaw, 1989), Mali (Madsen et al., 1987) and the Senegal Basin (Malek & Chaine, 1981). There is a large area of more-or-less continuous distribution in West Africa, reviewed for francophone countries by Sellin et al. (1980). B. truncatus seems to be most successful in the Sahelian region of West Africa, but it occurs also near some parts of the coast, e.g. the lower Volta Basin (McCullough, 1962a). Elsewhere in tropical Africa, where morphologically similar diploid snails may occur, the precise distribution of the tetraploid has yet to be established thoroughly; it seems likely that many localities will be added. PARASITES. S. haematobium: B. truncatus is the only intermediate host in the Near East and North Africa, and it contributes to transmission in Sudan, the Sahelian region and in West Africa generally. The snail’s part in epidemiology

248 SYSTEMATIC SYNOPSIS: PULMONATES

has been described in detail for Lake Volta (Chu et al., 1981; Scott et al., 1982) and the Gezira irrigated area of Sudan (Babiker et al., 1985). The parasite exists in two groups of strains, most compatible with either B. truncatus or with members of the B. africanus group (McCullough, 1959; Frandsen, 1979c; Betterton et al., 1988; Véra et al., 1990). In Equatorial Africa, however, the only known truncatus-borne focus of infection is in lower Zaire (Mandahl-Barth et al., 1974; Frandsen, 1979c), and thus none seems to be present in most of the equatorial area where the snail occurs. Potentiality for transmission by southern snail populations is indicated by their compatibility in experimental exposures to parasite isolates from other areas (Brown & Wright, 1972; Mandahl-Barth et al., 1976; Southgate & Knowles, 1977a; Frandsen, 1979c). S. bovis: B. truncatus seems to be the only intermediate host in North Africa; further south it is one of several Bulinus used by the parasite. Natural transmission is reported for Sudan (Majid et al., 1980), Ethiopia (Lo & Lemma, 1975) and western Kenya (Southgate & Knowles, 1975a,b). The apparent rarity of transmission by B. truncatus in Senegal is surprising as experimental infections were successful using snail and parasite stocks from this country (Southgate, Rollinson et al., 1985; Diaw & Vassiliadès, 1987). S. margrebowiei: successful experimental infection (Southgate & Knowles, 1977b). Calicophoron microbothrium: B. truncatus is the main intermediate host in North Africa (Dinnik, 1965) and was implicated by experiment as a host in Niger (Tager-Kagan, 1977). Prevalences of paramphistomes and other helminths in naturally infected snails were investigated in Egypt (Rysavy et al., 1974). Echinostoma: second intermediate host in experiments (Christensen et al., 1980). Bulinus yemenensis Paggi, Orecchia, Bullini, Nascetti & Biocca, 1978. Type locality: Yemen, Tai’zz. 12.5×8 mm (holotype). According to the original description, distinguishable from B. ‘truncatus truncatus’ by differences in the shell (higher spire, weaker costulation and the irregularly curved outer lip) and in 4 enzyme loci. On this evidence it seems unlikely that this is a distinct species. Chromosome number: 2n=72 (Paggi et al., 1978). Reported only from the type locality. 3) B. forskalii group. Shell generally more slender than in the other groups, the spire may be distinctly higher than the aperture; whorls shouldered and carinate in some species, regularly spaced ribs may be present. Lacking the characteristic microsculpture and renal ridge of the B. africanus group. Aphallic specimens are unknown. It is difficult to define clear morphological differences from the B. truncatus/tropicus complex, but the B. forskalii group was well separated by enzyme electrophoresis (Jelnes, 1987, Fig. 3). The evolutionary relationships among the species are not clear; non-African species are segregated at the end of this account. Chromosome number: 2n=36. Some species have been placed in the genus or subgenus Pyrgophysa Crosse, 1879 (for P. mariei of Nossi Bé), but since this group includes B. senegalensis,

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the type species of Bulinus Müller, the correct subgeneric name would be Bulinus (Bulinus). Bulinus forskalii (Ehrenberg, 1831, Isidora). Type locality: Egypt, Damietta. Fig. 112. 17×5.4 (smaller in many localities). Spire high and slender when fully grown; whorls shouldered to some degree and sometimes carinate; strong ribs commonly present and may bear fringes of periostracum. Copulatory organ with penis sheath about equal in length to the preputium (thus proportionally smaller than in B. scalaris). Morphology described in detail for snails from Angola (Wright, 1963a), Ethiopia (Brown, 1965), Liberia (Walter, 1968), Madagascar (Starmühlner, 1969, B. mariei) and Mozambique (Azevedo et al., 1961). Marked changes in shell shape take place with growth, juveniles being comparatively broad and low-spired. This added to what appears to be withinspecies variation among populations in fully-grown size and form has resulted in many named species being treated as synonyms (Mandahl-Barth, 1957b). Shells from some Egyptian localities are particularly high-spired (Figs 112a,b); similar specimens from South Africa were named Physa wahlbergi Krauss, 1848. The small form Physa vitraea Sowerby, 1873 (Fig. 112c) seems likely to have been collected in Angola like P. benguelensis described in the same publication (see under B. scalaris). Other small forms are named Physa gradata Melvill & Ponsonby, 1898, from South Africa and P. dautzenbergi Germain, 1905 from Lake Chad. Variation seems particularly wide in Angola (Figs 112d–i); this country is the origin of no less than 12 species which possibly are not different from B. forskalii (Mandahl-Barth, 1957b; Wright, 1963a). In Madagascar B. mariei (Crosse, 1879, the type of Pyrgophysa) appears to be a form of B. forskalii (whereas B. bavayi may be a distinct species, see below). An unusually broad form found on São Tomé Island was identified as B. forskalii with doubt (Brown, 1991), and the possibility remains that distinct species are confused within this assemblage of forms. Generally a rather low genetic diversity is indicated by enzyme electrophoresis (Jelnes, 1980, 1986; Dogba & Jelnes, 1985; Mimpfoundi & Greer, 1989, 1990d) and reproduction appears to be mainly by self-fertilisation (Mimpfoundi & Greer, 1990d). However, the finding of distinctive loci in some East African populations led Jelnes (1979c, 1980) to name two new species (B. barthi and B. browni, below) even though no morphological differences from B. forskalii could be detected. Some alleles show evidence for a geographical pattern of occurrence in Cameroon (Mimpfoundi & Slootweg, 1991). Unfortunately no enzyme data are yet available for areas of high morphological diversity such as Angola. Chromosome number: n=18 or rarely 19 (Natarajan et al., 1965), 2n=36 (Jelnes, 1980). HABITAT. Various natural and artificial situations, including lake margins, permanent swamps and irrigation systems (Betterton, 1984b; Madsen et al., 1988) and, above all, small waterbodies that may be flowing or stagnant,

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Fig. 112. Bulinus forskalii. (a,b) Egypt, Qalyubiya. (c) Probably from Angola (syntype of Physa vitraea Sowerby, BMNH46.8.21.141–5; see text), (d) Angola (syntype of P. apiculata Morelet, BMNH1893.2.4.647–50). (e) Angola (syntype of P. capillacea Morelet, BMNH1893.2.4.654–5). (f) Angola (syntype of P. clavulata Morelet, BMNH1893.2.4. 643–6). (g) Angola (syntype of P. semiplicata Morelet, BMNH1893.2.4.621–3). (h) Angola (holotype of P. turriculata Morelet, BMNH1893.2.4.505). (i) Angola (syntype of P. schmidti Dunker; Zoologische Museum, Berlin). Scale lines: 4 mm (a–c) or 6 mm (d–i). Shells (d–i) were figured by Wright (1963a, Pl. 7).

perennial or temporary and are sometimes polluted (Smithers, 1956; Sellin et al., 1980; Wibaux-Charlois et al., 1982; Thomas & Tait, 1984; Ndifon & Ukoli, 1989; Greer et al., 1990). Although B. forskalii does not live in such briefly-

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filled rainpools as are inhabited by B. senegalensis, these two species often occur together (Goll, 1981; Betterton et al., 1983; Betterton, Ndifon et al., 1988; Greer et al., 1990). Growth has been studied in natural populations in Chad (Lévêque, 1968) and SE Zaire (Malaisse & Ripert, 1977). DISTRIBUTION (Fig. 128). Essentially Afrotropical, reaching the Mediterranean only in lower Egypt. The most northerly sites for extinct Late Pleistocene-Holocene populations are in S Libya (Fig. 128 and Van Damme, 1984). Cape Verde Islands (Panelius, 1958; Groh, 1983). In NE Africa B. forskalii is common in S Sudan (Brown, Fison et al., 1984), occurs in scattered localities in Ethiopia up to an altitude of about 1800 m (Lake Tana; Brown, 1965) and from the Webbi Shebeli region of Somalia southwards. In W Africa living populations occur northwards to the Senegal River Basin and middle Niger Basin in the region of Mopti. The more recent of detailed surveys covered northern Nigeria (Betterton, 1984a,b; Betterton, Ndifon et al., 1988) and Cameroon (Greer et al., 1990). The range extends southwards into Namibia, the lower Orange River and eastern Cape Province. B. forskalii is not found in the cool highlands of eastern and southern Africa, nor in most of western Cape Province. Its south-western distribution is indeed rather uncertain because of possible confusion with B. scalaris (see Brown, Curtis et al., 1992). Madagascar: B. forskalii is probably widespread (Mandahl-Barth, 1957b, 1965; Degrémont, 1973; B. mariei of Wright, 1971); maps were given by Starmühlner (1969) and Fischer-Piette & Vukadinovic (1973) but they regarded B. bavayi as a synonym. PARASITES. S. haematobium: no focus is known to be transmitted by B. forskalii, despite some inconclusive reports (e.g. Akouala et al., 1988). Attempted experimental infections failed (Frandsen, 1979f) and no infected snail was found among thousands field-collected in Tanzania (Webbe, 1962b) and Somalia (Shunzhang & Hongming, 1980). Goll (1981) pointed out that it could have been confusion between B. forskalii and B. senegalensis in West Africa that resulted in the former being suspected as an intermediate host. S. intercalatum: natural transmission in Cameroon (Wright et al., 1972; Greer et al., 1990), Gabon (Brown, Sarfati et al., 1984), São Tomé Island (Brown, Grácio et al., 1989; Brown, 1991) and probably other countries including Nigeria (Arene et al., 1989) and Equatorial Guinea (Simarro et al., 1990). Two parasite strains exist, one transmitted by B. forskalii and the other by snails of the B. africanus group (e.g. Wright et al., 1972; Frandsen, 1979a). S. bovis: B. forskalii is one of the intermediate hosts in both eastern Africa (Kinoti, 1964; Southgate & Knowles, 1975a; Majid et al., 1980; Mutani et al., 1983; Mwambungu, 1988) and West Africa (Diaw & Vassiliadès, 1987). S. margrebowiei: natural infection in Zambia (Wright, Southgate & Howard, 1979a). Echinostoma: second intermediate host in experiments (Christensen et al., 1980).

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Calicophoron microbothrium: natural transmission (Graber & Daynes, 1974; Tager-Kagan, 1977). Intermediate host for other amphistome flukes (Dinnik, 1965; Wright, Southgate & Howard, 1979b) and also Gastrodiscus aegyptiacus: Le Roux, 1958; Tager-Kagan, 1977. Multiple trematode infections occur (Hira, 1968b); a total of 7 cercarial species were obtained from naturally infected snails collected in NW Tanzania (Loker et al., 1981). Bulinus barthi Jelnes, 1979c. Type locality: Kenya, Coast Province, Mariakani Dam. Morphology ‘very similar to B. forskalii’, but with distinctive enzymes (Jelnes, 1979c, 1980). Chromosome number: 2n=36 (Jelnes, 1980). HABITAT AND DISTRIBUTION. Kenya and Tanzania: the coastal region, in dams, a pond and a swamp (Jelnes, 1980). Bulinus browni Jelnes, 1979c. Type locality: Kenya, Nyanza Province, Obtuso (possibly referring to a stream named Obuso on the Kano Plain near Kisumu). Morphology ‘very similar to B. forskalii’, but with distinctive enzymes (Jelnes, 1979c, 1980). Chromosome number: 2n=36 (Jelnes, 1980). HABITAT AND DISTRIBUTION. W and central Kenya: found on the Kano Plain together with B. forskalii and B. scalaris in drains filled briefly with rainwater. PARASITE. S. bovis: suspected transmission in W Kenya, according to shedding of ‘mammalian type schistosome cercariae’ (Jelnes, 1983b). Bulinus scalaris (Dunker, 1845, 1853, Physa). Type locality: Angola, marshy streams and lakes near Benguela. Figs 113a–f. 12×4.5 mm. Distinguished from B. forskalii by the broader shell, with the lower whorls more smoothly curved, lacking a shoulder and regular ribs; the copulatory organ is larger with the penis sheath much swollen by a long and coiled epiphallus (Wright, 1963a; Mandahl-Barth, 1965; Jennings et al., 1974; Wright, Southgate & Howard, 1979a). Specimens from W Kenya could be separated from other taxa in the B. forskalii group according to their enzymes (Jelnes, 1980). Possible synonyms, so far as can be judged from the shell alone, include B. benguelensis (Sowerby, 1873) (Figs 113d–f); although Egypt was the country of origin given by Sowerby, this seems to be an error resulting from confusion with the village of Egito in Benguela, Angola (Wright, 1963a, p. 489). Other similar forms are B. nyangweensis (Putzeys, 1898, E Zaire) and B. fischerianus (Bourguignat, 1856), the latter being represented perhaps by a smooth-whorled population found in highland Ethiopia (Bulinus sp. of Brown, 1965, p. 65) (Fig. 113i). Chromosome number: 2n=36 (Jelnes, 1980). HABITAT. Seasonal pools, usually lacking vegetation, in Ethiopia (Brown, 1965) and W Kenya (Chapter 9; Kano Plain). Habitats in Angola and Namibia

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included a concrete-lined irrigation channel (Jennings et al., 1974) and some main channels on the Okavango flood-plain, though the snail was more frequent in isolated pools (Brown, Curtis et al., 1992). DISTRIBUTION. Eastern and southern Africa. Highland Ethiopia (Brown, 1965), Uganda (Mandahl-Barth, 1954a), W Kenya (Mandahl-Barth, 1954a; Brown, 1980a; Jelnes, 1980), Zambia (Wright, Southgate & Howard, 1979a; Brown, 1980a), Zimbabwe (Brown, 1980a), SE Zaire (Mandahl-Barth, 1968a), Angola (Wright, 1963a; Jennings et al., 1974), Namibia (Jennings et al., 1974; Brown, Curtis et al., 1992). PARASITES. S. intercalatum: successful experimental infection (Wright et al., 1972). S. margrebowiei: natural transmission in Zambia (Wright, Southgate & Howard, 1979a). Bulinus canescens (Morelet, 1868, Physa). Type locality: Angola, marshes near the Bengo River, near Quicuje (between Luanda and Ambriz). Figs 113g,h. 15×6.2 mm (syntype figured by Wright, 1963a). Shell like B. scalaris, but according to Mandahl-Barth (1968a) a distinct species, with the copulatory organ like that of B. forskalii. I have examined many specimens from the Mulonde River identified by Mandahl-Barth; the shell (Fig. 113h) is ribbed on the upper whorls. Snails from Zambia identified as B. scalaris by Wright (1963a) were considered to be B. canescens by Mandahl-Barth (1968a), but they conform to scalaris according to my examinations of the copulatory organ. Knowledge of the anatomy of snails from the type locality is needed for a better understanding of this taxon. Chromosome number: 2n=36 (Jelnes, 1985). DISTRIBUTION. Angola: type locality. SE Zaire: lower Luapula region and Mulonde River (Mandahl-Barth, 1968a). Zambia: Lochinvar Farm (controversial identification, see above). PARASITES. No schistosome infection reported. Bulinus senegalensis Müller, 1781 (new name for ‘le Bulin’ of Adanson, 1757). Type locality: Senegal, Podor. Figs 114a,b. 12×5 mm (rarely to 18 mm high). Whorls evenly curved and not carinate (like B. canescens and B. scalaris); usually smooth though sometimes ribbed, when the most reliable difference from B. forskalii is the lack of any shoulder on the early whorls (Goll, 1981; Betterton et al., 1983). The spire may be tall and almost cylindrical (Fig. 114b) or considerably broader (Wright, 1959, Pl. 1; Brown, 1991, Fig. 7). Originally described from immature specimens less than 4 mm high (Fischer-Piette, 1942); B. ludovicianus (Mittre, 1841, of St Louis in Senegal) is founded on an unusually large shell of 18 mm high (Wright, 1956a, 1959). Copulatory organ like that of B. forskalii, but mesocone larger and more angular (Mandahl-Barth, 1957b, 1965); there is however considerable overlap in tooth size (Brown, 1991, Fig. 6).

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Fig. 113. (a–c) Bulinus scalaris; Angola (syntypes, Zoologische Museum, Berlin), (d–f) B. scalaris; Angola (syntypes of Physa benguelensis Sowerby, BMNH1962.80). (g) B. canescens; Angola (syntype, BMNH1893.2.4.606–7). (h) B. canescens; SE Zaire, Mulonde River, (i) Bulinus sp.; Ethiopia, 4 km N of Medhanie Alem (see under B. scalaris). Scale line 4 mm (h) or 6 mm (a–g,h). Shells (a–g) were figured by Wright (1963a, Pl. 9), (i) by Brown (1965).

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Different from B. forskalii in some enzymes, with no evidence of interbreeding (Wright, Rollinson & Goll, 1979; Jelnes, 1980, 1986; Goll, 1981; Betterton et al., 1983; Mimpfoundi & Greer, 1989; Mimpfoundi & Slootweg, 1991). Low genetic diversity in B. senegalensis is possibly related to its specialised ecological requirements (Mimpfoundi & Greer, 1989). Chromosome number: 2n=36 (Natarajan et al., 1965; Jelnes, 1980). HABITAT. B. senegalensis is the only snail present in some seasonal rainpools, especially on the laterite plateau in Gambia (Smithers, 1956, 1958); these habitats and seasonal changes in snail populations were described in detail by Goll & Wilkins (1984). Identified later from more varied pools, also ricefields and irrigation channels (Goll, 1981; Betterton et al., 1983; Betterton, 1984a,b), often occurring with B. forskalii. Extensive surveys in N Nigeria (Betterton, Ndifon et al., 1988) and Cameroon (Greer et al., 1990) showed that most habitats dry out seasonally; populations are maintained in pools that are dry for 6–8 months in a year (Goll & Wilkins, 1984; Diaw et al., 1989). An annual period of aestivation seems to be essential to the well-being of the snail (Betterton et al., 1983). Probably this is the snail which Moreau (1972, pp. 222, 237) mentioned as an important food for two migratory birds, the Wood Sandpiper (Tringa glareola) and the Garganey Duck (Anas querquedula). DISTRIBUTION. Mainly Sahelian, from Senegambia through the middle Niger Basin (Madsen et al., 1987; Mouchet, Labo et al., 1987) to NE Nigeria (Betterton et al., 1983) and Cameroon north of 8° N latitude (Greer et al., 1990; Mimpfoundi & Slootweg, 1991). Southern limits need to be established through careful identification; senegalensis is recently reported from S Nigeria (Okafor, 1990b) and Sierra Leone (Nagel, 1991). PARASITES. S. haematobium: B. senegalensis is an intermediate host of importance in Gambia (Smithers, 1956; Goll & Wilkins, 1984) and Niger (Véra et al., 1992), a suspected host in N Nigeria (Betterton, Ndifon et al., 1988, p. 569) and N Cameroon (Greer et al., 1990, p. 577). S. bovis: natural transmission in Gambia (Smithers, 1956; Wright, Rollinson & Goll, 1979), but apparently not in Senegal (Diaw & Vassiliadès, 1987) and poorly compatible in experiments (Southgate, Rollinson et al., 1985). S. curassoni: low compatibility in experiments (Southgate, Rollinson et al., 1985), natural infection was not found (Diaw & Vassiliadès, 1987). S. intercalatum: successful experimental infection (Wright et al., 1972). Other parasites found as natural infections in Senegambia (Wright, Rollinson & Goll, 1979) included Calicophoron microbothrium and Echinostoma revolutum (probably E. caproni; see Huffman & Fried, 1990). Bulinus camerunensis Mandahl-Barth, 1957b. Type locality: Cameroon, Lake Barombi Kotto, SW of Kumba. Fig. 114c. 9×4.5 mm. Described originally from juveniles, larger shells are more slender (Wright, 1965; Brown, 1991), but broader than most forms of B. forskalii, the number of whorls increasing more slowly in relation to shell size (Brown, 1991, Fig. 10). Both species may be carinate (Brown, 1991, Table 1). Mandahl-Barth

256 SYSTEMATIC SYNOPSIS: PULMONATES

(1957b, 1965) described the radular teeth as smaller than in B. forskalii, but the size ranges partly overlap (Brown, 1991, Fig. 6). There were differences from B. forskalii in egg proteins (Wright & Ross, 1966) but not among 15 allozyme loci (Mimpfoundi & Greer, 1989). Further investigation is needed into the standing of B. camerunensis as a distinct species and of its relationship to the somewhat similar population of B. forskalii in São Tomé Island (Brown, 1991). Chromosome number: not reported. HABITAT. Mainly in shallow water of Lake Barombi Kotto, down to 1 m depth, living on dead leaves and other decaying vegetable matter, but not found on water plants (Duke & Moore, 1976). This was the only mollusc found in Lake Debundsha, which has a very low conductivity of 11–13 µmhos (Green et al., 1974). DISTRIBUTION. W Cameroon: crater lakes Barombi Kotto and Debundsha. PARASITES. S. haematobium: transmitted in Lake Barombi Kotto, where the parasite strain might have resulted from hybridisation with S. intercalatum (Wright et al., 1972, 54–55; Duke & Moore, 1976, p. 312). S. intercalatum: successful experimental infections (Wright et al., 1972). S. bovis: successful experimental infections (Southgate & Knowles, 1975a). S. curassoni: low compatibility in experiments (Southgate, Rollinson et al., 1985). Bulinus crystallinus (Morelet, 1868, Physa). Type locality: Angola, Quiapose River near Sange. Fig. 114d. 9.5×5.2 mm (sometimes more slender). Shell unusually broad for this speciesgroup; whorls shouldered with strong ribs all over (Wright, 1963a; Brown, 1991, p. 148). No difference was detected between snails from Angola and Gabon in 8 enzymes (Jelnes & Highton, 1984). Chromosome number: 2n=36 (Jelnes, 1985). HABITAT. Slowly flowing streams and irrigation channels (Wright, 1963a). DISTRIBUTION. N Angola: type locality and Salazar area (Wright, 1963a). S Gabon: Gamba (Jelnes & Highton, 1984). PARASITES. S. haematobium: suspected transmission in Angola (Wright, 1963a, p. 518). S. intercalatum: suspected host in Gabon (Jelnes & Highton, 1984), successful experimental infections with parasite from Cameroon (Wright & Southgate, 1976, p. 69; Jelnes & Highton, 1984). S. bovis: successful experimental infections (Southgate & Knowles, 1975b; Southgate, Rollinson et al., 1980). Bulinus beccarii (Paladilhe, 1872, Physa). Type locality: dry stream-bed near Aden. Fig. 114e. 7×3.4 mm. Shell like B. forskalii, but the whorls are little if at all shouldered or ribbed (Wright, 1963a, 1971; Mandahl-Barth, 1965). Chromosome number: n=18 (Natarajan et al., 1965).

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Fig. 114. (a) Bulinus senegalensis; Gambia, Njoren pool, (b) B. senegalensis; Gambia, Belal pool, (c) B. camerunensis; Cameroon, Lake Barombi Kotto. (d) B. crystallinus; Angola (syntype, BMNH1893.2.4.636–8). (e) B. beccarii; South Yemen (W Aden), Wadi Hassan. (f) B. cernicus; Mauritius, Port Louis, (g) B. bavayi; Aldabra, South Island, (h) B. reticulatus; Tanzania, Misungi near Mwanza. (i) B. wrighti; South Yemen (E Aden Protectorate), Raidal al Sa-ar district. Scale line: 4 mm (a–c,e–i) or 6 mm (d). Shell (d) was figured by Wright (1963a, Pl. 11).

HABITAT. Perennial streams, springs and man-made waterbodies (Wright,

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1963a; Brown & Wright, 1980; Magzoub & Kasim, 1980; Hazza et al., 1983; Arfaa et al., 1989). DISTRIBUTION. Western Arabia. South Yemen (Western Aden Protectorate; Wright, 1963b). Yemen Arab Republic (North Yemen; Hazza et al., 1983; Alsafadi, 1990). Saudi Arabia: coastal lowlands of mid-western and south-western regions (Azim & Gismann, 1956, B. forskalii; Arfaa, 1976; Brown & Wright, 1980; Magzoub & Kasim, 1980; Arfaa et al., 1989; Ghandour et al., 1990). PARASITES. S. haematobium: transmission in Saudi Arabia (Magzoub & Kasim, 1980; Arfaa et al., 1989; Ghandour et al., 1990) and probably the Yemens (Wright, 1963c; Hazza et al., 1983). Bulinus cernicus (Morelet, 1867, Physa). Type locality: Mauritius. Fig. 114f. 9×5 mm (may be more slender). Though formerly regarded as a form of B. forskalii (e.g. Germain, 1921a; Cowper, 1953), the last whorl of cernicus is distinctively larger in proportion to earlier whorls (Wright, 1956b, 1971; Mandahl-Barth, 1957b, 1965; Rollinson & Wright, 1984). Whorls evenly curved and almost smooth, spire commonly decollate. Differences from B. forskalii in the radula are described (Mandahl-Barth, 1957b), but variation among populations is considerable (Wright, 1971; Rollinson & Wright, 1984). Enzymes showed regional differences in Mauritius and some interpopulation differences were maintained over 6 years, but this did not seem to involve reproductive isolation (Rollinson & Wright, 1984; Rollinson, Kane et al., 1990). Strahan et al. (1991) used this species in an attempt to develop DNA probes for taxonomic purposes. Chromosome number: 2n=36 (Jelnes, 1980). HABITAT. Slowly flowing streams (Starmühlner, 1976b), various natural and man-made habitats (Courtois & Gébert, 1979), tolerating a wide range of calcium concentrations (Rollinson & Wright, 1984). Resistant to drought; snails appeared to survive in a dried habitat for 3 years (Courtois & Gébert, 1979). Capacities for both cross- and self-fertilisation, and storage of partner’s sperm for long periods are seen as adaptations to life in ephemeral waterbodies (Rollinson et al., 1989). DISTRIBUTION. Mauritius; Réunion (Barré et al., 1982). PARASITES. S. haematobium: transmission in Mauritius (reviewed by Courtois & Gébert, 1979), successful experimental infections with parasite isolates from Africa (Frandsen, 1979b,c,f; Rollinson & Wright, 1984). S. intercalatum: successful experimental infections (Wright et al., 1972; Frandsen, 1979a). S. bovis: compatible with parasite from Kenya (Rollinson & Wright, 1984). Paramphistomum phillerouxi: transmission in Mauritius (Dinnik, 1965, B. forskalii). Bulinus bavayi (Dautzenberg, 1894, Pyrgophysa). Type locality: Madagascar, near Diego Suarez. Fig. 114g. 12.5×6.5 mm. Whorls increasing in size more rapidly than in B. forskalii, less shouldered, ribs less regularly spaced (Mandahl-Barth, 1965; Wright, 1971). Immunological reactions (Wright, 1971) showed a closer relationship with B.

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cernicus. Formerly confused with B. mariei (Crosse), the name by which B. forskalii was known in Madagascar (e.g. Starmühlner, 1969). Placed by Gerlach (1987) mistakenly in the terrestrial genus Bulimus and said to have an operculum. Chromosome number: 2n=36 approximately (Wright, 1971, Fig. 2, 34). HABITAT. Shallow highly-alkaline ponds on South Island, Aldabra (Wright, 1971). Various waterbodies in Madagascar, including rice-fields and sites of considerable salinity (Degrémont, 1973). DISTRIBUTION. Madagascar: probably widespread, though occurrence has yet to be established precisely in relation to B. forskalii. Aldabra Atoll, South Island (Wright, 1971). PARASITES. S. haematobium: apparently no transmission by B. bavayi in Madagascar (Degrémont, 1973), yet snails of Aldabran origin were compatible with parasite isolates from Mauritius and Africa (Wright, 1971; Southgate & Knowles, 1975b, p. 306). Other schistosomes: experimental infections successful to varying degree with S. mattheei (Wright, 1971), S. bovis (Southgate & Knowles, 1975b) and S. margrebowiei (Southgate & Knowles, 1977b). 4) B. reticulatus group. Small snails rarely more than 6 mm high, with strongly convex whorls, a widely-reflected columellar lip and large umbilicus. This group was established by Wright (1971) for B. reticulatus and B. wrighti, partly because of their distinctive egg proteins. Chromosome number: 2n=36. Jelnes (1985) defined this group using only shell characters and added the further species hightoni, obtusispira and umbilicatus, which all are placed here in the B. africanus group. Neither B. reticulatus nor B. wrighti were included in a ‘B. reticulatus group’ within a dendrogram showing relationships according to enzyme electrophoresis (Jelnes, 1987, Fig. 3). Bulinus reticulatus Mandahl-Barth, 1954. Type locality: Kenya, Kanyakar Well near Kisumu. Fig. 114h. 7×5 mm. Shell small, broad, sometimes almost globose; whorls shouldered giving the spire a stepped appearance, with fine ribs and spiral grooves producing a reticulate pattern; columellar margin wide and umbilicus large (Mandahl-Barth, 1954a, 1957b, 1965; Van Eeden & Oberholzer, 1965; Wright, 1971). Radular teeth and copulatory organ described by Van Eeden & Oberholzer (1965). Egg proteins different from those of the B. forskalii group (Wright & Ross, 1966; Wright, 1971; Hamilton-Atwell & Van Eeden, 1981b). Chromosome number: 2n=36 (Jelnes, 1985). HABITAT. Small, briefly-filled pools; found on the Kano Plain, W Kenya only during the main rains from March to May. B. reticulatus is often the only mollusc to be found in a rainpool. DISTRIBUTION. Eastern and southern Africa; an inconspicuous species, probably yet to be found in many localities. Scattered occurrence reported for Ethiopia (Brown, 1967c), Kenya (Brown, 1980a), Tanzania (Mandahl-Barth, 1954a; Brown, 1980a), Zimbabwe (Brown, 1980a), Zambia (Mandahl-Barth, 1957b), S Mozambique (Brown, 1980a) and South Africa, where the snail is

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quite common within a central area (Van Eeden & Oberholzer, 1965; Oberholzer & Van Eeden, 1967; De Kock et al., 1974; Pretorius et al., 1974). PARASITES. S. haematobium: no evidence for natural transmission, but experimental infections achieved with parasite from Cameroon and Mauritius (Southgate & Knowles, 1975b, p. 307), and a low compatibility found between the snail and parasite from South African localities (K.De Kock, in litt. to Brown, 1993). S. intercalatum: successful experimental infection (Southgate & Knowles, 1975b, p. 307). S. bovis and S. mattheei: successful experimental infections in snails from Kenya (Southgate & Knowles, 1975b, pp. 307, 311). Echinostoma: second intermediate host in experiments (Christensen et al., 1980). Bulinus wrighti Mandahl-Barth, 1965 (B. reticulatus wrighti for B. reticulatus of Wright, 1963b). Type locality: South Yemen (formerly Western Aden Protectorate), Upper Aulaqui District at Rassais, SE of Nisab, Wadi Hatib, at about 1280 m (4000 feet), Fig. 114i. 7×5.7 mm. Usually more globose than B. reticulatus and with an even larger umbilicus. Lateral teeth of radula with a broad single cusp instead of the normally separate mesocone and endocone seen in reticulatus (Mandahl-Barth, 1965; Wright, 1971; Brown & Gallagher, 1985). Egg proteins provided further differences between the two species (Wright & Ross, 1966; Wright, 1971). Restriction enzyme analysis of DNA was performed by Rollinson & Kane (1991). Chromosome number: n=18 (Natarajan et al., 1965, ‘B. reticulatus’). HABITAT. Small pools associated with springs or collecting rain, usually among rocks and lacking aquatic vegetation; also artificial pools or cisterns (Wright, 1963b; Brown & Wright, 1980; Hazza et al., 1983; Brown & Gallagher, 1985). DISTRIBUTION. Arabia. South Yemen (Western Aden Protectorate): Hadhramaut (Connolly, 1941, B. truncatus var.) and Upper Aulaqui District (Wright, 1963b, 1971). North Yemen (Hazza et al., 1983; Al-safadi, 1990). Saudi Arabia: central and western areas (Wright, 1971; Arfaa, 1976; Brown & Wright, 1980; Arfaa et al., 1989). Oman: Jabal Akhdar and Eastern Hajar Mountains, from 200– 2000 m altitude (Brown & Gallagher, 1985) and in Dhofar at Ain Anaar, about 30 km west of Salalah (collected in 1990 by Dr M.A.Idris; Oman Natural History Museum, no. 1737). PARASITES. S. haematobium: transmission in South Yemen (Wright, 1963c, B. reticulatus) and possibly Saudi Arabia (Arfaa, 1976; Arfaa et al., 1989); successful experimental infections with many parasite isolates of different African origins (Wright, 1971; Southgate & Knowles, 1977a; Frandsen, 1979b,c,f). S. bovis: successful experimental infections (Southgate & Knowles, 1975b; Southgate, Rollinson et al., 1980, 1985; Mutani et al., 1983).

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Fig. 115. Physidae. (a) Physa acuta; Kenya, upper Tana River, Kamburu Dam. (b) Aplexa waterloti; Ghana, Bomfa. (c,d) A. waterloti; South Africa, Durban (possibly representing Physa mosambiquensis Clessin). Scale line: 5 mm.

Other schistosomes: successful experimental infections in S. curassoni (Southgate, Rollinson et al., 1985), S. intercalatum (Wright et al., 1972; Frandsen, 1979a,f), S. leiperi (Southgate et al., 1981), S. margrebowiei (Southgate & Knowles, 1977b) and S. mattheei (Wright et al., 1972). Family Physidae Medium-sized sinistral snails; spire sharply pointed, whorls smooth. Tentacles long and slender, foot pointed, pseudobranch lacking; mantle expanded to a varying extent, its margin ranging from smooth to scalloped and digitate (with finger-like processes, Fig. 12d). Shell like those of some species of Bulinus, but distinguishable by the generally more pointed spire, shallower suture and smoother surface. Anatomical differences from Bulinus include the expanded fringe of the mantle, simple penis, oblique rows of radular teeth, and the lack of both pseudobranch and blood haemoglobin. Eggs are deposited in soft elongate masses unlike the capsules of Bulinus (which are flatter, firm and circular in outline). Classification is far from stability at any level (Te, 1980; Taylor, 1988). Two subfamilies are recognised, the Physinae (with preputial gland) and Aplexinae (lacking preputial gland). Both groups are present in Africa, but it is unclear how many species occur or what are their correct names, whether the genus or species (D.W.Taylor, in litt. to Brown, 1988–93). Many African species of snail were named originally as Physa; most are now placed in Bulinus and

262 SYSTEMATIC SYNOPSIS: PULMONATES

only two true physids bear species-names given to type specimens from tropical Africa (see subfamily Aplexinae). Subfamily Physinae Preputium with a large gland visible externally as a bulge (Fig. 13b). Taylor (1988) recognised the one broad genus Physa Draparnaud, 1801 (for Bulla fontinalis Linnaeus, 1758, probably of Sweden), with several subgenera defined by differences in shell and anatomy. Snails known in Africa as Physa acuta were placed by Taylor (1988) in the subgenus Haitia Clench & Aguayo, 1932, according to examination of specimens from Kenya, Lake Naivasha (BME). Physa acuta Draparnaud, 1805. Type locality: France, River Garonne. Fig. 115a. 15×9 mm. Shell similar to Bulinus truncatus but differing in its more acute apex and smoother surface lacking ribs. In at least some African populations the mantle margin has finger-like processes in two posterior groups (Fig. 12d and Brown, 1965). Investigation is needed of the relationship with a physid found in Jordan, with apparently only one group of mantle processes (Burch, 1985, as Physella acuta). Some aspects of the anatomy, reproduction and growth of Egyptian P. acuta were described by Aboul-Ela & Beddiny (1969a,b). Careful study is needed of so-called P. acuta throughout Africa, with particular attention to supposed synonyms, e.g. P. borbonica Férussac of the Mascarene Islands (Starmühlner, 1983) and P. subopaca Lamarck of Egypt, Sinai and the Near East (Aboul-Ela & Beddiny, 1969a; Tchernov, 1971). The morphology of the spermatozoon could possibly be of taxonomic value (Brackenbury & Appleton, 1991b). HABITAT. Particularly common in both stagnant and flowing waters in or near towns, and remarkably well tolerant of pollution. In South Africa, this is an invasive species, apparently still spreading and capable of rapid migration upstream (Appleton & Branch, 1989; De Kock et al., 1989, Fig. 2). Under experimental conditions P. acuta proved superior reproductively to the indigenous Bulinus tropicus, suggesting a reason for the success of the invader (Brackenbury & Appleton, 1991c). DISTRIBUTION (Fig. 151, Chapter 11). P. acuta of authors appears to be a composite of species in Africa, all originating from the Americas and introduced by human agency. Reported from Arabia (Brown & Wright, 1980; Magzoub & Kasim, 1980), Jordan (Burch, 1985, Physella), Sinai (Tchernov, 1971, P. subopaca) and the Mediterranean countries of Africa. In the Afrotropical region known from Ethiopia (Brown, 1965), Kenya (Brown, 1980a; Clark et al., 1989; Clark & Baroudy, 1990), Cameroon (Dupouy & Mimpfoundi, 1986), Nigeria (Kristensen & Ogunnowo, 1992), Zaire (Mandahl-Barth et al., 1974; De Clercq, 1987), Zimbabwe (Brown, 1980a), Namibia (Brown, 1980a; Curtis, 1991) and South Africa (Hamilton-Atwell et al., 1970; De Kock et al., 1989). Also

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Madagascar (Brygoo, 1968), Mauritius and Réunion (early authors and Barré et al., 1982; Starmühlner, 1983, P. borbonica). PARASITES. An unconfirmed experimental infection with S. haematobium was reported (Magzoub & Kasim, 1980), but there is no other evidence that P. acuta could be a host. Echinostoma liei: snails of Egyptian origin were highly susceptible as second intermediate hosts (Christensen et al., 1980). Subfamily Aplexinae Preputial gland lacking (Fig. 13b). One or more species in Africa. The generic and subgeneric positions of African populations have yet to be firmly established. Here the recent classification in Aplexa is maintained (although a different group name may be preferable eventually). Aplexa waterloti (Germain, 1911a, Physa). Type locality: Dahomey, PortNovo. Figs 115b,c. 13×7 mm. Shell more slender than P. acuta and with shallower sutures; surface smoother, more glossy. Lack of a preputial gland was first reported by Te (1974), contrary to Ranson & Cherbonnier (1951) who described, according to my own observations, merely a swelling at the junction between the penis sheath and preputium. The egg masses are elongate and curved. Te (1974) applied the name of the Antillean species Aplexa (Stenophysa) marmorata (Guilding, 1828) to this West African physid. Although widely adopted (Danish Bilharziasis Laboratory, 1978; Van Damme, 1984; Appleton et al., 1989), this usage is probably incorrect (D.W.Taylor in litt. to Brown, 1988– 92). A slender physid found recently in South Africa (Appleton et al., 1989) possibly represents Physa mosambiquensis Clessin, 1886 (of Tette (or Tete) in Mozambique; Connolly, 1925a, 1939, and Kilias, 1961). Connolly (1945) regarded mosambiquensis and waterloti as conspecific. If so the former and older name would take precedence, but until the nature of mosambiquensis is more firmly established it seems advisable to hold this name in reserve; it was prematurely treated as a distinct species by Brown & Kristensen (1989). HABITAT. Nigerian localities were various flowing and standing waters, mostly modified by man (Thomas & Tait, 1984), especially moderately polluted shaded sites (Ndifon & Ukoli, 1989). First found in South Africa in artificial canals and ponds, and then in a natural lake (Appleton et al., 1989, p. 343, footnote). DISTRIBUTION. West Africa and south-eastern Africa. Dahomey, Togo, Ghana (mainly in the coastal region, though as far north as Bomfa near Lake Bosumptwi), Nigeria: Ibadan (Thomas & Tait, 1984) and the south-west (Ndifon & Ukoli, 1989). Mozambique and South Africa: NE Transvaal and Natal (Appleton et al., 1989).

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Notes to Figs 116–128 1. The stippled areas are intended to represent the main areas of occurrence; continuity of distribution is not implied and there may be significant discontinuities within the stippled areas. 2. The more isolated localities are indicated separately; solid circles (●) for populations living or believed to have been living when found, and open circles (○) for records of weathered ‘subfossil’ shells of uncertain age, though usually of the Late Pleistocene-Holocene period in North Africa (Van Damme, 1984).

References (for Chapters 3 and 4) An author’s work cited only in attribution of the name of a species or other taxon is not included. Aboul-Ela, I.A. & Beddiny, E.A. 1969a. Anatomical and functional studies on the reproductive system of Physa acuta Draparnaud, 1805. Proceedings of the Zoological Society of the United Arab Republic, 3:131–162. Aboul-Ela, I.A. & Beddiny, E.A. 1969b. Reproduction, embryonic development and growth of the pulmonate gastropod Physa acuta. Proceedings of the Zoological Society of the United Arab Republic, 3:163–186. Aboul-Ela, I.A. & Beddiny, E.A. 1970a. Morphological and histological studies on the genitalia of Lanistes bolteni Chemnitz, 1786. Ain Shams Science Bulletin, 13: 145–176. Aboul-Ela, I.A. & Beddiny, E.A. 1970b. On the reproductive processes and the development of Lanistes bolteni. Ain Shams Science Bulletin, 13:177–221. Aboul-Ela, I.A. & Beddiny, E.A. 1980. Factors affecting the reproductive capacity and population dynamics of Helisoma duryi (Wetherby). 1. Effect of temperature. Journal of Egyptian Parasitology, 10:135–150. Adam, W. 1957. Mollusques quaternaires de la région du Lac Edouard. Exploration du Parc National Albert, Mission J.de Heinzelin de Braucourt (1950), 3:1–172. Adanson, M. 1757. Histoire naturelle du Sénégal, Coquillages. Paris. Adegoke, O.S., Dessauvagie, T.F. & Yoloye, V.L. 1969. Biology and population dynamics of two sympatric species of Neritina from southern Nigeria. Malacologia, 9:47– 51. Ahmed, M.D., Upatham, E.S., Brockelman, W.Y. & Viyanant, V. 1986. Population responses of the snail Bulinus (P.) abyssinicus to differing initial social and crowding conditions. Malacological Review, 19:83–89. Ajao, E.A. & Fagade, S.O. 1990a. The ecology of Neritina glabrata in Lagos Lagoon, Nigeria. Archiv für Hydrobiologie, 119:339–350. Ajao, E.A. & Fagade, S.O. 1990b. The distribution and abundance of Pachymelania aurita in Lagos Lagoon, Nigeria. Archiv für Hydrobiologie, 119:475–488. Ajao, E.A. & Fagade, S.O. 1990c. Production and population dynamics of Pachymelania aurita Müller. Archiv für Hydrobiologie, 120:97–109.

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Fig. 116. Distribution in Africa of Lymnaea natalensis. This species and the closely related L. auricularia also occur in Arabia (Brown & Gallagher, 1985). Some peripheral or isolated localities are numbered. 1. Gambia and Senegal river basins (Daget, 1961; Malek & Chaine, 1987). 2. Mauritania; Agueraktem (Fischer-Piette, 1949). 3. Nigeria; Malumfashi. 4. Lake Chad (Lévêque, 1967). 5,6. Chad/Libya; Itchouma and Tejerhi (Fischer-Piette, 1948). 7. Chad; Begour Crater (Sparks & Grove, 1961). 8. Sudan; Wadi Howar (Sandford, 1936, recently living). 9. Sudan; Zalingei. 10. Sudan; Erkowit (Tothill, 1946). 11. Ethiopia; Assaita and Harar. 12,13. Somalia; Nogal River (Connolly, 1928a) and Uebi River (Bacci, 1951). 14. Kenya; Marsabit (Verdcourt, 1960b). 15. Zanzibar (Mozley, 1939). 16. Namibia; Cunene and Okavango rivers (Oberholzer, 1970; Brown, Curtis et al., 1992). 17. Namibia; Gobabis (L. damarana Boettger). 18,19. South Africa: Upington and Knysna districts (Van Eeden & Combrinck, 1966). 20. South Africa; Wepener district (De Kock et al., 1974). 21. South Africa; Breede River (Van Bruggen, 1970a). 22. Comoro Islands (Starmühlner, 1983; Julvez et al., 1990) and Madagascar (Fischer-Piette & Vukadinovic, 1973, L. hovarum). Van Damme (1984) gives additional Late Pleistocene-Holocene sites for subfossil shells in the Sahara and a few old records in N Algeria and Tunisia for living populations, which may now be extinct.

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Fig. 117. Distribution of Lymnaea truncatula in Africa, Arabia, the Near East and southern Europe (partly after Hubendick, 1951). Some discrete areas and peripheral or isolated localities are numbered. 1. Morocco: Agadir and Asni (DBL). 2. Algeria; Ahaggar (Sparks & Grove, 1961) and other Late Pleistocene-Holocene sites (Van Damme, 1984). 3. Egypt; Cairo and Beheira districts (DBL). 4. Israel: Lake Tiberias (DBL) and Jordan (Burch, 1985). 5. Egypt; Baharia Oasis (Malek, 1958). 6. Egypt; oases of Dakhla and Kharga (Malek, 1958). 7. Chad; Tibesti (Chaix, 1974). 8. North Yemen and South Yemen; highland areas (Wright, 1963b; Arfaa, 1972). 9. Ethiopia; highlands (Brown, 1965; Goll & Scott, 1979). 10. Kenya; central highlands. 11. Zaire; Blukwa (Dartevelle, 1952b) and Kisenyi (DBL). 12. Tanzania; Lushoto (DBL). 13. Namibia; Gobabis (L. subtruncatula) 14. South Africa; Vryburg (Connolly, 1939). 15–20. South Africa; Stellenbosch, Beaufort West, Rouxville, Potchefstroom, Lydenberg, and Umlaas (Connolly, 1939; Van Eeden et al., 1965; De Kock et al., 1974) and widespread in Lesotho (Prinsloo & Van Eeden, 1973b).

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Fig. 118. Distribution of Burnupia. On present evidence there is little justification for maintaining most of the many named species; the whole range might be inhabited by the one variable species B. caffra. Some peripheral or isolated localities are numbered. 1–4. Ethiopia; Gorgora, Debra Berhan, Adolla and Wolisso (Brown, 1965). 5. Angola; Salazar (Wright, 1963a). 6. Lake Mweru at Lukonzolwa (Dautzenberg & Germain, 1914). 7. Lake Tanganyika (Leloup, 1953). 8. Lake Edward (Pilsbry & Bequaert, 1927). 9. Kenya; highlands. 10. Tanzania; Mbeya. 11,12. Zimbabwe; Inyanga and Matopos. 13,14. E Transvaal; Kruger National Park (Oberholzer & Van Eeden, 1967) and Soutpansberg (Connolly, 1939). 15. Natal; Lake Sibaya (Appleton, 1977c). 16. lower Orange River (De Kock et al., 1974). 17–19. Great Namaqualand, Ngamiland and Kamanyab (Connolly, 1939, B. trapezoidea). 20. Namibia; Naukluftberge (State Museum, Windhoek).

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Fig. 119. Distribution of Ceratophallus natalensis (after Brown & Mandahl-Barth, 1973, with additional localities). Although the range is shown to include the tropical eastern coast, this species seems uncommon in much of this region. Some peripheral or isolated localities are numbered. 1. Lake Chad. 2. W Zaire. 3,4. E Zaire. 5–8. Ethiopia; Asmara district, Jimma, Lake Abaya (Margherita) and highland west of Harar (Brown, 1965). 9. Upper Lufira and Luapula regions (Mandahl-Barth, 1968a). 10. South Africa; lower Orange River (De Kock et al., 1974). 11. Anjouan (Starmühlner, 1976a, Ceratophallus sp.).

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Fig. 120. Distribution of Lentorbis. Some peripheral or isolated localities are numbered; species identified as L. junodi unless indicated otherwise. 1. Lake Chad (DBL, L. benguelensis). 2. W Zaire (Mandahl-Barth et al., 1974, L. benguelensis). 3. SE Zaire (Mandahl-Barth et al., 1972). 4. Lake Albert at Butiaba (Mandahl-Barth, 1954a). 5. S Sudan (Mandahl-Barth, 1973a; Brown et al., 1984). 6. Kenya; Tana River, pools at Galole (Hola). 7. Ethiopia; Lakes Awasa and Zwai. 8. Ethiopia; Ciaffa swamp, south of Kombolchia (Brown, 1965). 9. Zanzibar (Mozley, 1939). 10. Angola; Benguela (L. benguelensis). 11. Lake Malawi; Monkey Bay. 12. Mozambique; Sena (Azevedo et al., 1961). 13. E Transvaal; Kruger National Park (Oberholzer & Van Eeden, 1967, L. carringtoni). 14. Natal; Lakes Sibaya and Ngoboseleni (Appleton, 1977c). 15. Natal; Durban, Mhlangana River (Brown, 1967a). 16. Madagascar; Ilakatra (DBL, genus needs confirmation).

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Fig. 121. Distribution of Segmentorbis kanisaensis. Some peripheral or isolated localities are numbered. 1. Gambia (Smithers, 1956). 2. Sierra Leone (Hubendick, 1977). 3. Nigeria; Kainji district (Walsh & Mellink, 1970). 4. Niger; between Tara and Gaya (DBL). 5. Chad; Lake Léré (Dejoux et al., 1971). 6. Sudan; Kanisa (type locality). 7,8. Ethiopia; Ciaffa swamp, south of Kombolchia (Brown, 1965) and Lake Awasa. 9. Kenya; Galole (Hola). 10. Pemba (DBL). 11. Angola; near Luanda (Wright, 1963a). 12. SE Zaire; Lac de Retenue (Mandahl-Barth et al., 1972). 13. E Transvaal; Kruger National Park (Oberholzer & Van Eeden, 1967). 14,15. South Africa; Tongaland (Appleton, 1977c) and Durban (Brown, 1967a), 16. Namibia; Okavango River at Rundu (Brown, Curtis et al., 1992).

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Fig. 122. Distribution of the Biomphalaria pfeifferi group and of B. alexandrina (localities 1 and 15 only). Eastern limit of B. pfeifferi in Tanzania after Sturrock (1965a). The shaded area in Arabia represents scattered localities for living and for extinct populations, including those recorded as B. arabica. Some peripheral or isolated localities are numbered. 1. Libya; Taourga (Doumenge et al., 1987, B. alexandrina). 2. Libya; Tejerhi (FischerPiette, 1948). 3,4. Algeria; Tassili N’Ajjar (B. germaini Ranson, 1953) and Tin Tahart (Pallary, 1934). 4a. Algeria; Tabelbala (Chevallier, 1969). 5. Mauritania and NW Niger; many localities (Fischer-Piette, 1949). 6. Niger; Air (Fischer-Piette, 1948). 7. Chad; Largeau (Faya) (Ranque & Rioux, 1963). 8. Sudan; Wadi Howar (Sandford, 1936, recently living). 9. Lower Senegal Basin (Diaw, 1980; Diaw et al., 1990; Malek & Chaine, 1981; Talla et al., 1990). 9b. Mali; Kedougou (Schneider & Malek, 1984). 10. Mali; Bandiagara (Sellin et al., 1980; Madsen et al., 1987). 11. Nigeria; Funtua. 12. Lake Chad (Lévêque, 1967; Brown, 1974). 13. Sudan; Jebel Marra (Malek, 1958, p. 727). 14. Sudan; Zeidab (Malek, 1958) and Gezira area (Williams & Hunter, 1968; Madsen et al., 1988). 15. Egypt; delta and southwards to Lake Nasser (Vrijenhoek & Graven, 1992). 16. Israel; Yarkon River (probably extinct). 17. Sudan; Erkowit (Tothill, 1946). 18. Ethiopia; Asmara district (Brown, 1965; Itagaki et al., 1975). 19. Ethiopia; Assaita (B. barthi, subfossil). 20. Somalia; Hargeisa district (Ayad, 1956). 21,22. Kenya; Marsabit and Kibwezi. 23. Tanzania; Dodoma district (Sturrock, 1965a). 24. Mozambique; Nyassa Province, above 1000 m (Azevedo et al., 1961). 25. Angola; Vila da Ponte (Wright, 1963a). 26. Botswana, Lake Ngami (Connolly, 1939) and Okavango Delta (Brown, Gurtis et al., 1992). 27. South Africa; Taung district (Van Eeden & Combrinck, 1966). 28–30. South Africa; Lydenburg, Pietermaritzburg and Port St Johns (Van Eeden et al., 1965). 31. Namibia; Okaputa Pan (B. hermanni). 32. Madagascar; widespread (Fischer-Piette & Vukadinovic, 1973).

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Fig. 123. Distribution of the Biomphalaria sudanica group. Some peripheral or isolated localities are numbered. B. sudanica. 1. Lake Chad (Lévêque, 1967). 2. Sudan; Kosti (Mandahl-Barth, 1960) and Jebel Aulia (Williams & Hunter, 1968). 3. Ethiopia; lakes Zwai, Awasa and Abaya (Margherita) (Brown, 1965; Itagaki et al., 1975). 4,5. Kenya; lakes Naivasha and Jipe (Brown et al., 1981). 6. Tanzania; Arusha (Sturrock, 1965a). 7. N Zambia (MandahlBarth, 1960, B. s. rugosa). 8. SE Zaire; Lac de Retenue (Mandahl-Barth et al., 1972). 9. Zaire; Kongolo (Mandahl-Barth, 1957a). Van Damme (1984) gives Late PleistoceneHolocene sites in Sudan, Chad and Niger. B. camerunensis. 10. Ghana; Kumasi (McCullough, 1965a). 11,12. Cameroon; southern equatorial zone (Wright, 1965; Greer et al., 1990). 13,14. Zaire; Banzyville and Kisangani (B. c. wansoni). 15. Zaire; lower region including Kinshasa (Mandahl-Barth et al., 1974). B. salinarum. 16. Angola; Malange district (Wright, 1963a). 17. Namibia; Grootfontein (a doubtful record; Brown, Curtis et al., 1992).

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Fig. 124. Distribution of some members of the Bulinus africanus group; the largest shaded area represents the combined ranges of B. africanus, B. globosus and B. ugandae. It is noteworthy that no subfossil shells have been reported from the Sahara. Some peripheral or isolated localities are numbered. 1. Lower Senegal basin (Diaw. 1980; Chaine & Malek, 1981; B. globosus). 2. Mali; Niger River, Goundam (Madsen et al., 1987; B. globosus). 3. Lake Chad (Betterton, 1984a; B. globosus). 4. Sudan; Ed Dueim (Malek, 1958; B. ugandae). 5,6. Ethiopia; Medhanie Alem and Jimma district (Brown, 1965; B. africanus). 7. Ethiopia; Lake Abaya (Margherita) (Brown, 1965, B. ugandae). 8. Ethiopia; lower Awash River (Brown & Lemma, 1970, B. abyssinicus). 9. Somalia; lower Uebi River basin (Mandahl-Barth, 1960 and Arfaa, 1975; B. abyssinicus). 10. Kenya; Bungoma district (B. africanus). 11. Kenya; Tana River, Galole irrigation scheme (B. globosus). 12. Namibia; Cunene River (Oberholzer, 1970, Fig. 84, Physopsis sp.). 13. Namibia and Botswana; lower Okavango and delta (Brown, Curtis et al., 1992, B. globosus). 14. Botswana; Machudi (B. globosus). 15,16. South Africa; districts of Warrenton and Lydenburg (Van Eeden & Combrinck, 1966, B. (Physopsis) sp.). 17. South Africa; Newcastle (Brown, 1966, B. africanus). 18. South Africa; Humansdorp (Van Eeden et al., 1965, B. (Physopsis) sp.). 19. Zanzibar and Pemba (Mozley, 1939, B. globosus). 20. Madagascar; western region (B. obtusispira).

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Fig. 125. Distribution of some members of the Bulinus africanus group. Some peripheral or isolated localities are numbered. 1–6. B. umbilicatus. 1. Mauritania; Kiffa (Mandahl-Barth, 1973b). 1a. Reported from the Senegal and Gambia river basins (Albaret et al., 1985; Jelnes, 1986; Diaw & Vassiliadès, 1987; Kristensen & Christensen, 1989). 2. Mali; Mopti (DBL) and Bandiagara (Madsen et al., 1987). 3. Niger; Gaya (DBL). 4. Nigeria; Yau. 5. Sudan; Kordofan, Leghareh district 6. Chad; Wadi Tourba, Ennedi Mountains. 7,8. B. obtusus. Chad; Fort Lamy and Goz Beida (Mandahl-Barth, 1973b). 9–13. B. nasutus; localities after Mandahl-Barth (1960, 1965). 9. Uganda; Lango district. 10. Tanzania; Shinyanga. 11. Kenya; Kitui. 12,13. Tanzania; Mbarali and Tunduma. 14. B. hightoni. Kenya; Galole (Hola) district.

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Fig. 126. Distribution of the Bulinus natalensis/tropicus complex. Shaded areas represent the main areas occupied by populations known or thought likely to be diploid. It seems likely that this diploid complex is more widespread, particularly in Angola and Zaire. Some peripheral or isolated localities are numbered. 1–4. Ethiopia; Lake Ashangi, Dangila, Dodola and Langei (Brown & Burch, 1967; Brown & Wright, 1972). 5. South Africa; Christiana (Brown et al., 1967). 6a. Botswana; Gabarones. 6b. Central Namibia (Brown et al., in preparation). 6c. lower Okavango River and East Caprivi (Brown, Curtis et al., 1992; probably diploid). 7. Zimbabwe; Bulawayo (Wright & Brown, 1972). 8. Tanzania; Mwanza and Usagara (Burch, 1964). 9–11. Kenya; Maralal district, Mount Kenya and Lake Jipe (Brown et al., 1991). 12. Kenya; Marsabit (Verdcourt, 1960; probably diploid). 13. W Cameroon, above 1000 m (Mimpfoundi & Greer, 1990c). 14. Madagascar; Basibasy (Wright, 1971, B. liratus) and probably widespread.

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Fig. 127. Distribution of the tetraploid species Bulinus truncatus. Some peripheral or isolated localities are numbered; chromosome number is known for the southern localities 25–33, but not for all of those further north. 1–4. Near East. 1. Iran; Bandar Anzali (Mansoorian & Kristensen, 1992). 2. Syria, Iraq and Iran; Euphrates Valley and Khuzistan region of W Iran (Doumenge et al., 1987). 3. Israel; Ramleh (Mienis, 1977). 4. Jordan; sites reviewed by Burch (1985). 5–8. Arabia. 5. Saudi Arabia; scattered localities in western regions (Arfaa, 1976; Brown & Wright, 1980; Arfaa et al., 1989; Ghandour et al., 1990). 6. North and South Yemen (Wright, 1963b; Arfaa, 1972, 1976; B. yemensis Paggi et al., 1978; Hazza et al., 1983; Alsafadi, 1990). 7,8. Saudi Arabia (subfossil; Azim & Gismann, 1956). 9–14. Europe. 9. Portugal; Algarve (Grácio, 1983). 10. Spain; authors cited by MandahlBarth (1965, under B. contortus). 11. France; between Collioures and Port Vendres (type locality for B. contortus). 12. Sardinia (Arru et al., 1980) and Corsica (Orecchia et al., 1981). 13. Sicily; type locality of several synonyms named in the nineteenth century (Mandahl-Barth, 1965); apparently extinct. 14. Greece; Kalamata and Crete (Larambergue, 1939, p. 118). 15–24. North Africa; for additional localities in the Sahara, mostly Late PleistoceneHolocene, see Van Damme (1984). 15. Algeria; Hoggar (Ahaggar) and Djanet (Fort Charlet) (Larambergue, 1939, p. 99). 16. Algeria; Anefid (Chevallier, 1969). 17. Libya; Sebha region (Itagaki & Yasuraoka, 1975). 18,19. Mauritania; Atar district and Tagent Plateau (Brown, 1980a). 20. Niger; Aïr (Fischer-Piette, 1948). 21. Chad; Largeau (Faya) (Ranque & Rioux, 1963). 22. Sudan; Jebel Marra (Malek 1958). 23. Egypt; Lake Nasser (Doumenge et al., 1987). 24. Egypt; Kharga, Dakhla and Baharia oases. 25–33. Tropical Africa. 25. Ethiopia; Eritrea (Brown & Burch, 1967). 26,27. Ethiopia; Lake Abaya (Margherita) (Brown & Wright, 1972) and middle Awash valley (Kloos & Lemma, 1974). 28. Kenya; Kitui district (Jelnes & Ouma, 1981) and Lake Naivasha (Brown & Shaw, 1989, p. 514). 29. Tanzania; Mwanza area (Brown, 1980a). 30. Malawi; Karonga (Mandahl-Barth et al., 1976). 31. lower Zaire (Mandahl-Barth et al., 1974). 32. Tanzania; Ujiji (Brown et al., 1982, B. coulboisi). 33. Malawi; near Blantyre (Brown & Rollinson, 1982).

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Fig. 128. Distribution of Bulinus forskalii. Some peripheral or isolated localities are numbered. 1. Libya; Tejerhi (Fischer-Piette, 1948). 2. Mali; El Guettara (Fischer-Piette, 1949). 3. Niger; Air, Tarouadji Mountains (Fischer-Piette, 1948). 4. Basins of Rivers Gambia (Goll, 1981) and Senegal (Diaw, 1980; Malek & Chaine, 1981). 4a. Mali; Niger Basin (Sellin et al., 1980; Madsen et al., 1987). 5. Nigeria; Kano area (Betterton, Ndifon et al., 1988). 6. Lake Chad (Lévêque, 1967; Betterton, 1984a). 7. Sudan; Zalingei (Brown, 1980a). 8. Sudan; Zeidab (Malek, 1958) and Gezira irrigated area (Madsen et al., 1988). 9. Egypt; between Luxor and Suez (Malek, 1958). 10. Ethiopia; NE Eritrea (Bacci, 1951). 11. Ethiopia; Awash River Basin (Brown & Lemma, 1970). 12. Somalia; lower Uebi Shebeli (Arfaa, 1975). 13. Okavango Basin; B. forskalii is reported but only B. scalaris was identified recently (Brown, Curtis et al., 1992). 13a. Angola; Cuanza River valley (Wright, 1963a). 14. South Africa; Pretoria (Connolly, 1939). 15–18. South Africa; NE of Ermelo, Mooi River, Port St Johns and Mossel Bay (Van Eeden et al., 1965). 19,20. South Africa; Upington and Okiep districts (De Kock et al., 1974). 21. Madagascar; widespread (Fischer-Piette & Vukadinovic, 1973, B. mariei). 22. São Tomé (Brown, 1991). Van Damme (1984) gives additional Late Pleistocene-Holocene sites in Mauritania, Chad, Sudan and Egypt. Note: there are considerable discontinuities within the main range, e.g. B. forskalii is not found in the cooler highland areas, and its south-western distribution is uncertain because of likely confusion with B. scalaris.

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White, P.T., Gbakima, A.A. & Amara, S.V. 1989. Schistosoma mansoni in Sierra Leone: an invader extending its range? Annals of Tropical Medicine and Parasitology, 83: 191– 193. Wibaux-Charlois, M., Yelnik, A., Ibrahima, H., Samé-Ekobo, A. & Ripert, C. 1982. Etude epidémiologique de la bilharziose à S. haematobium dans le perimètre rizicole de Yagoua (Nord-Cameroun). 2. Distribution et écologie des hôtes intermédiaires. Bulletin de la Société de Pathologie exotique, 75:72–93. Williams, N.V. 1970a. Studies on aquatic pulmonate snails in central Africa. 1. Field distribution in relation to water chemistry. Malacologia, 10:153–164. Williams, N.V. 1970b. Studies on aquatic snails in central Africa. 2. Experimental investigation of field distribution patterns. Malacologia, 10:165–180. Williams, S.N. & Hunter, P.J. 1968. The distribution of Bulinus and Biomphalaria in Khartoum and Blue Nile provinces, Sudan. Bulletin of the World Health Organisation, 39:949–954. Williamson, P.G. 1985. A first record of Potadoma (Swainson) from eastern Africa. Journal of Conchology, 32:135–139. Winterbourn, M. 1970. The New Zealand species of Potamopyrgus. Malacologia, 10: 283– 321. Winterbourn, M. 1972. Morphological variation of Potamopyrgus jenkinsi (Smith) from England and a comparison with the New Zealand species, P. antipodarum (Gray). Proceedings of the Malacological Society of London, 39:139–149. Wium-Andersen, G. 1973. Electrophoretic studies on esterases of some African Biomphalaria spp., etc . Malacologia, 12:115–122. Wium-Andersen, G. 1974. A systematic examination of a Biomphalaria species from Namibia by means of esterase electrophoresis. Steenstrupia, 3:183–186. Woolhouse, M.E.J. 1988. Passive dispersal of Bulinus globosus. Annals of Tropical Medicine and Parasitology, 82:315–317. Woolhouse, M.E.J. 1989. On the interpretation of age-prevalence curves for schistosome infections of host snails. Parasitology, 99:47–56. Woolhouse, M.E.J. & Chandiwana, S.K. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology, 98:21–34. Woolhouse, M.E.J. & Chandiwana, S.K. 1990a. Population biology of the freshwater snail Bulinus globosus in the Zimbabwe highveld. Journal of Applied Ecology, 27: 41–59. Woolhouse, M.E.J. & Chandiwana, S.K. 1990b. Population dynamics model for Bulinus globosus, intermediate host for S. haematobium, in river habitats. Acta Tropica, 47:151– 160. Woolhouse, M.E.J. & Taylor, P. 1990. Survival rates for Bulinus globosus during aestivation. Annals of Tropical Medicine and Parasitology, 84:293–294. Worthington, E.B. 1929. A Report on the Fishing Survey of Lakes Albert and Kyoga. London: Crown Agents. Wright, C.A. 1956a. The anatomy of six species of the molluscan genus Bulinus (Planorbidae) from Senegambia. Proceedings of the Malacological Society of London, 32: 8–105. Wright, C.A. 1956b. Bulinus (Pyrgophysa) forskalii (Ehrenberg) as a vector of S. haematobium. Nature, London, 177:43.

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Wright, C.A. 1957. Studies on the structure and taxonomy of Bulinus jousseaumei (Dautzenberg). Bulletin of the British Museum (Natural History), Zoology, 5:1–28. Wright, C.A. 1959. A note on the distribution of Bulinus senegalensis. West African Medical Journal, 8:142–148. Wright, C.A. 1961. Taxonomic problems in the molluscan genus Bulinus. Transactions of the Royal Society of Tropical Medicine and Hygiene, 55:225–231. Wright, C.A. 1963a. The freshwater gastropod Mollusca of Angola. Bulletin of the British Museum (Natural History), Zoology, 10:449–528. Wright, C.A. 1963b. The freshwater gastropod molluscs of Western Aden Protectorate. Bulletin of the British Museum (Natural History), Zoology, 10:257–274. Wright, C.A. 1963c. Schistosomiasis in the Western Aden Protectorate; a preliminary survey. Transactions of the Royal Society of Tropical Medicine and Hygiene, 57: 142– 147. Wright, C.A. 1965. The freshwater gastropod molluscs of West Cameroon. Bulletin of the British Museum (Natural History), Zoology, 13:75–98. Wright, C.A. 1971. Bulinus on Aldabra and the subfamily Bulininae in the Indian Ocean area. Philosophical Transactions of the Royal Society of London, B, 260:299–313. Wright, C.A. 1977. Co-evolution of bulinid snails and African schistosomes. In Medicine in a Tropical Environment: 291–300. Gear, J.H. (Ed.). Capetown: Balkema. Wright, C.A. & Brown, D.S. 1962. On a collection of freshwater gastropod molluscs from the Ethiopian highlands. Bulletin of the British Museum (Natural History), Zoology, 8:285–312. Wright, C.A. & Brown, D.S. 1980. The freshwater Mollusca of Dhofar. Journal of Oman Studies, Special Report No. 2:97–102. Wright, C.A. & Rollinson, D. 1979. Analysis of enzymes in the Bulinus africanus group by isoelectric focusing. Journal of Natural History, 13:263–273. Wright, C.A. & Rollinson, D. 1981. Analysis of enzymes in the Bulinus tropicus/ truncatus complex. Journal of Natural History, 15:873–885. Wright, C.A. & Ross, G.C. 1965. Electrophoretic studies of some planorbid egg proteins. Bulletin of the World Health Organisation, 32:709–712. Wright, C.A. & Ross, G.C. 1966. Electrophoretic studies on planorbid egg proteins. The Bulinus africanus and B. forskalii species groups. Bulletin of the World Health Organisation, 35:727–731. Wright, C.A. & Southgate, V.R. 1976. Hybridization of schistosomes and some of its implications. Symposia of the British Society for Parasitology, 14:55–86. Wright, C.A., Klein, J. & Eccles, D.H. 1967. Endemic species of Bulinus in Lake Malawi. Journal of Zoology, London, 151:199–209. Wright, C.A., Rollinson, D. & Goll, P.H. 1979. Parasites in Bulinus senegalensis and their detection. Parasitology, 79:95–105. Wright, C.A., Southgate, V.R. & Howard, G.W. 1979a. Observations on the life cycle of Schistosoma margrebowiei and its possible interactions with S. leiperi in Zambia. Journal of Natural History, 13:499–506. Wright, C.A., Southgate, V.R. & Howard, G.W. 1979b. A note on the life cycles of some amphistome flukes in Zambia. Journal of Helminthology, 53:251–252. Wright, C.A., Southgate, V.R. & Knowles, R.J. 1972. What is Schistosoma intercalatum Fisher, 1934? Transactions of the Royal Society of Tropical Medicine and Hygiene, 66:28– 64.

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Wu, S.K. 1972. Comparative studies on a polyploid series of the African snail genus Bulinus. Malacological Review, 5:95–164. Wu, S.K. & Burch, J.B. 1975. Bulinus sericinus from Ethiopia. Malacological Review, 8: 31–46. Wurzinger, K.H. 1979. Allozymes of Ethiopian Bulinus sericinus and Egyptian B. truncatus. Malacological Review, 12:51–58. Wurzinger, K.H. & Saliba, E.K. 1979. A cytological and electrophoretic comparison of Jordanian Bulinus with three other tetraploid Bulinus populations. Malacological Review, 12:59–65. Yoloye, V. & Adegoke, O.S. 1977. A new species of Neritina, etc. from the Lagos Lagoon. Malacologia, 16:303–309. Yousif, F. & Ibrahim, A. 1978. The first record of Angiostrongylus cantonensis from Egypt. Zeitschrift für Parasitenkunde, 56:73–80. Zumstein, A. 1983. A study of some factors influencing the epidemiology of urinary schistosomiasis at Ifakara (Kilombero District, Tanzania). Acta Tropica, 40: 187–204.

Chapter 5. Snails and schistosomes

Schistosomiasis (Bilharziasis) is a parasitic infection of various mammals including man and domestic livestock, caused by ‘blood-flukes’ of the genus Schistosoma. Two hundred million people are estimated to be infected and a further 500–600 million people at risk (Doumenge et al., 1987; World Health Organisation, 1993). The most extensive areas of infection are in Africa, China and the neotropics. A comprehensive general account of schistosomiasis is provided by Jordan & Webbe (1982) and Jordan et al. (1993); particular aspects of the biology of the parasites and hosts are considered in specialised reviews (Loker, 1983; Rollinson & Simpson, 1987; Basch, 1991). The adult worms of African species live in the abdominal blood system of their mammalian (definitive) hosts, usually in veins associated with the intestine or those around the bladder. Schistosome eggs pass through the wall of the intestine or bladder and are voided with the faeces or urine. If the eggs fall into water they hatch, producing a ciliated swimming larva (miracidium) that must within a few hours locate and penetrate a suitable snail. In Africa this snail belongs to the family Planorbidae, a species of Biomphalaria for the common parasite of the intestinal venous system (S. mansoni), and a Bulinus for the common parasite of the bladder (S. haematobium). Development within the snail proceeds through two generations of sporocysts; the second one produces many cercariae, which eventually break free from the snail and swim in the water seeking a definitive host. The time from penetration by the miracidium to the shedding of cercariae is termed the prepatent period or cercarial incubation period. This lasts for a minimum of about 3 weeks under favourable conditions, and varies widely according to the host/parasite combination and environmental factors, especially temperature (reviewed by Loker, 1983). Multiplication within the sporocysts can result in several thousands of cercariae developing from a single miracidium. An individual snail may shed cercariae for several months, more or less continuously (Fryer & Probert, 1988). Cercariae emerge from many of the snail’s organs, especially the mantle collar and pseudobranch, rupturing the epithelium and causing loss of haemolymph (Pan, 1965). They penetrate the skin of the mammalian host and migrate through the host’s blood circulatory system, meanwhile developing into mature worms.

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The sexes are separate, though the mature worms remain permanently paired, with the male carrying the more slender female, which grows to 2–3 cm long in some species. The preparent period from infection of the mammalian host to the first appearance of eggs in its excreta varies widely according to species of schistosome (Loker, 1983; Basch, 1991); it may be as short as 35 days for S. mansoni, but about twice as long for S. haematobium. Some mammals including man may be infected naturally by more than one species of schistosome. This can be achieved in rodents, which serve as hosts in the laboratory, in order to produce pairing between worms of different species. The infectivity of hybrid miracidia to snails can then be tested. The production of cercariae from an individual snail during a 24 hour period fluctuates widely, with a rhythm characteristic of each schistosome species (and which perhaps varies among some conspecific strains). Usually there is a single main peak of cercarial emergence, more rarely two (in S. margrebowiei). The timing of the main peak(s) appears adapted to the behavioural patterns of the main definitive hosts, thereby increasing the chances of host-parasite contact. S. haematobium is reported to show a ‘shadow response’, whereby the emergence of cercariae could be stimulated by the change in light intensity caused by a person’s shadow falling on a snail. Raymond & Probert (1991) reviewed work on the daily emission rhythms of cercariae; specific references are cited under the appropriate schistosome later in this chapter. It is difficult to diagnose schistosome infection from the external appearance of a snail. Investigators commonly wait for field-collected snails to shed cercariae in the laboratory. A better estimate of prevalence of infection can be obtained by crushing snails and examining them by means of a simple device incorporating a magnifier (Teesdale et al., 1986). Schistosome cercariae of ‘mammalian type’ can be rapidly distinguished from other types of cercariae (Frandsen & Christensen, 1984), but the specific identification of those infective to man requires more elaborate techniques. Enzyme analysis may be helpful (Mahon & Shiff, 1978) and also cercarial surface structure (Albaret et al., 1985), but passaging the parasite through a mammalian host in the laboratory is desirable to confirm an identification. Ten species of Schistosoma are currently recognised to occur in Africa; they are listed in Table 5.1 with notes on definitive and intermediate hosts. Identification is based on egg shape, morphological characters of adult worms and cercariae, timing of cercarial emergence (Mouchet et al., 1992; Véra et al., 1992) and molecular characters. Insights into relationships among species and of variation within species are provided by studies of enzymes (Ross et al., 1987; Rollinson & Southgate, 1987) and increasingly by molecular analyses (Simpson, 1987; Johnston et al., 1993). Enzyme analysis has been helpful for identifying larval stages of schistosomes and other digenean parasites in field-collected snails (Mahon & Shiff, 1978; Wright, Rollinson & Goll, 1979; Southgate, Brown et al., 1989).

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The species may be grouped according to whether the position of the egg spine is terminal (the S. haematobium group) or lateral (S. mansoni group). The S. mansoni group develops only in Biomphalaria, whereas the S. haematobium group develops almost entirely in Bulinus. Early claims that S. haematobium was transmitted by Planorbarius in Portugal and Morocco have not been substantiated, but this snail was found to transmit S. bovis in Spain (RamajoMartin, 1972) and may do so in NW Africa (Southgate, Wright et al., 1984). The limpet Ferrissia is reputed to carry S. haematobium in a small focus in India (Southgate & Agrawal, 1990), but though common in Africa Ferrissia is not implicated there in transmission of any schistosome. Reports of schistosome infections in African snails belonging to other genera (e.g. Porter, 1938) have not been confirmed. To understand host-specificity, the outcome of complex interactions between schistosomes and their snail hosts depends on gaining knowledge of genetic variation in both organisms (Rollinson & Southgate, 1985); enzyme analyses are contributing valuable information, but linkage has not yet been Table 5.1 The Schistosoma species found in Africa and the Near East, their main mammalian (definitive) hosts and snail (intermediate) hosts involved in natural transmission. For reviews, see Pitchford (1977), Christensen et al. (1986) and Rollinson & Southgate (1987). Schistosome

Main mammalian hosts

Snail host: genus or species group

Man

Bulinus spp. of several groups B. africanus group and B. forskalii group Bulinus spp. of several groups Planorbarius (in Spain) Bulinus africanus group

S. haematobium group S. haematobium (Bilharz, 1852) S. intercalatum Fisher, 1934

Man

S. bovis (Sonsino, 1876)

Cattle

S. mattheei Veglia & Le Roux, 1929 S. curassoni Brumpt, 1931

Cattle, sheep

S. margrebowiei Le Roux, 1933 S. leiperi Le Roux, 1955 S. mansoni group S. mansoni Sambon, 1907 S. rodhaini Brumpt, 1931 S. edwardiense Thurston, 1964

Cattle, sheep

B. africanus group and B. forskalii group Antelopes, cattle, goat Bulinus natalensis/tropicus complex. B. forskalii group Antelopes, cattle, sheep B. africanus group Man Rodents Hippopotamus

Biomphalaria spp. Biomphalaria spp. Biomphalaria sp.

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Schistosome

Main mammalian hosts

Snail host: genus or species group

S. hippopotami* Thurston, 1963

Hippopotamus

Unknown

* possibly a senior synonym of S. edwardiense; Pitchford & Visser, 1981

established between enzyme markers and genes controlling infectivity or susceptibility. Comparative study of quantitative information about reproduction by schistosomes led Loker (1983) to postulate a degree of integration between different stages in the life-cycle not previously appreciated. The number of cercariae produced by snails is positively correlated with snail size, and comparisons among species suggest that low rates of cercarial production in the snail host may be compensated for by rapid rates of egg production in the definitive host. For example, Loker pointed out that the rapid egg production of S. margrebowiei might compensate for the limited cercaria-producing potential of its snail hosts in nature, B. forskalii and B. scalaris, which are small and whose shedding period may be restricted by their type of habitat, commonly small ephemeral pools. Conceivably there are differences in reproductive strategy between different strains of a schistosome such as S. haematobium according to whether development occurs in a small or a large species of Bulinus. To confirm or refute such relationships, further information is needed on the quantitative aspects of cercarial production from infected snails in nature. Host finding by miracidia Schistosome miracidia remain infective for about 8–12 hours and snails can be infected over a distance of at least 5 m from a source of miracidia (Jordan & Webbe, 1982, p. 56). A generalised plan of behaviour (Wright, 1959, 1971; reviews by Christensen, 1980, and Jourdane & Théron, 1987) envisages a first phase of responses to physical stimuli of the environment, which tend to bring the miracidium into the area of habitat frequented by a snail host. There follow chemotactic responses to substances of snail origin, though a positive response is not necessarily limited to a compatible species. Although miracidial behaviour is correlated with the ecology of a potential snail host (Wright, 1962, 1966), many miracidia may perish through attraction to an unsuitable ‘decoy’ snail (Frandsen, 1976). Shiff (1969, 1974) studied the S. haematobium miracidium in aquaria and outdoor experimental ponds in Zimbabwe and found that the response to light was influenced by temperature. Miracidia were photonegative under warm conditions, but became photopositive below 15°C. In a natural habitat during the summer (temperature 20–30°C) infection of Bulinus globosus occurred on the bottom or in shade at the surface, while in winter (2–22°C) snails were mostly infected near the surface. Miracidial behaviour thus was related to the seasonal

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habits of the snail, which in summer frequented the cool pond bottom, but in winter usually basked at the warmer surface. Establishment of miracidia in snails; assessment of compatibility The miracidium penetrates a snail’s epithelium with the aid of histolytic secretion. Successful establishment in the snail depends on surviving the host’s defences, which are both cellular and humoral (Bayne & Loker, 1987; van der Knaap & Loker, 1990; Preston & Southgate, 1994), the outcome of coevolution between parasite and host (Wright & Southgate, 1981). Further attention is given at the end of this chapter to resistance by snails to infection. Many publications give rates of infection obtained by exposing snails to infection with schistosomes in the laboratory, but comparisons among studies often are impossible because of lack of standardisation (discussed by Frandsen, 1979b). A particular snail/schistosome combination may be successful to a greater or lesser degree, depending on numerous factors including not only innate properties of both organisms, but also their condition at the time of the experiment, the experimental procedure and the aftercare received by the snails. The host/parasite relationship can be expressed in terms of a spectrum of compatibility (Woodruff, 1985; Bayne & Loker, 1987). In a good compatible relationship there is a high rate of infection, few snails die, the preparent period is short and many cercariae are shed. Poor compatibility is characterised by a low infection rate, high snail mortality, long preparent period and production of few cercariae. A useful index of degree of compatibility is an estimate of the entire cercarial production over the whole life-span of an infected snail (Frandsen, 1979b). Compatibility appears to be affected by genetically-based variation among and within populations of both snail and schistosome. It is therefore important that researchers should specify precisely the geographical origin, methods of sampling and history in the laboratory of the organisms used. Compared with the neotropical species Biomphalaria glabrata little is known of the genetical control of susceptibility to infection in African snail hosts, but production in the laboratory of inter-specific hybrids between African schistosomes has led to interesting observations on the infectivity of hybrid miracidia, considered later in this chapter. Schistosomes of man (S. mansoni, S. haematobium, S. intercalatum) For these schistosomes man is the essential definitive host or at least the major one. S. mattheei also is found in man but is primarily a parasite of domestic livestock (see next section).

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S. mansoni This parasite occurs in Madagascar, Arabia, Egypt, and the greater part of Africa south of the Sahara. It is endemic also in eastern South America and on some Caribbean islands. Identification presents few difficulties and the form named rodentorum Schwetz (from rodents in Zaire) seems to be conspecific and founded on insignificant variation in egg shape (Teesdale & Nelson, 1958; Pitchford & Visser, 1960; Saoud, 1965). High prevalences of S. mansoni in baboons in some localities in East Africa suggest that these animals can maintain foci of infection in the absence of man (Nelson et al., 1962; Fenwick, 1969). All the African species of Biomphalaria tested have proved compatible with S. mansoni to a greater or lesser degree. Frandsen (1979b) obtained infection in all tested populations of B. pfeifferi from widely scattered geographical origins, but the degree of compatibility varied greatly according to the origins of both snail and parasite. In contrast B. alexandrina was susceptible only to local S. mansoni from Egypt, while B. camerunensis was most compatible with the parasite from Central Africa. Thus it appears (Christensen et al., 1986) that in Africa S. mansoni is composed of two major types, one in Egypt transmitted by B. alexandrina and one in other parts of Africa transmitted by a number of Biomphalaria species, among which B. pfeifferi is the most important because of its wide distribution. Yet enzyme analyses of S. mansoni by Fletcher et al. (1981), including isolates from South America, Egypt and tropical Africa, suggested that little intraspecific genetic differentiation has occurred. It may be added that neotropical S. mansoni is compatible with some African Biomphalaria species (Taylor, 1970; Frandsen, 1979b), while B. glabrata was infected with S. mansoni from Uganda (Frandsen, 1979b). The minimum prepatent period is 17–36 days at room temperature in the tropics (Cridland, 1955; Sturrock, R.F. 1965), but much more variable in subtropical southern Africa, according to season. In a very extensive study at Nelspruit, eastern Transvaal (Pitchford & Visser, 1965), batches of 30 snails were exposed every two weeks to miracidia over a period of two years. The snails were kept in aquaria under semi-natural conditions, out-of-doors though protected from extremes of weather; in mid-winter (June/July) water temperature fell below 10°C. Prepatent period varied widely, from 4–5 weeks in summer to 20–21 weeks in winter. For snails exposed in winter, shedding started simultaneously in the spring (September/October) and lasted about 3 months. For spring to mid-summer exposures (September–January) prepatent periods were short (31–63 days) and there was generally a short shedding period of 1–6 weeks. Late summer exposures (February/March) resulted in short preparent periods also, but long shedding periods of 5–8 months. Some of these snails stopped shedding for part of the winter and started again in the spring. Further studies by Pitchford et al. (1969) in South Africa demonstrated reduced cercarial output not only in winter but also at temperatures above 32°C. There is a strong seasonal influence on the production of schistosome cercariae

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also on the plateau of Zimbabwe (Shiff et al., 1975; Woolhouse & Chandiwana, 1989). It is therefore possible that the effect of climatic temperature on the intramolluscan stages could play a part in determining the parasite’s distribution, which may not coincide exactly with that of its snail host. S. haematobium This is the only schistosome parasite of mammals in Africa that lives usually in the blood vessels of the bladder rather than the intestine. The main area of endemic infection comprises Mauritius, Madagascar, Iran, Arabia and Africa from the Mediterranean to about latitude 32° South. Some authors have regarded as distinct from typical S. haematobium of Egypt, the species S. capense (Harley, 1864) described originally from Uitenhage in eastern South Africa. This question will be considered in some detail because infectivity to snails was central to the argument, the essential point being made that the parasite causing urinary schistosomiasis is transmitted by B. truncatus in North Africa but by snails belonging to the B. africanus group in southern Africa (Le Roux, 1958). Later investigations showed the situation to be more complex. Compatibility between North African S. haematobium and B. truncatus, and incompatibility with snails of the B. africanus group (probably B. globosus), was observed early (Archibald, 1933; Cowper, 1947; Gismann, 1954; Le Roux, 1958). Soon the existence in West Africa was demonstrated of two strains of parasite, accepted as S. haematobium, one transmitted by B. globosus, and the other by B. truncatus (=B. rohlfsi) (McCullough, 1959; Paperna, 1968; Taylor, 1970; Webbe & James, 1971a; Wright & Knowles, 1972; Chu et al., 1978). In East Africa, S. haematobium is apparently transmitted only by the B. africanus group; Southgate & Knowles (1977a) found the parasite was not infective to local B. truncatus. Although urinary schistosomiasis is transmitted in most of southern Africa by B. africanus and B. globosus, there is an isolated B. truncatusborne focus in western Zaire (Mandahl-Barth et al., 1974). The case for recognising S. capense as a distinct species (Le Roux, 1958) was based on supposed morphological differences from S. haematobium and differences in intermediate host-specificity. However, no convincing morphological distinctions have been found (Pitchford, 1965), nor were any developmental characteristics of the parasite found to be correlated with the species-group of the snail host (Webbe & James, 1971b, 1972; Wright & Knowles, 1972). Enzymes from isolates of S. haematobium transmitted by different snail hosts did not show any significant variation (Wright & Ross, 1983), in agreement with the conclusion drawn from the similarity in their development in rodent hosts, that the globosus-borne and truncatus-borne strains have evolved relatively recently (Wright & Knowles, 1972). Does intermediate host-specificity by itself justify recognition of S. capense as a distinct species or even an infra-specific taxon? A first consideration is that the parasite in West Africa is not entirely specific to either B. globosus or B.

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truncatus (Paperna, 1968; Chu et al., 1978). Then B. africanus-group snails from various countries are to some extent compatible with truncatus-borne S. haematobium from Iran (Howaldt & Armstrong, 1969; Webbe & James, 1971a), Egypt (Gismann, 1954; Webbe & James, 1971a; Frandsen, 1979b; Mamo & Redda, 1989), Sudan and Zaire (Frandsen, 1979b). Since hybridisation between the truncatus-borne and globosus-borne strains is suspected to occur (Wright & Southgate, 1976), it may be the explanation for the wide enzymic variation in S. haematobium from the Gezira region of the Sudan (Wright & Ross, 1983) and the ability of this isolate to develop in both kinds of snail. From the available evidence it appears that S. haematobium (including S. capense) is a single species comprising many local strains that differ to a greater or lesser degree according to their most compatible species of snail host. The main divisions seem to lie between strains adapted most closely to B. truncatus, to B. globosus or, in smaller geographical areas, to members of the B. forskalii group (B. camerunensis and B. senegalensis in West Africa, and B. cernicus in Mauritius). Adaptation to a particular snail host is not necessarily exclusive; for example, S. haematobium derived from B. truncatus and from B. globosus in north-eastern Nigeria could also develop in B. senegalensis (Fryer & Probert, 1988). In Niger, however, although isolates of the parasite from two of the three localities studied by Véra et al. (1990) were highly compatible with both B. senegalensis and B. truncatus, a third isolate, from a locality where B. truncatus was very common but B. senegalensis rare, was compatible with B. truncatus alone. Moreover, all these isolates of the parasite were almost entirely incompatible with B. globosus. The parasite thus appears to be genetically heterogeneous and capable of evolving compatibility with a variety of snail hosts, depending on local circumstances. This view avoids the problem of taxonomic subdivision, but makes it essential to define precisely the origin of a parasite isolate under study and to be highly cautious in taking snail/parasite relationships observed in a particular locality as representative of a wider area. Species and distributions of snails hosting S. haematobium are summarised in Table 5.2. All the species-groups of Bulinus are represented, but notable absentees are the widely distributed species B. forskalii and B. tropicus; if the parasite were to evolve compatibility with these two common snails the prevalence of urinary schistosomiasis would be greatly increased. Compatibility with the parasite shows only limited correlation with polyploidy in the snail. Most diploid populations within the B. truncatus/tropicus complex seem resistant, though infection has been achieved in the laboratory (Lo et al., 1970; Mandahl-Barth et al., 1976; Frandsen, 1979b). On the other hand, the tetraploid B. truncatus is generally compatible with a suitable parasite strain, while B. octoploidus was susceptible in the laboratory (Lo, 1972). Yet the tetraploid B. permembranaceus, believed to have evolved independently in the Kenyan highlands, shows no evidence of compatibility.

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Table 5.2 Territorial distribution of snails transmitting S.baematobium: (?) indicates need for further evidence of local transmission. Modified from Brown (1980) and Rollinson & Southgate (1987), according to data from Doumenge et al. (1987) and additional references for Guinea Bissau (Grácio et al., 1992), Mali (Madsen et al., 1987), Niger (Véra et al., 1990, 1992), Nigeria (Betterton, 1984; Betterton et al., 1988; Okafor, 1990; Ozumba et al., 1989), Senegal (Albaret et al., 1985; Chaine & Malek, 1983; Southgate, Rollinson et al., 1985) and Sudan (Brown et al., 1984). B. africanus group B. truncatus/tropicus B. forskalii group complex Arabia

B. truncatus

Mediterranean Africa (Algeria, Egypt, Libya, Morocco, Tunisia) Afrotropical Region Angola

B. truncatus

Botswana Cameroon Central African Republic Chad Congo Republic Ethiopia Gabon Gambia Ghana Guinea Bissau Kenya

Liberia Madagascar Malawi Mali Mauritania Mauritius

B. africanus B. globosus B. africanus B. globosus B. globosus B. globosus

B. truncatus B. truncatus

B. beccarii B. wrighti (a member of the reticulatus group)

B. camerunensis

B. truncatus ?B. truncatus B. abyssinicus B. jousseaumei B. globosus B. globosus B. africanus B. nasutus ?B. globosus B. globosus B. obtusispira B. globosus B. globosus

?B. truncatus B. truncatus B. truncatus B. truncatus

B. truncatus ?B. truncatus

B. senegalensis

?B. senegalensis B. cernicus

330 FRESHWATER SNAILS OF AFRICA

B. africanus group B. truncatus/tropicus B. forskalii group complex Mozambique Niger Namibia Nigeria Senegal Sierra Leone Somalia South Africa Sudan Tanzania (mainland)

Uganda Zaire (eastern) Zaire (lower) Zambia Zanzibar/Pemba Zimbabwe

B. africanus B. globosus B. africanus B. globosus B. globosus B. jousseaumei B. umbilicatus B. globosus B. abyssinicus B. africanus B. globosus ?B. globosus B. africanus B. globosus B. nasutus B. globosus

B. truncatus

B. senegalensis

B. truncatus

?B. senegalensis B. senegalensis

B. truncatus

B. nasutus B. africanus B. globosus B. truncatus B. africanus B. globosus B. globosus B. nasutus B. globosus

Seasonal variation in the parasite’s development in B. (Physopsis) sp. (probably B. globosus) was followed by Pitchford & Visser (1965) using the experimental method described for S. mansoni. Preparent periods were consistently longer than for S. mansoni and S. mattheei, lasting from 35–42 days in summer and up to 170 days during winter. Snails exposed to infection during autumn and winter began shedding cercariae in the spring. The development of S. haematobium in B. globosus shows a similar seasonal interruption during winter on the highveld of

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Zimbabwe (Shiff et al., 1975; Woolhouse & Chandiwana, 1989). The retarding effect of low climatic temperature on the intra-molluscan development could play an important part in limiting the distribution of the parasite in South Africa (Pitchford & Visser, 1969). Most cercariae of S. haematobium are shed during a midday period of about 6 hours (Pitchford et al., 1969; McClelland, 1967; Lo, 1972; Webbe & James, 1972). A minor peak of cercarial emergence was found by experiment to be induced by a period of darkness, as short as only 8 seconds (Raymond & Probert, 1987). Changes in light intensity had the same effect, suggesting that cercariae can emerge in response to a shadow cast on to the snail host. The high production of cercariae from individual B. globosus compared to other species of infected snail is related partly to the long lifespan of this species and the correspondingly long duration of infection (Fryer & Probert, 1988). After an initial peak during the first 10 weeks of shedding, cercarial production declines to a low level, but some individual snails show a second period of high cercarial production about 6 months later. S. intercalatum The name signifies that the egg shape is intermediate between those of S. haematobium and S. bovis. S. intercalatum was discovered in the Kisangani (Stanleyville) area of eastern Zaire by Chesterman (1923), followed by Fisher (1934) who identified the host snail as ‘Physopsis africanus’ (actually B. globosus according to later observations by Frandsen et al., 1978). When the parasite was found to be transmitted by B. forskalii in Gabon (Deschiens & Poirier, 1967) and Cameroon (Delas et al., 1968), it was thought to have adopted a new intermediate host and to be spreading into new areas (Deschiens & Delas, 1969). It appears rather that there are two distinct strains, which may be long established. The strain transmitted by B. globosus (and compatible in the laboratory with other snails belonging to the B. africanus group) is known from part of the Zaire/ Lualaba river basin in NE Zaire (Gillet & Wolfs, 1954; Frandsen et al., 1978) and Kinshasa, where a small focus seems to be recently established (De Clercq, 1987). The strain transmitted by B. forskalii (and compatible in the laboratory with other members of this species-group) occurs in Gabon, Cameroon, São Tomé Island (Corachan et al., 1988; Grácio, 1988, 1990; Brown et al., 1989; Southgate, Rollinson et al., 1994; Tchuem Tchuente & Jourdane, 1993), Nigeria (Arene et al., 1989) and probably Equatorial Guinea (Simarro et al., 1990). The intermediate host is not yet identified for foci of human infection found in Central African Republic and Chad (Doumenge et al., 1987). Each strain is normally unable to develop in a species of snail with which the other is compatible (Wright et al., 1972; Frandsen, 1975, 1979a). There are other strain differences in patency periods and egg shape (Wright et al., 1972; Bjornebøe & Frandsen, 1979), peak emergence time for cercariae (Pages &

332 FRESHWATER SNAILS OF AFRICA

Théron, 1990a) and enzymes (Wright, Southgate & Ross, 1979; Brown, Sarfati et al., 1984). The two strains interbreed in the laboratory (Frandsen, 1978), though the failure of miracidia to hatch from eggs laid by the second generation of hybrid worms indicates significant genetic differences. The recombination of genes controlling infectivity was demonstrated by the successful infection of both B. forskalii and B. globosus by hybrid miracidia. The B. forskalii-borne strain of S. intercalatum hybridises with S. haematobium, both in the laboratory and in nature (Wright, Southgate et al., 1974; Southgate et al., 1976; Wright & Southgate, 1976; Burchard & Kern, 1985; Mutani et al., 1985; Ratard & Greer, 1991). The infectivity to snails of hybrid miracidia will be discussed later in this chapter and here we will consider the effect of hybridisation on the status of S. haematobium and S. intercalatum as species (Southgate, Rollinson et al., 1982; Rollinson & Southgate, 1985). These two species are thought to have diverged from a common stock, S. intercalatum as a parasite of primates in forest areas, S. haematobium as a parasite of the ancestors of man in savannah. Contact between the two is now occurring increasingly because of incursion by people into the tropical rain forest and consequent alteration of habitat. Hybridisation seems to be resulting in S. intercalatum being replaced by S. haematobium and the hybrid in Loum, Cameroon. Worms reared as mixed infections in hamsters did not show any specific mate-recognition system, and males of S. haematobium were more successful than males of S. intercalatum at obtaining a mate (Southgate, Rollinson et al., 1982); if the same situation holds in man the gradual disappearance of pure S. intercalatum is to be expected. Cercariae of S. intercalatum are shed mostly during the afternoon (Pitchford & Du Toit, 1976; Pages & Théron, 1990a,b). The peak shedding time for cercariae from experimental hybrids among S. intercalatum, S. haematobium and S. bovis demonstrated genetic determination of cercarial emergence rhythm (Pages & Théron, 1990b). Unlike cercariae of other schistosomes S. intercalatum concentrates at the surface of the water, aggregating together and adhering to objects, possibly as an adaptation to infecting animals that make only superficial contact with water (Wright et al., 1972). Aggregation is caused by a sticky secretion discharged in response to increase in temperature; Southgate (1978) suggested that premature discharge of this secretion might occur in waterbodies outside the protective canopy of the forest, and this could impair infectivity of the cercariae and contribute to the restricted distribution of the parasite. Schistosomes found in domestic stock (S. bovis, S. curassoni, S. leiperi, S. margrebowiei and S. mattheei) Interest in schistosomes with non-human definitive hosts was stimulated by the concept of heterologous immunity, whereby people exposed to infection by cercariae of these species could acquire immunity to the species primarily

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infecting man (Taylor et al., 1973). The prevalence of schistosomiasis in cattle in Africa may be even higher than in man; infection rates over 50% are reported from eastern Africa (Dinnik & Dinnik, 1965). Numerous deaths of cattle attributed to S. bovis have occurred in the Sudan (Eisa, 1966) and of cattle and sheep due to S. mattheei infection in southern Africa (Reinecke, 1970; Lawrence & Condy, 1970; Van Wyk et al., 1974). All these schistosomes appear to live normally in the intestinal blood vessels of the definitive host. S. leiperi and S. margrebowiei These are parasites primarily of antelopes and have comparatively restricted distributions. S. leiperi occurs in eastern central Africa and was originally described from the Sitatunga (Tragelaphus spekei), though Pitchford (1976) believes the main hosts to be the Lechwe (Kobus leche) and Puku (K. vardoni). Cattle, sheep and goats are also infected. Naturally infected snails have not yet been reported, but the parasite is compatible with members of the B. africanus group in the laboratory (Le Roux, 1955; Pitchford & Du Toit, 1976; Southgate, Ross & Knowles, 1981). Snails shed cercariae mostly in the late afternoon and evening, favouring transmission to the antelope hosts (Pitchford & Du Toit, 1976). S. margrebowiei is known from northern Botswana, Zambia and Katanga (Pitchford, 1976), and Chad (Graber, 1978). The main hosts are probably Kobus antelopes and the parasite occurs in cattle. The rounded eggs differ from those of all other African schistosomes. Naturally infected snails have been collected in the Lochinvar Park, Zambia; Bulinus forskalii and B. scalaris by Wright, Southgate & Howard (1979) and B. tropicus by Southgate, Howard et al. (1985). Laboratory infections have been achieved in B. truncatus by Southgate & Knowles (1977b), and in B. depressus and B. natalensis by Pitchford & Du Toit (1976). The latter authors and also Raymond & Probert (1991) observed peaks of cercarial emergence at dawn and dusk, the times when watering places are visited by antelopes and waterbuck. S. bovis Originally described from worms obtained from cattle in lower Egypt; natural infections occur in various domestic livestock, antelopes and rodents, but rarely if ever in man (Nelson et al., 1962; Pitchford, 1977; Christensen et al., 1983). Although eggs are found occasionally in human stools (e.g. Chunge et al., 1986; Mouchet et al., 1988), their viability has not been proved and it seems that such Table 5.3. Intermediate hosts for S. bovis in tropical Africa, according to Christensen et al. (1983, Table 1) with additions according to references cited below. Bulinus africanus group

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B. africanus B. abyssinicus B. globosus B. nasutus B, ugandae B. truncatus/tropicus complex B. natalensis: Graber & Daynes (1974) B. octoploidus: Graber & Daynes (1974) B. tropicus: Ouma & Waithaka (1984); Southgate, Brown et al. (1985) B. truncatus B. forskalii group B. browni: Jelnes (1983) B. forskalii B. senegalensis

eggs could have been ingested with food by the apparent host. S. bovis is reported from a large area of northern and tropical Africa (Dinnik & Dinnik, 1965), but its southern limit of distribution is not entirely clear in relation to S. mattheei, which is the common schistosome parasite of cattle in southern Africa (see below). These are believed to be distinct species, however, according to hybridisation experiments (Taylor, 1970) and enzyme analysis (Ross et al., 1978). S. bovis is of particular interest for the great variety of its snail hosts, which include members of all the species groups of Bulinus, and also Planorbarius in Spain and possibly north west Africa (Ramajo-Martin, 1978; Southgate, Wright et al., 1984; Touassem & Jourdane, 1986). The principal intermediate host in the Mediterranean region is B. truncatus, while in tropical Africa a number of species maintain transmission (Table 5.3). Northern isolates of B. truncatusborne S. bovis do not usually develop well in snails belonging to the B. africanus group (Southgate & Knowles, 1975a; Frandsen, 1979c). More evidence for adaptation to a local snail was obtained in experiments (Lo & Lemma, 1975) with S. bovis collected from different localities in Ethiopia where transmission was by either B. abyssinicus or B. truncatus. Yet S. bovis isolated from B. africanus-group snails collected in western Kenya was no less compatible in the laboratory with B. truncatus, B. forskalii and B. reticulatus (Southgate & Knowles, 1975a). Later observations in western Kenya (Southgate & Knowles, 1975b) confirmed the existence of natural infections in B. truncatus and B. forskalii as well as the B. africanus group, and isolates of the parasite from each kind of snail were infective to the other two (Southgate & Knowles, 1978). Compatibility with snails is similarly broad in north-western Tanzania (Southgate, Rollinson et al., 1980) and the southern highlands (Mutani et al., 1983). Perhaps S. bovis is so broadly compatible with host snails in eastern

SNAILS AND SCHISTOSOMES 335

Africa simply because many species of Bulinus are present; another possibility (Southgate & Knowles, 1975a) is that this strain is a hybrid with S. mattheei and combines the compatibilities of both parental species. S. bovis has had little success, however, in utilising diploid snails belonging to the B. truncatus/tropicus complex. An early report of B. tropicus naturally infected in Kenya with ‘an animal schistosome’ (probably S. bovis) (Teesdale, 1962, p. 760) was followed by reports of naturally infected B. natalensis in Ethiopia (Graber & Daynes, 1974) and experimental infection of diploid ‘B. truncatus’ from Zimbabwe (Frandsen, 1979b). Not until recently was the natural infection of B. tropicus in Kenya confirmed (Ouma & Waithaka, 1984; Southgate, Brown et al., 1985, 1989), and the interesting circumstances are described in the subsequent section ‘Resistance in the snail host’. The daily peak of emergence of cercariae from snails is generally earlier than for S. haematobium, though there are differences in timing among isolates of S. bovis from different localities, possibly in relation to local ecological conditions (Mouahid et al., 1987, 1991). S. mattheei A sheep from Humansdorp in Cape Province, South Africa, was the source of the specimens first described; other primary definitive hosts include cattle, antelopes, wildebeeste and buffalo (reviews by Pitchford, 1977; Christensen et al., 1983). This schistosome is common in cattle in South Africa and adjacent countries, and is reported from as far north as Tanzania, Chad and Nigeria (Pitchford, 1977). Its northern limit in relation to S. bovis is not entirely clear, though the two species appear to be distinct, according to evidence mentioned under S. bovis. High prevalences of S. mattheei are commonly found in cattle and in some areas low-to-moderate prevalences are reported for man, according to the excretion of mattheei-like eggs found usually in the urine (Van Wyk, 1977, 1983; Chandiwana et al., 1987). The nature of such eggs has been the subject of extended investigation and discussion. Infection in man occurs where people share water resources with cattle; the snail hosts for S. mattheei are Bulinus africanus and B. globosus, which both also transmit S. haematobium in southern Africa. The generally low prevalence of S. mattheei in man compared with cattle suggests that man is not a good host, while the frequent presence of S. haematobium in people excreting mattheei-like eggs led to the view, supported by experiments, that such eggs are the product of hybridisation between mattheei and haematobium (Pitchford, 1959, 1961). Enzyme electrophoresis provided confirmation of natural hybridisation in man (Wright & Ross, 1980) and experimentally-produced F1 hybrids showed increased infectivity to snails. A further investigation by means of enzyme electrophoresis indicated that all mattheei-like eggs from human urine were the product of pairing between S. mattheei females and S. haematobium males (Kruger & Evans, 1990). As the

336 FRESHWATER SNAILS OF AFRICA

number of hybrid eggs released into the environment was found to be small in comparison to the eggs of S. haematobium, Kruger (1990) calculated that hybridisation between the two species is unlikely to proceed to the extent of producing a strain with significantly enhanced infectivity to man or snails. Although different hybrid strains may be evolving with varying infectivity to man, the variation in local prevalence of the cattle schistosome in man could also be explained by other influences (Kruger et al., 1990), including seasonal differences in the quantities of cercariae shed from snails and local practices for management of domestic stock. From the sum of observations it appears that S. mattheei and its hybrid are of no more than minor public health importance (Chandiwana et al., 1987; Kruger, 1990). Although natural infections with S. mattheei in snails have been recorded only for the B. africanus group, infection has been achieved experimentally in ‘B. truncatus’ (Pitchford, 1965; doubtful identification, see Brown et al., 1967, 1971), B. truncatus from Iran (Howaldt & Armstrong, 1969) and B. wrighti by Wright et al. (1972). The lack of reported infection in B. tropicus would be surprising if the parasite occurs in western Cape Province as indicated by Dinnik & Dinnik (1965, Fig. 5), for there this snail is the commonest species of Bulinus. However, according to Van Wyk (1983) the distribution of S. mattheei is like that of S. haematobium; mainly in the lowveld of Transvaal, in parts of Natal and the eastern coastal area southwards to Humansdorp. Thus, the distribution of both schistosomes corresponds closely to the distribution of the B. africanus group, and such snails were the intermediate host for S. mattheei in a westerly focus in south west Transvaal (Joubert et al., 1987). The daily peak of emergence of cercariae from snails is earlier than for S. haematobium (Pitchford et al., 1969); marked seasonal variation in the duration of intra-molluscan development (Pitchford & Visser, 1965, 1969) suggested that low climatic temperature contributes to limiting the distribution of both parasites (Pitchford, 1981). S. curassoni This is a parasite of sheep, goats and cattle in parts of West Africa: Senegal, Mauritania and Mali (Vercruysse et al., 1984; Southgate, Rollinson et al., 1985; Rollinson et al., 1990), northern Nigeria (Ndifon et al., 1988) and Niger (Mouchet et al., 1989). Reports of infection in man have not been confirmed (Rollinson et al., 1987). The distribution overlaps that of S. bovis; mixed pairs of worms are found as well as apparently hybrid individuals, and hybridisation has been achieved in the laboratory (Rollinson et al., 1990). It is not clear how the two species maintain their integrity, though differences in specificities to intermediate and to definitive hosts may play a part. For S. curassoni, Bulinus umbilicatus appears to be the most important natural host snail (Southgate, Rollinson et al., 1985; Albaret et al., 1985; Diaw & Vassiliadès, 1987), whereas natural infections with S. bovis in Senegal were observed only in B. globosus and B. forskalii. Further, S. curassoni develops in a smaller range of snails than S.

SNAILS AND SCHISTOSOMES 337

bovis in the laboratory (Southgate, Rollinson et al., 1985). The two species showed a similar daily rhythm in the emergence of their cercariae in Niger (Mouchet et al., 1992). S. rodhaini Though this schistosome is closely related to S. mansoni, it is only rarely a parasite of man. Hybridisation between the two occurs in the laboratory but apparently not in nature; there are differences in enzymes and other characteristics (reviewed by Brémond et al., 1989). The definitive hosts are usually rodents, but infections have been found also in dogs and a serval cat (Pitchford, 1977). Foci of transmission are reported for eastern Zaire (Schwetz, 1954 and earlier papers) and Burundi (Gryseels, 1985), Uganda (Berrie & Goodman, 1962; Fripp, 1968), Kenya (Nelson et al., 1962) and Zimbabwe (Chandiwana & Taylor, 1985). Biomphalaria pfeifferi and B. sudanica are the natural intermediate hosts (Schwetz, 1954; Berrie & Goodman, 1962; Gryseels, 1985). Cercariae are shed mostly at night (Pitchford et al., 1969) presumably in adaptation to nocturnal definitive hosts. Natural history of transmission Within the broad areas where human schistosomiasis is endemic there is wide variability in the amount of infection locally. This focal pattern of transmission is related essentially to the distribution and abundance of host snails, and the force of infection to which they are exposed; the complex of interacting factors involved includes the habits of the human host (Southgate & Rollinson, 1987). Mathematical modelling has clarified ideas about the field observations still needed of snail-parasite relationships (Anderson & May, 1979), and the interplay between theory and field study has been well reviewed by Woolhouse & Chandiwana (1990a). Among the more recent major field studies are investigations made in Lake Volta (Chu et al., 1981a,b), the Gezira Irrigated Area in Sudan (Babiker et al., 1985), Ifakara area in Tanzania (Marti et al., 1985) and the highveld of Zimbabwe (Woolhouse & Chandiwana, 1989, 1990a,b; Woolhouse, 1989a,b). The effects of the development of water resources in increasing prevalence of infection were reviewed by Hunter et al. (1993). The entire literature is very extensive and here we can examine but briefly a few aspects. Distribution and adundance of snails; brackish water Geographical distribution and factors which affect the occurrence and numbers of snails locally are considered in Chapters 9–12. Bulinus and Biomphalaria are generally tolerant of the whole ranges for the commonly measured chemical and physical variables in waters that can be termed ‘fresh’, but higher concentration

338 FRESHWATER SNAILS OF AFRICA

of salinity is clearly unfavourable and plays an important part in preventing transmission of schistosomiasis in many inland and coastal brackish waters. Thus, no disease transmission takes place in the numerous saline waters of northern Africa, nor in many lakes in the East African Rift Valley. Lake Turkana in Kenya is a borderline example; so far no potential intermediate host has been found among the few living species of snail collected in this lake, which has the highest salinity of any African lake inhabited by freshwater snails. There is interest in the possibility of transmission of schistosomiasis in brackish waters at the coast because many estuaries and lagoons are in densely populated regions, some popular as holiday areas. Laboratory studies in South Africa (Donnelly et al., 1983, 1984a,b) showed that the snail host (Bulinus africanus) could survive in a salinity of up to 3.5‰. The free-living stages of the parasite were better adapted to salinity than the snail host; cercariae remained infective in salinities up to 7‰. During a 2-year study of the Manzimtoti lagoon system (Donnelly, Appleton et al., 1984), both infected and uninfected B. africanus occurred in the brackish stretch of the river, though the snail did not breed there and specimens were passively transported downstream from breeding areas in freshwater. Transmission of schistosomiasis appeared to be possible in this lagoon and also in at least 24 other brackish waterbodies on the Natal coast. The potential for transmission is increasing due to several factors, including the accelerating sedimentation of lagoons, closure of river mouths by sand swept along the coast by ocean currents, and the construction of weirs. A permanent reduction in salinity caused by engineering works that impede tidal flow can lead to regular schistosomiasis transmission in waters that were previously free of the disease (Chippaux et al., 1990). The recently increased abundance of Biomphalaria pfeifferi and transmission of S. mansoni in the lower Senegal River Basin is perhaps a consequence of the construction of an antisalinity barrage (Diaw et al., 1990; Talla et al., 1990). Prevalence of infected snails: spatial variation Although the snail hosts of schistosomes tolerate a wide range of environmental conditions their local distribution may be patchy, often showing marked aggregations along short distances of the margin of a lake or stream. Such aggregation in conjunction with the customary preference of people for traditional water contact points produces localised or ‘focal’ transmission of schistosomiasis. In Lake Volta the water contact sites studied by Chu, Vanderburg & Klumpp (1981) were usually distinct and consistent; during the season of high water level both snails and miracidia were concentrated in calm water in small pocket-shaped clearings in the marginal emergent vegetation. In Zimbabwe the prevalence of patent infections (detected by cercarial shedding) in B. globosus living in a river varied from 0% to 70% over distances of less than 100 m (Woolhouse & Chandiwana, 1990a). Here the prevalence of snail infection was less closely related to human water contact sites than in Lake

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Volta, perhaps partly because of dispersal by flowing water of miracidia and infected snails (Woolhouse & Chandiwana, 1989). Patchiness in snail distribution reflects such factors as protection from water flow, wave-action and desiccation, availability of food, presence of vegetation and suitable surfaces for attachment. People choose water contact sites for reasons of accessibility, suitability for washing clothes and for children to swim safely. Schistosomiasis transmission sites are noticeably restricted where there are crocodiles (Appleton & Bruton, 1979). Fortunately for schistosomes, human activities attract snails, which thrive in moderate pollution, while domestic rubbish such as plastic bags provides excellent surfaces for feeding, egg-laying and the growth of hatchlings. In rivers the variation in water flow may be the major cause of snail aggregations, which may reflect simply the recent history of floods and droughts (Woolhouse & Chandiwana, 1990b). Spatial variation in the prevalence of patent snail infection is related essentially to the force of infection (supply of miracidia derived from human excreta). It is related also to a complex of interacting processes affecting the chances that infection will develop to patency within an individual snail; among such factors are the genetic constitution of the snail, its age, and the length of the preparent period compared with the snail’s life expectancy (which is related to seasonal environmental changes). Non-random distribution of infection among individual snails, termed ‘overdispersion’, has been demonstrated for S. haematobium in B. globosus by Woolhouse et al. (1990). Comparison between the proportions of single-sex and mixed-sex infections showed that the number of snails infected by two or more miracidia exceeded statistical expectation based on random distribution. One effect of overdispersion is to increase the probability that exposure to cercariae from a single snail will result in a mixed-sex, and therefore symptomatic, infection in the human host. Many authors have observed surprisingly low prevalences of patent snail infections in known schistosomiasis transmission sites, of the order of only a few percent. But data on B. globosus in Zimbabwe (Woolhouse & Chandiwana, 1989) indicate that if preparent infections are taken into account, the overall infection rate sometimes may approach 100%, and absolute snail density may limit snailto-man transmission rates. Seasonal variation in prevalence of infected snails and production of cercariae Changes in snail populations over time (Chapters 10, 11) in absolute numbers and age-structure are related mainly to seasonal variation in rainfall and temperature. Temperature also influences strongly the speed of development by the intra-molluscan stages of the schistosome, and during the cool season development slows or ceases, while shedding of cercariae is reduced or entirely inhibited (Pitchford & Visser, 1969; Shiff et al., 1975; Pitchford, 1981). Human

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water contact is also encouraged by warm weather, especially swimming by children. The relationship between snail age and prevalence of infection may vary seasonally and for complex reasons (Woolhouse, 1989a). The combined seasonalities in snail populations, parasite development and human behaviour produces peak periods for disease transmission according to local circumstances. On the highveld of Zimbabwe, few if any infections mature in snails during the June–August cold season, and peak prevalences occur in October–November late in the hot-dry season (Woolhouse & Chandiwana, 1989, 1990a). The overall range in the prevalence of patent infections with S. haematobium in B. globosus, estimated from 22 sampling sites over an 840 m stretch of a river, was from 2% in the cold season to 16% in November (Woolhouse & Chandiwana, 1989). Discrepancies between snail and schistosome distributions On continental maps the distributions of potential host snails and schistosomes appear to coincide, but there are considerable local discrepancies. Although S. haematobium is capable of developing in numerous species of Bulinus, through the adaptation of local parasite strains, not all potential intermediate hosts are exploited throughout their geographical ranges. It is particularly evident that S. haematobium is not always utilising B. truncatus when available; for example in Senegal where B. senegalensis is the main host (Chaine & Malek, 1983; Southgate, Rollinson et al., 1985), highland Ethiopia where the parasite is not found at all, and over the vast area south of latitude 4°N where the only proved focus of transmission by B. truncatus is in lower Zaire. Where there is a transition from the tropical to the temperate climatic regime in southern Africa it appears that populations of potential host snails can exist, at least temporarily, in localities too cool for the intra-molluscan development of schistosomes (Pitchford & Visser, 1969; Pitchford, 1981). The effect of altitude in lowering prevailing temperature and inhibiting parasite development probably contributes to the absence of S. mansoni from above about 2200 m in highland Ethiopia, though B. pfeifferi is widespread above this level (Kloos et al., 1978; Doumenge et al., 1987). The two strains of S. intercalatum are restricted to the tropical rainforest, though the host snails are widespread over savanna. Explanations suggested for this (Southgate, 1978) are based on the behavioural peculiarities of the cercaria and the possibility of introgressive hybridisation with S. haematobium. Changes in transmission patterns Man aids the schistosome life cycle by creating habitats suitable for host snails and dispersing the parasites through the travel of infected people, while the growing human population increases the intensity of transmission. New transmission sites have quickly developed in irrigation schemes and water impoundments, ranging from small earth dams to man-made lakes, in many

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areas, e.g. north-west Tanzania (McCullough et al., 1968), Lake Volta (Scott et al., 1982) and the lower Volta River (Wen & Chu, 1984), south-east Zaire (Polderman et al., 1985), Sudan (Babiker et al., 1985; Madsen et al., 1988), Cameroon (Ripert & Raccurt, 1987, 1988), Burundi (Gryseels & Nkulikyinka, 1988) and Sierra Leone (White et al., 1989). Further information for man-made lakes is given in Chapter 12. Expansion of towns may also intensify transmission, for host snails can tolerate considerable disturbance of habitat and pollution (e.g. Sodeman, 1979; Sarda et al., 1985). The consequences for schistosomiasis transmission of some man-made environmental changes may take years to develop. It has been suggested that reduction in the range of extreme water temperatures below large dams could allow host snails to spread into new areas of South Africa (Pitchford & Visser, 1969; Pitchford, 1981). No report of this occurring seems to have appeared, but during the past 15 years major changes have become evident in the epidemiological pattern of schistosomiasis in the Nile valley of Egypt, following construction of the Aswan High Dam (Medhat et al., 1993, and earlier sources cited). Although the underlying cause(s) are unknown, a decline has occurred in Lower Egypt of the abundance of Bulinus truncatus relative to Biomphalaria alexandrina, which is extending its distribution in Middle and Upper Egypt. Associated with these changes in snail populations is a decline in the incidence of S. haematobium in northern Egypt and a spread of S. mansoni infection southwards. The effects of salinity on snail hosts and the free-living stages of schistosomes were touched on when brackish water was considered in an earlier section of this chapter. Marked changes in snail populations and increased incidence of schistosomiasis can arise after interference in the salinity regimes of coastal waters. The blocking of tidal flow by a bridge in a South African estuary created a freshwater swamp which was colonised by B. globosus and provided the threat of schistosomiasis transmission in an important tourist area (Appleton & Bruton, 1979, p. 558). Both urinary and intestinal schistosomiasis became wellestablished in a similar situation in Benin (Chippaux et al., 1990). An antisalinity barrage constructed at Diama in the Senegal Delta contributed, it seems, to the dramatic increase in the 1980s of Biomphalaria pfeifferi and S. mansoni. Both were previously rare (Diaw, 1980; Monjour et al., 1981; Malek & Chaine, 1981), but within a few years Biomphalaria became abundant in the lower delta and further inland in the Lac de Guiers and irrigation canals at Richard-Toll, where a high prevalence of human infection appeared (Diaw et al., 1990, 1991; Talla et al., 1990, 1992). Human activities played an essential part in changes in the epidemiology of schistosomiasis at Loum in Cameroon (Southgate, Van Wijk & Wright, 1976; Rollinson & Southgate, 1985). S. haematobium is believed to have been introduced into this area, where previously only S. intercalatum was known, from other places in Cameroon. Its transmission was favoured by changes in the snail populations in Loum town. In 1973 B. forskalii, host for S. intercalatum, was

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predominant in the upper courses of the Mbette River and tributaries flowing through the town, but it was replaced further downstream by B. truncatus (=rohlfsi), the host for S. haematobium. The patterns of snail distribution were interpreted as the result of recent colonisation by B. truncatus following clearing of forest. The distributions for the two schistosome species in people followed those of their intermediate hosts, intestinal schistosomiasis due to S. intercalatum being commonest in the upstream area, while urinary schistosomiasis due to S. haematobium occurred mainly downstream. However, many people passed eggs of hybrid shapes in both urine and stools. This evidence for hybridisation between the schistosomes was first seen in the early 1970s, and was followed by progressive replacement of intestinal by urinary schistosomiasis, apparently due to the breakdown of the intercalatum gene-pool and its introgression into the dominant gene-pool of S. haematobium. Examples of situations where schistosomiasis infection may result from future demand for resources from the human population can be seen in eastern South Africa and Namibia. For Tongaland, situated immediately south of the Mozambique border, Appleton & Bruton (1979) described how economic development and human population influx could lead to the establishment of S. mansoni, partly through a decline in crocodile and hippopotamus populations, which discourage people from contact with the deeper waterbodies, to which Biomphalaria is confined. That both S. haematobium and S. mansoni are absent from southern Namibia and western Cape province was regarded by Pitchford (1981) as an anomaly in view of the suitable temperature regime in this region. The explanation is the lack of any compatible species of snail, probably due to the low rainfall which does not sustain suitable habitats. This situation could be changed in Namibia through the transfer of water southwards from the Okavango River, even over 600 km into the Windhoek area, and the appearance of irrigated cultivation and permanent storage dams in semi-arid areas where the only snail habitats at present are seasonally-filled dams for livestock. Finally there are possibilities for change in schistosome transmission arising from change in compatibility with snails. For example, if S. haematobium were to evolve compatibility with B. forskalii, transmission of urinary schistosomiasis might greatly increase. One way in which this might happen is suggested by the observation that hybrid miracidia from the cross S. intercalatum×haematobium combine the compatibilities towards snails of both parental schistosomes (see also next section). Thus, hybrid miracidia are infective to B. forskalii as well as the normal intermediate hosts for S. haematobium. Apparently there is no genetic barrier that would prevent genes for compatibility with B. forskalii being transferred from the gene pool of S. intercalatum to the gene pool of S. haematobium. The resulting schistosome strain could have a broad spectrum of compatibility with host snails, like S. bovis in western Kenya. One would expect, though this has yet to be demonstrated, such schistosome strains to have a competitive advantage over strains with narrower compatibilities. Ratard & Greer (1991) reported the recent establishment of hybrid S.

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haematobium×intercalatum in a Cameroonian village within the transition zone between forest and savanna, a region where neither parental species was established and the only snail host available was B. forskalii. Another route by which a shift in the compatibility between schistosome and snail might occur has been suggested to explain the finding in Kenya of S. bovis in the unusual intermediate host B. tropicus. Here a pre-existing infection with a digenean parasite from a different family seems to facilitate infection by the schistosome, thereby providing the latter with the opportunity of adapting to a snail which generally seems to resist infection (see the later section ‘Resistance in the snail host’). Infectivity of hybrid miracidia The first step towards hybridising two species of schistosome in the laboratory is to infect a number of snails each with a single miracidium, from one or other of the schistosomes. Since the sex of the miracidium was determined during the meiosis which preceded egg formation in the definitive host, the cercariae produced by each snail are of one sex. This can be determined within about 6 weeks by the infection of a mammalian host and the subsequent recovery of either male or female worms. Mammalian hosts can now be infected with cercariae of both sexes, one from each of the two schistosome species. Pairing between worms of different species and the production of eggs does not necessarily indicate that interbreeding has occurred, for a female worm carried by a male of a different species has been known to produce eggs by parthenogenesis. Criteria used to detect true hybrid nature include egg shape, infectivity of miracidia to snails, and enzymic characters; a further possible characteristic is rhythm of cercarial emergence (Pages & Théron, 1990b). Early experiments on hybridisation between schistosomes of different species (Le Roux, 1954; Taylor, 1970; reviewed by Wright & Southgate, 1976) indicated that hybrid miracidia combined the infectivities of their parental species towards snails. This was amply confirmed by observations on hybrid miracidia obtained by interbreeding S. intercalatum from Cameroon with S. haematobium and S. mattheei. The hybrid miracidia S. intercalatum (Cameroon)×haematobium (Cameroon) were infective to both B. forskalii and B. truncatus (=rohlfsi), while hybrid S. intercalatum×mattheei was infective to both B. forskalii and snails of the B. africanus group (Wright et al., 1974; Wright & Southgate, 1976). This dual infectivity persisted into the second hybrid generation, even though the parasite was passaged through only the paternal intermediate host in each generation. Infectivity to both B. forskalii and B. globosus was retained at least up to the fifth hybrid generation of the cross S. intercalatum (Cameroon) ×haematobium (Tanzania) in experiments by Mutani et al. (1985) using a hybrid line passaged through B. wrighti. Interbreeding between the two strains of S. intercalatum from Cameroon and Zaire produced hybrid miracidia that developed in both parental intermediate

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hosts, B. forskalii and B. globosus, but cercarial production was low and miracidia did not hatch from eggs laid by worms of the second hybrid generation (Frandsen, 1978). Observations on the infectivity to snails of miracidia helped in the early interpretation of the focus of schistosomiasis at Loum in Cameroon, when changes took place that were suspected to be due to hybridisation between S. intercalatum and S. haematobium (Wright et al., 1974; Southgate, Van Wijk & Wright, 1976). Miracidia hatched from ‘intermediate’ eggs were infective to snails of both the B. truncatus and B. forskalii groups, thus suggesting their hybrid origin. But in order to eliminate the possibility that people were carrying a mixed infection of the two distinct schistosomes, cercariae derived from the different groups of infected snails were passaged separately through hamsters, and the infectivities of the next generation of miracidia were tested. The retention of dual infectivity in both lines confirmed that the original miracidia had combined the infectivities of the two parental species. In a new focus of apparently hybrid S. intercalatum×haematobium at Kinding Njabi, Cameroon studied by Ratard & Greer (1991), miracidial infectivity did not conform to the hybrid population at Loum, from where the parasite was believed to have been introduced to the new locality. Instead of being infective to the host snails for both parental schistosomes, stool-derived miracidia were infective only to B. forskalii, while urine-derived miracidia were infective only to B. truncatus. This might indicate mixed infections with non-interbreeding populations of the two schistosomes, but Ratard & Greer concluded that the sum of their observations (including data on egg shape and snail distribution) provided strong evidence for hybridity. Further study of such hybrid populations is necessary to understand them fully. Resistance in the snail host For a schistosome its host snail is a resource to be efficiently converted into cercariae. Though the relationship is a product of co-evolution and one that in the interests of the parasite should be long-term, it is detrimental to the individual snail as shown by many observations on mortality rate (Woolhouse, 1989b), pathology and reproduction (the latter reviewed by Hurd, 1990). Host castration may result from mechanical damage and nutrient depletion. Moreover, there is growing evidence that trematode products may depress host reproduction indirectly through manipulation of the host’s endocrine system (de Jong-Brink, 1990). Compatibility can be seen as a dynamic state, evolving through adaptation between local populations of snails and schistosomes, according to encounters between genetically variable individual snails and miracidia. The assessment of compatibility, and its component snail resistance, requires techniques that can distinguish between infectivity of the miracidium and susceptibility of the snail. Quantitative estimates of cercarial production per snail (Frandsen, 1979b; Fryer

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& Probert, 1988) are more informative than records simply of the proportion of the exposed snails that survive to shed cercariae, but it is very difficult to standardise conditions under which snails are exposed to infection. Some difficulties may be avoided by using histological sections of snail tissues to evaluate the success of miracidial penetration and development (e.g. Touassem & Jourdane, 1986). A further refinement is the microsurgical implantation of schistosome larvae into snails, which is a most promising technique for the study of host resistance (Jourdane, 1982). Resistance by snails to schistosome infection depends on cellular reaction mediated by humoral factors (reviewed by Bayne & Loker, 1987; van der Knaap & Loker, 1990; Preston & Southgate, 1994). In the molluscan system for discriminating between self and non-self, agglutinating substances play a part and their presence in the African species Bulinus nasutus has been demonstrated (Daniel et al., 1992; Harris et al., 1993). The killing of the parasite follows its encapsulation by haemocytes; death may result from a combination of oxidative cytotoxicity and mechanical damage (van der Knaap & Loker, 1990). Little is known of the genetic basis for snail-schistosome relationships in Africa, compared with S. mansoni and Biomphalaria glabrata of the neotropics (Richards, 1975; Mulvey et al., 1988). The finding of highly localised gene combinations in Kenyan populations of B. pfeifferi led Bandoni et al. (1990) to suggest that considerable variation in susceptibility to S. mansoni could exist on a small biogeographical scale. Reports by Joubert et al. (1990, 1991) of variation among South African populations of Bulinus africanus in the susceptibility to S. haematobium from eastern Transvaal are open to a different interpretation. While the most resistant snail population (Natal, Newlands) may have been identified correctly, the snails from the Transvaal localities probably were B. globosus, and thus the apparently inter-population difference could have been inter-specific. Increasing resistance to S. haematobium in a laboratory-bred population of B. nasutus was attributed by McClelland (1965) to the regular return to the stock, over a 4-year period, of snails that had been exposed to miracidia but did not shed cercariae. Another laboratory stock of B. nasutus provided evidence that selection for survival under laboratory conditions favoured individuals that were by chance resistant to infection (Sturrock, B.M., 1967, 1968). Since reproduction by snails is damaged by trematode infection, and assuming that mechanisms for resistance are heritable, there arises the question of why snail populations do not more commonly evolve resistance to schistosome parasites. There are at least three possible reasons. First, the genetic diversity of the parasite may be sufficient to counter whatever defence mechanisms are available to the host. Secondly, interaction among host genes may restrain the selection in favour of resistance. Thirdly, as common species of snail are parasitised by several species of trematode, the selection pressures exerted by different parasites could contribute towards maintaining genetic heterogeneity in the host population, thereby hindering the evolution of an effective defence against any one of the parasites.

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One way that a schistosome could broaden its compatibility with snail hosts is suggested by observations that followed the finding of S. bovis in Bulinus tropicus, a snail in which this schistosome does not usually develop. Of 406 B. tropicus collected in Kenya (Southgate, Brown et al., 1985, 1989), 50 were carrying this parasite, and of these all but one were infected also with Calicophoron microbothrium, an amphistome trematode parasite of cattle. Such a high frequency of double infection suggested that snails infected with the amphistome were somehow rendered susceptible to infection by the schistosome. This hypothesis was later supported by the results of experiments; the same isolate of S. bovis developed in B. tropicus only if the snail was infected also with the amphistome. When established the schistosome appeared to suppress the amphistome, for there was a switch from the shedding of amphistome to schistosome cercariae. The mechanism by which the B. tropicus defence system was prevented from excluding the schistosome is not understood, though probably it depends on interference by the amphistome with the activities of host haemocytes. Such interference occurs when the resistance of particular strains of Biomphalaria glabrata to S. mansoni is eliminated by the presence of echinostome larvae (reviewed by van der Knaap & Loker, 1990). That the defence mechanisms of Bulinus and Biomphalaria can be evaded in this way has potential importance for man, as it suggests a way by which a schistosome strain could eventually acquire the ability to develop unaided in a new snail host, resulting possibly in a major change in the epidemiology of transmission. References Albaret, J.L., Picot, H., Diaw, O.T., Bayssade-Dufour, C., Vassiliadès, G. et al. 1985. Enquête sur les schistosomes de l’homme et du bétail au Sénégal, à l’aide des identifications spécifiques fournies par la chétotaxie des cercaires. Annales de Parasitologie humaine et comparée, 60:417–434. Anderson, R.M. & May, R.M. 1979. Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology, 79:63–94. Appleton, C.C. & Bruton, M.N. 1979. The epidemiology of schistosomiasis in the vicinity of Lake Sibaya, with a note on other areas of Tongaland (Natal, South Africa). Annals of Tropical Medicine and Parasitology, 73:547–561. Archibald, R.G. 1933. The endemiology and epidemiology of schistosomiasis in the Sudan. Journal of Tropical Medicine and Hygiene, 36:345–348. Arene, F.O.I., Ukpeibo, E.T. & Nwanze, E.A. 1989. Studies on schistosomiasis in the Niger Delta: Schistosoma intercalatum in the urban city of Port Harcourt, Nigeria. Public Health, 103:295–301. Babiker, S.M., Blankespoor, H.D., Wassila, M., Fenwick, A. & Daffalla, A.A. 1985. Transmission of Schistosoma haematobium in North Gezira, Sudan. Journal of Tropical Medicine and Hygiene, 88:65–73.

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Pitchford, R.J. & Visser, P.S. 1960. Some observations on Schistosoma mansoni in rodents in the Transvaal. Annals of Tropical Medicine and Parasitology, 54: 247–249. Pitchford, R.J. & Visser, P.S. 1965. Some further observations on schistosome transmission in the eastern Transvaal. Bulletin of the World Health Organisation, 32: 83–104. Pitchford, R.J. & Visser, P.S. 1969. The use of behaviour patterns of larval schistosomes in assessing the bilharzia potential of non-endemic areas. South African Medical Journal , 43:983–995. Pitchford, R.J. & Visser, P.S. 1981. Schistosoma Weinland, 1858 from Hippopotamus amphibius Linnaeus, 1758 in the Kruger National Park. Onderstepoort Journal of Veterinary Research, 48:181–184. Pitchford, R.J., Meyling, A.H., Meyling, J. et al. 1969. Cercarial shedding patterns of various schistosome species under outdoor conditions in the Transvaal. Annals of Tropical Medicine and Parasitology, 63:359–371. Polderman, A.M., Mpamila, K., Manshande, J.P., Gryseels, B. & Van Schayk, O. 1985. Historical, geological and ecological aspects of transmission of intestinal schistosomiasis in Maniema, Kivu Province, Zaire. Annales de la Société Belge de Médecine tropicale, 65: 251–261. Porter, A. 1938. The larval Trematoda found in certain South African Mollusca with special reference to schistosomiasis. Publications of the South African Institute for Medical Research, 42:1–492. Preston, T.M. & Southgate, V.R. 1994. The species specificity of Bulinus-Schistosoma interactions. Parasitology Today, 10(2):69–73. Ramajo-Martin, V. 1972. Contribucion al estudio epizootiologico de la esquistosomiasis bovina (S. bovis) en la Provincia de Salamanca. Revista Iberica de Parasitologia, 32: 207– 242. Ramajo-Martin, V. 1978. Observaciones acerca de la receptividad de diversas poblaciones de Planorbarius metidjensis, Bulinus (B.) truncatus y Biomphalaria glabrata a Schistosoma bovis de España. Revista Ibérica de Parasitologia, 38:537–549. Ratard, R.C. & Greer, G.J. 1991. A new focus of Schistosoma haematobium/S. intercalatum hybrid in Cameroon. American Journal of Tropical Medicine and Hygiene, 45:332–338. Raymond, K.M. & Probert, A.J. 1987. The effect of light and darkness on the production of cercariae of Schistosoma haematobium from Bulinus globosus. Journal of Helminthology, 61:291–296. Raymond, K.M. & Probert, A.J. 1991. The daily cercarial emission rhythm of Schistosoma margrebowiei with particular reference to dark period stimuli. Journal of Helminthology, 65:159–168. Reinecke, R. 1970. The epizootiology of an outbreak of bilharziasis in Zululand. Central African Journal of Medicine, 16, supplement: 10–12. Richards, C.S. 1975. Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology, 70:231–241. Ripert, C.L. & Raccurt, C.P. 1987, 1988. The impact of small dams on parasitic diseases in Cameroon . Parasitology Today, 3(9):287–289 and 4(7):199. Rollinson, D. & Simpson, A.J.G. (Eds). 1987. The Biology of Schistosomes. From Genes to Latrines. London: Academic Press.

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Southgate, V.R. & Agrawal, M.C. 1990. Human schistosomiasis in India? Parasitology Today, 6(5):166–168. Southgate, V.R. & Knowles, R.J. 1975a. Observations on Schistosoma bovis Sonsino, 1876. Journal of Natural History, 9:273–314. Southgate, V.R. & Knowles, R.J. 1975b. The intermediate hosts of Schistosoma bovis in western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene, 69: 356–357. Southgate, V.R. & Knowles, R.J. 1977a. On the intermediate hosts of Schistosoma haematobium from western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene, 71:82–83. Southgate, V.R. & Knowles, R.J. 1977b. On Schistosoma margrebowiei Le Roux, 1933: the morphology of the egg, miracidium and cercaria, the compatibility with species of Bulinus, etc. Zeitschrift für Parasitenkunde, 54:233–250. Southgate, V.R. & Knowles, R.J. 1978. Studies on Schistosoma bovis from different geographical areas. In Proceedings of Second European Multicolloquy of Parasitology, Trogir, 1975:135–142. Petrovic, Z. (Ed.). Belgrade: Association of Yugoslav Parasitologists. Southgate, V.R. & Rollinson, D. 1987. Natural history of transmission and schistosome interactions. In The Biology of Schistosomes: 347–378. Rollinson, D. & Simpson, A.J.G. (Eds). London: Academic Press. Southgate, V.R., Ross, G.C. & Knowles, R.J. 1981. On Schistosoma leiperi Le Roux, 1955: scanning electron microscopy of adult worms, compatibility with species of Bulinus, development in Mesocricetus auratus, and isoenzymes. Zeitschrift für Parasitenkunde, 66: 63–81. Southgate, V.R., Van Wijk, H.B. & Wright, C.A. 1976. Schistosomiasis at Loum, Cameroun: S. haematobium, S. intercalatum and their natural hybrid. Zeitschrift für Parasitenkunde, 49:145–159. Southgate, V.R., Brown, D.S., Rollinson, D., Ross, G.C. & Knowles, R.J. 1985. Bulinus tropicus from central Kenya acting as a host for Schistosoma bovis. Zeitschrift für Parasitenkunde, 71:61–69. Southgate, V.R., Brown, D.S., Warlow, A., Knowles, R.J. & Jones, A. 1989. The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitology Research, 75:381–391. Southgate, V.R., Howard, G.W., Rollinson, D., Brown, D.S., Ross, G.C. & Knowles, R.J. 1985. Bulinus tropicus, a natural intermediate host for Schistosoma margrebowiei in Lochinvar National Park, Zambia. Journal of Helminthology, 59:153–155. Southgate, V.R., Rollinson, D., Ross, G.C. & Knowles, R.J. 1980. Observations on an isolate of Schistosoma bovis from Tanzania. Zeitschrift für Parasitenkunde, 63: 241– 249. Southgate, V.R., Rollinson, D., Ross, G.C. & Knowles, R.J. 1982. Mating behaviour in mixed infections of Schistosoma haematobium and S. intercalatum. Journal of Natural History, 16:491–496. Southgate, V.R., Rollinson, D., Ross, G.C., Knowles, R.J. & Vercruysse, J. 1985. On Schistosoma curassoni, S. haematobium and S. bovis from Senegal: development in Mesocricetus auratus, compatibility with species of Bulinus and their enzymes. Journal of Natural History, 19:1249–1267. Southgate, V.R., Rollinson, D., Kaukas, A., Almeda, J., Sousa, A.M., Castro, F., Soares, E. & Corachan, M. 1994. Schistosomiasis in the Republic of São Tomé and Principe:

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characterisation of Schistosoma intercalatum. Transactions of the Royal Society of Tropical Medicine and Hygiene, in press. Southgate, V.R., Wright, C.A., Laaziri, H.M. & Knowles, R.J. 1984. Is Planorbarius metidjensis compatible with Schistosoma haematobium and S. bovis? Bulletin de la Société de Pathologie exotique, 77:499–506. Sturrock, B.M. 1967. The effect of infection with Schistosoma haematobium on the growth and reproduction rates of Bulinus (P.) nasutus productus. Annals of Tropical Medicine and Parasitology, 61:321–325. Sturrock, B.M. 1968. Resistance of B. (P.) nasutus productus to infection by S. haematobium. Annals of Tropical Medicine and Parasitology, 62:393–397. Sturrock, R.F. 1965. Studies on the biology of Biomphalaria angulosa Mandahl-Barth and on its ability to act as an intermediate host of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology , 59:1–9. Talla, I., Kongs, A., Verlé, P., Belot, J., Sarr, S. & Coll, A.M. 1990. Outbreak of intestinal schistosomiasis in the Senegal River Basin. Annales de la Société Belge de Médecine tropicale, 70:173–180. Talla, I., Kongs, A. & Verlé, P. 1992. Preliminary study of the prevalence of human schistosomiasis in Richard-Toll (Senegal River Basin). Transactions of the Royal Society of Tropical Medicine and Hygiene, 86:182. Taylor, M.G. 1970. Hybridisation experiments on five species of African schistosomes. Journal of Helminthology, 44:253–314. Taylor, M.G., Nelson, G.S., Smith, M. et al. 1973. Studies on heterologous immunity in schistosomiasis, 7. Bulletin of the World Health Organisation, 49:57–65. Tchuem Tchuente, L.A. & Jourdane, J. 1993. Further data on the compatibility between Schistosoma intercalatum (Lower Guinea strain) and Bulinus forskalii: epidemeological consequences. Tropical Medicine and Parasitology, 44:221–222. Teesdale, C. 1962. Ecological observations on the molluscs of significance in the transmission of bilharziasis in Kenya. Bulletin of the World Health Organisation, 27: 759– 782. Teesdale, C. & Nelson, G.S. 1958. Recent work on schistosomes and snails in Kenya. East African Medical Journal, 35:427–438. Teesdale, C.H., Baltes, R. & Manjolo, C.H. 1986. A simple device for the detection of the infected snail intermediate hosts of schistosomiasis in the field. Tropical Medicine and Parasitology, 37:186–187. Touassem, R. & Jourdane, J. 1986. Etude de la compatibilité de Schistosoma bovis du Soudan de d’Espagne vis-à-vis de Bulinus truncatus de Tunisie et Planorbarius metidjensis du Maroc. Annales de Parasitologie humaine et comparée, 61:43–54. van der Knaap, W.P. & Loker, E.S. 1990. Immune mechanisms in trematode-snail interactions. Parasitology Today, 6(6):175–182. Van Wyk, J.A. 1977. Transmission of Schistosoma mattheei from animals to man. In Medicine in a Tropical Environment: 705–707. Gear, J.H. (Ed.). Cape Town: Balkema. Van Wyk, J.A. 1983. The importance of animals in human schistosomiasis in South Africa. South African Medical Journal, 63:201–204. Van Wyk, J.A., Bartsch, R.C., Van Rensburg, L.J., Heitmann, L.P. & Goosen, P.J. 1974. Studies on schistosomiasis. 6. A field outbreak of bilharzia in cattle. Onderstepoort Journal of Veterinary Research, 41:39–50.

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Véra, C., Jourdane, J., Sellin, B. & Combes, C. 1990. Genetic variability in the compatibility between Schistosoma haematobium and its potential vectors in Niger. Epidemiological implications. Tropical Medicine and Parasitology, 41:143–148. Véra, C., Mouchet, F., Brémond, P., Sidiki, A., Sellin, E. & Sellin, B. 1992. Natural infection of Bulinus senegalensis by Schistosoma haematobium in a temporary pool focus in Niger: characterisation by cercarial emergence patterns. Transactions of the Royal Society of Tropical Medicine and Hygiene, 86:62. Vercruysse, J., Southgate, V.R. & Rollinson, D. 1984. Schistosoma curassoni Brumpt, 1931 in sheep and goats in Senegal. Journal of Natural History, 18:969–976. Webbe, G. & James, C. 1971a. Infra-specific variations of Schistosoma haematobium. Journal of Helminthology, 45:403–413. Webbe, G. & James, C. 1971b. A comparison of two geographical strains of S. haematobium. Journal of Helminthology, 45:271–284. Webbe, G. & James, C. 1972. Host-parasite relationships of Bulinus globosus and B. truncatus with strains of S. haematobium. Journal of Helminthology, 46:185–199. Wen, S.T. & Chu, K.Y. 1984. Preliminary schistosomiasis survey in the lower Volta River below Akosombo Dam, Ghana. Annals of Tropical Medicine and Parasitology, 78: 129–133. White, P.T., Gbakima, A.A. & Amara, S.V. 1989. Schistosoma mansoni in Sierra Leone: an invader extending its range? Annals of Tropical Medicine and Parasitology, 83: 191– 193. Woodruff, D.S. 1985. Genetic control of schistosomiasis: a technique based on genetic manipulation of intermediate host snail populations. Comparative Pathobiology, 8: 41– 68. Woolhouse, M.E.J. 1989a. On the interpretation of age-prevalence curves for schistosome infections in host snails. Parasitology, 99:47–56. Woolhouse, M.E.J. 1989b. The effect of schistosome infection on the mortality rates of Bulinus globosus and Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology, 83:137–141. Woolhouse, M.E.J. & Chandiwana, S.K. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology, 98:21–34. Woolhouse, M.E.J. & Chandiwana, S.K. 1990a. The epidemiology of schistosome infections of snails: taking the theory into the field. Parasitology Today, 6(3):65–70. Woolhouse, M.E.J. & Chandiwana, S.K. 1990b. Population biology of the freshwater snail Bulinus globosus in the Zimbabwe highveld. Journal of Applied Ecology, 27: 41– 59. Woolhouse, M.E.J., Chandiwana, S.K. & Bradley, M. 1990. On the distribution of schistosome infections among host snails. International Journal of Parasitology, 20: 325– 327. World Health Organisation 1993. The Control of Schistosomiasis. WHO Technical Report Series, 830. Geneva: World Health Organisation. Wright, C.A. 1959. Host-location by trematode miracidia. Annals of Tropical Medicine and Parasitology, 53:288–292. Wright, C.A. 1962. The significance of infra-specific taxonomy in bilharziasis. In Ciba Foundation Symposium on Bilharziasis: 103–126. Wolstenholme, G.E. & O’Connor, M. (Eds). London: Churchill.

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Wright, C.A. 1966. Relationships between schistosomes and their molluscan hosts in Africa. Journal of Helminthology, 40:403–412. Wright, C.A. 1971. Flukes and Snails. London: George Allen & Unwin. Wright, C.A. & Knowles, R.J. 1972. Studies on Schistosoma haematobium in the laboratory. 3. Strains from Iran, Mauritius and Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene, 66:108–118. Wright, C.A. & Ross, G.C. 1980. Hybrids between Schistosoma haematobium and S. mattheei and their identification by isoelectric focusing of enzymes. Transactions of the Royal Society of Tropical Medicine and Hygiene, 74:326–332. Wright, C.A. & Ross, G.C. 1983. Enzyme analysis of Schistosoma haematobium. Bulletin of the World Health Organisation, 61:307–316. Wright, C.A. & Southgate, V.R. 1976. Hybridisation of schistosomes and some of its implications. In Genetic Aspects of Host-parasite Relationships: 55–86. Taylor, A.E. & Muller, R. (Eds). Oxford: Blackwell Scientific Publications. Wright, C.A. & Southgate, V.R. 1981. Coevolution of digeneans and molluscs, with special regard to schistosomes and their intermediate hosts. In The Evolving Biosphere: 191–205. Forey, P.L. (Ed.). London: British Museum (Natural History). Wright, C.A., Rollinson, D. & Goll, P.H. 1979. Parasites in Bulinus senegalensis and their detection. Parasitology, 79:95–105. Wright C.A., Southgate, V.R. & Howard, G.W. 1979. Observations on the life-cycle of Schistosoma margrebowiei in Zambia. Journal of Natural History, 13:499–506. Wright, C.A., Southgate, V.R. & Knowles, R.J. 1972. What is Schistosoma intercalatum Fisher, 1934? Transactions of the Royal Society of Tropical Medicine and Hygiene, 66:28– 64. Wright, C.A., Southgate, V.R. & Ross, G.C. 1979. Enzymes in Schistosoma intercalatum and the relative status of the Lower Guinea and Zaire strains of the parasite. International Journal of Parasitology, 9:523–528. Wright, C.A., Southgate, V.R., Van Wijk, H.B. et al. 1974. Hybrids between Schistosoma haematobium and S. intercalatum in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene , 68:413–414.

Chapter 6. Other snail-transmitted parasitic infections

These infections do not cause disease in man to the same extent as the schistosomes. The most important in Africa seems to be paragonimiasis; heterophyiasis is even more localised, and human fascioliasis is rarely reported. Two of the other infections included here, echinostomiasis and angiostrongyliasis, are not known from man in Africa, but there appears to be potential for human infection to occur in this continent. For livestock the most serious infections are paramphistomiasis and fascioliasis. None of these parasites is dependent on man as a host; the life cycles where man does play some part are examples of zoonoses (Malek, 1980; Ukoli, 1984; Geerts et al., 1987). A summary follows of the systematic positions of the parasites, the infections caused and the definitive hosts. Class Trematoda: Subclass Digenea

Family Paragonimidae: Genus Paragonimus Braun. Paragonimiasis of man in West Africa. Family Fasciolidae: Genus Fasciola Linnaeus. Fascioliasis of livestock and wild grazing animals, rarely of man in Africa. Family Heterophyidae: Genus Heterophyes Cobbold. Heterophyiasis of man and domesticated animals in Egypt. Family Paramphistomatidae: Genus Calicophoron Näsmarck and other genera. Paramphistomiasis of domesticated and wild grazing animals. Gastrodiscus Leuckart. Gastrodisciasis of donkeys and other equines. Family Echinostomatidae: Genus Echinostoma Rudolphi. Echinostomiasis of aquatic or semi-aquatic birds and mammals, including man in Asia but not reported from man in Africa. Class Nematoda

Family Metastrongylidae: Genus Angiostrongylus. Angiostrongyliasis of man in Asia, but not reported from man in Africa.

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Paragonimiasis Human infection with lung flukes (paragonimiasis) is commonest in eastern Asia, where the species found in man is usually Paragonimus westermani (Kerbert), a parasite primarily of carnivores and especially the cat family. The eggs may be passed in faeces and are commonly present in the sputum of man. Hatching takes place in water to produce a free-swimming miracidium and further development proceeds in a suitable prosobranch snail, which serves as the first intermediate host. Cercariae emerge after about three months and then encyst within the gills or muscles of certain kinds of freshwater crab, the second intermediate host. Infection of man and other definitive hosts results from the eating of raw or lightly-cooked crab tissue containing encysted metacercariae. In Africa paragonimiasis is commonest in parts of Cameroon, Nigeria and Liberia. The first systematic search (Zahra, 1952) revealed a prevalence of 4% in the lower Bakossi area of south-west Cameroon. Studies continued in this area (Vogel & Crewe, 1965; Voelker & Sachs, 1977) and later 5.6% positives were found among 900 sputum examinations (Kum & Nchinda, 1982). Other endemic areas in Cameroon (Ripert et al., 1981) are likewise located in rain forest, where the civet cat Viverra civetta Schreber seemed to be the main natural definitive host. Prevalences of 5–10% were estimated for endemic areas in southeast Nigeria, where the recent appearance of infection in man was attributed to the increased consumption of inadequately-cooked crabs when civil war caused food shortage (Nwokolo, 1974). The extent of the endemic areas in this part of Nigeria was defined by Voelker & Sachs (1977) according to the occurrence of infected crabs. There is a high prevalence of paragonimiasis in children in Liberia (Sachs & Cumberlidge, 1990) and scattered cases are reported from Gambia, Ivory Coast, Upper Volta and Zaire (Nozais et al., 1980). The identification of lung flukes infecting man in Africa remained uncertain for some years. Eventually worms obtained from the mongoose Crossarchus obscurus in Cameroon were described as the new species Paragonimus africanus by Voelker & Vogel (1965). The eggs of these specimens closely resembled those found in man in the same region. A smaller species obtained from a dog in Cameroon, and from a swamp mongoose (Atilax paludinosus) in Liberia, was named P. uterobilateralis Voelker & Vogel, 1965. Human infection in Nigeria and further westwards seems due entirely to P. uterobilateralis. According to the prevalences of the two infections in crabs, P. africanus is predominant in south-west Cameroon, whereas P. uterobilateralis becomes increasingly common towards the north and was the only species found in the upper reaches of the Cross River flowing into Nigeria (Voelker & Sachs, 1977). The status of Poikilorchis congolensis described from Zaire (Fain & Van de Pitte, 1957) is unclear. What part, if any, the distribution of the snail host may play in the occurrence of human paragonimiasis in Africa is unknown, because its identity has not yet been discovered. Metacercariae have been found in freshwater crabs of the

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genera Sudanautes in Cameroon and Nigeria (Vogel & Crewe, 1965; Nwokolo, 1974; Voelker & Sachs, 1977; Ripert et al., 1981) and Liberonautes in Liberia (Sachs & Cumberlidge, 1989, 1991). But the identity of the snail host remains elusive, despite extensive investigations. Immediate suspects are the common prosobranchs of forest streams within the endemic areas; Potadoma freethi in Cameroon (Vogel & Crewe, 1965), P. liberiensis (=sancti-pauli) and Afropomus balanoidea in Liberia (Voelker, 1973). However, no infection was found in over 6000 specimens of A. balanoidea from Liberia and over 2000 Lanistes sp. from Nigeria examined by Voelker and colleagues (cited in Sachs & Cumberlidge, 1989) or in many P. freethi dissected in Cameroon (Ripert et al., 1981). Cercariae obtained from P. freethi and identified as Paragonimus africanus by Moyou et al. (1984) were a different trematode according to Sachs & Cumberlidge (1989). These authors described microcercous Paragonimus-like cercariae from a subulinid landsnail Homorus (Striosubulina) striatella Rang collected in Liberia. The infected snails lived in humid microhabitats beneath dead or decaying vegetation, between 20 and 100 m from a creek where crabs carrying metacercariae of P. uterobilateralis were found; the parasite caused castration of the host snail (Berthold, 1990). But the later finding of metacercariae in species of crabs which never leave large rivers suggested that the search for the first intermediate host should again be directed towards fully aquatic snails (Sachs & Cumberlidge, 1991). It may be concluded that further investigations of both semi-terrestrial and aquatic snails are needed to clarify the identity and habitat of the snail host in Liberia, and in all areas of endemic paragonimiasis in Africa. A report of a case of human paragonimiasis in Natal Province, South Africa (Proctor & Gregory, 1974) is of interest. The eggs were not identified with certainty, but similar eggs were obtained from cats in the Durban area and possibly belong to the species P. kellicotti, which does not normally infect man. Melanoides tuberculata is the most likely first intermediate host in this area, where it is the only freshwater prosobranch snail known to occur. Fascioliasis According to Kendall (1965), the trematode genus Fasciola probably comprises only two true species, Fasciola hepatica (Linnaeus, 1758) and F. gigantica (Cobbold, 1855). Both occur in Africa and at least two other species have been described from this continent, F. nyanzae Leiper, 1910, of the hippopotamus and F. tragelaphi Pike & Condy, 1966, known only from an antelope, the Sitatunga (Tragelaphus spekei). Adult liver flukes normally inhabit the bile ducts and gallbladders of grazing animals which become infected by ingesting vegetation carrying encysted metacercariae. Eggs are passed with the faeces and can remain viable for up to several months, though in the laboratory separation from faecal material is necessary for normal development and hatching (Kendall, 1965). Development of

364 OTHER SNAIL-TRANSMITTED PARASITIC INFECTIONS

the egg is also dependent on suitable humidity and temperature. Eggs of F. hepatica hatch after about 12 days at 26°C, but not until 60 days at 12°C, and development is inhibited below 9–5°C (data summarised by Kendall, 1965). The stimulus of light appears to be necessary for the successful emergence of the miracidium, which swims freely and seeks the intermediate host, a species of Lymnaea. Usually the intra-molluscan development of Fasciola proceeds through the larval stages of sporocyst and rediae, but direct metamorphosis of the F. gigantica miracidium into a first-generation redia is reported (OgamboOngoma & Goodman, 1976). Cercariae of F. hepatica can leave the snail after only 21 days at 27°C (Kendall, 1965), but the prepatent period may be much longer at lower temperatures. The subsequent behaviour of the cercaria is in striking contrast to that of a schistosome, for within about one hour of its emergence from the host snail it encysts as a metacercaria, upon a suitable surface such as a plant stem; the cercaria of Fasciola thus plays no direct part in locating a mammalian host. Fasciola gigantica is the commonest liver fluke in Africa and is widely distributed, while F. hepatica seems reliably reported from perhaps only the highlands of Ethiopia (Goll & Scott, 1978, 1979), Kenya (Ogambo-Ongoma, 1969) and Lesotho (Prinsloo & Van Eeden, 1977, and earlier papers). The explanation of this pattern may be that the preferred snail host of F. hepatica is Lymnaea truncatula, which is commonest in the cooler areas of the eastern highlands, whereas L. natalensis is the host for F. gigantica and occurs throughout tropical and sub-tropical Africa. Human infection with liver fluke is rare in tropical Africa (Goldsmid, 1975; World Health Organisation, 1990), probably because it is not the usual habit to eat watercress plants, the common source of the infection acquired by people in temperate northern countries. Moderate prevalences have been found in wild grazing animals, although infection rates are generally low (Hammond, 1972). Infection is heavier in cattle and sheep and can cause considerable economic loss, for example in Kenya (£160 000 sterling for 1972–74; Preston & Castelino, 1977), Zimbabwe (Lawrence & Condy, 1970) and West Africa (Schillhorn van Veen, 1980a). Prevalence of infection in cattle from different localities in Ethiopia ranged from 29% to 78%, while in Kenya 20% of 8700 bovine livers from a large area were infested (Preston & Castelino, 1977). The snail hosts of Fasciola are confined to the Lymnaeidae. For F. gigantica they belong to the superspecies L. auricularia, distributed through Europe, Asia and Africa, where it is represented by L. natalensis. This species is also the intermediate host for F. nyanzae of the hippopotamus (Dinnik & Dinnik, 1961). F. hepatica is transmitted usually by L. truncatula in Africa, Europe and South West Asia. In West Pakistan, F. hepatica replaces F. gigantica above an altitude of 1200 m (4000 feet) in relation to the distributions of their different snail hosts, and the parasites do not appear to share an intermediate host (Kendall, 1954). In the laboratory F. hepatica proved almost entirely non-infective to L. natalensis from East Africa (Kendall, 1965).

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An additional potential intermediate host for Fasciola in some parts of Africa is Lymnaea columella, an introduced snail of American origin. It is known to have become a host in some other parts of the world where it has been introduced, including Hawaii (Alicata, 1953) and New Zealand (Pullan & Whitten, 1972). In Australia L. columella has spread from metropolitan areas into grazing lands, and natural infection with F. hepatica is reported (Boray et al., 1985). L. columella is also widely distributed in South Africa, but any contribution it may make to transmission of fascioliasis has not yet been evaluated. The semi-amphibious habits of this snail would favour the encystment of metacercariae on the marginal vegetation likely to be eaten by grazing animals. The role of wild mammals in the epidemiology of fascioliasis has received attention, in relation to the infection of domestic livestock and out of concern that fascioliasis could damage animals protected within game reserves. Hammond (1972) reviewed fifty records of infection in fifteen species of artiodactyls and the elephant; F. gigantica is the most frequently recorded liverfluke, being known from the buffalo, wildebeeste, kob, eland and hartebeeste. In addition this fluke has been found in the warthog (Troncy et al., 1972). Deaths of wild animals due to fascioliasis have been recorded in Zimbabwe (Rhodesia). Prevalences of about 50% in buffalo, hartebeeste and kob in some areas of Uganda suggest that fascioliasis is maintained there in the absence of domestic livestock. F. nyanzae is known only from the hippopotamus, in which prevalences reach almost 100%. In general, however, the prevalence of fascioliasis in wild grazing animals seems low. This could be because the water resources available to animals confined within game reserves are often so severely trampled that aquatic vegetation is destroyed and snail populations are drastically reduced or eliminated. Variations in the epidemiology of fascioliasis transmission are related to the timing of intra-molluscan development, fluctuations in snail populations and primarily to the availability of the host snail. A seasonal pattern was clearly evident in the development of F. gigantica in outdoor aquaria at an altitude of 2073 m (6800 feet) in the highlands of Kenya, north-west of Nairobi, and cercarial production ceased entirely during the coldest periods (Dinnik & Dinnik, 1963). Yet at the even higher altitude of 2667 m (8743 feet) in the Nandi Hills of western Kenya, snails capable of shedding cercariae were present in a moderately large dam throughout the year (Preston & Castelino, 1977). Continuous shedding at this higher altitude can perhaps be explained by the moderating effect upon the temperature of the dam of its much greater volume of water compared with the outdoor aquaria. Small waterbodies are also more vulnerable to seasonal reduction in rainfall, and the disappearance of surface water from some sites inhabited by L. natalensis in the Kenyan highlands (Bitakaramire, 1968) would interrupt emission of cercariae. At the lower altitude of Lake Victoria the warmer climate favours continuous transmission of fascioliasis, but a marked seasonality is imposed by fluctuation

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in rainfall. During the dry season many eggs of F. gigantica fail to hatch when dung dries rapidly (Ogambo-Ongoma, 1971). A further limitation to fascioliasis transmission in Uganda is the rarity of Lymnaea natalensis in the dense stands of papyrus that commonly fringe the rivers and cover swamps (Ogambo-Ongoma, 1972). Prevalence of F. gigantica in West Africa (reviewed by Schillhorn van Veen, 1980a) varies widely according to distribution of L. natalensis, grazing habits of cattle, accessibility of snail habitats and seasonal variation in rainfall. Juvenile Fasciola infections in snails are most common during the beginning of the dry season; metacercariae are acquired by grazing animals mainly during the middle of the dry season. In the savanna area of Zaria, Nigeria, the presence of livestock in snail-inhabited areas during the early rainy season is important in disseminating fascioliasis, for it is the infection of young snails of the rainyseason generation that leads to the peak of cercarial production in the dry season, and the consequent infection of cattle when they follow the receding water into the drying floodplains (Schillhorn van Veen, 1980b). An even more strictly seasonal life cycle is shown by F. hepatica on the central highland plateau of Ethiopia (Goll & Scott, 1978, 1979). In 1974, near Debra Berhan, active snail populations of the snail host, Lymnaea truncatula, were present for a period of only about 40 days, during July-August, when the pastures were thoroughly saturated by the long rains. Snails emerging from aestivation began immediately to shed cercariae developed from infections carried over from the previous rainy season. The resulting metacercariae were the primary source of infection acquired by sheep, although in favourable habitats new snail infections did mature rapidly enough to produce metacercariae during the same wet season. No attempt appears to have been made on a large scale to control transmission of Fasciola in Africa, but two trials of the molluscicide N-tritylmorpholine against Lymnaea populations were carried out in the 1970s. From the results in Kenya, it was considered feasible to eradicate L. natalensis from dams by means of a few treatments (Preston & Castelino, 1977). In Lesotho, a single treatment proved effective for only short-term control of L. truncatula; with this amphibious snail the timing of application of the molluscicide was critical, in order to avoid the growth of dense vegetation that would prevent penetration of the chemical to the substrate (Prinsloo & Van Eeden, 1977). However, it was concluded that mollusciciding could still be important, in conjunction with antihelminthic drugs, in controlling fascioliasis in Lesotho, since fencing livestock off from marshes would be impracticable because of their importance as sources of water and winter grazing, and draining of damp pastures would be undesirable as it would contribute to soil erosion.

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Heterophyiasis When adult, the species of Heterophyes are parasites in the intestine of a variety of wild mammals and birds, though near human habitations dogs and domestic cats are important hosts. Man is infected incidentally, though quite commonly in certain areas and especially in the Near East and Far East, where fish is eaten raw or lightly cooked. Human heterophyiasis due to Heterophyes heterophyes (Siebold, 1852) has long been known in Egypt, with high prevalences in children of some communities, though incidence may be decreasing (review by Taraschewski, 1984). The life cycle of H. heterophyes includes two intermediate hosts. Eggs passed with the faeces of the definitive host hatch in water and the miracidium penetrates a snail of the family Potamididae; in Egypt this is Pirenella conica, which lives in brackish and even highly saline lagoons. The freely swimming cercaria encysts within the muscles of a fish, commonly a member of the mullet family Mugilidae. Definitive hosts become infected by eating fishes containing metacercarial cysts. In Africa human heterophyiasis seems to be confined to Egypt and is particularly prevalent in the Nile Delta. Infection with H. heterophyes in P. conica was found also in the two inland saline lakes Timsah and Qarun, and at sites on the Red Sea coast (Taraschewski, 1985). The possibility for H. heterophyes to maintain its life cycle further south should be borne in mind, as the southern limit for the distribution of P. conica is not clear and other potamidid snails, such as Cerithidea, occur in brackish water on the coast of eastern Africa southwards into Natal. Paramphistomiasis The Paramphistomatidae and related trematode families comprise numerous genera and species, of which a limited number sometimes produce massive infections in domestic livestock and wild grazing animals in Africa (Dinnik, 1964). In a world-wide review, Horak (1971) stressed the difficulty of classifying and identifying these flukes; their taxonomy has been much improved by the revisions of Eduardo (1983, and earlier papers). These worms are commonly Table 6.1. Amphistome parasites of grazing animals, and snails found naturally infected in Africa, the Near East, Madagascar and Mauritius. Amphistome

Host snail

Country and authority

Calicophoron microbothrium

Bulinus tropicus

South Africa (‘B.schakoi’ of Le Roux, 1930; Dinnik, 1964). Kenya (Dinnik & Dinnik, 1954; Southgate et al., 1989).

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Amphistome

Host snail

Country and authority

B. liratus

Madagascar (Prod’hon et al., 1968). Ethiopia (Graber & Daynes, 1974) Israel (Lengy, 1960) Iran (Arfaa, 1962) Ethiopia (Graber & Daynes, 1974) Zambia (Wright et al., 1979a) Gambia (Wright et al., 1979b) Zambia, Mauritius (Dinnik, 1961) Kenya and Zambia (Dinnik, 1965). Ethiopia (Graber & Daynes, 1974) Kenya (Dinnik, 1962) Togo (Albaret et al., 1978) Zambia (Dinnik, 1965) Zambia (Wright et al., 1979a) Kenya, Zambia (‘Anisus’ of Dinnik, 1965) Madagascar (Grétillat, 1959) Mauritius (‘B.forskali’ of Dinnik, 1965)

B. natalensis B. truncatus B. octoploidus B. globosus B. Senegalensis Paramphistomum phillerouxi P. sukari

B. forskalii, B. cernicus

P. daubneyi P. togolense Carmyerius parvipapillatus Carmyerius sp.

Lymnaea truncatula Bulinus forskalii Bulinus globosus B. forskalii

C. mancupatus and C. exoporus C. dollfusi Stephanopharynx compactus

Ceratophallus natalensis

Biomphalaria pfeifferi

B. ‘mariei’ B. cernicus

known as stomach flukes, conical flukes or ‘amphistomes’. They commonly live attached to the lining of the rumen, in groups of as many as several hundred individuals, of one or more species. Disease is caused when heavy infestation with immature flukes results in acute gastroenteritis with high morbidity and mortality, particularly in young animals. In Kenya 80% of high-grade beef cattle were found to be infected in the highlands (Dinnik, 1964) and serious outbreaks occur in sheep (Roach & Lopes, 1966). The most widely reported species causing harm to domestic livestock in Africa is Calicophoron microbothrium (Fischoeder, 1901, Paramphistomum) (Eduardo, 1983); this identification was confirmed recently according to the morphology of worms derived from naturally infected Bulinus tropicus collected in Kenya (Southgate et al., 1989). Some other species identified from grazing animals in Africa are listed in Table 6.1. A number have been found in the lechwe (Kobus leche) (Wright et al., 1979a).

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The life cycle of C. microbothrium in Africa south of the Sahara was first discovered by Le Roux (1930), who identified the parasite as Cotylophoron cotylophoron (Fischoeder) for reasons discussed by Dinnik (1965). Further details were studied in Kenya (Dinnik & Dinnik, 1954) and South Africa (Swart & Reinecke, 1962). Eggs passed in the faeces of the definitive host hatch in water after about 12 days at 27°C, producing free-swimming miracidia that enter a snail through the pneumostome (Dinnik & Dinnik, 1954). Cercariae may be shed as early as 30 days after infection, though prepatent periods of 51 days and more have been reported (Southgate et al., 1989). Infected snails may live and continue to shed cercariae for at least as long as a year. Cercariae encyst as metacercariae on various objects, including vegetation and snail shells, and may remain viable for more than 30 days in moist conditions. Metacercariae are ingested by definitive hosts; development into fully grown flukes takes 5 to 9 months. The snail host for C. microbothrium (Table 6.1) is commonly Bulinus tropicus in at least South Africa and Kenya, and B. truncatus in North Africa, the Near East and SW Asia. Naturally acquired infections have been reported also for B. globosus, B. octoploidus, B. senegalensis and diploid snails resembling B. natalensis (sources in Table 6.1). Isolates of C. microbothrium from Kenya (Dinnik, 1964; Southgate et al., 1989) developed in both B. tropicus and B. truncatus. Although experimental infections of B. africanus-group snails were almost entirely unsuccessful (Dinnik, 1964, 1965), a few field-collected B. globosus have produced metacercariae identified as C. microbothrium following infection of sheep (Dinnik, 1965; Wright et al., 1979a). Although the B. forskalii group seems to play little part in transmission, an experimental infection of B. forskalii itself is reported (Tager-Kagan, 1977) and infected B. senegalensis have been collected in the field (Wright et al., 1979b). The snail hosts known for other stomach flukes are listed in Table 6.1. Animals die from acute paramphistomiasis when an exceptional combination of environmental conditions favours a high density of viable metacercariae on the pasture (Dinnik, 1964). This can happen when snail populations are concentrated by the contraction of shallow pools during the dry season, resulting in a heavy metacercarial infestation of vegetation on damp ground surrounding the residual water. Almost every B. tropicus from some pools may be heavily infested with amphistome larvae, apparently of C. microbothrium. The cercariae are recognisable by their large size and darkly pigmented eyespots. The body of an infested snail may be occupied almost entirely by amphistome larvae and it is astonishing that the host remains alive. Swart & Reinecke (1962) reported that B. tropicus more than 21 days old were resistant to infection; they suggested that this could be important in allowing the very survival of the host species.

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Gastrodisciasis Gastrodiscus aegyptiacus Cobbold is a common intestinal fluke, though apparently of small economic importance, found in the horse, donkey and mule in Africa (Malek, 1980). Le Roux (1958) exposed to infection Lymnaea natalensis and a number of species of Biomphalaria and Bulinus, of which only B. forskalii and B. senegalensis proved susceptible. Immediately after emergence the cercariae moved towards the source of light and encysted on glass or blades of grass floated on the water. Naturally infected B. forskalii were collected in Sudan (Malek, 1960) and this snail was infected experimentally in Niger (TagerKagan, 1977). Echinostomiasis Echinostoma is a large and cosmopolitan digenean genus for which the vertebrate hosts are principally aquatic or semi-aquatic birds and mammals: the adult worms live in the intestines and bile ducts. Man is a subsidiary host for some species in SE Asia and the Far East, acquiring infection by eating raw snails, tadpoles or freshwater fishes containing encysted metacercariae. The biology of the better-known species was reviewed by Huffman & Fried (1990). Although echinostomiasis is apparently unknown in man in Africa, there is potential for infection in the wide distribution of the snail genera Gyraulus and Pila, which respectively provide the first and second intermediate hosts for Echinostoma ilocanum, a parasite of man and other mammalian hosts in SE Asia (Malek, 1980). Echinostomes are of interest also as possible biological agents for controlling transmission of schistosomes (Combes, 1982, and see Chapter 8), while certain species are so easily maintained in the laboratory that they provide an ideal model for experiments on parasite biology. The life cycle of the widely-distributed African species E. caproni Richard, 1964 (originally described from Madagascar) is known from extensive observations. These include, according to recent systematic revisions (reviewed by Huffman & Fried, 1990), studies of two synonymous African species, E. liei Jeyarasasingam et al., 1972, of Egypt and E. togoensis Jourdane & Kulo, 1981, of Togo, as well as the African echinostome commonly identified as E. revolutum. Vertebrate hosts in the wild are commonly domestic ducklings and rodents. Eggs passed in their faeces hatch in water; the miracidium continues its development in a species of Biomphalaria. Free-swimming cercariae are shed from the snail and encyst as metacercariae within a wide range of second intermediate hosts, including various species of snails and Rana tadpoles. Christensen et al. (1980) obtained viable metacercariae from all tested species of Biomphalaria and Bulinus, as well as members of 4 other snail genera. Vertebrate hosts become infected by eating second intermediate hosts containing metacercarial cysts.

FRESHWATER SNAILS OF AFRICA 371

Angiostrongyliasis Although parasitic members of the Nematoda do not have such specialised dispersive forms of larvae as the miracidium and the cercaria, some have complex life cycles and pass through intermediate hosts, which may be molluscs. Angiostrongylus cantonensis (Chen), the rat lung-worm, is widespread in southeastern Asia and is a cause of eosinophilic meningitis in man (Alicata, 1969, 1988; Muller, 1975). Man is not a normal host and the larval worms degenerate in the central nervous system. Although A. cantonensis is present in Mauritius and Madagascar (Alicata, 1969), Egypt is the only country in Africa where it has been identified, found in the snail Lanistes and the rat but not yet in man (Yousif & Ibrahim, 1978; Yousif et al., 1980). Rats become infected through eating molluscs containing infective third-stage larvae. Eggs passed in the rat’s faeces hatch, if conditions are moist, producing first-stage larvae that continue their development in a molluscan host, which may be entered with food or possibly by penetrating the body surface. Within the mollusc the larvae may reach their third stage of development in about two weeks. Completion of the life cycle follows on the molluscan host being eaten by a definitive host, though further development may be delayed, in Asia, if the mollusc is eaten by a land planarian, crab or freshwater prawn; such organisms may serve as ‘paratenic’ hosts, carrying the parasite larvae until they are ingested by a definitive host. In Egypt the snail Lanistes carinatus and the rat Rattus norvegicus are respectively the intermediate and definitive hosts (Yousif et al., 1980). Infection was found in 23% of the larger snails (20 mm or more in diameter) collected from a canal; one individual contained over 20 000 larvae. The parasite is capable of utilising a wide variety of molluscan hosts including terrestrial snails and slugs as well as freshwater snails. Achatina fulica Bowdich is a common source of human infection on some Pacific islands, and Pila ampullacea (Linnaeus) in Thailand. In experiments (Richards & Merritt, 1967; Yousif & Lämmler, 1975) infective third-stage larvae were obtained from a variety of African freshwater pulmonate snails, including Biomphalaria, Bulinus and Physa acuta. Alicata (1969, 1988) has advanced the idea that A. cantonensis was introduced into the Pacific area via Asia from Africa in the ‘Giant African landsnail’, Achatina fulica, which has been dispersed widely by man (Mead, 1961). However, the parasite is not known to occur in tropical Africa at present. Perhaps it does occur in eastern Africa and has escaped notice because non-marine molluscs are not popular as human food in this region. However, A. cantonensis seems unknown also in the parts of West Africa where quantities of Achatina are marketed for human consumption. The lack of records of A. cantonensis for countries such as Ghana, where conditions for transmission appear to be ideal, is a considerable difficulty for the hypothesis that the parasite has its origin in tropical Africa.

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References Albaret, J.L., Bayssade-Dufour, C., Guihon, J. et al., 1978. Cycle biologique de Paramphistomum togolense n. sp. Annales de Parasitologie humaine et comparée, 53:495– 510. Alicata, J.E. 1953. The snail Pseudosuccinea columella (Say), new intermediate host for the liver fluke, Fasciola gigantica (Cobbold). Journal of Parasitology, 39:673–674. Alicata, J.E. 1969. Present status of Angiostrongylus cantonensis infection in man and animals in the tropics. Journal of Tropical Medicine and Hygiene, 72:56–63. Alicata, J.E. 1988. Angiostrongyliasis Cantonensis (eosinophilic meningitis): historical events in its recognition as a new parasitic disease of man. Journal of the Washington Academy of Sciences, 78:38–46. Arfaa, F. 1962. A study of Paramphistomum microbothrium in Khuzistan, SW Iran. Annales de Parasitologie humaine et comparée, 37:549–555. Berthold, T. 1990. Parasitic castration in Homorus (Striosubulinus) striatellus (Gastropoda, Pulmonata, Subulinidae) by trematode infection in an endemic focus of pulmonary Paragonimiasis in Liberia, West Africa. Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg, new series, 31/32:5–13. Bitakaramire, P.K. 1968. Bovine fascioliasis in Kenya. Bulletin of Epizootic Diseases in Africa, 16:107–113. Boray, J.C., Fraser, G.C., Williams, J.D. & Wilson, J.M. 1985. The occurrence of the snail Lymnaea columella on grazing areas in New South Wales and studies on its susceptibility to Fasciola hepatica. Australian Veterinary Journal, 62:4–6. Combes, C. 1982. Trematodes: antagonism between species and sterilizing effects on snails in biological control. Parasitology, 84:151–175. Christensen, N.O., Frandsen, F. & Roushdy, M.Z. 1980. The influence of environmental conditions and parasite-intermediate host-related factors on the transmission of Echinostoma liei. Zeitschrift für Parasitenkunde, 63:47–63. Dinnik, J.A. 1961. Paramphistomum phillerouxi sp. nov. and its development in Bulinus forskali. Journal of Helminthology, 35:69–90. Dinnik, J.A. 1962. Paramphistomum daubneyi sp. nov. from cattle and its snail host in the Kenya highlands. Parasitology, 52:143–151. Dinnik, J.A. 1964. Intestinal paramphistomiasis and P. microbothrium Fischoeder in Africa. Bulletin of Epizootic Diseases in Africa, 12:439–454. Dinnik, J.A. 1965. The snail hosts of certain Paramphistomatidae and Gastrothylacidae (Trematoda) discovered by the late Dr P.L.LeRoux in Africa. Journal of Helminthology, 39:141–150. Dinnik, J.A. & Dinnik, N.N. 1954. The life cycle of Paramphistomum microbothrium Fischoeder, 1901. Parasitology, 44:225–299. Dinnik, J.A. & Dinnik, N.N. 1961. On the morphology and life history of Fasciola nyanzae (Leiper, 1910) from the Hippotamus. Journal of Helminthology, R.T.Leiper Supplement: 53–62. Dinnik, J.A. & Dinnik, N.N. 1963. Effect of the seasonal variations of temperature on the development of Fasciola gigantica in the snail hosts in the Kenya highlands. Bulletin of Epizootic Diseases in Africa, 11:197–207. Eduardo, S.L. 1983. The taxonomy of the family Paramphistomatidae Fischoeder, 1901 with special reference to the morphology of the species occurring in ruminants: 3.

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Revision of the genus Calicophoron Näsmark, 1937. Systematic Parasitology, 5: 25–79. Fain, A. & Van de Pitte, J. 1957. Description du nouveau distome vivant dans les kystes ou abcès retro-articulaires chez l’homme au Congo Belge. Annales de la Société Belge de Médecine tropicale, 37:251–253. Geerts, S., Kumar, V. & Brandt, J. (Eds). 1987. Helminth Zoonoses. Dordrecht: Martinus Nijhoff. Goldsmid, J.M. 1975. Ecological and cultural aspects of human trematodiasis (excluding schistosomiasis) in Africa. Central African Journal of Medicine, 21:49–53. Goll, P.H. & Scott, J.M. 1978. The interrelationship of Lymnaea truncatula and ovine fascioliasis in the Ethiopian central highlands. British Veterinary Journal, 134: 551– 555. Goll, P.H. & Scott, J.M. 1979. Fascioliasis in the Ethiopian central highlands. 1. Dynamics of intermediate snail host populations and their relation to infection in sheep. Miscellaneous Reports, Centre for Overseas Pest Research, 47:12 pp. Graber, M. & Daynes, P. 1974. Mollusques vecteurs de Trématodoses humaines et animales en Ethiopie. Revue d’Elevage et de Médecine vétérinaire des Pays tropicaux, 27: 307–322. Grétillat, 1959. Recherches sur le cycle evolutif de Carmyerius dollfusi Golvan, Chabaud et Grétillat, 1957 (Trematoda: Gastrothylacidae) à Madagascar. Comptes Rendus Hebdomadaire des Séances de l’Academie des Sciences, Paris , 248:1873–75. Hammond, J.A. 1972. Infections with Fasciola spp. in wildlife in Africa. Tropical Animal Health and Production, 4:1–13. Horak, I.G. 1971. Paramphistomiasis of domestic ruminants. In Advances in Parasitology, 9:33–72. Dawes, B. (Ed.). London and New York: Academic Press. Huffman, J.E. & Fried, B. 1990. Echinostoma and echinostomiasis. In Advances in Parasitology, 29:215–269. Baker, J.R. & Muller, R. (Eds). London and New York: Academic Press. Kendall, S.B. 1954. Fascioliasis in Pakistan. Annals of Tropical Medicine and Parasitology, 48:307–313. Kendall, S.B. 1965. Relationships between the species of Fasciola and their molluscan hosts. In Advances in Parasitology, 3:59–98. Dawes, B. (Ed.). London and New York: Academic Press. Kum, P.N. & Nchinda, T.C. 1982. Pulmonary paragonimiasis in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene, 76:768–772. Lawrence, J.A. & Condy, J.B. 1970. The developing problem of schistosomiasis in domestic stock in Rhodesia. Central African Journal of Medicine, 16, supplement: 19–22. Le Roux, P.L. 1930. A preliminary communication on the life cycle of Cotylophoron cotylophoron and its pathogenicity for sheep and cattle. Report of the Director of Veterinary Services and Animal Industries, Union of South Africa, 16:243–254. Le Roux, P.L. 1958. Life cycle of Gastrodiscus aegyptiacus (Cobbold, 1876). Transactions of the Royal Society of Tropical Medicine and Hygiene, 52:14–15. Lengy, J. 1960. Study on Paramphistomum microbothrium, a rumen parasite of cattle in Israel. Bulletin of the Research Council of Israel, 9B: 71–130. Malek, E.A. 1960. Bulinus (B.) forskalii Ehrenberg, 1831: intermediate host of Gastrodiscus aegytiacus (Cobbold, 1876) Looss, 1896. Journal of Parasitology, 46, supplement: 16.

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Malek, E.A. 1980. Snail-transmitted parasitic diseases. 2 vols. Boca Raton, Florida: CRC Press. Mead, A.R. 1961. The Giant African Snail: a Problem in Economic Malacology. Chicago: University Press. Moyou, S.R., Enyong, P.A. & Kouamouo, J. 1984. Isolation of Paragonimus africanus cercariae from a wild caught mollusc Potadoma freethi. In Abstract and Poster Volume, XI International Congress of Tropical Medicine and Malaria, Calgary/ Canada, 1984:208. Muller, R. 1975. Worms and Disease. A Manual of Medical Helminthology. London: William Heinemann Medical Books. Nozais, J.P., Douchet, J., Dunan, J. & Assale N’Dri, G. 1980. Les paragonimoses en Afrique noire. A propos d’un foyer récent de Côte d’Ivoire. Bulletin de la Société de Pathologie exotique, 73:155–163. Nwokolo, C. 1974. Endemic paragonimiasis in Africa. Bulletin of the World Health Organisation, 50:569–571. Ogambo-Ongoma, A.H. 1969. The incidence of Fasciola hepatica Linnaeus 1758 in Kenya cattle. Bulletin of Epizootic Diseases in Africa, 17:429–431. Ogambo-Ongoma, A.H. 1971. Field epidemiology of fascioliasis in Port Bell, Uganda. Bulletin of Epizootic Diseases in Africa, 19:341–351. Ogambo-Ongoma, A.H. 1972. Fascioliasis survey in Uganda. Bulletin of Epizootic Diseases in Africa, 20:35–41. Ogambo-Ongoma, A.H. & Goodman, J.D. 1976. Fasciola gigantica Cobbold, 1856 in the snail. Journal of Parasitology, 62:33–38. Preston, J.M. & Castelino, J.B. 1977. A study of the epidemiology of bovine fascioliasis in Kenya and its control using N-tritylmorpholine. British Veterinary Journal, 133: 600–608. Prinsloo, J.F. & Van Eeden, J.A. 1977. Control of Lymnaea truncatula in Lesotho. Wetenskaplijke Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 93:15 pp. Proctor, E.M. & Gregory, M.A. 1974. An ultrastructural study of ova of Paragonimus species from human and cat faeces. South African Medical Journal, 48:1947–1948. Prod’hon, J., Richard, J., Brygoo, E.R. et al. 1968. Presence de Paramphistomum microbothrium à Madagascar. Archives de l’Institut Pasteur de Madagascar, 37: 27–30. Pullan, N.B. & Whitten, L.K. 1972. Liver fluke, Fasciola hepatica, in New Zealand. A spreading parasite in sheep and cattle. New Zealand Veterinary Journal, 20:69–72. Richards, C.S. & Merritt, J.W. 1967. Studies on Angiostrongylus cantonensis in molluscan intermediate hosts. Journal of Parasitology, 53:382–388. Ripert, C., Carrie, J., Ambroise-Thomas, P., Baecher, R., Kum, N.P. & Samé-Ekobo, A. 1981. Etude épidémiologique et clinique de la paragonimose au Cameroun. Résultats du traitement par de Niclofolan. Bulletin de la Société de Pathologie exotique, 74: 319– 331. Roach, R.W. & Lopes, V. 1966. Mortality in adult ewes resulting from intestinal infestation with immature paramphistomes, complicated by severe fascioliasis. Bulletin of Epizootic Diseases in Africa, 14:317–323. Sachs, R. & Cumberlidge, N. 1989. Isolation of microcercous cercariae from snails caught in an endemic focus of Paragonimus uterobilateralis in Liberia, West Africa. Tropical Medicine and Parasitology, 40:69–72.

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Sachs, R. & Cumberlidge, N. 1990. Distribution of metacercariae in freshwater crabs in relation to Paragonimus infection of children in Liberia, West Africa. Annals of Tropical Medicine and Parasitology, 84:277–280. Sachs, R. & Cumberlidge, N. 1991. First record of the spiny river crab, Liberonautes chaperi (A.Milne-Edwards 1887), as a second intermediate host of Paragonimus uterobilateralis in Liberia. Annals of Tropical Medicine and Parasitology, 85: 471–472. Schillhorn van Veen, T.W. 1980a. Fascioliasis (Fasciola gigantica) in West Africa: a review. Veterinary Bulletin, 50:529–533. Schillhorn van Veen, T.W. 1980b. Dynamics of Lymnaea natalensis populations in the Zaria area (Nigeria) and the relation to Fasciola gigantica infections. Acta Tropica, 37: 183–194. Southgate, V.R., Brown, D.S., Warlow, A., Knowles, R.J. & Jones, A. 1989. The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitological Research, 75:381–391. Swart, P.J. & Reinecke, R.K. 1962. Studies on paramphistomiasis. 2. The mass production of metacercariae of P. microbothrium. Onderstepoort Journal of Veterinary Research, 29: 189–195. Tager-Kagan, P. 1977. Contribution a l’étude de l’épidémiologie des principales trématodoses des animaux domestiques dans la region du fleuve Niger. Revue d’Elevage et de Médecine vétérinaire des Pays tropicaux, 30:11–18. Taraschewski, H. 1984. Heterophyiasis, an intestinal fluke infection of man and vertebrates transmitted by euryhaline gastropods and fish. Helgolander Meeresuntersuchungen, 37:463–478. Taraschewski, H. 1985. Investigations on the prevalence of Heterophyes species in twelve populations of the first intermediate host in Egypt and Sudan. Journal of Tropical Medicine and Hygiene, 88:265–271. Troncy, P.M., Graber, M. & Thal, J. 1972. Enquête sur la pathologie de la fauna sauvage en Afrique Centrale, etc. Revue d’Elevage et de Médecine vétérinaire des Pays tropicaux, 25: 205–218. Ukoli, F.M.A. 1984. Introduction to Parasitology in Tropical Africa. Chichester, New York: John Wiley. Voelker. J. 1973. Morphologische-taxonomische Untersuchungen über Paragonimus uterobilateralis, etc. Zeitschrift für Tropenmedizin und Parasitologie, 24:1–20 Voelker, J. & Sachs, R. 1977. Uber die verbreitung von Lungenegeln (Paragonimus africanus und P. uterobilateralis) in West-Kamerun und Ost-Nigeria auf grund von untersuchungen an süsswasserkrabben auf befall mit metacercarien. Tropenmedezin und Parasitologie, 28:120–133. Voelker, J. & Vogel, H. 1965. Zwei neue Paragonimus-Arten aus West Afrika, etc. Zeitschrift für Tropenmedezin und Parasitologie, 16:125–148. Vogel, H. & Crewe, W. 1965. Beobachtungen über die Lungenegel-Infektion in Kameroun (Westafrika). Zeitschrift für Tropenmedezin und Parasitologie, 16: 109–125. World Health Organisation. 1990. Progress in the assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Unpublished Document, WHO/ SCHISTO/ 90.104. Geneva: World Health Organisation. Wright, C.A., Southgate, V.R. & Howard, G.W. 1979a. A note on the life-cycles of some amphistome flukes in Zambia. Journal of Helminthology, 53:251–252.

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Wright, C.A., Rollinson, D. & Goll, P.H. 1979b. Parasites in Bulinus senegalensis (Mollusca: Planorbidae) and their detection. Parasitology, 79:95–105. Yousif, F. & Ibrahim, A. 1978. The first record of Angiostrongylus cantonensis from Egypt. Zeitschrift für Parasitenkunde, 56:73–80. Yousif, F. & Lämmler, G. 1975. The suitability of several aquatic snails as intermediate hosts for Angiostrongylus cantonensis. Zeitschrift für Parasitenkunde, 47:203–210. Yousif, F., Roushdy, M. & El-Emam, M. 1980. The host-parasite relationships of Angiostrongylus cantonensis in Egypt. 1. Natural and experimental infection of the snail intermediate host Lanistes carinatus. Journal of the Egyptian Society for Parasitology, 10:399–412. Zahra, A. 1952. Paragonimiasis in the southern Cameroons: a preliminary report. West African Medical Journal, 1:75–82.

Chapter 7. The biology of Bulinus

There is sufficient information to devote a chapter to Bulinus, rather than Biomphalaria, partly because its species are more diverse. Another reason for Bulinus having received more attention is the great variation among its species in compatibility with schistosomes. Observations on living Bulinus appear in many other parts of this book (especially in relation to parasites and abiotic ecological factors). This chapter concentrates on three aspects: the taxonomic history and development of biological concepts of the species, the attributes that contribute to their success and, more speculatively since the facts are unfortunately meagre, evolution within the genus. Taxonomic history and taxonomic characters Advances in morphological, cytological and biochemical studies made untenable some of the earlier definitions of species of Bulinus, but an entirely satisfactory classification is not yet within reach. Some species can be defined clearly, for example by differences in chromosome number and molecular characters, but problems remain in the characterisation and identification of many taxa. This reflects the difficulty of applying a simple species-concept to a hermaphrodite organism such as Bulinus, capable of self-fertilisation as well as outcrossing and living in discrete patches of habitat, where isolation favours genetic differentiation among populations. Taxonomic history The recorded history of Bulinus is as long as the written story of freshwater molluscs in Africa. Michel Adanson (1757) gave the name ‘Le Bulin’ (French bulle=a bubble) to small snails he collected in Senegal, because they contained a bubble of air and floated at the water surface. Le Bulin became the type species of the genus as Bulinus senegalensis, named by Müller in 1781, although during the nineteenth century many newly described species of Bulinus were placed in the genus Physa, which has a similar shell but very different anatomy. A dramatic increase in the number of published descriptions of species now placed in Bulinus (many of them originally in Physa) took place towards the end

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of the nineteenth century (Wright, 1971a, Fig. 13). By 1915 when the life cycle of Schistosoma haematobium became known, over one hundred species had been described, almost all known from only the shell. Present-day malacologists are still occupied with the task of defining the comparatively small number of biological species represented by the many available names. A major advance occurred in 1957 with the publication of a monograph by Georg Mandahl-Barth, in which shell variation was more fully taken into account, and the soft parts and radula were extensively used in taxonomy for the first time. This classification recognised 27 species and subspecies; some of these taxa have since been placed in synonymy and some species then treated as synonyms are now regarded as distinct. A few additional species have been described and the total now recognised is 36 (Table 7.1). The species of Bulinus may be divided into four groups (Table 7.1), which have their origins in the four species groups of Mandahl-Barth (1957), but differ in the separation of a B. reticulatus group (Wright, 1971b) and the fusion of Mandahl-Barth’s groups for B. truncatus and B. tropicus into a single B. truncatus/ tropicus complex (Brown, 1976, 1980, 1981). Biocca et al. (1979) proposed that their biochemical data in combination with morphological differences justified a division of Bulinus into three genera, and that this name should be restricted to the B. forskalii group. This classification has not been generally accepted and it has serious disadvantages (Brown, 1981). These proposed groups lack clear diagnostic characters and there is a need to study more species in adequate detail. To continue using a system of species groups offers the advantage that species may be easily rearranged, with minimal formal taxonomic procedure, according to advances in knowledge. Another consideration is the confusion that would be caused by using three or more generic names for the different species of snail serving as intermediate hosts for Schistosoma haematobium. Sources of taxonomic characters Differences among taxa have been sought by analysis of morphological variation, determination of chromosome number and comparisons of molecular properties by means of chromatography, immunodiffusion, electrophoresis, isoelectric focusing and most recently DNA probes. Morphology Although it may be difficult to identify a species of Bulinus from its shell, there is still need for precise conchological descriptions in modern taxonomic study, for at least the reason that the original descriptions of so many species are restricted to shell characters. Those used so far, of size, shape, ornamentation, degree of umbilication and form of the columellar margin, are continuous variables and subtle differences are not easy to describe verbally. Individual

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variation may be great, while size is commonly related allometrically to other variables. It is unfortunately difficult to standardise shell variables because in Bulinus growth is not determinate, that is the shell lacks a recognisable mature form and grows throughout the life of the snail. Such a shell is not a good subject for morphometric investigation; a priority is to increase the number of adequately standardised variables. Quantitative analysis of shell variation began with the use of simple ratios between dimensions (e.g., Wright, 1957). Brown et al. (1971a) introduced a system of scoring for the variation in the umbilicus, costulation and columella (Fig. 129). Multivariate analyses have been carried out by the methods of principal components (Shaw & Brown, 1986; Brown et al., 1986, 1991; Kristensen & Christensen, 1989) and stepwise discriminant functions (Kristensen, 1986; Kristensen et al., 1987; Kristensen & Christensen, 1989). In the radula, variation in the size of the first lateral tooth and the shape of its mesocone (Fig. 105) was utilised as a source of taxonomic characters by Table 7.1. The species of Bulinus arranged within groups in alphabetical order. B. forskalii group (=Bulinus sensu stricto) B. barthi Jelnes, 1979 B. bavayi (Dautzenberg, 1894) B. browni Jelnes, 1979 B. beccarii (Paladilhe, 1872) B. camerunensis Mandahl-Barth, 1957 B. canescens (Morelet, 1868) B. cernicus (Morelet, 1867) B. crystallinus (Morelet, 1868) B. forskalii (Ehrenberg, 1831) B. scalaris (Dunker, 1845) B. senegalensis Müller, 1781 B. africanus group (=Physopsis) B. abyssinicus (Martens, 1866) B. africanus (Krauss, 1848) B. globosus (Morelet, 1866) B. hightoni Brown & Wright, 1978 B. jousseaumei (Dautzenberg, 1890) B. nasutus (Martens, 1879) B. obtusispira (Smith, 1882) B. obtusus Mandahl-Barth, 1973 B. ugandae Mandahl-Barth, 1954

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B. umbilicatus Mandahl-Barth, 1973 B. truncatus/tropicus complex (=Isidora) B. angolensis (Morelet, 1866) B. depressus Haas, 1936 B. hexaploidus Burch, 1972 B. liratus (Tristram, 1863) B. natalensis (Küster, 1841) B. nyassanus (Smith, 1877) B. octoploidus Burch, 1972 B. permembranaceus (Preston, 1912) B. succinoides (Smith, 1877) B. transversalis (Martens, 1897) B. trigonus (Martens, 1892) B. tropicus (Krauss, 1848) B. truncatus (Audouin, 1827) B. yemenensis Paggi et al., 1978 (if different from B. truncatus) B. reticulatus group B. reticulatus Mandahl-Barth, 1954 B. wrighti Mandahl-Barth, 1965

Mandahl-Barth (1957, 1965). But analyses of such characters are complicated by increase in tooth size with snail size, while mesocone shape varies both individually and according to snail size (Schutte, 1965; Oberholzer et al., 1970). The quality of the image of the mesocone given by the optical microscope is sometimes unsatisfactory. Scanning electron microscopy (Brown, 1982) showed that some previously described mesocone shapes were artifacts, though the distinction between the angular and non-angular types was confirmed. Other morphological features used in taxonomy so far are: pigmentation (mantle patterns are heritable; Larambergue, 1939, and Rudolph & Bailey, 1983, while albinism occurs in certain populations); presence of a renal ridge within the mantle cavity (characteristic of some species of the B. africanus group); proportions of the component parts of the copulatory organ (characteristic of certain species); occurrence of aphally (absence of the copulatory organ in a proportion of individuals in some species); and size of egg (comparatively large in B. octoploidus).

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Fig. 129. Bulinus natalensis/tropicus complex. Shells from Natal province, South Africa, representing (a,b) B. tropicus, (c–e) B. natalensis and (f) B. zuluensis (regarded as a form of B. natalensis). Their columellar margins are examples of 4 character states: 1, concave (a,b); 2, straight (c,d); 3, twisted (e), and twisted and reflected (f). Scale line: 5 mm. From Brown et al. (1971a, Fig. 3).

Sperm morphology deserves investigation as possibly being characteristic of a species (Brackenbury & Appleton, 1991). No characters of taxonomic value have yet been found in other parts of the reproductive system or in the digestive, circulatory and nervous systems. Chromosomes Since 1960, when Burch reported that B. truncatus was tetraploid (2n=72) in contrast to planorbid snails in general (2n=18), the chromosome number has been determined for over 600 population samples of Bulinus representing most of the species (reviewed by Jelnes, 1985). Polyploidy has been found only within the B. truncatus/tropicus complex, in which occur the chromosome numbers 2n=36, 72, 108 and 144. A few supernumerary chromosomes have been seen in some individuals of the diploids B. natalensis and B. forskalii. It must be added that the generally-used squash preparations of ovotestis or whole embryos rarely provide entirely well-spread chromosomes, so that precise counting is usually difficult and especially so for polyploid sets. Early karyotype studies (Claugher,

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1971) need to be extended; banding techniques have so far been applied to only a few populations (Goldman et al., 1980, 1984). Three species were discovered through the determination of chromosome number: B. hexaploidus (2n=108) and B. octoploidus (2n=144) of Ethiopia (Brown & Burch, 1967; Burch, 1972) and B. permembranaceus (2n=72) of Kenya (Brown, 1976). Despite careful study, however, no clear-cut morphological characters have been found to define any of these species. Chromosome number is a valuable diagnostic character also in establishing the distribution of B. truncatus, in areas where this tetraploid overlaps in distribution the morphologically similar diploids B. natalensis and B. tropicus. Body surface mucus After separation by paper chromatography, the body surface mucus of Bulinus may show brilliant bands of fluorescence in ultraviolet light. Although no fluorescence has been obtained from the B. africanus group and only a single band in the B. forskalii group, an array of 3 to 5 bands per individual are seen in the B. truncatus/tropicus complex (illustrated in colour by Wright, 1974). Repeated testing indicated that the pattern of bands remains constant for an individual throughout life. Some populations are apparently homogeneous, while others give two or more different patterns in varying proportions. Particularly conspicuous is the presence of a brilliant outer band which appears when the chromatogram of some individuals is exposed to ammonia fumes. This band was observed for certain diploid populations in Madagascar and Transvaal (Wright, 1971b), Ethiopia (Brown & Wright, 1972) and Kenya (Brown et al., 1991). These fluorescent substances deserve further investigation for their potential in taxonomy and as genetic markers in breeding experiments. Proteins of muscle and eggs Early immunodiffusion experiments using foot muscle proteins showed differences between diploid and tetraploid species (Burch & Lindsay, 1970, 1971). More data were obtained for egg proteins from some species of all the groups (Wright, 1971b; Brown & Wright, 1978). Yet variation in quality of antisera was a technical problem (Wright, 1974) and immunological analysis has not played a recent part in the taxonomic study of Bulinus. Isoelectric focusing of proteins from whole egg capsules showed differences among species (Saladin et al., 1976), but the greatest taxonomic value has emerged from electrophoretic separation of ‘egg proteins’, obtained by extracting the perivitelline fluid bathing the embryos. The method was developed by C.A. Wright and colleagues, and information is available for about 200 population samples (major papers are: Wright & Ross, 1965, 1966; Brown et al., 1971b, 1986, 1991; Brown & Wright, 1972; Brown, 1976; Brown & Shaw, 1989). Technical modifications and further comparisons among species were described

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Fig. 130. Egg proteins (in the perivitelline fluid) of Kenyan Bulinus, stained with nigrosin after electrophoresis on cellulose acetate strips. Each pattern is for an individual snail (a) B. permembranaceus (tetraploid) from Kipkabus; (b,d) B. tropicus (=alluaudi) (diploid) from Ol Kalau and from Nairobi; (c) B. truncatus (tetraploid) from the Kano Plain. Rabbit serum was run as a control; globulin fraction (x), albumin fraction (y). From Brown (1976, Fig. 5).

in a series of papers published from 1976 to 1981 by Hamilton-Atwell & Van Eeden (1981a,b, and references therein). The perivitelline proteins differ to a varying degree among species and the most important taxonomic application has been to distinguish B. truncatus from other members of the B. truncatus/tropicus complex (Fig. 130). Enzyme analyses Since early experiments with Bulinus tissues (Wright et al., 1966), particularly foot muscle (Burch & Lindsay, 1967; Wu, 1972) and digestive gland (Wright & File, 1968; Wright, 1971b), extensive enzyme data with taxonomic relevance have been obtained by starch gel electrophoresis and isoelectric focusing (major

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papers include Nascetti & Bullini, 1980; Rollinson & Wright, 1984; Jelnes, 1986; Mimpfoundi & Greer, 1989, 1990a–d; Rollinson et al., 1990: reviews by Wright, 1974, and Jelnes, 1985, 1987). Technical progress led to the analysis of many enzymes for an individual snail (Jelnes, 1979c) and improvements in the standardisation of results (Jelnes, 1985). Enzyme analyses made major taxonomic contributions in the discrimination between B. liratus and B. obtusispira (Wright, 1971b; Jelnes, 1984), characterisation of B. permembranaceus (Jelnes, 1977; Brown & Shaw, 1989), separation of species in the B. africanus group (Jelnes, 1979a), and improvement of understanding of geographical variation in B. truncatus (Jelnes, 1979b, 1986; Wurzinger, 1979; Wurzinger & Saliba, 1979). Enzyme data provided reasons, though perhaps not entirely adequate, for naming three new species: B. yemenensis Paggi et al. (1978), B. barthi Jelnes (1979c) and B. browni Jelnes (1979c). The application of enzyme analyses to taxonomy, however, is not entirely straightforward. Discrepancies have arisen between different identifications based on enzymes and morphometric data (Jelnes, 1991; Kristensen & Christensen, 1991), and because of geographical variation, an enzyme that serves to discriminate a species in one part of its range may not do so in another area. Study of enzymic variation of B. truncatus in the Mediterranean region led to the conclusion that there is a need for new infra-specific taxonomic units, conceived as enzymically-defined populations or ‘biotypes’ rather than the traditional category of subspecies (Nascetti & Bullini, 1980; Bullini, 1982). DNA Analysis of DNA from Bulinus has potential for the characterisation and identification of species; a ribosomal RNA probe was used for restriction enzyme analysis by Rollinson & Kane (1991) and DNA probes were developed by Strahan et al. (1991). A further technical advance is the use of random amplified polymorphic DNA markers (RAPDs) (Langand et al., 1993). Development of species concepts within the groups The B. africanus group Typical members of this group (which is equivalent to Physopsis Krauss 1848, used by some authors as genus or subgenus) are distinguished by the presence of nodular shell sculpture, a ridge or twist in the columellar margin of the aperture and a ridge on the kidney (first described by H.Watson in Connolly, 1925; no function is known). Not all these characters are consistently present in every species, and biochemical evidence has played a part in the decisions to place some species in this group (hightoni, obtusispira and umbilicatus). Some of the species

FRESHWATER SNAILS OF AFRICA 385

are important intermediate hosts for S. haematobium and other schistosomes. The group is confined to tropical Africa and Madagascar (where B. obtusispira alone occurs). The chromosome number is entirely diploid (2n= 36). We will follow the development, doubtless still incomplete, of concepts of the widespread species B. globosus, and the two more localised species B. umbilicatus ad B. obtusispira, which both were once classified in the B. truncatus/tropicus complex. Bulinus globosus This is the most widespread and probably the most important intermediate host for S. haematobium in tropical Africa. It was named by Morelet (1866) from shells collected by F.Welwitsch in Angola; eighteen years earlier similar shells collected near Durban had been described as B. africanus by Krauss (1848). For nearly a century these species were distinguished only by poorly defined characters of the shell (such as aperture shape, degree of columellar truncation and size of umbilical opening), until Mandahl-Barth (1954, 1957) described a more reliable difference in the copulatory organ, which in B. globosus has the penis sheath small in proportion to the preputium. Identified from the copulatory organ, B. globosus occurs practically throughout the tropical region, whereas B. africanus is found mostly in eastern Africa. In south-eastern Africa, where distribution has been studied in detail, B. globosus is less common than B. africanus in the cooler climatic areas (Brown, 1966). Experiments confirmed that B. africanus was better adapted to low temperature than B. globosus and less tolerant of warmth (Joubert et al., 1984, 1986). Further differences were found for enzymes (Jelnes, 1979a; Rollinson & Southgate, 1979) and egg proteins (Hamilton-Atwell & Van Eeden, 1981a). Yet the intermediate appearance of the copulatory organ in some populations suggests inter-specific hybridisation (Mandahl-Barth, 1968) and it would be interesting to look for further evidence of genetic differences between these two species, if so they be. In West Africa it may be difficult to decide whether a snail should be identified as B. globosus or B. jousseaumei (Dautzenberg, 1890), which has a comparatively small shell with weaker microsculpture and slighter columellar twisting (Mandahl-Barth, 1957). From observations on size variation from Angola to Gambia, Wright (1957) concluded that B. jousseaumei was merely a small form of B. globosus at the northern limit of its range. This hypothesis was dismissed by Mandahl-Barth (1965) who examined more material and found typical large specimens of B. globosus throughout the geographical range. Controversy continues, with jousseaumei reduced to a synonym of globosus according to enzyme analyses (Jelnes, 1986, 1991), but maintained as a distinct species by shell morphometry (Kristensen & Christensen, 1989, 1991). A further difficulty in West Africa is to separate clearly B. globosus from B. umbilicatus Mandahl-Barth, 1973; enzyme analyses and shell morphometry produced

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different identifications for some populations (Jelnes, 1986, 1991; Kristensen & Christensen, 1989, 1991). Two forms of B. globosus differing in the shell, pigmentation, copulatory organ and susceptibility to infection by S. haematobium, were collected from different localities in northern Nigeria (Fryer et al., 1987). Breeding experiments using enzyme markers showed that cross-fertilisation occurred; it was concluded that though conspecific these snail populations had diverged as a result of geographical isolation. In eastern Africa the range of B. globosus extends northwards into Kenya, Uganda and Sudan. Here as in West Africa there are taxonomic problems, though different. The subspecies B. g. ugandae was founded by Mandahl-Barth (1954) on small darkly-pigmented snails with weaker microsculpture than is usual in B. globosus. The new form was raised to full species-status because it was found with typical globosus in some areas, and proved resistant to infection with S. haematobium (Mandahl-Barth, 1957, 1965). The type locality for B. ugandae is Jinja Bay, Lake Victoria, and it is especially associated with papyrus swamps. Continuous variation in the shell, however, connects the typical forms of ugandae and globosus, and they have yet to be satisfactorily characterised, despite the application of shell morphometry (Kristensen et al., 1987; Archer, 1988) and enzyme analysis (Jelnes, 1979a; Wright & Rollinson, 1979; Archer, 1988). Difficulty has been experienced in deciding for snails from the coastal region of East Africa whether they should be identified as B. globosus or B. nasutus. Although the shell of B. globosus is generally broader and less extensively covered with microsculpture, the two species seemed to Mandahl-Barth (1957) to merge in north eastern Tanzania. Yet differences between them in the same area were observed in the copulatory organ (Pringle et al., 1971) and enzymes (Rollinson & Southgate, 1979). It may be hoped that the application of molecular analysis to more populations will enable the distributions of these species and also B. africanus to be determined with more confidence. Further progress in understanding B. globosus as a biological species and in defining it as a taxon will depend on malacologists describing morphological and molecular characters, population by population, in critical geographical areas. Meanwhile it will encourage future study if snails are identified as precisely as possible in the light of current taxonomic knowledge. It is regrettable that Joubert et al. (1990, 1991) used the name B. africanus indiscriminately for snails that probably were B. globosus. In this experimental comparison among snail populations of compatibility with S. haematobium, a detailed characterisation of the different snail populations would have been relevant. Most of the snails used in these experiments originated from the lowveld of eastern Transvaal, where only B. globosus occurs according to identifications from the copulatory organ.

FRESHWATER SNAILS OF AFRICA 387

B. umbilicatus and B. obtusispira The first words published about B. umbilicatus refer to an unusually large form of B. truncatus collected at Abu Duloh near Gebelain in the Sudan with an ‘extraordinary expansion of the columellar margin’ (Connolly, 1941). Specimens found later near Zalingei in the Darfur region of Sudan by J.M.Watson in 1965– 66 were submitted to C.A.Wright and G.Mandahl-Barth, who both believed this to be an undescribed species of the B. africanus group. When he described B. umbilicatus, Mandahl-Barth (1973) concluded that it was intermediate between the groups of africanus and truncatus, since the microsculpture is fine, the columellar ridge weak if present at all, and not all specimens have a renal ridge. Evidence of a closer relationship to the africanus group was seen in egg proteins (Wright, 1977; Brown & Wright, 1978) and enzymes (Wright & Rollinson, 1979). Enzyme polymorphism was reported by Jelnes (1986) who found a difference between specimens from Sudan and West Africa. Although Jelnes (1985) classified B. umbilicatus in the B. reticulatus group according to the shell, the sum of morphological and molecular characters seem to favour classification in the africanus group. Further investigation is needed in West Africa, where although some populations are readily identifiable as B. umbilicatus, the identification of others is controversial, especially in Senegambia (Jelnes, 1991; Kristensen & Christensen, 1991). Natural transmission of schistosomes by B. umbilicatus has been demonstrated in Senegal, for S. haematobium and S. curassoni. B. obtusispira of Madagascar was at one time treated as a synonym of B. liratus, which possibly is not a species different from B. tropicus of the African mainland. But the discovery of snails naturally infected with S. haematobium aroused interest in the possibility of B. obtusispira being a distinct species with a wide distribution in the western part of the island (Brygoo & Moreau, 1966). Its species-status was confirmed by morphological and molecular studies (Wright, 1971b; Saladin et al., 1976; Brown & Wright, 1978; Jelnes, 1984). S. haematobium is transmitted on Madagascar mainly and probably entirely by B. obtusispira; some features used to distinguish the intermediate host from B. liratus in the field are its paler colour, more globular and blunter-spired shell, and the pointed end of the foot (Degrémont, 1973; Moyroud et al., 1983). The earlier confusion of B. obtusispira with B. liratus is understandable as the shell shows almost no characteristic of the B. africanus group. Although placed by Jelnes (1985) in the B. reticulatus group, defined primarily by an open umbilicus, B. obtusispira is not more than narrowly perforate (rimate). On close examination some specimens show a finely rippled microsculpture reminiscent of the B. africanus group, but there is no columellar ridge and nor is there a ridge on the kidney. Analyses of egg proteins provided the main evidence of affinity with the africanus group (Wright, 1971b; Brown & Wright, 1978). The phylogenetic relationships of B. obtusispira deserve further study and this snail may represent a primitive stock of the genus isolated on Madagascar.

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The B. truncatus/tropicus complex Perhaps the only positive character of this group is that it is the only one in which polyploidy is known. Otherwise the group is defined negatively, for example the shell lacks the microsculpture typical of the B. africanus group, is not so slender as in the B. forskalii group and lacks the broad columellar reflection and large umbilicus of the B. reticulatus group. The oldest name available as subgenus is Isidora Ehrenberg 1831. Chromosome numbers form a polyploid series (2n=36, 72, 108, 144). According to the original definitions (Mandahl-Barth, 1957), species in the B. truncatus group had the angular (arrowhead-shaped) type of radular mesocone, were frequently aphallic and included intermediate hosts for S. haematobium. In the B. tropicus group the mesocone was non-angular (triangular) and there was no intermediate host. The discovery that B. truncatus is tetraploid (2n=72) whereas B. tropicus is diploid (2n=36) led to the concept of a polyploid and potentially susceptible B. truncatus group found mainly in northern Africa and a diploid resistant B. tropicus group confined to eastern and southern Africa. This distinction was progressively weakened by descriptions of continuous variation in mesocone shape, the finding that some diploid populations (B. natalensis, B. depresses) have angular mesocones and aphallic individuals, and the successful experimental infection of snails from some diploid populations with S. haematobium. We will trace developments in the understanding of species in three areas of study, diploid snails in southern Africa, diploid and polyploid populations in Ethiopia and Kenya, and the tetraploid forms of tropical Africa. B. natalensis and B. tropicus in southern Africa B. natalensis (Küster, 1841) was collected by F.Krauss from streams in the Umgeni valley near Durban and is the first Bulinus to be described from southern Africa. In 1848 Krauss named B. tropicus from shells obtained by Wahlberg in the Transvaal, and this name became more frequently used because the species seemed easily recognisable and widely distributed. Despite its seniority B. natalensis remained in obscurity. Connolly (1939) regarded it as a distinct species ‘recognisable by the thin columella with distinct twist on its inner margin’, but Mandahl-Barth (1957) placed it in the synonymy of B. tropicus. In the late 1950s J.A.Van Eeden discovered that snails from northern Transvaal did not conform to B. tropicus in the soft parts but resembled B. truncatus of northern Africa in being aphallic and having an angular radular mesocone; these snails were identified as B. depressus (Haas) and found to be diploid (Schutte, 1966; Hamilton-Atwell & Van Eeden, 1969). Interest was increased by the report (Pitchford, 1965) that South African snails resembling B. truncatus were susceptible to infection by S. haematobium. As Burch (1963, 1964) had reported that B. tropicus was diploid in contrast to the tetraploidy of

FRESHWATER SNAILS OF AFRICA 389

B. truncatus in northern Africa, the further investigation of chromosome number was fundamental to the study of the South African ‘truncatus’. In the first of two investigations all snails examined from 87 localities in South Africa and Mozambique were diploid (with occasional supernumerary chromosomes; Brown et al., 1967). But only some populations had the nonangular (triangular) mesocone shape characteristic of B. tropicus. In other populations the mesocone was angular (arrowhead-shaped) as in B. truncatus and some individuals were aphallic. It thus appeared, in conjunction with observations by Van Eeden and colleagues in Transvaal, that diploid snails customarily identified as B. tropicus comprised at least two morphologically different forms. The ‘truncatus-like’ snails found in Natal had generally low-spired shells conforming to the original description of B. natalensis. Such populations were found in the comparatively warm climatic area along the coast, whereas B. tropicus occurred further inland. However because of variation in the shell (Fig. 129) and mesocone shape, some population samples were classified in an ‘intermediate’ category. A second investigation (Brown et al., 1971a,b) concentrated on Natal Province, because of the presence there of the type locality of B. natalensis and the ‘tropical corridor’. This term refers to the coastal plains of southern Mozambique and Natal in which there is a transition between the biota of the tropical region, defined by the 18°C July isotherm (Fig. 131), and the southern temperate region. Wide variation in climate over a small geographical area (associated with increase in both latitude and altitude) provided an attractive situation for testing the hypothesis that B. natalensis was associated with warm climate. Snails were collected in such contrasting environments as the foothills of the Drakensberg where snow can fall, and tropical lakes near the Indian Ocean. Morphometric analyses of nearly 6000 shells and 1500 radulae (Brown et al., 1971a,b; Oberholzer et al., 1970) from 86 localities in South Africa and Mozambique showed geographical variation most clearly for relative height of the spire, mesocone shape and frequency of aphallic individuals. Population samples with a low spire (Figs 129e–f) were mostly from north-eastern Natal; their ratios for shell length divided by aperture length (L/AL) were less than 1.20. Shells from Lake Sibayi and nearby lakes had the particularly low spire and strongly-reflected columellar margin characteristic of B. zuluensis (Melvill & Ponsonby, 1903) (Fig. 129f) described from ‘east Zululand’, but it was impossible to separate this form clearly from B. natalensis. That low-spired populations may occur in small waterbodies as well as lakes is discussed below. Populations with a high spire (L/AL exceeding 1.50; Figs 129a,b) were found mostly in southern and western Natal. The significance of the geographical distribution of spire height is enhanced when mesocone shape is considered as well. All populations with the angular shape predominant (at least 50% of the mesocones examined) occurred near the coast (Fig. 131), while almost all the

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populations sampled in western Natal and Orange Free State had mainly nonangular mesocones. Further, aphallic individuals were obtained almost exclusively near the coast. The data for samples from Natal were re-examined by principal components analysis (Shaw & Brown, 1986). Characters contributing most to separation between samples were mesocone shape and tooth size, followed by height of spire. The existence was confirmed of two morphs with different geographical distributions, though connected by apparently continuous variation. A substantial body of evidence thus indicates a significant biological difference between the taxa B. natalensis and B. tropicus, even though there may not be complete reproductive isolation between them. Although observations of compatibility between S. haematobium and B. natalensis are few and all experimental (Chapter 4: B. natalensis), they are of great interest as there is no convincing evidence of compatibility with B. tropicus. Yet these snail taxa are not easily differentiated and it has been most practicable in some studies to use the taxon B. natalensis/tropicus complex. No clearly specific character was found in analyses of 5 enzymes (Wright & Rollinson, 1981). An indication of partial reproductive isolation between the two putative species was obtained by Wu (1972) who observed successful interbreeding when B. natalensis from Lake Sibayi acted as male but not when female. Karyotype differences reported (Goldman et al., 1980, 1984) were based on snails from eastern Transvaal identified as B. natalensis, although no morphological information was given. B. depressus from northern Transvaal (Hamilton-Atwell & Van Eeden, 1969) has a higher frequency of aphally than B. natalensis in Natal, but further evidence is needed to show that they are different species. A reported difference in egg proteins (Hamilton-Atwell, 1976) was based on a laboratory-bred stock identified as B. natalensis, originating in the Eastern Transvaal (‘a local Nelspruit snail of the B. truncatus group’; Pitchford, 1965, and Schutte, 1966); this did not necessarily represent natalensis as known in Natal. B. natalensis has been recorded from a large area of southern and eastern Africa, with a recent tentative identification for Cameroon (Mimpfoundi & Greer, 1990c). Over such a large range it is likely that local groups of populations evolve largely independently. The characters of B. natalensis in Natal possibly are associated with local conditions in the warm coastal plain and particularly the lakes. Natural selection conceivably could maintain a distinct gene-pool even in the absence of reproductive isolation from the B. tropicus populations of the cooler areas. Although the low spire of B. natalensis can hardly be an adaptation to warm conditions, the lakes could have favoured the low-spired form, which seems well suited to avoiding dislodgement from plant stems by wave-action. During dry climatic phases a large lake such as Sibayi might have provided a refuge for aquatic life, from which low-spired snails could have colonised smaller waterbodies nearby when moister conditions returned. In general a large and comparatively stable lake is likely to be a source of colonising organisms for the smaller and shorter-lived waterbodies in the area.

FRESHWATER SNAILS OF AFRICA 391

Fig. 131. Distribution in SE Africa of populations belonging to the B. natalensis/tropicus complex, classified according to the dominant (≥50%) shape of mesocone on the first lateral tooth of the radula. Populations with the mesocone predominantly angular are associated with the warmer coastal region. The eastern side of the Drakensberg escarpment is indicated by the 1500 m contour. The 18°C July (coldest month) isotherm represents the southern limit of the tropical climatic region. Type localities for 5 nominal species are indicated. From Brown et al. (1971b, Fig. 2).

392 THE BIOLOGY OF BULINUS

Thus in other parts of Africa too, the presence of low-spired populations of the B. natalensis/tropicus complex in a small waterbody could be the result of selection pressures within a lake some distance away. Finally there is the possibility that interbreeding between B. natalensis and B. tropicus has been favoured by breakdown of ecological barriers through human activities. In the lower Umgeni valley, where there is much variation in the shell, coastal forest has been cleared almost entirely and marshes extensively drained. Some of the observed shell variation perhaps arises in response to man-made habitats. The higher-spired populations in this area lived in a borrow-pit and a farm dam, and in Mozambique in a cement-lined channel (Brown et al., 1971a, localities 5,36,77). The B. truncatus/tropicus complex in Ethiopia These snails received close attention because of uncertainty about the part they might play in transmission of S. haematobium in Ethiopia. Despite careful morphological study, problems of species identification were not resolved until variation in chromosome number was discovered. At first all specimens were identified as B. sericinus (Jickeli) (Mandahl-Barth, 1957) or B. truncatus sericinus (Wright & Brown, 1962; Brown, 1965; Mandahl-Barth, 1965). Morphological variation was obviously high and when 4 different cytological forms were found (Brown & Burch, 1967; Burch, 1967) a further investigation was undertaken to seek correlations between chromosome number and other characters. This study (Brown & Wright, 1972) was based on 4 months of fieldwork, chromosome radulae. These observations are the basis of the following account unless another counts for 69 populations and morphometric data for 1800 shells and 400 source is cited. Table 7.2. Morphological features compared between diploid and polyploid forms of Bulinus living in Ethiopia and belonging to the B. truncatus/tropicus complex (from Brown & Wright, 1972).

Shell Maximum size Spire

Columella

Umbilicus

Diploid

Tetraploid

Hexaploid

Octoploid

Small to moderate Highly variable (depressed to exserted) Usually concave or straight Usually open or semi-open

Small

Moderate to large Moderately high

Generally large

Usually concave or straight Usually open or semi-open

Usually concave or straight Usually open or semi-open

Moderately depressed with shouldered whorl Commonly twisted Commonly rimate or closed

High

FRESHWATER SNAILS OF AFRICA 393

Radula Predominant mesocone shape

Copulatory organ Size of egg

Diploid

Tetraploid

Hexaploid

Octoploid

Highly variable (non-angular, angular or intermediate) Aphallic snails in some populations Small

Angular or intermediate

Angular or intermediate

Angular or intermediate

Aphallic snails in all samples examined Small

No aphallic snails found

No aphallic snail found

Not determined

Large

Variation in shell sculpture and size of the first lateral radular tooth showed no relations with chromosome number, but there were some correlations for other morphological characters (Table 7.2). Characterisation and identification were clearest for the tetraploid populations. Their shells were comparatively small and low-spired, with shouldered whorls, the columella commonly twisted and the umbilicus closed. Some aphallic individuals were obtained in all localities. These snails were identified as B. truncatus according to their morphology and egg proteins; the same identification was reached in investigations of tetraploid populations in other Ethiopian localities (Wu & Burch, 1975; Wurzinger, 1979). The identification of B. truncatus in Ethiopia settled the status of the two nominal species B. sericinus and B. schackoi, which are important taxonomically as senior species-names for members of the B. truncatus/tropicus complex in northeast Africa. They have the same type locality, ‘the Toquor’ (presumably a stream or river) near Mekerka in the ‘Abyssinian province of Hamasen’ at 1830 m (6000 feet; Jickeli, 1874). Given this altitude, Amberson & Schwarz (1953) were mistaken to place this locality as Tokar on the Red Sea plains. According to Malek (1958, p. 725) Hamasen province is shown in 19th century maps to be on the plateau in the region of Asmara. The type locality could be a rocky stream near the village Mekerka situated about 16 km (10 miles) north-west of Asmara near the Cheren road (Brown, 1965; Burch, 1967). Only tetraploidy was observed in Bulinus collected here (Burch, 1967, 1969); from the morphology and molecular properties of the snails it appears that B. sericinus and B. schackoi are conspecific and synonyms of B. truncatus (Brown, 1965; Wu & Burch, 1975; Wurzinger, 1979). Consequently neither of Jickeli’s names could be used for a newly discovered polyploid species. The better-known of the two higher polyploids is the octoploid, which has been collected more frequently than the hexaploid. Octoploid snails tend to grow large, be high-spired and lay large eggs (Fig. 132). Hexaploids have a similar shell though a somewhat lower spire. No aphallic individual was found in either hexaploid or octoploid populations and their mesocone shape is similarly more or less angular. No clearly-differentiating character emerged from a detailed morphological study of one hexaploid and one octoploid population (Wu, 1972).

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Fig. 132. Size of eggs laid in the laboratory by field-collected Bulinus from Ethiopian populations having different numbers of chromosomes. Each symbol represents a single population; measurements were taken of at least 20 eggs in 4 or 5 randomly chosen capsules. The broken line shows the overall upper range in size of single eggs. From Brown & Wright (1972, Fig. 11a).

Egg proteins and esterases were heterogeneous among octoploid populations and no character to differentiate the whole group could be found (Brown & Wright, 1972). Although difficult to characterise in conventional taxonomic terms, the two higher polyploids can be regarded as reproductively isolated species and they were named B. hexaploidus and B. octoploidus by Burch (1972). Reproductive barriers between polyploid and diploid snails were tested by pairing albino B. tropicus with pigmented polyploid individuals (Wu, 1972). No albino partner appeared to have been cross-fertilised, but some tetraploid, hexaploid and octoploid partners apparently were fertilised by the diploid, according to analyses of foot muscle esterase from their F1 progeny, which were infertile. No information was given about chromosome number in the supposed hybrid progeny. Ethiopian diploid Bulinus populations are highly diverse. Wide variation in spire height produced a bimodal distribution of samples. Variation among populations is comparable to that described for the B. natalensis/tropicus complex in southern Africa. Identified according to the angular mesocone shape, B. natalensis occurs in lakes Ashangi, Awasa and Zwai, and B. tropicus in some pools and streams, mostly in the highlands. However, many Ethiopian populations do not fit readily into either taxon; their mesocones are mostly of intermediate shape. Unlike eastern South Africa, the distribution in Ethiopia of B. natalensis is not noticeably related to climate, for Lake Ashangi (92% angular

FRESHWATER SNAILS OF AFRICA 395

mesocone) is in the cool highland, whereas lakes Awasa and Zwai are in the warm Rift Valley. Breeding between B. natalensis from Lake Zwai and B. tropicus was demonstrated using albinism as a marker (Brown & Wright, 1972). Thus in Ethiopia, as in southern Africa, although some populations are strikingly different, the taxonomic boundaries between B. natalensis and B. tropicus are not clear. The ecology of diploid populations and B. truncatus in Ethiopia is varied. Diploids are widespread, living in diverse habitats including lakes and rainpools, most commonly below 2100 m altitude, though isolated diploid populations are known above 2400 m (north-east of Addis Ababa and in Lake Ashangi; Brown & Wright, 1972). B. truncatus is also most frequent at low altitude, being present in lakes Abaya (Margherita), Awasa and Zwai, as well as irrigation systems in the middle Awash valley, but it has also been found rarely on the plateau, near Lake Tana (1830 m) and in streams near Addis Ababa and Dessie. Both higher polyploids are clearly associated with high altitude. Their lowest known localities lie at about 2100 m in tributaries of the Awash River west of Addis Ababa, and in the Guder River near Ambo; the highest at about 2865 m between Shano and Debra Berhan. The snails live in streams flowing through the undulating grasslands of the plateau, reduced to residual pools in the dry season and with dense growths of waterplants, especially Potamogeton spp. The climate here is temperate, though winter is less cool than on the South Africa highveld. The comparative rarity of the hexaploid, reported from about 5 localities in all, suggests that its survival is precarious. Zonation in relation to altitude does not entirely segregate the higher polyploids from diploid and tetraploid populations. However, no more than one chromosome number was observed in any sample of snails from a particular locality on the plateau, which is surprising since the different chromosome numbers do not appear to be associated with different habitats. Perhaps cytological examination of larger population samples would reveal mixtures, but it seems that usually a single chromosome number is dominant in a particular locality. Both diploid and tetraploid snails occur in lakes Awasa and Zwai, but in different biotopes, B. natalensis on the open shores and B. truncatus in marshes (Brown & Burch, 1967). These observations led to a much improved understanding of the potential for transmission of urinary schistosomiasis in Ethiopia. Happily, the indications for the highlands are reassuring. It was puzzling in earlier years that despite the abundance of snails known as ‘B. truncatus sericinus’, endemic S. haematobium was not found in the highlands. Various authors suggested explanations, referring particularly to the coolness of the climate and the low human population density. Now it is known that the snails once identified as B. truncatus and regarded as susceptible to infection, comprise at least 4 different cytological forms, of which only the tetraploid is this species. These is still no evidence that S. haematobium is transmitted in highland Ethiopia, and it seems

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that the comparative rarity and discontinuous distribution of true B. truncatus could be the effective barrier to the parasite, regardless of other factors. Where B. truncatus occurs in the middle and lower Awash Valley, foci of S. haematobium are known, but this snail plays no evident part in transmission, and the intermediate host is B. abyssinicus (a member of the B. africanus group). If a parasite strain compatible with B. truncatus is not already present in Ethiopia, one is quite likely to be introduced and the colonisation of irrigation schemes by this snail is unwelcome (Kloos & Lemma, 1974). Fortunately in lakes Awasa and Zwai the potential for transmission of S. haematobium is much reduced by the preference of B. truncatus for marshes; the firm open shores which attract people are inhabited by diploid snails which probably are resistant to infection. The B. truncatus/tropicus complex in Kenya Although the highlands of Kenya and Ethiopia are separated today by about 500 km of lower and drier country, posing a barrier to dispersal of aquatic organisms, there have been periods of cooler climate when montane forest may have extended more or less continuously across the gap (Moreau, 1966). Therefore it would not be surprising to find the higher polyploids of Bulinus in Kenya, but they have not been found even though many populations living at high altitude (up to 2900 m) have been examined. Yet the search did reveal the presence in a high altitude zone of a unique tetraploid species, and showed that variation among diploid populations is comparable to that in Ethiopia and South Africa. At one time B. tropicus was the only member of the B. truncatus/tropicus group recognised to occur in Kenya apart from Lake Victoria (Mandahl-Barth, 1957). Then determinations of chromosome number and analyses of egg proteins led to the identification of B. truncatus, found commonly in the western lowlands of Nyanza province (Brown & Wright, 1974). Tetraploid snails with different characters, however, were found at that time in the Mau and Aberdare highlands, and are identified as B. permembranaceus (Preston, 1912; Brown, 1976; Brown & Shaw, 1989). This species differs from B. truncatus in the larger and higher-spired shell, less angular mesocone shape, lack of aphally, and characteristics of egg proteins (Fig. 130) and enzymes. Further, the highland tetraploid seems resistant to infection with S. haematobium. To distinguish it from high-spired forms of B. tropicus, it is necessary to determine chromosome number or molecular characters. The two tetraploid species are allopatric, B. truncatus being found rarely so high as 1900 m whereas B. permembranaceus occupies the altitude range 1940–1760 m. Restraints on the distribution of B. permembranaceus may be imposed by adaptation to cool climate and perhaps also by interaction with B. tropicus; some diploid populations have been found above the lower altitudinal limit for the tetraploid, but not in the same localities. The diploid populations in Kenya appear to be one species from their overall continuity in morphological variation and its lack of geographical pattern. But there are considerable differences among populations in shell form, which

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Fig. 133. Bulinus truncatus/tropicus complex in Kenya. Polygons enclosing distributions for individual shells of B. tropicus (n=796), B. truncatus (●, n=100) and B. permembranaceus (▲, n =291) plotted on the first 2 axes of a principal components analysis of 8 variables derived from the shell. These components accounted for 73% of the variation. Outlines of shells are: B. tropicus (A,C,E and F), B. permembranaceus (B) and B. truncatus (D). Shells C, D and F are twice the magnification of the others. Variation for B. tropicus overlaps almost completely both of the tetraploid species, and occupies alone an area of extremely high-spired shells (E) and a broader form (F) associated with ephemeral rainpools. From Brown et al. (1991, Fig. 5).

overlaps almost completely the combined variations for the two tetraploid species (Fig. 133); mesocone shape varies from non-angular to angular and enzymes are polymorphic. All 65 population samples studied by Brown et al. (1991) were classified as B. tropicus, though subdivision of this taxon might be justified. Although some populations have the mesocones mostly angular, they were not identified as B. natalensis, because the shell is comparatively high-

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spired; aphallic individuals were not found and geographical distribution was not distinct. A distinct shell form (Fig. 133F), small, globosely conic with a large umbilicus and corresponding to B. rumrutiensis (Preston), is associated with small rainpools. These pools last no longer than a few months and may lack even semi-aquatic vegetation. Similar snails occur in small pools in South Africa (Stiglingh et al., 1962), Ethiopia (Brown & Wright, 1972) and other countries. B. rumrutiensis is a strong candidate for recognition as a distinct species, but some interbreeding with snails of a different shell form was demonstrated by means of an enzyme marker (Brown et al., 1991). Both diploid and tetraploid populations of the B. truncatus/tropicus complex occur in Lake Victoria within Kenya and elsewhere, but their taxonomic position is obscure. Classified here as B. trigonus and B. transversalis, they may be lacustrine morphs of, respectively, B. tropicus and B. truncatus. Both forms live on stony beaches near Kisumu, and this is the closest association known between diploid and tetraploid snails of this complex. Although members of the B. truncatus/tropicus complex are widespread in the highlands and western lowlands of Kenya, and live in a great variety of habitats, none has been found in the entire eastern coastal district. Perhaps the climate there is too warm for B. tropicus, as it appears to be in northeast South Africa, but it is surprising that B. natalensis and B. truncatus do not occur in coastal Kenya. Tetraploidy in tropical Africa In the last decade considerable changes in the taxonomy of tetraploid snails related to B. truncatus living south of the Sahara resulted from morphological analyses and molecular observations. The trend has been for species regarded previously as distinct to be reduced to synonymy with B. truncatus. Yet variation in enzymes suggests that there may be a need to recognise local taxa below the species-level. The tropical distribution of B. truncatus is not entirely known, but it is far greater than once supposed. A large distribution in eastern and central Africa was formerly attributed to B. coulboisi (Bourguignat, 1890: type-locality near the western shore of Lake Tanganyika). The species was then known from morphological characters only and Mandahl-Barth (1965) commented that it was extremely difficult to separate from some forms of B. tropicus, though aphallic individuals were common and compatibility with S. haematobium had been reported. To establish the taxonomic position of B. coulboisi more clearly, examples collected near Lake Tanganyika were brought alive to London for study; they were B. truncatus according to their tetraploidy, morphology, egg proteins and enzymes (Brown et al., 1982). This snail lives in small waterbodies near Lake Tanganyika but apparently not in the main body of the lake. Further investigation is needed to

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determine the chromosome number of populations reported as B. coulboisi over a wider area, as some may be diploid. In the whole of West Africa from Senegal to eastern Nigeria, only tetraploid snails belonging to the B. truncatus/tropicus complex are found. They have been identified as B. guernei (Dautzenberg, 1890; type-locality in Senegal) or B. rohlfsi (Clessin, 1886; type-locality Lake Chad), treated as two full species or as subspecies of B. truncatus. Mandahl-Barth (1965) distinguished the two taxa by characters of the shell and mesocone shape, but Jelnes (1979b) recognised only a single West African taxon according to electrophoresis of enzymes. Further analyses of morphology and enzymes (Brown et al., 1986; Jelnes, 1986) indicated that guernei and rohlfsi are conspecific and indistinguishable from B. truncatus of North Africa. That a number of morphologically defined species seem inseparable from B. truncatus brings a welcome simplification to snail identification, by encouraging the use of one name for a species distributed from Iran to Senegal. But there is growing evidence of biological complexity at the population level. Enzyme analyses reveal interpopulation differences in fixed heterozygous loci that could be used to define different ‘biotypes’ (Nascetti & Bullini, 1980; Biocca et al., 1981; Bullini, 1982). Twenty populations of B. truncatus sampled in Cameroon by Mimpfoundi & Greer (1990c) were divisible into 4 groups, each distinguished by a unique combination of enzymes, and only one was associated with transmission of S. haematobium. The known distribution of B. truncatus in tropical Africa has been extended progressively southwards, through determination of chromosome number, into Kenya (Brown & Wright, 1974), lower Zaire (Mandahl-Barth et al., 1974), the Lake Tanganyika area (Brown et al., 1982) and south Malawi (Brown & Rollinson, 1982). Probably many more localities will be found by checking the chromosome number of snails supposed to be the diploid B. natalensis. As S. haematobium is transmitted by B. truncatus in lower Zaire, it is necessary to take into account the risk that this parasite strain might be dispersed into new areas where B. truncatus occurs or is present but not yet detected. The B. forskalii group The shell is slender and the spire generally higher than the aperture when adult. Some species are intermediate hosts for S. haematobium and other schistosomes. The group has representatives in Arabia, Africa, Madagascar and the Mascarene Islands. The chromosome number is diploid (2n=36). In this group the species recognised as valid in early morphological studies (Wright, 1963a; Mandahl-Barth, 1965, 1968) remain almost unchanged, though enzyme analyses have contributed interesting data at the population level and were used to define two new taxa. There is still need for critical revision of a number of species with type localities in Angola, and thought to be synonyms of B. forskalii.

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B. forskalii is reported from a very large area of Africa and it occurs in Madagascar. The shell varies widely and an unusually broad form occurs in São Tomé Island (Brown, 1991). This transmits S. intercalatum, as does B. forskalii in Cameroon. Although this species is not believed to transmit S. haematobium the possibility should be kept under review, as analyses of 15 enzymes (Mimpfoundi & Greer, 1989) showed no difference from B. camerunensis, which is an intermediate host. The genetic diversity of B. forskalii was rather low in surveys carried out in Kenya (Jelnes, 1980) and Cameroon, where the rarer alleles showed geographical distribution patterns that may be related to habitat (Mimpfoundi & Greer, 1990d) or associated with routes of dispersal (Mimpfoundi & Slootweg, 1991). Two new species were defined by enzymic characters (Jelnes, 1979c) both morphologically ‘very similar to B. forskalii’: B. barthi from the coastal area of Kenya and Tanzania, and B. browni from western Kenya and Zimbabwe. Criticism of this taxonomic procedure (Rollinson, 1979) was partly answered by Jelnes (1980) who reported the common occurrence of normal B. forskalii and B. browni in the same waterbody without any intermediate enzymic phenotype, while B. forskalii and B. barthi occurred in the same geographical area and without intermediates; self-fertilisation was rejected as an explanation of the data. Enzyme analyses over a larger geographical area are needed to support the case for giving these taxa species-status. Once known only from seasonal pools in Senegambia, B. senegalensis later appeared to occur with B. forskalii in alluvial pools and ricefields, and was eventually identified unequivocally with the aid of enzyme analyses (Goll, 1981). It is now known to occur through an area extending eastwards into Niger and Cameroon, and the existence of mixed populations of senegalensis and forskalii, without intermediates, is confirmed by observations on enzymes. Precise information about the distribution of B. senegalensis is of importance, as the snail is a host for S. haematobium, and undetected snail populations may be involved in transmission. The spatial isolation between small pools inhabited by the snail in the Gambia, and the drastic reduction in population size due to annual drying-up of the water led Wright (1961) to suggest the likely occurrence of genetic drift. Little genetic variation, however, is indicated among populations by enzyme analyses (Wright et al., 1979; Mimpfoundi & Slootweg, 1991). The low polymorphism seen among populations of B. senegalensis, as compared to B. forskalii, is perhaps an example of lower genetic diversity in a specialist versus a generalist species (Mimpfoundi & Greer, 1989). B. cernicus of Mauritius was once considered to be a form of B. forskalii, but it differs in shell shape among other characters and there have been suggestions that the Mauritian snails might belong to more than one local species, as populations vary markedly in the shell, radula, genital organs and enzymes (Courtois & Gébert, 1979; Jelnes, 1980), and compatibility with schistosomes (Frandsen, 1979). Differences in the shell, radula and enzymes among population

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samples from 25 localities were observed by Rollinson & Wright (1984) but breeding experiments indicated a lack of reproductive isolation. All 13 snail stocks tested were susceptible to a local strain of S. haematobium, and though compatibility varied it was not correlated with enzyme variation. It was concluded that all the populations belonged to one variable species. Eight populations were re-sampled 6 years later and genetic distance analysis confirmed the differences previously observed between snails from the northwest and southeast of the island (Rollinson et al., 1990). Allelic frequencies were generally consistent in the different populations over the 6-year period, suggesting little gene flow between them even though they are geographically close. The enzymic variation seen in B. cernicus is higher than observed in other members of the B. forskalii group; this could reflect the fact that crossfertilisation is commoner in B. cernicus. The B. reticulatus group The group comprises the two species B. reticulatus of Africa and B. wrighti of Arabia, which are related according to morphology and molecular characters (Wright, 1971b). The species hightoni, obtusispira and umbilicatus were added by Jelnes (1985) on the basis of shell characters, but these seem better placed in the B. africanus group. The chromosome number is diploid (2n=36). On naming B. reticulatus from specimens collected in western Kenya, Mandahl-Barth (1954) commented that they might turn out to be no more than an unusual variety of B. forskalii. But the new species proved clearly distinct and readily recognisable from the shell alone. Lack of close relationship to B. forskalii was indicated by electrophoretic analyses of egg proteins (Wright & Ross, 1966; Wright, 1971b; Hamilton-Atwell & Van Eeden, 1981b). B. reticulatus is a specialised inhabitant of seasonal rainpools and may be active for no more than a few months each year. Unless searched for at this time it is unlikely to be found, and should be much commoner than is indicated by scattered records from the large area extending from the South African highveld to the highlands of Ethiopia. B. wrighti was first collected by the British Museum (Natural History) Expedition 1937–38 to South-West Arabia, and these shells were recorded by Connolly (1941) as a small form of B. truncatus. Over twenty years later similar snails were found in South Yemen (Western Aden Protectorate) and identified as a form of B. reticulatus, with an unusual fusion between two cusps on the lateral radular teeth (Wright, 1963b). This difference proved to be consistent in all Arabian populations, which were named subspecies B.r.wrighti Mandahl-Barth, 1965, and later given full species-status according to the immunological reactions of egg proteins (Wright, 1971b). Like B. reticulatus, the Arabian species occupies a specialised niche, being found usually in small pools among rocks in wadis. Besides being a natural host for S. haematobium in Arabia, B. wrighti has been found compatible with all strains and species in the S.

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haematobium group to which it has been exposed and has thus played an important part in experimental work. The success of Bulinus Bulinus occurs almost throughout Africa and is abundant in a variety of habitats. It is broadly tolerant of climate, living from sea-level at the Equator up to the highest altitude at which aquatic snails are found in the mountains of East Africa, and in the coolest part of the southern temperate region. Able to survive in stagnant water and through drought, to grow rapidly and reproduce abundantly, Bulinus excels at exploiting the small seasonal waterbodies that are the only kind of habitat available in large areas of Africa. The genus is not wellrepresented in rapidly flowing water, deep lakes or, it would seem, in rain forest. The occurrence of dense populations in streams and rivers may depend precariously on niches protected from the full force of the current during floods and the formation of stagnant pools when flow slackens during the dry season. In big lakes Bulinus inhabits mainly the shallow margins, with the notable exception of the deep-water form of B. nyassanus in Lake Malawi, while B. natalensis lives in weedbeds down to 7 m depth in Lake Sibaya (Appleton, 1977). Although little is known about aquatic molluscan faunas in undisturbed forest, Paperna (1968) observed in south-east Ghana that the forest population of B. globosus was sparse and occurred mostly in streams and pools disturbed by human activities. Forest clearance favoured increasing distribution and abundance of B. truncatus (=rohlfsi) in Cameroon (Southgate et al., 1976). It may be concluded that species of Bulinus common in the savanna of today were probably much less widespread during past periods when the African climate was cooler and/or wetter and dense forest more extensive. Four inter-related aspects of the biology of Bulinus stand out for closer consideration in relation to the success of the snails: 1 aestivation; allows survival in small, nutrient-rich waterbodies that temporarily dry out; 2 breeding system; achieves rapid increase in numbers during short breeding seasons; 3 polyploidy; one of the most successful species is the tetraploid B. truncatus, which probably could not have arisen without the ability to self-fertilise; 4 tolerance of parasites; the efficient utilisation of environmental resources and a high capacity for reproduction allow Bulinus to maintain dense populations and to support a large biomass of trematode parasites. Aestivation (anhydrobiosis) A period of dormancy known as aestivation (from the Latin aestivus, relating to summer) occurs regularly in many populations of Bulinus when free-standing water disappears from the habitat during the dry season. As the dry period can

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occur in either the warm or the cool season, Stiglingh & Van Eeden (1977, p. 16) proposed the general term ‘anhydrobiosis’, but aestivation continues to be used regardless of season. Aestivation for as long as 6 months has been reported for several species; the behavioural and physiological aspects are described in Chapter 10. Life expectancies for aestivating B. globosus calculated from experiments range from 3 to 19 weeks (Woolhouse & Taylor, 1990). Species such as B. reticulatus and B. senegalensis are characteristic of seasonal pools and perhaps require an annual period of prolonged dormancy in order to maintain their populations. Other species aestivate irregularly according to local conditions, and the ability to aestivate seems to be a factor in the success of all the species of Bulinus apart from the few living in deep lakes. Aestivation could have some epidemiological importance as a schistosome infection can be carried over a dry period within a dormant snail (Webbe, 1962; Hira, 1968). However, B. globosus with patent infections at the beginning of aestivation had a significantly lower survival rate than non-patent snails (Woolhouse & Taylor, 1990). Although populations survive, many individual snails die as surface water disappears and there is further loss during dormancy. Recovery from the population crash when water returns depends on the high breeding performance of the survivors, measured by the demographic parameter r, the intrinsic rate of natural increase. A species which aestivates successfully but has a low r is unlikely to become common. The abundant B. globosus combines a good tolerance of desiccation with a high r over the temperature range experienced in tropical to subtropical climates (see Chapter 10). A similar strategy of adaptation is observed for B. tropicus in South Africa, though here in relation to the cooler conditions of the southern temperate climate. Breeding system The high rate of increase of a Bulinus population is the outcome of a reproductive strategy that includes two main components, the life cycle, which is adapted to the environment (Chapter 11), and the breeding system discussed here. Bulinus is a hermaphrodite able to reproduce by both cross-fertilisation (outcrossing) and self-fertilisation (selfing). The classic study of reproduction in B. truncatus (=contortus) by Larambergue (1939) resulted in four fundamental findings: 1 isolated virgin snails produce progeny resulting from self-fertilisation rather than parthenogenesis (according to cytological observations); 2 cross-fertilisation also occurs (demonstrated by using mantle pigmentation as a genetic marker); 3 populations in different localities may be exclusively aphallic (lacking the copulatory organ) or euphallic (normal), or have intermediate prevalences of aphally; 4 aphally has a complex genetic basis.

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The relative proportion of selfing to outcrossing in Bulinus is of particular interest for its effects on population genetic structure, knowledge of which is relevant to understanding interactions with parasites. This leads to assessment of the practicability of attempting to alter the genetic structure of snail populations by introducing genes for resistance to infection by schistosomes. Modification of the mating system in some species by aphally presents opportunities for investigating the partitioning of resources between reproduction and other demands, and the evolution from hermaphroditism to gonochorism. For such reasons attention to the reproductive biology of Bulinus has increased sharply in recent years and only selected references are given here: for reviews see Rollinson & Southgate (1985), Jarne & Delay (1991), and Jarne et al. (1993). In a copulating pair one snail acts as male; mating is often seen in the field and occurs readily in the laboratory (Rudolph, 1979, 1983; Rudolph & Bailey, 1985). That cross-fertilisation occurs commonly has been confirmed by analyses of polymorphic loci in natural populations and by parent-offspring analysis in the laboratory for B. cernicus of Mauritius (Rollinson & Wright, 1984; Rollinson et al., 1989) and for several species living in Africa (Rollinson, 1986). Insemination by more than one partner can occur and sperm storage after copulation allows isolated B. cernicus to reproduce by outcrossing for at least 70 days. Selfed and outcrossed individuals of B. globosus were distinguished by means of enzyme markers (Njiokou et al., 1992) and DNA fingerprinting (Jarne, Delay et al., 1992). It seems that many species of Bulinus show a preference for outcrossing. Rollinson & Southgate (1985) pointed out that for species living in ephemeral habitats, where populations undergo large fluctuations in size, mechanisms such as outcrossing, sperm storage and multiple insemination might play a role in maintaining heterogeneity; the effective gene pool of a population depleted by drought could be increased by snails storing the sperm of one or more partners. Although outcrossing may be preferred, isolated virgin Bulinus usually reproduce successfully, and the low enzyme diversity observed in natural populations of B. forskalii indicated that this species reproduces principally by self-fertilisation (Mimpfoundi & Greer, 1990d). All individuals in some populations of B. truncatus show the same multibanded electrophoretic pattern, sometimes referred to as ‘fixed heterozygosity’ (Paggi et al., 1978; Jelnes, 1979b; Wurzinger, 1979; Nascetti & Bullini, 1980). This has been attributed to parthenogenesis (Jelnes, 1979b), but seems more likely to be due to an allotetraploid origin for this species (Nascetti & Bullini, 1980) and a combination of sexual reproduction by self- and cross-fertilisation (Njiokou et al., 1993). Self-fertilisation evidently plays a part in the natural reproduction of Bulinus and among its advantages may be (1) the possibility of reproduction even when no partner is available, (2) conservation of locally adapted combinations of genes, and (3) saving the costs of copulation in time and effort. A major disadvantage of selfing in organisms generally is inbreeding depression, demonstrated in a stock of B. globosus originating from Niger by Jarne, Finot et al. (1991), who observed that outcrossing was more favourable according to

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three measures of fitness: number of eggs laid, survival at birth of young and number of snails reaching sexual maturity. Therefore it was concluded that the original population was predominantly outcrossing. In another stock of B. globosus, originating from Elevi in Ivory Coast, the fitness of selfing and outcrossing was about the same, and it appeared that this population was predominantly selfing (Njiokou et al., 1992). Variation among populations in mating system is thus a factor for consideration in analyses of population genetic structure in Bulinus. One factor that might promote selfing is aphally, for at least the reason that a high prevalence of aphally means a corresponding reduction in opportunities for copulation. Within Bulinus aphally is found regularly only in B. truncatus and B. natalensis (though it occurs also in unrelated genera such as Ferrissia). In addition to aphallic individuals, some snails have an incomplete and nonfunctional copulatory organ. Such abnormalities were found only rarely by Larambergue (1939, pp. 109–111) who believed they were not inherited, but in B. natalensis up to 16% of snails from different sites in Lake Sibayi were abnormal (Brown et al., 1971a). So high a frequency suggests that ‘partial aphally’ may be inherited, for it could have a selective value comparable to full aphally. By not producing the copulatory organ an aphallic snail saves resources that can be invested in other activities; experiments showed a higher fitness for aphallic than euphallic snails, and there was an average of 20% more eggs in the capsules of aphallic snails than euphallics (Jarne, Finot et al., 1992). Within a group of snails infected with S. haematobium, euphallics produced fewer eggs, smaller egg masses and fewer hatchlings reaching maturity than aphallics (Schrag & Rollinson, 1994). Mechanisms determining the phallic state are complex. Larambergue (1939) found evidence for heritability, to the extent that different and fairly constant proportions of aphallic and euphallic individuals were maintained through several self-fertilised generations of B. truncatus from Morocco, Senegal and Egypt. Aphally showed little if any heritability in snails originating from Nigeria, and it appeared that environmental determination might play a part (Schrag et al., 1992). Further studies (Schrag & Read, 1992) showed that the proportion of aphallics was greater at high maintenance temperature (30°C) than at low temperature (22°C). Temperature exerted its effect not on parental snails but on eggs after oviposition and on hatchling young; it presumably acts as a cue to future environmental conditions that will tend to favour either aphally or euphally (and the ability to outcross). Polyploidy In the Near East, Arabia and Mediterranean Africa, the tetraploid B. truncatus is the most widespread and abundant Bulinus (Figs 125–128). No closely-related diploid species is found in this area and it appears that the evolution of tetraploidy allowed a considerable expansion in the distribution of the genus. It is

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possible, however, that diploid populations once existed in this northern area but were displaced by tetraploid ones (see later section: Evolution). B. truncatus thrives in a wide variety of natural and artificial habitats and its distribution could still be increasing. It is noticeable that most of the waterbodies in Kenya where this snail has been found are man-made or much altered by human activities, and the southernmost locality known is an earth dam in Malawi. We can perhaps see a genetic basis for the success of B. truncatus in varied habitats in the numerous ‘biotypes’ differing in fixed heterozygous loci. The evolution of the tetraploid B. permembranaceus in Kenya and of B. hexaploidus and B. octoploidus in Ethiopia has enabled Bulinus to colonise highland plateaux more thoroughly than would otherwise have been possible. Only two diploid populations were found among 18 populations of the B. truncatus/ tropicus complex living at or above 2500 m in Kenya; the rest were B. permembranaceus and no other member of the genus was found at this altitude (Brown & Shaw, 1989; Brown et al., 1991). The restricted distribution of the highland polyploids suggests that they are specially adapted to local conditions and unlikely to expand their geographical ranges. Confirmation is needed of the reported occurrence of an octoploid in Arabia (Burch, 1964); suitable conditions might exist in the south-western highlands, but subsequently only tetraploid Bulinus have been found (Orecchia et al., 1973; Paggi et al., 1978). Tolerance of parasites Snails in their natural habitats are subjected to a ‘barrage of miracidia derived from numerous species of trematodes’ (Basch, 1975), and many trematode species have opportunities to evolve compatibility with a common species of snail. To remain common a snail must provide for its own needs and the demands of those parasites that overcome its defences. A contribution towards this end could be made by the high intrinsic rate of increase that enables populations to increase rapidly during a short breeding season, while quick growth and early sexual maturity allow egg production before the reproductive system has been seriously damaged by the parasites. High fecundity also enables a few uninfected individuals to re-populate a locality when many of their generation have suffered parasitic castration. Damage caused by trematode larvae in nature is seen clearly in B. tropicus, of which most medium-to-large specimens collected from some localities have their ovotestis destroyed by larval paramphistomes. The continued survival of such populations seems to depend on a few snails that have either escaped infection or have not yet developed mature infection. Another trematode, Echinoparyphium, found commonly in B. truncatus in Egypt by Moravec et al. (1974) was pathogenic, while the ovotestes of snails found naturally infected in Sardinia were almost completely destroyed (Mouahid & Moné, 1990). Cercariae of the ‘ornatae’ type, probably having an amphibian for their definitive host, were found by Betterton (1984) in 20% of B. truncatus collected from an irrigation

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channel in northern Nigeria during May; infected snails laid far fewer egg capsules than uninfected snails. The adverse impact of trematode infection has been advanced as an explanation for the restricted distributions of certain members of the B. forskalii group (see later section: Evolution). Of great interest would be an estimate of the pathogenic effects exerted on a natural snail population by its entire fauna of trematode parasites. This line of investigation is still at the early stages of identification and recording of prevalences. Four cercarial species other than schistosomes were observed in B. truncatus collected from an irrigation system in Egypt (Rysavy et al., 1974). At least 7 different trematodes were present in B. senegalensis from Gambia and Senegal (Wright et al., 1979). The most comprehensive study of Bulinus so far is by Loker et al. (1981), who examined nearly 4000 individuals of 5 species collected in the Mwanza district of Tanzania. Comparison of these results with those from earlier investigations centred on Lake Albert (Fain, 1953) and Lake Kivu (Vercammen-Grandjean, 1960) indicated that at least 15 trematode species infect Bulinus in this region, with an overall prevalence of 4.4%. In this genus the greatest diversity of parasites was found in B. forskalii with 7 species and an overall infection rate of 7% (Loker et al., 1981). Evolution We are obliged to interpret the evolution of Bulinus almost entirely from the living species because little has been deduced from the fossil record. Freshwater pulmonates are generally poorly represented as fossils in Africa, compared with prosobranchs and bivalves, until the late Pleistocene-Holocene period (Van Damme, 1984). This could be due partly to the poor chances of preservation for a fragile shell such as Bulinus, though it is suggested (Van Damme, 1984, pp. 113– 114) that ‘the rise and divergence of the pulmonates’ followed a widespread extinction of freshwater molluscs during the mid-Pliocene in the lake basins of eastern Africa. According to data reviewed by Van Damme, the earliest findings of Bulinus are in Pliocene beds: Bulinus sp. from deposits aged about 5.5–3.0 million years (m.y.) in the Turkana Basin; B. succinoides and B. nyassanus from deposits aged 3.0 m.y. in the Malawi Rift; B. truncatus from deposits aged 3.1–2. 6 m.y. in the Afar Depression in eastern Ethiopia. B. truncatus was also identified by Williamson (1981) from an extensive Pliocene-Pleistocene sequence in the Turkana Basin. Yet although no member of the B. forskalii group is known from earlier than the mid-Pleistocene in Africa, a fossil shell very like this group has been found in rocks of Eocene age (40–50 m.y.) in Canada (Russell, 1957, Fig. 6, ‘Aplexa ricei’; I am indebted to Dr Dwight Taylor for drawing my attention to this interesting shell). The sister group of Bulinus is Indoplanorbis, which has a discoid shell and lacks distinctive microsculpture. Therefore we might conclude that the primitive shell form within Bulinus is depressed to globose, with a large umbilicus, whereas the slender and high-spired forms are derived. Further, the characteristic

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nodular microsculpture of some species in the B. africanus group also seems to be derived, along with the columellar ridge and renal ridge. Otherwise the phylogenetic relations among the species groups seem to me obscure, at least on the morphological evidence, and molecular data are hardly more helpful at present. According to estimates of genetic distance based on 20 loci for 12 enzymes, analysed for some members of three species groups (Biocca et al., 1979), the B. forskalii group and the B. truncatus/tropicus complex were more closely related to each other than either was to the B. africanus group. The different dendrogram of Jelnes (1987), based on 7 enzymes, shows members of the B. africanus group and the B. truncatus/tropicus complex clustered together and separately from the B. forskalii group. Genetic distance analyses based on a better coverage of species and infra-specific variation are needed in order to understand the origins of the groups, and we will turn to more recent events. From immunological data for some members of the B. africanus group, Wright (1971b, p. 311) suggested that ‘the ancestral stock of B. obtusispira became isolated on Madagascar at a time when the africanus group had relatively recently diverged from the rest of the bulinid line’. If the ancestor of B. obtusispira were present on Madagascar at the time of its separation from mainland Africa in the early Cenozoic, a period of at least 60 million years must be allowed for the history of the africanus group. Its origin in East Africa was suggested by Wright (1961, 1963a) because he found populations of this group living in the coastal region to have rather indefinite species-characters; Wright proposed further that migration from this area in different directions led to the isolation of gene-pools and the differentiation of species. But given the great age proposed for the B. africanus group, it seems to me unlikely that traces of any such radiation would be detectable in the geographical pattern of variation today. To explain the much greater geographical distribution of B. forskalii compared with the smaller and peripheral distributions of B. senegalensis of West Africa, B. bavayi of Madagascar and Aldabra, and B. beccarii of Arabia, Wright (1971b, 1977) suggested a partly ecological explanation. These less common species can perhaps survive longer periods of drought than B. forskalii and they thrive under conditions tolerated by few if any other freshwater molluscs, ranging from the rainpools lacking almost any calcium inhabited by B. senegalensis to the alkaline waters colonised by B. bavayi. Wright suggested that the present distributions of such species could be remnants of formerly greater ranges where they had suffered from competition from other species including B. forskalii. Unfortunately for this theory there is no fossil evidence that any of the supposed ‘relict’ species was formerly more widespread, and it is now known that B. senegalensis and B. forskalii live together in many habitats. A further advantage that B. forskalii might have over the ‘relict’ species, according to Wright (1971b, 1977), was a lesser compatibility with schistosome parasites. B. forskalii, however, is frequently parasitised by other trematodes (Hira, 1968; Loker et al., 1981), and Wright et al. (1979) conceded that the entire parasite fauna needs to

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be taken into account when attempting to relate snail distribution to parasite pressure. Evolution in Bulinus can be most profitably discussed for the B. truncatus/ tropicus complex, where directions of change are indicated by chromosome numbers greater than the normal diploid complement (2n=36). There are at least two tetraploid (2n=72) species, the widely distributed B. truncatus and the very local B. permembranaceus, found only in the highlands of Kenya. Hexaploid (2n =108) and octoploid (2n=144) species occur in the highlands of Ethiopia. Each tetraploid species could have arisen from an individual snail, with double the usual number of chromosomes and which reproduced by self-fertilisation to found a new population. The establishment of tetraploidy was probably a necessary step in the evolution of hexaploidy and octoploidy. Because chromosomes of polyploid Bulinus form pairs at meiosis instead of multivalents, it was early deduced (Burch & Huber, 1966) that these chromosomal complements are allopolyploid in nature, i.e. they are composed of two or more different genomes, derived through hybridisation between species or genetically different conspecific populations. Further evidence for hybridisation in the origin of B. truncatus came from electrophoretic analyses of enzymes that showed a high proportion of loci fixed in the heterozygous condition (Nascetti & Bullini, 1980) and the occurrence of particular marker chromosomes in pairs rather than in sets of four (Goldman & LoVerde, 1983). Possible ancestors of B. truncatus could have been B. tropicus and B. natalensis, two diploid species showing many of the alleles found in the tetraploid (Nascetti & Bullini, 1980); presumably this natalensis genome included genes favouring aphally and compatibility with S. haematobium. Perhaps B. truncatus originated from a single polyploidization event and spread rapidly to occupy its present great range. This would accord with the uniformity of the electrophoretic pattern given by egg proteins as well as the overall continuity in genetic variation (Nascetti & Bullini, 1980). The egg protein pattern is clearly different in B. permembranaceus, which is a distinct species according to other characters and its allopatric distribution. There is however some evidence for multiple origins in B. truncatus, from genetic differences among populations (Jelnes, 1979b, 1986; Nascetti & Bullini, 1980; Mimpfoundi & Greer, 1990c). Diploid populations are unknown from the northern and most of the western areas of the range of B. truncatus. Possibly B. truncatus originated in eastern Africa and spread into areas unoccupied by the ancestral diploid species. The presence of subfossil shells identified as B. truncatus in Mid-Pleistocene deposits in Egypt and the Sahara (Van Damme, 1984) suggests that the range was largely established more than 100 000 years ago. The tetraploid might have been enabled by hybrid vigour (heterosis) to colonise areas unfavourable to the diploid ancestors (Nascetti & Bullini, 1980). It is also possible, however, that diploid populations of the B. truncatus/ tropicus complex once existed far to the north of their present range, but have

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been eliminated in competition with B. truncatus. Besides the competitive advantage that hybrid vigour could give to B. truncatus, this species could benefit further from the high fecundity of aphallic individuals if they lay more eggs than euphallic diploids, as they do compared with conspecific euphallics (Jarne, Finot et al., 1992). Possibly a relict of a greater diploid distribution in the past, a few diploid euphallic populations were recently found in Cameroon far from the main range (Mimpfoundi & Greer, 1990c). Tetraploidy might even have originated in a vanished diploid population that lived north of the Sahara, or in the Near East, from where the polyploid could have invaded tropical Africa. References Amberson, J.M. & Schwartz, E. 1953. On African schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 47:451–502. Appleton, C.C. 1977. The freshwater Mollusca of Tongaland, with a note on molluscan distribution in Lake Sibaya. Annals of the Natal Museum, 23:129–144. Archer, R.C. 1988. Taxonomic Study of the Bulinus africanus group in Kenya. M. Phil. Thesis, University of London. 174 pp. Basch, P.P. 1975. An interpretation of snail-trematode infection rates: specificity based on concordance of compatible phenotypes. International Journal of Parasitology, 5: 449–452. Betterton, C.C. 1984. Spatiotemporal distributional patterns of Bulinus rohlfsi (Clessin), B. forskalii (Ehrenberg) and B. senegalensis Muller in newly irrigated areas in northern Nigeria. Journal of Molluscan Studies, 50:137–152. Biocca, E., Bullini, L. & Chabaud, A. 1981. Classification of the subfamily Bulininae and of the Isidora truncata complex on morphogenetic criteria. In Parasitological Topics: 34–38. Canning, E.U. (Ed.). Special Publication 1, American Society of Protozoologists. Biocca, E., Bullini, L., Chabaud, A., Nascetti, G., Orecchia, P. & Paggi, L. 1979. Subdivisions su base morfologica e genetica del genere Bulinus in tre generi: Bulinus Müller, Physopsis Krauss e Mandahlbarthia gen. nov. Rendiconti della Classe di Scienza fisiche, matematiche e naturali, Accademia Nazionale dei Lincei, ser. 8, 66: 276–282. Brackenbury, T.D. & Appleton, C.C. 1991. Morphology of the mature spermatozoon of Bulinus tropicus (Krauss, 1848). Malacologia, 33:273–280. Brown, D.S. 1965. Freshwater gastropod Mollusca from Ethiopia. Bulletin of the British Museum (Natural History), Zoology, 12:37–94. Brown, D.S. 1966. On certain morphological features of Bulinus africanus and B. globosus and the distribution of these species in south-eastern Africa . Annals of the Natal Museum, 18:401–415. Brown, D.S. 1976. A tetraploid freshwater snail (Planorbidae: Bulinus) in the highlands of Kenya. Journal of Natural History, 10:257–267. Brown, D.S. 1980. Freshwater Snails of Africa and their Medical Importance. London: Taylor & Francis.

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Brown, D.S. 1981. Generic nomenclature of freshwater snails commonly classified in the genus Bulinus (Mollusca: Basommatophora). Journal of Natural History, 15: 909–915. Brown, D.S. 1982. The radula mesocone as a source of taxonomic characters in Bulinus. Malacologia, 22:505–508. Brown, D.S. 1991. Freshwater snails of São Tomé, with special reference to Bulinus forskalii (Ehrenberg), host of Schistosoma intercalatum. Hydrobiologia, 209: 141–153. Brown, D.S. & Burch, J.B. 1967. Distribution of cytologically different populations of the genus Bulinus in Ethiopia. Malacologia, 6:189–198. Brown, D.S. & Rollinson, D. 1982. The southern distribution of the freshwater snail Bulinus truncatus. South African Journal of Science, 78:290–293. Brown, D.S. & Shaw, K.M. 1989. Freshwater snails of the Bulinus truncatus/tropicus complex in Kenya: tetraploid species. Journal of Molluscan Studies, 55:509–532. Brown, D.S. & Wright, C.A. 1972. On a polyploid complex of freshwater snails (Planorbidae: Bulinus) in Ethiopia. Journal of Zoology, London, 167:97–132. Brown, D.S. & Wright, C.A. 1974. Bulinus truncatus as a potential intermediate host for Schistosoma haematobium on the Kano Plain, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene, 68:341–342. Brown, D.S. & Wright, C.A. 1978. A new species of Bulinus from temporary freshwater pools in Kenya. Journal of Natural History, 12:217–229. Brown, D.S., Matovu, D.B. & Rollinson, R. 1982. Bulinus coulboisi of Lake Tanganyika: assessment of its taxonomic position and role as intermediate host for S. haematobium. Journal of Natural History, 16:673–687. Brown, D.S., Oberholzer, G. & Van Eeden, J.A. 1971a. The Bulinus natalensis/tropicus complex in south-eastern Africa. 1. Shell, mantle, copulatory organ and chromosome number. Malacologia, 11:141–170. Brown, D.S., Oberholzer, G. & Van Eeden, J.A. 1971b. The Bulinus natalensis/tropicus complex in south-eastern Africa. 2. Some biological observations, taxonomy and general discussion. Malacologia, 11:171–198. Brown, D.S., Shaw, K.M. & Rollinson, D. 1991. Freshwater snails of the Bulinus truncatus/ tropicus complex in Kenya: diploid populations. Journal of Molluscan Studies, 57:143– 166. Brown, D.S., Schutte, C.H.J., Burch, J.B. & Natarajan, P. 1967. Chromosome numbers in relation to other morphological characters of some southern African Bulinus. Malacologia, 6:175–188. Brown, D.S., Shaw, K.M., Southgate, V.R. & Rollinson, D. 1986. Bulinus guernei (Mollusca: Gastropoda) of West Africa: taxonomic status and role as host for schistosomes. Zoological Journal of the Linnean Society, 88:59–90. Brygoo, E.R. & Moreau, J.P. 1966. Bulinus obtusispira (Smith, 1886) hôte intermédiaire de la bilharziose à Schistosoma haematobium dans le nord-ouest de Madagascar. Bulletin de la Société de Pathologie exotique, 59:835–839. Bullini, L. 1982. Genetic, ecological and ethological aspects of the speciation process. In Mechanisms of Speciation: 241–264. Barigozzi, C. (Ed.). New York: Alan Liss. Burch, J.B. 1960. Chromosome numbers of schistosome vector snails. Zeitschrift für Tropenmedizin und Parasitologie, 11:450–452. Burch, J.B. 1963. A cytological study of African bulinine snails, vectors of urinary schistosomiasis. Annual Reports of the American Malacological Union, 30:15–16.

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Burch, J.B. 1964. Cytological studies of Planorbidae. 2. The African subgenus Bulinus s.s. Malacologia, 1:387–400. Burch, J.B. 1967. Some species of the genus Bulinus in Ethiopia, possibly intermediate hosts of Schistosoma haematobium. Ethiopian Medical Journal, 5:245–257. Burch, J.B. 1969. The chromosome number of Bulinus sericinus from Ethiopia. Malacological Review, 2:113–114. Burch, J.B. 1972. Names for two polyploid species of African Bulinus. Malacological Review, 5:7–8. Burch, J.B. & Huber, J.M. 1966. Polyploidy in mollusks. Malacologia, 5:41–43. Burch, J.B. & Lindsay, G.K. 1967. Electrophoretic analysis of esterase in Bulinus. Reports of the American Malacological Union, 34:39–40. Burch, J.B. & Lindsay, G.K. 1970. An immuno-cytological study of Bulinus s.s. Malacological Review, 3:1–18. Burch, J.B. & Lindsay, G.K. 1971. The immunological response of South African Bulinus natalensis antigens to diploid and polyploid Bulinus antisera. Zoologica Africana, 6: 39– 44. Claugher, D. 1971. Karyotype analysis of bulinid snails. Bulletin of the World Health Organisation, 45:855–858. Connolly, M. 1925. The non-marine Mollusca of Portuguese East Africa. Transactions of the Royal Society of South Africa, 12:105–220. Connolly, M. 1939. A monographic survey of the South African non-marine Mollusca. Annals of the South African Museum, 33:1–660. Connolly, M. 1941. South Arabian non-marine Mollusca. British Museum (Natural History) Expedition to South West Arabia, 1937–8, 1(4):17–42. Courtois, C.M. & Gebert, F. 1979. Recent observations on schistosomiasis in Mauritius. Tropical and Geographical Medicine, 31:381–387. Degrémont, A.A. 1973. Mangoky Project. Campaign against schistosomiasis in the lower Mangoky (Madagascar). Basle: Swiss Tropical Institute. Fain, A. 1953. Contribution à l’étude des formes larvaires des Trématodes au Congo belge et spécialement de la larve de Schistosoma mansoni. Mémoires, Institut Royal Colonial Belge, section des Sciences naturelles et médicales, 22:1–312. Frandsen, F. 1979. Further studies on the compatibility between S. intercalatum from Cameroun and Zaire and species of Bulinus. Zeitschrift für Parasitenkunde, 58: 161– 167. Fryer, S.E., Rollinson, D. & Probert, A.J. 1987. Studies on the morphology and crossbreeding ability of two populations of Bulinus globosus from northern Nigeria. Journal of Molluscan Studies, 53:153–162. Goldman, M.A. & LoVerde, P.T. 1983. Hybrid origin of polyploidy in freshwater snails of the genus Bulinus. Evolution, 37:592–600. Goldman, M.A., LoVerde, P.T. & Chrisman, C.L. 1980. Comparative karyology of the freshwater snails Bulinus tropicus and B. natalensis. Canadian Journal of Genetics and Cytology, 22:361–367. Goldman, M.A., LoVerde, P.T., Chrisman, C.L. & Franklin, D.A. 1984. Chromosomal evolution in planorbid snails of the genera Bulinus and Biomphalaria. Malacologia, 25: 427–446. Goll, P.H. 1981. Mixed populations of Bulinus senegalensis (Müller) and B. forskalii (Ehrenberg) in the Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75:576–578.

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Hamilton-Atwell, V.L. 1976. Electrophoresis of the perivitelline fluid of molluscan eggs: 4. Protein characteristics determining the taxonomic position of B. (B.) depressus Haas and B. (B.) natalensis (Kuster). Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 76:37 pp. Hamilton-Atwell, V.L. & Van Eeden, J.A. 1969. The shell, radula, pallial organs and reproductive system of Bulinus (B.) depressus Haas. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 9:54 pp. Hamilton-Atwell, V.L. & Van Eeden, J.A. 1981a. Electrophoresis of the perivitelline fluid of molluscan eggs: 5. A comparison between Bulinus africanus (Krauss) and B. globosus (Morelet). Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 77:15 pp. Hamilton-Atwell, V.L. & Van Eeden, J.A. 1981b. Electrophoresis of the perivitelline fluid of molluscan eggs: 6. The electrophoretic patterns of Bulinus forskalii (Ehrenberg) and B. reticulatus Mandahl-Barth. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 78:10 pp. Hira, P.R. 1968. Larval trematodes from Bulinus (B.) forskalii Ehrenberg in Ibadan, Nigeria. Nigerian Journal of Science, 2:121–130. Jarne, P. & Delay, B. 1991. Population genetics of freshwater snails. Trends in Ecology and Evolution, 6:383–386. Jarne, P., Vianey-Liaud, M. & Delay, B. 1993. Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biological Journal of the Linnean Society, 49:99–125. Jarne, P., Finot, L., Delay, B. & Thaler, L. 1991. Self-fertilization versus crossfertilization in the hermaphrodite freshwater snail Bulinus globosus. Evolution, 45: 1136–1146. Jarne, P., Finot, L., Bellec, C. & Delay, B. 1992. Aphally versus euphally in self-fertile hermaphrodite snails from the species Bulinus truncatus. American Naturalist, 139: 424– 432. Jarne, P., Delay, B., Bellec, C., Roizes, G. & Cuny, G. 1992. Analysis of mating systems in the schistosome-vector hermaphrodite snail Bulinus globosus by DNA fingerprinting. Heredity, 68:141–146. Jelnes, J.E. 1977. An electrophoretic character useful in the distinction between Bulinus tropicus and B. permembranaceus. Steenstrupia, 4:139–141. Jelnes, J.E. 1979a. Taxonomical studies on Bulinus using isoenzyme electrophoresis with special reference to the africanus group on the Kano Plain, Kenya. Malacologia, 18: 147–149. Jelnes, J.E. 1979b. Experimental taxonomy of Bulinus. 1. Electrophoretic studies on esterase and phosphoglucose isomerase of Bulinus truncatus. Archiv für Molluskenkunde, 109:237–248. Jelnes, J.E. 1979c. Experimental taxonomy of Bulinus. 2. Recipes for horizontal gel electrophoresis of ten enzymes in Bulinus and description of internal standard systems and of two new species of the B. forskalii complex. Journal of Chromatography, 170: 405–411. Jelnes, J.E. 1980. Experimental taxonomy of Bulinus. 3. Electrophoretic observations on Bulinus forskalii, B. browni, B. barthi and B. scalaris from East Africa, with additional electrophoretic data on the subgenus Bulinus s.s. from other parts of Africa. Steenstrupia, 6:177–193.

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Jelnes, J.E. 1984. Taxonomie expérimental de Bulinus. 6. Possibilité d’utiliser des charactères enzymatiques pour la distinction entre les espèces Bulinus liratus et B. obtusispira à Madagascar. Archives de l’Institut Pasteur de Madagascar, 51:89–96. Jelnes, J.E. 1985. Experimental taxonomy of Bulinus (Gastropoda, Planorbidae)—past and future activities. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjøbenhavn, 146:85–100. Jelnes, J.E. 1986. Experimental taxonomy of Bulinus: the West and North African species reconsidered, based upon an electrophoretic study of several enzymes per individual. Zoological Journal of the Linnean Society, 87:1–26. Jelnes, J.E. 1987. Enzymelektroforese anvendt til belysning af afrikanske og amerikanske bilharziosesnegles systematik. Privately published (in Danish with English summary). Jelnes, J.E. 1991. Morphometry versus classical and experimental taxonomy: a dilemma posed by studies on West African Bulinus. Journal of Molluscan Studies, 57: 297–299. Jickeli, C.F. 1874. Fauna der Land- und Süsswasser Mollusken Nord-Ost-Afrikas. Nova Acta Academiae Caesareae Leopoldino-Carolinae, 37:1–352. Joubert, P.H., Kruger, F.J. & Pretorius, S.J. 1990. Susceptibility of South African Bulinus africanus to infection with Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene, 84:100–102. Joubert, P.H., Pretorius, S.J. & Kruger, F.J. 1991. Further studies on the susceptibility of Bulinus africanus to infection with Schistosoma haematobium. Annals of Tropical Medicine and Parasitology, 85:253–258. Joubert, P.H., Pretorius, S.J., De Kock, K.N. & Van Eeden, J.A. 1984. The effect of constant low temperatures on the survival of Bulinus africanus, Bulinus globosus and Biomphalaria pfeifferi. South African Journal of Zoology, 19:314–316. Joubert, P.H., Pretorius, S.J., De Kock, K.N. & Van Eeden, J.A. 1986. Survival of Bulinus africanus, Bulinus globosus and Biomphalaria pfeifferi at constant high temperatures. South African Journal of Zoology, 21:85–88. Kloos, H. & Lemma, A. 1974. Bilharziasis in the Awash Valley. 2. Molluscan fauna in irrigation farms and agricultural development. Ethiopian Medical Journal, 12: 157– 173. Krauss, F. 1848. Die Südafrikanischen Mollusken. Stuttgart: Ebner & Seubert. Kristensen, T.K. 1986. The significance of numerical taxonomy in the analysis of morphological differences between taxa of Bulinus (Gastropoda: Planorbidae): B. africanus group from East Africa. In Proceedings of the Eighth International Malacological Congress: 131–136. Pintér, L. (Ed.). Budapest: Hungarian Natural History Museum. Kristensen, T.K. & Christensen, A.G. 1989. Bulinus africanus-group species in West Africa differentiated by morphometric analysis. Journal of Molluscan Studies, 55: 103–110. Kristensen, T.K. & Christensen, A.G. 1991. Morphometry versus electrophoresis in Bulinus taxonomy—a reply. Journal of Molluscan Studies, 57:299–300. Kristensen, T.K., Frandsen, F. & Christensen, A.G. 1987. Bulinus africanus-group snails in East and South East Africa differentiated by use of biometric multivariate analysis on morphological characters. Revue de Zoologie Africaine, 101:55–69.

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Langand, J., Barral, V., Delay, B. & Jourdane, J. 1993. Detection of genetic diversity within snail intermediate hosts of the genus Bulinus by using Random Amplified Polymorphic DNA markers (RAPDs). Acta Tropica, 55:205–215. Larambergue, M.de, 1939. Etude de l’autofécondation chez les Gastéropodes pulmonés. Recherche sur l’aphallie et fécondation chez Bulinus (Isidora) contortus Michaud. Bulletin biologique de la France et de la Belgique, 73:19–231. Loker, E.S., Moyo, H.G. & Gardner, S.L. 1981. Trematode-gastropod associations in 9 non-lacustrine habitats in the Mwanza region of Tanzania. Parasitology, 83: 381–399. Malek, E.A. 1958. Distribution of the intermediate hosts of bilharziasis in relation to hydrography. Bulletin of the World Health Organisation, 18:691–734. Mandahl-Barth, G. 1954. The freshwater molluscs of Uganda and adjacent territories. Annales du Musée Royal du Congo Belge, Tervuren, série 8°, Sciences zoologiques, 32:1–206. Mandahl-Barth, G. 1957. Intermediate hosts of Schistosoma, African Biomphalaria and Bulinus. 2. Bulinus. Bulletin of the World Health Organisation, 17:1–65. Mandahl-Barth, G. 1965. The species of the genus Bulinus, intermediate hosts of Schistosoma. Bulletin of the World Health Organisation, 33:33–44. Mandahl-Barth, G. 1968. Freshwater molluscs. Exploration hydrobiologique BangweuluLuapula, 12:1–68. Mandahl-Barth, G. 1973. Descriptions of new species of African freshwater molluscs. Proceedings of the Malacological Society of London, 40:277–286. Mandahl-Barth, G., Ripert, C. & Raccurt, C. 1974. Nature du sous-sol, répartition des mollusques dulcaquicoles et foyers de bilharzioses intestinale et urinaire au BasZaire. Revue de Zoologie Africaine, 88:553–584. Mimpfoundi, R. & Greer, G.J. 1989. Allozyme comparisons among species of the Bulinus forskalii group in Cameroon. Journal of Molluscan Studies, 55:405–410. Mimpfoundi, R. & Greer, G.J. 1990a. Allozyme variation among populations of Biomphalaria pfeifferi (Krauss, 1848) in Cameroon. Journal of Molluscan Studies, 56:461– 467. Mimpfoundi, R. & Greer, G.J. 1990b. Allozyme variation among populations of Biomphalaria camerunensis (Boettger, 1941) in Cameroon . Journal of Molluscan Studies, 56:373–381. Mimpfoundi, R. & Greer, G.J. 1990c. Allozyme comparisons and ploidy levels among species of the Bulinus truncatus/tropicus complex in Cameroon. Journal of Molluscan Studies, 56:63–68. Mimpfoundi, R. & Greer, G.J. 1990d. Allozyme variation among populations of Bulinus forskalii (Ehrenberg, 1831) in Cameroon. Journal of Molluscan Studies, 56: 363–371. Mimpfoundi, R. & Slootweg, R. 1991. Further observations on the distribution of Bulinus senegalensis Müller in Cameroon. Journal of Molluscan Studies, 57:487–489. Moravec, F., Barus, V., Rysavy, B. et al. 1974. Antagonisms of Echinoparyphium recurvatum against Schistosoma haematobium in the snail Bulinus truncatus. Folia Parasitologia, 21: 127–141. Moreau, R.F. 1966. The Bird Faunas of Africa and its Islands. London and New York: Academic Press.

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Morelet, A. 1866. Coquilles nouvelles recueillies par le Dr Fr.Welwitsch dans l’Afrique équatoriale, et particulièrement dans les provinces portugaises d’Angola et de Benguella. Journal de Conchyliologie, série 3, 6:153–163. Mouahid, A. & Moné, H. 1990. Interference of Echinoparyphium elegans with the hostparasite system Bulinus truncatus-Schistosoma bovis in natural conditions. Annals of Tropical Medicine and Parasitology, 84:341–348. Moyroud, J., Breuil, J., Dulat, C. & Coulanges, P. 1983. Les mollusques hôte intermédiaires des bilharzioses humaines à Madagascar, état actual des connaissances. Archives Institut Pasteur Madagascar, 50:39–65. Nascetti, G. & Bullini, L. 1980. Genetic differentiation in the Mandahlbarthia truncata complex (Gastropoda: Planorbidae). Parassitologia, 22:269–274. Njiokou, F., Bellec, C., N’Goran, E.K., Yapi Yapi, G., Delay, B. & Jarne, P. 1992. Comparative fitness and reproductive isolation between two Bulinus globosus populations. Journal of Molluscan Studies, 58:367–376. Njiokou, F., Bellec, C., Jarne, P., Finot, L. & Delay, B. 1993. Mating system analysis using protein electrophoresis in the self-fertile hermaphrodite species Bulinus truncatus. Journal of Molluscan Studies, 59:125–133. Oberholzer, G., Brown, D.S. & Van Eeden, J.A. 1970. Taxonomic characters of the radula in the Bulinus natalensis/tropicus complex in eastern southern Africa. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 10:41 pp. Orecchia, P., Paggi, L. & Parinello, A. 1973. Su di un Bulinus raccolto nella zone di Tai’zz (Yemen). Parassitologia, 15:267–272. Paggi, L., Orecchia, P., Bullini, L., Nascetti, G. & Biocca, E. 1978. Studi morfologici, biologici e biochimici su una nuova specie di Bulinus. Parassitologia, 20:1–7. Paperna, I. 1968. Studies in the transmission of schistosomiasis in Ghana. 1. Ecology of Bulinus (Physopsis) globosus, the snail host of S. haematobium in south-east Ghana. Ghana Journal of Science, 8:30–51. Pitchford, R.J. 1965. Differences in the egg morphology and certain biological characters of some African and middle eastern schistosomes, etc. Bulletin of the World Health Organisation, 32:105–120. Preston, H.B. 1912. Diagnoses of new species of terrestrial and fluviatile shells from British East Africa and Uganda. Revue Zoologique Africaine, 1:322–329. Pringle, G., Otieno, L.H. & Chimtawi, M.B. 1971. Notes on the morphology, susceptibility to Schistosoma haematobium and genetic relationships of Bulinus (Physopsis) nasutus and B. (P.) globosus from north-eastern Tanzania. Annals of Tropical Medicine and Parasitology, 65:211–219. Rollinson, D. 1979. The use of enzymes in taxonomy of Bulinus. Transactions of the Royal Society of Tropical Medicine and Hygiene, 73:601. Rollinson, D. 1986. Reproductive strategies of some species of Bulinus. In Proceedings of the Eighth International Malacological Congress, Budapest, 1983:221–225. Pintér, L. (Ed.). Budapest: Hungarian Natural History Museum. Rollinson, D. & Kane, R.A. 1991. Restriction enzyme analysis of DNA from species of Bulinus (Basommatophora: Planorbidae) using a cloned ribosomal RNA probe. Journal of Molluscan Studies, 57:93–98. Rollinson, D. & Southgate, V.R. 1979. Enzyme analyses of Bulinus africanus group snails from Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 73: 667–672.

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Rollinson, D. & Southgate, V.R. 1985. Schistosomes and snail populations: genetic variability and parasite transmission. In Ecology and Genetics of Host-Parasite Interactions: 91–109. Rollinson, D. & Anderson, R.M. (Eds). London: Academic Press. Rollinson, D. & Wright, C.A. 1984. Population studies on Bulinus cernicus from Mauritius. Malacologia, 25:447–463. Rollinson, D., Kane, R.A. & Lines, J.R. 1989. An analysis of fertilization in Bulinus cernicus (Gastropoda: Planorbidae). Journal of Zoology, London, 217:295–310. Rollinson, D., Kane, R.A., Warlow, A., Southgate, V.R. & Gopaul, A.R. 1990. Observations on genetic diversity of Bulinus cernicus (Gastropoda: Planorbidae) from Mauritius. Journal of Zoology, London, 222:19–26. Rudolph, P.H. 1979. An analysis of copulation in Bulinus (Physopsis) globosus (Gastropoda: Planorbidae). Malacologia, 147–155. Rudolph, P.H. 1983. Copulatory activity and sperm production in Bulinus globosus. Journal of Molluscan Studies, 49:125–132. Rudolph, P.H. & Bailey, J.B. 1983. Inheritance of mantle pigmentation patterns in Bulinus (Physopsis) africanus. Freshwater Invertebrate Biology, 5:56–59. Rudolph, P.H. & Bailey, J.B. 1985. Copulation as females and use of allosperm in the freshwater snail genus Bulinus. Journal of Molluscan Studies, 51:267–275. Russell, L.S. 1957. Mollusca from the Tertiary of Princetown, British Columbia. Bulletin of the National Museum of Canada, 147:84–95. Rysavy, B., Moravec, F., Barus, V. et al. 1974. Some helminths of Bulinus truncatus and Biomphalaria alexandrina from the irrigation system near Cairo. Folia Parasitologica, 21:97–105. Saladin, B., Degrémont, A.A. & Weiss, N. 1976. Isoelectric focusing in the taxonomy of bulinid snails. Acta Tropica, 33:376–379. Schrag, S.J. & Read, A.F. 1992. Temperature and determination of male outcrossing ability in a simultaneous hermaphrodite. Evolution, 46:1698–1707. Schrag, S.J. & Rollinson, D. 1994. Effects of Schistosoma haematobium infection on reproductive success and male outcrossing ability in the simultaneous hermaphrodite Bulinus truncatus (Gastropoda: Planorbidae). Parasitology, 88:27–34. Schrag, S.J., Rollinson, D., Keymer, A.E. & Read, A.F. 1992. Heritability of male outcrossing ability in the simultaneous hermaphrodite Bulinus truncatus. Journal of Zoology, London, 226:311–319. Schutte, C.H.J. 1965. Notes on the radula mesocone as a criterion for distinguishing between the tropicus and the truncatus groups of the genus Bulinus. Annals and Magazine of Natural History, 8:409–419. Schutte, C.H.J. 1966. Observations on two South African bulinid species of the truncatus group. Annals of Tropical Medicine and Parasitology, 60:106–113. Shaw, K.M. & Brown, D.S. 1986. Multivariate analyses of morphometric studies in Bulinus. In Proceedings of the Eighth International Malacological Congress, Budapest, 1983: 239–243. Pintér, L. (Ed.). Budapest: Hungarian Natural History Museum. Southgate, V.R., Van Wijk, H.B. & Wright, C.A. 1976. Schistosomiasis at Loum, Cameroun, Schistosoma haematobium, S. intercalatum and their natural hybrid. Zeitschrift für Parasitenkunde, 49:145–159.

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Stiglingh, I. & Van Eeden, J.A. 1977. Population fluctuations and ecology of Bulinus tropicus. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 87:1–37. Stiglingh, I., Van Eeden, J.A. & Ryke, P.A. 1962. Contribution to the morphology of Bulinus tropicus. Malacologia, 1:73–114. Strahan, K., Kane, R.A. & Rollinson, D. 1991. Development of cloned DNA probes for the identification of snail intermediate hosts within the genus Bulinus. Acta Tropica, 48:117–126. Van Damme, D. 1984. The Freshwater Mollusca of Northern Africa. Distribution, Biogeography and Palaeoecology. Dordrecht: W.Junk. Vercammen-Grandjean, P.H. 1960. Les trématodes du Lac Kivu Sud. Annales Musée Royal de l’Afrique Centrale, Tervuren, nouvelle série 4°, Sciences zoologiques, 5: 1–171. Webbe, G. 1962. The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bulletin of the World Health Organisation, 27:59–85. Williamson, P.G. 1981. Palaeontological documentation of speciation in Cenozoic molluscs from the Turkana Basin. Nature, London, 293:437–443. Woolhouse, M.E.J. & Taylor, P. 1990. Survival rates of Bulinus globosus during aestivation. Annals of Tropical Medicine and Parasitology, 84:293–294. Wright, C.A. 1957. Studies on the structure and taxonomy of Bulinus jousseaumei (Dautzenberg). Bulletin of the British Museum (Natural History), Zoology, 5:1–28. Wright, C.A. 1961. Taxonomic problems in the molluscan genus Bulinus. Transactions of the Royal Society of Tropical Medicine and Hygiene, 55:225–231. Wright, C.A. 1963a. The freshwater gastropod Mollusca of Angola. Bulletin of the British Museum (Natural History), Zoology, 10:449–528. Wright, C.A. 1963b. The freshwater gastropod molluscs of Western Aden Protectorate. Bulletin of the British Museum (Natural History), Zoology, 10:257–274. Wright, C.A. 1971a. Flukes and Snails. London: George Allen & Unwin. Wright, C.A. 1971b. Bulinus on Aldabra and the subfamily Bulininae in the Indian Ocean area. Philosophical Transactions of the Royal Society, B, 260:299–313. Wright, C.A. 1974. Biochemical and immunological taxonomy of the Mollusca. In Biochemical and Immunological Taxonomy of Animals: 351–386. Wright, C.A. (Ed.). London and New York: Academic Press. Wright, C.A. 1977. Co-evolution of bulinid snails and African schistosomes. In Medicine in a Tropical Environment: 291–302. Gear, J.H. (Ed.). Cape Town: Balkema. Wright, C.A. & Brown, D.S. 1962. On a collection of freshwater gastropod molluscs from the Ethiopian highlands . Bulletin of the British Museum (Natural History), Zoology, 8:285–312. Wright, C.A. & File, S.K. 1968. Digestive gland esterases in the genus Bulinus. Comparative Biochemistry and Physiology, 27:871–874. Wright, C.A. & Rollinson, D. 1979. Analysis of enzymes in the Bulinus africanus group (Mollusca: Planorbidae) by isoelectric focusing. Journal of Natural History, 13: 263– 273. Wright, C.A. & Rollinson, D. 1981. Analysis of enzymes in the Bulinus tropicus/ truncatus complex (Mollusca: Planorbidae). Journal of Natural History, 15: 873–885. Wright, C.A. & Ross, G.C. 1965. Electrophoretic studies of some planorbid egg proteins. Bulletin of the World Health Organisation, 32:709–712,

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Wright, C.A. & Ross, G.C. 1966. Electrophoretic studies on planorbid egg proteins. The Bulinus africanus and B. forskali species groups. Bulletin of the World Health Organisation, 35:727–731. Wright, C.A., File, S.K. & Ross, G.C. 1966. Studies on the enzyme systems of planorbid snails. Annals of Tropical Medicine and Parasitology, 60:522–525. Wright, C.A., Rollinson, D. & Goll, P.H. 1979. Parasites in Bulinus senegalensis (Mollusca: Planorbidae) and their detection. Parasitology, 79:95–105. Wu, S.K. 1972. Comparative studies on a polyploid series of the African genus Bulinus. Malacological Review, 5:95–163. Wu, S.K. & Burch, J.B. 1975. Bulinus sericinus (Gastropoda: Planorbidae) from Ethiopia. Malacological Review, 8:31–46. Wurzinger, K.H. 1979. Allozymes of Ethiopian Bulinus sericinus and Egyptian B. truncatus. Malacological Review, 12:51–58. Wurzinger, K.H. & Saliba, E.K. 1979. A cytological and electrophoretic comparison of Jordanian Bulinus with three other tetraploid Bulinus populations. Malacological Review, 12:59–65.

Chapter 8. Snail control

Attempts to reduce or eliminate populations of freshwater snails in Africa have been concentrated on the intermediate hosts of schistosomes; the control of Lymnaea has been undertaken in only a few places (see Chapter 6: Fascioliasis). Control measures have been applied experimentally against Lanistes, a herbivore, in rice fields (Crossland, 1965). Less emphasis than in the past is now placed on the chemical control of snails for the purpose of reducing transmission of schistosomiasis, though as a concept snail control is an accepted part of the integrated control strategies that are most likely to succeed (Webbe & Jordan, 1982; Combes & Cheng, 1986; McCullough, 1986, 1992; Mott, 1987a; Thomas, 1987a; Chandiwana & Christensen, 1988; Webbe & El Hak, 1990; World Health Organisation, 1993). The performance of molluscicides has not always been up to expectations and the value of continuing to attempt snail control by chemical means has been questioned (Warren & Mahmoud, 1976). A serious restraint on the use of synthetic molluscicides on a large scale is their high cost in relation to the restricted budgets available for the control of communicable diseases in many countries. There is increasing interest in measures for snail control that are affordable in local community self-help projects, particularly the efficient use of molluscicide in a focal manner, the development of molluscicides of plant origin, and techniques for modifying water-contact sites used by people to make them unfavourable for snails. The importance of snail control should not be overlooked, for despite greatly improved chemotherapy by single-dose oral treatment with praziquantel, there are logistical problems in mass treatment, the threat of re-infection remains (Wilkins, 1989) and vaccination is still a distant prospect (Butterworth, 1992). Measures aimed at controlling transmission of schistosomiasis through reducing snail populations must be thorough to be effective, for a moderate reduction of snail numbers may result in an increased proportion of the remaining snails becoming infected. This follows from the ability of miracidia actively to seek a snail host and is a density-dependent effect demonstrated by mathematical modelling (Woolhouse & Chandiwana, 1990). Snail control measures can be divided into the three following categories: chemical, environmental and biological. Control is attempted most often in

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waterbodies modified or entirely made by man, ranging from various small habitats (e.g. earth dams, small rice-fields, ditches) to large irrigation systems and man-made lakes. Snail populations and schistosome transmission can be greatly reduced solely by chemical means, but the costs of chemicals and skilled labour are recurrent, as the programme needs to be maintained permanently if effective disease control is to be achieved. In some situations the available funds may be better spent on making environmental modifications, so that potential habitats will be unsuitable for snails over the long term; newly constructed irrigation channels and dams can be designed with this aim. Another concept is that of regulating populations of intermediate hosts by biological agents, especially snail competitors. Chemical methods Mollusciciding can be an effective means of reducing snail populations, at least temporarily, and has played an important part in schistosomiasis control, reviewed comprehensively by McCullough (1986, 1992). Since costeffectiveness is greatest where the volume of water to be treated is small in relation to the number of people at risk, mollusciciding is particularly well suited to small seasonal transmission sites in semi-arid areas. Special problems are posed by rivers, man-made lakes, large irrigation schemes and dams. Yet mollusciciding can be effective even in the largest waterbodies, where transmission of schistosomiasis usually is focal rather than widespread (Fenwick, 1987; Klumpp & Chu, 1987). Complete eradication of snails is rarely achieved. Three main reasons are the difficulty of achieving adequate concentration of molluscicide in all the varied niches occupied by snails within a waterbody, the limited persistence of the chemical and the high ability of snails to re-colonise and re-populate the treated areas. After completion of a mollusciciding campaign, snails are likely to reappear and transmission of schistosomiasis will soon be established again unless an efficient programme of chemotherapy has been carried out in the human population, backed up by the provision of effective sanitation and safe water supplies, as well as by education. Development of molluscicides During the last two decades there have been three main trends in studies of molluscicides and their use: to search for compounds with selective toxicity to snails; to improve delivery systems in order to achieve cost-effectiveness and reduce damage to other organisms; to change from area-wide (blanket) application to focal treatment of small sites where active transmission of schistosomes is known to occur.

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Studies of the mode of action of molluscicides have been carried out partly to see whether there are any metabolic pathways, enzymes or systems peculiar to snails that might expose them to specific chemical control (Duncan, 1987). No common mode of action has been evident that might provide a basis for ‘designing’ a new molluscicide; all chemical molluscicides that have been developed to the stage of field study and use have originated from empirical screening methods. One possible approach to finding a specifically molluscicidal substance was suggested by growth inhibition observed in crowded colonies of snails. Berrie & Visser (1963) extracted a toxin, identified as a complex ester, from pond water in which inhibition of growth had been observed in a crowded population of Biomphalaria sudanica. Since the toxicity seemed due partly to surfaceactivity, over one hundred surface-active agents were tested on this snail (Visser, 1964, 1965), but no correlation between surface-activity and toxicity was found. Extensive later experiments provided no good evidence of Biomphalaria populations being regulated by inhibitory substances; depletion of resources and competition among individuals seemed to account for the adverse effects of crowding, and the substance isolated by Berrie & Visser may have originated from a plant (Thomas, 1973; Thomas et al., 1975). Another line of inquiry for a selective molluscicide was stimulated when Mandahl-Barth (1970) suggested that Helisoma duryi secreted some substance(s) that might inhibit the development of eggs and the growth of young Bulinus and Biomphalaria. Early experiments in which water conditioned by Helisoma apparently exerted inhibiting effects on other snails (Abdallah & Nasr, 1973; Malek & Malek, 1978), led to an extensive series of investigations (Madsen, 1992, and references therein), from which it was concluded that there is no evidence for the secretion of inhibiting ‘allelopathic’ factors, and that the inhibiting effects of water conditioned by Helisoma may be due to waste products and/or depletion of essential elements. This explanation could account for the ‘inhibitory compound’ reported to be released by Bulinus tropicus into culture water (Chaudhry & Morgan, 1986a,b; Chaudhry, 1988). Among manufactured products, copper sulphate has long been used for snail control, but it has disadvantages, including adsorption by organic matter and toxicity to other organisms (Webbe & Jordan, 1982; Appleton, 1985). Yet copper sulphate may be useful at limited foci in flowing water, as it is slowly dispersed (Willmott, 1987). In order to find better molluscicides many manufactured substances have been tested (McCullough et al., 1980; Webbe & Jordan, 1982), but only two came into regular use in Africa: N-tritylmorpholine (FresconR, triphenmorph or trifenmorph) and niclosamide (BayluscideR, MollutoxR). Now only niclosamide is widely used and commercially available (McCullough, 1992). Other manufactured products suggested for application in snail control include Ivermectin, a compound used for parasite control in livestock and which has molluscicidal effects (Okafor, 1990). An ingenious means for controlling snails

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might be to remove iron ions from the water by means of a chelating agent, thereby depriving the molluscs of an element needed in their reproductive tissues (Michelson, 1992). The product B-2, PhebrolR (sodium 2,5-dichloro-4bromophenol) showed promise in trials in Africa (Lo & Ayele, 1990; Joubert & Pretorius, 1991), though niclosamide remains the most effective molluscicide available for the control of aquatic snails. Growing concern about possible dangers in the large-scale use of molluscicides prompted a detailed review of the biological properties of niclosamide (Andrews et al., 1983). An estimated 330 000 metric tonnes (costing nearly 6 million US dollars) were used in Middle and Upper Egypt in the year 1984 alone (Willmott, 1987, p. 36). Fortunately, niclosamide is non-toxic to man, and though sufficiently persistent to kill snails effectively, it is degradable by sunlight and micro-organisms. When used at mollusciciding concentrations niclosamide kills fish and amphibians, but does not seem to be a serious threat to the aquatic fauna when applied focally. Plant molluscicides Interest in finding molluscicides derived from locally growing plants has increased in the hope that such substances might be cheaper than synthetic molluscicides and with the aim of involving local communities more closely in schistosomiasis control. The identification of plants with molluscicidal properties, however, is only the first step in a complex process, during which problems of large-scale production and standardisation must be overcome in an economical way if a plant is to be used effectively (Mott, 1987b). More than 1000 plant species, though not all from Africa, have been tested for molluscicidal activity (Kloos & McCullough, 1987; Farnsworth et al., 1987). About 100 products have been isolated, but few satisfy the criteria for large-scale application; saponins from the two African species Swartzia madagascariensis and Phytolacca dodecandra are among the most powerful plant-derived molluscicides and have activities of the same order of magnitude as synthetic products (Hostettmann & Marston, 1987). P. dodecandra is a climbing shrub known by its Ethiopian name of Endod; its berries have provided the most studied plant molluscicide, used in field trials at Adwa in northern Ethiopia (Goll et al., 1983; Lemma et al., 1984). S. madagascariensis is a tree yielding a large crop of saponin-containing fruits; encouraging field trials were carried out at Ifakara in Tanzania (Suter et al., 1986). Additional contributions to those cited by Mott (1987b) include observations in Nigeria of the molluscicidal effects of extracts from the leaves of Alternanthera sessilis by Ndifon & Ukoli (1984) and of the berry of the tree Tetrapleura tetraptera by Adewunmi (1991). In South Africa the bark of the tree Warburgia salutaris yielded a highly effective molluscicide; since this tree grows within the endemic area for schistosomiasis and is already planted for medicinal purposes by rural people, warburganal seems well qualified as a potentially useful plant molluscicide (Appleton et al., 1993).

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For theoretical reasons based on the evolution of interactions between snails and aquatic plants, Thomas (1987b) suggested that molluscicidal factors should be sought in the emergent parts of plants growing in the draw-down areas of waterbodies. Wherever found, and if the practical problems of producing a plant molluscicide in quantity can be overcome, the substance will need testing for toxicity and environmental effects as required for synthetic products. It may be some time before any potentially useful plant molluscicide comes into use. Application of molluscicides Careful consideration has been given to improving the methods of applying molluscicides (McCullough, 1992). Effectiveness can be improved by timing applications to take advantage of seasonal changes in the life cycles of snails and parasites (Shiff et al., 1979; Appleton, 1985; Willmott, 1987; Shehata, 1989). There has been a general change from area-wide application to focal treatment at defined sites where schistosomiasis transmission is known to occur. Active transmission sites can be identified by collecting snails and examining them for infection (Sturrock, 1986) or by detecting cercariae in the water by means of filtration (Théron, 1986). This shift in emphasis arose partly from the need to lower costs and also because area-wide mollusciciding, even though carried out over a period of years, did not always sufficiently reduce snail populations to prevent the annual re-infection of children (Willmott, 1987). Focal application of niclosamide can be effective in the flowing water of streams (Saladin et al., 1983) and large irrigation canals (Madsen et al., 1986); the latter authors stress the importance of giving careful attention to snails living in submerged vegetation and the need for skilled personnel. Management of the water flow is important in the successful use of the chemical, allied to accurate knowledge of the volume being treated. Allowance should be made for water current bringing snails into a treated area from distances over 100 m upstream (Marti & Tanner, 1988; Woolhouse, 1988). Another approach towards the delivery of a minimum effective quantity of molluscicide to precisely where it is needed, is to incorporate the killing agent in controlled slow-release formulations (reviewed by Cardarelli, 1974; Shiff & Evans, 1977; Webbe, 1987). A successful field evaluation of soluble glasses releasing copper compounds was made in Zimbabwe (Chandiwana et al., 1987). There is, unfortunately, still a danger to non-target organisms from long exposure to low concentrations of molluscicides (Appleton, 1985). An interesting possibility is to improve the efficiency of slow-release formulations, and to selectively kill target snails, by adding substances that are specific attractants, arrestants and feeding stimulants. An extensive series of experiments, to detect such substances and explain the mechanisms of chemoreception in snails, was carried out by J.D.Thomas and colleagues, with particular attention to interactions between plants and snails (Thomas, 1982). Some species, including Lymnaea natalensis are attracted particularly by short-chain carboxylic acids,

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whereas Biomphalaria pfeifferi and Bulinus globosus are relatively unresponsive to these substances (Thomas et al., 1983). Octanoic acid was attractive to B. truncatus, but only at high concentration and in a narrow pH range (Thomas et al., 1985). In some situations a mollusciciding programme may greatly reduce snail numbers, but without achieving a proportional reduction in the number of snails shedding schistosome cercariae. Because miracidia actively seek their snail host, continued contamination of a treated site may even result in a higher proportion of infections in the smaller population of snails (Woolhouse & Chandiwana, 1990). Therefore the benefit of snail control needs to be evaluated with knowledge of its actual impact on parasite transmission. Cost-benefit analyses (Jobin, 1979) vary widely for the major schistosomiasis control schemes where mollusciciding has played or still plays an important part. A selection of these schemes (Table 8.1) are reviewed below. Cameroon Schistosomiasis control was attempted in two crater lakes (Duke & Moore, 1976a–c), where N-tritylmorpholine was used to control Bulinus truncatus (=rohlfsi) and B. camerunensis, overcoming the technical difficulty of applying an adequate concentration at the lake bottom by means of an applicator tube 2 m long attached to a pump in a boat. B. truncatus proved the easier species to control and it was practically eradicated from shallow water in both lakes. During two years of post-control observation, however, this snail slowly recolonised the lake margins and low-level transmission resumed. B. camerunensis occurred in Lake Table 8.1. Some major schistosomiasis control programmes where mollusciciding played an important part. Locality

Snail host(s)

Author(s)

Cameroon: lakes Barombi Kotto and Barombi Mbo

Bulinus truncatus (=rohlfsi) Bu. camerunensis Bu. senegalensis Bu. truncatus (=rohlfsi) Biomphalaria alexandrina Bu. truncatus Bi. alexandrina Bu. truncatus Bi. pfeifferi Bu. africanus group Bu. obtusispira

Duke & Moore (1976) Moyou et al. (1984)

Willmott (1987) Webbe & El Hak (1990) Highton & Choudhry (1974) Degrémont (1973)

Bi. pfeifferi Bulinus spp.

Appleton (1985)

Gambia Ghana: Lake Volta Egypt: Nile Delta Egypt: Middle and Upper Kenya: irrigation projects Madagascar: Mangoky River South Africa: Transvaal

Goll et al. (1984) Scott et al. (1982) Gilles et al. (1973)

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Locality

Snail host(s)

Author(s)

Sudan: Gezira

Bi. pfeifferi Bu. truncatus

Tanzania: Arusha Chini Tanzania: Misungwi

Bi. pfeifferi Bu. nasutus

Tunisia Zimbabwe: Hippo ValleyTriangle Area

Bu. truncatus Bi. pfeifferi Bu. globosus

Amin et al. (1982) Daffalla & Fenwick (1982) Gaddal (1985) Fenwick (1972a,b) McCullough et al., (1968, 1972) Rey et al. (1982) Evans (1983)

Barombi Kotto and was more difficult to control, because of its comparatively short generation time and higher reproductive potential. The interval between molluscicide applications was reduced from 6 to 4 weeks and then to 3 weeks, but sufficient snails remained to continue transmission of S. haematobium by acquiring infection from viable eggs still being excreted by people despite the chemotherapy programme. Transmission was checked only when the snail population was reduced to a very low level, as the result of applying molluscicide every two weeks. After mollusciciding ceased, B. camerunensis rapidly re-established its population. Duke & Moore (1976c) concluded that to reach the break-point in transmission would have required practically total eradication of the snails, and that the high cost (nearly US 10 dollars per protected person per annum) ‘is only likely to be acceptable where schistosomiasis causes much ill health and reduced economic activity’. Ten years after this control programme ended, the prevalence of infection in Barombi Kotto had recovered to 76% (Moyou et al., 1984). Egypt More money has been spent on the use of molluscicides in Egypt than in any other African country and perhaps even in all other African countries combined. During the Egypt-49 Project in the Nile Delta, area-wide applications of molluscicides (mainly niclosamide) were made to canals and drains from 1963– 70. A follow-up assessment, however, showed that transmission of S. haematobium had not been satisfactorily interrupted (Gilles et al., 1973); one reason appeared to be that molluscicide application had not been concentrated during the main transmission season (July–September). Schistosomiasis control by means of chemotherapy and mollusciciding in Middle and Upper Egypt was first evaluated in 1984–85 (Willmott, 1987) and later using data extending into 1989 (Webbe & El Hak, 1990). By 1984 the prevalence of S. haematobium had been reduced from 30% to about 8.5%, and it was recommended that area-wide mollusciciding should be replaced with more cost-effective focal mollusciciding, to be concentrated on water-contact sites

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where infected snails were found. Evidence of annual re-infections in children implied that area-wide snail control measures had not adequately limited cercarial transmission in some areas. Efforts were made to apply focal mollusciciding, but transmission of infection continued (Webbe & El Hak, 1990), apparently because of defects in the coverage of both chemotherapy treatment and application of molluscicide, due to lack of logistic resources. More frequent chemotherapy treatments and complementary focal mollusciciding were recommended to maintain and improve the control of S. haematobium in Middle and Upper Egypt. Gambia Transmission of S. haematobium by Bulinus senegalensis was interrupted for a period of three years by applying niclosamide to seasonal rainwater pools (Goll et al., 1984). Snail populations were reduced progressively to about 1% of the numbers in untreated pools, and practically no new infections were acquired by children during the period of intervention. In the year after mollusciciding ended, snail populations rapidly reached levels approaching those in untreated pools, and the authors emphasised that in the absence of eradication, which would be virtually unattainable, the cost of snail control would be a recurrent expense. Ghana The value of focal mollusciciding at known transmission sites, according to careful observation of human water-contact behaviour, is well demonstrated by the WHO Schistosomiasis Research Project established to study epidemiology in the area of the man-made Volta Lake (Scott et al., 1982). S. haematobium infection was generally light in people living in the part of the Volta Basin to be flooded, but by 4 years after closure of the Volta Dam, prevalence was 90% in the children of some settlements along the new lake shoreline. In 1973–74 it was practically impossible to find an uninfected person in the Afram and Pawmpawm branches. The intermediate host is B. truncatus (=rohlfsi); other species of Bulinus and also Biomphalaria were uncommon in the new lake. Dense snail populations were associated with luxuriant growths of the submerged plant Ceratophyllum demersum, possibly because its stiff leaves protect snails and their eggs from predators (Odei, 1973). The main transmission season occurs when the water level is high and there is a dense stand of marginal vegetation, mainly Polygonum and grasses. During this period, human water-contact is concentrated in pocket-shaped clearings in the marginal vegetation, and large snail populations develop in the submerged Ceratophyllum growing in clear water within the pockets (Klumpp & Chu, 1980; Chu et al., 1981). During the period of low water, open beaches are exposed and water-contact by people is dispersed; some transmission still occurs, but mainly where beds of Ceratophyllum are growing offshore.

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Control was attempted by a 3-year programme of focal application of niclosamide at water-contact points, accompanied by removal of Ceratophyllum and selective chemotherapy. The effectiveness of mollusciciding the pockets and bays was improved by using a plastic curtain to screen treated water from the open lake. Prevalence was reduced by 72% in the area of low endemicity and by 40% in an area of high endemicity, while intensity of infection (measured by number of eggs passed in urine) was reduced by about 78% in both areas. Population movements prevented precise measurements of incidence of new infections. It was concluded (Chu et al., 1981) that these methods were not sufficient to stop transmission, though they gave good results in short-term control of the intensity of infection; permanent control would require the virtual eradication of schistosomiasis in a wide zone along the lake shore. Kenya Snail populations in irrigated estates (200–4600 ha) were greatly reduced or eliminated by molluscicides; no systematic data were obtained on schistosomiasis transmission, though the costs of mollusciciding were carefully assessed and compared favourably with those at Arusha Chini in Tanzania (Highton & Choudhry, 1974). Madagascar Operations to control Bulinus in the lower Mangoky River irrigation project (the initial 2000 ha out of a planned 40 000 ha) were complicated by extensive seepage areas that provided important snail habitats (Degrémont, 1973). The addition of urea to the applications of N-tritylmorpholine increased the adverse effect upon snails, apparently by encouraging growth of plankton and thereby reducing oxygen tension in the water (Perret et al., 1972). However, the nitrogen in the urea also promoted growth of waterplants that hampered application of the chemicals. Dense vegetation was generally a serious obstacle to spraying and extensive clearing work was necessary. Degrémont concluded (1973, pp. 148, 153) that snail control was efficient, but at such cost that ‘similar actions would only be economic if limited in time and space, and if they resulted in total interruption of transmission’. South Africa Trials with molluscicides in the Transvaal over some two-and-a-half decades from 1950 seldom achieved satisfactory control of snails (Appleton, 1985). Extensive experience was gained in the use of several molluscicides, particularly copper sulphate and niclosamide, in natural watercourses and irrigation channels. Considerable reductions in prevalence of schistosomiasis were observed in some

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areas, but mollusciciding was abandoned, partly because of its cost, in favour of environmental control, mainly by preventing human water-contact. Sudan The Gezira-Managil Scheme is one of the largest irrigation projects in Africa and has a long history of snail control. Area-wide aerial application of Ntritylmorpholine over about 80 000 ha in 1974–77 reduced snail populations to about 1–5% of their normal levels, yet there was no significant reduction in incidence of S. mansoni infections in people living in the treated area compared with the adjacent untreated area (Amin & Fenwick, 1977; Amin et al., 1982). There were two reasons for this failure (Fenwick, 1987). First, the molluscicide was not stable enough to penetrate down the canal network to kill snails at the ends of canals. Secondly, the prevalence of schistosomiasis was so high from the outset that it was not possible, in the absence of chemotherapy, to reduce the snail population low enough to break transmission. Further surveys of children in 1981 showed that S. mansoni had recovered to a higher prevalence than before control operations began, while prevalence of S. haematobium had increased from less than 1% to 75%; the abandoned intervention might have contributed in some way to this worsened situation (Daffalla & Fenwick, 1982). In the Blue Nile Health Project started in 1979, mollusciciding formed part of an integrated strategy for schistosomiasis control in the Gezira-Managil area and the newer Rahad Scheme (Gaddal, 1985). Chemotherapy and mollusciciding began in 1982–83 in the Gezira-Managil area; from the start niclosamide was applied focally at water-contact sites, as transmission of schistosomiasis in this area is highly focal as well as seasonal (Babiker, Blankespoor et al., 1985; Babiker, Fenwick et al., 1985). The aim in the Rahad area was to prevent host snails from becoming established and all snail populations found were treated. Within the initial study area in Gezira prevalence of schistosomiasis had fallen from over 50% to the target of 10% by mid-1983, and water-contact sites appeared free of snails (Gaddal, 1985). Although mollusciciding seems to have played a part in this success, later control strategies attempted to reduce dependence on chemical control of snails by developing methods for biological and environmental control. Tanzania: Arusha Chini Mollusciciding and chemotherapy were used to control S. mansoni in an irrigated estate of about 4000 ha at Arusha Chini (Fenwick, 1972a,b). Application of Ntritylmorpholine practically eliminated B. pfeifferi from the irrigation channels and it was estimated that the snail population was held below 0.1% of its original size. There appeared to be a complete cessation of new infection of young children. This was attributed mainly to the snail control programme rather than to chemotherapy, which had been administered before the beginning of snail control

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without any evident effect on transmission. Cost-benefit analysis justified continuation of the snail control programme, in view of costs that might be saved on chemotherapy. Tanzania: Misungwi Project An experimental project in an area of 100 km2 near Mwanza was begun in 1968 to compare the effects on prevalence of S. haematobium of: 1) mollusciciding with niclosamide; 2) mollusciciding and chemotherapy; 3) no intervention, and 4) chemotherapy alone. The most favourable habitats for Bulinus nasutus, the principal intermediate host, were furrows, bunded rice fields and seepages, though dams and ponds were important transmission sites (McCullough et al., 1968, 1972). Post-control evaluation showed that the combined programme was superior to either single factor programme in reducing prevalence of schistosomiasis, though it was not possible to compare precisely the costs of mollusciciding and chemotherapy (Jobin, 1979). Tunisia Bulinus truncatus was eliminated from nearly 200 sites in the Saharan and subSaharan area of southern Tunisia during 1972–79, by application of niclosamide (Rey et al., 1982). Chemotherapy was carried out concurrently, and the transmission of urinary schistosomiasis was halted. No new human infection has been reported since 1982, and surveillance is permanently maintained in order to prevent re-establishment of the snail host (World Health Organisation, 1993). The success of this control programme can be attributed in part to the circumscribed nature of the aquatic habitats, some being oases, and the low chance of snails being reintroduced from the arid neighbouring areas. Zimbabwe Successful schistosomiasis control through mollusciciding was achieved in an irrigated area of 38 000 ha in the Hippo Valley-Triangle area (Shiff et al., 1973; Evans, 1983). Systematic chemotherapy was considered to be impracticable because of the instability of the human population, due to high labour turnover, mobility of dependants and influx of refugees from war-torn Mozambique. Niclosamide was focally applied according to the numbers of snails found during regular monitoring of channels and dams. During a 9-year control period (1971– 1980) there was a substantial reduction in snail numbers and sites infested, and the mollusciciding became increasingly focused, so reducing the quantity of chemical used. A particularly effective technique was ‘dam-and-flush’; streams and drains were dammed at bridges using a metal plate, then the impounded water was heavily treated, left for two hours and then released to flush the watercourse. Once this technique was in regular use no new infections with S.

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mansoni or S. haematobium were acquired by children within the control area. The continuing moderate prevalence in children (about 40% for S. haematobium and 20% for S. mansoni) seems to have been due to infections acquired elsewhere. The costs of this snail control programme compared well with other schemes; it was concluded that because of the instability of the human population and the ease of re-colonisation by snails, mollusciciding was indispensable for control of schistosomiasis transmission. Resistance to molluscicides Snail control operations are not known to have been hampered by any resistance to molluscicides and it seems unlikely that this will ever attain the importance of resistance to insecticides (McCullough et al., 1980; Duncan, 1987). It is, however, desirable to monitor snail populations for resistance and a field test kit has been devised (Duncan & Brown, 1988). Another technique for testing genetically-based variation for resistance is described by Lam et al. (1989), who found evidence for variation in response among individuals of Biomphalaria glabrata to a molluscicide of plant origin. B. truncatus collected from an area in Iran that had been treated with niclosamide for about 10 years appeared to be more tolerant of the chemical than a laboratory stock of this snail that originated from the same area before molluscicide was applied (Jelnes, 1977). Increased tolerance resulted from selection of snails which had survived exposure to molluscicide over a sequence of 5 generations (Jelnes, 1987). A small but statistically significant difference was observed (Daffalla & Duncan, 1979) in susceptibility to N-tritylmorpholine between two collections of B. truncatus from the Gezira region of Sudan, one from an untreated area and one from an area treated for 6 years. No difference, however, in response to niclosamide was shown by B. senegalensis from pools after three years of treatment in comparison with snails from untreated pools (Goll et al., 1984). Environmental control Much has been written about the theory and practice of modifying man-made and natural waterbodies so as to reduce or eliminate snail populations (Jordan & Webbe, 1982). Considerable success has been achieved in reducing habitats for Oncomelania, the amphibious intermediate host for Schistosoma japonicum in the Far East, but such methods have not been applied to a great extent in Africa, where the snail hosts are truly aquatic. Environmental factors which influence snail distribution and which might be manipulated to achieve snail control in Africa were suggested by Thomas & Tait (1984): light, water chemistry (especially oxygen tension), water flow, sediment type, seasonal drying, aquatic and subaquatic plants, other snail species (especially Melanoides tuberculata, considered here under ‘Biological control’). Field observations in the Ibadan area, Nigeria, led Thomas & Tait to emphasise

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the focality of persistent snail habitats with favourable aquatic vegetation, and the importance of these refugia in providing colonists to replenish populations in less favourable habitats. Measures to eliminate such refugia were discussed, including drainage and canalisation of the source areas of streams, dredging and straightening lower watercourses, and removal of favourable vegetation from the water and stream-banks. For standing waterbodies the control measures suggested were removal or control of vegetation and the management of fish ponds as ecosystems lacking macrophytes. However, proposals for interfering with natural watercourses by engineering should be treated with great caution. The likely consequences of removing vegetation and increasing rate of flow in streams are soil erosion and flooding, producing environmental damage which could outweigh any reduction achieved in transmission of schistosomiasis. Another reason for caution in modifying watercourses by engineering or clearance of vegetation is the weakness in the biological justification put forward for such proposals. For example, contrary to reports cited by Thomas & Tait (1984) that shade is favourable to freshwater snails, there is evidence from laboratory experiments and from field observations that shade is unfavourable to Biomphalaria species (Loreau & Baluku, 1991); see also Chapter 10: Light and shade. The suggestion that B. pfeifferi might be controlled through shade provided by reafforestation of streamsides (Baluku et al., 1989) is in accordance with the view put forward earlier by Jackson (1965), that it serves the purpose of schistosomiasis control to protect the indigenous bushes and trees which grow thickly beside undisturbed streams. Many schistosomiasis transmission sites are man-made and may be more amenable to modification than natural waterbodies. Especially in urban areas numerous snail habitats are created by careless engineering and general construction activities. These small waterbodies include seepages, borrow-pits and pools in quarries, and could easily be eliminated by infilling, though often they are important sources of water for local people. Simple modifications in the construction of small dams could reduce contact by people with surface water infested by cercariae (Brinkmann & Steingruber, 1986). Snail control can be associated with the efficient management of irrigation schemes, for the removal of aquatic vegetation promotes free flow of water and also removes shelter and food sources for snails, while the prevention of seepage eliminates marshy habitats in which snail hosts can thrive. Bulinus abyssinicus was unable to colonise canals that were fast-flowing, lacked plants and dried out for long periods, though the snails were present nearby in standing waters (Upatham et al., 1981). Weed control is, however, costly and plants speedily recover, with only a small effect on snail populations (Hilali et al., 1985). The grass carp Ctenopharyngodon idella proved to be the most effective means for aquatic plant control and reducing snail populations in Egyptian canals (Van Schayck, 1986). Periodic drying out of irrigation canals reduces snail populations, but the intermediate hosts for schistosomes can survive for several weeks in drying mud

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and populations remain in small residual pools associated with structures such as siphons and sluice gates. Efforts are under way, particularly in Zimbabwe, to make irrigation systems unfavourable for snails by modifications in design and operation (Bolton, 1988). Principal aims are the creation of a high rate of flow in channels, fluctuation of water level in storage reservoirs and periodic drying of the system. To these ends, use is made of concrete lining, modification of weirs and off-take structures, and careful scheduling of water release. Such measures contributed to the control of schistosomiasis in newly established smallholder irrigation schemes (Chandiwana et al., 1988). Snail populations were rapidly reduced and apparently eliminated by modifying the flow regime of a river in Tanzania (Fritsch, 1993). Under natural conditions Biomphalaria pfeifferi and Bulinus globosus were abundant during the dry season, when water was almost stagnant, but these populations were greatly reduced by the floods of the rainy season. A weir was constructed to impound the low river discharge during the dry season, and this water was released as a flood or ‘flushing wave’, repeated several times at intervals of up to 12 days. The impressive success of this operation in dislodging snails appeared to depend mainly on the generation of turbulent flow and brief periods of high shear stress, particularly in the transition zone between the bankside vegetation and the river bed sediments, the area where most of the snails were living. Biological control Biological methods for the control of freshwater snails were ably reviewed by Madsen (1990, 1992), who concluded that more emphasis should be put on searching for pathogens or microparasites as agents for control. Biological control is still largely at the experimental stage and so far most attention has been given to trematode parasites, predators and competitors. The most promising approach is the use of suitable snails, which are not compatible hosts for schistosomes of medical or veterinary importance, as competitors of the intermediate hosts. Genetic manipulation has been considered as a means for altering the compatibility between a snail population and its schistosome parasites. Pathogens and parasites Fungi, protozoa and bacteria have all been reported, mostly without precise identification, to produce adverse effects in species of Bulinus and Biomphalaria (publications reviewed by Madsen, 1990), but there has been little systematic screening of micro-organisms. Infection with schistosomes and other trematode parasites can be harmful to the snail host (see Chapter 5: Resistance in the snail host, and Chapter 7: Parasite burden) and one kind of trematode may be antagonistic towards another. The idea of utilising these interactions for the control of African schistosomiasis has

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been familiar for at least 40 years (Bayer, 1954). Particular attention has been given to trematode species belonging to the Echinostomatidae that may castrate the snail host and severely disturb the development of any schistosome larvae present (Rysavy et al., 1973, 1974; Combes, 1982; Mouahid & Moné, 1990). The only feasible stage for introducing a trematode into the field appears to be the egg; all field trials so far reported have been carried out in the Far East and in the French West Indies. Combes (1982) gave a list of trematode species as candidate control agents and reviewed 6 requirements for a suitable species: complete and permanent sterilizing effect; clear dominance over target trematodes; strong infectivity to molluscs of all ages; high egg productivity in the definitive host; lack of pathenogenicity towards man and domestic animals; ease and low cost of maintenance of the life-cycle. However, there is little evidence that trematode parasites provide a practical means for controlling snail hosts of schistosomes. Predators The predators considered here actively seek their prey; the eggs and young of freshwater snails may be sometimes ingested by the same or a different species of snail, but apparently as an incidental part of the diet, and all snails evaluated as agents for biological control are considered in the next section, as competitors. A predator may also be a competitor, e.g. the crayfish Procambarus clarkii eats snails and also the water plants that support them (Hofkin, Mkoji et al., 1991). Of interest, though without practical application, is an African bird, the Open-billed Stork, Anastomus lamelligerus, with its gaping bill adapted for holding large prosobranchs and bivalves. Many African species of fish feed to a greater or lesser degree on molluscs (Slootweg, Malek & McCullough, 1993). In Lake Victoria alone, 4 species of non-cichlid fishes and about 12 species of Cichlidae are molluscivorous (Corbet, 1961; Greenwood, 1974). Some cichlids have modified teeth for extracting the snail’s body from its shell or the whole animal may be crushed in a pharyngeal mill. In Lake Malawi too, certain species of cichlid are exclusively molluscivorous and this predation seems of importance in determining the behaviour and distribution of snails (Louda et al., 1984; McKaye et al., 1986). A population of the cichlid genus Saratherodon living in a spring-pool studied by Campbell (1981) was predatory upon snails, an unusual diet for this genus, and he made the interesting suggestion that the habit may be learned by one fish from another. The importance of group behaviour in snail-eating by fishes was demonstrated by Chiotha et al. (1991) for another cichlid, Trematocranus placodon, from Lake Malawi.

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Experiments by Acra et al. (1986) showed that Gambusia affinis, the fish widely used to control mosquito larvae, was an effective predator of juvenile Bulinus truncatus in the laboratory. Other species of fish have been assessed as predators of snails in outdoor situations such as small dams, fish ponds and artificial channels, e.g. in south-eastern Zaire (De Bont & De Bont Hers, 1952; De Bont, 1956), Cameroon (Bard & Mvogo, 1963; Mvogo & Bard, 1964; Slootweg, Vroeg & Wiersma, 1993), Kenya (MacMahon et al., 1977; Kat & Kibberenge, 1990) and Sudan (Daffalla et al., 1985). Particular attention has been given to the molluscivorous cichlid Astatoreochromis alluaudi, which was introduced about 30 years ago into small dams in western Kenya, resulting initially in a reduced snail population (MacMahon et al., 1977). But a follow-up study in 1986–87 (Kat & Kibberenge, 1990) showed that Bulinus and Biomphalaria persisted in dams with A. alluaudi; these populations were only in a few cases significantly lower than in dams lacking this fish, and they were actually higher at some sites with fish. From this study two main causes emerged for the inability of A. alluaudi to reduce snail populations significantly: first, the presence of refuges at the dam margins (within dense stands of vegetation in shallow water) and around dams (associated small pools and streams), where snails were accessible only to fishes too small to eat them, and secondly, the tendency of A. alluaudi towards a general diet, indicated by analysis of stomach contents. In another recent study (Slootweg Vroeg & Wiersma, 1993) no significant reduction in numbers of Bulinus truncatus and B. forskalii resulted from introducing this fish into ponds in North Cameroon. The early optimism that A. alluaudi would control snail populations arose from the diet of adult fish in Lake Victoria, where the hard-shelled prosobranch snail Melanoides tuberculata is a major food item. But snail-eating by this fish is not obligatory (Kat & Kibberenge, 1990; Witte et al., 1990, and references therein). The strongly developed pharyngeal jaw apparatus (PJA) is developed by young fish when about 40 mm long, if they change from a soft diet mainly of insects to one mainly of hard-shelled snails. Growing fish that continue with a soft diet do not develop a strong PJA. The more easily eaten soft food items may be preferred, but competition from other species in Lake Victoria is believed to encourage young A. alluaudi to switch to a diet of snails. In small habitats such as dams and fishponds the fish seems to find soft food in such quantity that molluscs form only a small part of the diet and the PJA remains weak. If these insights into the feeding biology of A. alluaudi are true of other molluscivorous cichlids then not much can be expected of them as a means for controlling snails. The best known invertebrates that are exclusively predators of freshwater snails are leeches of the family Glossiphoniidae and the larvae of flies belonging to the family Sciomyzidae (Greathead, 1980, and other publications cited by Madsen, 1992). Snail-eating by leeches has been little studied in Africa, apart from observations by Wilken & Appleton (1991) of avoidance responses by 4 species of snail towards Helobdella conifera. Alboglossiphonia polypompholyx is a parasite rather than a predator of Bulinus truncatus in Egypt (El-Shimy &

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Davies, 1991). Larvae of the sciomyzid fly Sepedon scapularis were effective predators of Bulinus and Physa in experiments in South Africa (Maharaj et al., 1992). Another apparently obligatory molluscivore is the large water-bug Limnogeton fieberi (Hemiptera, Belostomatidae); individuals reared from the egg in the laboratory consumed a daily average of 2.7 snails over a period of 40–50 days (Voelker, 1968). Freshwater snails form part of the diet, to a greater or lesser degree, for many different kinds of invertebrate. It is not unusual in Africa to find snails being attacked by the aquatic larva of the beetle family Lampyridae (which includes the ‘glow-worms’). Lampyrid larvae collected in Liberia were capable of consuming about one individual of Bulinus and Biomphalaria a day (Sodeman et al., 1980). Other predators include Ostracoda (Deschiens et al., 1953; Lo, 1967; Matovu, 1974), the larvae of Odonata (Lagrange, 1956), crabs and crayfish. Freshwater crabs are common in Africa and some species have long been known to be molluscivorous (Deschiens et al., 1955). In Lake Tanganyika there appears to have been co-evolution between predatory crabs and the endemic prosobranch snails, which have developed thick-walled shells resistant to crushing (West & Cohen, 1991); predation pressure from crabs could also explain the general rarity of the comparatively thin-shelled pulmonate snails on the open shores of Lake Tanganyika. Crayfish (Crustacea) are not native to tropical Africa, but by the 1970s the Louisiana Red Swamp Crayfish, Procambarus clarkii, had become wellestablished in central Kenya and was abundant in Lake Naivasha, as a result of deliberate introduction in 1970 (Parker, 1974; Lowery & Mendes, 1977; Harper et al., 1990). One effect of this alien species, in conjunction with other ecological factors (Chapter 12, Lake Naivasha), was a marked change in the molluscan fauna, with the apparent disappearance of Biomphalaria and Bulinus, which were not found in 1983–84 (Clark et al., 1989). The possibility of using crayfish for the control of freshwater snails had been suggested earlier, following the observation that crayfish in aquaria ate snails including Biomphalaria and Bulinus (Deschiens & Lamy, 1955). P. clarkii is partly molluscivorous (waterlilies are also eaten readily) in the laboratory and in natural habitats in Kenya (Harper et al., 1990; Hofkin et al., 1991). A survey of 53 habitats showed a strong negative association between snails and P. clarkii, suggesting that intermediate hosts for schistosomes may be controlled and/or eliminated by crayfish predation (Hofkin et al., 1991). This crayfish has, however, serious disadvantages for use as means for biological control; it is known to eat rice seedlings, to adversely affect freshwater fisheries and to undermine earth banks by burrowing. The prospect of major damage to the aquatic environment led Van Eeden et al. (1983) to urge great caution when contemplating the introduction of P. clarkii into South African waters. Experiments with a crayfish indigenous to Madagascar indicated that it is not an effective predator of snails (Breuil et al., 1983).

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Competitors The various aspects of the biological control of freshwater snails by using competitors, including principles, experimental data and practical applications, are described in the outstanding review by Madsen (1992). A competitor affects the target species through competition for resources, though it may also be a predator, e.g. the snail Marisa cornuarietis which eats snails as well as water plants. A number of freshwater snails have been suggested as potential biological control agents of African intermediate hosts for schistosomes, on the basis of laboratory experiments and/or observations in the field (Table 8.2). Most of these may be dealt with briefly before we examine Helisoma duryi, for which the available data are by far the most extensive. Potamopyrgus jenkinsi First noted on the Mediterranean island of Corsica in 1961, this snail had colonised most waterbodies there by 1973 (Léger & Léger, 1974). During this invasion a number of local snails, especially Bulinus truncatus, became much less common (Doby et al., 1966a,b). In 1980 two types of habitat were distinguishable, those in which P. jenkinsi was very abundant and B. truncatus was not found, and others in which both species were present and apparently in equilibrium (Albaret et al., 1981). Marisa cornuarietis Effective control of Biomphalaria by this large prosobranch (growing to over 50 mm in diameter), which is native to South America, was demonstrated in Puerto Rico (World Health Organisation, 1982), and it has been used in small-scale field trials in Africa. Purposeful predation on Biomphalaria and Bulinus occurred in experiments performed in Egypt (Demian & Lufty, 1965a,b, 1966) and Tanzania (Msangi & Kihauli, 1972). Predatory activity is higher for sexually mature females than males (Cedeño-Léon & Thomas, 1983). Marisa also Table 8.2. Snail species discussed as competitors or predators of intermediate hosts for schistosomes in Africa. Snail species

Recent reference(s)

PROSOBRANCHIA Hydrobiidae Potamopyrgus jenkinsi Ampullariidae Marisa cornuarietis

Albaret et al. (1981)

Pila ovata

World Health Organisation (1982) Madsen (1992) Stryker et al. (1991) Hofkin et al. (1991)

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Snail species Lanistes carinatus Saulea vitrea Thiaridae Melanoides tuberculata

Melanopsis praemorsa PULMONATA Physidae Physa acuta Planorbidae Bulinus tropicus Helisoma duryi

Recent reference(s) Stryker et al. (1991) Karoum & Madsen (1989) Stryker et al. (1991) White et al. (1989) Thomas & Tait (1984) Madsen et al. (1988) Mkoji et al. (1992) Dupouy et al. (1980)

El-Hassan (1974) Hairston et al. (1975) Joubert & De Kock (1989, 1990) Madsen (1992)

readily eats vegetable food and any attached egg capsules or young snails. The ability of M. cornuarietis to regulate populations of Biomphalaria glabrata by predation was matched by Pila ovata and Lanistes carinatus under some conditions in the laboratory (Hofkin et al., 1991; Stryker et al., 1991). Reduction or elimination of pulmonate snails was seen in field trials carried out in ditches in Egypt (Demian & Kamel, 1972), a permanent dam in Tanzania (Nguma et al., 1982) and irrigation canals in Sudan (Karoum & Madsen, 1989). Marisa survived in a temporary pond through a dry season of about 15 weeks (Msangi & Kihaule, 1972), but populations failed if introduced into habitats in the Sudan which dried out, and introduction was successful only in permanent ponds and canals (Haridi et al., 1985). Although resistant to infection with Schistosoma spp., M. cornuarietis may serve as a decoy for schistosome miracidia, though there is no evidence of penetration (Combes & Moné, 1987). Although Marisa may destroy young rice plants when no other food is available, the snail probably would not be a threat in rice paddies, since other food sources are abundant (Madsen, 1992). Calculations on population dynamics indicated that the snail would not be able to establish significant populations in rice fields in the Nile Valley as the flooded periods are too short (Haridi & Jobin, 1985). Pila ovata This snail was generally a more efficient predator of Biomphalaria glabrata eggs and juveniles than were M. cornuarietis and Lanistes carinatus under laboratory conditions (Hofkin et al., 1991; Stryker et al., 1991). It was concluded

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that P. ovata, being an indigenous African species, should be given preference over the alien M. cornuarietis as a biocontrol agent. Lanistes carinatus Reports of this snail having a negative affect on the occurrence of Bulinus and Biomphalaria in the Gezira Irrigated Area of the Sudan were not confirmed by later study (Madsen et al., 1988). Introduction of L. carinatus into canals where it was not previously found had no clear impact on the intermediate hosts, during a two year period (Karoum & Madsen, 1989). From laboratory observations it appeared that L. carinatus has relatively little potential as an effective biocontrol agent in Kenya (Stryker et al., 1991). Saulea vitrea In waterbodies where this prosobranch occurred in Sierra Leone, no intermediate hosts for schistosomes were found, and the prosobranch ate the eggs and adults of intermediate hosts in the laboratory, suggesting potentiality for biological control (White et al., 1989). Further observations in areas where this species is endemic are desirable. Melanoides tuberculata Observations made on dense populations of this snail led Thomas & Tait (1984) to suggest that it might exclude other species from eroding substrates in flowing water. The introduction of M. tuberculata into watercress beds on Martinique, French West Indies, was followed by the disappearance of Biomphalaria (Pointier et al., 1989), but no evidence was obtained by Madsen et al. (1988) in the Sudan for any negative effect of this prosobranch on intermediate hosts in irrigation canals. It is in permanent and stable habitats that competition from M. tuberculata should be strongest, according to its population dynamics in the laboratory (Pointier et al., 1991). In Kenya it co-exists with pulmonates (Mkoji et al., 1992). Melanopsis praemorsa In some areas of Algeria the distribution of Bulinus truncatus appeared to be limited by M. praemorsa, which occurred at very high densities in streams (Dupouy et al., 1980). Snails identified as M. dufouri (=praemorsa) progressively replaced B. truncatus in irrigation canals in some Algerian oases (Dupouy, 1979; Dupouy et al., 1980).

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Physa acuta Although P. acuta has been considered as a competitor (El-Hassan, 1974), physid snails often co-exist with Biomphalaria and/or Bulinus in Africa (Wright, 1968; Hamilton-Atwell et al., 1970; Thomas & Tait, 1984). Although dense populations of Physa may be found where other freshwater snails are lacking, such sites are, in my experience, often polluted to an extent that would be unfavourable to other species, whether or not Physa were present. Bulinus tropicus The introduction of a diploid form of Bulinus resistant to infection by schistosomes might serve as a means for biological control, especially in newly-made waterbodies, of an intermediate host such as B. truncatus (Brown & Burch, 1967; Brown & Wright, 1972). In Zimbabwe the introduction of B. tropicus into a stream was followed by the disappearance of B. globosus, though only temporarily (Hairston et al., 1975). It now appears less likely that B. tropicus could be a successful competitor of B. truncatus, at least the aphallic form, as aphally may be associated with superior reproductive fitness (Jarne et al., 1992). Helisoma duryi The major input to the extensive studies made of H. duryi as a biocontrol agent has been made by H.Madsen and colleagues at the Danish Bilharziasis Laboratory, initiated by G.Mandahl-Barth in 1941–42 (Frandsen & Madsen, 1979). There is a large literature; Madsen and co-workers have contributed over 25 relevant publications and the present account is based on the review by Madsen (1992). Laboratory experiments show that competition from H. duryi results in reduced growth and reproduction for a number of species of Biomphalaria and Bulinus. H. duryi does not secrete any inhibiting factor, though water conditioned by this snail does have negative effects, which may be due to waste products or depletion of essential elements. An important part is played by food competition and interference competition; the latter includes physical contact causing ‘stress’ to other snails and both incidental and deliberate predation of their eggs and young. Life-tables for H. duryi and Bulinus africanus maintained either together or separately showed that H. duryi had the higher capacity for growth and increase in population, and these measures for B. africanus were reduced in the presence of H. duryi (Joubert & De Kock, 1989). Similar experiments using H. duryi and Biomphalaria pfeifferi showed the former to increase in numbers more rapidly than the latter when they were separate, but B. pfeifferi was not adversely affected by the presence of H. duryi. In nature, however, under conditions of limited food supply, the more rapidly increasing H. duryi might be an effective competitor (Joubert & De Kock, 1990).

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H. duryi has been established for many years in some small artificial waterbodies in Africa, especially ornamental ponds, but it usually has not spread into more natural habitats, for reasons which are not understood. In laboratory trials H. duryi performed as well or better than Biomphalaria and Bulinus in response to most of the environmental variables tested (Madsen, 1992). Field trials made in Tanzania, Sudan and Saudi Arabia showed that introduced H. duryi were effective in reducing populations of intermediate host snails under certain conditions, though low temperature and unstable water conditions were unfavourable to the alien snail. Careful supervision and repeated introductions were necessary; these requirements could present practical difficulties. Since snail host populations usually undergo great seasonal fluctuations in density, the factors responsible would presumably also affect H. duryi; careful monitoring of its populations would therefore normally be required. A technical problem that could arise is the difficulty of separating Biomphalaria from a form of H. duryi that has a closely similar shell and is safely identifiable only through dissection (Prentice et al., 1977; Madsen, 1984). H. duryi is, however, well suited as a biocontrol agent as it is resistant to infection by schistosomes and unlikely to damage rice plants; it can be produced in large numbers by simple methods and is transported easily. Madsen (1992) concludes that neither H. duryi nor any other competitor is likely to be able to control intermediate hosts for schistosomes under all conditions. Success will depend on determining the characteristics of habitats most amenable to application of biological control, and the development of optimal procedures for breeding, introducing and maintaining the competitor. There may be potential for local community participation, once standard procedures are developed. Genetic manipulation The finding that compatibility with schistosomes can vary genetically within a snail species has raised the possibility of controlling parasite transmission by introducing snails with a resistant genotype into compatible conspecific populations (Woodruff, 1985). The feasibility of such introductions would depend partly on the status of any reproductive isolation between the two populations and the contribution (or cost) of resistance to individual fitness (Njiokou et al., 1992). Search for a resistant genotype yielded one population of ‘B. africanus’ that was partially resistant (Joubert et al., 1991), but this population could have been of a species different from the other populations tested (possibly B. globosus, see under that species in Chapter 7). Prospects for snail control Snail control has a future as one among several methods that should all play a part in controlling the transmission of schistosomes; others will be directed

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towards reducing input of schistosome eggs into snail habitats and minimising human contact with unsafe water. The need for control of transmission is increasing as growing human populations become more dependent on irrigated cultivation (Service, 1989). Where eradication is the objective, snail control becomes essential in support of other measures. Eradication of the snail host seems to have been achieved in Tunisia, and is feasible in some other countries, such as Algeria, Morocco and Mauritius, where habitats are not extensive and the chance of snails being reintroduced is small. More commonly the most that can be reasonably expected is a reduction in the intensity of transmission. The fundamental task is to identify the most important sites and seasons of transmission, and then the feasibility of snail control can be assessed realistically in relation to availability of resources and infrastructure, and to local public health considerations. Cost-effectiveness and environmental acceptibility will need to be demonstrated. In short, proposals for snail control should carefully address all the questions posed by McCullough (1986, 1992): where, when, how and by whom? It is increasingly evident that to be sustainable, snail control measures will need to be incorporated into primary health care systems (Tanner, 1989), using simple and practicable methods. Synthetic molluscicides will be cost-effective when used in suitable focal situations, but there is strong incentive to find cheaper molluscicides of plant origin. Whatever the means adopted, the success of snail control operations depends on personnel with suitable motivation, training and experience; more of these people are needed, particularly in tropical Africa. References Abdallah, A. & Nasr, T. 1973. Helisoma duryi as a means of biological control of schistosomiasis vector snails. Journal of the Egyptian Medical Association, 56: 514–520. Acra, A., Milki, R., Raffoul, Z., Karahagopian, Y. & Fletcher, M. 1986. Laboratory evaluation of Gambusia affinis fish as predators of the schistosome-bearing snails Bulinus truncatus. Journal of Tropical Medicine and Hygiene, 89:7–12. Adewunmi, C.O. 1991. Plant molluscicides: potential of aridan, Tetrapleura tetraptera, for schistosomiasis control in Nigeria. Science of the Total Environment, 102:21–33. Albaret, J.L., Orecchia, P., Lanfranchi, P., Picot, H. & Bayssade-Dufour, C. 1981. Potamopyrgus et bulins en Corse (Octobre 1980). Annales de Parasitologie, Paris, 56:559– 562. Amin, M.A. & Fenwick, A. 1977. The development of an annual regimen for blanket snail control on the Gezira irrigated area of the Sudan. Annals of Tropical Medicine and Parasitology, 71:205–212. Amin, M.A., Fenwick, A., Teesdale, C.H., McLaren, M., Marshall, T.F.de C. & Vaughan, J.P. 1982. The assessment of a large snail control programme over a three-year period in the Gezira irrigated area of the Sudan. Annals of Tropical Medicine and Parasitology, 76:415–424.

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Andrews, P., Thyssen, J. & Lorke, D. 1983. The biology and toxicology of molluscicides, Bayluscide. Pharmacological Therapeutics, 19:245–295. Appleton, C.C. 1985. Molluscicides in bilharziasis control—the South African experience. South African Journal of Science, 81:356–360. Appleton, C.C., Drewes, S.E., Mashimbye, M.J. & Cunningham, A.B. 1993. Observations on molluscicidal properties of warburganal on South African Bulinus africanus. Journal of Medical and Applied Malacology, in press. Babiker, S.M., Blankespoor, H.D., Massila, M., Fenwick, A. & Daffalla, A.A. 1985. Transmission of Schistosoma haematobium in North Gezira, Sudan. Journal of Tropical Medicine and Hygiene, 88:65–73. Babiker, A., Fenwick, A., Daffalla, A.A. & Amin, M.A. 1985. Focality and seasonality of Schistosoma mansoni transmission in the Gezira irrigated area, Sudan. Journal of Tropical Medicine and Hygiene, 88:57–63. Baluku, B., Josens, G. & Loreau, M. 1989. Etude préliminaire de la densité et de la répartition des mollusques dans deux cours d’eau du Zaire oriental. Revue de Zoologie Africaine, 103:291–302. Bard, J. & Mvogo, L. 1963. Note d’information sur l’Astatoreochromis alluaudi poisson molluscophage utilisable dans la prophylaxie de la bilharziose . Bulletin de la Société de Pathologie exotique, 56:119–120. Bayer, F.A.H. 1954. Larval trematodes found in some freshwater snails: a suggested biological method of bilharzia control. Transactions of the Royal Society of Tropical Medicine and Hygiene, 48:414–418. Berrie, A.D. & Visser, S.A. 1963. Investigation of a growth-inhibiting substance affecting a natural population of freshwater snails. Physiological Zoology, 36:167–173. Bolton, P. 1988. Schistosomiasis control in irrigation schemes in Zimbabwe. Journal of Tropical Medicine and Hygiene, 91:107–114. Breuil, J., Moyroud, J. & Coulanges, P. 1983. Eléments de la lutte écologique antibilharziose à Madagascar. Archives de l’Institut Pasteur de Madagascar, 50 (1982): 131– 144. Brinkmann, A. & Steingruber, R. 1986. Possible modifications in the construction of small dams to prevent the spread of schistosomiasis. Tropical Medicine and Parasitology, 37:199–201. Brown, D.S. & Burch, J.B. 1967. Distribution of cytologically different populations of the genus Bulinus in Ethiopia. Malacologia, 6:189–198. Brown, D.S. & Wright, C.A. 1972. On a polyploid complex of freshwater snails (Planorbidae: Bulinus) in Ethiopia. Journal of Zoology, London, 167:97–132. Butterworth, A.E. 1992. Vaccines against schistosomiasis: where do we stand? Transactions of the Royal Society of Tropical Medicine and Hygiene, 86:1–2. Campbell, K.L.I. 1981. Fishes of the genus Sarotherodon (Pisces, Cichlidae) of springs along the northern Uaso Ngiro, Kenya. Journal of the East African Natural History Society, 173:1–12. Cardarelli, N. 1974. Slow-release molluscicides and related materials. In Molluscicides in Schistosomiasis Control: 177–240. Cheng, T.C. (Ed.). New York: Academic Press. Cedeño-Léon, A. & Thomas, J.D. 1983. The predatory behaviour of Marisa cornuarietis on eggs and neonates of Biomphalaria glabrata, the snail host of Schistosoma mansoni. Malacologia, 24:289–297.

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Thomas, J.D. 1982. Chemical ecology of the snail hosts of schistosomiasis: snail-snail and snail-plant interactions. Malacologia, 22:81–91. Thomas, J.D. 1987a. A holistic view of schistosomiasis and snail control, Memorias do Institute Oswaldo Cruz, 82, supplement 4:183–192. Thomas, J.D. 1987b. An evaluation of the interactions between freshwater pulmonate snail hosts of human schistosomes and macrophytes. Philosophical Transactions of the Royal Society, London, B, 315:75–125. Thomas, J.D. & Tait, A.I. 1984. Control of the snail hosts of schistosomiasis by environmental manipulation: a field and laboratory appraisal in the Ibadan area, Nigeria. Philosophical Transactions of the Royal Society, London, B, 305:201–253. Thomas, J.D., Goldsworthy, G.J. & Aram, R.H. 1975. Studies on the chemical ecology of snails: the effect of chemical conditioning by adult snails on the growth of juvenile snails. Journal of Animal Ecology, 44:1–27. Thomas, J.D., Ndifon, G.T. & Ukoli, F.M.A. 1985. The carboxylic and amino acid chemoreception niche of Bulinus rohlfsi (Clessin), the snail host of Schistosoma haematobium. Comparative Biochemistry and Physiology, 82C:91–107. Thomas, J.D., Ofosu-Barko, J. & Patience, R.L. 1983. Behavioural responses to carboxylic and amino acids by Biomphalaria glabrata (Say), the snail host of Schistosoma mansoni (Sambon), and other freshwater molluscs. Comparative Biochemistry and Physiology, 75C: 57–76. Upatham, E.S., Koura, M., Ahmed, M.D. & Awad, A.H. 1981. Studies on the transmission of Schistosoma haematobium and the bionomics of Bulinus (P.) abyssinicus in the Somali Democratic Republic. Annals of Tropical Medicine and Parasitology, 75: 63–69. Van Eeden, J.A., De Kock, K.N. & Pretorius, S.J. 1983. Introduction of a freshwater crayfish in South African waters. Journal of the Limnological Society of Southern Africa, 9:49. Van Schayck, C.P. 1986. The effect of several methods of aquatic plant control on two bilharzia-bearing snail species. Aquatic Botany, 24:303–309. Visser, S.A. 1964. Molluscicidal activity of surface-active agents on the snail Biomphalaria sudanica, a vector of Bilharzia. Nature, London, 204:492. Visser, S.A. 1965. Molluscicidal properties and selective toxicity of surface-active agents. Bulletin of the World Health Organisation, 32:713–719. Voelker, J. 1968. Untersuchungen zu Ernahrung, Fortpflanzungsbiologie und Entwicklung von Limnogeton fieberi Mayr (Belostomatidae, Hemiptera). Entomologische Mitteilungen aus dem Zoologischen Staatsinstitüt und Zoologischen Museum, Hamburg, 3:1–24. Warren, K.S. & Mahmoud, A.A.F. 1976. Targeted mass treatment: a new approach to the control of schistosomiasis. Transactions of the Association of American Physicians, 89: 195–204. Webbe, G. 1987. Molluscicides in the control of schistosomiasis. In Plant Molluscicides: 1–26. Mott, K.E. (Ed.). New York: John Wiley. Webbe, G. & El Hak, S. 1990. Progress in the control of schistosomiasis in Egypt 1985– 1988. Transactions of the Royal Society of Tropical Medicine and Hygiene, 84: 394– 400. Webbe, G. & Jordan, P. 1982. Control. In Schistosomiasis. Epidemiology, Treatment and Control: 293–349. Jordan, P. & Webbe, G. (Eds). London: William Heinemann Medical Books.

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West, K. & Cohen, A. 1991. Morphology and behaviour of crabs and gastropods from Lake Tanganyika, Africa: implications for lacustrine predator-prey coevolution. Evolution, 45; 589–607. White, P.T., Gbakima, A.A. & Amara, S.V. 1989. Schistosoma mansoni in Sierra Leone: an invader extending its range? Annals of Tropical Medicine and Parasitology, 83: 191– 193. Wilken, G.B. & Appleton, C.C. 1991. Avoidance reponses of some indigenous and exotic freshwater pulmonate snails to leech predation in South Africa. South African Journal of Zoology, 26:6–10. Wilkins, H.A. 1989. Reinfection after treatment of schistosome infections. Parasitology Today, 5(3):83–88. Willmott, S. (Ed.). 1987. Report of an independent evaluation mission on the National Bilharzia Control Programme in Egypt, 1985 (abridged version). Transactions of the Royal Society of Tropical Medicine and Hygiene, 81 (supplement): 1–57. Witte, F., Barel, C.D. & Hougerhoud, J.C. 1990. Phenotypic plasticity of anatomical structures and its ecomorphological significance. Netherlands Journal of Zoology, 40: 278–298. Woodruff, D.S. 1985. Genetic control of schistosomiasis: a technique based on the genetic manipulation of intermediate host populations. Comparative Pathobiology, 8: 41–68. Woolhouse, M.E.J. 1988. Passive dispersal of Bulinus globosus. Annals of Tropical Medicine and Parasitology, 82:315–317. Woolhouse, M.E.J. & Chandiwana, S.K. 1990. The epidemiology of schistosome infections in snails: taking the theory into the field. Parasitology Today, 6(3):65–70. World Health Organisation, 1982. Data sheet on the Biological Control Agent Marisa cornuarietis (Linn.). Unpublished report WHO/VBC/82.837. Geneva: World Health Organisation. World Health Organisation, 1993. The Control of Schistosomiasis. WHO Technical Report Series, 830. Geneva: World Health Organisation. Wright, C.A. 1968. Some views on biological control of trematode diseases. Transactions of the Royal Society of Tropical Medicine and Hygiene, 62:320–329.

Chapter 9. Local snail faunas

Much effort has been devoted to studying the distribution in some parts of Africa of freshwater snails in relation to variation in environmental conditions, within and among waterbodies. Common motives are to determine the distribution of snail hosts for schistosomes, in order to plan measures for controlling transmission of the parasites, and to assess the potential for an intermediate host to colonise man-made waterbodies. Examples of local snail faunas are described here, essentially in terms of general natural history, followed by discussions of the diversity of species, their relative abundance and associations among species. Seasonal changes in abundance are touched on briefly and are treated more fully in Chapter 11. Lastly, some influences on local distribution are examined, with particular attention to three biotic factors: dispersal, associations with aquatic plants and the availability of food (abiotic factors such as water chemistry are dealt with mostly in Chapter 10). Faunal surveys Invertebrates have been surveyed comprehensively in the major river systems of South Africa, with the primary objective of assessing pollution (e.g. Allanson, 1961; Chutter, 1971; Harrison, 1958; Oliff, 1960–65), but surprisingly few species of gastropods were recorded and these usually in small numbers. Two probable reasons are that molluscs are distributed discontinuously in rivers, and may be under-represented by sampling methods that are used for insect larvae. But it is generally true that snails appear, in Africa, to contribute less to the invertebrate fauna of large rivers than of streams, pools and lakes. There are many descriptions of local snail faunas which cannot be referred to in detail in the space available here (e.g. Hart, 1979; Diaw, 1980; WibauxCharlois et al., 1982; Betterton, 1984; Brown et al., 1984, 1992; Betterton et al., 1988; Madsen et al., 1987, 1988; Fashuyi, 1990; Greer et al., 1990; Okafor, 1990). The reader’s attention is drawn to an exceptionally thorough study of the Mooi River in the western Transvaal (De Kock & Van Eeden, 1969). I have selected studies for six areas, beginning with two where I have personal experience: western Kenya, south-eastern Transvaal, lower Zaire, eastern Zaire, Lake Chad and south-western Nigeria. Then attention is focused on human

FRESHWATER SNAILS OF AFRICA 455

activities in relation to the snail fauna of urban areas and in producing changes in snail distribution. The term ‘biotope’ is used for a particular set of defined conditions; several biotopes may be recognisable within a habitat. Western Kenya: Kano Plain Situated near Kisumu, and not far south of the equator, this plain extends about 30 km eastward from the head of the Winam (Kavirondo) Gulf, the north-eastern arm of Lake Victoria. The altitude of the plain is about 1160 m, and Table 9.1. Snail faunas in various aquatic biotopes near Kisumu in western Kenya (data from Brown, 1975, 1980). Species 1 2 3

4 5 6 7 8 9

10 11 12

13

Bellamya unicolor B. jucunda Melanoid es tubercula ta Gabbiella humerosa G. barthi Pila ovata Cleopatra guillemei Lymnaea natalensis Biomphal aria choanom phala B. pfeifferi B. sudanica Ceratoph allus natalensis C. kisumiens is

Biotope 1

2

3

4

5

×

×

—

—

—

—

×

—

—

—

×

×

—

—

—

×

—

—

—

—

— — —

— × —

— × —

— × —

× × ×

—

×

×

—

—

—

×

—

—

—

—

—

—

—

×1

—

—

×

—

—

—

—

×

×

×

—

×

—

—

—

456 LOCAL SNAIL FAUNAS

Species

Biotope 1

2

3

4

5

14

—

×

×

—

—

—

—

×

—

—

—

—

×

—

—

—

×

—

—

—

—

—

—

×2

—

—

—

×

—

—

— —

— ×

— ×

×2 —

— —

—

—

×

×

×

—

—

—

—

×

—

—

—

—

×

—

—

—

×

—

—

×

—

—

—

×

×

—

—

—

—

×

—

—

—

—

×

—

×

—

4

14

10

7

8

Segmento rbis angustus 15 S. kanisaens is 16 Lentorbis junodi 17 Gyraulus costulatus 18 Bulinus africanus 19 B. globosus 20 B. nasutus 21 B. ugandae 22 B. forskalii 23 B. reticulatu s 24 B. scalaris 25 B. truncatus 26 B. transvers alis 27 B. trigonus 28 Burnupia sp. 29 Ferrissia sp. Totals per biotope

1. Where relatively permanent seepage is present. 2. On sandy soil. Biotopes: 1, bottom sediment in Lake Victoria; 2, stony beach at the edge of the lake; 3, permanent swamp with papyrus; 4, pools (borrow-pits and yaos) of which some become regularly dry; 5, ephemeral habitats, some containing water for only a few months each year.

FRESHWATER SNAILS OF AFRICA 457

bordering hills in the north and east rise to over 1800 m. Many streams and small rivers drain across the plain into Lake Victoria, but even the biggest, the Nyando River, ceases to flow in the most severe dry seasons, and many pools and marshes regularly dry out. On the plain and shore of Lake Victoria 29 species of aquatic gastropod were found in 1971–75 (Brown, 1975, 1980); their distribution can be related to 5 main biotopes (Table 9.1): 1. Lake bottom. The maximum depth of the Winam Gulf near Kisumu is about 18 m, and the bottom sediment is mostly fine organic detritus derived from the papyrus swamps. The prosobranchs Melanoides tuberculata, Bellamya unicolor and Gabbiella humerosa were abundant on this sediment; a diploid Bulinus sp. (possibly B. trigonus) occurred in small numbers on stones and large bivalve shells. Almost all specimens of Gabbiella found had egg capsules attached to their shells, perhaps because of a shortage of other sites for oviposition (the other prosobranchs are viviparous). 2. Stony beaches. These are exposed each day by a rise and fall of about 50 cms in the level of Lake Victoria, and wave action can be violent in the afternoon. The greatest variety of species occurred here. Pila ovata lays its eggs just above the highest water-level, while young snails of most species were found high on the beach beneath stones with only the base moistened. On wave-washed stones Burnupia presumably experiences well-oxygenated conditions like those in stony streams; Ferrissia seems equally at home on these stones as on vegetation in stagnant water. The presence of Gyraulus costulatus is interesting because it was not found on the Kano Plain, but occurred in streams descending the eastern hills; a possible explanation is that this species, like Burnupia, finds well-oxygenated water on the beach. 3. Permanent swamp. Conditions change considerably from the landward fringe where semi-aquatic grasses and sedges are grazed by cattle, to the interior where the tall papyrus grows as a mat over deeper water. The water is brownish in colour and poorly oxygenated. At the fringes, which may shift considerably following the seasonal rise and fall in the lake level, Biomphalaria sudanica, Bulinus globosus, B. ugandae and Ceratophallus natalensis are abundant, and other species (Table 9.1) less common. Deeper within the swamps, only B. sudanica and Pila ovata were found, the latter growing much larger than on the beaches. 4. Pools. Numerous small pools (yaos) are dug in the drier areas of the Kano Plain to supplement roadside borrow-pits as sources of water for livestock and domestic use. The pools sometimes become dry, their water is generally turbid, and aquatic vegetation is sparse or absent. The occurrence of Bulinus species is usually associated with the presence of aquatic vegetation, though other factors may be involved since B. africanus and B. nasutus were found in pools on sandy soils, but not on the central part of the plain, which is composed of black ‘cotton’ soil. In contrast, B. truncatus and B. forskalii were common in some pools on cotton soil.

458 LOCAL SNAIL FAUNAS

5. Ephemeral pools. Water is present for no more than a few months each year on the plain in slight hollows, ditches or even wheeltracks, where large populations of certain species occur. B. forskalii and Ceratophallus natalensis reach their highest densities in these pools, and B. reticulatus and B. scalaris were found in no other biotope. Gabbiella barthi and Cleopatra guillemei were found too in rainpools, but much less commonly than the other species. Conditions in streams and rivers on the Kano Plain vary greatly in relation to rainfall; they may be rushing torrents or almost entirely dry, and the extreme instability and associated soil erosion are responsible for a poor molluscan fauna. Biomphalaria pfeifferi is common in some of the smallest of the seasonallyflowing streams on the fringe of the Kano Plain, and in associated seepage areas, but seems unable to establish itself on the main area of the plain. Irrigation schemes provide additional aquatic habitats. In drains of the Kano I scheme at Ahero, Bulinus forskalii was common and occasionally B. globosus and B. truncatus were found (Brown, 1975); it may be that more extensive establishment of snails was prevented by the regular mollusciciding carried out (Highton & Choudhry, 1974). Biomphalaria was common in a drain of the Kano II scheme at the edge of Lake Victoria in 1986 (Brown, unpublished observations). Continuing attention to irrigation schemes in this area seems necessary in order to avoid the establishment of sites of transmission for schistosomes. Differences in distribution among species within the small geographical area of the Kano Plain seem to have significance in view of the apparently good opportunities of dispersal for snails. Aquatic birds are abundant and many of the surface waters are interconnected by flooding during heavy rainfall. Kinoti (1971) suggested that some unfavourable factor derived from cotton soil might be responsible for the absence of B. africanus and B. nasutus from the central part of the plain. For some species the length of the seasonal dry period seems to be a critical factor. Further factors may be the disturbance and pollution of habitats by people and livestock. South-Eastern Transvaal: Crocodile/Komati river system In contrast to the equatorial Kano Plain where altitude and climate vary little, the south-eastern Transvaal varies greatly in altitude, so that climatic temperature and the speed of flow in streams have important effects on snail distribution. The sources of the streams lie on the highveld plateau at about 1830 m altitude, and the Komati River enters the Indian Ocean at Maputo (Lourenço Marques). Streams descend the Drakensberg escarpment and then flow through the lowveld, which is undulating country with a predominantly tropical vegetation. Before joining the Komati, the Crocodile River forms the southern boundary of the Kruger National Park. The temperate climate of the highveld, where frost occurs on many nights every year, contrasts sharply with the subtropical warmth below the escarpment, and in general the prevailing temperature increases

FRESHWATER SNAILS OF AFRICA 459

eastwards. However, even in the lowveld the temperature can fall so low at night that indigenous trees beside the Crocodile River at Nelspruit are shrivelled by frost. Aquatic habitats include rivers, streams (perennial or reduced to residual pools during the dry season), pools, dams, and cement reservoirs; in contrast to the Kano Plain, there is no lake and no extensive area of swamp. Many waterbodies are man-made, especially in the Kruger National Park, to supplement the limited water resources provided by the few perennial rivers. At least 20 gastropod species (Table 9.2) are found in the Crocodile River system, (Schutte & Frank, 1964; Hughes, 1966; Oberholzer & Van Eeden, 1967; Brown & Van Eeden, 1969; Appleton, 1974a, 1975). One of these, Lymnaea columella, is an introduced alien. Some species are restricted to either the upper western zone (taken to extend down to about 600 m altitude) or the eastern lowlands. Lymnaea truncatula is one of two species characteristic of the western zone; many small areas of seepage in the lowveld appear suitable for this snail but it has not been found. Gyraulus connollyi is common in streams on the highveld and descends the Drakensberg escarpment down to about 850 m, living amongst marginal grasses and on stones. Burnupia is common on stones in these streams; it descends almost to 600 m near Nelspruit, and though absent from most of the lowveld reappears in streams flowing eastwards from hills in Table 9.2. Snail fauna of the Crocodile River system, SE Transvaal. Species restricted to the cool western zone (W); species restricted to the warm eastern zone (E). Bellamya capillata Lanistes ovum Melanoides tuberculata M. victoriae Cleopatra ferruginea

(E) (E)

(E)

Lymnaea natalensis L. truncatula L. columella Gyraulus costulatus G. connollyi Segmentorbis angustus S. kanisaensis Lentorbis junodi Biomphalaria pfeifferi Bulinus africanus B. globosus B. tropicus B. forskalii Burnupia spp. Ferrissia spp.

(W)

(W) (E) (E) (E)

the Kruger National Park. The key to the distribution of Burnupia seems to be the availability of well-oxygenated water, which is likely to be flowing, cool and unpolluted, so that topography, climate and human activities may all combine to produce a discontinuous distribution.

460 LOCAL SNAIL FAUNAS

Six species are confined to the warm eastern lowlands of the southern Transvaal; the prosobranchs Bellamya capillata, Lanistes ovum and Cleopatra ferruginea, and the pulmonates Lentorbis junodi, Segmentorbis kanisaensis and S. angustus. The pulmonates live usually amongst aquatic plants in permanent standing waters, and they could be restricted by a shortage of suitable habitat, but the prosobranchs are all capable of surviving in residual pools in streambeds lacking vegetation, and there appears to be no lack of suitable localities for them in the western lowveld. It seems likely that they are absent because the water temperature in winter is too low. The species confined to the eastern lowlands are in fact ‘tropical’, with ranges extending into the coastal plain of Mozambique and northward into the main tropical area. Some other species are more widespread in the lowveld, occurring westward to the foothills of the Drakensberg escarpment, yet these too are essentially tropical in character (Chapter 12: Southern Africa). Melanoides tuberculata and M. victoriae live in rivers and streams. Biomphalaria pfeifferi, Bulinus africanus and B. globosus occur in various natural and artificial waterbodies, mostly east of longitude 31° and below 900 m. Their distribution was analysed in relation to chemical factors (Schutte & Frank, 1964), but no clearly limiting effects were apparent. B. africanus seemed more frequent than B. globosus in the west; in eastern areas B. globosus alone occurs (Oberholzer & Van Eeden, 1967). This suggests that B. africanus is better adapted to cool conditions, as appears to be the case in Natal (Brown, 1966). B. forskalii occurs throughout the whole lowveld in small waterbodies, though less commonly in the west where it reaches an upper altitudinal limit at about 800 m. ‘Bulinus tropicus’ recorded in the eastern lowveld presents a taxonomic problem; morphological studies show some resemblance to B. natalensis, of which the typical form lives in the subtropical region of Natal (Brown et al., 1971). This complex of snails is wellrepresented on the highveld Table 9.3. Snail fauna of the Gladdespruit, SE Transvaal: physical zones and highest altitude recorded for each species, and maximum current speed tolerated (data from Appleton, 1975; most altitudes estimated from Appleton’s Fig. 2). Species

Zones

Highest altitude (m) Maximum current speed (m sec −1)

Melanoides victoriae M. tuberculata Bulinus forskalii Biomphalaria pfeifferi Bulinus (Physopsis) sp. Lymnaea columella Ferrissia cawstoni Lymnaea natalensis Gyraulus costulatus

4 4 4 4 4 3,4 3,4 3,4 3,4

740 750 823 823 838 910 920 980 1070

1.9 0.3 — 0.3 0.3 1.7 1.4 1.9 —

FRESHWATER SNAILS OF AFRICA 461

Species

Zones

Highest altitude (m) Maximum current speed (m sec −1)

G. connollyi Burnupia spp.

3,4 1070 1,2,3,4 1600

1.4 3.2

by populations identified as B. tropicus. The apparent break in distribution in the western lowveld indicates at least a physiological difference between the two groups of populations. Lymnaea natalensis and Gyraulus costulatus occur almost throughout the Crocodile catchment. The upper altitudinal range of G. costulatus overlaps the lower limit for G. connollyi on the Drakensberg escarpment, and they are often found together. One tributary of the Crocodile River, the Gladdespruit, has been studied in detail (Appleton, 1975). This perennial stream rises at about 1620 m on the edge of the highveld, is about 40 km long and joins the Crocodile River at 655 m near Nelspruit. Four physical zones were distinguished by Appleton: 1. cliff waterfall zone, from 1620 to 1300 m. Intermittent waterfalls over steep faces of granite, fed in a stepwise fashion from pools densely shaded by trees; 2. foothill torrent zone, from 1300 to 1060 m. Shallow stream flowing over stones and coarse sand, lined with coarse grasses; 3. foothill soft bottom zone, from 1060 to 900 m. Rapidly flowing, canal-like sandy run bordered by trailing grasses, reeds and sedges; 4. granite zone, from 900 to 655 m. Unevenly eroded granite containing depressions with pools, backwaters and potholes beside the main channel. Emergent and aquatic plants are common; trees shade some stretches. Molluscs were collected at 31 sampling stations (Table 9.3), Bulinus (Physopsis) sp. possibly comprises both Bulinus africanus and B. globosus. The four species of Burnupia listed by Appleton are combined in Table 9.3, because of the dubious distinctions among species in this genus. The upper altitude reached by the Melanoides species was lower than for any pulmonate. Bulinus and Biomphalaria were confined to the lowest zone (4), occurring in pools and backwaters but not under heavy shade or in runs with currents above about 0.3 m s−1. Current speeds more than four times greater were tolerated by the other species (Table 9.3), and Appleton believed current speed was the most important influence on altitudinal ranges of snails in the Gladdespruit. It is noteworthy, however, that breeding by Biomphalaria and B. (Physopsis) was interrupted during winter in the lowest zone of the Gladdespruit (Appleton, 1974b); therefore breeding seasons could have been further curtailed by the lower temperature at higher altitude, and this might have contributed to the absence of these snails higher in the foothill zones. In the much larger Komati River, Appleton (1975) gave particular attention to the discontinuous distribution of Biomphalaria and B. (Physopsis) over a distance of about 140 km. Two types of population were distinguishable; those that persisted despite the annual floods, and those which were practically

462 LOCAL SNAIL FAUNAS

eliminated by floods, because of the instability of the substrata in their habitat. Persistent populations occurred where granite and basalt were exposed and not overlain by alluvial sediments; pools formed in the hard rock provided protected niches for snails. On unstable substrata amongst soft rocks, or on alluvial sand, either no snails were found or the populations were obviously vulnerable to destruction. Altitudinal ranges for molluscs in the Komati and its tributaries were similar to those observed in the Crocodile system. Gyraulus connollyi was found down to 850 m, and Burnupia down to about 600 m. Biomphalaria and B. (Physopsis) occurred up to about 1000 m, thus somewhat higher than in the Gladdespruit, perhaps because of the availability of larger pools, where the greater volume of water would not cool so much in winter. Lower Zaire In contrast to the areas so far described, the western part of Zaire lying between Kinshasa and the coast, a distance of about 300 km, is of generally low altitude (mostly below 500 m) and has extensive areas of forest. The geological formations are predominantly acidic, producing soft surface waters, though there are extensive calcareous plains in the area including Kimpese and Kisantu. Below Kinshasa, the Zaire River flows through many rapids and receives numerous tributaries from the hills to the north and south. These streams flow rapidly in their upper courses, but meander on reaching the plains, where there are marshes in poorly drained depressions and some cultivation by irrigation. Riverbanks and hills are forested to a varying extent, while further west is a coastal area of savanna. Rainfall varies from 1000 to 1500 mm per year, and many streams are perennial, with substrata of sand or gravel, aquatic plants and clear water. The molluscs of the lower Zaire River itself are poorly known, though some remarkable endemic species have been discovered. However, the territory lying immediately north and south has been well searched (Mandahl-Barth et al., 1974); a total of 21 gastropod species was obtained from 229 sampling stations. The most abundant prosobranch, Lanistes congicus, occurred mostly in rivers with clear water and firm substrata; L. ovum was less common, living in marshes or muddy rivers, sometimes choked with papyrus or water hyacinth. Potadoma freethi was associated with rivers flowing over rocks or gravel, and lacking aquatic plants. Melanoides recticosta seemed to be confined to the streams of the calcareous plain. Apart from this species, which was not found in water of pH less than 6.8, all these prosobranchs occurred in water of pH below 6.0 (minimum 5.2). The 4 prosobranchs Pila ovata, P. wernei, Hydrobia luvilana and Funduella incisa were each found in only a single locality. The most widespread pulmonates were Lymnaea natalensis (31% localities) and Biomphalaria pfeifferi (13% localities); both were associated with slowly flowing water. B. camerunensis (6% localities) was not found with B. pfeifferi, and its habitats included stagnant waters dominated by papyrus; in this respect B.

FRESHWATER SNAILS OF AFRICA 463

camerunensis is analogous with B. sudanica in western Kenya. Gyraulus costulatus was obtained rarely, from a few rapidly flowing rivers, but Afrogyrus coretus, Lentorbis benguelensis and Segmentorbis kanisaensis occurred in marshy and stagnant localities. B. truncatus rohlfsi occurred in clear moderately fast-flowing rivers on the calcareous plains, where pH varied between 6.5 and 7. 3. B. globosus was found only in a few rivers. Ferrissia occurred in various waterbodies, but surprisingly no Burnupia was reported from the numerous rapidly flowing streams. Bulinus forskalii was the commonest member of its genus reported by Mandahl-Barth et al. (1974), living in pools, the slowly flowing parts of rivers and small artificial waterbodies. This snail was found also in rivers near Kinshasa, where it was at one time abundant in this town (Bennike et al., 1976). By 1984–85, however, B. forskalii had become uncommon in Kinshasa (De Clercq, 1987), having been apparently replaced by the introduced Physa acuta. In view of the small range in altitude, temperature seems unlikely to influence the distribution of snails in lower Zaire. Substratum, current speed, oxygenation and turbidity probably all play a part, but the underlying influence of the acidity of the water seems to dominate the broad pattern of distribution. No molluscs were found during these surveys in the brown-coloured acidic waters of the plateaux, and snails were common only on the calcareous plains. Eastern Zaire The survey of two streams by Baluku et al. (1989) is distinguished by a quadrat sampling technique, well-tested in preliminary studies. The total of 7 species of snail found was small, and their distributions and abundance were thoroughly established by means of more than 2500 samples. In each stream 5 or 6 sampling areas were marked, each judged to be a homogeneous biotope in respect of current speed, nature of sediment, amount of aquatic vegetation and degree of shading. Samples were taken monthly or bimonthly over periods of 9 and 10 months with an interval of one year between them. The two streams were different in character and were dominated by different species. The Virunga Stream is situated at 1740 m altitude and is a perennially flowing tributary of the Lwiro River, which enters the south-western shore of Lake Kivu. The stream is in an area of high rainfall, with a short dry season and a moderate average temperature of 19.5°C. Potadoma ignobilis was the dominant snail and absent from only the uppermost sampling station near the source, where Lymnaea natalensis occurred alone, perhaps because of unusual chemical conditions (low levels of dissolved oxygen and sulphate), and possibly also due to competition from Biomphalaria pfeifferi. During the second sampling period B. pfeifferi was almost lacking from one station where it was previously abundant, apparently because of the shade from banana trees planted in the interval between the sampling periods. Tomichia kivuensis was associated with a fast current speed of about 0.30 m s−1, a gravel bottom and few plants.

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The Bilala ‘stream’ was actually a long-established drain for irrigated cultivation on the Ruzizi Plain at 800 m altitude; rainfall was comparatively low and the dry season long, with an average temperature of 25°C. This watercourse became almost entirely dry between the sampling periods. Pila ovata was the dominant species in biomass because of its large size. B. pfeifferi was the commonest pulmonate and here, unlike in the Virunga, coexisted with L. natalensis; to account for this difference, Baluku et al. (1989) suggested that competition between the two species was greater in the Virunga because feeding conditions were poorer there, while the permanency of this stream allowed full development of the effect of competition. Bulinus truncatus was comparatively uncommon and was associated with dead leaves; B. forskalii was found rarely and seemed to enter the Bilala stream only occasionally from nearby rice-fields. B. truncatus and L. natalensis were the species most badly affected by desiccation. According to these observations a ‘Biomphalaria-biotope’ was characterised as having a slow current, little or no shading and a rich aquatic vegetation of macrophytes and unicellular algae. The biology of this snail was described further in detail (Baluku et al., 1987; Loreau & Baluku, 1987; Baluku & Loreau, 1989). Lake Chad Although confined to a single waterbody, the extensive observations made on the benthic prosobranchs of Lake Chad deserve to be included among major studies of local faunas, as the area surveyed in detail is so large (20 000 km2). Most of the observations (summarised by Carmouze et al., 1972, and Lévêque et al., 1983) were made between 1968 and 1971, during a ‘normal Chad’ period. The lake level dropped rapidly after 1972, changing the distribution patterns of snails and little is known about the evolution of the benthic communities during this drying phase. The generally shallow depth of the lake allowed the use of the Ekman grab sampler to obtain substantial quantitative data for molluscs, worms and insects. Although about 24 species of gastropods are known from the swampy margins, islands and open lake (Lévêque, 1967; Brown, 1974; Betterton, 1984; Chapter 12: Table 12.6), only three of them, Melanoides tuberculata, Bellamya unicolor and Cleopatra bulimoides (=cyclostomoides) are abundant on the bottom sediments, where bivalves are also common. The distributions of the prosobranchs are summarised here; further information about population fluctuations, life-cycles and productivity is included in Chapters 10 and 11. The main source of water for Lake Chad is the Chari River, which enters at the southern end. There is no outflow and evaporation causes salinity to rise sharply with distance from the Chari Delta. The distribution of the benthic molluscs can be related to variations in salinity and to the 5 main types of sediment: sand, mud, peat, soft clay and granular clay. ‘Normal Chad’ was partly divided into a north

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and a south basin by a ridge, the Grande Barrière; falling water level resulted in separation of these basins in 1973 and the northern basin dried up in 1975. A preliminary investigation was made of 110 collecting stations near Bol, on the south-eastern arm of the lake, where salinity, water movement and temperature were uniform (Lévêque, 1972). Each prosobranch species was present on all the sediment types, but with significant differences in relative abundance. Sand and peat were apparently ‘neutral’ biotopes, where the presence or absence of a species seemed due mainly to chance. On the other hand, granular clay was inhabited by 3 species of bivalve in addition to the prosobranchs and seemed to be especially favourable. Population densities were very high at some sampling stations; Lévêque (1973) recorded nearly 1500 M. tuberculata per m2 at Samia, and over 400 Cleopatra per m2 at Baga Kawa. It thus appears that competition for living space could have occurred, although no causal reason is evident for the associations between snails and sediment type. Investigations were extended throughout Lake Chad in 1968 and 1970 when samples were taken at intervals of about 5 km in all the navigable areas (Lévêque, 1972, 1973). It became evident that the distribution patterns of the molluscs were not related simply to type of sediment. Melanoides was present throughout the lake with the exception of the most northerly part, where all the snails seemed to be excluded by high salinity. Cleopatra and Bellamya were most abundant in the central zone, including the Grande Barrière. The significance of increasing salinity in limiting distribution was indicated by the presence of shells where no living snails were found, and the absence of these prosobranchs from other moderately saline waters associated with Lake Chad. At the other end of the scale, low salinity seemed also to be unfavourable for Bellamya, which was rare in the vicinity of the Chari Delta. For the period 1968–70 the whole of Lake Chad could be divided into 7 ecological zones according to their molluscan communities (Lévêque et al., 1983). However, changes occurred in some molluscan communities during this period, and were more evident in 1972 when further limited sampling was carried out in the south-eastern archipelago. These modifications were related to the decreasing lake level; one possible direct effect on the molluscs was the increased amount of sediment in suspension at the sediment-water interface, resulting from greater perturbation by waves (Dejoux et al., 1971). It is clear that the benthic snail populations of Lake Chad are far from being randomly distributed, and are subject to great changes in density. This knowledge is an important step towards understanding the biological productivity of this lake, to which prosobranch snails make a substantial contribution (see Chapter 11). South-western Nigeria Twenty-four collecting sites in standing and flowing waters in the Ibadan area (Thomas & Tait, 1984) yielded 10 species of snail, most frequently Melanoides

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tuberculata, Lymnaea natalensis, Bulinus forskalii and Biomphalaria pfeifferi. Two generalisations emerged: 1) persistent snail populations occurred in certain restricted foci where they were protected from flooding and unstable water level, and 2) snails were discontinuously distributed in time and space. Persistent foci within stream systems occurred in small pools and swampy ground, characterised by the presence of the plants Nymphaea and Ceratophyllum. In dams and lakes, Table 9.4. Freshwater snails of south-western Nigeria (data from Ndifon & Ukoli, 1989). Relative abundance: A, widely distributed and common: B, infrequent: C, rare. Pila wernei Lanistes libycus L. ovum Melanoides tuberculata Potadoma moerchi

C A C A B

Lymnaea natalensis Ferrissia sp. Gyraulus costulatus Segmentorbis sp. Biomphalaria pfeifferi Bulinus globosus B. truncatus (=rohlfsi) B. forskalii Physa (Aplexa) waterloti

B C A C B A C A B

refuges were provided by bays and deep marginal inlets. Most species of snail were associated with fine sediment and aquatic plants, but Melanoides tuberculata was most abundant on coarse sediment in eroding watercourses. The composition and geographical distribution of the snail fauna in a much larger area of south-western Nigeria is known from data for 404 collecting stations, some sampled in the rainy season and others in the dry season (Ndifon & Ukoli, 1989). The dry season lasts about 7 months in the northern part of the study area and about 4 months in the wetter southern part. There is a transition from forest in the south to savanna in the north, though vegetation is much modified by man. The Yoruba Plateau (300–900 m altitude) occupies most of the area and descends in the north-east into the Niger Basin. Some rivers flow all year round, unless the year is exceptionally dry, but streams flow only during the rainy season, and many of the habitats for snails are man-made. Snails were found in 190 (44%) of these Nigerian sites; the total of 14 species included 5 which were widely distributed and common (Table 9.4). Bulinus globosus and Gyraulus costulatus were the most widely distributed pulmonates; Biomphalaria pfeifferi was found chiefly in permanent waterbodies on the plateau. Melanoides tuberculata and Lanistes libycus were the commonest prosobranchs; Pila wernei and Lanistes ovum were confined to the Niger Basin. All waterbodies where snails were found contained aquatic or subaquatic plants. Distributions were analysed in relation to type of habitat, degrees of shading and pollution, type of vegetation and presence of other species of snail. The common species (Table 9.4) occurred in all the five types of waterbody (dams, fishponds, pools, rivers and streams). Among the more restricted species, B. truncatus

FRESHWATER SNAILS OF AFRICA 467

(=rohlfsi) was found only in fishponds, while the prosobranchs apart from M. tuberculata were usually confined to streams and rivers. Biomphalaria pfeifferi and Lymnaea natalensis preferred minimal shade, but Lanistes libycus, Gyraulus costulatus and Aplexa waterloti were most frequent in high shade. Organic pollution seemed favourable to B. globosus but not B. pfeifferi, while A. waterloti occurred mainly in polluted waters near human settlements. Most of the significant snail-plant associations were with emergent plants, e.g. B. globosus with Alternanthera and Commelina. Significant associations among some species suggested shared ecological requirements, yet most species occurred frequently alone and the generally low species-diversity (mean 1.7 species per sampling station) was attributed to the seasonal nature of most of the waterbodies. Snails in urban areas Freshwater snails including hosts for schistosomes live in many African towns and there is much urban transmission of schistosomiasis. Even in areas where piped water is supplied many people and especially children make frequent contact with water in rivers, streams, pools and drains. Some snail species tolerate considerable pollution and disturbance of habitat. In 1972–76 I found Bulinus africanus and Biomphalaria pfeifferi abundantly in streams within Nairobi but not in the more heavily polluted water where only Physa acuta was seen. Intermediate hosts have been found commonly also in Johannesburg (Van Eeden et al., 1964), Lusaka (Hira, 1974a,b), Addis Ababa (Lemma et al., 1968) and Mwanza (McCullough et al., 1972). Populations of B. pfeifferi and Bulinus globosus in urban sites in Liberia were relatively unaffected by seasonal changes, allowing year round transmission of schistosomiasis (Sodeman, 1979). More recently, species of Bulinus and Biomphalaria were among 10 species of snail found in Dar es Salaam (Sarda et al., 1985), 6 species in Kinshasa (De Clercq, 1987) and 7 species in Bamako (Madsen et al., 1987). Few waterbodies in Dar es Salaam were free from B. nasutus or B. globosus (both transmitting S. haematobium); these snails appeared well-adapted to the city environment, tolerating flooding and pollution from factories (Sarda et al., 1985). Man-made changes in local snail faunas Changes in the distribution of intermediate hosts for schistosomes are considered in relation to transmission of the parasites Chapter 5 (Changes in transmission patterns). Such activities as irrigation, construction of dams and salinity barrages, and forest clearance may all change the composition of a snail fauna, affecting different species in various ways. Swamp rice farming as practised in parts of West Africa has a marked effect (White et al., 1982). Construction involves removing the climax vegetation of a valley swamp and replacing it by an ordered system of paddies. The natural swamp is deeply shaded, poor in

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aquatic plants and harbours few snails apart from Saulea vitrea. After clearance and exposure to light, aquatic plants become common and 9 species of snail were found in swamps 5–6 years after construction. Biomphalaria and Bulinus become established to a varying extent according to local conditions (Kazura et al., 1985; White et al., 1989). Changes in an urban snail fauna are described by De Clercq (1987) in Kinshasa, where over a period of about 15 years Biomphalaria camerunensis was replaced by B. pfeifferi, while Bulinus forskalii declined greatly, possibly as the result of an increase in Physa acuta. This species and another invasive snail, Lymnaea columella, have become common in South Africa (Chapter 12: Introduced species). Further changes could follow other introductions, whether accidental (e.g. Amerianna and Indoplanorbis) or deliberate (Marisa, Helisoma). Diversity of species and relative numbers The number of species of snail living in a waterbody generally increases with the variety of conditions. Thus, a small muddy pool may contain only a single species, while a nearby swamp with a rich aquatic vegetation may support 10 or more. Specific associations between snails and plants involving food selection are believed to play a part in the distribution of snails in the northern hemisphere (Lodge et al., 1987), but have not yet been demonstrated in Africa (see the later section ‘Food’ in this chapter). Molluscs are most diverse in large lakes, where there are many different biotopes in relation to the depth gradient and type of shore (marshy, sandy or rocky). Besides the conditions of today, the composition of a local snail fauna may reflect opportunities for speciation in the past. In this connection the depth of a lake is more important than its surface area, because the deeper lakes are likely to be old enough for adaptation by snails to the different biotopes within them to have led to speciation. For example, Lake Victoria with an area of 68 000 km2 and a greatest depth of 80 m, contains no more than about 30 species of snail, whereas Lake Tanganyika with about half the area but reaching over 1400 m in depth supports about 100 species (see also Chapter 12: Natural lakes). Speciation that has occurred in major rivers such as the Zaire has also depended on the long existence of different biotopes. At the other end of the scale, conditions in small seasonal pools restrict their snail fauna directly by eliminating species that are intolerant of drying and indirectly by preventing growth of aquatic plants. Even in a large waterbody instability in water level can be unfavourable for snails, as in man-made lakes with a large draw-down and rivers that flood violently. Another factor limiting species-diversity is high concentration of dissolved salts, so that to the disappointment of a malacologist, Lake Turkana (Rudolf), though both natural and large, contains no more than about 7 living gastropod species, and none at all are present in the more saline lakes of eastern Africa. An average of 3.8 species was obtained from 285 sampling stations in western Kenya, mostly on the Kano Plain (Table 9.5). Most of these sites were sampled

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by two collectors for half an hour, and probably all species present were found. The smallest diversity for a particular biotope was 2.0 for ephemeral rainpools. High diversities were associated with large swamps (5.4) and the beaches of Lake Victoria (6.5). From 1–8 species were obtained per collecting station in Ibadan; average species-diversity per site was lower in streams with eroding substrates (1.4) than in streams with a depositing substrate and aquatic plants (6.5) and permanent standing waters (6.2) (data calculated from Thomas & Tait, 1984, pp. 204–208). In the Jonglei region of Sudan, the mean number of species per collecting station varied from 1.4 for rainpools to 4.0 for rivers and backwaters (Brown et al., 1984). Average diversity was 2.7 species for habitats in south-western Nigeria, mostly pools and streams (Ndifon & Ukoli, 1989). The low species-diversities for snails in small waterbodies in Africa are comparable to the 2.1 species per pool reported for southern England (Boycott, 1936, p. 125) and 1.12 species per ‘puddle’ in Norway (Økland, 1990, p. 324). Low diversity can be explained, as we have seen, by adverse physicochemical factors, related to seasonal desiccation. The few African species characteristic of rainpools (e.g. the Bulinus forskalii group and B. reticulatus) might have been driven into them by competition from other species, the reason suggested by Boycott (1936, p. 128), to account for the restriction of some European freshwater Table 9.5. Numbers of gastropod species found in different aquatic biotopes in western Kenya. Original data for 285 sampling stations visited in 1971–73. Biotopes: (1) bottom sediment of Lake Victoria; (2) stony beaches of the lake; (3) permanent swamps; (4) pools, borrow-pits, yaos; (5) ephemeral water-bodies. No. of species found

Biotope

1

2

3

4

5

1 2 3 4 5 6 7 8 Total sampling stations Mean no. of species per station

— — — 1 — — — — 1 4.0

— — — — 1 — 3 — 4 6.5

— — — 7 27 16 3 2 55 5.4

19 20 10 7 2 — — — 58 2.2

Total sampling stations 52 69 36 8 2 — — — 167 2.0

71 89 46 23 32 16 6 2 285 3.8

snails to ‘ecological slums’. But such species may also be regarded as successful specialists, taking advantage of resources beyond the reach of other molluscs.

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The relative numbers of different species of snail living in the same habitat are an indication of their comparative success, though a better insight is given by estimates of biomass and production. In smaller waterbodies the relative numbers of coexisting species may change greatly with the season and also over a longer time-scale with changes in the habitat, such as increase or decrease of shading vegetation. Populations of different species tended to fluctuate synchronously over a period of 18 months in a pond and a stream in Uganda (Cridland, 1957a,b; 1958), but in a ditch Lymnaea natalensis was replaced by Bulinus forskalii, apparently as a result of the ditch drying out temporarily. In Tanzania, B. forskalii and Ceratophallus natalensis appeared abruptly in a pond, became abundant and then disappeared (Pringle & Msangi, 1961; see also Chapter 11: Population fluctuations, numerical studies). An inverse relationship between the numbers of Bulinus obtusispira and B. liratus in a borrow-pit in Madagascar was related to changes in salinity (Chapter 10: Total dissolved salts). Fluctuations in the relative numbers of Bulinus ugandae and Biomphalaria sudanica in a ditch in Uganda were attributed to the effect of drought in causing many B. ugandae to move from a nearby swamp into the ditch (Berrie, 1964). Bulinus globosus replaced Biomphalaria pfeifferi almost entirely, over a period of a few months, in a newly constructed dam in northern Nigeria (Tayo & Jewsbury, 1978). Extensive data on numbers, biomass and production are available for Lake Chad, where the benthic molluscan fauna varies according to type of sediment and salinity (see earlier in this Chapter). From 3–7 species of prosobranch and bivalve occurred in a particular defined biotope (Daget & Lévêque, 1969; Lévêque, 1972; see also Chapter 11: Prosobranch biomass and production). The approximately linear relationship among the logarithms for both number of individuals and biomass for each species found in one biotope (soft clay) is illustrated in Fig. 134. Similar relationships were observed in other biotopes, and the slope of the regression line on log x (numbers or biomass) was characteristic for given biotope; it is partly dependent on the number of species and is thus an index of diversity. Molluscan faunas living in the main benthic biotopes of Lake Chad were definable by 3 parameters, number of species, total population density and a constant (Daget et al., 1972). These studies imply interesting interrelationships among coexisting populations of different molluscs; more of such investigations are desirable, giving attention to defining homogeneous biotopes and finding out if different species are in equilibrium. Instability is a common feature of freshwater snail faunas, and the possibilities of chance extinction and re-colonisation need taking into account when analysing the results of a local snail survey. Unfortunately the findings are likely soon to become out-of-date in detail. As precise data about distribution and abundance of intermediate hosts are required for effective planning of control of transmission of schistosomiasis, health authorities need experienced field workers continuously available to monitor snail faunas.

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Fig. 134. Relative abundance of different species of mollusc living on soft clay in Lake Chad. Logarithms for the numbers (a) and biomasses (b) of each species (numbered along the horizontal scale) are arranged in decreasing order from left to right (after Daget & Lévêque, 1969, Fig. 1A). B, Bellamya unicolor; C, Cleopatra bulimoides; M, Melanoides tuberculata: other points represent species of bivalve.

Associations among species Two or more species of snail may be commonly found together in the same habitat and such associations encouraged searches for ‘marker’ species, whose presence would indicate the suitability of a habitat for an intermediate host for schistosomes if one were not already present. Mozley (1944) found in Zimbabwe that Lymnaea natalensis was associated in decreasing frequency with B. pfeifferi, B. globosus and B. tropicus. L. natalensis was a good indicator of ecological suitability for B. pfeifferi also in Kenya (Van Someren, 1946) and Ethiopia (Brown, 1964). No particular association between these species was noted by Van Eeden & Combrinck (1966) in South Africa, where it appeared that areas in which L. natalensis was abundant relative to B. tropicus were potentialy suitable for ‘B. (Physopsis)’ (comprising both B. africanus and B. globosus). Yet the existence of ecological differences among these species is indicated by their responses to different temperature regimes (Prinsloo & Van Eeden, 1969, 1973) and their life cycles (Appleton, 1974b, 1978, p. 5). L. natalensis in fact occurs over extensive areas of the South African highveld and the highlands of eastern Africa where the B. africanus group seems to be excluded by too cool a climate (Chapter 11: Temperature). Positive associations among snail species can be used to predict their occurrence locally, but not on a regional scale. Only rarely, as in the case of an invasive species such as Lymnaea columella, will there be genuine grounds for predicting a significant increase in distribution.

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Negative associations have been sought as evidence of competition among species, which might be utilised against intermediate hosts for schistosomes. Disappointingly, recent analyses for hosts and non-hosts in Nigeria (Thomas & Tait, 1984; Ndifon & Ukoli, 1989) and Sudan (Madsen et al., 1988) provided no evidence of competitive exclusion. On the contrary, all significant associations were positive and microhabitat preferences appeared similar. Thomas & Tait (1984), however, suggested that feeding niches may not precisely overlap, and that potential competition could sometimes be restrained by checks on population increase by predation and other factors. Factors affecting local distribution Influences upon the distribution of freshwater snails may be divided into two groups, biotic (pertaining to living organisms) and abiotic (direct affects of physicochemical factors). An outstanding account of freshwater snail distribution is provided by Økland (1990), whose extensive investigations in Norway showed two main influences on the presence and abundance of snails, total water hardness (or calcium concentration) and aquatic macrovegetation. It may be that abiotic factors are generally more important on a regional scale than locally (Lodge et al., 1987), but in Africa their effects can be evident within small areas (within a single waterbody and among different waterbodies over distances of a few hundred metres). Examples for water chemistry and temperature are given in the introduction to Chapter 10, where these and other abiotic factors will be considered. Here we will look at three factors of particular importance locally, dispersal, relationships between snails and plants, and food sources. Dispersal and colonisation Passive transportation with consignments of aquarium fish and plants is an important means whereby snails are spread outside their natural geographic area (Madsen & Frandsen, 1989), and the activities of aquarists should be taken into account when studying the freshwater fauna near an African city. The main natural means of transportation are thought to be birds (snails on feet or in plumage), mammals (snails lodged in hooves or in mud on the body), and large aquatic insects (snails adhering to legs, wings or elytra). Such dispersal is observed only rarely; there appears to be no report of it in Africa, though Mienis (1977) presents circumstantial evidence that Bulinus truncatus was carried to an isolated pool in Israel by waterbirds. Within lakes and rivers snails are passively transported by floating aquatic plants and debris, and human activities. The invasive floating plant Salvinia played an important part in the colonisation by Biomphalaria pfeifferi of Lake Kariba (Hira, 1969, 1970). In Lake Volta, Bulinus rohlfsi was dispersed by the floating plants Pistia, Salvinia and Spirodela, sprigs of Ceratophyllum, twigs, fishing nets and fish traps (Odei, 1972, 1973). The upstream dispersal of

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Biomphalaria alexandrina in the Nile above Cairo may have depended on snails attached to boats or carried within automobile tyres used as boat fenders (Vrijenhoek & Graven, 1992). Passive dispersal of snails by water currents occurs both by flooding, when the velocity is high enough to sweep away adhering snails, and also by slower drifting as a result of the habit of some species, especially of pulmonates, to release their hold, rise to the surface and attach to the surface film. Snails behaving in this way could be searching for new food sources, though they may actually feed at the surface film, and possibly there is a deliberately dispersive element in the behaviour, as it seems to me that an unusually large proportion of Bulinus appear at the surface immediately after rain has first re-filled pools that were dry. Marked Biomphalaria and Bulinus were released into a vegetation-free canal flowing rapidly at 0.42 m s−1 and some were recovered as far as 4 km downstream after 1 day, but no marked snail was found upstream from the point of release (Dazo et al., 1966). Drifting with the current must also have been the most important means whereby marked specimens of B. globosus released in a stream in Tanzania travelled 100–120 m downstream within 3 days (Marti & Tanner, 1988). Experiments with marked B. globosus in small rivers in Zimbabwe (Woolhouse, 1988) showed that rain storms can deposit snails several hundred metres downstream from a densely-populated site. Active dispersal has been measured in a few situations. Daily movement by Lanistes nyassanus on the sandy bottom of Lake Malawi averaged about 3 m and was nondirectional (Louda & McKaye, 1982). Individual Biomphalaria pfeifferi travelled up to 66 cm within 24 hours on the shore of a reservoir (Thomas & Tait, 1984, p. 216). In a rapidly flowing canal, no marked Biomphalaria or Bulinus were found upstream from the point of release (Dazo et al., 1966), and only a single B. globosus moved upstream (a mere 50 cms) of a release point in a stream (Marti & Tanner, 1988). However, an 11-year study of the invasive snail Physa acuta in a stream in South Africa indicated an upstream migration rate of 2.5 km per year against a current sometimes exceeding 0.30 m s−1 (Appleton & Branch, 1989). Since an individual snail carries only part of the total genetic variation of its population, colonies established by the recent dispersal of a single snail or a small group of snails are expected to show reduced genetic diversity compared with their parental population. Vrijenhoek & Graven (1992) found evidence of this effect in Biomphalaria alexandrina in Egypt, where colonisation of the Upper Nile proceeded by a stepwise series of founder events, resulting in losses of allelic diversity at several polymorphic loci. The capacity for self-fertilisation possessed by snails such as Biomphalaria and Bulinus seems likely to favour the foundation of new colonies, and Madsen et al. (1983) point out that Helisoma duryi may be less able to spread because it seems obliged to cross-fertilise.

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Snails and plants The greatest species-diversities, though not necessarily the densest populations, of freshwater snails are usually associated with aquatic or subaquatic (emergent) leafy plants (macrophytes). There may be a symbiotic relationship between snails and aquatic macrophytes, evolved over a long period (Thomas, 1982, 1987). Plants provide snails with shelter from solar radiation and the water current, sources of food and egg-laying sites. The classic example is the important part played by Ceratophyllum in the ecology of Bulinus truncatus in Lake Volta (Odei, 1973; Klumpp & Chu, 1980). This snail was also common (and 8 other species were found) in Ceratophyllum beds in Lake Chad (Lévêque, 1975). Submerged weedbeds in sheltered bays of Lake Sibaya, South Africa, yielded 7 gastropod species (Appleton, 1977); the finding of egg capsules and juvenile snails indicated breeding at depths down to 4.5–5.0 m by Lymnaea natalensis, Biomphalaria pfeifferi, Bulinus natalensis and Burnupia sp. Oviposition by Bulinus globosus was concentrated on the leaves of Cyperus exaltatus in breeding ‘pockets’ more or less isolated from a stream in Tanzania (Marti et al., 1985). Breeding by this snail was associated with high abundance of Cyperus spp., Typha latifolia and Potamogeton thunbergii in Zimbabwe (Woolhouse & Chandiwana, 1989). Snail-plant associations differ among species and localities. In Nigeria Biomphalaria pfeifferi, for example, was positively associated with Commelina in a pond and with Nymphaea, Lemna and Ceratophyllum in a lake, but negatively associated with Salvinia (Thomas & Tait, 1984). Snail-plant associations observed in irrigation canals in Sudan included a positive association between B. pfeifferi and Potamogeton spp., but a negative association with floating plants, which tended to cover the water surface (Madsen et al., 1988). In south-western Nigeria most of the positive associations were with subaquatic plants (Ndifon & Ukoli, 1989), chiefly Alternanthera, Commelina and Paspalum. Although snails are attracted to aquatic plants, they do not readily consume fresh tissues, but feed mainly on decaying tissue, epiphytic organisms and adhering detritus. The earlier observations on snail-plant associations reviewed by Thomas & Tait (1984) are broadly in agreement with later results, but the causative mechanisms for differences among snail species have yet to be elucidated. The generally negative associations between snails and floating plants such as Salvinia, which densely cover the surface, may be due to the effect of shade in excluding submerged plants and decreasing the oxygenation of the water. Food The major portion by volume of crop contents from Biomphalaria pfeifferi living in a lake consisted of diatoms, detritus, bacteria and macrophyte

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fragments (Thomas & Tait, 1984). It is not known, however, to what extent the different components of such a varied diet may be digested and assimilated. Although the green alga Chlorella was readily ingested by Bulinus globosus and B. tropicus, it was not assimilated (Van Aardt & Wolmarans, 1981). Those snail species cultured in the laboratory appear readily to adapt to artificial diets (e.g. De Kock & Joubert, 1989). The most detailed description to date of the diets of freshwater snails in Africa under natural conditions is by Madsen (1992), for 5 species of pulmonate and 4 prosobranchs, living in irrigation canals and ponds in Sudan. Detritus was the major component of their stomach contents, and the other major food items were epiphytic algae and decaying macrophyte tissue (no fragments of fresh macrophyte were found in the stomach contents). All these species of snail had a similar diet; although blue-green algae were generally avoided, there was little evidence of any selection among the other algal species available in the habitats. This evidence for broad overlap among species of snail in their feeding niches suggests the possibility of competition for food. Poor food quality appeared to limit populations of B. globosus during most of the year in reservoirs near the Kenyan coast (O’Keeffe, 1985). Captive cohorts of snails were reared in netted enclosures and fed on different diets of natural vegetation; growth, reproduction and survival were compared among cohorts and with the natural populations in the reservoirs. The natural populations performed only as well as the least successful of the captive cohorts, while growth rate and reproduction were significantly higher in the cohorts provided with a high quality diet (water-lily leaf). It therefore appeared that the inferior demographic performance of the poorly-fed cohorts and the natural populations was foodlimited. The snails’ potential for increasing their population was realised only when heavy rain fell during cool months, and O’Keeffe suggested that run-off water replenished nutrients in the reservoirs and so increased the food-resource provided by the microflora. Good feeding conditions are not dependent on the presence of living macrophytes. While the beds of seasonal pools are dry they accumulate dead materials of plant and animal origin, and these rot after the pool is refilled, providing a rich food resource for snails emerged from aestivation. A correlation was observed in Eastern Zaire between the population dynamics of Biomphalaria pfeifferi and seasonal variation in the abundance and consumption of unicellular algae; the higher production of snails in an artificial channel than in a stream seemed to be related to the greater abundance of algae in the channel (Baluku et al., 1987). Dense snail populations can develop on bare substrates of mud, concrete, and stones. Discarded plastic bags are a favourite site where snails browse on the coating micro-organisms. Some species are favoured by moderate organic pollution (e.g. Ndifon & Ukoli, 1989); waste materials may provide food directly, while soluble nutrients increase the growth of micro-organisms.

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Lévêque, C. 1967. Mollusques aquatiques de la zone est du lac Tchad. Bulletin de l’Institut Fondamental d’Afrique Noire, 29:1494–1533. Lévêque, C. 1972. Mollusques benthiques du lac Tchad: écologie, étude des peuplements et estimation des biomasses. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 6:3–45. Lévêque, C. 1973. Dynamique et peuplements, biologie et estimation de la production des mollusques benthiques du lac Tchad. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 7:117–147. Lévêque, C. 1975. Mollusques des herbiers à Ceratophyllum du lac Tchad: biomasses et variations saisonnières de la densité. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 9:25–31. Lévêque, C., Dejoux, C. & Lauzanne, L. 1983. The benthic fauna: ecology, biomass and communities. In Lake Chad. Ecology and Productivity of a Shallow Tropical Ecosystem: 233–272. Carmouze, J.P., Durand, J.R. & Lévêque, C. (Eds). Monographiae Biologicae, 53. The Hague, Boston, Lancaster; W.Junk. Lodge, D.M., Brown, K.M., Klosiewski, S.P., Stein, R.A., Covich, A.P., Leathers, B.K. & Bronmark, C. 1987. Distribution of freshwater snails: spatial scale and the relative importance of physicochemical and biotic factors. American Malacological Bulletin, 5: 73–84. Loreau, M. & Baluku, B. 1987. Population dynamics of the freshwater snail Biomphalaria pfeifferi in eastern Zaire. Journal of Molluscan Studies, 53:249–265. Louda, S.M. & McKaye, K.R. 1982. Diurnal movements in populations of the prosobranch Lanistes nyassanus at Cape Maclear, Lake Malawi, Africa. Malacologia, 23:13–21. Madsen, H. 1992. Food selection by freshwater snails in the Gezira irrigation canals, Sudan. Hydrobiologia, 228:203–217. Madsen, H. & Frandsen, F. 1989. The spread of freshwater snails including those of medical and veterinary importance . Acta Tropica, 46:139–146. Madsen, H., Coulibaly, G. & Furu, P. 1987. Distribution of freshwater snails in the river Niger basin in Mali with special reference to the intermediate hosts of schistosomes. Hydrobiologia, 146:77–88. Madsen, H., Thiongo, W.A. & Ouma, J.H. 1983. Egg laying and growth in Helisoma duryi (Wetherby). Effect of population density and mode of fertilisation. Hydrobiologia, 106:185–191. Madsen, H., Daffalla, A.A., Karoum, K.O. & Frandsen, F. 1988. Distribution of freshwater snails in irrigation schemes in the Sudan. Journal of Applied Ecology, 25: 853–866. Mandahl-Barth, G., Ripert, C. & Raccurt, C. 1974. Nature du sous-sol, répartition des mollusques dulcaquicoles et foyers de bilharzioses intestinale et urinaire au BasZaire. Revue de Zoologie Africaine, 88:553–584. Marti, H.P. & Tanner, M. 1988. Field observations on the influence of low water velocities on drifting of Bulinus globosus. Hydrobiologia, 157:119–123. Marti, H.P., Tanner, M., Degrémont, A.A. & Freyvogel, T.A. 1985. Studies on the ecology of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara area, Tanzania. Acta Tropica, 42:171–187. McCullough, F.S., Webbe, G., Baalawy, S.S. & Maselle, S. 1972. An analysis of factors influencing the epidemiology and control of human schistosome infections in Mwanza, Tanzania. East African Medical Journal, 49:568–582.

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Thomas, J.D. 1987. An evaluation of the interactions between freshwater pulmonate snail hosts of human schistosomes and macrophytes. Philosophical Transactions of the Royal Society of London, B, 315:75–125. Thomas, J.D. & Tait, A.I. 1984. Control of the snail hosts of schistosomiasis by environmental manipulation: a field and laboratory appraisal in the Ibadan area, Nigeria. Philosophical Transactions of the Royal Society of London, B, 305: 201–253. Van Aardt, W.J. & Wolmarans, C.T. 1981. Evidence for non-assimilation of Chlorella by the African freshwater snail Bulinus (Physopsis) globosus. South African Journal of Science, 77:319–320. Van Eeden, J.A. & Combrinck, C. 1966. Distributional trends of 4 species of freshwater snails in South Africa with special reference to the intermediate hosts of bilharzia. Zoologica Africana, 2:95–109. Van Eeden, J.A., Allanson, B.R. & De Kock, K,N. 1964. The incidence and distribution of the intermediate hosts of bilharzia in the northern municipal area of Johannesburg and further north towards the Hartebeespoort Dam. Tydskrif vir Natuurwetenskappe, 4:52–66 (in Afrikaans, with English summary). Van Someren, V.D. 1946. The habitats and tolerance ranges of Lymnaea (Radix) caillaudi, the intermediate snail host of liverfluke in East Africa. Journal of Animal Ecology, 15: 170–197. Vrijenhoek, R.C. & Graven, M.A. 1992. Population genetics of Egyptian Biomphalaria alexandrina. Journal of Heredity, 83:255–261. White, P.T., Coleman, M. & Jupp, B.P. 1982. Swamp rice development, schistosomiasis and onchocerciasis in southeast Sierra Leone. American Journal of Tropical Medicine and Hygiene, 31:490–498. White, P.T., Gbakima, A.A. & Amara, S.V. 1989. Schistosoma mansoni in Sierra Leone: an invader extending its range? Annals of Tropical Medicine and Parasitology, 83: 191– 193. Wibaux-Charlois, M., Yelnik, A., Ibrahima, H., Samé-Ekobo, A. & Ripert, C. 1982. Etude epidémiologique de la bilharziose à S. haematobium dans le périmetre rizicole de Yagoua (Nord-Cameroun). 2. Distribution et écologie des hôtes intermédiaires. Bulletin de la Société de Pathologie exotique, 75:72–93. Woolhouse, M.E.J. 1988. Passive dispersal of Bulinus globosus. Annals of Tropical Medicine and Parasitology, 82:315–317. Woolhouse, M.E.J. & Chandiwana, S.K. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology, 98:21–34.

Chapter 10. Chemical and physical factors

Some factors influencing the local distribution of snails, particularly the biotic effects of plants and food supply, and dispersal ability, were considered in Chapter 9. The present chapter reviews the abiotic environment (physicochemical factors and habitat disturbance in the form of desiccation), with particular reference to observations on snail distribution and related laboratory experiments. These factors are considered further in Chapter 11, in relation to life cycles, growth and population dynamics. The three chapters are closely interrelated, since the successes and failures of local snail populations are reflected in the geographical distribution of their species. An investigator of freshwater snail distribution in Africa will learn much from the account by Økland (1990) of these organisms in Norway, which deals with small waterbodies as well as lakes. It may be misleading to make a distinction between factors determining freshwater snail distribution on a large scale and a small scale, as was attempted by Lodge et al. (1987). In Africa, at least, the same factor may be important at both the regional and local levels. Water chemistry may thus be important regionally, for reasons of underlying geological formation, while persistent snail populations are restricted to a few waterbodies among many within a single ‘dallol’ valley in Niger, because of wide variation in maximum levels of salinity among habitats (Grétillat & Gaston, 1975). Similarly, temperature is a major factor determining the geographical ranges of the species associated with either the tropical or the temperate climatic areas in southern Africa, and is also the significant factor in the micro-distribution of Biomphalaria within the coastal plain of north-eastern Natal (Appleton, 1977a,b). Physicochemical factors do not usually act simply and directly in determining snail distribution. Sometimes, one factor produces obvious mortality, for example a temporary shortage of oxygen or an increase in salinity. More commonly the establishment and survival of a population depends on a combination of circumstances. It is therefore of only limited value to determine the lethal level for a particular factor in the laboratory. A wider understanding of the distribution and varying abundance of a snail species results from knowledge of the ways in which its growth, reproduction and mortality respond to the range of conditions commonly encountered. The parameter ‘intrinsic rate of natural increase’ or rm provides an objective assessment of the performance of an

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organism under a particular set of conditions. Talling (1992) provides a major review of the physicochemical environment in African shallow waterbodies. Water chemistry Readings of pH are reported for many waterbodies, but it is difficult to interpret the biological significance of the measurement, which has not contributed much by itself to understanding the distributions of freshwater organisms (Macan, 1974, pp. 269–71). pH will not be given detailed consideration in the present account. In general, both diversity of species and abundance of individuals decrease towards the lower and upper extremes of dissolved chemical content. Two examples among local faunas were described in Chapter 9: in lower Zaire, no molluscs were found in brown-coloured waters on the plateau (Mandahl-Barth et al., 1974), while prosobranchs are excluded from the northern part of Lake Chad by high salinity (Lévêque, 1972). Yet the range of conditions under which a common species can thrive may be wide enough for there to be no evident correlation between water chemistry and snail distribution, even over extensive areas. Broad tolerance is possibly due partly to adaptation by local populations. Among species there is wide variation in their interaction with the chemical environment, presumably genetically determined, demonstrated by two examples of independence between the degree of calcification of the shell and the dissolved chemical content of the water. Both extremely light-shelled and extremely heavy-shelled species belonging to each of the genera Bellamya and Lanistes occur in Lake Malawi (Mandahl-Barth, 1972). The Jong River in Sierra Leone has very little dissolved calcium but supports dense populations of Sierraia (Bithyniidae), with heavily-calcified shells and opercula. Calcium Units of ionic concentration are given in various forms by different investigators. The concentration of an ion is often expressed in milliequivalents per litre (meq 1 −1), which is the weight of the ion in milligrams divided by its equivalent weight per litre (Beadle, 1981, p. 60). Another measure is millimoles (mM), or weight of ion in mg divided by atomic or molecular weight. In many studies, concentrations are given in parts per million (ppm), which is the same as milligrams per litre (mg 1−1). For calcium: 1 ppm or mg Ca++ 1−1=0.05 meq Ca++ 1−1=4 mg CaCO3 1−1=0.025 mM Ca++ 1−1. Data for the presence or absence of snails have produced some evidence for an influence by calcium on snail distribution. Chemical and physical factors were analysed by Schutte & Frank (1964) in 155 waterbodies situated to the east of the Drakensberg escarpment in an area of about 26 000 km2 in the south-eastern Transvaal. The waterbodies were divided into 4 categories:

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Fig. 135. Frequency of occurrence of snails in different types of water in SE Transvaal (after Schutte & Frank, 1964, Fig. 6A). Total number of localities examined in each category is given above each group of histograms.

very soft (0–10 ppm Ca); soft (11–30 ppm Ca); hard (over 30 ppm Ca); very hard (over 150 ppm CaCO3). Mean conductivities for these categories respectively were 54, 103, 216 and 696 µmhos. The hardness of the last group was frequently due not to calcium but to magnesium, according to Appleton (1978, p. 3). Snails of some kind were found in 80% of the very hard waters, but in only 30% of the very soft waters. Biomphalaria pfeifferi, Bulinus (‘Physopsis’) sp. and Lymnaea natalensis occurred in some waterbodies of all types, though with generally decreasing frequencies from very hard to very soft (Fig. 135). In the Bangweulu-Luapula region of south-eastern Zaire, only one or two species of snails occurred in the waters with the least concentrations of calcium, while 5 species lived in the hardest water, and 13 in the Luapula River where calcium was present in the intermediate range of 0.2–0.6 meq 1−1 (Symoens, 1968). In order to understand physicochemical influences better, it is helpful to record not only the presence or absence of a snail species, but also its population density, preferably through a complete annual cycle. This approach was taken by

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Williams (1970a) in a study of small waterbodies near Harare, Zimbabwe. Measurements of calcium and bicarbonate concentrations, and estimates of snail populations were made at monthly intervals over one year at 5 soft water stations, 6 medium water stations, and 3 hard water stations, classified as follows:

The densities of all snail species were very low in soft waters, high in medium waters and somewhat lower in hard waters. Bulinus globosus was present over the whole range of calcium bicarbonate concentration though most common in medium waters. Biomphalaria pfeifferi, however, was almost restricted to the medium and hard waters. This finding conforms with the observation by Schutte & Frank (1964) that B. pfeifferi was uncommon relative to Bulinus in very soft waters (Fig. 135). To supplement his observations on natural waterbodies, Williams (1970b) evaluated the effects of a wide range of calcium and bicarbonate concentrations in the laboratory, at a constant temperature of 25°C. B. globosus and B. pfeifferi were cultured in media containing 0–800 mg 1−1 of bicarbonate anions, and in other experiments with 0–50 mg 1−1 Ca (both ranges exceed those observed in the natural waters studied). One of the culture media was a natural ‘medium’ water, from Lake McIlwaine near Salisbury; other media were prepared from this water by dilution or the addition of analytical reagents. Each group of snails comprised a cohort of 50 individuals derived from two or three egg capsules, maintained at densities of 1–1.5 individuals per litre. The culture media were tested every two or three days, and the concentrations of ions were adjusted if necessary. From rates of fecundity and mortality it was calculated that both species achieved maximum values for the intrinsic rate of natural increase (rm) in the natural medium water from Lake McIlwaine. Concentrations of bicarbonate below 35 mg 1−1 were particularly unfavourable to B. pfeifferi, in agreement with the field observations (Harrison et al., 1970). Before Williams’ observations for B. pfeifferi were published, they were criticised by Harrison & Shiff (1966), who pointed out that the stocks of snails used were from Lake McIlwaine and thus they performed best in their own water, to which they might have been adapted. However, repeated experiments with snails originating from hard water habitats (Harrison & Shiff, 1966; Harrison et al., 1970) showed that the highest values for rm were again obtained in the medium water from Lake McIlwaine. It was also demonstrated (Harrison, 1968), according to rate of oxygen consumption, that a bicarbonate concentration of 35 mg 1−1 (within the ‘medium’ range of Williams) was favourable for all three stocks of B. pfeifferi regardless of differences in water chemistry among their localities of origin. The investigations by Harrison and colleagues thus confirmed Williams’ finding that moderate concentration of CaCO3 is most

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favourable to B. pfeifferi, though at the same time evidence was obtained that snails from different populations do not respond in exactly the same way to the same set of experimental conditions. In further experiments (Nduku & Harrison, 1976) snails were maintained, though without breeding, at 2 mg 1−1 Ca as bicarbonate. The importance of the bicarbonate ion was demonstrated by the poor performance of the snails when calcium was provided as sulphate. It is noteworthy that one of the strains of B. pfeifferi used by Nduku & Harrison was stated to be from ‘Tanga, Tanzania’, but the species is not known to occur near this town and the record should not be taken as precise (Harrison, 1977, in litt. to Brown). Examples of B. pfeifferi thriving in unusually soft natural waters come from Madagascar (2.9 ppm Ca, 38 µmhos; Pflüger, 1977) and eastern Zaire, where populations became established in artificial lakes created by mining activities, with 2.4–3.7 ppm Ca, 28–55 µmhos (Polderman et al., 1985). Low calcium concentration appears to be the direct or indirect cause of the poor snail fauna in three African lakes with exceptionally low salinities (conductivities 15–32 µmhos; 0.03–0.07 meq 1−1 Ca) (Beadle, 1981, pp. 65–67). Lake Lungwe, situated at an altitude of 2700 m to the west of the Ruzizi valley between Lakes Kivu and Tanganyika is small, with less than 1 km2 of open water; fish are not found, but the molluscs Gyraulus sp., Ferrissia (‘Gundlachia’) sp. and the bivalve Pisidium are present, though all have unusually thin and fragile shells (Marlier et al., quoted by Beadle, 1981). The much larger Lake Tumba (about 740 km2), situated in the central Zaire basin, has many species of fish and some groups of invertebrates are abundant, but not molluscs or crabs. Lake Nabugabo (about 20 km2) lies close to the western shore of Lake Victoria, but receives its water separately by drainage through swamps and, consequently, is much poorer in salts, having only 0.6 meq 1−1 Ca. Nabugabo has, however, a fairly rich invertebrate fauna and about 20 species of fish, including mollusc-eaters. No molluscs or crabs are found in the open water, but a few isolated and small colonies of snails live in swamp (Beadle, 1981, p. 66). As the concentrations of calcium in these lakes approach the minimum at which snails can maintain their calcium balance in the laboratory, Beadle suggests that the populations are specially vulnerable to predation. The few species present in Lake Lungwe may be able to exist there because predatory fish are absent. In Tumba and Nabugabo, where such fish occur, snails are either absent or confined to dense vegetation where they may be protected from predators. Other African waters with very little calcium and few molluscan species are: Debundsha Lake in Cameroon, conductivity 11–13 µmhos, Bulinus camerunensis only (Green et al., 1974); Opi Lake in Nigeria, Ca++ 1.8–3.2 mg 1−1, Ferrissia sp. only (Hare & Carter, 1984);

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Jong River in Sierra Leone, Ca++ 0.5–1.5 mg 1−1 (Wright, R., 1982), Sierraia leonensis and S. whitei only (Brown, 1988). The possibility that calcium was depleted by growing vegetation and thus caused the decline of a population of Bulinus senegalensis was noted by Goll & Wilkins (1984). Snail numbers were high at the beginning and end of the season when vegetation was sparse and Ca++ concentration was about 6.0 mg 1−1, but low in midseason when the vegetation was dense and Ca++ concentration dropped to about 1.0 mg 1−1. Besides the absolute concentration of calcium, its concentration relative to other ions has been investigated as a possible influence on snail distribution, but with inconclusive results. Ionic ratios quoted from studies reviewed here have been standardised as the proportion of Ca to another ion (as unity). In the eastern Transvaal a high proportion of sodium (Ca/Na ratio of less than 0.42) appeared unfavourable to Biomphalaria pfeifferi, though high magnesium concentration (Ca/Mg ratio of 0.12; calculated from Schutte & Frank, 1964, p. 397) did not. In Zimbabwe, however, a high proportion of magnesium seemed the likely cause of the rarity or lack of snails in streams situated in the Umvukwes Hills, north-west of Harare, and experiments were performed to test this hypothesis (Harrison et al., 1966). B. pfeifferi laid few eggs in stream waters with a Ca/Mg ratio of 0.08 and none in water with a ratio of 0.05. Adjustment of these ratios to 1.0 by the addition of calcium chloride produced a significant increase in egg production. This response was attributed by Harrison et al. (1966) to change in the Ca/Mg ratio, but Thomas et al. (1974) suggested that the effects were possibly due to changes in calcium concentration by itself. Further experiments, however, in which calcium concentration was kept constant, demonstrated adverse effects on B. pfeifferi of high proportions of magnesium, sodium and potassium on population dynamics (Nduku & Harrison, 1976), and of magnesium and sodium on biochemical responses of body tissues (Nduku & Harrison 1980a) and water relations (Nduku & Harrison, 1980b). Nduku & Harrison (1976) suggested that magnesium would tend to compete with calcium for absorption sites on the exposed body surface of a snail; they further commented that the less harmful effect of a high proportion of sodium was not surprising, as low calcium to sodium ratios are fairly common, especially in coastal regions. The presence of magnesite mining in Tunisia encouraged an investigation of the distribution of Bulinus truncatus in relation to variation in the Ca/Mg ratio (Meier-Brook et al., 1987). No correlation was evident; the entire range of Ca/ Mg ratios from 0.63–3.4 for the 53 sampling stations seemed well-tolerated. In experiments, a significant decline in egg production occurred only when the Ca/ Mg ratio was reduced below 0.2. In the field the distribution of B. truncatus appeared to be limited by the absolute concentrations of certain ions; Ca>425 ppm, Mg>135 ppm and chloride of about 600 ppm. The ‘softest’ water in Tunisia contained 97 ppm Ca, whereas only 5 ppm was the borderline between soft and medium waters as classified in Zimbabwe and water with >40 ppm Ca

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was ‘hard’ (Williams, 1970a; Harrison et al., 1970). This led Meier-Brook et al. (1987) to suggest that an inability to thrive in very hard water may be the reason why Biomphalaria is less widespread than B. truncatus in semi-arid areas of northern Africa, where electrolyte concentrations are generally high. Total dissolved chemical content (electrolyte content or salinity) For inland waters the salinity (also known as total dissolved chemical content or total electrolytes) is commonly estimated as electrical conductivity. Measurements are expressed as the reciprocal of the resistance (1/ohms×10−6 or µmhos) of 1 cm of water at a given temperature, usually 20°C (K20) (Beadle, 1981, p. 60). Waters may be divided into three classes according to their conductivity (Beadle, 1981, p. 71): very dilute (K20<40), the ‘freshwater’ range (K20 40–6000) and the hypersaline (K20>6000). Like pH, conductivity is a measurement that expresses a complex of chemical and physical variables, and it is no more than a guide to the factors which actually influence an organism. Salinity may also be expressed as parts per thousand (‰), in grams per volume of water, of total dissolved salts or sodium chloride alone (for seawater and brackish waters in coastal regions). Fresh waters termed brackish or saline in a narrow sense, are those in coastal regions which have their chemical content influenced by the sea, commonly by way of increased sodium chloride concentration. Among pulmonate snails only the Ellobiidae are successful in this environment, but several prosobranch families have members that thrive in waters of widely varying salinity on the coast of Africa. These prosobranchs (of the families Neritidae, Hydrobiidae, Pomatiopsidae, Assimineidae, Thiaridae and Potamididae) are characteristic of estuaries, lagoons and especially the mangrove habitat. This fauna and its ecology are reviewed by Plaziat (1982) and Zabi & Le Loeuff (1992). The estuarine environment extends a long way up some rivers in West Africa to nearly 280 km from the sea in the Gambia River, which is the lowest level at which a freshwater snail (Bellamya unicolor) has been found (Plaziat, 1982, Fig. 6). An exceptionally tolerant species is Tomichia ventricosa (Pomatiopsidae), which has adapted to fresh, brackish and hypersaline water on the southern coast (Davis, 1981, pp. 230–232). The effects of NaCl concentration and other aspects of salinity on freshwater pulmonate snails were reviewed by Madsen (1990). It appears that high salinity will rarely prevent the establishment of intermediate hosts for schistosomes in waters where the free-living stages of the parasite are likely to survive. Some ponds on the coastal plain of Tanzania have high chloride concentrations (Webbe & Msangi, 1958); 714–1120 ppm Cl were recorded in habitats for Bulinus globosus and Cleopatra ferruginea, and 468–2220 ppm Cl for B. nasutus. These concentrations exceed the upper limit of about 600 ppm Cl for B. truncatus in Tunisia (Meier-Brook et al., 1987). Marine influence was also evident in Zeekoe

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Vlei near Cape Town (Harrison, 1962), with 746 ppm Cl in 1947 when B. tropicus, Burnupia and Tomichia were living there. An inverse relationship between salinity and abundance of B. africanus was observed in the Manzimtoti lagoon system on the coast of Natal, where the survival of juvenile snails seemed to be inhibited by a salinity range of 2–6.6‰ (Donnelly et al., 1984). This was in accordance with the results of experiments, in which survival of hatchlings was adversely affected by salinity as low as 1.0‰ whereas adult snails were unaffected by concentrations below 3.5‰ (Donnelly et al., 1983). There is no clear point at which water becomes too saline to support a typical freshwater fauna and flora (Beadle, 1981, p. 334); an upper limit of about 5‰ salinity (total dissolved content) can be used as a practical definition of fresh water. Lake Turkana (Rudolf) (2.5‰) is the most saline of the large lakes to have a typical freshwater fauna according to Beadle (1981), though it must be added that few molluscan species live there. On comparing gastropod faunas in different African lakes (Chapter 12, Table 12.5), a progressive elimination of species is evident above a salinity of about 1‰ (1100 µmhos). Salinity varies widely within Lake Chad and was one of the influences on variation in distribution and abundance of benthic prosobranchs, demonstrated by observations made in 1968–72 (reviewed by Lévêque et al., 1983; see also Chapters 9 and 12: Lake Chad). The Chari River enters the southern shore and brings water with a low conductivity of about 90 µmhos. Due to rapid evaporation, salinity increases with distance from the Chari Delta and reached about 600 µmhos near the northern shore in 1969–70. During this period benthic prosobranchs were abundant on some areas of the bottom sediments, but were rare or absent wherever conductivity exceeded 550 µmhos (Fig. 136). Too little salinity also seemed unfavourable for Bellamya (Fig. 136), which was found only rarely near the Chari delta and not at all in the smaller Lake Léré, where conductivity was similarly low (Dejoux et al., 1971a). Examples of the influence of salinity on snail distribution and local abundance in smaller waterbodies are provided by investigations in Niger, South Africa and Tunisia. The dallols of Niger are ‘fossil valleys’ draining from the Sahara towards the Niger River. Various species of aquatic snail are widespread in the dallols during the rainy season (Grétillat & Gaston, 1975), but during the dry season (November to April) salinity increases by evaporation until all snails are killed in the residual lakes and pools on the valley floors. Snails survive only at the valley sides in a few pools supplied by freshwater springs. Biomphalaria pfeifferi and Bulinus truncatus were more tolerant of salinity than B. forskalii and Afrogyrus coretus, while Lymnaea natalensis was the most sensitive species. With the onset of the rains, snails spread from the refuges and re-colonise the valleys, allowing seasonal though important transmission of trematode parasites. The decline of B. africanus in a pool on the South African highveld was associated with an almost three-fold increase in salinity, due to drought (Pretorius et al., 1982). In southern Tunisia, B. truncatus (the only pulmonate found) occurred in waters with a salinity range of 1220–2440 µmhos at 18°C

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Fig. 136. Abundance of benthic prosobranchs in ‘normal’ Lake Chad (1968) in relation to salinity (after Lévêque, 1972, Fig. 4).

(Meier-Brook et al., 1987); all the prosobranchs found were more tolerant of salinity, the upper limit being 10 500 µmhos for Mercuria, Hydrobia and Melanoides tuberculata. Examples of the association in some habitats between low salinity and a poor snail fauna, believed to be due primarily to shortage of calcium, have been considered in the preceding section. The outstanding contrary example of adaptation to very soft water is the genus Sierraia, which produces dense populations in West African rivers with hardly any dissolved chemical content. Investigations of snail distribution carried out in detail at the Mangoky Irrigation Project, south-western Madagascar (Degrémont, 1973) provide much data about waters of high conductivity, and demonstrate interesting differences among the responses of 3 species of Bulinus. During the year 1971, 119 sites were sampled once or twice each month, and a further 186 sites were sampled at least 3 times. Sites in which no snails were found or where some species (not Bulinus) were present occasionally (categories A and B of Degrémont), had relatively high conductivities (averaging 1005 µmhos for site means). Melanoides tuberculata showed the widest tolerance, occurring in canal water of conductivity 200 µmhos and in a saline lake of 20 000 µmhos. Bulinus bavayi lived in some sites with high conductivities averaging over 1000 µmhos; however, this level fell considerably during the rainy season, and during the dry season when salinity was particularly high in the residual water, the snails were probably aestivating. B. liratus tolerated a wider range of salinity (150–1500 µmhos) and bred in the laboratory in water of conductivity 2100 µmhos. In

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contrast, B. obtusispira did not establish populations where conductivity exceeded 600 µmhos, while hatching and development of young were inhibited at higher salinity in the laboratory. In some of the Mangoky localities where both B. liratus and B. obtusispira occurred, they showed asynchronous changes in population density, corresponding to changes in salinity. Attention was drawn to variation among conspecific snail populations in their physiological characteristics by Harrison (1966, 1968) and Harrison & Shiff (1966) with particular reference to Biomphalaria pfeifferi. Yet a moderate concentration of CaCO3 was generally favourable, regardless of chemical conditions in localities where snails came from (see the preceding section: Calcium). Similarly, a laboratory culture of this species originating from a pool with a conductivity of only 50 µmhos performed best, according to rm values, over the range 300–400 µmhos (Jennings et al., 1973). It therefore seems that although local adaptation is likely to play a part in the occasional success of B. pfeifferi in habitats with unusually low conductivities, the capacity is retained to benefit from any increase in chemical resources. It may be that the change from high to low conductivity is more stressful, for about one-third of Bulinus africanus from a South African Dam (837 µmhos) died when transferred to an aquarium water of 223 µmhos, whereas all the snails from a river (74 µmhos) survived the change (Heeg, 1975). A two-stage process of acclimation, in which snails from the dam spent 7 days in each of 2 intermediate waters (584 and 415 µmhos), eliminated the high mortality. Although B. truncatus was not found in Tunisia in natural waters of conductivity more than 2440 µmhos, a staged process of acclimation to higher salinity resulted in egg-laying in conductivity of 3900 µmhos (calculated from Meier-Brook et al., 1987, Fig. 5). In conclusion, field studies in Africa suggest that the concentration of dissolved salts limits the distribution of pulmonate snails when it is unusually high or low. The importance of calcium is supported by experiments in the laboratory, though it is difficult to separate its influence from those of carbonate and other ions. Excess of magnesium seems unfavourable for Biomphalaria pfeifferi and this snail is generally less tolerant of soft water than the Bulinus africanus group; yet some populations of B. pfeifferi thrive in soft water, possibly as a result of local adaptation. Over large areas of Africa, however, the range of chemical variation encountered in waterbodies lies within the tolerance of pulmonate species, and it is their abundance and life cycles, rather than presence or absence, that are affected by water chemistry. There is a much greater range of chemical tolerance among the prosobranchs. A species of Tomichia thrives in habitats that vary from fresh water to practically brine, while at the other extreme Sierraia builds heavy shells in rivers of almost pure rainwater. Prosobranchs are the dominant gastropods in coastal brackish waters, but even they are excluded from some inland lakes of high salinity.

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Turbidity Turbid water (opaque with suspended matter) may have adverse effects upon snails. Water from a stream in Zimbabwe with 360 mg 1−1 suspended solids (mainly the minerals illite and sericite) prevented development and hatching of eggs of Biomphalaria pfeifferi (Harrison & Farina, 1965). Yet neither Bulinus globosus nor Lymnaea natalensis were adversely affected at this concentration, and eggs of all three species hatched normally when the water was diluted to 190 mg 1−1. Turbidity was one of the factors thought to limit benthic snail populations in Lake Chad (Dejoux et al., 1971b). Oviposition by B. truncatus (=rohlfsi) was suppressed during periods of high turbidity in water above mud, caused primarily by suspended clay (Klumpp et al., 1985). Sometimes turbidity appears to be beneficial. I have seen B. nasutus egglaying freely in thickly muddied water after emerging from aestivation in western Kenya, while B. senegalensis was most abundant during a period of high turbidity in a reservoir in Nigeria (Betterton et al., 1988). Abundance of B. truncatus in fishponds in Cameroon was also associated with high turbidity, which was believed to indicate a high nutritional level (Slootweg et al., 1993). Oxygen Field studies and laboratory experiments indicate that snail distribution may be limited by a low level of dissolved oxygen. All species of limpet belonging to the genus Burnupia seem to have a particularly high requirement for oxygen, as they are almost entirely confined to perennial well-oxygenated streams and lake shores exposed to wave-action. Yet species characteristic of seasonal waterbodies, where aestivation is essential, are capable of reducing their oxygen consumption rate to a low level during long periods of dormancy, possibly by change to a different metabolic pathway (Heeg, 1977; and section on Desiccation in this Chapter). Atmospheric air is commonly taken into the mantle cavity by pulmonates, though oxygen is also absorbed through the general body surface, especially the pseudobranch, which is particularly elaborate in Bulinus. The presence of a type of haemoglobin in the blood of the Planorbidae further increases efficiency in respiration. Prosobranchs of the family Ampullariidae, of which some species emerge from the water to lay their eggs, have the mantle cavity divided into two compartments, one with a gill and the other serving as a lung. The level of oxygenation may be an important influence on distribution within habitats. There is a zone of high oxygen concentration available to snails immediately beneath the floating leaves of water-lily (Nymphaea spp.; Wright, C.A., 1956). Unfavourable conditions, however, can be caused by dense floating vegetation preventing snails from reaching the surface when there is shortage of dissolved oxygen. The death of many B. globosus was associated with mats of Azolla in Ghana (McCullough, 1957) and the grass Leersia in Lake Chilwa

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(Cantrell, 1981). The water column beneath densely-packed floating plants such as Pistia and Salvinia can be anoxic (Thomas & Tait, 1984, p. 234), apparently because the exclusion of light reduces photosynthesis by submerged plants. Low oxygen concentration (<2.5 ppm) below a mat of floating Ludwigia apparently caused the temporary disappearance of Biomphalaria pfeifferi and interrupted transmission of schistosomiasis (Donnelly & Appleton, 1985). A negative association was observed between snails and the emergent plants covering the surface of canals and creating poor oxygen conditions (Madsen et al., 1988). Papyrus swamps are extensive areas of habitat with little if any dissolved oxygen (Jones, 1964). Biomphalaria sudanica is the only planorbid to occur abundantly, though Pila ovata may be common at the margins. An indirect effect of poor oxygenation in the waters of papyrus swamps and other habitats, is the reddish-brown precipitate of ferric hydroxide formed by certain bacteria. Van Someren (1946) suggested that a contributory factor to the rarity of snails in many such localities could be a shortage of food, caused by the adverse effect of colloidal iron on the growth of algae. In the laboratory, B. globosus showed a clear preference for high oxygen concentration (Van Aardt & Frey, 1979), though oxygen consumption was reduced in relation to deteriorating concentration in the water (Van Aardt & Frey, 1981). The mobility of B. globosus was reduced by low oxygen concentration in experiments, providing an explanation for the inability of the snails to escape from deteriorating oxygenation in a marsh by migrating into open water (Cantrell, 1981). Many though not all pulmonate species regularly visit the water surface to replenish the air bubble in the mantle cavity. Dives to deeper water by Biomphalaria sudanica averaged 38 minutes in well-aerated water, but only 24 minutes when dissolved oxygen was lacking (Jones, 1964). Most Bulinus globosus remained at the surface when oxygen concentration was low, though they dived frequently to the bottom in oxygen-saturated water (Van Aardt & Frey, 1979). Oxygen requirement can, however, be supplied by cutaneous respiration alone under a range of conditions of oxygen concentration and temperature (Alberts, 1966). Further experiments by Alberts (1966), in which snails deprived of their air bubble were allowed access to nitrogen, suggested that the presence of a bubble, even though it contains no oxygen, enables a snail to switch from aerobic to anaerobic respiration. Respiration is aerobic, however, during aestivation (Heeg, 1977). A need to renew the air bubble seems likely to be a factor restricting the depth to which most pulmonate species can live. Yet some species of Biomphalaria and Ceratophallus descend to depths of between 6–18 m (20–60 feet) in East African lakes, while Bulinus nyassanus has been dredged from 90 m (300 feet) in Lake Malawi; these species presumably can live without access to atmospheric air. Biomphalaria, Bulinus and other pulmonates were found by Appleton (1977c) living down to depths of 4.5–5.0 m in submerged weedbeds in Lake

494 CHEMICAL AND PHYSICAL FACTORS

Sibaya; since the weed fronds did not reach the surface it appeared that these snails did not migrate to the surface, but obtained their oxygen solely by cutaneous respiration among the weeds, where dissolved oxygen was high due to photosynthesis. Prosobranchs are much more successful in exploiting the opportunities for life on the bottom sediments of large African lakes, but lack of oxygen limits the depth to which they can live in deeper lakes such as Kivu and Tanganyika (Chapter 12). Pollution may deplete dissolved oxygen to a level that excludes snails. No oxygen was detectable immediately below the entry of effluent into a stream in Nigeria (Smith, 1982); snails were absent from the worst affected area, and although a few individuals survived in very low oxygen concentration, breeding was observed only further downstream. Temperature The influence of temperature on life cycles and population dynamics is described in Chapter 11. Here we will discuss snail distribution in nature in relation to data for climatic temperature and the responses of snails to different temperature regimes in the laboratory; in this respect the best-studied snails are Bulinus globosus and Biomphalaria pfeifferi. The power of temperature to limit distribution was simply demonstrated by Pitchford & Visser (1969), who observed that B. (Physopsis) sp. (probably B. globosus) maintained in outdoor aquaria in localities in South Africa outside the normal area of distribution were all killed during the winter when night temperatures fell repeatedly below freezing. B. africanus survived constant low temperatures of 0–8°C in the laboratory longer than either B. globosus or Biomphalaria pfeifferi, though no snail lived for more than 8 days at 8°C (Joubert, Pretorius et al., 1984). Greater tolerance of constant low temperature was shown by Bulinus tropicus and Lymnaea natalensis, which survived respectively for 31 days and about 16 days at 4°C (Joubert et al., 1986). When B. africanus, B. globosus and Biomphalaria pfeifferi were exposed to constant high temperatures of 34–40°C, B. globosus survived the longest, for a maximum of 40 days at 34°C (Joubert, Pretorius et al., 1986). High summer temperature of 39– 40°C caused great mortality of snails in a stream in Mali (Coulibaly & Madsen, 1990). Clearly snails may be killed by temperatures above or below lethal limits, but it is not easy to assess this direct mortality in the field, because there are considerable temperature gradients within even a small waterbody, and snails can seek the microhabitats where temperature is most favourable (Shiff, 1966). A further complexity is that temperature influences snail distribution through its effects on reproduction and growth of juveniles, as well as on the survival of adults. There is little or no breeding by B. globosus and Biomphalaria pfeifferi during the winter in subtropical areas such as the plateau of Zimbabwe and the lowveld

FRESHWATER SNAILS OF AFRICA 495

Fig. 137. Fecundity of Biomphalaria pfeifferi over a 10-week experimental period at 6 above-optimal temperature regimes (from about 2 to 75 degree hours above 27°C per day). Vertical bars indicate the standard errors. From Appleton & Eriksson (1984, Fig. 3). Temperature fluctuated daily in the experimental regimes. Pooled data for 60 snails up to 4.5 mm diameter at the beginning of the experiments. The fall in fecundity (viable eggs) under warmer conditions was accompanied by an increase in production of infertile eggs. The two warmer regimes approximated to conditions in habitats on the coastal plain of northern Natal that were not inhabitated by B. pfeifferi, thus supporting the conclusion from field observations that warm temperature is an important factor limiting the occurrence of this snail.

of south-eastern Transvaal (Shiff, 1964b,c; Appleton, 1974; Woolhouse & Chandiwana, 1989). Mark-recapture data obtained in Zimbabwe show the recruitment rate into B. pfeifferi populations to increase over the range 13–24°C (Woolhouse, 1992). It may be supposed that under the even cooler climatic conditions of the temperate region of southern Africa, the potential breeding season is so short that persistent populations cannot be maintained. At the other extreme, the adverse effects of high temperature on the growth, fecundity and survival of Biomphalaria pfeifferi observed in the laboratory led Sturrock (1966) to suggest that the snails’ absence from suitable habitats on the coastal plain of East Africa might be due to high temperature there. In Madagascar too it was early suspected that the rarity of B. pfeifferi in the warmer regions of the south and west was due to the adverse effects of high temperature (Brygoo, 1967). Further and substantial evidence for the vulnerability of B. pfeifferi to high temperature comes from investigations that link the restricted occurrence of this snail on the coastal plain of north-eastern Natal to the adverse effects on fecundity of the high temperature in shallow habitats (Appleton, 1977a,b). Experiments with young snails under fluctuating above-optimal temperature regimes (simulating natural conditions) showed a sharp fall in egg production (Fig. 137) at high levels of degree-hours above 27°C per day, due to the impaired development of the ovotestis (Appleton & Eriksson, 1984). The level of warmth

496 CHEMICAL AND PHYSICAL FACTORS

for maximum fecundity in the laboratory was higher than the critical upper level estimated for successful population maintenance in the field; this was explained by supposing that the short periods of intensely hot weather experienced in the field were more damaging to the snails than longer exposure to lower levels of above-optimal heat in the laboratory. For cohorts of Bulinus globosus reared in reservoirs on the Kenyan coast, rm was inversely related to increasing mean water-temperature above 25°C (O’Keeffe, 1985). At mean temperatures above 28.5°C the rm was negative (Chapter 11, Fig. 142), indicating that such cohorts were unable to increase, and these habitats appeared to be sub-optimal for B. globosus except during the cooler months of the year. Therefore it seems that this snail may be excluded by high temperature from some waterbodies in the coastal area of Kenya. Even so, B. globosus seems better adapted to high temperature than Biomphalaria pfeifferi, which is absent from the entire area; and on the coastal plain of Natal B. globosus occurs in shallow habitats that are too warm for Biomphalaria. Optimal temperature for B. globosus in the laboratory lies at about 25°C according to a distinct peak for rm values (evidence reviewed by Appleton, 1978), whereas for B. pfeifferi there is a plateau of optimality ranging from about 20°– 29°C (De Kock & Van Eeden, 1981; Appleton & Eriksson, 1984). B. globosus seems well adapted to multiply rapidly during brief periods of optimal conditions, by virtue of its sensitivity to changing temperature and high innate capacity for increase, and thus to survive in temporary waterbodies. B. pfeifferi on the other hand seems more suited to the stable conditions of permanent waterbodies such as isolated pools fed by perennial springs (De Kock & Van Eeden, 1981). Comparison between the distributions of B. globosus and B. africanus in southeastern Africa suggests that the latter species is the more tolerant of cool conditions (Brown, 1966). Support for this view came from experiments by De Kock (1973; cited by Appleton, 1978) which showed peak values for rm in the temperature range of 26–28°C for B. globosus and 23–26°C for B. africanus. In accordance with these results, B. africanus survived longest at low temperatures (Joubert, Pretorius et al., 1984), while B. globosus survived longest at high temperatures (Joubert, Pretorius et al., 1986). Other experimental investigations of temperature in relation to geographical distribution have been made for Lymnaea natalensis and B. tropicus. The performance of the latter in experiments was in keeping with its abundance in the cooler southern regions of Africa, including the highveld and the highlands of Lesotho, where this snail is often the only one living in temporary vleis (marshes), seasonal streams and farm dams. The high rm observed under warm conditions (Prinsloo & Van Eeden, 1969; De Kock & Van Eeden, 1985), would allow rapid repopulation after a dry habitat is refilled by the summer rain. On the other hand, a good tolerance of low temperature allows B. tropicus to survive and even breed during cool winters (Stiglingh & Van Eeden, 1977; Joubert et al., 1986) in areas where night temperature often falls to freezing point. The low rm

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values observed by Prinsloo & Van Eeden (1969) for Lymnaea natalensis at higher temperatures were not consistent with its natural distribution, known to be concentrated in the warmer rather than the cooler areas of southern Africa; to explain this discrepancy, Appleton (1978) and Brown (1980) alluded to the fact that L. natalensis breeds during the cooler months in the subtropical eastern Transvaal (Appleton, 1974). But the higher rm values reported for this species by De Kock & Van Eeden (1985) indicate an optimal temperature of 20–26°C and are more consistent with its natural distribution; these workers concluded that the snail is adapted to permanent waterbodies and this accords with my own knowledge of its habitats. However, there does not seem to me to be a basis for the further conclusions of De Kock & Van Eeden (1985), that temperature is of less importance in governing the distribution of L. natalensis than B. tropicus, and moreover that hardly any area of South Africa is unsuitable in respect of its temperature for colonisation by both these species. Joubert et al. (1986) showed L. natalensis to be somewhat less tolerant than B. tropicus of low temperature, and commented that where the former occurs in the cooler areas of South Africa it does so mostly in permanent waterbodies, where temperature would not fall so low as in the small seasonal habitats of B. tropicus. The invasive Physa acuta has colonised many river systems in South Africa; this snail’s ability rapidly to repopulate habitats denuded of snails by flooding has been linked to the effects on its reproductive potential of temperature in the laboratory (Brackenbury & Appleton, 1991). At different constant temperatures (15, 25 and 28°C) the acceleration of gametogensis in response to increasing temperature was more rapid than for the indigenous B. tropicus. This, together with greater fecundity and a shorter incubation period could give P. acuta a reproductive advantage over the indigenous species, and contribute to the success of the invader. Caution is needed in making use of data from experiments on snails at constant temperature to explain their distribution in nature, for water temperature is rarely constant for long in natural shallow waterbodies. Fecundity at room temperature exceeded that observed at any constant temperature (Shiff & Garnett, 1967), suggesting that temperature fluctuations have an important stimulatory effect upon egg production. This was supported by experiments with temperature regimes incorporating daily fluctuations, in which Lymnaea natalensis, Bulinus tropicus and Biomphalaria pfeifferi all produced their best reproductive performance under the oscillating regime of 5°C above and below 23°C (De Kock, 1985; De Kock & Van Eeden, 1986). Another influence on the distribution of snails in the field is the spatial variation of temperature within waterbodies, resulting for example from depth and shading. Snails may be able to move among different microhabitats according to the availability of favourable temperature. During sunny winter days on the plateau of Zimbabwe the surface layer of a pond can be several degrees warmer than the bottom (Shiff, 1966); a greater proportion of populations of Bulinus globosus, Biomphalaria pfeifferi and Lymnaea natalensis

498 CHEMICAL AND PHYSICAL FACTORS

were present within 25 cm of the surface in winter than in summer. Experiments with B. globosus in choice chambers showed a significant movement of snails into the warmer zones within 2–5.5 hours; the snails responded to temperature differences of 4°C and perhaps less. When high water temperature approaches a lethal level for snails, a substratum of mud may provide a cooler refuge (Klumpp et al., 1985). More information is needed about seasonal and geographical variation in water temperature. The temperature regime within a small lake in Ghana was described in detail by Thomas & Ratcliffe (1973), but without analysing the distribution of snails. Maximum information is yielded by continuous recording devices over periods of at least one year. Particularly useful measurements are the amount of heat experienced at a site in degree-hours and the magnitude of brief periods of unusually high or low temperature. A valuable investigation was carried out by Appleton (1976) for a small stream, the Gladdespruit, which descends from the Drakensberg in south-eastern Transvaal (see also Chapter 9: South-East Transvaal). Continuous temperature readings were gathered for about two years from localities distributed over 40 km, covering an altitudinal range from 655 m to 1242 m. Degree-hours per week (deg-h/wk) were compared between the main stream, a backwater and a detached pool. Appleton regarded current speed as the major factor determining the upper altitudinal limits for snail species in the Gladdespruit, but temperature also seems to play a part. The lowest constant temperature at which Bulinus globosus could maintain a population in the laboratory was 18°C (Shiff, 1964a), which is the equivalent of about 3000 deg-h/wk. Appleton recorded an average of 3200 deg-h/wk over 55 weeks in a pool at 831 m situated close to the highest locality where B. globosus was found. Thus observations in the laboratory and the field are consistent with the view that in this area the distribution of B. globosus is limited by a too cool climate. Continuous recording was also used (Appleton, 1977a) to analyse temperature regimes in different types of habitat on the coastal plain of north-eastern Natal, in relation to the distribution of Biomphalaria pfeifferi. We have already referred to the absence of this species from shallow pans in this area, explained by the relatively high thermal regime and its adverse effect on the fecundity of the snail. Temperature rose almost as high as in the shallow pans at the surface of the deeper pans where B. pfeifferi did occur, but cooler water was available to the snails at greater depth. In conclusion, temperature appears to be a major factor in the distribution of freshwater snails in Africa. Although experimental data to support this view are available only for a few pulmonate species, it seems that decline in ambient temperature with increasing altitude and, in southern Africa, latitude, limits the geographical range of species that are adapted to tropical conditions. On the other hand, too warm conditions apparently restrict the occurrence of Biomphalaria pfeifferi, even though it is widely distributed in the tropical region. Differences among some species in the effects on their population dynamics of

FRESHWATER SNAILS OF AFRICA 499

different temperature regimes in the laboratory can be interpreted as showing adaptation to either permanent or temporary habitats. However, experimental investigations need to take into account the physiological effects of fluctuating temperature, daily and seasonal, and also temperature variation within a habitat at any one time. The value of obtaining comprehensive temperature data in the field as well as in the laboratory is demonstrated by the insight gained into the microdistribution of B. pfeifferi on the coastal plain of Natal. Desiccation Surface water commonly disappears from small waterbodies, either regularly according to seasonal rainfall, or occasionally due to prolonged drought. Desiccation is a catastrophe for a snail population and it is the major restraint on the number of species that live in seasonal waterbodies; often only one or two are found. Some African freshwater snails have a remarkable ability to survive the absence of surface water and their surprising reappearance soon after rain has refilled a previously dry locality has often been reported (early literature reviewed by Appleton, 1978). Survival through the dry season is important in the success of Bulinus (Chapter 7: Aestivation). A distinction was drawn (Richards, 1967) between diapause (spontaneous climbing out of water and entering a state of dormancy) and aestivation (prolonged survival by dormant snails out of water). A third type of behaviour, spontaneous and short-term, has been distinguished as ‘water-quitting’ (Green et al., 1992). Diapause and water-quitting are of interest in relation to the avoidance by snails of molluscicide, but this behaviour is little known for African species. Here we consider the long-term survival of snails through periods of seasonal desiccation in Africa, referred to as aestivation (for remarks on the definition and usage of this term see Chapter 7: Aestivation). Table 10.1. Common African freshwater snails arranged in three groups according to their ability to aestivate, as indicated by their habitat. A. Good aestivators

B. Moderately successful aestivators

C. Poor aestivators

Lanistes spp. Pila ovata Lymnaea truncatula Bulinus nasutus B. reticulatus B. scalaris B. senegalensis B. tropicus B. forskalii Ceratophallus natalensis

Lymnaea natalensis Bulinus africanus B. globosus B. truncatus Biomphalaria pfeifferi Bi. sudanica Segmentorbis kanisaensis

Melanoides tuberculata Gyraulus costulatus Lentorbis junodi Segmentorbis angustus Burnupia spp.

500 CHEMICAL AND PHYSICAL FACTORS

A. Good aestivators

B. Moderately successful aestivators

C. Poor aestivators

Ferrissia spp. A. Occurring in ephemeral waters that may not be recognisable as aquatic habitats in the dry season. B. Localities with aquatic or marginal vegetation that retains a distinctive appearance during the dry season. C. Localities with a comparatively stable volume of water; there may be a well developed aquatic flora.

The record for long aestivation is held by Lanistes ovum, which emerged from lumps of dried mud when placed in water two years after collection in Angola (Morelet, 1868, quoted by Pilsbry & Bequaert, 1927, p. 544). B. tropicus is claimed to have survived in dry pans for 18 months (Annecke & Peacock, 1951). Other long periods reported are 5–8 months for Bulinus nasutus and B. globosus (Webbe & Msangi, 1958), 6–7 months for B. senegalensis (Smithers, 1956) and 7 months for B. obtusispira (Degrémont, 1973). Prosobranchs might be expected to aestivate more successfully than pulmonates, by virtue of their ability to close the aperture by the operculum, but this does not seem to confer any general advantage. Although Pila ovata is common in seasonally filled pools in western Kenya, several species of Planorbidae also are abundant. Commonly occurring snails may be grouped according to their capacities for aestivation (Table 10.1). According to this scheme good aestivators can live where a potential waterbody may not be recognisable during the dry season, for water is present too briefly for characteristic vegetation to develop. Moderately successful aestivators are found in localities where at least a semi-aquatic vegetation is seen. The species least tolerant of desiccation are taken to be those restricted to perennial watercourses, permanent swamps or pools with a rich fully-aquatic flora. Survival time out of water for eggs is generally poor apart from the species of Pila, which lay hard-shelled eggs above the water surface. The categories in Table 10.1 are not to be thought of as clearly distinct, and within them considerable variation in aestivating ability is to be expected. There is probably a general correlation between success in aestivation and a high capacity for increase (rm), enabling rapid repopulation of a habitat when water returns. Rates of egg-laying and feeding were higher for Bulinus recently emerged from aestivation than for controls (Matovu & Nditi, 1978; Oyeyi & Ndifon, 1990). Some individual Ferrissia, of several species, modify the shell apparently in anticipation of aestivation. Their aperture is reduced from its normal size by the growth of a septum (Fig. 85a), formed in response to stimuli that precede drying of the habitat, including high temperature, low oxygen tension and high organic content in the water (Richardot, 1977). The apparent rarity of septate Ferrissia in tropical Africa is perhaps due to their short period of activity if they die soon after emerging from aestivation. The formation of apertural lamellae by some

FRESHWATER SNAILS OF AFRICA 501

individuals of Biomphalaria glabrata of South America is associated with emergence from water and possibly enhances survival through a long period of aestivation (Richards, 1968; Pieri & Thomas, 1986; Dannemann & Pieri, 1993). Lamellate Biomphalaria have been found in few populations in Africa (MandahlBarth, 1958, p. 15; McCullough, 1958); no connection with aestivation has been demonstrated, but there could be some adaptive value as lamellate individuals may be quite common locally (McCullough found 15% lamellate among 353 shells from one locality in Ghana). Field observations on pre-aestivation behaviour by Bulinus indicate two different strategies. B. nasutus in Tanzania and B. senegalensis in Gambia aestivated around the margins of temporary pools (Webbe, 1962; Goll & Wilkins, 1984). This behaviour seems to be adaptive in preventing snails from being revived by isolated showers at the beginning of the rainy season and in enabling them to emerge only when the pools are well filled. B. truncatus (=rohlfsi) and B. globosus in northern Nigeria aestivated towards the bottom of drying-out habitats and both species were prematurely revived by early rainstorms; it appeared that the infrequent occurrence of B. globosus in northern Nigeria might be due to the unsuitability of its aestivation behaviour for life in small pools receiving unpredictable rainfall (Betterton et al., 1988). Aestivating behaviour is evidently stimulated before the final disappearance of water (Webbe, 1962; Goll & Wilkins, 1984), though B. truncatus did not begin aestivating in a reservoir until late in the dry season, when the area of water had contracted considerably (Betterton et al., 1988). The stimulatory factors are still obscure; fall in water temperature and increasing salinity due to evaporation could be involved (Betterton et al., 1983). None of the physical parameters monitored by Betterton et al. (1988) showed abrupt change when aestivation began, though the period did coincide with the dying-off of an algal bloom, and the environmental changes associated with this could have stimulated the snails. Burrowing by snails to depths of a few cms has been observed for B. truncatus in Iran (Chu et al., 1967), B tropicus in South Africa (Stiglingh, 1971) and both B. senegalensis and B. umbilicatus in Senegal (Diaw et al., 1989). B. globosus, however, was not seen burrowing by Odei (1966) or Hira (1968), who found dormant snails lying on the surface of mud shaded by vegetation. Yet, in exposed sites it is likely that predation and trampling by man and livestock ensures that only buried snails survive the dry period. There are few field studies of aestivation by other species of snail in tropical Africa. Tomichia ventricosa survived in a dry sunbaked pan by burrowing into the sandy substratum (Davis, 1981). Although Lymnaea natalensis is not usually found in temporary habitats (Van Someren, 1946; McCullough, 1965), it survived in dry mud in Kenya (Bitakaramire, 1968); in Nigeria juvenile snails survived in mud at shaded sites for at least 6 weeks, but adults rarely more than 2 weeks (Schillhorn van Veen & Usman, 1979). Eggs and hatchlings of L. natalensis survived for a few weeks without water on damp mud (Shiff, 1960) and Nymphaea leaves (Schillhorn van Veen & Usman, 1979). In contrast, L.

502 CHEMICAL AND PHYSICAL FACTORS

truncatula spends the greater part of the year in aestivation; active populations were present for not more than about 40 days on a sheep ranch in highland Ethiopia, where young snails of the new generation entered aestivation soon after hatching and well before the pasture became dry again (Goll & Scott, 1979). Biomphalaria sudanica is associated with the margins of lakes and papyrus swamps and was classified as a poor aestivator by Brown (1975, 1980). Yet this snail is reported to aestivate at the margin of Lake Zwai in Ethiopia during periods of low water (Goll, 1982) and apparently also in Lake Chad, where specimens may have survived for 5 months in beds of the grass Vossia cuspidata uncovered during the annual low-water period (Betterton, 1984). B. sudanica could therefore be classified as a moderately successful aestivator, but its habitats are extensive marshes during at least part of the year and this snail is not found in small seasonal waterbodies. The experimental study of aestivation is hampered by two main difficulties. First, if aestivation is an active process and not merely the snail’s response to being stranded by drying-up of water, it cannot be assumed that drying in the laboratory will provide the stimuli needed for a proper preparation for dormancy. Secondly, the period of survival is influenced by the degree of humidity in the air surrounding the snails, and unless this variable is standardised the results from different experiments are not closely comparable. In tests of survival of desiccation on different soils in boxes (Cridland, 1967), Lymnaea natalensis was less successful than other species (Bulinus globosus, B. africanus and Biomphalaria pfeifferi), which survived to 90 days in black cotton soil and sandy soil; in these experiments the moisture content of the substrata fell to as low as 1. 3%. Experiments performed in ‘cement bags’ (Vassiliadès, 1978; Diaw et al., 1988), apparently in more humid conditions, produced survival times of 60–90 days for L. natalensis, while 29% of B. truncatus survived for 8–9 months and 40% of B. globosus for 9–10 months. Aestivating snails have to cope with both shortage of water and starvation. Aestivating Bulinus africanus consumed oxygen at a lower rate than individuals starving in water (Heeg, 1977), suggesting that aestivation is a physiological state distinct from starvation itself. Heeg further observed that aestivating snails use metabolic reserves more slowly than starving snails. Respiration seemed to be aerobic in aestivating B. africanus and B. nasutus, which was stimulated to emerge from aestivation when placed in nitrogen. Previously Coles (1969) had suggested that the anaerobic conditions produced by the wetting of mud might reactivate snails under natural conditions. In the case of B. obtusispira it appeared to Degrémont (1973) that aestivation could have been ended not simply by the refilling of the habitat, but by the marked drop in salinity following heavy rainfall (Degrémont, 1973). High mortality amongst snails aestivating under natural conditions was quantified by Shiff (1964c). In early August, just before the disappearance of surface water from a pool, the estimated population of Bulinus globosus

FRESHWATER SNAILS OF AFRICA 503

exceeded 9300, of which about 2000 emerged after the return of water at the end of November. However, these survivors actually were the remnant of a far greater Table 10.2. Survival rates of Bulinus globosus under natural drought conditions and experimental desiccation on mud substrates (from Woolhouse & Taylor, 1990). Source

Conditions

Survival rate (per week)

Shiff (1964c) Hira & Muller (1966) Woolhouse & Chandiwana (1990b) Shiff (1960) Hira and Muller (1966) Cridland (1967) Woolhouse & Taylor (1990) Woolhouse & Taylor (1990) (infected snails)

Field, pond Field, river Field, river Experimental, outdoor Experimental, indoor Experimental, outdoor Experimental, indoor Experimental, indoor

0.82–0.86 0.79–0.87 0.95 0.88 0.87 0.72–0.80 0.81 0.57

population estimated at over 47 000 in early July, when the area of the pond was much larger than in early August, when it had already contracted considerably and many snails probably had begun to aestivate. Survival during aestivation is possibly related to individual size. Emerging B. senegalensis were consistently small (about 3.0 mm high) in laterite pools in the Gambia (Goll & Wilkins, 1984), but mostly medium-to-large in marshes in Senegal (Diaw et al., 1989). Further extensive mortality may occur after emergence (Betterton et al., 1988, p. 577). Yet survival rates of 0.87–0.95 per week for uninfected B. globosus during desiccation (Table 10.2) compared favourably with survival rates for snails active in the field of 0.76–0.82 per week (Woolhouse & Taylor, 1990). Pre-aestivation behaviour can vary among individual snails (Heeg, 1977; Pieri & Thomas, 1986), and natural selection is likely to favour any genetic component associated with successful aestivation. It would be interesting to investigate the possibility that pre-aestivating behaviour varies in a genetically polymorphic manner, as an adaptation to the variable conditions in temporary waterbodies. Current speed Some snails are adapted to fast-flowing water and have the shell modified to resist dislodgement. Such current-loving (rheophilous) species include assimineids endemic to the rocky torrents of the lower Zaire River, the genus Sierraia in West African rivers and Burnupia in streams. A strong current for only a brief seasonal period may prevent a non-specialised species from establishing itself in a river. The underlying influence of geological formations in southern Africa has been described (Appleton, 1975; Appleton & Stiles, 1976; see also Chapter 9: South-eastern Transvaal). Where the bedrock is hard a river contains many boulders and pools, which provide refuges for snail populations

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where they are protected from current speeds above the tolerable maximum of about 0.3 m s−1. In small rivers and streams that are slowly flowing or stagnant for most of the year, sudden spates following heavy rainfall sweep away many snails and cause major fluctuations in population density. The water current may be an important means for the dispersal of snails (Chapter 9: Factors affecting local distribution). Seasonal floods swept away almost the entire population of B. globosus at some sites in Zimbabwe, and this effect was included in a model of population dynamics (Woolhouse & Chandiwana, 1990a,b). The adverse effect of strong current on B. globosus was attributed also to sweeping away of food and stress caused to the snails (Marti, 1986). The stressful effect of strong current was suggested independently by Loreau & Baluku (1987) as one cause, together with high juvenile mortality, of the critical influence of current speed on the population dynamics of Biomphalaria pfeifferi. Measuring currents experienced by snails in the field is difficult because of sharp variations in time and space. Although a speed of 0.66 m s−1 was measured in the middle of a stream, it was only 0.09 m s−1 behind leaves of Cyperus exaltatus at the margin (Marti & Tanner, 1988). From measurements taken near snails, Appleton (1975) estimated tolerance ranges with upper limits ranging from 0.3 m s−1 for Biomphalaria pfeifferi, Bulinus (Physopsis) sp. and Melanoides tuberculata to 3.2 m s−1 for Burnupia. In an experimental flowingwater system, Bulinus jousseaumei withstood high flow of 0.86 m s−1 for longer than other species tested (not from tropical Africa) (Dussart, 1987). The exclusion of snails from irrigation systems by means of a high rate of flow is probably impracticable in earth channels, where aquatic vegetation provides refuges from the current. Even where canals are concrete-lined, changes in design are needed to minimise the reduction of current velocity caused by sumps, syphons and offtake structures (Bolton, 1988). The desirable objective in irrigation canals may be occasional periods of strongly turbulent flow, rather than a steady rapid current, as Fritsch (1993) found that the success of an artificial flushing regime in eliminating snail populations from a river was due mainly to brief periods of turbulent shear stresses, rather than to the drag force exerted by steadily flowing water. Light and shade, circadian rhythms Snail hosts for schistosomes are reported to survive for several generations in almost total darkness (literature reviewed by Appleton, 1978), but adverse effects were observed by El-Emam & Madsen (1982). There is evidence of regular patterns of activity in relation to the 24-hour cycle of day and night (circadian rhythms). Bulinus globosus laid eggs mainly at night (Kuma, 1975; Appleton, 1978), but B. africanus laid eggs only by day and the rhythms for oviposition and other activities were shown to be endogenous (Morgan & Last, 1982). This surprising difference between two closely-related species needs to be

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investigated for more populations. It is too early to speculate on the significance of these circadian rhythms, though the reason why more individuals of Lanistes nyassanus bury in the sand at the bottom of Lake Malawi during the morning than in late afternoon or evening could be to avoid fish hunting by sight (Louda & McKaye, 1982). In assessing the effect of solar radiation on snails in the field it is difficult to separate the effects of light and temperature. Shaded sites are unfavourable for Biomphalaria pfeifferi and shading by trees is suggested as a means for controlling this snail (Chapter 8: Environmental control). Dense shade beneath mats of floating vegetation is generally unfavourable for snails (Chapter 9: Snails and plants). The adverse effect of shade is thought to be indirect and due to depression of the growth of sub-aquatic vegetation that provides snails with food and oxygenates the water. Yet some species may be found most frequently in high shade (e.g. Ndifon & Ukoli, 1989; Lanistes libycus, Gyraulus costulatus and Physa waterloti). When reviewing the effects of physicochemical factors on the snail hosts for schistosomes, Appleton (1978) concluded that temperature and current velocity were largely responsible for their distribution and abundance in southern Africa. This still seems to be true and later observations show the importance of these factors further north. Water chemistry can limit snail distribution, though within the range of normal freshwater conditions its influence is more evident in population dynamics than in the presence or absence of a species. Low oxygen concentration can be limiting in local situations, especially where there is pollution. Desiccation is a major constraint on the snail fauna; pulmonate species that thrive in temporary habitats are specialised for aestivation and quickly repopulate when water returns. Shade may be either favourable or unfavourable. References Alberts, L.E. 1966. Some aspects of the respiratory physiology of three South African freshwater pulmonate snails, Bulinus (P.) africanus, B. (B.) tropicus and Lymnaea natalensis. South African Journal of Science, 62:215–223. Annecke, S. & Peacock, P.N. 1951. Bilharziasis in the Transvaal. South African Medical Journal, 25:692–698. Appleton, C.C. 1974. The population fluctuations of 5 freshwater snail species in the eastern Transvaal lowveld, and their relationship with known bilharzia transmission patterns. South African Medical Journal, 70:145–150. Appleton, C.C. 1975. The influence of stream geology on the distribution of the bilharzia host snails Biomphalaria pfeifferi and Bulinus (Physopsis) sp. Annals of Tropical Medicine and Parasitology, 69:241–255. Appleton, C.C. 1976. Observations on the thermal regime of a stream in the eastern Transvaal, with reference to certain Pulmonata. South African Journal of Science, 72: 20–23.

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Appleton, C.C. 1977a. The influence of temperature on the life cycle and distribution of Biomphalaria pfeifferi in southeastern Africa. International Journal of Parasitology, 7: 335–345. Appleton, C.C. 1977b. The influence of above-optimal constant temperatures on South African Biomphalaria pfeifferi (Krauss). Transactions of the Royal Society of Tropical Medicine and Hygiene, 71:140–143. Appleton, C.C. 1977c. The freshwater Mollusca of Tongaland, with a note on molluscan distribution in Lake Sibaya. Annals of the Natal Museum, 23:129–144. Appleton, C.C. 1978. Review of literature on biotic and abiotic factors influencing the distribution and life cycles of bilharziasis intermediate host snails. Malacological Review, 11:1–25. Appleton, C.C. & Eriksson, I.M. 1984. The influence of fluctuating above-optimal temperature regimes on the fecundity of Biomphalaria pfeifferi. Transactions of the Royal Society of Tropical Medicine and Hygiene, 78:49–54. Appleton, C.C. & Stiles, G. 1976. Geology and geomorphology in relation to the distribution of snail intermediate hosts of bilharzia in South Africa. Annals of Tropical Medicine and Parasitology, 70:189–198. Beadle, L.C. 1981. The Inland Waters of Tropical Africa. 2nd Edn. London, New York: Longman. Betterton, C. 1984. Ecological studies on the snail hosts of schistosomiasis in the South Chad Irrigation Project area, Borno State, northern Nigeria. Journal of Arid Environments, 7:43–57. Betterton, C., Fryer, S.E. & Wright, C.A. 1983. Bulinus senegalensis (Mollusca: Planorbidae) in northern Nigeria. Annals of Tropical Medicine and Parasitology, 77: 143–149. Betterton, C., Ndifon, G.T. & Tan, R.M. 1988. Schistosomiasis in Kano State, Nigeria. 2. Field studies on aestivation in Bulinus rohlfsi (Clessin) and B. globosus (Morelet) and their susceptibility to local strains of Schistosoma haematobium. Annals of Tropical Medicine and Parasitology, 82:571–579. Bitakaramire, P.K. 1968. The survival of Lymnaea natalensis in drought conditions. Bulletin of Epizootic Diseases of Africa, 16:473–475. Bolton, P. 1988. Schistosomiasis control in irrigation schemes in Zimbabwe. Journal of Tropical Medicine and Hygiene, 91:107–114. Brackenbury, T.D. & Appleton, C.C. 1991. Effect of controlled temperatures on gametogenesis in the gastropods Physa acuta and Bulinus tropicus. Journal of Molluscan Studies, 57:461–469. Brown, D.S. 1966. On certain morphological features of Bulinus africanus and B. globosus and the distribution of these species in south eastern Africa. Annals of the Natal Museum, 18:401–415. Brown, D.S. 1975. Distribution of intermediate hosts of Schistosoma on the Kano Plain of western Kenya. East African Medical Journal, 52:42–51. Brown, D.S. 1980. Freshwater Snails of Africa and their Medical Importance. 1st Edn. London; Taylor & Francis. Brown, D.S. 1988. Sierraia: rheophilous West African river snails (Prosobranchia: Bithyniidae). Zoological Journal of the Linnean Society, 73:313–355. Brygoo, E.R. 1967. La temperature et la répartition des bilharzioses humaines à Madagascar. Bulletin de la Société de Pathologie exotique, 5:433–441.

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Cantrell, M.A. 1981. Bilharzia snails and water level fluctuations in a tropical swamp. Oikos, 36:226–232. Chu, K.Y., Massoud, J. & Arfaa, F. 1967. The survival time and fecundity of Bulinus truncatus after desiccation in mud. Annals of Tropical Medicine and Parasitology, 61:139– 143 (and previous papers). Coles, G.C. 1969. Observations on weight loss and oxygen uptake of aestivating Bulinus nasutus, an intermediate host of Schistosoma haematobium. Annals of Tropical Medicine and Parasitology, 63:393–398. Coulibaly, G. & Madsen, H. 1990. Seasonal density fluctuations of intermediate hosts of schistosomes in two streams in Bamako, Mali. Journal of African Zoology, 104: 201– 212. Cridland, C.C. 1967. Resistance of Bulinus (P.) globosus, B. (P.) africanus, Biomphalaria pfeifferi and Lymnaea natalensis to experimental desiccation. Bulletin of the World Health Organisation, 36:507–513. Dannemann, R.D.A. & Pieri, O.S. 1993. Prolonged survival out of water of polymorphic Biomphalaria glabrata (Say) from a seasonally drying habitat of North-East Brazil . Journal of Molluscan Studies, 59:263–265. Davis, G.M. 1981. Different modes of evolution and adaptive radiation in the Pomatiopsidae (Prosobranchia: Mesogastropoda). Malacologia, 21:209–262. Degrémont, A.A. 1973. Mangoky Project. Campaign Against Schistosomiasis in the Lower Mangoky (Madagascar). Basle: Swiss Tropical Institute. Dejoux, C., Lauzanne, L. & Lévêque, C. 1971a. Prospection hydrobiologique du lac de Léré (Tchad) et des mares avoisinantes. 4. Faune benthique. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 5:179–188. Dejoux, C, Lauzanne, L. & Lévêque, C. 1971b. Nature des fonds et répartition des organisms benthiques dans la region de Bol (archipel est du lac Tchad). Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 5:213–223. De Kock, K.N. 1985. Effect of programmed circadian temperature fluctuations on population dynamics of Bulinus tropicus (Krauss) amd Lymnaea natalensis Krauss. Journal of the Limnological Society of Southern Africa, 11:71–74. De Kock, K.N. & Van Eeden, J.A. 1981. Life table studies on freshwater snails. The effect of constant temperature on the population dynamics of Biomphalaria pfeifferi (Krauss). Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B: Natuurwetenskappe, 107:1–17. De Kock, K.N. & Van Eeden, J.A. 1985. Effect of constant temperature on population dynamics of Bulinus tropicus (Krauss) and Lymnaea natalensis Krauss. Journal of the Limnological Society of Southern Africa, 11:27–31. De Kock, K.N. & Van Eeden, J.A. 1986. Effect of programmed circadian temperature fluctuations on population dynamics of Biomphalaria pfeifferi (Krauss). South African Journal of Zoology, 21:28–32. Diaw, O.T., Seye, M. & Sarr, Y. 1988. Resistance à la sécheresse de mollusques du genre Bulinus vecteurs de trématodoses humaines et animales au Sénégal. 1. Essais en laboratoire. Revue et Elevages de Médecine veterinaire des Pays tropicaux, 41: 289–291. Diaw, O.T., Seye, M. & Sarr, Y. 1989. Resistance à la sécheresse de mollusques du genre Bulinus vecteurs de trématodoses humaines et animales au Sénégal. 2. Etude dans les

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conditions naturelles en zone Nord-soudanienne. Revue et Elevages de Médecine vétérinaires des Pays tropicaux, 42:177–187. Donnelly, F.A. & Appleton, C.C. 1985. Observations on the field transmission dynamics of Schistosoma mansoni and S. mattheei in southern Natal, South Africa. Parasitology, 91: 281–290. Donnelly, F.A., Appleton, C.C. & Schutte, C.H.J. 1983. The influence of salinity on certain aspects of the biology of Bulinus (Physopsis) africanus. International Journal of Parasitology, 13:539–545. Donnelly, F.A., Appleton, C.C., Begg, G.W. & Schutte, C.H.J. 1984. Bilharzia transmission in Natal’s estuaries and lagoons: fact or fiction? South African Journal of Science, 80:455–460. Dussart, G.B.J. 1987. Effects of water flow on the detachment of some aquatic pulmonate gastropods. American Malacological Bulletin, 5:65–72. El-Emam, M.A. & Madsen, H. 1982. The effect of temperature, darkness, starvation and various food types on growth, survival and reproduction of Helisoma duryi, Biomphalaria alexandrina and Bulinus truncatus. Hydrobiologia, 88:265–275. Fritsch, M. 1993. Environmental Management for Schistosomiasis Control. River Flushing — A Case Study in Namwala, Kilombero District, Tanzania. Zürich: Verlag der Fachvereine. Goll, P.H. 1982. Seasonal changes in the distribution of Biomphalaria sudanica sudanica (Martens) in Lake Zwai, Ethiopia. Annals of Tropical Medicine and Parasitology, 76: 159– 164. Goll, P.H. & Scott, J.M. 1979. Fascioliasis in the Ethiopian highlands. 1. Dynamics of intermediate snail host populations and their relation to infection in sheep. Miscellaneous Reports, Centre for Overseas Pest Research. 47:1–12. Goll, P.H. & Wilkins, H.A. 1984. Field studies on Bulinus senegalensis Müller and the transmission of Schistosoma haematobium infection in a Gambian community. Tropenmedizin und Parasitologie, 35:29–36. Green, J., Corbet, S.A. & Betney, E. 1974. Ecological studies on crater lakes in West Cameroon. Debundsha Lake. Journal of Zoology, London, 173:199–223. Green, P., Dussart, G.B.J. & Gibson, C. 1992. Surfacing and water-leaving behaviour of the freshwater pulmonate snails Lymnaea peregra (Müller), Biomphalaria glabrata (Say) and Bulinus jousseaumei (Dautzenberg). Journal of Molluscan Studies, 58: 169–179. Grétillat, S. & Gaston, G. 1975. Sur quelques particularités écologiques de la faune malacologique vectrice de trématodes dans les Dallols nigériens. Annales de Parasitologie, Paris, 50:595–601. Hare, L. & Carter, J.C.H. 1984. Diel and seasonal physico-chemical fluctuations in a small natural West African lake. Freshwater Biology, 14:697–610. Harrison, A.D. 1962. Hydrobiological studies on alkaline and acid still waters in the Western Cape province. Transactions of the Royal Society of South Africa, 36: 213–244. Harrison, A.D. 1966. The study of the biology of schistosome host snails. Central African Journal of Medicine, 12:124–127. Harrison, A.D. 1968. The effects of calcium bicarbonate concentration on the oxygen consumption of the freshwater snail Biomphalaria pfeifferi. Archiv für Hydrobiologie, 65: 63–73.

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Harrison, A.D. & Farina, T.D. 1965. A naturally turbid water with deleterious effects on the egg capsules of planorbid snails. Annals of Tropical Medicine and Parasitology, 59:327–330. Harrison, A.D. & Shiff, C.J. 1966. Factors influencing the distribution of some species of aquatic snails. South African Journal of Science, 62:253–258. Harrison, A.D., Nduku, W. & Hooper, A.S. 1966. The effects of a high calcium-tomagnesium ratio on the egg laying of an aquatic snail, Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology, 60:212–214. Harrison, A.D., Williams, N.V. & Greig, G. 1970. Studies on the effects of calcium bicarbonate concentrations on the biology of Biomphalaria pfeifferi (Krauss). Hydrobiologia, 36:317–327. Heeg, J. 1975. A note on the effect of drastic changes in total dissolved solids on the aquatic pulmonate snail Bulinus africanus (Krauss). Journal of the Limnological Society of Southern Africa, 1:29–32. Heeg, J. 1977. Oxygen consumption and use of metabolic reserves during starvation and aestivation in Bulinus (P.) africanus . Malacologia, 16:549–560. Hira, P.R. 1968. Studies on the capability of the snail transmitting urinary schistosomiasis in western Nigeria to survive dry conditions. West African Medical Journal, 17: 153– 160. Hira, P.R. & Muller, R. 1966. Studies on the ecology of snails transmitting urinary schistosomiasis in western Nigeria. Annals of Tropical Medicine and Parasitology, 60: 198–211. Jennings, A.C., De Kock, K.N. & Van Eeden, J.A. 1973. The effect of the total dissolved salts in water on the biology of the freshwater snail Biomphalaria pfeifferi. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 50:26 pp. Jones, J.D. 1964. Respiratory gas exchange in the aquatic pulmonate Biomphalaria sudanica. Comparative Biochemistry and Physiology, 12:297–310. Joubert, J.A., Pretorius, S.J. & De Kock, K.N. 1986. Survival of Bulinus tropicus, Lymnaea natalensis and Biomphalaria cf. glabrata at low temperatures. South African Journal of Science, 82:322–323. Joubert, P.H., Pretorius, S.J., De Kock, K.N. & Van Eeden, J.A. 1984. The effect of constant low temperature on the survival of Bulinus africanus, B. globosus and Biomphalaria pfeifferi. South African Journal of Zoology, 19:314–316. Joubert, J.A., Pretorius, S.J., De Kock, K.N. & Van Eeden, J.A. 1986. Survival of Bulinus africanus, B. globosus and Biomphalaria pfeifferi at constant high temperatures. South African Journal of Zoology, 21:85–88. Klumpp, R., Chu, K.Y. & Webbe, G. 1985. Observations on the growth and population dynamics of Bulinus rohlfsi in an outdoor laboratory at Volta Lake. Annals of Tropical Medicine and Parasitology, 79:635–642. Kuma, E. 1975. Studies on the behaviour of Bulinus (Physopsis) globosus (Morelet). Zoologische Anzeiger, Jena, 194:6–12. Lévêque, C. 1972. Mollusques benthiques du lac Tchad: écologie, étude de peuplements et estimations des biomasses. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 6:3–45. Lévêque, C., Dejoux, C. & Lauzanne, L. 1983. The benthic fauna: ecology, biomass and communities. In Lake Chad: 233–272. Carmouze, J.P., Durand, J.R. & Lévêque, C. (Eds). The Hague, Boston, Lancaster: W.Junk.

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Lodge, D.M., Brown, K.M., Klosiewski, S.P. et al. 1987. Distribution of freshwater snails: spatial scale and the relative importance of physicochemical and biotic factors. American Malacological Bulletin, 5:73–84. Loreau, M. & Baluku, B. 1987. Population dynamics of the freshwater snail Biomphalaria pfeifferi in eastern Zaire. Journal of Molluscan Studies, 53:249–265. Louda, S.M. & McKaye, K.R. 1982. Diurnal movements in populations of the prosobranch Lanistes nyassanus at Cape Maclear, Lake Malawi, Africa. Malacologia, 23:13–21. Macan, T.T. 1974. Freshwater Ecology. 2nd Edn. London: Longman. Madsen, H. 1990. The effect of sodium chloride concentration on growth and egg laying of Helisoma duryi, Biomphalaria alexandrina and Bulinus truncatus. Journal of Molluscan Studies, 56:181–187. Madsen, H., Daffalla, A.A., Karoum, K.O. & Frandsen, F. 1988. Distribution of freshwater snails in irrigation schemes in the Sudan. Journal of Applied Ecology, 25: 853–866. Mandahl-Barth, G. 1958. Intermediate hosts of Schistosoma. African Biomphalaria and Bulinus. Geneva: World Health Organisation. Mandahl-Barth, G. 1972. The freshwater Mollusca of Lake Malawi. Revue de Zoologie et de Botanique Africaine, 86:257–289. Mandahl-Barth, G., Ripert, C. & Raccurt, C. 1974. Nature du sous-sol, répartition des mollusques dulcaquicoles et foyers de bilharzioses intestinale et urinaire au BasZaire. Revue de Zoologie Africaine, 88:553–584. Marti, H.P. 1986. Field observations on the population dynamics of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara area, Tanzania. Journal of Parasitology, 72:119–124. Marti, H.P. & Tanner, M. 1988. Field observations on the influence of low water velocities on drifting of Bulinus globosus. Hydrobiologia, 157:119–123. Matovu, D.S. & Nditi, H.P. 1978. Laboratory experiments on the effect of aestivation on oviposition in Bulinus (Physopsis) nasutus. In Proceedings of the International Congress on Schistosomiasis, Cairo, Egypt, 1975:515–519. Cairo: Ministry of Health. McCullough, F.S. 1957. The seasonal density of populations of Bulinus (P.) globosus and B. forskalii in natural habitats in Ghana. Annals of Tropical Medicine and Parasitology, 51:235–248. McCullough, F.S. 1958. The internal lamellae in the shell of Biomphalaria pfeifferi gaudi (Ranson) from Ghana, West Africa. Journal de Conchyliologie, Paris, 97:171–179. McCullough, F.S. 1965. Lymnaea natalensis and fascioliasis in Ghana. Annals of Tropical Medicine and Parasitology, 59:320–326. Meier-Brook, C., Haas, D., Winter, G. & Zeller, T. 1987. Hydrochemical factors limiting the distribution of Bulinus truncatus. American Malacological Bulletin, 5:85–90. Morgan, E. & Last, V. 1982. The behaviour of Bulinus africanus: a circadian profile. Animal Behaviour, 30:557–567. Ndifon, G.T. & Ukoli, F.M.A. 1989. Ecology of freshwater snails in south-western Nigeria. 1: Distribution and habitat preferences. Hydrobiologia, 171:231–253. Nduku, W.K. & Harrison, A.D. 1976. Calcium as a limiting factor in the biology of Biomphalaria pfeifferi (Krauss). Hydrobiologia, 49:143–170.

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Nduku, W.K. & Harrison, A.D. 1980a. Cationic responses of organs and haemolymph of Biomphalaria pfeifferi (Krauss), B. glabrata (Say) and Helisoma trivolvis (Say) to cat ionic alterations of the medium. Hydrobiologia, 68:119–138. Nduku, W.K. & Harrison, A.D. 1980b. Water relations and osmotic pressure in Biomphalaria pfeifferi (Krauss), B. glabrata (Say) and Helisoma trivolvis (Say) in response to cationic alterations of the medium. Hydrobiologia, 68:139–144. Odei, M.A. 1966. The behaviour and aestivating ability of Bulinus (P.) globosus Morelet under drought conditions. Ghana Journal of Science, 7:50–54. O’Keeffe, J.H. 1985. Population biology of the freshwater snail Bulinus globosus on the Kenya coast. 1. Population fluctuations in relation to climate. Journal of Applied Ecology, 22:73–84. Økland, J. 1990. Lakes and Snails. Oegstgeest, The Netherlands: Universal Book Services, Dr W.Backhuys. Oyeyi, T.I. & Ndifon, G.T. 1990. A note on the post-aestivation biology of Bulinus rohlfsi (Clessin), an intermediate host of S. haematobium in northern Nigeria. Annals of Tropical Medicine and Parasitology, 84:535–536. Pflüger, W. 1977. Ecological studies in Madagascar of Biomphalaria pfeifferi, intermediate host of Schistosoma mansoni. Archive de l’Institut Pasteur, Madagascar, 45:79–114. Pieri, O.S. & Thomas, J.D. 1986. Polymorphism in a laboratory population of Biomphalaria glabrata from a seasonally drying habitat in north-east Brazil. Malacologia, 27:313– 321 . Pilsbry, H.A. & Bequaert, J. 1927. The aquatic mollusks of the Belgian Congo, with a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History, 53:69–602. Pitchford, R.J. & Visser, P.S. 1969. The use of behaviour patterns of larval schistosomes in assessing the bilharzia potential of non-endemic areas. South African Medical Journal, 43:983–995. Plaziat, J.C. 1982. Introduction à l’écologie des milieux de transition eau douce-eau salée pour l’identification des paléoenvironments correspondants. Critique de la notion de domaine margino-littoral. Memoires de la Société Géologique de France, n.s., 144: 187–206. Polderman, A.M., Mpamila, K., Manshande, J.P., Gryseels, B. & Van Schayk, O. 1985. Historical, geological and ecological aspects of transmission of intestinal schistosomiasis in Maniema, Kivu Province, Zaire. Annales de la Société Belge de Médecine tropicale, 65: 251–261. Pretorius, S.J., Van Eeden, J.A. & Joubert, P.H. 1982. Mark-recapture studies on Bulinus (P.) africanus (Krauss). Malacologia, 22:93–102. Prinsloo, J.F. & Van Eeden, J.A. 1969. Temperature and its bearing on the distribution and chemical control of freshwater snails. South African Medical Journal, 43: 1363– 1365 . Richardot, M. 1977. Ecological factors inducing aestivation in the freshwater limpet Ferrissia wautieri. Malacological Review, 10:7–30. Richards, C.S. 1967. Estivation of Biomphalaria glabrata. Associated characteristics and relation to infection with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene, 16:797–802. Richards, C.S. 1968. Aestivation of Biomphalaria glabrata, genetic studies. Malacologia, 7:109–116.

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Schillhorn van Veen, T.W. & Usman, S. 1979. The limited ability of Lymnaea natalensis to survive drought conditions. Revue et Elevages de Médecine véterinaire de Pays tropicaux, 32:251–255. Schutte, C.H.J. & Frank, G.H. 1964. Observations on the distribution of freshwater Mollusca and chemistry of the natural waters in the southeastern Transvaal and adjacent northern Swaziland. Bulletin of the World Health Organisation, 30: 389–400. Shiff, C.J. 1960. Observations on the ability of freshwater vector snails to survive dry conditions. Journal of Tropical Medicine and Hygiene, 63:89–93. Shiff, C.J. 1964a. Studies on Bulinus (P.) globosus in Rhodesia. 1. The influence of temperature on the intrinsic rate of natural increase. Annals of Tropical Medicine and Parasitology, 58:94–105. Shiff, C.J. 1964b. Studies on B. (P.) globosus in Rhodesia. 2. Factors influencing the relationship between age and growth. Annals of Tropical Medicine and Parasitology, 58: 106–115. Shiff, C.J. 1964c. Studies on B. (P.) globosus in Rhodesia. 3. Bionomics of a natural population existing in a temporary habitat. Annals of Tropical Medicine and Parasitology, 58:240–255. Shiff, C.J. 1966. The influence of temperature on the vertical movement of Bulinus (P.) globosus in the laboratory and in the field. South African Journal of Science, 62: 210– 214. Shiff, C.J. & Garnett, B. 1967. The influence of temperature on the intrinsic rate of natural increase of the freshwater snail Biomphalaria pfeifferi (Krauss). Archiv für Hydrobiologie, 62:429–438. Slootweg, R., Vroeg, P. & Wiersma, S. 1993. The effects of molluscivorous fish, water quality and pond management on the development of schistosomiasis vector snails in aquaculture ponds in North Cameroon. Aquaculture and Fisheries Management, 24: 123–128. Smith, V.G.F. 1982. Distribution of snails of medical and veterinary importance in an organically polluted watercourse in Nigeria. Annals of Tropical Medicine and Parasitology, 76:539–546. Smithers, S.R. 1956. On the ecology of schistosome vectors in the Gambia, with evidence of their role in transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene, 50:354–365. Stiglingh, I. 1971. Bulinus tropicus (Krauss) and digging behaviour. Newsletter of the Limnological Society of Southern Africa, 16:42–46. Stiglingh, I. & Van Eeden, J.A. 1977. Population fluctuations and ecology of Bulinus tropicus. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 87:1–37. Sturrock, R.F. 1966. The influence of temperature on the biology of Biomphalaria pfeifferi (Krauss), an intermediate host of S. mansoni. Annals of Tropical Medicine and Parasitology, 60:100–105. Symoens, J.J. 1968. La minéralisation des eaux naturelles. Exploration Hydrobiologique, Bangweulu-Luapula, 11:1–199. Talling, J.F. 1992. Environmental regulation in African shallow lakes and wetlands. Revue d’Hydrobiologie tropicale, 25:87–144.

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Thomas, J.D. & Ratcliffe, P.J. 1973. Observations on the limnology and primary production of a small man-made lake in the West African savanna. Freshwater Biology, 3:573–612. Thomas, J.D. & Tait, A.I. 1984. Control of the snail hosts of schistosomiasis by environmental manipulation: a field and laboratory appraisal in the Ibadan area, Nigeria. Philosophical Transactions of the Royal Society, London, B, 305:201–253. Thomas, J.D., Benjamin, M., Lough, A. et al. 1974. The effects of calcium in the external environment on the growth and natality rates of Biomphalaria glabrata (Say). Journal of Animal Ecology, 43:839–860. Van Aardt, W.J. & Frey, B.J. 1979. Oxygen consumption and responses of the freshwater snail Bulinus (P.) globosus to gradients of different oxygen tensions. South African Journal of Zoology, 14:202–207. Van Aardt, W.J. & Frey, B.J. 1981. Oxygen-binding characteristics of the haemolymph of the freshwater snail Bulinus (P.) globosus. South African Journal of Zoology, 16: 1–4. Van Eeden, J.A. & Combrinck, C. 1966. Distributional trends of 4 species of freshwater snails in South Africa, with special reference to the intermediate hosts of bilharzia. Zoologica Africana, 2:95–109. Van Someren, V.D. 1946. The habitats and tolerance ranges of Lymnaea (Radix) caillaudi, the intermediate host of liver fluke in East Africa. Journal of Animal Ecology, 15:170– 197. Vassiliadès, G. 1978. Capacité de resistance à la sécheresse de la limnée (Limnaea natalensis), mollusque hôte intermédiaire de Fasciola gigantica, au Sénégal. Revue et Elevages de Médécine véterinaire de Pays tropicaux, 31:57–62. Webbe, G. 1962. The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bulletin of the World Health Organisation, 27:59–85. Webbe, G. & Msangi, A.S. 1958. Observations on three species of Bulinus on the east coast of Africa. Annals of Tropical Medicine and Parasitology, 52:302–314. Williams, N.V. 1970a. Studies on aquatic pulmonate snails in central Africa. 1. Field distribution in relation to water chemistry. Malacologia, 10:153–164. Williams, N.V. 1970b. Studies on aquatic pulmonate snails in central Africa. 2. Experimental investigation of field distribution patterns. Malacologia, 10:165–180. Woolhouse, M.E.J. 1992. Population biology of the freshwater snail Biomphalaria pfeifferi in the Zimbabwe highveld. Journal of Applied Ecology, 29:687–694. Woolhouse, M.E.J. & Chandiwana, S.K. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and the epidemiology of their infection with schistosomes. Parasitology, 98:21–34. Woolhouse, M.E.J. & Chandiwana, S.K. 1990a. Population biology of the freshwater snail Bulinus globosus in the Zimbabwe highveld. Journal of Applied Ecology, 27: 41– 59. Woolhouse, M.E.J. & Chandiwana, S.K. 1990b. Population dynamics model for Bulinus globosus, intermediate host for Schistosoma haemtobium, in river habitats. Acta Tropica, 47:151–160. Woolhouse, M.E.J. & Taylor, P. 1990. Survival rates of Bulinus globosus during aestivation. Annals of Tropical Medicine and Parasitology, 84:293–294. Wright, C.A. 1956. A note on the ecology of some molluscan intermediate hosts of African schistosomiasis. Annals of Tropical Medicine and Parasitology, 50: 346–349.

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Wright, R. 1982. Seasonal variations in water quality of a West African river (R.Jong in Sierra Leone). Revue de Hydrobiologie tropicale, 15:193–199. Zabi, G.S.F. & Le Loeuff, P. 1992. Revue des connaissances sur la faune benthique des millieux margino-littoraux d’Afrique de l’Ouest. Revue d’Hydrobiologie tropicale, 25: 209–251.

Chapter 11. Life cycles and populations

A brief review is given here of some aspects of life cycles (reproduction, growth, seasonality) and populations (dynamics and productivity). Life cycles are classified into two basic types (Calow, 1978): iteroparous (when the individual has repeated cycles of reproduction during its lifetime) and semelparous (when there is only one breeding period and parents die after reproduction). The type of life cycle is not necessarily constant for a species throughout its geographical range but can vary among populations according to local conditions. Knowledge of fluctuations in snail populations in a focus of snail-borne disease is fundamental to achieving successful control of the intermediate host. Snails are important too in the flow of energy through freshwater ecosystems; these organisms contribute a major proportion of the invertebrate biomass and produce large quantities of organic and inorganic matter (in the form of the shell). Population fluctuations in African freshwater gastropods are best known for pulmonates, but productivity has been most studied for a few of the prosobranchs. Prosobranchs Reproduction, growth, seasonality The sexes are separate in all the families considered here apart from the Valvatidae. Males have a penis in most families (Neritidae, Ampullariidae, Assimineidae, Hydrobiidae, Pomatiopsidae and Bithyniidae), while the Viviparidae have the right tentacle modified as a copulatory organ. But there is generally no intromittent organ in the Thiaridae, Melanopsidae and Potamididae. For many African prosobranchs the mode of reproduction is unknown, including even the commonly occurring snails Cleopatra and Potadoma, and so the following generalisations are provisional. Oviparity seems to be universal in the families Neritidae, Ampullariidae, Valvatidae, Pomatiopsidae Bithyniidae and Melanopsidae, and is common in the Hydrobiidae and Assimineidae. Also oviparous are some members of the Thiaridae (e.g. Melanatria and Spekia). ‘Viviparity’, or more strictly speaking ovoviviparity (fully formed eggs are

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retained and hatched inside the body, and the young emerge either as swimming larvae or as small crawling snails) occurs throughout the Viviparidae and is widespread in the Thiaridae. The eggs of thiarid snails may be brooded in the pallial oviduct (e.g. Potadomoides and Lavigeria) or transferred into a separate brood pouch in the neck (e.g. Thiara and Melanoides). Ovoviviparity appears also to occur, though uncommonly, in the Hydrobiidae (e.g. H. guyenoti) and Assimineidae (Pseudogibbula). The calculation of sex ratios may be complicated by sexual dimorphism in size; females tend to grow larger than males in Sierraia, though both sexes complete shell growth over a wide size range. There may be few males in a sample of large specimens of such a species, though the sexes could be equally represented in the whole population of adults. Males do appear to be significantly rarer than females in the assimineids Septariellina and Pseudogibbula, while observations made outside Africa have shown that some populations of the thiarids Melanoides tuberculata and Thiara scabra have few males if any and females usually reproduce by parthenogenesis. In Israel male frequencies in M. tuberculata were found to range from 0% to 66% (Heller & Farstey, 1990); it would be of great interest to make similar studies of this and congeneric species in Africa. Growth may be determinate, ceasing when the shell reaches a distinct mature form, e.g. Sierraia, though it is more commonly indeterminate, e.g. Lanistes nyassanus, which adds an annual increment to the shell throughout an adult life that may approach 10 years (Louda & McKaye, 1982). Few prosobranch life cycles are well known; at least the larger species seem to be iteroparous. A comparison may be made between Tomichia ventricosa, a pomatiopsid flourishing under the stressful conditions of unstable coastal lagoons, and viviparid and thiarid prosobranchs living in the very different environment of a large inland lake. T. ventricosa has adapted to exceptionally variable conditions in the coastal region of Cape Province (Davis, 1981). Some populations live in pans and vleis that dry out annually; water when present is saline to a varying degree. Snails that survive the dry period emerge during the rainy season into water reaching about 10‰. Probably they reproduce rapidly at this time and then with the return of the dry season and increasing salinity the snails are forced into an amphibious life or aestivation. Those that do not find a safe refuge die, as the salinity reaches 130–160‰ in the residual pools. The life cycles of Neritina and Pachymelania are also related to seasonal variations in salinity (Ajao & Fagade, 1990a,b). Compared with these coastal lagoons, Lake Chad is a much less demanding environment (although high salinity excludes molluscs from some parts; see Chapter 10). Life cycles of the benthic prosobranchs found in great abundance on some areas of the bottom sediments were revealed by observations on changes in size distribution in natural populations and in caged colonies living in the lake (Lévêque, 1971, 1973). Bellamya unicolor. This viviparous species began to reproduce at about 2.5 months of age in the warm season (3 months in the cool season) and continued to

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do so until death. Fecundity varied in relation to seasonal changes in temperature, with a low birth-rate of 1.5 young per adult per month in February, and a high birth-rate of 6 or 7 young per month in May to June. The greatest age reached in captivity was 15 months, and most snails lived for less than one year. Shell height was 17–18 mm by an age of 3 months; thereafter growth proceeded slowly to a maximum height of 23 mm. Cleopatra bulimoides. Thought to be oviparous, but did not breed freely in the cages. In natural populations reproduction seemed to continue throughout the year without marked seasonal variation, though asynchronous periods of maximum breeding activity were evident. Reproduction began at about 3 months of age, when height was about 13 mm (Lévêque, 1971, Fig. 18; rather than at about the same size as in Bellamya as stated by Lévêque, 1973, p. 131). Melanoides tuberculata. Reproduction began at about 2.5 months of age, at a height of 9–10 mm and continued until death, though less intensively during the cool season. Maximum size was generally 17–18 mm; in some sites 20–30 mm. There was a marked difference between the growth patterns of Bellamya and Cleopatra, which both grew little after beginning to reproduce, and Melanoides which continued to grow vigorously during reproductive life. Although the prosobranchs living on the bottom of Lake Chad do not experience the same degree of environmental instability as Tomichia in a coastal lagoon, indications of seasonality were observed in their life cycles that seem related to comparatively small changes in temperature. In the cooler climatic area of eastern South Africa, Appleton (1974) found that M. tuberculata has a single main generation per year, breeding mostly in the autumn (March–May) and reaching peak abundance during the summer. For the Ampullariidae, the life cycles have been studied of one indigenous and one introduced species in north-eastern Africa. In Egypt Lanistes carinatus (=bolteni) lays eggs mostly during the warm season (May–August) and breeding ceases in the winter (Aboul-Ela & Beddiny, 1970). Egg-laying began in the laboratory at an age of about 11 months and a shell width of about 27 mm. Since adults commonly grow to over 50 mm wide, it seems that the life cycle must be iteroparous, with an individual experiencing at least two breeding seasons. When Marisa cornuarietis was introduced into the Sudan from Puerto Rico, as a potential competitor of schistosome-transmitting snails, it was feared that its breeding might be inhibited by the high water temperatures of more than 30°C during the hottest period (April–June). No evidence was obtained, however, of seasonality in the life cycle of Marisa in the Sudan (Haridi et al., 1985); breeding in ponds proceeded continuously with a generation time of 4 months, and individuals reached 40 mm in diameter at one year old. Adaptation to predation by fish appears to have resulted in a life history of mixed strategy for Lanistes nyassanus of Lake Malawi (Louda & McKaye, 1982). First, there is a juvenile period when the thin-shelled young are highly vulnerable to predation but grow rapidly and live in a protected microhabitat, among roots in weedbeds. Secondly, there is an adult period when growth is slow

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and the development of a thick shell gives protection from predation; the snails now live exposed on the open sandy bottom and they tend to burrow during the day, thus further reducing danger from predators. The estimated life span is 5–10 years. Productivity of prosobranch populations Prosobranchs contribute a major part of the invertebrate biomass (standing crop) in tropical African lakes, e.g. Chad, Malawi, Tanganyika and Victoria. The most detailed observations were made in Lake Chad in 1968–71 and showed a high productivity by a few prosobranch species living on the bottom sediments. A substantial fall in the lake level began in 1972 and caused changes in the mollusc populations, and the recent situation in ‘little’ Chad may be very different from that described for the earlier ‘normal’ lake (Beadle, 1981; Lévêque Table 11.1. Productivity of prosobranchs in different localities in Lake Chad, 1967–70 (data from Lévêque, 1973, Table 7). Mean biomass or standing crop (B, dry body weight and for weight of shell, in g m−2) and production (P, in g m−2 for a period of one year). The data for Melanoides and Cleopatra are the lowest and the highest values for production observed among a greater number of sites. Species

Station

Dry body weight

Shell

B

P

P/B

B

P

P/B

Melanoides tuberculata Cleopatra bulimoides Bellamya unicolor

Samia 1 Samia 2 Baga Kawa 3 Bol 3 in 1968 Baga Kawa 2 Baga Kawa 3

3.5 0.7 3.4 0.3 2.8 2.1

15.5 2.0 11.9 0.7 13.6 12.9

4.4 3.0 3.5 2.5 5.5 6.1

28.5 5.6 25.5 2.2 18.0 13.9

141.3 17.6 92.6 66.4 95.3 90.5

5.0 3.1 3.6 2.9 6.0 6.5

et al., 1983). The abundance of prosobranchs and bivalves in Lake Chad seems due to its general shallowness and the richness of the bottom sediments as a food source. The biomass of molluscs in the eastern part calculated by Dejoux et al. (1969) was about ten times those of oligochaete worms and insects. The total biomass of benthic molluscs in the entire lake during 1970 was estimated at 775 000 metric tons or a mean of 388 kg per ha (alcoholic weight with shells); prosobranchs contributed 83% of this total, in the form of 3.5×1012 individuals (Lévêque, 1972). Hopson (quoted by Beadle, 1981, p. 222) calculated the combined biomasses of Bellamya and Melanoides to be over 1000 kg per ha near Malamfatori. The weight of shell greatly exceeded dry body weight (Table 11.1). Shell formation may play an important part in removing ions, especially calcium, from the water. Production (the total biomass produced per unit area over one year) was highest for Melanoides; values for the production index (P/B) mostly lay between 2 and 6 (Table 11.1) and were generally lower for Cleopatra. In

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Lake Léré, situated about 150 km south of Lake Chad and having a comparatively low salinity of 90 µmhos (Dejoux et al., 1971), estimated biomasses of oligochaetes were 1.7 kg per ha, insects 45 kg per ha and molluscs 195 kg per ha. In contrast to Lake Chad, Bellamya was not found and 75% of the molluscan biomass in Lake Léré was contributed by Cleopatra, which reached a maximum weight of 777 kg per ha in the marginal zone down to 1 m depth. In southern Africa, Bellamya and Melanoides provide a major part of the invertebrate biomass of Lake Sibaya, but the levels of the standing stocks and production are generally lower than in Lake Chad. Average biomasses (dry weight, apparently including shells) for the entire lake (Hart, 1979, Table 6) were estimated at 0.40 g m−2 for B. capillata and 1.74 g m−2 for M. tuberculata. The poorer productivity of Lake Sibaya could be due to the paucity of phosphorus and nitrogen (Hart, 1979, p. 151). Molluscs in the man-made Lake Kariba (Machena & Kautsky, 1988) made up almost the entire biomass of benthic animals (bivalves 95.8% and prosobranchs 4.1%). Average biomasses over the depth range sampled (0–10 m) were B. capillata 0.28 g m−2 (dry weight in cluding shell), M. tuberculata 4.08 g m−2 and Cleopatra sp. 0.66 g m−2 (calculated from Machena & Kautsky, Table 2). The high population densities achieved by M. tuberculata in African lakes are in accordance with observations on its life cycle and population dynamics in the laboratory, which indicate adaptation to maintaining large populations in stable habitats, by virtue of a low intrinsic rate of natural increase (r) and a long mean generation time (Pointier et al., 1991). Pulmonates Because researchers into the reproduction, seasonal life cycle and population fluctuations of African freshwater pulmonates have concentrated on Lymnaea, Biomphalaria and Bulinus, the rest of this chapter is devoted almost entirely to these genera. Reproduction Freshwater pulmonates are hermaphrodite, with an ovotestis producing eggs and sperm during much of the lifetime. But although isolated individuals of some species readily reproduce by self-fertilisation (and this capacity may be widespread among the many taxa not yet studied in this respect), the continuing value of outcrossing is indicated by the presence of a functional penis in most species. Yet the high frequency in some species of individuals lacking a copulatory organ but still producing sperm, known for Bulinus and Ferrissia and possibly to be found in other groups, suggests that self-fertilisation can be a successful mating system. Recent investigations show that reproductive strategies are varied in Bulinus (see Chapter 7: Breeding System), involving self-fertilisation and outcrossing, aphally, multiple insemination and sperm storage. Freshwater

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Fig. 138. Fitted growth curves for Bulinus globosus in cages in rivers on the Zimbabwean plateau; growth rates increased with temperature (from Woolhouse & Chandiwana, 1990a, Fig. 3d). Snails reached 5 mm in 4–5 weeks after hatching at temperatures above 21°C; this period was much greater at 14–16°C, although data were too sparse to construct the lower part of this curve. The maximum expected shell lengths at 21°C and above were 15– 17 mm.

pulmonates seem to be active in both sexual roles for most if not all of their reproductive life; evidence for protandry in Bulinus globosus and B. jousseaumei, where the male system developed ‘slightly earlier’ than the female organs, was presented by Wright (1957; pp. 16, 24–25). There may be similar complexities in the mating system of Biomphalaria, for whereas B. pfeifferi showed a high degree of self-fertilisation in Kenya (Bandoni et al., 1990), B. alexandrina is outcrossing (Vrijenhoek & Graven, 1992). Freshwater pulmonates are oviparous, depositing egg capsules of different types according to family. There may also be variation at lower taxonomic levels, not yet explored for the African fauna. The number of eggs per capsule varies from one (commonly in Ferrissia) to over one hundred in Lymnaea natalensis, and it may increase with the size of the parent snails (e.g. in Bulinus; McCullough, 1962, and Marti, 1986). Capsules are usually laid within water and on a firm surface; unusual oviposition sites reported are damp mud (L. natalensis; Shiff, 1960) and loose sand (Bulinus nyassanus; Wright et al., 1967). The large size of eggs laid by Ancylus fluviatilis has been interpreted as a possible adaptation towards the survival of young under adverse conditions (Bondesen, 1950). Such adaptation does not seem to have been looked for in the freshwater pulmonates of tropical Africa, though it may be relevant that eggs laid in the laboratory by Bulinus octoploidus from high altitude in Ethiopia were larger than the eggs of related species (Brown & Wright, 1972).

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Growth Growth in the shell of African freshwater pulmonates is indeterminate and continues long after the beginning of sexual maturity in at least Biomphalaria, Bulinus and Lymnaea. Although there is no distinct mature form of shell, changes in appearance during growth may be obvious, for example the proportional height of the spire tends to increase with size in Bulinus. An increase in the proportional width of B. jousseaumei was attributed to swelling of the accessory genital glands by Wright (1957). No other external criterion apart from size has been found for judging the sexual condition or age of an African freshwater pulmonate. Body weight and shell height or width are convenient measures of size and age. The construction of growth curves (Fig. 138) plays an important part in the study of population dynamics; these curves are summations of the varied performances of individuals under particular sets of conditions. Growth rate is one of the attributes monitored in laboratory experiments carried out to assess the effects of environmental factors in the ecology of snails. These data are available for a few species of Biomphalaria, Bulinus and Lymnaea; some of the studies are referred to in Chapter 10 (Nduku & Harrison, 1976, for calcium; Madsen, 1990, for sodium chloride; Jennings et al., 1973, for total salinity). Studies of the relationship between growth and temperature carried out in the laboratory and the field are reviewed below. Growth rates under natural and semi-natural conditions in Africa have been investigated by 3 methods: 1. comparing size-frequency distributions of snails collected in successive samples over a period of time; a widely-used technique, e.g. for Bulinus (Webbe, 1962; Shiff, 1964b,c; Dazo et al., 1966; Betterton, 1984; Goll & Wilkins, 1984; Marti, 1986; and Biomphalaria (Dazo et al., 1966; Loreau & Baluku, 1987b; Baluku & Loreau, 1989); 2. measuring marked and recaptured individuals in natural populations, e.g. of Bulinus forskalii by Lévêque (1968), B. africanus by Pretorius et al. (1982), B. globosus by Woolhouse (1988) and Woolhouse & Chandiwana (1990a), and Biomphalaria sudanica by Berrie (1968); 3. measuring individuals in captive cohorts, e.g. of B. truncatus by Demian & Kamel (1972) and B. globosus by O’Keeffe (1985a,b), Marti (1986), Woolhouse & Chandiwana (1990a). Temperature is generally an important influence on growth rate, but other factors seem to be dominant in some localities. In Lake Volta, where temperature varied little through the year, seasonal variation in the growth rate of Bulinus truncatus (=rohlfsi) seemed due mainly to changes in biotopes (Klumpp et al., 1985); it was found that growth was favoured by a substratum of mud, possibly because of the rich food source provided by the microflora. Food shortage contributed to limiting the growth of B. globosus in a reservoir in coastal Kenya (O’Keeffe, 1985b) and Biomphalaria pfeifferi in a stream in eastern Zaire (Baluku & Loreau, 1989). High current speed seemed to cause a seasonal

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reduction in growth by B. globosus in a stream in Tanzania, both directly by stressing the snails and indirectly through reducing food supply (Marti, 1986). Negative effects on growth exerted by crowding have been deduced from observations on natural populations as well as experiments in the laboratory (see later section in this chapter: Crowding Effects). The influence of water temperature on the growth of snails was early demonstrated in two areas of Africa experiencing a distinctly cool winter season, the highveld plateau of Zimbabwe (Shiff, 1964a–c, for B. globosus) and lower Egypt (Dazo et al., 1966, and Demian & Kamel, 1972, for B. truncatus and Biomphalaria alexandrina). Hatching time for eggs of B. truncatus in Egypt varied from 8 days in July (a hot month) to 20 days in the cold month of January (Dazo et al., 1966). Young snails reached a height of 2.5 mm at an age of 11 days when the prevailing water temperature was 25°C, but could take 80 days to reach this size at 15°C (El Hassan, 1974). In the classic study of B. globosus by Shiff, the most rapid increase in shell height was at 25°C, when different cohorts were reared in the laboratory at constant temperatures of 18, 22.5, 25 and 27°C (Shiff, 1964a,b). At 18°C egg production was delayed until snails were about 23 weeks old, more than twice the age of first oviposition at 25°C. Growth rate in a population in a temporary pond (Shiff, 1964b) was high for a cohort hatched in November and growing during the warm season; after 100 days shell height was 13 mm. In a cohort hatched in April and growing during the cool season, shell height was only 6 mm after 100 days. Individual B. globosus commonly grew to over 15 mm high in the laboratory and the pond. Also studying B. globosus on the highveld plateau of Zimbabwe, but observing populations in rivers, Woolhouse & Chandiwana (1990a) too found growth rates were positively correlated with temperature (Fig. 138). Maximum shell heights were 15–17 mm, as in the pond studied by Shiff. In contrast to the highveld of Zimbabwe, where B. globosus grew best in the warm season, conditions in a dam near the coast of Kenya were sub-optimal for this snail, partly because the water temperature was too warm for much of the year (O’Keeffe, 1985a,b). Few snails reached a height of 11 mm; cohorts hatching in November and December during the hot season showed particularly poor growth. Investigations into the influence of temperature on the growth of other species are less extensive than for B. globosus. Biomphalaria pfeifferi grew better in the laboratory at 25°C than at 19°C or 30°C (Sturrock, R.F., 1966); Appleton (1977) found similarly that growth was satisfactory at 25°C and 27°C, but was ‘severely stunted’ at 29°C. An elaborate study of Bulinus tropicus and Lymnaea natalensis was carried out by Prinsloo & Van Eeden (1969, 1973), in which snails were reared at six different constant temperatures over the range 15–30°C. Conditions were standardised to a high degree by continuously circulating water from a storage tank through all the aquaria, and each aquarium was partitioned by a gauze so that both species could be kept separately in the same aquarium. Growth was measured by weighing each snail at monthly intervals. B. tropicus

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grew most rapidly at 27°C and 25°C, though all the snails died between 4.5 and 5.5 months (Fig. 139). At these temperatures oviposition began at an age of about 1.5 months, but not until about 3 months at 15°C. L. natalensis performed better at lower temperatures (Fig. 139); its best rate of growth was at 18°C, though snails reared at 15°C achieved the same weight at 6.5 months. Eggs were generally laid later than B. tropicus, after about 5 months at 15°C (Fig. 139). Finding considerable differences in growth rate among individual B. globosus, Shiff (1964b) speculated that slowly-growing snails might die when young in nature, thus accounting for the higher average growth rates he observed in a pond compared with laboratory-reared cohorts. High variation in growth was still observed, however, in cohorts of B. globosus reared in natural habitats (Woolhouse & Chandiwana, 1990a). Individual weights within groups of B. tropicus and Lymnaea natalensis, hatched from eggs deposited during one 24hour period and reared at 25–27°C, varied at the age of 2.5 months by the surprisingly large factor of almost 20, that is from 6–114 mg (Prinsloo & Van Eeden, 1973, Table 2). Another complication when making an assessment of the growth of snails under natural conditions is infection by trematode parasites, which may cause accelerated growth and ‘gigantism’ in their host. Accelerated growth rates were observed by Sturrock, B.M. (1966, 1967) in both Biomphalaria pfeifferi and Bulinus nasutus when infected by schistosomes. Such an effect on L. natalensis by Fasciola gigantica was postulated by Schillhorn van Veen (1980) as the explanation for size frequency distributions in a snail population that did not conform to the expected seasonal pattern. Seasonal life cycle The life cycles of those tropical African freshwater pulmonates that are well known in this respect are essentially iteroparous, sexual maturity being reached early in life and reproduction having the potential to proceed continuously during most of the life span. There is apparently no example of a clearly semelparous cycle, but little is known of breeding by the smaller species, in which semelparity is perhaps more likely to occur. A large reproductively-active Bulinus could be collected together with smaller snails belonging to several generations of its descendants. Seasonality is imposed by the environment on the life cycle in various ways, most obviously by drying-out of the habitat, which interrupts reproduction completely, and less obviously when, although egg production is continuous, the population structure is strongly heterogeneous and dominated by a few successive cohorts of individuals that can be regarded as different generations. Those species which live in the more ephemeral of the smaller waterbodies have their breeding season narrowly restricted by the brief availability of water; these life cycles could thus evolve towards a more semelparous pattern, and it would be interesting to look for innate rhythms in such species (e.g. Bulinus senegalensis, B. reticulatus, B. tropicus). A tendency towards semelparity possibly occurs also in populations living in the cooler

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Fig. 139. Average growth (grams per month) of (a) Bulinus tropicus and (b) Lymnaea natalensis, reared at constant temperatures. Snails maintained at 25 and 27°C all died before the end of the experiments. Egg laying began at the ages indicated by arrows. After Prinsloo & Van Eeden (1973, Figs 1,2).

climatic areas where breeding may be compressed into a brief warm season (as

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at high altitude or generally in the southern temperate region). The earlier literature on life cycles was well reviewed by Appleton (1978) who stressed the important influence of the degree of permanency of the habitat. Temporary small habitats impose periods of physical stress, not only through drying-up but also through extremes of high and low temperature, and, in seasonal watercourses, flooding. In temporary habitats at least 4 different lifecycle strategies can be distinguished: 1. a single generation each year (e.g. Lymnaea truncatula on the Ethiopian plateau); 2. two main generations per year in North Africa, related to the drying of the canal systems in mid-winter and the occurrence of temperatures most suitable for breeding in the spring and autumn (e.g. Bulinus truncatus in lower Egypt); 3. two main generations each year in the tropics, timed in relation to the two major rainy seasons (e.g. Bulinus and Biomphalaria in East Africa); 4. a greater number of generations, overlapping and in quick succession, depending on the degree of permanence of the habitat (e.g. Bulinus senegalensis). In permanent habitats, although eggs may be laid throughout the year, there may be an obvious annual peak of breeding related to the main rainy season. Appleton (1978) commented that other distinct generations could have been overlooked in some studies because intervals between sampling periods were too long; he proposed a sequence of 3 generations per year as a more accurate interpretation of life cycles in tropical permanent habitats. The life cycle of Bulinus globosus is the best known of any African freshwater pulmonate, from extensive observations in both subtropical and tropical areas. A pioneering study by Shiff (1964a–c) on the plateau of Zimbabwe inspired other major investigations in the same area (Woolhouse & Chandiwana, 1989, 1990a,b), Kenya (O’Keeffe, 1985a,b) and Tanzania (Marti, 1986). Young snails commence egg-laying at an age of 5–7 weeks and a height of 6–7 mm; they continue breeding while growing to a maximum size of 12–17 mm. Eggs develop immediately and hatch about one week after being laid. In a large permanent lagoon in Zaire, where water temperature varied little during the year, a generation appeared about every two months (Malaisse & Ripert, 1977). More commonly an obvious seasonal life cycle is imposed by environmental factors. On the subtropical highveld plateau of Zimbabwe, egg production in ponds is reduced or ceases during the cooler months (Shiff, 1964b,c); in rivers differences among sites in the timing of peak abundance of young snails were related also to recent histories of flooding (Woolhouse & Chandiwana, 1990a). There seem to be at least 2 generations per year on the plateau of Zimbabwe, according to data for egg production and snail size-frequency distributions given by Shiff (1964c). Three overlapping generations were defined in another sub-tropical area, the south-eastern Transvaal, where the life cycle seems also to be essentially temperature-dependent (Appleton, 1974; B. (Physopsis) sp., which probably was B. globosus). But although B. globosus experiences a generally warm climate in

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the tropical Lake Chilwa, southern Malawi, its life cycle there also is strongly seasonal, in relation to fluctuating water level (Cantrell, 1981); snails moved annually with the rising water into the previously dry marginal swamp, where there ensued a brief peak of oviposition on lily leaves during a period of two months. There were marked peaks of egg production in reservoirs on the coast of Kenya following rainfall in the cooler months (O’Keeffe, 1985a,b); here reproduction seemed inhibited by both high temperature and poor quality of food, which was perhaps improved when the reservoirs received nutrients in run-off water during the rains. A similar pattern of reproduction by B. globosus on the Kenyan coast, according to the greater abundance of young snails during the cooler months, had earlier been observed by Teesdale (1962, Table 6). In another tropical area, near Ifakara in Tanzania, eggs were laid throughout the year, but most frequently during the late dry season in a stream, and during the rainy season in a pool (Marti et al., 1985; Marti, 1986). Since temperature in these habitats seemed favourable for much of the year, Marti (1986) suggested that depression of fecundity in the stream could have been due to shortage of food caused by the high current speed during the rainy season, while reproduction in the pool may have been inhibited by the high population density there until this was reduced by the rise in water level during the rainy season. The life cycle of B. truncatus shows clear seasonality in North Africa; although eggs may be laid in all months, peak egg production occurs from February to April, possibly stimulated by increasing temperature and/or heavy rainfall, and there is a secondary peak of oviposition in the autumn after the unfavourably high temperature of summer (Dazo et al., 1966). A similar cycle was observed in experimental ditches by Demian & Kamel (1972), who pointed out that a third ‘winter generation’ is recognisable, derived from the few snails that survive the annual closure in January of water supply to the canals. In dams in northern Ghana, McCullough (1962) noted breeding throughout the year, though with a peak during the period including the end of the rains and the early dry season; mortality of juvenile snails was then high and the re-establishment of populations after the dry season apparently depended on the survival of a few large snails. Oviposition was also observed throughout the year in irrigation channels in northern Nigeria (Betterton, 1984), but survival of eggs and juveniles varied seasonally, being favoured it seemed by cooler conditions and higher oxygen tension. In Lake Volta the life cycle of B. truncatus (=rohlfsi) was related to seasonal changes in biotopes, particularly in water level and vegetation (Klumpp & Chu, 1977; Klumpp et al., 1985); the minimum egg-to-egg cycle was 27 days and highest fecundity occurred where turbidity was low. Life cycles are known to a varying extent for some other species of Bulinus. B. nasutus bred continuously in pools and dams in western Tanzania, with a peak of oviposition immediately following the main rains (Webbe, 1962); egg production commenced at a shell height of about 8 mm reached at 8 weeks, and continued throughout the life span. Full size was not achieved in less than 12 months and after one or two periods of aestivation. The activity of B.

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senegalensis observed by Betterton et al. (1983) lasted for only 5–6 months regardless of whether water was still present in the habitat, and this snail possibly requires a regular period of aestivation in order to maintain a vigorous population. Difficulty was experienced in identifying successive generations of B. senegalensis in temporary pools in the Gambia (Goll & Wilkins, 1984), but 5 or 6 generations were evident in a rainpool during a period of about 20 weeks for a population identified as B. forskalii by Lévêque (1968), but probably B. senegalensis. The life cycle of B. camerunensis in Lake Barombi Kotto, Cameroon, ensured a high rate of reproduction that proved a severe obstacle to control by mollusciciding (Duke & Moore, 1976). Breeding was prolific throughout the year, apparently because of high constant temperature and good food supply; minimum hatching time for eggs was 5 days, and young snails reached maturity and began to lay eggs only 11 days later. The apparently closely-related species B. forskalii has, in some situations at least, a more leisurely life cycle; only a single generation was detected in a pool over a 3–4 month period in Zaire (Malaisse & Ripert, 1977). An interesting difference was observed between the life cycles of two species of Bulinus in the area of Potchefstroom, in the western Transvaal of South Africa. B. africanus here approaches the limit of its penetration into the southern temperate climatic region; breeding takes place mainly during the warmer rainy season, with little or no oviposition during the cool dry winter months (Pretorius et al., 1982). B. tropicus occurs throughout the temperate region and breeds continuously at Potchefstroom, though with two peaks of oviposition, one in early summer and another in mid-winter, even though the water temperature drops below 10°C (Stiglingh & Van Eeden, 1977). How this life cycle responds to environmental factors is not understood; perhaps there is an innate rhythm adapted to the particularly demanding conditions in these habitats. Biomphalaria, like Bulinus, seems to be an iteroparous breeder and the proportion of juvenile snails varied little throughout a year in Nairobi Dam (Teesdale, 1962). Usually, however, seasonal cycles have been observed. Breeding by B. pfeifferi occurred mainly during the warm season in the highlands of Madagascar (Pflüger, 1977), forest zone of Cameroon (Dupouy & Mimpfoundi, 1986), plateau of Zimbabwe (Woolhouse & Chandiwana, 1989; Woolhouse, 1992) and south-eastern Transvaal (Appleton, 1974). In the last area, 3 generations were completed during the year, resulting in a nearly continuous output of schistosome cercariae (Fig. 140). A similar sequence of generations was found in the warmer climatic regime of the coastal plain of north-eastern Natal, though here the density of the summer generation (January and February) was much reduced, due to the adverse effect of high temperature on the fecundity of the previous generation (Appleton, 1977). B. alexandrina seems to be similarly sensitive to high temperature in Egypt, as peak egg production occurred between February and April, and could have been stimulated by low mid-winter temperature in December to February (Dazo et al., 1966). Detailed studies of the life cycle of B. pfeifferi in eastern Zaire revealed

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Fig. 140. Diagram showing the sequence of 3 generations of Biomphalaria pfeifferi in a stream in eastern Transvaal, South Africa (from Appleton, 1974, Fig. 6). Observations covered a period of 15 months; the first generation is taken to begin in August (A), the 2nd in December (D) and the 3rd in March (M).

interesting differences between the populations of two streams (Loreau & Baluku, 1987b; Baluku & Loreau, 1989). Although breeding never entirely ceased during the year, there was a single main generation in the Virunga stream, producing maxima of egg production and population density during the early dry season in June (Fig. 141); this seasonality was attributed to the adverse effects on the snails and their food resources of the high current speed during the rainy season. The second stream, the Bilala, offered more favourable conditions of temperature, calcium concentration and food supply; the longer season of low rainfall allowed time for the completion of 2 main generations (Fig. 141). Breeding by Lymnaea natalensis seems restricted to a moderate range of temperature. In Nairobi Dam (altitude 1670 m) the young appeared throughout the year, but were least abundant during the cool months of June to August (Teesdale, 1962), while at the higher altitude of Nandi (2667 m) no eggs at all were found during the colder months (Preston & Castelino, 1977). Breeding was mainly in the cool season, however, in the warmer climatic areas of south-eastern Transvaal (Appleton, 1974) and Nigeria (Schillhorn van Veen, 1980). Data for L. columella in Africa are available only for the south-eastern Transvaal, where the life cycle followed that of L. natalensis, with only one generation per year (Appleton, 1974). Rainfall is the major factor controlling the life cycle of L. truncatula in Ethiopia; extensive populations were active for a period of only 40 days in a year on temporarily flooded pasture on the plateau (Goll & Scott, 1979). Although egg capsules were found, no newly hatched generation was detected and it appears that the hatchlings retreated early into aestivation. In Lesotho rainfall is generally higher and many of the marshes inhabited by L.

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Fig. 141. Variations in the population density (individuals per square metre) of Biomphalaria pfeifferi in two streams, the Bilala (solid line) and the Virunga (broken line), in eastern Zaire. Data from two study periods, in 1982–83 and 1984–85 (after Baluku & Loreau, 1989, Fig. 1). The single main generation in the Virunga produced a population peak in June 1984; the 2 main generations in the Bilala were completed during the longer favourable period of low rainfall, from June to October. The intrinsic rate of natural increase (r), measured monthly in the Virunga stream was clearly positive only in April–June 1984 (Loreau & Baluku, 1987b).

truncatula are fed by perennial springs; reproduction can continue throughout the year, although the cool drier winter months are less favourable, and violent summer floods may interrupt the life cycle (Prinsloo & Van Eeden, 1976). Crowding effects Inhibition of growth and reproduction in crowded cultures of snails in the laboratory has long attracted the attention of students of African freshwater pulmonates. Among many possible causes suggested are production of inhibitory substances by the snails (Wright, 1960; Chaudhry & Morgan, 1987), depletion of chemical resources in the water and accumulation of waste products (Thomas, 1973; Thomas et al., 1976), and shortage of food of high quality, especially diatoms, even though food is supplied apparently in excess of requirements (Loreau & Baluku, 1987a). B. globosus reared by O’Keeffe (1985b) in netted enclosures in their own habitat at different densities, showed at lower densities significantly better growth, longer survival and greater capacity for population increase. It is difficult to design experiments to demonstrate precisely the effects of crowding and their causes; no investigator has yet been entirely confident in explaining the effects observed. Reported optimum densities for the maintenance in the laboratory of different species of Bulinus range from one to about 10 snails per litre of water (Shiff, 1964b; Sturrock, R.F., 1965; Lévêque, 1968; Webbe & James, 1971; Simões et al., 1974; Ahmed et al., 1986). Whatever their cause, the

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effects of population density must be considered when designing experiments on the growth and reproduction of freshwater snails. The term ‘crowding effect’ has been sometimes applied specifically to the density-dependent regulation of snail populations thought to be caused by substances originating from the snails themselves. This has been seen as a lead towards a means for snail control; the search for a toxic substance that arose from the observation of inhibited growth in a dense population of Biomphalaria in Uganda (Berrie & Visser, 1963; Berrie, 1968) has been described in Chapter 8: Development of molluscicides. That a toxic substance might have accumulated in the habitat was one possible cause considered by Lévêque (1968) to account for the reduction in growth rate and maximum size in snail populations (identified as Bulinus forskalii but perhaps B. senegalensis) during recolonisation of temporary pools after drought. In another instance where crowding was thought to regulate a natural population, there could have been a different cause. Jobin & Michelson (1967) found that the data of Shiff (1964c) for the population fluctuations of B. globosus were best fitted by a mathematical model that included the assumptions that food was a limiting factor and that the population was adversely affected by high density. It appeared significant that during the population peak in January, egg production was low, despite a temperature optimal for breeding; it was therefore suggested that there could have been a food shortage in December immediately after the pond was refilled by rain after drought. Density-dependent effects in the broad sense, including competition for food, may not be unusual in some habitats, but as pointed out by Woolhouse & Chandiwana (1990b, p. 55), snail densities in nature are usually far less than the densities in reported experiments, and water movements would in any case disperse any inhibitory products. Population fluctuations: General considerations Fluctuations in populations of snails, whether seasonal or long-term over a period of years, are linked to the basic instability of the freshwater habitat. Populations are probably most stable in the depths of the large ancient lakes, and they evidently are highly unstable in small seasonal pools, where during a single year a population may be almost eliminated and then increase until the maximum carrying-capacity of the habitat seems to be reached. Mozley (1955) gave an illuminating discussion of instability in freshwater habitats, which is drawn on freely below. During a period of a few years a newly-made pond, if undisturbed, passes from a juvenile stage when it has little vegetation and few species of snail, to an intermediate phase in which plants are abundant and snails more varied, and then a senile condition when plants become so dense as to crowd out most aquatic macro-invertebrates including the snails. A similar pattern of succession tends to take place, though more slowly, in large shallow dams. The few species of snail present in the early stage may be very abundant. As the waterbody matures, the

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number of species increases, while the number of individuals per species decreases. This pattern of development may be disturbed in three main ways: 1) by temporary drying-out of the habitat, due to the seasonal pattern of rainfall; 2) by flooding that erodes the substratum, and 3) by the activities of people and livestock at the margins. These disturbances prevent the growth of vegetation and check the ecological succession. On a wider scale, deforestation and overgrazing destabilize freshwater habitats over large areas, by causing spasmodic and violent run-off of rainfall, with soil erosion and deposition of silt, while dambuilding can change the ecology of wetlands on floodplains by up-setting the seasonal rhythm of flooding. Some snails, especially species of Bulinus are adapted to unstable waterbodies and exploit brief periods of favourable conditions, lasting only a few months, to reproduce rapidly and build up dense populations. Occasionally a population is encountered where the density is abnormally high, due to favourable circumstances that are local and unusual. In a channel near a sugar factory in southern Mozambique, I found Bulinus tropicus in such abundance that several hundred were collected within one minute; favourable factors evident were a constant slow flow of water and the pollution with domestic refuse, which provided food and surfaces of attachment for the snails. The occasional occurrence of population densities very much higher than usual is predicted by the long-term model (Woolhouse & Chandiwana, 1990b) for B. globosus, reviewed in the next section. Population fluctuations: Numerical studies Fluctuations in populations, and other numerical aspects of change in them (population dynamics) make up a complex field of study. The amount of data published in recent years for the African intermediate hosts of schistosomes is so great that the present section, more than any other in this book, serves as a brief and selective introduction to a large literature. One of the most ambitious numerical studies of snail populations was carried out from 1959 to 1962 in a fish pond at Korogwe, north-eastern Tanzania (Pringle & Msangi, 1961; Pringle & Raybould, 1965). The objective was to obtain data about natural fluctuations, with particular reference to Bulinus globosus, that could be used when assessing the effectiveness of snail control operations. The pond was first drained in order to remove fish, clear away reeds, install structures to aid sampling, and to assess the snail populations initially present; it was refilled with water passed through a fine screen. The 3 snail species found at first were B. globosus, Melanoides tuberculata and Cleopatra ferruginea (=amaena). Different methods of sampling (including hand-picking, submerged trays, and bamboo rafts) were compared during a preliminary trial lasting 22 weeks (Pringle & Msangi, 1961). The initial estimated population of about 900 B. globosus increased to about 7000 within a month, mainly it seemed due to the emergence of snails from aestivation. Breeding was intense and by the third week about 132 000 young snails were present, but after the 14th week the

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population declined until it had returned almost to the original level. Three species were not found initially but appeared soon after refilling: B. forskalii and Ceratophallus (=Anisus) natalensis quickly built up large populations, but then declined and disappeared, while Lymnaea natalensis appeared in irregularly fluctuating numbers and never became common. The two prosobranchs showed the narrowest fluctuations, Cleopatra being consistently commoner than Melanoides. The interventions in the Korogwe pond clearly favoured at first B. globosus, B. forskalii and C. natalensis, but conditions became increasingly unsuitable for them all. The early establishment of large populations could have been due partly to a good food supply, which included decaying algae and rotting reeds left after the preparations and a high production of algae in the water soon after refilling. Also, any fish that might have competed with the snails for vegetable food had been removed. The pond was evidently rejuvenated by the interventions, especially the removal of dense vegetation, but it was highly unstable and the rapid regrowth of the plants soon almost eliminated all open water. After 5 months only the prosobranchs were still flourishing, perhaps because of their bottom-feeding habit. In an attempt to learn more about what had happened and to establish reproducible conditions for the study of B. globosus, the pond was emptied again and refilled in a further series of trials (Pringle & Raybould, 1965). The results were disappointingly inconsistent, but are a valuable illustration of the complexities and frustrations to be encountered in such investigations. One trial was abandoned because all the snail populations suffered high mortality as a result of the anaerobic decay of vegetation. B. globosus became abundant in one trial, but not a single snail appeared in another trial where the conditions were apparently the same. A possible explanation for the inconsistencies came to light when it was discovered that the water used for filling the pond contained varying amounts of effluent from a sisal factory. Seasonal fluctuations in populations have already been touched on in the preceding section on seasonality in the life cycle, since it is partly observations of varying abundance that have provided evidence for the succession of generations. The earlier studies (reviewed by Appleton, 1978) showed cyclical changes in relation to seasonal variations in rainfall and temperature or environmental conditions associated with these climatic variables. The degree of permanence of the habitat is another important influence. Thus, the same densityindependent factors may govern the seasonal cycles in both reproduction and numbers; density-dependent influences, such as food shortage, seem more likely to operate in permanent habitats (see preceding section on crowding effects). The expectation that a peak in population should follow a peak in egg production is commonly fulfilled, e.g. by Bulinus truncatus in Egypt (Dazo et al., 1966; Demian & Kamel, 1972), and both Bulinus and Biomphalaria in tropical eastern Africa (Webbe, 1965a, and references therein; Appleton, 1974). Changes were similar in snail density and egg production for B. pfeifferi over a period of two years in eastern Zaire (Loreau & Baluku, 1987b). Population density is not,

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however, necessarily related simply to seasonal variation in egg production, but may depend more on the rate of survival of eggs and young (see B. truncatus, below). Population fluctuations are the outcome of changes within populations that are evaluated by means of a statistic r or rm, the intrinsic (or innate) rate of natural increase. This is a synthetic statistic calculated from a group of biological parameters, usually presented in life tables, expressing the relationship between the rates of birth and death in a population at a particular time. It may be calculated for a cohort of individuals, i.e. a group of similar age recruited into a population at the same time. The pioneers in this field of study in Africa were Webbe (1962, 1965b), who described population dynamics for Bulinus nasutus in ponds in Tanzania, and Shiff (1964a–c) who investigated B. globosus by experiments and in natural habitats in Zimbabwe. Experimental techniques were described and discussed in a series of papers by De Kock & Van Eeden (1981, and references therein); see also De Kock et al. (1986). Comparison of r values among different studies is difficult because of the widely different experimental conditions; Loreau & Baluku (1987a) pointed out that some researchers started observations several weeks after egg-laying, thereby eliminating high mortality in early life and overestimating values for r. With regard to natural populations, Loreau & Baluku (1987b, pp. 259–60) discuss another difficulty, that r represents the rate of increase of a population reaching a stable age-distribution under constant conditions, whereas the objective of field study is usually to investigate seasonal changes, with no assumption of stability in environmental conditions or in age distribution. These authors proposed that under these circumstances, Ro (net reproductive rate) can be validly compared among cohorts, but a version of r should be calculated in a time-dependent manner, e.g. month by month, for the whole population. Bulinus tropicus and Lymnaea truncatula both have high intrinsic rates of increase that enable them rapidly to build up large populations in habitats liable to drying, but their ecologies are different. Because L. truncatula is semiamphibious its population dynamics are determined partly by factors that influence the humidity and feeding conditions on the mud of damp pastures (Prinsloo & Van Eeden, 1976). There is a complex interaction in Lesotho between temperature, rainfall, humidity and plant growth. Dense plant growth in spring and summer increases evaporation of ground moisture, while the reduction of light reaching the substratum reduces the growth of algae on which the snails feed. Conditions vary greatly from one season to another, and among local areas, so that population peaks of L. truncatula in Lesotho may occur at any time during the year, though mostly in either summer or in winter according to area. Among the studies of snails that have recorded population fluctuations in particular detail, those selected for further consideration are of Bulinus truncatus in Ghana and Nigeria, B. globosus in the Equatorial zone and Zimbabwe, and Biomphalaria pfeifferi in Zimbabwe and eastern Zaire.

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B. truncatus in Ghana and Nigeria The populations in two dams in northern Ghana, which did not dry up completely during the dry season, showed an annual cycle of two pronounced phases, one of expansion and the other of contraction (McCullough, 1962). Increase in density and reproductive activity began during the warm rainy season and reached a peak in the cooler dry season. At Yendi this expansion phase ended early in the dry season, when aquatic vegetation had almost disappeared. At Tamale, expansion continued towards the end of the dry season, while Nymphaea leaves were still abundant. The onset of the contraction phase was abrupt and preceded by intense oviposition, but few of the resulting young snails appeared to survive. During the contraction phase there were few mature snails and little reproductive activity; the few mature snails that survived this phase were of critical importance to the continuity of the population. It was the marked increase in survival of young during the late rainy season and early dry season that led to the population peak; despite intense oviposition at other times, survival of young snails was poor. A similar pattern of fluctuation was observed by Betterton (1984) for a population of B. truncatus (=rohlfsi) in a canal of the South Chad Irrigation Scheme in northern Nigeria. A leaf mat sampling technique was used to make weekly counts of snails and eggs over a period of 16 months. Snail numbers increased during the cool dry season and declined sharply in May, when the temperature reached 30°C, just before the beginning of the rainy season. A burst of egg production occurred just before the population crash, as found by McCullough in Ghana. However, there were two indications of reduced population viability in the canal during the few months before the crash: 1) the small proportion of juveniles, despite intense oviposition, suggested high mortality of eggs and/or juveniles during a period when conditions were favourable for adults (a similar situation was described by McCullough for Tamale dam); 2) a reduction in egg mass size, possibly resulting from heavy infections with a larval trematode. There was no marked increase in egg production before the phase of population expansion, which thus appeared to result from improved survival of eggs and young, as found by McCullough in Ghana. A factor that appeared to Betterton to be likely to influence survival was oxygen tension, which would tend to be higher when the water was cooler during the dry season. In Lake Volta, where temperature varies little throughout the year, sharp reductions in populations of B. truncatus (=rohlfsi) during the periods of rising water were caused by the stranding of snails in deeper water. Rapid expansion of populations from November to February was due to the more stable high-water level, less stagnant water, and growths of the plants Polygonum and Ceratophyllum, which provide the most favourable habitats (Klumpp & Chu, 1977).

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B. globosus in the Equatorial zone and Zimbabwe The important influence of rainfall and associated environmental factors on population dynamics has been stressed by numerous investigators, e.g. in Cameroon (Ngonseu et al., 1991), Ghana (McCullough, 1957; Kuma, 1979), Liberia (Sodeman, 1979; Dennis et al., 1983), Mali (Coulibaly & Madsen, 1990), Kenya (Teesdale, 1962; O’Keeffe, 1985a,b; Noda et al., 1988) and Tanzania (Marti et al., 1985; Marti, 1986). Rainfall directly causes population fluctuations through drought and flooding, and it appears to influence rates of oviposition and survival in ways that are not entirely clear. Marti (1986) suggested two different effects of high rainfall; from his observations it appeared that a strong current damaged the food supply for snails in a stream, while rising water level in pools seemed to encourage breeding, possibly by reducing the population density and thus removing a density-dependent inhibition of reproduction. Where temperature was found to be of importance comparable to rainfall, in dams on the coast of Kenya (O’Keeffe, 1985a), growth and reproduction were inhibited during hot periods; this, added to poor feeding conditions, resulted in population increase being possible in only a few months of the year (Fig. 142). Fluctuations of B. globosus populations have been studied in particular detail on the highveld plateau of Zimbabwe (Shiff, 1964c; Woolhouse & Chandiwana, 1989, 1990a,b). Marked changes in numbers occur in time and space, mainly in relation to rainfall and temperature, but in this comparatively cool climatic area it is the warmer periods that are favourable for growth and breeding. The chief seasonal influences are the cold winter, when breeding ceases almost entirely, the drying-up of some habitats and the violent flooding which washes away many snails. Drought and flooding vary in timing and intensity from one year to another; their effects modify to a varying degree the population cycle that would proceed under the sole influence of seasonal changes in temperature. All the major environmental influences were demonstrated by Shiff (1964c) in habitats that for most of the year were ponds, but after exceptionally heavy rainfall were scoured by floods. At the beginning of the sampling period in March, near the end of the rainy season (Fig. 143), both the numbers of snails and the production of eggs were increasing. By May the rains had ceased and water temperature had fallen; few eggs were found but the population continued to increase as the cooler conditions were good for survival. A population peak was reached in June, but from then onwards the water began to dry up, the population declined and the entire habitat became dry in early August. Rain refilled the ponds towards the end of November and snails that emerged from aestivation began immediately to lay eggs; the population peaked in January 1963 during a warm period of heavy rainfall, though no great run-off had yet occurred. Later in January there was severe flooding and the population was greatly reduced in February and March. Jobin & Michelson (1967) applied a population dynamics model to these data (referred to also in the preceding section: Crowding Effects). On the assumption

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Fig. 142. Mean monthly rates of intrinsic natural increase for cohorts of B. globosus in reservoirs near the Kenya coast during 1980 and 1981, in relation to mean water temperature at a cohort age of 3 months. All positive values for r, indicating a potential for population increase, were recorded at mean temperatures below 28.5°C; mostly for cohorts hatched during the months March–June. From O’Keeffe (1985a, Fig. 6).

of no crowding effects, this model predicted a population greatly exceeding the observed numbers (Fig. 143, broken line); the observed data were best fitted by the assumption that adverse crowding effects would arise at densities above one snail per 100 litres (Fig. 143, solid line). However, this model was criticised by Woolhouse & Chandiwana (1990b, p. 159) for its emphasis on dubious densitydependent effects and the lack of provision for the effect of temperature. In the small rivers on the Zimbabwean highveld studied by Woolhouse & Chandiwana (1990a,b) and in a stream in Zambia (Shehata, 1989), the population dynamics of B. globosus seem to be dominated by density-independent factors. Woolhouse & Chandiwana observed floods and droughts to cause variable and irregular reductions in abundance. Year-to-year fluctuations were largely due to the effects of sudden spates, which washed away snails from some sites and deposited them in others. Low rainfall resulted in the drying-out of some pools inhabited by B. globosus in rivers, probably also contributing to long-term fluctuations. Woolhouse & Chandiwana (1990b) developed a mathematical model to describe the population dynamics, taking into account the effects of temperature on the recruitment and mortality rates of adult snails, and the

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Fig. 143. Changes in the population density of Bulinus globosus in a natural habitat on the plateau of Zimbabwe observed in 1962 and 1963 by Shiff (1964c) compared with changes predicted by a mathematical model; after Jobin & Michelson (1967, Fig. 2). Circles represent the natural population. The solid line is the predicted population assuming adverse effects of crowding to begin at a density of one snail per 100 litres of water; the broken line is the model prediction in the absence of any crowding effect. For criticisms of this model see Woolhouse & Chandiwana (1990b).

frequency and effects of spates. Some simulated fluctuations in abundance over 2 years, incorporating the effects of spates, indicated a net decline in density (Fig. 144). Simulations over 10 or more years predicted 10-fold fluctuations in snail abundance (Fig. 144). The model suggests that B. globosus is relatively rare in a particular habitat for long periods, but for short intervals may increase to out standingly high numbers. This implies that in a given year, snails are comparatively rare at most sites and approach maximum potential densities in only a few. This conclusion is consistent, as pointed out by Woolhouse & Chandiwana, with field observations, and it perhaps is applicable to other ‘opportunistic’ freshwater pulmonates. Biomphalaria pfeifferi in Zimbabwe and eastern Zaire Seasonal variations in the abundance of this snail in river sites in Zimbabwe were related to temperature and water flow (Woolhouse, 1992). Comparative data for Bulinus globosus in these sites, obtained during the same study

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Fig. 144. Fluctuations in the population density of B. globosus in river habitats on the plateau of Zimbabwe, predicted by a mathematical model (Woolhouse & Chandiwana, 1990b). (a) For a simulated 2 year period, incorporating standard water temperatures and the effects of rainfall (2 spates in the first year and one in the second, indicated by arrows). This results in a net decline in abundance over the 2 year period (logarithmic scale). From Woolhouse & Chandiwana (1990b, Fig. 4b). (b) Over a 30 year period; example of a simulation incorporating stochastic effects of rainfall. Abundances estimated for the last week of November in each year (linear scale); initial abundance set at 1000 snails. From Woolhouse & Chandiwana (1990b, Fig. 5).

period, indicate that Biomphalaria pfeifferi has both higher mortality rates and higher maximum recruitment rates. Woolhouse points out that this suggests higher rates of changes in abundance for B. pfeifferi, which accords with the greater spatial and temporal variation in abundance for this species in Zimbabwe.

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The population dynamics of B. pfeifferi were investigated in both the laboratory, at ambient temperature, and in the field in two areas of eastern Zaire, differing in climate: 1) Lwiro (altitude 1740 m) and a nearby stream, the Virunga (Loreau & Baluku, 1987a,b), and 2) Uvira (altitude 800 m) and a drain, the Bilala, near Kiliba (Baluku & Loreau, 1989). Growth in field populations was similar to growth in the laboratory, but population dynamics were very different in the field. Despite continuous reproduction, field populations were dominated by either one main generation (Virunga) or two (Bilala). The Virunga population reached its peak during the period from May to July (Fig. 141), the dry season, and this group of snails dominated the population for the rest of the year. Mortality of newly-hatched snails was much higher than in the laboratory; estimated values for survivorship after hatching were no more than one-tenth of the 81% in the laboratory. There were well-marked seasonal changes in mortality and fecundity, but throughout the year reproduction was strongly restrained compared to the potential calculated from laboratory data. Only cohorts born early in the year (January to April) grew up to experience breeding conditions which were favourable enough for any increase in population. The parameter r was clearly positive only during the months April–June; the main cohort born about June made little if any positive contribution to the population. Current speed seemed to be the most important environmental factor determining population dynamics in the Virunga. There was some evidence that juvenile snails sheltered in the substratum to avoid unfavourable conditions, and it was concluded that the fate of newly-hatched snails deserves further investigation. The population dynamics of B. pfeifferi in the Bilala drain differed, mainly because of the longer dry season of about 5 months, which allowed time for two successive main generations during the period June–October 1984 (Fig. 141); fecundity was higher than in the Virunga. Conditions that seemed more favourable in the Bilala were a warmer temperature, higher calcium concentration, better food supply in the form of diatoms and a generally lower current speed. Productivity of pulmonate populations The study of Lake Kariba by Machena & Kautsky (1988) provides apparently the only available estimates for biomass of aquatic pulmonates in tropical Africa. They contributed a mere 0.1% of the total biomass of benthic animals in this lake, in comparison with the 4.1% made up by prosobranchs. The two higher biomasses recorded for limited areas were 0.24 g m−2 (dry weight including shell) for Bulinus sp. in the depth zone 5–6 m, and 0.11 g m−2 for Biomphalaria pfeifferi at 0–1 m depth.

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Haridi, A.A.M., El Safi, S.H. & Jobin, W.R. 1985. Survival, growth and reproduction of the imported ampullarid snail Marisa cornuarietis in central Sudan. Journal of Tropical Medicine and Hygiene, 88:135–144. Hart, R.C. 1979. The invertebrate communities: zooplankton, zoobenthos and littoral fauna. In Lake Sibaya: 108–160. Allanson, B.R. (Ed.). Monographiae Biologicae, 36. The Hague, Boston, London: W.Junk. Heller, J. & Farstey, V. 1990. Sexual and parthenogenetic populations of the freshwater snail Melanoides tuberculata in Israel. Israel Journal of Zoology, 37:75–87. Jennings, A.C., De Kock, K.N. & Van Eeden, J.A. 1973. The effects of the total dissolved salts in water on the biology of the freshwater snail Biomphalaria pfeifferi. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 50:26 pp. Jobin, W.R. & Michelson, E.H. 1967. Mathematical simulation of an aquatic snail population. Bulletin of the World Health Organisation, 37:657–664. Klumpp, R.K. & Chu, K.Y. 1977. Ecological studies of Bulinus rohlfsi, the intermediate host of Schistosoma haematobium in the Volta Lake. Bulletin of the World Health Organisation, 55:715–730. Klumpp, R.K., Chu, K.Y. & Webbe, G. 1985. Observations on the growth and population dynamics of Bulinus rohlfsi in an outdoor laboratory at lake Volta. Annals of Tropical Medicine and Parasitology, 79:635–642. Kuma, E.E. 1979. Morphology and life cycle of forest and savanna populations of Bulinus globosus in Ghana. Ghana Journal of Science, 17:51–64. Lévêque, C. 1968. Biologie de Bulinus forskali de la région de Fort-Lamy (Tchad). Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, Série Hydrobiologie, 2:79– 90. Lévêque, C. 1971. Equation de von Bertalanffy et croissance des mollusques benthiques du lac Tchad. Cahiers de l’Office de la Recherche Scientifique et Technique OutreMer, Série Hydrobiologie, 5:263–283. Lévêque, C. 1972. Mollusques benthiques du lac Tchad: écologie, études des peuplements et estimations des biomasses . Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, Série Hydrobiologie, 6:3–45. Lévêque, C. 1973. Dynamique des peuplements, biologie et estimations de la production des mollusques benthiques du lac Tchad. Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, Série Hydrobiologie, 7:117–147. Lévêque, C., Dejoux, C. & Lauzanne, L. 1983. The benthic fauna: ecology, biomass and communities. In Lake Chad: 233–272. Carmouze, J.P., Durand, J.R. & Lévêque, C. (Eds). Monographiae Biologicae, 53. The Hague, Boston, Lancaster: W.Junk. Loreau, M. & Baluku, B. 1987a. Growth and demography of populations of Biomphalaria pfeifferi (Gastropoda, Planorbidae) in the laboratory. Journal of Molluscan Studies, 53: 171–177. Loreau, M. & Baluku, B. 1987b. Population dynamics of the freshwater snail Biomphalaria pfeifferi in eastern Zaire. Journal of Molluscan Studies, 53:249–265. Louda, S.M. & McKaye, K.R. 1982. Diurnal movements in populations of the prosobranch Lanistes nyassanus at Cape Maclear, Lake Malawi, Africa. Malacologia, 23:13–21. Machena, C. & Kautsky, N. 1988. A quantitative diving survey of benthic vegetation and fauna in Lake Kariba, a tropical man-made lake. Freshwater Biology, 19: 1–14.

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Madsen, H. 1990. The effect of sodium chloride concentration on growth and egg laying of Helisoma duryi, Biomphalaria alexandrina and Bulinus truncatus (Gastropoda: Planorbidae). Journal of Molluscan Studies, 56:181–187. Malaisse, F. & Ripert, C. 1977. Dynamique des populations de Biomphalaria pfeifferi, B. sudanica rugosa, Bulinus globosus et B. forskalii (Planorbidae) dans la région du Lac de Retenue de la Lufira (Shaba, Zaire). International Journal of Tropical Ecology and Geography, 3:189–208. Marti, H.P. 1986. Field observations on the population dynamics of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara area, Tanzania. Journal of Parasitology, 72:119–124. Marti, H.P., Tanner, M., Degrémont, A.A. & Freyvogel, T.A. 1985. Studies on the ecology of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara area, Tanzania. Acta Tropica, 42:171–187. McCullough, F.S. 1957. The seasonal density of populations of Bulinus (Physopsis) globosus and B. forskalii in natural habitats in Ghana. Annals of Tropical Medicine and Parasitology, 51:235–248. McCullough, F.S. 1962. Further observations on Bulinus truncatus rohlfsi (Clessin) in Ghana. Bulletin of the World Health Organisation, 27:161–170. Mozley, A. 1955. Sites of Infection. Unstable areas as sources of parasitic diseases: schistosomiasis and fascioliasis. London: Lewis. Nduku, W.K. & Harrison, A.D. 1976. Calcium as a limiting factor in the biology of Biomphalaria pfeifferi (Krauss). Hydrobiologia, 49:143–170. Ngonseu, E., Greer, G.J. & Mimpfoundi, R. 1991. Dynamique des populations et infestation de Bulinus globosus en zone soudano-sahelienne du Cameroun. Annales de la Société Belge de Médecine tropicale, 71:295–306. Noda, S., Shimada, M., Sato, K., Ouma, J., Thiongo, F.W. et al. 1988. Effect of mass chemotherapy and piped water on numbers of Schistosoma haematobium infections and prevalence in Bulinus globosus in Kwale, Kenya. American Journal of Tropical Medicine and Hygiene, 38:487–495. O’Keeffe, J.H. 1985a. Population biology of the freshwater snail Bulinus globosus on the Kenya coast. 1. Population fluctuations in relation to climate. Journal of Applied Ecology, 22:73–84. O’Keeffe, J.H. 1985b. Population biology of the freshwater snail Bulinus globosus on the Kenya coast. 2. Feeding and density effects on population parameters. Journal of Applied Ecology, 22:85–90. Pflüger, W. 1977. Ecological studies in Madagascar of Biomphalaria pfeifferi, intermediate host of Schistosoma mansoni. 1. Seasonal variations and epidemiological features in the endemic area of Ambositra. Archives de l’Institut Pasteur de Madagascar, 45:79–114. Pointier, J.P., Toffart, J.L. & Lefèvre, M. 1991. Life tables of freshwater snails of the genus Biomphalaria (B. glabrata, B. alexandrina, B. straminea) and of one of its competitors Melanoides tuberculata under laboratory conditions. Malacologia, 33: 43–54. Preston, J.M. & Castelino, J.B. 1977. A study of the epidemiology of bovine fascioliasis in Kenya and its control using N-tritylmorpholine. British Veterinary Journal, 133: 600–608.

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Pretorius, S.J., Van Eeden, J.A., De Kock, K.N. & Joubert, P.H. 1982. Mark-recapture studies on Bulinus (Physopsis) africanus (Krauss) (Mollusca, Pulmonata). Malacologia, 22:93–102. Pringle, G. & Msangi, A.S. 1961. Experimental study of water snails in a fishpond in Tanganyika. 1. Preliminary trial of the method. East African Medical Journal, 38: 275–293. Pringle, G. & Raybould, J.W. 1965. The experimental study of water snails in a fishpond in Tanganyika. 2. Attempts to establish reproducible conditions. East African Medical Journal, 42:289–296. Prinsloo, J.F. & Van Eeden, J.A. 1969. Temperature and its bearing on the distribution and chemical control of freshwater snails. South African Medical Journal, 43: 1363–1365. Prinsloo, J.F. & Van Eeden, J.A. 1973. The influence of temperature on the growth rate of Bulinus tropicus (Krauss) and Lymnaea natalensis Krauss. Malacologia, 14:81–88. Prinsloo, J.F. & Van Eeden, J.A. 1976. Population dynamics of freshwater snails in Lesotho with particular reference to Lymnaea truncatula, the intermediate host of Fasciola hepatica. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 72:60 pp. Schillhorn van Veen, T.W. 1980. Dynamics of Lymnaea natalensis populations in the Zaria area (Nigeria) and the relation to Fasciola gigantica infection. Acta Tropica, 37:183– 194. Shehata, M.A. 1989. Field studies on schistosomiasis in Zambia. 1. Seasonal fluctuations in the population density of Biomphalaria pfeifferi and Bulinus globosus in a schistosomiasis endemic area in Zambia. Zambia Journal of Science and Technology, 8:36–46. Shiff, C.J. 1960. Observations on the capability of freshwater vector snails to survive dry conditions. Journal of Tropical Medicine and Hygiene, 63:89–63. Shiff, C.J. 1964a. Studies on Bulinus (Physopsis) globosus in Rhodesia. 1. The influence of temperature on the intrinsic rate of natural increase. Annals of tropical Medicine and Parasitology, 58:94–105. Shiff, C.J. 1964b. Studies on B. (P.) globosus in Rhodesia. 2. Factors influencing the relationship between age and growth. Annals of Tropical Medicine and Parasitology, 58: 106–115. Shiff, C.J. 1964c. Studies on B. (P.) globosus in Rhodesia. 3. Bionomics of a natural population existing in a temporary habitat. Annals of Tropical Medicine and Parasitology, 58:240–255. Simo s, M., Grácio, M.A. & Azevedo, J.F.de, 1974. Effects of the population density on the growth and fecundity of the specimens of the Bulinus sp. Anais do Institute de Higiene e Medicina Tropical, Lisboa, 2:535–539. Sodeman, W.A. 1979. A longitudinal survey of schistosome vector snail populations in Liberia. American Journal of Tropical Medicine and Hygiene, 28:531–538. Stiglingh, I. & Van Eeden, J.A. 1977. Population dynamics and ecology of Bulinus tropicus. Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 87:37 pp. Sturrock, B.M. 1966. The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology, 60:187–197.

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Sturrock, B.M. 1967. The effect of infection with Schistosoma haematobium on the growth and reproduction rates of Bulinus (Physopsis) nasutus productus. Annals of Tropical Medicine and Parasitology , 61:321–325. Sturrock, R.F. 1965. Studies on the biology of Biomphalaria angulosa Mandahl-Barth and on its ability to act as an intermediate host of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology, 59:1–9. Sturrock, R.F. 1966. The influence of temperature on biology of Biomphalaria pfeifferi (Krauss), an intermediate host of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology, 60:100–105. Teesdale, C. 1962. Ecological observations on the molluscs of significance in the transmission of bilharziasis in Kenya. Bulletin of the World Health Organisation, 27: 759– 782. Thomas, J.D. 1973. Schistosomiasis and the control of molluscan hosts of human schistosomiasis with particular reference to possible self-regulatory mechanisms. Advances in Parasitology, 11:307–394. Thomas, J.D., Powles, M. & Lodge, R. 1976. The chemical ecology of Biomphalaria glabrata; the effects of ammonia on the growth rate of juvenile snails. Biological Bulletin of the Marine Biological Laboratory, Woods Hole, 151:386–397. Vrijenhoek, R.C. & Graven, M.A. 1992. Population genetics of Egyptian Biomphalaria alexandrina (Gastropoda, Planorbidae). Journal of Heredity, 83:255–261. Webbe, G. 1962. The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bulletin of the World Health Organisation, 27:59–85. Webbe, G. 1965a. Natural trends in snail populations in relation to control of bilharziasis in East Africa. East African Medical Journal, 42:605–613. Webbe, G. 1965b. Transmission of bilharziasis. 1. Some essential aspects of snail population dynamics and their study. Bulletin of the World Health Organisation, 33: 147–153. Webbe, G. & James, C. 1971. The importation and maintenance of schistosomes of medical and veterinary importance. Symposia of the British Society of Parasitologists, 9: 77–107. Woolhouse, M.E.J. 1988. A mark-recapture method for ecological studies of schistosomiasis vector snail populations. Annals of Tropical Medicine and Parasitology, 82: 485–497. Woolhouse, M.E.J. 1992. Population biology of the freshwater snail Biomphalaria pfeifferi in the Zimbabwe highveld. Journal of Applied Ecology, 29:687–694. Woolhouse, M.E.J. & Chandiwana, S.K. 1989. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology, 98:21–34. Woolhouse, M.E.J. & Chandiwana, S.K. 1990a. Population biology of the freshwater snail Bulinus globosus in the Zimbabwe highveld. Journal of Applied Ecology, 27: 41– 59. Woolhouse, M.E.J. & Chandiwana, S.K. 1990b. Population dynamics model for Bulinus globosus, intermediate host for Schistosoma haematobium, in river habitats. Acta Tropica, 47:151–160. Wright, C.A. 1957. Studies on the structure and taxonomy of Bulinus jousseaumei (Dautzenberg). Bulletin of the British Museum (Natural History), Zoology, 5:1–28. Wright, C.A. 1960. The crowding phenomenon in laboratory colonies of freshwater snails. Annals of Tropical Medicine and Parasitology, 54:224–232.

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Wright, C.A., Klein, J. & Eccles, D.H. 1967. Endemic species of Bulinus (Mollusca: Planorbidae) in Lake Malawi (=Lake Nyasa). Journal of Zoology, 151:199–209.

Chapter 12. Regions, lakes and rivers: Biogeography

Like most northerners I scan the map of Africa from north to south and my bird’s-eye view of its snails begins at the Mediterranean coast. By looking first at northern Africa we can examine the southern limits for species derived from the Palaearctic Region and then study the limits of penetration by tropical species towards the cool southern tip of the continent. The success of introduced pulmonates is a feature of southern Africa and they are discussed together with the other snails introduced into African fresh waters. A large part of the tropical fauna is then covered in accounts for islands, major lakes and the larger river basins. A summary of biogeographical aspects follows; the Afrotropical freshwater snail fauna is highly distinctive in comparison with other continents, in relation to its origins and subsequent history. Northern Africa Fresh waters in the coastal region of North Africa are separated from those in tropical Africa by about 2000 km of desert. This distinct zone of habitats is itself subdivided, as fresh waters are few between Tunisia and the Nile Delta, so that the aquatic molluscan fauna can be considered in two parts, that of North West Africa and that of Egypt. The coastal plains and mountains of Morocco, Algeria and western Tunisia form a substantial area of comparatively high rainfall known as the Maghreb, which extends up to 250 km south from the coast (Fig. 145). In the eastern Maghreb many lakes (chotts) are saline, especially in the Touggourt Depression, although various prosobranchs can live where the concentration of salts is less extreme (Beadle, 1943). In southern Tunisia too, prosobranchs (Hydrobiids, Melanoides, Melanopsis) are widespread and showed a greater tolerance than Bulinus truncatus to high conductivity and high chloride concentration (Meier-Brook et al., 1987). A list of gastropod species for the Maghreb (Table 12.1) shows that the majority are of palaearctic origin and only two tropical species occur, Melanoides tuberculata and Bulinus truncatus; the bivalves seem entirely palaearctic. The palaearctic molluscs can be divided into 4 groups (Van Damme, 1984): 1) species common in northern Europe, but rare or absent in southern Europe, and represented in the Maghreb by relict populations at higher altitude (e.g. Lymnaea stagnalis); 2) species with a broad palaearctic

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range (e.g. Ancylus fluviatilis, Planorbis planorbis); 3) species with a southern European/Mediterranean range (e.g. Hydrobia aponensis, Melanopsis and Planorbarius metidjensis); 4) groups of palaearctic origin and which have evolved endemic taxa (Theodoxus, Hydrobiidae). Members of groups 2 and 3 are widespread in the Maghreb and some occur south of the Atlas Mountains in oases and springs in the Algerian desert (Ancylus and Melanopsis). Some of the palaearctic species obtained in North West Africa by early collectors are no longer found, probably because of habitat destruction by man and perhaps also due to competition from Melanopsis, which is highly resistant to drought, tolerant of salinity and can live at high population density (Dupouy et al., 1980). Only 6 species of freshwater snail are found in both North West Africa and in Egypt (Table 12.1): Melanoides tuberculata, Lymnaea stagnalis, L. truncatula, Table 12.1. The freshwater snails of North West Africa and Egypt; modified from Brown (1980) with reference to Van Damme (1984) and Kristensen (1985). Most of the species found in NW Africa occur in the Maghreb area; the two tropical species Segmentorbis angustus and Biomphalaria pfeifferi are known only from SE Algeria. P indicates palaearctic affinity. (†) No recent record and probably extinct. Species or genus Prosobranchs Theodoxus (3 endemic species) P T. niloticus P Bellamya unicolor Lanistes carinatus Pila ovata Valvata nilotica P Hydrobia P Pseudamnicola P Hydrobioid genera of uncertain number P Bithynia tentaculata P Gabbiella senaariensis Cleopatra bulimoides Melanoides tuberculata Melanopsis praemorsa P Pulmonates Lymnaea peregra P L. palustris P L. truncatula P L. stagnates P L. natalensis L. columella (introduced)

North West Africa

Egypt

× — — — — — × × × × — — × ×

— × × × × × × × — — × × × —

× × × × — —

— — × × × ×

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 549

Fig. 145. Africa, showing areas (stippled) where rainfall is less than 10 mm per month in at least three consecutive months (according to Balinsky, 1962). The past southern limit for species from the Palaearctic Region (solid line; according to Van Damme, 1984) extended into the Sahara and included the basins of lakes Chad and Turkana. At present palaearctic species are concentrated in the Maghreb, the area of relatively high rainfall in the extreme north-west of the continent (unstippled).

550 FRESHWATER SNAILS OF AFRICA

Species or genus

North West Africa

Egypt

Ancylus fluviatilis P Ferrissia Planorbis planorbis P Armiger crista P Gyraulus sp. (?laevis) P G. ehrenbergi P Anisus P Afrogyrus coretus Hippeutis complanatus P Segmentorbis angustus S. eussoensis Biomphalaria pfeifferi B. alexandrina Planorbarius metidjensis P Helisoma duryi (introduced) Bulinus truncatus B. forskalii Physa acuta

× — × × × — † — † × (SE Algeria) — × (SE Algeria) — × — × — ×

— × × × — × — × — — × — × — × × × ×

Planorbis planorbis, Bulinus truncatus and Physa acuta. Some of these species are quite likely to have been transported by human agency (especially Melanoides and Physa), while L. stagnalis has been found in Egypt only once. There thus is little evidence of natural dispersal between the Maghreb and Egypt. The snail fauna of Egypt is in fact dominated by tropical species and its palaearctic species could all have originated from the Near East. In Egypt fresh waters have long been much modified by human activities (papyrus may be extinct) and it might be suspected that the snail fauna has been impoverished by habitat destruction and pollution. But the species found as shells of Neolithic age in the Faiyum Depression (Gardner, 1932) seem hardly different from those of modern Egypt, after taking into account nomenclatural changes. It is likely, however, that increasing salinity of lakes in the delta has eliminated some freshwater species (Rzoska, 1976), e.g. in Lake Mariut (Mareotis) M. tuberculata is the only freshwater snail recently found (Samaan & Aleem, 1972). Palaearctic species have not penetrated the lower Nile to a great extent; only Theodoxus, Valvata and Planorbis are known to have reached so far south as the north Sudan (Martin, 1968). Lymnaea truncatula is known from Egyptian oases, but its extensive range in eastern Africa did not necessarily depend on dispersal via the Nile. Routes other than the Nile could also account for the presence of palaearctic species in Ethiopia (see below, the Nile Basin). The failure of some tropical species common in East Africa to have dispersed further northwards,

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 551

despite the route offered by the Nile, is surprising (e.g. the Bulinus africanus group and the genus Ceratophallus). At present there is little possibility of contact among the snail faunas of tropical Africa, Egypt and the Near East, because of aridity in the lower Nile Basin and in the Sinai Peninsula, but this isolation may be relatively recent, as there is little endemism in the Egyptian snail fauna. The local species Theodoxus niloticus, Valvata nilotica and Gyraulus ehrenbergi seem closely related, respectively, to T. jordani, V. saulcyi and G. piscinarum of the Near East. Afrogyrus oasiensis (Demian) seems indistinguishable from A. coretus of tropical Africa. The Sahara has long been the major influence on distribution of aquatic organisms in northern Africa, and the distributions of snails have ebbed and flowed with the succession of dry and wet phases. Big changes have occurred within the comparatively short period of the last 12 500 years, which includes a major series of wet phases, the ‘Last Pluvial’. The climatic history and changes in snail faunas are described in detail by Beadle (1981) and Van Damme (1984) and the data are too copious to summarise adequately here. Living or recently living gastropods are found in refuges in mountainous areas, e.g. in southern Algeria (Tassili N’Ajjer and Ahaggar or Hoggar), northern Niger (Air) and Chad (Tibesti), where palaearctic and tropical species appear to live or to have recently lived together (Van Damme, 1984, Table 4). In some places underground water emerges as springs, which are particularly numerous in the Fezzan region of southern Libya, where B. truncatus is quite widespread in associated irrigation channels and cisterns (Itagaki & Yasuraoka, 1975). Within the last few thousand years the shrinking waterbodies in the Sahara have suffered much disturbance by people and livestock and some species of snail could have been eliminated, that would otherwise still be living in refuges today. The limits of distribution for palaearctic and tropical species are considered further in the discussion of biogeography at the end of this chapter. Southern Africa Taking its northern boundary to include the basins of the Zambezi and Cuanza rivers, southern Africa is a very large area and has a correspondingly varied ecology (Werger, 1978). The inland waters were reviewed, though with little attention to snails, by Allanson et al. (1990). Amongst the freshwater habitats there are striking differences between the lagoons and meandering rivers on the eastern tropical plains and the streams and temporary pools of the southern highveld and mountains, where the winter is cold and frosty nights are frequent (Fig. 146). Lakes Malawi and Sibaya are dealt with in a later section of this chapter, and as snail faunas of the major river basins seem to have few if any distinctive species, we are concerned here mostly with the gastropods of small waterbodies. The total of species probably does not exceed 50 and their distribution is known in some detail, partly from early collecting by amateur naturalists (Connolly, 1939) and subsequently from a survey during the last 40

552 FRESHWATER SNAILS OF AFRICA

Fig. 146. Relief map of southern Africa showing the annual frequency of nights with minimum temperature below 0°C (from Schulze, 1965, Fig. 85). In decreasing order of size, the areas outlined experience averages of between 5 and 90 frosty nights per year. The coldest area is centred on the Drakensberg range in Lesotho. Reproduced by courtesy of the Weather Bureau, Department of Transport, Republic of South Africa.

years, carried out in great detail by J.A.Van Eeden and colleagues in the University of Potchefstroom. Distribution and dispersal, especially of aquatic organisms, are limited in the central and western parts of southern Africa by the ‘drought’ corridor (Fig. 145), which connects the Karoo-Namib arid region with the drier part of East Africa. But there is no such major barrier to dispersal in the eastern region; here differences between the molluscan faunas of the tropical and temperate climatic regions are particularly evident and are well marked in the eastern Transvaal and Natal. Thus the freshwater gastropods of southern Africa may be divided into two groups; tropical species that penetrate southwards to a varying extent and a smaller number of species associated with the cooler climate area of the southern temperate region. Before considering the tropical and the temperate faunas, a brief reference may be made to a faunal classification of the freshwater invertebrates in southern Africa proposed by Harrison (1965, 1978), with particular reference to the insects of running waters. This system recognised two main groups:

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 553

1) A ‘South temperate Gondwanian fauna’. Species related to organisms found in the southern tips of other continents. They are found mostly in Cape Province and are adapted to cool conditions in the upper zones of montane rivers and streams. The genus Tomichia conforms to this group to the extent that it is of Gondwanaland origin, being most closely related to pomatiopsids in SE Asia (Davis, 1981), but its species are mostly specialised for life in coastal lagoons and isolated springs in arid areas. 2) A ‘Pan-Ethiopian fauna’, comprising 5 subgroups: (a) Widespread and eurythermal species. Perhaps the introduced species Lymnaea columella and Physa acuta are potentially of this nature, but no native snail seems to occur independently of climatic temperature. Those that are more than usually widespread appear to be adapted primarily to tropical conditions (e.g. Lymnaea natalensis, Gyraulus costulatus and Bulinus reticulatus), whereas the widely distributed Ceratophallus natalensis is more common in temperate areas, (b) Warm stenothermal tropical species. Many freshwater gastropods belong to this group, including the intermediate hosts for schistosomes. They penetrate to varying distances southwards in the warm lowlands, (c) Highveld or ‘warm temperate’ species. These are characteristic of the highveld, though some extend down to sea level in the cooler parts of Cape Province. Gyraulus connollyi conforms well to this group, and also Lymnaea truncatula and Bulinus tropicus. Possibly further examples will be recognised when the taxonomy of the Ancylidae of southern Africa is better known, (d) Cold stenothermal montane species, (e) Temporary mountain stream species: gastropod molluscs seem entirely lacking from both groups. The tropical fauna of Southern Africa Of the freshwater gastropods found in southern Mozambique, an entirely tropical area, most occur also in south-eastern Transvaal and in northern Natal (Table 12.2); only some of these penetrate further southwards into eastern Cape Province and even fewer are found in the western Cape (notable absentees being Biomphalaria and the Bulinus africanus group). The distributions of these species are associated with the relatively warm climatic zone in the eastern coastal area, of which the part in Natal is known as the ‘tropical corridor’ (Chapter 5, Fig. 131). To this are related the distributions of various organisms, including amphibians (Poynton, 1964; Stuckenberg, 1969). In Natal I found that freshwater gastropod species nearing the southern limit of their ranges occurred in Table 12.2. The freshwater snails of some areas of southern Africa: Mozambique (south of the Zambezi River) and 4 parts of the Republic of South Africa. T indicates association with the temperate climatic area (the other indigenous species belong to the tropical fauna).×= present; (×)=comparatively uncommon. Longitude 24° is taken as an arbitrary boundary between the eastern and western parts of Cape Province. Further investigations

554 FRESHWATER SNAILS OF AFRICA

are needed particularly of the distributions of members of these pairs of taxa: Afrogyrus and Ceratophallus, Bulinus africanus and B. globosus, B. natalensis and B. tropicus. Mozambique E Transvaal lowveld Natal E Cape W Cape Prosobranchs Neritina (3 species) Septaria borbonica Bellamya capillata Lanistes ovum L. ellipticus Pila ovata Tomichia natalensis Tomichia (6 species in total) Cleopatra elata C. ferruginea Thiara amarula Melanoides tuberculata M. victoriae Pulmonates Lymnaea natalensis L. truncatula T L. columella (introduced) Burnupia spp Ferrissia spp Afrogyrus coretus Ceratophallus natalensis Gyraulus costulatus G. connollyi T Lentorbis spp Segmentorbis kanisaensis Segmentorbis, other spp Biomphalaria pfeifferi Helisoma duryi (introduced) Bulinus africanus B. globosus B. natalensis B. tropicus

× — × × × × — —

— — × (×) — — — —

× × (×) (×) — — × —

— — — — — — — ×

— — — — — — — ×

× × — × —

— (×) — × ×

— (×) × × —

— — — × —

— — — — —

× — ×

× — ×

× × ×

× × ×

(×) × ×

— × — ×

× × — ×

× × × ×

× × — ×

× × — ×

× — × ×

× (×) (×) ×

× × × ×

× × — —

— × — —

× × —

— × —

× × ×

(×) (×) —

— — ×

(×) × × ×

— × × ×

× × × ×

× — — ×

— — — ×

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 555

Mozambique E Transvaal lowveld Natal E Cape W Cape B. forskalii B. reticulatus Physa acuta (introduced) Aplexa waterloti (? introduced)

× × ×

× × (×)

× — ×

× × ×

(×) × ×

×

×

×

—

—

scattered localities and in small numbers. Such populations are vulnerable to local extinction and some probably have been eliminated by human activities. But although man has greatly modified this environment, the coastal region between the rivers Pongola and Umzimvubu is an important natural ‘subtraction zone’ where the number of species of tropical molluscs (in fresh and in brackish waters) decreases from north to south. The more narrowly-restricted of the southern tropical species are not found south of Natal (Table 12.2; Figs 69, 70, 74, 120, 121). The more widelydistributed ones extend into Cape Province and may also be widespread in the northern Transvaal and further westwards in the Vaal Basin. Biomphalaria and the Bulinus africanus group show this pattern of distribution (Fig. 147), but Melanoides tuberculata is the only prosobranch to do so (Chapter 3, Fig. 73). In an eastern area including Natal, where the distributions of B. africanus and B. globosus were mapped separately by Brown (1966), globosus was found in a warmer climatic area than africanus. Biomphalaria pfeifferi is noticeably less well represented in southern and western areas than the Bulinus africanus group (Fig. 147 ) and this could indicate a need for greater warmth, but interpretation of the distribution pattern of B. pfeifferi is complicated by the fact that this snail is known to be adversely affected by high climatic temperature in the coastal area (Appleton, 1977b). Bulinus forskalii (Chapter 3, Fig. 128) and B. natalensis (Chapter 7) also have distributions of the tropical type. It is noteworthy that although B. forskalii is not found in western Transvaal, it is known from the lower Orange River. Lymnaea natalensis is more widespread, occurring in much of the highveld, the Orange River basin and the southern coastal region, but its comparative rarity at high altitude and also in the western Cape suggests it is better adapted to tropical and subtropical conditions. In the western half of southern Africa the southern limits for some genera lie much further north than on the eastern side. Aridity is probably important in restricting distributions in the south-west, although low temperature could also be unfavourable in areas such as southern Botswana, where night temperatures sometimes fall below zero (Fig. 146). Pila and Gabbiella occur no further south than the lower Okavango River, and a number of genera reach their southwestern limit here: Bellamya, Lanistes, Cleopatra and Segmentorbis (Brown et al., 1992). Further east in Zimbabwe and the northern Transvaal, the only

556 FRESHWATER SNAILS OF AFRICA

Fig. 147. Distribution in the Republic of South Africa of Biomphalaria pfeifferi and Bulinus (Physopsis) (africanus and globosus), in one-sixteenth degree squares (from Appleton & Stiles, 1976, Fig. 2). These snails occur mostly on the harder rock formations (enclosed by dotted lines). These hard formations extend, though without snails, into the SW Cape, and there is an isolated snail-less outcrop in Lesotho. Triangles indicate anomalous areas discussed by Appleton & Stiles. It is concluded (present text) that cool climatic temperature plays an important part in limiting the distribution of these snails.

widespread prosobranch is Melanoides and the winters seem too cool for most prosobranchs. Too little seems to be known about current climatic trends to judge whether or not tropical freshwater snails have stable distributions in southern Africa. It is a matter of concern that intermediate hosts for schistosomes might colonise major basins such as the Orange River where these snails have not been found (De Kock et al., 1974). One of the largest impoundments constructed in the upper Orange Basin is the Verwoerd Dam at about 1220 m altitude. In small waterbodies near this dam site, Pitchford & Visser (1969) found that the wide

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 557

extremes of temperature were unsuitable for Biomphalaria and the B. africanus group. But it was also found that the effect of impoundment on water temperature below the Verwoerd Dam was to increase winter minima and to reduce summer maxima, to an extent that might favour these snails (Pitchford & Visser, 1975). It seems even more likely that habitats suitable for tropical molluscs could be created by impoundments in the lower Orange Basin, where winter temperatures are not so low. Snails of the southern temperate region Gyraulus connollyi is the only freshwater snail known to be confined to the southern temperate region. It is found only in a cool climatic area of South Africa (Fig. 148), whereas G. costulatus occurs mostly in the warmer areas of Natal and Transvaal and its range extends far into the tropics. Both these apparently closely-related species are common in perennial streams and they often occur together, but G. connollyi is abundant in areas where G. costulatus is lacking, notably the heart of the highveld and the southern Cape. G. connollyi is not found in the subtropical or tropical areas where G. costulatus is common. G. connollyi lives near sea-level in Cape Province, but not below 850 m on the Drakensberg escarpment in the warmer climatic area of the south-eastern Transvaal (Brown & Van Eeden, 1969; Appleton, 1975). From data for temperature in a stream in this area (Appleton, 1976) it appears that G. connollyi does not tolerate warmth in excess of about 3200 degree-hours (°C) per week. Lymnaea truncatula is also commonest in the temperate region of southern Africa, being particularly common in Lesotho, and lives also in highlands in East Africa. B. tropicus too seems adapted to a temperate climate, at least in southern Africa; it is abundant on the highveld, but less common in the warmer regions of South Africa where it is replaced by B. natalensis and B. depressus (see Chapter 7; B. natalensis/tropicus complex). The concentration of species of Tomichia in Cape Province may be related not so much to the temperate climatic zone as to the adaptation of these snails to life in coastal lagoons. The mountainous territory of Lesotho is the climatic heart of the southern temperate region. Average annual air temperature is only about 11°C at 2190 m altitude, and no more than 6°C at 3000 m in the eastern highlands where snow can fall at any time of the year. Marshy habitats abound and include characteristic ‘spring-swamps’ (peatbogs). Aquatic molluscs have been thoroughly investigated with particular regard to the high prevalence of liverfluke infection in livestock (Prinsloo & Van Eeden, 1973, 1974). Only 5 species of gastropod and 3 species of bivalve were found, and others seem unlikely to have escaped notice as 1411 collecting stations were examined over a period of one year. No species is endemic to Lesotho and all found there are widely distributed elsewhere. Most common was the bivalve Pisidium viridarium, followed by Bulinus tropicus (307 stations) and Lymnaea truncatula (281 stations). Much less frequent were Ceratophallus, Burnupia and Ferrissia. B.

558 FRESHWATER SNAILS OF AFRICA

Fig. 148. The distribution in southern Africa of Gyraulus costulatus (open circles) and G. connollyi (solid circles) in one-sixteenth degree squares (from Brown & Van Eeden, 1969, Fig. 18, with further localities for the Orange River Basin added from De Kock et al., 1974).

tropicus is characteristic of the western lowlands, where it lives in pans, dams and pools. L. truncatula is commonest in the swamps of the foothills and low

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 559

mountain plateaux; it is rarer in the lowlands where humidity is generally lower, and is absent from swamps in the higher mountains, where the climate seems to be too cold. Perhaps the cool climate also explains why Lymnaea natalensis, Gyraulus connollyi and Bulinus reticulatus have not been found in Lesotho, although they are present in surrounding parts of South Africa (De Kock et al., 1974). However, the dense populations of people and livestock in Lesotho have effects on the aquatic habitats, and this disturbance combined with the rigours of the climate might have eliminated some species from the western lowlands. Temperature and snail distribution in southern Africa The foregoing account has more than once assumed that climatic temperature is an important influence on the distribution of freshwater organisms. This view was challenged by Stuckenberg (1969), who suggested that the observed decrease in the number of species of anuran amphibians in the coastal plain of Natal was due to the progressive narrowing of the plain towards the south. This explanation implies competition for resources and living space (including warm sites), but this does not seem to be likely for freshwater snails. To Appleton (1978) snail distribution patterns in southern Africa seemed to be determined more by permanence of habitats than by temperature differences. The evidence for this explanation is that in South Africa Biomphalaria and the Bulinus africanus group occur mainly on hard rock formations (Fig. 147) that are resistant to erosion and thus favour the formation of permanent pools in rivers, providing refuges for snails in times of flood (Appleton & Stiles, 1976). But large areas of South Africa lacking these snails have apparently suitable habitats, and here it seems that climatic temperature limits distribution. In fact the area without these snails may be seen to correspond closely to the area of coolest climate (compare Figs 146 and 147). Evidence for direct influences by temperature on snail biology come from observations on life cycles under natural conditions, where in southern Africa there is a break in egg production during the winter (e.g. Bulinus globosus and Biomphalaria; see Chapter 11: Pulmonate life cycles). Experiments in the laboratory have demonstrated relationships between temperature and the rates of growth, fecundity and mortality of these and several other pulmonate species (Chapter 10: Temperature). Of particular interest is the finding by Appleton & Eriksson (1984) that the reduced density of the summer generation of Biomphalaria pfeifferi in the coastal plain of Natal can be attributed to a reduction in the fecundity of the preceding spring generation, due to the impairement of development of the gonad caused by above-optimal temperature.

560 FRESHWATER SNAILS OF AFRICA

Introduced species Freshwater snails introduced into Africa from abroad have been most successful in southern Africa, where the two species Lymnaea columella and Physa acuta have become widespread during a few decades. L. columella originates from North and central America and apparently was first found in Africa during the 1940s, in the western Cape Province. It seems to have arrived with imported fish or aquatic plants. By the mid-sixties this snail was widespread in all the provinces of South Africa (Van Eeden & Brown, 1966), being found in 132 loci (1/16 square degrees). During the period 1966– 88 a further 225 loci were recorded in the National Snail Collection, University of Potchefstroom (De Kock et al., 1989), making L. columella the third most widely distributed freshwater snail in South Africa (Fig. 149), after L. natalensis and Bulinus tropicus. Its habitats are commonly rivers and streams with a perennial slow flow, and stagnant waterbodies with plentiful vegetation and a muddy substrate; it also colonises small man-made habitats such as storage tanks and cattle troughs. The snail’s presence in the warm lowlands of Natal as well as in the cool highveld shows a wide climatic tolerance, but it seems unable to colonise either the transitory waterbodies in the dry western area where B. tropicus occurs, or the coolest central area including Lesotho. In the total of 2341 sites of collection (De Kock et al., 1989), L. columella was found alone in 21%; the other species with which it was most frequently found was L. natalensis (36% of sites). Compared with L. natalensis in the laboratory, L. columella had a reproductive superiority that could give it a competitive advantage. The spread of this invading snail has economic implications for livestock farming, as it is an intermediate host for liver flukes (see Chapter 6: Fasciola). It would seem from the broad climatic zone and the variety of habitats occupied by L. columella that it should flourish in a much larger area of Africa, but though reported from a few tropical countries and Egypt, the species seems unable, for no evident reason, to spread so freely as in South Africa. The presence of physid snails in Africa is believed to be due entirely to introduction in recent historical time from the Americas. Since 1956 when Physa acuta is first known to have been collected in South Africa, it has become widely distributed (Fig. 150), though less so than L. columella. Most records lie in 4 main areas (Hamilton-Atwell et al., 1970; De Kock et al., 1989): south-western Cape, Natal, the Johannesburg area and the lower Vaal basin. Physa commonly lives where pollution from sewage is obvious and its occurrence seems to be closely associated with human activities (more so than L. columella). Compared with Bulinus tropicus in the laboratory, P. acuta had a reproductive superiority that could enable it more rapidly to repopulate habitats denuded of snails by flooding (Brackenbury & Appleton, 1991). Elsewhere in Africa physid snails occur in many countries, usually in or near towns (see systematic account), although they seem less widespread than in South Africa. Aplexa has been known from West Africa since early this century, and physid snails were known

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 561

Fig. 149. Distribution of Lymnaea columella in the Republic of South Africa (with a few records for Swaziland, southern Mozambique and Namibia), in loci of one-sixteenth degree squares (from De Kock et al., 1989). The 132 loci reported by Van Eeden & Brown (1966) indicated by dots; 225 loci found since 1966 indicated by circles.

from North Africa and the Near East about one hundred years earlier. It is still uncertain whether one or more species is represented by African snails identified as P. acuta. Helisoma is yet another introduction to Africa from America, now found in scattered localities in many countries (see systematic account), though not so well-established as are L. columella and the physid snails. The potential of H. duryi to spread is perhaps limited by its inability to self-fertilise (Madsen et al., 1983). Its habitats usually are artificial, e.g. pools in botanical gardens, ponds at a paper-mill (Brown, 1967) and a storage tank (Van Bruggen, 1974). Helisoma seems to occur only rarely in natural watercourses (Appleton, 1977c). Although this snail has been introduced deliberately into irrigated areas of Tanzania and Sudan as a competitor against the intermediate hosts for schistosomes (Chapter 8: Biological Control), there is so far no evidence of its spreading widely in these areas.

562 FRESHWATER SNAILS OF AFRICA

Fig. 150. Distribution of Physa acuta in the Republic of South Africa (with one locus in Swaziland), in loci of one-sixteenth degree squares (from De Kock et al., 1989). The 58 loci reported by Hamilton-Atwell et al. (1970) are represented by circles; 43 loci found since 1970 are indicated by dots.

Other freshwater snails introduced, accidentally or deliberately, into Africa have a much smaller presence (although they may have potential to spread). Of particular interest in relation to transmission of Schistosoma mansoni are reported occurrences of the neotropical Biomphalaria glabrata in Egypt (Pflüger, 1982) and similar snails in Durban, South Africa (Joubert et al., 1986). Large numbers of the prosobranch Marisa were transported in the 1980s from Puerto Rico to the Gezira irrigated area of the Sudan as a competitor against intermediate hosts for schistosomes (Chapter 8: Biological Control). Two planorbids native to southern Asia, Amerianna carinata and Indoplanorbis exustus, have been found in restricted areas of West Africa (see systematic account).

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 563

Islands Madagascar, Aldabra and the Comoro Islands Madagascar has about the same area as Kenya and is about 400 km distant from Africa at its nearest point on the Mozambique coast. According to palaeomagnetic evidence (Smith, 1976) Madagascar separated from Africa more than 90 million years ago, perhaps not long after the detachment of Africa from Gondwanaland. Table 12.3. The freshwater snails of Madagascar, according to the present systematic synopsis; the list of species given by Starmühlner (1983, Table 7.2 is far from complete). The Potamididae and Ellobiidae, of brackish habitats, are omitted. E=endemic. Prosobranchs Clithon, 2 species Neritina, 3 species Septaria borbonica Neritilia consimilis Lanistes grasseti E Pila cecillei E Melanatria, 2 species, E Cleopatra, 3 species, E Thiara scabra T. amarula Melanoides tuberculata M. psorica E (if different from tuberculata) Pulmonates Lymnaea natalensis (=hovarum) Ferrissia modesta E Afrogyrus crassilabrum E A. starmuehlneri E Segmentorbis angustus (?)Lentorbis sp. Biomphalaria pfeifferi (=madagascariensis) Bulinus obtusispira E B. liratus E B. forskalii (=mariei) B. bavayi E Physa acuta (=borbonica)

The snail fauna could thus include species of ancient origin as well as colonists from Africa, possibly arriving via the ‘stepping stones’ provided by the Comoro

564 FRESHWATER SNAILS OF AFRICA

Islands situated about midway across the Mozambique Channel. Such a large island has a wide variety of fresh waters (Aldegheri, 1972), including Lake Alaotra with an area of 200 km2, but which seems to lack any endemic species of mollusc. About 30 strictly freshwater species of gastropod are recognised to occur in Madagascar (Table 12.3), of which many are apparently endemic; the most distinctive are the species of Melanatria, Cleopatra and Afrogyrus, as well as Bulinus obtusispira and B. bavayi (others seem likely to prove indistinguishable from African species). Extensive data are available on snail distribution (Starmühlner, 1969; Fischer-Piette & Vukadinovic, 1973); Starmühlner (pp. 388–93) recognised 3 faunal regions: 1. subtropical highlands, lacking prosobranchs apart from Pila, but with a variety of pulmonates including Afrogyrus starmuehlneri (‘Gyraulus apertus’) found only in streams above 1800 m; 2. escarpments descending steeply to the east and northwest coasts, with extensive primary forest and soft-water streams and rivers where Melanatria and Cleopatra are common; 3. southwestern and western areas where waters are richer in dissolved salts, and including the lower Mangoky River (Chapter 10: Total dissolved chemical content). Of the 9 species recorded in the Mangoky and irrigated areas (Degrémont, 1973) the commonest were Lanistes grasseti and ‘Anisus’ (probably Afrogyrus crassilabrum). Cool water-temperatures exclude Bulinus obtusispira from the central highlands of Madagascar and most of the eastern coastal area, whereas these are the areas where Biomphalaria is most abundant, because of its poor tolerance of the higher temperatures in the western part of the island (Brygoo, 1972; Pflüger, 1977; Moyroud et al., 1983). Aldabra Atoll lies about 400 km north-west of the northern tip of Madagascar. The only freshwater snail found there is Bulinus bavayi, which seems likely to have been transported from Madagascar by man. Comoro Islands Transportation by man or birds is believed to account for the presence of the 16 species of freshwater snail (apart from Ellobiidae) found in the Comoro Islands (Backeljau et al., 1986). Running water is lacking on Grand Comore, which has only three species. The next largest island, Anjouan (424 km2), has numerous streams and 15 species; Starmühlner (1976) found only Lymnaea natalensis and Ceratophallus sp. above 150 m altitude, while the lower water-courses were dominated by neritids, Neritilia occurring as high as 120 m. Smaller numbers of species are reported for Moheli and Mayotte (Julvez et al., 1990). The report by Backeljau et al. (1986) of Thiara scabra for Anjouan is not correct in my opinion; these specimens seem to be a different species and like T. (Plotia) datura of Réunion (Barre et al., 1982). Being situated midway between the Mozambique coast and Madagascar, the Comoros are well placed to receive

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 565

colonists from the east (e.g. Neritilia consimilis and Afrogyrus crassilabrum) and the west (e.g. Lymnaea natalensis and Ceratophallus). Mascarene Islands and the Seychelles About 20 species of snail from fresh or slightly brackish water are known for each of the islands of Mauritius, Réunion and Rodriguez (Starmühlner, 1977, 1979, 1983, 1986; Barré et al., 1982). At least Helisoma duryi in Réunion (identified at first as Indoplanorbis by Starmühlner, 1979, pp. 719–21) and probably also Bellamya bengalensis in Mauritius have been introduced by man. Species related to the Afrotropical fauna include Afrogyrus rodriguezensis and Bulinus cernicus; the distribution and biology of the latter have been studied closely (e.g. Rollinson et al., 1990). On the other hand, Asian affinities are shown by Lymnaea mauritiana and Gyraulus mauritianus. It is of great interest that the specialised lymnaeid Lantzia carinata was recently rediscovered after more than a century in a highland waterfall on Réunion. About a dozen species of snail are found in the streams of the Seychelles Islands (Starmühlner, 1983), of which only one might be of African origin, a Lymnaea tentatively identified as L. natalensis. ‘Cleopatra’ ajanensis was also regarded as a faunal link with Africa, but this is a species of Paludomus and Table 12.4. The freshwater snails of Zanzibar and Pemba, according to Mozley (1939), with additional records for L. farleri by Martens (1897) and T. scabra by Kristensen (1987). Names used by Mozley are given in brackets. P=Pemba; Z=Zanzibar. Prosobranchs Neritina pulligera (knorri) PZ N. natalensis P Lanistes purpureus (olivaceus) PZ L. farleri Z Thiara amarula (vouamica) Z T. scabra PZ Cleopatra ferruginea Z Pulmonates Lymnaea natalensis (caillaudi) Z (?)Ceratophallus sp. (Planorbis gibbonsi) PZ (?)Lentorbis junodi (Hippeutis) Z Bulinus globosus PZ B. nasutus PZ B. forskalii PZ

566 FRESHWATER SNAILS OF AFRICA

therefore probably derived from Asia (Brown & Gerlach, 1991). The other exclusively freshwater species found are Neritilia consimilis, Melanoides tuberculata and Gyraulus mauritianus. Zanzibar, Pemba and Socotra Snails found in the numerous freshwater habitats of Zanzibar and Pemba seem to be entirely Afrotropical in character (Table 12.4), although no comprehensive account of this fauna has been published for over 50 years since that of Mozley (1939). The lack of any member of the Bulinus truncatus/tropicus complex or of Biomphalaria is consistent with their absence from near the coasts of northern Tanzania and Kenya. However, both B. globosus and B. nasutus occur and are hosts for S. haematobium (Savioli et al., 1989). Socotra has only few freshwater snails (Godwin-Austen, 1883), including Indoplanorbis exustus reported by Wright (1971) and two apparently endemic species (?)Ceratophallus socotrensis and Gyraulus cockburni. The Atlantic islands Freshwater species are lacking from the present and past molluscan faunas of St Helena (Crowley, 1978). All the few species found on islands in the Gulf of Guinea seem widespread in western Africa, although a distinctive form of Bulinus forskalii occurs on São Tomé. Also reported for this island (Brown, 1991) are Neritina afra and Ferrissia eburnensis, and species of ‘Lymnaeidae and Physidae were possibly introduced…a few years ago’ (Grácio, 1989). The presence of Lanistes in Fernando Po and a ‘Melania’ in this island group was mentioned by Germain (1925, p. 12), but there seem to be no recent records. Table 12.5. The number of gastropod species living in African lakes arranged in order of increasing salinity. Lake (and source of data)

No. of species

Area (km2)

Maximum depth Salinity (m) (Conductivity in µmhos)

Lungwe (c) Tumba (c) Nabugabo (c) Bangweulu (c) high water level Mweru (a) Victoria (c) Tana (a) George (c)

2 0 1 7

1 740 20 2800

— 5 5 10

15–17 24–32 25 35

15 28 9 9

4580 75 000 3500 290

37 80 14 4.5

70–125 91–98 150 200

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 567

Lake (and source of data)

No. of species

Area (km2)

Maximum depth Salinity (m) (Conductivity in µmhos)

Malawi (Nyasa) (a) Naivasha (b) Chad (e) in 1960s Zwai (d) Tanganyika (a) Albert (a) Abaya (Margherita) (d) Edward (a) Awasa (d) Kivu (a) Langano (d) Turkana (c) Shala (d)

28

30 800

758

220

6 24

113 20 000

14 7

335 50–1000

12 60 15 11

434 32 900 5600 1162

7 1470 58 13

393 610 675–730 900

13 12 7 0 7 0

2300 129 2700 230 7200 409

117 22 489 46 120 266

900–925 1084 1240 (surface) 2290 2200–3300 25 000

Physical data from: (a) Welcomme (1972), (b) Richardson & Richardson (1972), (c) Beadle (1981), (d) Grove et al. (1975), (e) Carmouze & Lemoalle (1983). Much information on chemical composition was collated by Talling & Talling (1965).

The Cape Verde Islands and Azores The freshwater molluscan fauna of the Cape Verde Islands has been identified from shells only (Panelius, 1958; Groh, 1982); it deserves to be better known as the composition is interesting. Here some Palaearctic species are reported from far south of their main range, at least in western Africa (Hydrobia ventrosa, Lymnaea auricularia, Gyraulus laevis and an Ancylus). An Afrotropical element is evident in Melanoides tuberculata, Lymnaea natalensis and Bulinus forskalii; but shells identified as Afrogyrus by Groh (1982) appear from his illustration to be juvenile Gyraulus. No Afrotropical species is found in the Azores (Backhuys, 1975). Natural lakes The ‘Great Lakes’ vary in size from Edward (about 2500 km2) to Victoria (about 75 000 km2); the largest man-made lake is nearly 9000 km2 (Volta). The number and the variety of molluscs living in a lake is related to its area, depth and salinity (Table 12.5), as well as to the range of biotopes, while endemism in the

568 FRESHWATER SNAILS OF AFRICA

fauna depends on the availability of ancestral stocks having the potential for radiation, and there being enough time for this to occur. Salinity becomes the dominant restraining influence near the upper and the lower limits of concentration tolerable to a normal freshwater fauna. Some lakes in the Rift Valley are too Table 12.6. The snails of Lake Albert. E=an endemic species or one represented by a local form. Based on Mandahl-Barth (1954, 1968b). Prosobranchs

Pulmonates

Bellamya rubicunda E Pila ovata Gabbiella candida E G. humerosa alberti E G. walleri E Melanoides tuberculata butiabiae E Cleopatra bulimoides emini E

Biomphalaria sudanica B. stanleyi ?E B. elegans E (?=B. choanomphala) Ceratophallus natalensis C. bicarinatus Lentorbis junodi Segmentorbis angustus S. kanisaensis Bulinus ?truncatus (chromosome number unknown)

saline for any mollusc to survive, while Lake Turkana seems to be at the borderline (it has only half the number of species found in the smaller though less saline Lake Albert) (Table 12.5). At the other extreme, Lake Tumba in Zaire has very little dissolved chemical content and apparently no molluscs, even though it is a large lake. A combination of favourable circumstances in Lake Tanganyika, including its great age, accounts for the outstanding variety of its endemic snails. However, the possibility of a highly distinctive species evolving in a lake of insignificant size is illustrated by the presence of Ceratophallus pelecystoma in Lake Chala, Kenya, with an area of scarcely 1 km2. The African Rift lakes provide good opportunities for studies of speciation and longer-term evolution in ancient lakes. Recently interest has focused on the specialised species of Lanistes in Lake Malawi (Berthold, 1990a,b) and the discovery through a combination of morphological and ecological observations and enzyme analyses of a species-flock of Lavigeria in Lake Tanganyika (Michel et al., 1992). The interpretation of sequences of fossil shells in the Turkana Basin caused controversy in relation to the concept of punctuated equilibrium in evolution (Williamson, 1981, and papers cited under Lake Turkana). A search for general explanations of gastropod evolution in ancient lakes including Lake Tanganyika led Gorthner (1992) to conclude that not all the variety of shell ornamentation has a functional explanation. Lakes selected for detailed consideration follow in alphabetical order, and then sections dealing with lakes in southern Ethiopia and with crater lakes. For most

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 569

of these lakes an indispensable source of information on hydrology, history and biology is provided by Beadle (1981). Lake Albert (Mobutu) Altitude: 615 m. Area: 5600 km2. Maximum depth: 56 m. The formation of this basin began probably in the Miocene and the present lake lies above thick sediments, that extend down to the original valley floor now sunk to 1800 m below sea-level. Some deposits have been left exposed above the present lake level and contain many shells from rich Pleistocene molluscan faunas, which differed greatly from that of today (Adam, 1959; Gautier, 1970; Williamson, 1990). The living gastropods (Table 12.6) show endemism at the level only of the species or below; two forms of Biomphalaria are shown as doubtful endemics because knowledge is needed of their genetical relationships to populations with similar shell forms found in other lakes (e.g. Chad and Victoria). Lake Bangweulu Altitude: 1200 m. Area: 2800 km2. Maximum depth: 10 m. Shallow and swampy like Lake Chad, this lake in northern Zambia is smaller than ‘normal Chad’ and has a lower conductivity (Table 12.5). No endemic gastropod species is recognised among the 7 found in Lake Bangweulu (Mandahl-Barth, 1968a). Lake Chad Altitude: 280 m. This shallow lake has passed through several phases of major expansion and contraction during the Pleistocene and more recently. About 6000 years ago ‘Mega-Chad’ covered up to 400 000 km2 and was five times the present area of Lake Victoria. The ‘normal’ lake in the 1960s had an area of about 20 000 km2 and a maximum depth of about 7 m. This was reduced in the 1970s to a small remnant in the southern basin (‘Little Chad’). In 1974– 77 the southern basin returned nearly to normal but the northern basin almost dried up (Carmouze & Lemoalle, 1983). During 1979–81 the southern part consisted of pools of open water scattered amongst belts of thick emergent vegetation (Betterton, 1984); pulmonate populations fluctuated greatly in relation to seasonal changes in lake level, and preferred habitats were stands of the grass Vossia cuspidata. Very extensive observations were made on the general ecology and benthic molluscs of ‘normal Chad’ (reviewed by Beadle, 1981, and Lévêque et al., 1983). Benthic prosobranchs were exceedingly abundant and their distribution and numbers were analysed in detail (see Chapters 9: Faunal surveys; 10: Salinity; 11: Prosobranch reproduction and productivity). The total of about 20 species of snail found in Lake Chad (Lévêque, 1967; Mandahl-Barth, 1968b; Brown, 1974; Betterton, 1984) shows little endemism. On present evidence one

570 FRESHWATER SNAILS OF AFRICA

cannot be entirely confident of the distinctness of the few species reported as endemic (Gabbiella neothaumaeformis, G. tchadiensis and Biomphalaria tchadiensis). Local evolution cannot have been favoured by the highly unstable water level, shallow depth and low diversity of biotopes (there is no sublittoral zone and no rocky shoreline). Lake Chilwa Altitude: 627 m. Area: 700 km2, open water (high level). Shallow and swampy like Bangweulu and Chad, and subject to large fluctuations in level and salinity, this lake sometimes dries out practically entirely. During periods of high salinity the benthic fauna, including molluscs, survives only in the peripheral swamps where there are refuges of less saline water (Morgan & Kalk, 1970; McLachlan, 1974; McLachlan, 1979). The effects of seasonal changes in water level on the biology of Bulinus globosus were described by Cantrell (1981). No endemic species of snail is known to occur in Lake Chilwa. Lake Edward (Rutanzige) and Lake George Altitude: 920 m. Area: 2150 km2. Maximum depth: 112 m. Lake Edward is connected by the slender 40 km-long Kazinga Channel to the smaller Lake George (250 km2). The bottom of George is covered by soft flocculent sediment and molluscs are almost lacking; only Melanoides tuberculata has been reported and is uncommon (Mandahl-Barth, 1954; Darlington, 1977). The molluscan fauna of Lake Edward is comparatively rich and has been so since at least the Early Pleistocene (Adam, 1957; Williamson, 1990). Many species of the earliest fauna known are extinct, but most of the 20 species reported for the Late Pleistocene-Early Holocene (Adam, 1957) seem recognisable among the 15 species recorded for the present lake and the Kazinga Channel (Mandahl-Barth, 1954). In the present lake the few gastropods that perhaps qualify for recognition as endemic taxa are Gabbiella humerosa edwardi, Burnupia edwardi, (?) Ceratophallus apertus and Biomphalaria smithi. Lake Kivu Altitude: 1463 m. Area: 2700 km2. Maximum depth: 490 m. The shores slope steeply to a depth where oxygen is lacking, so that molluscan life is confined to a narrow littoral zone. Salinity near the surface is about twice that in Lake Tanganyika and calcium carbonate is precipitated continuously (Beadle, 1981). The one endemic taxon of snail that has been recognised is Gabbiella humerosa kivuensis Mandahl-Barth (1968b). This was by far the most abundant species in collections totalling about 190 000 snails (Gillet et al., 1960, ‘Bithynia alberti’); 7 gastropod species in all were found and maximum depths ranged from 0.2 m for Lymnaea natalensis to 7 m for Melanoides.

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 571

Lake Malawi Altitude: 473 m. Area: 29 600 km2. Maximum depth: 770 m. Lake Malawi resembles Lake Tanganyika in its area and slender shape (over 600 km long), but it is only about half as deep and one-third as saline. Its endemic molluscan fauna is much less diverse than that of Lake Tanganyika, yet it is still impressive. A link between the snail faunas of these two lakes was suggested by Crowley et al. (1964) according to the supposed presence in both of the viviparid genus Neothauma, but the species ecclesi of Malawi was classified later by MandahlBarth (1972) in the widespread genus Bellamya. The evolution of the specialised molluscan faunas of these two lakes thus seems completely independent. Of the 15 prosobranch species endemic to Lake Malawi (Table 12.7), all but one are contributed by the genera Bellamya, Lanistes and Melanoides, whereas in Lake Tanganyika these three groups are represented by only the single endemic species M. admirabilis. The shores of Lake Malawi are mostly rocky or sandy and marshes are restricted to the small estuaries and to some bays. Inflowing watercourses are mostly short and descend steep escarpments, so that the lake level is particularly sensitive to fluctuations in rainfall. The first snail shells to be described (Dohrn, 1865) were collected by John Kirk, who accompanied Livingstone on his Zambezi Table 12.7. The snails of Lake Malawi. E=endemic species. Based on a revision by Mandahl-Barth (1972). Prosobranchs

Pulmonates

Bellamya capillata B. jeffreysi E B. robertsoni E B. ecclesi E (‘Neothauma’ ecclesi, Crowley & Pain, 1964) Lanistes ovum L. ellipticus L. solidus E L. nyassanus E L. nasutus E Gabbiella stanleyi E Melanoides tuberculata M. nodicincta E M. pergracilis E M. pupiformis E M. turritispira E M. polymorpha E M. nyassana E

Lymnaea natalensis Biomphalaria pfeifferi Ceratophallus natalensis Gyraulus costulatus Segmentorbis angustus Bulinus globosus B. nyassanus E B. succinoides E B. forskalii

572 FRESHWATER SNAILS OF AFRICA

Prosobranchs

Pulmonates

M. truncatelliformis (if distinct from nyassana) M. magnifica E

expedition. Later visitors picked up from the beaches shells of ‘Melania’, whose variety inspired Bourguignat (1889) to name about 40 endemic species (now reduced to a few species of Melanoides). For many years the molluscs of Lake Malawi continued to be known almost entirely from empty shells (Crowley et al., 1964), and then collections of living specimens allowed substantial revision (Wright et al., 1967; Mandahl-Barth, 1972). A total of 28 species is recognised to live within the lake and on the swampy parts of its shores (Table 12.7), of which the only endemic pulmonates are two Bulinus. Most of these species live in the shallow littoral zone and only few have been found in the deep sublittoral; maximum depth records (Mandahl-Barth, 1972) are 90 m for B. ecclesi and Lanistes nasutus and 100 m for Gabbiella sp., while Bulinus nyassanus has been dredged from 95 m (52 fathoms), the greatest depth known to be reached by a pulmonate in any African lake. In striking contrast to Lake Tanganyika, there are no prosobranchs specialised for life on rocky shores in Lake Malawi. One possible reason could be the abundance about the rocks in Lake Malawi of fishes capable of eating molluscs (Fryer, 1959), and perhaps fluctuations in water level have inhibited adaptation by snails to this biotope; it could also be that the original gastropod stock, from which the present fauna of the lake is derived, lacked species with a genetic constitution adaptable to life on wave-swept rocks (Beadle, 1981). Interesting observations have been made on the biology of snails living on the sandy shores of Lake Malawi. The important food resource provided by Vallisneria plants, particularly the epiphytic algae attached to the leaves, was described by Fryer (1959) who found 4 species associated with these plants, Lanistes ovum (=procerus), Melanoides tuberculata, Gabbiella stanleyi and Bulinus ‘nyassanus’. Wright et al. (1972) observed that B. succinoides (probably the correct name for Fryer’s nyassanus) avoided direct light in the laboratory and pointed out that this behaviour could serve to keep the snails at the bases of the Vallisneria rosettes, where they might be sheltered from predatory fish; in contrast Gabbiella, which has a much stronger shell, crawled all over the leaves. In these studies Bulinus nyassanus also showed features interpreted as adaptations to lacustrine life, including its egg capsule and the fine cusps on the radular teeth, which seemed suitable for collecting fine sediment. More recently the ecology of snails on the sandy bottom was revealed by observations made by SCUBA-diving down to depths of 26 m at Cape Maclear. The life cycle of Lanistes nyassanus appears clearly adapted to minimise the impact of predation by fishes; while the thin-shelled juveniles shelter in weedbeds, the thick-shelled adults move about on the open sand and tend to burrow during the day (Louda & McKaye, 1982; Louda et al., 1984). These

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observations and other evidence (Louda et al., 1983; McKaye et al., 1986) suggest strongly that fish predation is an important influence on the distribution and abundance of gastropods in Lake Malawi. Support is thus available for the view of Fryer (1959) that fish predation could have prevented the evolution of a rock-adapted prosobranch fauna. The evolution of the three species of Lanistes endemic to Lake Malawi has occurred within the lake rather than outside, according to their comparative morphology and ecology (Berthold, 1990a). The derived characters of these species can be explained in relation to three types of adaptation, to wave action, to predation and to food resources. Both L. nyassanus and solidus are most abundant in comparatively shallow water where they are exposed to wave action and to predatory fishes; these species develop thick-walled shells, whereas the shell is thin-walled in L. nasutus, which lives at greater depths (40–90 m) sheltered from wave action and below the zone inhabited by molluscivorous cichlids. The unbanded light-coloured shells of these species also seem to contribute to reducing predation, by camouflaging the snails on a light sandy substrate. All three species show modifications of the stomach and radula in relation to the ingestion of sand while feeding on detritus. Lake Mweru (Moero) Altitude: 922 m. Area: 4850 km2. Maximum depth: 15m. This is an example of a lake with a low conductivity (usually less than 100 µhmos) that nonetheless has a rich fauna of invertebrates and fishes (Beadle, 1981). The southern end receives the Luapula River and has extensive marshes; most of the bottom is soft mud. The average depth in the southern basin is only 3 m (Welcomme, 1972), and Pilsbry & Bequaert (1927) commented that the entire lake might soon be reduced to a remnant, when its endemic molluscs would likely be exterminated. Fortunately most of them were collected alive in 1955–66 by the Belgian hydrobiological survey of the Bangweulu-Luapula Basin (Mandahl-Barth, 1968a). The 15 species of snail found (Table 12.8) include 8 endemic species of prosobranch (Bellamya, Cleopatra and Melanoides), of which some occur also in the lower Luapula River. Highly distinctive bivalves are also present. The lake must have been much deeper in the past to have existed long enough for these Table 12.8. The snails of Lake Mweru. E=endemic species, though possibly present also in the lower Luapula River. Based on Pilsbry & Bequaert (1927) and Mandahl-Barth (1968a). Prosobranchs

Pulmonates

Bellamya crawshayi E B. pagodiformis E B. mweruensis E Pila ovata

Lymnaea natalensis Biomphalaria pfeifferi Bulinus globosus B. tropicus

574 FRESHWATER SNAILS OF AFRICA

Prosobranchs

Pulmonates

Lanistes ovum (L. ovum mweruensis Pain, 1954) Cleopatra mweruensis E C. johnstoni E Melanoides mweruensis E M. imitatrix E M. crawshayi E

Burnupia sp.

endemic molluscs to have evolved; both lake and fauna now seem near the end of their life. Lake Naivasha Altitude: 1890 m. Area: 150 km2. Maximum depth: 18 m. Although few in species and lacking any known endemic form, the molluscs of Lake Naivasha are of interest for the conspicuous changes in the fauna during recent decades. When I first visited the lake in the early 1970s the blue water lily Nymphaea caerulaea fringed much of the shoreline; Bulinus tropicus was abundant on the east and the west shores and smaller numbers were found of Biomphalaria, Lymnaea natalensis and Ceratophallus natalensis. In 1986 the water lilies had gone and the only snail I could find was Physa acuta, which was living at great density on muddy sediment. The changes in the lake’s ecology and fauna have been extensively studied (Clark et al., 1989; Harper et al., 1990) and are due mainly to the introduction of the crayfish Procambarus clarki, and the arrivals of the Coypu Myocastor coypus and the floating plant Salvinia molesta; submerged macrophytes greatly declined as well as the water lilies. Comments by Clark and colleagues on changes in the molluscan fauna are unfortunately marred by flaws in taxonomy as well as the omission of records of Biomphalaria and Bulinus by other investigators (Cambridge Kenya Schistosomiasis Expedition, 1970; Brown, 1976; Brown et al., 1981). Clark and colleagues believed that all three gastropod species listed by Jenkin (1936; Lymnaea elmeteitensis, Bulinus baringoensis and Planorbis gibbonsi) were different from those found in their studies (L. natalensis, Ceratophallus natalensis, Physa acuta and Ferrissia sp.). However, L. elmeteitensis Smith, 1894 is a synonym of L. natalensis, while P. gibbonsi was very likely identified from juveniles of C. natalensis. The significant change in this snail fauna has been the decline of all the indigenous species and the rise of a dense population of the alien Physa. Biomphalaria was common enough in Lake Naivasha during the 1960s for there to be fears that S. mansoni might be transmitted, but this was not found to occur (Pamba & Roberts, 1979) and the snail seemed too rare in the 1980s for foci of regular transmission to exist. But concern over the possibility of schistosomiasis at Lake

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 575

Naivasha is not entirely over, for the first record of a potential intermediate host for S. haematobium is provided by the Table 12.9. The snails of Lake Tana. According to Bacci (1951) and with a revised list based on Brown (1965 and unpublished data). Bacci (1951)

Revised list

Prosobranchs Theodoxus africanus Bellamya unicolor unicolor B. u. abyssinica Melanoides tuberculata — Pulmonates Radix peregra R. caillaudi caillaudi — Biomphalaria rüppellii — Bulinus hemprichi sericinus — — —

— B. unicolor M. tuberculata Valvata nilotica — Lymnaea natalensis Gyraulus costulatus B. pfeifferi Ceratophallus natalensis — Bulinus truncatus B. africanus B. forskalii

identification of Bulinus truncatus from specimens collected at Crescent Island in 1987–88 (Brown & Shaw, 1989, pp. 514, 530). Lake Sibaya Altitude: near sea-level. Area: 60–70 km2. Maximum depth: 30–40 m. This unusual lake is separated from the Indian Ocean by a high forest-covered sanddune. The chloride content of the water is high, but a normal freshwater fauna is found, with the remarkable addition of some animals that normally are estuarine (Allanson et al., 1966). Although no endemic form of mollusc is known to occur, observations made on the ecology of the prosobranchs and pulmonates are of considerable interest, and the distribution and standing crop of some species have been studied in detail (Boltt, 1969; Appleton, 1977a; Hart, 1979). Lake Tana (Tsana or Dembea) Altitude: 1828 m. Area: 3156 km2. Maximum depth: 14 m. The climate in the basin is cooler than in the regions of the other lakes considered here except perhaps for Naivasha. In the 1960s I visited the mainly rocky shores at Gorgora

576 FRESHWATER SNAILS OF AFRICA

and Bahr Dar, where vegetation was sparse, though there are swamps on the shoreline that are among the highest localities for papyrus in Africa. Bottom sediments dredged near Bahr Dar were mainly fine gravel and contained few molluscs compared to the organic silt of Lake Victoria. Early lists of molluscs (Piersanti, 1940; Bacci, 1951) have been considerably revised and extended, but still the known fauna of 10 gastropods (Table 12.9) is surprisingly small. Recognition of only a single endemic taxon of snail seems possibly justifiable, the slender form of Bellamya unicolor named abyssinica Martens. The lack of Pila, Lanistes and Cleopatra is perhaps due to the cool climate of these highlands, although the rapids and falls on the Blue Nile may have also restricted the lake fauna by preventing colonisation from the Sudan plains (Beadle, 1981). The presence of supposed ‘palaearctic’ molluscs in Lake Tana has attracted unmerited attention (Rzoska, 1976). The records of Theodoxus and Lymnaea peregra are almost certainly incorrect; the latter was identified by Piersanti (1940) from shells that seem from his illustration to be L. natalensis, while Theodoxus has not been found in highland Ethiopia since the single record by Bourguignat (1883). On present evidence there is little justification for giving Lake Tana special importance as a southern outpost for palaearctic molluscs, but they certainly are characteristic of the small waterbodies of highland Ethiopia (see below, Nile Basin). Lake Tanganyika Altitude: 773 m. Area: 32 900 km2. Maximum depth: 1470 m (south basin). Lake Tanganyika combines large area with great age (about 6 million years) and depth (it is the second deepest lake in the world, after Lake Baikal in Russia). This whole ecosystem deserves high priority for conservation, as its evolutionary history and the diversity of its organisms are of outstanding interest (Beadle, 1981; Coulter, 1991; Cohen, 1991; Michel et al., 1992). The varied shoreline has rocky outcrops as well as sandy beaches, swamps and estuaries; the water has a rather high conductivity of about 600 µmhos. The unique prosobranchs of Lake Tanganyika first became known to science from shells picked up by John Speke on a beach in 1858; they included the two species to be named Melania (now Lavigeria) nassa and Lithoglyphus (now Spekia) zonata by Woodward (1859), who remarked that the latter ‘would be taken for a sea-shell if its history were not well authenticated’. More travellers and missionaries who followed Burton and Speke to Lake Tanganyika sent back shells to conchologists in Europe. Further species reminiscent of the sea-shore were found, and J.R.Bourguignat coined the term ‘thalassoid’ for them, meaning marine-like. J.E.S.Moore led expeditions to the lake on behalf of the Royal Society in 1895 and 1899, and he was one of the supporters of the theory that the thalassoid snails had a marine origin (Moore, 1903). This idea was eventually rejected decisively by Cunnington (1920), who argued in favour of the view that the endemic organisms of Lake Tanganyika had

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evolved entirely within fresh water, in response to the unique opportunities within such a large and long-lived lake. This explanation is now generally accepted, although the term thalassoid is still used to describe conveniently the group of endemic species that show no close relationship to any other freshwater snails. The non-thalassoid species are either widely distributed or if endemic to the lake they appear to have close relatives in the outside fauna. A total of about 60 species (Table 12.10) is found in the open lake or on its shores according to a recent revision (Brown & Mandahl-Barth, 1987), which modified earlier taxonomic treatments (Pilsbry & Bequaert, 1927; Leloup, 1953). An early period of excessive naming of species defined by trivial differences between shells, provoked in reaction a phase of over-conservative taxonomy that culminated in the revision of Leloup (1953), who placed so many names in synonymy that he could recognise only 20 thalassoid species. The present list Table 12.10. The snails of Lake Tanganyika, according to Brown & Mandahl-Barth (1987). Some names used by Leloup (1953) are given in brackets; Melania tanganyicensis is excluded for reasons given in the systematic synopsis under Melanoides polymorpha. Non-thalassoid species (E=endemic)

Thalassoid species (all endemic prosobranchs)

Prosobranchs Bellamya capillata (Viviparus unicolor) Neothauma tanganyicense E Pila ovata Lanistes ovum L. graueri ( ?)Tomichia guillemei Gabbiella humerosa tanganyicensis E Melanoides tuberculata M. admirabilis E Cleopatra ferruginea C. guillemei (Viviparus brincatianus) Potadomoides pelseneeri E

Anceya giraudi A. terebriformis Martelia tanganyicensis Syrnolopsis gracilis S. lacustris S. minuta Lavigeria nassa L. grandis Lavigeria, other spp. Mysorelloides multisulcata Hirthia littorina H. globosa Spekia zonata Tanganyicia rufofilosa Stanleya neritinoides Reymondia, 3 or more spp. Bridouxia, 6 or more spp. Stormsia minima Paramelania, 3 or more spp. Bathanalia howesi B. straeleni Tiphobia horei

Pulmonates Lymnaea natalensis Burnupia caffra Ferrissia tanganyicensis E Afrogyrus coretus Ceratophallus natalensis Gyraulus costulatus (Planorbis apertus) Lentorbis junodi

578 FRESHWATER SNAILS OF AFRICA

Non-thalassoid species (E=endemic)

Thalassoid species (all endemic prosobranchs)

Segmentorbis angustus S. kanisaensis Biomphalaria pfeifferi B. sudanica Bulinus (?)globosus (B. africanus) B. truncatus (angolensis and coulboisi) B. forskalii

Limnotrochus thomsoni Chytra kirki

of over 30 thalassoid species includes those of Lavigeria, which seems best placed in this group, although regarded as non-thalassoid by Brown (1980), because of a similarity in the radula to Potadomoides. Additional species of Lavigeria and Paramelania are recognisable though not yet incorporated into the formal taxonomic system (Cohen, 1989; Johnston & Cohen, 1987; Michel et al., 1992). Still more thalassoid species are known from specimens collected in recent years for which the generic position is uncertain (unpublished observations, 1989–93, by Brown and by West). There are about 30 non-thalassoid species, which include all of the pulmonates, of which it seems justifiable to recognise only a single endemic taxon, Ferrissia tanganyicensis. Although the ancylids occur in the open lake and live down to considerable depths (100 m is recorded for Burnupia caffra), the other pulmonates are restricted almost entirely to the marginal swamps and lagoons. The four non-thalassoid endemic prosobranchs are Neothauma (apparently closely related to Bellamya), a little-known snail classified tentatively as Tomichia, a local form of Gabbiella humerosa, Melanoides admirabilis and Potadomoides pelseneeri, which is known only from the Malagarasi Delta. In contrast to Lake Malawi, there is no lacustrine species of Lanistes, and only the single endemic Melanoides. The thalassoid species are all prosobranchs and they live only in the main lake. There seems to be a fundamental difference in ecological adaptation between the snails living in the main lake (whether thalassoid or non-thalassoid) and those of the peripheral marshes and tributaries. Detailed knowledge of the distributions of some species living offshore has been obtained by SCUBAdiving (Cohen, 1989; Michel et al., 1992) and more use of this technique is to be hoped for. The brief outline of snail distributions in general that follows is based on earlier observations made from above the surface and by dredging (Leloup, 1953; Coulter, 1991). Some rocks are battered too violently by waves to harbour any molluscan life, but in general the rocky shores have a rich fauna, including Lavigeria, Paramelania, Reymondia, Spekia, Stanleya, Stormsia and Tanganyicia, all browsing on encrusting algae. On calm days Spekia and Stormsia are described as emerging from the water to feed on moist exposed rock

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 579

surfaces even in full sunlight. Few molluscs are found on bare sandy beaches, but where detritus accumulates there may occur Anceya, Chytra, Limnotrochus, Martelia, Neothauma, Reymondia and Syrnolopsis. Some of these snails are small, with smooth shells, and can move easily through the sediment, perhaps thereby avoiding exposure to predators. The finer, soft muddy sediments present a snail with the problem of maintaining its position, and the spines and siphonal processes of species such as Paramelania damoni and Tiphobia horei may serve to prevent them from sinking too deeply. As pointed out by Coulter (1991), the nature of the bottom, rather than depth in itself, seems the principal physical factor determining distribution, while near shore the degree of water turbulence is also important. The distribution of species therefore tends to be patchy rather than zoned. Mud-dwelling species, for example, are found not only in deep water, but also where suitable sediment has accumulated in sheltered shallow regions. Molluscan life is excluded from the large area of bottom below about 200 m depth by lack of oxygen and increasing concentration of hydrogen sulphide (Beadle, 1981). Where the bottom shelves steeply, empty shells tend to be displaced down the slope; through this and other mechanisms shells may accumulate in large numbers on substrates and at depths where the living snail does not occur (Cohen, 1989). Viviparity occurs in some of the species found on soft sediments and in some of those found on rocks exposed to wave-action. In each case an advantage can be seen in brooding and giving birth to welldeveloped young; their large size could enable them to maintain their position on fine sediment, while their strength could help them withstand the force of turbulent water. Much has been written about the origin and evolution of the prosobranchs peculiar to Lake Tanganyika (e.g. Hubendick, 1952; Boss, 1978; Beadle, 1981; Van Damme, 1984; Michel et al., 1992) and it is impossible to do justice here to this widely-ranging debate. Since rejection of the idea that their origin was marine, and also of the suggestion that their shell forms could have been influenced by a high level of salinity in the lake (contrary arguments summarised by Beadle, 1981), the divergence of species and genera has been attributed mainly to adaptation to varied biotopes and to the isolation among populations that can arise in such a large lake basin. Two main isolating mechanisms have been proposed for Lake Tanganyika and other African Rift lakes: habitat fragmentation (e.g. the division of a rocky shoreline by the soft substrata of a river delta) and changes in lake level (whereby populations evolve independently in separate small lakes while water level in the main basin is low, and maintain their distinctness when reunited by rising water level). Viviparity and brooding of young in Lavigeria seem to favour high inter-population variation and speciation (Johnston & Cohen, 1987). There is a complex of morphospecies in Lavigeria, distinguished by shell morphology, enzyme analyses and habitat; the main ecological division is between rock-dwellers and species associated with soft substrata. Sampling by means of SCUBA diving along much of the shoreline showed that the distributions of the morphospecies conformed to the major

580 FRESHWATER SNAILS OF AFRICA

habitat barriers, not to the areas of the three smaller lakes into which Lake Tanganyika was divided during a period of low water level in the past (Michel et al., 1992). Major discontinuities in distributions of morphospecies occur at the inflows of the Malagarasi and Ruzizi rivers. Detailed studies at the northern end of the lake provided evidence that a rock-dwelling species is diverging on either side of the Ruzizi Delta, but no divergence was evident in a species tolerant of soft substrata. One reason for the evolution in Lavigeria and other groups of strong shells resistant to crushing could be predation by crabs (West et al., 1991). However, Gorthner (1992) doubts that all of the diversity of shell ornamentation of gastropods in Lake Tanganyika and other ancient lakes can be explained in terms of function. It appears probable that the thalassoid snails are descended from several ancestral species that lived in central Africa before the formation of Lake Tanganyika and which belonged to the same stock as the modern Thiaridae. Amongst living thiarids the genus Potadomoides seems to have the strongest claim for consideration in relation to this ancestry (Brown, 1980). As it lives in the Malagarasi Delta on the east side of Lake Tanganyika and in rivers in eastern Zaire, this genus or its ancestral stock could have been widespread in the area now traversed by the Tanganyika Rift. The same snail stock seems to have lived also further north in the Lake Albert-Edward Basin during the early Pleistocene, in view of the similar range of shell form (pointed out by Van Damme, 1984) displayed by fossils named Platymelania. The variety of shell shape and ornamentation among the living species of Potadomoides suggests that their ancestors could have possessed the potential for a profuse radiation in the young Lake Tanganyika. Lake Turkana (Rudolf) Altitude: 375 m. Area: 7200 km2. Maximum depth: 120 m. This large and alkaline lake is now in a closed basin, although it has been connected with the Nile, most recently about 7500 years ago (Beadle, 1981). Extensive collecting (Cohen, 1986) showed a low diversity of invertebrates; some of the few gastropod species found were rare and none was common outside restricted areas. There are fewer gastropod species than in other freshwater lakes of comparable size (Table 12.5) and the high alkalinity seems to be an important restraint on the molluscan fauna (Brown, 1992), although there may be other adverse factors (Beadle, 1981, p. 183). Seven species are found alive in the main lake (Cohen, 1986): Melanoides tuberculata, Cleopatra bulimoides, (?)Tomichia sp., Gabbiella rosea, (?)Gyraulus sp., Ceratophallus natalensis and Segmentorbis angustus. Pila is known from only the Omo Delta at the north end of the lake. I have seen shells of Bulinus (?)truncatus and Biomphalaria sp. from in or near the lake, but of uncertain age. The littoral substrata are mainly of sand, rock and shingle; muddy substrata are more restricted and marshes are confined to a few areas, which are most

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 581

extensive in the Omo Delta. Sandy bottoms were generally devoid of molluscs at all depths. Three benthic faunal associations were distinguished by Cohen (1986): 1. a littoral soft-bottom association; pulmonates were surprisingly absent from the vegetated areas except in the Omo Delta; 2. a littoral rocky-bottom association; Gabbiella, Ceratophallus and (?) Tomichia occurred on exposed surfaces, grazing on epilithic algae; 3. a profundal muddy-bottom association (at depths greater than about 5 m); Melanoides, Cleopatra, Gabbiella and (?)Gyraulus occurred at low densities, and were thin-walled and appeared stunted. Gastropod biomass was estimated for each type of habitat (Cohen, 1984) and was highest on the littoral rocky bottom. Although the total animal biomass for the littoral muddy bottom was comparable to that reported for Lake Chad, it was made up mostly of ostracods, whereas gastropods and insects were dominant in Lake Chad. The late Cenozoic history of mollusc faunas in the Turkana Basin is known from fossil sequences spanning 4 million years, in which ‘long-term stasis in all lineages is punctuated by rapid episodes of major change’ (Williamson, 1981). During an episode of change, novel shell morphs appeared and were believed by Williamson to represent a cluster of speciation events. Some opponents of this interpretation argued that the novel morphs could have been produced ecophenotypically, by modification of shells in direct response to stresses such as high alkalinity in the water (Fryer et al., 1983, 1985), a view strongly contested by Williamson (1985a,b). If this ecophenotypic explanation were true, snails living in the alkaline modern Lake Turkana might be expected to show a degree of modification in their shells, similar to the modifications of the fossil morphs. Since they do not (Brown, 1992), Williamson’s novel morphs appear to represent considerable genetic changes, whether or not they were products of full speciation. Lake Victoria Altitude: 1240 m. Area: 75 000 km2. Maximum depth: 80 m. Although more than twice the area of Lake Malawi and of Lake Tanganyika, Lake Victoria is comparatively shallow and young and its endemic molluscs are much less distinctive. Its conductivity is rather low and only about one-sixth that of Lake Tanganyika. A variety of biotopes is provided by sandy beaches, wave-washed Table 12.11. The snails of Lake Victoria. E=endemic species. Generic changes are indicated in relation to the list given by Mandahl-Barth (1954). Prosobranchs

Pulmonates

Bellamya unicolor B. phthinotropis (E)

Lymnaea natalensis Biomphalaria sudanica

582 FRESHWATER SNAILS OF AFRICA

Prosobranchs

Pulmonates

B. trochlearis (E) B. costulata (E) B. constricta (E) B. jucunda (E) Pila ovata Gabbiella humerosa Melanoides tuberculata Cleopatra cridlandi (E)

B. choanomphala (E) Ceratophallus (=Anisus) natalensis C. (=Gyraulus) subtilis (E) C. (=Gyraulus) kisumiensis (E) C. (=Gyraulus) concavus (E) C. (=Gyraulus) crassus (E) C. (=Gyraulus) kigeziensis Gyraulus costulatus Lentorbis junodi Segmentorbis angustus Bulinus sp. (diploid) (possibly B. trigonus) Bulinus sp. (tetraploid) (possibly B. transversalis) B. globosus B. ugandae Burnupia stuhlmanni (E) Ferrissia kavirondica (E)

stony shores, extensive papyrus swamps and soft bottom sediments. Differences among some biotopes in their gastropod faunas have been described (Chapter 9: Faunal surveys, western Kenya). Mandahl-Barth (1954) listed 42 full species and subspecies of gastropod, mostly endemic, but the number of species recognised here is only 28 (Table 12.11), of which less than half are endemic. Cleopatra guillemei is excluded from the present list because it seems to live only in pools separate from the lake. Present knowledge of spatial variation in shell morphology within the lake seems too slight to justify maintaining the array of endemic subspecies recognised by Mandahl-Barth (1954). The level of endemism would fall still further if Biomphalaria choanomphala should turn out to be the same species as B. elegans of Lake Albert, or if the two ancylids are no different from more widespread species. There are uncertainties in the identification of the Bulinus populations, but probably all the taxa belong to widely-distributed species. The prominence of the genus Ceratophallus in the endemic fauna of Lake Victoria is the most distinctive feature of its snails. Lakes in the southern Ethiopian rift valley These lakes comprise a northern group of four known as the Galla lakes (Abiata, Langano, Shala and Zwai) and the more southerly lakes Awasa, Abaya (Margherita) and Stefanie (Chew Bahir). Among the Galla lakes there are marked differences in salinity (Table 12.5). Abiata and Shala appear obviously too saline for living molluscs, although populations might persist at the mouths of inflowing streams. Langano seems just above the borderline, having a variety of

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 583

fish and aquatic insects, but only snail shells are found (Melanoides and Bulinus). The Galla lakes were united about 10 000 years ago, when the combined lake overflowed Table 12.12. The snails of the Ethiopian lakes Abaya (Margherita), Awasa and Zwai. Based on Bacci (1951) and Brown (1965, 1967 and unpublished data).×= living. 0=known only from shells. Lake Abaya (Margherita) Lake Awasa Lake Zwai Prosobranchs Bellamya unicolor Valvata nilotica Melanoides tuberculata Pulmonates Lymnaea natalensis Planorbis planorbis Gyraulus costulatus Afrogyrus coretus Ceratophallus natalensis C. bicarinatus Segmentorbis angustus S. kanisaensis Lentorbis junodi Biomphalaria sudanica B. pfeifferi Bulinus ugandae B. natalensis (B. sp. of Brown, 1965) B. truncatus B. forskalii Ferrissia sp. Burnupia sp.

— — ×

— — ×

0 0 ×

× — — × × — × — × × note 1 × —

× — — × — × × × × × — — ×

× 0 × × × × × — × × — — ×

× × — —

× × × —

× × — note 2

1. B. pfeifferi occurs close to Lake Abaya at Arba Minch 2. Present in lacustrine deposits near Lake Shala.

northwards into the Awash valley (Grove et al., 1975). A faunal connection in that direction might account for the finding in an extinct fauna of Lake Shala of shells resembling Biomphalaria barthi, known otherwise only from the lower Awash valley. Lake Zwai (or Ziway) is the largest Galla lake at present, having an area of over 400 km2 and maximum depth of 7 m, with some marshy shores and also open substrata of mud and fine gravel. Although Melanoides tuberculata is the only prosobranch found in Zwai, there are 11 pulmonates (Table 12.12), including the strictly lacustrine Ceratophallus bicarinatus.

584 FRESHWATER SNAILS OF AFRICA

Subfossil shells from the bed of an older and larger Lake Zwai include two palaearctic species, Valvata nilotica and Planorbis planorbis, which do not live so far south now (Grove & Goudie, 1971; Brown, 1973). Lake Awasa situated about 100 km south of Lake Zwai is less than one-third of its size, but has a similar snail fauna (Table 12.12). Lake Abaya (Margherita) has over twice the area of Zwai; its molluscs are poorly known and more species are to be expected than the 10 found so far (Table 12.12). The presence in Abaya of Bulinus ugandae is of interest because this is the only locality known for the B. africanus group in the whole southern rift valley of Ethiopia. The lack of the prosobranchs Pila, Lanistes and Cleopatra from this area is surprising as the climate seems suitable for them (all are known from Lake Stefanie, near the Kenya border). Crater lakes Some of the lakes in craters of extinct volcanoes are too saline for molluscan life and oxygenation may be poor due to permanent stratification of the water. Where snails do occur the number of species is few, it would seem partly because of the small chance of colonists being transported over a crater rim. Further discussion is restricted to three groups of lakes, in Cameroon, Ethiopia and East Africa. In Cameroon there are snails in Lakes Barombi Mbo, Barombi Kotto and Debundsha, and also Lake Wum, although this may have a different origin (Wright, 1965). A total of 12 species is recorded, although no one species is found in more than two lakes. In contrast to a rich endemic fish fauna, only a single species of snail is endemic to these crater lakes, Bulinus camerunensis, which is the only mollusc found in Lake Debundsha where the water has an extremely low conductivity (Green et al., 1974). Some crater lakes in Cameroon have populations of a diploid Bulinus (resembling B. natalensis), living far from the main area of distribution for similar populations in eastern Africa (Mimpfoundi & Greer, 1990). The cluster of crater lakes around the town of Debra Zeit (Bishoftu) south of Addis Ababa has so far yielded only a poor gastropod fauna of Gyraulus costulatus, Biomphalaria pfeifferi and diploid populations belonging to the Bulinus natalensis/tropicus complex (Connolly, 1928; Brown, 1964, 1965). From the numerous crater lakes in western Uganda, about 8 gastropod species are recorded, of which Gabbiella kichwambae and Bulinus tropicus toroensis are endemic taxa (Mandahl-Barth, 1960, 1968b), though further evidence in support of their distinctness is desirable. A more marked morphological divergence is seen in Lake Chala, near Mount Kilimanjaro, in Ceratophallus pelecystoma. Knowledge of the age of this lake would provide an estimate of the maximum time taken by this highly distinctive species to evolve.

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 585

Man-made lakes Some man-made lakes in Africa are of a size comparable to large natural lakes. The four described below have areas greater than 1000 km2 and have been established for 20 years or more. Man-made lakes bring economic benefits, but they may also damage human health, particularly by creating sites for transmission of schistosomiasis. In Lake Volta this disease soon became a serious problem and there is the potential for similar difficulties in a new lake anywhere in tropical or subtropical Africa. Most man-made lakes have a big seasonal draw-down, caused by regulating the outflow to make room each year for the large inflows during the main rainy seasons. The resulting instability of the littoral zone places special stresses on the aquatic life and probably is one of the factors restricting the number of species. Despite loss of much water through evaporation, the salinity of these lakes remains quite low, because annual flows are so large. Beadle (1981) gives a valuable summary of hydrological and limnological data for man-made lakes; effects on the transmission of parasitic diseases are reviewed by Hunter et al. (1993). Lake Kariba Area: 4300 km2. Maximum depth: 125 m. Year of closure: 1958 (filled in 1963). This lake lies in the middle section of the Zambezi valley and is about 300 km long. While it was filling the floating plant Salvinia grew explosively and aided the establishment of snail populations by providing shelter from wave-action and serving as a means for transport. Five species were found at Siavonga in 1968 by Hira (1969, 1970), including Biomphalaria pfeifferi, which proved to be transmitting S. mansoni. In 1969 Bulinus tropicus was present on mud on sheltered and on exposed shores (McLachlan & McLachlan, 1971), but was not found on submerged trees, which supported a rich fauna of other invertebrates (McLachlan, 1970). In the 1980s a quantitative survey of the biomasses of macrophytes and invertebrates was carried out along the Zimbabwean shore by SCUBA-diving (Machena & Kautsky, 1988). Among the 7 species of snail found, prosobranchs were dominant (Melanoides tuberculata, Cleopatra sp. and Bellamya capillata), while the pulmonates were mainly restricted to vegetation in the shallower and sheltered areas (Biomphalaria pfeifferi, Bulinus tropicus, Bulinus sp. and Lymnaea natalensis). Melanoides contributed 80% of the snail biomass and was widely distributed, occurring down to 9–10 m depth. Snails belonging to the Bulinus africanus group also occur in Lake Kariba, on both the Zimbabwean and Zambian shores, but their specific identity is not entirely clear. Although Hira (1969, 1970) reported B. africanus, all snails of this group collected on the same shoreline in 1991 were B. globosus, according to their morphology and enzymes (Brown, Rollinson, Smith & Southgate, unpublished observations).

586 FRESHWATER SNAILS OF AFRICA

Lake Volta Area: 8800 km2. Maximum depth: 80 m. Year of closure: 1964. The outstanding feature of the colonisation of Lake Volta by snails has been the success of Bulinus truncatus (=rohlfsi); few other species are found and they are not common. The spread of B. truncatus and the consequent high level of transmission of urinary schistosomiasis is documented in a notable series of publications (e.g. Odei, 1972, 1973; Klumpp & Chu, 1977, 1980). In the preimpoundment area B. truncatus was rare compared with B. globosus, but the latter failed to exploit the habitat in the new lake, possibly because it could not tolerate the wide annual fluctuation in the shoreline caused by the seasonal drawdown in water level. The key factor in the success of B. truncatus is the aquatic vegetation, especially the submerged plant Ceratophyllum demersum. When the water level is high there is a dense stand of emergent vegetation at the margin, mainly of Polygonum and tall grasses. Dense populations of B. truncatus develop in clumps of Ceratophyllum growing in pockets of open water, protected by the marginal vegetation from wind and wave action. At the same time these pockets are the main water-contact points for people and are the foci of schistosome transmission. During periods of low water, open beaches of sand or mud are exposed; few snails survive being stranded on these shores, but the population of B. truncatus is maintained in Ceratophyllum growing offshore. Although neither B. globosus nor Biomphalaria pfeifferi became established in Lake Volta, both snails appeared in Lake Kpong, a small lake created subsequently by a dam built 20 km further down the Volta River (Wen & Chu, 1984). B. pfeifferi was found in large numbers on floating Pistia. It may be that conditions in the smaller lake will support a snail fauna different from that of Lake Volta, with corresponding differences in disease transmission. Lake Nasser Area: 6000 km2. Maximum depth: 80–90 m. Year of closure: 1964. Until 1971 aquatic plants were almost lacking, although Potamogeton and Najas later became abundant (Entz, 1976). Nonetheless, Bulinus truncatus and infection with S. haematobium appeared early. Before macrophytes were established, the snails lived on sandy beaches and rocks. For some time the only other snail reported was Physa, but during the 1980s Biomphalaria alexandrina was found, following the progressive expansion in its distribution southwards from lower Egypt (Vrijenhoek & Graven, 1992). Lake Kainji Area: 1600 km2. Maximum depth: 60 m. Year of closure: 1970. About 13 species of snail, including Bulinus truncatus, were obtained in 1961 and 1967 from the pre-impoundment area (Walsh & Mellink, 1970). In 1970, after closure

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 587

of the dam, B. forskalii, B. globosus and Biomphalaria were found on the northwest shore (Dazo & Biles, 1972). When the same investigators again visited the Jinjima district in 1971, the water had receded by about 500 m and only B. globosus was found (Dazo & Biles, 1973). Another record of B. truncatus was given by Bidwell & Clarke (1977). This is the snail that would be expected to flourish in Lake Kainji, with its large annual draw-down, in view of events in Lake Volta. Yet B. truncatus does not appear to be established in Lake Kainji, and intermediate hosts for schistosomes have not been found at all on parts of the eastern shore (Adekolu-John & Abolarin, 1986), apparently because fluctuations in the lake level within short periods are too stressful. Schistosomiasis is endemic, however, in communities around Lake Kainji and there is a need for foci of transmission to be precisely defined, whether in the lake itself or in associated waterbodies, which include irrigation schemes. Rivers About one-third of the African surface is drained by 4 major river systems, the Niger, Nile, Zaire and Zambezi. The present account of the Niger is extended to include West Africa as a whole, while the account of the Nile Basin looks also at areas of the Ethiopian highlands that lie just outside this basin. Some snails are found in all these river basins, e.g. Biomphalaria pfeifferi, Bulinus globosus and B. forskalii, but many species are confined to only one. Table 12.13. Freshwater snails endemic to West Africa (west of Cameroon) or extending only narrowly outside this region. G=confined to the coastal area including Guinea in the west and Ivory Coast in the east. V=confined to the Volta Basin. Prosobranchs

Pulmonates

VIVIPARIDAE ?Bellamya liberiana G

PLANORBIDAE Bulinus jousseaumei B. senegalensis

AMPULLARIIDAE Pila africana Lanistes varicus L. libycus Afropomus balanoidea G Saulea vitrea G HYDROBIIDAE Hydrobia accrensis H. guyenoti G H. lineata G BITHYNIIDAE Gabbiella africana

PHYSIDAE Aplexa waterloti (though also reported from south-east Africa)

588 FRESHWATER SNAILS OF AFRICA

Prosobranchs

Pulmonates

Sierraia, 4 spp. G Soapitia dageti G THIARIDAE Melanoides voltae V M. manguensis V Potadoma moerchi P. vogelii G P. togoensis V P. liberiensis G P. bicarinata V ?P. buttikoferi G Pseudocleopatra voltana V Ps. togoensis V

The Niger Basin and the West African region (see also Lakes Chad, Kainji and Volta) Despite its great length the Niger lacks any known endemic species of snail and it seems to have played no part in the evolution of the distinctive West African snail fauna discussed below. Although endemic species could yet be found in the headwaters or in the lower river, both little investigated, the snails of the middle basin are quite well known (Madsen et al., 1987) and all are widely distributed species. Absence of endemism could be due partly to the youth of the upper and middle courses (Beadle, 1981), as well as to climatic fluctuations in the Sahelian area that must cause marked changes in water level in the main rivers, while small tributaries may be only intermittently flowing. Such instability would not favour the evolution of a local fauna. Most of the freshwater snails endemic to West Africa (west of Cameroon) (Table 12.13) are restricted to the area south-west of the Niger Basin. Most of them live in the river systems draining from the lowland forest into the Gulf of Guinea. There are concentrations of species in the coastal area including Guinea in the west and Ivory Coast in the east, and also in the Volta Basin (Table 12.13). The distinctive fauna of Sierra Leone (Hubendick, 1977; Brown, 1988) includes Afropomus, Saulea and 4 species of Sierraia, the latter remarkable for living in rivers that are practically devoid of dissolved chemical content in some seasons. The Zaire (Congo) Basin (see also Lakes Kivu, Mweru and Tanganyika) This basin includes the largest expanse of lowland tropical forest in Africa. It is considerably larger than the region known popularly as ‘the Congo’, as it

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 589

includes the Malagarasi River in western Tanzania and the Chambeshi River in northern Zambia. The classic account of the aquatic molluscs of the former Belgian Congo by Pilsbry & Bequaert (1927) was supplemented by studies in the south-eastern region (Mandahl-Barth, 1968a; Mandahl-Barth et al., 1972) and lower Zaire (Mandahl-Barth et al., 1974). Many authors refer to the northern shore of the Zaire as the ‘right’ bank and the southern shore as the ‘left’ bank. The Zaire system remained comparatively stable during a period when some river systems were being drastically altered (Beadle, 1981), and this stability must be counted an important factor in the evolution of a rich endemic molluscan fauna. The periphery of the basin rises to above 1000 m in the southeast, where there are mountain torrents, but much of the upper catchment is fairly level with sluggish streams. These descend abruptly to the central basin where the river falls only about 100 m over the long stretch of 2000 km from Kisangani to Kinshasa, and deposits many banks of sand and mud. Below Kinshasa the lower Zaire plunges through rapids for much of the 350 km to Matadi, and from there to Boma flows for about 40 km in a narrow and deep channel with rocky sides. From Boma the salinity increases and there is a gradual transition between the faunas of fresh and brackish water. Excluding those confined to the large lakes, about 100 species of aquatic gastropod occur in the Zaire Basin, of which about half are found only here (Tables 12.14, 12.15). The 8 endemic groups comprise 5 monotypic genera of ‘rheophilous’ snails (Table 12.14) classified in the Bithyniidae and Assimineidae (Congodoma, Liminitesta, Pseudogibbula, Septariellina and Valvatorbis), Funduella (Bithyniidae), Lobogenes (Hydrobiidae; also found in eastern Zambia) and Potadomoides (present also east of Lake Tanganyika in the Malagarasi Delta). The rheophilous snails are specialised for life in the rapids of the lower Zaire River. They were found first in the upper part of the Matadi-Boma channel, where they adhere to bare rock, resisting a swift current and tolerating wide variation in the water level (Bequaert & Clench, 1936, 1941). The most modified is the curious ancylid-like Septariellina. Many of the endemic species are thiarids including 12 of Melanoides. Of particular interest is the presence in the lower Zaire River of Pseudocleopatra, found otherwise only in the Volta River, West Africa. There is little precise information about the distribution of molluscs in the central Zaire Basin. The apparent absence of Potadoma is surprising in view of its presence in lower Zaire and in the north-eastern basin (Table 12.15). Other molluscs are likely to be uncommon in the many forest streams that have little Table 12.14. Prosobranchs endemic to the lower Zaire Basin (some extend inland at least as far as the Stanley Pool). R=‘rheophilous’. Based on Pilsbry & Bequaert (1927), Bequaert & Clench (1936, 1941) and Mandahl-Barth et al. (1974). VIVIPARIDAE

ASSIMINEIDAE

Bellamya leopoldvillensis

Pseudogibbula duponti R

590 FRESHWATER SNAILS OF AFRICA

VIVIPARIDAE AMPULLARIIDAE Lanistes intortus L. bicarinatus L. congicus HYDROBIIDAE Hydrobia luvilana1 H. plena R H. rheophila R H. schoutedeni R

ASSIMINEIDAE Septariellina congolensis R Valvatorbis mauritii R THIARIDAE Potadoma freethi graptoconus P. wansoni R Pseudocleopatra bennikei R P. dartevellei R Melanoides agglutinans R M. kinshassaensis M. langi zambiensis M. liebrechtsi3

BITHYNIIDAE Gabbiella spiralis2 G. matadina Funduella incisa1 Congodoma zairensis R Liminitesta sulcata R 1 . Present also in the basin of the Kouilou river. 2. Also recorded from an unspecified locality in ‘Equateur’. 3. Also recorded from an unspecified locality in ‘Upper Congo’.

dissolved salts and are darkly stained with decaying organic matter. They seem absent from Lake Tumba, apparently because of its extremely low salinity (Beadle, 1981). In the main river endemic species of Melanoides are abundant, buried just below the surface of sandbanks. Pilsbry & Bequaert stressed the adverse effects on other molluscs of the fluctuating water level, which is responsible for an almost complete lack of aquatic plants. Two types of headwater stream in the upper Zaire basin were distinguished by Pilsbry & Bequaert. Those in the Ituri forest region of the northeast, meander gently in dense shade and appear to be inhabited only by species of Potadoma. In contrast, streams in the southeast (Katanga) are only a few inches deep, moderately fast-flowing, with bottoms of fine gravel, and have a variety of snails (Table 12.15) including the small hydrobiid Lobogenes, and possibly endemic species of Segmentorbis and Burnupia. All that is known of the ecology of Potadomoides in eastern Zaire is that the species live in the Lualaba River and tributaries; these habitats seem considerably different from that of P. pelseneeri in the Malagarasi Delta of Lake Tanganyika.

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 591

The Zambezi (see also Lakes Kariba and Malawi) The upper Zambezi River may formerly have flowed westwards into the Zaire Basin, while some fishes are believed to have reached the Zambezi River from Lake Malawi (Beadle, 1981). However, the snail fauna of the river shows no influences from Zaire or Lake Malawi. Species named from specimens collected immediately above the Victoria Falls appear to be merely local forms of the Table 12.15. Gastropods endemic to the middle and upper parts of the Zaire Basin (excluding lakes Mweru, Tanganyika and Kivu). NE=confined to north-east; SE=confined to southeast; other species are known from few localities or have indeterminate eastern distributions. Prosobranchs VIVIPARIDAE Bellamya contracta SE AMPULLARIIDAE Lanistes nsendweensis SE L. graueri SE HYDROBIIDAE Lobogenes, 3 species SE (2 endemic) ASSIMINEIDAE ?Pseudogibbula cara THIARIDAE Potadoma liricincta NE P. alutacea NE P. ignobilis NE P. ponthiervillensis NE Cleopatra obscura SE C. elata SE C. langi C. pilula SE Potadomoides bequaerti P. hirta P. schoutedeni P. pelseneeri (Malagarasi delta) ?Potadomoides broecki Melanoides anomala SE Melanoides, 7 species with eastern distributions Pulmonates Biomphalaria sudanica rugosa SE Segmentorbis excavatus SE Burnupia spp. SE

592 FRESHWATER SNAILS OF AFRICA

widespread species, Bellamya capillata, Lanistes ovum and Cleopatra nsendweensis. The species of Ferrissia with local type localities also seem unlikely to be distinct from members of this genus living in other river basins. Thus the endemic element in this fauna seems to be restricted to Gabbiella balovalensis and G. zambica, which are poorly known and found in few localities. Speciation has probably been inhibited by the instability of these watercourses in comparison to the Zaire system, though additional endemic species may yet be discovered, particularly in the little known headwaters and lower tributaries. The Nile (see also lakes Albert, Edward, Tana and Victoria) From its sources in the highlands of East Africa to the delta the Nile travels about half the length of Africa; its history and biological features are reviewed by Rzoska (1976) and Beadle (1981). The lower course and the Blue Nile date back to at least the Miocene but the system as a whole is comparatively young, some parts having achieved their present arrangement as recently as 30 000 years ago. Lake Turkana last overflowed into the White Nile basin only 9000 years ago. During this recent phase the lower basin has become arid, and the connection between the freshwater faunas of Egypt and tropical Africa is now restricted to the slender thread of the main river. Aquatic molluscs in Egypt and the Sudan have been investigated intensively in relation to schistosomiasis and also because shells provide evidence of past ecological conditions (Gardner, 1932; Williams & Adamson, 1974). As the headwaters in Ethiopia and East Africa have also been searched with some thoroughness, the snail fauna of the Nile system is the best known of any large African river. A list of species (Table 12.16), which excludes those restricted to the major lakes (Albert, Edward, Tana and Victoria), comprises 15 prosobranchs and 37 pulmonates (including ancylids as genera only), of which Lymnaea columella, Helisoma and Physa are recent introductions. The total of nearly 50 indigenous taxa includes a group of 8 species with palaearctic affinities, belonging to the genera Theodoxus, Valvata, Lymnaea, Planorbis, Armiger and Ancylus. Some of the 9 species seemingly endemic to the Nile Basin (Table 12.16) may not be distinct from closely-related species living in the Near East (Theodoxus, Valvata, Gyraulus ehrenbergi). In the extensive wetland of the Sudd, only the single species Gabbiella schweinfurthi is perhaps restricted to the region (Brown et al., 1984). Speciation in the White Nile system has probably been restrained by instability in flow, demonstrated by the periodic interruption of outflows from Lakes Albert and Victoria, the lost connection with Lake Turkana and fluctuations in water level in the Sudd region. No molluscs are known from the Blue Nile in its deep gorge in Ethiopia, and it seems unlikely that any could tolerate the conditions in this stretch of the river.

REGIONS, LAKES AND RIVERS: BIOGEOGRAPHY 593

The total of gastropod species known from the Nile Basin excluding the large lakes is not much more than half the number for the Zaire Basin, and the proportion of endemic species is much lower (Table 12.17). The Nile has only 15 species of prosobranch in comparison with 74 for the Zaire, and the two basins have only 5 prosobranchs is common (Lanistes ovum, Pila ovata, P. wernei, Cleopatra guillemei and Melanoides tuberculata). In contrast the Nile Basin has more pulmonate species than the Zaire (Table 12.17). Since the prosobranchs and the pulmonates present in both the Nile and Zaire basins are even more widely distributed, this similarity is much less significant than the marked differences between these basins. There are clear differences also between the Nile and Niger basins, for less than one-third of the Nile species are found also in the Niger Basin (Table 12.17). Much of the distinctive character of the Nile fauna is derived from the occurrence of a high proportion of pulmonate species that are restricted to northeast and eastern Africa (especially of Bulinus), and to the presence of the 8 palaearctic species. Palaearctic species are established not only in the lower Nile, but also in the headwaters of the Blue Nile in highland Ethiopia. Here the collector from the northern hemisphere will be reminded of moorlands by the landscape of undulating grassland with many small streams and bogs. One route for northern organisms to have reached the Ethiopian plateau might have been the Nile, and Table 12.16. The freshwater snails of the Nile Basin, including the headwater streams in Ethiopia and Kenya, but excluding the large lakes Albert, Edward, Tana and Victoria. E= endemic. P=affinity with the Palaearctic Region. Z=present also in the Zaire Basin. Names used by Pilsbry & Bequaert (1927, pp. 568–9) are shown in brackets. Prosobranchs NERITIDAE Theodoxus niloticus EP VIVIPARIDAE Bellamya unicolor VALVATIDAE Valvata nilotica EP AMPULLARIIDAE Lanistes carinatus L. ovum (L. adansoni; procerus; pyramidalis) Z Pila ovata (P. congoensis) Z P. wernei (P. chevalieri; leopoldvillensis) Z BITHYNIIDAE Gabbiella humerosa (Victoria Nile and lakes) G. kichwambae E G. parva E G. senaariensis

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G. schweinfurthi E G. barthi E THIARIDAE Cleopatra bulimoides C. guillemei Z (Lake Tanganyika) Melanoides tuberculata Z Pulmonates LYMNAEIDAE Lymnaea natalensis Z L. truncatula P L. stagnalis P L. columella (introduced) ANCYLIDAE Ancylus fluviatilis P A. regularis EP (and S Ethiopian rift) Burnupia spp. Z Ferrissia spp. Z PLANORBIDAE Planorbis planorbis P Afrogyrus coretus (Planorbis gibbonsi) Z Armiger crista P Ceratophallus natalensis Z C. kigeziensis ?Z (possibly Planorbis avakubiensis) Gyraulus costulatus Z G. ehrenbergi E Lentorbis junodi Segmentorbis angustus Z S. eussoensis S. kanisaensis Z Biomphalaria alexandrina E B. pfeifferi (Planorbis adowensis; bridouxianus) Z B. sudanica Z Helisoma duryi (introduced) Bulinus africanus Z B. globosus (Physopsis choziensis) Z B. nasutus B. ugandae E (also in S Ethiopia)

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B. umbilicatus B. natalensis/tropicus complex (diploid) ?Z B. truncatus (tetraploid) Z B. hexaploidus E (Nile/Awash watershed) B. octoploidus E (Nile/Awash watershed) B. permembranaceus (tetraploid) E (W Kenya highlands) B. forskalii (B. lamellosus) Z B. scalaris Z B. reticulatus PHYSIDAE Physa acuta Z (introduced) Table 12.17. The snail faunas of three large African river basins (excluding species restricted to large lakes). Numbers of endemic species are given in brackets. Ferrissia and Burnupia are treated only as genera. Number of species Zaire Nile Zaire and Nile Nile and Niger

Prosobranchs

Pulmonates

Total (endemic)

74 (57) 15 (6) 5 5

22 (3) 36 (4) 16 approx. 9

96 (60) 51 (10) 21 14

another the chain of hills bordering the western shore of the Red Sea. The presence of Ancylus fluviatilis in Ethiopia and in western Arabia perhaps derives from the continuity of these areas before they were separated by the Red Sea; this connection could account also for the occurrence in Arabia of Bulinus wrighti and of its closest relative B. reticulatus in Africa. Valvata is widely distributed on the Ethiopian plateau, and in the past lived in the Galla lakes region of the southern rift valley; this might have been the route through which the genus became established in the Pliocene-Pleistocene fauna of Lake Turkana. Ancylus fluviatilis is common in stony streams draining towards the Nile from northeast of Addis Ababa, while A. regularis lives in other small tributaries of the Nile flowing from forest in the south-western highlands; both limpets can be found living on stones together with Burnupia, their African counterpart. The coexistence of palaearctic and tropical species is a fascinating sight; a memorable experience for me was to find Armiger crista living together with Ceratophallus natalensis and Segmentorbis angustus in a small pool beside a torrential stream just before it plunged down a precipitous gorge leading towards the Blue Nile.

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Biogeography: a continental perspective Probably fewer than 400 species of freshwater gastropod occur in the whole of Africa, while in the Afrotropical Region alone there are several thousand species of land molluscs (Van Bruggen, 1977, 1986). The comparative poverty of the aquatic gastropods probably reflects the instability of most inland waters on the evolutionary time-scale, so that isolated diverging populations often do not survive long enough to complete the process of speciation. This low taxonomic diversity, except in the oldest river systems and in the most long-lived lakes, has the advantage of simplifying biogeographical analysis. Information of a biogeographical nature has already appeared in many places in this chapter and in some earlier parts of this book (Chapters 3, 4 and 9), since the basic materials for biogeographical analysis are taxonomic units and maps of their distributions. There is a need for caution, as for most species considered here there is no genetic evidence of their distinctness, so that there is the danger of circular reasoning when discussing the biogeographical significance of taxa which may be recognised partly on account of their distributions. Four biogeographical aspects of the African freshwater snails will now be considered: faunal regions, the transition between the Palaearctic and Afrotropical (Ethiopian) faunas, species diversity in relation to latitude, and the origins of the African fauna and its relationships to those of other continents. Faunal regions Africa is divided between two major faunal areas, the Palaearctic Region, confined to northern Africa, and the Afrotropical (‘Ethiopian’) Region (Crosskey & White, 1977), comprising the rest of the continent, Madagascar and the Mascarene Islands. Although the formally defined Palaearctic Region extends from Europe only into North West Africa, some palaearctic species are more widespread now and were even more so in the past; their southern limits are discussed in the following section. The Afrotropical Region can be subdivided according to clusterings among the distributions of species, which suggest particularly favourable conditions for speciation and also imply barriers to dispersal. Much of this data has been touched on in the foregoing account of the snail faunas of lake basins and river systems. Two major tropical subregions have been recognised; the West African Subregion, comprising the West African coastal area and the Zaire basin, and the ‘East and South African Subregion’ composed of all the rest of the tropical area (Van Damme, 1984). The West African Subregion is largely an area of lowland forest and is distinguished by the presence of a large number of endemic prosobranch species and genera including Potadoma; few pulmonate species are restricted to this area. Within the West African Subregion the freshwater snail fauna is far from homogeneous; Lake Tanganyika has an obviously different assemblage of species, while south-east Zaire (Katanga) is

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comparatively poor in prosobranchs, and there are a number of areas with distinct groups of species (e.g. in the Guinea coastal area, Volta basin, lower Zaire and eastern Zaire). But the distributions of snails are not well-enough known, in my opinion, to support the hierarchical system of sub-areas proposed by Van Damme (1984). It seems likely that there are relationships between the clusters of endemic species living in streams within the lowland forest region and the distribution of Pleistocene forest refuges (Mayr & O’Hara, 1986), which persisted through dry periods when the forest contracted. At present there is a break in the forest cover, named the Dahomey Gap, which may be of significance in the biogeography of aquatic gastropods. The so-called East and South African Subregion (Van Damme, 1984) actually includes all of northern Africa apart from the North West. Compared with the West African Subregion the prosobranch fauna is less diverse (lacking Potadoma), but there are more species of Gabbiella and Cleopatra, while the pulmonate fauna is much richer (especially in species of Ceratophallus and Bulinus). Here too I doubt the value of the large number of sub-areas (15) defined by Van Damme (1984). The more distinct local features are evident in the area comprising Egypt and Ethiopia (the presence of palaearctic species), the southern tip of the continent (the progressive subtraction of tropical species, the presence of species adapted to cool climate and the occurrence of Tomichia), and in Madagascar (presence of Melanatria). The Palaearctic-Afrotropical interface in the Sahara Between the freshwater gastropod faunas of the Palaearctic and Afrotropical regions there is in the Sahara a zone of overlap, in which subfossil shells show that snail distributions have fluctuated in response to changes in climate. Palaearctic species live not only in North West Africa but also southern Algeria, Egypt and the highlands of Ethiopia. Lymnaea truncatula alone penetrates much further south, but this seems due to dispersal through the highlands of eastern Africa, thus bypassing the Sahara. The southern limit estimated by Sparks & Grove (1961) for palaearctic species in the Sahara during Quaternary cool phases was extended by Van Damme (1984) considerably to include (Fig. 145): the Tibesti Mountains and Chad Basin, according to several localities for subfossil shells reported as Valvata tilhoi Germain (1909, type locality in Eguei district, between Tibesti and Lake Chad); the Ethiopian highlands and the area southwards to Lake Turkana, according to the finding in the Turkana Basin of shells of PliocenePleistocene age, identified as Valvata by Van Damme & Gautier (1972) and Williamson (1981). During the cooler and wetter phases some tropical species extended northwards to a limited extent and in some places may have co-existed with palaearctic

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species, as they may do so occasionally at present (Van Damme, 1984, Table 4). But generally there is no evidence for any great change in the zone of overlap, e.g. a rich snail fauna in the Taoudenni Basin of northern Mali during a wet period was entirely tropical (Rosso, 1983, according to Van Damme, 1984, p. 148). It appears that the areas where an almost entirely palaearctic fauna or an almost entirely tropical fauna occur have remained little changed throughout the Quaternary. Fluctuations have been limited to changes in the proportions of palaearctic and tropical species within the zone of mixed fauna. Three possible reasons for the small success of tropical species dispersing northwards through the Sahara are: 1) wet periods may have been too brief to be exploited by snails with limited powers of dispersal; 2) cool temperatures during wet periods may have been unfavourable to them; 3) they may have been opposed by competition from northern species. Species diversity in relation to latitude It is generally true that the number of species of organisms in the humid tropics is much greater than at higher latitudes, as is clearly demonstrated by the freshwater fishes of Africa (Beadle, 1981, pp. 142–146). Although depressed by aridity in the Sahara, the estimated totals for gastropod species of fresh and brackish waters in 5° zones of latitude, show a distinctly richer fauna in the Equatorial Region, 10°N–10°S (Fig. 151). These totals include only genera for the more poorly known groups (Hydrobiidae of North Africa and the ancylids Burnupia and Ferrissia) and recently introduced species were omitted (Lymnaea columella, Amerianna, Helisoma and Indoplanorbis). Also omitted were species endemic to large lakes, as these tend to have rich faunas whether situated in tropical or in temperate areas; if included the lacustrine species would greatly boost the total for the Equatorial zone. From 30–20°N almost all the territory is desert or semi-arid and the comparatively few species found are associated with refuges in the Sahara or with the Nile. There are large arid areas also within 20– 15°N, but a 4-fold increase in species is due to the Senegal Basin, the Sudanese Nile and the plateau of northern Ethiopia. Within the Equatorial zone the total is swelled within 10–15°N by prosobranchs endemic to the West African coastal area and from 5°N to 10°S there is a major contribution from the genera Potadoma and Melanoides in eastern Zaire. Decline in number of species from 15° southwards is partly due to increasing aridity in the south-west, especially in Botswana, Namibia and western Cape. From 25–35°S much of the area lies within the cool temperate climatic region, notably the highveld plateau including Lesotho. Few tropical species extend south of 30°, but the total here is increased by the species of Tomichia associated with the Cape coastal area. Improvements in the taxonomy of the Hydrobiidae, Assimineidae and Ancylidae will perhaps result in sizeable increases in the numbers of species for northern and southern Africa, but hardly to an extent comparable to the numbers found in the Equatorial zone. It might be argued that the number of species tends

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to decrease southwards from the Equatorial zone partly because the land area decreases progressively. However, the more important requirement for evolution of a rich fauna of freshwater molluscs appears to be that diverse habitats and isolating mechanisms should persist long enough for speciation to occur. Where these conditions exist, a large geographical area seems unnecessary, to judge from the concentrations of endemic species in lakes and in small patches of West Africa. Relationships with other continental areas: origins of the African snail fauna The living snail fauna of fresh and brackish waters in tropical Africa is welldifferentiated from that of other continents. The few genera found in both Africa and in tropical America are Neritina, Neritilia, Lymnaea, Ferrissia and Biomphalaria (further long-established trans-Atlantic affinities are mentioned below concerning Potadoma, Thiara and Pachymelania). Transportation by man seems to account for the presence in the Americas and Africa of Helisoma and the Physidae. Most of the palaearctic genera found in northern Africa are represented in India, some by the same species (Subba Rao, 1989), but only 5 tropical species are reported for both Africa and India: Neritina pulligera, Thiara amarula, T. scabra, Melanoides tuberculata and the recent introduction to Africa, Indoplanorbis exustus. The only other tropical genera present in both Africa and India are Septaria, Bellamya, Pila, Lymnaea, Ferrissia and Gyraulus. The systematic position of (?)Potamopyrgus of West Africa is too uncertain for it to be linked to the occurrence of this genus in the Andaman Islands (Subba Rao, 1989, p. 65) or anywhere else. Outstanding features of the Afrotropical fauna compared with that of India and South East Asia (Brandt, 1974; Davis, 1982) are its greater richness in species of Ampullariidae, Bithyniidae, Thiaridae and Planorbidae. The Afrotropical area lacks any hydrobioid radiation as great as that in the Mekong River and it has far fewer species of Potamididae and Ellobiidae adapted to fresh or moderately brackish waters. There are other families well represented in coastal areas of southern Asia but unknown in Africa (Stenothyridae, Iravadiidae etc; see Brandt, 1974). Discussion of the history and origins of the Afrotropical freshwater snail fauna appears in a large literature, with major contributions by Davis (1982), MeierBrook (1984), Van Damme (1984) and Taylor (1988). A review by Bǎnǎrescu (1990, pp. 325–360) of the distribution of freshwater snails on a global scale contains an unfortunate number of errors in both text and figures in relation to Africa. Davis (1982) made the important and still valid point, that many families are not yet known well enough in respect of their systematics, fossil record and ecology for objective discussion to be possible. It appears that the freshwater molluscs of Africa have generally evolved within the area of the present continent, from the fauna that this area carried while it was first part of Pangaea (the single great continent that began to break up about 150 million years ago)

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Fig. 151. Estimated numbers of gastropod species of fresh and brackish waters in the African continent. Totals are given for each zone of 5° latitude. Hydrobiidae of North Africa are included only as genera, as also are the ancylids Burnupia and Ferrissia. Neither the species endemic to lakes nor introduced species are included. The total for the northern zone 30–35° is for all of Africa lying north of 30° latitude.

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and then part of Gondwanaland (the southern supercontinent that comprised South America, Arabia, India, Australia, New Zealand and Antarctica). Subdivision of the Gondwanaland biota was the major event that determined the ground-plan of the snail faunas in the developing southern continents of today, according to Davis, 1982) who stressed the subsequent importance of dispersal and ecology in the development of the continental faunas of the present. Emphasis is thus placed not on derivation of species from other continental areas (via narrow ‘land bridges’ or by passive transportation across ocean gaps), but on dispersal within habitats of the kind occupied today (Taylor, 1988). To the influence of Gondwanaland is attributed the presence of some snail groups in Africa as well as in other southern land masses; these distribution patterns are of two types (Davis, 1982, pp. 391–92): 1. South America-Africa-India/Asia. Pomatiopsidae and Ampullariidae (both discussed further below); Thiaridae (the related genera Pachychilus of S America, Potadoma of Africa and Brotia of SE Asia). Further trans-Atlantic links lie in close relationships between Thiara and Hemisinus of South America (Taylor, 1988, Fig. 18), and between Pachymelania of West Africa and fossil species in North America (Taylor, 1988, Fig. 12). Biomphalaria seems to fit here, as it lives in Africa and S America, and is known as Eocene fossils in N America, Europe and Asia (Taylor, 1988, Fig. 16). 2. Africa-India-SE Asia. Viviparidae (Bellamya), Thiaridae (Thiara and Melanoides), Planorbidae (Bulininae). Taylor (1988) gives maps of the prosobranch distributions. In order to reconstruct the history of a snail fauna it is important to establish correctly the directions of evolutionary change, and this depends on recognising which are the more primitive among the living species. Where are such species likely to be found? While discussing variation within Bulinus (Chapter 7: B. natalensis and B. tropicus) it was suggested that lakes are long-term sources of snail colonists for short-lived habitats in surrounding areas. Thus lakes should contain taxa representative of comparatively old lineages, especially if they are as large and old as Lakes Malawi and Tanganyika. Even ancient lakes, however, are outlived by some river systems, and here even older stocks of organisms may survive: probable examples are Potadomoides in watercourses to the east and west of Lake Tanganyika, and taxa endemic to rivers and streams in the western lowland forest region (e.g. Saulea, Sierraia, Soapitia, Pseudocleopatra). Some elements of this western fauna seem to have extended further eastwards in the past, presumably in association with past expansions of the forested area and its watercourses. Saulea is reported from the Miocene of Kenya (Pain & Beatty, 1964), and Potadoma from Pliocene deposits in the western Turkana Basin (Williamson, 1985c,d). According to Van Damme (1984) the molluscan fauna of a large area of Africa outside the western lowland forest region reached its modern composition

602 FRESHWATER SNAILS OF AFRICA

during the last half million years. Centres of adaptive radiation have been provided by lakes in the eastern rift valleys, but being closely adapted to lacustrine conditions these faunas have not contributed to the fauna outside their catchments. Van Damme considered that a radiation of pulmonate genera started after a phase of extinction in the Plio-Pleistocene period, in some lakes filling niches formerly occupied by extinct prosobranchs. However, the precise sequence of events in the history of molluscan faunas in the eastern lake basins is still a matter of debate (e.g. Williamson, 1990). Doubtless the shell-rich sediments and the living molluscs of this region will continue to be of interest in relation to the study of evolution. Already the fossil molluscs of the Turkana Basin have been a focus for controversy over the ‘punctuated equilibrium’ model of speciation, while the living snails of Lakes Tanganyika and Malawi provide insights into the process of adaptative radiation (see under these lakes). Reasons can only be guessed at for such distinctive features as the greater radiation in Africa of the Ampullariidae, Bithyniidae, Thiaridae and Bulininae, compared to SE Asia, where the Viviparidae and ‘hydrobioid’ Pomatiopsidae are much more diverse. Davis (1982) emphasised the part played by ecology and suggested that the comparatively extensive habitat in Africa provided by swamps and slowly flowing muddy rivers accounts for the success of ampullariids and bithyniids. This may be true for ampullariids, but not I think for the Bithyniidae, whose species endemic to Africa live mostly in lakes, rocky rivers and clear streams. I agree with Davis that the smallness of the hydrobioid radiation in tropical Africa could be due to a paucity of limestone-rich areas and of suitable rocky substrata in perennial rivers. Although there are perennial rocky rivers in western Africa, notably the lower Zaire and some rivers in the Guinean coastal area, their dissolved chemical content tends to be low. The presence in fresh water in SE Asia but not in eastern Africa of representatives of a number of prosobranch families which are essentially marine-brackish groups can be explained (Davis, 1982) by changes in sea-level over the shallow Sunda shelf. These changes affected a large area with major river systems; repeated transitions from marine to brackish to fresh conditions, and back again to marine, provided numerous opportunities for adaptation to fresh water. The poorer fauna of Ellobiidae in eastern Africa compared with SE Asia can also be explained by the lack of such conditions in the African coast. For Afrotropical prosobranchs, evolutionary history is best understood for the Ampullariidae and Pomatiopsidae. The latter is considered to have a Gondwanaland origin (Davis, 1981), with relict groups living in South America, South Africa and Australia. After reaching Asia via India, dispersal continued eastwards and eventually into North America; the subfamily Triculinae radiated explosively in the Mekong River of SE Asia. Davis related the modern and the past distributions of Tomichia in South Africa to changing ecological conditions since the Miocene; increasing aridity in the west led to the drying up of perennial fresh water, resulting in adaptation by different species to a wide range of conditions, including seasonal cycles of high salinity. In the Ampullariidae,

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found in tropical-subtropical areas of America, Africa and Asia, comparative morphology (Berthold, 1989) indicates that the genera of Africa and Asia represent an older stock than those of the neotropics. Within Lanistes, endemic to Africa, there seems to have been a trend to increase the size of the lung sac (Brown & Berthold, 1990). A small radiation of three species within Lake Malawi (Berthold, 1990a) involved adaptations to predatory fishes, a sandy substratum for feeding and to life in deep water. The pulmonates of African fresh waters, like those of other continents, are less varied than the prosobranchs, for reasons that are partly ecological. Pulmonates have difficulty in invading deep-water biotopes within lakes, as they are adapted to filling the lung with atmospheric air, and they do not thrive in turbulent rivers. The exclusively freshwater pulmonates excel at achieving high density in shallow seasonal waterbodies and, being self-fertilising hermaphrodites, they are well equipped for dispersal and colonisation. However, speciation will not be favoured in ephemeral habitats with short-lived populations of individuals well suited for dispersal. But although no pulmonate family is endemic to Africa, there are some distinctive genera of small planorbid snails (Afrogyrus, Ceratophallus, Segmentorbis, and Lentorbis). The first two belong to the ‘tribe Planorbini’ (a group of genera including also Planorbis and Gyraulus) for which a western Palaearctic origin has been postulated (Meier-Brook, 1984). Afrogyrus and Ceratophallus appear to have been an early offshoot from the stem species of Planorbis; they may have evolved during the Cretaceous (65–136 million years ago) and before Madagascar separated from Africa (since Madagascar has two species of Afrogyrus). Meier-Brook also suggested that the subgenus Gyraulus (Caillaudia) evolved in Africa, following subdivision of the stock of Gyraulus by the separation of Africa from Europe. Bulinus is the pulmonate genus with the most living species confined to the Afrotropical Region; what little is known of its history is reviewed in Chapter 7 (Bulinus: Evolution). The fossil record is poor, but directions of change are clearly indicated in at least the B. truncatus/ tropicus complex by increases upon the basic chromosome number. The attention of the world’s naturalists was first attracted to the freshwater molluscs of Africa by the discovery of the thalassoid snails of Lake Tanganyika and the puzzle of their origin. Over a century later another prominent controversy about evolution was aroused by the fossil shells of the Turkana Basin. But it was the working-out of the life cycle of African schistosomiasis that made some of the freshwater snails of Africa familiar to many people besides scholars. Future discoveries may not have such a dramatic impact, but there can be no doubt that the improving knowledge of the living species will continue to provide essential information for the control of snail-transmitted diseases and contribute towards our understanding of the ecology and evolution of freshwater faunas on a global scale.

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Starmühlner, F. 1976. Contribution to the knowledge of the freshwater fauna of the isle of Anjouan (Comores). Cahiers de l’Office de la Recherche Scientifique et Technique OutreMer, série Hydrobiologie, 10:255–265. Starmühlner, F. 1977. Contribution to the knowledge of the freshwater fauna of la Réunion (Mascarene). Cahiers de l’Office de la Recherche Scientifique et Technique OutreMer, série Hydrobiologie, 11:239–250. Starmühlner, F. 1979. Results of the Austrian Hydrobiological Mission, 1974, to the Seychelles, Comores and Mascarene archipelagos: Part 1. Annalen des Naturhistorischen Museums, Wien, 82:621–742. Starmühlner, F. 1983. Results of the Hydrobiological Mission, 1974, of the Zoological Institute of the University of Vienna. 8: Contributions to the knowledge of the freshwater gastropods of the Indian Ocean islands (Seychelles, Comores, Mascarenearchipelagos). Annalen des Naturhistorischen Museums, Wien, 84/B:127–249. Starmühlner, F. 1986. Checklist of the fauna of mountain streams of tropical Indopacific islands. Annalen des Naturhistorischen Museums, Wien, 88/89B:457–480. Stuckenberg, B.R. 1969. Effective temperature as an ecological factor in southern Africa. Zoologica Africana, 4:145–197. Subba Rao, N.V. 1989. Handbook: Freshwater Molluscs of India. Calcutta: Zoological Survey of India. Talling, J. & Talling, I.B. 1965. The chemical composition of African lake waters. Internationale Revue der Gesamten Hydrobiologie, 50:421–463. Taylor, D.W. 1988. Aspects of freshwater mollusc ecological biogeography. Palaeogeography, Palaeoclimatology, Palaeoecology, 62:511–576. Van Bruggen, A.C. 1974. Alien planorbid from South West Africa erroneously recorded as Biomphalaria pfeifferi. Zoologische Mededelingen Leiden, 48:11–18. Van Bruggen, A.C. 1977. A preliminary analysis of African non-marine Gastropoda Euthyneura families. Malacologia, 16:75–80. Van Bruggen, A.C. 1986. Aspects of the diversity of the land molluscs of the Afrotropical Region. Revue de Zoologie Africaine, 100:29–45. Van Damme, D. 1984. The Freshwater Mollusca of Northern Africa. Distribution, Biogeography and Palaeoecology. Dordrecht, Boston, Lancaster: W.Junk. Van Damme, D. & Gautier, A. 1972. Molluscan assemblages from the late Cenozoic of the lower Omo Basin, Ethiopia. Quaternary Research, 2:25–37. Van Eeden, J.A. & Brown, D.S. 1966. Colonization of fresh waters in the Republic of South Africa by Lymnaea columella Say (Mollusca: Gastropoda). Nature, London, 210: 1172–1173. Vrijenhoek, R.C. & Graven, M.A. 1992. Population genetics of Egyptian Biomphalaria alexandrina (Gastropoda, Planorbidae). Journal of Heredity, 83:255–261. Walsh, J.F. & Mellink, J.J. 1970. Freshwater snails of the Kainji Lake basin with special reference to the transmission of schistosomes. In Kainji, a Nigerian Man-made Lake, 1, Ecology: 105–111. Visser, S.A. (Ed.). Ibadan: Nigerian Institute for Social and Economic Research. Welcomme, R.L. 1972. The Inland Waters of Africa. CIFA Technical Paper No. 1. Rome: Food and Agricultural Organisation of the United Nations. Wen, S.T. & Chu, K.Y. 1984. Preliminary schistosomiasis survey in the lower Volta River below Akosombo Dam, Ghana. Annals of Tropical Medicine andParasitology, 78: 129–133.

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Werger, M.J. (Ed.) 1978. Biogeography and Ecology of Southern Africa, 2 volumes. The Hague: W.Junk. West, K., Cohen, A.S. & Baron, M. 1991. Morphology and behaviour of crabs and gastropods from Lake Tanganyika, Africa: implications for lacustrine predator-prey coevolution. Evolution, 45:589–607. Williams, M.A.J. & Adamson, D.S. 1974. Late Pleistocene desiccation along the White Nile. Nature, London, 248:584–586. Williamson, P.G. 1981. Palaeontological documentation of speciation in Cenozoic molluscs from the Turkana Basin. Nature, London, 293:437–443. Williamson, P.G. 1985a. Punctuated equilibrium, morphological stasis and the palaeontological documentation of speciation: a reply to Fryer, Greenwood & Peake’s critique of the Turkana Basin sequence. Biological Journal of the Linnean Society, 26: 307–324. Williamson, P.G. 1985b. In reply to Fryer, Greenwood and Peake. Biological Journal of the Linnean Society, 26:337–340. Williamson, P.G. 1985c. A first record of Potadoma (Swainson) from eastern Africa. Journal of Conchology, 32:135–139. Williamson, P.G. 1985d. Evidence for an early Plio-Pleistocene rainforest expansion in East Africa. Nature, London, 315:487–489. Williamson, P.G. 1990. Late Cenozoic mollusc faunas from the North Western African Rift (Uganda-Zaire). Virginia Museum of Natural History, Memoir, 1:125–139. Woodward, S.P. 1859. On some new freshwater shells from Central Africa. Proceedings of the Zoological Society of London, 1859:348–350. Wright, C.A. 1965. The freshwater gastropod molluscs of West Cameroon. Bulletin of the British Museum (Natural History), Zoology, 13:75–98. Wright, C.A. 1971. Bulinus on Aldabra and the subfamily Bulininae in the Indian Ocean area. Philosophical Transactions of the Royal Society, B, 260:299–313. Wright, C.A., Klein, J. & Eccles, D.H. 1967. Endemic species of Bulinus in Lake Malawi (Lake Nyassa). Journal of Zoology, London, 151:199–209.

Appendix

Regional bibliography for the identification of the freshwater snails of Africa and Arabia, and for study of their distribution. See also Chapters 3,4,9–12. The selected works cited here are of the more general kind and were mostly published comparatively recently. Of the extensive earlier literature only a few of the more outstanding contributions are included. North East Africa (Egypt, Sudan, Ethiopia) Brown, D.S. 1965. Freshwater gastropod Mollusca from Ethiopia. Bulletin of the British Museum (Natural History), Zoology, 12:37–94. Brown, D.S., Fison, T., Southgate, V.R. & Wright, C.A. 1984. Aquatic snails of the Jonglei region, southern Sudan, and transmission of trematode parasites. Hydrobiologia, 110:247–271. Danish Bilharziasis Laboratory, 1983. A Field Guide to freshwater Snails in Countries of the WHO Eastern Mediterranean Region. Copenhagen: Danish Bilharziasis Laboratory. Danish Bilharziasis Laboratory, 1986. A Field Guide to African Freshwater Snails. 3. North East African Species. 2nd edition. Charlottenlund: Danish Bilharziasis Laboratory. Itagaki, H., Suzuki, N., Ito, Y. et al. 1975. Study on the Ethiopian freshwater molluscs, especially on identification, distribution and ecology of vector snails of human schistosomiasis. Japanese Journal of Tropical Medicine and Hygiene, 3:107–134. Madsen, H., Daffalla, A.A., Karoum, K.O. & Frandsen, F. 1988. Distribution of freshwater snails in irrigation schemes in the Sudan. Journal of Applied Ecology, 25: 853– 866. Tchernov, E. 1971. Freshwater molluscs of the Sinai Peninsula. Israel Journal of Zoology, 20:209–221. Van Damme, D. 1984. The Freshwater Mollusca of Northern Africa. Distribution, Biogeography and Palaeoecology. Dordrecht, The Netherlands: W.Junk.

North West Africa (Algeria, Morocco, Tunisia, Libya) Dupouy, J., Abdelhak, F. & Yazid, F. 1980. Compétition interspècifique entre Melanopsis praemorsa L. (Prosobranchia: Thiaridae) et certains basommatophores en Oranie et au Sahara nord-occidentale. Journal of Molluscan Studies, 46:1–12. Kristensen, T.K. 1985. Guide Pratique des Gastéropodes d’Eau Douce Africains. 7. Espèces présentes en Afrique du Nord-Ouest. Charlottenlund: Danish Bilharziasis Laboratory. Meier-Brook, C, Haas, D., Winter, G. & Zeller, T. 1987. Hydrochemical

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factors limiting the distribution of Bulinus truncatus (Pulmonata: Planorbidae). American Malacological Bulletin, 5:85–90. Van Damme, D. 1984. The Freshwater Mollusca of Northern Africa. Distribution, Biogeography and Palaeoecology. Dordrecht, The Netherlands: W.Junk.

West Africa (Lake Chad and westwards to the coasts of Senegal and Mauritania) Betterton, C. 1984. Ecological studies on the snail hosts of schistosomiasis in the South Chad Irrigation Project area, Borno State, northern Nigeria. Journal of Arid Environments, 7:43–57. Binder, E. 1957. Mollusques aquatiques de Côte d’Ivoire. 1. Gastéropodes. Bulletin de l’Institut Fondamental d’Afrique Noire, 19:97–125. Binder, E. 1968. Répartition des mollusques dans la Lagune Ebrié (Côte d’Ivoire). Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 11:3–34. Brown, D.S. 1974. A survey of the Mollusca of Lake Chad, Central Africa. Appendix A (Planorbidae and Ancylidae). Revue de Zoologie Africaine, 88:331–343. Brown, D.S. & Kristensen, T.K. 1993. A Field Guide to African Freshwater Snails. 1. West African Species. Revised 2nd edition. Charlottenlund: Danish Bilharziasis Laboratory. Hubendick, B. 1977. Freshwater gastropods of Sierra Leone. Acta Regiae Societatis Scientarum et Litterarum Gothoburgensis, Zoologica, 11:1–30. Lévêque, C. 1967. Mollusques aquatiques de la zone est du Lac Tchad. Bulletin de l’Institut Fondamental d’Afrique Noire, série A, 4:1494–1533. Madsen, H., Coulibaly, G. & Furu, P. 1987. Distribution of freshwater snails in the River Niger Basin in Mali, with special reference to the intermediate hosts of schistosomes. Hydrobiologia, 146:77–88. Ndifon, G.T. & Ukoli, F.M.A. 1989. Ecology of freshwater snails in south-western Nigeria. 1. Distribution and habitat preferences. Hydrobiologia, 171:231–253. Sellin, B., Simonkovich, E. & Roux, J. 1980. Etude de la répartition des mollusques hôtes intermédiaires des schistosomes en Afrique de l’ouest. Médecine tropicale, 40: 31–39. Van Damme, D. 1984. The Freshwater Mollusca of Northern Africa. Distribution, Biogeography and Palaeoecology. Dordrecht, The Netherlands: W.Junk.

Central Africa (Cameroon, Central African Republic, Gabon, Congo, Zaire) Baluku, B., Josens, G. & Loreau, M. 1989. Etude préliminaire de la densité et de la répartition des mollusques dans deux cours d’eau du Zaire oriental. Journal of African Zoology, 101:291–302. Bequaert, J. & Clench, W.J. 1941. Additions to the rheophilous mollusk fauna of the Congo estuary. Bulletin of the Museum of Comparative Zoology, Harvard, 88:3–13. Danish Bilharziasis Laboratory. 1982. Guide de Terrain des Gastéropodes d’Eau douce Africains. 5. Afrique centrale. Charlottenlund: Danish Bilharziasis Laboratory. Mandahl-Barth, G. 1968. Freshwater molluscs. Exploration Hydrobiologique du Bassin du Lac Bangweolo et du Luapula, 12:1–97.

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Mandahl-Barth, G., Malaisse, F. & Ripert, C. 1972. Etudes malacologiques dans la région du lac de Retenue de la Lufira (Katanga), etc. Bulletin de la Société de Pathologie exotique, 65:146–165. Mandahl-Barth, G., Ripert, C. & Raccurt, C. 1974. Nature du sous-sol, répartition des mollusques dulcaquicoles et foyers de bilharzioses intestinale et urinaire au BasZaire. Revue de Zoologie Africaine, 88:553–584. Pilsbry, H.A. & Bequaert, J. 1927. The aquatic mollusks of the Belgian Congo, with a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History, 53:69–602. Wright, C.A. 1965. The freshwater gastropod molluscs of West Cameroon. Bulletin of the British Museum (Natural History), Zoology, 13:75–98.

Southern Africa (Angola and the area south of the Zambezi River) Appleton, C.C. 1975. The influence of stream geology on the distribution of bilharzia host snails, Biomphalaria pfeifferi and Bulinus (Physopsis) sp. Annals of Tropical Medicine and Parasitology, 69:241–255. Appleton, C.C. 1977. The freshwater Mollusca of Tongaland, with a note on molluscan distribution in Lake Sibayi. Annals of the Natal Museum, 23:129–144. Brown, D.S. 1967. A review of the freshwater Mollusca of Natal and their distribution. Annals of the Natal Museum, 18:477–494. Brown, D.S. 1978. Freshwater molluscs. In Biogeography and Ecology of Southern Africa, 2: 1155–1180. Werger, M.J.A. (Ed.). The Hague: W.Junk. Brown, D.S. & Kristensen, T.K. 1989. A Field Guide to African Freshwater Snails. 8. Southern African Species. Charlottenlund: Danish Bilharziasis Laboratory. Brown, D.S., Curtis, B.A., Bethune, S. & Appleton, C.C. 1992. Freshwater snails of East Caprivi and the lower Okavango River Basin in Namibia and Botswana. Hydrobiologia, 246:9–40. Connolly, M. 1925. The non-marine Mollusca of Portuguese East Africa. Transactions of the Royal Society of South Africa, 12:105–220. Connolly, M. 1939. A monographic survey of the South African non-marine Mollusca. Annals of the South African Museum, 33:1–660. De Kock, K.N., Pretorius, S.J. & Van Eeden, J.A. 1974. Voorlopige kommentaar aangaande die vorkomens van die varswaterslakke in die Oranjerivier. 1. Die opvanggebied, 2. Die Hendrik Verwoerd Dam. In The Orange River. 187–212. E.M.Van Zinderen Bakker (Ed.). Bloemfontein: University of The Orange Free State. Machena, C. & Kautsky, N. 1988. A quantitative diving survey of benthic vegetation and fauna in Lake Kariba, a tropical man-made lake. Freshwater Biology, 19:1–14. Makura, O. & Kristensen, T.K. 1991. National freshwater snail survey of Zimbabwe. In Proceedings of the Tenth International Malacological Congress: 227–232. MeierBrook, C. (Ed.). Tübingen: Institute for Tropical Medicine and Unitas Malacologica. Oberholzer, G. & Van Eeden, J.A. 1967. The freshwater molluscs of the Kruger National Park. Koedoe, 10:1–42. Pretorius, S.J., Jennings, A.C., Coertze, D.J. & Van Eeden, J.A. 1975. Aspects of the freshwater Mollusca of the Pongola River flood plain pans. South African Journal of Science, 71:208–212. Prinsloo, J.F. & Van Eeden, J.A. 1973. The distribution of the freshwater molluscs in Lesotho, with particular reference to the intermediate host of Fasciola hepatica.

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Wetenskaplike Bydraes van die Potchefstroomse Universiteit, B, Natuurwetenskappe, 57:13 pp. Van Eeden, J.A. & Combrinck, C. 1966. Distributional trends of four species of freshwater snails in South Africa, with special reference to the intermediate hosts of bilharzia. Zoologica Africana, 2:95–109. Schutte, C.H.J. & Frank, G.H. 1964. Observations on the distribution of freshwater Mollusca and water chemistry of the natural waters in the south-eastern Transvaal. Bulletin of the World Health Organisation, 30:389–400. Wright, C.A. 1963. The freshwater gastropod Mollusca of Angola. Bulletin of the British Museum (Natural History), Zoology, 10:449–528.

South East Africa (Malawi, northern Mozambique, Zambia; excluding prosobranchs endemic to Lake Tanganyika) Azevedo, J.F.de, Medeiros, L.M.de et al. 1961. Freshwater mollusks of the Portuguese Overseas Provinces. 3. Mollusks of Mozambique. Estudos, Ensaios e Documentos do Junta Investigacao Ultramar, 88:1–394. Danish Bilharziasis Laboratory. 1977. A Field Guide to African Freshwater Snails. 4. South East African Species. Charlottenlund: Danish Bilharziasis Laboratory. Machena, C. & Kautsky, N. 1988. A quantitative diving survey of benthic vegetation and fauna in Lake Kariba, a tropical man-made lake. Freshwater Biology, 19:1–14. Mandahl-Barth, G. 1968. Freshwater molluscs. Exploration Hydrobiologique du Bassin du Lac Bangweolo et du Luapula, 12:1–97. Mandahl-Barth, G. 1972. The freshwater Mollusca of Lake Malawi. Revue de Zoologie et de Botanique Africaine, 86:257–289.

Lake Tanganyika Leloup, E. 1953. Gastéropodes. Exploration Hydrobiologique du Lac Tanganyika, 3: 1–273. Brown, D.S. & Mandahl-Barth, G. 1987. Living molluscs of Lake Tanganyika: a revised and annotated list. Journal of Conchology, 32:305–327.

East Africa (Somalia, Kenya, Uganda, Rwanda, Burundi and Tanzania; excluding the prosobranchs endemic to Lake Tanganyika) Brown, D.S., Jelnes, J.E., Kinoti, G.K. & Ouma, J. 1981. Distribution in Kenya of intermediate hosts for Schistosoma. Tropical and Geographical Medicine, 33: 95–103. Danish Bilharziasis Laboratory. 1987. A Field Guide to African Freshwater Snails. 2. East African Species . 2nd edition. Charlottenlund: Danish Bilharziasis Laboratory. Mandahl-Barth, G. 1954. The freshwater mollusks of Uganda and adjacent territories. Annales du Musée Royal du Congo Belge, Tervuren, Série 8°, Sciences Zoologiques, 32:1– 206.

Indian Ocean Islands Backeljau, T., Janssens, L. & Joqué, R. 1986 (1985). Report on the freshwater molluscs of the Comoro Islands, collected by the Zoological Mission 1983 of the ‘Koninklijk Museum voor Midden-Afrika, Tervuren’. Revue de Zoologie Africaine, 99:321–330.

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Barré, N., Isautier, H., Frandsen, F. & Mandahl-Barth, G. 1982. Inventaire des mollusques d’eau douce de la Réunion. Revue d’Elevage et de Médecine vétérinaires des Pays tropicaux, 35:35–41. Degrémont, A.A. 1973. Mangoky Project Campaign against Schistosomiasis in the Lower Mangoky (Madagascar). Basle: Swiss Tropical Institute. Julvez, J., Ali Halidi, M.A. & Brown, D.S. 1990. Inventaire des mollusques d’eau douce à Mayotte, archipel des Comores. Revue d’Elevage et de Médecine vétérinaires des Pays tropicaux, 43:173–176. Mozley, A. 1939. The freshwater Mollusca of the Tanganyika territory and Zanzibar Protectorate, and their relation to human Schistosomiasis. Transactions of the Royal Society of Edinburgh, 59:687–744. Starmühlner, F. 1969. Die Gastropoden des Madagassischen Binnengewässer. Malacologia, 8:1–434. Starmühlner, F. 1976a. Contribution to the knowledge of the freshwater fauna of the Isle of Anjouan (Comores). Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 10:255–265. Starmühlner, F. 1976b. Contribution to the knowledge of the fauna of running waters of Mauritius. Bulletin of the Mauritius Institute, 8:105–128. Starmühlner, F. 1977. Contribution to the knowledge of the freshwater fauna of La Réunion (Mascarene). Cahiers de l’Office de la Recherche Scientifique et Technique Outre-Mer, série Hydrobiologie, 11:239–250. Starmühlner, F. 1983. Results of the Hydrobiological Mission 1974 of the Zoological Institute of the University of Vienna. 8. Contributions to the knowledge of the freshwater gastropods of the Indian Ocean Islands (Seychelles, Comores, MascareneArchipelagos). Annalen des Naturhistorischen Museums, Wien, 84B:127–249.

Arabia and the Near East Al-safadi, M.M. 1990. Freshwater molluscs of Yemen Arab Republic. Hydrobiologia, 208: 245–251. Brown, D.S. & Gallagher, M.D. 1985. Freshwater snails of Oman, south-eastern Arabia. Hydrobiologia, 127:125–149. Brown, D.S. & Wright, C.A. 1980. Molluscs of Saudi Arabia: Freshwater molluscs. In Fauna of Saudi Arabia, 2:341–358. Wittner, W. & Buttiker, W. (Eds). Basel: Basel Natural History Museum. Burch, J.B. (Ed.) 1985. Handbook on Schistosomiasis and Other Snail-mediated Diseases in Jordan. Ann Arbor, U.S.A.: University of Michigan and University of Jordan. Danish Bilharziasis Laboratory. 1983. A Field Guide to Freshwater Snails in Countries of the WHO Eastern Mediterranean Region. Copenhagen: Danish Bilharziasis Laboratory. Ghandour, A.M., Al-Ghamdi, H.S. & Al-Robai, A.A. 1990. A review of snail intermediate hosts of schistosomiasis in Saudi Arabia. Journal of Medical and Applied Malacology, 2:79–91. Tchernov, E. 1975. The molluscs of the Sea of Galilee. Malacologia, 15:147–184. Wright, C.A. 1963. The freshwater gastropod molluscs of Western Aden Protectorate. Bulletin of the British Museum (Natural History), Zoology, 10:257–274.

Index to snail names

Names of species are arranged alphabetically (not grouped under genera). Names in brackets are those of genera and species adopted in the present account. Bold type is used for the adopted names of genera and for the main page references to family, genus and species. Subgenus=s–g. abyssinica (Bellamya unicolor) 46, 47(fig.), 526 abyssinicus (Ancylus fluviatilis) 161 abyssinicus (Bulinus) 212(fig.), 214, 259(map), 310, 314, 369, 401 accrensis (Hydrobia) 71–2(fig.), 78(fig.), 537 Achatina 347 aclopus (Planorbarius metidjensis) 206 Acroloxus 155 Acroloxidae 155 acuta (Auriculastra radiolata) 153 acuta (Physa) 26(fig.), 28(fig.), 231, 248(fig.), 347, 406–7; habitat 427, 431, 436, 457–8; distribution 504–5, 507–8, 513–16, 525, 543 Acutorbis s–g. of Segmentorbis 194 adansoni (Lanistes various) 60 adansoniana (Neritina) 42, 44(fig.) admirabilis (Anceya giraudi) 132 admirabilis (Melanoides) 101(fig.), 102, 522, 528–9 adowensis (Biomphalaria pfeifferi) 195 adspersa (Gabbiella) 25(fig.), 86(fig.), 87, 148(map) adusta (Pila ovata) 54–5(fig.) aequinoxialis (Neritina afra) 42–44(fig.) aethiopica (Eussoia) 96(fig.), 98 aethiopica (Jubaia) 89(fig.), 91 aethiops (Bellamya capillata) 47

affinis (Lanistes ellipticus) 63–4(fig.) afra (Neritina) 43, 44(fig.), 518 africana (Cleopatra) 122(fig.), 123 africana (Gabbiella) 87, 88(fig.), 148(map), 537 africana (Pila) 55(fig.), 537 africana (Potadoma zenkeri) 118 africanus (Bulinus), see also africanus group 209, 212(fig.), 259(map), 359–60, 408; aestivation 460, 462; chemical and physical factors, reponses to 450–2, 455, 457; circadian rhythm 464; distribution 259, 359, 424, 505, 508–10, 512, 526, 535, 543; growth and life cycle 479, 484; habitat 201, 421–4, 431, 435; intermediate host, as 310–11, 314–15, 317, 324, 409 africanus group (Bulinus), see also member species 209, 256–60 (maps); distribution and habitat 435, 452, 505, 507, 509–10, 533, 535; evolution 379–80; intermediate host, as 305, 308–9, 312– 14, 316, 322, 345; taxonomic characters and species concepts 355–6, 358–61 africanus (Theodoxus niloticus) 39, 526 621

622 FRESHWATER SNAILS OF AFRICA

Afrocanidea 14 Afrogyrus 2, 27, 29(fig.), 176, 183, 427, 451; distribution 504–5, 508, 516–17, 519, 528, 533, 542, 550–1 Afropomus 18, 19, 66, 339, 537–8 agglutinans (Melanoides) 105, 108(fig.) 539 ajanensis (Paludomus) 124(fig.), 127, 517 alabastrina (?Tomichia) 80(fig.) alberti (Gabbiella humerosa) 82, 522 albus (Gyraulus) 185 alexandri (Lanistes) 61 alexandrina (Biomphalaria) 3, 199(fig.), 200, 204, 257(map), 395, 477; breeding season 485; dispersal 436–7; distribution 257(map), 504, 536; growth 479; intermediate host, as 307, 320, 395 alirata (Lanistes farleri) 66 alluaudi (Bulinus tropicus) 230, 357(fig.) alta (Burnupia) 168, 169(fig.) altior (Bellamya jucunda) 48 alutacea (Potadoma) 117, 120(fig.), 540 amarula (Thiara) 22(fig.), 100, 101(fig.), 508, 516, 518, 548 amaena (Cleopatra ferruginea) 121, 488 Amerianna 7, 15, 24, 27, 175, 210(fig.), 515 ampullacea (Pila) 54, 347 Ampullaria see Pila and also balanoidea, grasseti, libycus Ampullariidae 6, 7, 16, 18, 53, 453, 473, 475, 548–50 Ancylidae 6, 7, 15, 23, 25–6, 152, 160, 206, 507, 546 Ancylus 6, 14, 25–6, 161, 171, 477–8, 502, 504, 519, 541–3 and see species of Burnupia and Ferrissia Anceya 132, 528–9 anderssoni (Afrogyrus coretus) 177 angolensis (Bulinus) 220, 221(fig.) angolensis (Melanoides) 106(fig.), 108 angulata (Gyraulus costulatus) 185–6 angulata (Potadoma) 119, 120(fig.) angulifera (Littoraria) 69

angulosa (Biomphalaria) 199(fig.), 200, 201 angustus (Segmentorbis) 26(fig.), 190–2 (fig.), 194, 421, 424, 460; distribution 504, 516, 520, 523, 531–33, 543–4 Anisus 177, 179–80, 188, 504, 517 and see chudeaui (Afrogyrus), natalensis (Ceratophallus), oasiensis, dalloni anomala (Melanoides) 25(fig.), 105, 110(fig.), 112(fig.), 540 antipodarum (Potamopyrgus) 74 apertus (?Ceratophallus) 178, 183, 185(fig.), 522 apiculata (Bulinus forskalii) 237(fig.) aponensis (Hydrobia) 70, 71(fig.), 74, 502 Aplexa 28, 249, 379, 430, 508, 514, 537 arabica (Biomphalaria pfeifferi) 195, 197 arabica (Lymnaea natalensis) 156 argenteus (Ancylus fluviatilis) 161 Armiger 26–7, 179, 504, 541–2, 544 ashangiensis (Ancylus) 162 Assimania misspelling of Assiminea Assiminea 21, 95 and see aethiopica (Eussoia), aurifera, leptodonta Assimineidae 6, 7, 15, 16, 21, 94, 95, 449, 463, 473, 538, 546 athiensis (Cleopatra) 125(fig.), 126 Auricula see catonis, durbanica, gaziensis, labrella, subula auricularia (Lymnaea) 156, 160, 251, 341, 519 Auriculastra 25–6, 152 auriculata (Neritina) 40 Auriculodes 25, 153 aurifera (Omphalotropidinae) 94 aurisfelis (Cassidula) 153 aurita (Pachymelania) 112, 113(fig.) Australorbis 194 and see camerunensis (Biomphalaria) avakubiensis (Ceratophallus kigeziensis) 182 Baizea see Bridouxia 139

INDEX TO SNAIL NAMES 623

balanoidea (Afropomus) 19(fig.), 66, 67(fig.), 76(fig.), 339, 537 balovalensis (Gabbiella) 88, 89(fig.), 540 bangweolicus (Lanistes ovum) 63 baringoensis (Bulinus tropicus) 525 barthi (Biomphalaria) 199(fig.), 200, 257(map), 533 barthi (Bulinus) 239, 358, 372 barthi (Gabbiella) 76(fig.), 86(fig.), 90, 148(map), 421–2, 542 Basommatophora 9, 152 Bathanalia 140, 528 bavayi (Bulinus) 238, 243(fig.) 245, 380, 451, 516–17 bavayi (Melanoides) 105 beccarii (Bulinus) 243(fig.), 244, 310, 380 Belgrandia 70 bella (Anceya giraudi) 132 Bellamya 6, 17, 18, 24, 46; distribution 146(map), 504, 508, 510, 517, 520, 522–6, 528, 532–3, 535, 537, 539–40, 542, 548–9; habitat and local occurrence 421, 424, 428–9, 434–5, 450–1, 474–6 bengalensis (Bellamya) 53, 517 benguelensis (Bulinus scalaris) 239–40 (fig.) benguelensis (Lentorbis) 190, 191(fig.), 255(map), 427 bennikei (Pseudocleopatra) 22(fig.), 128(fig.), 129, 539 bequaerti (?Ceratophallus faini) 183 bequaerti (Potadoma liberiensis) 117 bequaerti (Potadomoides) 130(fig.), 540 bernardianus (Lanistes libycus) 58(fig.), 60–1 bicarinata (Helisoma) 205 bicarinata (Potadoma) 116(fig.), 117, 537 bicarinatus (Ceratophallus) 182, 184(fig.), 520, 533 bicarinatus (Lanistes) 59(fig.), 539 bifasciata (Assiminea) 95(fig.), 96(fig.) Biomphalaria 27, 194, 205, 409; aestivation 460–2; biomass 495; chemical factors, reponses to 445–9, 451–4;

control of 392, 394–5, 398, 400–01, 403–08; dispersal 436–7; distribution 7, 257(map), 258(map), 317, 320, 424–7, 430–1, 504, 507–13, 515–18; food 437–8; habitat 7, 321, 421–5, 427–31, 434–5, 464–5; intermediate host, as 3, 303, 305, 307, 316, 318, 321, 324–5, 344–7; of lakes 396, 404, 437, 522–3, 525–6, 531–6; life cycle and population fluctuations 401, 433, 464, 477–80, 482, 484–7, 489, 494–5; temperature, responses to 455–59, 512– 13 Bithynia or Bythinia 15, 19, 82, 504, 522 and see species in Gabbiella and Mysorelloides Bithyniidae 6, 7, 15, 16, 19, 20, 81, 473, 538, 548–50 blanfordi (Ceratophallus) 182(fig.) Blauneria 25, 153 bloyeti (Thiara scabra) 102 boissyi (Biomphalaria alexandrina) 3, 200 bolteni, boltenianus (Lanistes carinatus) 59, 475 borbonica (Physa acuta) 248–9 borbonica (Septaria) 17(fig.), 24(fig.), 43– 4(fig.), 45, 508, 516 bourguignati (Lanistes farleri) 65 Bridouxia 137, 528 bridouxiana (Biomphalaria pfeifferi) 195, 203 bridouxiana (Cleopatra guillemei) 126 brincatiana (Cleopatra guillemei) 126 broecki (?Potadomoides) 130(fig.), 540 Brondelia 14, 163 Brotia 549 browni (Bulinus) 239, 314, 358, 372 brunnea (Burnupia) 165 Buccinum see fluminea, praemorsa, scabra (Thiara), truncatula bulimoides (Cleopatra) 121, 122(fig.), 151(map), 428–9, 434, 474–6, 504, 520, 531, 542

624 FRESHWATER SNAILS OF AFRICA

Bulimus see aurisfelis, coniformis, kisalensis Bulin, Le (Bulinus senegalensis) 2, 241, 352 Bulininae 7, 24, 175, 206, 549 Bulinus 2, 3, 15, 24, 28–9(figs), 208, 352– 89; aestivation 6, 7, 375, 460–3; biochemical features 356–58; biology and success 374–79; breeding system 375–7; chemical factors, responses to 394, 445–455; circadian rhythm 464; control of 392, 394–409; distribution 259–64(maps), 502, 504–5, 507–13, 516–21, 523–6, 528, 531–7, 541, 543, 545, 551; evolution 379–81; habitat and local occurrence 181, 201, 421–2, 424–38; intermediate host, as 303, 305, 308–25, 344–7, 378–9; physical factors, responses to 455–64; polyploidy 356, 377–8; reproduction, growth and life cycle 477–495; species groups and concepts 358–74; subgenus, as 236; taxonomic characters 352–8 Bulla see fontinalis (Physa) and hypnorum 248 burnupi (Ferrissia) 172(fig.), 173 Burnupia 25, 26(fig.), 163, 164(fig.), 171, 183; distribution 253(map), 423–7, 508, 512, 539–40, 542–3, 546–7; habitat 6, 171, 421–6, 437, 450, 453, 460, 463–4, 539, 543; in lakes 171, 421–2, 437, 522, 525, 528, 532–3 Burtonilla see Anceya 133 butiabiae (Melanoides tuberculata) 109 buttikoferi (?Potadoma) 116(fig.), 118, 537 byronensis (Pachymelania) 112, 113(fig.) Bythinella 70 Bythinia rejected spelling of Bithynia Bythoceras see Paramelania

caffer (Burnupia caffra) 163 caffra (Burnupia) 162(fig.), 164, 253(map), 528 caillaudi (Lymnaea natalensis) 156, 518, 526 Caillaudia s–g. of Gyraulus 185–6, 551 camerunensis (Biomphalaria) 201, 202(fig.), 258(map), 307, 427, 431 camerunensis (Bulinus) 242, 243(fig.), 309–10, 372, 394–5, 448, 484, 534 candida (Gabbiella) 88, 89(fig.), 520 canescens (Bulinus) 240(fig.), 241 capensis (Burnupia) 165(fig.), 166 capillacea (Bulinus forskalii) 237(fig.) capillata (Bellamya) 47(fig.), 146(map), 424, 476, 508, 523, 528, 535, 540 cara (?Pseudogibbula) 99, 540 carinata (Amerianna) 175, 176(fig.), 210(fig.), 515 carinata (Lantzia) 160, 517 carinatus (Lanistes) 19(fig.), 57, 58(fig.), 147, 347, 406, 475, 504, 542 carinifera (Syrnolopsis minuta) 131–2(fig.) carinulata (Cleopatra madagascariensis) 127 cariosa see Melanopsis praemorsa 144(fig.) carringtoni (Lentorbis) 190, 191(fig.) Cassidula 25–6, 153 catonis (Auriculastra radiolata) 153 cawstoni (Ferrissia) 173, 425 cawstoni (Tomichia) 78(fig.), 80 cecillei (Pila) 56(fig.), 516 Ceratophallus 26–7, 29(fig.), 180, 344; distribution 254(map), 505, 507–8, 512, 517–18, 520, 522–3, 525–6, 528, 531–4, 542, 544–5, 550; habitat 421–2, 433, 454, 460, 488 Cerithidea 23, 143, 343 Cerithium see obtusum cernicus (Bulinus) 243(fig.), 244, 309–10, 344, 373, 376, 517 charmetanti (Lanistes farleri) 65 chevalieri (Segmentorbis angustus) 190 choanomphala (Biomphalaria) 196(fig.), 198, 421, 532 choziensis (Bulinus globosus) 543 chudeaui (Afrogyrus coretus) 178

INDEX TO SNAIL NAMES 625

chudeaui (Ferrissia) 172 Chytra 142, 528–9 ciliatus (Lanistes) 58(fig.), 61 ciliatus (?Potamopyrgus) 74, 75(fig.), 76(fig.) clavulata (Bulinus forskalii) 237(fig.) Cleopatra, and see cara, dupuisi and species of Potadomoides, 6, 22, 25, 120, 129, 473–5; biomass and numbers 434, 476–7, 488; distribution 151(map), 424, 504, 508, 510, 516, 518, 520, 524–6, 528, 531–3, 535, 540–42, 545; habitat 421–2, 428–9, 450–1, 488, 535 clessiniana (Ferrissia) 170 clifdeni (Ferrissia) 173, 174(fig.) Clithon 17, 24, 43, 516 Cochliopinae 74 cockburni (Gyraulus) 188–9(fig.), 518 colbeaui (Cleopatra) 127–8(fig.) columella (Lymnaea) 7, 157, 158(fig.), 164(fig.), 341, 423–5, 435, 485, 504, 507–8, 513–14, 541–2 complanatus (Hippeutis) 188, 504 complanatus (Planorbis planorbis) 176 compressus (Ancylus fluviatilis) 161 concavus (Ceratophallus) 182, 184(fig.), 532 congener (Cleopatra bulimoides) 121 congicus (Lanistes) 58(fig.), 60, 426, 539 Congodoma 20, 91, 538–9 congoensis (Pila ovata) 54 congolensis (Septariellina) 21(fig.), 99, 539 conica (Pirenella) 23(fig.), 144(fig.), 145, 343 coniformis (Melampus) 155 connollyi (Ferrissia) 173, 174(fig.) connollyi (Gyraulus) 185, 186, 187(fig.), 189(fig.), 423–6, 507–8, 510–12 connollyi (Lanistes ovum) 63, 64(fig.) Conogabbia s–g. of Gabbiella 90 consimilis (Neritilia) 45, 516–18 consobrina (Melanoides nsendweensis) 106(fig.), 107 constricta (Bellamya) 50, 52(fig.), 532 contortus (Bulinus truncatus) 3, 233, 375 contracta (Bellamya) 52(fig.), 540

convexa (Cleopatra hemmingi) 126 convexiusculus (Gyraulus) 185 Coret, Le (Afrogyrus coretus) 2, 177 coretus (Afrogyrus) 2, 177(fig.), 181, 427, 451, 504–5, 508, 528, 533, 542 cornea (Planorbarius) 206 corneus (Bulinus tropicus) 229(fig.) 230 cornuarietis (Marisa) 65(fig.), 68, 405–6, 475 costulata (Bellamya) 47(fig.), 48, 532 costulatus (Gyraulus) 183, 185, 186, 187(fig.); distribution 424–5, 430, 507–08, 510– 11, 542; habitat 421–2, 425, 427, 430, 460, 465; in lakes 421–2, 523, 526, 528, 532–4 coulboisi (Bulinus truncatus) 221, 232(fig.), 233, 371 Coulboisia see Bridouxia 139 crassigranulata (Paramelania damoni) 140 crassilabrum (Afrogyrus) 178, 179(fig.), 516–17 crassistriata (Burnupia) 167(fig.), 168 crassus (Ceratophallus) 183, 184(fig.), 532 crawfordi (Melanoides victoriae) 110(fig.), 111 crawshayi (Bellamya) 49(fig.), 50, 525 crawshayi (Melanoides) 101(fig.), 102, 525 cridlandi (Cleopatra) 122(fig.), 123, 532 crista (Armiger) 26(fig.), 180, 180(fig.), 504, 542, 544 cristata (Neritina) 37(fig.), 41(fig.), 42 cristata (Valvata) 68 cristatus (Armiger crista) 180 crystallinus (Bulinus) 243(fig.), 244 Cyclostoma see bulimoides, carinatus (Lanistes), unicolor cyclostomoides (Cleopatra bulimoides) 121, 428 dageti (Soapitia) 20(fig.), 78(fig.), 94, 537 dagusiae (Bellamya costulata) 47(fig.), 48 dalloni (Afrogyrus coretus) 178 damarana (Lymnaea natalensis) 251(map) damoni (Paramelania) 135(fig.), 140, 529 dartevellei (Pseudocleopatra) 129, 130(fig.), 539

626 FRESHWATER SNAILS OF AFRICA

datura (Thiara) 101, 517 dautzenbergi (Bulinus forskalii) 236 dautzenbergi (Cleopatra ferruginea) 121 dautzenbergi (Martelia tanganyicensis) 133 decollata (Cerithidea) 23(fig.), 143, 144(fig.) densestriata (Bellamya monardi) 47(fig.), 48 depravata (Melanoides) 105, 106(fig.) depressa (Gabbiella) 89(fig.) depressus (Bulinus) 221(fig.), 222, 225, 313, 362, 363, 511 differens (Tomichia) 78(fig.), 79, 80(fig.) Drepanotrema 176 drouetiana (Brondelia) 163 dufouri (Melanopsis) 407 dufouri (Planorbarius metidjensis) 206 duponti (Bellamya unicolor) 46 duponti (Pseudogibbula) 21(fig.), 96(fig.), 99, 539 dupotetiana (Pseudamnicola) 70, 73(fig.) dupuisi (Melanoides) 105, 106(fig.) duryi (Helisoma) 26(fig.), 205, 207(fig.), 392, 406, 408–9, 437, 504, 508, 514, 517, 543 durbanica (Auriculastra radiolata) 153 duveyrieri (Hydrobia aponensis) 70, 74 dykei (Potadoma freethi) 114 eburnensis (Ferrissia) 173, 518 ecclesi (Bellamya) 51(fig.), 522–3 Edgaria see Lavigeria 134 edwardi (Gabbiella humerosa) 82 edwardiana (Burnupia) 168, 522 ehrenbergi (Gyraulus) 185, 187(fig.), 504– 5, 541–2 elata (Cleopatra) 122(fig.), 123, 124(fig.), 151(map), 508, 540 elatior (Bellamya unicolor) 46, 47(fig.) elatior (Lanistes ovum) 63 elegans (Biomphalaria choanomphala) 198, 520, 532 ellipticus (Lanistes) 63, 64(fig.), 508, 523 Ellobiidae 6, 7, 15, 23, 25, 152, 449, 548, 550 elmeteitensis (Lymnaea natalensis) 525

emicans (Segmentorbis angustus) 190 emini (Cleopatra bulimoides) 121 Endodontidae 188 equeefensis (Ferrissia burnupi) 173 Erinna 160 euchelius (Planorbarius metidjensis) 206 euphaeus (Hippeutis complanatus) 188 eussoensis (Segmentorbis) 192(fig.), 193(fig.), 504, 543 Euthyneura 14, 36 Eussoia 21, 25, 94, 97 exarata (Cleopatra) 122(fig.), 123 excavatus (Segmentorbis) 192, 194(fig.), 540 excentrica (Jubaia) 20(fig.), 25(fig.), 86(fig.), 90 exilis (Gyraulus costulatus) 186 expansilabrum (Sierraia) 92, 93(fig.) exserta (Lymnaea natalensis) 156 exsilium (Blauneria) 153 exustus (Indoplanorbis) 207(fig.), 208, 515, 518, 548 Fagotia 142 faint (?Ceratophallus) 183, 185(fig.) farleri (Lanistes) 64, 65(fig.), 518 farquhari (Burnupia) 165(fig.), 166 farquhari (Ferrissia) 173, 174(fig.) Ferrissia 25–6(fig.), 164(fig.), 169, 304, 421–2, 424–5, 427, 430, 447–8; aestivation 460–1; aphally 377, 477; distribution 504, 508, 512, 516, 518, 525, 528, 532–3, 540, 542, 546–8 ferruginea (Cleopatra) 22(fig.), 121, 122(fig.), 151(map), 424, 450, 488, 508, 518, 528 fischerianus (Bulinus scalaris) 239 fluminea (Melanatria) 113, 115(fig.), 149(map) fluviatilis (Ancylus) 26(fig.), 161, 162(fig.), 164(fig.), 171, 477, 502, 504, 542–3 fluviatilis (Theodoxus) 37(fig.) fontinalis (Ferrissia) 173, 174(fig.) fontinalis (Physa) 248

INDEX TO SNAIL NAMES 627

formosa (Segmentorbis kanisaensis) 193(fig.), 194 forskalii (Bulinus), see also forskalii group, 236, 237(fig.), 239, 241–2, 245, 264(map), 356, 372– 3, 403; aestivation 460; breeding system 376; distribution 264, 380, 424–5, 427, 430, 504, 508, 510, 516, 518–19, 543; growth and life cycle 479, 484; habitat 239, 242, 421–2, 425, 428–9; intermediate host, as 305, 309, 311–14, 316, 321–3, 344–5, 379; lakes, in 523, 526, 528, 533, 536; population fluctuations 431, 433, 487– 88 forskalii group (Bulinus), see also member species, 235, 305, 309, 314, 323, 345, 353, 356, 372–3, 379– 80, 432 fouladougouensis (Afrogyrus coretus) 178 freethi (Potadoma) 22(fig.), 114, 115(fig.), 149(map), 339, 426, 539 fulica (Achatina) 347 Funduella 19, 20, 91, 427, 538–9 fusca (Pachymelania) 22(fig.), 112, 113(fig.), 145 fuscatus (Tympanotonus) 144(fig.), 145 Gabbia see depressa, kichwambae, parva, senaariensis Gabbiella 6, 20, 25, 82, 421–2; distribution 148(map), 504, 510, 520– 4, 528–9, 531–2, 534, 537, 539–42, 545 gabonensis (Hydrobia) 71, 73(fig.) gagates (Neritina) 38(fig.), 40 Galba s–g. of Lymnaea 158 gardei (Gyraulus costulatus) 186 gangetica (Auriculodes) 153 gaudi (Biomphalaria pfeifferi) 195 gaulus (Burnupia caffra) 164 gaziensis (Auriculodes) 153, 154(fig.) germaini (Biomphalaria pfeifferi) 195, 257(map) gibbonsi (Afrogyrus coretus) 178, 525 giraudi (Anceya) 132(fig.), 528

giraudi (Bridouxia) 139 Giraudia see Bridouxia 139 glabra (Lymnaea) 160 glabrata (Biomphalaria) 204, 307, 324, 325, 400, 406, 461, 515 glabrata (Neritina) 17(fig.), 42, 44(fig.) globosa (Hirthia) 136, 138(fig.), 528 globosus (Bulinus) 212(fig.), 213, 214, 216, 218, 259(map), 359–60, 408; aestivation 375, 460–3; breeding system 376–7, 477; chemical factors, responses to 394, 466– 7, 450, 452–4; circadian rhythm 464; current speed, effect of 463–4; dispersal 436; distribution 259, 424, 427, 430, 508–9, 518, 521, 543; food 438; growth 478–80; habitat 210–11, 320, 374, 421–2, 430– 1, 434–5, 437; intermediate host, as 306, 308–9, 311– 12, 314–16, 318–20, 322–24, 344–5, 395; lakes, in 523, 525, 528, 532, 535–6; life cycle and population fluctuations 433, 482–3, 486–9, 491–4; temperature, responses to 455–459 globulus (Assiminea) 96 Goodrichia see Potadoma trochiformis 118 gordonensis (Burnupia) 162(fig.), 166 gracilior (Bellamya unicolor) 46 gracilis (Syrnolopsis) 131, 132(fig.), 528 gradata (Bulinus forskalii) 236 gradata (Pila ovata) 54, 55(fig.) grandidieri (Cleopatra) 127, 128(fig.) grandidierana (Bridouxia praeclara) 139 grandis (Lavigeria) 134, 135(fig.), 528 granulosa (Pachymelania fusca) 112 graptoconus (Potadoma freethi) 114 grasseti (Lanistes) 63, 64(fig.), 147, 516– 17 graueri (Lanistes) 65(fig.), 66, 528, 540 gravieri (Lymnaea natalensis) 156, 158(fig.) grayana (Assiminea) 96 gribinguensis (Lanistes nsendweensis) 60

628 FRESHWATER SNAILS OF AFRICA

guernei (Bulinus truncatus) 222, 232(fig.), 233, 371 guillemei (Cleopatra) 125(fig.), 126, 421– 2, 528, 532, 541–2 guillemei (?Tomichia) 81, 528 guinaicus (Lanistes varicus) 60 guineensis (Potadoma freethi) 114 Gundlachia 170, 447 and see burnupi, clifdeni, equeefensis, farquhari, l’hotellieri guyenoti (Hydrobia) 72, 72(fig.), 473, 537 Gyraulus, see also species of Afrogyrus and Ceratophallus, 27, 29(fig.), 177, 179, 180, 183, 185, 346; habitat and local occurrence 421–7, 430, 447, 460, 465; distribution 504–5, 507–8, 510–11, 517–19, 523, 526, 528, 531–34, 541–2, 548, 550–1

and see junodi (Lentorbis) hirta (Potadomoides) 130(fig.), 540 Hirthia 135, 528 Homorus 339 Horatia 70 horei (Reymondia) 137, 138(fig.) horei (Tiphobia) 141(fig.), 528–9 hovarum (Lymnaea natalensis) 156 Hovorbis s–g. of Afrogyrus 176 howesi (Bathanalia) 140, 141(fig.), 528 humerosa (Gabbiella) 76(fig.), 82, 83(fig.), 421, 520, 522, 528–9, 532, 542 Hydrobia, and see rogersi and tristis, 18, 70, 80, 427, 451, 502; 504, 519, 537, 539 Hydrobiidae 6, 7, 16, 18, 20, 69, 449, 473, 502, 538, 546–7 Hydrobiinae 70 Hydrocena 45 Hydrocenidae 45

Hadziella 14, 70 Haitia 248 hargeri (Cleopatra smithi) 125 Heideella 70 Heleobia 70, 74 Helisoma 7, 26(fig.), 27, 195, 205, 392, 406, 408, 437; distribution 504, 508, 514, 517, 541, 543, 548 Helix see amarula, ampullacea, cornea, planorbis, stagnalis, tentaculata, varicus Hemisinus 549, and see zenkeri hemmingi (Cleopatra) 125(fig.), 126 hemprichii (Bulinus truncatus) 219, 526 hendrickxi (Tomichia) 80(fig.), 81 hermanni (Biomphalaria pfeifferi) 195, 197, 257(map) hessei (Assiminea) 96, 97(fig.) hexaploidus (Bulinus) 222, 223(fig.), 356, 367–8, 378, 380, 543 hidalgoi (Paludinella) 95 hightoni (Bulinus) 217(fig.), 219, 260(map), 358 hildebrandti (Afrogyrus crassilabrum) 178 Hippeutis 188, 504, 518

ignobilis (Potadoma) 116(fig.), 117, 149(map), 427, 540 imbricatus (Armiger crista) 180 imitatrix (Melanoides mweruensis) 101(fig.), 525 Incertihydrobia 20, 25, 90, and see aethiopica (Jubaia), parvipila and verdcourti incisa (Funduella) 20(fig.), 89(fig.), 91, 427, 539 Indoplanorbis 7, 15, 23, 27, 208, 379, 515, 517–18, 548 inhambanica (Melanoides tuberculata) 109 inopina (Eussoia) 21(fig.), 25(fig.), 95(fig.), 96(fig.), 98 inops (Pila cecillei) 56(fig.), 57 intermedia (Marisa) 67 intortus (Lanistes) 59(fig.), 539 iridescens (Paramelania) 135(fig.), 140 Iravadiidae 548 Isidora s–g. of Bulinus 209, 219, 361, and see forskalii, guernei, jousseaumei, transversalis, trigonus isseli (Ferrissia) 170

INDEX TO SNAIL NAMES 629

jeffreysi (Bellamya) 51(fig.), 523 jenkinsi (Potamopyrgus) 74, 405–6 johnsoni (Melanatria fluminea) 113, 115(fig.) johnstoni (Cleopatra) 124, 125(fig.), 525 jordani (Theodoxus) 37(fig.), 39, 505 jouberti (Cleopatra guillemei) 126 jousseaumei (Bulinus) 212(fig.), 216, 310, 359, 464, 477–8, 537 Jubaia 20, 25, 90 jucunda (Bellamya) 48, 49(fig.), 421, 532 junodi (Ferrissia) 172(fig.), 173 junodi (Lentorbis) 189(fig.), 190, 191(fig.), 255(map), 421, 424, 460, 518, 520, 528, 532–3 kadeii (Potadoma) 119(fig.) kalingwisiensis (Bellamya capillata) 47(fig.), 48 kanisaensis (Segmentorbis) 190, 194, 193(fig.), 256(map), 421, 424, 427, 460, 508, 520, 528, 533, 543 kavirondica (Ferrissia) 171(fig.), 532 katanganus (Lanistes neavei) 60 kempi (Burnupia) 168, 169(fig.) kempi (Segmentorbis angustus) 190, 192 keniana (Assiminea) 96(fig.), 97 kichwambae (Gabbiella) 84, 83(fig.), 534, 542 kigeziensis (Ceratophallus) 182, 184(fig.), 532, 542 kimililoensis (Burnupia) 168 kinshassaensis (Melanoides) 106(fig.), 107, 539 kirki (Chytra) 141(fig.), 142, 528–9 kisalensis (Gabbiella) 83(fig.), 84, 148(map) kisangani (Melanoides) 107 kisumiensis (Bellamya jucunda) 48 kisumiensis (Ceratophallus) 182, 184(fig.), 421, 532 kivuensis (Gabbiella humerosa) 82 kivuensis (Tomichia) 80(fig.), 81, 428 knorri (Neritina pulligera) 40, 518 kobelti (Lanistes congicus) 60 kuramoensis (Neritina) 43 kyogae (Gabbiella humerosa) 82

labrella (Cassidula) 26(fig.), 154(fig.) lactea (Hydrobia) 70 lacustris (Acroloxus) 155 lacustris (Ferrissia) 173 lacustris (Syrnolopsis) 131, 132(fig.), 528 Laemodonta 152 laevis (Gyraulus) 185, 504, 519 lamyi (?Ceratophallus, see under Gyraulus connollyi) 186 langi (Cleopatra) 124, 151(map) langi (Melanoides) 107, 539, 540 Lanistes 6, 14, 15, 18, 19, 57, 339, 346–7, 390, 406–7; distribution 147(map), 504, 508, 510, 516–18, 520, 522–6, 528–9, 533, 537, 539–42, 550; habitat and local occurrence 424, 426, 430, 436, 445, 459–60, 464–5, 474–5 Lantzia 160, 517 latior (Potadoma liricincta) 116(fig.), 117 Lavigeria 112(fig.), 134, 473, 520, 527–30 Lechaptoisia see Bridouxia 139 Lentorbis 27, 188, 194, 421, 424, 427, 460; distribution 255(map), 508, 516, 518, 520, 528, 532–3, 542, 550 leonensis (Ferrissia) 172(fig.), 173 leonensis (Sierraia) 92, 93(fig.), 96(fig.) leopoldvillensis (Bellamya) 48, 52(fig.), 146, 539 leopoldvillensis (Pila wernei) 56 leptodonta (Eussoia) 96(fig.), 98 Leroya s–g. of Lanistes 64 leroyi (Thiara scabra) 102 lesnei (Paludomus) 124(fig.), 127 letourneuxi (Pila ovata) 54 leucochilus (Ceratophallus natalensis) 181 leucoraphe (Bridouxia giraudi) 138(fig.), 139 l’hotelleriei (Ferrissia) 170 liberiana (?Bellamya) 52(fig.), 53, 118 liberianus (Melampus) 154(fig.), 155 liberiensis (Potadoma) 116(fig.), 117, 149(map), 339, 537 libycus (Lanistes) 58(fig.), 60, 430, 465, 537 liebrechtsi (Melanoides) 107, 108(fig.), 539 Liminitesta 20, 91, 538–9

630 FRESHWATER SNAILS OF AFRICA

Limnotrochus 142, 528–9, see also kirki (Chytra) lineata (Hydrobia) 72(fig.), 537 lineata (Septaria borbonica) 45 lirata (Tomichia tristis) 77, 80(fig) liratus (Bulinus) 218, 221(fig.), 224, 344, 358, 361, 433, 451, 516 liratus synonym of Bulinus tropicus 224 liricincta (Potadoma) 116(fig.), 149(map), 540 Lithoglyphus 527 and see neritinoides, rufofilosa, zonata Littoraria 23(fig.), 69 littorina (Hirthia) 136, 528 Littorinidae 7, 16, 69 Littorinopsis s–g. of Littoraria 23(fig.), 69 Lobogenes 18, 20, 74, 538–40 longispina (Clithon) 24(fig.), 43, 44(fig) ludovicianus (Bulinus senegalensis) 241 luvilana (Hydrobia) 72(fig.), 73, 427, 539 Lymnaea 6, 7, 28(fig.), 156, 548; chemical factors, responses to 394, 445– 6, 451, 453; control 342–3, 390; distribution 251–2(maps), 502, 504–5, 507–8, 510–19, 522–3, 525–8, 532–3, 535, 541–2; intermediate host, as 340–5; habitat and local occurrence 421, 423– 5, 427, 429–30, 433–5, 437; physical factors and 455, 457–8, 460– 3; population fluctuations 488, 490; reproduction, growth and life cycle 477–8, 480–2, 485–6 Lymnaeidae 7, 14, 15, 24, 156, 518 madagascariensis (Biomphalaria pfeifferi) 195, 197 madagascariensis (Cleopatra) 127, 128(fig) madagascariensis (Melanatria) 114 madagascariensis (Pila cecillei) 56(fig.), 57 magnifica (Melanoides) 102, 108(fig.), 523 magnus (Lanistes ovum) 62

Mandahlbarthia see Bulinus 209, 219 manguensis (Melanoides) 108(fig.), 109, 537 manoeli (Neritilia) 17(fig.), 24(fig.), 44(fig.), 45 manzadica (Biomphalaria camerunensis) 201 mareoticus (Gyraulus ehrenbergi) 185 maresi (Theodoxus) 37 mariei (Bulinus forskalii) 236, 238, 245, 344 Marisa 7, 14, 15, 67, 405–6, 475, 515 marmorata (Physidae) 249 Martelia 133, 528–9 matadina (Gabbiella) 84, 88(fig.), 148(map), 539 mauritiana (Lymnaea) 156, 517 mauritianus (Gyraulus) 178, 188, 189(fig.), 517–8 mauritii (Valvatorbis) 21(fig.), 99, 539 Meladomus s–g. of Lanistes 62 Melampus 25–6, 97, 154, 155 Melanatria 6, 113, 149(map), 473, 516, 545 Melania 518, 523, 527–8 and see species in most genera of Thiaridae Melaniidae see Thiaridae Melanoides 6, 22, 25, 102, 340, 404, 406–7; distribution 502, 504–5, 508–10, 516, 518–20, 522–6, 528–9, 531–3, 535, 537–42, 546, 548–9; habitat and local occurrence 421, 424– 6, 428–30, 434, 450–1, 460, 464, 474, 475–7, 488 Melanopsidae 6, 7, 16, 142, 473 Melanopsis 22, 142, 406–7, 502, 504 meneliki (Bulinus abyssinicus) 214 Mercuria 70, 451 meridionalis (Theodoxus) 39 metidjensis (Planorbarius) 206, 207(fig.), 502, 504 michaelis (Lobogenes) 75(fig.) millestriatus (Lanistes varicus) 60 minima (Stormsia) 138(fig.), 139, 528–9 minor (Reymondia pyramidalis) 137, 138(fig.)

INDEX TO SNAIL NAMES 631

minuta (Syrnolopsis) 131, 132(fig.), 528 misellus (Afrogyrus coretus) 177(fig.) moerchi (Potadoma) 114, 115(fig.), 149(map), 430, 537 modesta (Ferrissia) 173, 516 monardi (Bellamya) 48, 51(fig.) 146 mooiensis (Burnupia) 166 morelli (Cleopatra nsendweensis) 125(fig.) mosambiquensis (Aplexa waterloti) 248(fig.), 250 mterizensis (Cleopatra smithi) 125 multisulcata (Mysorelloides) 134, 138(fig.), 528 mungwana (Potadoma ignobilis) 117 Murex see fusca, fuscatus musaensis (Hydrobia) 70, 71(fig.) mustelina (Cassidula) 155 mutandaensis (Bulinus truncatus) 232(fig.), 233 mutans (Pachymelania fusca) 112 mweruensis (Bellamya) 49(fig.), 50, 525 mweruensis (Cleopatra) 124, 125(fig.), 525 mweruensis (Lymnaea truncatula) 158 mweruensis (Melanoides) 101(fig.), 102, 525 Mysorella see Mysorelloides Mysorelloides 134, 528 nairobiensis (Biomphalaria pfeifferi) 195 nana (Burnupia) 165(fig.), 166 nassa (Lavigeria) 112(fig.), 134, 135(fig.), 528 nasutus (Bulinus) 210(fig.), 212(fig.), 213, 489; aestivation 460–3; chemical and physical factors, reponses to 453; distribution 260(map); growth and life cycle 480, 484; habitat 210, 399; intermediate host, as 310–11, 314, 399 nasutus (Lanistes) 62(fig.), 523–4 natalensis (Bulinus) 210(fig.), 220(fig.), 222, 224, 226(fig.), 229–30, 377; distribution 261(map), 508, 510–11, 518, 533–4, 543–4;

habitat and local occurrence 374, 377, 381, 395, 421–3, 424–5, 431, 437, 450; intermediate host, as 313–15, 324, 344– 5; taxonomic characters and species concept 355(fig.), 356, 360, 362–5, 367–8, 370–72 natalensis (Ceratophallus) 26(fig.), 177, 180, 181(fig.), 344, 421–2, 433, 460, 488; distribution 254(map), 507–8, 520, 523, 526, 528, 531–3, 542 natalensis (Ferrissia) 174 natalensis (Lymnaea) 6, 28(fig.), 156, 158(fig.), 164(fig.); chemical factors, responses to 394, 445– 6, 451, 453; distribution 251(map), 504, 507–8, 510, 512–13, 516–19, 522–3, 525–8, 532–3, 535 542; habitat and local occurrence 421, 424– 5, 427, 429–30, 433–5, 437; intermediate host, as 341–5; physical factors, responses to 455, 457– 8, 460–2; population fluctuations 488; reproduction, growth and life cycle 477, 480–1(fig.), 485 natalensis (Neritina) 17(fig.), 24(fig.), 38(fig.), 40, 518 natalensis (Tomichia) 76(fig.), 78(fig.), 79(fig.), 508 natalensis/tropicus complex (Bulinus), see also member species, 261, (map), 305, 355(fig.), 363, 364(fig.), 367, 534, 543 Nautilus see Armiger 179 neavei (Lanistes) 58(fig.), 60 Neothauma 6, 17, 18, 53, 522, 528 neothaumaeformis (Gabbiella) 84, 148, 521 Nerita 39 and see adansoniana, aurita, fluviatilis (Theodoxus), oweniana, pulligera, tuberculata Neritaea (Theodoxus) 36 Neritidae 6, 7, 15–17, 36–45, 449, 473 Neritilia 17, 24, 45, 516–18, 548

632 FRESHWATER SNAILS OF AFRICA

Neritina 17, 24, 37–8(figs), 39, 474, 508, 516, 518, 548, see also manoeli, maresi, meridionalis, niloticus, numidicus, rubida neritinoides (Stanleya) 135(fig.), 137, 528– 9 neritoides (Lanistes) 65(fig.), 66 neumanni (Gabbiella) 85, 88(fig.) nevillei (Auriculastra radiolata) 153 nilotica (Valvata) 24(fig.), 68, 69(fig.), 504–5, 533, 542 niloticus (Theodoxus) 38(fig.), 39, 504–5, 542 nimbae (Afropomus balanoidea) 66 nodicincta (Melanoides) 103, 104(fig.), 523 noticola (Hydrocena) 45 nsendweensis (Cleopatra) 25(fig.), 125(fig.), 151(map), 540 nsendweensis (Lanistes) 58(fig.), 60, 540 nsendweensis (Melanoides) 106(fig.), 107 nucleus (Cassidula mustelina) 155 numidicus (Theodoxus) 37, 38(fig.) nyangweensis (Bulinus scalaris) 239 nyangweensis (Melanoides) 106(fig.), 107 nyanzae (Ceratophallus kigeziensis) 182 nyanzae (Cleopatra guillemei) 126 nyanzae (Pila ovata) 54, 55(fig.) nyassana (Melanoides) 103, 104(fig.), 523 nyassanus (Bulinus) 221(fig.), 225, 379, 454, 477, 523–4 nyassanus (Lanistes) 61, 62(fig.), 436, 464, 474–5, 523–4 Nyassia see Melanoides magnifica 102 nyongensis (Potadoma) 118, 119(fig.) oasiensis (Afrogyrus coretus) 177(fig.), 505 oblonga (Eussoia) 97(fig.), 98(fig.) occidentalis (Pila) 54, 56(fig.) obscura (Cleopatra) 122(fig.), 123, 540 obtusata (Burnupia) 166, 169(fig.) obtusispira (Bulinus) 217(fig.), 218, 224, 259(map), 310, 358, 361, 380, 395, 433, 451, 460, 462, 516–17 obtusum (Cerithidea) 143 obtusus (Bulinus) 218(fig.), 260(map)

octoploidus (Bulinus) 223(fig.), 226, 309, 314, 344–5, 355–6, 367, 378, 380, 478, 543 olivaceus (Lanistes ovum) 62, 518 Omphalogabbia s–g. of Gabbiella 89 Omphalotropidinae 94 Oncomelania 77, 400 outambensis (Sierraia) 94, 93(fig.) ovata (Pila) 19(fig.), 54, 55(fig.), 57(fig.), 406, 421–2, 427–8, 454, 460; distribution 504, 508, 520, 525, 528, 532, 541–2 ovoideus (Bulinus africanus) 209 ovum (Lanistes) 62, 64(fig.), 76(fig.), 147(map), 424, 426, 430, 459–60; distribution 147(map), 508, 523, 526, 528–9, 540–2 oweniana (Neritina) 17(fig.), 37(fig.), 40, 41(fig.) Pachychilus 549 Pachymelania 21, 22, 111, 474, 548–9 pagodiformis (Bellamya) 49(fig.), 50, 525 pallaryi (Ferrissia) 170 Paludestrina (Hydrobia) 70 Paludina see colbeaui, constricta, cyclostomoides, leopoldvillensis (Bellamya), liberiana, madagascariensis (Cleopatra), senaariensis, zwellendamensis Paludinella 95 Paludomus 120, 124(fig.), 127, 517–18 palustris (Lymnaea) 159(fig.), 160, 504 palustris (Terebralia) 23 (fig.), 144(fig.), 145 Paramelania 139, 528–9 parenzani (Planorbis planorbis) 176 parietalis (Bulinus angolensis) 221 parva (Gabbiella) 84, 88(fig.), 542 parvipila (Gabbiella 83(fig.), 84 148(map) passargei (Bellamya capillata) 48, 146 Patella see borbonica (Septaria) paucicostata (Lavigeria) 134, 135(fig.) pauli (Cleopatra bulimoides) 121 pelecystoma (Ceratophallus) 183, 184(fig.), 520, 534

INDEX TO SNAIL NAMES 633

pelseneeri (Potadomoides) 129, 130(fig.), 528–9, 539–40 peraudieri (Hydrobia aponensis) 70 peregra (Lymnaea) 159(fig.), 160, 504, 526–7 pergracilis (Melanoides) 103, 108(fig.), 523 Peringia 30 permembranaceus (Bulinus) 227(fig.), 232(fig.), 309, 356, 357(fig.), 358, 369– 70, 378, 380–1, 543 Pettancylus s–g. of Ferrissia 170 pfeifferi (Biomphalaria) 195, 196(fig.), 201, 204; aestivation 460, 462; biomass, 495; chemical factors, responses to 445–49, 451–4; control 394, 398, 401, 408; current speed, effect of 464; dispersal 436; distribution 203, 257(map), 320, 427, 430, 504, 508–10, 512–13, 516, 523, 525–6, 528, 533–6, 543; food 437–8; growth 479–80; habitat 401, 421–2, 427, 429–30, 434– 5, 437, 464; intermediate host, as 307, 316, 318, 321, 324, 344, 395; life cycle and population fluctuations 433, 438, 464, 484–6, 489, 494–5; reproduction and growth 477–80, 494– 5; shade, effect of 464–5; temperature, responses to 455–59, 512– 13 philippi (Planorbis planorbis) 176 phthinotropis (Bellamya) 47(fig.), 48, 532 Physa 26, 28, 231, 248, 347, 352, 404, 406– 7; distribution 504–5, 507–8, 513–16, 525, 536, 541, 543; habitat and local occurrence 427, 430– 1, 436, 457–8, 465, and see carinata (Amerianna) and species of Bulinus Physella 248, 249

Physidae 7, 15, 24, 26, 28, 247, 518, 548 Physopsis (Bulinus) 209, 311, 358, 425–6, 435, 445, 455, 464, 483, and see Bulinus africanus group Pila 18, 19, 24, 54, 346–7, 406; distribution 504, 508, 510, 516, 520, 525–6, 528, 531–3, 537, 541–2, 548; habitat and local occurrence 421–2, 427, 430, 454, 460 Pilidae see Ampullariidae pilsbryi (Potadoma trochiformis) 118 pilula (Cleopatra) 124(fig.), 126, 151(map), 540 Pirenella 22, 23, 145, 343 pirothi (Cleopatra bulimoides) 121, 122(fig.) piscinalis (Valvata) 68 piscinarum (Gyraulus) 185, 505 planodiscus (Segmentorbis) 191, 193(fig.) Planorbarius 206, 304–5, 314, 502, 504 Planorbella 205, 206 Planorbidae 6, 7, 14, 26, 27, 152, 175, 453, 548–9 Planorbinae 7, 15, 23, 24, 27, 175 Planorbis 26, 27, 176, 177, 185, 502, 504– 5, 533, 541–2, 550–1, and see species in most other genera of Planorbinae planorbis (Planorbis) 26(fig.), 176, 179(fig.), 185, 502, 504–5, 533, 542 Platymelania 530 platyrhynchus (Ferrissia) 170 Plecotrema 152 plena (Hydrobia) 73(fig.), 539 Pleuroceridae 131 Plotia s–g. of Thiara 101, 102 polymorpha (Melanoides) 103, 104(fig.), 523 Pomatiopsidae 6, 7, 16, 18, 76, 449, 473, 507, 549–50 Ponsonbya see Bridouxia ponsonbyi (Bridouxia) 138(fig.), 139 ponsonbyi (Burnupia) 166, 167(fig.) ponthiervillensis (Potadoma) 116(fig.), 118, 540 Popel, Le (Tympanotonus fuscatus) 145

634 FRESHWATER SNAILS OF AFRICA

Potadoma 6, 22, 25, 114, 129, 149(map), 339, 426–7, 430, 473, 537–40, 544–6, 548–9, and see Melanoides agglutinans Potadomoides 22, 129, 473, 528–30, 538– 40, 549 Potamididae 6, 7, 16, 22, 143, 343, 449, 473, 548 Potamopyrgus 18, 74, 405–6, 548 praeclara (Bridouxia) 137, 138(fig.), 139 praeclara (Bulinus nasutus) 213 praemorsa (Melanopsis) 22(fig.), 143, 144(fig.), 406–7, 504 procerus (Lanistes ovum) 63 producta (Tomichia ventricosa) 77, 78(fig.) productus (Bulinus nasutus) 212(fig.), 213 Prosobranchia, prosobranch 6, 7, 10, 14– 23, 36–151, 379, 404; distribution 502, 510, 521, 523, 529–30, 541, 543–5, 549–50; habitat and local occurrence 438, 449– 50, 452, 454, 460, 473–77, 495 Pseudamnicola 70, 504 Pseudancylus see Ancylus 161 Pseudocleopatra 22, 25, 128, 537–9, 549 Pseudogibbula 21, 98, 474, 538–40 Pseudosuccinea s-g. of Lymnaea 157 psorica (Melanoides) 109, 110(fig.), 516 pulligera (Neritina) 17(fig.), 38(fig.), 39, 518, 548 Pulmonata, pulmonate 6, 7, 10, 14, 23–28, 152–264, 379, 404; distribution 523, 528, 535, 541, 543–5, 549–50; habitat and local occurrence 438, 453, 460, 477–495, 523, 528, 535, 541, 543– 5, 549–50 pupiformis (Melanoides) 103, 104(fig.), 523 purpureus (Lanistes) 19(fig.), 63, 64(fig.), 147, 518 pusilla (Lobogenes) 20(fig.), 75(fig.), 76 pyramidalis (Reymondia) 137 Pyrgophysa see Bulinus 236 and bavayi 245 Pythia 152

radiolata (Auriculastra) 26(fig.), 153, 154(fig.) Radix s–g. of Lymnaea 156, 160, 526 recticosta (Melanoides) 106(fig.), 109, 426 regulars (Ancylus) 161, 162(fig.), 164(fig.), 542–3 regular is (Ferrissia) 170 reticulatus (Bulinus), see also reticulatus group, 243(fig.), 246–7, 373–4, 432; aestivation 375, 460, 482; distribution 507–8, 512, 543; habitat 181, 421–2; intermediate host, as 314 reticulatus group (Bulinus), and see member species, 246, 353, 361, 373–4 Reymondia 137, 528–9 rheophila (Hydrobia) 73(fig.), 539 Rhinomelania see Potadoma zenkeri 118 rhodesiensis (Biomphalaria) 196(fig.), 198 ricei (Aplexa) 379 riperti (Potadoma) 119(fig.), 120 Rissoa 80 and see ponsonbyi (Bridouxia) robertsoni (Bellamya) 51(fig.), 52, 523 rodriguezensis (Afrogyrus) 177(fig.), 178, 517 rogersi (Tomichia) 78, 79(fig.) rohlfsi (Bulinus truncatus) 228, 233, 308, 321, 322, 371, 374, 394, 396, 427, 430, 436, 461, 479, 484, 490, 535 rosea (Gabbiella) 86(fig.), 88, 148(map), 531 rotundata (Bridouxia) 139 ruandensis (?Ferrissia) 172(fig.) rubicunda (Bellamya) 49(fig.), 50, 520 rubida (Neritilia) 45 rubricata (Neritina) 41 (fig.), 42 rufocincta (Anceya giraudi) 132(fig.) rufofilosa (Tanganyika) 135(fig.), 136, 528–9 rugosa (Biomphalaria sudanica) 203 rugosa (Cleopatra) 124(fig.), 126, 151(map) rumrutiensis (Bulinus tropicus) 229(fig.), 230, 370(fig.) rüppelli, rueppelli (Biomphalaria pfeifferi) 195, 526

INDEX TO SNAIL NAMES 635

salinarum (Biomphalaria) 202(fig.), 203, 258(map) sambesiensis (Bellamya monardi) 48 sanagaensis (Lanistes libycus) 61 sancti-pauli (Potadoma liberiensis) 117, 339 saulcyi (Valvata) 68, 505 Saulea 18, 19, 66, 406, 431, 537–8, 549 scabra (Littoraria) 69 scabra (Thiara) 22(fig.), 100, 101(fig.), 474, 516–18, 548 scalaris (Bulinus) 239, 240(fig.), 241, 305, 313, 421–2, 460, 543 schackoi (Bulinus truncatus) 366 schmidti (Bulinus forskalii) 237(fig.) schoutedeni (Hydrobia) 72(fig.), 74, 539 schoutedeni (Potadoma) 114, 115(fig.) schoutedeni (Potadomoides) 130, 540 schweinfurthi (Gabbiella) 87, 541–2 scioana (Valvata nilotica) 68 sclateri (Melanoides tuberculata) 111 Segmentina 188 see also angustus, chevalieri, emicans, eussoensis, formosa, kanisaensis, kempi Segmentorbis, see also carringtoni (Lentorbis), 26, 27, 183, 190, 421, 424, 427, 430, 460; distribution 256(map), 504, 508, 510, 516, 520, 523, 528, 531–3, 539–40, 543–4, 550 semiaratus (Melampus) 26(fig.), 154(fig.), 155 semiplicatus (Bulinus forskalii) 237(fig.) Semisinus see zenkeri 118 semisulcatus (Melampus semiaratus) 155 senaariensis (Gabbiella) 86(fig.), 148(map), 504, 542 senegalensis (Bulinus) 2, 209, 216, 237–8, 241, 243(fig.); aestivation 375, 460–61, 463; control, 395–6, 400; distribution 380, 537; growth and life cycle 482, 484, 487; habitat and local occurrence 448, 453, 460–1; intermediate host, as 309–10, 314, 319, 344–5, 352, 372–3, 375, 379;

taxonomy and species concept 352, 372–3 senegalensis (Cleopatra bulimoides) 121, 122(fig.) Septaria 14–17, 24, 43, 508, 516, 548 Septariellina 14, 15, 21, 99, 474, 538–9 sericinus (Bulinus truncatus) 227, 234, 365–6, 368, 526 Sierraia 15, 19, 92, 445, 448, 451–2, 463, 473–4, 537–8, 549 Siphonariidae 163 simonsi (Melanoides nodicincta) 103 smithi (Biomphalaria) 195, 198, 199(fig.), 522 smithi (Cleopatra) 124, 125(fig.) smithiana (Bridouxia) 139 Soapitia 14, 16, 19, 20, 94, 537, 549 socotrensis ( ?Ceratophallus) 183, 185(fig.), 188, 518 soleilleti (Bulinus abyssinicus) 214 solidus (Lanistes) 61, 62(fig.), 523–4 soror (Melanoides nsendweensis) 106(fig.), 107 speciosa (Pila) 55, 56(fig.) Spekia 112(fig.), 136, 137, 473, 527–9 sperabilis (Ceratophallus natalensis) 181 spiralis (Gabbiella) 85, 88(fig.), 539 spiralis (Lobogenes) 75(fig.), 76 spirorbis (Anisus) 188 spoliata (Potadoma ponthiervillensis) 116(fig.), 118 stagnalis (Lymnaea) 159(fig.), 160, 502, 504–5, 542 Stagnicola s–g. of Lymnaea 160 Stanleya 136, 528–9 stanleyi (Biomphalaria) 198, 199(fig.), 520 stanleyi (Gabbiella) 83(fig.), 85, 148(map), 523–4 starmuehlneri (Afrogyrus) 178, 180(fig.), 183, 516 stenochorias (Burnupia) 166, 167(fig.) Stenophysa see waterloti 249 Stenothyridae 548 Stormsia 139, 528–9 straeleni (Bathanalia) 140, 528 Streptoneura 14, 36 striatella (Homorus) 339 striatissima (Burnupia capensis) 166

636 FRESHWATER SNAILS OF AFRICA

strigosa (Bulinus trigonus) 229 Strombus see byronensis stuhlmanni (Burnupia) 167(fig.), 168, 532 stuhlmanni (Lanistes) 59(fig.), 65(fig.) subangulatus (Planorbis planorbis) 176 subbadiella (Gabbiella adspersa) 87 subopaca (Physa) 248, 249 subtilis (Ceratophallus) 182, 184(fig.), 186, 532 subtruncatula (Lymnaea truncatula) 158, 252(map) subula (Auriculastra) 152, 153 Succinea 28(fig.) succinea (Neritilia) 45 Succineidae 14, 24 succinoides (Bulinus) 221(fig.), 228, 379, 523–4 sudanica (Biomphalaria) 202(fig.), 203, 258(map), 392; aestivation 460, 462; distribution 258, 520, 528, 532–3, 540, 543; habitat 421–2, 427, 454; intermediate host, as 316; population fluctuations 433 sulcata (Liminitesta) 20(fig.), 92, 96(fig.), 539 superba (Potadoma ponthiervillensis) 118 Syrnolopsis 131, 528–9 tanganyicense (Neothauma) 18(fig.), 49(fig.), 53, 528 tanganyicensis (Biomphalaria sudanica) 202(fig.), 204 tanganyicensis (Ferrissia) 172(fig.), 528 tanganyicensis (Gabbiella humerosa) 82 tanganyicensis (Melanoides polymorpha) 103, 104(fig.), 528 tanganyicensis (Martelia) 133(fig.), 528–9 tanganyicensis (Reymondia) 137, 138(fig.) Tanganyicia 136, 528–9 tanschaurica (Paludomus) 124(fig.), 127 tchadiensis (Biomphalaria) 201, 521 tchadiensis (Gabbiella) 83(fig.), 85, 148, 521 teesdalei (Incertihydrobia) 25(fig.), 86(fig.), 90

Telescopium telescopium 23, 145 tentaculata (Bithynia) 82, 83(fig.), 504 tenuis (Ferrissia) 170 Terebralia 23, 145 terebriformis (Anceya) 132(fig.), 133, 528 tessellaria (Septaria borbonica) 45 tetragonostoma (Biomphalaria sudanica) 204 Theodoxus 17, 36, 502, 504–5, 526–7, 541–2 Thiara 21–2, 100, 474, 508, 516–18, 548– 9 Thiaridae 6, 7, 16, 21, 100, 449, 473, 530, 548–9 thomsoni (Limnotrochus) 141(fig.), 142, 528–9 tiassalensis (Neritina) 37(fig.), 41(fig.), 42 tigrina (Potadoma freethi) 114, 115(fig.) tilhoi (Afrogyrus coretus) 178 tilhoi (Gabbiella senaariensis) 87, 148(map) tilhoi (Valvata) 68, 545 Tiphobia 141, 528–9, see also damoni, nassa togoensis (Potadoma) 116(fig.), 149(map), 537 togoensis (Pseudocleopatra) 25(fig.), 128(fig.), 537 Tomichia 18, 77, 428, 450, 452, 461, 474– 5, 507–8, 511, 528, 531, 545–6, 550 tornata (Potadoma liricincta) 116(fig.), 117 toroensis (Bulinus tropicus) 229(fig.), 230, 534 toroensis (Ferrissia) 171(fig.) toukotoensis (Afrogyrus coretus) 178 tournieri (Gabbiella africana) 87, 88(fig.) trabonjiensis (Cleopatra madagascariensis) 127, 128(fig.) transvaalensis (Burnupia) 166, 167(fig.) transversalis (Bulinus) 228, 232(fig.), 370, 421, 532 trapezoidea (Burnupia) 166, 169(fig.), 253(map) Triculinae 77 trigonus (Bulinus) 228, 232(fig.), 370, 421– 2, 532

INDEX TO SNAIL NAMES 637

tristis (Tomichia) 77, 78(fig.), 80(fig.) trisulcata (Bellamya trochlearis) 50 trivialis (Afrogyrus crassilabrum) 179 trochiformis (Potadoma) 118, 119(fig.) trochlearis (Bellamya) 18(fig.), 24(fig.), 49(fig.), 50, 532 tropicus (Bulinus), see also tropicus group, 220(fig.), 222, 225, 229(fig.), 261, (map); aestivation 460–1; chemical and physical factors, responses to 450, 455, 457–8; distribution 261(map), 356, 424, 507– 8, 511–13, 525, 534–5; growth, life cycle and population fluctuations 375, 480–1(fig.), 482, 484, 488, 490; habitat and local occurrence 228, 361– 71, 434–5, 488; intermediate host, as 309, 313–316, 324–5, 344–5, 378; taxonomic characters and species concept 355(fig.), 357(fig.), 361–71, 381 tropicus group (Bulinus) 219, 353, 361–2 Truncatella see ventricosa 77 truncatelliformis (Melanoides nyassana) 103, 523 truncatula (Lymnaea) 158(fig.), 160; distribution 252(map), 504–5, 507–8, 510–12, 542, 545; habitat and life cycle 423–4, 460, 462, 482, 485–6, 490; intermediate host, as 341–4 truncatus (Bulinus), see also truncatus/tropicus complex and truncatus group, 175–6(fig.), 218, 221–3(figs), 229–30, 231, 232(fig.); aestivation 460–2; biochemical features 356–58; breeding system 375–7; chemical factors, responses to 394, 450– 3; control of 394–6, 399–400, 403–5, 407– 8; distribution 262–3(map), 502, 504–5, 520, 526, 528, 531, 533, 535–6, 543; evolution 380–1;

growth and life cycle 479, 482–4, 489– 91; habitat and local distribution 228, 374, 421–2, 427–8, 430, 436–7; intermediate host, as 3, 308–11, 313– 16, 319–23, 344–5, 378–9; population fluctuations 489–91; species concept 360–2, 365–72, 374; tetraploidy 356, 375, 377–8, 380–1 truncatus group (Bulinus) 219, 323, 353, 361–2 truncatus/tropicus complex (Bulinus), and see member species, 219, 309, 314–15, 353, 356–7, 361–73, 378–81, 518, 551 Turbonilla see Anceya 133 tuberculata (Melanoides) 22(fig.), 102, 109, 110(fig.), 112(fig.); biomass and numbers 475–7, 488; as competitor of other snails 406–7; distribution 150(map), 502, 504–5, 508–9, 516, 518–20, 522–3, 528, 531– 3, 535, 541–2, 548; habitat and local occurrence 421, 424– 5, 428–30, 434, 451, 460, 464; intermediate host, as 340; predation by fish 404; reproduction, growth and life cycle 474–5; salinity tolerance 451, 505 turriculata (Bulinus forskalii) 237(fig.) turrita (Neritina) 40 turritispira (Melanoides) 103, 104(fig.), 523 turtoni (‘Ancylus’) 14, 163, 165(fig.) Tympanotonus 23, 143 ugandae (Bellamya costulata) 47(fig.), 48 ugandae (Bulinus) 212(fig.), 216, 228, 233, 259(map), 314, 360, 421–2, 433, 532–3, 543 ugandae (Gabbiella senaariensis) 86 umbilicatus (Bulinus) 217(fig.), 218, 260(map), 310, 316, 358–61, 461, 543 umlaasiana (Lymnaea truncatula) 158 unicolor (Bellamya) 18(fig.), 46, 47(fig.), 146(map), 421, 428–9, 434, 450, 474–6, 504, 526, 532–3, 542

638 FRESHWATER SNAILS OF AFRICA

Valvata 7, 24, 36, 68, 504–5, 526, 533, 541–3, 545 Valvatidae 16, 68, 473 Valvatorbis 21, 99, 538–9 varicus (Lanistes) 58(fig.), 60, 147, 537 ventricosa (Tomichia) 77, 78(fig.), 79(fig.), 461, 474 ventrosa (Hydrobia) 70, 71(fig.), 519 verdcourti (Gabbiella) 83(fig.), 85, 148(map) verreauxi (Burnupia) 164, 168 vicinus (?Ferrissia) 171(fig.), 172 victoriae (Melanoides) 110(fig.), 111, 112(fig.), 424–5, 508 victoriensis (Ferrissia) 174(fig.) vitraea (Bulinus forskalii) 236, 237(fig.) vitrea (Saulea) 19(fig.), 67(fig.), 406–7, 431, 537–8 Vivipara see Viviparus Viviparidae 6, 7, 16, 17, 46, 473, 549 Viviparus and Vivipara 46, and see bridouxiana and brincatiana (Cleopatra guillemei) and species under Bellamya vogeli (Potadoma) 25(fig.), 115(fig.), 116, 149(map), 537 voltae (Melanoides) 106(fig.), 111, 537 voltana (Pseudocleopatra) 128(fig.), 129, 537 vouamica (Thiara amarula) 100, 518 vulcanus (Burnupia) 168 wagenia (Melanoides) 108(fig.) wahlbergi (Bulinus forskalii) 236 walkeri (Burnupia) 168 walleri (Gabbiella) 76(fig.), 86(fig.), 90, 520 wansoni (Biomphalaria camerunensis) 201 wansoni (Potadoma) 117, 120(fig.), 539 waterloti (Aplexa) 28(fig.), 248(fig.), 249, 430, 465, 508, 537 wautieri (Ferrissia ?clessiniana) 170 welwitschi (Bulinus angolensis) 220, 221 (fig.) welwitschi (Cleopatra nsendweensis) 125 wernei (Pila) 24(fig.), 56(fig.), 57(fig.), 427, 430, 541–2

whitei (Sierraia) 93(fig.), 94 Williamia 163 woodwardi (Melanoides turritispira) 103, 104(fig.) wrighti (Bulinus) 243(fig.), 246, 310, 316, 323, 374, 543 yemenensis (Bulinus) 235, 358 zairensis (Congodoma) 20(fig.), 91, 97(fig.), 539 zambesiensis (Ferrissia) 174(fig.) zambiensis (Ferrissia) 174 zambiensis (Melanoides langi) 107 zambica (Gabbiella) 87, 148(map), 540 zanguebarensis (Cleopatra ferruginea) 121 zanzebaricus (Bulinus tropicus) 230 zengana (Melanoides tuberculata) 111 zenkeri (Potadoma) 118, 119(fig.) zonata (Spekia) 112(fig.), 135(fig.), 136, 528–9 zuluensis (Bulinus natalensis) 224, 226(fig.), 355(fig.), 363 zwellendamensis (Tomichia) 77, 79(fig.)

Index to other organism names

Plants and animals other than snails, and including bivalve molluscs. These are mostly organisms assigned to a genus or species. See the Subject Index for common names (e.g. baboon, buffalo) and general categories (e.g. cattle, insects, plants). Algae, blue-green 75, 438; diatoms 495, and see Chlorella and Spirodela Alboglossiphonia polypompholyx 404 Alternanthera 430, 437; sessilis 393 Amphibians 507, 512, and see Rana Amphistome see Calicophoron, Carmyerius, Cotylophoron, Paramphistomum, Stephanopharynx Anas querquedula 242 Anastomus lamelligerus 403 Angiostrongylus 338; cantonensis 59, 346 Astatoreochromis alluaudi 403–4 Atilax paludinosus 339 Azolla 453

parvipapillatus 344 Carp, Grass see Ctenopharyngodon Ceratophyllum 84, 85, 234, 429, 436–7, 491; demersum 396–7, 535 Chlorella 438 Cichlidae 403, and see Astatoreochromis, Saratherodon, Trematocranus Civet Cat see Viverra Commelina 430, 437 Cotylophoron 344 Coypu see Myocastor Crab, freshwater see Liberonautes, Sudanautes Crayfish see Cambarus, Procambarus Crossarchus obscurus 339 Crustacea 404 Ctenopharyngodon idella 401 Cyperus 437; exaltatus 437, 464

Birds see Anas, Anastomus, Tringa Bivalve 403, 434, 476, 477, 512, and see Etheria, Pisidium, Teredo Belostomatidae see Limnogeton 404

Digenea 338–46

Calicophoron 338, 344–5; microbothrium 224, 231, 235, 238, 242, 325, 344–5 Carmyerius 334; dollfusi, 344; exoporus 344; mancupatus 344;

Echinoparyphium 378 Echinostoma, echinostome 185, 197, 213, 228, 231, 235, 238, 246, 338, 346; caproni 242, 346; ilocanum 346; liei 200, 249, 346; revolutum 200, 242, 346; 639

640 FRESHWATER SNAILS OF AFRICA

togoensis 346 Echinostomatidae 338, 402 Eichhornia 87, 186, 204 Etheria 131 Fasciola 157, 340–43, 513; gigantica 340–42; hepatica 157, 159, 340–42; nyanzae 340–41; tragelaphi 340 Fasciolidae 338 Fish see Astatoreochromis, Ctenopharyngodon, Gambusia, Mugilidae, Saratherodon, Trematocranus Gambusia affinis 403 Garganey Duck see Anas Gastrodiscus 338; aegyptiacus 238, 345 Glossiphoniidae 404 Helobdella conifera 404 Heterophyes 338; heterophyes 145, 343 Hemiptera see Limnogeton Heterophyidae 338 Insects, aquatic see Lampyridae, Limnogeton Odonata, Sciomyzidae, Sepedon Jussiaea repens 74 Kobus; leche 313, 344; vardoni 313 Lampyridae 404 Lechwe see Kobus leche Leech see Alboglossiphonia, Glossiphoniidae, Helobdella Leersia 453 Lemna 81, 437 Liberonautes 339 Limnogeton fieberi 404

Louisiana Red Swamp Crayfish see Procambarus Ludwigia 454 Metastrongylidae 338 Mongoose see Atilax, Crossarchus Mugilidae 343 Mullet see Mugilidae Myocastor coypus 525 Najas 536 Nematoda 338, 346 Nymphaea 60, 429, 437, 453, 490 Odonata 404 Oligochaete worms 476 Open-billed Stork see Anastomus Ostracoda, ostracods 404, 531 Paragonimidae 338 Paragonimus 114, 338–40; africanus 339; kelicotti 340; uterobilateralis 339–40; westermanni 338 Paramphistomum, paramphistome 197, 378; daubneyi 344; phillerouxi 245, 344; sukari 197, 198, 344; togolense 344 Paramphistomatidae 338 Paspalum 437 Phytolacca dodecandra (Endod) 393 Pisidium 447; viridarium 512 Pistia 436, 453, 536 Poikilorchis congolensis 339 Polygonum 396, 491, 535 Potamogeton 368, 437, 536; thunbergi 437 Procambarus clarkii 403, 404–5, 525 Puku see Kobus vardoni Rana 346 Rattus norvegicus 347

641

Salvinia 436–7, 453, 535; molesta 525 Sandpiper, Wood see Tringa Saratherodon 403 Schistosoma, schistosome 208, 303–325, 484–5, 510; bovis 206, 211, 213, 215, 218–19, 225, 227, 231, 235, 238–9, 242, 244–7, 305, 313–16, 324–5; capense (haematobium) 308–9; curassoni 216, 219, 242, 244, 247, 305, 316; edwardiense 203, 305; haematobium 170, 209, 211, 213–19, 222, 224–5, 227, 231, 235, 238, 242, 245–47, 303–06, 308–12, 315, 318–22; 323–4, 352–3, 406, 536 hippopotami 305; intercalatum 211, 216, 219, 238, 241–2, 244–7, 305, 311–13, 320–3; leiperi 211, 216, 219, 247, 305, 313; mansoni 195, 197–8, 200–01, 203–04, 303, 305, 307–8, 318, 320–1, 325, 484– 5, 515; margrebowiei 227, 231, 235, 238, 241, 247, 304–5, 313; mattheei 211, 216, 222, 246–7, 305, 313, 315–16, 322; rhodaini 197, 204, 305, 316–17; rodentorum (mansoni) 307 Sciomyzidae 404 Sepedon scapula 404 Shipworms see Teredo Sitatunga see Tragelaphus spekei Spirodela 436 Stephanopharynx compactus 344 Sudanautes 339 Swartzia madagascariensis 393 Teredo 74 Tragelaphus spekei 313, 340 Tetrapleura tetraptera 393 Trematocranus placodon 403 Trematoda, trematode 157, 181, 198, 204, 216, 217, 239, 338–346, 378–9, 402, 480, 491 Tringa glareola 242

Typha latifolia 437 Unionicola macani 63 Vallisneria 42, 85, 112, 228, 523–4 Viverra civetta 339 Vossia cuspidata 462, 521 Warburgia salutaris 393 Water-bug, Giant see Limnogeton Water Hyacinth see Eichhornia Water-lily see Nymphaea Water-mite see Unionicola Wood Sandpiper see Tringa

Subject index

See also preceding indexes of Snails Names and Other Organism Names. Further information about Habitat, Distribution and Parasites may be found under the main entries for genera and species in the Systematic Synopsis. This index does not include all entries in the Glossary (Chapter 2) or the citations of localities in the legends to figures of shells. Abbreviations 8, 9 Aberdare Range see Mountains Abgoville (Ivory Coast) 116 Abu Duloh (Sudan) 218–19, 360 Abu Simbel (Egypt) 200 Abyssinia see also Ethiopia 1, 98, 195, 214, 366 Academy of Natural Sciences, Philadelphia 99 Accra (Ghana) 55, 71, 150 Ad-Duwem (Sudan) 147 Ada (Ghana) 71, 155 Adanson, Michel 2, 352 Addis Ababa (Ethiopia) 222–3, 227, 368, 431, 543 Aden, Aden Protectorate see Yemen, South Adolla (Ethiopia) 253 Adowa (Ethiopia) or Adua or Adwa 393 Adzope (Ivory Coast) 109 Aestivation behaviour 459–63, 484, 492 Bulinus 374–5 definition 375, 459 extended periods 218–19, 242, 245, 342, 459–60 fascioliasis transmission interrupted 342 feeding after 438 life expectancy of snails 375 schistosome infection carried over 375

shell modified for 169, 460–1 water-quitting 459 Afar Depression (Ethiopia) 379 Africa checklist of species 29–34 composition of snail fauna summarised 6–7 numbers of species in relation to latitude 546–7 Afrotropical Region 1, 4, 6, 310, 364, 423, 544–5 snail fauna 319, 341, 359, 362–4(fig.), 371–2, 375, 424, 459, 502, 504–5, 507– 10, 517–18, 543–7, 548–51 south-east tropical corridor 362–3, 507– 8 Agadir (Morocco) 252 Agglutinating substances 324 Agherrar (Somalia) 126, 151 Agueraktem (Mauritania) 251 Agulhas (South Africa) 77 Ahaggar (Algeria) 161, 252, 263 Ahero (Kenya) 422 Ain Khadra (Algeria) 37 Air (Niger) 257, 263, 264, 505 Akaki (Ethiopia) 68 Akwamu (Ghana) 128 Albert/Edward Basin 53, 530 Albertville (Zaire) see Kaliemé Albinism see Genetic markers 642

SUBJECT INDEX 643

Aldabra Islands 245, 517 Alexandria (Egypt) 46, 54, 57, 68, 121, 170, 200 Algae 228, 428, 438, 454, 461, 488–90, 523, 529, 531 diatoms 437, 486, 495 Algarve (Portugal) 263 Algeria prosobranchs 37, 39, 68, 70, 82, 111, 143, 150, 407 pulmonates 159–61, 163, 170, 176, 180, 185–6, 188, 191, 195, 197, 206, 234, 252, 262–3 snail control 407, 409 snails living in south-eastern refuges 502, 504, 505 Allozyme see Enzymes Altitude, related to snail distribution East Africa 368–9 South Africa 363–4, 424–5 (table), 426, 458–9, 507–12 Ambo (Ethiopia) 368 America North 68, 157, 160, 205, 549 South 68, 74, 307, 461, 549–50 Ammonia, excretion of 231 Amphibians 378, 392, 507, 512 Amphibious life of snails, see also Aestivation prosobranchs 66, 78–9, 95 pulmonates 152, 341 Amphistome, see also Paramphistomiasis 325, 344 Anatomy of snails, prosobranch 46, 53, 57, 66, 69, 127 pulmonate, 28(fig.), 29(fig.), 175–7, 179–80, 185, 194, 204–6, 208–9, 247–8 Andaman Islands 548 Anefid (Algeria) 263 Angiostrongyliasis 338, 346–7 Ango-Ango (Zaire) 73, 99 Angola, prosobranchs 42, 43, 48, 54, 59– 60, 63, 84, 108–9, 113, 125, 145–8, 151 pulmonates 163, 177, 186, 190, 194, 197, 203, 214, 220–21, 236, 239, 241, 244, 253, 257–8, 264, 359, 372, 460 schistosomiasis and host snails 233, 244, 310

Anhydrobiosis see Aestivation Anjouan Island see Comoro Islands Ankasatasa (Madagascar) 147 Anseba (Ethiopia) 87 Antelope 305, 313, 315, 340 Antisirabe district (Madagascar) 178 Apaso (Ghana) 111, 116, 128–9 Aphallic condition, Aphally Bulinus 220, 222, 224, 228–9, 231, 233, 355, 361–3, 366, 371, 376–7, 381, 408, 477 environmental determination 377 Ferrissia 169, 477 Lentorbis 190 partial aphally 377 Arabia definition 9 prosobranchs 111, 120, 142, 145, 150– 1 pulmonates 156–7, 159, 161, 197, 208, 234, 244, 247, 249, 263, 373–4, 377–8, 543 Arba Minch (Ethiopia) 533 (table) Arid regions, and snail distribution, see also Sahara 321, 503, 505, 506, 550 Arua (Uganda) 211 Arusha, Arusha Chini (Tanzania) 204–5, 258, 398 Asia, parasites 338, 346 prosobranchs 46, 54, 68, 74, 82, 100, 102, 111, 127–8, 548–50, pulmonates 160, 170, 176, 180, 185, 208, 341, 515, 517–18, 548–50 snail fauna compared with Africa 548– 50 Asmara (Ethiopia) 87, 190, 197, 254, 257, 366 Asni (Morocco) 252 Assaita (Ethiopia) 200, 214, 251, 257 Associations among snail species 434–5 Aswan (Egypt) 200, 320 Asyut (Egypt) 186 Atar (Mauritania) 263 Athi Plains (Kenya) 126 Aulaqui District (South Yemen) 247 Australia, 63, 74, 152, 170, 175, 341, 550 Awasi (Kenya) 90

644 FRESHWATER SNAILS OF AFRICA

Azores, islands 519 Baboon 307 Bacteria 437, 454 Baga Kawa (Lake Chad) 429, 476 Bagamoyo (Tanzania) 54, 61, 98, 213 Bahr al Ghazal (Sudan) 203 Bahr Dahr (Ethiopia) 526 Bakossi (Cameroon) 339 Balakuna (Ghana) 11 Balovale (Zambia) 88 Bamako (Mali) 431 Banana (Zaire) 59, 74, 96, 155 Bandar Anzali (Iran) 263 Bandiagara (Mali) 257, 260 Bangweulu-Luapula area (Zaire) 445–6 Banzyville (Zaire) 105, 181, 201, 258 Bardera (Somalia) 126, 147 Basibasy (Madagascar) 261 Basommatophora African fauna summarised 6–7 checklist of species 33–4 keys to families and genera 23–8 systematic synopsis 152–302 taxon 9, 152 Basutoland see Lesotho Batkan (Sierra Leone) 92 Bator (Ghana) 42 Bavia (Liberia) 53, 117, 118 BayluscideR see Niclosamide Beaufort West (South Africa) 252 Bechuanaland see Botswana Beetle (Coleoptera) 404 Begour Crater (Chad) 251 Beheira district (Egypt) 252 Bekong Bogs (Lesotho) 231 Beles Cogani (Somalia) 126 Belgian Congo, see Zaire, Belgian Hydrobiological Survey of the Bangweulu-Luapula Basin 524 Bengou (Niger) 148 Benguela (Angola) 113, 190, 239, 255 Beni Suef (Egypt) 148 Benin (formerly Dahomey) 72, 115, 249– 50, 320 Bibundi (Cameroon) 45 Bilala stream (Zaire) 428, 485, 495

Bilharziasis see Schistosomiasis Bingerville (Ivory Coast) 72, 173 Biochemical studies see Enzymes, Molecular analysis, Mucus and Proteins Biogeography, see also Dispersal, Distribution, and Faunas of snails faunal classification in southern Africa 507 general 544–51 Biomass 433–4, 475–7, 495, 531, 535 Biotope Biomphalaria 428 definition 420 diversity in lakes 432, 529–30 types in western Kenya 421–2(table), 432–3(table) Biotypes, of Bulinus 233, 358, 371, 378 Bipindi (Cameroon) 118 Bir Natrun (Sudan) 150 Birds 158–9, 242, 343, 346, 403, 423, 435– 7, 517 Birket Qarun (Egypt) 70, 145 Bishoftu see Debra Zeit and Crater lakes Bivalve molluscs 422, 429, 433–4, 476, 502, 512, 524 Blantyre (Malawi) 263 Blue Nile Health Project 398 Blukwa (Zaire) 252 Bol (Lake Chad) 85, 428–9 Boma (Zaire) 538 Bomfa (Ghana) 250 Bône (Algeria) 163 Botletle district (Botswana) 48 Botswana, see also Okavango Delta prosobranchs 54, 84, 125, 146–8, 150 pulmonates 163, 166, 259, 261 schistosomes and host snails 310, 313 Boum Kabir (Chad) 218 Bourbon Island see Réunion Bourguignat, J.R. 2, 527 Brackish water, see also Salinity, biogeography of snails adapted to 550 cercarial survival in 317 coastal 2, 6, 449–50

SUBJECT INDEX 645

prosobranchs; 69, 70–1, 74, 77–9, 95, 98, 102, 110–13, 143–5, 343, 550 pulmonates 152–4, 317–18, 550 schistosomiasis transmission 317–18 Brak (Libya) 178 Brazzaville (Congo Republic) 59, 91, 205 Brazzaville Congo see Congo Republic Breeding experiments Bulinus 359, 363, 367, 370, 373 genetic markers 356, 360, 367, 368, 370, 376 Breeding season see Life cycle Breeding system of Bulinus 373, 375–7, 437, 477 British Museum (Natural History) 160 Expedition to Arabia 1937–8, 374 Brood pouch, brooding 100, 102, 129, 134, 136, 141, 473, 529 Brumbé (Chad) 218 Buffalo 315, 341 Bugondo (Uganda) 213 Bujagali (Uganda) 182 Bukama (Zaire) 123 Bukavu (Zaire) 81 Bukoba (Uganda) 48, 198, 229 Bukome (Lake Victoria) 228 Bulawayo (Zimbabwe) 261 Buloburti (Somalia) 147 Bulongo see Bukama Bumbide (or ?Bumbiri) Island (Lake Victoria) 228 Bungoma (Kenya) 259 Burkino Faso 60, 339 Burton, R.F. 527 Burundi 197, 200, 204, 316, 320 Bushmanland (Namibia) 54 Busisi (Lake Victoria) 168 Butiaba (Uganda) 88, 182, 255 Buvuma Channel (Lake Victoria) 123, 183 Cairo 68, 200, 252 Calabar (Nigeria) 42 Calcium see Chemical properties of water Cameroon crater lakes 225, 242–4, 394, 484, 534 paragonimiasis 339

prosobranchs 42–3, 45, 61, 74, 89, 118– 20 pulmonates 159, 177, 195, 201, 203, 233–4, 236, 238, 242, 249, 258, 261, 365, 371–3, 381, 453, 484 schistosomiasis and host snails 197, 238, 242, 244, 310–12, 320–3, 371–2 snail control 394–5, 403 Canada 379 Canary Islands 161 Cangandala (Angola) 203 Cape Flats (South Africa) 77 Cape of Good Hope (South Africa) 164, 168 Cape Guardafui (Somalia) 55, 127 Cape Mount (Liberia) 66 Cape Peninsula (South Africa) 166 Cape Point (South Africa) 205 Cape Province (South Africa) eastern 80, 238, 507–8 general 77–80, 181, 474, 507–11 Cape Province (South Africa) (cont.) western 79, 157, 231, 238, 316, 321, 507–8, 510, 513 Cape Town 77, 205, 450 Cape Verde Islands 178, 238, 519 Caprivi (Namibia) 54, 111, 123, 221, 222 Caribbean Region 45, 111, 307 Cat, domestic, 340, 343 Cataract, Second see River Nile Cattle 305, 313–16, 325, 341, 342, 344 Cellular defenses of snails, see Resistance Cenozoic 114, 380, 531 Central African Republic 60, 87, 117, 149, 203, 310, 312 Cercaria daily rhythm in emergence 304, 311– 13, 315–17 identification 304 metacercariae 339–46 ornatae type 378 Paragonimus-like 339–40 quantity produced by snail 305–06, 311, 324 schistosome 303–6, 308, 311–13, 315– 17 seasonal variation in production 307–8, 311, 315–16

646 FRESHWATER SNAILS OF AFRICA

shadow response 304, 311 trematodes other than schistosome 338, 340, 342–3, 345–6, 378–9 Chad prosobranchs 47, 56, 63, 68, 70, 87, 111, 505 pulmonates 180, 186, 191, 197, 204, 218, 219, 238, 251–2, 256, 260, 263, 505 schistosomiasis and host snails 310, 312, 315 Chambeshi or Chambezi area (Zambia) 124, 201 Chelating agent, as molluscicide 392 Chemical properties of water, see also Salinity bicarbonate 447 calcium 445–9, 476 chloride 448–50, 502, 526 general 444–52 hard water 349–50, 445–9 hydrogen sulphide 529 iron 454 magnesium 445, 448–9 nitrogen 454, 462, 476 phosphorous 476 sodium 448–50 soft water 349–50, 426–7, 445–9 sulphate 427, 447 total dissolved content 449–53 units of ionic concentration 445 Chipata (Zambia) 87, 148 Chipoka (Malawi) 51 Chiredzi (Zimbabwe) 205 Chirundu (Zimbabwe) 123, 147–8, 151 Christiana (South Africa) 261 Chromosomes, see also Chromosomes, number in Bulinus Amerianna 175 Ancylus 161 Bellamya 46 Bulinus 356, 377–8, 380–1 karyotype studies 225, 230, 233, 356, 363 supernumerary 356, 362 Chromosomes, number in Bulinus

diploid 209, 213–14, 216, 218–19, 222, 224–5, 229–30, 236, 239, 241, 244–7, 309, 314–15, 345, 356, 361–2, 366–73, 377–8, 380–1, 408, 421–2, 534 evolution 377–8, 380–1 hexaploid 222, 366–8 octoploid 227, 366–8, 378 tetraploid 222, 227–8, 233–5, 309, 356, 361–2, 366–72, 377–8, 380–1 Ciliary feeding 81 Circadian rhythms snail activity 231, 464 emergence of cercariae 304, 311–13, 315–17 Climate, see also Rainfall, Temperate Region, Temperature and Tropical Region past 374, 537, 545–6 Sahelian 537, 545–6 schistosome distribution limited by 308, 311, 316 seasonal abundance of snails 473–5, 480–6, 489–95 snail distribution related to 359, 362– 71, 423–6, 455–9, 502–13, 537, 545–6 Cohort, definition 489 Collectors, collecting 2, 3 Comoro Islands 40, 43, 45, 95, 100, 102, 251, 517 Anjouan 45, 101, 157, 181, 254, 517 Grand Comore 153–5, 179, 517 Mayotte 157, 179, 517 Moheli 517 Compatibility, between schistosomes and host snails, see also Resistance and Schistosomiasis assessment and definition 306–7 broad in S. bovis 314 changes possible 321–2, 324–5 Competition between species of snail 201, 380–1, 403, 427–8, 432, 435, 504, 512–13, 546 biological control agents suggested 405–09 Composition of snail faunas see Faunas of snails Conchology, conchologists 2–3, 527

SUBJECT INDEX 647

Conchological terms 10–13 Conductivity, see also Salinity, 449 Congo, Congo Basin, see also Congo Republic and River Zaire, 42, 59, 107, 205 Congo, Republic of the 60, 66, 73, 91, 109, 114, 205, 310 Conservation see Human activities, extinctions Constance (South Africa) 168 Control of snails see Snail Control Copper, copper sulphate 231, 392, 394, 397 Copulatory organ, see also Aphally and Penis, parasitic castration of snail 323 prosobranchs 46, 53–4, 66, 67, 73, 473 pulmonates 28(fig.), 29(fig.), 161, 163, 169, 175, 190, 194–5, 206, 209, 213– 14, 236, 239, 241, 248–9, 355, 359–60, 366 Coromandel coast (India) 100, 109 Crabs, freshwater 53, 339–40, 404, 530 Crater lakes Barombi Kotto 394, 534 Barombi Mbo 534 Bishoftu 534 Cameroonian 225 Chala 534 Debundsha 243, 534 Fort Portal 84, 230 Kichwamba 84 Mirambi 198 Ugandan 534 Wum 534 Crayfish 404–5, 525 Crescent Island (Lake Naivasha) 526 Cretaceous Period 551 Crete 263 Crocodile 318, 321 Crowding effects 391–2, 479, 486–7, 492– 3 Ctenidium 36 Current, water see Flowing water Daboya (Ghana) 129 Dagusi Island (Lake Victoria) 123, 182

Dahomey see Benin; Dahomey Gap 545 Dakar (Senegal) 195 Dallol 450–1 Dams, see also Man-made lakes design to reduce schistosome transmission 401 favourable to snails 157, 222, 230, 234, 320, 430 seasonality in Bulinus populations 483, 490–1 snail control by fish 403–04 Verwoerd Dam 510 Damietta (Egypt) 236 Dangila (Ethiopia) 261 Danish Bilharziasis Laboratory (DBL) 3, 408 Dar-es-Salaam 65, 431 Darfur (Sudan) 218, 360 Debra Berhan (Ethiopia) 68, 180, 253, 342, 368 Debra Zeit (Ethiopia) 534 Defences of snail against infection see Resistance Definitive host of schistosomes 303, 305(table) Denmark 68 Depth, reached by snails in lakes breeding in weedbeds 437 prosobranchs 46, 48, 50–3, 61–2, 68, 82, 85, 89–90, 103, 123, 129, 131, 133– 7, 140–2, 522–4, 529, 535 pulmonates 165, 172, 182–3, 198, 225, 228–9, 242, 454, 522–3 Desert see Sahara Desiccation of habitats, see also Aestivation ecological effects 459–63 life cycle of Bulinus 360, 372 species-diversity restricted 432 Dessie (Ethiopia) 227, 368 Development of water resources increasing prevalence of schistosomiasis 317, 320, 321 Dhofar (Oman) 195, 247 Diama (Senegal Delta) 320 Diapause 459

648 FRESHWATER SNAILS OF AFRICA

Diatoms see Algae Die Kelders, cave (South Africa) 79 Diego Suarez (Madagascar) 245 Dilla (Ethiopia) 162 Diploid, Bulinus, see Chromosomes, number Dispersal active 433, 436 development of African snail fauna 548 foundation of new colonies 436–7 passive 433, 435 routes to Ethiopia 541, 543 Distribution of snails, see also Altitude, Biogeography, Faunas, Habitat and Salinity abiotic factors 444–65 associations among species 434–5 biotic factors in local occurrence 435–8 changes 321, 378, 427, 429, 433, 525 Distribution of snails (cont.) climatic temperature and 197, 215, 225, 362–4(fig.), 455–9, 479–80, 482– 5, 506(fig.), 509(fig.), 510–13, 517, 526–7 current speed limiting 425–6 food supply affecting 197 forest clearance 197, 321 increase related to polyploidy in Bulinus 378, 381 man-made habitats and spread of B. truncatus 378 maps 146–51, 251–63, 364, 509, 511, 514–15 patchiness 318 pollution effects 197, 215, 318 Diurnal activity see Circadian rhythms Diversity of species equatorial region, rich fauna 546–7 freshwater snails versus landsnails 544 habitats and sampling stations 430–33 (table) pulmonates versus prosobranchs 550 Djanet (Algeria) 191, 263 Djugu (Zaire) 160 DNA see Molecular analysis Dodola (Ethiopia) 261 Dodoma (Tanzania) 257 Dogs 316, 339, 343

Dolisie (Congo Republic) 91 Dolo (Ethiopia) 55 Donkey 345 Drakensberg Escarpment see Mountains Duck, ducklings 346 Dungo (Angola) 203 Duque de Braganza (Angola) 220 Durban 40, 79, 96, 155, 190, 194, 201, 204, 209, 211, 255–6, 340, 359, 362 East and eastern Africa Angiostrongylus, hypothetical origin 347 Bulinus truncatus/tropicus complex 362, 365, 369–71, 381 coastal region 343, 371, 380, 455–6 Pliocene-Pleistocene snail fauna 379 prosobranchs 63, 66, 343, 550 pulmonates 163, 168, 171–2, 213, 341, 360, 362, 365, 380–1, 455–6, 482, 489, 505 schistosomes and host snails 232, 238, 307–8, 313–14, 317 snail fauna 544–6, 550 Eastern Cape (South Africa) see Cape Province Ebb en Floed (South Africa) 166 Echinostome, echinostomiasis host snails 185, 197, 200, 213, 228, 231, 235, 238, 242, 246, 249 interference with snail’s defence against schistosome 325 parasite and life cycle 338, 346 Economic loss, fascioliasis causing 341 Ecophenotypic variation 531 Ed Dueim (Sudan) 259 Eggs, egg laying, see also Egg production prosobranchs 39, 47, 54, 57, 60, 81–2, 85, 92, 94, 422, 473–5 proteins, differences among species 201, 209, 218–19, 222, 224, 228, 230– 1, 242, 246, 356–7(fig.), 365–7, 369, 371, 373–4, 381 pulmonates 156, 160–1, 175, 225, 227– 8, 247, 249, 437, 448, 453, 460–2, 464, 477–8, 481–5, 489–92

SUBJECT INDEX 649

size in polyploid Bulinus 227, 355, 366– 7(fig.) turbidity, effect of 453 Egg production gametogenesis affected by temperature 456, 458 seasonal peaks 479, 482–5, 490–2 turbidity depressing 453 Egito (Angola) 239 Eguei (Chad) 545 Egypt Angiostrongylus 346–7 Echinostoma and host snail 200 Egypt-49 Project 395 heterophyiasis 343 invertebrate agents for snail control 404–6 paramphistomes and host snails 235 prosobranchs 37, 39, 46, 54, 59, 68, 70, 82, 87, 121, 145, 475, 504–5 pulmonates 156–7, 159–60, 170, 176– 8, 185–6, 191, 205, 231, 233–8, 248, 252, 257, 262–4, 381, 436–7, 479, 485, 489, 504–5 schistosomiasis and host snails 200, 307–8, 313, 320 snail control 392, 395–6, 401, 404–6 snail fauna 504–5, 541, 545 trematode cercariae, unidentified 379 Eil (Somalia) 98 El Golea (Algeria) 176, 206 El Guettara (Mali) 264 Eland 341 Electrical conductivity of water, see also Salinity 449 Elephant 341 Elizabethville (Zaire) see Lubumbashi Embryos, see also Protoconch shell 51, 107, 208 size in Bellamya 46–7 Embu (Kenya) 211 Empangeni (South Africa) 79 Endemism in snail faunas lakes 520, 523, 525, 528, 532(tables) Madagascar 516(table) river basins 539–40, 542–3(tables) West African Region 537(table) 544–5

Endod 393 England 96, 432 Entebbe (Uganda) 183, 198, 205 Enzymes Biomphalaria 195, 200, 201, 203 Bulinus 209, 213–14, 216, 218, 224–5, 230, 233, 235–6, 239, 241–2, 244–6, 358, 360–1, 363, 367, 369, 371–3, 376, 379–81, 535 schistosomes 304–5, 307–9, 312, 314– 16 Eosinophilic meningitis 346 Eocene Period 379, 549 Epipodial lobe of Ampullariidae 53 Epitaenial fold 81 Equatorial Guinea 238, 312 Equatorial Region, richness of snail fauna 546 Eritrea 70, 156, 264 Erkowit (Sudan) 251–2, 257 Ermelo (South Africa) 264 Erosion, danger from ill-advised management of watercourses 400–01 Escarpment, see Mountains Estuaries, estuarine snail fauna, see also Mangrove 317, 449–50 Ethiopia Bulinus 211, 214, 217, 222–3, 225–7, 231–4, 236, 238–9, 241, 246, 259(map), 261–4(maps), 365–70, 378– 9, 532–4 dispersal to and from 541, 543 fascioliasis 340–2 Galla lakes 532–3 molluscicide trial 393 palaearctic snails 505, 543–5 paramphistomiasis 344 prosobranchs 39, 46–7, 55, 59, 68, 87, 90–1, 121, 146–8, 151, 532–3 pulmonates (other than Bulinus) 156– 64, 168, 170, 175–7, 180–2, 186, 190– 1, 194–7, 200, 204, 249, 251–8, 435, 462, 482, 485–6, 532–4, 543–4 rift valley 47, 532–3 schistosomiasis and host snails 204, 225, 227, 235, 310, 314–15, 319–20, 368–9 Ethiopian Region 1

650 FRESHWATER SNAILS OF AFRICA

Etosha Pan (Namibia) 221 Europe, see also Palaearctic Region Eocene fossil Biomphalaria 549 prosobranchs 37, 68, 74, 82, 142–3 pulmonates 156–7, 160, 170, 176, 180, 206, 263, 341, 502, 551 Euphrates Valley (Iran) 263 Euthyneura 36 Evolution, see also Speciation African snail fauna 548–51 Bulinus 379–81 co-evolution between snails and predatory crabs 404 endemic Lanistes of Lake Malawi 524 episodic change in Turkana Basin 531 old lineages in rivers 549 rock-adapted snails lacking from Lake Malawi 524 S. intercalatum 312 speciation of Ceratophallus in small lake 520 thalassoid snails of Lake Tanganyika 527, 529–30 Exhalent siphon 81–2, 90–2 Expeditions, to Lake Tanganyika, 3 Experimental Taxonomy Division 3 Extinctions see Human activities Faiyum (Fayum) (Egypt) 39, 505 Falls Chanler (Kenya) 192 Gordon (South Africa) 166 Victoria 63, 111, 125, 174, 539–40 Far Abis (Somalia) 90 Fascioliasis control 312–3 host snails 157, 159, 341 parasite and life cycle 338, 340–3 seasonality in transmission 342 wild animals infected 341–2 Faunas of snails in Africa, see also Distribution biogeography 507, 544–51 continental composition 6–7, 548–51

habitats with very low dissolved chemical content 447–8 islands 515–19 lakes 519–536 latitudinal zonation 546–7 local distribution 420–38 North Africa 502–505 origins 548–51 Faunas of snails in Africa (cont.) regional faunas 502–15, 536–48 river basins 536–44 urban areas 431 Faya (Largeau, Chad) 257, 263 Fecundity see Egg production Feeding see Food Ferguson’s Gulf (Lake Turkana) 81 Fernando Po Island 43, 114, 518 Ferric hydroxide, precipitated by bacteria 454 Fezzan (Libya), 186, 505 Finboni (Kenya) 61, 123 Fish aquarium trade and snail dispersal 435 dispersal into Zambezi River 539 malacophagous or molluscivorous 61, 85, 403–04, 448 molluscicide kill 392 second intermediate host for Heterophyes 343 Fishponds snails in 430, 453, 488–9 snail control 400, 403–4 Flies with snail-eating larvae 404 Flowing water artificial flushing regime 401–2 current speeds measured 40, 113, 425– 6, 428, 436, 463–4 drifting by snails 436 ecological effects 463–4, 479, 483, 491– 5 floods and spates 426, 429, 436, 463–4, 483, 486, 491–4 refuges for snails 426, 495 stress on snails 464 turbulence 402, 464 Food of snails and feeding 432, 436, 437–8, 454, 464–5, 479, 488–9, 491 Forest,

SUBJECT INDEX 651

see also Rain forest, 322, 365, 369, 374, 401, 430, 538–9, 545 Fort Jameson see Chipata Fort Lamy (Chad) 218, 260 Fort Portal (Uganda) 171, 230 Fossil record, see also Subfossil 114, 379 France 248, 263 Frankadua (Ghana) 111, 117 FresonR see N-tritylmorpholine Freshwater fauna, definition 2, 450 Frost see Southern Africa 506(fig.) Funtua (Nigeria) 257 Gabarones (Botswana) 261 Gabon 42, 60–1, 71, 84, 114, 238, 244, 310–12 Gagnoa (Ivory Coast) 87 Galla lakes 532–3, 543 Galole (Kenya) 59, 147, 219, 255–6, 259– 60 Gamba (Gabon) 71, 244 Gambia 42–3, 146–7, 150–1, 194, 216, 219, 242, 310, 339, 344, 359, 373, 379, 396, 461, 463, 484 Game reserves, fascioliasis 341–2 Gastrodisciasis 238, 338, 345 Gastropod molluscs 36 Gaya (Niger) 256, 260 Gazi (Kenya) 94, 153, 181 Gebelain (Sudan) 360 Gene pool 322, 376 Genetic determination aestivation behaviour 463 aphally 377 calcification of shell 445 individual variation in growth 480 mantle pigmentation 376 novel shell morphs of the Turkana Basin 531 resistance to infection in snail 306–7 rhythm of cercarial emergence 312 shell shape in Ancylidae 161 Genetic heterogeneity biotype 233, 358, 371, 378 Bulinus 236, 241, 273, 372–3, 376

genetic distances within Bulinus 379– 81 geographical distribution of alleles 372 heterozygous loci, fixed 233, 371, 376, 381 reduction in new colonies 200, 436–7 S. haematobium 309 Genetic markers see Breeding experiments Geological formations chemical properties of water 426–7 substrate 426, 509, 512 Germany 158, 161, 180 Gezira (Sudan), Gezira-Managil Irrigation Scheme, 235, 257, 264, 317, 398, 400, 407 Ghana prosobranchs 60, 71, 109, 111–12, 114– 17, 128–9, 149–50 pulmonates 155–7, 203, 250, 258, 374, 396–7, 453, 461, 490–1 schistosomiasis and snail hosts 310 snail control 396–7 water temperature in lake 458 Gill 36, 68 Gingindlovu (South Africa) 79 Giza (Egypt) 200 Gladdespruit (stream, South Africa) 425–6, 458–9 Goats 305, 313, 316 Gobabis (Namibia) 158, 251, 252 Gondar (Ethiopia) 211, 227 Gondwanaland, Gondwanian fauna 507, 515, 548, 550 Gorgora (Ethiopia) 253, 526 Goundam (Mali) 259 Goz Beida (Chad) 218, 260 Grahamstown (South Africa) 173 Grand Comore see Comoro Islands Greece 263 Griffiths, O. 160 Grootfontein (Namibia) 203, 258 Growth of snails determinate versus indeterminate 474 growth curves 478 individual variation 480 inhibitory compounds, supposed 392 limitation in crowded snails 391–2 parasites affecting 480

652 FRESHWATER SNAILS OF AFRICA

prosobranchs 473–5 pulmonates 478–80 Guinea 94, 117, 537(table), 538 Guinea Bissau 310 Guinea Danica 114 Habitat, see also Distribution, Ecology, Irrigation and Rainpools artificial, man-made 208, 378, 423, 430–1, 438, 447, 513–14 damage by man 45, 504–5, 508, 512 ecological slums 433 instability 434, 487–8 microhabitats within temperature gradients 455, 458 refuges for snail populations 365, 426, 429–30, 451, 512, 521, 545 rivers 420, 422, 536–44 Hadhramaut (South Yemen) 247 Hamasen Province (Ethiopia) 190, 366 Harar (Ethiopia) 215, 254 Harare (Zimbabwe) 181, 205, 211, 446–7 Hardness of water see Chemical properties of water Hargeisa district (Somalia) 257 Harrison, A.D. 447 Hartebeeste 341 Hawaii 160, 341 Hellville (Madagascar) 56 Hermaphrodite reproductive system 68, 152, 375 Heterologous immunity 313 Heterophyiasis 145, 338, 343 Heterozygous loci, fixed 233, 371, 376, 381 Hexaploid see Chromosome number Highveld South Africa 374, 423–5, 435, 457, 507, 510–11, 513 Zimbabwe 317, 319, 479–80, 483, 491– 4 Hippo Valley-Triangle area (Zimbabwe) 399 Hippopotamus 305, 321, 340 History biogeographical, of snail fauna 548–51

collectors, early 2 freshwater snails, study of 2–3 introduced species 7 taxonomy and species concepts of Bulinus 352–74 Hoggar see Ahaggar Hola see Galole Horse 345 Host specificity between parasite and snail 304–5, 309, 324–5 Hot spring 81, 179 Hubendick, B. 159 Human activities breakdown of ecological barriers 321, 365 changes in snail faunas 431, 487–8, 505 extinctions of snails 45, 80, 504–5, 508, 512 forest clearance 374 ponds 487 snail dispersal 436, 505, 513, 517–18 Humansdorp (South Africa) 211, 259, 315, 316 Hunter’s Lodge (Kenya) 98 Hybridisation Bulinus 359, 365, 381 infectivity of hybrid miracidia 312, 315 strains and species of schistosome 309, 312, 314–16, 321–3 Hydrobioid snails, low diversity in tropical Africa 549–50 Ibadan (Nigeria) 157, 175, 178, 250, 400, 429–30, 432 Idris, M.A. 247 Ifakara (Tanzania) 66, 317, 393, 483 Ifrane (Morocco) 180 Ilakatra (Madagascar) 255 Ile du Prince 43 Illite 453 Immunological studies 245, 356–7, 374, 380 India 53, 77, 100, 109, 135, 170, 208, 548– 9 Indian Ocean, islands 157, 205–6 Indo-Pacific Region

SUBJECT INDEX 653

prosobranchs 43, 45, 54, 94, 100, 101, 111, 143, 145 pulmonates 152–155 Infection of snails by parasites, see also Miracidium detection of schistosomes 304 harm to snail 323, 345 mixed-sex schistosome infections 319 overdispersion 318–19 paramphistomes common 345 prevalence of schistosome infections 318–19 Infesafari (Lake Chad) 85 Inheritance see Genetic determination Insects agents for snail dispersal 436 predatory on snails 404 production, in lakes 428, 476, 531 Intermediate hosts Angiostrongylus 346–7 Echinostoma 185, 197, 200, 213, 238, 231, 235, 238, 241, 246, 249, 346 Fasciola 157, 159, 341–3 Gastrodiscus 345 Heterophyes 145, 343 introduction of Biomphalaria glabrata 515 Paragonimiasis 339 Paramphistomes 197–8, 224, 231, 235, 238, 241, 245, 344–5 Schistosoma 170, 197–8, 200–01, 203– 04, 206, 208, 211, 213–19, 222, 224–5, 227–8, 231, 235, 238–9, 241–2, 244–7, 303–25 trematodes, other 157, 181, 197, 204, 216–17, 239 Intrinsic rate of natural increase (r or rm) 234, 375, 378, 444, 447, 456–7, 460, 477, 489–90, 492, 495 Introduced snails 67–8, 157, 175, 204, 208, 249–50, 341, 406, 408–9, 427, 431, 457– 8, 475, 513–15 Inyanga (Zimbabwe) 253 Iran 263, 308, 309, 316, 400 Iraq 263 Iringa (Tanzania) 201, 211 Iron see Ferric hydroxide Irrigation systems,

see also Irrigation projects control of snails 394–9, 401, 406–7, 464 non-schistosome cercariae recovered 378–9 schistosome transmission 320–21 snails of 95, 201, 213–15, 234, 236, 242, 244, 368–9, 422–3, 437–8, 451–2, 483, 490–1, 505 Isiolo (Kenya) 98 Islands, snails of 515–19 Isoelectric focusing 357–8 Isoenzymes see Enzymes Israel 82, 109, 143, 155, 252, 257, 262–3, 344, 436, 474 Italy 170 Itchouma (Libya) 251 Ituri (Zaire) 117, 539 Ivermectin 392 Ivory Coast paragonimiasis 339 prosobranchs 42, 60–1, 66, 72, 87, 109, 112, 114, 116–17, 148–9, 151, 537–8 pulmonates 173, 177–8, 208, 377 Jabal Akhdar (Oman) 247 Jackals 56 Jebel Aulia (Sudan) 204, 258 Jebel Marra (Sudan) 257, 263 Jickeli, C.F. 2 Jimma (Ethiopia) 162, 211, 254, 259 Jinja (Uganda) 182, 216, 360 Jinjimma (Nigeria) 536 Johannesburg 150, 201, 205, 431, 513 Jonglei (Sudan) 87, 432 Jordan 46, 143, 146, 249, 252, 262–3 Kabanza (Zaire) 105 Kabare (Zaire) 168 Kafue (Zambia) 75 Kainana (Zaire) 60 Kainji district (Nigeria), and see Lake Kainji, 191, 146, 151, 256 Kakondo (Zaire) 81 Kala Kala (Zaire) 73, 99, 105, 129 Kalamata (Greece) 263 Kalangwe (Zaire) 168

654 FRESHWATER SNAILS OF AFRICA

Kalawanga island (lower Zaire River) 91 Kalemié (Zaire) 204 Kalenga Swamp (Tanzania) 201 Kalidje Canal (Alexandria) 57, 121 Kamanyab (Namibia) 166, 253 Kanisa (Sudan) 194, 256 Kano (Nigeria) 264 Kano Plain (Kenya) 90, 148, 239, 246, 357 Kapalala (Zambia) 203 Kapopo (Zambia) 60 Karkloof (South Africa) 166 Karoo-Namib arid area 506 Karyotype see Chromosomes Kasai region (Zaire) 126, 151 Kasonga (Malawi) 263 Kasongo (Zaire) 66, 130 Kassala (Sudan) 147 Kassarassi Island (Lake Victoria) 48 Kasulu (Tanzania) 86 Katanga see Shaba Kavirondo Gulf see Winam Gulf Kedougou (Mali) 257 Kentaur (Gambia) 150 Kenya Bulinus 211, 213, 219, 224, 227–35, 239, 241, 246, 259–64, 357, 360, 369– 73, 378, 404–5, 421–3, 453, 456, 479– 80, 482–3, 491–2 crayfish 404–5 fascioliasis 341–3 Kano Plain, snail fauna 420–3, 433 paramphistomiasis 197, 231, 344–5 prosobranchs 40, 46, 55–6, 59, 61, 63, 84–5, 90, 94, 97–8, 102, 121, 123, 126, 143, 146–8, 151, 420–22, 460, 549 pulmonates other than Bulinus 153, 155, 157, 159, 168, 171, 181–3, 188, 192, 195, 204–5, 248–9, 251–8, 404–5, 420–3 schistosomes and host snails 197, 204, 211, 213, 231, 235, 239, 310, 314–17, 322, 325 snail control 397, 403, 407 Keyberg (Zaire) 123 Khartoum 200, 146 Khedire (Morocco) 160 Khuzistan area (Iran) 263 Kiala district (Katanga) 52

Kibale (Zaire) 117 Kibombo (Zaire) 105 Kibwezi (Kenya) 257 Kichwamba (Uganda), see also Crater lake, 84 Kiffa (Mauritania) 260 Kigezi (Uganda) 168, 182, 190 Kigoma (Tanzania) 131 Kikondja (Zaire) 84 Kiliba (Zaire) 495 Kilifi (Kenya) 94, 97 Kilui stream (Angola) 48 Kimpese (Zaire) 91, 426 Kinangop Plateau (Kenya) 228 Kinding Njabi (Cameroon) 323 Kindu (Zaire) 130, 146 Kinshasa (Zaire) prosobranchs 52, 85, 91–2, 105, 107–8, 125, 129 pulmonates 190, 192, 201, 258, 427, 431, 538 schistosomiasis 312 Kipkabus (Kenya) 228, 357(fig.) Kirima (Zaire) 183 Kirk, J. 2, 522 Kisangani (Zaire, formerly Stanleyville) 60, 99, 107, 117–18, 124, 151, 258, 311, 538 Kisantu (Zaire) 73, 426 Kisenyi (Zaire) 252 Kisumu (Kenya) 50, 169, 171, 182, 198, 228–9, 239, 246, 371, 420–1 Kitui (Kenya) 157, 213, 260, 263 Kiubu Rapids in Zaire River 53 Knysna (South Africa) 251 Kob 341 Kokstad (South Africa) 80 Kombe (Lake Tanganyika, Zambia) 139, 142 Kombolchia (Ethiopia) 227, 255, 256 Kongolo (Zaire) 123, 258 Kordofan (Sudan) 121, 260 Korogwe (Tanzania) 488 Kosti (Sudan) 148, 200, 258 Koto (Sierra Leone) 92, 94 Kouri Archipelago (Lake Chad) 201 Kpong (Ghana) 111 Krauss, F. 2, 362

SUBJECT INDEX 655

Kribi (Cameroon) 118 Kruger National Park 151, 253, 255–6, 423–4 Kuka (Lake Chad) 228 Kumasi (Ghana) 258 Kumba (Cameroon) 242 Kuramo Water (Lagos Lagoon) 43 Kwamouth (Zaire) 105 Lac see Lake Lagoa Delagosa (Angola) 147 Lagoon di Hordio 145 Ebrié 72 Lagos 43 Manzimtoti 450 Lagos (Nigeria) 208 Lagune, Laguna see Lagoon Lake, see also Crater lakes and Depths reached by snails crater 534 depths 519(table) man-made 534–6 natural 519–534 refuges during dry periods 365 Lake Abaya or Margherita (Ethiopia) 204, 254, 258–9, 263, 368, 532–3 Abiata (Ethiopia) 146, 532 Alaotra (Madagascar) 127, 173, 516 Albert 50, 82, 88, 90, 109, 121, 150, 182–3, 198, 200, 211, 255, 379, 519(table), 520–1, 532 Lake (cont.) Ashangi (Ethiopia) 163, 182, 261, 367– 8 Awasa (Ethiopia) 182, 204, 225, 255– 6, 258, 367–9, 519(table), 532–3 Baikel (Russia) 527 Bangweolo or Bangweulu (Zambia) 211, 222, 519(table), 521 Baringo (Kenya) 121 Barombi Kotto (Cameroon) 242–4, 484 Barombi Mbo (Cameroon) 534 Bolero (Ruanda) 172 Bosumptwi (Ghana) 250 Bunyoni (Uganda) 84

Burra (Kenya) 59 Chad benthic snail fauna 428–9, 433–4, 453, 474–6 endemism, low 521 physical characteristics 519(table), 521 plants and snails 437 prosobranchs 46, 56, 84–5, 111, 146– 8, 428–9, 433–4, 450, 474–6 pulmonates 157, 173, 178, 181–2, 190–1, 200–01, 204, 215, 228, 233, 236, 251, 254–5, 257–9, 264, 462 salinity 428–9, 450, 519 subfossil palaearctic shells in the Chad basin 545 Chala (Kenya) 183, 520 Chem Chem (Kenya) 84 Chew Bahir see Lake Stephanie Chilwa (Malawi) 453, 483, 521 Chrissie (South Africa) 173 Cohoha (Burundi) 200 de Guiers (Senegal) 321 de Retenue (Zaire) 60, 76, 256, 258 Debundsha (Cameroon) 242, 448 Dembea see Tana Edward 82, 150, 168, 182–3, 198, 204, 229, 519(table), 522 Galla group (Ethiopia) 532–3, 543 George (Uganda) 519(table), 522 Haik (Ethiopia) 182 Haussa (Ethiopia) 87 Jilore (Kenya) 59, 84, 90 Jipe (Kenya) 204, 258, 261 Kainji (Nigeria) 536 Kariba 205, 211, 436, 476–7, 495, 535 Katebe (Zaire) 75 Kisale (Kaire) 84, 204 Kivu 81–2, 150, 168, 182, 379, 454, 519(table), 522 Kpong (Ghana) 536 Kyoga (Uganda) 82, 198, 213 Langano (Ethiopia) 162, 519(table), 532 Léré (Chad) 85, 87, 150–1, 256, 450, 476 Luhondo (Ruanda) 172 Lungwe (Zaire) 447–8, 519(table)

656 FRESHWATER SNAILS OF AFRICA

Lutoto (Uganda) 84 Lyadu (Ethiopia) 214 Malawi (formerly Nyassa) malacophagous fishes 61, 85, 403, 523–4 physical characteristics 519(table), 522–4 prosobranchs 61–4, 85, 102–3, 148, 150, 436, 445, 522–4 pulmonates 255, 228, 454, 522–4 Margherita see Abaya Mariut or Mareotis (Egypt) 505 McIlwaine (Zimbabwe) 447 Mutanda (Uganda) 186, 217, 233 Mweru 50, 102–3, 124–5, 253, 519(table), 524–5 Nabugabo (Uganda) 448, 519(table) Naivasha (Kenya) 204, 230, 248, 258, 263, 404–5, 519(table), 525–6 Nasser (Egypt) 200, 234, 257, 536 N’Dogou (Gabon) 71 Ngami (Botswana) 150, 257 Ngoboseleni (South Africa) 255 Ngwasi (Tanzania) 200 Nyasa or Nyassa see Malawi Opi (Nigeria) 448 Qarun (Egypt) 343 Rudolf see Turkana Shala (Ethiopia) 519(table), 532–3 Sibayi or Sibaya (South Africa) 48, 178, 224–5, 253, 255, 363, 365, 377, 437, 454, 476, 526 Stephanie or Stefanie (Ethiopia) 151, 532–3 Tana (Ethiopia) 39, 46, 68, 146, 156, 211, 238, 368, 519(table), 526–7 Tanganyika basin 233 early expeditions 3 molluscivorous crabs 404 number of species 432, 519(table) physical characteristics 519(table), 527–30 prosobranchs 48, 50, 53, 81–2, 102–3, 126, 129, 131–42, 454 pulmonates 165, 172, 183, 186, 195, 204, 220–1, 253, 371–2 snail fauna 527–30

thalassoid snails 131, 527–30, 551 Tchad see Chad Tiberias (Israel) 252 Timsah (Egypt) 343 Togo (Togo) 71 Toho Todougba (Benin) 72 Tshohoha see Cohoha Tumba (Zaire) 448, 519(table), 539 Turkana or Rudolph, see also Turkana Basin 68, 81, 88–9, 109, 114, 148, 151, 317, 432, 450, 519(table), 530–1, 541, 543, 545 Victoria Bulinus 370–1 fascioliasis 342 malacophagous fishes 403–4 number of snail species 432–3, 519 physical characteristics 519(table), 531–2 prosobranchs 46, 48, 50, 54, 82, 123, 126, 420–2, 533 pulmonates 168–9, 171, 182–3, 190, 198, 204, 211, 213, 216–17, 228–9, 360, 370–1, 420–3, 533 snail fauna 533 Volta (Ghana) 55, 234–5, 317–18, 320, 396, 436–7, 479, 484, 491, 535–6 Wum (Cameroon) 89, 148 Zwai (Ethiopia) 68, 182, 200, 204, 225, 255, 258, 367–9, 462, 519, 532–3 Lakeside (South Africa) 77, 166 Lambaréne (Gabon) 84 Landsnails 1, 14, 188, 347, 544 Langei (Ethiopia) 261 Lango District (Uganda) 213, 260 Larache (Morocco) 160 Largeau see Faya Largeau Laterite plateau in Gambia 242 Latitude, related to faunal diversity 546–7 Leeches 404 Leghareh district (Sudan) 260 Lekemti (Ethiopia) 141–2 Leopoldville see Kinshasa Lesotho fascioliasis 341, 343 snails 158–9, 166, 211, 231, 252, 457, 486, 490, 511–12

SUBJECT INDEX 657

Libenge (Zaire) 59 Liberia 42, 53–4, 55, 66–7, 74, 117–18, 149, 155, 236, 310, 339, 404, 431, 491 Libya prosobranchs 47, 68, 111, 121, 146, 150–1 pulmonates 171, 178, 186, 200, 233, 238, 251, 257, 262–4, 505 schistosomiasis and host snails 200 Life cycles of snails seasonal breeding 455–59 iteroparous 473–5, 480, 484 semelparous 473, 482 prosobranch 473–5 pulmonate 477–86, 490–5 Life expectancy of aestivating Bulinus 375 Light, effects on snails and habitats 464–5, 490 Liver fluke see Fascioliasis Livingstone, D., Zambezi Expedition 522– 3 Lochinvar (Zambia) 241, 313 Lodwar (Kenya) 126 Lokandu (Zaire) 130 Loudima (Congo Republic) 73 Loum (Cameroon) 312, 321, 323 Lourenço Marques see Maputo Louvila (Congo Republic) 73 Lowveld 316, 360, 423–5 Luanda (Angola) 109, 256 Luapula district, see River Luapula Lubarika (Zaire) 81 Lubembe region (Zaire) 60 Lubumbashi (Zaire) 75–6, 168 Lubutu (Zaire) 117 Lufira region (Zaire) 53 Lukonzolwa (Lake Mweru) 253 Lukula (Zaire) 114 Lukuta (Zaire) 126 Lundezi Tembwe (Zambia) 87 Lung fluke see Paragonimiasis Lung worm, rat 346 Lusaka (Zambia) 205, 211, 431 Lushoto (Tanzania) 252 Luxor (Egypt) 264 Lwiro (Zaire) 81, 495 Lydenberg (South Africa) 252, 257, 259

Machudi (Botswana) 259 Macrophytes see Plants Madagascar Angiostrongylus 346 Biomphalaria 447, 455, 484 Bulinus 356, 359, 380, 433 Echinostoma 197 Mangoky region 397 paramphistomes 224, 344 prosobranchs 40, 43, 45, 47, 54, 57, 63, 100, 102, 109, 111, 113–14, 127, 146– 7, 149–51, 516–17 pulmonates 156–7, 173, 178–9, 183, 190–1, 197, 218, 224, 236, 238, 245, 249, 251, 255, 257, 259, 261, 264, 356, 359, 380, 447, 455, 484, 516–7 schistosomiasis and host snails 218, 224, 307–8, 310, 397 snail fauna 515–17, 551 Madeira 161 Madsen, H. 408 Maghreb 502–5 Magila (Tanzania) 64 Mago (Morocco) 160 Mahmoudich or Mahmudi Canal, Alexandria 68, 170 Mahenge (Tanzania) 65 Maitland (South Africa) 173 Majunga (Madagascar) 146 Makatini Flats (South Africa) 146–7 Malabar (India) 208 Malagarasi Delta 65, 172, 530, 539 Malakal (Sudan) 148 Malamfatori (Nigeria) 201, 476 Malange (Angola) 203, 258 Malawi 201, 205, 234, 263, 310, 372, 378– 9 Malela (Zaire) 74, 107, 113 Mali prosobranchs 56, 60, 146–7, 151 pulmonates 157, 172, 178, 194, 219, 234, 257, 259–60, 264, 455, 491, 545–6 schistosomes and host snails 197, 310, 316 Malindi (Kenya) 59, 84, 153, 205 Malumfashi (Nigeria) 251 Mambrui (Kenya) 102 Man-made lakes,

658 FRESHWATER SNAILS OF AFRICA

see also Lakes Kainji, Kariba, Nasser and Volta 320, 534–6 Mandahl-Barth, G. 352, 360, 408 Mangoky region (Madagascar) 63, 397, 451 Mangrove 40, 42–3, 69, 74, 96–7, 143, 145, 153–5 Mangu (Ghana) 109 Mankono (Ivory Coast) 151 Mantle, mantle cavity, see also Renal ridge cavity and diverticulum 57, 64, 66, 94, 453–4 pigmentation 355 prosobranchs 57, 68, 100, 102, 113–14, 120, 126–7, 129, 131, 134–7, 139–143, 145 pulmonates 152, 247, 453–4 Manzimtoti (South Africa) 317, 450 Maputo (Mozambique) 190 Maralal (Kenya) 261 Mariakani (Kenya) 239 Marine molluscs, mistaken for freshwater 14 Marsabit (Kenya) see Mountain Masai Steppe (Tanzania) 85 Mascarene Islands 9, 40, 43, 248, 517 Masingbi (Sierra Leone) 67 Massawa (Ethiopia) 39, 152, 154–5 Matadi (Zaire) 73, 84, 91, 99, 105, 117, 129, 148, 160, 538 Matanda (Zambia) 174 Mathematical models 487, 492–4 Mating system see Breeding system Matopos (Zimbabwe) 253 Mau escarpment 228, 369 Mau Narok (Kenya) 228 Maun (Botswana) 54 Mauritania 70, 150, 178, 219, 234, 251, 257, 260, 262–3, 310, 316 Mauritius Angiostrongylus 346 paramphistome 245 prosobranchs 45, 53, 101, 517 pulmonates 153–4, 156, 188, 206, 244– 5, 249, 344, 373, 376, 517 schistosomes and host snails 245, 308– 10, 373, 409

Mawambi (Zaire) 117 Mayotte see Comoro Islands Mazabuka (Zambia) 198 Mbabane (Swaziland) 188 Mbarali (Tanzania) 213, 260 Mbesuma (Zambia) 201 Mbeya (Tanzania) 253 Meakins, R.H. 231 Medhanie Alem (Ethiopia) 259 Medine (Senegal) 216 Mediterranean region 142–3, 145, 185, 233, 249, 308, 310, 314, 358, 377, 502 Mekerka (Ethiopia) 190, 366 Meru (Kenya) 158 Meshra-el-Req (Sudan) 203 Mesocone in radula of Bulinus, see Radula, Metacercariae 339–46 Miandrivaso (Madagascar) 147 Microhabitats within temperature gradients 455, 458 Mida Creek (Kenya) 97, 143 Migiurtina (Somalia) 145 Mikel (Cameroon) 120 Mimosa Island (in Zaire River) 129 Mining activities creating snail habitats 447, 449 Miocene period 541, 549, 550 Miracidium infectivity of hybrid miracidia 313, 315, 321–24 schistosome 303, 306, 322–3, 318–19, 322–4, 390, 394 trematodes other than schistosomes 338, 340, 343, 345–6 Misungwi (Tanzania) 399 Mitidjah (Algeria) 206 Mleroes (Lake Tanganyika) 140 Mlilo (Lake Tanganyika) 132 Moçamedes see Mossamedes Mogadiscio or Mogadishu (Somalia) 90 Mogeyenga (Ghana) 128 Molecular analysis DNA 245, 247, 358, 376 RAPDs 358 restriction enzyme analysis 358 RNA 358 Molluscicides 391–400

SUBJECT INDEX 659

application in schistosomiasis control 393–99 copper, copper sulphate 392, 394, 397– 8 dam-and-flush treatment of canals 399 Endod 393 ivermectin 392 N-tritylmorpholine 392, 394, 397–8, 400 niclosamide 392, 394–400 PhebrolR 392 plant sources 393 resistance of snails 400 slow-release formulations 394 warburganal 393 Molo (Kenya) 228 Mombasa (Kenya) 61, 146, 205 Mongongo (Cameroon) 201 Monkey Bay (Lake Malawi) 62, 255 Monkey Island (in Zaire River) 129 Moore, J.E.S. 527 Mopti (Mali) 147, 238, 260 Moreau, R.E. 4 Morocco prosobranchs 37, 39, 70, 82, 143, 150 pulmonates 159–61, 176, 180, 206, 252, 262–3 schistosomes and host snails 304 Morphology as source of taxonomic characters Bulinus 353, 355–6 morphometry versus enzyme data 358, 359 ordination of shell data 370(fig.) Mortality, caused by aestivation 462–3 current speed 464 Moshi (Tanzania) 205 Moshi salt spring (Zambia) 75 Mossamedes (Angola) 145, 151, 221 Mossel Bay (South Africa) 264 Mountains, mountain ranges Aberdare 168, 227–8, 369 Atlas 502 Ahaggar or Hoggar 505 Ankaratra (Madagascar) 178 Begour crater 251

Drakensberg 363–4(fig.), 423–5, 445, 506(fig.), 510 Ennedi 260 Hajar, Eastern (Oman) 247 Hoggar see Ahaggar Kenya 168, 261 Kilimanjaro 183 Marsabit 146, 192, 251, 257, 261 Mau 168, 228, 369 Ngaliema (Zaire) 92 Nimba (Ivory Coast) 117 Stanley see Ngaliema Tarouadji (Niger) 264 Tassili N’Ajjar 505 Tibesti 191, 252, 505 Usambara 65 Mozambique Bulinus 362–5, 488 prosobranchs 40, 54, 62, 64, 84, 96, 98, 147, 424, 508 pulmonates 153, 157, 173, 190, 211, 236, 246, 250, 257, 362–5, 424, 488, 508, 514(fig.) schistosomiasis and host snails 310 snail fauna 507–8 Mpala (Lake Tanganyika) 133 Mpulunga (Zambia) 172 Mtossi (Lake Tanganyika) 136 Mtubatuba (South Africa) 192 Mucus, fluorescence 356 Muheza (Tanzania) 65 Muizenberg Vlei (South Africa) 77 Multivariate analysis see Morphology Muséum d’Histoire naturelle, Geneva 61 Muscat (Oman) 208 Muséum Royale Africaine Centrale, Tervuren 160 Mwanza (Tanzania) 48, 50, 198, 201, 205, 211, 213, 261, 263, 379, 399, 431 Mweru misspelling for Meru (Kenya) 158 Mzima Springs (Kenya) 98 N-tritylmorpholine 392, 394, 397–8, 400 Nairobi 195, 211, 342, 357, 431, 484–5 Nacala (Mozambique) 190 Namaqualand 186, 253 Namibia

660 FRESHWATER SNAILS OF AFRICA

prosobranchs 46, 48, 54, 84, 111, 125 pulmonates 158–9, 163, 165, 177–8, 192, 195, 197, 203, 206, 211, 221–2, 231, 238–9, 241, 249, 251–3, 256–9, 261, 264, 514(fig.) schistosomes and host snails 203, 310, 321 Namutoni Spring (Namibia) 150 Nandi (Kenya) 342 Natal Povince (South Africa) Biomphalaria, life cycle 456–7, 484–5 Bulinus 355, 362–5 Natal Povince (South Africa) (cont.) prosobranchs 40, 45, 48, 63, 79, 100, 123, 146–7, 150, 343, 508 pulmonates 153, 156, 190–1, 205, 211, 225, 230, 250, 253–7, 259, 261, 264, 355, 362–5, 456, 459, 484, 508–9, 513 schistosomiasis and host snails 211, 316–18 snail fauna 507–09, 512 National parks see Kruger, Outamba and Game reserves Naukluftberge (Namibia) 165, 178, 253 Ndola (Zambia) 60, 157 Near East definition 9 faunal connections with Africa 505, 541 parasites 343, 345 prosobranchs 37, 68, 70, 82, 111, 142– 3, 150–1 pulmonates 159, 176, 234–5, 248, 377, 381, 514 Nelspruit (South Africa) 307, 365, 423, 425 Nematode worms 338, 346–7 Neolithic Period 505 Neotropical Region biogeography 548–9 Gundlachia restricted to 170 Newcastle (South Africa) 259 New Caledonia 142 New Ireland 152 New Zealand 74, 142, 157, 341 Ngamiland (Botswana) 166, 253 Ngandu (Zaire) 105 Niamkolo (Lake Tanganyika) 172 Niclosamide see Molluscicides

Niger gastrodisciasis 345 prosobranchs 47, 60, 69–70, 87, 148 pulmonates 194, 197, 204, 216, 219, 242, 256–7, 260, 262–4, 373, 377, 450– 1, 505 schistosomiasis and host snails 197, 242, 309–10, 316 Niger Basin, see also River Niger, 157, 215, 238, 242, 264, 430, 537, 541, 543(table) Nigeria fascioliasis 342 paragonimiasis 339 plant molluscicide 393 prosobranchs 43, 54, 56, 60, 63, 97, 112, 114–15, 147, 149–51, 429–30 pulmonates 157, 175, 191, 208, 219, 234, 238, 242, 249–51, 256–7, 260, 264, 359–60, 371, 377, 429–30, 433, 437, 453, 461, 483–5, 490–1 schistosomiasis and host snails 238, 242, 309–10, 315–16, 359–60, 435 snail distribution and diversity 400, 429–30, 432, 433 unidentified trematode cercaria 378 Nile Basin and Delta see River Nile Njala (Sierra Leone) 94 Nkota Kota (Malawi) 201 North, northern Africa, see also North West Africa, Mediterranean region and Sahara paramphistomes and host snail 235, 345 prosobranchs 70 pulmonates 156, 170, 175, 234–5, 263, 362, 449, 482–3, 514 schistosomes and host snails 235, 308, 317 snail fauna 502–05 North America see America North West Africa 9, 37, 70, 82, 143, 160– 1, 234, 304, 314, 502–05, 545 North Yemen see Yemen Arab Republic Northern Rhodesia see Zambia Norway 432, 435, 444 Nossi Bé Island (Madagascar) 56, 114, 127, 173, 236

SUBJECT INDEX 661

Nsendwe (Zaire) 105, 107, 125 Nsombe (Zambia) 222 Numbers of individual snails; proportional representation of different species 433–4, 487 Numbers of species of snail geographical latitude related to 546–7 lakes 519–20 Lake Tanganyika 527–8 landsnails 544 local faunas 421–33, 487 major river basins 543(table) Nyabira (Zimbabwe) 146 Nyae Nyae Pan (Namibia) 54 Nyamgotso (Lake Victoria) 48 Nyangwe (Zaire) 105, 107, 130 Nyanza Province (Kenya) 239, 369 Nyassa Province (Mozambique) 257 Oaklands, Johannesburg 201 Oasis, oases Algerian 502 Baharia 252, 263 Dakhla 177, 252, 263 Djanet 191 Egyptian 505 Kharga 252, 263 Siwa 54, 150, 176 Obrdlik, P. 175 Ogaden (Ethiopia) 91 Okaputa Pan (Namibia) 197, 257 Okavango Delta 57, 63, 82, 123, 147–8, 186, 191, 197, 215, 257, 259 Okiep (South Africa) 264 Ol Kalau (Kenya) 357 Oman 101, 156, 247 Oman Natural History Museum 247 Omaruru (Namibia) 206 Omo Basin and Delta (Ethiopia) 90, 531 Oniassoué (Ivory Coast) 109 Operculum absent or weak in some prosobranchs 14, 36 descriptive terms 13 identification, use in 14 structure 36–7(fig.), 39–40, 42–3, 45– 6, 53–4, 56–7, 66–9, 74, 76–7, 81–2,

84, 87, 89–92, 94–5, 100, 102, 111, 113–14, 120, 126–9, 131, 134, 136–7, 139–43 Orange Free State (South Africa) 363 Ostracods 531 Ouallen (Algeria) 143 Ouarai (Chad) 218 Oukérewé, Nyanza (Lake Victoria) 126 Outamba National Park (Sierra Leone) 92, 94 Ovamboland (Namibia) 54, 177, 192, 221 Overdispersion of infection in snails 318– 19 Oviparity, see also Eggs, egg laying 53, 68, 76, 81, 100, 111, 113, 131, 136, 142, 152, 473– 4 Ovoviviparity 69, 75, 111, 120, 473 Oxygen ecological factor 453–55, 462, 465, 491 high tension 422, 424 low tension 397, 422, 427, 437, 461, 522, 529 Pacific islands, see also Indo-Pacific Region 347 Pakistan 341 Pala (Lake Tanganyika) 126, 136 Palaearctic Region 2, 4, 188, 503, 544, 545 snail fauna 502–05, 527, 533, 541–6, 548, 550–1 southern limit of snail fauna 503(fig.), 545–6 Pambete (Lake Tanganyika) 131 Pana (Cameroon) 119 Pangani (Tanzania) 65 Pangaea 551 Papyrus, papyrus swamp Biomphalaria in 204, 422, 454 habitat for snails 50, 216, 229, 342, 360, 421–2, 427, 454 high altitude for, in Lake Tana 526 oxygen shortage in 204, 454 rarity in Egypt 505 Paragonimiasis 338–40 Paramphistomiasis

662 FRESHWATER SNAILS OF AFRICA

host snails 197–8, 224, 231, 235, 238, 242, 245, 344(table), 345, 378 parasites and life cycles 338, 343–45 Parasites, see also Infection and Schistosomes adverse affects on snails 378–9, 491 candidate agents for snail control 402 burden on snails 378 Nematoda 338, 346–7 schistosomes 303–25 snails as intermediate hosts for trematodes 157, 159, 170, 181, 185, 197–204, 206, 208, 211, 213–19, 221– 8, 231, 235, 238–9, 241–7, 249, 303– 25, 338–47, 491 snail’s growth accelerated 480 success of Bulinus related to tolerance 375, 378–9 water-mite 63 Parasitology and advance in study of snails 3 Paratenic host 347 Parthenogenesis prosobranchs 99, 100, 102, 109–10, 474 pulmonates 161, 376 Pathogens of snails 402 Pemba Island (Tanzania) 40, 102, 111, 311 Pemba (Zaire, Lake Tanganyika) 137, 147, 518 Penis, see also Aphally and Copulatory organ prosobranchs 69, 81, 87, 91–2, 94, 141, 473 pulmonates 28(fig.), 29(fig.), 160, 175– 81, 185, 188, 190, 194–5, 200, 206, 208–9, 213, 236, 239, 247, 249, 477 sclerotisation 29(fig.) stylet 29(fig.) ultrapenis 29(fig.), 208 Petauke (Zambia) 125 Peters, W. 2 pH 426–7, 444 Philippine Islands 40, 152 Phylogeny see Evolution Physicochemical properties of water, see also Chemical properties 444–465

Pietermaritzburg (South Africa) 164, 166, 178, 181, 257 Pilgrims’ Rest (South Africa) 188 Plants, higher or macrophytes, see also Algae hampering mollusciciding 343, 397 molluscicidal properties of 393 oxygen shortage caused by 453–4 relationships with snails 204, 215, 394, 396–7, 400, 424, 428–32, 435–8, 460, 487, 489–91, 523–5, 535–6 snails egg-laying on 57, 437 water weed control 401 Pleistocene-Holocene distribution forest refuges 545 lake faunas 520, 522, 530 prosobranchs 47, 56, 59, 68, 70, 84, 90, 111, 121, 143 pulmonates 157, 176, 178, 180, 183, 186, 191, 197, 204, 209, 234, 238, 379, 381 Pliocene and Pliocene-Pleistocene periods 379, 543, 545, 549 Podor (Senegal) 177, 241 Pointe Noire (Congo Republic) 66, 73 Pollution favourable or well-tolerated by snails 188, 215, 237, 249–50, 318, 320, 430– 1, 438, 488, 513 Physa more tolerant than other snails 408, 431 sisal factory 489 unfavourable to snails 423, 454–5 Polyploidy, see also Chromosomes, number allopolyploidy 381 discovery 361–2, 365 evolution 380–1 morphology of Ethiopian polyploids 366–7 success of Bulinus related to 375, 377– 8 Ponthierville see Ubundi Popa Falls Namibia 48 Population density of snails, see also Intrinsic rate of natural increase abnormally high 488, 493–4

SUBJECT INDEX 663

crowding effects 391–2, 479, 483, 486– 7, 492–3 fluctuations 433, 487–95 limited by food supply 438 mathematical models 487, 492–4 maximum potential 493–4 prosobranchs in Lake Chad 429 Population dynamics see Population density, fluctuations Port Alfred (South Africa) 77, 163 Port Elizabeth (South Africa) 69, 77, 80, 111, 143, 150, 154, 166, 190, 230 Port Harcourt (Nigeria) 97 Port Leven (Madagascar) 178 Port Natal see Durban Port Novo (Benin) 249 Port St Johns (South Africa) 191, 257, 264 Port Shepstone (South Africa) 173 Portugal 206, 234, 263, 304 Portuguese Guinea see Guinea Bissau Potchefstroom (South Africa) 166, 168, 173, 484, 506 Potchefstroom University, Institute for Zoological Research 3, 506, 513 Praziquantel 390 Predators, predation of snails avoidance of 53, 61, 464, 475 control of snails 403–5 fish 53, 61, 464, 475 Prepatent period definitive host 303 intermediate host 303, 307–8, 311–12, 318, 340, 345 Pretoria (South Africa) 173, 264 Principe Island 45 Production, productivity see biomass Prosobranchia, prosobranchs African fauna summarised 6–7 checklist of species 29–32 classification 10, 36 diversity higher than of pulmonates 550 keys to families and genera 14–23 systematic synopsis 36–151 Proteins; see also Eggs, proteins 356 Protoconch 94, 175, 208 Pseudobranch 152, 161, 163, 175, 180, 185, 208, 247

Puerto Rico 157, 405 Pulmonata, pulmonates African fauna summarised 6–7 checklist of species 33–4 classification 10, 152 diversity lower than of prosobranchs 550 keys to families and genera 23–28 systematic synopsis 152–302 Pungo Andongo (Angola) 151 Quaternary period 545–6 Quicuje (Angola) 241 Radula, see also Mesocone descriptive terms 13 mesocone of Bulinus 219–20(fig.), 222– 3, 241, 247, 353, 355, 361–4, 366–70 prosobranchs 36–7, 39, 45–6, 53, 66, 68–9, 72–4, 77, 81–2, 85–7, 89–92, 94– 9, 103, 105, 109, 111, 112(fig.)–114, 120, 128–9, 131, 134, 136–7, 139–40, 142 pulmonates 152, 175, 195, 198, 200, 203, 219–20(fig.), 222–30, 242, 245, 247, 353, 355, 361–7, 369, 371, 374 Rahad Irrigation Scheme (Sudan) 398 Rain Forest Bulinus not successful in 374 clearance affecting snail distribution 321 evolution of S. intercalatum 312–13, 320 freshwater crabs and paragonimiasis 339 Rainfall aestivation behaviour of snails 461 fluctuations in population density 489– 95 salinity reduced 451 seasonality in snail breeding 483–6 Rainpools, see also Small waterbodies, 230, 237, 242, 246, 370, 372–4, 396, 422, 431, 461, 484 Rambe (Egypt) 170

664 FRESHWATER SNAILS OF AFRICA

Ramleh (Israel) 263 Ranjesfontein (South Africa) 173 Ras Hafoun (Somalia) 127 Rat and Rat lung-worm 346–7 Red Sea 145, 343, 543 Rediae 340 Refuge see Habitat Regent (Sierra Leone) 173 Renal ridge in Bulinus 209, 218, 355, 358 Reproduction in snails, see also Breeding system and Life cycle prosobranchs 473–5 pulmonates 477–8 Reservoirs see Dams and Man-made lakes Resistance of snails to infection, see also Compatibility agglutinating substances 324 genetics 324 cellular reactions 324–5 co-evolution 306, 323 evolution of resistance 323–4 humoral factors 324 Respiration, see also Oxygen 453–4, 462 Réunion Island 43, 45, 95, 101, 160, 206, 245, 249, 517 Rheophilous prosobranchs 463, 538, 539(table) Rhodesia, southern see Zimbabwe Rhythm of activity see Circadian rhythms Rice-fields, rice plants 63, 127, 179, 208, 215, 218, 242, 245, 372, 390, 399, 405– 6, 409, 431 Richard-Toll (Senegal) 321 Rift Valley East African 317, 519–20, 549 Ethiopia 47, 368, 532–3 Tanganyikan 530 Rikatla (Mozambique) 98, 173, 190 River Agnéby 116 Albert Nile (Uganda) 198 Aruwimi (Zaire) 130 Awash (Ethiopia) 87, 121, 148, 151, 156, 200, 214, 259, 263–4, 368–9, 533 Bakoy (Mali) 172, 178 Bandama (Ivory Coast) 42

Bengo (Angola) 241 Black (South Africa) 173 Blue Nile 39, 527, 541, 544 Botletle (Botswana) 146 Brackloof (South Africa) 173 Breede (South Africa) 251 Bushimaie (Zaire) 126 Chari (Chad) 429 Chobe (Botswana) 125 Chozi (Zambia) 124, 201 Cocos (Rodrigues Island) 178 Como (Gabon) 42 Comoe (Ivory Coast) 109 Congo see Zaire Creole (Mauritius) 45 Crocodile (South Africa, SE Transvaal) 423–6 Cross (Cameroon) 339 Cuanza (Angola) 109, 264 Cuije (Angola) 84, 146, 148, 203 Cunene 48, 54, 111, 125, 146, 251, 259 Dande (Angola) 108, 214 Davo (Ivory Coast) 87 Deea (Liberia) 74 Dikulwe (Zaire) 52 Eerste (South Africa) 77 Equeefa (South Africa) 173 Eusso Nyiro (Kenya) 98, 192 Fish (Namibia) 150 Gambia 151, 251, 260, 264, 450 Giuba or Juba (Somalia) 40, 59, 84, 90, 98, 121, 126, 148, 214 Great Scarcies (Sierra Leone) 94 Guder (Ethiopia) 368 Gwebi (Zimbabwe) 146 Ituri (Zaire) 117 Jong or Taia (Sierra Leone) 92, 94, 445, 448 Juba see Giuba Kadei (Cameroon) 119 Kafubu (Zaire) 192 Kafue (Zambia) 75, 125 Kalungwisi (Zambia) 48 Karakoro (Mauritania) 150 Kasai (Zaire) 105 Kibovu (Zaire) 76 River (cont.) Kigera 183 Kimililo (Zaire) 76, 123, 168

SUBJECT INDEX 665

Kingani (Tanzania) 65, 102 Kisanga (Zaire) 168, 192 Komati 96, 98, 423, 426 Konkouré (Guinea) 94 Kouilou (Congo Republic) 66, 109, 114, 539(table) Kyngani see Kingani Lepenula (South Africa) 229 Liesbeeck (South Africa) 205 Little Scarcies (Sierra Leone) 92, 94 Lovoi (Zaire) 105, 121 Lualaba (Zaire) 60, 105, 107, 118, 123, 130, 168, 312, 539 Luapula (Zaire and Zambia) 102–3, 105, 124, 168, 174, 198, 241, 254, 446 Lufira (Zaire) 76, 105, 254 Lufubu (Zambia) 198 Lukonje (Cameroon) 118 Luvua (Zaire) 130 Lwiro (Zaire) 427 Malagarasi (Tanzania) 65, 86, 126, 129, 172, 530 Man (Cameroon) 118 Mangoky (Madagascar) 397, 516–17 Manzimtoti (South Africa) 317 Mbette (Cameroon) 321 Mekong (Thailand) 77, 548, 550 Mhlangana (South Africa) 255 Moa (Sierra Leone) 92, 94 Mooi (South Africa, Natal) 264 Mooi (South Africa, Transvaal) 166, 168, 173, 420 Mulonde (Zaire) 241 Niger, see also Niger Basin 56, 146, 151, 153, 157, 259, 537 Nile, see also Albert, Blue, Victoria and White Nile basin 157, 540–44 delta 145, 200, 146–8, 150–1, 257, 262–4, 343, 395, 505 dispersal of snails 436–7, 505, 541 human activities 505 past connection with Lake Turkana 541 prosobranchs 39, 54, 57, 59, 68, 145, 406, 541–3

pulmonates 157, 194, 541–4 schistosomiasis 320 Second Cataract 39, 68, 87, 146–8, 151 Njala see Jong Nogal (Somalia) 251 Nyando (Kenya) 421 Nyong (Cameroon) 89, 118 Ogowe (Gabon) 71 Okavango prosobranchs 48, 54, 57, 63, 82, 84, 111, 123, 125, 147–8 pulmonates 186, 191, 194, 197, 215, 221–2, 239, 251, 256–7, 259, 264, 321, 510 Omatako or Omurambo Omatako (Namibia) 151 Omo (Ethiopia) 90, 531 Orange (South Africa) 222, 238, 253– 4, 510, 511(fig.) Oriso (Ghana) 117 Oti (Ghana) 109, 128 Pongola (South Africa) 508 Quiapose (Angola) 244 Rokel (Sierra Leone) 92, 94 Rufiji (Tanzania) 153 Ruzizi (Burundi and Zaire) 82, 530 Sagan (Ethiopia) 147 St Paul’s (Liberia) 53, 117, 118 Senegal, see also Senegal Basin 42, 151, 186, 197, 216, 264, 320–1 Sewa (Sierra Leone) 94 Shebeli (Somalia) 214 Shiloango (Zaire) 114 Sokoto (Nigeria) 150 Sululta (Ethiopia) 222 Tabe (Sierra Leone) 92 Taia see Jong Tana (Kenya) 55, 121, 147, 219, 255, 259 Tchangwe (Cameroon) 118 Toquor (Ethiopia) 190, 366 Tshopo (Zaire) 107, 117, 118 Ubangi (Zaire) 105 Uebi see Webbi Shebelli Umgeni (South Africa) 40, 166, 180, 186, 191, 195, 224, 362, 365

666 FRESHWATER SNAILS OF AFRICA

Umkomaas (South Africa) 155 Umlaas (South Africa) 158 Umzimai (South Africa) 150 Umzimkulu (South Africa) 40 Umzimvubu (South Africa) 508 Vaal (South Africa), see also Vaal Basin 211, 222 Victoria Nile (Uganda) 50, 82, 169, 182, 198 Volta (Ghana) 42, 60, 111–12, 115, 117, 128–9, 320, 537 Vouami see Wami Wami (Tanzania) 61, 65, 100, 102 Webbi Shebelli or Shibeli (Somalia) 59, 84, 98, 121, 148, 214, 238, 251, 259, 264 White Nile (Sudan) 56, 87, 147, 151, 541 White Volta (Ghana) 116 Yarkon (Israel) 257 Yobe (Nigeria) 85 Zaire fauna of lower basin 426–7 prosobranchs 42, 52, 59, 73–4, 85, 91– 2, 99, 105, 107, 109, 113, 538–9, 542– 3 pulmonates 155 rheophilous snails 538–9(table) snail fauna of river basin 538–43 Zambezi 62–3, 123, 125, 127–8, 174, 539–40 Rodents 305, 309, 313, 316, 346 Rodrigues Island 178, 517 Rosetta (Egypt) 200 Roseires (Sudan) 151 Rouxville (South Africa) 252 Royal Society, The 3, 527 Ruaha Swamp (Tanzania) 201 Ruanda 172, 197 Rumuruti (Kenya) 168 Rundu (Namibia) 48, 256 Ruzizi Plain 81, 428 Sadani (Tanzania) 61 Sahara Desert see also Oases and Late PleistoceneHolocene distribution

dispersal across 505, 545–6 history 505, 545–6 prosobranchs 70, 111, 502, 545–6 pulmonates 157, 159, 197, 229, 234, 381, 450–1, 502, 505, 545–6 refuges for living snails 234, 502, 505 subfossil shells, 47, 381, 545 Sahel, Sahelian zone 157, 216, 234–5, 242, 537 St Gabriel (Rodriguez Island) 178 St Helena 518 St Louis (Senegal) 241 Sakbayeme (Cameroon) 118 Salalah (Oman) 247 Salazar (Angola) 244, 253 Saliboko (Lake Albert) 183 Salinity acclimation of snails 452 electrical conductivity 449 high salinity, effects on snail distribution 197, 200, 210, 224, 234, 245, 317–18, 320–21, 428–9, 432, 449– 52, 474, 502, 504–5, 521, 530–2, 550 limiting snail distribution in Tunisia 449, 451 low salinity, effects on snail distribution 243, 447–8, 451, 534, 550 number of species in lakes, related to 519–20 range in normal freshwater 450 reduction, followed by increased transmission of schistosomiasis 320–21 schistosome transmission limited by 317, 451–2 shell form affected by 112 summary 452 Salisbury see Harare Salt springs 75 Samanga (Cameroon) 119 Samia (Lake Chad) 429, 476 San Salvador (Angola) 60 Sange (Angola) 244 São Tomé 43, 45, 173, 236, 238, 242, 264, 312, 518 Sardinia 233–4, 263, 378 Saudi Arabia 82, 143, 151, 156, 160–1, 186, 244, 247, 263, 408 Savanna 320, 322, 342, 374, 430

SUBJECT INDEX 667

Schistosomes, schistosomiasis, see also Transmission 303–325 control 390–4 definitive hosts 303, 305, 307, 313, 315–16 detection of infection in snail 304 distribution in relation to host snails 319–20, 368–9 domestic livestock infected 313–16 evolution of S. intercalatum 312 focality of infection in snails 317 host snails 170, 197–204, 206, 208, 211, 213–19, 221–8, 231, 235, 238–9, 241–7, 249, 303–25, 368–9, 372–4, 431, 484–5, 525–6 intra-molluscan development affected by seasonal temperature 307–8, 319–20 life cycle 303, 305, 551 prevalence in snails 318–19 species found in Africa 304–5 strain differences within a schistosome species 215, 304, 307–9, 312, 314–16 transmission affected by interacting factors 317–22 SCUBA diving 524, 529, 530, 535 Seasonal waterbodies see Small waterbodies Seasonality, see also Population density population density 489–95 production of cercariae 307–8, 311 Seasonality (cont.) prosobranch life cycle 473–5 pulmonate life cycle 455–9, 480–6, 489–95 Sebha region (Libya) 263 Second Nile Cataract 68, 87, 146, 148, 151 Sediments see Substrate Self-fertilisation see Breeding system Sena (Mozambique) 255 Senaar (Sudan) 86 Senegal, see also Senegambia Adanson’s visit 2, 352 basin 215–16, 234, 257, 238, 251, 257, 259–60, 264, 318 delta and estuary 42, 216, 320 prosobranchs 60, 113, 145–7, 151

pulmonates 155, 177, 219, 222, 233, 235, 241–2, 371, 461, 463 schistosomes and host snails 197, 216, 219, 235, 310, 316, 319–21 trematodes, non-schistosome 242, 379 Senegambia prosobranchs 42, 47, 60, 121, 146–7, 151 pulmonates 157, 233, 242, 372–3 Sericite 453 Serval cat 316 Sex ratio of prosobranchs 473–4 Seychelles 40, 45, 127, 188, 517–18 Shaba Province (Zaire) 52, 181, 211, 313, 539 Shade, effects on snails 401, 427–8, 430, 464–5 Shano or Sheno (Ethiopia) 226, 368 Sheep 305, 313, 315–16, 341, 342, 344 Shell, see also Protoconch and Subfossil apertural lamellae of Biomphalaria 461 discoidal, orientation 175 descriptive terms 10–13 ecophenotypic variation 531 Ethiopian polyploid Bulinus 366–7 form affected by salinity 112, 145 low spire of Bulinus associated with lakes 365 morphometric analysis 353, 358–60, 363, 370(fig.) ornamentation, perhaps non-functional 530 septum formation in Ferrissia 169, 460– 1 taxonomic characters in Bulinus 353 thickened in response to predation 530 variation in Bulinus 355(fig.), 369–70 (fig.) Shinyanga (Tanzania) 213, 260 Shipworms 74 Siavonga (Zambia) 535 Sibling species 134, 139 Sicily 39, 263 Sierra Leone prosobranchs 42, 66–7, 69, 92–4, 407, 431, 445, 538 pulmonates 173, 194, 242, 256, 431

668 FRESHWATER SNAILS OF AFRICA

schistosomes and host snails 310, 407 Simonstown (South Africa) 77 Sinai Peninsula 70, 109, 143, 150, 248–9 Singida (Tanzania) 121 Sinistrality, occasional in normally dextral Lanistes 56 Sire (Ethiopia) 161 Sirwa Island (Lake Victoria) 50 Size eggs 477–8 growth curves 478–9 indeterminate growth 478 maximum, of some prosobranchs 474– 5 sexual dimorphism in Sierraia 473 Small waterbodies, see also Rainpools 432, 461, 482, 487– 8 Snails faunas see Faunas of snails Snail control, see also Snail control projects biological methods 402–09 Biomphalaria and Bulinus 390–410 cost-benefit analysis 394–5, 397–9 danger to non-target organisms 392, 394 environmental methods 400–02 Lanistes 390 Lymnaea 342–3 molluscicides 391–400 prospects 409–10 Snail control projects Cameroon 394–5 Egypt 395–6 Gambia 396 Ghana 396–7 Kenya 397 Madagascar 397 South Africa 397–8 Sudan 398 Tanzania 398–9 Tunisia 399 Zimbabwe 399 Snail faunas see Faunas of snails Soapiti (Guinea) 94 Socotra Island 70, 111 Soft water see Chemical properties of water

Soil see Substrate Somalia prosobranchs 40, 55–6, 59, 63, 68, 70, 84, 90, 98, 100, 121, 126–7, 145, 147– 8, 151 pulmonates 153, 214, 238, 251, 257, 259, 262, 264 schistosomes and host snails 214, 238, 310 Somerset West (South Africa) 157 South Africa, see also Cape Province, Natal, Orange Free State, Southern Africa and Transvaal Bulinus 355, 362–5, 370, 374, 452, 461, 484, 507–13 climatic temperature and snail distribution 455–9, 484, 507–15 fascioliasis 157, 341 invertebrate predators of snails 404 highveld 374, 423–5, 435, 457, 507, 510–11, 513 introduced snails 436, 513–15 lowveld 316, 360, 423–5 paragonimiasis 340 paramphistomiasis 344–5 plant molluscicide 393 prosobranchs 40, 45, 77–80, 96, 475, 550 pulmonates 155–8, 163–8, 173–4, 181, 186–97, 205, 209–11, 215, 222, 224–5, 229–31, 236, 246, 249–57, 259, 261, 264, 355, 362–5, 374, 434, 436, 452, 455–9, 461, 484, 507–15 schistosomiasis and host snails 197, 211, 308, 310–11, 313, 315, 317, 320– 1, 362 snail control 397–8 snail distribution 420, 423–6, 455–9, 507–15 temperature and life cycles 475 South America 68, 74, 307, 461, 549, 550 South Chad Irrigation Scheme (Nigeria) 490–1 South Coast Junction (South Africa) 174 South Yemen see Yemen, People’s Democratic Republic South West Africa see Namibia

SUBJECT INDEX 669

Southern Africa 313, 319–20, 362–5, 455– 9, 506–15, 544–6 Southern Rhodesia see Zimbabwe Southern Africa 313 Soutpansberg (South Africa) 253 Spain 160, 206, 263, 304, 314 Spanish Guinea see Equatorial Guinea Spates see Flowing water, floods Speciation of snails episodes in Turkana Basin 531 inhibition by instability of waterbodies 540–1, 544, 550 Lake Chala 520 Lake Tanganyika 530 Species, see also Faunas of snails associations among 434–5 concepts of 7–8, 258–74, 544 groups in Bulinus 208–9, 353–4, 358– 74 numbers present locally 431–4 Speke, J.H. 2, 3, 527 Speke Gulf (Lake Victoria) 50 Sperm morphology 230, 249, 355 Spitzkoppe (Namibia) 206 Sporocyst 303, 340 Stanley Pool (Zaire River) 52, 107, 146, 539(table) Stanleyville see Kisangani State Museum, Windoek (Namibia) 165, 206 Stellenbosch (South Africa) 252 Stillbaai (South Africa) 79 Streptoneura 36 Subfossil shells, see also Late Pleistocene-Holocene distribution and Sahara prosobranchs 47, 48, 126, 533, 545 pulmonates 158–9, 163, 166, 175, 381, 533, 545 Substrate detritus 529 gravel 526, 539 hard 423, 463, 509 mud 477, 479, 525, 529, 531, 535 rocks 433, 463, 512, 523, 529–31, 536, 538, 550

sandy 475, 523–4, 529, 531, 535–6, 539 sediment types in lakes 428–9, 522, 529–30 sediment texture and snail distribution in Nigeria 430 soils 422–3, 462 stability of substrate related to persistence of snail populations 423, 463, 495, 512 submerged trees 535 Subterranean habit of Auriculastra 153 Sudan gastrodisciasis 345 prosobranchs 39, 46, 54, 56, 59, 63, 68, 86–7, 121, 146–8, 150–1, 475 pulmonates 157, 170, 176, 186, 190–1, 194, 200, 203–4, 215, 217–19, 234–5, 238, 251, 255–60, 262–4, 345, 360, 437–8 schistosomes and host snails 197, 217, 235, 309–10, 313, 317, 320, 400, 435 snail control 398, 403, 406–8 snail fauna 432, 541 Sudd area (Sudan) 150, 541 Suez (Egypt) 151, 264 Sululta (Ethiopia) 222 Sumbu (Lake Tanganyika) 140 Sunda Shelf (SE Asia) 550 Surface film, snails attaching to 181, 436 Susceptibility of snails to infection see Compatibility and Resistance Swaziland 150, 188, 211, 514(fig.), 515(fig.) Syracuse (Sicily) 39 Syria 46, 120, 151, 263 Tabelbala (Algeria) 257 Tadpoles 346 Tagent Plateau (Mauritania) 263 Tahiti 45 Taita (Kenya) 61 Ta’iz or Tai’zz (Yemen Arab Republic) 146, 151, 235 Takaungu (Kenya) 90 Tamale (Ghana) 490 Tams, G. 2

670 FRESHWATER SNAILS OF AFRICA

Tananarive (Madagascar) 173, 218, 224 Tanga (Tanzania) 447 Tanganyika see Tanzania Tangier (Algeria) 160 Tanzania molluscicide trials 393 prosobranchs 46–8, 54, 61, 64–6, 85–6, 98, 102, 123, 126, 129, 488 pulmonates 153, 155, 159, 168, 181, 198, 200–01, 204–5, 211, 213, 217, 238–9, 246, 251–64, 360, 372, 433, 436–7, 461, 479, 482–4, 488–9, 491 snail fauna of fishpond 433, 488–9 snail control 398–9, 401–2, 405–6, 408 schistosomes and host snails 198, 201, 204, 211, 213, 238, 310, 314–15, 317, 320 trematodes, non-schistosome 198, 213, 216–17, 239, 379 Taoudenni Basin (Mali) 545–6 Taourga (Libya) 200, 257 Tara (Niger) 256 Tassili N’Ajjar (Algeria) 161, 186, 257, 505. Taung (South Africa) 257 Taveta (Kenya) 85, 148, 183 Taxonomy and taxonomic characters of Bulinus 352–8 Taylor, D.W. 248, 249, 379 Tchad see Chad Tejerhi (Libya) 146, 150–1, 186, 257, 264 Temperate climatic region of southern Africa, see also Highveld, 1, 319, 363, 375, 423–6, 455, 457, 482, 484, 506–12 Temperature aphally of Bulinus related to 377 climatic effects on snail distribution 362–3, 365, 368–9, 371, 423–6, 455–9, 479–80, 482–5, 506(fig.), 509(fig.), 510–13, 517, 526–7 downstream effect from man-made lake 320, 510 experimental investigations 455–8, 479–81 gradients within waterbodies 455, 458 growth rate of snails related to 479–81 population density fluctuations 489–95

schistosome distribution 308 seasonality in snails’ life cycle 482–5 summary 459 Temporary pools see Small waterbodies Tete or Tette (Mozambique) 62–3, 147, 250 Tetraploid see Chromosomes, number of Thailand 347 Thalassoid snails see Lake Tanganyika Thermal spring see Hot spring Thomas, J.D. 394 Tiassalé (Ivory Coast) 42 Tibesti, see also Mountains, 191, 252, 505 Tigre Province (Ethiopia) 182 Tin Tahart (Algeria) 257 Tiwi (Kenya) 97 Togo 71–2, 115–16, 128, 197, 250, 344, 346 Togoville (Togo) 72 Tokar (Sudan) 366 Tongaland (South Africa) 151, 256, 321 Total dissolved salts see Salinity Touggourt Depression (NW Africa) 502 Transkei (South Africa) 197 Transmission of schistosomes, see also Intermediate hosts and Schistosomiasis brackish water 317 changes 320–22, 372 focality and related factors 317–19 increased by human activities 320–1, 401 man-made lakes 534–6 potential, in Lake Naivasha 525–6 prevalence increased by reduction in salinity 317–18, 320–21 prevented by cool climate 319–20, 368, 510 seasonal peak 319, 451 urban 431 water contact points for people 318–19, 396–7 Transvaal, see also South Africa physicochemical factors and snail distribution 435–6, 448 prosobranchs 111, 146, 150, 508–09

SUBJECT INDEX 671

pulmonates 190, 197, 222, 250, 253, 255–7, 259, 261, 264, 356, 360, 362–3, 365, 420, 445–6, 455, 457–8, 483–5, 508–10 snail fauna of eastern Transvaal 423–6, 507–8 S. mattheei 316 Trematode see Parasites Tripoli (Libya) 171 Tropical area and snail fauna see Afrotropical Region and Faunas of snails Tuabo (Senegal) 222 Tukoto (Mali) 172 Tulear (Madagascar) 147 Tumbatu Island (Zanzibar) 94 Tunduma (Tanzania) 198, 260 Tunduru (Tanzania) 213 Tunisia, Tunis 39, 70, 143, 150, 161, 399, 409, 449–52 Turbidity 453, 484 Turkana Basin 114, 379, 531, 549, 551

Urea 397 Usagara (Tanzania) 261 Usambara (Tanzania) 64, 65 Uvira (Zaire) 66, 495

Ubangi (Zaire) 59, 60, 125 Ubuari Peninsula (Lake Tanganyika) 134 Ubundi (Zaire) 118 Ufipa (Lake Tanganyika) 131, 136 Uganda fascioliasis 341–2 prosobranchs 59, 82, 84, 87, 88, 90, 123, 534 pulmonates 168, 171, 181–3, 186, 190, 198, 204–5, 211, 213, 216–17, 228–9, 233, 241, 255, 260, 360, 433, 534 schistosomes and host snails 198, 204, 213, 217, 307, 310, 316 Uitenhage (South Africa) 308 Ujiji (Tanzania) 53, 134, 136, 141, 263 Umgeni Valley (South Africa), see also Umgeni River, 191, 195, 362, 365 Umkomaas (South Africa) 79 Umlaas (South Africa) 252 Umtwalumi (South Africa) 173 Umvukwes Hills (Zimbabwe) 448 Upington (South Africa) 251, 264 Upper Volta see Burkino Faso Urban areas, snails of 431

Wadi El Natroun (Egypt) 160 Erhina (Socotra) 188 Hatib (South Yemen) 247 Howar (Sudan) 54, 56, 147, 251, 257 Tourba (Chad) 260 Wahlberg, J.A. 362 Wallaga Province (Ethiopia) 161 Wallo Province (Ethiopia) 162 Wardere (Ethiopia) 91 Warrenton (South Africa) 259 Warthog 341 Water current see Flowing water Waterbuck 313 Watercress plant 341, 407 Waterfalls see Falls Water-lily 219, 438, 453, 483, 525 Water-quitting see Aestivation Watson, H. 358 Watson, J.M. 360 Welwitsch, F. 2, 359 Wepener (South Africa) 251 West, K. 528 West Africa Angiostrongylus lacking 347

Vaal Basin (South Africa) 211, 509, 513 Van Eeden J.A. 362, 506 Vanga (Kenya) 97 Vereeniging (South Africa) 186 Verwoerd Dam (South Africa) 510 Victoria (Cameroon) 45 Victoria Falls see Falls Vila Artur de Paiva (Angola) 203 Vila da Ponte (Angola) 257 Virunga stream (Zaire) 427–8, 485, 495 Vivi (Zaire) 99 Viviparity, see also ovoviviparity, 46, 72, 99, 129, 134, 136, 139–40, 473–4, 529–30 Volta Basin (Ghana) 234, 537 Vryberg (South Africa) 252

672 FRESHWATER SNAILS OF AFRICA

estuarine brackish water penetrating far inland 450 fascioliasis 341–2 prosobranchs 40, 45, 55, 61, 66, 87, 121, 143, 451 pulmonates 172–3, 177–8, 197, 218, 233–5, 238, 250, 359, 371, 380, 514 schistosomes and host snails 215, 235, 238, 308–9, 316 snail fauna 537–8, 544–6, 549 West Indies 68, 102, 111 Western Aden Protectorate see Yemen, South WHO Schistosomiasis Control Project, Ghana 396 Wildebeeste 315, 341 Wilderness (South Africa) 96 Winam Gulf (Lake Victoria, Kenya) 123, 171, 421–2 Windhoek (Namibia) 321 Witkop (Botswana) 166 Wolisso (Ethiopia) 253 World Health Organisation (WHO) 1, 3, 396 Wright, C.A. 357, 360 Yamoussoukro (Ivory Coast) 208 Yaoundé (Cameroon) 119 Yau (Nigeria) 85, 260 Yebbi Souma (Chad) 150 Yemen, North see Yemen Arab Republic Yemen Arab Republic 46, 146, 151, 156, 161, 233, 235, 244, 247, 252, 257, 262–3 Yemen, South (People’s Democratic Republic) 161, 186, 227, 244, 246–8, 252, 257, 262–3, 374 Yendi (Ghana) 490 Yesor Swamp (Ghana) 71 Yo see Yau York (South Africa) 166 Yoruba Plateau (Nigeria) 430 Zaire, see also River Zaire basin 105, 538–9 fish predation of snails 403 paragonimiasis 339

prosobranchs 48, 53–4, 56, 60, 64, 66, 69, 73–6, 81, 84–5, 91, 96–7, 99, 107– 9, 114, 117–18, 121, 123–6, 129–31, 146, 148–9, 151, 426–8, 538–40(table), 541–3 pulmonates 159–60, 163, 168, 181, 183, 190, 192, 201, 203–4, 211, 222, 234–5, 238–9, 241, 249, 252, 254–9, 262–4, 372, 427–8, 438, 447, 479, 483–5, 489, 495, 539–40(table) schistosomes and host snails 197, 204, 211, 235, 308–9, 311–12, 316, 319–20, 323 snail fauna, distribution and ecology 426–8, 445–7, 538–43 waters of low salinity 538–9 Zalingei (Sudan) 218, 251, 264, 360 Zambi (Zaire) 42, 59, 107 Zambia paramphistomes and host snails 198, 344 prosobranchs 54, 60, 75, 84, 87–8, 124– 5, 139, 142, 148 pulmonates 157, 174, 198, 201, 203–5, 211, 222, 231, 241, 246, 258, 493, 535 schistosomes and host snails 211, 231, 238, 241, 311, 313 Zanguebar 121 Zanzibar prosobranchs 54, 63, 65, 94, 102, 111, 121, 123, 147–8, 518 pulmonates 153, 178, 190, 206, 230, 251, 255, 259, 311, 518 Zaria (Nigeria) 342 Zeekoe Vlei (Cape Town) 450 Zeidab (Sudan) 257, 264 Zerguin (Algeria) 37 Zimbabwe fascioliasis 341–2 prosobranchs 111, 123, 146–8 pulmonates 151, 157, 163, 173, 205, 211, 225, 241, 246, 249, 253, 261, 434, 436–7, 446–8, 453, 455, 458, 479–80, 482–4, 489, 491–5, 510, 535 schistosomes and host snails 197, 306, 308, 311, 316–19 snail control 394, 399, 401, 408 Zoetendal Valley (South Africa) 77

SUBJECT INDEX 673

Zoonoses 338 Zoutpansberg (South Africa) 165 Zululand 46, 57