Advances in Plant Pathology, Volume 11 (Advances in Plant Pathology)

Advances in

Plant Pathology Volume 11

EDITORIAL BOARD Michael J. Daniels

The Sainsbury Laboratory, Norwich, UK Richard I. Hamilton

Agriculture Canada Research Station, Vancouver, Canada David S. Ingram

Royal Botanic Garden, Edinburgh, UK Paul H. Williams

University of Wisconsin-Madison, USA

Advances in

Plant Pathology series edited by

j . H . Andrews

I.C. Tommerup

Department of Plant Pathology The University of Wisconsin Jvladison, Wisconsin USA

and

Volume 11

ACADEMIC PRESS Harcourt Brace & Company, Publishers London San Diego New York Sydney Tokyo Toronto

Boston

CSIRO Laboratoryfor Rural Research Wembley, Western Australia Australia

ACADEMIC PRESS LIMITED 24/28 Oval Road, London NW1 7DX

United States Edition published by ACADEMIC PRESS INC. San Diego, CA 92101 This book is printed on acid free paper Copyright 9 1995 by Academic Press Limited

All Rights Reserved No part of this book may be reproduced in any form by photostat, microfilm, or any other means, without written permission from the publishers

A catalogue record for this book is available from the British Library ISBN 0-12-033711-8

Typeset by Colset Private Ltd, Singapore Printed and Bound in Great Britain by T.J. Press (Padstow) Ltd, Padstow, Cornwall

Contents

Contributors Preface 1. The Concept of Agricultural Sustainability A. Hamblin

vii ix 1

2. Prehistoric Agricultural Methods as Models for Sustainability W. M. Denevan

21

3. Sustainable Agriculture: An Agroecological Perspective S. R. Gliessman

45

4. Developing Biofertilizer and Biocontrol Agents that Meet Farmers' Expectations M. E. Leggett and S. C. Gleddie

59

5. Pathogens' Responses to the Management of Disease Resistance Genes J. K. M. Brown

75

6. Three Sources for Non-chemical Management of Plant Disease: Towards an Ecological Framework A. P. Maloney

103

7. Classical Biological Control of Plant Pathogens J. K. Scott

131

8. Economic Thresholds and Nematode Management R. McSorley and L. W. Duncan

147

9. Evaluation of Micro-organisms for Biocontrol: Botrytis cinerea and Strawberry, a Case Study J . C . Sutton

173

I0. Biodiversity and Biocontrol: Lessons from Insect Pest Management M.A. Altieri

191

1 I. Plant Protection Using Natural Defence Systems of Plants B.J. Deverall

211

12. The Role of Soil Microbiology in Sustainable Intensive Agriculture C. E. Panldaurst and J. M. Lynch

229

vi

Contents

13. World Integrated Pathogen and Pest Management and Sustainable Agriculture in the Developing World J . W . Bentley, J. Castafio-Zapata and K. L. Andrews

249

14. The Diversity of Fungi Associated with Vascular Plants: the Known, the Unknown and the Need to Bridge the Knowledge Gap P. F. Cannon and D. L. Hawksworth

277

15. Adventures of a Rose Pathologist C. Harwood

303

Index

317

Contributors

M.A. ALTIERI, Division of Biological Control, University of California at Berkeley, Berkeley CA 94 720, USA K. L. ANDREWS, Escuela Agricola Panamericana, Apartado Postal 93, Tegucigalpa, Honduras j . w . BENTLEY, CasiUa 1663, Cochabamba, Bolivia. j. K. M. BROWN, John Innes Research Institute, Norwich Research, Colney, Norwich

NR4 7UH, UK P. F. CANNON, International Mycological Research Institute, Bakenham Lane, Egham, Surrey TW20 9TY, UK

J. CASTANO-ZAPATA, Escuela Agricola Panamericana, Apartado Postal 93, Tegucigalpa, Honduras W. M. DENEVAN, Department of Geography, 455 Science Hall, University of Wisconsin, Madison 53706, USA B.J. DEVERALL, Department of Crop Sciences, The University of Sydney, N S W 2006, Australia LARRY DUNCAN, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA S. C. GLEDDIE, PhilomBios, #318-111 Research Drive, Innovation Place, Saskatoon SASK S7N 3R2, Canada S. R. GLIESSMAN, AgroecologicalProgram, University of California Santa Cruz, Santa

Cruz, CA 95064, USA

A. HAMBLIN, Bureau of Resource Sciences, PO Box Ell, Queen Victoria Terrace, Canberra, ACT 2600, Australia C. H A R W O O D , Bear Creek Gardens Inc., P.O. Box 9100, Medford, Oregon 97501,

USA

viii

Contributors

D.L. HAWKSWORTH, International Mycological Research Institute, Bakenham Lane, Egham, Surrey TW20 9TY, UK M. E. LEGGETT, PhilomBios, #318-111 ResearchDrive, Innovation Place, Saskatoon, SASK S7N 3R2, Canada j. M. LYNCH, Horticultural Research Institute, Worthing Road, Littlehampton, West Sussex BN17 6LP, UK

A.P. MALONEY, Department of Plant Pathology, CorneU University, Ithaca N Y 14853, USA R. McSORLEY, Department of Entomology aria Nematology, University of Florida, PO Box 110620, GainesviUe, Florida 32611 0620, USA C. E. PANKHURST, CSIRO Division of Soils, Private Bag No 2, Glen Osmond 5064, Australia j . K . SCOTT, CSIRO Division of Entomology, Private Bag, PO Wembley 6014, Australia j . c . SUTTON, Department of Environmental Biology, Ontario Agricultural College, University ojc Guelph, Guelph, Ontario N1G 2W1, Canada

Preface

The series Advances in Plant Pathology publishes articles on issues of current or future interest and importance in plant pathology. Since its initiation one decade ago, the hallmark of Advances in Plant Pathology has been that the articles are essentially essays rather than merely reviews. The emphasis on ideas, together with flexibility of format, length and content will continue. Our goal is both to draw insights and concepts from relevant disciplines into the realm of plant pathology and to reveal the general biological principles of plant pathology to the broad audience of biologists. Thus, thought-provoking articles ranging from a very basic to an applied focus on a wide variety of topics will continue to be written for diverse readers, including undergraduate and postgraduate students, researchers and teachers. While most volumes will have no particular theme, others, such as the recent volume on mycorrhiza, will treat a particular subject in depth. Controversial viewpoints will be encouraged. Articles that are fundamentally editorial in scope will be included periodically in the series. We want to serve the interests of all plant pathologists and welcome suggestions for specific articles or future volumes in the series. These comments or ideas should be sent to John Andrews, Department of Plant Pathology, 1630 Linden Drive, University of Wisconsin, Madison, WI 53706, USA (Fax 608-263-2626). Madison, Wisconsin, USA & Perth, WA, Australia, 1994

j . H. Andrews & I. C. Tommerup

This Page Intentionally Left Blank

THE CONCEPT OF AGRICULTURAL SUSTAINABILITY Ann Hamblin

Bureau of Resource Sciences, PO Box Ell, Queen Victoria Terrace, Canberra, A C T 2600, Australia (current addressfor correspondence: Cooperative Research Centrefor Soil & Land Management, Private Bag 2, Glen Osmond 5066, Australia).

I. Introduction II. Attributes of Sustainable Agriculture III. Agricultural Sustainability: a Realistic Concept for High Productivity Farming? IV. Integrating Ecological and Economic Aspects of Plant Disease Control in Sustainable Agriculture V. High Production Versus Low Production Environments and Farming Systems VI. Conclusions References

1 4 7 13 !5 16 17

I. I N T R O D U C T I O N The word sustainability does not appear in most English language dictionaries. It is a word of the late twentieth century; an abstract concept coined from a verb meaning to support, endure or maintain for a prolonged period. It has, however, come into common usage as a broad ethical concept, implying moral choices relating to the use and distribution of material goods within and between societies, both present and future (Pearce et al., 1988). Long-expressed concerns over the effects of indefinite material growth and the need for balanced development (Daly, 1988) were given a special focus by the World Commission on Environment and Development (WECD) report 'Our Common Future' (1987). This focused public attention on the nexus between poverty, population growth and environmental deterioration. The report proposed a solution based on 'sustainable development'. The Commission's thesis was that it is possible to meet the needs of present populations without compromising future generations' needs by limiting the exploitation of natural resources through effective management and social organization. Economic growth is essential for poor countries, but the present solution of providing this through natural resource exploitation is unsustainable. These propositions require hard decisions and changes in the distribution of wealth, and organization of goods and trade, between rich and poor countries, and within rich countries. ADVANCES IN P L A N T P A T H O L O G Y - - V O L . 11 ISBN 0-12-033711-8

Copyright 9 1995 Academic Press Limited All rights of reproduction in any form reserved

2

A. Hamblin

The thinking embodied in ' O u r Common Future' is not new, but it presents strong challenges to the neoclassical economic stance that natural resources are an infinite good, which do not require intrinsic valuation. It also challenges the assumption that optimization of wealth distribution occurs most readily through competition. If it were actually possible to have totally free trade and markets this might be the case, but in the current world situation the frequency of market failure (lack of monetary value for things that are greatly valued by the community) is so common that alternative methods of resource preservation have to be found. While many environmentalists would like to see more regulation to achieve this, the most effective long-term solution is for people to decide that they want to preserve, and give them the means to do that. Education, democratization through communication networks, and access to alternative economic opportunities may be some of the alternatives that bring progressive, permanent improvement. In recent years there has been a plethora of publications on what constitutes sustainable agriculture. Many western governments have espoused the term (e.g. Science Council of Canada, 1991; Australian Agricultural Council, 1991), but the notion of what sustainable agriculture means at national level varies from country to country, culture to culture. While northern hemisphere industrial countries place substantial emphasis on the preservation of rural landscapes and wildlife habitats in their definitions of sustainable agriculture (OECD, 1992) the principal goals of the developing world are to alleviate rural poverty and provide long-term production security (World Bank, 1992). Sustainable agriculture is discussed substantially in terms of land management, agricultural policy, pesticide reduction programmes, at the level of general goals, rather than at the specific level of mechanisms for widespread implementation. The implications for plant pathologists, agronomists and other agricultural scientists are that great expectations are placed on increased use of various biological control strategies for pest management. The concept of sustainable development also implies that reducing the dependence on pesticides should not be at the expense of desired levels of food production and farm viability. The conservation of biodiversity has also become a significant international goal, with the development of the International Convention on Biodiversity (1992) as part of the United Nations Conference on Environment and Development (1992). However, conservation of biodiversity in sustainable agriculture is still at best a hazily articulated concept (Sandlund et al., 1992), as what constitutes biodiversity varies with the type of life form, the scale of the organisms and environment, and the extent of knowledge about the biota in question. For example, with animal organisms, from plankton to whales, abundance of organisms appears related to body size (Damuth, 1987). In plant species, isozyme surveys of genetic material have shown about 80% of molecular diversity of the species occurs in any one population; however, Brown and Schoen (1992) argue that this does not imply redundancy in the majority of populations as abundance of plant genetic diversity also depends on the mating

The Concept of Agricultural Sustainability

3

system of the plant category, the pattern of species heterozygosity, and the spatial demography of the germplasm. Even greater complexity may surround the estimation of microbial biodiversity, because of shear lack of taxonomic knowledge, as well as such microbial attributes as lack of mobility, and functional coevolution with plants which additionally affect rates of genetic change (Holdgate, 1991). Wilson (1988) for example, estimated the total number of species of bacteria worldwide to be no more than 3600, compared with 46 983 species of fungi (a remarkably precise figure surely?), whereas Erwin (1982) has speculated that there may be up to 30 million species of insects unreported in tropical environments, compared with the 750 000 so far recorded, and May (1988) prudently cautioned against such simplistic number-counting by demonstrating how dependent estimates were upon base assumptions of host-specificity and habitat characterization. Conservation of biodiversity for sustainable agriculture is often translated to mean the conservation of the genetic resources of domesticated species and their progenitors, in which context it has long been actively promoted by FAO (Food and Agriculture Organization), the Consultative Group on International Agricultural Research (CGIAR) and the International Plant Genetic Resources Institute (IPGRI), particularly for plant species. Habitat conservation and in situ genetic resource conservation are less well catered for in most countries, or internationally. Yet the significance of such conservation cannot be over emphasized in relation to the future success of biological control programmes that are dependent on utilization of natural predators of exogenous pests, weeds and vectorborne diseases. Well-known examples of successful biocontrol are frequent in Australia, where the relatively recent introduction of alien pests has often been sufficiently well documented to enable location of predators from the region of origin to be identified, introduced and established. A formal system of identification, preconditioning, quarantine, testing and controlled release exists in Australia for biological control organisms, both for control of insect and other invertebrate pests (mainly in horticultural and animal production systems) and for weed control, particularly in aquatic parks and reserves, and remote or inaccessible environments where other forms of control are unsuitable or impossible (Corey et al., 1993). Biological control of weed species through the introduction of herbivorous predatory insects and fungal pathogens from the centres of origin has been successful in a number of cases, as in control of prickly pear, blackberry, and skeleton weed, and Cullen (1993) documented 35 other species which are currently being investigated for biological control measures. However, the success rate is relatively low in cases where the original ecosystems have deteriorated, or where the pest species is introduced into a different climatic environment and pest-pathogen life cycles become non-synchronous (see also Scott, Chapter 7, this volume). Today, many of the South African, Middle Eastern, and South American environments which have yielded the pathogens and predators of these Australian aliens are increasingly genetically eroded, making the chances of success for

4

A. Hamblin

control of current or future pathogens and pests either lower or more costly. Similarly in north America some 50-80 % of pathogens are estimated to be alien, the majority from Europe. In the United States the loss to food and fibre crops from insect pests has been estimated at 13 %, and total pathogen, pest and weed losses of the order of 37 % of production - all in a country which strives to maintain low pathogen and pest levels through widespread use of pesticides and cultural practices (Pimentel etal., 1991). Ironically, however, Pimentel (1993) considered that this dependence on pesticides for pathogen control has led to a doubling of the crop losses (from 7 to 13% attributable to insect pests for example) between 1945 and 1991, because of the abandonment of traditional forms of crop protection, such as wide rotations, integration of animal and plant production systems on farm, and narrowing of the genetic pool in monocultured crop varieties. Biological control has not been used as a main-line strategy, compared with the investment in resistance breeding (and more recently genetic manipulation of the host for herbicide resistance) and in increasingly selective pesticides. The implications of loss or threats to native habitats have been only cursorily considered at the political and scientific policy level in relation to such environmentally benign agricultural strategies as resistance breeding, biological control of soft-borne pathogens and plant-symbiont nutrition. An opportunity currently exists, however, with the International Convention on Biodiversity (1992) which the majority of developed countries have ratified, to advocate for the restricted use of pesticides in, and preservation of, agricultural regions in close proximity to biomes known to contain progenitors and land-races of agricultural plant species. Such advocacy will be dependent on the specialized knowledge of plant pathologists, breeders and agronomists being presented into the arena of international conventions and politics. Professional societies and Academies have an important role in advocating such policies to national governments.

II. ATTRIBUTES OF SUSTAINABLE AGRICULTURE Despite the differences in national interpretation of sustainable agriculture, there is substantial agreement among agricultural scientists, ecologists and economists on the properties of sustainable agricultural system - sometimes termed agroecosystems. Ecological concepts of resilience and diversity have been incorporated into the characterization of such systems (Holling, 1973). Conway (1985), Marten (1988) and others have distinguished the attributes of productivity, stability, sustainability and equitability in such traditional agroecosystems as the village-garden agriculture of Indonesia, in which sustainability is associated with the ability to maintain production over long time periods, relative to human life. These systems are resilient in that they recover from stresses (such as seasonal droughts or insect pests) and from major perturbations (such as climatic fluctuations or wars), as shown in Fig. 1. Systems based in environments of low intrinsic fertility (old,

The Concept of Agricultural Sustainability

5

Productivity

Yield

High

Time r

Stability

Yield Low

High

Time Sustainability With Stress

l Yield

Low

W-V High

y

Time Sustainability With Perturbation

Yield High Time Fig. 1. Definitions of high (day) and low (night) levels of productivity, stability, sustainability with stress (~) on sustainability with perturbation (+) adapted from Conway (1985).

6

A. Hamblin

weathered soils, arid zones), which have low potential productivity, may also often have low stability of production because of the erratic nature of the rainfall or erosivity of the soils, as in most of the semi-arid tropics and subtropics. Such systems are inherently less resilient to exogenous stresses than those in environments of high intrinsic fertility (postglacial and alluvial softs) and high climatic stability (e.g. cool and warm temperate climates with low rainfall variability). However, all ecosystems can be pressured beyond their limits if their traditional, sustainable farming practices are intensified, either by shortening the time between biological stresses (as has been the case in the decrease from 20 years to 5 or fewer years between clearing events in tropical forests traditionally used for shifting agriculture, as population pressure increases) or by increasing the loading of inputs into the system within a given period (as in the case of nitrate loading in European cereal production). In high input agricultural systems, typical of the developed world and irrigated regions, strategies for reducing the use of pesticides and inorganic fertilizers have become central to most discussions on sustainable agriculture, as evidence of the adverse environmental, human health and trading effects of the increasing use of these agricultural chemicals accumulates (OECD, 1992). In low-input systems, typical of non-irrigated agriculture in the developing world, lack of fertilizer, overgrazing, and vegetation clearance from population pressure, are the symptoms of unsustainability most frequently identified (FAO, 1989). In both these end-members of the full range of global farming systems, solutions to inadequate farming practices are sought in the greater use of rotations for weed control and crop health, continued reliance on both conventional plant breeding and genetic engineering for pest and disease control, residue retention and minimum tillage for organic matter build-up, and the interspersing of agroforestry with conventional cropping or pastures. All solutions appear to place heavy reliance on farmers and scientists having a good understanding of both biology and economics of the production system, and being capable of managing plant health and nutrition by the relatively sophisticated and complex regimes of integrated pest management, biological control and appropriate rotational agronomy. In a number of European countries national policies have recently been developed to gradually reduce the use of agricultural pesticides, improve their efficacy and regulate their application. Sweden, Denmark and the Netherlands have now embarked on such programmes of agricultural chemical reduction (Hurst, 1992). This is expected to provoke other agricultural exporting countries into similar action because of the advantage which low pesticide users can command in trade. Non-commercial barriers may be erected in the same way in which unilateral banning of older generations of pesticides has operated in favour of those countries which remove declared pesticides from use. However, reduction in overall levels of pesticide use requires wide consensus from all sectors, including producers, chemical compa~nies, government agencies, and research and development organizations. In the Netherlands, reducing the dependence on soil sterilants and

The Concept of Agricultural Sustainability

7

pesticides in the production of lucrative, export-quality bulb, tuber and root crops, to which nearly 9 million kilograms of pesticides are applied per year (Zadoks, 1993), requires major change to farming practice, legislation and monitoring, and to research directions. It may also result in lower production in a sector of the economy responsible for a large proportion of export earnings. While Rabbinge (1991) estimated that the European Community as a whole could reduce its cultivated area by 60 % and its pesticide used by 80 % and still feed itself comfortably, without producing vast surpluses of subsidized commodities that distort world trade, the political will to change is still to come, and with it the scientific support to help producers transform their systems without large production and economic loss. For nearly all systems of agricultural production which are now dependent to some degree or other on control of weeds, pests and diseases by chemical pesticides, such reduction programmes will require a high level of information, education and co-operation between producers and agricultural servicing institutions. In some farming environments, however, the increasing prevalence of pesticide resistance in weed species (Powles and Matthews, 1992), and in pests such as Helicoverpaarmiga (Forrester, 1990) may threaten long-term capacity to produce certain types of crops at an economic rate of return.

III. AGRICULTURAL SUSTAINABILITY: A REALISTIC CONCEPT FOR HIGH PRODUCTIVITY FARMING? In the 1960-1980s the successes of the cereal breeding programmes associated with the 'Green Revolution' led to the consensus among agronomists that potential yield set by radiation and temperature was the realistic target for field production, with the progressive removal of abiotic and biotic stresses, the former through inputs of irrigation, fertilizers and pest-controlling chemicals, the latter through continued refining of the plant canopy by breeding (MAFF, 1978; CIMMYT, 1989). In addition, in North America and western Europe producer subsidy protection over the period 1975-1990 was equivalent to 25-55 %, compared with an average of 10-15 % in Australia for example (OECD, 1980-1990). This has encouraged inefficient, high use of inputs above the effective rate of return. The result has been extraordinarily large and continued increases in biological productivity, that is, expressed as yields (kg ha-1 year-1), but not necessarily in economic productivity (ratio of all outputs to inputs expressed in $). The amount of nitrogen fertilizer required to produce a tonne of wheat in the UK is 6.5 times that used in Australia, for example, but the average profit margin per tonne is little different. Other striking differences between increases in productivity and inputs of fertilizer and pesticides which show the differences between developing and industrial countries are shown in Table I, where we can see an example of the marginal rate of return for increased application of pesticide, by comparing the Netherlands, France and the UK. 'Low input' countries such as Australia and

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Table I. Kilograms of N, P, and K fertilizer, and active pesticide used per hectare of crop land for selected countries compared with yields and yield increase in cereals. ,,

Country India Pakistan Argentina United Kingdom The Netherlands France USA Australia

hak~_~NPK applied (1987-1990)

kg active ingredient ha-1 ( 1 9 8 2 - 1 9 8 5 )

% Increase in cereals 1979-1989

Average cereal yield: kg ha-1 1988-1990

62 85 5 359 662 405 95 26

0.30 0.09 0.40 5.07 10.35 5.16 1.97 0.75

42 27 16 5 19 31 6 17

1865 1745 2262 5792 6681 6101 4341 1650

Source: Food and Agriculture Organization of the United Nations (several years) and World Resources Institute (1992).

Argentina still have sufficient difference in intrinsic fertility that this is reflected in their relative yields. Although these are gross averages across many different crops and production environments, the heavy reliance on pesticides and fertilizers in western Europe is particularly noticeable. The economic consequences of subsidized production in high-income countries is now recognized to be causing severe distortion to world prices of agricultural commodities, with increasingly adverse environmental consequences in the countries of production, while failing to halt the declining terms of trade experienced by commercial farmers in those countries. The revised Common Agricultural Policy (European Community, 1992), and the so-called Blair House agreement of the General Agreement on Tariffs and Trade (GATT), linalized in December 1993, both seek to reign back the extent and intensity of agricultural production in the northern industrial countries through progressive reduction in subsidies and removing some land from agricultural production. The impact of both on farming practice may be small unless they are accompanied by an objective rethinking of the production environment by nutritionists, agronomists and pathologists. Such innovation is necessary to utilize the principle of biological diversification more effectively so that the identified advantages of mixtures of varieties, wider rotations, mosaics of biotypes within fields, companion species, predator refuges and conservation strips, as for example described by Strange (1993), can be implemented on a much wider scale in commercial agriculture. The introduction of alternative, minor crops and pasture plants such as legumes, which are constituents of nutritionally sustainable systems, and provide alternative income sources, have notoriously high disease and pest susceptibility, particularly where hosts (often with accompanying pathogens) are introduced into new environments (Allen, 1983). Allen points out that traditional farming systems (in Latin America and Africa) which use companion cropping of legume-cereals (such as

The Concept of Agricultural Sustainability

9

maize/cowpea, or maize/15'ean) nearly always have lower incidence and severity of leaf fungal pathogens than where the same crops are grown as single, more densely planted stands, even within the same environment. Current attempts on the part of agronomists to reverse the 'monoculture-intensification' trend of the past two decades pose significant challenge to plant pathologists. As epidemiologists and geneticists have frequently pointed out, domesticated species are often most susceptible to their normally endemic (co-evolved) pathogens when introduced into new environments. Harlan (1976) cited such classic cases of rust epidemics in maize after its introduction from Mexico into Africa, coffee rust in the New World and Panama disease of banana, as examples of this type of disruption of the normal host-pathogen fitness and virulence levels. He pointed out that the 'virtual carpet' of wheat from northern Canada to Argentina, and of rice from Korea to Indonesia and India, had put an unprecedented pressure on conventional breeding strategies, given the narrowness of the genetic base and the lack of co-evolution of these cereals' major pathogens that is now occurring. Where grain, shrub and pasture legumes are introduced into such cropping systems to improve stability and diversification, the new introductions are frequently beset by almost epidemic attacks of their otherwise endemic fungal or viral pathogens (Allen, 1983). Another practical problem for pathologists charged with protecting the production of minor crops is that investment in their resistance breeding is small relative to that devoted to cereals, both internationally (Consultative Group on International Agricultural Research, 1992) and at national level in many instances (Clements etal., 1992). Support for biocontrol agents capable of suppressing major fungal pathogens in woody and perennial species, such as Phytophthora cinnamoni for example, which attacks some 200 tree crop species worldwide is a similar area of under-investment compared with such heavily researched pathogens as Pythium spp. and Puccinia spp.; many of the tree species concerned are of more significance to plantations and conservation management than to the annum income-generation of commercial agriculture, so conventional economic justification has been harder to demonstrate. The rate of development of resistance to pesticides in some instances has been documented as being as little as one year (Lolium rigidum to Chlorosufuron; Powles and Matthews, 1992), although more generally resistance may occur between 5 and 10 years' use. In this species the occurrence of multiple resistance, sometimes to herbicides which have never been applied to the population in question, has also been noted in Australia. While the very wide gene pool of L. rigidum, and its strongly competitive ability against most other species, have made its resistance a particularly difficult problem in minimum-tillage systems of pasture-croprotations, herbicide resistance is now a widespread phenomenon of many cropping environments in which systemic compounds have been in use for a number of years. Quantification of disease levels and resistance breeding is more advanced for fungal than bacterial pathogens as a whole; for example, the epidemiology

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A. Hamblin

Table II. World records of resistance to pesticides in Arthropoda 1970-1989. ,,.

Cases (number by species) by pesticide group

1970

1976

1980

1989

DDT Cyclodeine Organophosphate Carbamate Pyrethroid Fumigant Others Total

98 140 54 3 3 3 12 313

203 225 147 36 6 8 20 646

229 369 200 51 22 17 41 829

263 291 260 85 48 12 40 99

Source: Georghiou and Lagunes-Tejeda (1991).

and genetics of cereal rusts are particularly well documented. The International Centre for Improvement in Wheat and Maize has reported the breakdown in resistance of wheat cultivars to Puccinia recondita f.sp tritici (stem rust) within 3-5 years on average (Roelfs and Bushnell, 1985), and in an unusually welldocumented case, changes in the pathogenicity of stripe rust (Puccinia striiformis f.sp. tritic0 have been followed from the first detection in Australia in 1979 over a period of 10 years. Wellings and McIntosh (1990) observed 15 different pathotypes in Australia and New Zealand, with single gene mutations being the most likely cause of variation. Resistant varieties were effectively developed against the identified pathotypes, but breakdown against the first genes isolated (Yr2, Yr3, Yr4) occurring within one season. Subsequent spread of new pathotypes occurred at the rate of one to two a year, resulting from a single mutational event in each generation, in a step-wise progression. Using this example McIntosh (1992) has stressed the need to recognize and exploit longer-lasting (durable) resistance based on the concept of race-non-specific mechanisms such as multiple-gene resistance with adult-plant stage control, conferring non-hypersensitive response (Johnson and Law, 1975). Resistance in plant insect pests has become a very significant concern in a number of intensive annual and perennial cropping environments, and the current status of resistance to pesticides in arthropods is graphically illustrated in Table II, showing the continued increase in the resistance to the 'softer' pyrethroid group of insecticides in the 1980s, as these have been introduced to lessen the deleterious effects of the organophosphate and D D T groups which were so heavily used in the previous decade. The introduction of integrated pest management (IPM) systems has for long been heralded as the strategic, safe and sustainable alternative to the problem of resistance against such effective and devastating pests as Helicoverpa armigera (boll worm) in cotton. However, this system is not in fact sustainable, but represents a best-bet option for delaying the onset of resistance, as work in the Australian cotton industry demonstrates. The present, highly successful Australian cotton industry is some 25 years old. It has expanded rapidly to a position of being the

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fourth largest trader of cotton internationally earning more in exports than the total export value of fisheries and rivalling forest products, and is characterized by a sophisticated and well-informed producer population. Cotton is a notoriously heavy user of pesticide, fertilizer and defoliant chemicals, but the earlier near-obliteration of the Australian cotton industry in northern Australia in the 1960-1970s, by over-use of D D T and organochlorines, sharpened producer and scientist awareness for a programme of IPM from the inception of the present industry in northern New South Wales in the mid 1970s. The strategy has consisted of a number of components: breeding of hairy-leafed ('ockra') type varieties which offer physical barriers to insect attack; production of early-season varieties which avoid the optimum temperature development period of Helicoverpa sp. build up; use of an early-warning and risk-optimization model (Sirotac) to minimize the use of aerial spraying in conjunction with 'pestscouts' reporting the population build up; and a highly sophisticated chemical strategy which has used a sequence of pyrethroid-substitution compounds differing stepwise in their functional radical to minimize the selection challenge for pest resistance. Nevertheless, resistance to pyrethroids and endosulphan has occurred, and continues to increase with a progressive narrowing of the 'window' of use from 12 to 6 weeks in most districts. While current pyrethroid substitutions are delaying the rate of reduction of the window of effective control, they cannot stop it. Alternative strategies being investigated currently are the growing of buffer (alternative host) crops around each block of cotton, the use of Bacillus thuringiensis (Bt) mixed with, or instead of, pyrethroids, suppression of the resistance mechanism (via oxidative detoxification) with piperonyl butoxide, and the projected development of genetically engineered host-plant resistance (Forrester, 1990). At the same time increasing pressure is being placed on the industry from environmental and community groups for scaling down even further the number of pesticide applications, with particular concerns being expressed about the residue levels occasionally found in tailing waters and outflows from irrigation areas which form part of the Darling River Basin, relatively high up in this major catchment. I have gone into some detail over this one example because it presents all the challenges which pathologists of the high-input systems of the northern hemisphere face as countries in that region implement pesticide reduction programmes. Simply put, there are strong vested commercial and national interests in maintenance of high productivity systems, which for some crop environments are extremely difficult to achieve without reliance on practices which can be environmentally damaging. Even where strategies are devised to overcome the reliance on chemical control of a pathogen there may be substantial grower, processor or marketer resistance, or inability, to use the strategy. The theoretical attractiveness of the use of multiple-gene resistance by physically growing mixtures of varieties of similar architecture and phenology has long been advocated (Frey, 1976; Hamblin etal., 1976). However, successful commercialization has been the exception rather than the rule. The attempt to

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introduce Maris Tricorn, a mixture of three varieties of malting barley developed by the Plant Breeding Institute, Cambridge, illustrates this nicely. In the early 1980s this varietal mixture was promoted to reduce the reliance on a similar 'replacement strategy' use of fungicides against powdery mildew (Erysiphegraminis DC. f.sp. hordd Marchal), which had developed all the same problems of ineffective fungicide control due to the vast haploid population of that pathogen in which pathogenicity is frequently the result of sorting in individual gene frequencies (Wolfe, 1987). Despite the simplicity and cost effectiveness of the diverse mixture strategy, it was not attractive to the industry because of the reluctance of maltsters to accept the mixture, although the composition and malting qualities of all individual varieties were well known. The mixture strategy will not, as Wolfe pointed out, work well if the foliar disease is migratory, with new waves of inoculum entering the crop environment every few generations, and works best where genetic shift occurs as the result of within-crop spread. Varieties must also have sufficiently close phenologies, nutritional requirements and quality attributes to satisfy production demands. Nevertheless, it remains an under-utilized strategy in which market resistance is largely traditional rather than based on valid technical grounds. Such social, institutional and political aspects of high productivity agricultural systems are as significant to the successful introduction of alternative strategies of plant protection as the scientific problems posed by them. However, even in the scientific arena, there is a curious dearth of discussion within the scientific establishment on the anticipated longer-term biological outcomes of some of the proposed strategies. Such discussion has largely been within the ambit of non-government environmentalist organizations, and vary from the frankly emotive anti-science stand to the informed and thoughtful prospect of replacing one flawed system with another. Take the case of the significant amount of current interest and investment in the use of Bacillus thuringiatsis (Bt) strains as biocides, in IPM and resistance breeding. The natural toxins in different strains of Bt are selective amino acids which bind to receptor proteins in insect gut, causing the gut wall to disintegrate; over 50 compounds have been identified, often with very selective targets. They have been widely heralded as benign, not only because of their natural origin, but also because the strategy of using mixtures of the toxins was expected to reduce to almost zero the odds of resistance developing in any target pathogen. By altering the toxin spectrum over time, or by producing a suite of genetically altered host varieties with a range of toxins, it was inferred that crop pest and disease levels will be able to be kept at current very low levels without the environmental and resistance problems of current chemicals. However, recent reports of resistance in Colorado beetle and diamondback moths to Bt are indicative that even with these precautions there can never be a completely resistance-free insecticide (Holmes, 1993). Moreover, the insertion of Bt genes into crop plants may present a stronger selection pressure than the simpler use of the toxins as sprays, which break down rapidly in UV light. Strategies such as growing refuge areas of non-transgenic forms adjacent to transgenic

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crops of potatoes and cotton are being tested in limited-scale field situations, to diminish the possibility of any selection towards insect resistance, but the size of such refuge areas, ratios of transgenic to non-transformed plants, and producer willingness to forfeit a proportion of production as a hedge against future possible mutation are all unknown at the present time. It is against such complex issues that the claims by proponents of'organic farming' that this is more sustainable than conventional methods of plant protection should be weighed. However, the focus of much of the writing about, and research towards, more sustainable agricultural systems seldom considers plant protection in these terms.

IV. INTEGRATING ECOLOGICAL AND ECONOMIC ASPECTS OF PLANT DISEASE CONTROL IN SUSTAINABLE AGRICULTURE What then should be the position of responsible plant pathologists in seeking to provide more sustainable plant protection from the great host of diseases, insect vectors and predators, and alternate hosts associated with weed infestations? Should research continue to be directed to systems which will rely on pesticide applications, even if this is by means of inserting herbicide-resistance genes into target crops, as in the case of cotton and potato currently being developed como mercially? Can reliance on breeding as a strategy against leaf fungal diseases of annual crops continue indefinitely, in agroecosystems that are subjected to widespread fungicide applications several times every year, and where target efficiency may average little more than 50%, according to the significant improvements that have been demonstrated in calibration, operating conditions and reduced non-target loss experimentally (Hurst, 1992)? Would it not frequently be more effective to reduce the density of the crop canopy, and lower the dependence on the small range of crops currently grown in most environments that encourages large expanses of monocultures based on a narrow genetic base? Is the use of benefit-cost analysis as frequently invoked as Koch's postulates in plant pathology management? Let us look first at all the possible strategies, their current status and the plant types at which they are directed. For some 20 years the theoretical treatment of ecology has been stimulated by the insights of Robert MacArthur and his associates into relationships between the abundance and diversity of species and their environments. MacArthur's most pertinent contribution was to demonstrate the extremes in strategies employed by different species to maximize their numbers and persistence in island biogeographies (MacArthur and Wilson, 1967). Starting from the proposition that species cannot maximize both growth rate and competitive advantage (as metabolic energy and genetic transformation trade-offs occur between these), there are two basic strategies which can be employed to maximize one or the other. These are the 'r-strategy' and 'K-strategy'. r-~pe species are exploiters, opportunistic in behaviour, maximizing their growth rate whenever conditions are favourable, and profiting from uncrowded or

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Table IlL Principal control strategies for different pest problems (after Conway, 1981).

Strategy Pesticides Biocontrol

Cultural controls Resistance breeding

Mating control

r-pests Widely based on forecasting Not often practicable

K-pests

Intermediate Selective Introduction of natural predators and pathogens < ............

Time of planting, cultivation, sanitation ............. > General, polygenic .......... > < .......... Not effective?

Precisely targeted on monitoring

Change in rotation, destruction of alternate hosts Specific, monogenic Sterile mating, attractants ,,

unstable environments. K-type species are highly competitive, and favoured by crowded or stable environments. Their growth rates are lower than for r-strategists, but their competitive ability is greater; they have evolved in stable habitats where populations are maintained at relatively constant levels, often through low fecundity, high longevity and larger size. These concepts have been fruitfully pursued by May (1981) and Conway (1981) in relation to the most effective strategies for disease and pest control. The classical economic evaluation of the effectiveness of any strategy of pathogen control is, as mentioned, to apply a cost-benefit analysis, in which the total costs of control and the total revenues from control are assessed to identify the marginal rate of return for each additional cost increment. Conway (1981) considered a number of pathogen-control strategies for r and K classic pest types and for a range of intermediates, which include most introduced pathogens (frequently having been introduced in association with the cultivated host), separated from their natural predators or regulating climatic regime. Such intermediate types have often assumed the dimensions of a severe pathogen inadvertently through deliberate control of another, perceived threat; the weed science literature is rich in examples of little-known mosses, sedges or minor grasses suddenly becoming intractable weeds after selective herbicides have been used against another spectrum of weed types. Conway argued for a conceptual framework which would consider all pest and pathogen types within a farming system, and compare the pest 'strategies' with the possible control strategies, along the lines of the matrix shown in Table III. The effectiveness of any strategy should be assessed according to the frequency and scale of economic loss (yield or quality), the pathogen range, and the feasibility of implementation of the control measure. Table III does not go so far as to consider the interactions of different pathogens and strategies within the farming system, although this is the reason why plant resistance is so often a preferred strategy, as it allows more than one pathogen to be accounted for within a single 'package' of genetic composition. If agricultural scientists who service high-productivity farming systems are going to be effective in devising alternative pest and pathogen

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management strategies which are less reliant on selective pesticides and narrow gene resistance, it is essential that such systematic consideration of the total host and pest-pathogen spectrum be viewed together in this way.

V. HIGH PRODUCTION VERSUS LOW PRODUCTION ENVIRONMENTS AND FARMING SYSTEMS Misunderstanding abounds in popular literature as to what constitutes a high production system versus a low production system, the two often being confused with the level of inputs into the system. As noted earlier, some environments are intrinsically more productive than others, but increases in productivity are everywhere possible by the reduction of environmental constraints such as fluctuating water supply (as for example by supplementary irrigation to high biomass crops in sandy soils, even where grown in reliable rainfall regions of humid temperate zones). Intrinsically low-productivity regions can be made modestly secure by such strategies as planting dates which avoid climatic extremes (frost or high temperatures), or the use of compound fertilizers and soil amendments to overcome gross nutritional deficiencies (e.g. phosphate in most African and Asian alfisols, or the small quantities ofCu, Mo, Zn and B needed to rectify a wide range of minor and micronutrient deficiencies in Brazilian and Australian ultisols). There is a convincing body of evidence on the positive feedback between overcoming such gross nutritional deficiencies and the increased resistance of most crop species to root disease infection (Huber and McCay-Buis, 1993). These improvements in the stability (reduced variation) of the production system also provide increased sustainability, not only by reduction in food production shortfall, but also by maintaining a denser or more complete plant cover, capable of better protection against erosion and with a potential for increased residue and organic matter retention. Advocates of a universal reduction in the use of pesticides, fertilizers and other inputs based on the extremes of high input systems in the northern hemisphere are misguided; for the low input systems of the developing world, and the extensive production systems of Australia, south America and Canada, such a move would represent a significant deterioration, and in the tropics an absolute collapse, in the current fragile level of sustainability of production systems that are normally severely nutrient deficient (Pieri, 1992; Hamblin and Kyneur, 1993). For each economic and physical production environment there are a number of best-bet optimizations, but in all cases there will be a spectrum of plant pathogens to contend with. Breeders working across a range of production environments in the eastern Mediterranean have found that a general shift in the type of pathogen occurs where the crop biomass increases from an equivalent (in barley and wheat) yield of less than 1-2 t ha-1 to over some 3 t ha-1 (Ceccarelli et al., 1992; Hamblin, AI-Taweel, Yau and Walker, unpublished data). Lower yielding environments are, in rainfed conditions, typified by abiotic stresses in the soft;

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water deficiency or excess, nutritional imbalance and root pests and diseases. Higher yielding environments (with irrigation or higher, more reliable rainfall) are typified by biotic constraints deriving from the humid microclimate of the crop, and the specific attributes of the plant canopy in relation to radiation capture. They are the pre-eminent focus of leaf pests and diseases. Thus, where improvements in the production systems of low-yielding environments (through wide rotations, increased nutrition, retention of mulches and other soil structural improvement practices) increase the crop biomass to 8-10 t ha-1 of dry matter, leaf fungal pathogens increase in significance, whereas with the reduction of inputs in currently high-input systems in the Netherlands and Denmark as a result of their pesticide reduction programme, there may be a progressive scaling back in plant populations and lowering of fertilizer input to match, and a possible resumption of root pathogen problems.

VI. CONCLUSIONS Few natural, and almost no agricultural, ecosystems would today qualify for being in a 'steady-state' condition, physically, chemically or microbially. Over the past 40 years novel germplasm has been widely introduced into all but the most remote food production systems and many plantation and perennial grazing systems; there has been a significant narrowing of the genetic base in most commercially produced plant and animal varieties; a rapid increase in the use of inorganic fertilizers and pesticides; cultural changes that have included narrowing of rotational practices, the development of extensive monocultures, increasing mechanization and expansion of irrigation. In addition there has been a massive expansion into low-productivity environments in the tropical and subtropical regions as the result of population pressure and the continuing belief in agriculture as the engine to economic growth (World Bank, 1989). Add to these changes the more subtle environmental effects such as loss of remnant native vegetation habitats, hedgerows in Europe, wetlands in North America, and 'bush' reserves in the southern continents, which provided predator niches and influenced the microclimates of adjacent arable lands, and we can appreciate the extent and unprecedented rate at which agriculture's biophysical environment has been perturbed. Current scientific strategies to maintain and improve yields in support of high-input agricutture place great emphasis on 'fail-safe' techniques for each component of the production sequence with little consideration of the integration of these componeats in a holistic, systems approach. Research for sustainable agricultural practices requires a far greater emphasis on such an approach than is now fashionabl,.', despite all the rhetoric given politically to sustainability. It requires every scientist to step outside his or her field of specialization, develop common goals and methods of communication, and consider a much wider set of spatial and temporal scales and interactions than is usual. Perhaps before

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all this is possible, there must be an emotional and mental disengagement from the conventional mind-set which seeks to achieve supremacy over every pathogen for higher and yet higher yields, and replaces it with a goal of increased product diversity, increased profit per unit of input, and increased stability of production.

REFERENCES Allen, D.J. (1983). 'The Pathology of Tropical Food Legumes: Disease Resistance in Crop Improvement'. Wiley Interscience, Chichester. Australian Agricultural Council. ( 1991). ' Sustainable Agriculture'. Report of the Working Group on Sustainable Agriculture. Standing Committee on Agriculture Technical Report Series 36. CSIRO, Melbourne. Brown, H. D. and Schoen, D.J. (1992). Plant population genetic structure and biological conservation. In 'Conservation of Biodiversity for Sustainable Development' (O. T. Sandlund, K. Hindar and A. H .D. Brown, eds), pp. 88-104. Scandinavian University Press, Oslo. Ceccarelli, S., Grando, S. and Hamblin, J. (1992). Relationship between barley grain yield measured in low- and high-yielding environments. Euphytica 57, 49-58. CIMMYT (1989). see International Maize and Wheat Improvement Centre. Clements, R.J., Rosielle, A.A. and Hilton, R. D. (1992). 'National Review of Crop Improvement in the Australian Grains Industry'. A report to the Board of the Grains Research and Development Corporation, Canberra. Conway, G. (1981). Man and pests. In 'Theoretical Ecology: Principles and Applications' (R.M. May, ed.), pp. 161-178. Blackwell, Oxford. Conway, G. (1985). Agroecosystem analysis. Agricultural Administration 20, 31-55. Consultative Group on International Agricultural Research, (CGIAR) (1992). 'Review of CGIAR Priorities and Strategies - Part 1. CGIAR'. The World Bank, Washington (unpublished). Corey, S. A., Dall, J. D. and Milne, W. M. (1993). 'Pest Control and Sustainable Agriculture', CSIRO, Melbourne. Cullen, J. M. (1993). Opportunities and challenges in biological control. In 'Pest Control and Sustainable Agriculture' (S. A. Corey, J. D. Dall. and W. M. Milne, eds), pp. 44-50. CSIRO, Melbourne. Daly, H. E. (1988). On sustainable development and national accounts. In 'Economics, Growth and Sustainable Environments' (D. Collard, D. Pearce and D. Ulph, eds), pp. 38-56. MacMillan, London. Damuth, J. (1987). Interspecific allometry of population density in mammals and other animals; the independence of body mass and population energy use. Biology Journal of the Linnean Society 31, 193-246. Erwin, T. L. (1982). Tropical forests; their richness in Coleoptera and other arthropod species. Coleopterist's Bulletin 36, 74- 75. European Community (1992). 'Revised Common Agricultural Policy'. EC, Brussels. Food and Agriculture Organization (FAO) (1980-90). Annual Yearbooks for 'Fertilizer Use' and 'Food Production Statistics'. FAO, Rome. Food and Agriculture Organization (FAO) (1989). 'Environment and Agriculture; Environmental Problems Affecting Agriculture in the Asia and Pacific Region'. World Food Day Symposium, 11 October 1989. FAO Regional Office for Asia and the Pacific, Bangkok. Forrester, N. W. (1990). Resistance management in Australian cotton. In 'The Australian

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Cotton Industry Under the Microscope', pp. 361-368. Fifth Australian Cotton Conference, August 8-9th, 1990. Broadbeach, Queensland. Frey, K.J. (1976). Breeding concepts and techniques for self pollinated crops. In 'International Worshop on Grain Legumes' January 13-16, 1976, pp. 257-278. ICRISAT, Hyderabad. Georghiou, G.P. and Lagunes-Tejeda, A. (1991). 'The Occurrence of Resistance to Pesticides in Arthropods. An Index of Cases Reported Through 1989'. Food and Agriculture Organization of the United Nations, Rome. Hamblin, A. and Kyneur, G. (1993). 'Trends in Wheat Yields and Soil Fertility in Australia'. Bureau of Resource Sciences, Australian Government Publishing Services, Canberrra. Hamblin, J., Rowell, J . G . and Redden, R. (1976). Selection for mixed cropping. Euphytica 20, 97-106. Harlan, J. R. (1976). Diseases as a factor in plant evolution. Annual Review of Phytopathology 14, 31-51. Holdgate, M. W. (1991). Conservation in a world context. In 'The Scientific Management of Temperate Communities for Conservation' (I. F. Spellberg, F. B. Goldsmith and M. G. Morris, eds), pp. 1-26. Blackwell, Oxford. HoUing, C.S. (1973). Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4, 1-24. Holmes, R. (1993). The perils of planting pesticides. New Scientist 1888, 34-37. Huber, D. M. and McCay-Buis, T. S. (1993). A multiple component analysis of the takeall disease of cereals. Plant Disease 77, 437-447. Hurst, P. (1992). 'Pesticide Reduction Programmes in Denmark, the Netherlands and Sweden'. World Wide Fund International in collaboration with the Pesticides Trust, London, Gland, Switzerland. International Maize and Wheat Improvement Centre. (1989).' 1987-88 CIMMYT World Wheat Facts and Trends, the Wheat Revolution Revisited: Recent Trends and Future Challenges'. CIMMYT, Mexico, DF. Johnson, R. and Law, C. N. (1975). Genetic control of durable resistance to yellow rust (Puccinia striiformis) in the wheat cultivar Hybride de Bersee. Annals of Applied Biology. 81, 385-391. MacArthur, R . H . and Wilson, E.O. (1967). An equilibrium theory in insular zoogeography. Evolution 17, 373-387. McIntosh, R. A. (1992). Close genetic linkages of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathology 41,523-527. Marten, G. G. (1988). Productivity, stability, sustainability, equitability and autonomy as properties for agroecosystem assessment. Agricultural Systems 26, 291-316. May, R. M. (1988). How many species are there on earth? Science 241, 1441-1449. May, R. M. (ed). (1981). 'Theoretical Ecology: Principles and Applications', 2nd edn. Blackwell, Oxford. Ministry of Agriculture, Fisheries and Food, (MAFF). (1978). 'Maximising Yields of Crops'. Proceedings of a Symposium of the Agricultural Development and Advisory Service and the Agricultural Research Council, 17-19 January, 1978. HMSO, London. Organization of Economic Development and Co-operation. (1980-1990). 'Agricultural Policies, Markets and Trade Monitoring Outlook'. OECD, Paris. Organization of Economic Development and Co-operation, (OECD). (1992). 'Agents for Change'. OECD Workshop on Sustainable Agriculture, Technology and Practices, Paris, February 11-13, 1992. OCDE/GD (92)49, OECD, Paris. Pearce, D., Markandya, A. and Barbier, A. B. (1989). 'Blueprint for a Green Economy'. Earthscan, London.

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Pieri, C. V. M-G. (1992). 'Fertility of Soils and the Future of Farming in the West African Savannah'. Springer Verlag, Berlin, Heidelberg. Pimentel, D. (1993). Cultural controls for insect pest management. In 'Pest Control and Sustainable Agriculture' (S. A. Corey, J. D. Dall and W. M. Milne, eds), pp. 33-38. CSIRO, Melbourne. Pimentel, D., McLaughlin, L., Zepp, A., Lakitin, B., Kraus, T., Kleinman, P., van Ceni, F., Roach, W. J., Graap, E., Keeton, W. S. and Selig. G. (1991). Environmental and economic impacts of reducing U.S. agricultural pesticide use. In 'Handbook of Pest Management in Agriculture', Vol. 1, pp. 679-719. CRC Press, Boca Raton, FL. Powles, S. B. and Matthews, J. M. (1992). Multiple herbicide resistance in annual ryegrass (Lolium rigidum). A driving force for the adoption of integrated weed management. In 'Achievements and Developments in Combating Pest Resistance' (I. Denholm, A. Devonshire and D. Holloman, eds), pp. 1-13. Elsevier, London. Rabbinge, R. (1991). 'Perspectives for Rural Areas in the European Community'. Presentation to the Council of Ministers. October 1 1991. WRR, The Hague. Roelfs, A. P. and Bushnell, W. R. (1985). 'The Cereal Rusts. Vol 2. Diseases, Distribution, Epidemology and Control'. Academic Press, Orlando. Sandlund, O. T., Hindar, K. and Brown, A. H. D. (1992). 'Conservation of Biodiversity for Sustainable Development'. Scandinavian University Press, Oslo. Science Council of Canada. (1991). 'It's Everybody's Business'. Publications Office, Science Council of Canada, Ottawa. Strange, R.N. (1993). 'Plant Disease Control: Towards Environmentally Acceptable Methods'. Chapman & Hall, London. Wellings, C. R. and McIntosh, R. A. (1990). Puccinia striiformis f.sp. tritici in Australasia: pathogenic changes during the first 10 years. Plant Pathology, 39, 316-325. Wilson, E. O. (1988). 'Biodiversity'. National Academy Press, Washington, DC. Wolfe, M. S. (1987). Trying to understand and control powdery mildew. In 'Populations of Plant Pathogens: their Dynamics and Genetics' (M. S. Wolfe and C. E. Caten, eds), pp. 253-277. Blackwell, Oxford. World Bank (1989). 'Renewable Resource Management in Agriculture. A World Bank Operations Evaluation Study'. Operations Evaluation Department, The World Bank, Washington, DC. World Bank (1992). 'Development and the Environment'. World Development Report 1992. Oxford University Press, New York. World Commission on Environment and Development. (1987). 'Our Common Future'. Oxford University Press, Oxford. World Resources Institute. (1992). 'World Resources 1992-93'. Oxford University Press, New York. Zadoks, J. C. (1993). Antipodes on crop protection in sustainable agriculture. In 'Pest Control and Sustainable Agriculture', (S. A. Corey, D.J. Dall and W. M. Milne, eds) pp. 3-12. CSIRO, Melbourne.

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2 PREHISTORIC AGRICULTURAL METHODS AS MODELS FOR SUSTAINABILITY William M. Denevan Department of Geography, University of Wisconsin, Madison, Wisconsin 53706-1491, USA

I. Introduction II. Literature Review III. Forms of Prehistoric Agriculture A. Shifting Cultivation B. Rainfed Cultivation C. Agroforestry-Garden-Field Crop Integration D. Dryland Farming E. Terracing F. Drained Fields IV. Soil and Pest Management A. Soil Fertility B. Pests V. Sustainability vs. Collapse VI. Conclusions References

21 22 23 23 24 25 26 27 29 31 31 32 33 37 39

I. I N T R O D U C T I O N In recent years scholars have argued that agricultural methods employed in prehistoric times could serve as models for sustainable agriculture today (Denevan, 1980a; Smith, 1987; Treacy, 1989; Erickson, 1992). Many such methods continue in use (terracing, irrigation), by both modern (fossil-fuel based) and traditional farmers. What are particularly instructive are production systems that originated in prehistory and continued in place for long periods of time, thus demonstrating sustainability. Such methods and systems will be examined here. Many early crop systems, of course, ultimately did collapse owing to environmental change, excessive pressure on the agricultural environment, or social breakdowns. On the other hand, some ancient agricultural systems have continued in production to the present. 'Prehistory' here will refer to before 1492 for the New XJVorld and a more arbitrary BC for the Old World (Barker, 1985), without being bound strictly for ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rights of reproductionin anyform reserved

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either. By'agriculture' I refer to all forms of planting and managing crops (which may or may not be fully domesticated). By 'methods' I mean the techniques used to construct crop fields, to plant them, and to manipulate the physical character of the crop environment (soil, water, slope, microclimate, plant and animal competition, and disease). By 'model' I mean viable methods which are instructive for making present agriculture more sustainable. By 'sustainable' I refer to methods and agroecosystems based on local inputs and on recycling, to potentially continuous duration, and to a deterioration of the resource base which is manageable or reversible. The topic is enormous and has received considerable attention, especially in the last 25 years as the result of the discovery of vast remains of ancient fields throughout the world, primarily by means of aerial photography. Here I only attempt to provide a general view of prehistoric agroecological systems and methods (forms, functions, extent, antiquity), plus some brief case studies of agricultural collapses. The focus is on field technology, not on crops themselves. In the Conclusion, I comment on the relevance of prehistoric agricultural methods to agricultural development today. A lengthy bibliography leads the reader to further information and analyses.

II. LITERATURE REVIEW

Surveys of prehistoric agricultural technology are relatively few and are mostly recent. Books and articles on the topic before 1952 are remarkably simplified, speculative, and inaccurate. Entire systems of cultivation are unmentioned. Treatments of prehistoric agriculture often gave much more attention to crop domestication (e.g. Struever, 1971; Bender, 1975). This reflected minimal interest in early agricultural technology by archaeologists and historians. However, this has now changed dramatically, especially in the New World where there have been major interdisciplinary projects on pre-Columbian cultivation practices. Classical descriptions of the methods of ancient agriculture include the works of Hesiod, Xenophon, Varro, Cato, and Columella (Fussell, 1972). Butzer (1994) diagrams the evolution of Classical Greek and Roman writing on agronomy, 700 BC to AD 600, in his excellent discussion of Islamic traditions of agroecology. Prior to 1952 modern descriptions of prehistoric agricultural practices were mainly brief sections of regional studies. Two noteworthy exceptions were 'Farmers of Forty Centuries' on East Asia by King in 1911 and Latcham's 1936 book on the Andes. Examples of specific topical and regional studies include Schilling (1938) on the chinampas of Mexico, Cook (1916) on Peruvian terraces, Bryan (1941) on the southwest USA, and Curwen (1938) and others on northwest Europe. Several important studies were published in the mid 1950s, and research has since accelerated. 'Plough and Pasture: The Early History of Farming' by

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Curwen and Hatt (1953), was the first book-length modern synthesis. A briefer review the same year was 'Conquest of the Land Through Seven Thousand Years', by Lowdermilk (1953). Volumes were published on soil and civilization by Hyams (1952) and by Carter and Dale (1955). These were followed rapidly by articles on qanats (Cressey, 1958), terraces (Spencer and Hale, 1961), and irrigation (Steward, 1955; Wittfogel, 1957). The first survey of prehistoric agriculture in the New World was by Armillas in 1961. A classic history of husbandry is 'The Care of the Earth' by Lord (1963). We now have a large number of regional studies and surveys and reports on particular techniques, reflecting an increased archaeological focus on remnants of ancient fields. Some of the most useful regional syntheses and collections include: Bradley (1978), Mercer (1981), Fowler (1983) and Barker (1985) on northwest Europe; Evenari et al. (1971) on the Negev; Hutterer (1983) on Southeast Asia; Raychaudhuri (1964) on India; Harrison and Turner (1978) on the Maya; Denevan etal. (1987) on the Andes; Doolittle (1992) on North America; Smith (1987) and Denevan (1980c) on Latin America; Denevan (1980b), Matheny and Gurr (1983), and Scarborough and Isaac (1993) on the Americas; Rojas (1988) on Mexico; Farmington (1985)on the tropics; Killion (1992) and Whitmore and Turner (1992) on Mesoamerica; and Woods (1992) on the midwest USA. Books on specific field systems include Kosok (1965) on irrigation in Peru; Darch (1983) on drained fields in Latin America; Siemens (1989) on raised fields in Mexico; Donkin (1979) on New World terraces; Doolittle (1990) on irrigation in Mexico; Rojas (1983) on chinampas in Mexico; Turner and Harrison (1983) on raised fields in Belize; and Turner (1983) on terraces in Yucaffm.

III. FORMS OF PREHISTORIC AGRICULTURE Agiculture can be classified into a few basic types based on environmental manipulation for the purpose of improving conditions for crop gowth. For prehistoric times these forms can be determined from field remnants which can be measured and studied archaeologically and in their environmental context. Additional information can be derived from artistic representations, early writing, and from inference from ethnohistoric or ethnographic analogy.

A. Shifting Cultivation One of the most widespread forms of agriculture, past and present, is the alternation of short periods of cultivation with longer periods of grass, scrub, or forest fallow which permits soil recovery and reduction of pest competition. This technique is sustainable under a modified forest cover as long as the fallows are sufficient. However, population densities (under 30 per kmZ) and productivity per area are relatively low. Shifting (swidden) cultivation occurs on good as well as

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poor soils, its advantage being labor efficiency, given plentiful land (Boserup, 1965). Relatively little labor is required to clear forest in contrast to the labor needed to practice permanent cultivation requiring soil fertility maintenance, water management and pest control. The problem with describing prehistoric shifting cultivation is that it is almost impossible to demonstrate its occurrence. Swidden fields leave no physical signature and hence their past presence can only be inferred. Pollen and other studies can demonstrate forest clearance, but cannot indicate whether cropping was permanent or shifting. The same is true of sediment transfer studies which indicate accelerated erosion from deforestation. An argument can be made that long-fallow shifting cultivation was not at all common when forest clearing was by stone axes, which are very inefficient compared to metal axes (Denevan, 1992), especially for large trees and hardwood trees such as are found in tropical forests. Clearing would have concentrated on light woody vegetation, softwoods, and young secondary formations. Once cleared of forest, near-permanent cultivation rather than shifting cultivation was likely, especially on good softs. Once a plot was opened it was probably more efficient to maintain it permanently or semi-permanently in crops by means of high labor inputs to combat pests and to maintain soil fertility than it was to practice shifting cultivation. Fire may have been a more important means of forest removal in Europe than clearing with either stone or early metal axes. However, it has been demonstrated experimentally that deciduous forest could have been cleared in Neolithic Europe with flint stone axes (Iverson, 1956). Whatever the means of clearing, patterns of village abandonment in Denmark suggest that early fields remained in production for 50 years or so (Iverson, 1956). Rowley-Conwy (1981) provides a convincing argument that Neolithic agriculture in Europe was primarily permanent not shifting, made possible by usually being located on good soil (also Vasey, 1992). Efficient bronze axes do not appear in Europe until after 2000 BC, and there were no metal tree-cutting axes in the Americas until after 1492. Doolittle (1992) believes that shifting cultivation was rare in prehistoric eastern North America.

B. Rainfed Cultivation

Rainfed cultivation is the most common form of agriculture, here referring to cropping dependcnt on adequate rainfall, good soil fertility, and relative permanence. It was the usual form of temperate agriculture in Europe and Asia, based on various types of soil turning tools. The oldest traction plows date to about 3000 BC in Mesopotamia (Curwen and Hatt, 1953:64). There were no traction plows in the Americas until after 1492, although foot plows were used in the Andes (Gade and Rios, 1972). The earliest agriculture in western Europe was based on digging sticks, hoes, and footplows. The light plow (ard, spade plow, coulterless plow) appears by 1000 BC in Britain. It could be used only on well-drained soils, usually upland, and is

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associated with the so-called 'Celtic' field system of square plots, which continued into the Roman period. This cultivation was based on the use of manure and humus transport, rotation of crops, and periodic fallow. The life span of some field systems was several hundred years (Curwen and Hatt, 1953; Bradley, 1978). Iron plowshares and heavy plows (coulter plows) capable of plowing ridges in heavy bottomland soils appear in Britain by 100 BC, creating narrow strip fields. By the Middle Ages a characteristic three-field system prevailed with rotation of wheat with barley-oats-beans and with pasture. Most early rainfed agicuhure is difficult to identify on the landscape because usually it was ephemeral and left no traces after lengthy abandonment or destruction of plow traces by later cultivation activity. An exception is the lynchet, many of which have survived to the present in northwest Europe. Lynchets were created by both non-plow and light-plow cultivation. By breaking the soil, soil moved to the lower edge of slope fields creating low ridges. Some of the lynchets produced by the light plow are very high (4 m) indicating lengthy cultivation by a settled population (Curwen and Hatt, 1953:66). Some surface and buried plow marks made by the light plow and by spades occur in uplands (Bradley, 1978; Halliday et al., 1981). Ridge and furrow patterns created by the coulter plow in Medieval times survive in many parts of western Europe (Beresford, 1948). These various plow marks are indicative of permanent fields.

C. Agroforestry-Garden-Field Crop Integration In tropical forests especially, field systems may be less clearly defined than elsewhere. Farmers rely on different strategies simultaneously, and over time a plot of land may rotate through a sequence of varied forms of management. These can include horticultural polyculture fields, swiddens, house gardens, managed fallows, and forest manipulation of both wild and cultivated plants. A single household may be involved in all of these as a means of food security. The diversity and rotation of systems and plants also permits environmental protection and recovery, whether intentional or a byproduct. Current examples of such integrated agroforestry systems in the Americas have been described for the Bora in eastern Peru (Denevan and Padoch, 1988) and for other tribes (Alcorn, 1989, 1990). The Huastec, for example, have a ' sequential agroforestry system' or 'working succession', in which 'there is a mosaic of maize fields, gardens, (managed) fallow thickets, and forested plots', involving deforestation and forest recovery over 15-20 years (Alcorn, 1990). Over time, the forest associated with such a system becomes an anthropic forest in which species composition, density, and distribution are to a large extent determined by human activity. Such 'economic' forests may have a reduced biodiversity and biomass, but they nevertheless are forests, forests that are sustainable and protective of soil, water and wildlife, in contrast to sites where forests are converted to grassland and scrub.

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It is difficult, however, to identify such integrated systems of land use in prehistoric times, since little physical evidence has survived. The argument is mostly inferential (Alcorn, 1981; Gordon, 1982; G6mez-Pompa and Kaus, 1990). Stone walls forming compounds around ruins of Mayan houses probably contained house gardens, as they do today. The current unnatural concentrations of economic plant species in forests have been attributed to a long history of human forest manipulation in Yucauln, Central America, and elsewhere. Large quantities of fruit pollen in the archaeological site of Araracuara on the R~o Caquet~ in the Colombian Amazon suggest fruit orchards or agroforestry (Fernanda Herrera etal., 1992). Also, a reliance on inefficient stone axes, as mentioned earlier, would seem to have encouraged small permanent fields and gardens and forest management rather than shifting cultivation (Denevan, 1992). Integration of field, garden, and forest could have been productive, protective, and sustainable and it was probably common prehistorically in the tropics as well as elsewhere. Surviving examples provide models for ecologically viable production systems under difficult soil and climatic conditions.

D. Dryland Farming Lawton and Wilkie (1979) indicate five forms of dryland farming, and others can be added (also see Scarborough, 1992). The first is 'dry farming' in which fields are often planted but are only harvested when there has been adequate rainfall. Dry farming can be inferred for prehistory, and was probably common, but no archaeological evidence survives. It may date to 5000 BC on the fertile loess softs of Shensi Province, China (Lawton and Wilkie, 1979:24). 'Runoff farming' occurs where fields are located to receive runoff from adjacent, unprepared slopes into natural catchment basins or into plots surrounded by stone or earthen walls, such as in the Anasazi southwest USA (AD 200-1500) (Vivian, 1974). Stonewall check dams across intermittent streams (wadis, arroyos) trap water (and soft) for small garden plots. Prehistoric check dam remnants are common in the Middle East (Evenari etal., 1971) and the southwest USA/northwest Mexico (Doolittle, 1985). 'Water harvesting' refers to the concentration of runoff from prepared watersheds, cleared and compacted, and directed by stone walls. This has been described by Evenari et al. (1971) for the Negev Desert where it dates to 1000 BC and irrigated 300 000 ha during Nabataean times (250 B C - A D 630). Evenari has attempted to re-establish this system at the ancient sites of Shivta and Avdat. 'Floodwater farming' refers to flood plains planted in crops after flood waters have receded or where fields are watered by flash floods on alluvial fans. A variation is 'recessional' or 'decrue' farming (Vasey, 1992:119-120) in which moist river banks are planted as river levels drop. Such 'natural irrigation' undoubtedly preceded canal irrigation but there is little archaeological evidence. In Egypt, there was 'artificial floodwater farming' along the Nile. The area cultivated was

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increased by controlling the length of time water remained in natural flood basins by means of dams, dredging, deepening overflow channels, and digging ditches to breach natural levees; the earliest evidence is c. 3100 BC or Late Predynastic (Butzer, 1976:19-21). 'Irrigation farming', or canal irrigation, involves the artificial transfer of water from source to field via canals fed by a regulated, reliable source of water. Enormous complex systems developed early involving dams, reservoirs, headgates, diversion embankments, terraces, and other features. Prehistoric irrigation was widespread throughout the arid lands of the Mediterranean and Middle East, extending to China, and including the padi systems of wetlands in East and Southeast Asia. In the New World, irrigation extended from Colorado to central Chile. Because remains of ancient canal structures are so widespread in arid lands and are associated with early civilizations, irrigation is probably the best studied form of prehistoric cultivation. Canals reflect sophisticated engineering skills and massive labor inputs. In Iran, small-scale ditch irrigation dates to 5500 BC, and by 700 BC large complex irrigation systems had been developed (Lawton and Wilkie, 1979). In the Middle East subsurface canals/chains of wells (qanats) date to at least 500 BC in I r a n - I r a q - T u r k e y (English, 1968). Irrigation canals and reservoirs were developed in central Mexico by 600-700 BC, in coastal Peru by 400 BC, and by the Hohokam culture of Arizona by 300 BC (Lawton and Wilkie, 1979; Doolittle, 1990). There are other ancient types of dryland farming. 'Sunken fields' in Peru include pukios, or depressions dug down to the water table in coastal valleys, and cultivated cochas, or artificial ponds that collect rainfall on the Lake Titicaca plain. Rock mulches, piles of or strips of rocks or layers of gravel, occur by the hundreds of thousands in the Negev (Evenari et al., 1971), in the southwest USA (Lightfoot, 1993), and elsewhere. 'Manual irrigation' involves the transfer of water directly from lakes or rivers (or wells) by hand (splash irrigation and container or pot irrigation) or by simple lift devices such as the shaduf (pole and bucket lever) in the Middle East and the water wheel. In Egypt, buckets were used by 3000 BC, the shadufby 2700 Be, and water wheels by 300 BC (Lawton and Wilkie, 1979).

E. Terracing Agricultural terraces serve to control erosion, increase soil depth, modify microclimate, and especially to help manage irrigation water on slopes. In fact, the distribution of terraces corresponds closely to the distribution of dry-land irrrigation, although there are rainfed terraces, especially in the Asian wet tropics. The distribution of prehistoric terraces fairly well matches the present distribution of cultivated terraces, given that most terraces originated in prehistory (Fig. 1). While there are considerable differences in terrace form, size, and organization, the two basic types are sloping-field terraces, usually rainfed, and bench

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Fig. 1. Prehistoric terraces still in cultivation, Pisac, Peru (photographed by R. Shippee and G. Johnson in 1931, reproduced by permission of the American Museum of Natural History).

terraces which are flat floored with vertical back walls and which are usually irrigated by an associated canal system. Bench terraces may have evolved as a response to uncertain or decreased rainfall (Donkin, 1979). Thus, in contrast to other forms of ancient agriculture whose non-sustainability was related to climatic change or human-induced environmental problems (deforestation, siltation, erosion, or soil decline caused by population pressure on the land), terracing actually evolved as a means of controlling these problems and changes. Because terrace walls frequently collapse and must be repaired, and because the terrace field itself is disturbed by cultivation, dating is difficult. Irrigated bench terraces (padi rice) were probably in use in China by 2500 ac (Hallsworth, 1987). Wadi check-dam terraces were in use in the Negev by 2000 BC (Evenari et al., 1971). In the New World in central Mexico and Peru, terraces date to 500-600 8c (Donkin, 1979). Some of the most impressive ancient terracing, in terms of size, stone work, and extent (over 1 million ha) is in the Andes, described by numerous sixteenth century writers. For example, Garcilaso de la Vega (1966:241-242) wrote: In order to make these terraces they would construct three walls of solid masonry', one in front and one at each end. They sloped back slightly.., so as to withstand the weight of earth with which they are filled to the level of the top of the walls.

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Above the first platform they built another smaller one, and above that another still smaller.., like stairs in a staircase, and all the cultivable and irrigable land being put to use. If there were rocky places, the rock~ were removed and replaced by earth brought from elsewhere to form the terraces. F. Drained Fields

Prehistoric drained fields have received less attention than other forms of ancient intensive agriculture. Recent discoveries indicate that drainage technology was widespread, but the technique is now entirely abandoned in many areas of former occurrence. Drainage of periodically flooded terrain or lake and river margins was accomplished by ditching, artificial raised fields or beds (mounds, ridges, platforms), or a combination of both. Some of the platform fields are enormous - up to 25 m wide, 400 m long, and 2 m high (Denevan, 1970). Early drainage for agriculture was undertaken in Roman England (Fens), by the Etruscans in Italy (Pontine Marshes), and in the ninth century AD in the Netherlands (polders) (Wagret, 1968). However, remains of older and more extensive systems of raised fields and canals have been found in the tropical lowlands of Asia and Latin America and in highland basins in Mexico and the Andes from Colombia to Bolivia. A system of dug drains, apparently for agriculture, has been uncovered beneath peat in Kuk Swamp in highland Papua New Guinea, which dates to about 7000 BC and continued with interruptions to the present (Golson, 1977). If correct, this would be one of the oldest dates for water-managed fields anywhere. Raised fields on the shores of Lake Titicaca (waru waru) date to c. 850-800 BC (Kolata, 1993:215), and those in the Basin of Mexico (chinampas) are at least 1500 years old. Large zones of tropical prehistoric raised fields occur in the Mayan lowlands of Mexico-Belize, upper Amazonia in Bolivia, the Venezuelan Llanos, the Guayas Basin of Ecuador, northern Colombia, and the Guiana coast (Fig. 2). Declining soil fertility was not likely a factor in sustainability. Organic muck rich in decomposed aquatic vegetation and wild life, algae and silt was transferred periodically from the ditches to field surfaces, making continuous cultivation possible, even where natural soils were of low fertility. This has been demonstrated by excavations of prehistoric raised fields at Lake Titicaca; in addition, remains of fish were spread over those fields and plant residues and dung were probably also used (Kolata, 1993; Carney et al., 1993). Experimental raised fields at Titicaca gave potato yields of 8-16 t ha compared to only 1-6 t on comparable flat-surface fields (Erickson, 1993; Kolata, 1993). Other functions of raised fields in addition to drainage and fertility management include frost induction (water in ditches acts as a heat sink, releasing energy at night) in highland regions, improved aeration and tilth, and reduction of weeds, insects, and pathogens (Kolata, 1993). A small form of raised field (1-2 m wide), not usually associated with poor drainage, is the garden bed or lazy bed, found in many parts of the world, past

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Fig. 2. Abandoned prehistoric raised fields, Llanos de Mojos, Bolivian Amazon (T. English, Bristow Helicopters Inc. 1961, provided by W. M. Denevan).

and present. Prehistoric remnants have been found in Ireland dating to 2000 BC (Fowler, 1983) and in Wisconsin and Michigan in the USA dating to 1100-1200 AD (Gallagher, 1992). Several hundred sites have been reported in the USA since the nineteenth century, but most have now been destroyed. Functions were likely similar to those of the larger raised fields. A variation is the Indian corn hill, a

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practice that continued after European settlement; remains of a few of these still survive (Gallagher, 1992). All the large New World raised fields have long been abandoned, except for a few sectors of chinampas at the edge of Mexico City. Most of the relic fields are in remote areas, now largely depopulated, which may explain abandonment either before or after European arrival. Changing climate and water regimes could also have been factors. Remnants of millions of raised fields survive in the Americas. They stand out clearly from the air, even when little relief remains, and they are easily mapped from air photos. They cover 122 000 ha of ditch and field surface at Lake Titicaca (Erickson, pers. comm.) and over 9 0 0 0 0 h a in the San Jorge savannas of northern Colombia (J.J. Parsons, pers. comm.), with lesser extents elsewhere. Large sectors of raised fields have been destroyed by human activity, burial under sediment, and by erosion. They are a lost system of agriculture in Yucat~in and in South America, but they once helped feed the Classic Maya civilization and the Tiwanaku empire in Bolivia. Several attempts at restoration have been made, the most successful being on both the Peruvian and Bolivian sides of Lake Titicaca - over 1000 ha of fields in over 50 communities - thanks in large part to the efforts of archaeologists Erickson and Kolata.

IV. SOIL AND PEST MANAGEMENT For an agricultural system to be sustained, several critical components of the agro-ecosystem must be controlled, including water, soil depth and fertility, and pests (weeds, insects, animals, pathogens). We have already discussed means of water control and erosion control. Fertility and pest control merit separate attention.

A. Soil Fertility The use of fertilizer to maintain or improve soil fertility may be nearly as old as agriculture itself, but it is difficult to demonstrate archaeologically unless there are chemical or biological indicators. Most important were organic additives: human and animal wastes, ash, garbage, crop residues, leaves, compost, cleared weeds, seaweed, mulch, urine, stable straw, ant-nest refuse, turf and muck. Manure, including human waste and compost, was used in India and China at least by 500 BC (Raychaudhuri, 1964; Thurston, 1992). The Chinese developed its use into a high skill 'which made agriculture permanent' (Curwen and Hatt, 1953; also see King, 1911). Manure was used by the early Greeks (Mather and Hart, 1956). In Europe, stable dung was the common manure, and manuring was also accomplished by grazing livestock on stubble or by folding (rotating pens

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on fields). Manuring was common during the Iron Age (Vasey, 1992). Roman farmers were competent in using various manures. Forms of early manuring in northern Europe are described by Fenton (1981). There are numerous sixteenth century descriptions of Inca use of fertilizers in Peru. Guano was applied on coastal fields and was transported by llama caravan for at least short distances into the interior (Julien, 1985). Fish were also used for fertilizer on the coast (Donkin, 1979). In the Andes, llama dung was used to fertilize potato crops, and there is one report of human manure (Garcilaso de la Vega, 1966). In highland Mexico, a soldier of CortSz reported stacks of human waste along the Aztec roads, probably for use as fertilizer (Armillas, 1961). Organic muck from the ditches between chinampas in Mexico was used as a fertilizer (Armillas, 1971; Wilken, 1987). The sunken fields of coastal Peru were fertilized with amendments of decomposing vegetation according to Latcham (1936). Inorganic additives were also transported short distances to fields, including silts, nitrates and ash in Bolivia (Soria Lens, 1954:92) and silt trap fields were cultivated in Peru and Mexico. In the Colombian Amazon at Araracuara (AD 800), alluvial sediments were transferred from flood plains to bluff top farms; organic wastes were also added (Fernanda Herrera etal., 1992). In the Brazilian Amazon prehistoric settlement sites with rich black anthropogenic softs (terra preta) were sought out by farmers (Smith, 1980). Green manuring (planting of nitrogen-fixing legumes) is difficult to identify archaeologically; however, the interplanting of beans served this function and was widespread in both the Old and New Worlds. An Inca fertilizer practice near Cuzco (now rare) is that of llakoshka, which increases yields by 20% or more (Anonymous, 1985). Seeds are dipped into a putrefying and fermenting mixture of dried llama dung, salt, and chicha (maize beer), and sometimes juice from the fruit of the molle tree (Schinus moUe). Resulting biochemical processes make inorganic elements in the soil more easily assimilated; parasites and aerobic organisms are destroyed; an anaerobic bloom is created; the dung provides nutrients for the seedlings and root system; yeast from the chicha turns seed starch to sugar which is advantageous to root development; plus there are other positive effects.

B. Pests

It is also virtually impossible to determine means of pest control through archaeology, and early written descriptions are rare. We can infer that crop losses were minimized by intercropping numerous species and varieties in each field. Also, a certain amount of crop loss was simply tolerated and compensated for by having larger fields, as long as land was plentiful. However, the biblical plagues of locusts were not myths and crop destruction was periodically devastating.

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An excellent study by Thurston (1992)examines traditional practices of plant disease management. Most examples are contemporary, but they are suggestive of prehistoric methods. There are some specific examples from the past of plant pathogen control. Homer (eighth century BC) mentioned 'pest averting sulfur'; Pliny (420 BC) reported that amurca (liquid waste) of olives was applied to plants to prevent blight; and other Greeks and Romans mentioned the use of amurca to control plant diseases and insects and as a fertilizer; Cato (200 BC) suggested burning sulfur to fumigate trees; ashes were used to control plant disease in ancient India (Thurston, 1992). Biological control of diseases particularly included multicropping. The use of manure and other organic additives was a common means of control. In China c. 300 BC, farmers used the yellow citrus ant to protect citrus fruit (Thurston, 1992). On the north coast of Peru, farmers today use lady bugs as a predator to control cotton insects, and a portrayal of a similar insect on a late prehispanic textile suggests that the practice was ancient (Vreeland, 1986). The current chinarnpa raised fields of Mexico have a reduced level of fungi and nematodes, probably because of high aquatic-related biological activity. This was also true of prehistoric raised fields in various parts of the world (Thurston, 1992). Other traditional methods mentioned by Thurston for controlling diseases include spacing, depth of planting, time of planting, disease-free soil, flooding, mulching, fallowing, and burning. Control of animal, especially bird, pests was commonly done by scare devices, crop guards and noise makers. On the other hand, large animal pests such as deer and monkeys may have been tolerated in fields so they could be more readily killed as game. The sixteenth century Peruvian chronicler and artist Guam~n Poma de Ayala (1980) depicted Inca farmers protecting crops from birds with slings, noise makers and guards. The control of weeds by traditional farmers is by shading, planting of companion plants, and removal by hand or with simple cutting tools (Altieri and Liebman, 1986). Gordon (1982) believes that in the tropics in prehistoric times, before the availability of metal machetes, weeding was more selective and less indiscriminate of the plants to be removed. Useful plants were thus allowed to survive in fields and fallows. Also, when weeds were pulled out by the roots the scattering of seeds was minimized and weed invasion thus reduced.

V. SUSTAINABILITY VS. COLLAPSE Sustainability of ancient field systems is demonstrated by continuance over long periods of time. Prehistoric agriculturalists, based on sophisticated environmental and agronomic knowledge, developed ecologically sound systems of land management that were productive, utilizing local resources and recycling. However, it is a mistake to believe that sustainable agriculture was a universal characteristic of our ancestors. There were massive crop failures and field abandonments due to

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environmental change and mismanagement, social disruptions. The following are a few examples of sustained and failed cultivation systems in prehistory under different circumstances. Lake Titicaca. The raised fields around Lake Titicaca in Peru and Bolivia were the major provider of food for the Tiwanaku civilization (AD 100-1000) and may have supported over 1 million people. They were still in use during the Inca period (AD 1450-1532), but terrace agriculture had become more important. There were earlier periods of regional abandonment. In particular, there was contraction of raised fields in the northern Titicaca basin during the expansion of raised fields during the Tiwanaku period in the south. Kolata (1993) believes that the collapse of the Tiwanaku state resulted from raised field abandonment caused by prolonged drought starting about AD 1000, as evidenced by ice cores. Erickson (1988), on the other hand, attributes field contraction to shifts in regional political power. In any event, few raised fields were still in cultivation in the sixteenth century, probably because of depopulation from European diseases. An entire agrotechnology vanished. In part, this was because the Spaniards converted the lake plain lands into cattle and sheep haciendas. One argument about the evolution and abandonment of raised fields is that this form of agriculture is extremely labor intensive and therefore is not economically practical under low population densities. Erickson (1993), however, has demonstrated that while construction labor costs are high, the maintenance costs are low, so that over a period of a decade or more, raised field cultivation is actually more labor efficient than flat-field cultivation, especially given the much higher crop yields of raised fields. Colca Valley. A large portion of terraced land in the Andes is abandoned. An interdisciplinary project in the Colca Valley (elevation c. 3500 m) in southern Peru examined the history and causes of abandonment (Denevan, 1987). Since most of the Colca terraces are irrigated, decreased precipitation has been considered the reason for large sectors going out of production (Donkin, 1979). Climatic change probably was the reason for abandonment of unirrigated sloping field terraces c. AD 500-600. However, this apparently stimulated the construction of irrigated bench terraces. If so, climatic change led to more sophisticated terracing, not a decline (Treacy and Denevan, 1994). On air photos we measured 62% terrace abandonment (Denevan, 1987). Most of this occurred in the early colonial period when the population declined by 75 % mainly from epidemics. The terraces most distant from the surviving villages on the valley floor were abandoned and remain out of use. Previously, rural settlement was more dispersed with people living on their fields or in small defensive villages on hilltops and ridges. Options for other food production or migration, given a dense regional population, were limited. People now tend to migrate and seek opportunities elsewhere rather than make large labor investments in restoring and maintaining terraces and canals in a rugged landscape. The Intravalley Canal of Peru. This is the longest (74 km) canal and one of the largest construction projects in prehistoric America (Posorski and Posorski 1982;

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Kus, 1984; Ortloff etal., 1985). It was built by the north coast Chimu state between A D 1000 and 1300 to move water from the Chicama Valley south to the Moche Valley to expand irrigated desert cultivation in the vicinity of the great Chimu city of Chan Chan. However, examination of sediments in the canal shows that the southern portion never functioned. Recent measurements of the canal indicate that some sections run uphill, as much as 31 m, making gravity flow impossible. Explanations, hotly disputed, include: (1) inept surveying, which seems improbable given known Chimu engineering skills; (2) tectonic uplift, which would have had to have been substantial over just a few hundred years or less; and (3) the canal was never intended to function, but rather was a periodic, massive public works project to keep discontented people occupied during droughts, with no concern for viability requiring the maintenance of a down-slope gradient. Regardless, if the canal had ever functioned, only a small portion of the water entering would have reached its destination given a high rate of loss due to evaporation and seepage. In addition, functioning portions of the system were periodically destroyed by floods associated with El Nifio climatic events; also river down cutting caused by both uplift and flooding resulted in cut offs of inlet canals. Today, only 35-40% of ancient irrigated lands in the Moche Valley are still under cultivation. Thus, we have explanations for ancient agricultural failure here which are technical, environmental and social, considerations which all come into play in agricultural collapses elsewhere. Ceylon. Some irrigation canal systems and associated fields were in near continuous use for very long periods. A monumental system of canals, dams (up to 30 rn high), and reservoirs (tanks) on the island of Ceylon (Sri Lanka) fed rice padi fields from AD 100-1300 (Murphey, 1957). One huge reservoir covered 2500 ha at Anuradhapura and fed fields by canal 90 km distant. This system took 1400 years to build, an incremental process characteristic of most intensive, landscaped cultivation. Production was halted by periodic invasion and resulting destruction and breakdown of management, but the final collapse resulted more from depopulation due to virulent malaria than from environmental factors such as climatic change, siltation, soil decline, or floods that breached the tanks. With control of malaria, part of the ancient system has been restored, but new deforestation causing soil erosion has been severe. North China. Over thousands of years China developed some of the most sophisticated and sustainable methods of agriculture in the world (King, 1911)" irrigation, terracing, padi, diking, soil conservation, manuring. Nevertheless, massive failures have occurred. In Shansi Province, deep, rich loess soils experienced tremendous erosion following deforestation for agriculture dating back 4000 years. This resulted in extensive abandonment of crop land and depopulation. In addition, enormous quantities of silt from this erosion flowed into the Hwang Ho (Yellow River) causing siltation of canals and flooding of entire regions of cropland, not to mention the destruction of villages and loss of millions of lives (Lowdermilk, 1953).

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Mesopotamia. The Mesopotamian story is well known but complex (Jacobsen and Adams, 1958). Irrigation agriculture dates to 4000 BC along the TigrisEuphrates and was well developed with canals, dams, and reservoirs during the Sumerian Empire (2500-2000 BC). By the Sasserian period (AD 226-640) massive state-managed canal systems had been developed, which (1) extended irrigation, and (2) maintained the system in the face of siltation of canals and flooding, in part related to deforestation in the headwater mountains to the north. Groundwater salinization had been managed by fallowing, but this was increasingly shortened with population growth, and salinization became serious, leading to land abandonment and new canals. During periods of state decline due to invasions, internal disorder, and depopulation, centralized irrigation management collapsed, but irrigation still continued at the local level with simpler canal methods such as had existed before the rise of states. State control actually contributed to irrigation failure by making the system dependent on state man power and capital for maintenance and by extending the length of canal networks making them vulnerable to greater and more rapid siltation (Adams, 1974; Gibson, 1974). Thus in Mesopotamia we see enduring sustainability at the local level, despite human-induced environmental problems, and expansion, overshoot, and collapse at the state level, with state management both exacerbating the environmental problems and not being able to cope with them when the state was weakened. The collapse of agricultural systems in prehistory resulted from natural and human-induced environmental change, both over population and depopulation, and political/social/managerial breakdowns. Often we do not know what the critical factors were, or at least the triggering factor. The Classic Maya (AD 300-900) is an example, for which there was political collapse, depopulation, and change from intensive to extensive agriculture (Harrison and Turner, 1978). Natural environmental change at times may have been crucial. In northern Mesopotamia at 2200 BC, drought seems to have contributed to agricultural abandonment leading to migrations and invasions into the irrigated lands to the south which caused the collapse of the Akkadian empire there (Weiss et al., 1993). Political and demographic collapse do not necessarily mean there was complete agicultural abandonment and loss of agroecological knowledge. The people surviving may have continued production, with technological and/or spatial adjustments. Butzer (1976:111) points out that in the Nile floodplain, during the rise and fall of kingdoms over thousands of years, there was 'an unexpected continuity in environmental exploitation strategies between prehistoric communities of the Pleistocene and the much more complex and sophisticated cultures of historical times'. In the Andes, although some detail has been lost, the terracing and irrigation technology at the community level today is basically the same as that for adjacent fields abandoned 500 years or more ago. Complete loss of technology, as with the raised fields of South America and Yucat~in, was unusual.

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VI. CONCLUSIONS We have briefly examined the forms, functions, antiquity, extent and success of prehistoric agricultural methods. The topic is large and fascinating, and the literature is considerable. Many ancient methods have continued to the present, providing clues to former techniques, viability, and productivity; however, such analogy is not necessarily valid. Change and innovation have been continuous. The distribution and extent of many of these methods is suggested by surviving field features, but most ancient fields have been destroyed by subsequent agriculture, other human and natural activity, or have been buried under sand and sediment. We know most about intensive forms of agricultural landscape modification and least about shifting cultivation, agroforestry, rainfed cultivation, flood water farming and dry farming. Thus, conclusions about the sustainability and longevity of ancient methods may be distorted. Landscaped fields require high labor inputs to construct and often also to maintain. To justify such inputs, such fields need to be utilized every year, or with only brief fallow periods, and for long periods of time without abandonment. For this to be possible, soil maintenance and pest control techniques must be employed. Prehistoric terraced, irrigated, drained, and padi fields appear to have been sustainable because of the endurance of their landscaped components, but they were sustainable because of effective soil and pest management. The presence of such fields alone implies such management and suggests continuous cultivation. Thus the agroecological lessons to be learned from the study of ancient fields and methods are derived from both (1) a soft technology (ephemeral) based on cultivation techniques and on the management of soils and pests, and (2) a hard technology (enduring) based on landscape modification to improve the cultivation medium by increasing water availability, by drainage, by erosion control and by microclimatic modification. Sustainability is dependent on the former, but cultivation may not even be possible without the latter. Knowledge of the former mainly comes from sketchy written evidence. Knowledge of the latter mainly comes from remnant fields and field features from which considerable detail about methods can be derived. The techniques for both are similar to techniques practiced by traditional farmers today, but some former methods have been lost entirely. Ancient fields have served as models for revivals, as witness the building or rebuilding of raised fields and terraces in Mexico and South America and runoff fields in the Negev. However, viable ancient agricultural methods are not necessarily successfully transferable to different times, environments, and cultures (Chapin, 1988); the same is true, of course, of modern methods. Both ephemeral and landscaped methods of cultivation involved long-term, sustainable crop production. For the ephemeral fields, this was made possible by usually being located on the best soils. However, in time, even fertile soils decrease in tilth, increase in pest levels, and decrease in productivity. As populations grew, good land decreased and opportunities for expanding the cultivated

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area were thus reduced, and soils were maintained by short-term fallowing, application of fertilizer, green manuring, and other techniques. Long-fallow shifting cultivation was unlikely until the availability of metal tools for clearing forest. Pathogens, animal and insect pests, and weeds were controlled by a variety of methods. Environmental disturbance is the inevitable result of any form of agriculture. Deforestation is required and soils are modified. Fertility declines, erosion occurs, pests increase, and water regimes are altered. It can be hypothesized that techniques of sustainability evolved in response to these habitat changes in order to continue an adequate level of productivity, given limited land. Of course such adaptation is not inevitable, and field abandonment and agricultural collapse may occur as result of excessive pressure on the land due to population growth, inappropriate or inadequate technology, or environmental change (natural or man made). Examples are commonplace in prehistory as we have seen, just as they are today. Furthermore, knowledge of sustainable technology does not suffice if sources of fertilizer are depleted, if infestations of pests are overwhelming, or if long-term climatic change occurs. On the other hand, landscaped cultivation systems are fully dependent on maintenance of the physical infrastructure (terraces, etc.). If this is neglected, the system will collapse in full or in part. The reasons may be environmental (floods, drought, tectonic, volcanic), demographic decline (the most labor intensive fields will be abandoned), or social (warfare, managerial, costs). Failure to restore abandoned fields may reflect other food getting options or migration, as we found with terrace abandonment in the Colca Valley of Peru (Denevan, 1987). Ecological and social factors, of course, may interact to bring about agrarian collapse, as for example drought or sedimentation/salinization of irrigation systems and warfare in Mesopotamia. William Clarke (1977) has delineated seven 'principles of permanence' in traditional agriculture in the Pacific that allowed continuing (or sustainable) cultivation for centuries or millennia: 1. 2. 3. 4. 5.

Cultivation is not dependent on external energy or nutrient sources. Agricultural systems are not self polluting. Net energy yields are positive. Only renewable resources are used. Agricultural resources are spread throughout a community rather than being concentrated. 6. Resources are considered as 'productive capital' to be preserved for future generations. 7. Agriculture is based on polyculture and integration of tree and non-tree crops and wild plants. These principles characterized much of prehistoric agriculture and made possible a resiliency in the face of environmental, demographic and social change. Much more research is needed, however, to understand more fully the bases for prehistoric agricultural permanence. Insights are provided by successful existing

Prehistoric Agricultural Methods as Models for Sustainability

39

methods of traditional agriculture, which provide models for sustainability (see Klee, 1980; Wilken, 1987; Browder, 1989; Thurston, 1992). However, prehistoric methods are particularly instructive as they provide a long-term perspective on successful, sustained crop production. Out of prehistoric agricultural methods emerged two pattems: (1) continuity (with continuing modification) maintained by traditional farmers, and (2) evolution into modern agriculture, with increasing emphasis on machinery, nonrenewable energy, and use of chemicals. Now, given the high cost of fossil fuels and environmental decline, arguments are being made that we must integrate the two approaches, seeking a compromise between the sustainability of the former and the high productivity of the latter.

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SUSTAINABLE AGRICULTURE: AN AGROECOLOGICAL PERSPECTIVE Stephen R. Gliessman Agroecology Program, Board of Environmental Studies, University of California, Santa Cruz, CA 95064, USA

I. Introduction II. An Agroecological Approach A. The Ecosystem Foundation B. The Agroecosystem C. Sustainable Agriculture III. Plant Pathology in the Agroecosystem A. The Pathosystem B. Traditional Agroecosystem Management C. Strawberries and Methyl Bromide IV. Plant~Pathogens in Sustainable Agroecosystems Acknowledgments References

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I. I N T R O D U C T I O N Agriculture worldwide has benefited from several decades of increasing yields and surplus production of many commodities. But the costs of maintaining these yields, from ecological, economic, and social perspectives, have led to the current debate about how to ensure the long-term sustainability of our food and agricultural systems, yet still meet the needs of a burgeoning human population (Edwards et al., 1990; Allen et al., 1991; Schaller, 1993). A sustainable agriculture must balance the needs of ecological soundness, economic viability and social equity. Current agricultural practices are pointed to as the principal area in which to begin the shift towards more sustainable food and agricultural systems (Francis and Madden, 1993). Some of us involved in the discussions about sustainability believe that the widespread use of synthetic chemical fertilizers and pesticides is contributing to the degradation of most agricultural systems. Others insist that without the use of these inputs, production levels would immediately collapse. But what is often lost in this debate is that sustainable agriculture is not a way to ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPress Limited All rights of reproduaion in anyform reserved

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farm - rather it is an approach to understanding how our food and fiber systems might be designed and managed so as to lessen or avoid our dependency on these external inputs in the first place (Gliessman, 1990a; Edwards etal., 1993). It is a focus that brings together the all too often isolated fields of agronomy and ecology in order to go beyond crop yields. It is an agroecological approach that simultaneously strives to improve yields, as well as understand the processes that permit the maintenance of those yields. The primary goal is to establish a means of determining the long-term sustainability of agricultural systems (Gliessman, 1990a). Such an approach could have special application in the area of plant pathology.

II. AN AGROECOLOGICAI. APPROACH A. The Ecosystem Foundation There has been a recent emergence of research activity on the ecology of agricultural systems (Altieri, 1987; Carroll et al., 1990; Gliessman, 1990a). After a long history of separation and lack of interaction, ecologists and agronomists have begun to combine forces in order to study and help solve the problems confronting our food production systems. Out of this the field of agroecology has taken form. The primary foundation of agroecology is the concept of the ecosystem, defined as a functional system of complementary relations between living organisms and their environment, delimited by arbitrarily chosen boundaries, which in space and time appears to maintain a steady yet dynamic equilibrium (Gliessman, 1990a). Such an equilibrium can be considered to be sustainable in a definitive sense. A well-developed, mature natural ecosystem is relatively stable, selfsustaining, and able to maintain productivity using energy inputs of solar radiation alone (Fig. 1). In examining agricultural systems from an ecosystem perspective, we have a basis for looking beyond a primary focus on system outputs (yield or harvest), and instead look at the complex set of biological, physical, and chemical interactions that determine the processes that permit us to achieve and sustain those yields. Hence, agroecology becomes much more process oriented. An understanding of the chief characteristics of natural ecosystems, as well as the differences that are introduced once human manipulation of the system takes place for the purpose of agricultural production, can be an important step in an analysis of sustainability. These characteristics are as follows:

1. Energy Flow Energy flows through a natural ecosystem as a result of complex sets of trophic interactions, certain amounts being dissipated at different stages along the food chain, with the greatest amount of energy in the system ultimately moving along the detritus pathway (Odum, 1971). Annual production of the system can be

Sustainable Agriculture: An Agroecological Perspective ATMOSPHERE AND RAIN

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Fig. 1. Diagramatic representation of the components of a natural ecosystem, including energy flow (solid lines), nutrient cycles (dotted lines), and major compartments of activity. Nutrient loss is primarily through leaching or runoff. calculated in terms of net primary productivity or biomass, each component with its corresponding energy content.

2. Nutrient Cycles Small amounts of nutrients continually enter an ecosystem through several hydrogeochemical processes. Through complex sets of interconnected cycles, these nutrients then circulate within the ecosystem, where they are most often bound in organic matter (Borman and Likens, 1967). Biological components of each system become very important in determining how efficiently nutrients move, ensuring that a m i n i m u m are lost from the system. In a mature ecosystem, these small losses are replaced by local inputs, maintaining a nutrient balance. Productivity is linked very closely to the annual rates at which nutrients are able to be recycled.

3. Population Regulating Mechanisms Through a complex combination of biotic interactions and limits set by the availability of physical resources, population levels of the various organisms are controlled, and thus link eventually to the productivity of the ecosystem. Selection through time tends towards the establishment of the most complex structure

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biologically possible within the limits set by the environment, permitting the establishment of diverse trophic interactions and niche diversification.

4. Dynamic Equilibrium The species richness or diversity of mature ecosystems permits a degree of resistance to all but very damaging perturbations. In many cases, periodic disturbances ensure the highest diversity, and even highest productivity (Connell, 1978). System stability is not a steady state, but rather a dynamic and highly fluctuating one that permits ecosystem recovery following disturbance. This permits the establishment of an ecological equilibrium that functions on the basis of sustained resource use which the ecosystem can maintain indefinitely or shift if the environment changes. At the same time, rarely do we witness what might be considered large-scale disease outbreaks in healthy, balanced ecosystems.

B. The Agroecosystem An agroecosystem is created when human manipulation and alteration of an ecosystem take place for the purpose of establishing agricultural production. This introduces several changes in the structure and function of the natural ecosystem (Fig. 2). Some key changes are as follows:

1. Energy Flow Energy flow in agroecosystems is altered greatly by human interference (Rappaport, 1971; Pimentel and Hall, 1984). Although solar radiation is still a major source of energy, many other inputs are derived from human sources and are often not self-sustaining. Agroecosystems become open systems, in which considerable energy is directed out of the system at the time of each harvest, rather than being stored in biomass which could otherwise accumulate within the system, or contributing to driving important internal ecosystem processes (e.g. organic detritus returned to the soil serving as an energy source for microorganisms that are essential for efficient nutrient cycling).

2. Nutrient Cycling Recycling of nutrients is minimal and considerable quantities are lost from the system with the harvest or as a result of leaching or erosion due to a great reduction in permanent biomass levels held within the system (Tivy, 1990). The frequent exposure of bare soil between crop plants during the season, or from open fields between cropping seasons, creates 'leaks' of nutrients from the system. Modern agricultme has come to rely heavily upon nutrient inputs derived from, or obtained with, petroleum-based sources to replace these losses.

3. Population Regutating Mechanisms Owing to human-directed genetic selection and domestication, as well as the overall simplification of agroecosystems (i.e. the loss of niche diversity and a

Sustainable Agriculture: An Agroecological Perspective

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Fig. 2. Diagramatic representation of an agroecosystem, showing the relative importance of the major compartments of activity and removal of materials as a result of harvest exports. Nutrient cycles (dotted lines) and energy flow (solid lines) are also shown. reduction in trophic interactions), populations of crop plants or animals are rarely self-reproducing or self-regulating. H u m a n inputs in the form of seed or control agents, often dependent on large energy subsidies, determine population sizes. Biological diversity is reduced, natural pest control systems are disrupted, and many niches or microhabitats are left unoccupied. The danger of catastrophic pest or disease outbreak is high, often even despite the availability of intensive human interference.

4. Dynamic Equilibrium Owing to the reduction of structural and functional diversity, much of the resilience of the system is lost, and constant human-derived external inputs must be maintained. A focus on harvest outputs upsets the former equilibrium, and can only be sustained if such outside interference continues.

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C. Sustainable Agriculture Once an ecosystem is disturbed for the purpose of converting it into an agroecosystem, the original equilibrium and resilience is altered and replaced by something that reflects a combination of ecological and socioeconomic constraints and factors. The challenge for agroecology is to find a research approach that maximizes the reliance on natural ecosystem processes and minimizes the dependence on external interference with these processes. Ecological sustainability is built on this premise, and the concepts of ecosystem resilience and stability are measureable with the tools and methods developed for the study of ecosystem structure and function. Agroecology is the application of ecological concepts and principles to the design and management of sustainable agroecosystems (Gliessman, 1990a). Owing to the complex interplay between ecological and socioeconomic factors in agriculture, a single comprehensive definition of sustainable agriculture has been difficult to develop. The most useful definition of sustainability not only must acknowledge environmental issues as priorities equivalent to those of production, society and economics, but also must recognize the need for compromise between the disparate but highly interactive elements that comprise agriculture. Toward this purpose, the following definition has been offered: 'A sustainable agriculture is one that equitably balances concerns of environmental soundness, economic viability, and social justice among all sectors of society' (Allen et al., 1991). One can easily see the whole-systems nature of this definition, and the need to extend sustainability through time to include future generations. But at the same time, one can see the difficulty in actually being able to measure or monitor such complex sustainability. The quantitative nature of agroecology, and the vast set of analytical tools that have been developed in ecology, provides a system-level approach to sustainability. Ecological sustainability, then, is the building block upon which to build our understanding of sustainability at the larger level.

III. PLANT PATHOLOGY IN THE AGROECOSYSTEM A. The Pathosystem Classical plant pathology has made tremendous contributions to the identification, control and management of pathogenic organisms in agriculture. Understanding the etiology of plant diseases and devising control strategies have assisted greatly in maintaining agricultural production. But only recently does it appear that plant pathologists have begun to look at disease organisms as part of a larger system, referred to as the pathosystem (Robinson, 1987). The plant pathosystem, as a subsystem of a natural ecosystem, is a stabilized, co-evolved set of interacting components made up of the plant host, the disease organism, and the environment. In an agroecosystem, though, owing to changes brought about by human

Sustainable Agriculture: An Agroecological Perspective

51

interference in all three of these components, the pathosystem subset of the system usually requires constant intervention and control. This control takes the form of such things as plowing, sowing, weeding, plant breeding, and the application of pesticides and fertilizers. Unfortunately, such control of the crop pathosystem is not perfect, and great losses due to diseases can occur. As we are now becoming aware, the economic and ecological costs of preventing these losses can be very high and, as we are also beginning to realize, probably not sustainable. Therefore, an agroecological approach to plant pathogens takes a system-level perspective, where management of the entire pathosystem becomes a priority. Such management relies more on way.s that the agroecosystem keeps the organism from becoming pathogenic in the first place.

B. Traditional Agroecosystem Management Throughout most of the developing world, local or traditional knowledge still provides the basic foundation for agroecosystem management, especially at the small farm level (Marten, 1986; Altieri and Hecht, 1990; National Research Council, 1993). Studies of traditional agroecosystems, and pathogen management within those systems, have demonstrated the great value such systems have for contributing to the development of ecologically sound practices of broad application (Thurston, 1992). These systems often make use of locally available, renewable resources, and production takes place in ways that focus more on the long-term sustainability of the system, rather than an over-emphasis'on obtaining the highest yields (Gliessman et al., 1981; Gliessman, 1990b). An agroecological approach to understanding how such systems function can provide valuable information on more sustainable practices. Such an approach to disease reduction has been applied to the study of softborne plant pathogens in several agroecosystems in Mexico (Lumsden etal., 1990). After observing much lower incidence of several common plant pathogens in crops of two indigenous cropping systems as compared to nearby modern farming systems, a study was carried out to help explain how soils of the traditional systems so effectively suppressed damping-off diseases caused by Pythium spp. The idea of suppressive softs has been known for some time (Schneider,1982), but relatively little knowledge exists on how such suppressiveness is connected to agroecosystem management. The two traditional systems examined were the familiar raised-field and canal systems known as Chinampas in the upland central valley of Mexico (Coe, 1964; Armillas, 1971) and a less familiar swampland cropping system locally known as Popal used in the tropical lowlands of Tabasco, Mexico (Gliessman, 1991). Both systems are farmed with little to no reliance on purchased synthetic inputs, depending instead on high organic matter inputs, locally adapted seeds, crop rotations, and even periodic flooding of the fields. Soils from these two systems were able to suppress damping-off diseases when compared to soils from nearby fields

S. R. Gliessman

52

Table I. The populations of Pythium aphanidermatum, P. ultimum and Rhizoctonia solani and the incidence of damping-off of radish and cucumber seedlings (reproduced from Lumsden et al., 1990, by courtesy of Springer-Verlag). ,,,,

Propagules/g a Soil Chapingo Chinampa Tabasco Popal

%

% Damping-off

P. aphanidermatum

P. ultimum

colonization b

R. solani

Radish (20~

Cucumber (30~

8. laC O.Ob 1.8a 2.9a

254b 3530a Oc Oc

6.2a 5.3a 0.8b 1.0b

56.7b 19.2cd 75.0a 4.2d

33.3a 14.2b 18.3b 2.5c

a Numbers estimated on five batches of soil with use of selective media for P. aphanidermatum and P.

ultimum.

b Percentage colonization (average of three batches of soil) of beet seed added to soil, incubated 3 days, recovered, and plated on water agar. c Values in each column followed by the same letter are not significantly different at P = 0.05, according to Duncan's multiple range test.

(called Chapingo and Tabasco respectively) that had been farmed for many years with conventional synthetic chemical fertilizers and pesticides. For example, two species of Pythium and one of Rhizoctonia were suppressed in laboratory tests with radish and cucumber seedlings (Table I), and the incidence was reduced of damping-off by P. aphanidermatum of cucumber seedlings infested with increasing quantities of oospores of the fungus (Fig. 3). Apparently, in the two traditional agroecosystems, a dynamic ecological equilibrium exists, in which intense management, especially the addition of large amounts of organic matter, maintains levels of organic and mineral nutrients that stimulate biological activity in the soil. A good part of this increased activity is probably organisms that are antagonistic to soil-borne plant pathogens. Shortterm disease suppression comes about due to increased microbial activity reducing the pathogen's ability to germinate in soil and cause disease. Long-term suppression operates over a much longer time period, lowering population levels of the disease-causing organisms in the first place. Microbial activity in the soil, mycoparasitic activity, lower pH in the soil, and periodic flooding all interact to provide resistance to disease at the agroecosystem level.

C. Strawberries and Methyl Bromide Many present-day farming systems have achieved remarkable yield advances and profitability due to the introduction of very powerful and effective soil fumigants. One of these systems is strawberry production along coastal California, where the mild mediterranean climate and the fumigant methyl bromide have combined to promote the development of very high yielding technologies. In the small coastal county of Santa Cruz alone, the gross value of strawberries produced in 1993 on 3256 acres was just over $104 million (Santa Cruz County Agricultural Commissioner, 1994). Production and harvest costs for the year can exceed $25 000 per

Sustainable Agriculture: An Agroecological Perspective

53

100 !" -,.m-,-CHA -.-o-.- CHS 90 - --,.,e,,-,.TAB --o,--POP 80 I.i. I.I.

70

I

60

z ~..

so

O

40 30

20 10 50

100

OOSPORES ADDED / ML SOIL Fig. 3. Incidence of damping-off of cucumber seedlings in Mexican soils (CHA, soil from conventionally farmed field, Chapingo, Mex.; CHS, soil from traditional chinampa, Xochimilco, Mex.; TAB, soil from conventionally farmed field, Cardenas, Tabasco, Mex.; and POP, soil from traditional popal, Cardenas, Tabasco, Mex.) infested with 0, 50 and 100 oospores of P. aphanidermatum per gram soil. Soils were incubated for 1 week at 30~ in the greenhouse. acre (Welch, etal., 1989), of which as much as $2000 per acre is the cost of fumigation. Recently methyl bromide has come under heavy attack as a Class I ozonedepleter and for potential farmworker safety concerns, and will probably be phased out completely by the end of the century. In the California strawberry industry, there is concern that loss of methyl bromide will not allow maintenance of current high production levels, partly due to an increased potential for diseases caused by pathogenic fungi and nematodes. There is discussion about the need to find a substitute chemical. An alternative approach, though, is not to eradicate soil organisms (both pathogenic and beneficial in the case of methyl bromide), but to manage the soil ecosystem in ways that prevent or suppress the outbreak of the disease organisms (Agroecology Program, 1993). As part of a study designed to compare the effects of conventional synthetic chemical and certified organic inputs in a commercial strawberry production system (Gliessman et al., 1990, unpublished), populations of pathogenic fungi that grow on the roots of the crop were monitored over three cropping seasons to see how the absence of methyl bromide (in this case combined with chloropicrin) would affect these potentially yield-limiting organisms (Rosado-Mey et al., 1994). The study also examined trends in populations of benign and beneficial soil organisms

54

S. R. Gliessman

Table II. Maximum per cent incidence encountered in cultured roots during the production season of root fungi genera in conventional and organic strawberry production systems after 3 years of comparison (adapted from Agroecology Program, 1993). ==

Conventional

,,

Organic

Fusarium Year 1 Year 2 Year 3

90 9 6

88 15 13

Pythium Year 1 Year 2 Year 3

18a 8 2a

30b 11 13b

Rhizoctonia Year 1 Year 2 Year 3

17a 5 9

28b 10 3

Verticillium Year 1 Year 2 Year 3

2a 8a 5a

9b 3b 2b

5a 8a

9b 86b 86b

Cylindrocarpon Year 1

Year 2 Year 3

Trichoderma Year 1 Year 2

Year 3

44a

6a

23a

19a

Ib

4b

1b

Values with different letters are significantly different at P = 0.05, based on Duncan's multiple range test.

to gain an understanding of the overall ecology of the different management systems, and looked for correlations between the types of inputs and disease incidence. Strawberry roots from both the organic and conventional systems bore fungi from six different genera that can potentially cause diseases in strawberries: Fusarium, Pythium, Rhizoctonia, Cylindrocarpon, Trichoderma and Verticillium. Phytophthora was not present. Trends for these organisms over the 3-year period of the experiment are shown in Table II. Both Pythium and Fusarium were more commonly seen from the organic production system, but produced no obvious disease symptoms. The more pathogenic Verticillium and Rhizoctonia were more frequent, but in low numbers, in the conventional system, and almost non-existent in the organic system. Trichodermawas encountered in year three, mainly in the conventional production system. Trichoderma is hyperparasitic on other fungi, and may play a role in the suppression of root pathogens (Schroth and Hancock, 1981). It may also be resistant to fumigation. Cylindrocarpon increased dramatically during the second year of organic

Sustainable Agriculture: An Agroecological Perspective

55

management, and even increased in year three in the conventional system when fumigation was not used and the plants from year two were left in the ground for an additional year of production. This fungus appears to require at least a year without fumigation to become evident in either system. Cylindrocarpon is a saprophyte in the soil and on root surfaces, and has been shown to be more evident is soils farmed with organic practices (Elmholt and Kjoller, 1989). Although thought to be part of the complex of fungi associated with strawberry black root rot (Yuen etal., 1991), Cylindrocarpon can also enhance plant growth and phosphorus uptake, especially when present on mycorrhizal roots (Paget, 1975). Such diversity in the rhizosphere of organically managed strawberry roots, in association with increased mycorrhization (Werner et al., 1990) and higher levels of free-living predacious and microbial feeding nematodes (Agroecology Program, 1993), might combine to suppress plant diseases in organic production systems. Management strategies that promote this diversity will become critical for strawberry growers looking for alternatives to chemical soil fumigation.

IV. PLANT PATHOGENS IN SUSTAINABLE AGROECOSYSTEMS An agroecological approach to plant pathogens is based on research that applies an integrated systems-level focus concerned with management for long-term sustainability as well as short-term yields (Gliessman, 1987, 1990a). Knowledge of the ecological interactions occurring within the agroecosystem and the sustainable functioning of the system as a whole become the overall goals of this approach. The plant pathogen becomes a part of a complex, dynamic and interacting system. In present-day agriculture, plant sanitation to avoid diseases is quickly becoming untenable. Fumigation and chemical control are becoming less viable options as the concerns grow around issues of environmental health and safety, as well as for increasing problems of pesticide resistance. A more sustainable approach is needed. Sustainability can be achieved in an agriculture that is ecologically sound, resource-conserving and not environmentally degrading. The understanding of sustainability in ecological terms comes from the knowledge generated through the study of existing production systems where either inputs other than human labor and local resources were not available (Gliessman et al., 1981; Altieri, 1987), or where alternatives have been found that reduce, eliminate or replace the artificial inputs common to conventional agriculture (Gliessman et al., 1990). An ecologically sustainable agriculture manages plant pathogens as much as possible through internal regulating mechanisms that function as a result of interactions between the plant host, the pathogen, and the environment. Managing the agroecosystem and choosing practices that enhance these interactions is the role of the farmer. The plant pathologist who applies an agroecological approach to understanding the consequences of these choices at the disease level can begin to assess an important component of the sustainability of the resulting production

56

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system. From such studies an understanding can begin to develop for finding alternatives that reduce inputs, lessen the impacts of inputs when they are used, and establish a basis for redesigning systems that help farmers sustain the viability of their farms. ACKNOWLEDGMENTS

The ideas and opinions expressed in this paper are the result of long and fruitful collaboration with a remarkable interdisciplinary team of students, colleagues and farmers. I especially acknowledge the suggestions and editorial comments of Emerson Nafzinger, Polly Goldman, Hollis Waldon, Marc Los Huertos and Phillip Fujiyoshi. REFERENCES

Agroecology Program (1993). Beyond methyl bromide: managing the soil ecology of strawberry crops. The Cultivar (University of California, Santa Cruz) 11 (2), 5-6. Allen, P.A., Van Dusen, D., Lundy, J. L. and Gliessman, S. R. (1991). Integrating social, environmental, and economic issues in sustainable agriculture. AmericanJournal of Alternative Agriculture 6, 34-39. Ahieri, M.A. (1987). 'Agroecology: the Scientific Basis of Alternative Agriculture'. Westview Press, Boulder, CO. Altieri, M.A. and Hecht, S.B. (1990). 'Agroecology and Small Farm Development'. CRC Press, Boca Raton, FL. Armillas, P. (1971). Gardens on swamps. &/ence 174, 653-661. Borman, F. H. and Likens, G. E. (1967). Nutrient cycling. Science 155, 424-429. Carroll, C . R . , Vandermeer, J. H., and Rosset, P.M. (eds) (1990). 'Agroecology'. McGraw Hill, New York. Coe, M. D. (1964) . The chinampas of Mexico. Scientific American 211, 90-98. Connell, J . H . (1978). Diversity in tropical rainforests and coral reefs. Science 199, 1202-1210. Edwards, C. A., Lal, R., Madden,J. P., Miller, R. H., and House, G. (eds) (1990). 'Sustainable Agricultural Systems'. Soil and Water Conservation Society, Ankeny, Iowa. Edwards, C. A., Grove, T. L., Harwood, R. R., and Pierce Colfer, C.J. (1993). The role of agroecology and integrated farming systems in agricultural sustainability. Agriculture, Ecosystems and Environment 46, 99-121. Elmholt, S. and Kjoller, A. H. (1989). Comparison of the occurrence of the saprophytic soil fungi in two differently cultivated field soils. Biological Horticulture and Agriculture 6, 229-239. Francis, C. A. and Madden, J. P. (1993). Designing the future: sustainable agriculture in the US. Agriculture, Ecosystems and Environment 46, 123-134. Gliessman, S. R. (1987). Species interactions and community ecology in low externalinput agriculture. American Journal of Alternative Agriculture 2, 160-165. Gliessman, S. R. (ed.) (1990a). 'Agroecology: Researching the Ecological Basis for Sustainable Agriculture. Springer-Verlag, New York. Gliessman, S.R. (1990b). Understanding the basis of sustainability for agriculture in the tropics: experiences in Latin America. In 'Sustainable Agricultural Systems' (C. A. Edwards, R. Lal, J. P. Madden, R. H. Miller and G. House, eds), pp. 378-390.

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Soil and Water Conservation Society, Ankeny, Ohio. Gliessman, S.R. (1991). Ecological basis of traditional management of wetlands in tropical Mexico: learning from agroecosystem models. In 'Biodiversity: Culture, Conservation, and Ecodevelopment' (M. L. Oldfield and J. B. Alcorn, eds), pp. 211-229. Westview Press, Boulder, CO. Gliessman, S. R., Garcia, E. R., and Amador, A. M. (1981). The ecological basis for the application of traditional agricultural technology in the management of tropical agroecosystems. Agro-Ecosystems 7, 173-185. Gliessman, S. R., Swezey, S., Allison, J., Farrell, J., Kluson, R., Lundy, J., RosadoMay, F., and Werner, M. R. (1990). The conversion to low-input organic management for strawberry production on the central California coast. California Agriculture 44, 4-7. Lumsden, R.D., Garcia-E. R., Lewis, J. A., and Frias-T, G. A. (1990). Reduction of damping-off disease in soils from indigenous Mexican agroecosystems. In 'Agroecology: Researching the Ecological Basis for Sustainable Agriculture' (S. R. Gliessman, ed.), pp. 82-103. Springer-Verlag, New York. Marten, G. G. ed. (1986). 'Traditional Agriculture in Southeast Asia: A Human Ecology Perspective'. Westview Press, Boulder, CO. National Research Council (1993). 'Sustainable Agriculture and the Environment in the Humid Tropics'. National Academy Press, Washington, DC. Odum, E. P. (1971). 'Fundamentals of Ecology'. W. B. Saunders, Philadelphia. Paget, D. K. (1975). The effect of Cylindrocarpon on plant growth responses to vesiculararbuscular mycorrhiza. In 'Endomycorrhizas' (F. E. Sanders, B. Mosse and P. B. Tinker, eds), pp. 593-606. Academic Press, London. Pimentel, D. and Hall, C. W. (eds) (1984). 'Food and Energy Resources'. Academic Press, Orlando. Rappaport, R. A. (1971). The flow of energy in an agricultural society. Scientific American 225, 116-132. Robinson, R.A. (1987). 'Host Management in Crop Pathosystems'. Macmillan, New York. Rosado-May, F.J., Werner, M. W., Gliessman, S. R., and Webb, R. (1994) Incidence of strawberry root fungi in conventional and organic production systems. Applied Soil Ecology (in press). Santa Cruz County Agricultural Commissioner. (1994). Crop Report, 1993. Santa Cruz County, Santa Cruz. Schaller, N. (1993). The concept of agricultural sustainability. Agriculture, Ecosystems and Environment 46, 89-97. Schneider, R.W. (ed.) (1982). 'Suppressive Soils and Plant Disease'. The American Phytopathological Society, St Paul, MN. Schroth, M. N. and Hancock, J. G. (1981). Selected topics in biological control. Annual Review of Microbiology 35, 453-476. Thurston, H. D. (1992). 'Sustainable Practices for Plant Disease Management in Traditional Farming Systems'. Westview Press, Boulder, CO. Tivy, J. (1990) 'Agricultural Ecology'. Longman Scientific, Essex. Welch, N. C., Greathead, A. S., and Beutel, J. A. (1989). Strawberry production and costs in the central coast of California. Leaflet 2959, pp. 1-7. Agricultural Extension, University of California. Werner, M. R., Kluson, R. A., and Gliessman, S. R. (1990). Colonization of strawberry roots by VA mycorrhizal fungi in agroecosystems under conventional and transitional organic management. Biological Agriculture and Horticulture 7, 139-151. Yuen, G. Y., Schroth, M. N., Weinhold, A. R., and Hancock, J. G. (1991). Effects of soil fumigation with methyl bromide and chloropicrin on root health and yield of strawberry. Plant Diseases 75, 416-420.

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4 DEVELOPING BIOFERTILIZER AND BIOCONTROL AGENTS THAT MEET FARMERS" EXPECTATIONS M . E . Leggett and S. C. Gleddie Philom Bios Inc., 318-111 Research Drive, Saskatoon, SK, S 7 N 3 R 2 Canada

I. Introduction II. Market-driven Research and Product Development A. Customer Demand B. Market Potential C. Critical Success Factors III. The Commercialization Process A. Production B. Formulation C. Application D. Efficacy E. Regulatory F. Reliability IV. Education V. Conclusions Acknowledgments References

59 61 61 62 62 63 63 64 66 68 69 71 72 73 73 73

I. I N T R O D U C T I O N Agricultural biotechnology is a collective description of a wide range of biological fields. Perhaps the largest of these fields is plant biotechnology using genetic manipulation to develop improved plant varieties. This is an area of accelerated advances and the primary focus of corporate and academic investment and media attention. However, we should not let the concentrated effort on plant genetics overshadow the proven and promised scientific and commercial value of plant biotechnology using micro-organisms to improve crop productivity. Others have reviewed the status of crop inoculation to enhance crop performance or control crop pests (,Jutsum, 1988; Macdonald, 1989; Boland, 1990; Charudattan, 1991). A n u m b e r of inoculants are currently available to farmers. W e have chosen two biofertilizers and three bioherbicides which we will use as examples throughout the paper. Rhizobium inoculants, marketed under the name Nitragin T M at the turn of ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 Academic Press Limited All rights of reproduction in anyform reserved

60

M. E. Leggett and S. C. G/eddie

the century, were the first commercial inoculants available to farmers in North America (Smith, 1992). In the last 20 years, a number of Rhizobium inoculants have appeared, each with differing species, strains, or formulations. P R O V I D E TM is a microbial seed inoculant which increases the availability of phosphate to crop plants. The active ingredient in P R O V I D E TM, Penicillium bilaii, was isolated by researchers at the Agriculture Canada Research Station in Lethbridge, Alberta (Kucey, 1983). P R O V I D E TM is a wettable powder which is suspended in water and applied to seed. The fungus P. bilaii colonizes plant rhizospheres, releasing organic acid metabolites which solubilize otherwise unavailable phosphates from the area surrounding the root zone. Inoculation with P R O V I D E TM allows a reduction in phosphate fertilizer application rates. Philom Bios Inc., a biotechnology company headquartered in Saskatoon, Saskatchewan, developed and manufactures P R O V I D E TM. P R O V I D E TM is registered under The Canadian Fertilizers Act for use with wheat, Triticum aestivum (Kucey, 1988; Gleddie et al., 1991; Chambers, 1992); canola, Brassica spp. (Gleddie et al., 1993); pea, Pisum sativum (Gleddie, 1992; Gleddie etal., 1993); and lentil, Lens culinarus (Gleddie etal., 1993) and is currently marketed in western Canada by DowElanco Canada Inc. DeVine TM, postemergent bioherbicide for the control of stranglervine (Morenia odorata) in citrus groves, was the first bioherbicide to be registered in the United States. The active ingredient in DeVine TM, Phytophthora palmivora, was isolated from a dying stranglervine by The Department of Plant Industries, Florida Department of Agriculture (Kenney, 1986). Abbott Laboratories began cooperative research with the Department in the late 1970s, and currently manufactures and markets DeVine TM. DeVine TM gives greater than 90% control of stranglervine and control lasts for at least 2 years after application. Collego TM, a selective postemergent bioherbicide for the control of northern jointvetch (Aeschynomene virginica) in rice (O(yza sativa) and soybean (Glycine max), was the first commercially available bioherbicide for use on an annual weed in annum crops in the United States (Bowers, 1986). The active ingredient in Collego TM, Colletotrichum gloesporiodes f.sp. aeschynomenes, was discovered by USDA and University of Arkansas scientists. The Upjohn Company developed the production protocols and formulations and continues to produce Collego TM. However, it is now owned and marketed by Ecogen Inc. (Charudattan, 1991). Collego TM provides excellent control of northern jointvetch when used as directed (Bowers, 1986). BioMal TM, a postemergent bioherbicide for the control of round-leaved mallow (Malva pusilla) in agricultural crops, was the first bioherbicide to receive registration for use in Canada. The active ingredient in BioMal TM, CoUetotrichum gloeosporioides f.sp. malvae, was isolated from diseased round-leaved mallow tissue by scientists at the Agriculture Canada Research Station, Regina, Saskatchewan (Mortensen, 1988). Philom Bios collaborated with Agriculture Canada to develop the organism as a bioherbicide. BioMal TM gives consistently greater than 90% control of round-leaved mallow. BioMal T M is marketed in western Canada by DowElanco Canada Inc.

Developing Biofertilizer and B/control Agents

61

It is one thing to identify an organism and show it can do something useful, but it is quite another to put it into a user-friendly, environmentally-friendly formulation which is stable, efficacious, can be registered and can withstand the rigors of commercial distribution and handling. The flowsheet from discovery to customer is a continuum with discovery representing about 5 % of the total effort, and the balance demanding enormous financial, ci'eative, registration, manufacturing and marketing efforts. But these challenges can be met and matched. The objective of this chapter is to describe the process of commercializing biologicals which meet farmers' expectations.

II. MARKET-DRIVEN RESEARCH AND PRODUCT DEVELOPMENT Confirmed market demand is the precursor to all commercial research and development. A farmer's expectations cannot be met by companies driven to bankruptcy by pursuing the development of unprofitable products.

A. Customer Demand It is important to distinguish between societal need for biological products and actual customer demand. Biocontrol decreases the social costs of agriculture by decreasing water and soil pollution, reducing detrimental effects on non-target organisms, decreasing health hazards, either through direct exposure or in food, and by reducing the development of a pesticide-resistant pest population (Reichelderfer, 1981) and marketing more efficient use of non-renewable resources.

These factors are generally overlooked by farmers making short-term decisions based solely on their direct costs and benefits. However, social issues are having increasing effects on farm management decisions demonstrated by recent trends towards sustainable agriculture, organic farming, integrated pest management, and intensive crop management. Thus, societal needs for biological products may increasingly affect farmer demand and the farmers' perception of the value of biologicals. Customer demand may exist for a biological product before the product is developed. When BioMal TM was developed, no effective method existed for the control of round-leaved mallow, and the weed was spreading rapidly. In this case, only the extent of customer demand was determined by survey prior to commercialization. In other cases, there may be no initial demand simply because the customer does not recognize the need for the product. For example, there were no obvious benefits of using P R O V I D E T M compared to phosphate fertilizer until the inefficiencies of phosphate fertilizer were pointed out. In these cases, the expected benefits of P R O V I D E TM were explained to prospective customers prior to determining demand by survey and focus groups.

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M. E. Leggett and S. C. Gleddie

Accurate estimates of customer demand are essential to the development of biological products which meet farmers' expectations. Product demand must be confirmed. Without demand, there can be no perception of value to the customer. Price is a component of value and must be included in the market assessment.

B. Market Potential Biologicals can be successful in any market as long as they are as good as or better than existing technology in terms of cost, efficacy or reliability; or where they have significant toxicological or environmental advantages (Jutsum, 1988). Toxicological and environmental advantages are continuing to expand the market opportunities for biologicals. Biologicals will also be successful where current technology either cannot solve, or inefficiently solves, a production problem. Smaller market niches are more suitable for biologicals than traditional chemicals because of lower discovery and regulatory costs and reduced lead time to get a new product to market (Lethbridge, 1989). Biologicals also suit markets where effective chemical inputs do not exist, where chemicals are too expensive, or where the use of chemicals is limited by regulations or by the development of resistance.

C. Critical Success Factors Critical success factors for the selection and commercialization of biologicals are as follows: 1. Adequate customer demand and market size to ensure return on investment in a reasonable time. 2. Cost effective manufacturing. 3. Effective, easy-to-use formulations. 4. Compatability with distribution and agricultural practices. 5. Highly efficacious and reliable field performance. 6. Ability to obtain patents and registrations. 7. Adequate revenues to support sales and to continue product improvements. Success is achieved when each factor is accomplished while providing return on investment. M a n y projects may be technically feasible without being economically feasible (Reichelderfer, 1981). Economical feasibility may be defined as the probability of the technology to increase returns to farmers. If products are developed at excessive cost, the resulting selling price will be a deterrent to farmers. Such products obviously fail to meet farmers' expectations. The most dollars must be spent on the critical success factors which have the greatest impact on the farmers' satisfaction with the product.

Developing Biofertilizer and Bicontrol Agents

63

III. THE COMMERCIALIZATION PROCESS Although the concept of microbial inoculation of crops to increase yields or control pests goes back over 100 years, very few biofertilizers or biocontrol agents are available for use by farmers despite extensive research (Lethbridge, 1989; Charudattan, 1991). Some contend that the low number of commercialized biologicals is not surprising given that agrochemical companies routinely screen thousands of compounds to arrive at one new chemical product (Charudattan, 1991). Lethbridge (1989) suggests that the lack of biological products is because the performance of microbial inoculants falls below that of chemicals. Perhaps the most significant reason for the lack of market-ready inoculants is the multifaceted complexity of the research coupled with a general lack of understanding and application of the principles of market-driven research. A market-driven commercialization process follows the critical success factors outlined in the previous section. The areas of production, formulation, application, efficacy, regulatory, and reliability occur more or less simultaneously, and there must be continuous communication, feedback, and compromise between each area. In each area, particular attention and resources should be allocated to research that is critical to producing a product which meets farmers' expectations. Successful commercialization of research cannot occur in a vacuum. Every objective must be continually checked against and adjusted for the needs of the marketplace, both at the start of the project and looking 5-10 years to the future when the product will be launched. Biological products are based on living organisms. This is a fundamental concept which must be fully appreciated because it affects every aspect of commercial development (Kenney, 1986).

A. Production The initial step in producing a product is to discover a way to produce economically a large amount of inoculum with minimal contamination. The research involves detailed studies on all aspects of the process from the production of the stock cultures through the parameters of fermentation, to downstream processing and production of the final product. The complex studies involved in this process are beyond the scope of this chapter. It is important, however, that the production of the active ingredient is not separated from the other procedures involved in the development of a biofertilizer or biocontrol agent. Even the production specialist must be aware of a farmer's needs. The fermentation process offers one of the best ways to control the cost of production. Increases in yield markedly reduce the cost of the final product. Low contamination levels are an important production target. Contaminants may compete with the active ingredient and reduce its effectiveness. Production specialists should also communicate with agronomists to determine the important characteristics of the end product.

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B. Formulation The best technology is of no value unless it can be placed in the customers' hands in a form they can easily use. Hence, developing a safe, easy to use, cost-effective formulation that will keep the micro-organism alive is one of the most important steps in developing a biological product. Formulation is the blending of active ingredients such as fungal spores with inert carriers such as diluents and surfactants in order to alter the physical characteristics to a more desirable form (Boyette et al., 1991). Lethbridge (1989) stated that the final formulation of a crop production and enhancement agent must have a minimum shelf life of 2 years at room temperature, be easy to handle, insensitive to abuse and must be stable over a range of - 5 to + 30~ This is the ideal situation and should be kept as the ultimate aim for developing a formulation for a biological. Failure to meet these rigid standards, however, should not stop the commercialization of biologicals. Few of the biological products currently on the market meet all of Lethbridge's requirements. A biological agent does not need to be stable for 2 years at ambient temperature to be a viable commercial product. Rhizobial inoculants have been widely accepted in North America since 1930 (Smith, 1992) even though most have only a 1-year shelf life. DeVine TM, which has been used for over a decade, must be kept refrigerated and has an expiry date of 6 weeks (Kenney, 1986). P R O V I D E TM has been marketed in western Canada since 1991. P R O V I D E TM spores must be stored frozen to maintain product quality for one season. The requirement for frozen storage has not been an insurmountable problem. P R O V I D E TM pouches are small and are easily stored in a small freezer. Two thousand pouches, which treat over 3200 wheat seed prior to sowing, occupy less than 1 m 3 of freezer ( - 2 0 ~ space. The one-season shelf life is not a major inconvenience for farmers as they can easily purchase only what they need for a season. It does, however, put pressure on marketers as they must be more precise in their predictions of sales for a given year and on the retailers who must manage their inventory. Managing limited shelf life provides the shortest route to the marketplace (Kenney, 1986). A formulation should be easy to use. However, farmers will spend the extra time and effort if they see a real value in the product. Collego TM which has had good grower acceptance (Charudattan, 1991), is a two-component system (Bowers, 1986). Having to demand a certain degree of care in handling the product should not stop its commercialization. Farmers in the 1990s must be sophisticated consumers and managers. They are certainly capable of reading and following instructions and understanding that living organisms must be treated carefully. However, they must be given clear and reasonable storage and handling instructions. The development team must rigorously test the product for viability and performance under a variety of conditions which mimic storage, distribution, and on-farm conditions. For example, although P R O V I D E TM must be stored frozen to maintain

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product viability, extensive studies showed that the product may go through several periods at ambient temperature in the distribution system and can reach ambient temperatures for a total of 48 h without loss of potency. The manufacturer takes the responsibility of clearly labelling the package so that the limitations for product handling are obvious. The marketing and sales team must inform and educate dealers and farmers of the extra care required for handling biologicals. The formulation must minimize user exposure to the product. The bran formulation originally used in P R O V I D E T M research (Kucey, 1988) was extremely dusty and unpleasant to use. The wettable powder now on the market is added to water and user exposure is minimal. Care must also be taken to ensure that inert materials used in a formulation are safe for people using the product and for non-target organisms. Regulatory agencies should be consulted early in the development phase to ensure that the proposed inert carriers are permitted. Materials used in seed treatments should be tested to make sure they do not inhibit or delay emergence. Adding nutrients such as sugar to biologicals will be tempting as they may enhance the growth of the active ingredient. This should be done with care as these nutrients may also stimulate pathogens which could compete with the product organism or seriously harm a crop plant (Cook and Baker, 1983). A completely safe product is impossible, of course, since any material can harm a person or the environment if it is mistreated or used to excess, but a safely used product is achievable. The instructions for safe handling must be clearly labelled. Experiments with DeVine T M showed that some non-target plants were susceptible to the fungus if it was used at 200 times the recommended level. It was decided that this did not represent field conditions and the label was designed to prevent potential problems (Kenney, 1986). The expectation of attaining a reasonable cost target must be high before the development begins. Why develop the perfect formulation if it costs more to produce than the farmer can afford? The cost of goods (COG), the total cost of product manufacture from fermentation through formulation and packaging should be determined for each product (Stowell, 1991). Philom Bios put considerable effort into developing a granular formulation for canola before we discovered that an unexpected increase in the cost of the raw materials made the cost of producing the granules prohibitive. The acceptable C O G for any product will depend on the value of the crop as well as the performance value of the product. For example, the granular formulation of P R O V I D E T M rejected for canola is acceptable for more intensively managed higher value crops. The development of effective formulations is complicated and still remains more of an art than a science (Daigle and Connick, 1990). Formulation development requires the co-operation of microbiologists, plant pathologists or entomologists, agronomists, formulation chemists, marketing experts, regulatory personnel, and economists. All people involved in developing a new formulation must be creative and willing to compromise. Many of these experts will have come from chemical industries and can draw on this experience. It is essential,

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however, that they be willing to look beyond the concepts they accept as standard. Marketing experts in charge of developing DeVine TM were willing to accept a product that had to be handled like fresh milk (Kenney, 1986). Processes and ingredients associated with the food industry may be more appropriate for formulation of biologicals than the technology developed for chemical pesticides (Connick et al., 1991). All the experts must keep in mind that their purpose is to develop a product for the farmer and these needs are paramount. Formulation development is an ongoing process. It is always possible to evolve a new formulation with improved stability or that is easier to use. Liquid inoculant formulations provide convenience and good seed coverage (Smith, 1992). It may also be advisable to have several formulations available. Liquid Rhizobium preparations do not provide a substantial particle matrix that may help the organism withstand environmental stress (Smith, 1992) and consequently may not be suitable for regions where conditions for Rkizobium growth may be marginal. In these cases, granular inoculants may be more suitable (Smith, 1992).

C. Application The manufacturers' responsibility for a biological agent does not end with the sale of the product. Comprehensive guidelines for the use of the material must also be developed, to ensure that the product is compatible with other standard farming practices. The simplest means of determining where problems may occur is to go through mentally all the steps a farmer would follow when using a product. In addition to person-to-person discussions with farmers, retailers and sales representatives, group sessions focused on identifying application procedures are very effective. Each crop must be examined separately. P R O V I D E TM is registered for wheat, canola, pea, and lentil. Wheat, pea and lentil are treated onfarm often together with seed treatment fungicides or Rhizobium inoculants just prior to seeding. Canola is purchased from seed processors who apply the fungicides, with or without a polymer coating, up to 6 months before seeding. As a consequence, P R O V I D E TM for wheat, pea, and lentil is sold for use on farm, while P R O V I D E TM for canola is sold only as inoculated seed. Application procedures depend on the formulation of the product. Wettable powders are suspended in water before they are sprayed on the field or applied to seed. Care must be taken to avoid chemical residues that remain in the spray tank or mixing container (Bowers, 1986). P R O V I D E TM must be agitated gently to keep the spores in suspension. This can be done easily with standard farm equipment, but an inexpensive P R O V I D E TM applicator developed by a Saskatchewan company (Spray Tech) simplifies the process. As the applicator is dedicated to P R O V I D E TM, concern over chemical residues is eliminated. The length of time the spores can remain in the suspension should be carefully determined. Farmers need to know if a delay of a few hours because of equipment problems or inclement weather will destroy the value of the product.

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It is important to remember that biologicals will not completely replace chemical agents; rather they supplement or enhance their benefits. Hence the interaction between chemical pesticides or other biologicals which might be used in conjunction with the product should be carefully evaluated. Most bioherbicides are specific for one weed, yet other weeds in the crop must still be controlled, either by chemical herbicides, or, in the future, with the use of two or more bioherbicides. Chemical herbicides may enhance or suppress the activity of bioherbicides (Smith, 1991). Each interaction must be studied separately in order to develop a complete set of recommendations for using mixtures of products (Charudattan, 1988). Problems with incompatibility can be overcome by careful sequencing of application of the bioherbicide before or after certain chemicals (Charudattan, 1988). Combinations of two or more bioherbicides to control more than one weed are possible. A mixed spore suspension of pathogens active against winged water primrose, Ludwigia decurrens, and northern jointvetch, Aeschynomene virginia, controlled both weeds (Daigle and Connick, 1990). Products applied to seed must be carefully tested to make sure they are not affected by or do not interfere with seed treatment fungicides. P R O V I D E TM can be applied with Vitavax Single | or Vitavax Dual | on wheat, with Vitavax RS | Premiere | or Rovral ST | on canola and with Thiram 75WP on peas, as long as the materials are added sequentially and the materials are allowed to dry thoroughly between applications. Compatability data are best gathered through co-operative research between scientists working for the companies producing the various products. The co-operation between Philom Bios and Gustafson, Zeneca (ICI), and Rh6ne Poulenc has been very productive. Combinations of biological seed treatments must also be evaluated. Since all pea and lentil in western Canada are inoculated with rhizobia, Gleddie's studies showing that R. leguminosarum and P. bilaii can be used as co-inoculants are commercially important (Gleddie, 1992). Individual formulations should also be evaluated and this may involve a non-partisan approach. A farmer cannot be expected to purchase all his materials from one company. Although Philom Bios produces its own rhizobial inoculant (N-PROVETM), we established a cooperative study with Lipha Tech to confirm the compatability of P R O V I D E TM with their liquid rhizobium inoculant, Cell Tech | The maximum time allowed between inoculating and seeding must be known. The test conditions should mimic those occurring in practice. Survival studies done at 4~ when the seed will be kept at temperatures above 10~ are of no value. The degree of concern will change depending on the crop and on other treatments. Rhizobium is very sensitive to desiccation and seed inoculated with Rhizobium must be sown within 24 h. P R O V I D E TM used on pea or lentil in combination with Rhizobium will be governed by the same limitations. This eliminates the need for long-term storage studies of P R O V I D E TM on pea. P R O V I D E TM can be applied to untreated wheat 14 days before seeding, or to wheat treated with Vitavax Single | or Vitavax Dual | 7 days before seeding. All evaluations must be done to ensure that the seed will be covered with enough viable fungal spores or

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bacterial cells at planting time to be effective. If viability loss is expected, safety factors must be built into the dosage levels.

D. Efficacy Regrettably, several questionable 'new technology' products have come to the market in recent years. These products have succeeded only in building scepticism towards new technology in the farmer's mind. Legitimate biological products must be distanced from the negative perceptions of these bogus products. The only sure way to do this is to gather extensive performance data. Without demonstrated scientific pedigree, a new biological product is doomed to failure. 1. Field Research The farmers' expectations of efficacy, credibility, and value will be largely determined by the results of field experimentation. The objectives of field research are to: (1) perform preliminary experiments to determine the suitability of the product for commercialization; (2) test the efficacy of the product across the range of environmental conditions encountered in the potential market area; (3) establish credibility for the product with farmers and their advisors; (4) collect response data which will assist marketers in establishing product benefits and statements of product efficacy; and (5) provide feedback to the areas of formulation and application regarding necessary product improvements and conversely, test resulting innovations. Preliminary evaluation experiments may be utilized to test whether responses obtained in growth room experiments can be repeated in the field, to select optimal species or strains from a number of candidate organisms, or to determine such factors as optimal application rates and timing of application (Gomez and Gomez, 1984). These experiments typically involve a large number of treatments and should be carried out at several locations over several years. Replications per trial should be determined by expected experimental error and the anticipated magnitude of response differences between treatments. In many cases, especially for fertility products, four or five replicates per trial will not adequately separate treatment differences. In our experience, ten or more replicates per trial may be required. As many questions on product efficacy as possible must be answered at this stage in order to limit the experimental variables for the technology adaptation experiments in the next phase of field research. Technology adaptation experiments, as defined by Gomez and Gomez (1984), are designed to estimate the range of adaptability of new production technologies. Trials are established at many locations over several years. Locations are not selected at random, but are chosen to represent the range of environments in which the product will be marketed. Because these trials are performed at a large number of sites, the size of each trial is usually small, and its design simple. As

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the emphasis is on the overall performance of the inoculants, multiple location analyses are of primary importance. Each trial should have the same treatments and use the same experimental design to facilitate combining data across locations for analysis. Appropriate controls should be included, not just an untreated check, but also comparisons to currently used agricultural practices. These trials are designed to test the efficacy claims of the product. The results of these trials will form the basis of product performance claims used in marketing, and will largely define the parameters of product efficacy and value for the farmer. Properly done, these trials will also form the basis of product credibility for the farmer and their advisors. During the process of field testing, most of the products' shortcomings in terms of formulation and compatability should be identified. Continuous feedback between the field and formulation and application research groups will stimulate product improvements and optimize performance. 2. External Research External field research, conducted by parties with no formal affiliation with the commercialization of the product, is critical to confirming the results of corporate research and establishing the credibility of the product in the agricultural community. It is important to realize that the credibility of the product and its efficacy claims in the eyes of the farmer will be largely determined by what advisors, public or private extension personnel, say about the product. In addition, regulatory requirements may include supportive independent research. 3. Agronomic Interactions Product development research must, by its very nature, be proactive and conducted with an eye towards changes in agronomic practices 5-10 years in the future. For example, the trend towards minimum tillage causes increased infestation of perennial weeds demanding new approaches to weed control. Agronomic practices may significantly affect the way the product being commercialized may be used, and how it performs in the farmers' hands. This must be addressed by appropriate proactive research designed to answer the questions or address the issues before they occur.

E. Regulatory The requirements for submission of toxicological and, in some cases, efficacy data to gain government approval for sale of a product have been regarded by some as being impediments to the commercialization process. In reality, these data would be generated anyway as part of the commercialization process, and regulatory requirements can greatly aid in satisfying farmers' expectations for reliable, credible products. However, delays in processing submissions can add to the development time required to commercialize products.

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1. Toxicology Extensive pathological, toxicological, and environmental fate data on the organism and formulation are generally required as part of the registration process. Because many biological products consist of naturally occurring organisms, these requirements may be met with less cost and fewer studies than are currently required for chemical products. Often tiered safety testing systems are put in place. If the results of tier 1 testing are satisfactory, tier 2 and 3 testing are usually waived. In Canada, depending on the type of product, toxicology data are required by The Pest Control Products Act or The Fertilizers Act, and are reviewed as appropriate by Agriculture Canada, Health and Welfare Canada, and Environment Canada. In the United States, biocontrol products are regulated by The Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) with the Environmental Protection Agency (EPA) and the Animal and Plant Health Inspection Service of the USDA (USDA-APHIS) sharing responsibilities for review of toxicology data. Biofertilizer products are not regulated at the federal level, but fall into the jurisdictions of the state departments of agriculture. With few exceptions, most states do not require formal registration submissions containing toxicology data for biofertilizer products. Common regulatory requirements between countries would greatly facilitate the commercialization and expansion of markets for biological products and current efforts toward this end are being co-ordinated by the Organization of Economic Co-operation and Development (OECD). The toxicological and environmental fate data required for registration assure the user safety of the biological product and assure society in general of the low safety and environmental hazards of registered biologicals and also, the safety of food produced with these inputs. These assurances benefit biological products and aid in satisfying the farmers' expectation of value. 2. Efficacy Requirements for data submissions to support product efficacy claims vary between countries. In Canada, extensive field research data supporting the efficacy claims of biofertilizers and biocontrol agents must be submitted to obtain registrations under The Fertilizers Act or Pest Control Products Act. Data generated by independent researchers must also be included in registration submissions. Once both the toxicological and efficacy requirements are met, registrations may be issued under these Acts. Regulatory requirements for efficacy data are not as stringent in the United States. In Canada, the requirement for efficacy data as a condition of registration greatly aids in establishing product credibility at the farm gate. All product claims and guarantees must be approved by the regulatory agencies. Additionally, Agriculture Canada inspectors from the Food Production and Inspection branch randomly collect product samples from the manufacturer and retail outlets to ensure the products meet label guarantees. This helps to satisfy the farmers' requirements for reliable, quality products. Enforcement of the regulatory Acts

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in Canada results in high quality, credible products being made available to Canadian farmers.

F. Reliability Farmers expect a product which has consistently high quality. It is, however, difficult for them to identify a poor quality product because they do not have the ability to carry out the analytical procedures used to test the viability of the material. Each company producing biologicals must have a commitment to maintaining a high quality inoculant. Early experience with rhizobial inoculants was poor with many companies selling low quality inoculants (Thompson, 1991). This led many countries to implement regulations and to set up testing facilities to regulate inoculant quality. In Canada, the quality of legume inoculants is strictly controlled through random sampling by Agriculture Canada at the retail level. Samples which do not meet the standards are confiscated. The methods used to assay these products were developed by Agriculture Canada research scientists with years of experience with Rhizobium. Agriculture Canada also monitors the quality of P R O V I D E TM. Since Philom Bios staff had extensive experience working with the product, the setting of product quality standards and developing of testing methods was done by close co-operation between company and government staff. This co-operative approach based on mutual trust and respect (Thompson, 1991) will become increasingly important as new products are developed. Companies are responsible for maintaining consistently high standards as the bitterness of poor quality remains long after the sweetness of low price is forgotten. Quality control must have the total commitment of the senior management. Biologicals present several unique problems in developing comprehensive quality control programs. Since the product is usually produced in batches and there is a potential for variation between batches (Thompson, 1991), every batch must be checked. Methodology is another major problem. The assays tend to be slow. Dilution plating takes from 3 to 7 days. Legume inoculants produced in non-sterile carriers must be assayed using some form of plant nodulation test which can take from 3 to 6 weeks. These methods are labor intensive and costly. Development of such methods is an important function of any quality control laboratory. Quality assurance must have the total commitment of every member of the production company. Random samples from production runs are also assayed, but responsibility for quality may extend beyond monitoring of the product. P R O V I D E TM for canola is sold to farmers as inoculated seed. There are approximately 400 seed treaters across the Canadian prairies and their equipment varies from a simple cement mixer to complicated batch or continuous flow systems. Each system can have a different effect on the viability of P R O V I D E TM spores. A certification system was developed to maintain control over the quality of the product reaching the farmers' hands. To be certified, processors must successfully

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inoculate seed with P R O V I D E TM and maintain product stability in their warehouse. Only certified processors can use P R O V I D E TM on canola. Random samples from production runs are also assayed. Quality assurance must have the total commitment of every member of the production company.

IV. EDUCATION To appreciate fully the value of biological products, the farmer must be taught the limitations and benefits of the new technologies. As these are technologies which farmers are not familiar with, the concept of bioherbicides in the case of DeVine TM, Collego TM and BioMal TM, and the concept of phosphate solubilization in the case of P R O V I D E TM must be taught to farmers prior to or during market launch. This establishes a baseline from which the limitations of biologicals may be understood, and the benefits derived. Addressing the limitations of biological products up front is critical to setting realistic expectations for product performance. For example, farmers must understand that bioherbicides have a narrower spectrum, and decreased speed of action compared to chemical herbicides. Once these limitations are understood, the benefits ofbioherbicides such as efficacious season long control, flexible timing of application, and crop safety may be established. Limitations and benefits may then be combined to arrive at consistently attainable expectations of value. Similarly, issues concerning ease of use must also be proactively addressed. Biologicals consist of living organisms, and must be handled differently from traditional agricultural products. Biological products may require special storage conditions and may require precautions when used with chemical products. This i- balanced by benefits such as user safety, environmental safety, and, in the case of biofertilizers such as P R O V I D E TM, reduced shipping and handling costs of bulk commodities such as phosphate fertilizer. Once again, if the limitations and benefits are properly addressed, realistic and satisfiable expectations of ease of use may be set. Education of farmers and retailers is critical to establishing attainable expectations of efficacy, value and ease of use for biological products. Considerable resources have been spent by marketing and sales on biological products such as Collego TM (Bowers, 1986) and P R O V I D E TM to educate farmers prior to and during the successful market launches of these products. 'Selling knowledge' is as critical to the success ofbiologicals as selling the product itself. If realistic expectations are consistently set by marketing and sales, biological products will meet the expectations of farmers. Just as educating farmers ensures their satisfaction, farmers can in turn educate the development team. Feedback from farmers during the life of a product is critical to product improvements and innovations. Acting upon this feedback will further increase the farmers' level of satisfaction with biological products.

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V. CONCLUSIONS The successful development of biologicals that meet farmers' expectations is characterized by co-operation, creativity and responsiveness. The development team must co-operate with related industries and the public sector. New technology development demands flexibility of approach. The customer knows more than the brightest scientist; thus the development team must listen, absorb, and respond. Response time must be short. For this reason, smaller companies, in partnerships with larger companies, are perhaps best suited to develop biological products. To meet farmers' expectations, the product must deliver function and value. To succeed, those developing the product must deliver knowledge. This is what the farmer expects, whether the developer consciously recognizes this today or not. Farming is the oldest wealth-creating business known to man. Biological products that meet and exceed farmers' expectations will drive productivity gains of benefit to all society.

ACKNOWLEDGMENTS We thank John Cross for his advice and support while preparing the manuscript and Margaret Kenny, Ken Kennedy, Murray McLaughlin and Dan Polenenko for reviewing the final draft.

REFERENCES Boland, G.J. (1990). Biological control of plant diseases with fungal antagonists: Challenges and opportunities. Canadian Journal of Plant Pathology 12, 295-299. Bowers, R. C. (1986). Commercialization of Collego - An industrialist's view. WeedScience 34 (Suppl. 1), 24-25. Boyette, C. D., Q.uimby, P. C. Jr, Connick, W.J., Daigle, D.J. and Fulgham, F. E. (1991). Progress in the production, formulation and application of mycoherbicides. In 'Microbial Control Of Weeds' (D. O. TeBeest, ed.), pp. 201-222. Chapman & Hall, New York. Chambers, J. w. (1992). Influence of a commercial fungal inoculant (PB-50) on plant nutrient availability and crop growth. MSc Thesis, University of Manitoba, Winnipeg. Charudattan, R. (1988). Inundative control of weeds with indigenous fungal pathogens. In 'Fungi in Biocontrol Systems' (M. N. Burge, ed.), pp. 86-110. Manchester Union Press, Manchester. Charudattan, R. (1991). The mycoherbicide approach with plant pathogens. In 'Microbial Control of Weeds' (D.O. TeBeest, ed.), pp. 24-57. Chapman & Hall, New York. Connick, W. J. Jr, Boyette, C. D. and McAlpine, J. R. (1991). Formulation ofmycoherbicides using a pasta like process. Biological Control 1,281-287. Cook, R.J. and Baker, K. F. (1983). 'The Nature and Practice of Biological Control of Plant Pathogens'. The American Phytopathological Society, St Paul, MN. Daigle, D.J. and Connick, W . J . J r (1990). Formulation and application technology

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for microbial weed control. In 'Microbes and Microbial Products as Herbicides' (E. Hoagland ed.), pp. 288-304. American Chemical Society, Washington. Gleddie, S.C. (1992). Response of pea to inoculation with the phosphate-solubilizing fungus PeniciUium bilaji. MSc Thesis, University of Saskatchewan, Saskatoon. Gleddie, S.C. (1993). Response of pea and lentil to inoculation with the phosphatesolubilizing fungus Penicillium bilaii (PROVIDETM). In 'Proceedings of the Soils and Crops Workshop, University of Saskatchewan, Saskatoon, Saskatchewan, pp. 47-52. Gleddie, S.C., Hnatowich, G. L. and Polonenko, D. R. (1991). A summary of wheat response to PROVIDE TM Penicillium bilaji in Western Canada. In 'Proceedings of the Alberta Soil Science Workshop, Lethbridge, Alberta, pp. 306-313. Gleddie, S.C., Schlechte, D. and Turnbull, G. (1993). Effect of inoculation with Penicillium bilaii (PROVIDE TM) on phosphate uptake and yield of canola in Western Canada. In 'Proceedings of the Alberta Soil Science Workshop, University of Alberta, Edmonton, Alberta, pp. 155-160. Gomez, K. and Gomez, A. (1984). 'Statistical Procedures for Agricultural Research', 2nd edn. John Wiley, New York. Jutsum, A. R. (1988). Commercial application of biological control: status and prospects. Philosophical Transactions of the Royal Society of London. B. 318, 357-373. Kenney, D. S. (1986). DeVine | - The way it was developed - An industrialist' s view. Weed Science 34 (Suppl. 1), 15-16. Kucey, R. M. N. (1983). Phosphate-solubilizing bacteria and fungi in various cultivated and virgin Alberta softs. CanadianJournal of Soil Science 63, 671-678. Kucey, R. M. N. (1988). Effect of Penicillium bilaji on the solubility and uptake of P and micronutrients from soil by wheat. CanadianJournal of Soil Science 68, 261-270. Lethbridge, G. (1989). An industrial view of microbial inoculants for crop plants. Special Publication of the Societyfor General Microbiolog? 25, 11-27. Macdonald, R. M. (1989). An overview of crop inoculation. Special Publication of the Society for General Microbiology 25, 1-9. Mortensen, K. (1988). The potential of an endemic fungus, CoUetotrichumgloeosporioides, for biological control of round-leaved mallow (Malva pusiUa) and velvetleaf (Abutilon theophrast~). Weed Science 36, 473-478. Reichelderfer, K . H . (1981). Economic feasibility of biological control of crop pests. Beltsville Symposia in Agricultural Research 5, 403-417. Smith, R . J . J r (1991). Integration of biological control agents with chemical pesticides. In 'Microbial Control of Weeds' (D. O. TeBeest, ed.), pp. 189-208. Chapman & Hall, New York. Smith, S. (1992). Legume inoculant formulation and application. Canadian Journal of Microbiology 38, 485-492. Stowell, L.J. (1991). Submerged fermentation of biological herbicides. In 'Microbial Control of Weeds' (D. O. TeBeest, ed.), pp. 225-261. Chapman & Hall, New York. Thompson, J. A. (1991). Legume inoculant production and quality control. In 'Expert Consultation on Legume Inoculant Production and Quality Control' (J. A. Thompson, ed.), pp. 15-32. Food and Agriculture Organizations of the United Nations, Rome.

5 PATHOGENS" RESPONSES TO THE MANAGEMENT OF DISEASE RESISTANCE GENES James K. M. Brown Cereals Research Department, John Innes Centre, Colney Lane, Norwich, N R 4 7UH, England

I. The Rise of Monoculture II. The Boom-and-Bust Cycle in Theory III. The Boom-and-Bust Cycle in Agriculture A. The Rise and Fall of Resistance Genes B. The Dynamics of Virulence IV. Resistances in Monoculture A. Durable Resistance B. Strategies for Introducing New Resistance Genes C. Managed Deployment of Resistance Genes V. Genetically Diverse Cropping Systems A. Multilines and Variety Mixtures B. Diversification Schemes VI. Uniformity or Diversity? Acknowledgements References

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I. THE RISE OF M O N O C U L T U R E O f the many changes to agriculture brought about in the twentieth century, one of the most profound is the spread of monoculture. A h u n d r e d years ago, crops were diverse mixtures of genotypes, indigenous to a local area, or, in the most advanced parts of Europe, unimproved varieties selected from these land-races. This genetic diversity has been transformed to uniformity by modern farming, so that each field is sown with a single variety of a crop, while the same variety may be grown by farmers hundreds of miles apart. The paradigm of monoculture, which originated in the industrialized countries, has, by now, displaced land-race cultivation of most crops in most parts of the world. Monoculture began in England and France in the nineteenth century, when wealthy farmers realized that, a m o n g the many plants growing in a field, some were superior to others, and could be extracted as pure lines (Barrett, 1981). These early varieties were chosen to provide the m a x i m u m economic return to ADVANCES IN PLANT PATHOLOGYmVOL. 11 ISBN 0-12-033711-8

Copyright 9 1995 AcademicPressLimited All rights of reproductionin anyform reserved

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the farmer. Several decades later, industrialists realized that monoculture could also be beneficial to them (Marshall, 1977). Nowadays, the production of goods as diverse as bread, whisky, coffee and cotton thread, to name but a few, depend on certain phenotypic characteristics of the plants, which are the raw materials of production, being highly uniform. The wisdom of monoculture has often been questioned on the grounds that genetic uniformity makes crops particularly vulnerable to disease (Marshall, 1977; Barrett, 1981). If a strain of a pathogen can infect one plant in a field, it can also infect all the others, and, environmental conditions permitting, all other plants of the same variety grown elsewhere. Monoculture has provided the driving force for major epidemics of diseases that were either serious in former times, such as stem rust of wheat (Pucciniagraminis f.sp. tritict), of minor importance, such as powdery mildew of barley (Erysiphe graminis f.sp. hordeO, or unknown, such as Victoria blight of oats (Helminthosporium victoriae) (Barrett, 1981). Even despite the severe erosion of genetic diversity by modern agriculture, genetic resistance to many diseases is available. Much attention has been given in the plant pathology literature as to how plant resistance genes can best be managed so that the incidence and severity of diseases can be stabilized and reduced. Some pathologists have proposed ways of using resistances so that the commercial benefits of monoculture can be retained. Others, who have questioned the need for a high degree of genetic uniformity, have sought ways of controlling disease by a managed level of genetic diversity, while maintaining the economic value of the crop. Various strategies of managing resistance genes have been described elsewhere, and reference will be made to reviews of these subjects. The purpose of this chapter is to take the discussion a stage further, to ask how pathogens respond to different management systems, and how genetic variation in fungi affects the success of these plans. Firstly, the adaptation of pathogens to resistance genes used in monoculture is described. Then, various ways of managing resistances in monoculture, so as to reduce the rate of pathogen adaptation, are presented. Finally, attempts to replace monoculture by managed diversity are discussed.

II. THE BOOM-AND-BUST CYCLE IN THEORY The theory of population genetic interactions between plants and pathogens owes a great deal to rather idealized models of wild ecosystems. Haldane (1949) appears to have been the first to recognize that genetic diversity might be sustained by interactions between hosts and parasites. Others have developed Haldane's theoretical concepts further, in relation to diseases of both animals (Jayakar, 1970; Clarke, 1976, 1979) and plants (Person, 1966; Leonard, 1977; Barrett, 1988). Most of the models of the co-evolution of plants and pathogens assume a gene-for-gene relationship between resistance and virulence genes, such that an interaction between the products of a resistance allele in the host

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and an avirulence allele in the parasite induces an incompatible interaction (Flor, 1956). In these models, and in others that have developed the theory further, frequencies of host resistance genes and pathogen virulence genes undergo linked, cyclical fluctuations. In each complete cycle, there are four phases (Fig. 1). At the start of phase 1, the frequencies of both the host's resistance gene and the pathogen's virulence gene are low. Since the frequency of the virulence is low, the corresponding resistance is effective. Plants with resistance to disease have, on average, greater mean fitness than those without, so the frequency of resistance increases. In phase 2, the higher frequency of resistance increases the selection on the pathogen population for virulence, so that the frequency of virulence now rises too. Increasing virulence reduces the relative fitness conferred by the resistance gene, and so halts its rise in frequency. During phase 3, the frequency of the resistance falls. This is because most theoretical models include a cost of resistance, such that a plant with a resistance gene has lower fitness, on average, than one with the susceptibility allele of that gene, if both are equally diseased. When the virulence gene is common, so that all plants are heavily diseased, the resistance gene no longer confers much advantage, and any fitness deficit causes its frequency to fall. Phase 4 follows the fall in the frequency of the resistance. The advantage conferred on a pathogen by being virulent then diminishes. If unnecessary virulence confers a fitness deficit, similar to that of unnecessary resistance, the frequency of virulence also falls. The cycle is now completed, and the frequency of resistance can rise again. The sequence of cycles can continue indefinitely. This pattern has been described as a boom-and-bust cycle, the 'boom' being the rise of the resistance in phase 1, and the 'bust' its demise in phase 3. The cycles are sustained by a form of linked, frequency-dependent selection (Clarke, 1976, 1979; Barrett, 1988), since the resistance gene's contribution to the host's fitness is determined by the frequency of the virulence gene, and vice versa. III. THE BOOM-AND-BUST CYCLE IN AGRICULTURE All four phases of the boom-and-bust cycle can occur in agriculture. An example of repeated boom-and-bust cycles, using data on the frequencies of the barley mildew resistance Mlal2 and its matching virulence, was given by Wolfe (1984). However, the progress of the cycle is by no means so predictable as in the theoretical models, and the mechanisms which drive the cycle differ in several important respects from those assumed by the basic model (Fig. 2). A. The Rise and Fall of Resistance Genes

1. The Choice of Crop Varieties In the first phase of the theoretical cycle, the increase in frequency of the resistance is driven by its own fitness, conferred by the low frequency of the virulence in the

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Fig. 1. The theoretical 'boom-and-bust' cycle of the frequencies of a host plant resistance allele and the corresponding pathogen virulence allele. The diagram is loosely based on Fig. 3 of Clarke (1976). The four phases of the cycle operate as follows: 1, The resistance allele is selected when the virulence allele's frequency is low; 2, the virulence allele is selected as the resistance allele' s frequency rises; 3, the possession by a plant of resistance, which is not effective against the current pathogen population, incurs reduced fitness; the resistance allele's frequency therefore falls when that of the virulence allele is high; 4, the possession by a pathogen of virulence, which is not required to infect the current plant population, incurs reduced fitness; the virulence allele's frequency therefore falls when that of the resistance allele is low.

pathogen population. In the cycle' s third phase, the fall in frequency of a defeated resistance gene is driven by ineffective resistances reducing the fitness of the host plant. This model assumes that the population size of the host is extremely large (effectively infinite), and that a resistance gene is not associated with any other character that affects fitness, so that its frequency is determined only by its own effect on fitness.

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Fig. 2. Modifications of the theoretical 'boom-and-bust' cycle in agriculture. 5, the resistance allele's frequency rises if crop varieties carrying it are popular; 6, an effective resistance allele is not used if varieties carrying it are not popular, even if the frequency of the matching virulence allele is low; 8, the virulence allele is selected as the acreage of varieties which have the resistance allele rises (see phase 2 in Fig. 1); 9, the frequency of an ineffective resistance allele may remain high, because the varieties which have it also have other, desirable characters, or because the gene is combined with more effective resistances in new varieties; 10, the resistance aUele's frequency falls if varieties with more effective resistances replace those with the defeated resistance; 11, the virulence allele's frequency rises if this gene is associated with virulences which overcome newly introduced resistances, but falls if it is dissociated from them; 7, the resistance is durable, so that varieties with it do not select virulent pathogens. T h e s e two a s s u m p t i o n s do not hold in m o d e r n agricultural systems, however. Firstly, in most crops, few varieties are widely grown, so that, although there are m a n y individual plants, there are c o m p a r a t i v e l y very few genotypes. Secondly, the frequency of a resistance gene in the p o p u l a t i o n of a crop is d e t e r m i n e d indirectly, by h u m a n i n t e r v e n t i o n in choosing varieties (point 5 in Fig. 2).

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Resistance to a disease can be a significant factor in a farmer's choice of which variety to plant, but control of any single disease is only one of many factors which a farmer must consider. If effective fungicides are available, disease resistance may be a relatively minor consideration, compared to yield and quality. Since the number of varieties is limited, any single resistance gene is inevitably associated with other characters which may be more important in determining farmers' choices of varieties. The frequency of a resistance is therefore not determined directly by the frequency of the corresponding virulence, but by farmers' estimates of the profitability of varieties with that resistance. Some effective resistances have been introduced in new varieties, but, in contrast to the prediction of phase 1 of the theoretical cycle, have not reached high frequencies because the varieties carrying them were not very popular (point 6 in Fig. 2). Examples of such genes are the powdery mildew resistances Mlal and Mla9 in barley (Brown and J#rgensen, 1991). Furthermore, breeders may have difficulty in transferring a useful resistance into commercial cultivars. Despite the fact that the gene mlo, for resistance to barley mildew, has been used in popular spring barley varieties for 15 years (J#rgensen, 1992), no commercial winter barley variety has yet been bred with mlo perhaps because of the difficulty of breeding successful varieties from crosses of winter and spring cultivars.

2. The Fate of Ineffective Resistances The need to consider the overall value of varieties may cause a resistance to be widely used, even when the matching virulence is at a high frequency, in contrast to phase 3 of the model cycle (point 9 in Fig. 2). For instance, many wheat varieties carry a segment of chromosome 1R, translocated from rye. The translocated chromosome, designated 1B-1R, carries the gene Yr9 for resistance to yellow rust (Macer, 1975). Many popular British wheat varieties have the 1B-1R translocation, and therefore Yr9 too, even though the matching virulence has been at a high frequency for several years (Bayles and Stigwood, 1993). This is because the principal target of selection by breeders is increased yield, and the 1B-1R chromosome appears to increase the yield of wheat varieties which carry it (Rajaram etal., 1983). Furthermore, the simple model considers only a single resistance and its corresponding virulence. However, even when a resistance is no longer effective, it may still be presellt in breeding programmes, if the varieties which carried it are considered to be good parents because of their other properties. The old, defeated resistance may th,:refore be combined with effective resistances in new varieties. This has happened repeatedly in barley breeding, where the seven alleles at the Mla locus that ha,,e been used in breeding have been combined with alleles at at least seven other 13ci (Wolfe, 1984; Brown and J~rgensen, 1991). The genes Mlg and Mlra are particularly common in modern barley varieties, despite having little effect against most of the (E. graminis) E.g.f.sp. hordei population in Europe (Limpert, 1987a; Brown and Wolfe, 1990; Wolfe etal., 1992).

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Even when a resistance gene does fall into disuse, this does not happen because possession of that gene causes an inherent lack of fitness in plants which carry it. Firstly, the generalization that resistances to pathogens impose a fitness cost on plants which carry them is not actually valid (Parker, 1992). Secondly, its frequency falls because other, more effective resistance genes, are carried by varieties that are selected by breeders and chosen by farmers (Person, 1966) (point 10 in Fig. 2). As with the introduction of a new cuhivar in the cycle's first phase, many factors other than susceptibility to one single disease contribute to the withdrawal of a variety from cultivation.

B. The Dynamics of Virulence

1. Selectionfor Virulence The second part of the model cycle, the increase in the frequency of virulence, is caused by natural selection on the pathogen population, effected by plants which carry the matching resistance gene. There are three prerequisites for natural selection to occur: there must be variation in a character, the variation must affect fitness and these varying characters, which affect fitness, must be inherited. If these criteria are fulfilled, natural selection is inevitable in a large population (Crow and Kimura, 1970). In many pathogens, including those that cause rusts, smuts and powdery and downy mildews, many virulences conform to the gene-for-gene hypothesis of Flor (1956). Individual isolates of these fungi vary in carrying the virulence or avirulence allele of any one such gene. Which allele the pathogen carries has a major effect on its fitness, by affecting its ability to reproduce on a plant which carries the corresponding resistance. Numerous studies have shown that avirulence is inherited, and have revealed the nature of its genetic control (Thompson and Burdon, 1992). Virulence should therefore be subject to natural selection, and indeed, pathogens have adapted to many host resistance genes. The plant pathology literature contains many examples of selection for virulence. One of the clearest is that of the evolution of yellow rust of wheat (Puccinia striiformis f.sp. triticz) in Australia (Wellings and McIntosh, 1990). There, wheat was free of this serious disease until 1979, when the first outbreaks were caused by race 104E137A-. This race subsequently mutated stepwise to virulence on three resistance genes, YrA, Yr6 and Yr7, carried by Australian varieties which were unaffected by the original epidemic. Phase two of the theoretical cycle can therefore occur in agriculture (point 8 in Fig. 2). However, we can distinguish two different processes by which a virulence may be selected. One follows the introduction of a new resistance gene, when the matching virulence has not previously been selected, while the other follows the rise in frequency of a resistance gene in subsequent cycles.

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2. Adaptation to a New Plant Resistance When a new resistance gene loses its effectiveness, because the pathogen has adapted to it, the resistance is said to have broken down. The breakdowns of three barley powdery mildew resistances in the British Isles have been studied in detail. One clone of E.g.f.sp. hordei broke the resistance of cv. Triumph, conferred by Ml(Ab) + Mla7, in the early 1980s (Brown and Wolfe, 1990; Brown et al., 1990), while another clone broke the resistance of cv. Klaxon (Mla7 + Mlk + MlLa) in 1986 (Brown etal., 1993). The resistance of a group of varieties, conferred by Mlal3, broke down through the emergence of several clones, of which two were especially important (Brown et al., 1991). The isolates in each of these clones had many other factors in common, including other virulences, characteristic responses to fungicides and genetic fingerprints, produced by a D N A probe which can identify whether or not several isolates are members of the same clone (Brown and Simpson, 1994). The exact sequence of events which led to the emergence of these predominant clones is not known, but reasonable hypotheses can be proposed. In none of these three cases had the virulent clone been detected in Britain before the new resistance was introduced. The factors that can introduce a new virulence into a population are mutation, recombination or migration. The T r i u m p h gene, Ml(Ab), had not previously been used in commerce, so the virulent clone was probably a novel mutant from within the British population of E.g.f.sp. hordei. O f the three resistance genes in Klaxon, MILa had not previously been used together with M/a 7 or Mlk in a popular variety. The virulent clone may therefore have been either a mutant or a recombinant progeny of a cross between an isolate with virulence on MlLa and one virulent on Mla7 and Mlk. In the case of Mlal3, one of the two clones which initiated much of the epidemic was probably a migrant from further east in Europe, while the other may have been a novel, indigenous mutant (Wolfe et al., 1992). W h y the population of E.g.f.sp. hordei with virulence towards a new resistance should be so strongly clonal can be explained by thinking of the evolution of each clone as a kind of founder event. Clearly, each clone multiplied rapidly from a low frequency, since the resistance had previously been effective. Once such a clone had successfully infected a plant in a field sown as a monoculture, there would have been no further barrier to its spread, by means of airborne conidiospores, to other, genetically identical plants in the same field, and thence to other fields of the same variety or of other varieties with the same resistance. If dispersal were sufficiently rapid, there would have been little competition with other clones. Since mutation and recombination are both random processes, it is likely that the identities of the predominant, virulent clones were largely determined by chance. The effective population size of a subpopulation of E.g.f.sp. hordei that is virulent on varieties with a new resistance may therefore be extremely small. This simple model may be relevant to some other pathogens, but not to others. The genetic uniformity of E . g . f . s p . hordei populations on newly susceptible

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varieties, over large areas, indicates that the pathogen's rate of dispersal is high relative to the rate of mutation. If it were not, we would expect to have seen local, virulent populations, which were genetically different from one another. The model therefore assumes that mutants to virulence are quite rare, and that the pathogen reproduces and disperses sufficiently rapidly for its propagules to be quickly dispersed over a wide area. The adaptation of E.g.f.sp. hordei to new resistances through the emergence of a genetically uniform pathogen population may therefore be applicable to other pathogens which have high dispersal rates, but not to those with more restricted dispersal rates. The spectacular epidemics of stem rust on wheat in the northern prairies of the USA earlier in this century were often caused by one physiologic race of (P. graminis) P.g.f.sp. tritici. For instance, race 56 caused severe rust on the bread wheat variety Ceres in 1934 and 1937, while race 15B devastated durum wheat in 1953 and 1954 (Stakman, 1955). It is tempting to speculate that, had modern methods of molecular analysis been available, races such as these might have been identified as clones. In barley mildew, therefore, and perhaps in other crop diseases, the breakdown of a resistance occurs through the evolution of one clone, or very few clones, of the pathogen. This process differs from that in the theoretical cycle. The model assumes that each virulence is an independent factor, the dynamics of which depend only on its own fitness. As with resistant varieties, however, the entity that is selected is not a single gene, but an entire genotype.

3. Reselection of a Virulence by a Recycled Resistance Once a virulence gene has evolved in E.g.f.sp. hordei, however, the subpopulation of individuals that carry it rapidly becomes genetically diverse, either by selection of further mutants (Wolfe etal., 1983) or by recombination (Welz and Kranz, 1987; Brown and Wolfe, 1990). Therefore, when a resistance gene is used again, in a subsequent cycle, it is faced by a genetically diverse population of the pathogen, in which the selected virulence is less tightly associated with other characters. In this situation it might be expected that the dynamics of well-established virulences would fit theoretical predictions. This indeed appears to be the case, since the frequencies of virulence genes in the E.g.f.sp. hordei population in a barley-growing area in Denmark were found to be generally close to the values expected from a simple model (Hovm~ller etal., 1993). The contrast between these two kinds of selection for virulent isolates emphasizes that the population genetics of plant pathogens are inseparable from their population structure. Our understanding of the evolution of host-pathogen interactions in crops must be based on a broad view of the ecology of the disease, rather than on simple principles drawn from the theory of natural selection in large, outbreeding populations (Barrett, 1987; Frank, 1992; Thompson and Burdon, 1992).

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4. The Fate of Unnecessary Virulence In the fourth phase of the simple, model cycle, virulences that are no longer necessary for infection of the plant population cause a reduction in the fitness of pathogens that carry them, so that their frequency decreases. However, there is no evidence that selection against unnecessary virulence is a general phenomenon (Parlevliet, 1981 ; Antonovics and Alexander, 1989), although Leonard (1969) presented an important counter-example, in which the possession of virulence genes reduced the competitive ability of isolates of oat stem rust (P. graminis f.sp.

a0enag), The actual behaviour of virulence genes which become unnecessary for infection of the crop can be understood in relation to the pathogen' s population structure. When a resistance gene is withdrawn from commercial varieties, the frequency of the corresponding virulence may either rise or fall (point 11 in Fig. 2). The direction in which it changes depends on the sign of the covariance, or gametic disequilibrium, between it and virulences that are required to overcome the resistance of new varieties (Hovm~ller et al., 1992; Brown, 1994). If the newly selected virulences occur in clones which do not carry the old, unnecessary virulence, so that gametic disequilibrium is negative, the frequency of the old virulence will fall. However, if the old and new virulences are associated, so that gametic disequilibrium is positive, the frequency of the old virulence can rise. For instance, the clone of E.g.f.sp. hordeiwhich broke the resistance of Triumph barley had three unnecessary virulence genes, which matched resistances that were no longer used in commercial barley varieties (Brown and Wolfe, 1990). These virulences persisted in the population of E.g.f.sp. hordei, because of their association with the virulence V(Ab), which was required to infect Triumph (the letters following V in the symbol for a virulence gene correspond to the suffix of the matching Ml resistance gene). The frequency of one of these unnecessary virulences, Va6, later fell, because the clone that broke the resistance of Klaxon carried its avirulence allele (Brown etal., 1993). This effect, known as hitch-hiking selection, is particularly strong in pathogens that reproduce clonally, being greatly weakened if even a limited amount of sexual reproduction breaks up gametic disequilibrium (Brown, 1994). Even if there were a small cost associated with virulence, the fact that fitness is characteristic of the entire genome in a clonal pathogen means that a virulence need not be counterselected, if it is associated with genes that are positively selected (Osterg~trd, 1987; Brown, 1994). Consequently, after a resistance gene is no longer used, the frequency of the corresponding virulence gene may fall, rise or stay constant.

5. Durable Resistance A final, and most important, way in which agricultural systems deviate from the simple, theoretical models is that not all resistances select increased virulence (point 7 in Fig. 2). Many are durable, in that they have remained effective despite being exposed to large amounts of pathogen inoculum (Johnson, 1984). The failure of pathogens to adapt to durable resistances is discussed further below.

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6. Co-evolution of Plants and Pathogens in Agriculture To understand the co-evolution of crops and their pathogens, we must indeed consider the selection for resistance exerted by the pathogen population, and that for virulence imposed by the crop, which occurs in theoretical models of natural systems. However, although these model systems provide some insights into the evolution of pathogens on crops, there are many features of agricultural systems which differ from the simple, theoretical predictions. Among those that must be considered are, on the plant side, the need for breeders and farmers to balance many factors in producing and growing new varieties, the possibility of combining several resistances in a single variety and the existence of durable resistances. We must also take account of the processes by which pathogens adapt to new resistances, by mutation, recombination or migration, the unique population structure of each pathogen, caused by its ecology and epidemiology, and, consequently, the often unpredictable changes in virulence gene frequencies. Proposals for managing resistance genes, in order to control diseases reliably, can be evaluated against the background of the boom-and-bust cycle and the ways in which it is modified in agriculture.

IV. RESISTANCES IN MONOCULTURE A. Durable Resistance By no means all resistances that have been used in crops grown in monoculture have broken down. Indeed, the history of plant breeding includes many examples of successful control of diseases by durable resistances, which have remained effective despite prolonged, widespread use in environments that are favourable to the disease (Johnson and Law, 1975). Durable resistance has been discussed frequently in the plant pathological literature, both in general terms and in relation to many specific diseases, for instance by Johnson (1984, 1993). From a pathogen's point of view, a resistance gene may have a durable effect for two reasons. Firstly, the epidemiology of the disease may prevent rapid evolution, in that a resistant variety may not be exposed to large amounts of inoculum, so that there is relatively little opportunity for the pathogen to adapt to it. Secondly, a genetic factor may prevent the pathogen from adapting quickly to a resistance, despite its population size being large. Johnson (1984) has emphasized that durability is only a description about the past behaviour of a resistance. Even if a pathogen population has so far been unable to adapt to a resistance, it cannot be guaranteed that it will continue to fail to do so. The example discussed in the next paragraph illustrates this point.

1. Durability and Epidemiology The first case is illustrated by the resistance of barley to wheat vtem rust, P.g.f.sp. tritici, (Steffenson, 1992). This disease was previously serious in the Red River

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Valley, a major barley-producing region in the northern part of the American prairies. Since 1942, barley varieties in this area have been protected against stem rust by resistance based on the gene Rpgl. For over 40 years, losses due to rust were minimal. However, a race of P.g.f.sp. tritici, Q C C , virulent on Rpgl cultivars, was first detected in Canada in 1988 (Martens et al., 1989), and caused moderate epidemics during 1990 and 1991. The longevity of the Rpgl resistance was at least partly due to epidemiological factors, rather than purely to properties of Rpgl itself. One factor was that barley is sown and harvested early in the Red River Valley, so that crops probably escaped the worst damage from rust inoculum blown northwards, from Mexico and Texas towards the northern prairies, on the 'Puccinia pathway'. Another was that the population size of P.g. f.sp. tritici was reduced by the use of resistant varieties of another host, wheat, and by the barberry eradication programme. If these two factors did indeed reduce the population size of the pathogen, they would also have reduced the number of virulent mutants that might have started an epidemic of stem rust on barley.

2. Durability and Genetics The second reason for durability is shown by another barley disease resistance gene, mlo. This gene has provided almost complete control of powdery mildew since its introduction into commercial varieties in 1979 (JCrgensen, 1992). Like Rpgl, mlo fits Johnson's (1984)definition of durable resistance, since varieties carrying it have been grown on a total of several million hectares in northern Europe, an environment which is not only highly conducive to barley mildew, but in which mildew is extremely common. Unlike mlo, other single genes for mildew resistance, which fit the gene-for-gene model, have broken down within 2-4 years (Wolfe and Schwarzbach, 1978; Wolfe, 1984; Brown etal., 1991). The apparent inability of E.g.f.sp. hordei to adapt to mlo may be due to the mechanism of this resistance, which differs from those of race-specific resistances (JCrgensen, 1992). Isolates of E.g.f.sp. hordei with increased aggressiveness towards mlo have been selected in the laboratory, although they formed fewer colonies than wildtype, virulent isolates did on varieties without mlo (Schwarzbach, 1979). However, isolates with even this low level of increased aggressiveness have apparently not yet been selected in natural populations by the extensive cultivation of mlo varieties (Schwarzbach, 1987; Andersen, 1991). This lack of adaptation by E.g.f.sp. hordei indicates either that mutants to high aggressiveness on mlo barley occur at an extremely low frequency, and are thus very rarely available to be selected on these varieties, or that mlo-aggressive mutants have low fitness, which outweighs favourable selection by the resistant host.

3. The Absence of General Models for Durable Resistance The durable Rpgl and mlo resistances illustrate a common misconception about durable resistance. Following the experiences of Vanderplank (1968) in breeding potatoes for resistance to late blight (Phytophthora infestans), some pathologists have assumed that resistances that are based on single genes, and which provide

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complete protection against disease, will break down rapidly, while polygenic resistances that do not show a hypersensitive response to infection will be more durable. Some durable resistances are indeed polygenic, but some such resistances have been found to have some degree of race-specific effect on the pathogen (Parlevliet, 1993). However, many more durable resistances than the two discussed above are based on one gene or other simple genetic systems (Johnson, 1984, 1993). There is no single model for durable resistance, either for its genetic control or for the phenotype of its expression. A corollary of the absence of a single model is that there is no simple formula for breeding for durable resistance, to which a pathogen will not be able to adapt. A sensible strategy is to select resistant progeny from crosses of parents with durable resistances, but the success of even this method cannot be absolutely guaranteed (Johnson, 1984, 1993). Breeding for durable resistance to a particular disease must be firmly based on knowledge of the genetics of both the host and the pathogen, rather than on broad, general concepts. However, a long-term commitment to breeding for durable resistance may be repaid by success. In Australia, for example, stem rust of wheat has declined greatly in importance through such a programme (McIntosh, 1992).

B. Strategies for Introducing New Resistance Genes

1. Pyramiding Resistance Genes As an alternative to introducing each new resistance gene by itself in a separate cuhivar, several resistances could be combined in a single variety. This strategy, of deploying pyramids of resistance genes, might prolong the usefulness of the resistance genes if a pathogen could only reproduce on the resistant variety if it carried all the virulences matching the genes in the pyramid. In theory, the probability that a single, mutant individual would arise, with independent mutations to all the virulences, should be extremely low. The aim of pyramiding new resistance genes is therefore to reduce the pathogen's effective rate of mutation to virulence. However, pyramiding has not been uniformly effective in providing durable resistance. The enormous size of many pathogen populations allows multiple mutants to appear, and furthermore, in some cases, the frequency of mutation to multiple virulence may be higher than the product of the separate mutation rates (Mundt, 1990). While many resistance pyramids have broken down, those that have been most effective appear to have been particular combinations of resistance genes. In North America, combinations of resistance genes which have included Sr2 have provided durable resistance to stem rust, while gene combinations including Lrl3 or Lr34 have been durably effective in controlling leaf rust (Puccinia recondita f.sp. tritic0 (Kolmer etal., 1991). Mundt (1991) suggested that some such resistance pyramids may be durable because pathogen races with the corresponding combination of virulences lack

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fitness. This hypothesis is certainly worth further exploration, since at least one virulence, matching the Cf9 resistance of tomato to Cladosporiumfulvum, is caused by deletion of the region of chromosome which carries the avirulence gene, avr9 (van den Ackerveken et al., 1992). Fitness might be reduced if the deletion of avr9 also caused the loss of other functions in the pathogen. Isolates of C. fulvurn that lack avr9 have not been found in cultivated tomato crops (R. P. Oliver, pers. comm.), but as yet, the contributions to fitness of the virulence and avirulence alleles have not been compared. Resistance gene pyramids are also likely to have greater durability if the pathogen has a wholly asexual life cycle, and cannot bring together separate mutations by recombination (Marshall, 1977). Combinations of resistance genes have provided good resistance to wheat stem rust in Australia for many years (Mclntosh, 1992). One factor that might favour this is that the alternate host of P.g.f.sp. tritici does not occur in Australia. Breeders can therefore create combinations of resistance genes in new varieties which are effective against current races of P.g.f.sp. tritici, and even against races which might arise in future, by a small number of mutations, without having to fear the rapid emergence of virulent, recombinant pathogen clones. Pyramiding has provided some successful, durable resistances, but in future, the use of molecular genetic markers to tag genes might make it easier to introduce a group of several resistances into a new variety. For instance, there are two sources of durable resistance to eyespot of wheat, caused by Pseudocercosporella herpotrichoides. One is derived from the French variety Capelle Desprez, the other from V P M , derived from a cross of wheat with a wild grass, Aegilops ventricosa. Molecular markers linked to both these resistance genes have been discovered (Worland et al., 1988; Koebner and Martin, 1990). Plants with both genes have better eyespot resistance than those with either alone (Doussinault and Douaire, 1978). It is difficult to assess levels of eyespot infection accurately, so the use of molecular tags should make it easier for breeders to select plants that carry both resistances.

2. Introducing Resistance Genes Separately By contrast, breeders have sometimes introduced different resistances into cultivation in different varieties, intentionally or otherwise. Some resistances cannot be combined in a single variety, since, in several plants, genes for resistance to one disease are clustered, with many alleles mapping to a single locus (Pryor and Ellis, 1993). When resistance genes are introduced separately, virulences matching the different resistances usually evolve in different pathogen clones, so that gametic disequilibrium between the virulences is negative (Osterg~rd and Hovm#ller, 1991). Such a situation arose in the E.g.f.sp. hordei population in Britain in the 1970s, when different barley varieties with Mla7 + Mlk, Mlal2 or MILa were introduced. The gametic disequilibria between the matching virulences were strongly negative, especially those between Va7 and VLa and between Val2 and Va7 (Wolfe, 1984).

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The fact that different fractions of the pathogen population carried different virulences could be exploited in the design of variety mixtures (Wolfe, 1985) or diversification schemes (Priestley and Bayles, 1980). However, any such benefits are likely to be short-lived if the pathogen has a sexual phase in its life cycle, as does E.g.f.sp. hordei. Races with the combination of virulences required to overcome the combined resistances could be produced by sexual recombination between those with the separate virulences (Wolfe and Barrett, 1976). The composition of the E.g.f.sp. hordei population that broke the resistance of Klaxon is at least consistent with this hypothesis (Brown etal., 1993).

C. Managed Deployment of Resistance Genes Both the identification of durable resistances and the creation of resistance gene pyramids aim to create single varieties in such a way as to restrict the evolution of virulent pathogens. A different approach which aims to limit pathogen evolution is to manage the deployment of varieties in order to control the spread of virulent pathogen populations.

1. The Puccinia Pathway in North America Several pathogens are dispersed over long distances by the wind. A number of proposals have been made to exploit this aspect of their epidemiology in schemes for prolonging the effectiveness of resistance genes. One of these sought to exploit annual movements of populations of the oat crown rust pathogen, Puccinia coronata, through three geographical zones, during the late 1960s and the 1970s (Frey etal., 1977). This fungus overwinters on the small area of production of winter oats in northern Mexico and the southern USA. In spring, spores move through a second region, the central prairies in the USA, and finally, in summer, infect spring oats in the northern USA and southern Canada. Plant breeders in these three regions agreed to use different crown rust resistance genes in their oat breeding programmes. The aim of this plan was to impose selection for different virulences in populations of P. coronata in the three regions. The southern rust population would then be unable to infect the northern oat crop in spring, and vice versa in autumn. However, a sharp decline in the area sown to oats led to this scheme being abandoned because it was too administratively complex to be worthwhile (Mundt and Browning, 1985). A similar proposal was made by Knott (1972), to control stem rust of wheat, caused by Puccinia graminis f.sp. tritici. Dividing the North American continent into the same three areas as described in the previous paragraph, Knott proposed that breeders in the southern zone should use resistances that were not race specific, or else race-specific resistances that were not to be used further north. However, this proposal has not been implemented.

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2. Mildew Resistance Genes in Europe Another proposal for the spatial deployment of resistance genes was based on movements of the barley mildew pathogen across Europe over several years. Several changes in frequencies of virulence genes are consistent with populations of E.g.f. sp. hordeimoving from west to east, in the direction of the prevailing wind, by about 110 km each year (Limpert, 1987a, b). Using these results, Limpert and Fischbeck (1987) proposed that new genes for mildew resistance should be introduced first in countries in eastern Europe. Later, they could be used in countries successively further west. Limpert and Fischbeck (1987) predicted that these genes would still be effective in more westerly countries, because the local population of mildew clones would not include virulent immigrant spores from the east. This proposal has, in fact, been subjected inadvertently to a test, and its effectiveness disproved. The barley mildew resistance gene Mlal3 was introduced into cultivars first in Czechoslovakia in 1978 (Br/ickner, 1987; Dreiseitl, 1993), then in Germany and Scandinavia in the early 1980s (Brown and J~rgensen, 1991), then in the British Isles in 1986, where Val3 mildew first became common in 1988 (Brown et al., 1991). One of the two clones which broke down the Mlal3 resistance was indistinguishable from samples obtained earlier in Czechoslovakia (Wolfe et al., 1992). The ineffectiveness of Limpert and Fischbeck's (1987) plan can be understood by considering the epidemiology of barley mildew further. Two patterns of wind dispersal of mildew in Europe can be distinguished, one of which is the gross movement of populations of E.g.f.sp. hordei by the prevailing wind over some 110 krn each year (Limpert, 1987a, b). On the other hand, individual spores of E.g.f.sp. hordei have been found to be blown several hundred kilometres, across the North Sea, in a single day (Hermansen et al., 1978). This latter form of dispersal presumably occurs whatever the direction of the wind. Easterly winds are unusual in Europe, but do occur several times a year. The combined epidemiological and genetic evidence indicates that it is highly probable that the mildew epidemic on Mlal3 barley was initiated by spores from further east. Even a single dispersal event would have been sufficient, since, to a virulent spore, a field of a resistant variety would be an unoccupied niche, and therefore, once a single infection was established, a potential focal source of disease propagules. Although bulk spore movement is from west to east, the possible dispersal of spores by the wind in every direction in Europe apparently allows epidemics to be initiated in ways that are not necessarily consistent with the prevailing wind. 3. Lettuce Downy Mildew: Combining Resistance Genes with Fungicides The failure of schemes for deploying resistance genes in cereals contrasts with the success of a management plan for genes for resistance to downy mildew (Bremia lactucae) in lettuce grown under glass or other protection in England (Crute, 1989, 1992). There is a long history of breeding lettuce for downy mildew resistance but, between 1978 and 1983, mildew was effectively controlled by a fungicide, metalaxyl (Crute, 1987). Between 1983 and 1986, a strain of B. lactucaewhich was

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resistant to phenylamide fungicides, including metalaxyl, caused failures of mildew control (Crute etal., 1987). It was recognized that the most common phenylamide-resistant isolates carried avirulence towards a resistance gene, Dm11, which was present in several varieties at the time. Control of mildew was therefore re-established by advising lettuce growers to use varieties with Droll and to treat them with metalaxyl (Crute, 1989, 1992). This strategy provided good control for a time, until metalaxy-resistant isolates of B. lactucae, virulent on Dm11, became common. However, these isolates were avirulent on the resistances Dm6, Din16 and R18, so metalaxyl could still be used to control mildew on varieties which had one of these resistances (Crute, 1992). Two factors have contributed largely to the success of this scheme for controlling lettuce downy mildew. Firstly, the disease presents a severe economic threat to growers. Sales of lettuce depend to a large extent on heads being seen, by consumers, to be of high quality. Even modest blemishes, caused by disease, can render the crop unmarketable. The high cost of mildew infection therefore means that growers are receptive to workable schemes for controlling it (Crute, 1989). Secondly, several effective resistance genes are present in advanced breeding material. Selections from these lines, which have both a chosen combination of downy mildew resistances and good, marketable quality, can be multiplied and entered into trials in as short a time as one season after new resistance gene combinations are demanded. Lettuce breeders can therefore respond effectively to pathologists' recommendations (I. R. Crute, pers. comm.). In cereals, by contrast, low levels of diseases on cereals do not greatly affect the market value of the crop, while the long lead time required to produce a new variety means that breeders cannot respond immediately to advice from pathologists. These factors have, no doubt, been partly responsible for the lack of enthusiasm for resistance gene management schemes in cereals.

V. GENETICALLY DIVERSE CROPPING SYSTEMS A. Multilines and Variety Mixtures An alternative to monoculture is the use of heterogenous cropping systems, in which seeds of several varieties of a crop species are sown in the same field. Two forms of this kind of cropping have been studied. Multilines are mixtures of different lines of a single variety, differing mainly in their resistance to one disease (Browning and Frey, 1969). They can be developed by introducing different resistance genes into the genetic background of the chosen variety by backcrossing (e.g. Briggle, 1969; K#lster etal., 1986). In variety mixtures, by contrast, different varieties, each with different genes for resistance to the target disease, are sown together (Jensen, 1952; Wolfe and Barrett, 1980; Mundt and Browning, 1985; Wolfe, 1985). Both multilines and variety mixtures can produce considerable reductions in

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the severity of disease. This can lead to lower expenditure on fungicides, improved yield and quality and greater stability of performance across different environments and in different years (Wolfe, 1985). Mixed varieties have several advantages over multilines, in that they can control diseases other than the one that is the primary target for control and can also buffer the crop against nonbiological stresses, so that temporal and geographical variation in the crop's performance is reduced (Mundt and Browning, 1985; Wolfe, 1985). However, one of the major obstacles to the widespread use of spring barley mixtures in Britain has been the reluctance of maltsters to consider using a variety mixture, because of the possible differences in malting quality of the component varieties (Wolfe, 1984). If the market requires a highly uniform end product, multilines should be acceptable even when variety mixtures are not, because of their greater genetic uniformity in characters other than disease resistance (Wolfe, 1985).

1. Control of Disease in Mixtures Mixtures - whether multilines or mixed varieties - control disease in several ways. The principal mechanisms are epidemiological, in restricting the spread of spores from one compatible host to another. If a clone of a pathogen is virulent on some varieties in a mixture, but not on the others, its rate of increase is reduced, partly because the distance between susceptible host plants is greater than in a stand of a pure variety, and partly because resistant plants act as barriers to spore dispersal (Burdon, 1978; Chin and Wolfe, 1984a). A physiological mechanism may also restrict the growth of virulent pathogens in mixtures. This is induced resistance, a process in which prior infection by an avirulent pathogen limits the development of a later infection by a virulent one. This would enhance the effect of a mixture if each plant were infected by a population comprising both virulent and avirulent spores (Chin and Wolfe, 1984a). Induced resistance is a rather weak, localized effect in cereals, both in response to rusts (Johnson, 1978) and mildew (Woolacott and Archer, 1984; Martinelli, 1990). However, in many dicotyledonous crop species, which express induced resistance strongly (Kuc, 1982), it might be exploited in designing mixtures. Many theoretical studies of the behaviour of pathogen populations in mixtures can be interpreted in terms of the distance and barrier effects. It has been proposed that the reduction of disease in a mixture, compared to a pure variety, depends on the relative rates of autodeposition of spores, on the plant on which they were formed, and allodeposition, on other plants. If the varieties in a mixture are fully randomized, increasing allodeposition would increase the effectiveness of a mixture, since both the distance and barrier effects would make greater contributions to reducing the severity of disease, because the rate of transmission of spores between plants is restricted (Barrett, 1980; Ostergaard, 1983). More generally, increasing the probability of alloinfection, by increasing the chance that a spore would land on a plant of a different variety to that on which it was formed, has been predicted to increase the effectiveness of a mixture (Mundt and Leonard, 1986; Mundt et al., 1986). This probability can be manipulated experi-

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mentally by altering the layout of the mixture, such that the unit areas occupied by plants of the same variety are varied. Reducing the unit area would increase the barrier effect, and thus reduce the rate of successful alloinfection.

2. Pathogen Populations in Mixtures: Theory Interest in the genetic adaptation of pathogens to mixtures has focused on the prediction that races of the pathogen, capable of attacking all varieties in the mixture, may be selected. The evolution of such super-races, and their importance relative to simpler races, is favoured in theoretical models if there is little or no selection against unnecessary virulence (Groth, 1976; Barrett and Wolfe, 1978; Marshall and Pryor, 1978). A second factor which is predicted to favour complex pathogen races is a high rate of allodeposition, so that there is a relatively high probability of spores, formed on one variety, infecting another (Barrett, 1978, 1980; Ostergaard, 1983). Barrett (1980) showed that, if the rate of allodeposition is low, complex races of the pathogen may be favoured early in the epidemic, when a pathogen clone which is able to infect all components of the mixture would have an advantage. Later, simple races should replace the more complex ones, because, once the disease is well established, individuals with optimum fitness on one host variety would be favoured. With a high rate of allodeposition, however, complex races would predominate and ultimately become fixed. To summarize the conclusions of these theoretical models, the dynamics of pathogen race frequencies depend on the balance between the advantage to the pathogen of being able to reproduce on a greater proportion of the mixture and the cost of the ability to infect more varieties successfully.

3. Pathogen Populations in Mixtures: Data There have been comparatively few attempts at critical tests of hypotheses about the evolution of pathogen populations in mixtures. The influence of pathogen fitness on the evolution of complex races has been particularly neglected. However, the hypothesis that greater alloinfection would favour more complex races has been tested. Huang et al. (1994) investigated the selection of races of E.g.f. sp. hordei, capable of attacking all three varieties in a barley variety mixture, in relation to the relative proportions of auto- and alloinfections. They studied changes in race frequencies in pure stands and in four layouts of mixture. In one type of mixture, plants of the three varieties were sown randomly, so that the host genotypes were thoroughly mixed. The three other types of mixtures were sown as alternating rows, with blocks of one, three or six rows of the different varieties. The rate of alloinfection therefore decreased in the different types of plot, going from random mixtures, through one-, three- and six-row mixtures, to pure stands. There was no evidence that more complex pathogen races, with virulence on more varieties, had a selective advantage over simpler races in pure stands or in six-row mixtures. The rate of selection for complex races was successively greater, however, in three-row, one-row and random mixtures. The hypothesis

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that greater alloinfection would favour more complex races of mildew could therefore be accepted. Other reports of experimental work on pathogen evolution in mixtures have described changes in the composition of the population and commented on possible reasons for these observations. Munk (1983) found an increase of complex races of E.g.f.sp. hordei in a mixture of seven barley varieties with different mildew resistance genes, in which there was a particularly high rate of alloinfection. Chin and Wolfe (1984b) found selection for complex races in some mixtures, but not in others. In some experiments, simple races predominated on plants of one variety in a mixture, but complex races on another. Observations of race frequencies in field trials are consistent with Barrett's (1980) prediction that complex races may be favoured at the start of the season and later replaced by simpler ones (Barrett and Wolfe, 1980). The greatest use of variety mixtures in modern agriculture was in the former German Democratic Republic (GDR), where most spring barley was grown as mixtures between 1984 and 1991 (Wolfe et al., 1992). However, the genetic diversity in these mixtures was limited. Most mixtures included varieties with the mildew resistance genes Mlal2, Mlal3 and mlo. In a survey carried out in 1990, there was a significant increase in the frequency of pathogen races with combined virulence for the two race-specific genes, Mlal2 and Mlal3; as mentioned above, mlo is still effective against all known clones of E.g.f.sp. hordei. In 1991, however, the frequency of the complex race, with Val2 + Val3, fell relative to that of simple races, which carried either Val2 or Val3, but not both (Schaffner et al., 1992). Isolates with the combined virulence were generally more sensitive to ergosterol C14 demethylation inhibitor (DMI) fungicides than isolates with single virulences, so the increased use of D M I fungicides during 1991 m a y h a v e selected against the complex virulence (Wolfe et al., 1992).

4. Pathogen Fitness in Mixtures Theoretical analyses of the fitness of pathogens in mixtures have concentrated on the cost of unnecessary virulence genes, which allow a pathogen to overcome racespecific resistances. However, a more general aspect of pathogen fitness is adaptation to different host varieties. Many other genes in a plant, apart from recognized resistance genes, may affect quantitatively the ability of an individual pathogen isolate to grow and reproduce. If there were no such adaptation to the genetic 'background' of a plant variety, one would expect a mixture of different varieties, carrying the same resistance genes, to have a similar level of disease to that on the varieties grown as pure stands. However, three different barley mixtures, each of which consisted of three varieties with the same identified resistance genes, all reduced the amount of mildew substantially compared to that on pure stands of the same varieties, although the reduction was not as great as that in a mixture of three varieties with different resistances (Wolfe et al., 1981). Unidentified, 'background' genes may therefore have influenced the performance of these mixtures.

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There is some evidence for adaptation of pathogens to different varieties in several diseases. Adaptation of this kind, not governed by race-specific resistances, has been found in potato late blight, with isolates of P. infestans being better adapted, in general, to the potato variety from which they were isolated than to other varieties (Jeffrey et al., 1962; Caten, 1974). In work on other diseases Leonard (1969) observed adaptation of (P. graminis) P.g.f.sp. avenae to Craig or Clintand A oats, Clifford and Clothier (1974) detected adaptation of brown rust (Puccinia hordes) isolates to the barley varieties Julia, Sultan or Vada, and Chin and Wolfe (1984b) discovered isolates of E.g.f.sp. hordei which were differentially adapted to Hassan or Wing barley. Clearly, future results on changes in the composition of pathogen populations in variety mixtures need to be interpreted in relation to the fitness of isolates on varieties, not just in terms of the costs and benefits of particular race-specific virulences. If adaptation of isolates to varieties' genetic backgrounds is indeed a general phenomenon, a mixed variety should be expected to provide better control of disease than a muhiline, the components of which carried the same resistance genes as did the varieties in the mixture. I am not aware that this hypothesis has been tested.

5. Predicting the Peorormance of a Mixture A further, important question which has not received much attention is the extent to which the genetic composition of a pathogen population affects the performance of a mixture. MartineUi (1990) predicted that a mixture of varieties with different resistance genes, effective against different fractions of the pathogen population, would control disease more effectively than a mixture in which the resistances in the different varieties were effective against the same pathogen clones. In a field trial, the choice of varieties to include in mixtures was made on the basis of knowledge of the frequencies of virulence genes and genotypes in the previous year. The prediction was confirmed. A mixture of three varieties which were susceptible to mildew, but to different clones of E.g.f.sp. hordei that were then prevalent in the population, was more effective in reducing disease and increasing yield than a mixture of three other varieties, which also carried different resistances but which were susceptible to the same, common clones of E.g. f.sp. hordei. These results indicate that the value of a mixture might be optimized by choosing the component varieties carefully, taking into account the contemporary genetic composition of the target pathogen (Wolfe and Barrett, 1980). Much of the theory of the genetic composition of pathogen populations in mixtures has studied equilibrium frequencies of genotypes (Groth, 1976; Barrett and Wolfe, 1978; Marshall and Pryor, 1978; q)sterg~trd, 1983). Martinelli's (1990) results, however, indicate that the long-term equilibria of genotype frequencies, and the question of whether simple or complex races will predominate, is essentially irrelevant to the performance of a mixture in any given season. Much more significant is the composition of the population at the start of that season itself, since a pathogen goes through a small number of

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generations in each season, and the effect that the mixture is expected to have on that population.

B. Diversification Schemes A less extreme type of genetic heterogeneity than variety mixtures is diversification of varieties between fields (Priestley and Bayles, 1980). A farmer using a diversification scheme would plant neighbouring fields with varieties which, if not resistant, are susceptible to different races of the pathogen. This is a form of deployment of varieties in monoculture, but the principle is the same as that of variety mixtures, since the pathogen is being manipulated through its inability to grow on more than one variety. It might be expected that this kind of varietal diversification would not control disease very effectively if spores were mainly dispersed to other plants in the same field, as is the case for many foliar diseases. Studies of oat crown rust showed that this is indeed the case if the initial inoculum is dispersed evenly over the crop (Mundt and Leonard, 1985). However, inter-field diversification can inhibit the spread of a pathogen if an epidemic is initiated from a strongly focal source, by disrupting the progress of the epidemic front (Mundt and Leonard, 1985; Mundt and Brophy, 1988). Diversification schemes might therefore provide some control of diseases which are dispersed from a few point sources, but be relatively ineffective against diseases which are well dispersed at the start of each year's epidemic, as are powdery mildew and yellow rust of cereals in Britain.

Vl. UNIFORMITY OR DIVERSITY? Monoculture is a highly attractive system, both for farmers and for consumers. For the farmer, it offers the opportunity to choose the varieties that will return the greatest profit, and to maximize the efficiency of his operations. For consumers, especially those that are food-processing companies, it allows optimization of production runs and thus savings in costs (Marshall, 1977). However, monoculture clearly has risks, because of the rapid adaptation of pathogen populations to crop varieties. Monoculture need not be abandoned, but in order for it to be successful, the performance of crop varieties should be predictable. Clearly, this is not so if crops are vulnerable to the sudden, unpredictable emergence of virulent pathogens. Durable resistance is therefore an essential component of successful monoculture. Whether it is achieved by the chance discovery of genetic systems which provide effective resistance, or by the deliberate combination of proven genes, there is no single formula for durable resistance (Johnson, 1984, 1993), and no substitute for hard work and good luck. Mixed varieties have proved to be effective in controlling many diseases

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(Wolfe, 1985), and are a valid alternative to chemical control of disease. They offer the possibility of increasing yields, or at least stabilizing them, while reducing input costs. From a pathologist's point of view, some questions about the control of disease in mixtures need to be answered by further research. However, the greatest obstacle to the use of.mixtures is the demand for uniform produce. Much of the output of cereal production in the industrialized world is used for animal feed; here the progress of mixtures should not be limited by the fastidiousness of consumer demand. For many other uses of cereals and other crops, the require: ment that produce should have predictable characteristics may be more justified. Perhaps the greatest need for research on mixtures is therefore in assessing whether the produce of variety mixtures is indeed more variable in quality than that of pure lines and, if it is, in reducing this variation to such a level that mixtures can be used to provide the raw material for food and drink processing. At present, many farmers face a multitude of conflicting pressures, many of them political in nature. Much of the general public demands that farms should be run on environmentally benevolent lines and, at the same time, wishes to buy high quality produce, free of disease. The political insistence on reducing the production of crops which are in surplus conflicts with the need of farmers to increase output, because of falling prices. Whether they are presented within the framework of uniformity or diversity, plans for controlling disease by the use of genetic resistance must take account of the economic pressures on farmers and, in particular, must allow them to grow the most profitable varieties.

ACKNOWLEDGEMENTS

I thank John Barrett, Roy Johnson, Chris Mundt and Martin Wolfe for helpful comments on a draft of this review, and Ian Crate for discussion on lettuce downy mildew. Work on cereal pathology at the John Innes Centre is supported by the Ministry of Agriculture, Fisheries and Food.

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THREE SOURCES FOR NON-CHEMICAL MANAGEMENT OF PLANT DISEASE: TOWARDS AN ECOLOGICAL FRAMEWORK Alan Maloney Department of Plant Pathology, Cornell University, Ithaca, NY 14853, USA

I. II. III. IV.

Goals for Disease Management in the Coming Decades Context: Sustainability Sustainability and Non-chemical Approaches to Disease Management Non-chemical Disease Management-Three Lines of Research A. Traditonal Farming: Learning from Sustainable Peasant Agriculture B. Role of Biotechnology (Molecular Biology) in Developing Alternatives to Chemical Disease Management C. Biological Control V. Conclusions Acknowledgments References

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I. GOALS FOR DISEASE MANAGEMENT IN THE COMING DECADES The growing interest in non-chemical methods of disease control, pest management and weed control are in part a reaction to the environmental and health hazards resulting from modern agriculture's enormous dependence on chemical inputs. Some of the problems associated with the chemical paradigm of modern agriculture as currently practiced are pollution and negative health effects resulting from toxicity, overuse and overdependence on chemical pesticides, large inefficiencies of energy and resource use, interruption of natural ecological nutrient cycling, land and water degradation, and destruction of biological communities that otherwise support crop production. Practices that use or disperse fewer chemicals, whether in agriculture or in other industries, are perceived as more beneficial, because they offer the promise of less environmental pollution. Other problems associated with the chemical paradigm of modern agriculture are economic in nature. To be certain, improved agricultural productivity has been achieved in many cases, especially as measured by macroeconomic criteria in the short term. However, this apparent progress has often been undermined by other effects of modern agriculture: pollution and illness, concentration of ADVANCES IN P L A N T P A T H O L O G Y - - V O L . 11 ISBN 0-12-033711-8

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economic power, disempowerment and displacement of rural communities, rampant land degradation, and wholesale loss of traditional knowledge and social structures. Because of the narrower margin for absorbing failure in agrarian societies, these social costs may be more apparent in the developing countries. Social, political and economic critiques have been leveled at modern agriculture, and its promotion in developing countries (Altieri, 1987; Blaikie and Brookfield, 1987; George, 1990; Wright, 1990). According to these critics, agriculture that depends less on the chemical paradigm and industrial technology is perceived as more beneficial, because it allows for more stable economic and social/political structures in agriculture. My intention here is to present a conceptual framework that identifies three different lines of research that can contribute to non-chemical approaches to disease management. These are traditional farming practices, biotechnology and biological control. In addition, a revised definition of biological control will be presented. My hope is that comparing and contrasting these three categories will be useful both for analyzing existing practices and identifying fertile territory for future research directions in plant disease management. Before discussing the particular categories, I place this work in the context of agroecology and sustainable agriculture. II. CONTEXT: SUSTAINABILITY

This chapter seeks to establish ways to discover and understand how to make disease management in agriculture more environmentally sustainable. The principles of sustainability in agriculture are taken from the principles of applied ecology and agroecology. As applied ecology, agriculture must be based in basic ecological theory, including particularly r- and K-selection, island biogeography, community structure, stability and invasiveness, and succession (Thomas and Kevan, 1993). Agroecology recognizes the importance of ecological theory in agriculture, but explicitly acknowledges agriculture as a human activity, carried out within ecosystems in which human social systems are an integral part (Altieri, 1987). There are a number of criteria that can be used to evaluate whether agricultural practices and tools are ecologically sustainable: 1. Emphasizing land management for the long term (Blaikie and Brookfield, 1987) and employing practices that enhance the long-term productivity of the soil, diversifying the agricultural landscape, protecting the soil from erosion, recharging groundwater supplies and maintaining the soil organismal communities for efficient organic residue recycling and disease control. 'The wincipal basis of sustainable land use is the long-term maintenance of the productive capacity of soils' (Thomas and Kevan, 1993). 2. Putting a full array of natural processes to work directly and indirectly in

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commodity production, rather than paying to eclipse all but a few such processes. 3. Minimizing energy loss in agriculture by increasing the efficiency of energy (fossil fuel or biological) transfer between trophic levels or steps during commodity production. These are necessary, though not sufficient, criteria. Additional criteria will need to be added for local conditions or particular practices. In addition to environmental sustainability, this chapter recognizes the related issues of economic sustainability, which usually top the lists of features of sustainable agriculture. Sustainable agriculture and sustainable development have become expressed goals of most governments, the United Nations, businesses, environmental groups and trade organizations. Government policy for sustainable agriculture customarily responds to shrinking numbers of farms, diminishing farm profitability, and other aspects of an economically vulnerable agricultural sector. Its responses include setting priorities for diversifying or preserving the agricultural sector of a region (which is defacto social and environmental, not just economic, policy), and implementing a variety of policies to enhance farmers' ability to stay in business. These actions are clearly critical for maintaining farming and related agricultural practices as a part of a region's social and economic fabric: for agricultural operations to be sustainable, they must be economically viable. Therefore, in discussing disease management in the context of sustainable agriculture, we must attend to both economic and environmental sustainability and must recognize the interdependence of the two. We must recognize that humans are not separate from ecosystems, but major actors within ecosystems, and as such, humans must protect the environmental support systems that allow ecosystems to maintain themselves. A primary goal of sustainability is therefore the maintenance or rehabilitation of the environmental support systems, by bringing human activities into balance with the rest of the ecosystems in which they are carried out. Therefore, while agricultural sustainability requires that farming and other forms of agriculture must be by some definition economically viable activity, there are environmental and ecological constraints which must be attended to if human populations are to live without diminishing the capacity of their environment to sustain them. This will be an ongoing process, with dual challenges. The first is to discover and understand how to make human activities, such as agriculture, both environmentally and economically sustainable. The second is to effect those changes. Hawken (1993) has defined sustainability in a way that neatly ties together economic and environmental aspects of sustainability, in this case in a discussion of the relationship between business and the environment. He describes it primarily in relation to business in a broad sense, but it applies well to agriculture. He recognizes the tensions between economic activities and the environment, and offers some general ideals for designing those activities to replenish the environment. Sustainability is defined:

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9 in terms of the carrying capacity of the ecosystem, and described with inputoutput models of energy and resource consumption. Sustainability is an economic state where the demands placed upon the environment by people and commerce can be met without reducing the capacity of the environment to provide for future generations. It can also be expressed in the simple terms of an economic golden rule for the restorative economy: Leave the world better than you found it, take no more than you need, try not to harm life or the environment, make amends if you do. Sustainability means that your service or product does not compete in the marketplace in terms of its superior image, power, speed, packaging, etc. Instead, your business must deliver clothing, objects, food, or services to the customer in a way that reduces consumption, energy use, distribution costs, economic concentration, soil erosion, atmospheric pollution, and other forms of environmental damage (Hawken, 1993).

III. SUSTAINABILITY AND NON-CHEMICAL APPROACHES TO DISEASE M A N A G E M E N T Sustainability is a new paradigm for modern agriculture, and the design and assessment of specific practices to approach a goal of sustainability is necessarily an ongoing process. This sets a challenge to be met by researchers, farmers, and others. Answering this challenge will take the form of a dialectic between our understanding of available practices and our expanding knowledge of ecological relationships in agroecosystems. Discussions of sustainability commonly comprise discourses on 'macroecological' questions, such as fertilizer use, groundwater nitrification, soil erosion, and overall productivity 9 They rarely treat the topic of disease management, though as with all aspects of agriculture, disease management can be assessed within a conceptual framework of sustainability and a theoretical ecological framework. It must be noted that although this chapter exclusively addresses non-chemical means for disease management within a context of sustainability, it should not be inferred that any particular methodology or set of practices is a priori excluded. For instance, because organic agriculture explicitly rules out the use of external chemical inputs, some may assume that 'sustainable' agriculture is a synonym for 'organic' agriculture. I do not make such an assumption, for to believe that sustainability would be achieved only by the complete removal of chemical inputs would be far too simplistic. M u c h current design of chemical approaches to disease or pest management places a very high priority not only on efficacy and retarding the development of pathogen resistance to fungicides and insecticides, but also on the specificity and biodegradability of pesticides (De Waard et al., 1993). This trend is a direct result of environmental concerns about chemical pesticides. The place of chemical control in sustainable agriculture was addressed recently (Corey et al., 1993).

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IV. NON-CHEMICAL DISEASE MANAGEMENT: THREE LINES OF RESEARCH The remainder of this chapter consists of a discussion of the potential for research to contribute to the development of non-chemical disease management in the coming decades. Three sources of'non-chemical' disease management strategies are discussed: traditional farming systems, biotechnology and biological control. The three are rarely considered together, except as one is perceived to threaten to replace another in the development of modern agriculture. Too often it is assumed that one particular lens for agriculture is the only one that can be used. In contrast, I am proposing a different way to frame the relationship among these sources of non-chemical methods. Rather than regard traditional farming systems and biotechnology as opposing poles, I propose to view biological control as a bridge that draws from and connects these two approaches. In doing so, I hope to demonstrate the potential of all three lines of research to contribute to sustainable agricultural practices that will far exceed the results delivered to date. Furthermore, I suggest that by comparing and contrasting these approaches, we can derive fresh perspectives, tools, and practices for the development of nonchemical approaches to disease management. From judicious and balanced attention to all three, we can improve our chances to foster wisdom in our interactions with the land. This chapter recognizes the cultural basis of both science and agriculture. The term agriculture will usually be used with the modifiers 'traditional' or 'modern' to generally distinguish between peasant agriculture in developing countries and the more mechanized, high-input variety commonly associated with industrialized nations. 'Western science' will be used to denote research and development fostered mainly in and by universities and corporations in the industrialized nations. Much of this chapter refers to culturally specific practices and traditions in agriculture. To avoid confusion, the term 'cultural practices', commonly used in both agricultural and anthropological literature, will be replaced with 'agronomic practices'. In each major section devoted to different lines of research, examples will be cited only to illustrate the discussion; they will not be exhaustive.

A. Traditional Farming: Learning from Sustainable Peasant Agriculture Many traditional farming practices and systems are &facto sustainable, because they have supported sizable human populations on the same lands for hundreds and sometimes thousands of years. Sustainable traditional farming systems have evolved in many different cultures, in many different regions of the world, under a diverse variety of climatic conditions. Sustainable farming practices have developed because they have proven flexible and resilient. Traditional farming practices, as described by Thurston (1992) and many anthropologists and ecologists, are part and parcel of the practices of agrarian

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societies and traditional farming systems in particular ecological settings. Sustainability in traditional systems has not been achieved by the application of any Western definition of scientific research, but has been derived through long tenure on the same or similar land, trial and error with crops and practices, and sharing of knowledge within and among families in rural communities. Indigenous knowledge applicable to farming is site-specific and dynamic, not static. Traditional farmers in developing countries, like their counterparts in 'modern' and organic agriculture in the industrial nations are constantly experimenting (Chambers et al., 1989; Thurston, 1992), and in so doing, generating new knowledge. Some practices endure, others pass away. Indigenous knowledge of agriculture and ecosystems has been long ignored, and undermined, by Western agricultural sciences (Thurston, 1992). 'Most scientists and many of the world's farmers have abandoned traditional farming practices and systems in an effort to increase food production and income and to improve the efficiency of land and labor use' (Trutmann and Thurston, 1993). A large body of literature on traditional farming systems is already accessible, but most of it is not in the agricultural science literature. Reporting on indigenous knowledge systems has come from ' . . . anthropologists, ethnobotanists, archaeologists, and geographers- and to a lesser extent, ecologists, economists, and sociologists...' (Thurston, 1992). In any case, it has been done by scientists and social scientists who have attempted to understand not only the specific practices but also the cultural underpinnings of these practices. Crossing geographic and cultural divides between industrial agricultural and traditional systems is seriously needed in agricultural science. If our goal is to develop sustainable agricultural practices, it seems reasonable to try to understand how these practices work. The importance of understanding such practices in the context of agricultural sustainability is easily established, because many of the features of peasant agriculture satisfy goals of agricultural sustainability (Trutmann and Thurston, 1993). Traditional agricultural practices are less fossil-fuel intensive and chemical intensive than 'modern' agricultural practices. Most traditional farming systems utilize crops with a broad genetic base. Many include the return of considerable amounts of organic material to the land, ensuring high levels of microbial diversity in soils. And many are highly productive and resilient to the effects of local pests and pathogens, over the long term. Study of traditional farming systems presents a great challenge in itself. Western scientists often minimize of dismiss farmer practices, unless they persist and look carefully at what the farmers do. Western scientists must surmount cultural and/or linguistic boundaries that isolate them from traditional farmers, if they are to understand traditional farming systems. One example, from one of the few projects that has involved both anthropologists and a plant pathologist, illustrates this point. In a research project to understand constraints to bean production in Rwanda, anthropologists concluded from surveys that farmers regarded insect pests as the worst problems they faced, and that plant diseases were rarely considered a problem. Only after further studies did the team discern

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that the farmers did not identify particular diseases, but identified different periods and kinds of rain that led to plant putrefaction. From the Western science perspective, the rains predisposed crops to seed and seedling rots by various kinds of pathogens, and thus were a related rather than a central factor (P. Trutmann, pers. comm.) Furthermore, when resurveyed, farmers placed 'rain tolerance' (disease resistance) second in importance on a list of factors for which they selected varieties for their planting mixtures (Trutmann et al., 1993). At least two features are critical to good studies of traditional farming systems: (1) interdisciplinary collaboration among scientists and social scientists; and (2) collaboration with those most knowledgeable about these systems, the local farm families, understand and develop methods and technology (after Chambers, 1990). The initial emphasis should be on learning from the farmer about her or his crops, fields, practices and beliefs. Observational research must be emphasized, including: extended discussion with farmers about their own perceptions of their practices, the diseases present and how farmers deal with them; (Western) scientific assessment of disease, the suppressive potentials of the individual practices, and overall farming system; and finally, comparison of these with modern agriculture. It should go without saying that the visiting scientist must have respect for the culture and practices of the traditional farmers, and avoid judgmentalism. Assertions that particular practices are 'right' or 'wrong', 'good' or 'bad' too often have simplistic and culture-bound connotations.

1. Plant Disease Management in Traditional Farming Systems Thurston (1992), in 'Sustainable Practices for Plant Disease Management in Traditional Farming Systems', has made by far the most extensive study and compilation of traditional agricultural practices that are specifically relevant to plant disease management. The general lesson of this important book is that there is a wealth of diverse sustainable agricultural practices used in traditional farming systems throughout the world, and that workers in international agriculture need to understand these practices and the sociocultural context in which they are used. In the context of this chapter, the importance of his book lies in its usefulness as a starting point for research into traditional farming practices for sustainable disease management strategies. 2. Examples Although there are many distinct sets of practices that make up traditional agricultural systems, the plant disease management implications of very few have received any attention from agricultural scientists. Genetic heterogeneity of crops seems to be a linchpin of disease management in many systems. In a study of bean production in central Africa (Trutmann et al., 1993), farmers preferred mixtures to single varieties, and selected their varieties on the basis of yield and, apparently, disease resistance, although the farmers involved in the study were unable to express the methods they used to select varieties with physiological resistance to disease. One of their techniques, however, was to test germplasm

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themselves, either by planting it directly in with their own mixtures or in isolated portions of their fields. Direct evaluation of germplasm by the Western scientists demonstrated that many varieties were completely resistant to local strains of important pathogens. The proportion, in mixtures, of varieties resistant to anthracnose (Colletotrichum lindemuthianum) was higher in areas in which this disease was a severe problem, and lower in areas where it was less favorable to anthracnose development. Mixtures whose varieties had resistance to various pathogens offered protection for the entire crop in a field, preventing epidemics of any single disease, and guaranteeing the farmer at least some harvest. Varietal mixtures reduced disease severity and spread more than the mean of the disease resistance of the individual varieties in the mixtures (Wolfe, 1985; Trutmann and Graf, 1993). Farmers in this study also culled blemished seed (damaged or infested by pathogens) from their mixtures before planting, thus reducing the inoculum of various pathogens (Trutmann etal., 1993). Another feature of many traditional systems, with implications for disease management, is the addition of 'copious quantities of organic amendments' (Thurston, 1992). This practice undoubtedly builds a high degree of microbial diversity in soils, which has been shown by research in biological control to enhance the suppression of soilborne pathogens. However, reports on the microbiology of traditional agricultural systems are almost non-existent. Slash/mulch agricultural practices have evolved in many locations around the world. The central characteristic of this kind of farming system is the cutting of the vegetative growth of perennial plants and leaving the cuttings in place as mulch, into which a crop is planted. Slash/mulch practices are used in many different climatic zones. Some utilize native plants without cultivating them; others plant trees or herbaceous legumes for the purpose of providing mulch. The use of slashed mulches is a multipurpose practice which serves to insulate soils from temperature extremes, retain soil moisture, return nutrients to the roots of crop plants, suppress weed growth, and reduce or prevent erosion. Numerous slash/ mulch systems are used in drier settings around the world, also. For example fast-growing leguminous trees such as Erythrina and Leucaena are used as shade for perennials such as coffee, mulch, green manures, forage and live fences. Fixed nitrogen and rapid cycling of nutrients are obtained by mulching with the periodically pruned branches and leaves, in between tree rows (Ramfrez et al., 1993). Although there is little or no information available as to the effects of these practices on plant disease (H. D. Thurston, pers. comm.), one such system in Mexico has been documented by Garcia-Espinosa and colleagues (Garcia-Espinosa, 1980; Garcia-Espinosa etal., 1994). In Tabasco, large swampy areas are inundated for up to 7 months of the year. The dominant vegetation is popdl grass (Thalia geniculata) or other marsh grasses, which are cut down at the beginning of the dry season. Short-season maize varieties or other crops are planted in the high-organic-content soils. As the seedlings emerge, a superficial burn of the mulch is carried out, scorching but not killing the germinating maize nor damaging the regrowth of the grasses. The popdl system produces high yields of maize

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(higher than neighboring mechanized maize cropping), and requires minimal input besides labor. Experiments to investigate soilborne plant disease demonstrated that popdl soils suppressed the severity of several pathogens (GarciaEspinosa, 1980; Lumsden et al., 1981). Plastic mulches have become widely used in vegetable and fruit cropping in North America (an excellent example of an environmentally non-sustainable practice, considering the many square kilometres of plastic sheeting that are discarded every year). Organic mulches as used in traditional farming systems are used by some farmers. Researchers at the US Department of Agriculture have been experimenting with a slash/mulch system using vetch species (Abdul-Baki and Teasdale, 1993). Seeded in the fall, the vetch was cut down in spring and left in place, and~'omato seedlings were planted directly into the slashed legume. Fruit yields were higher than with plastic mulch, and far higher than for non-mulched tomatoes. Damage from potato beetle was minimal and there were indications of reduced disease incidence. The use of organic mulches resembles the use of crop residues in biological control (Cook and Baker, 1983). Crop residues can have positive or negative effects on pathogens (e.g. Rickerl etal., 1992). Some foliar pathogens can overwinter successfully in crop residues, providing next season's inoculum, but different pathogens may be affected by different cultural practices during distinct phases of crop growth or times of the year, or pathogens of some crop species may be inhibited by mulches consisting of the residues of other plant species. As for other traditional practices, there is abundant anecdotal evidence of the impact of slash/mulch systems on plant diseases. However, almost no specific attention has been given to disease-reduction in slash/mulch or other traditional practices, or to ways of improving the disease management in such systems or integrating the use of such practices to modern agriculture.

3. Research in Disease Management of the Role of Traditional Practices Study of disease management implications of traditional farming systems may lead to the emergence of several kinds of knowledge relevant to sustainable agriculture. One has to do with improvements in developing-country agriculture, one with integration of sustainable practices into modern agricultural systems, and the other with a possible overriding lesson for modern agriculture. What conclusions can be drawn from research on disease management in traditional agricultural systems so far? 1. Many improvements in traditional farming systems are undoubtedly possible and desirable, but practices and technologies developed for disease management in industrialized countries cannot be transferred wholesale to developing countries. The dominant model of Western agriculture emphasizes monocultures, heavy and repeated applications of fossil-fuel derived inorganic fertilizers to satisfy nutrient demands of high-yielding monocultures, pesticides to combat a wide array of weeds, insects, and pathogens; substitution of

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mechanization for human or animal labor at every opportunity; cultivar uniformity; and, finally, nearly exclusive reliance by growers on corporations for these inputs. These features are in direct contrast to traditional farming systems which have evolved in the absence of all these inputs. Traditional farming in developing countries typically involves peasant agriculture on small farms. Peasant agricultural practices result from a long-term process of adjusting to the environment (Teri and Mohammad, 1988). They are holistic, pragmatic, culturally embedded, site-specific and based on ethnobotanical knowledge. It is clear that direct transfer of technology from industrialized nations usually fails in traditional agricultural settings. Wholesale importation of Western technology and practices disrupts longstanding integrated crop production systems, destabilizes communities economically and lacks the environmental sensitivity to maintain ecological sustainability. In addition to all the specific detailed questions that Western studies may have investigated in traditional production systems, they should return to a few very basic questions. What factors and practices, from both farmers' and scientists' perspectives, keep the crops healthy? Are particular practices in traditional systems responsible for suppression of particular diseases? Or does only an integrated ensemble of practices provide sustainable disease protection? The answers could lead to insights about how to improve traditional systems, or to transfer certain lessons or practices to modern agriculture. 2. Traditional farming systems provide a potentially rich source for finding new approaches for disease management in industrialized countries. They represent applied ecological science in cultural contexts different from those that give rise to science as we describe it. How to understand this knowledge, and how to integrate it into modem agricultural science, is not obvious. It is no doubt as foolish to expect traditional practices to transfer wholesale to industrialized countries as vice versa. Knowledge in traditional farming systems takes the form of local specific knowledge of a particular place: its particular softs, weather, crops, animals and neighboring plants. But the ecological lessons from such systems should inform agricultural science in the industrialized countries. This requires one to learn to understand the traditional practices within the frame of reference of the farmers themselves, to expect that farmers' practices are based on internally consistent world views, and to persist in learning the descriptive language and customs, and then recast these in terms of Western scientific practice. 3. Neither of the previous two conclusions admits yet another possibility, namely that traditiomd farming systems may provide the nucleus for an agricultural paradigm that offers an alternative to modern agricultural systems. For instance, one of the central characteristics of traditional agricultural systems that seems to be the main component of disease management potential is the diversity in the genetic base, soil microbial communities, management options, and heterogeneity of the cropping systems and surrounding ecosystems. This

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is in marked contrast to modern agricultural trends towards homogenenizing and simplifying the genetic base of crops, losing diversity in microbial populations, and depending on a few uniform external inputs. The lessons known by and learned from peasant farmers need to be reconciled with the practices of industrial agriculture. The benefits of understanding traditional farming are not restricted to traditional systems themselves, but ' . . . may reveal important ecological clues for the development of alternative production and management systems. Industrial countries have much more to learn and probably will benefit more from the study of traditional agriculture than will developing countries . . . ' (Altieri, 1987).

B. Role of Biotechnology (Molecular Biology) in Developing Alternatives to Chemical Disease Management The second group of disease management practices discussed are those derived from agricultural biotechnology, and these are explored in relation to their economic and environmental sustainability. They present striking contrasts to the traditional systems in that they involve newly acquired techniques, are undertaken primarily in industrialized nations, and rely most heavily on Western practices of laboratory science. Just as important insights into non-chemical methods of disease management await us through the study of traditional farming systems, significant contributions may also be derived from molecular biological research. As with most other fields of agricultural research in the industrialized nations, plant pathology has undergone rapid expansion in molecular biology research during the past decade and a half. Agricultural biotechnology could be defined as including almost any use of selective breeding, biochemical experimentation to modify plant or animal varieties, and tissue culture methods to produce somatic mutants or disease-free plant material. A more specific definition is used here, namely, the use of recombinant DNA or molecular biological technologies to modify and study plants, animals or microbes. Whereas traditional farming systems represent applied ecology, agricultural biotechnology is applied molecular biology. To a great extent, agricultural biotechnology has so far been an extension of conventional genetic or breeding research. There are at least two important differences between the two kinds of research. First, whereas conventional breeding work is carried out at least with exposure to agroecosystems, agricultural biotechnology begins with experimentation and design that is completely removed in time and place from agroecosystems, and placed in isolation in laboratories. Second, in agricultural biotechnology, genetic combinations between non-related organisms can be made and are a primary focus of this kind of work. Among the first priorities for agricultural biotechnology research has been

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the generation of crop varieties with improved agronomic or nutritional characteristics, herbicide tolerance, and pest- or disease-resistance. Transgenic crop varieties are anticipated to serve a variety of specific purposes, from simplifying the management, protection, or storage of crops, modifying the nutrient composition of crops, and increasing the efficiency of microbial adjuncts to crop varieties. Although the major emphasis in agricultural biotechnology is on the generation of new plant and microbial varieties, this has not been its exclusive focus. Several classes of molecular biological techniques - particularly DNA hybridization and sequence amplification methods such as Southern hybridization and polymerase chain reaction (PCR) - provide the capability to detect genes and microbial organisms with great precision and sensitivity, and are increasingly important in plant disease diagnostic applications and the study of microbial ecology. Agricultural biotechnology is still in its infancy. The use of recombinant technology to develop a commercially useful disease-resistant cuhivar has not yet proven a shortcut to conventional breeding approaches. Isolating appropriate genes and establishing stable transgenically derived resistance that is durable in the field requires lengthy experimentation. No plants constructed for resistance in such a way have yet been commercialized. A number of biological hurdles confront researchers in understanding the mechanism of expression of transgenic resistance. However, as more resistance genes are isolated and methodologies for locating them are improved, recombinant approaches will probably accelerate the development of new varieties. For any particular type of genetic modification, the initial few examples will require the longest research time, and subsequent varieties will be quicker to develop. In addition, for ecological, social and political reasons, such organisms require much more scrutiny for environmental safety than conventionally derived organisms do. Finally, the environmental sustainability of genetically engineered organisms is uncertain. So far, the primary motivation for agricultural biotechnology has been the development of products for use in modern agricultural contexts. Molecular biological methodologies have given scientists the power to alter organisms' genomes rapidly by making changes in their genetic structures that probably would never have occurred in nature, and to select organisms that express specific traits. Many countries' legal systems allow these organisms to be patented. The perceived control that recombinant methodologies gives scientists over the genetics of organisms, and the results for product ownership and potential profit, make for an obvious linkage between corporations (or governments) and agricultural biotechnology. Many hundreds of millions of dollars have already been spent on such research in the industrial nations. Thus, the emphasis in agricultural biotechnology has been economic, which predisposes it more to considerations of economic sustainability. Environmental sustainability of particular genetically modified organisms, and the fit between them and ecosystems in which they might be placed, is not an ongoing concern of research in agricultural biotechnology. If considered, it is separate from and

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pursued much later than the economic usefulness of a genetically engineered organism. The genetic manipulation of plants and animals for agriculture is as old as agriculture itself, and biotechnological modification represents part of a continuum of technological approaches to that end. However, since its inception, genetic engineering has been a social issue as well as an environmental one. The question of what amounts to 'appropriate deployment' has become a critical question regarding the use of genetically engineered organisms (Altieri, 1987). Debates on the use of genetically engineering and genetically engineered organisms in the environment often spill over into political arenas (witness the ongoing debates in Europe and the United States over bovine somatotropin and licensing of and public acceptance of, tomatoes modified for extended shelf life). The importance of the social aspect of the deployment of genetically engineered organisms is regrettably trivialized by those who maintain that public resistance occurs only because the public is scientifically illiterate. The only aspects of these concerns that are routinely required by government policies are 'scientific risk assessment' aspects of environmental and human health safety issues pertaining to genetic engineering (Lesser and Maloney, 1993, Maloney, 1995). It must be noted, however, that scientific risk assessment addresses only one small component of environmental sustainability. It only asks whether a genetically engineered organism will do no environmental harm, over a short term. It does not ask the far more important question for environmental and economic sustainability, namely, 'Will it fit into an agroecosystem or into an economic system, over the long term'. Possibly more important for environmentally sustainable plant disease management in the future will be the impact of molecular biological tools on pathogen identification and microbial ecology. Hybridizational and PCR techniques already available are increasingly important for detection and diagnosis of particular pathogens or for monitoring their population levels before they attain critical disease thresholds. More important in the long run, these techniques are useful in investigating organismal ecology. In some cases they permit the re-examination of problems previously intractable for want of appropriate tools. Mutational labeling of microbial strains facilitates selection and tracking of microbial isolates. PCR technology, especially, provides a qualitative improvement in detecting microbial populations that are dispersed, uncommon, or unculturable. Pathogen taxonomic and epidemiological studies now routinely include DNA sequence or restriction fragment-length polymorphism (RFLP) analysis. These and other basic methods have been introduced into the majority of plant pathology research operations in industrialized countries, and are being used increasingly in developing countries and international agricultural centers. Such research does not necessarily lead to the development of disease-resistant plant varieties. Application of various recombinant DNA techniques may greatly broaden our understanding of plant disease interactions and microbial-plant ecology and provide a basis for new biological control strategies (Nelson and Maloney, 1992, 1994).

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1. Examples Transfer to plants of pathogen genes whose presence or expression confers pathogen resistance to a crop ('pathogen-derived resistance'; Sanford and Johnston, 1985) represents one recombinant approach to non-chemical disease management. Numerous transgenic lines resistant to different virus strains have now been established, with varying levels and breadths of protection to different viral strains (Fitchen and Beachy, 1993). The mechanisms of resistance are not yet well understood in most cases. Single-gene resistance to bacterial or fungal pathogens has been demonstrated to be accessible and transferable through cloning based on molecular mapping (Martin et al., 1993b). A tomato gene that confers resistance to races of Pseudomonas syringae has been isolated from a resistant cultivar and transferred to susceptible cultivars (Martin et al., 1993a). The molecular engineering of endophytic and epiphytic microbes has not yet been applied to plant disease management, but is a commercially appealing strategy for disease protection. The basic approach is to transfer traits to plant symbionts or other plant-associated microbes to confer some kind of protection to the plant through production of a pathogen-suppressive chemical (toxin) or nutrients that change the epiphytic microbial community (Andrews, 1992). Technical feasibility of this approach has already been demonstrated for insect pest management: Clavibacter strains were engineered to express 6-endotoxin from Bacillus thuringiensis in maize (Fahey et al., 1991). In other experiments, the potential for entirely artificial plant-microbe symbioses has been explored, using transgenic plants that synthesize opines (normally conferred on a plant only by Agrobacterium tumefaciens parasitism), and transgenic P. fluorescens strains that have been engineered to utilize the same opines (Farrand et al., 1994). Modification of Pseudomonas syringae strains for loss of ice nucleation properties is an example of genetic engineering of an epiphytic bacterium. Plant protection, in this case from cold temperatures rather than disease, was achieved by displacing a resident microbial strain with the non ice-nucleating strain (Lindow, 1987). By themselves, the developments listed here are significant breakthroughs in technology and disease management, and provide insight into the genetic and cellular basis of plant disease processes. Used appropriately, modified plants and microbes could be integrated into agricultural production systems for significant improvements in the management of refractory diseases. 2. Conclusions Several features of agricultural biotechnology have been discussed in this section. What roles may there be for applied molecular biology in sustainable disease management practices? 1. So far, agricultural biotechnology research is predisposed toward improvements to modern agriculture in industrialized regions of the world. Agricultural biotechnology is research intensive, and emphasizes the innovation of

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individual varieties of plants or microbes. A number of planned and anticipated genetically engineered plants are predicted to reduce the need for chemical pesticides. These would therefore contribute to non-chemical plant disease management, and should be evaluated for their sustainability. Agricultural biotechnology emphasizes the development of marketable products for use in agriculture. Its focus is more on innovations for economic usefulness than for ecological appropriateness, thus it is oriented more toward a context of economic than environmental sustainability. Risk assessment of genetically engineered organisms (GEOs) addresses only whether GEOs will do obvious harm in the short run. It does not address whether a genetically engineered organism will fit within a context of either economic or environmental sustainability. Therefore it should not be regarded as a major criterion for agricultural sustainability. The operational basis of agricultural biotechnology is the development, in laboratories, of genetically engineered organisms that meet particular economic needs of corporations or farmers. This practice inherently disconnects agricultural ecosystems from their component organisms, by isolating the organisms from their environments during the entire process of their genetic modification. Field testing is essential to eventual use of the modified plants, but as currently practiced is aimed mainly at establishing the efficacy of the modified organism; only incidentally does it address the fit of such organisms within an ecosystem. Reconciling the tendency of biotechnology research to undermine holistic perspectives with an agroecological framework for sustainable agriculture is a critical challenge. The greatest relevance to sustainable plant disease management of agricultural biotechnology may lie in the tools it provides for understanding microbial ecology, plant-microbe interactions, and the importance of biological diversity in agroecosystems.

C. Biological Control Although they are by no means identical, next to 'organic agriculture', 'biological control' probably most typifies for the public the notion of non-chemical pest or disease management. Introduced as a specific term in the early twentieth century, the definition of biological control has undergone several modifications. Biological control of insects is better known than that for plant disease, through widespread use of integrated pest management based heavily on principles of insect population ecology and parasitology. Insect predators and parasitoids are widely used on some cropping systems, as is the bacterial lepidopteran pathogen Bacillus thuringiensis and, increasingly, baculoviruses. In their important book 'The Nature and Practice of Biological Control of Plant Pathogens' (1983), Cook and Baker suggested that biological control offers the chance of improving crop production ' . . . within existing resources, avoiding pathogen resistance to chemicals, and relatively pollution- and risk-free

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c o n t r o l . . . ' , making biological control environmentally attractive. One of their descriptions identifies it as a non-chemical means of disease management" ' . . . Biological control may be accomplished: through cultural practices (habitat management) that create an environment favorable to antagonists, host plant resistance, or both; through plant breeding to improve resistance to the pathogen or suitability of the host plant to the activities of antagonists; through the mass introduction of antagonists, nonpathogenic strains, or other beneficial organisms or agents' (Cook and Baker, 1983). They gave a formal definition of biological control in plant disease applications" 'The reduction of the amount of inoculum or disease-producing activity of a pathogen accomplished by or through one or more organisms other than man . . . ' (Cook and Baker, 1983). However, this definition gives the impression that biological control is a result mainly of direct interactions between individual antagonists and pathogens, and that human activity is somehow peripheral to biological control. This impression is tacitly contradicted by their book's detailed discussions, but should be explicitly addressed. First, it has been shown repeatedly, especially for soils and composts, that biological control depends on the activity of microbial communities. Second, although many individual antagonists with biological control potential have been isolated, upon subsequent field experimentation their activity is commonly not maintained or is insufficient to explain directly the extent of disease suppression that may be seen in the field. Third, many traits have been hypothesized to be significant in microbial interactions, but there are few cases in which any single trait has been shown to play a definitive role in disease suppression. Finally, human intervention is integral to the enhancement of biological control, whether through individual species or through agronomic practices. We are left with the knowledge that plant disease can be suppressed by microbial activity, and that in agroecosystems, human manipulation is needed to enhance the conditions for that microbial activity. The effectiveness of this manipulation is often predictable, though we cannot often identify or control the individual traits or species which effect this suppression. Therefore, ensembles of properties and organisms, and indirect effects of agronomic practices, microbial species and microbial communities on pathogens, should be accommodated in a definition of biological control; pragmatically, they may be more important for pathogen suppression than are direct interactions between individual organisms. Therefore, a revised definition is offered here to fully legitimate agronomic practices, the indirect effects of practices on disease management, and the necessary role of human intervention within biological control: Biological control involves the stimulation or enhancement of biological activity in ord~,rto reduce the amount of inoculum or disease-producing activity of pathogens.

1. Two Subdisciplines a. Agronomic Practices Biological control has come to have two distinct subdisciplines. The first is based on 'exploitation or manipulation of natural com-

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munities' for pathogen control (Cook, 1993). It consists mainly of agronomic practices utilized for their tendency to enhance plant health or to directly reduce the incidence of disease. Examples include crop or cultivar rotation, various tilling strategies, addition of organic amendments such as compost, mulch or manures, sanitation practices, flooding before planting, soil aeration or solarization, and so forth. Overlap between agronomic practices for biological control and traditional practices that affect disease management provides a major link between biological controland traditional practices. 'Biological control' provides a Western scientific lens with which to interpret many of the traditional farming practices that should be evaluated for plant disease management potential. A number of cases of direct relationships are known between particular practices and the decline or occurrence of particular pathogens (Palti, 1981; Cook and Baker, 1983). Reports of research that could be relevant to biological control of plant disease is dispersed in the agricultural and ecological literature. Conversely, research that focuses on agronomic characteristics, such as yield, and their relationship to cropping practices (cultivar or crop rotation, for instance), tillage, fertility management, and so forth, commonly includes only anecdotal reports of disease pressure.

b. Microbial Antagonism The second subfield of biocontrol has come to be called microbial antagonism: the deliberate use of specific antagonist organisms for prevention or management of specific diseases. Research into microbial antagonism has expanded so much, relative to research into agronomic controls, that the term 'biological control' is often used nearly synonymously with microbial antagonism (cf. Andrews, 1992). Microbial antagonists have been sought and studied for several reasons, including the relative ease of working with individual microbial isolates compared to systems or communities. Microbes, especially bacteria and viruses, and to a somewhat lesser extent, fungi, lend themselves to genetic manipulation and the study of cause-effect relationships of their behavior. The advent of recombinant DNA technology has provided new methods for manipulating and studying the behavior of microbial antagonists (Nelson and Maloney, 1992; Cook, 1993; Kluepfel, 1993). As noted before, microbial antagonism has been attractive because of its anticipated similarity to pesticide-style control for a variety of diseases. The isolation and development of a microbial antagonist follows a somewhat routine path (Maloy, 1993). Typically, microbial field isolates are screened for their effectiveness in reducing the severity of a particular disease or their ability to interfere with pathogen growth or reproduction. This step can derive from field observations, but is most commonly performed in vitro. Isolates' physiological characteristics may be studied. Strains are then assessed for performance in the field. Further strain selection, genetic manipulation, and formulation may be carried out to improve their effectiveness against particular pathogens, efficacy in the field, simplify their dispersal, and increase their shelf life. There are numerous examples of this procedure in temperate agriculture (e.g. Handelsman etal.,

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1990), and a few from tropical agriculture (e.g. Mew and Rosales, 1986). Cook (1993) recently outlined the process, from screening of field isolates to commercial use, of biocontrol agents for the suppression of take-all (Gaeumannomycesgraminis var. triticz)on wheat. Recombinant DNA methodologies are now used extensively in microbial antagonism research. There has been a resurgence in research on antagonists during the past decade, partially stimulated by the availability of recombinant DNA methods to study their behavior, genetics and physiology (Nelson and Maloney, 1992; Sutton and Peng, 1993). Topics of such research range from tracking microbial distribution and fate in soils, understanding or enhancing antagonist suppressiveness, and the role of antibiosis in survival of bacteria in the rhizosphere, to research on the molecular basis of piant-microbe associations, directed at the possibility of creating artificial symbioses that would effect control of pathogens (Weller, 1988).

2. Biocontrol- Slow to Develop? Biological control, especially when limited to the definition as 'microbial antagonism', is often considered to have fallen far short of its promise. Direct field experimentation with promising individual strains has resulted in only a very few consistently effective and economical (or commercially viable) antagonist formulations (Adams, 1990; Cook, 1993). The central criticism of biological control acknowledged by Cook and Baker in 1983 ' . . . [T]here was nothing to sell the grower . . . ' is still true today (Andrews, 1992). Indeed, only eight products for biological control are currently registered for sale in the United States (Becker and Schwinn, 1993). This has led to considerable pessimism for the future of biological control as a significant contributor to plant disease management, if only saleable products are counted (el. Andrews, 1992). Development has been hampered by several factors, among them the success of the chemical paradigm - the creation of toxins and other inputs that enhanced productivity in the short term - and the failure of microbial antagonists to meet the same criteria as effective fungicides, such as rapid action, cost- or laborefficiency, ease of application, and broad effectiveness. Finally, there are many microbial isolates that have been demonstrated to have potential as antagonists for different pathogens. This has rarely been followed by intensive efforts on formulation of the antagonists to optimize their performance and to make their storage and packaging convenient (Cook, 1993). Research efforts and funding in biological control have not been as sustained or intensive as efforts in chemical control. Funding and research effort dedicated to an ecological approach to plant disease management has been small relative to that which has been devoted to plant physiochemistry and chemical pesticides. It is no surprise that biological control is in its infancy (Adams, 1990; Andrews, 1992). Authors are alternately optimistic and pessimistic about the prospects that biocontrol will ever provide much economic control of plant pathogens (Adams, 1990; Andrews, 1992; Sutton and Peng, 1993). However, they are in general

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agreement that sustained, prolonged research into the ecological mechanisms that underlie biocontrol is vital to the eventual availability of biological control strategies.

3. Ecological Basis of Biological Control Essentially, biological control is applied microbial ecology for plant disease management: it emphasizes the behavior and activity of microbes in suppressing plant diseases. It represents a very different approach to plant disease management than does chemical control. Broader usefulness of biological control will rely on greater understanding of the relationships among microbial populations, between microbial populations and soils, and between microbes and plants. A strong theoretical ecological basis for research in biological control exists. New techniques for the study of microbial ecology and physiology, including methods for assessing microbial activity and recombinant DNA-based manipulation and detection methods, are readily available along with the entire spectrum of more classical approaches. With appropriate support for such research, and incentives for interdisciplinary collaboration on biological control, this work should flourish. One of the most difficult but important research areas related to biological control is the composition and microevolution of rhizosphere and phylloplane microbial communities. This topic has widespread implications for biological control and agroecology, because it addresses the diversity and interactions within microbial communities, and thus the role of direct and indirect effects of both microbial antagonism and agronomic practices in pathogen suppression. Increasing breadth and detail in such research is possible by combining conventional microbiological techniques with the use of selectable markers, sophisticated statistical approaches, and computer simulations.

4. Evaluating for Agroecological Sustainability The effective application of ecological principles in the design of biological control strategies contributes in general to their environmental sustainability: strategies' fit in a particular agroecosystem is not a priori guaranteed, but resulting disease management strategies will already have taken many ecological relationships into account. Agronomic practices and microbial anatagonists can be considered from the standpoints of prevention of pathogen establishment or control of established pathogen populations (after Huber and Watson, 1970). Categories describing the practical applicability of biocontrol strategies can be a basis of criteria for economic and environmental sustainability of biological control practices. Microbial antagonists, for example, can be considered in terms of the temporal durability of the control they provide: self-sustaining control resulting from the single application of a biocontrol agent; partially self-sustaining, requiring occasional reapplication; and transient control requiring repeated application (the mode of use of typical fungicides) (Cook, 1993). Identification, study and development of agromic practices with biological control potential that meet criteria of agroecological sustainability should be promoted.

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5. Examples The use of organic amendments, ranging from crop residues to manure to dredged canal mud is a feature of many traditional and modern agricultural systems (Thurston, 1992; Cook and Baker, 1983). Specific effects of particular organic amendments on individual pathogens have not been well described. It may be that the use of diverse organic amendments serves to prevent establishment of pathogens as much as control existing pathogen populations. Research on, and use of, composted materials for pathogen suppression is increasingly important in biological control for container and field use (Hoitink and Fahy, 1986; Nelson and Craft, 1992). The relationship of suppressiveness of compost microbial communities to compost starting material and compost age is critical for reliable use of composts in disease management applications (Boehm et al., 1993). Many microbial antagonists - mycoparasitic, fungal and bacterial - display disease-suppressive qualities (Cook and Baker, 1983). More microbial antagonist research has been performed on soilborne pathogens than foliar ones (Andrews, 1992; Becker and Schwinn, 1993), in part because of the importance of soilborne diseases in many crops, and the prohibitive costs or health hazards of chemical control for many soilborne pathogens (Cook, 1993). Several reviews, which examine various aspects of microbial antagonism research, have been published in the past few years (Cook, 1993; Sutton and Peng, 1993; Adams, 1990; Baker, 1987), so examples will be presented only briefly here. The best known mechanism of biological control is mycoparasitism. Several mycoparasites, such as Sporidesmium sclerotivorum, Talaromycesflavus and Coniothyrium minitans, have been demonstrated to have great potential for the control of sclerotia-forming fungal parasites such as Sclerotinia and Sclerotium spp. Pythium nunn shows promise for use in control of pathogenic Pythium species. Trichoderma harzianum, although a poor competitor in non-sterile soils, is useful in many biocontrol applications if it is the initial colonizer of a substrate. S. sclerotivorum is the most thoroughly understood mycoparasite from an ecological perspective (Adams, 1990). A considerable body of research now exists on the production of antibiotics by several strains of Pseudomonasfluorescens, which provide significant suppression of several soilborne pathogens, including Pythium species and Gaeumannomyces graminis var. tritici (take-all of wheat) (Howie and Suslow, 1991; Mazzola and Cook, 1991; Mazzola etal., 1992; Keel etal., 1992). Progress has been made in understanding the role of antibiosis as a mechanism to enhance colonization and population growth; current emphasis includes the regulation of antibiosis biosynthesis in natural environments. Agrobacterium radiobacter strain K84, and its recombinant derivative K1026, are the premier examples of economical biological control with a bacterial antagonist (Ryder and Jones, 1990). This case illustrates how multiple dominant antagonist traits can be understood and combined with appropriate application methods to generate a disease-management strategy that is apparently ecologically sound (,Jones and Kerr, 1989). The effectiveness of A. radiobacter strains in controlling

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crown gall (A. tumefaciens) on fruit trees is commonly attributed to their production of agrocin and at least one other antibiotic. However, their effectiveness also depends on their ability to colonize tree roots efficiently. This is enhanced by dipping bare root stocks in antagonist suspensions, thus applying the antagonist directly to the pathogen's normal infection courts (Cook, 1993). Finally, strain K1026 was engineered to prevent transfer of agrocin resistance from A. radiobacter to A. tumefaciens, and, interestingly, is the only recombinant microbe licensed in any country for commercial use in agriculture. Mechanisms of antibiosis have received the bulk of attention in recent years. The roles of several other microbial traits are being studied as well, including siderophore production (Loper, 1988; Keel et al., 1989; Kraus and Loper, 1992), nutrient competition and pathogen stimulant inactivation (Maloney et al., 1994). Handelsman and colleagues found that a strain of Bacillus cereus (UW85) was effective in field trials against alfalfa damping off caused by Phytophthora megasperma f.sp. medicaginis (Handelsman et al., 1990). Using discriminant analysis, they found that application of UW85 resulted in significant alteration in the entire rhizosphere community, in terms of the distribution and abundance of other rhizosphere species. However biological control was effective, and microbial community alteration occurred without the persistence of high populations of UW85, which were found to be greatly reduced in the rhizosphere soon after application (Gilbert et al., 1993).

6. Conclusions 1. The redefinition of biological control given here, by emphasizing the stimulation of biological activity for the reduction of disease or pathogen activity, legitimizes direct and indirect effects of microbial behavior, and recognizes the central role of human actions in enhancing these effects. 2. Development of biological control methods should proceed with conscious attention to ecological principles. Greater understanding of community ecology of the rhizosphere should be possible with further application of increasingly well-developed and applicable ecological theory and molecular and statistical techniques. The linkage to microbial ecology, and the use of microbes resident in local agroecosystems, predispose biological control approaches to a high degree of environmental sustainability. 3. Under the definition given in this chapter, biological control as a scientific discipline works well as a bridge among different approaches for non-chemical disease management. It can accommodate a wide variety of agronomic practices. Furthermore, it can serve as a Western scientific lens to both learn from and interpret the disease management implications of traditional farming practices and acknowledge the indigenous knowledge underlying traditional farming systems. On the other hand, because it incorporates research and use of individual microbial varieties, and because it can use recombinant DNA methods in ecological studies, it also can draw on and overlap with perspectives from agricultural biotechnology.

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4. Greatly increased support for research is needed for the study of the relationship of agronomic practices to microbial community ecology and disease management, the basis of disease management through the use of individual antagonists, and the integration of agronomic practices that reinforce disease management in individual cropping systems. 5. Strengthening the economic sustainability of biological control approaches to plant disease management is critical. This can take the form of expansion of research on antagonist formulations for ease of use and efficacy, the relation and development of agronomic practices for plant disease management, and integrating, into modem agriculture, alternative criteria by which disease management strategies can be valued and which enhance the economic and cultural stability of farms and farming communities.

V. C O N C L U S I O N S

Although there are some critics of agriculture who value wilderness over all else, and believe that a hunter-gatherer lifestyle is the only way that human populations can achieve environmental sustainability, this chapter does not accept these views. It is the perspective of this chapter that agriculture is an activity basic to, and embedded in, human culture. Agroecology is taken as the best overall framework within which to develop disease management strategies for agriculture, and by which to assess sustainability in agriculture. It is a unique agricultural science because it is inclusive and sensitive toward human social and cultural systems, rather than treating agriculture as something separate from social systems. Agroecological research emphasizes agricultural sustainability through 'defining the principles upon which to base agroecosystem design, farmer evaluation and adoption of technologies, and validation of local practices that have emerged over centuries of agricultural activities' (Altieri and Hecht, 1990). In a broad sense, then, agroecology's strength is that it can accommodate both economic and ecological components of sustainability. Its customary focus is developing world agriculture, but it would be a wise approach to adopt for research in modern agricultural systems as well. 1. This chapter has presented three perspectives within which research on nonchemical disease management strategies exist and can be developed: traditional farming systems, biological control, and agricultural biotechnology. Valuable insight and methods for environmentally sustainable disease management strategies can be gained from all three. 2. A subtheme of this chapter has been to emphasize that no single research discipline can provide comprehensive disease management strategies. Forging an ecological framework for disease management will require a great expansion of interdisciplinary research in agriculture. Interdisciplinary collaborations are sorely needed to develop disease management strategies and

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3.

4.

5.

6.

7.

125

to understand their ecological basis, so they can be applied effectively and for maximum economic and environmental sustainability. They should probably be the norm rather than the exception for research in both modern and traditional agricultural systems. This is one of the most difficult and exciting challenges in research today. To develop non-chemical disease management, it is critical that diverse research be supported. Commercial products are clearly important, but farmers and other agriculturists must have a wide range of practices and management options at their disposal. They must also have access to all the information and knowledge that might benefit them, to enhance their ability to adopt approaches that are economic and increasingly environmentally sustainable. A diverse base for research and outreach must be supported, in industrialized and agrarian nations, which emphasizes interdisciplinary collaboration, and farmer research, as well as university and corporate-based research. In addition to the research base in universities and corporations, extension and outreach networks of universities, government agencies and non-governmental development organizations will be more, not less, important to the long-term accomplishment of these on-going processes. Farmers should be encouraged to carry out their own research, as many farmers already do, and to communicate their knowledge to others, thereby adding to the 'indigenous' knowledge base. Biological control stands at the center of the spectrum of the three perspectives described in this chapter. Focusing biological control research through a lens of applied ecology predisposes biological control approaches to environmental sustainability. The philosophical roots and the ecological basis of biological control make it the best perspective in Western science from which to build ecological approaches to disease management for sustainable modern agriculture. If agriculture is to evolve towards both economic and environmental sustainability, many of the criteria by which it is evaluated will be changed or reordered. Incorporating long-term land and crop management perspectives into modern agriculture is crucial to the development of alternatives to the narrowly short-term economic criteria by which disease management methods are currently evaluated. Many, possibly most, biocontrol strategies may be more suitable for long-term rather than short-term land and crop management by farmers. Thus, biological control approaches, while not easily adapted to customary notions of fungicide control, for example, are pre-adapted to fit into long-term sustainable agricultural systems. The redefinition of biological control described in this chapter focuses on indirect effects on disease by antagonist and agronomic practices. In so doing, it further emphasizes biological control as a pragmatic and holistic approach to disease management, particularly for modern agricultural contexts. Environmental sustainability is an indispensable criterion for agricultural

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practices, but risk analysis is insufficient as an indicator of environmental sustainability. 8. Economic sustainability of agricultural practices is an indispensable criterion for agricultural practices, and must be examined critically in relationship to social structures. 9. Research on microbial biological control and on traditional agricultural systems needs a dramatic increase in funding support. Biotechnological research relevant to disease management already has a strong corporate base, and is not threatened. However, broad-based ecological analysis should be incorporated into biotechnological research and development projects long before the risk assessment or field-testing stage. 10. 'The challenge for sustainable agricultural research will be to learn how to share innovations and insights between industrial and developing countries and to end the one-way transfer of technology from the industrial world to the Third World' (Altieri, 1987). It is essential that researchers and practitioners respect the differences in agriculture as practiced in different parts of the world. Science is a culturally embedded practice, which operates under particular assumptions which may not be shared in different cultures. Agriculture is also a cultural practice, but with great differences in kinds of knowledge, integration with communities and ecosystems, and types of social and economic priorities in different cultures. Neither Western science nor modern agriculture should be regarded as the arbiters of validity of agricultural knowledge. Western definitions of science are not needed to legitimize the importance of traditional practices. However, traditional practices do not necessarily provide exact models by which to achieve transformations of modern agriculture to sustainability.

ACKNOWLEDGMENTS

I thank J. Confrey for invaluable comments and suggestions on the organization and content of this chapter, P. Trutmann, H. D. Thurston and C. StockweU for critical reading of the manuscript, and E.B. Nelson for the suggestion to pursue the topic.

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Altieri, M. A. and Hecht, S. B. (1990). Preface to 'Agroecology and Small Farm Development'. CRC Press, Boca Raton, FL. Andrews, J. H. (1992). Biological control in the phyllosphere. Annual Review of Phytopathology 30, 603-635. Baker, K. F. (1987). Evolving concepts of biological control of plant pathogens. Annual Review of Phytopathology 25, 67-85. Becker, J. O. and Schwinn, F.J. (1993). Control of soil-borne pathogens with living bacteria and fungi: status and outlook. Pesticide Science 37, 355-363. Blaikie, P. and Brookfield, H. (1987). 'Land Degradation and Society', Metheun, London. Boehm, M.J., Madden, L.V. and Hoitink, H . A . J . (1993). Effect of organic matter decomposition level on bacterial species diversity and composition in relationship to Pythium damping-off severity. Applied and Environmental Microbiology 59, 4171-4179. Chambers, R. (1990). Farmer-first: a practical paradigm for the third agriculture. In 'Agroecology and Small Farm Development' (M. A. Altieri and S.B. Hecht, eds), pp. 237-244. CRC Press, Boca Raton, FL. Chambers, R., Pacey, A. and Thrupp, L. A., (eds) (1989). 'Farmer First: Farmer Innovation and Agricultural Research'. Intermediate Technology Publications, London. Cook, R.J. (1993). Making greater use of introduced microorganisms for biological control of plant pathogens. Annual Review of Phytopathology 31, 53-80. Cook, R.J. and Baker, K. F. (1983). 'The Nature and Practice of Biological Control of Plant Pathogens', American Phytopathological Society Press, St Paul, MN. Corey, S. A., Dall, J. D. and Milne, W. M. (1993). 'Pest Control and Sustainable Agriculture'. CSIRO, Melbourne. De Waard, M.A., Georgopoulos, S.G., Hollomon, D.W., Ishii, H., Leroux, P., Ragsdale, N. N. and Schwinn, F.J. (1993). Chemical control of plant diseases: Problems and prospects. Annual Review of Phytopathology 31,403-421. Fahey, J. W., Dimock, M. B., Tomasino, S. F., Taylor, J. M. and Carlson, P. S. (1991). Genetically Engineered Endophytes as Biocontrol Agents: A Case Study from Industry In 'Microbial Ecology of Leaves' (J. H. Andrews and S. S. Hirano, eds), pp. 401-411. Springer-Verlag, New York. Farrand, S. K., Wilson, M., Lindow, S. E. and Savka, M. A. (1994). Modulating colonization by plant-associated microbes. 'In Improving Plant Productivity with Rhizosphere Bacteria'. (M. H. Ryder, P. M. Stephens and G. D. Bowen, eds), pp. 233-236. CSIRO Press, Adelaide. Fitchen, J. H., and Beachy, R.N. (1993). Genetically engineered protection against viruses in transgenic plants. Annual Review of Microbiology 47, 739-763. Garcia-Espinosa, E. R. (1980) Incidencia de algunos fitopatogenos del suelo en maiz, con enfasts en Pyttilum sp. bajo dos tipos distinto de agroecosistemas en el tropico humedo. Agricultural Tropical (CSA T) 2, 98-104. Garcia-Espinosa, E. R., Quiroga-Madrigal, R. and Granados-Alvarez, N. (1994). Agroecosystems for sustained corn productivity in hot wet regions of Mexico. In 'Slash/ Mulch: How Farmers Use It and What Researchers Know about It' (H. D. Thurston, M. Smith, G. Abwi and S. Keart, eds), pp. 61-74. Cornell International Institute on Food Agriculture and Development, Cornell. George, S. (1990). 'Ill Fares the Land: Essays on Food, Hunger, and Power'. Penguin Books, London. Gilbert, G. S., Parke, J. L., Clayton, M. K. and Handelsrnan, J. (1993). Effects of an introduced bacterium on bacterial communities on roots. Ecology 74, 840-854. Handelsman, J., Raffel, S., Mester, E. H., Wunderlich, L. and Grau, C. R. (1990). Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Applied and Environmental Microbiology 56, 713-718.

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7 CLASSICAL BIOLOGICAL CONTROL OF PLANT PATHOGENS John K. Scott CSIRO Division of Entomology, Private Bag PO, Wembley WA 6014, Australia

I. Introduction A. Theory of Classical Biological Control B. Examples of Classical Biological Control II. Biological Control and Plant Pathogens III. Classical Biological Control and Plant Pathogens IV. Classical Biological Control Using the Example of Phytophthora cinnamomi A. Taxonomy B. Region of Origin C. Survey for Mycoparasites D. Host Specificity E. Effectiveness of Exotic Biological Control Agents F. Suitability of Release Areas V. Conclusions Acknowledgements References

131 132 133 133 135 136 136 137 137 138 138 140 141 142 142

I. I N T R O D U C T I O N Biological control as broadly understood is the use of organisms for the control of pest species. Historically, one of the first methods used was classical biological control. This involves the importation of natural enemies of a pest from the native range to the country of introduction, and subsequent release of these agents (Wapshere etal., 1989). This type of biological control remains the principal means adopted against weeds and insect pests (Wapshere et al., 1989; Debach and Rosen, 1991; Julien, 1992). The term 'biological control' covers many methods including increasing or augmenting the density of local natural enemies, competitively displacing the pest species from the site of infestation, manipulating the environment or other organisms to favour natural enemies and conferring resistance on the host plant. Biological control of plant pathogens has mostly been concerned with using methods other than the classical approach favoured for weeds and insects (Cook, 1990). Research into controlling plant pathogens by biological means has been directed to manipulation of the environment to ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rights of reproductionin anyform reserved

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encourage resident antagonists (--biological control agents) or the introduction of antagonists (Cook, 1990). In the latter case, the introduced antagonists already exist in the pest's environment. The purpose of this chapter is to bring a different perspective to the subject of biological control of plant pathogens. Using the example of a major pathogen, Phytophthora cinnamomi, I will approach the question of its control as if it were an introduced weed that was to be subjected to classical biological control. I will outline the theory of classical biological control, give examples of the wide range of types of organisms and habitats that have been involved in this method, and present a case for the classical biological control of

P. cinnamomi.

A. Theory of Classical Biological Control Biological control is a practical application of the science of population biology (Schroeder and Goeden, 1986). The dynamics of natural enemy populations are manipulated to reduce and stabilize those of the pest species. Classical biological control is based on three principles; the host specificity of natural enemies, the pre-adaptation of natural enemies to the new environments infested by the pest species, and the control of pest populations by natural enemies.

1. Host Specificity Some natural enemies have evolved host specificity where they will only feed on one host species or a group of closely related host species. Often there is evidence for co-evolution between the agent and the target in that related agents are found on related targets, suggesting an 'arms race' over a long co-evolutionary history. Demonstrating host specificity is an essential part of the risk assessment undertaken before introducing organisms into a new environment. Host specificity may give an agent selective advantage over polyphagous species. The hypotheses suggested to explain host specificity include reduced competition by having the ability to use a toxic host or enemy-free space (Jaenike, 1990). To maintain host specificity it is imperative that the agent has mechanisms for locating the host and often the life cycles of the target and host are closely intertwined. This close association is important in that it increases the likelihood of the agent being able to locate the host in the area of introduction and subsequently, to control the host' s density. The selection pressure to evolve traits enabling a response to a particular pest's density would be less for a polyphagous natural enemy that could seek out alternative hosts.

2. Pre-adaptation to the Region of Introduction Many physiological studies have shown that organisms have definable environmental limits for existence. There are also many other habitat constraints, for example soil type (Bruehl, 1987). It is possible to measure these constraints and to determine if a biological control agent is adapted to the proposed area of

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introduction. One of the commonest methods used in biological control is to select agents from areas that match closely the climate of the region infested by the pest. However, the suitability of the climate of the introduction area may not be immediately evident. In some cases an area of introduction without a climate matching the source region can prove to be more suited to a biological control agent than both the source region and areas that match it for climate (Scott, 1992).

3. Potentialfor Regulation of Pest Populations Classical biological control is not attempting to restore the 'natural balance' (Wapshere et al., 1989). This is impossible to achieve since the exotic pest has created a new situation in the region of introduction. At present it is not possible to predict the degree of reduction in a pest population caused by natural enemies introduced as biological control agents. In biological control of weeds all agents are host specific, just over two-thirds of agents that are released become established in their new environment, and about a third had an impact on the pest population (Julien etal., 1984; Waage and Greathead, 1988; Crawley, 1989). This impact becomes stabilized, hopefully at a point below the threshold importance of the pest. The effectiveness of a biological control agent in its region of origin does not necessarily transfer to the region of introduction. In the beststudied biological control system, that of the winter moth, Operothtera brumata, an insignificant parasitoid in the native range, the tachsinid fly Cyzenis albicans, proved to be an important control agent (Hassell, 1978). The reasons for this could not be predicted beforehand (soil conditions were important) and most biological control releases are based on an ad hoc assessment of the potential for population regulation. Despite the difficulties of prior identification of effective biological control agents, the practice of classical biological control has led to many successes.

B. Examples of Classical Biological Control A wide range of organisms has been subjected to classical biological control (Table II). The type of agents used ranges from insects to fungi and viruses. There appears to be no known limits to the habitats where classical biological control could operate. By definition, the region of origin of the pest is excluded.

II. BIOLOGICAL CONTROL AND PLANT PATHOGENS Baker and Cook (1982) defined the biological control of plant pathogens as 'the reduction of inoculum density or disease-producing activities of a pathogen or parasite in its active or dormant state, by one or more organisms, accomplished naturally or through manipulation of the environment, host or antagonist, or by mass introduction of one or more antagonists'. The biological control of plant

Table 1. Examples of classical biological control showing the diversity of taxa and habitat. Examples of target organisms

Examples of exotic control agents

Species Algae Pteridophyta Monocotyledonae Dicotyledonae

Species

Mollusca Myriapoda lnsecta

Various species Salvinia modesta Pistia stratiotes Opuntia stricta Hakea sericea Chondrila juncea Theba pisana Ommatoiulus moreleti Neodiprion sertifer

Pisces lnsecta lnsecta lnsecta lnsecta Fungus lnsecta lnsecta Virus

Arachnida Amphibia Mammalia

Oryctes rhinoceros Sirex noctilio Tetranychus urticae Bubus marinus Oryctolagus cuniculus

Baculovirus Nematoda Arachnida Various diseases Virus

Various fish species Cyrtobagous singularis Neohydronomus affinis Cactoblastis cactorum Carposina autologa Puccinia chondrillina Under investigation Under investigation European sawfly Polyhedrosis virus Rhabdionvirus oryctes Deladenus siridicola Ph ytoseiulus persimilis Under investigation Myxomatosis

Habitat

Reference

1992 1992 1992 1992 1992 1992

Aquatic habitats Water surface Water surface Range land Nature reserves Crops and pasture Crops and pasture Urban areas Canadian forests

Julien, Julien, Julien, Julien, Julien, Julien,

Pacific Islands Pine plantations Greenhouses Nature reserves Pasture and rangeland

Caltagirone, 1981 Taylor, 1981 Caltagirone, 1981

Bird, 1953

Fenner, 1983

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diseases has been reviewed extensively (Fravel, 1988; Nigam and Mukerji, 1988; Weller, 1988; Adams, 1990; Cook, 1990; Gabriel and Cook, 1990; Harman and Lumsden, 1990; Deacon, 1991; Sivan and Chet, 1992). Recently, three strategies have been identified: regulation of the pathogen population, exclusion of infection by use of beneficial micro-organisms and host plant resistance (Gabriel and Cook, 1990). Similar strategies exist against insects, although not usually called biological control, but not for weeds where host-plant resistance only applies against parasitic plants. Research on the biological control of soil borne pathogens has concentrated on crop rotations and stimulating resident antagonists (Cook, 1990). Adams (1990) remarks that mycoparasites have not been considered economical to use against plant pathogens because of the high dosages required. The use of introduced biological control organisms has been neglected because of the view that they would not establish or maintain populations any higher than that which occurred naturally (Cook, 1990). In the above context 'introduced' is equivalent to augmentative biological control as used against insects and weeds (Wapshere et al., 1989) where the introduced organisms already form part of the ecosystem and are not of exotic origin. In general, exotic agents have not been used in biological control against plant pathogens although there are some examples both as a result of deliberate or accidental introductions. III. CLASSICAL BIOLOGICAL CONTROL AND PLANT PATHOGENS The successful use of the mycoparasite Sporidesmium sclerotivorum against Sclerotinia and Sclerotium species (Adams and Ayers, 1982) is claimed to be an example of the classical biological control approach as used in entomology (Cook, 1990). This is not strictly true since the biological control agent was already known to be present in the region (Adams and Ayers, 1981) and was not a new introduction of an exotic species. There is, however, evidence from accidental introductions of mycoparasites of plant pathogens that classical biological control could be possible. The rust of poplars Melampsora larici-populina was accidentally introduced into Australia and caused premature defoliation in poplars. After 2-3 years the effect of the rust diminished. This was found to be due to a hyperparasite, Cladosporium tenuissimum, which presumably was also accidentally introduced (Sharma and Heather, 1978; Gibbs, 1986). The discovery of virus-mediated attenuation of fungal pathogenesis (Nuss, 1992) opens up a promising new area in biological control. This is best illustrated by the hypovirulence caused by double-stranded RNAs in the chestnut blight fungus Cryphonectria parasitica (Choi and Nuss, 1992) and Dutch elm disease, Ophiostoma ulmi (Rogers et al., 1987). The proposed introduction of viruses into the introduced Dutch elm disease population of New Zealand (C. M. Brasier, pers. comm.), if approved, will be the first example of classical biological control against a fungus.

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IV. CLASSICAL BIOLOGICAL CONTROL USING THE EXAMPLE OF PHYTOPHTHORA ClNNAMOMI The soilborne pathogenic fungus P. cinnamomi is probably the most destructive exotic organism present in the environment of south west Australia. It is the cause of the disease jarrah dieback, which has a major detrimental impact on the commercial use of jarrah forest (Eucalyptus marginata) and of pine plantations. The disease attacks plant species belonging to 40 different families. The fungus has spread to National Parks where it causes major changes to vegetation structure and is a threat to rare plant species (Malajczuk and Glenn, 1981; Dell and Malajczuk, 1989). It is also an important disease of container grown plants in nurseries (Hardy and Sivasithamparam, 1988) and is regarded as one of the most important plant pathogens of the world, especially for the avocado industry (Zentmyer, 1980). In south west Australia the disease was first reported in 1921 from the Darling Range near Perth. P. cinnamomi was first isolated from jarrah in 1964. Considerable research has been directed towards the control of P. cinnamomi with limited success (reviewed in Shearer and Tippett, 1989), although the spread of the disease has been lessened by a quarantine programme. Research in Western Australia and elsewhere is directed towards using phosphonic (phosphorous) acid as a fungicide (Pegg and De Boer, 1990), breeding resistance in the important timber species Eucalyptus marginata (Cahill et al., 1992) and examining the biotic causes of 'suppressive soils', soils where the fungus is present, but the disease absent (Malajczuk, 1983). Biological control by manipulation of the soil microflora has not been successful in south west Australia because of environmental conditions that cause a lack of suitable micro-organisms in soils that are nutrient poor and from which the litter is removed by regular fire management (Malajczuk, 1983). There has already been considerable research into using biological control agents against P. cinnamomi (Zentmyer, 1980; Malajczuk, 1983). However, this research has only taken place in areas where the pathogen is introduced. In classical biological control of insects and weeds it is usual to search for control agents in the region of origin of the pest species. It is assumed that at least some of the organisms attacking the pest species in its region of origin would have been associated with the pest sufficiently long to have evolved host specificity and effective mechanisms for locating the host. In the following sections, aspects usually used when assessing whether a weed could be a suitable target will be applied to P. cinnamomi with the objective of its control in south west Australia.

A. Taxonomy Correct taxonomic identifications are the foundation on which biological control studies are based. The target for biological control must be correctly identified to

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ensure that surveys for control agents in the region of origin are made of the same species (Rosen, 1986). The taxonomy of P. cinnamomi is well known (Zentmyer, 1980). Within P. cinnamomi the two mating types A1 and A2 are genetically isolated in Australia (Old etal., 1984). Isozyme work by Old et al. (1984) found low levels of variability within the A1 and A2 which suggests an extra-Australian origin for the fungus. The A2 form is widespread whereas the A1 is known from more restricted areas including Australia, Southeast Asia and the Cape Province of South Africa. Oudemans and Coffey (1991) report on a worldwide comparison of isozymes within P. cinnamomi, but their work does not indicate a source area for the fungus. Little variation was found within the A2 form which was distinct from the A1 form. The comparatively good understanding that exists for the taxonomy of P. cinnamomi ensures that surveys for biological control agents can examine the same fungus in both the regions where it is an introduced pest and in the regions of origin.

B. Region of Origin Zentmyer (1988) discusses the origin and distribution of the fungus. The Americas were excluded as were Western Australia and Victoria in southern Australia because of the historical incidence of large-scale vegetation changes due to the fungus. This leaves a large area of the world as the possible source, principally Southeast Asia and subSaharan Africa. The fungus was first described in 1922 as a new disease affecting cinnamon trees in Sumatra. This led to the assumption that the fungus is native to Southeast Asia. However, Von Broembsen and Kruger (1985) claim the fungus is indigenous to South Africa. Zentmyer (1988) concluded that the fungus has two possible origins, one in Southeast Asia, ranging from New Guinea through Indonesia, including Sumatra, Malaysia and Taiwan, the second in the southern Cape Province of South Africa.

C. Survey for Mycoparasites Many parasites of fungi are known (Darpoux, 1960; Bruehl, 1987; Sundheim and Tronsma, 1988) and 23 antagonists (mycoparasites, mycophages, antibiotic producers) are known to attack P. cinnamomi (Table II). A range of methods of attack, from antibiotics to oospore parasitism, are involved. There is only one report of organisms that feed on or destroy P. cinnamomi in its probable area of origin, Southeast Asia or south west South Africa. Maas and Kotze (1989) isolated bacteria (pseudomonads) and fungi (Penicillium spp., Trichoderma spp.) from different soils used to grow avocados in South Africa and found significantly more antagonistic organisms in pathogen-free soil. Methods are available for selecting amongst the antagonists that are undoubtedly present in the areas of origin (Merriman and Russell, 1990;

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Mulligan and Deacon, 1992). Surveys would also have to be made in Australia to establish whether or not the potential biological control agents are already present (and by implication proved to be ineffective).

D. Host Specificity A search of the literature indicates that none of the organisms listed in Table II is host specific to P. cinnamomi. This is to be expected since the source of the antagonists has always been in areas where the host is introduced, for example, Australia and USA. It is possible for a host-specific antagonist to migrate with the host fungus from a region of origin, but none has been detected so far. This would be exactly the pattern expected if a survey were made of the organisms attacking an introduced weed or insect, and it is only in the region of origin that host-specific organisms would be found. There have been few studies of host specificity among the mycoparasites, but the co-evolution of mycoviruses, bacteria, algae and fungi with fungi indicates that host specificity is widespread (Pirozynski and Hawksworth, 1988). Mycoparasites with limited host ranges are known (Pirozynski and Hawksworth, 1988). Some examples are Verticillium biguttatum which is used for the control of the soilborne pathogen, Rhizoctonia solani in potato (Van Den Boogert et al., 1990), and Olpidiopsis gracilis, which is a mycoparasite of a range of Phytophthora and Pythium species (Pemberton et al., 1990). The taxonomically isolated position of the Oomycetes with respect to other fungi (Brasier and Hansen, 1992) increases the likelihood of finding biological control agents that are host specific. Methods for determining host specificity of mycoparasites of P. cinnamorni would have to be developed, but could be based on the methods used in biological control of weeds. Testing starts with species closely related to the target, then tests are expanded to other related species before considering species of economic and environmental importance (Wapshere, 1974).

E. Effectiveness of Exotic Biological Control Agents Studies in South Africa give an indication that effective agents may exist. Phytophthora cinnamomi is a widely distributed pathogen in South Africa where it is a problem in nurseries, crops and plantations (Von Broembsen, 1984a,b). However, Von Broembsen and Kruger (1985) found that P. cinnamomi is widespread in native vegetation containing susceptible species in the south west Cape Province without the invasion and destruction that has accompanied the fungus in ecologically similar south west Australia. The non-invasive situation in south west Africa could be due to a number of explanations, soil type for example. Microbial activity is known to be an important cause of suppressive soils (Malajczuk, 1983) and this may be the case in the south west Cape Province.

Table 11. Organisms antagonistic t o P. cinnamomi. Mycorrhizal associations are excluded. Antagonistic organisms Bacteria and Actinomycetes Bacillus sp. Bacillus sp. Pseudomanas sp. Bacillus subtilis var. niger Streptomyces sp. Streptomyces sp. Streptomyces griseoloalbus Fungi Anguillospora pseudolongissima Catenaria anguillulae Epicoccum purpurascens Humicola fuscoatra Hyphochytrium catenoides Myrothecium roridum Oidiodendron maius Penicillium funiculosum Pythium nunn Trichoderma harzianum Trichoderma koningii Trichoderma viride Amoebas Arachnula impatiens Gephyramoeba sp. Unidentified leptomyxid

Reaction recorded

Specificity level

Antagonistic t o growth Antibiotic production Antagonistic t o growth Sporangium abortion Antagonistic t o growth Inhibited growth Antibiotic production Oospore parasite Oospore parasite Antibiotic production Oospore parasite Oospore parasite Antibiotic production Antagonism Antagonism Hyphal parasitism Hyphal lysis from antibiotic production Antibiotic production Hyphal lysis from antibiotic production Lysis of hyphae and chlamydospores Mycophagous Mycophagous

Oornycetes Non-specific Non-specific Oomy cetes Oomycetes Non-specific Nonspecific ? Non-specific Non-specific Non-specific

Where studied

Reference

Australia USA Australia Australia Australia Australia USA

Malajczuk et a/., 1977 Hutchins, 1980 Malajczuk etal., 1977 Broadbent and Baker, 1974 Malajczuk e t a/., 1977 Halsall, 1982 Rose etal., 1980

USA USA Europe USA USA USA Europe USA USA USA Australia Europe

Daft and Tsao, 1983 Daft and Tsao, 1984 Brown etal., 1987 Daft and Tsao, 1983 Daft and Tsao, 1983 Gees and Coffey, 1989 Schild etal., 1988 Fang and Tsao, 1989 Lifshitz et al., 1984 Kelley and Rodriguez-Kabana, 1976 Simon et a/., 1988 Reeves, 1975

Australia

Old and Oros, 1980

Australia Australia

Chakraborty etal., 1983 Chakraborty etal., 1983

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Table III. Climate matches between sites in Western Australia and the rest of the world. MI is the match index calculated in the match climates option in CLIMEX. MI ranges from 0 to 1, the latter being an identical climate pattern of rainfall and temperature. The three highest matching sites with MI over 0.70 are shown. ,

Sites in High matching sites in Southwest Australia eastern Australia Dwellingup Eneabba

None None

Esperance

Victor Harbour

Jarrahwood

Robe None

Port Lincoln

MI

High matching sites elsewhere

Jonkershoek (South Africa) Iraklion (Greece) Larache (Morocco) 0.83 Cape Town (South Africa) 0.83 Elsenburg (South Africa) 0.80 Wingfield (South Africa) Groot Drakenstein (South Africa) Heldervue (South Africa) Jonkershoek (South Africa)

MI 0.74 0.74 0.74 0.88 0.84 0.79 0.80 0.79 0.77

F. Suitability of R e l e a s e A r e a s

As a first step, exotic biological control agents are searched for in those regions of origin of the pest that closely resemble the pest-infested area. On a broad scale, the P. cinnamomi infested areas of south west Australia are jarrah forest on ironstone gravels with a sandy matrix and heathlands on low nutrient sands. The climate is Mediterranean. The places that could be searched for exotic biological control agents include Southeast Asia and South Africa. 1. Climate Four widely separated sites with comprehensive climate records and representative of P. cinnamomi-infested areas in south west Australia were selected for the comparison of climates (Table III). Eneabba and Esperance represent the climate of heathlands while DweUingup and Jarrahwood represent the climates ofjarrah forest. The climate of these sites within the P. cinnamomi-infested areas of south west Australia was compared with the world set of climate stations given in C L I M E X (4.2 version) (Sutherst and Maywald, 1985). The four sites from south west Australia resemble those of south west Cape Province more than other areas of the world, including eastern Australia (Table III). No sites in Southeast Asia are included among the sites with a high degree of climate match. 2. Vegetation and Soils Heathlands on low nutrient soils are found in south west Australia and south west Africa (Specht, 1979; Groves, 1983), but not in Southeast Asia apart from very small areas of lowland infertile sands and subalpine habitats (Specht and Womersley, 1979). Floristically, the heathlands of Australia are regarded as more similar to South Africa than other regions (Specht, 1979). Many plant families are shared between the two regions and only a few have penetrated into Indo-

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Malaya or elsewhere (Specht, 1979; Specht and Womersley, 1979). The jarrah forests do not have an analogous vegetation type in similar climates outside Australia (Dell and Havel, 1989). Fire plays an important role in the environment of both south west Australia and south west Africa (Gill and Groves, 1981). There appears to be little documentation of the role of fire in heathlands of Southeast Asia. Some of the soil types present in south west Australia are found in Southeast Asia and in south west Africa (FAO-Unesco, 1977, 1978, 1979); however, detailed comparisons of soil types between these areas are not available. The environment of south west Australia corresponds closely to that of south west Africa. This suggests that the south west Cape Province would be the most suitable region to search for biological control agents that are preadapted to south west Australian conditions.

V. CONCLUSIONS Classical biological control, as shown by successful programmes against weeds and insects, offers considerable advantages over other control methods. It is reasonably permanent, has no harmful side effects, attack is limited to a very small group of related species, agents are self perpetuating, often density dependent and self disseminating. Costs are non-recurrent and risks are known and evaluated before introduction (Wapshere et al., 1989). With these advantages it is surprising that classical approach to the biological control of plant pathogens has not been considered more often. P. cinnamorni conforms to the profile of an organism that could be targeted by classical biological control. It is exotic to south west Australia. It is known to be attacked by many organisms. However, the source areas have not been searched. A search should be made of the south west Cape Province to determine whether mycoparasites associated with P. cinnamomi have potential to be used as biological control agents. Such a project is technologically feasible given that considerable work has already been done on the biological control of P. cinnamorni. If a search in South Africa proved unsuccessful then a search for biological control agents in Southeast Asia should not be excluded. There might be other reasons for the different behaviour ofP. cinnamorni in native vegetation in south west Cape Province. A study of this area could lead to a better understanding of the management of P. cinnamorni in Australia. A successful project would lead not only to the protection of natural resources in Australia, but potentially to the development of methods of control for a worldwide problem. There is strong evidence for the importance of hyperparasites of soil fungi (Bruehl, 1987). Other important plant diseases that are exotic species could be considered as targets for classical biological control. An example would be late blight of potato, Phytophthora infestans, which originates from Mexico and is now an exotic introduction in many parts of the world (Zentmyer, 1988; Fry et al., 1992).

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Classical biological control is unlikely to be the only solution to a pest problem and certainly will not eradicate the pest. Modern weed and insect control is an integration of biological, cultural and chemical control. This is also likely to be the case with plant pathogens (Sivan and Chet, 1992), especially for P. cinnamomi which occurs over a wide diversity of habitats.

ACKNOWLEDGEMENTS I thank Drs C. M. Brasier, G. E. St. J. Hardy, N. Malajczuk, K. M. Old, J. Ridsdill-Smith, and I. T o m m e r u p for debate over the different types of biological control.

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Von Broembsen, S. L. (1984a). Occurrence of Phytophthora cinnamomi on indigenous and exotic hosts in South Africa, with special reference to the south-western Cape Province. Phytophylactica 16, 221-225. Von Broembsen, S. L. (1984b). Distribution of Phytophthora cinnamomi in rivers of the south-western Cape Province. Phytophylactica 16, 227-229. Von Broembsen, S. L. and Kruger, F.J. (1985). Phytophthora cinnamomi associated with mortality of native vegetation in South Africa. Plant Disease 69, 715-717. Waage, J. K. and Greathead, D.J. (1988). Biological control: challenges and opportunities. Philosophical Transactions of the Royal Society of London B 318, 111-128. Wapshere, A.J. (1974). A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology 77, 201-211. Wapshere, A.J., Delfosse, E.S. and Cullen, J. M. (1989). Recent developments in biological control of weeds. Crop Protection 8, 227-250. Weller, D. M. (1988). Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26, 379-407. Zentmyer, G.A. (1980). Phytophthora cinnamomi and the diseases it causes. American Phytopathological Society Monograph 10, 1-96. Zentmyer, G. A. (1988). Origin and distribution of four species of Phytophthora. Transactions of the British Mycological Society 91, 367-378.

8 ECONOMIC THRESHOLDS AND NEMATODE MANAGEMENT R. McSorley* and L . W . Duncan t * University of Florida, IFAS, Department of Entomology and Nematology, Gainesville, FL 32611, USA t University of Florida, IFAS, Citrus Research and Education Center, Lake Alfred, FL 33850 USA

I. Introduction II. Modeling Nematode-Host Interactions A. Nematode-Crop Damage Functions B. Models of Nematode Population Change C. Management Functions and Optimum Control D. Model Limitations E. Derivation and Use of the Economic Threshold III. Nematode Population Management A. Host-plant Resistance B. Crop Rotation C. Other Cultural Practices D. Biological Control E. Integrated Management IV. Perspectives References

147 148 149 150 150 152 154 155 155 157 158 159 161 161 162

I. I N T R O D U C T I O N Models to estimate economic threshold population levels of plant-parasitic nematodes are increasingly used to help manage these pests. Originally derived to aid in preplant decisions regarding nematode management, equations relating crop yield to nematode population density are now being used as components of more complex models to help investigate long-term behavior of cropping systems. As such, economic models are required for the development and implementation of integrated pest management (IPM) systems for nematode management (Barker and Noe, 1987; Dale etal., 1988; Kerry, 1990; Luc etal., 1990; Duncan, 1991; McSorley and Phillips, 1993). Indeed, as strategies to manage nematodes become more complex to reduce the reliance on pesticides (Alphey et al., 1988; Ferris and Greco, 1990; Sasser and Uzzell, 1991), the need to understand the relative economics of various permutations of cropping systems and control methods intensifies. ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rightsof reproductionin anyform reserved

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Increased research has also reinforced awareness that valid estimates of economic thresholds are difficult to attain. Methods to assess more accurately levels of nematodes in soil and plant material are needed (Ferris et al., 1990; Schomaker and Been, 1992). Similarly, the accuracy of economic predictions based on the measurement of plant-parasitic nematodes depends heavily on factors that influence the host-parasite interaction (McSorley, 1992). Variation in the characteristics of a given soil environment (e.g. soil texture, cultural practices, presence or absence of competing organisms) and those extraneous factors that will occur at an unknown frequency or intensity (e.g. rainfall, temperature, crop prices), compromise the value of current efforts to forecast nematode-induced crop loss. The ability to reflect the influence of these factors on economic thresholds is key to the development of nematology IPM systems. Our intent in this chapter is to review methods that have been developed to estimate nematode population thresholds and apply the information for nematode control. Interest in alternatives to nematicides for nematode control is high. Quantitative models of the effects on nematode populations of crop rotation, biological control, resistance and tolerance, cultural practices and other control measures have been developed to help foster research progress and to aid in their application in the field. Accordingly, some methods to manage nematodes are reviewed as are methods to predict their effects on nematode populations.

II. MODELING N E M A T O D E - H O S T INTERACTIONS Research to characterize effects of nematodes on farm profits has emphasized the development of mathematical functions describing (1) nematode-crop damage; (2) nematode population change; and (3) control efficacy. In the context of this chapter, we refer to these equations as nematode management functions. Information derived from management functions and knowledge of production and control costs and expected crop values are used to estimate the economic effects of nematodes and various management options on farm profits during one or more growing seasons. Most of the equations used to model nematode-crop relationships are of simple form. Many are referred to as critical-point models, because they relate one event (yield, or end-of-season population density) to another (often preplant population density) at a single point in time (Duncan and McSorley, 1987). Such equations have proven useful in nematology because few management methods can be used after a crop is planted, migration does not appreciably affect nematode population change during a growing season, and, within limits discussed below, population dynamics of many species tend to be somewhat stable in response to normal patterns of climatic variation. When management decisions pertain to a single cropping season, or to a predetermined sequence of management options, the economic threshold - that population density at which the cost of nematode management equals the value

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of the increased crop yield expected from management - may be of prime concern. An extension of the concept of economic threshold is the optimizing threshold (Ferris, 1978) - that population density (following management) at which the difference in the predicted value of a crop and the management cost to attain that density are maximized. For the case of a single cropping season, determination of an optimizing threshold usually requires more precision in the required control-cost vs. efficacy models and in the ability to characterize nematode density than is currently possible. Therefore, the examples presented here involve economic thresholds rather than optimizing thresholds. Nevertheless, long-term profits and agricultural sustainability are affected by the cumulative impact of nematodes and nematode management programs. The concept of optimization is fundamental to the use of discrete models to select the most profitable long-term management strategies from a variety of management options (Ferris, 1978; Noe etal., 1991).

A. Nematode-Crop Damage Functions Equations used to describe the effects of nematodes on crop yield frequently reflect intraspecific competition among nematodes. The damage attributable to individual nematodes often decreases with increasing density. Thus, while yield may be inversely related to preplant nematode density (Pi) in a linear manner (Rodriguez-Kabana and King, 1985; Todd, 1989), often logarithmic transformations are required to linearize the relationships (Oostenbrink, 1966; Kimpinski and McRae, 1988; McSorley and Dickson, 1989; Sasser and Uzzell, 1991). Linear models have also been used to describe effects of more than one nematode species on yield by adding together population densities weighted for pathogenicity (Hijink, 1964), or by considering them in a multiple regression model (Noling, 1987). Quadratic models have been well-fit to the yield-nematode relationship (Barker et al., 1981) as have inverse logistic (Noe et al., 1991), exponential decay (Timmer and Davis, 1982), and inverse linear functions (Elston etal., 1991). Seinhorst (1965) proposed the crop-loss model Y=m

+ (1 - m ) z t ' - v

for

P > T,

and

Y - 1.0

for

P< T

where P is the nematode density, Y is the yield at a density of P nematodes/yield in the absence of nematodes, m is the minimum yield observed at high nematode density, T is the highest value of P below which yield is unaffected (Fig. 1) and z - the proportion of undamaged root at P - 1.0 (a constant slightly less than 1.0). Both the model and its descriptive parameters have been used widely to characterize basic plant-nematode relationships (Duncan and Ferris, 1983b; Inserra et al., 1983; Ferris and Greco, 1990; Trudgill, 1991). The model was also extended to include effects of multiple species infections (Duncan and Ferris, 1983a; Jones and Kempton, 1978).

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Fig. 1. Comparison of shape of hypothetical damage functions for a tolerant cultivar (A) and an intolerant cultivar (B). With use of the more tolerant cultivar, the tolerance limit increases from Tb to Ta and relative yield is greater through most of the range of initial nematode densities (Pi). B. Models of Nematode Population Change

Quantitative models of nematode population change are most often expressed as critical point equations relating end of season population density (Pf) to preplant density (Seinhorst, 1966; Jones and Kempton, 1978; Ferris, 1985), although some multiple function simulation models have been developed (Ferris, 1976; McSorley and Ferris, 1979; Jaffee a al., 1992). As with most damage functions, density-dependent effects are an important component of all population growth models (Fig. 2). Population decline in the absence of hosts or due to nematode antagonists, or chemical nematicides, has also been modeled using density-dependent (Ferris, 1985; Jaffee et al., 1992) and density-independent (Kinloch, 1982; Schmitt aal., 1987; Noe aal., 1991) functions. Cost-control functions used to derive optimization thresholds have also been estimated from damage functions and equations relating crop yield and nematicide dose (Schmitt a al., 1987). C. Management Functions and Optimum Control

True profit maximization requires a long-range approach to all aspects of farming systems. By determining appropriate and varied criteria, management functions

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10000

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Fig. 2. Relationship between Pf and Pi (log scale) for Meloidogyne incognita on corn, calculated from Seinhorst's (1966) model Pf - aEPi[(a - 1)Pi + E] -1, with E - equilibrium density - 505 and a - maximum multiplication rate - 475. Model is compared to actual Pf data (McSorley and Gallaher, 1993a), and the bold line indicates the maintenance line where Pr - Pi (reproduced by the permission of the Society of Nematologists). can be used to investigate effects of nematode management on agricultural sustainability. Specific criteria can include effects of management on crop profitability (Duncan, 1983; Noe, 1988), movement and fate of nematicides in soil (Swartz et al., 1989), and the effects of various management practices on nontarget organisms, soil conservation, and fertility. Particularly as management options diversify, some form of system modeling is required to understand and compare the dynamics of nematode control for different management sequences. The potential use of nematode management functions to investigate long-term behavior of management systems was proposed early in the development of these models (Jones and Kempton, 1978). Computer algorithms employing various combinations of management functions in temporal sequence have been used to investigate long-term effects of nematodes and nematode management on yields of annual and perennial crops (Jones and Kempton, 1978; Duncan, 1983; Ferris etal., 1986; Kinloch, 1986; Noling and Ferris, 1987; Ferris and Greco, 1990; Noe etal., 1991). The associated crop prices and control costs have been used to estimate the relative values of large numbers of potential management sequence permutations, which have included crop rotation, use of resistant varieties, and use of chemical and biological control. The effects of variable control costs and fluctuating crop values on the relative value of different management options have been described.

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To date, no data have been published to validate the specific output of any of these models in the form of field comparisons of particular cropping and management sequences. Nevertheless, promising sequences of multiple pest control options have been published (Ferris and Greco, 1990; Noe et al., 1991) and should stimulate such research.

D. Model Limitations 1. Methods

Data for deriving damage functions for nematode management have been obtained in pot studies, in microplots, and in small field plots. All such methods have important advantages and serious limitations. Studies in pots are useful to determine basic host-nematode relationships, such as pathogenicity and host resistance (Seinhorst, 1966; Trudgill, 1991), but plant growth and nematode distribution in soil are necessarily artificial. Similar problems can occur in microplot studies in which nematode inoculum is introduced as part of the experiment. Such experiments permit good control of experimental variables, but for this reason may not produce results similar to those from field plots with more natural conditions (McSorley and Phillips, 1993). Techniques have been developed to establish small field plots with a wide range of naturally occurring nematode densities. Methods include the use of preliminary surveys to identify such plots (Duncan and Ferris, 1983a, b; Noe, 1988; McSorley and Dickson, 1989) as well as prior manipulation of nematode populations using nematicides (Sasser et al., 1975; Ferris, 1985), combinations of crop species with variable host efficacy (Oostenbrink, 1966; Ferris, 1985), and, to minimize environmental variability, combinations of variably resistant cultivars of the same crop species (Francl and Kenworthy, 1989). Although nematode distribution in soil and the nematode-host interaction in field plots are natural, other problems are well noted. Population densities in field plots are unknown and must be estimated. Ferris (1984a) has proposed methods to reduce effects of sample error on model derivation. Perhaps the most serious problem encountered in small field plots is the lack of experimental control. Variation of edaphic (Schmitt et al., 1987), chemical (Trudgill, 1987), and biotic factors (Duncan and Ferris, 1983b) between plots influences nematode densities and behavior as ,*'ell as plant growth and yield. Researchers must attempt to identify important covariate factors (Duncan and Ferris, 1983b; Noe and Imbriani, 1986) with the knowledge that measured relationships may still be confounded by unmeasured variables. Measurements of average nematode density in the field do not provide information about the spatial patterns of nematodes. Because the relationship between nematode density and yield is not linear, there is a tendency to overestimate crop loss using damage functions derived from small plots (Seinhorst, 1973; Perry, 1983; Noe and Barker, 1985). Better understanding of potential relationships

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between the population mean and population aggregation parameters for various systems may help resolve this problem (Ferris, 1984a; Noe and Barker, 1985).

2. Variability in Nematode Management Functions Environmental conditions affect the shape of all management functions, so that the accuracy of generalizations depends on the degree to which these conditions vary between years and sites. Tylenchulus semipenetrans population change is affected by changes in the mass density and probably the carbohydrate level in citrus roots, which can vary annually as well as seasonally (Duncan and Eissenstat, 1993; Duncan etal., 1993). Seasonal variation in reproduction and damage functions has also been reported (Barker etal., 1985; McSorley and Dickson, 1989). Soil texture is the most notable edaphic characteristic affecting the shape of the damage function (Schmitt and Barker, 1981; Trudgill, 1986). Other causes of variation in management functions include temperature (Nardacci and Barker, 1979), fertility level (Noe and Imbriani, 1986), plant cultivar (Fig. 1; Inserra etal., 1983), other pests (Duncan and Ferris, 1983a, b), and different isolates of the same nematode (Inserra et al., 1983; Noe, 1991).

3. Characterizing Population Density Estimates of nematode population density are required in most research to derive damage functions and are the basis for subsequent management decisions. However, population estimates for nematodes can be highly variable due to aggregated spatial patterns of nematodes in fields (Noe and Campbell, 1985; McSorley, 1987; $chomaker and Been, 1992). Sample confidence interval halflengths equal to 50-100% of the mean are routinely attained in research and advisory work (Davis, 1984; McSorley and Dickson, 1991). Progress is possible only because ranges of nematode densities between plots or fields are often very large. Thus, the use of population density classes in combination with damage functions has proven useful for advisory purposes (Barker and Noe, 1987). Although methods have been proposed to address the problem of variability in determination of damage functions (Ferris, 1984a), improved techniques for sampling and enumerating nematodes are required (Barker and Imbriani, 1984; Noe and Campbell, 1985; Francl, 1986; Belair and Boivin, 1988; Ferris etal., 1990; Duncan, 1991). An important aspect of estimating nematode density is that sample size is usually very small, due to the cost of processing samples of soil and root material. Subsamples are often processed from well-mixed composite samples of soil and/or roots obtained from numerous sites within a field or experimental plot. Thus, the number of processed samples is usually far fewer than the actual number of sampled sites within an area. Problems of estimating variance and estimating proper sample size for the case of small sample numbers have been noted (Schmitt etal., 1990; Duncan etal., 1994). Progress in sampling will likely result from a combination of improved understanding of sampling requirements (Shomaker and Been, 1992), mechanization of equipment to collect the requisite material

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(Ferris et al., 1990), and improvements in processing efficiency (McSorley, 1987) including new methods to quantify nematodes in samples (Schots et al., 1992).

E. Derivation and Use of the Economic Threshold Derivation of an economic threshold population density for a single cropping season is straightforward when the damage function is linear, but becomes more involved for non-linear damage functions when incomplete nematode control is expected (Ferris, 1978; Schmitt etal., 1987; McSorley and Phillips, 1993). When sufficient information is available, it will be possible to include stochastic elements in economic threshold estimates and other model-derived predictions (Ferris, 1984b; McSorley and Phillips, 1993). Variability in management functions is due to factors that are intrinsic (e.g. soil texture, crop variety) or extrinsic (e.g. precipitation, temperature) to the system. To a certain extent, it is possible to identify important intrinsic factors, develop models that are appropriate for different cases and thereby reduce model variability (Schmitt and Barker, 1981). Similarly, it may be useful to develop predictive models for broad classes of extrinsic factors (e.g. wet and dry years) and to use historic data to estimate probabilities associated with those conditions (McSorley, 1992). As system conditions are defined with increased precision, methods to reflect sample and experimental error in point estimates (e.g. predicted yield based on estimated Pi) have been proposed (Ferris, 1984b). Probabilities based on extrinsic factors can also be imposed on these estimates. A similar approach would be to combine the use of management functions with plant growth models (Trudgill, 1992). Algorithms to simulate multiple cropping seasons can incorporate stochastic elements by iteratively assigning probabilities to extrinsic events based on historical data (Ferris and Wilson, 1987). Thus, estimation of forecast reliability requires identification of key extrinsic and intrinsic factors and model derivation for those conditions. Knowledge of these key factors is critical to optimize forecasting accuracy with respect to research costs for model development. Some key factors are likely to be discernible from current management strategies. For example, temperature during and shortly after planting is likely to contribute to variability of management functions for systems in which early or late planting can be used for nematode management. In some cases, desired models may be robust enough to include variation in several factors (McSorley and Gallaher, 1993a). However, strong interactions between key factors will add to research requirements to derive appropriate management functions. Nevertheless, this approach is an excellent way to test continually our understanding of the nematode-host interaction, and providing confidence estimates for predictions from incomplete models will only enhance their value.

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III. NEMATODE POPULATION MANAGEMENT As nematicide usage as a management tool becomes more limited due to environmental concerns, regulation, or loss of efficacy because of biodegradation (Felsott, 1989), it will be essential to develop and rely on effective alternatives for managing economic nematode pests. The status and prospects of alternative methods for managing nematode infestations are reviewed. Nevertheless, the importance of exclusion or quarantine as a first line of defense against nematode infestation should not be overlooked. Exclusion has limited the spread or infestation level of nematodes in many situations (Maas, 1987). For instance, it has been known for many years that the spread of Radopholus similis to new banana plantations can be limited by paring, heat treatment, or chemotherapy of planting material (Blake, 1969). Tylenchulus semipenetrans, Pratylenchuscoffeae and Radopholus citrophilus are excluded from many citrus orchards in Florida by a mandatory nursery certification program, and, in the case of the latter species, by the use of physical barriers (Duncan etal., 1990). Maas (1987) has recently reviewed quarantine and certification practices, including physical methods for disinfestation of soil (particularly in greenhouse and propagation situations) and planting material. Once sites are infested with economic levels of plant-parasitic nematodes, then other management methods must be sought, such as nematicides or the alternatives of host-plant resistance, crop rotation, other cultural practices, and biological control.

A. Host-plant Resistance The use of resistant or tolerant cultivars provides a relatively inexpensive yet highly effective means of managing certain nematodes on a number of crops (Roberts, 1982; Cook and Evans, 1987). Resistant cultivars have been particularly useful against Globoderaspp. on potato (Cook and Evans, 1987), Heterodera avenae and other nematodes on cereal crops (Cook, 1974), Heteroderaglycines and Meloidogyne spp. on soybean (Fassuliotis, 1982, 1987; Cook and Evans, 1987; Dropkin, 1988), and Meloidogyne spp. on tomato (Roberts, 1982; Fassuliotis, 1987), cotton (Fassuliotis, 1982), and tobacco (Slana and Stavely, 1981). In addition to these examples, resistant cultivars are available and used for many other nematode-host combinations (Sasser and Kirby, 1979; Fassuliotis, 1982, 1987; Roberts, 1982; Cook and Evans, 1987). Most nematologists use the terms resistance and susceptibility to refer to the degree of nematode reproduction and the terms tolerance and intolerance to refer to the effect of the nematode population on the plant (Cook, 1974; Roberts, 1982; Cook and Evans, 1987; Trudgill, 1991). Often, resistance and tolerance are found in the same host, but many exceptions occur. For example, the potato cultivar Maris Piper, which is susceptible to Globodera paUida, is more tolerant of the nematode than is the resistant clone 12380 ac2 (Trudgill, 1991).

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The plant damage function (Fig. 1) is an expression of tolerance since it is expressed in terms of plant response. The shape of the damage function will shift as cultivar usage is changed (Fig. 1). The damage function, while an expression of tolerance, is often the result of resistance. A given initial nematode density (Pi) may be less effective on a resistant host than on a susceptible host since a much lower percentage of the initial population available may actually infect the host plant. Several different mechanisms of resistance may operate against plant-parasitic nematodes. Nematode infection may be reduced by root exudates from plants such as asparagus, marigold, or neem (Rohde, 1972; Alam etal., 1975; Veech, 1981; Huang, 1985), or enhanced by exudates which stimulate egg hatch (Shepherd and Clarke, 1971; Veech, 1981). Nematodes which have already entered plant tissue may be affected by hypersensitive reactions (Huang, 1985; TrudgiU, 1991), host nutrition (Huang, 1985; Melakeberhan and Ferris, 1988; Powers and McSorley, 1993), or production of chemical products which interfere with nematode-host recognition. (Veech, 1981, 1982; Huang, 1985; Kaplan and Davis, 1987). More resistance methods are effective and, therefore, resistance more often available against sedentary endoparasites than against migratory endoparasites or ectoparasites (Roberts, 1982). Many plant species are non-hosts which support no reproduction and, therefore, are immune to certain nematode species (Nusbaum and Barker, 1971; Rohde, 1972; Roberts, 1982). However, even plants that are highly resistant (but not immune) may support some reproduction (Cook and Evans, 1987), and with many ectoparasites, resistance may be limited to differences in population densities among cuhivars (Cook, 1974). Description of these intermediate levels of resistance can be difficult and imprecise, particularly since nematode reproduction depends on Pi (Seinhorst, 1966, 1970; McSorley and Gallaher, 1992). Population models that relate final nematode density (Pf) to Pi (Seinhorst, 1966) are useful in expressing the host-parasite relationship over a range of Pi (Fig. 2). Their use provides a quantitative description of host status (Seinhorst, 1970; Nusbaum and Barker, 1971), which may change from good at low densities to poor at very high Pi for the same nematode-host combination (McSorley and Gallaher, 1993b). Because resistant cuhivars may permit some nematode reproduction, their continual usage can select for populations or pathotypes that can overcome host resistance. Widespread planting of the potato cultivar Maris Piper, which is resistant to Globodera rostochiensis, resulted in increased incidence of G. paUida (Cook and Evans, 1987). Overuse of resistant cultivars has caused similar problems with Heterodera glycines on soybean (Dropkin, 1988), M. incognita on tobacco (Cook and Evans, 1987), and H. avenae on some cereal crops (Cook and Evans, 1987). Rotation of cultivars has helped limit the ability of H. glycines to overcome resistance in soybean (Young, 1984), and growth of partially resistant potato cultivars with polygenic resistance has been useful against mixed pathotypes of Globodera spp. (Forrest and Phillips, 1984). Environmental factors, particularly temperature,

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may also limit efficacy of host resistance (Cook and Evans, 1987; Dropkin, 1988). For example, the M i gene conferring resistance in tomato to M. incognita is inactivated by temperatures greater than 32~ (Dropkin, 1969; Araujo et al., 1982). Much additional research will be needed not only to understand further the complex genetics of nematode resistance (Sidhu and Webster, 1981; Fassuliotis, 1987; Triantaphyllou, 1987; Trudgill, 1991), but also simply to identify the many crop cultivars which have never even been screened for their response to plantparasitic nematodes.

B. Crop Rotation Because soil-dwelling plant-parasitic nematodes are relatively immobile compared to foliar plant pathogens or insects, crop rotation has long been an important method for managing them (Good, 1968; Nusbaum and Ferris, 1973; Johnson, 1982; Trivedi and Barker, 1986). A non-host, cotton, can be rotated with peanut for managing M. arenaria (Rodriguez-Kabana etal., 1987a), maize can be rotated with soybean for management of H. g~cines (Ross, 1962; Schmitt, 1991) or M. incognita (Kinloch, 1983), rotations with legumes or other non-hosts are used against H. avenae on cereal crops (Brown, 1987), alfalfa rotations are useful against H. schachtii on sugarbeet (Weischer and Steudel, 1972), and many other examples of successful rotations are available (Good, 1968; Johnson, 1982; Trivedi and Barker, 1986). In locations warm enough for winter crop production, low value cover or forage crops may affect the nematode population in subsequent cash crops (Brodie etal., 1970). Damage from M. incognita to soybean was more severe after a winter cover crop of clover than after rye (McSorley and GaUaher, 1991). A winter crop of snap bean was more heavily damaged by Meloidogyne spp. after a summer cover crop of sesbania (Sesbania macrocarpa) than after hairy indigo (Indigofera hirsuta) or sorghum (Rhoades, 1976). Unusual non-host or antagonistic crops have been introduced into rotations in some locations to reduce nematode densities (Reddy et al., 1986; Rodriguez-Kabana et al., 1989). In some cases, favorable effects from crop rotation can persist for several seasons (McSorley and Gallaher, 1993b), but in other instances rotation effects may diminish after a single season (Rodriguez-Kabana and Touchton, 1984). The planning of crop (including weeds or fallow) sequences that minimize nematode population densities has been termed the cropping systems approach to nematode management (Trivedi and Barker, 1986; Noe, 1988). The design of a successful cropping system depends on economics (Ferris and Noling, 1987). In the southeastern United States, rotation of peanut with maize or sorghum for management of M. arenaria is unattractive because of the low economic value of these crops (Rodriguez-Kabana et al., 1989), but some 3-year sequences of peanut and soybean were profitable (Rodriguez-Kabana et al., 1988). Noe et al. (1991) developed models to determine the profitability of 3-year sequences of cotton and soybean based on density of Hoplolaimus columbus, damage functions, and economic data.

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With the long rotations used against some cyst nematodes, it may be necessary to project nematode populations and yields over many years to assess profitability of proposed crop sequences (Jones and Kempton, 1978). In perennial crops, it is essential to evaluate economics of management practices over the life of the crop, since short-term calculations may show a loss during the first few years when the crop is being established (Ferris and Noling, 1987). Designs of many cropping systems are complicated by the occurrence of several species of plant-parasitic nematodes in the same field (Christie, 1959). These situations can often be simplified by focusing on the key nematode pest (McSorley and Gallaher, 1991).

C. Other Cultural Practices The efficacy of solar heating beneath clear plastic mulch for nematode management was first recognized in the 1930s (Hagan, 1933). Within the past 15 years, the technique of soil solarization for nematode management has received increased attention and improvement. Optimum results are achieved during seasons of intense solar radiation and high temperature, when soil is moistened to improve heat conduction, when thin clear plastic tarps are used, and when tarps are maintained in place for 4-8 weeks (Katan, 1981; Heald, 1987). Best results have been obtained in locations with hot, relatively cloudless conditions during solarization including Israel (Katan, 1981), California (Stapleton and DeVay, 1983), and Texas (Heald and Robinson, 1987). Results obtained under subtropical conditions involving frequent rainfall and cloud cover have also been encouraging (McSorley and Parrado, 1986), although solarization was not as effective as soil fumigation under such conditions (Overman and Jones, 1986). Some cultural practices are relatively neutral toward plant-parasitic nematodes, and so their inclusion in sustainable systems may be based on other factors. Minimum tillage systems are adopted for their beneficial effects in conserving soil moisture, organic matter, and nutrients (Stinner and Crossley, 1982; Altieri, 1987; House and Brust, 1989), but the effect of tillage practices on plant-parasitic nematodes has often been minimal or inconsistent (Minton, 1986; McSorley and Gallaher, 1993b). Intercropping or mixed cropping may be beneficial in maintaining habitat diversity and reducing damage from some insect herbivores (Vandermeer, 1990). Occasional benefits in nematode management have been observed in crops interplanted with marigold (Khan etal., 1971; Davide, 1979) or sesame (Tanda and Atwal, 1988), but in general nematodes reproduce well on roots of interplanted host crops (Hackney and Dickerson, 1975; Powers et al., 1994). Other methods of nematode management are applicable in certain situations. Planting dates can be optimized to take advantage of reduced nematode development during cool seasons, as with M. incognita on winter wheat in California (Roberts etal., 1981), H. avenae on wheat in southern Australia (Brown, 1987), or H. schachtii and Ditylenchus dipsaci on sugarbeet (Weischer and Steudel, 1972).

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Adjustment of planting dates can also be used to increase nematode mortality from high soil temperatures (Schmitt, 1991). Flooding can be effective where it is practical (Trivedi and Barker, 1986), such as for managing M. graminicola in rice (Bridge and Page, 1982; Bridge etal., 1990). Fallow is highly effective in reducing nematode densities (Christie, 1959; Johnson, 1982; Rhoades, 1983; Duncan, 1986; Sarah, 1989) but the adverse effects on beneficial plant symbionts, soil fertility, and potential for erosion may not be compatible with sustainable systems. Trap crops were used for management of H. schachtii on sugarbeet in the 1800s but were ineffective against M. incognita on pineapple in Hawaii in the 1940s (Godfrey and Hagan, 1934). Manipulation of soil moisture through irrigation practices affects damage ofD. dipsaci to alfalfa (Griffin, 1992). Toppling of banana plants damaged by Radopholus similis can be reduced by propping or guying (Sarah, 1989). Control of weeds and proper management of groundcover is important in fruit groves (Nyczepir, 1991), and management of weed hosts (Rhoades, 1983) and volunteer plants (den Ouden, 1967) is essential for annual crops, too, as is destruction of old crop residues (Christie, 1959; Trivedi and Barker, 1986). Burning of crop residues can be effective against above-ground parasites such as D. angustus on rice (Bridge et al., 1990).

D. Biological Control Antagonists of nematodes are widely distributed among soil fungi (Stifling, 1984, 1991; Gray, 1988), bacteria (Sayre and Starr, 1988), arthropods (Walter etal., 1988), other nematodes (Small, 1987), and a variety of other invertebrate organisms (Small, 1988). Much of the effort to develop biological control of nematodes can be considered in three categories: (1) elucidation of natural control; (2) augmentation of antagonists; and (3) manipulation of the soil environment to enhance antagonistic activity. Elucidating natural control includes the detection and identification of antagonists of nematodes as well as attempts to document naturally occurring levels of nematode control. A growing body of evidence has been produced in the past 15 years showing that stable agricultural systems - perennial crops (Stifling et al., 1979; Stifling, 1984), monocultures (Kerry et al., 1982), or long-term rotations of crops which are all hosts to a nematode species (Minton and Sayre, 1989) - can foster density-dependent regulation of nematodes by antagonistic organisms. In most cases cited above, the equilibrium attained between antagonists and nematodes results in nematode densities below or near plant tolerance thresholds. Indeed, the lack of damage by nematodes under nominally conducive conditions has been used as a potential indicator of biological control (Stifling et al., 1979). Since a vast assay of potential nematode antagonists typically occur in most soils (Gray, 1987; Rodriguez-Kabana and Morgan-Jones, 1988), it is likely that natural control may often result from a combination of organisms rather than from a single antagonist.

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Exploitation of natural control will remain largely fortuitous until the conditions which sustain such systems are better understood (Stifling, 1991). Features common to most of the organisms shown to be capable of effective natural control are a high degree of specialization as parasites of nematodes and the existence of a survival stage for periods when nematode density is reduced. Although the longterm economics of natural control compared to other forms of nematode control may be favorable in some systems, a sustained period of crop loss due to nematodes can be anticipated before an equilibrium is established between the antagonist and nematode populations. Methods to minimize economic loss without reducing nematode populations (e.g. use of less-profitable but nematode-tolerant crops) during the establishment phase of such systems may be an interesting area for research. Effective biological control of nematodes has been achieved in pots and microplots augmented with a large variety of organisms antagonistic to nematodes (Stifling, 1991). However, with few exceptions (Cayrol etal., 1978; Cayrol, 1983), augmentation of biocontrol organisms has had very limited success at the commercial level. It is difficult to elucidate environmental requirements for survival (Kerry aal., 1980; McInnes and Jaffee, 1989), or the induction of nematophagy in facultative parasites (Gray, 1988), or factors involved in fungistasis (Jaffee and Zehr, 1985). It is even less feasible to create or to overcome such conditions, given the complexity and variety of soil environments (Kerry, 1990). Many of the most successful antagonists are fastidious and difficult to culture in large quantities (Stifling and Wachtel, 1980; Reise etal., 1988). Nevertheless, with accumulating experience, promising approaches to overcome some of these difficulties have become more apparent (Morgan-Jones and Rodriguez-Kabana, 1987; Gray, 1987; Kerry, 1990; Stifling, 1991) and considerable resources are currently devoted to research in this area. Attempts to manipulate the soil environment to enhance biological control have emphasized the use of organic amendments (Muller and Gooch, 1982) which can reduce populations of plant parasitic nematodes by a variety of mechanisms including release or production of toxic products (Prot and Kornprobst, 1983; Rodriguez-Kabana, 1986), increased community diversity with concomitant increase in antibiotics and allelochemicals (Spiegel a al., 1987), and possibly stimulation of predation and parasitism (Stirling, 1991). Current emphasis is on amendments containing substrates which are components of nematodes (such as chitin and collagen) and vulnerable to attack by enzymes released during substrate decomposition (Rodriguez-Kabana a al., 1987b; Galper et al., 1991). At least one soil-amendment for nematode control is commercially available (Spiegel et al., 1989). Integration of biological control in programs to manage nematodes can benefit from epidemiological studies that define the effects of epizootics on nematode population dynamics and the requirements for maintenance and activity of antagonist populations (Jaffee et al., 1992). Model development is constrained by difficulty in measuring and interpreting the population density and the propagule

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activity potential for many antagonists of nematodes (Kerry, 1990), although progress is being made (Stirling etal., 1979; Kerry etal., 1982; Mclnnis and Jaffee, 1989). Similarly, estimating the role of antagonists in nematode mortality can require complex methods (Kerry, 1980; Jaffee etal., 1988). As techniques are developed to measure important parameters of the interactions between nematodes and biological control agents, models to help predict optimum conditions to achieve economic control can be developed (Perry, 1978; Jaffee et al., 1992). The derivation of nematode management functions will be particularly important to validate systems involving biological control where anticipated nematode mortality may be low-to-moderate.

E. Integrated Management Some of the principles of integrated pest management (Andow and Rosset, 1990), which have been widely applied in the reactive chemical management of aboveground insect pests, are not particularly applicable in below-ground systems in which management decisions must often be made before the crop is planted. Nevertheless, integrated practices are increasing in importance in nematology, since they combine the advantages of several of the methods described above. Management of cyst nematodes on potatoes in the UK involves rotation, nematicides and use ofcultivars with various degrees of resistance (Jones and Kempton, 1978; Trudgill, 1986). Tylenchulus semipenetrans on citrus is managed by exclusion, resistant rootstocks, fumigation of planting sites, post-planting nematicide application, and maintenance of plant health (Duncan and Cohn, 1990). Management ofH. avenae on wheat in Australia includes use of crop rotation, optimum planting date, resistant or tolerant cultivars, favorable tillage practices and nematicide application, if sampling indicates populations are above the threshold (Brown, 1987). The management of R. similis on bananas can involve a combination of exclusion and plant inspection, treatment of planting sites by nematicides or fallow, preparation of nematode-free planting material, nematicide application after planting, and propping or guying of damaged plants (Sarah, 1989). When plants are seriously infected with plant-parasitic nematodes, integrating improved soil fertility (Good, 1968), use of mulches (Watson, 1945), and increased irrigation may be of some benefit in prolonging productivity. As the characteristics of sustainable agricultural systems become better understood, it will be necessary to recognize which nematode management practices are compatible for integration into specific systems.

IV. PERSPECTIVES Most scientists and producers recognize that maximizing profits and returns may not be the same as maximizing yields (Ferris, 1978; Ferris and Noling, 1987).

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Although cost and benefits are often calculated in terms of monetary values of inputs and yields, the long-term conservation of fertility, water, soils, and the agroecosystem itself must also be considered. Soil fumigation practices used extensively in the past (Lembright, 1990) were highly effective in increasing yields, but were very expensive and disruptive of entire soil ecosystems. Although much research was needed to perfect the application technology of soil fumigation (Lembright, 1990), relatively little knowledge of the biology of the soil system was needed to perform broad-spectrum soil fumigation. In contrast, many of the alternative methods described in this chapter (e. g. resistant cultivars, biological control, crop rotation) are highly specific, and their successful use requires considerable knowledge of the biology and ecology of specific nematodes on specific host cultivars. Not only is there a need for thresholds and damage functions for key nematode pests of many crops, but also for basic research knowledge to improve methods of nematode detection, sampling, recovery, and to identify more easily species, pathotypes, and populations (McSorley, 1987; Dropkin, 1988; Duncan, 1991). The collection of this information will depend on an increased number of agricultural scientists trained in nematology, plant pathology, agronomy, ecology, and related disciplines. The evidence presented in this chapter suggests that, although constant vigilance and attention are required, effective nematode management practices can be integrated into most sustainable systems. A major concern is that a level and system of production considered sustainable at one point in time cannot remain so for very long if demand is escalating from a rapidly growing h u m a n population (Paddock, 1992).

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9 EVALUATION OF MICRO-ORGANISMS FOR BIOCONTROL: BO TRYTIS ClNEREA AND STRAWBERRY, A CASE STUDY

j.c.

Sutton

Department of Environmental Biology, University of Guelph, Guelph, Ontario, Canada, N1G 2W1

I. II. III. IV.

Introduction Socioeconomic Goals and Obligations in Biocontrol Research Objectives Background Perspectives A. Strawberry Cropping Systems B. Pathogen Ecology and Gray Mold Epidemiology C. Disease Management Strategies D. Conventional Disease Management E. Selection of Biocontrol Organisms - the Challenge V. Biocontrol Research A. Selection of Organisms B. Biocontrol Tests C. Vectoring of Biocontrol Organisms by Bees D. Biocontrol Mechanisms of Gliocladium roseum VI. Conclusions and Future Directions Acknowledgments References

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I. I N T R O D U C T I O N Communities of indigenous organisms in cropping systems are vast and relatively unexploited reservoirs of antagonistic organisms that can suppress plant pathogens in developing crops, in crop residues and in the crop environment (Cook and Baker, 1983; Cook, 1993; Sutton and Peng, 1993). The antagonists usually are fungi, prokaryotes and microfauna, but larger arthropods and other organisms can also be important. Crop rotation, tillage methods, application of organic amendments and other cultural practices frequently capitalize on indigenous organisms to suppress pathogens. Indigenous organisms also can be isolated, evaluated for antagonism of pathogens, and introduced into crops as biocontrol agents. Experimental introduction of antagonists to suppress pathogens of ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

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foliage, flowers and fruits has had an erratic and sometimes disappointing history in which microbes that were promising under controlled conditions often performed poorly in the crop. However, several recent successes in biocontrol in crops have kindled a fresh enthusiasm and optimism among investigators such that introduced antagonists are now often seen as powerful tools to manage diseases that presently go uncontrolled and as good alternatives to chemical pesticides (Cook, 1993; Sutton and Peng, 1993). Prominent among recent successes in biocontrol are systems developed against Botrytis cinerea in strawberry, raspberry, grape, orchard fruits, spruce seedlings and other crops (Sutton and Peng, 1993). The present article focuses on microbial biocontrol of B. cinerea in strawberry, in which the pathogen causes gray mold fruit rot, a destructive disease of worldwide importance. Consideration is given to background perspectives, concepts, methods, strategies, pitfalls, progress and future directions in this biocontrol system.

II. SOCIOECONOMIC GOALS AND OBLIGATIONS IN BIOCONTROL The most important goal in biocontrol research is to develop methods and strategies that are effective in the cropping system. The literature is crammed with reports of biocontrol conducted solely under artificial conditions and of questionable relevance to crop conditions. Controlled studies can be meaningful and useful, however, when they complement or otherwise relate to research done in the crop. Demonstrations of effective biocontrol of pathogens in crops almost always invokes enthusiastic acclaim by growers and the public at large, and generally bodes well for continued support and advancement of biocontrol. For commercial application, biocontrol must be efficient, dependable, cost effective, and safe for humans, the crop and the environment (Scher and Castagno, 1986). Like other disease-management methods, biocontrol ideally aims to suppress disease sufficiently so that avoidable yield losses are minimized and crop quality is maintained at an acceptable level (Zadoks and Schein, 1979). Performance testing of biocontrol agents under representative cropping conditions, perhaps using a standard fungicide treatment as a yardstick, will be critical to assure efficiency and dependability of new biocontrol agents, and to convince growers that the new-fangled methods are worth adopting. In many instances, biocontrol may have to be integrated with other measures to achieve satisfactory disease management. Cost effectiveness of biocontrol is a function of production and marketing costs of the agents, methods and strategies of application, and treatment effectiveness. Investigators would do well to ponder these points when developing biocontrol. For example, there would be little point in extensively evaluating a biocontrol agent that would be overly expensive to produce and maintain, or to apply to a crop on a commercial scale. Biocontrol researchers usually are in the difficult situation of not knowing what regulations (if any) will be in place when the time comes to apply for registration

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of an organism as a biocontrol agent. Unfortunately, regulations developed to date are guided chiefly by principles pertaining to chemical pesticides instead of appropriate biological information. Cook (1992, 1993) proposed an imaginative framework to improve and expedite registration and oversight of biocontrol agents without compromising health and safety issues. Clearly it makes sense for investigators to screen out organisms that could represent a significant risk to humans, the environment, or the crop itself. Fortunately, health risks associated with organisms that do not grow above 35 ~ are chiefly allergies or toxicoses from microbial metabolites, and should normally be preventable through simple precautionary measures. Indigenous organisms, by their nature, should not threaten the environment when used judiciously. Preoccupied with selecting and evaluating antagonistic organism, many investigators resist the effort involved in applying for registration, developing formulations and scaled-up production, and organizing the marketing ofbiocontrol agents. Yet, as Cook (1993) pointed out, companies should not necessarily be expected to undertake ventures with biocontrol agents, most of which represent 'small potatoes' economically. Collective effort of researchers with growers' organizations, university alumni associations, or other groups, could ensure that biocontrol agents are put to use for the benefit of all.

III. RESEARCH OBJECTIVES The foregoing considerations were guiding principles in our attempts to develop biocontrol ofB. cinerea in strawberry. The primary objective was to develop a flexible biocontrol system that was at least as effective as conventional fungicides in suppressing B. cinerea and fruit rot under a broad range of microclimatic and cropping conditions in the field. The system would incorporate methods and strategies for applying biocontrol agents to optimize efficiency and minimize any ecological disturbance of microbial populations that might be counterproductive to strawberry health management. Attempts to integrate biocontrol with other disease management methods, and to register and commercialize the biocontrol agent(s) would await the outcome of the initial work. Earlier reports had indicated that microbial suppression of B. cinerea in strawberry appeared feasible (Bhatt and Vaughan, 1962, 1963; Tronsmo and Dennis, 1977).

IV. BACKGROUND PERSPECTIVES A. Strawberry Cropping Systems The cropping system is fundamental to an understanding of disease epidemics and to development of rational methods and strategies for disease management. Strawberry production systems were summarized recently by Galletta and

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Bringhurst (1990). A majority of strawberries in Ontario are June-bearing cuhivars that are grown as perennials in matted rows for up to 5-7 years, and a few are everbearers. Plantings are protected with straw mulch from December until April, when regrowth begins. June bearers flower and fruit from early May to July, and everbearers from late June until October. Renovation of June-bearer plantings is done after harvest and can include mowing of the foliage, tilling between the rows, plant thinning, and application of fertilizer and herbicide.

B. Pathogen Ecology and Gray Mold Epidemiology Studies on the biology, ecology and population dynamics of B. cinerea and on the epidemiology of gray mold in strawberry plantings provided important information for rational development of biocontrol. An insidious pathogen, B. cinerea in most instances symptomlessly infects the leaves, crowns, flowers and fruits of strawberry, and progressively colonizes the tissues only when they senesce, ripen, or die (Powelson, 1960; Jarvis, 1962a, b; Jarvis and Borecka, 1968; Bristow et al., 1986; Braun and Sutton, 1988; Simpson, 1989, 1991; Sutton, 1990). The leaves are infected chiefly when they expand, but the pathogen remains quiescent in the epidermis until the tissues senesce and die, when the fungus can progressively colonize the tissues (Braun and Sutton, 1988; Sutton, 1990). Mycelium in dead strawberry leaves is the chief source of inoculum (conidia) in gray mold epidemics in Ontario (Braun and Sutton, 1987; Sutton, 1990, 1991). Apothecia of the teleomorph, Bot~yotiniafuckeliana, were not found in systematic searches of Ontario strawberry fields (Sutton, 1990). Dispersed conidia can infect various parts of the flowers. Senescent sepals, petals, stamens, pistils and peduncles are important sources of mycelium of B. cinerea capable of invading contiguous receptacles and initiating fruit rot. While flower parts, especially stamens, are important pathways of fruit infection, direct infection of fruit by germ tubes may occur in some instances. Affected fruit develop a characteristic light brown rot, chiefly from the calyx end, as they ripen in the field or after harvest, and may become covered with grayish hyphae and conidiophores of the pathogen. Infection cycles of B. cinerea on the leaves occur year-round and in concert with leaf flushes. In June-bearers, leaves produced in flushes that peak in July (after renovation), September, and April-May, die in September-April, May, and June, respectively (Braun and Sutton 1986, 1988). Because B. cinerea does not produce lesions or accelerate senescence of the leaves, leaf life span is a critical factor that determines the duration of infection cycles and limits the rate of inoculum increase. Thus latent periods (infection to sporulation) are 7-8 months in leaves infected in Septe]nber, but only 6-8 weeks in leaves infected in April. Infection cycles may be abJx~ptly completed when the leaves are kiUed by frost, pesticides, or other agents.

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C. Disease Management Strategies From the ecological and epidemiological information, suppression of conidial production by B. cinerea in the dead leaves and protection of the flowers against infection by conidia are rational strategies for fruit rot control. The first oPthese might be achieved by protecting the green leaves against infection, by eradicating B. cinerea when it is quiescent in the epidermis, by suppressing colonization of dying leaves by the pathogen, or by destroying or inhibiting the fungus after it has colonized the tissues. In the second strategy, suppression of pre- and postinfection events on various flower organs can be visualized.

D. Conventional Disease Management Development of resistance to gray mold combined with other desired characteristics in strawberry has met with only moderate success, and the disease continues to be a serious threat in a majority of cultivars (Maas, 1978, 1984; Barritt, 1980; Simpson, 1991). In Ontario, careful site selection, weed control, irrigation scheduling, fertilization, foliage removal at renovation, and fruit handling and storage are recommended to suppress gray mold (Sutton etal., 1988; Sutton, 1990). The mainstay control, however, is fungicide sprays applied at intervals during flowering and fruiting, but this is threatened by pathogen resistance and public opposition. Chlorothalonil targeted at the pathogen in the foliage before flowering effectively controlled fruit rot without leaving residues in the fruit but has not been registered for this purpose in Canada (Sutton, 1990). Vulnerability of strawberry crops to gray mold in Ontario and elsewhere is unfortunately increasing with the decline in availability of effective fungicides. Can microbial biocontrol reverse this trend plus alleviate concerns with chemical residues?

E. Selection of Biocontrol Organisms - the Challenge Selection of antagonists to suppress effectively a pathogen in a cropping system is a formidable challenge given the staggering numbers of microbial isolates that could be evaluated. Which microbial species justify or do not justify evaluation? To what extent should intraspecific variation in biocontrol effectiveness be explored? Should genetically altered organisms be considered? How can the field of potential contestants be narrowed to manageable numbers without compromising the detection of exceptional antagonists? By what methods should candidate organisms be evaluated in order to provide a realistic estimate of their performance against a pathogen in a crop? Investigators of chemicals as potential fungicides or of host gene pools for disease resistance have long faced problems that parallel those in biocontrol and much could be learned from their experiences (Cook, 1992). In sharp contrast to the sparingly few microbes normally lined up in biocontrol tests, chemicals and genotypes are typically evaluated by the

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thousand. Logistical problems may not allow such numbers in biocontrol, but there may be rational means to narrow the field of organisms tested.

V. BIOCONTROL RESEARCH A. Selection of Organisms We subscribed to the views that ecological adaptation of the microbe to the crop plant would be advantageous, even prerequisite, for effective and sustained biocontrol in the cropping system, and that micro-organisms from strawberry would include the best-adapted forms. Strawberry plants in effect function as selective substrates and substrata in competitive colonization by indigenous organisms (Cooke and Rayner, 1984), and we can take advantage of this in narrowing the field of organisms for tests against B. cinerea. Ecological observations of the strawberry microflora was a further basis for selecting test organisms. As an initial step, the mycoflora of living, senescing, and dead leaves, flowers, and fruits of strawberries in plantings that were not treated with fungicides was quantified year round (McLean, 1988; McLean and Sutton, 1992). Washed and unwashed tissues were incubated in high humidity and on agar media in preparation for fungal identification or recovery. Total genera and species identified in leaves, calyces, petals, and fruits were 24, 15, 12, and 10, respectively, and thus notably low. Alternaria alternata, B. cinerea, Gloeosporium spp., Gnomonia comari, Penicillium spp., Trichothecium roseum and Verticillium spp. were frequent in all tissues studied. Golletotrichum dematium, Coniellafragariae, Epicoccum purpurascens and Gliodadium roseum were frequent only in the leaves, Cladosporium spp. were frequent in leaves, calyces and petals, but not in the fruits, and Rhizopus stolonifer was common only in the fruits. Other mycelial fungi and pink yeasts were infrequent, but white yeasts were abundant in all tissues examined. From their frequent occurrence or high densities in the tissues, E. purpurascens, G. roseum, T. roseum, Cladosporium spp. and several yeasts appeared well adapted and competitive as non-pathogens in strawberry. Weak pathogens also were retained for biocontrol tests because of potential antagonism of virulent forms through induced resistance or other mechanisms (Ku6, 1987). About 400 isolates of micro-organisms from living and dead foliage, flowers and fruit of strawberry plants in the field and in the wild formed the basis of our biocontrol screening program. When feasible, several isolates of the same species or genus were included. Isolates of mycelial fungi, yeasts, and bacteria were used.

B. Biocontrol Tests 1. General Considerations Effectiveness of micro-organisms in controlling foliage, flower and fruit diseases can be evaluated with confidence only in the cropping system or under conditions

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Plant population

" Environment (microclimate, soil, organisms) Cultural practices other human \ interference . Biocontrol agent I" population _..

Pathogen population

Fig. 1. Schematic illustration of interactions among plants, pathogens, biocontrol agents, environmental variables, and human interferences in biocontrol systems in crops (adapted from Burpee, 1990).

closely representative of the cropping system (Sutton and Peng, 1993). The rationale of this precept is clear. Disease epidemics involve spatiotemporal interactions between host and pathogen populations under the influence of the environment and human interferences (Kranz, 1974; Zadoks and Schein, 1979). Micro-organisms introduced into a crop to control a disease must be able to interact appropriately with the pathogen, the host, and other organisms under the prevailing microclimatic conditions in order to be effective (Fig. 1). The biocontrol system is highly dynamic and can involve growth and development of the host, infection cycles and serial dispersals of the pathogen, quantitative shifts in populations of the biocontrol agent and indigenous organisms, and microclimatic fluctuations. In general, epidemics cannot be satisfactorily simulated in the laboratory, growth room, and greenhouse, and biocontrol tests done in these conditions should be interpreted accordingly. Biocontrol tests under controlled conditions can serve effectively for use in preliminary screening of organisms and for complementing work done in the crop. A key objective in the design of biocontrol tests done in plots or in controlled environments is to minimize representational errors (Vanderplank, 1963; James, 1974; Zadoks and Schein, 1979; Aust and Kranz, 1988; Sutton, 1988) relative to the well-managed crop. Procedures in field plots for biocontrol tests should follow good crop recommendations and are generally similar to those used for plots to test chemical pesticides and other disease-control measures. Possible interplot interference by dispersal of test organisms among plots is a special consideration

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in the spacing of plots for biocontrol tests. In this respect, sprinkler irrigation may best be avoided in favor of trickle or furrow methods. In many field studies it is necessary to introduce the pathogen to assure adequate density and distribution of inoculum in plots. However, the common practice of applying a high population of pathogen propagules at about the same time as when the biocontrol agent is introduced is, in most instances, unrepresentative of natural dispersal patterns and densities of pathogens in the field, and may overwhelm biocontrol effectiveness of many organisms. A more realistic alternative is to provide a source of initial inoculum in plots early in the cropping season and allow infection cycles of the pathogen and disease increase to occur naturally. Even in controlled tests, measures such as plant growth conditions (light, fertilizer, etc.) and pathogen treatments can be taken to simulate those of the cropping system and to minimize cryptic errors. For logistical reasons, only a few organisms normally can receive intensive evaluation under representative crop conditions in the field. These tests usually are intensive and demand numerous measurements of biocontrol agents, pathogen populations, disease, plant growth, and microclimatic variables. Each organism may require a series of evaluations to answer critical questions pertaining to concentration, timing and targeting of inoculum applications. Organisms can be effectively evaluated in large numbers, however, using whole plants, attached plant organs, or detached tissues in the field, greenhouse, growth room, or lal~oratory, and selected observations of these tests compared with those in field plots. In vitro methods are unrealistic for screening and results usually do not correlate well with those obtained in the field (Andrews, 1985). 2. Screening Organisms The microbial isolates from strawberry were evaluated against B. cinerea in a sequence of tests on strawberry plants in the laboratory, growth room, greenhouse, and field plots (Peng and Sutton, 1991). It can be argued that the respective environments increasingly mimicked those of commercial strawberry crops microclimatically and microbiologically. Consistent with disease-management strategies, tests were done against B. cinerea in leaves, and to protect flowers and fruits against the pathogen. Initial screening was done using a leaf disc assay. Discs from 10-day-old leaves of greenhouse-grown plants were washed to remove incidental organisms, placed in humidity chambers, and inoculated with propagule suspensions first of the test organisms (107 ml -~) and 24 h later with B. cinerea (106 conidia ml-l). After a further 24 h to allow infection by the pathogen, the discs were transferred to an agar medium containing paraquat to kill the tissues and allow rapid production of conidiophores of the pathogen which were quantified as an indication of biocontrol effectiveness of the test organism. Biocontrol ranged from 0 to 100 %, but none of the organisms promoted the pathogen. Cluster analysis separated the organisms into five categories of biocontrol effectiveness. Bacteria, yeasts, Verticillium spp., T. roseum and Aspergillus spp. were relatively ineffective. Isolates of

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E. purpurascens and A. alternata turned up in three and all five clusters, respectively, underscoring the importance of quantifying biocontrol on an isolate basis. The most powerful cluster ( > 96% suppression) included all tested isolates of G. roseum, Myrothecium verrucaria and Trichoderma viride, plus some isolates of Penicillium spp., Fusarium spp., Colletotrichum gloeosporioides and E. purpurascens besides A. alternata. Eleven organisms, representing members of each cluster, were then evaluated against B. cinerea on detached petals, and on attached leaves and flowers of strawberry in the growth room and greenhouse (Peng and Sutton, 1991). Tissues were inoculated as before with test organisms and 24 h later with the pathogen. After a 24-h postinoculation humid period, discs cut from attached leaves and petals and stamens detached from test flowers were placed on the paraquat medium and conidiophores of B. cinerea were later estimated. Biocontrol effectiveness of the organisms among the assays was similar in pattern and ranking. A Pearson's r value of 0.96 (P _< 0.01) was obtained when observations of leaf-disc and petal assays were compared. Biosuppression on attached organs ranged from 24-65% to 97-100% and r values of 0.78-0.94 and 0.82-0.96 (P < 0.01) were obtained, respectively in comparisons of these observations with those in leaf disc and petal assays. While relative effectiveness of a majority of the organisms was similar in the different tests, E. purpurascens and M. verrucaria were notably less effective on attached than on detached tissues. G. roseum was completely effective or nearly so in all tests. The 11 organisms were evaluated over 2 years in the field using 4 m x 1 m plots in 2-3 year-old matted row plantings of 'Redcoat' strawberries, the same as used in the controlled environments (Peng and Sutton, 1991). The plantings were maintained according to Ontario recommendations but without fungicides, and trickle irrigation was used in place of sprinklers. A spore suspension of B. cinerea (2 x 103 conidia m1-1) was applied in the plots when flowering began in order to reduce marked irregularity in pathogen distribution. A more realistic method of introducing the pathogen would have been to apply infested host leaves, but this was not practical in these instances. Key remaining questions were when and how to introduce the test organisms. Recognizing that density of biocontrol organisms introduced to above-ground portions of plants usually declines precipitously, and that our purpose was to estimate relative, not optimal, performance of the organisms, it was decided to apply treatments four times on a weekly schedule during the flowering and fruiting period. As with fungicide treatments, weekly applications of biocontrol agents targeted primarily at the flowers were not ideal because flowers that opened shortly after treatment probably went untreated. Suspensions of fungal conidia and yeast cells (106 and 107 propagules ml -l water plus surfactant, respectively), a suitable check, and captan to serve as a standard of commercial disease control, were applied with a compressed air sprayer shortly before nightfall and dew onset. The importance of timing biocontrol treatments in relation to daily changes in microclimate remains in question. An open-top chamber was positioned over each plot during treatment to prevent

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spray drift. Incidence of B. cinerea in stamens and fruits were estimated to measure biocontrol effectiveness. Relative effectiveness of the organisms correlated significantly among the field tests (Pearson's coefficient, r, - 0.53 - 0.89, P _ 0.01 - 0.01) and among field and controlled tests (Spearman's ranking coefficient 0.42 - 0.82, P _ 0.10 0.01). Consistent ranking was evident for a majority of isolates but M. verrucaria and A. alternata ranked poorly in the field compared with controlled conditions. The generally similar rankings of isolates among controlled and field tests indicated that each of the controlled assays was suitable for preliminary appraisal of test organisms. It did not seem to matter whether leaves or flowers were used or whether they were attached or detached. The leaf disc assay, however, was least demanding in terms of plant materials, growth facilities, and time. In the field tests, isolates of G. roseum, Penicillium sp., T. viride, G. gloeosporioides, E. purpurascens and T. roseum were the more effective organisms and suppressed B. cinerea by 79-93 % in stamens and 48-76 % in fruits. Several of these isolates were at least as effective as captan. All except T. viride were prominent members of the strawberry mycoflora (McLean and Sutton, 1992). Isolates of G. roseum, Penicillium sp. and T. viride were selected for further evaluation as biocontrol agents; each were highly effective in a majority of tests and none had produced symptoms on strawberry. 3. Further Evaluation of Leading Candidates Suppression of B. cinerea in Redcoat plantings at two or three locations in two growing seasons gave no assurance of general effectiveness of the biocontrol candidates in strawberry cropping systems. The possibility that host genotype and microclimatic conditions not experienced in the initial tests could affect biocontrol (Fig. 1) prompted investigations of biocontrol by G. roseum in eight June-bearing cultivars (Annapolis, Blomidon, Governor Simcoe, Honeoye, Kent Redcoat, Vantage and Veestar) of differing parentage and susceptibility to B. cinerea (G. Xue, J. C. Sutton and J. A. Sullivan, unpublished). The studies were done in field plots during 2 years using methods similar to those in the previous studies. It turned out that the cultivars and biocontrol agent did not interactively affect B. cinerea. Gliocladium roseum suppressed B. cinerea in leaves, petals, stamens and fruits as effectively or better than did captan. Ranking of fruit rot incidence among the cultivars correlated well with that of sporulation density of B. cinerea on leaves and sporulation incidence on stamens (Spearman's coefficient - 0.76 in both cases), but negatively with sporulation density on petals ( - 0.82). The tests increased confidence that G. roseum was effective in a wide range of weather conditions. Biocontrol of B. cinerea in everbearer strawberries presented special challenges related to prolonged flowering and fruiting and sparse epidemiologic information. In a 2-year study, G. roseum, T. viride and captan were applied weekly for 12 weeks, starting at first flowering, to cuhivars Tribute and Tristar (A. Dale and J . C . Sutton, unpublished). Fruits harvested twice weekly from late July until

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October were assessed for incidence of B. cinerea. The test organisms were of similar effectiveness in both years. The biocontrol agents (applied at 107 conidia ml-1) and the fungicide suppressed incidence of B. cinerea in fruits by 32-70%, with the poorer performance levels during cool and humid conditions late in the cropping season. G. roseum reduced flower abortion from 9 to 2 % during August. The agents were about 10-25 % less effective than captan in suppressing B. cinerea in fruit harvested in late July and early August, but of similar or greater effectiveness in fruit of subsequent harvests. Possibly a build-up of the agents in the crop during the initial weeks of treatment raised the level of biocontrol. As in Junebearers, strategies to optimize timing of biocontrol treatments in everbearers remain to be worked out. The isolates of G. roseum, T. viride and Penicillium sp. were remarkably effective in suppressing sporulation potential of B. cinerea in strawberry leaves. Redcoat leaves were inoculated with B. cinerea (105-106 conidia m1-1) and treated 2-5 weeks later with the test isolates (107 conidia ml-1) or with chlorothalonil. The respective organisms suppressed B. cinerea by 97-100 % in attached leaves in the greenhouse, by 58, 64 and 48 % respectively in semisenescent overwintered leaves in the field, and by 81-100%, 59-100% and 53-87% when applied to green leaves in strawberry field plots in spring, late summer and early autumn (Peng and Sutton, 1990; Sutton and Peng, 1993). G. roseum was consistently as effective as ehlorothalonil, which in previous studies suppressed B. cinerea in strawberry leaves better than other commercially available fungicides and controlled fruit rot when applied only to the leaves before flowering began (Braun and Sutton, 1986; Sutton, 1990). Penicillium sp. and T. viride were as effective as chlorothalonil in the greenhouse but in only three of six field studies. G. roseum was selected for continued development as a biocontrol agent based on consistent effectiveness of all tested isolates under a wide range of conditions in strawberry cropping systems. The antagonist also has the advantages of easy inoculum production, sticky conidia which may help avoid allergic responses in the user, and common occurrence as an indigenous fungus in strawberry fields which may favor registration for commercial use.

C. Vectoring of Biocontrol Organisms by Bees Efficiency of application method could be a decisive factor in acceptability of biocontrol by strawberry growers. Spray methods are acceptable for treating foliage but are highly inefficient for treating flowers (Sutton, 1990). In seeking an alternative it was surmised that bees, including the European honey bee (Apis mellifera L.), might serve as vehicles to deliver biocontrol agents to strawberry flowers. Bees, after all, are well known as vectors of pollen, fungi and bacteria among flowers of various plant species (Free, 1970; Harrison et al., 1980). Honey bees were therefore examined as vectors of G. roseum to strawberry flowers. Vectoring was investigated using a powder formulation of the biocontrol agent

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and an inoculum dispenser to contaminate the bees with the formulation each time they left the hive (Peng et al., 1992). Constructed of wood, hardware cloth, and Plexiglas | the dispenser fitted inside the lower portion and front of the hive. A formulation of G. roseum with pure talc and corn meal (10:1, w : w ) at 5 x 108cfu g - ' was spread about 5-8 mm deep on a removable tray in the dispenser. Outgoing bees were obliged to crawl about 12 cm through the inoculum before leaving the hive. Bees emerging from dispensers carried an average of 570 000 cfu G. roseum per bee and deposited a mean of 1600-27 000 cfu on each flower. Inoculum density of G. roseum on flowers treated by bees was at least as high, and more stable, than on flowers in plots that received weekly sprays of 107 conidia G. roseum m l - ' water plus surfactant. Effectiveness of the bee and spray methods in suppressing B. cinerea on petals, stamens and fruits was in each instance high and did not differ significantly. While bees were effective delivery vehicles of G. roseum to strawberry flowers, absolute efficacy of this method in terms of inoculum required per unit area of strawberry planting remains to be estimated. In other recent biocontrol studies, honey bees successfully vectored G. roseum to raspberry flowers (Yu and Sutton, unpublished), species of Gliocladium, Epicoccum and Alternaria to rapeseed flowers (Israel and Boland, 1992), and Pseudomonas fluorescens and Erwinia herbicola to apple and pear flowers (Thomson et al., 1992; Johnson etal., 1993). Fungal agents were formulated with various talcum powders, pulverized corn meal, wheat flour, soya flour and corn starch, each with particle sizes generally in the range of 5-15 #m (Yu and Sutton, unpublished; Israel and Boland, 1992), while bacteria were adsorbed on apple and cattail pollen (Thomson et al., 1992) or were used as freeze-dried preparations with cryoprotective skim milk and xanthan (Johnson etal., 1993). Interestingly, this surge of studies on vectoring of biocontrol agents came a century after Waite (1891) first discovered that honey bees vectored the pathogen Erwinia amylovora to pear blossoms. Principal stages in vectoring of biocontrol agents are acquisition and transport of inoculum by the vector, and transfer of the inoculum from the vector to target sites. Sufficient inoculum must be vectored to suppress the pathogen adequately. In the vectoring studies of G. roseum, the bees acquired inoculum on almost all external surfaces, including those of the head, thorax, wings, abdomen and legs (Peng et al., 1992). Conidia and carrier particles were especially abundant on the setae. Stickiness of the conidia possibly facilitated acquisition; however, bees are able also to vector dry-spored fungi (Israel and Boland, 1992). Many bees attempted to remove inoculum, especially from the head and antennae, for about 20-50 s immediately prior to take-off, but otherwise did not show abnormal behavior or signs of stress. Accumulations of inoculum in front of dispensers and inoculum clouds sometimes visible around bees indicated considerable inoculum loss at take-off. Inoculum recovered from plants in check plots probably resulted from inoculum loss by overflying bees. Transfer of inoculum from the bee to the flower may involve direct contact of the bee with flower parts and possibly local dispersal

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while the bee actively moves when on the flower. Honey bees often make good contact with strawberry stamens, which probably is important for biocontrol. Redistribution of inoculum among flowers is possible and some inoculum is deposited in the hive, so it is questionable whether the honey should be used for human consumption. Mobility of bees presents problems in studies of vectoring in field plots. Screening materials used to separate bee treatments from those without bees results in substantial shading (e.g. 30-60%) and thus microclimatic shifts in plots. Construction of screened enclosures over all plots equalizes the microclimatic changes, but is expensive and sometimes impractical. Honey bees behave differently when confined in enclosures than when allowed to forage freely. Many spend considerable time attempting to escape, and usually do so should a hole develop in the screening. Bees allowed to forage freely may provide the most representative information on vectoring relative to that which would take place in crops, but check treatments must still be protected from intrusions by bees. Honey bees readily establish foraging patterns in preferred nectar sources outside plot areas, as occurred in our studies when nearby rapeseed bloomed (Peng et al., 1992). Chemical bee attractants applied in plots help to avoid external foraging but represent an additional interference factor. The importance of'foreign' bees and other insects as interference factors in vectoring studies is not known. Honey bees generally do not forage readily in cool ( < 17~ or rainy weather, but brief periods of unfavorable conditions did not markedly reduce vectoring of G. roseum and biocontrol of B. cinerea in strawberry. Species of bumble bees (Bombus spp.) that regularly forage when air temperature falls as low as 6~ (Heinrich, 1979) are now under investigation as vectors of G. roseum (Yu and Sutton, unpublished). Quantitative and spatial information of bee colonies in relation to vectoring of biocontrol agents and biocontrol effectiveness require field-scale studies. These kinds of observations in small plots are confounded by variable foraging by bees outside the plot area, either out of necessity or because of preferences in nectar sources. Outside foraging can diminish markedly as the planting area increases provided that suitable precautions are taken. It is well known, for example, that bees of colonies placed in a crop before flowering begins will probably establish foraging patterns outside the crop area and maintain these even after the crop begins to flower. This can be avoided by introducing colonies after flowering has begun. Because of bee foraging habits, quantitative information of vectoring in small plots, unlike that of spray treatments, should not be extrapolated to the field scale. Studies on the number, size and distribution of colonies in relation to vectoring and biocontrol of B. cinerea under various weather conditions are needed to provide information to optimize vectoring operations in crops. This information would also allow realistic comparisons on the efficiency of inoculum application by bees and as sprays.

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D. Biocontrol Mechanisms of Gliocladium roseum The effectiveness of G. roseum in suppressing B. cinerea in strawberry under a wide range of conditions is a function of its ecological relationships with strawberry and its ability to outcompete B. cinerea in the tissues under cool as well as warm temperatures. The ecological relationships are best known for strawberry leaves. Like B. cinerea, G. roseum is able to penetrate into the leaves while they are green and to colonize the tissues progressively when they senesce and die. After application to green leaves infected with B. cinerea, isolates of the antagonist markedly suppressed growth and sporulation of the pathogen when the leaves senesced and died (Sutton and Peng, 1993). Evidently, G. roseum colonizes and exploits the leaf tissues much more rapidly than B. cinerea and largely precludes colonization by the pathogen. Effectiveness of the antagonist was markedly reduced when it was applied to senescent or dead leaves, probably because the pathogen had a head start in colonizing the tissues under these circumstances. Unlike isolates of T. viride and Penicillium sp., those of G. roseum markedly suppressed G. roseum at 10~ and 15~ as well as at 20~ and 25~ (Sutton and Peng, 1993). From our studies, substrate competition rather than antibiosis or hyperparasitism is the key biocontrol mechanism of G. roseum against B. cinerea in strawberry leaves (Peng, 1991; Sutton and Peng, 1993). The antagonist is able to produce antifungal metabolites that suppress growth and germination of B. cinerea in vitro, but ultraviolet-light induced mutants that produced high, moderate, or non-detectable levels of the principal metabolite did not differ in biocontrol effectiveness against the pathogen. Although G. roseum is a well-known mycoparasite, no evidence was found for mycoparasitism of B. cinerea in strawberry leaves.

VI. CONCLUSIONS AND FUTURE DIRECTIONS Screening of strawberry-associated microflora against B. cinerea by means of assays on strawberry plant materials and field plot tests successfully identified biocontrol agents that performed well in the strawberry cropping system. Gliocladium roseum, Penicillium sp. and T. viride emerged as the best group of antagonists within the limits of the tests; however, field tests of additional organisms that were effective in the leaf disc assays would probably identify other useful agents, as might tests of further microflora from cultivated or wild strawberries, or other sources. Gliocladium roseum has numerous advantages for practical biocontrol of B. cinerea in strawberry. Because it is effective in leaves, flowers and fruits, it can be targeted successfully against B. cinerea at the inoculum source in the leaves or to protect the flowers and fruits directly. The ability of G. roseum to penetrate and survive in the leaves results in extraordinary persistence of the antagonist in the foliage for weeks or months after application, which is in sharp contrast to many biocontrol agents that are active against pathogens chiefly on the phylloplane and

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quickly decline in numbers and activity after application (Andrews, 1985). As a consequence of its persistence in green leaves and biocontrol activity when the leaves senesce and die, G. roseum applied once at any time while the leaves are green potentially controls B. cinerea in each leaf flush. As found in field studies and in contrast to chlorothalonil, G. roseum is less effective or ineffective when applied to senescing or dead leaves (Sutton and Peng, 1993). Inoculum production of G. roseurn is easily scaled up on cheap substrates such as wheat grains which should favor cost effectiveness of biocontrol. Besides its versatility against B. cinerea in strawberry, G. roseum also suppresses effectively the pathogen in raspberry and in spruce seedlings (Sutton, unpublished; Zhang etal., 1994) thereby widening the market potential of the antagonist. Further studies are needed to facilitate and optimize use of G. roseum in strawberry crops, and probably to satisfy registration requirements in Canada. Information is required on methods to produce, formulate, store and package inoculum on a commercial scale while maintaining important quality characteristics including viability and effectiveness of the biocontrol agent. Treatment methodology also requires further investigation. The possibility that a single spray applied to the leaves before flowering would suppress initial inoculum sufficiently to obviate the need to treat the flowers, as was observed with fungicide treatments (Braun and Sutton, 1986), is worth exploring. Studies are needed to optimize the timing of sprays applied to flowers in respect to frequency, host phenology, and microclimatic variables such as rain, daily periods of light and darkness, and dryness and wetness of the foliage and flowers. Much remains to be learned of spray nozzles, application pressures and droplet sizes in relation to spray applications. The newly emerging methods of inoculum delivery by bees will undoubtedly be further explored, and could be easy to implement since many growers already use bees to pollinate strawberries. Integration of biocontrol methods with other practices to protect and produce strawberries should not prove difficult; few potential conflicts are foreseen except in some instances between insecticides and bee vectors. Use of G. roseum or other agents to control B. cinerea on the farm would be a major step towards non-chemical disease management in strawberries.

ACKNOWLEDGMENTS Support by the Natural Sciences and Engineering Research Council of Canada, Grant OGP0006119, and of the Pesticides Advisory Committee of the Ontario Ministry of the Environment, is gratefully acknowledged.

REFERENCES Andrews, J. H. (1985). Strategies for selecting antagonistic microorganisms from the phyUoplane. In 'Biological Control on the Phylloplane' (C. E. Windles and S. E. Lindow, eds), pp. 31-44. The American Phytopathological Society, St Paul, MN.

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Aust, H.J. and Kranz, J. (1988). Experiments and procedures in epidemiological field studies. In 'Experimental Techniques in Plant Disease Epidemiology' (J. Kranz and J. Rotem, eds), pp. 7-17. Springer-Verlag, Berlin. Barritt, B. H. (1980). Resistance of strawberry clones to Bottytis fruit rot. Journal of the American Societyfor Horticultural Science 105, 160-164. Bhatt, D. D. and Vaughan, E. K. (1962). Preliminary investigations on biological control of grey mould (Botrytis cinerea) of strawberries. Plant Disease Reporter 46, 342-345. Bhatt, D. D. and Vaughan, E. K. (1963). Interrelationships among fungi associated with strawberries in Oregon. Phytopathology 53, 217-220. Braun, P.G. and Sutton, J . C . (1986). Management of strawberry gray mould by fungicides targeted against inoculum in crop residues. In 'Proceedings of the British Crop Protection Conference, Pests and Diseases' Vol. 3, pp. 915-921. British Crop Protection Council, Croydon. Braun, P. G. and Sutton, J. C. (1987). Inoculum sources of Botrytis cinerea in fruit rot of strawberry in Ontario. CanadianJournal of Plant Pathologj, 9, 1-5. Braun, P. G. and Sutton,J. C. (1988). Infection cycles and population dynamics of Botrytis cinerea in strawberry leaves. CanadianJournal of Plant Pathology 10, 133-141. Bristow, P.R., McNichol, R.J. and Williamson, B. (1986). Infection of strawberry flowers by Bot~ytis cinerea and its relevance to grey mould development. Annals of Applied Biology 109, 545-554. Burpee, L. L. (1990). The influence of abiotic factors on biological control of soilborne plant pathogenic fungi. Canadian Journal of Plant Pathology 12, 308-317. Cook, R.J. (1992). Reflections of a regulated biocontrol researcher. In 'Regulations and Guidelines: Critical Issues in Biological Control. Proceedings of a USDA/CSRS National Workshop, June 10-12, 1991, Vienna, VA (R. Charudattan and H.W. Browning, eds), pp. 9-24. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL. Cook, R.J. (1993). Making greater use of microorganisms for biological control of plant pathogens. Annual Review of Phytopatholog), 31, 53-80. Cook, R.J. and Baker, K. F. (1983). 'The Nature and Practice of Biological Control of Plant Pathogens'. The American Phytopathological Society, St Paul, MN. Cooke, R. C. and Rayner, A. D. M. (1984). 'Ecology of Saprotrophic Fungi'. Longman, London. Galletta, G.J. and Bringhurst, R. S. (1990). Strawberry Management. In 'Small Fruit Crop Management' (G. J. Galletta and D. G. Himelrick, eds), pp. 83-156. Prentice Hall, Englewood Cliffs, NJ. Free, J. B. (1970). 'Insect Pollination of Crop Plants'. Academic Press, London. Harrison, M. D., Brewer, J. W. and Merrill, L. D. (1980). Insect involvement in the transmission of bacterial pathogens. In 'Vectors of Plant Pathogens' (K. F. Harris and K. Maramorosch, eds), pp. 293-324. Academic Press, New York. Heinrich, B. (1979). 'Bumblebee Economics'. Harvard University Press, Cambridge, MA. Israel, M. S. and Boland, G.J. (1992). Influence of formulation on efficacy of honey bees to transmit biological controls for management of sclerotinia stem rot of canola. (Abstr.) Canadian Journal of Plant Pathology 14, 244. Jarvis, W. R. (1962a). The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Annals of Applied Biology 50, 569-575. Jarvis, W. R. (1962b). The epidemiology of Botrytis cinerea Pers. in strawberries. In 'Proceedings of the 16th International Horticultural Congress, August 31-September 8, 1982, Brussels, Belgium'. pp. 258-262. Duculot, Gembloux, Belgium. Jarvis, W. R. and Borecka, H. (1968). The susceptibility of strawberry flowers to infection by Botrytis cinerea. Horticultural Research 8, 147-154.

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James, w . c. (1974). Assessment of plant diseases and losses. Annual Review of Phytopathology 12, 27-48. Johnson, K. B., Stockwell, V. O., Burgett, D. M., Sugar, D. and Loper, J. E. (1993). Dispersal of Erwinia amylovora and Pseudomonasfluorescens by honey bees from hives to apple and pear blossoms. Phytopathology 83, 478-484. Ku6, J. (1987). Plant immunization and its applicability for plant disease control. In 'Innovative Approaches to Plant Disease Control' (I. Chet, ed.), pp. 255-274. Wiley, New York. Kranz, J. (1974). Comparison of epidemics. Annual Review of Phytopathology 12, 355374. Maas, J. L. (1978). Screening for resistance to fruit rot in strawberries and raspberries: a review. HortScience 13, 423-426. Maas, J. L. ed. (1984). 'Compendium of Strawberry Diseases'. The American Phytopathological Society, St Paul, MN. McLean, M. A. (1988). The microflora of strawberry in relation to biological control of grey mould fruit rot caused by Botrytis cinerea Pers. ex. Fr. MSc Thesis, University of Guelph, Guelph, Ontario. McLean, M. A. and Sutton, J. C. (1992). Mycoflora of strawberry in Ontario. Canadian Journal of Botany 70, 846-852. Peng, G. (1991). Biological control of grey mould (Botrytis cinerea) on strawberries. PhD thesis, University of Guelph, Guelph, Ontario. Peng, G. and Sutton, J. C. (1990). Biological methods to control grey mould of strawberry. 'Proceedings of the Brighton Crop Protection Conference, Pests and Diseases', Vol. 1, pp. 233-240. British Crop Protection Council, Farnham, UK. Peng, G. and Sutton, J. C. (1991). Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. CanadianJournal of Plant Pathology 13,247-257. Peng, G., Sutton, J. C. and Kevan, P. G. (1992). Effectiveness of honey bees for applying the biocontrol agent Gliocladium roseum to strawberry flowers to suppress Botrytis cinerea. Canadian Journal of Plant Pathology 14, 117-129. Powelson, R. L. (1960). The initiation of strawberry fruit rot caused by Botrytis cinerea. Phytopathology 50, 491-494. Scher, F. M. and Castagno, J. R. (1986). Biocontrol: A view from industry. CanadianJourhal of Plant Pathology 8, 222-224. Simpson, D. W. (1989). Botrytis cinerea infection in pistillate and hermaphrodite strawberry flowers. Acta Horticulturae 265, 555-560. 9 Simpson, D. W. (1991). Resistance of Botrytis cinerea in pistillate genotypes of the cultivated strawberry Fragaria ananassa. Journal of Horticultural Science 66, 719-723. Sutton, J . C . (1988). Predictive value of weather variables in the epidemiology and management of foliar diseases. Fitopatologia brasileira 13, 305-312. Sutton, J. C. (1990). Epidemiology and management of botrytis leaf blight of onion and gray mould of strawberry: a comparative analysis. CanadianJournal of Plant Pathology 12, 100-110. Sutton, J. C. (1991). Alternative methods for managing gray mold of strawberry. In 'The Strawberry into the 21st Century' (A. Dale and J. J. Luby, eds), pp. 183-191. Timber Press, Portland, OR. Sutton, J. C. and Peng, G. (1993). Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology 83, 615-621. Sutton, J. C. and Peng, G. (1993). Manipulation and vectoring of biocontrol organisms to manage foliage and fruit diseases in cropping systems. Annual Review of Phytopathology 31,473-493. Sutton, J. C., James, T. D. W. and Dale, A. (1988). Harvesting and bedding practices in relation to grey mould of strawberries. Annals of Applied Biology 113, 167-175.

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Thomson, S. V., Hansen, D. R., Flint, K. M. and Vandenberg, J. D. (1992). Dissemination of bacteria antagonistic to Erwinia amylovora by honey bees. Plant Disease 76, 1052-1056. Tronsmo, A. and Dennis, C. (1977). The use of Trichoderma species to control strawberry fruit rots. NetherlandsJournal of Plant Pathology 83, 449-455. Suppl. I. Vanderplank, J. E. (1963). 'Plant diseases: Epidemics and Control'. Academic Press, New York. Waite, M. B. (1891). Results from recent investigations in pear blight. (Abstr.) Botanical Gazette 16, 259. Zadoks, J. C. and Schein, R. D. (1979). 'Epidemiology and Plant Disease Management'. Oxford University Press, New York. Zhang, P. G., Sutton, J. C. and Hopkin, A. A. (1994). Evaluation of microorganisms for biocontrol of Bot~ytis cinerea in container-grown black spruce seedlings. CanadianJournal of Forest Research 24, 1312-1316.

10 BIODIVERSITY AND BIOCONTROL: LESSONS FROM INSECT PEST MANAGEMENT M i g u e l A. Altieri Division of Biological Control, University of California - Berkeley, 1050 San Pablo Avenue, Albany, CA 94706, USA

I. II. III. IV.

Introduction Ecological Theory Concerning Biodiversity and Biocontrol Agroecosystem Biodiversification and Biological Control Enhancing Natural Enemy Biodiversity in Agroecosystems: the Case of Parasitic Hymenoptera A. Multiple Introductions of Parasitoids B. Reducing Direct Mortality by Eliminating Pesticides C. Provision of Supplementary Resources D. Increasing Adjacent Vegetational Diversity E. Increasing Within-field Plant Diversity F. Manipulating Host-plant Attributes G. Manipulations with Semiochemicals V. Conclusions References

191 192 194 202 203 203 204 204 204 205 205 206 206

I. I N T R O D U C T I O N Agriculture is a process of artificially manipulating nature and implies the simplification of the structure of the environment over vast areas, replacing nature' s diversity with a small number of cultivated plant species and domesticated animals. This process of biodiversity simplification reaches an extreme form in agricultural monocultures, which constitute artificial ecosystems, lacking selfregulatory mechanisms and thus requiring constant human intervention in the form of agrochemical inputs to maintain productivity (Ahieri, 1987). Nowhere are the consequences of biodiversity reduction more evident than in the realm of agricultural pest management. The instability of agroecosystems becomes manifest as the worsening of most insect pest problems is increasingly linked to the expansion of crop monocultures at the expense of the natural vegetation and local habitat complexity (Altieri and Letourneau, 1982). Plant communities that are modified to meet the special needs of humans become subject to heavy pest damage and generally the more intensely such communities are ADVANCES IN PLANT PATHOLOGY~VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 Academic Press Limited All rights of reproduaion in anyform reserved

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modified, the more abundant and serious the pests. The inherent self-regulation characteristics of natural communities are lost when humans modify such communities through the shattering of the fragile thread of community interactions (Turnbull, 1969). Ecological theory suggests that this breakdown can be repaired by restoring the elements of community homeostasis through the addition or enhancement of biodiversity (Perrin, 1980). In modern agroecosystems, the experimental evidence suggests that biodiversity can be used for improved pest management (Flint and Roberts, 1988; Andow, 1991). Several studies have shown that it is possible to stabilize insect communities of agroecosystems by designing and constructing vegetational architectures which support populations of natural enemies and/or that have direct regulatory effects on pest herbivores. Biodiversity in agroecosystems can be as varied as the various crops, weeds, arthropods or micro-organisms involved, according to geographical location, climatic, edaphic, human and socioeconomic factors. Complementary interactions between the various biotic components can also be of a multiple nature. Some of these interactions can be used to induce positive and direct effects on the biological control of specific crop pests, as well as on soil fertility regeneration and/or enhancement and soil conservation. The exploitation of these interactions in real situations involves agroecosystem design and management and requires an understanding of the numerous relationships between soils, micro-organisms, plants, insect herbivores and natural enemies (Price et al., 1980). The idea is to enhance and/or regenerate the right kind of biodiversity that can subsidize the sustainability of agroecosystems by providing ecological services such as biological pest control but also nutrient cycling, water and soil conservation, etc.

II. ECOLOGICAL THEORY CONCERNING BIODIVERSlTY AND BIOCONTROL Mixing certain plant species with the primary host of a specialized herbivore gives a fairly consistent result: specialized species usually exhibit higher abundance in monoculture than in polycultures. In a recent review, Andow (1991) identified 209 published studies that deal with the effects of vegetation diversity in agroecosystems on herbivorous arthropod populations. Fifty-two per cent of the 287 total herbivore species examined in these studies were found to be less abundant in diversified systems than in monocultures, while only 15.3% (44 species) exhibited higher densities in polycultures. Among the various ecological hypotheses that have been offered to explain lower pest-population loads in multispecies plant association, only one pertains to the role of natural enemies. This 'natural enemy hypothesis' predicts that there will be a greater abundance and diversity of natural enemies of pest insects in polycultures than in monocultures (Root, 1973). Predators tend to be polyphagous and have broad habitat requirements, so they would be expected to

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encounter a greater array of alternative prey and microhabitats in a heterogeneous environment. Annual crop monocultures do not provide adequate alternative sources of food (pollen, nectar, prey), shelter, breeding and nesting sites for the effective performance of natural enemies (Rabbet al., 1976). The natural enemy hypothesis has been stated in the following way: 1. A greater diversity of prey and microhabitats is available within complex environments. As a result, relatively stable populations of generalized pre: dators can persist in these habitats because they can exploit the wide variety of herbivores that become available at different times or in different microhabitats (Root, 1973). 2. Specialized predators are less likely to fluctuate widely because the refuge provided by a complex environment enables their prey to escape widespread annihilation (Risch, 1981). 3. Diverse habitats offer many important requisites for adult predators and parasites, such as nectar and pollen sources, which are not available in monocultures, reducing the probability that they will leave or become locally extinct (Risch, 1981). According to Root' s enemies hypothesis, generalist and specialist natural enemies are expected to be more abundant in polycultures and, therefore, more effectively suppress herbivore population densities in polycultures than in monocultures. Generalist predators and parasitoids should be more abundant in polycultures than monocultures because (1) they switch and feed on the greater variety of herbivores that become available in polycultures at different times during the growing season; (2) they maintain reproducing populations in polycultures while in monocultures only males of some parasitoids are produced; (3) they can utilize hosts in polycultures that they would normally not encounter and use in monocultures; (4) they can exploit the greater variety of herbivores available in different microhabitats in the polycultures; and (5) prey or hosts are more abundant or more available in polycultures (Andow, 1991). Specialist predator and parasitoid populations are expected to be more abundant and effective in polycultures than monocultures because prey or host refuges in polycultures enable the prey or host populations to persist, which stabilizes predator-prey and parasitoid-host interactions, while in monocultures predators and parasitoids drive their prey or host populations to extinction and become extinct themselves shortly thereafter. Prey or host populations will recolonize these monocultures and rapidly increase (Andow, 1991). Finally, both generalist and specialist natural enemies should be more abundant in polycultures than monocultures because more pollen and nectar resources are available at more times during the season in polycultures than monocultures (Altieri and Letourneau, 1982). Sheehan (1986) and Russell (1989) have questioned the universal validity of the natural enemy hypothesis that explains the effects of agroecosystem diversification on searching behavior and success of arthropod natural enemies, and claims

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that such interactions are still poorly understood. Fifty per cent of the 18 studies reviewed by Russell (1989) found higher herbivore mortality from predation or parasitism in diverse systems, but according to Russell, a lack of adequate control in all but one study prevented researchers from concluding that the above difference in mortality is what really reduces the numbers of herbivores in complex systems. He further argues that the enemies hypothesis and the resource concentration hypothesis act as complementary mechanisms in reducing numbers of herbivores in polycultures, and that, therefore, both should be enhanced simultaneously to achieve maximum control. According to Sheehan (1986), the enemies hypothesis is simplistic in several respects. Victim location by generalist enemies may be hindered by increased plant density or patchiness in diverse agricultural systems. In fact, crop diversification may reduce enemy-searching efficiency and destabilize predator/prey interactions. Specialist enemies, often important in biological control programs, may be particularly sensitive to vegetation texture. Pest control by specialist enemies may be more effective in less diverse agroecosystems if concentration of host plants increases attraction or retention of these enemies. Thus, it is possible that certain specialist enemies may not necessarily respond to habitat diversification in the same way as generalists. Sheehan (1986) suggested that specialist parasitoids might be less abundant in polycultures than monocuhures because (1) chemical cues used in host finding will be disrupted and the parasitoids will be less able to find hosts to parasitize and feed upon in polycuhures; and (2) the indistinct boundary at the edges of polycultures will be hard to recognize and they will be more likely to leave polycultural habitats than monocultures. In addition, Andow and Prokrym (1990) showed that structural complexity, or the connectedness of the surface on which a parasitoid searches, can strongly influence parasitoid host-finding rates. An implication of their study is that structurally complex polycultures would have less parasitism than structurally simple monocultures. Factors that increase immigration to, and decrease emigration from, host-plant areas by specialist enemies (e.g. large patch size, close plant spacing, the presence of specific chemical or visual stimuli, and lower chemical or structural diversity of associated vegetation) may cause those enemies to remain longer and hunt more effectively in simple than in diverse agroecosystems, at least in those that are not too extensive.

III. AGROECOSYSTEM BIODIVERSIFICATION AND BIOLOGICAL CONTROL Crop monocultures are difficult environments in which to induce efficient biological pest control because these systems lack adequate resources for effective performance of natural enemies and because of the disturbing cultural practices often utilized in such systems. More diversified cropping systems already contain

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certain specific resources for natural enemies provided by plant diversity, and are usually not disturbed with pesticides (Altieri and Letourneau, 1984). Thus, by replacing or adding diversity to existing systems, it may be possible to exert changes in habitat diversity that enhance natural enemy abundance and effectiveness by (van den Bosch and Telford, 1964; Powell, 1986): 1. 2. 3. 4.

Providing alternative hosts/prey at times of pest host scarcity. Providing food (pollen and nectar) for adult parasitoids and predators. Providing refuges for overwintering, nesting, and so on. Maintaining acceptable populations of the pest over extended periods to ensure continued survival of beneficial insects.

The specific resulting effect or the strategy to use will depend on the species of herbivores and associated natural enemies, as well as on properties of the vegetation, the physiological condition of the crop, or the nature of the direct effects of particular plant species (Letourneau, 1987). In addition, the success of enhancement measures can be influenced by the scale upon which they are implemented (i.e. field scale, farming unit or region) since field size, within-field and surrounding vegetation composition, and the level of field isolation (i.e. distance from source of colonizers) will all affect immigration rates, emigration rates, and the effective tenure time of a particular natural enemy in a crop field. Perhaps one of the best strategies to increase effectiveness of predators and parasitoids is the manipulation of non-target food resources (i.e. alternate hostsprey and pollen-nectar) (Rabbet al., 1976). Here it is not only important that the density of the non-target resource be high to influence enemy populations, but that the spatial distribution and temporal dispersion of the resource be adequate also. Proper manipulation of the non-target resource should result in the enemies colonizing the habitat earlier in the season than the pest, and frequently encountering an evenly distributed resource in the field, thus increasing the probability of the enemy to remain in the habitat and reproduce (Andow and Risch, 1985). Certain polycultural arrangements increase and others reduce the spatial heterogeneity of specific food resources; thus particular species of natural enemies may be more or less abundant in a specific polyculture. These effects and responses can only be determined experimentally across a whole range of agroecosystems. The task is indeed overwhelming since enhancement techniques must necessarily be site-specific. The literature is full of examples of experiments documenting that diversification of cropping systems often leads to reduced herbivore populations. The studies suggest that the more diverse the agroecosystem and the longer this diversity remains undisturbed, the more internal links develop to promote greater insect stability. It is clear, however, that the stability of the insect community depends not only on its trophic diversity, but on the actual density-dependence nature of the trophic levels (Southwood and May, 1970). In other words, stability will depend on the precision of the response of any particular trophic link to an increase in the population from a lower level.

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Although most experiments have documented insect population trends in single versus complex crop habitats, a few have concentrated on elucidating the nature and dynamics of the trophic relationships between plants-herbivores and natural enemies in diversified agroecosystems. Several lines of studies have developed:

a. Crop-weed-insect interaction studies Evidence indicates that weeds influence the diversity and abundance of insect herbivores and associated natural enemies in crop systems. Certain weeds (mostly Umbelliferae, Leguminosae and Compositae) play an important ecological role by harboring and supporting a complex of beneficial arthropods that aid in suppressing pest populations (Beingolea, 1957; Leius, 1967; Altieri et al., 1977; Young and Teetes, 1977; Ahieri and Whitcomb, 1979). Specific examples of crop-weed associations that enhance biocontrol are provided in Table 1. b. Insect dynamics in annual polycultures Overwhelming evidence suggests that polycultures support a lower herbivore load than monocuhures. One factor explaining this trend is that relatively more stable natural enemy populations can persist in polycultures due to the more continuous availability of food sources and microhabitats (Risch, 1981; Helenius, 1989). The other possibility is that specialized herbivores are more likely to find and remain on pure crop stands, which provide concentrated resources and monotonous physical conditions (Root, 1973). Specific examples of insect suppressant polycultures are provided in Table 2. c. Herbivores in complex perennial crop systems Most of these studies have explored the effects of the manipulation of ground cover vegetation on insect pests and associated enemies. The data indicate that orchards with rich floral undergrowth exhibit a lower incidence of insect pests than clean-cultivated orchards, mainly because of an increased abundance and efficiency of predators and parasitoids (Altieri and Schmidt, 1985). In some cases, ground cover directly affects herbivore species which discriminate among trees with and without cover beneath. d. The effects of adjacent vegetation These studies have documented the dynamics of colonizing insect pests that invade crop fields from edge vegetation, especially when the vegetation is botanically related to the crop. A number of studies document the importance of adjoining wild vegetation in providing alternate food and habitat to natural enemies which move into nearby crops (van Emden, 1965; Wainhouse and Coaker, 1981). The available literature suggests that the design of vegetation management strategies must include knowledge and consideration of (1) crop arrangement in time and space; (2) the composition and abundance of non-crop vegetation within and around fields; (3) the soil type; (4) the surrounding environment; and (5) the type and intensity of management. The response of insect populations to

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Table 1. Selected example of cropping systems in which the presence of weeds enhanced the biological control of specific crop pests (based on Altieri and Letourneau, 1982; Andow, 1991). , .,.,,.,

Cropping systems Alfalfa

Alfalfa Apple

Weed species

Pest(s) regulated

Natural blooming weed complex

Alfalfa caterpillar

Grass weeds

Empoasca fabae

Phacelia sp. and Eryngium sp.

(Colias eurytheme)

San Jose scale

(Quadraspidio tus perniciosus) and aphids

Apple

Natural weed complex

Tent caterpillar

(Malacosoma americanum) and codling moth

Beans

Goosegrass

(Eleusine indica

and red sprangletop Broccolli Brussels sprouts

(Leptochloa filliformis)

Wild mustard Natural weed complex

(carpocapsa pomonella)

Increased activity of the parasitic wasp

Apanteles medicaginis ?

Increased activity and abundance of parasitic wasps

(Aphelinus mali

and Aphytis

proclia)

Increased activity and abundance of parasitic wasps

Leafhoppers

Chemical repellency or masking

Phyllotreta cruciferae

Trap cropping Alteration of colonization background and increase of predators

(Empoasca kraemer)

Imported cabbage butterfly ( P i e r i s rapae) and aphids

(Brevicoryne brassicae ) Delia brassicae Mamestra brassicae, Evergestis forficalis, Brevicoryne brassicae

Brussels sprouts Brussels sprouts

Sperpula arvensis Spergula arvensis

Cabbage

Crateagus sp.

Citrus

Hedera helix

Lachnosterna spp.

Citrus

Natural weed complex

Mites

Citrus

Natural weed complex Natural weed complex

Diaspidid scales

Coffee

Factor(s)involved

Diamondback moth

(Plutella rnaculipennis)

(Eotetranychus, Panonychus cirri, Metatetranychus cirri)

Pentatomid

Antestiopus intricata

?

Increaseof predators and interference with colonization Provision of alternate hosts for parasitic wasps (Herogenes sp.) Enhancement of

Aphytis lingnanensis ?

M. A. Altieri

198

Table II. (continued) Cropping systems

Weed species

Collards

Ragweed (Ambrosia artemisiifolia)

Collards

Amaranthus retroflexus, Chenopodium album, Xanthium strumarium Giant ragweed

Corn

Corn

Natural weed complex

Corn

Setaria viridis and S. feberii Ragweed

Cotton

Pest(s) regulated Flea beetle (Phyllotreta cruciferae) Green peach aphid (Muzus persicae)

European corn borer (Ostrinia nubilalis)

Heliothis zea, Spodop tera frugiperda Diabrotica virgifera and D. barberi Boll weevil (Anthonomus grandis)

Cotton

Ragweed and Rumex crispus

He/iothis spp.

Cotton

Salvia coccinae, Cissus adenecaulis Quick-flowering mustards

L ypus sp.

Mungbeans

Natural weed complex

Beanfly (Ophlomyia phaseol/~

Oil palm

Pueraria sp., Flemingia sp., ferns, grasses and creepers Ragweed

Scarab beetles (Oryctes rhinoceros and Chalcosoma atlas) Oriental fruit moth

Peach

Rosaceous weeds and Dactylis glomerata

Sorghum

Halianthus spp.

Leafhoppers ( Paraphlepsius irrorotus and Scaphytopius sp.) Schizophis graminun

Soybean

Broodleaf weeds and grasses Cassia obtusifolia

Cruciferous crops

Peach

Soybean

Cabbageworms (Pieris spp.)

Epilachira varivestis Nezara viridula, Anticarsia gemmatalis

Factor(s) involved Chemical repellency or masking Increased abundance of predators (Chrysopa carnea, Coccinellidae, Syrphidae) Provision of alternate hosts for the tachinid parasite L ydella grisescens Enhancement of predators

Provision of alternate hosts for the parasite Eurytoma tylodermatis Increased populations of predators ? Increased activity of parasitic wasps (Apanteles glomeratus) Alteration of colonization background ?

Provision of alternate hosts for the parasite Macrocen trus ancyliverus ?

Enhancement of Aphelinus spp. parasitoids Enhancement of predators Increased abundance of predators

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199

Table II. (continued) Cropping systems

Weed species

Pest(s) regulated

Soybean

Crotalaria sp.

Nezara viridula

Sugar cane

Euphorbia spp. weeds

Sugar-cane weevil (Rhubdosie/us obscurus)

Sugar cane

Grrssy weeds

Sugar cane

Berreria verticillata and Hyptis atrorubens Morning glory (Ipomoea sp.)

Aphid (Rhopalosiphum maidis) Cricket (Scapteriscus vicinus)

Sweet potatoes

Argus tortoise beetle (Chelymorpha cassidea )

Vegetable crops

Wild carrot (Daucus curola)

Japanese beetle (Popillia japonica)

Vineyards

Wild blackberry (Rubus sp.)

Grape leafhopper (Erythroneura elegantula)

Vineyards

Johnson grass (Sorghum halepense)

Pacific mite (Eotetranychus willamettel~

Factor(s)involved Enhancement of tachinid Trichopoda sp. Provision of nectar and pollen for the parasite Lixophaga sphenopheri Destruction of alternate host plants Provision of nectar for the parasite Larra americana Provision of alternate hosts for the parasite Emersonella sp. Increasedactivity of the parasitic wasp Tiphia popilliavera Increaseof alternate hosts for the parasitic wasp Amagrus epos Build-up of predaceous mites (Metaseiulus occidentalis)

Table II. Selected examples of multiple cropping systems that effectively prevent insect-pest outbreaks (based on Altieri et al., 1978; Altieri and Letourneau, 1982; Andow 1991 ). Multiple cropping system Beans grown in relay intercropping with winter wheat Brassica crops and beans Brussels sprouts intercropped with fava beans and/or mustard Cabbage intercropped with white and red clover Intercropping of Cajanus cajan with red, black and green gram Cassava intercropped with cowpeas

Pest(s) regulated

Empoasca fabae and Aphis fabae Brevicoryne brassicae and Delia brassicae

Factor(s) involved Impairment of visual searching behavior of dispersing aphids Higher predation and disruption of oviposition behavior Reduced plant apparency trap cropping, enhanced biological control

Flea beetle Phyllotreta crucifecae and cabbage aphid Brevicoryne brassicae Erioischia brassicae, cabbage aphids, and imported cabbage butterfly (Pieris rapae) Podborers, jassids and membracids

Delayed colonization of herbivores

Whiteflies Aleurotrachelus socialis and Trialeurodes variabilis

Changes in plant vigor and increased abundance of natural enemies

Interference with colonization and increase of ground beetles

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M. A. Altieri

Table II. (continued) Multiple cropping system

Pest(s) regulated

Factor(s) involved

Cauliflower strip-cropped with rape and/or marigold Corn intercropped with beans

Blossom beetle Meligethes

Trap cropping

Leafhoppers (Empoasca kraemen~ leaf beetle (Diabrotica balteata) and fall armyworm

Increase in beneficial insects and interference with colonization

Corn intercropped with fava beans and squash Corn intercropped with clover Corn intercropped with soybean Corn intercropped with sweet potatoes

Aphids, Tetranychus urticae and Macrodactylus sp.

Enhanced abundance of predators ?

European corn borer

Differences in corn varietal resistance Increase in parasitic wasps

Intercropping corn and beans Cotton intercropped with forage cowpea Intercropping cotton with sorghum or maize Cotton intercropped with okra Strip cropping of cotton and alfalfa

Strip cropping of cotton and alfalfa on one side and maize and soybean on the other Intercropping cowpea and sorghum Cucumbers intercropped with maize and broccoli Groundnuts intercropped with field beans Maize intercropped with canavalia Maize-bean intercropping Strip cropping of muskmelons with wheat Oats intercropped with field beans Peaches intercropped with strawberries

aeneus

(Spodoptera frugiperda)

Ostrinia nubilalis

Ostrinia nubilalis Leaf beetles (Diabrotica

spp.) and leafhoppers

(Ag aIlia lingula ) Dalbulus maidis

Boll weevil (Anthonomus

grandis)

Corn earworm (Heliothis

zea) Podagrica sp.

Interference with leafhopper movement Population increase of parasitic wasps (Eurytoma sp.) Increased abundance of predators Trap cropping

Corn earworm (Heliothis zea) and cabbage looper

Prevention of emigration and synchrony in the relationship between pests and natural enemies Increased abundance of predators

Leaf beetle (Oetheca

Interference of air currents

Plant bugs (Lygus hesperus + and L. elisus)

( Trichoplusia n/~

bennigsenl~ Acalymma vittatta Aphis craccivora

Prorachia daria and fall armyworm (Spodoptera frugiperda) Spodoptera frugiperda and Diatraea lineolata Myzus persicae Rophalosiphum padi Strawberry leafroller

(Ancylis comptana) Oriental fruit moth

(Grapholita molesta)

Interference with movement and tenure time on host plants Aphids trapped on epidermal hairs of beans Not reported Lower oviposition rates, trap cropping Interference with aphid dispersal Interference with secondary dispersal after alighting on the crop Population increase of parasites (Macrocentrus

ancylivora, Microbracon gelechise and Lixophaga variabilis)

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201

Table II. (continued) Multiple cropping system Peanut intercropped with maize Sesame intercropped with corn or sorghum Sesame intercropped with cotton Soybean strip cropped with snap beans Squash intercropped with maize

Tomato and tobacco intercropped with cabbage Tomato intercropped with cabbage 9, L

,

,,,,,

,,,'

Pest(s) regulated

Factor(s) involved

Corn borer (Ostrinia furnacalis) Webworms (Antigostra sp.)

Abundance of spiders (L ycosa sp.) Shading by the taller companion crop Increase of beneficial insects and trap cropping Trap cropping

Heliothis spp. Epilachna varivestis

Flea beetles (Phyllotreta cruciferae)

Increased dispersion due to avoidance of host plants shaded by maize and interference with flight movements by maize stalks Feeding inhibition by odors from non-host plants

Diamondback moth (Plutella xylostella)

Chemical repellency or masking

Acalymma thiemei, Diabrotica balteata

'

"

'"'

"

,,

,,,,,

,,

,,

environmental manipulations depends upon their degree of association with one or more of the vegetational components of the system. Extension of the cropping period, or planning temporal or spatial cropping sequences may allow naturally occurring biological control agents to sustain higher population levels on alternate host or prey and to persist in the agricultural environment throughout the year. Since farming systems in a region are managed over a range of energy inputs, levels of crop diversity and successional stages, variations in insect dynamics are likely to occur and may be difficult to predict. However, based on current ecological and agronomic theory, low pest potentials may be expected in agroecosystems that exhibit the following characteristics (Litsinger and Moody, 1976; Huffaker and Messenger, 1976; Perrin, 1977, 1980; Altieri and Letourneau, 1982; Andow, 1991): 1. High crop diversity through mixtures in time and space. 2. Discontinuity of monoculture in time through rotations, use of short maturing varieties, use of crop-free or preferred host-free periods, etc. 3. Small, scattered fields creating a structural mosaic of adjoining crops, and uncultivated land which potentially provides shelter and alternative food for natural enemies. Pests also may proliferate in these environments depending on plant species composition, however, the presence of low levels of pest populations and/or alternate hosts may be necessary to maintain natural enemies in the area. 4. Farms with a dominant perennial crop component. Orchards are considered to be semi-permanent ecosystems, and more stable than annual crop systems. Since orchards suffer less disturbance and are characterized by greater structural diversity, possibilities for the establishment of biological control agents are generally higher, especially if floral undergrowth diversity is encouraged.

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5. High crop densities or presence of tolerable levels of weed background. 6. High genetic diversity resulting from the use of variety mixtures or multilines of the same crop. These generalizations can serve in the planning of a vegetation management strategy in agroecosystems; however, they must take into account local variations in climate, geography, crops, local vegetation, inputs, pest complexes, etc., which might increase or decrease the potential for pest development under some vegetation management conditions. The selection of component plant species can also be critical. Systematic studies on the 'quality' of plant diversification with respect to the abundance and efficiency of natural enemies are needed. As pointed out by Southwood and Way (1970), what seems to matter is 'functional' diversity and not diversity per se. Mechanistic studies to determine the underlying elements of plant mixtures that disrupt pest invasion and that favor colonization and population growth of natural enemies will allow more precise planning of cropping schemes and increase the chances of a beneficial effect beyond the current levels.

IV. ENHANCING NATURAL ENEMY BIODIVERSITY IN AGROECOSYSTEMS: THE CASE OF PARASITIC HYMENOPTERA There are several environmental factors that influence the diversity, abundance and activity of parasitoids in agroecosystems" microclimatic conditions, availability of food (water, hosts, pollen and nectar), habitat requirements (refuges, nesting and reproduction sites, etc.), intra- and interspecific competition and other organisms (hyperparasites, predators, humans, etc.). The effect of each of these factors will vary according to the spatial and temporary arrangement of crops and the intensity of crop management. Since agroecosystems are dynamic and subjected to different kinds of management, crop mixes continually change in the face of biological and socioeconomic factors. Such landscape variations determine the degree of spatial and temporal heterogeneity characteristic of agroecosystems, which, in turn, may or may not benefit parasitic Hymenoptera diversity in specific cropping systems. Although parasitoids seem to vary widely in their response to crop distribution, density and dispersion, experimental evidence suggests that structural (i.e. spatial and temporal crop arrangement) and management (i.e. crop diversity, input levels, etc.) attributes of agroecosystems influence parasitoid diversity and dynamics. Based on the available information, parasitoid biodiversity can be enhanced and effectiveness improved in the following ways (van den Bosch and Telford, 1964; Wilson, 1966; Rabb etal., 1976; Carroll, 1978; Altieri and Letourneau, 1982; Powell, 1986).

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A. Multiple Introductions of Parasitoids Importation of parasitoids has been used since 1906 as a strategy to reach longterm suppression of pests. The practice of classical biological control could be regarded as a global experiment in restoring natural enemy biodiversity in agroecosystems where exotic insects reach pest status because they have been introduced from a geographic distance without their regulating natural enemies. According to Greathead (1986) there are records of 860 successful establishments of 393 species ofparasitoids against some 274 pest insects in 99 countries. In many of these cases, introduction of some 250 species of hymenopterous parasitoids has been rated as achieving satisfactory pest suppression in either a limited or substantial part of the pest's distribution range. Hymenopterous parasitoids were also aided by introduction of other parasitoid or predator species to achieve a useful reduction in pest numbers (Ehler, 1990). This fact gives support to the multiple-species introduction strategy (MSI) in classical biological control. Longtime practitioners such as Huffaker et al. (1971) have already argued in favor of MSI and have stated that 'importation of a diverse complex of natural enemies is the only practical manner of obtaining the best species for a given habitat, or the best combination for such habitat, or the best combination for the entire host range'. Clearly, enhancing or restoring natural enemy biodiversity through importation assures a better chance of success than single species introduction; the challenge is determining which species or combination of species to introduce in order to control a given target species in a specific situation (Ehler, 1990).

B. Reducing Direct Mortality by Eliminating Pesticides The use of chemical pesticides has often created complex and serious problems by immediate and time-lag effects on natural enemies. Non-selective insecticides have created pest problems by eliminating parasitoids. D D T and parathion have been particularly deleterious to various parasitoids in several agroecosystems. Organophosphorus insecticides such as azinphosmethyl, parathion, diazinon, dimethoate and malathion are particularly toxic to hymenopterous parasites of citrus scales and mealybugs. Total removal of pesticides can restore parasitoid diversity and lead to renewed biological control of specific pests. Within 2 years, virtually all banana insect pests in Golfito, Costa Rica dropped to below economic threshold levels, due to enhanced parasitization and predation, after stopping insecticide (dieldrin and carbaryl) sprays (Stephens, 1984). Similarly, in California's walnut orchards, natural biological control of the frosted scale and the calico scale was soon achieved by encyrtid parasitoids after removal of D D T sprays (Hagen et al., 1971).

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C. Provision of Supplementary Resources Most parasitoids have resource requirements such as hosts, food other than hosts, water, refuges, etc., which often are not available or found in sufficiency within a given cropping system. Several researchers have demonstrated that manipulating such resources can enhance parasitoid diversity and abundance and also improve their efficacy (Rabb ttal., 1976). Addition of host populations proved effective in controlling Pieris rapae in cabbage. The continuous release of fertile P/ms eggs increased the pest population nearly ten-fold above normal spring populations, enabling the parasites Trichogramma evanescens Westwood and Cotesia rubecula (Marshall) to increase early and maintain themselves at an effective level throughout the season (Parker and Pinnell, 1972).

D. Increasing Adjacent Vegetational Diversity Researchers are well aware of the importance of adjacent vegetational settings in determining the diversity of parasitoid species as well as their maintenance and effectiveness within agroecosystems (van den Bosch and Telford, 1964; Alteri and Todd, 1981; Altieri and Letourneau, 1982, 1984). Successful colonization by parasites depends upon the presence of the appropriate kind and abundance of primary hosts, alternative hosts, pollen and/or nectar in hedgerows and other neighboring habitats. For example, in Armenia, scelionid egg parasites of the sun pest Eu~ygaster integriceps Puton are very efficient in areas with small wheat fields surrounded by diverse vegetation. Under these conditions, the polyvoltine egg parasites have a number of other pentatomid hosts and favorable hibernating places. In California, Doutt and Nakata (1973) found that the egg parasite Anagrus epos Girault, was effective in controlling the grape leafhopper E(ythroneura elegantula Osborn, in vineyards adjacent to wild blackberries which harbor a non-economic leafhopper, Dikrella cruentata Gillette, whose eggs serve as the only overwintering resources for Anagrus. Also in California, Allen and Smith (1958) found that parasitization of the alfalfa caterpillar, Colias eutytheme, by Apanteles medicaginis was far greater in California's San Joaquin Valley where weeds were in bloom along irrigation canals in contrast to areas where the weeds were destroyed. In England, the proximity of certain flowering weeds increased the activity of parasitic Hymenoptera in wheat and cabbage fields (van Emden and Williams, 1974).

E. Increasing Within-field Plant Diversity Considerable plants within increase their showed that

work in the USSR has been devoted to the use of nectar-bearing orchards as a source of adult food for entomophagous insects to effectiveness. Field experiments conducted in the North Caucasus the growing of Phacdia spp. in orchards greatly increased the

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parasitization of Quadraspidiotus perniciosus (Comstock) by its parasite Aphytis proclia (Walker). These same plants have been shown to increase the abundance of the wasp Aphelinus mali for the control of apple aphids and improve the activity of Trichogramma spp. in apple orchards (Chumakova, 1977).

F. Manipulating Host-plant Attributes Several chemical, genetic and architectural attributes of plants can influence parasitoid action on insect pests. Rabb and Bradley (1968) found that parasitization of Manduca sexta (L.) eggs by Trichogramma minutum Riley and Telenomus sphingis (Ashmead) was inhibited by sticky exudates of tobacco leaves. Encarsia formosa Gahan, a normally effective parasitoid of the greenhouse whitefly, is greatly hindered by the hairs produced by cucumber (Price et al., 1980). It is also known that the nature of the host-plant habitat affects the degree of parasitization obtained from certain parasitoids. In northern Florida, parasitization rates of Heliothis spp. and plusiinae eggs by Trichogramma pretiosum Riley showed considerable variation in various crops grown in the same field (Martin et al., 1976). Moderate to high rates of parasitization were attained in tomatoes, collards and okra. The released parasites were ineffective against the target pests in tobacco. Although these differences could have been due to differences in host egg densities, various chemical and physical cues emitted by the different crops were significant in affecting the location of the host habitat by Trichogramma wasps. Similar results were obtained in New York state where parasitism by DiaeretieUa rapae was much higher when the aphid Myzus persicae (Sulzer) was on collard than when it was on beet (Read etal., 1970).

G. Manipulations with Semiochemicals Chemicals that stimulate host-searching behavior in parasitoids have been identified for a number of Hymenoptera species: Cardiochiles niciriceps, Trichogramma evanescens, T. pretiosum, Trissolcus sp., Telenomus sp., Microplitis croceips and Aphidius nigripes (Nordlund et al., 1981). Hexane extracts sprayed in field trials have consistently improved parasitization rates of H. zea eggs by T. pretiosum. The greatest utility of such kairomonal applications appears to be for aggregating or retaining released parasites in target locations (Lewis and Nordlund, 1985). Taking advantage of the fact that many parasitoids seek out particular habitats and are guided by volatiles emanating from plants, some researchers have applied certain plant extracts on crop plants to reinforce the host location behavior of parasitoids and have improved parasitization rates (Altieri et al., 1981). Spraying of plant-produced synomones attracted ovipositioning female parasitoids, enhancing the parasitization of H. zea and Anagasta kuehnieUa (Zeller) by Trichogramma wasps under soyabean field and greenhouse conditions respectively

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(Altieri et al., 1981; Altieri and Letourneau, 1982). Similar results were obtained by Titayavan and Altieri (1990) in broccoli plots. Direct application of an allylisothiocyanate emulsion at a rate of 0.25 ml per broccoli plant consistently gave higher parasitization rates of the cabbage aphid and/or number ofDiaeretiella rapae wasps per plant, than those observed on plants treated with 0.25 ml of water or with 0.25 ml of wild mustard extract. V. CONCLUSIONS Agroecosystems are complex and dynamic systems subjected to a whole range of vegetational designs and management intensities depending on farmers' preferences, environmental factors and socioeconomic constraints. Changes in plant diversity, plant density, crop dispersion and patch size will increase or reduce resources for natural enemies. Therefore, the size and structure of natural enemy communities should be expected to vary according to the biodiversity and heterogeneity of specific agroecosystems. When considering ways of enhancing natural enemy diversity and efficiency, what is difficult is that each agricultural situation must be assessed separately. Diversified vegetational settings will generally result in enhanced diversity and abundance of predators and parasitoids, although specifically which species will be enhanced will vary depending on the diversity and availability of primary and alternative host preys, location and size of the field, plant composition, floral diversity and phenology, surrounding environments and management technologies. One can only hope to elucidate the basic ecology of natural enemies, their relationships with other components of the agroecosystem and the ecological principles governing natural enemy biodiversity in crop fields. In this regard, manipulating agroecosystem components (habitat diversity, pesticide-free space, alternate food, semiochemicals, etc.) to provide the basic requirements needed by parasitoids and predators (hosts and prey, pollen and nectar, refuges, reproduction and nesting sites, etc.) is an effective way to apply ecological theory to improve biological control in agroecosystems. REFERENCES Allen, W. W. and Smith, R. F. (1958). Some factors influencing the efficiency of Apanteles medicaginis Muesebeck (Hymenoptera: Braconidae) as a parasite of the alfalfa caterpillar Colias eu~ytheme Boisduval. Hilgardia 28, 1-42. Altieri, M.A. (1987). 'Agroecology: the Scientific Basis of Alternative Agriculture. Westview Press, Boulder, CO. Altieri, M.A. and Letourneau, D. K. (1982). Vegetation management and biological control in agroecosystems. Crop Protection 1,405-1430. Altieri, M.A. and Letourneau, D.K. (1984). Vegetation diversity and insect pest outbreaks. CRC Critical Reviews in Plant Sciences 2, 131-169.

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Altieri, M. A. and Schmidt, L. L. (1985). Cover crop manipulation in northern California orchards and vineyards: effects on arthropod communities. Biological Agriculture and

Horticulturer 3, 1- 24. Altieri, M. A. and Todd, J. W. (1981). Some influences of vegetational diversity on insect communities of Georgia soybean fields. Protection Ecology 3,333-338. Altieri, M.A. and Whitcomb, W. H. (1979). The potential use of weeds in the manipulation of beneficial insects. Hortscience 14, 12-18. Altieri, M. A., van Schoonhoven, A. and Doll J. D. (1977). The ecological role of weeds in insect pest management systems: A review illustrated with bean (Phaseolus vulgaris L.) cropping systems. PANS 23, 195-205. Altieri, M. A., Francis, C. A., van Schoonhoven, A. and Doll, J. (1978). A review of insect prevalence in maize (Zea mays L.) and bean (Phaseolus vulgaris L.) polycultural systems. Field Crops Research 1, 33-49. Altieri, M. A., Lewis, W.J., Nordlund, D. A., Gueldner, R. C. and Todd, J. W. (1981). Chemical interactions between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259-263. Andow, D. A. (1991). Vegetational diversity and arthropod population response. Annual Review of Entomology 36, 561-586. Andow, D. A. and Prokrym, D. R. (1990). Plant structural complexity and host finding by a parasitoid. Oecologia 62, 162-165. Andow, D. and Risch, S.J. (1985). Predation in diversified agroecosystems: relations between a coccinellid predator Coleomegilla maculata and its food. Journal of Applied Ecology 22, 357-372. Beingolea, O. (1957) 'El Sembrio del Maiz y la Fauna Benefica del Algodonero'. Estacion Experimental Agricola, La Molina, Lima. Carroll, C. R. (1978). Beetles, parasitoids and tropical morning glories: a study in host discrimination. Ecological Entomology 3, 79-85. Chumakova, B. M. (1977). Ecological principles associated with augmentation of natural enemies. In 'Biological Control by Augmentation of Natural Enemies' (R. L. Ridgway and S. B. Vinson, eds), pp. 39-78. Plenum, NY. Doutt, R. L. and Nakata,J. (1973). The Rubus leaflaopper and its egg parasitoid: an endemic biotic system useful in grape-pest management. Environmental Entomology 2, 381-386. Ehler, L. E. (1990). Introduction strategies in biological control of insects. In 'Critical Issues in Biological Control' (M. Mackauer, L.E. Ehler and J. Roland, eds), pp. 111-134. Intercept, Andover, UK. Flint, M. L. and Roberts, P. A. (1988). Using crop diversity to manage pest problems: some California examples. American Journal of Alternative Agriculture 3, 164-167. Greathead, D.J. (1986). Parasitoids in classical biological control. In 'Insect Parasitoids' (J. Waage and D. Greathead, eds), pp. 290-318. Academic Press, London. Hagen, K.S., van den Bosch, R., and Dahlsten, D.L. (1971). The importance of naturally-occurring biological control in the Western United States. In 'Biological Control' (C. B. Huffaker, ed.), pp. 253-287. Plenum, NY. Helenius, J. (1989). The influence of mixed intercropping of oats with field beans and on the abundance of and spatial distribution of cereal aphids (Homoptera: Aphididae). Agricultural Ecosystems and the Environment 25, 53-73. Huffaker, C. B. and Messenger, P. S. (eds). (1976). 'Theory and Practice of Biological Control'. Academic Press, New York. Huffaker, C. B., Messenger, P. S. and DeBach, P. (1971). The natural enemy component in natural enemy control and the theory of biological control. In 'Biological Control' (C. B. Huffaker, ed.), pp. 16-67. Plenum, NY. Leius, K. (1967). Influence of wild flowers on parasitism of tent caterpillar and codling moth. Canadian Entomologist 99, 444-446.

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Letourneau, D. K. (1987). The enemies hypothesis: tritrophic interaction and vegetational diversity in tropical agroecosystems. Ecolog? 68, 1616-1622. Litsinger, J. A. and Moody, K. (1976). Integrated pest management in multiple cropping systems. In 'Multiple Cropping Systems' (P. A. Sanchez, ed.), pp. 293-316. ASA Publication 27. Madison, Wisconsin. Lewis, W.J. and Nordlund, D.A. (1985). Behavior-modifying chemicals to enhance natural enemy effectiveness. In 'Biological Control in Agricultural Integrated Pest Management Systems' (M. A. Hoy and D. C. Herzog, eds), pp. 89-101. Academic Press, NY. Martin, P. B., Lingren, P. D., Greene, G. L. and Ridgway, R. L. (1976). Parasitization of two species of Plusiinae and Heliothis spp. after releases of Trichogramma pretiosum in seven crops. Environmental Entomology 5, 991-995. Nordlund, D. A., Lewis, W.J. and Gross, H. R. (1981). Elucidation and employment of semiochemicals in the manipulation of entomophagous insects. In 'Management of Insect Pests with Semiochemicals Concepts and Practice' (E. R. Mitchell, ed.), pp. 463-475. Plenum, NY. Parker, F.D. and Pinnell, R.E. (1972). Further studies of the biological control of Pieris rapae using supplemental host and parasite releases. Environmental Entomology 1, 150-157. Perrin, R. M. (1977). Pest management in multiple cropping systems. Agro-Ecosystems 3, 93-118. Perrin, R. M. (1980). The role of environmental diversity in crop protection. Protection Ecology 2, 77-114. Powell, W. (1986). Enhancing parasitoid activity in crops. In 'Insect Parasitoids' (J. Waage and D. Greathead, eds), pp. 319-335. Academic Press, London. Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N. and Weis, A.E. (1980). Interactions among three trophic levels. Annual Review of Ecology and Systematics 11, 41-65. Rabb, R. L. and Bradley, J. R. Jr. (1968). The influence of host plants on parsitism of eggs of the tobacco hornworrn. Journal of Economic Entomology 61, 1249-1252. Rabb, R. L., Stinner, R. E. and van den Bosch, R. (1976). Conservation and augmentation of natural enemies. In 'Theory and Practice of Biological Control' (C. B. Huffaker and P. Messenger, eds), pp. 233-254. Academic Press, New York. Read, D. P., Feeny, P. P. and Root, R. B. (1970). Habitat selection by the aphid parasite Diaretiella rapae (Hymnenoptera: Braconidae) and hyperparasite Charips brassica (Hymenoptera: Cynipidae). Canadian Entomologist 102, 1567-1578. Risch, S. J. (1981). Insect herbivore abundance in tropical monocultures and polycultures. An experimental test of two hypotheses. Ecology 62, 1325-1340. Root, R. B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monographs 43, 95-124. Russell, E. P. (1989). Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environmental Entomology 18, 590-599. Sheehan, W. (1985). Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environmental Entomology 15,456-461. Southwood, T. R. E., and Way, M . J . (1970). Ecological background to pest management. In 'Concepts of Pest management' (R. L. Rabb and F.E. Guthrie, eds), pp. 6-29. North Carolina State University, Raleigh, NC. Stephens, C. S. (1934). Ecological upset and recuperation of natural control of insect pests in some Costa R ican banana plantations. Turrialba 34, 101-105. Titayavan, M. and Altieri, M. A. (1990). Synomone-mediated interactions between the parasitoid Diaeretiella rapae and Brevicoryne brassicaunder field conditions. Entomophaga 35, 499-507.

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Tumbull, A. L. (1969). The ecological role of pest populations. Proceedings of the Tall Timbers Conference on Ecological Animal Control by Habitat Management 1, 219-232. van den Bosch, R. and Telford, A. D. (1964). Environmental modification and biological control. In 'Biological Control of Insect Pests and Weeds' (P. DeBach, ed.), pp. 459-488. Chapman & Hall, London. van Emden, H. F. (1965). The role of uncultivated land in the biology of crop pests and beneficial insects. Scientific Horticulture 17, 121-136. van Emden H. F. and Williams, G . F . (1974). Insect stability and diversity in agroecosystems. Annual Review of Entomolog7 19, 455-475. Wainhouse, D. and Coaker, T. H. (1981). The distribution of carrot fly (Psila rosae) in relation to the fauna of field boundaries. In 'Pests, Pathogens and Vegetation: The Role of Weeds and Wild Plants in the Ecology of Crop Pests and Diseases' (J. H. Thresh, ed.), pp. 263-272. Pitman, MA. Wilson, F. (1966). The conservation and augmentation of natural enemies. Proceedings of the Food and Agriculture Organization Symposium on Integrated Pest Control 3, 21-26. Young, W. R. and Teetes, G. L. (1977). Sorghum entomology. Annual Review of Entomology 72, 193-218.

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11 PLANT PROTECTION USING NATURAL DEFENCE SYSTEMS OF PLANTS B.J. Deverall Department of Crop Sciences, University of Sydney, N S W 2006, Australia

I. Introduction II. Evidence from Laboratory TriMs A. Using Pathogens as Inducers B. Using Chemicals as Inducers III. Evidence from Field TriMs IV. Prospects for Sustainable Use Acknowledgements References

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I. I N T R O D U C T I O N The idea of inducing plants to use their natural defence systems at threatening times for disease development is attractive. It suggests the prospect of alternatives or supplements to present methods of plant protection in forestry, agriculture and horticulture. These present methods are largely the planting of resistant cultivars or the application of control agents. Resistant cultivars are produced by plant breeding after selection of recognitional genes for countering harmful strains of pathogens. Control agents are mainly fungicides developed in the chemical industry. Concerns about depleting genetic resources, evolution of new strains of pathogens and use of fungicides encourage exploration for other methods. There is a worldwide mission to use 'integrated pest and disease management' in plant protection. This means the selection and use of as many procedures as possible for minimizing loss caused by pests and diseases in a balanced way. A desirable component of such management would be manipulation of the active defence systems in plants. This review is about current ability and prospects in activating defence systems in plants with effective control of disease in mind. It focuses mainly on the induction of systemic resistance in plants. This means the heightening of resistance throughout a plant after an earlier localized inoculation with a pathogen or attenuated pathogen, or after treatment of the plant with a chemical agent that is not itself a fungicide, bactericide or viricide. Resistance can be ADVANCES IN PLANT PATHOLOGY--VOL. 11 Copyright 9 1995 Academic Press Limited ISBN 0-12-033711-8 All rights of reproduaion in any form reserved

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induced close to the point of the earlier treatment or throughout a plant (i.e. systemically) (Sequeira, 1983). Systemic induced resistance seems more likely to be useful in plant protection and is therefore my preferred major theme. Many potential defence systems can be activated in plants by inoculation and infection. These systems include the formation of structures such as cell wall depositions (e.g. silicon, callose, lignin and suberin) and new cellular structures (e.g. tyloses) and layers (e.g. periderm) (Aist, 1983), the synthesis of antimicrobial substances (e.g. phytoalexins) (Barley and Mansfield, 1982) and the production of pathogenesis-related proteins amongst which are glucanases and chitinases active on fungal cell walls (Linthorst, 1991). Systemic induced resistance may involve the particularly rapid reactivation of some or all of these systems in response to a second or challenge inoculation. It also involves the production and movement of signals from the site of the first or inducing inoculation. These signals either activate one or several of the defence systems directly or, in a largely unknown way, render remote cells sensitive to challenge so that they respond more rapidly than normal in producing defences to the challenge (Hammerschmidt and Ku~, 1995). This review does not deal in depth with the processes of induced resistance, but rather with the extent and strength of evidence for contributions of the processes to plant protection. Many earlier reviews describe the history and extent of development of knowledge of systemic induced resistance up to their respective dates (Chester, 1933; Goodman, 1978; Matta, 1980; Suzuki, 1980; Ku~., 1983, 1990; Sequeira, 1983). A comprehensive book on induced resistance to disease in plants is about to be published (Hammerschmidt and Ku~, 1995). This present review starts with evidence for effective disease control in laboratory and glasshouse/ growth room experiments, firstly using pathogens or other micro-organisms and secondly using chemical agents as inducers. It then deals with extents and duration of control in field trials that are directed towards commercial practice. Based on this evidence, prospects for application are evaluated.

II. EVIDENCE FROM LABORATORY TRIALS A. Using Pathogens as Inducers Substantial increases in resistance were brought about in a range of economically important plants (from legumes to grasses) by earlier inoculations with particular viruses, bacteria and fungi (Table II). The resistance was appreciable but never complete in these growth room and glasshouse tests. The persistence of the induced resistance was usually confirmed for periods up to 7 days, but in some cases for much longer. The resistance was usually manifest as a decrease in numbers of sites of infection in challenged plant parts and in a decrease in disease development at each of these sites. Most tests were done on leaves that emerged immediately above a first-inoculated leaf, but some were done with root systems

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revealing induction of resistance towards vascular wilt diseases caused by forms of Fusarium oxysporurn. Resisted foliar pathogens were of many types ranging from some viruses, lower fungi, including the potato blight pathogen and a downy mildew fungus, to representatives of the higher fungi such as powdery mildew and rust fungi. The results suggest that useful resistance should be capable of being brought about in many types of plants against many pathogens by these means. Effective inducing organisms tested were mainly plant pathogens, often those that caused local lesions. Most of the earlier work (Ross, 1961; Ku6, 1983) suggested that cellular incompatibility between inducer and host was a key factor in leading first to cellular disruption and then local lesion formation. As a consequence, systemic signals were thought to be released from the disrupted cells to the rest of the plant. The recent evidence in Table I that a rust fungus in broad bean and an endophytic fungus in tomato induced systemic resistance questions the idea that limited disruption of host cells is always an essential first step. From general understanding of their infection processes, both of these fungi would be expected to develop compatibly with the plant cells and not to cause local damage, at least until a much later stage in development. If close examination of the infections by the rust fungus and the endophyte confirms cellular compatibility with host cells during the inducing phase, then some new vistas of the activating steps in biologically induced resistance will be opened. The work with the endophyte also indicates prospects of choosing micro-organisms that are not pathogens for the special purpose of systemically bringing about induced resistance. Particularly interesting work on induction by a micro-organism is that of Smith et al. (1991) who found a highly effective strain of the bacterium Pseudomonas syringae pv. syringae that induced resistance in the next leaves of cucumber within the unusually short time of 1 day. By removing the first leaves at increasingly brief intervals after inoculation with the strain, it was deduced that a signal passed to the next leaves 6 h after inoculation. The signal was sent before the inducing bacterium caused cell death and hypersensitivity in the first leaf. A mutant of the bacterium that did not cause hypersensitivity failed to induce systemic resistance. Transformation of the mutant with a cosmid bearing a genetic sequence from the original strain restored the capacity to cause both hypersensitivity and systemic induced resistance. This work emphasizes the usual understanding that the inducing organism needs to have potential to cause limited cell death in the plant. It also indicates prospects for selecting micro-organisms with high ability for inducing resistance. Further work on inducing systemic resistance with a strain of P. syringae pv. syringae, but in this case in rice (Smith and M6traux, 1991), needs special emphasis for the way in which the resistance is brought about. No widespread enhancement of enzyme activities, including glucanases and chitinases, could be detected, in contrast to the prechallenge situation where resistance was induced systemically in tobacco (Pan et al., 1991) and some other plants. The rice work

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Stem

TMV

Leaves 1 t o 3 Leaves 2 t o 6

Tomato

Endophyte Acrernoniurn kiliense

Ph ytophthora infestans

Fusariurn oxysporurn f .sp. dianthi

Transplant into inoculated peat soil

First t w o leaves

Peronospora tabacina

Leaves 5-10

TMV and some other viruses Phytophthora parasitica var . nicotianae

Leaves 4 and 5

Fusariurn ox ysporurn f .sp. lycopersici Clavibacter rnichiganense Phytophthora infestans

Fusariurn oxysporurn f .sp. cucurnerinurn Fusariurn ox ysporurn f .sp. niveurn (avir.)

Pan etal.

High

To 21 days

Ross (1961)

Leaves 8 and 9

25-fold

25 days

Transplant t o infested soil Poured into soil

7-fold

7 days

c 50%

3 days t o

Mclntyre and Dodds ( 1 979) Mclntyre and Dodds ( 1 979) Bargmann and Schonbeck

20%

Leaves 3-6

Number down from 90 t o 68 Dry lesions down from 78 t o 15 80% decrease in necrosis

Fourth leaf

One half of split Fusariurn root system oxysporurn immersed for f .sp. lycopersici 10 min in l o 7 conidia m l -

Other half of Delay in root system symptom immersed for development 10 min in 1 o6 and less conidia ml-' disease 1 week later Leaves 2 and 3 c 50%

Roots dipped

Colletotrichurn lagenariurn Fusariurn oxysporurn f .sp. niveurn (vir.)

weeks

Root dipped

40-81 % less wilt

(1991)

( 1 992)

7 days t o

Bargmann and Schonbeck

10 days

Heller and Gessler

weeks

First three leaves

'

Watermelon

At least 21 days

Leaf area with lesions down from 90 t o

(1992) ( 1 986)

7 days tested

Christ and Mosinger

To 24 days after challenge

Kroon et al.

5 days

Biles and Martyn

40 days

Biles and Martyn

( 1 989)

(1991)

( 1 989) ( 1 989)

216

B. J. Deverall

leaves open the possibility that induced resistance can result from a heightened sensitivity to challenge as distinct from, or in addition to, an increased activity of defensive enzymes before challenge.

B. Using Chemicals as Inducers Substantial resistance to some fungal and bacterial pathogens in a few crop species representative of a potentially wide range has been brought about by application of chemical agents (Table II). The earliest of these successes in laboratory and growth room/glasshouse situations were with dichlorocyclopropane (Langcake and Wickens, 1975) and probenazole (Watanabe etal., 1977, 1979) against the blast disease in rice. Later came the report that carboxyalkenyl hydrazinium salts appeared to act systemically in preventing vascular wilt symptoms in tomato (Phillips et al., 1981). The activity of these compounds had become apparent in screening for potential systemic fungicides, coupled with the realization that they were more effective in controlling the disease than in affecting the germination and growth of the fungal pathogen in vitro. As described for many un-named chemical agents tested on rice and wheat in the ICI company (Rathmell, 1984), it is likely that numerous compounds were synthesized and found effective in the chemical industry for countering diseases in growth room and glasshouse trials, and that they may not have been antimicrobial in direct tests on pathogens in the laboratory. In a significant number of these cases, the chemical agents were damaging to plant tissues and Rathmell (1984) speculated that the damage may have been related to their disease-control ability, perhaps through inducing resistance. Partly because of this observed damage (phytotoxicity), but also for reasons of cost and other strategic considerations, companies have been slow in developing and releasing chemical agents of this type as plant protectants (Baldwin and Rathmell, 1988). Until recently there has been little outward sign of the plant protection industry attempting to use chemical agents for bringing about resistance. Omitted from Table II and of questionable relevance to the main theme of this review are the phosphonates, which have been classified as systemic fungicides with good activity against diseases caused by downy mildew fungi and Phytophthora spp. (Cohen and Coffey, 1986). There is evidence that these fungicides affect the fungi directly acting through the conversion product, phosphorous acid. There is also evidence, as discussed by Nemestothy and Guest (1990), that the defence mechanisms of infected plants are enhanced in the presence of these fungicides. Some controversy continues about the direct versus indirect mode of action of the phosphonates in controlling diseases, but it seems to be unlikely that they are working directly on host defence and that they are inducers of resistance in the sense used in this review. Apart from these past products of the chemical industry, interest in researching chemical agents as inducers of systemic resistance has resumed in three ways in recent years.

Plant Protection Using Natural Defence Systems

217

One is through the use of pathogen products that act as, or are related to, elicitors of defence in pathogen-host interactions. This comes the evidence (Table II) that resistance can be induced systemically to Phytophthora infestans in potato by hyphal wall fragments and unsaturated fatty acids. Proteinaceous elicitors of necrosis from several Phytophthora spp. induced resistance, at least locally, to the black shank disease of tobacco (Ricci etal., 1992). There is abundant evidence that many agents including a range of macromolecular products of pathogens will elicit defensive systems in plants, the elicitation of phytoalexin synthesis having been studied most frequently (Darvill and Albersheim, 1984; Ebel, 1986). Glucan elicitors have received most attention because of their high activity and there has been research and development in the plant protection industry inspired by the idea that glucans or a modification of them could be used to activate host defence. Highly active oligomers of both glucans and galacturonic acids have been synthesized as elicitors of phytoalexin synthesis (e.g. Hong and Ogawa, 1990; Nakahara and Ogawa, 1990). It is reasonable to expect that systemically mobile forms of such elicitors can be made and developed. No reports of their successful use in inducing resistance systemically have been found for inclusion in Table II. In most pathogen-plant interactions, phytoalexin formation is known only as a localized event and neither the natural elicitors nor the elicited phytoalexins have been shown to move from the site of the interactions. Some difficulty might be experienced in using these processes for plant protection, unless the active agents also affect systemic mechanisms as may be the case for the successful examples cited above for potato and tobacco plants. A second way is through the investigation of components of plants believed to be beneficial in controlling disease. For example, natural extracts of some plants, such as oxalate, have also been shown to cause systemic resistance in cucumber (Table II). A third way is through investigating the activity of chemical agents (Table II) that are not likely to be products of pathogens or plants. This has brought evidence that tripotassium phosphate will induce systemic resistance in broad bean and cucumber, as will EDTA in broad bean. A more deliberate examination of compounds produced in the chemical industry for capacity to induce resistance has led, for example, to interesting work with dichloro-isonicotinic acid, formulated for experimentation by Ciba-Geigy as CGA 41396. Following demonstrations of its effectiveness against some fungal pathogens in cucumber and tobacco (Ahl Goy etal., 1990; M6traux etal., 1990), further work showed CGA 41396 to induce resistance also to a bacterial pathogen in cucumber and to fungal and bacterial pathogens in beans (Table II). M6traux et al. (1991) also showed that dichloro-isonicotinic acid moved very rapidly from the point of application on the first leaf of cucumber to the young leaves, growing point and roots. It increased the activities of chitinase and glucanase in both the first leaf and the younger leaves of cucumber before they were challengeinoculated. At the present state of understanding, dichloro-isonicotinic acid

Table /I. Systemic resistance induced by chemical compounds in laboratory trials. Induction Plant species

Agent

Challenge Site

Beans Dichloroisonicotinic acid

First leaf

Broad bean

K3 PO4 or EDTA

Leaves 1 and 2

Cucumber

K3 Po4 Phosphates

Leaves

Oxalate

Leaves 1 and 2

Dichloroisonicotinic acid or its ester

Foliar spray

Dichloroisonicotinic acid or its ester

Organism

Pseudomonas phaseolicola Uromyces viciae-fabae lagenarium

Colletotrichum lagenarium Colletotrichum lagenarium

Soil drench

Soil drench

Site

Extent

Pseudomonas lachrymans

Duration

Reference cited

17 days tested

Colletotrichum lindemuthianum Second leaf Uromyces appendiculatus

I and 2 Colletotrichum

Foliar spray

Protection

12 days tested

Dann (1991) Deverall and Dann (1 995)

> 75%

7 days tested

Leaves 3 and 4

c 25% to > 50%

12 days

Walters and Murray

Leaves 3 and 4

c. 80%

7 days

New leaves above leaf 4 Leaves 3 and 4

85-90%

5 weeks

Gottstein and KuC (1 989)

30-85%

7 days

2 days later at leaf 2 stage

90% at 20 ppm

2 days later at leaf 2 stage 2 days later at leaf 2 stage

90% at 2 ppm

MBtraux et a/.

70% at 20 ppm

MBtraux et al.

2 days later at leaf 2 stage

?

(1992)

Doubrava et a/.

(1 988)

MBtraux et al.

(1 991)

(1991)

(1991)

MBtraux et al.

(1991)

Potato

Rice

Tomato

Wheat

Hyphal wall fragments Unsaturated fatty acids

Leaves 1-3

Dichlorocyclopropane

Soil drench

Probenazole

Soil treatment or drench Root drench

Pyricularia oryzae

Dispersal in sand layer above soil

Fusariurn Root dip ox ysporurn f .sp. lycopersici Soil inoculation

Prevention of vascular symptoms

Puccinia recondita

Variable

Diverse chemical compounds Carboxyalkenyl hydrazinium salts Diverse chemical compounds

Root drench

Phytophthora infestans

Leaves 4- 1 1

Wound inoculation of leaf 4 Leaves

84%

2 0 days

Up t o 100%

5 days, decreased at 12 days t o 18 days from drench

75% decrease in lesion elongation ? Variable

Leaves

Doke eta/. (1987) Cohen et a/. (1991 ) Langcake and Wickens (1975) Watanabe et a/. (1977, 1979) Rathmell ( 1984)

1 4 days

Phillips et a/. (1981)

2 4 days

Phillips et a/. (1981) Rathmell ( 1984)

220

B. J. Deverall

may be regarded as an artificial signal molecule moving rapidly from sites of application and contributing to systemic resistance by heightening the activities of defensive enzymes before challenge. It may be mimicking the action of natural signals, one of which may be salicylic acid, at least in tobacco, where it moves from sites of biological induction (Malamy et al., 1990) enhancing glucanase and chitinase activities in more distant parts of the plant (Yalpani etal., 1991). Chemical induction of resistance can be achieved, therefore, and is at a most promising stage in development for its application in plant protection.

III. EVIDENCE FROM FIELD TRIALS In his comprehensive review of theory and practice to that date, Sequeira (1983) observed that induced resistance was being used only minimally for the control of plant diseases. He referred to the use of lowly virulent strains of T M V to protect tomatoes against virulent strains of the virus in Japan and the Netherlands. He also cited the accidental but effective protection of potatoes against virulent strains of potato virus X as a result of continuous roguing that selected the bestlooking seed potatoes; these seed potatoes would have been infected naturally with mild strains of the virus. He also described the results of a very few field and commercial glasshouse trials on the use of induced resistance against fungal and bacterial diseases. Following the continued success in protecting plants against pathogens using pathogens, other micro-organisms and some chemicals under laboratory conditions (Tables I and II), the results of a limited number of trials in at least semi-commercial situations have been published (see Table III). The relatively early work on tobacco and bean showed significant protection in field trials for several weeks after the stems and first leaves respectively had been inoculated with pathogens. The recent reports on cucumber, grapevines, rice and watermelon describe work that is being targeted to commercial practice. Under the conditions of commercial growing of cucumbers in glasshouses, substantial protection against CoUetotrichum lagenarium was induced by the same pathogen and found to be effective for at least a week, but no protection was provided against the important powdery mildew pathogen (Descalzo etal., 1990). This last result is disappointing because management of the powdery mildew fungus is necessary under glasshouse conditions. Other induction techniques described in the report also failed to induce resistance against the powdery mildew fungus, leaving only the success against CoUetotrichum. Success in minimizing loss of watermelons to vascular wilt disease was achieved by sole reliance on application of an avirulent form of Fusarium oxysporum to root systems before planting them in soil infested with a virulent form of the pathogen (Martyn et al., 1991). Marketable fruit were produced in contrast to the situation where no application was made. Two important diseases of rice, fungal blast and bacterial blight, were con-

Plant Protection Using Natural Defence Systems

221

trolled by application of dichloro-isonicotinic acid or its ester to field water (M~traux et al., 1991). The success of this chemical inducer of resistance is most encouraging because it was demonstrated in comparison with the effects of normally used fungicides and bactericides. Success was also reported for foliar applications of the acid in the field control of important bacterial diseases of pear and pepper and fungal blue mould of tobacco. More detail of these field trials would be welcome and will doubtless become available if the chemical inducer is brought forward for registration for use in plant protection. Commercial vineyards were the sites for trials of induced resistance towards natural infestations of the Pacific spider mite (Karban and English-Loeb, 1990). Major decreases in population build-up of this damaging mite were brought about by limited feeding damage late in the previous season caused by deliberate introductions of the much less damaging Willamette spider mite. These trials followed earlier work by Karban and colleagues showing that feeding damage by mites can induce systemic resistance in grapevines and cotton. This type of work is most encouraging for development of integrated pest and disease management. The skilled manipulation of biological components of orchards, plantations and crops in order to decrease pest and disease problems is a clear goal.

IV. PROSPECTS FOR SUSTAINABLE USE Biological means of activating defence are abundant at the laboratory level and a wide selection of them are effective in labour-intensive and short-term field trials. The extents to which they will be used in sustainable systems depends upon the pressures against current methods and the costs and practicability of the alternatives. Major changes in outlooks and procedures would have to be forced by these pressures before the use of local lesion-causing pathogens could be considered as control procedures for diseases of aerial parts of plants. The use of avirulent strains of pathogens in protection is a more immediate prospect for highly managed situations such as intensive growing where soilborne pathogens require control and in glasshouse crops. Avirulent or mildly damaging strains of pathogens or pests may be considered for use in other highly managed places such as orchards and small plantations, including vineyards. Major advances in research and development are needed before organisms such as endophytes, root symbionts and biological additives to seeds are used for the specialized purpose of plant protection via the induction of defence mechanisms. The use of biological agents would require skilled direction and labour, constant monitoring and other activities that seem to be implicit for the adoption of integrated pest and disease management. Chemical means of inducing resistance throughout plants are available and some of them offer immediate prospects of use in plant protection. Subject to the lack of undesirable side effects on plants and the environment and to costs,

Table Ill. Systemic induced resistance tested in field trials. Induction Plant species

Agent

Challenge Application

Agent

Application

Bean

Colletotrichum lindemuthianum

Leaf 1 dipped in conidial suspension

Colletotrichum lindemuthianum

Plants sprayed to run-off 12 days later

Cucumber

Colletotrichum lagenarium

Droplets to surface of leaf 1 on 2-week-old plants

Colletotrichum lagenarium

Leaf 2 sprayed with inoculum 7 days later. Simulated commercial greenhouse conditions

Sphaerotheca fuliginea

Grapevines

Eotetranychus willamettei (Willamene spider mite)

Leaves with mites placed on vines in November 1987 (autumn)

Whole plants sprayed with spore suspensions 14 days later Tetranychus Natural infestation pacificus (Pacific in 1988 season spider mite)

Effectiveness

Reference cited

Light disease after Sutton (1982) 7 days, extensive disease in controls. Greater survival at 5 weeks and occurrence of flowering and pod-set, in contrast to controls Lesion numbers Descalzo et a/. decreased by (1990) 66% and lesion diameters smaller compared with controls, 7 days after challenge No induced Descalzo et a/. resistance 7, 14 (1990) and 21 days after challenge Nine-fold decrease in challenge populations in early June on treated vines. Acaricide used in late June reducing all mite populations to

Karban and English-Loeb (1 990)

Pear Pepper Rice

Tobacco

Watermelon

Dichloroisonicotinic acid or its ester Dichloroisonicotinic acid Dichloroisonicotinic acid or its ester

25 g hlspray

' foliar

25 g ha-' foliar spray2 kg ha to field water

near zero. Threefold decrease in challenge populations in September on vines first treated in November 1987. > 50% over unstated period

Erwinia amylovora

7

Xanthomonas vesicatoria Pyricularia oryzae

7 7

unstated period > 90% over unstated period

Xanthomonas oryzae

7

> 95% over

Peronospora tabacina

Stem injection 44-60 days after planting out

Peronospora tabacina

Dichloroisonicotinic acid Fusarium oxysporum f.sp. niveum race 1

20 g hl-' foliar spray To root system 3 days before transplant to challengeinfested soil

Peronospora tabacina Fusarium oxysporum f.sp. niveum race 2

Foliar spray 67 davs after pla.nting out

7 Present at 750 cfu g-' in soil receiving transplants

> 80% over

unstated period

MBtraux et al. (1991 ) MBtraux et al. (1991) MBtraux et a/. (1991) MBtraux et al. (1991) Cruickshank and Mandrvk (1960)

Significant decreases in foliar infection at 81 days in plants stem injected at 4 4 and 53 days; greater at 44 days > 50% over MBtraux et al. (1991) unstated period Symptoms Martyn et al. delayed. 35% (1991) fewer plants died compared with controls. Some marketable fruit produced; none in controls

224

B. J. Deverall

dichloro-isonicotinic acid and related compounds are likely candidates to be used as activators of plant defence in plant protection for the reasons summarized in Tables II and III and discussed earlier. Because of the attractiveness of these prospects, a short account of the procedures used in discovering these agents is given in order to present some perspective. Following the convincing demonstration of systemic induced resistance in cucurbits using fungal pathogens (Ku~ et al., 1975), Ciba-Geigy started a policy of triple-screening among some large numbers of new chemical products each year for ability to induce resistance. The first step in the screen is capacity to control selected and common diseases in seedling plants. The effective control agents are then screened for absence of direct effects on selected fungal pathogens in culture on laboratory growth media. The few compounds that emerge from this second screen are tested for their ability to cause the formation of pathogenesis-related proteins in uninfected plants. Dichloro-isonicotinic acid and its methyl ester were two of very few compounds that passed all three screens. They were patented on the basis of these properties, some of which were reported by M~traux et al. (1991). Approximately 8 years elapsed between discovery of their potential and this report and several more are likely to elapse before a decision is made about their registration and use. Related compounds, two chloroisonicotinamides, have been reported to have similar protective properties when tested against the rice blast disease (Yoshida et al., 1990; Seguchi etal., 1992). It can be anticipated that a few other compounds with similar properties are likely to come from Ciba-Geigy and other plant protection companies in the next few years. From this information, it can be seen that a considerable effort is undergone before any chemical agent becomes available for consideration for use in plant protection. When one emerges that has the special ability to induce resistance, it has advantages over biological agents of relative ease of application as a foliar spray or as a soil drench. There is now a very strong possibility of being able to protect a range of plants through their natural defence systems by using such a chemical agent. The protection is likely to be effective against a broad spectrum of pathogens and may be quite long lasting, with a possibility of being extended in duration through a growing season after a second ('boosting') induction. There is also the prospect of being able to return to use some of the older cultivars that had desirable qualities apart form their susceptibility to common diseases. The tecl~nology for using natural defence systems in plant protection is almost ready for use. Research and development on its durability under environmental stresses and on any negative effects for growth, yield and quality are proceeding. The choice of another major procedure for integration into plant protection towards sustainability can then be made.

Plant Protection Using Natural Defence Systems

225

A CKN O WLEDG EM EN TS I thank S . E . C o l e m a n for help in literature searching, V . F . Moschione for word-processing the text and tables and E. K. D a n n for c o m m e n t s on the text.

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International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Interlaken, Switzerland. (abstract) Aist, J. R. (1983). Structural responses as resistance mechanisms. In 'The Dynamics of Host Defence' (J. A. Bailey and B.J. Deverall, eds), pp. 33-70. Academic Press, Sydney. Bailey, J. A. and Mansfield, J. W. (1982). 'Phytoalexins'. Blackie, Glasgow. Baldwin, B. C. and Rathmell, W. G. (1988). Evolution of concepts for chemical control of plant disease. Annual Review of Phytopathology 26, 265-283. Bargmann, C. and Sch/Snbeck, F. (1992). Acremonium kiliense as inducer of resistance to wilt diseases on tomatoes. Journal of Plant Diseases and Protection 99, 266-272. Biles, C. L. and Martyn, R. D. (1989). Local and systemic resistance induced in watermelon by formae speciales of Fusarium oxysporum. Phytopathology 79, 856-860. Chester, K.S. (1933). The problem of acquired physiological immunity in plants. Quarterly Review of Biology 8, 119-154; 275-324. Christ, U. and Mosinger, E. (1989). Pathogenesis-related proteins of tomato: I. Induction by Phytophthora infestans and other biotic and abiotic inducers and correlations with resistance. Physiological and Molecular Plant Pathology 35, 53-65. Cloud, A. M . E . and Deverall, B.J. (1987). Induction and expression of systemic resistance to the anthracnose disease in bean. Plant Pathology 36, 551-557. Cohen, Y. and Coffey, M. D. (1986). Systemic fungicides and the control of Oomycetes. Annual Review of Phytopathology 24, 311-338. Cohen, Y., Gisi, U. and Mosinger, E. (1991). Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids. Physiological and Molecular Plant Pathology 38, 255-263. Cohen, Y., Reuveni, M. and Kenneth, R. (1975). Resistance to powdery mildew in tobacco induced by Peronospora tabacina. Phytopathology 65, 1313-1315. Cruickshank, I. A. M. and Mandryk, M. (1960). The effect of stem infestation of tobacco with Peronospora tabacina Adam. on foliage reaction to blue mold. Journal of the Australian Institute of Agricultural Science 26, 369-372. Dann, E. K. (1991). Studies on inducing systemic resistance in beans and broad beans by biological and chemical means. BSc Agr Thesis, University of Sydney. Darvill, A. G. and Albersheim, P. (1984). Phytoalexins and their elicitors - a defence against microbial infection in plants. Annual Review of Plant Physiology 35, 243-275. Descalzo, R. C., Rahe, J. E. and Mauza, B. (1990). Comparative efficacy of induced resistance for selected diseases of greenhouse cucumber. Canadian Journal of Plant Pathology 12, 16-24. Deverall, B. J. and Dann, E. K. (1995). Induced resistance in legumes. In 'Induced Resistance to Disease' (R. Harnmerschmidt and J. Ku~, eds). Kluwer, Dordrecht, in press. Doke, N., Rarnirez, A. V. and Tomiyama, K. (1987). Systemic induction of resistance in potato plants against Phytophthora infestans by local treatment with hyphal wall fragments of the fungus. Journal of Phytopathology 119, 232-239.

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Doubrava, N. S., Dean, R . A . and Ku6, J. (1988). Induction of sytemic resistance to anthracnose caused by Colletotrichum lagenarium in cucumber by oxalate and extracts from spinach and rhubarb leaves. Physiological and Molecular Plant Pathology 33, 69-79. Ebel, J. (1986). Phytoalexin synthesis: the biochemical analysis of the induction process. Annual Review of Phytopathology 24, 235-264. Goodman, R. N. (1978). Inducible resistance responses in plants to plant pathogenic bacteria. Mycopathologia 65, 107-113. Gottstein, H. D. and Ku~, J. (1989). Induction of systemic resistance to anthracnose in cucumber by phosphates. Phytopathology 79, 176-179. Hammerschmidt, R. and Ku~, J. (1995). 'Induced Resistance to Disease'. Kluwer, Dordrecht, in press. Hecht, E. I. and Bateman, D. F. (1964). Nonspecific acquired resistance to pathogens resulting from localised infections by Thielaviopsis basicola or viruses in tobacco leaves. Phytopathology 54, 523-530. Heller, W . E . and Gessler, C. (1986). Induced systemic resistance in tomato plants against Phytophthora infestans. Journal of Phytopathology 116, 323-328. Hong, N. and Ogawa, T. (1990). Stereocontrolled syntheses of phytoalexin elicitor-active 3-D-glucohexaoside and 13-D-glucononaoside. Tetrahedron Letters 31, 3179-3182. Karban, R. and English-Loeb, G. M. (1990). A 'vaccination' of Willamette spider mites (Acari: Tetranychidae) to prevent large populations of Pacific spider mites on grapevines. Journal of Economic Entomology 83, 2252-2257. Kroon, B. A. M., Scheffer, R . J . and Elgersma, D . M . (1991) Induced resistance in tomato plants against Fusarium wilt invoked by Fusarium oxysporum f.sp. dianthi. Netherlands Journal of Plant Pathology 97, 401-408. Ku~, J. (1983). Induced systemic resistance in plants to diseases caused by fungi and bacteria. In 'The Dynamics of Host Defence' (J. A. Bailey and B.J. Deverall, eds), pp. 191-221. Academic Press, Sydney. Ku~, J. (1990). Immunization for the control of plant disease. In 'Biological Control of Soil-borne Plant Pathogens' (D.J. Hornby, ed.), pp. 355-373. CAB International, Wallingford. Ku~, J., Shockley, G. and Kearney, K. (1975). Protection of cucumber against CoUetotrichum lagenarium by Colletotrichum lagenarium. Physiological Plant Pathology 7, 195-199. Langcake, P. and Wickens, S. G. A. (1975). Studies on the action of the dichlorocyclopropanes on the host-parasite relationship in the rice blast disease. Physiological Plant Pathology 7, 113-126. Linthorst, H . J . M . (1991). Pathogenesis-related proteins of plants. Critical Reviews in Plant Sciences 10, 123-150. Malamy, J., Carr, J. P., Klesig, D . F . and Raskin, I. (1990). Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-1004. Martyn, R. D., Biles, C. L. and DiUard III, E. A. (1991). Induced resistance to Fusarium wilt of watermelon under simulated field conditions. Plant Disease 75, 874-877. Matta, A. (1980). Defenses triggered by previous diverse invaders. In 'Plant Disease, an Advanced Treatise' (J. G. Horsfall and E. B. Cowling, eds), pp. 345-361. Academic Press, New York. McIntyre, J. L. and Dodds, J. A. (1979). Induction of localized and systemic protection against Phytophthora parasitica var. nicotianae by tobacco mosaic virus infection of tobacco hypersensitive to the virus. Physiological Plant Pathology 15, 321-330. M~traux, J. P., Ahl Goy, P., Staub, T., Speich, J., Steinmann, A., Ryals, J. and Ward, E. (1990). Induced systemic resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens. Proceedings of the 5th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Interlaken, Switzerland. (abstract)

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M~traux, J. P., Ahl Goy, P., Staub, T., Speich, J., Steinemann, A., Ryals, J. and Ward, E. (1991). Induced systemic resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens. In 'Advances in Molecular Genetics of Plant-Microbe Interactions, Vol. 1' (H. Hennecke and D. P. S. Verma, eds), pp. 432-439. Kluwer, Dordrecht. Murray, D.C. and Walters, D. R. (1992). Increased photosynthesis and resistance to rust infection in upper, uninfected leaves of rusted broad bean (Vicia faba L.). New Phytologist 120, 235-242. Nakahara, Y. and Ogawa, T. (1990). Stereoselective total synthesis of dodecagalacturonic acid, a phytoalexin elicitor of soybean. Carbohydrate Research 205, 147-159. Nemestothy, G. S. and Guest, D. I. (1990). Phytoalexin accumulation, phenylalanine ammonia lyase activity and ethylene biosynthesis in fosetyl-A1 treated resistant and susceptible tobacco cultivars infected with Phytophthora nicotianae var. nicotianae. Physiological and Molecular Plant Pathology 37, 207-219. Pan, S. Q., Ye, X.-S. and Ku6, J. (1991). Association of/3-1,3-glucanase activity and isoforrn pattern with systemic resistance to blue mould in tobacco induced by stem injection with Peronospora tabacina or leaf inoculation with tobacco mosaic virus. Physiological and Molecular Plant Pathology 39, 25-39. Phillips, J. N., Witrzens, B., Dalton, L. K. and Elmes, B. C. (1981). Induced resistance to Fusarium wilt in tomato seedlings. Phytopathologische Zeitschrift 101, 189-195. Rathmell, W.G. (1984). The discovery of new methods of chemical disease control: current developments, future prospects and the role of biochemical and physiological research. Advances in Plant Pathology 2, 260-288. Ricci, P., Trentin, F., Bonnet, P., Venard, P., Mouton-Perronet, F. and Bruneteau, M. (1992). Differential production of parasiticein, an elicitor of necrosis and resistance in tobacco, by isolates of Phytophthora parasitica. Plant Pathology 41, 298-307. Ross, A. F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340-358. Seguchi, K., Kurotaki, M., Sekido, S. and Yamaguchi, I. (1992). Action mechanism of N-cyanomethyl-2-chloroisonicotinamide in controlling rice blast disease. Journal of Pesticide Science 17, 107-113. Sequeira, L. (1983). Mechanisms of induced resistance in plants. Annual Review of Microbiology 37, 51-79. Smith, J. A. and M6traux, J.-P. (1991). Pseudomonas syringae pv. syringae induces systemic resistance to Pyricularia oryzae in rice. Physiological and Molecular Plant Pathology 39, 451-461. Smith, J . A . , Hammerschmidt, R. and Fulbright, D.W. (1991). Rapid induction of systemic resistance in cucumber. Physiological and Molecular Plant Pathology 38, 223-235. Sutton, D. C. (1979). Systemic cross protection in bean against Colletotrichum lindemuthianum by Colletotrichum lindemuthianum. Australasian Plant Pathology 8, 4-5. Sutton, D.C. (1982). Field protection in bean against Colletotrichum lindemuthianum by Colletotrichum lindemuthianum. Australasian Plant Pathology 11, 50-51. Suzuki, H. (1980). Defenses triggered by previous invaders: fungi. In 'Plant Disease, an Advanced Treatise' (J. G. Horsfall and E. B. Cowling, eds), pp. 319-332. Academic Press, New York. Walters, D. R. and Murray, D.C. (1992). Induction of systemic resistance to rust in Vicia faba by phosphate and EDTA: effects of calcium. Plant Pathology 41, 444-448. Watanabe, T., Igarashi, H., Matsumoto, K., Seki, S., Mase, S. and Sekizawa, Y. (1977). The characteristics of probenazole (Oryzemate) for the control of rice blast. Journal of Pesticide Science 2, 291-296. Watanabe, T., Sekizawa, Y., Shimura, M., Susuki, Y., Matsumoto, K., Iwata, M. and

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Mase, S. (1979). Effects of probenazole (Oryzemate) on rice plants with reference to controlling rice blast. Journal of Pesticide Science 4, 53-59. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D.A. and Raskin, I. (1991). Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. The Plant Cell 3, 809-818. Yoshida, H., Koishi, K., Nakagawa, T., Sekido, S. and Yamaguchi, I. (1990). Characteristics of N-phenylsulfonyl-2-chloroisonicotinamide as an anti-rice blast agent. Journal of Pesticide Science 15, 199-203.

12 THE ROLE OF SOIL MICROBIOLOGY IN SUSTAINABLE INTENSIVE AGRICULTURE C.E. Pankhurst* and J. M. Lynch T *CSIRO, Division of Soils, Glen Osmond, South Australia, 5064, Australia t School of Biological Sciences, University of Surrey, Guildford, Surrey G U2 5 X l l , UK

I. II. III. IV. V.

Introduction Numbers and Biodiversity of Micro-organisms in Soil Role of Soil Micro-organisms in the Conservation of Soil Structure Soil Micro-organisms and Nutrient Recycling in Soils Interactions of Soil Micro-organisms with Plants A. Nitrogen fixation B. Mycorrhizal Fungi C. Plant Growth-promoting Rhizobacteria D. Biological Control of Plant Root Diseases VI. Integrated Management and Control of Pests and Diseases VII. Opportunities for Soil Microbiological Inputs into Sustainable Agricultural Systems A. On-going Opportunities B. New Opportunities VIII. Potential Use of Soil Micro-organisms as Indicators of Soil Quality and Sustainability References

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I. I N T R O D U C T I O N Sustainable agriculture embraces several forms of non-convential agriculture that are often referred to as organic, alternative, ecological or low-input. However, these terms are not synonymous with sustainable agriculture, because each has a special focus of its own. To be sustainable the farm must produce adequate amounts of high-quality food, protect its resources and be both environmentally safe and profitable. Instead of depending on purchased materials such as fertilizers, a sustainable farm relies as much as possible on beneficial natural processes and renewable resources drawn from the farm itself. Reductions of chemical energy inputs to agriculture could lead to more economical production systems while minimizing pollution. This might be achieved by modifying farming systems (e.g. reduction of tillage), the use of improved efficiency organic ADVANCES IN PLANT PATHOLOGY~VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rightsof reproductionin anyform reserved

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fertilizers and the partial replacement of crop protection chemicals with microorganisms (including those that have been genetically modified). To understand the rationale for sustainable agriculture, one must appreciate the critical importance of soft. Soil is not just another component of crop production, like pesticides or fertilizers. Rather it is a complex, living, fragile medium that must be protected and nurtured to ensure its long-term productivity and stability. A healthy soil is a hospitable world for growth. It is composed of mineral particles and organic materials that combine and are held together as aggregates providing a three-dimensional fabric that retains moisture, allows air to circulate freely and to which plant nutrients may cling. It also contains vast populations of soil organisms, including micro-organisms (bacteria, fungi, actinomycetes and algae) and soil fauna (protozoa, nematodes, microarthropods, arthropods and earthworms), most of which are involved in the decomposition of organic matter. Decomposition of organic matter results in the formation of humus and the release of many nutrients important for plant growth. Some soil organisms contribute directly to soil fertility by fixing atmospheric nitrogen into forms of nitrogen that plants and other organisms use for growth. Others contribute to soil health by producing polysaccharides which help to bind soil particles together and help the soil resist erosion. To remain healthy, the soil must be fed organic materials such as various manures and crop residues. Because the maintenance of soil structure and fertility is of paramount importance for plant growth and because this in turn is dependent on the activities of soil organisms (especially soil micro-organisms), soil microbiology has a significant role to play in intensive sustainable agriculture. Consideration of this role will focus on those aspects of soil microbiology that contribute directly and indirectly to plant growth. This will include discussion of the importance of soil micro-organisms to: (1) the maintenance of soil structure; (2) their role in nutrient recycling; and (3) their beneficial and detrimental interactions with plants. Consideration will also be given to prospects for the management of soil micro-organisms in sustainable agricultural systems and the potential of using microbial activities and/or populations of soil micro-organisms as indicators of sustainability.

II. NUMBERS A N D BIODIVERSITY OF MICRO-ORGANISMS IN SOIL

Soil micro-organisms, including bacteria, actinomycetes, fungi, algae (mostly blue-green algae (cyanobacteria)) and protozoa constitute the major part of the soil biomass. In a fertile temperate soil, the microbial biomass may exceed 20 t ha-1. The diversity of this population of micro-organisms can only be estimated as current culturing methods are able to distinguish only a small proportion, probably <20%, of the taxa present. Current estimates of the number of species in some groups include bacteria (30 000), fungi (1 500 000), algae (60000) and protozoa (100000) (Hawksworth and Mound, 1991). How-

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ever, the potential diversity of these micro-organisms, especially bacteria, may be very much larger because of the potential gene flow between species. Even if it were possible to sample the full diversity of soil micro-organisms at a given site, the data would be of limited value since many micro-organisms are opportunistic, with the capacity for rapid population increase to exploit temporary availability of favourable substrates, followed by rapid decline and survival as spores or other resting stages until a suitable substrate again becomes available. Populations determined for such organisms depend on microdistribution of substrates and on microenvironmental conditions in the soil at the time of sampling. Typically, there are between 10 6 and 10 9 bacteria per gram of soil. In wellaerated soils, both bacteria and fungi are present; however, in conditions of low oxygen availability, bacteria may be dominant. Bacteria are of particular importance in soils because their diverse metabolic capabilities enable them to exploit many sources of energy and carbon in the soil. Unique metabolic features include anaerobic respiration, chemolithotrophic growth, fixation of molecular nitrogen and utilization of methane (Lynch, 1983), making soil bacteria the principal agents for the global cycling of many inorganic compounds, especially nitrogen, sulphur and phosphorus. Soil fungi, numerically less abundant than bacteria (between 104 and 10 6 fungal propagules per gram of soil) are the major contributors to and may account for as much as 70% by weight of the microbial biomass (Anderson and Domsch, 1978). Because of their filamentous growth, they are also able to exploit a diversity of substrates in the soil. They may be free-living or in symbiotic association (e.g. mycorrhiza) with plant roots. Like bacteria most soil fungi are opportunistic, becoming active when environmental conditions (e.g. moisture, temperature, aeration) are favourable. Soil fungi are active in the decomposition of cellulose and are the principal agents for the decomposition of lignins produced by plants. The breakdown of these polymers releases simple molecules that are subsequently used by other soil organisms, particularly bacteria. Like soil fungi, soil actinomycetes play an important role in the decomposition of organic compounds (especially recalitrant compounds) in the soil. Populations of actinomycetes are usually between 105 and 10 a propagules per gram of soil. Population densities of algae and protozoa in soils have been estimated to be between 10 and 10 6 per gram of soil for algae and between 10 4 and 105 per gram for protozoa (Atlas and Bartha, 1987). The abiotic environmental parameters regulating the growth of algae and protozoa in soils include sunlight and CO2 for algae and 02 for protozoa. Cyanobacteria, because of their ability to fix nitrogen, can make a valuable nitrogen input to soils (Metting, 1981). Both cyanobacteria and green algae also contribute to the organic carbon input of soil, and through the production of extracellular polymers may help to conserve soil structure (Lynch, 1983). Protozoa are important predators in soil and help to regulate the size of bacterial populations. This activity also promotes the release of nutrients especially nitrogen and phosphorus (Clarholm, 1981).

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III. ROLE OF SOIL MICRO-ORGANISMS IN THE CONSERVATION OF SOIL STRUCTURE An important component of any sustainable agriculture programme is the adoption of management practices that minimize soil erosion and conserve soil fertility. The success of these practices will be judged by their ability to maintain or create soil aggregrate structure, because the binding of soil particles into aggregated units creates structures that are not only resistant to erosion but also act as a sink for the capture of nutrients in the soil (Elliott and Coleman, 1988). Without the physical protection afforded within stable aggregates, organic matter and associated nutrients may be rapidly lost via both mineralization and erosion. The binding substances that hold soil particles together have both mineral and organic origins. In tropical and subtropical softs, stable aggregates are mainly created by the cementing of soil particles by mineral substances. In softs where organic matter is the major binding agent, several types of substance contribute to soil aggregation. Inorganic and relatively persistent organic binding agents are important for the stabilization of microaggregates (<0.25 mm diameter), but microaggregates are subsequently bound together into macroaggregates (>0.25 mm diameter) by a variety of primary organic mechanisms (Oades, 1984). The hyphae of both mycorrhizal and saprophytic fungi, along with fibrous roots, bind soil particles and microaggregates into larger, aggregated units (Oades, 1984; Gupta and Germida, 1988; Miller and Jastrow, 1992). Mucigels and polysaccharides produced by micro-organisms and roots can act as the gums and glues that bind and stabilize aggregates (Oades, 1984; Foster, 1985). The breakdown products of plant residues resulting from the actions of saprophytic microbes and other soil biota are also important in contributing to the creation of soil aggregates (Lynch and Bragg, 1985). ['he contribution of vesicular arbuscular (VA) mycorrhizal fungi to the formation of soil aggregates is of particular importance. Their symbiotic association with plant roots and their persistence in the soil for several months after plants have died (Tisdall, 1991) make them valuable stabilizers of soil aggregates. The mechanism by which this occurs is believed to be via the physical enmeshment by extraradical hyphae of mineral and organic debris, which facilites the development of microaggregates, and the subsequent enmeshment of these microaggregates by extraradical hyphae and plant roots to form macroaggregates (TisdaU, 1991; Miller and Jastrow, 1992). The macroaggregate structure can be further stabilized by intermicroaggregate and intermacroaggregate cementation with polysaccharides or other organic substances (Gupta and Germida, 1988). A positive relationship between the amount of macroaggregates in the soil and the quantity of VA mycorrhiza extraradical hyphae present has been established (Tisdall and Oades, 1980). Agricultural practices that reduce the population of VA mycorrhiza in the soil (e.g. tillage, fallow rotations) were also found to decrease the amount of soil held as macroaggregates (Tisdall and Oades, 1980). Currently, the tools available for maintaining soil structure are based on crop

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management practices such as minimizing tillage, avoiding fallow, and using rotations with plants possessing extensive mycorrhizal root systems. However, the possibility of improving structure by introducing micro-organisms or by manipulating existing soil microbial populations is worthy of further research. Manipulation of the mycorrhizal association may be possible if traits of both the plant and mycorrhizal fungi that are associated with improved soil aggregate structure can be identified. Examples of this would be selection of strains of VA mycorrhiza that produce a large amount of their biomass external to the plant root, and selection of plant genotypes that promote extraradical hyphal development by mycorrhizal fungi (Miller and Jastrow, 1992). Many soil rhizobacteria (notably species of the genera Pseudomonas, Agrobacterium, Azotobacter, Rhizobium, Bacillus, Be~ierinckia)produce exopolysaccharides that are highly viscous (Hebbar etal., 1992), and interest in the use of such polysaccharide-producing bacteria to improve soil structure in agricultural soils is increasing. Recently, Gouzou et al. (1993) demonstrated that inoculation of wheat with a rhizosphere strain of Bacillus polymyxa significantly increased the mass of soil adhering to the roots. Polysaccharides produced by the B. polymyxa increased aggregation of macroaggregates in the rhizosphere of inoculated plants resulting in the development of a more porous soil structure (Gouzou etal., 1993). IV. SOIL MICRO-ORGANISMS AND NUTRIENT RECYCLING IN SOILS Soil micro-organisms are the driving force behind the recycling of macroand micronutrients from soil organic matter, which is mostly derived from decomposing plant material. Most of these nutrients are held in complex soil organic matter components that must be mineralized by micro-organisms to an inorganic form before they can be used by plants. This biological mineralization produces inorganic N, P and S in ratios similar to the material being consumed indicating that the inorganic nutrient cycles in the soil are linked to each other and driven by microbial ultilization of C for energy. In the absence of externally applied nutrients, the limiting factor for plant production will be the rate of mineralization and the quality and quantity of soil organic matter. Classically, the decomposition of organic matter in the soil is considered to be brought about by successional populations of micro-organisms (Lynch, 1983), for example primary saprophytic colonization by sugar fungi, such as Mucor, followed by cellulolytic organisms and organisms able to degrade the more recalcitrant components of organic matter, such as the lignins in plant cells. The more readily degradable compounds, for example amino acids, mono- and oligosaccharides, become part of a 'fast/active' pool of nutrients which may cycle 8-10 times a year through microbial cells, the soil fauna which consumes them and plants (Coleman etal., 1983). More resistant materials form a 'slow/passive' pool. This passive pool, which contains the bulk of the humified soil organic matter, may be cycled through the soil microflora-soil fauna pathway only once every 10-100 years

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(Coleman etal., 1983). The bulk of the active microbial and grazing faunal biomass operates in the active organic pool and it is the rapid cycling of nutients within this pool that is the most relevant to plant growth. Intricate detritus food webs, involving complex interactions between the microflora and the micro-, meso- and macrofauna in soils are features of nutrient recycling in natural and agroecosystems and have a significant bearing on the rate, the timing and the nature of the nutrients released for plant growth (Hendrix etal., 1986; Elliott etal., 1988). In a comparison of conventionally tilled (ploughed) and zero-tillage agricultural systems in Georgia, USA, Hendrix et al. (1986) developed conceptual models of the detritus food webs that were operating. In the conventionally tilled system where plant residues were mixed into the upper layers of the soft, the initial breakdown of the plant tissue was predominantly mediated by bacteria which in turn were extensively fed upon by protozoa and bacterivorous nematodes. Decomposition and nutrient mineralization proceeded rapidly. In contrast, localization of plant residue on the soil surface in zero-tillage systems promoted fungal growth and immobilization of nutrient in the plant residue. Consequently, abundance and activity of fungivorous fauna increased in the surface layers, and mineralization proceeded more slowly. The models represent nutrient storages and transfers from decomposing plant residue through the food webs and abiotic soil components and back to plants. In similar studies in the Netherlands, Brussaard et al. (1990) compared the size, composition and temporal dynamics of soil organisms in soil under conventional and integrated (reduced tillage, reduced input of agrichemicals) f a m i n g systems. Increased organic matter as a result of more crop residues being incorporated in the integrated farming system resulted in a higher bacterial and fungal biomass being present in the top soil with this farming system. Bacteria constituted more than 90%, fungi approximately 5 %, and protozoa less than 2 % of the total biomass. However, the protozoa were shown to have a major role in augmenting the flow of C and N in both the conventional and integrated farming systems. Plant residues and their return to the soil have been long recognized as important for the maintenance and build-up of soil organic matter and for the improvement of soil physical properties, such as bulk density and water retention (Smith etal., 1992). However, it is the effect that plant residues have on the microbial biornass that is important in nutrient recycling. Because of this, it may be possible to control biotic activity and hence nutrient availability to plants through management of the quantity and quality of carbon inputs into the soft. For example, high carbon: nitrogen ratio material could be used to stimulate immobilization of other nutrients into microbial biomass, removing them from the soil solution. Nutrients in higher quality substrates (low carbon: nitrogen ratio) are more rapidly mineralized, resulting in less immobilization and greater nutrient availability. A key goal of soil biotic management is to manipulate the processes of residue decomposition, nutrient immobilization, and mineralization so that nutrient release is synchronized with plant growth (Sanchez et al., 1989).

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V. INTERACTIONS OF SOIL MICRO-ORGANISMS WITH PLANTS From seed germination until a plant reaches maturity, it lives in close association with soil micro-organisms. The vast majority of these microbes inhabit the rhizosphere, the zone of soil around plant roots in which the physics, chemistry and biology of the soil is influenced by the roots. Under normal growth conditions, the rhizosphere exists because of the continuous leakage (or rhizodeposition) of a wide range of plant metabolites from plant roots (Bowen and Rovira, 1991). The rhizosphere supports large populations of all the groups of soil micro-organisms. The biomass of these micro-organisms is usually greater in the rhizosphere than in the root-free soil (Bowen and Rovira, 1991). Within the rhizosphere, there is a continuous interaction between plant roots and the rhizosphere micro-organisms; these interactions have a major influence on plant growth and may be viewed as beneficial (if they promote plant growth) or detrimental (if they reduce plant growth). The major beneficial associations between the roots of agricultural crops and soil micro-organisms include: nitrogen fixation by symbiotic associations, nitrogen fixation by associative bacteria; plant growth promotion by other bacteria and/or mycorrhizal fungi; and biological control of root diseases. Appropriately managed, these associations have the potential to provide sustained and economically important inputs into most agroecosystems. A. Nitrogen fixation Biological nitrogen fixation by soil bacteria, either free-living or in a variety of symbiotic associations with plants, probably contributes as much nitrogen to plant production systems as does the approximately 75 million tonnes of N annually added as fertilizer. Not surprisingly much research has been directed at increasing the usage and efficiency of biological nitrogen fixation, particularly the symbiotic systems, and extending nitrogen fixation beyond the legume plant family. Nitrogen fixation by root nodules formed by bacteria of the genera Rhizobium and Bradyrhizobium on legumes has been exploited in agricultural systems for many decades and is a significant source of nitrogen input into soils in most present-day arable and intensive cropping agriculture. Inoculation of legume crops with Rhizobium to ensure effective nodulation and nitrogen fixation is standard practice in many countries. However the expansion of legume crop production into many developing countries, particularly crops such as soybean and chickpea, which require specific strains of root nodule bacteria, has highlighted the need for continued research on inoculant strain selection, inoculum production and usage, and the selection of plant cultivars that nodulate promiscuously and effectively with indigenous bacteria (Keyser et al., 1992). Selection of Rhizobium and Bradyrhizobium strains tolerant to stress conditions, such as those

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related to acidic and saline softs, would improve the performance of legumes grown in these softs. A major impediment to introducing new Rhizobium or Bradyrhizobium strains into softs is usually a large existing population that may not be as effective in fLxing nitrogen, but which is often competitive in forming nodules. Neither strain selection nor use of molecular genetics to construct new strains has so far been successful in overcoming this competition. Consequently the main hope for a response to nodulation remains for softs where the crop has been infrequently grown and indigenous Rhizobium/Bradyrhizobium populations are small (Keyser et al., 1992). Much of the current research effort targeted at the legume root nodule symbiosis is aimed at unravelling the bacteria/plant interactions that occur during nodule development. Many of the bacterial genes involved in host specificity, nodule formation and nitrogen fixation have been identified (McCardell et al., 1992) and much is known about the signals that are exchanged between host and bacterium during nodule induction (Long, 1989; Martinez etal., 1990). Whilst it has been possible to extend the host range of a Rhizobium strain to other legumes, the complexity of the nodulation process suggests that it will be extremely difficult to extend nodulation to other plants (Martinez et al., 1990). Factors that prolong nodule activity when soil water is limiting, but before the wilting-point is reached and that delay nodule senescence, would have a large impact on the amount of nitrogen fLxed. For soybean (Carroll et al., 1985), peas, and Phaseolus vulgaris (Park and Buttery, 1988), plant mutants have been selected that are not inhibited in their nodulation and nitrogen fLxation in the presence of nitrate in the soil. These mutants produce a large number of nodules (supernodulation) because the control exerted on further nodulation by the initially formed nodules is not operating. Such mutants of soybean have given increases in yield over the wild-type parent in soils containing variable levels of nitrate. Nodulation of these mutants was also found to be less sensitive to soil acidity than nodulation by the wild-type parent (Alva et al., 1988). Such research may be more fruitful than that focused on selection and/or genetic manipulation of Rhizobium strains (McCardell etal., 1992). Other soil micro-organisms that develop a nitrogen-fLxing symbiosis with plants include the nitrogen-fixing nodules formed on a diverse range of nonlegume plant families by the actinomycete Frankia and the symbiosis between the blue-green alga Anabaena azollae and the water fern Azolla. Different strains of Frankia nodulate different hosts, and there are many situations where inoculation with Frankia is necessary for nodulation to occur. Casuarina spp. and Alnus spp. are the two nodulated non-legumes of most importance in forestry and agriculture, fLxing nitrogen for their own and companion-crop growth (Dawson, 1992). Frankia is difficult to isolate, purify and grow in culture, and genetic analysis of the nodulation and nitrogen-fixation genes has only just begun and will prove to be a more difficult task than with Rhizobium. Since Frankia nodulates a wider range of host than Rhizobium, it may prove easier to extend the range

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of plants fixing nitrogen through genetic manipulation of Frankia than through Rhizobium. Azolla is a small freshwater fern that fixes nitrogen through the blue-green algal symbiont Anabaena azollae living in the leaf substomatal cavity. In rice paddies 1-2 kg N ha-1 can be fixed daily (Watanabe, 1988). The Anabaena strain cannot be grown in pure culture, but is naturally and invariably transmitted to AzoUa progeny (Plazinski, 1989). Molecular techniques have shown that different Azolla species contain different Anabaena strains, opening up the possibility of engineering different strain and host combinations that may fix more nitrogen and require less phosphorus than current associations (Plazinski, 1989). Azolla is used in rice culture in several Asian countries, particularly in China. Problems with extending its use depend on developing improved methods for its incorporation into soil during the growth of the rice crop, for reducing the rather large requirement for phosphorus in order to fix considerable nitrogen, and for increasing high-temperature tolerance. Species and strain variability for these latter characters offers hope for improving its useful range and for acceptance by farmers. Nitrogen fixation by free-living soil bacteria and cyanobacteria may contribute significantly to the nitrogen status of soils in some farming systems. Azotobacter chrococcum and other nitrogen fixing bacteria used as seed inoculants can enhance growth in non-sterile softs of a range of agricultural crops, including wheat and maize (Dart, 1986). More recent experiments describe increases in rice yields in Egypt following inoculation with AzospiriUum brasilense (Omar etal., 1992) and increases in maize yields in France following inoculation with Bacillus circulans and Azospirillum lipoferum (Berge et al., 1990). However, there is no conclusive evidence that these responses are due to nitrogen fixation by the rhizobacteria. Azospirillum can increase root growth and hence mineral and water uptake, possibly through hormone production. It may also reduce the effect of fungal pathogens on root growth (Dart, 1986). In a similar fashion, nitrogen fixation by free-living cyanobacteria has been reported to increase the growth of rice (Watanabe, 1988). However the contribution of nitrogen is small and management of the algae has proved to be difficult due to predation by insects. Confirmation of potential benefits and the development of an improved inoculation technology are required in order to further exploit these organisms.

B. Mycorrhizal Fungi Mycorrhiza are symbiotic fungal associations with plant roots which aid in the uptake from soil of relatively immobile nutrients such as phosphorus and zinc, and may also help plants withstand environmental stress (drought, salinity, heavy metals) and reduce attack from root pathogens (Fitter, 1989). Two types occur- endomycorrhiza which include the VA mycorrhiza and ectomycorrhiza the latter usally found on woody species. VA mycorrhiza readily colonize many plant families. VA mycorrhiza isolates do not appear to be restricted to particular

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hosts, and more than one strain can infect an individual plant. V A mycorrhiza isolates grow poorly, if at all, in culture, and are maintained as single-isolate associations with plants. This makes inoculum production for field, or even experimental, use difficult (Bethlenfalvay, 199'2). Yield responses of some agricultural plants (e.g. pasture legumes and grasses and beans (Phaseolus vulgaris)) to inoculation with VA fungi have been obtained (Howeler et al., 1987; Barea a al., 1993), but inoculation practices in broadacre agriculture have been limited by the difficulties with inoculum production. An alternative approach is to develop soil and crop management strategies that enhance populations and root colonization by naturally occurring or introduced VA fungi in the soil. Populations of VA fungi are responsive to most agricultural practices. Practices that reduce root and soil colonization by VA fungi include soil disturbance, fallowing, crop rotation (or monoculture) with nonoVA mycorrhiza hosts, high levels of phosphorus application and biocides (Bethlenfalvay, 1992; Barea a al., 1993). Through an understanding of these effects it may be possible to develop appropriate management strategies, for example crop sequences, reduced tillage and timing of fertilizer application to reduce impacts on VA mycorrhiza, that increase rather than decrease the activity of appropriate VA mycorrhiza. Another important limiting factor to the large-scale utilization of VA mycorrhizal fungi in agriculture is a lack of sufficient information needed to recommend specific VA mycorrhizal isolates for the alleviation of specific problems. Recent evidence suggests that each VA fungal isolate potentially elicits a different host response (Stahl and Christensen, 1991; Bethlenfalvay, 1992), making selection of the best inoculum from a large number of existing populations difficult. Research is therefore needed to better understand this diversity and to identify the cultural and environmental conditions that may be alleviated by the use of specific VA fungal isolates.

C. Plant Growth-promoting Rhizobacteria Soil bacteria that aggressively colonize the rhizosphere and exert beneficial effects on plant growth are termed plant growth-promoting rhizobacteria (PGPR) (Kloepper and Schroth, 1981; Leggett and Gleddie, Chapter 4 this volume). The nature of the growth promotion by the rhizobacteria has been variously reported to involve the production of hormones, enhanced mineral and water uptake, and biological control of root-colonizing bacteria or fungi that are deleterious to plant growth. In recent years, it has become apparent that there is no clear separation of growth promotion and biological control induced by PGPR inoculants (Kloepper, 1992). Bacterial strains selected initially for in vitro antibiosis frequently demonstrate growth promotion in the absence of the target pathogen. Similarly, PGPR selected initially for growth promotion in the absence of pathogens may demonstrate biological control activity when challenged with the

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pathogen. However, PGPR cannot simply be considered as a subset of biological control agents as there are many reported examples of direct growth promotion by PGPR. One such example is the stimulation of root growth, shoot height and P uptake by roots and shoots of canola (Brassica carnpestris) grown in a gnotobiotic assay, following inoculation of the roots with a strain of Pseudomonas putida (Lifshitz et al., 1987). Another example is the P. fluorescens induced increased root hair formation on tobacco in a pathogen-free gnotobiotic assay (Voisard et al., 1989). The bioproduction of plant growth regulators (e.g. auxin, cytokinins, gibberellins, ethylene) by such bacteria in the rhizosphere is a possible explanation for these effects. Many rhizosphere bacteria have been demonstrated to produce one or several of these compounds or their precursors in pure culture suggesting that they may also produce these compounds in the soil and rhizosphere (Arshad and Frakenberger, 1992).

D. Biological Control of Plant Root Diseases Biological control of plant root diseases is a burgeoning field of research. The attraction of replacing expensive crop-protectant pesticides with some form of natural biological control has resulted in a large research effort being directed at developing suitable biocontrol organisms for the major agricultural and horticultural rootpathogens. Pesticides not only pose problems to the environment, they may also eliminate beneficial micro-organisms in addition to the target pathogen and induce the development of resistance in the pathogen population. Biological control methods are generally less likely to disrupt ecosystems, may be highly specific to the target pathogen and potentially, at least, will be cheaper than chemical control. However, despite these advantages, biological control agents are currently little used for the control of plant root diseases in broadcare agriculture primarily because agents that show good biocontrol under controlled environmental conditions have generally performed poorly in the field (Weller, 1988). This lack of performance in the field is associated with a general lack of knowledge of the mechanism of action of the biocontrol agent and of the nutritional, physical and biological factors which govern the growth and survival of the biocontrol agent in the soil. Procedures for the isolation, screening and controlled testing of microorganisms as potential biocontrol agents for specific root pathogens are well developed (Weller, 1988; Baker and Dickman, 1992). The organisms are usually isolated from soil displaying 'diseases suppression' towards the pathogen and screened for the ability to inhibit or reduce the growth of the pathogen in laboratory culture. Organisms showing good antagonism are then tested for their ability to control root infection by the pathogen under controlled environment conditions. There have been many reports of sucessful control of fungal root diseases with either bacterial or fungal biocontrol agents. For example, specific strains of Pseudomonas fluorescens (Thomashow and Weller, 1991) and

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P. corrugata (Ryder and Rovira, 1993) have been shown to reduce take-all of wheat caused by Gaeumannomyces graminis var. tritici in laboratory and field experiments. With both Pseudomonas species, biocontrol was strongly associated with the production of antibiotics by the bacteria which inhibited the growth of the take-all fungus. In another case, the siderophore pyoverdine produced by P. fluorescens, was implicated in the observed biocontrol by this pseudomonad of Pythium damping-off of cotton (Loper, 1988). Biocontrol of fungal root pathogens by other fungi, especially via competition for nutrients or mycoparasitism (rather than antibiosis), may be more effective than biocontrol of fungi by bacteria. This is because the fungal biocontrol agent has the potential to displace the pathogen from its ecological niche (i.e. niche exclusion) and has the potential to control the pathogen during its saprophytic as well as its pathogenic growth phases. Thus competition for simple C substrates together with mycoparasitism is thought to operate in the substantial decrease of inoculum density of Pythium ultimum by P. nunn (Paulitz, 1989). Similarly, saprophytic competition and mycoparasitism are thought to be the major factors associated with the control of take-all of wheat by Trichoderma koningii (Simon and Sivasithamparam, 1989), of Rhizoctonia solani infection of potatoes by Verticillium biguttatum (Jager and Velvis, 1988) and of Sclerotinia minor by Sporodemium scleotivorum (Adams, 1989). Practical application of mycoparasites for biocontrol of root diseases has yet to be exploited. As with other biocontrol systems, the physical and nutritional environment must be favourable for the agents if they are to be active in biocontrol. Strategies to enhance the activities of biocontrol agents in the soil through crop and soil management have been investigated and could provide effective and practical opportunities for disease control. A good example of this is the suppressiveness of acid soil to the take-all fungus (Gaeumannomyces graminis var. tritic0 (Simon and Sivasithamparam, 1989). Addition of NH+SO+, with resultant acidification of conducive soils, induced suppressiveness to G. graminis, whereas reversal to conduciveness was observed upon addition of lime to the treated soil. An increase in activity of Trichoderma spp. antagonistic towards G. graminis was correlated with the onset of suppressiveness. Management of soil pH to increase the effectiveness of biocontrol agents is an attractive strategy and one that should be further investigated in intensive agricultural operations where fertilizers are routinely added to alter soil pH to favour crop growth. Another strategy is to incorporate crop residues to promote selectively enhanced activity of agents or to immobilize an element essential for successful infection by a plant pathogen. Some success has been found with this strategy; for example in Colorado, incorporation of bean straw into soil increased the population density of P. num, and the inoculum density of P. ultimum decreased to low levels (Lifshitz et al., 1984).

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VI. INTEGRATED MANAGEMENT AND CONTROL OF PESTS AND DISEASES Increasing emphasis is being placed on integrated management as the strategy most suited to the control of pest and diseases in sustainable agricultural systems. Efficient crop production relies on finding the right balance between the various inputs of cultivation, organic matter, fertilizer and pesticides and crop management strategies including rotations, cultural technique and plant variety. It is the interaction between all of these components of the agricultural system that will determine how effective pest and diseases are kept under control and how sustainable the agricultural system will be in the long term (Edwards, 1990). Crop rotation has long been used as a strategy to reduce the build up and carryover of specific root pathogens in the soil (Rovira et al., 1990) and is still considered an effective treatment in most situations. The most effective control of take-all of cereals in southern Australia is to rotate cereals with a non-host crop (e.g. peas, lupins) in which grass weeds (an alternative host for take-all) are controlled (Rovira, 1989). This significantly reduces the survival of the take-all fungus in the soil. However, continuous cropping results in a gradual depletion of organic matter in the soil and is thus not sustainable. It is necessary therefore for the land to be returned to pasture every 5 or 6 years to restore organic matter levels and improve soil structure (Rovira, 1990). Farmers need to remove grasses from the pasture (with herbicides) the year before returning to cereal cropping to reduce the carry-over of take-all which again builds up on the roots of the pasture grasses (Rovira, 1990). This crop management strategy is also based on reduced tillage and increased plant residue retention, additional practices that reduce machinery and fertilizer costs and promote nutrient recycling, soil macrofauna activity and the development of improved soil structure (Rovira, 1990). However, on the debit side, the use of sulphonylurea herbicides to control grasses and weeds has led to the development of herbicide-resistant grass varieties and in some instances led to a build up of herbicide residues in the soil that have been associated with increased severity of other cereal root diseases, notably Rhizoctonia bare-patch (Rovira, 1989). Also, adoption of minimum tillage practices, whilst having little effect on take-all, may increase disease severity by other pathogens such as Rhizoctonia and Pythium (Pankhurst etal., 1993). These problems are the subject of on-going research which has the ultimate aim of developing an integrated management package for improved crop yields, disease control and soil conservation. They also emphasize the need for a better understanding of the impact of various agricultural practices on the ecology of the root pathogens concerned and on the ecology of other components of the soil microflora, which may or may not affect the viability of the root pathogens. Concerns over the environmental impact of pesticides have spurred efforts for the development of integrated management packages for crop production. Numerous possibilities exist for reducing the use of pesticides and herbicides many of these require better understanding of the ecology and versatility and the

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organisms to be controlled and of their natural predators. In addition to crop rotations and appropriate cultivations to minimize pest attack, possibilities for reducing use of pesticides include" use of minimal amounts of pesticide based on reliable disease forcasting; improved application techniques using smaller amounts and better placement; timing of crop sowing to avoid disease incidence or climatic periods favourable to the disease; use of crop varieties that are tolerant or resistant to disease; and use of biocontrol agents alone or in combination with low levels of pesticide. Similarly, possibilities for reducing the use of herbicides include: use of rotations to avoid volunteer seedlings from previous crops; use of mechanical weed control; cover cropping to minimize weed seed germination; and use of mycoherbicides (controlled inundative release of fungi pathogenic to a particular weed species; see also Scott, Chapter 7, this volume). The development and adoption of these possibilities in conjuction with other low input farming practices will assist in the creation of agricultural systems which are sustainable.

VII. OPPORTUNITIES FOR SOIL MICROBIOLOGICAL INPUTS INTO SUSTAINABLE AGRICULTURAL SYSTEMS The above discussion has focused on the role and activity of soil micro-organisms in agricultural production systems. In all respects, soil micro-organisms have a central role to play in the maintenance of soil structure, soil fertility and soil health. Collectively these activities will determine the ability of the soil to sustain plant production. Opportunities abound for significant on-going and new microbiological research inputs into the development of innovative, cost effective, environmentally sound, approaches to sustainable agriculture. Some of these opportunities are listed below.

A. On-going Opportunities 1. There is a need to develop a full appreciation of the impact of agricultural practices (crop rotation, tillage, residue incorporation, fertilizer and pesticide application) on detritus food webs and on populations and biodiversity of important functional groups of micro-organisms in our softs. These microorganisms and the processes that they carry out (e.g. nitrogen fLxation, cellulose breakdown) are inadvertently managed when crops and softs are managed. Considerable basic information is required to increase our capabilities in soil micro-organism 'husbandry'. 2. There is a need for continued microbiological input into the development of integrated management approaches for pest control and reduction in the use of pesticides.

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3. Considerable improvement is required in our understanding of how to successfully introduce and establish beneficial micro-organisms (e.g. Rhizobium, PGPRs, biocontrol agents) into the rhizosphere and soil. 4. Opportunities for increased plant production and enhanced soil conservation exist with the continued selection and evaluation of known beneficial soil micro-organisms (e.g. Rhizobium, VA fungi) and exploitation of less well known groups (e.g. protozoa, cyanobacteria, green algae). 5. There is need for a better understanding of the importance and agronomic potential of interactions between different soil micro-organism groups and between micro-organisms and soil fauna.

B. New Opportunities 1. Development of diagnostic probes, based on DNA or immunotechnology for the detection and quantification of specific micro-organisms (e.g. root pathogens). This has considerable potential for disease forecasting and for monitoring selected micro-organisms in the soil environment. 2. Development of predictive models to aid disease monitoring and forecasting. 3. Genetic manipulation of soil micro-organisms to improve their selected capabilities (e.g. rhizosphere competence, biocontrol activity) and to detect their presence in the soil and rhizosphere. 4. Genetic manipulation and/or selection of plant varieties that promote the growth of selected beneficial micro-organisms in the rhizosphere. 5. Isolation of soil micro-organisms (including microalgae) which enhance soil aggregate formation. Such micro-organisms could have potential in the rehabilitation of degraded agricultural soils. 6. Development of microbiological and molecular biology methods for characterizing the biodiversity of functional groups of soil micro-organisms.

VIII. POTENTIAL USE OF SOIL MICRO-ORGANISMS AS INDICATORS OF SOIL QUALITY AND SUSTAINABILITY Our ability to assess soil quality and identify key soil properties which serve as indicators of sustainability is complicated by the many issues associated with defining quality and the multiplicity of physical, chemical and biological factors that control biogeochemical processes and their variation in time, space and intensity (Doran and Parkin, 1994). Soil quality assessment, however, will be invaluable in determining the sustainability of land management systems in the near and distant future. Basic indicators of soil quality have not been defined, but will include a range of physical (e.g. soil texture, bulk density, water content), chemical (e.g. pH, total C and N) and biological characteristics that are sensitive to variations in

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agricultural management and climate. Included in a list of biological characteristics of soil quality is microbial biomass, potentially mineralizable N and soil respiration (Doran and Parkin, 1994). In addition to these, Pankhurst (1994) included high populations of beneficial micro-organisms, low levels of pests and diseases, soil organism biodiversity and selected soil enzymes as potential bioindicators of soil health and sustainability. It should be noted, however, that none of these potential bioindicators will be sufficiently robust to be generally applicable. Rather, individual bioindicators will need to be validated for their usefulness in different agroecosystems. This validation of indicators will require considerable further research, especially in soil microbiology.

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Dart, P.J. (1986). Nitrogen fixation associated with non-legumes in agriculture. Plant and Soil 90, 303-334. Dawson, J. O. (1992). Nitrogen fixation in forests and agroforestry. In 'Soft Microbial Ecology: Applications in Agriculture and Environmental Management' (F. B. Metting Jr, ed), pp. 227-53. Marcel Dekker, New York. Doran, J. W. and Parkin, T. B (1994). Defining and assessing soil quality. In 'Defining Soil Quality for a Sustainable Environment' (J. W. Doran, D.C. Colemen, D. F. Bezdicek and B.A. Stewart, eds). pp. 3-21. Special Publication, Soil Science Society of America. Madison, Wisconsin. Edwards, C. A. (1990). The importance of integration in sustainable agricultural systems. In 'Sustainable Agricultural Systems' (C. A. Edwards, R. Lal, P. Madden, R . H . Miller and G. House, eds), pp. 249-264. Soil and Water Conservation Society, Iowa. Elliott, E. T. and Coleman, D. C. (1988). Let the soil work for us. Ecological Bulletin 39, 23-32. Elliott, E. T., Hunt, H. W. and Walter, D. E. (1988). Detrital food web interactions in North American grassland ecosystems. Agriculture, Ecosystems and Environment 24, 41-56. Foster, R. C. (1985). In situ localization of organic matter in soils. QuaestionesEntomologicae 21,609-633. Fitter, A. H. (1989). The role and ecological significance of vesicular-arbuscular myeorrhizas in temperate ecosystems. Agriculture, Ecosystems and Environment 29, 137-151. Gouzou, L., Burtin, G., Philippy, R., Bartoli, F. and Heulin, T. (1993). Effect of inoculation with Bacillus polymyxa on soil aggregation in the wheat rhizosphere: preliminary examination. Geoderma 56, 497-491. Gupta, V. V. S. R. and Germida, J . J . (1988). Distribution of microbial biomass and its activity in different soil aggregate size classes as affected by cultivation. Soil Biology and Biochemistry 20, 777-786. Hawksworth, D. L. and Mound, L. A. (1991). Biodiversity databases: the critical significance of collections. In 'The Biodiversity of Microorganisms and Invertebrates: Its Role in Sustainable Agriculture' (D. L. Hawksworth, ed.), pp. 17-29. CAB International, Wallingford. Hebbar, K. P., Gueniot, B., Heyraud, A., Colin-Morel, P., Heulin, T., Balandreau, J. and Rinaudo, M. (1992). Characterization of exopolysaccharides produced by rhizobacteria. Applied Microbiology and Biotechnology 38, 248-253. Hendrix, P. F., Parmelee, R. W., Crossley, D. A., Coleman, D. C., Odum, E. P. and Groffman, P. M. (1986). Detritus food webs in conventional and no-tillage agroecosystems. Bioscience 36, 374-380. Howeler, R . H . , Sieverding, E. and Saif, S. (1987). Practical aspects of mycorrhizal technology in some tropical crops and pastures. Plant and Soil 100, 249-283. Jager, G. and Velvis, H. (1988). Inactivation of sclerotia of Rhizoctonia solani on potato tubers by Verticillium biguttatum, a soil-borne mycoparasite. NetherlandsJournal of Plant Pathology 94, 225-230. Keyser, H.K., Somasegaran, P. and Bohlool, B.B. (1992). Rhizobial ecology and technology. In 'Soil Microbial Ecology: Applications in Agricultural and Environmental Management' (F. B. MettingJr, ed.), pp. 205-226. Marcel Dekker, New York. Kloepper, J . W . (1992). Plant growth-promoting rhizobacteria as biological control agents. In 'Soil Microbial Ecology: Applications in Agricultural and Environmental Management' (F. B. Metting, Jr, ed.), pp. 255-274. Marcel Dekker, New York. Kloepper, J. W. and Schroth, M. N. (1981). Plant growth-promoting rhizobacteria and plant growth under gnotobiotic conditions. Phytopathology 71,642-644. Lifshitz, R., Sneh, B. and Baker, R. (1984). Soil supressiveness to a plant pathogenic Pythium species. Phytopathology 74, 1054-1061. Lifshitz, R., Kloepper, J. W., Kozlowksi, M., Simonson, C., Carlson, J., Tipping, E. M.

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and Zaleska, I. (1987). Growth promotion of canola (rapeseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Canadian Journal of Microbiology 33, 390-395. Long, S. R. (1989). Rhizobium - legume nodulation: Life together in the underground. Cell 56, 203-214. Loper, J. E. (1988). Role of fluorescent siderophore production in biocontrol of Pythium ultimum by a Pseudomonasfluorescens strain. Phytopathology 78, 166-172. Lynch, J. M. (1983). 'Soil Biotechnology: Microbiological Factors in Crop Productivity'. Blackwell Scientific, Oxford. Lynch, J. M. and Bragg, E. (1985). Microorganisms and soil aggregate stability. Advances in Soil Science 2, 133-171. Martinez, E., Romero, D. and Palacios, R. (1990). The Rhizobium genome. CRC Critical Reviews in Plant Science 9, 59-93. McCardell, A., Sadowsky, M.J. and Cregan, P.B. (1992). Genetics and improvement of biological nitrogen fixation. In 'Soil Microbial Ecology: Applications in Agricultural and Environmental Management' (F. B. MettingJr, ed.), pp. 177-204. Marcel Dekker, New York, Basal, Hong Kong. Metting, B. (1981). The systematics and ecology of soil algae. Botanical Review 47, 195-312. Miller, R. M. and Jastrow, j. D. (1992). The role of mycorrhizal fungi in soil conservation. In 'Mycorrhizae in Sustainable Agriculture' (G. J. Bethlenfalvay and R. G. Linderman, eds), pp. 29-44. American Society of Agronomy, SpecialPublication 54. Madison, WI. Oades, J. M. (1984). Soil organic matter and structural stability: Mechanisms and implications for management. Plant and Soil 76, 319-337. Omar, N., Berge, O., Shalaan, S. N., Hubert, J.-L., Heulin, T. and Balandreau, J. (1992). Inoculation of rice with Azospirillum brasilense in Egypt. Results of five different trials between 1985 and 1990. Symbiosis 13, 281-289. Pankhurst, C. E. (1994). Biological indicators of soil health and sustainable productivity. In 'Soil Resilience and Sustainable Land Use' (D. J. Greenland and I. Szabolcs eds), pp. 331-351. CAB International, Wallingford. Pankhurst, C. E., Neate, S. M., Roget, D. K., Ryder, M. H. and Rovira, A. D. (1993). Control of soilborne root diseases of crops in ecologically sustainable farming systems. In 'Trends in Microbial Ecology' (R. Guerrero and C. Pedros-Alio, eds), pp. 659-662. Spanish Society for Microbiology, Spain. Park, S.J. and Buttery, B. R. (1988). Nodulation mutants of white bean (Phaseolus vulgaris L.) induced by ethyl-methane sulphonate. CanadianJournal of Plant Science 68, 199-202. Paulitz, T . C . (1989). Biochemical and ecological aspects of competition in biological control. In 'New Directions in Biological Control' (R. Baker and P. E. Dunn, eds), pp. 713-724. Alan R. Liss, New York. Plazinski, J. (1989). The Azolla-Anabaena symbiosis. In 'Molecular Biology of Symbiotic Nitrogen Fixation' (P. M. Gresshoff, ed.), pp. 51-75. CRC Press, Boca Raton, FI. Rovira, A. D. (1989). Ecology, epidemiology and control of take-all, Rhizoctonia bare patch and cereal cyst nematode in wheat. Australasian Plant Pathology 19, 101-111. Rovira, A. D. (1990). The impact of soil and crop management practices on soil-borne root diseases and wheat yields. Soil Use and Land Management 6, 195-200. Rovira, A. D., Elliott, L. F. and Cook, R.J. (1990). The impact of cropping systems on rhizoshpere organisms affecting plant health. In 'The Rhizosphere' (J. M. Lynch, ed.), pp. 389-436. John Wiley, New York. Ryder, M. H. and Rovira, A. D. (1993). Biological control of take-all of glasshouse-grown wheat using strains of Pseudomonas corrugata isolated from wheat field soil. Soil Biology and Biochemistry 25, 311-320.

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Sanchez, P. A., Palm, C. A., Szott, L. T., Cuezas, E. and Lal, R. (1989). Organic input management in tropical agroecosystems. In 'Dynamics of Soil Organic Matter in Tropical Ecosystems' (D. C. Coleman, J. M. Oades and G. Uehara, eds), pp. 125152. University of Hawaii Press, Honolulu. Simon, A. and Sivasithamparam, K. (1989). Pathogen-suppression: A case study in biological suppression of Gaeumannomyces graminis var. tritici in soil. Soil Biology and Biochemistry 21, 311-335. Smith, J. L., Papendick, R. I., Bezdicek, D. F. and Lynch, J. M. (1992). Soil organic matter dynamics and crop residue management. In 'Soil Microbial Ecology: Applications in Agricultural and Environmental Management' (F. B. Metting, Jr, ed.), pp. 65-94. Marcel Dekker, New York. Stahl, P. D. and Christensen, M. (1991). Population variation in the mycorrhizal fungus Glomus mosseae: breadth of environmental tolerance. Mycological Research 95, 303-307. Thomashow, L. S. and Weller, D. M. (1991). Role of antibiotics and siderophores in biocontrol of take-all disease of wheat. In 'The Rhizosphere and Plant Growth' (D. L. Keister and P. B. Cregan, eds), pp. 245-252. Kluwer Academic, Dordecht. Tisdall, J. M. (1991). Fungal hyphae and structural stability of soil. Australian Journal of Soil Research 29, 729-743. Tisdall, J. M. and Oades, J. M. (1980). The effect of crop rotation on aggregation in a red-brown earth. Australian Journal of Soil Research 18, 423-433. Voisard, C., Keel, C., Haas, D. and Defago, G. (1989). Cyanide production by Pseudomonasfluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO Journal 8, 351-358. Watanabe, I. (1988). Nitrogen fixation by nonlegumes in tropical agriculture with special reference to wetland rice. Plant and Soil 90, 343-357. Weller, D. M. (1988). Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26, 379-407.

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13 WORLD INTEGRATED PATHOGEN AND PEST MANAGEMENT AND SUSTAINABLE AGRICULTURE IN THE DEVELOPING WORLD Jeffery w. Bentley, Jairo Castafio-Zapata and Keith L. Andrews Zamorano, Apartado Postal 93, Tegucigalpa, Honduras

I. Introduction II. Chemical Control and Sustainability A. Insecticides B. Fungicides C. Reducing Synthetic Pesticides with Seed Treatments III. Cultural Control and Sustainability IV. Host-plant Resistance and Sustainability V. Biological Control and Sustainability VI. Weeds VII. Soil Health and Sustainability VIII. Social Systems and Sustainable Agriculture References

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I. I N T R O D U C T I O N Green Revolution euphoria has been challenged by too many critics to discuss here (see, for example Gore, 1992; van Veldhuizen and Hiemstra, 1993). By the 1960s and 1970s the advances in agricultural technology had led to environmental degradation and created skepticism about the benefits of science and technology (Ruttan, 1989). High input agriculture is increasingly recognized as degrading and not profitable (Stinner and House, 1987). The Green Revolution wasn't all bad; millions escaped starvation, the International Agricultural Research Centers (IARCS) formed a network for global agriculture and, if we learn from our mistakes, we now recognize that technical progress may have social and environmental costs we cannot pay. Hardly any one argues that modern agriculture is sustainable. According to Klaus Lampe, Director General of the International Rice Research Institute (IRRI), today's methods of rice production are not sustainable and a better use of land will be possible only through better family planning ( F E D E A R R O Z , 1993). It is time for scientists to stop glibly promising to feed a geometrically ADVANCES IN PLANT PATHOLOGYmVOL. 11 ISBN 0-12-033711-8

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expanding human population, when one day they will not be able to deliver (Ruttan, 1989). Sustainable agriculture includes a stable and lower human population. High yielding varieties (HYVs) and improved agricultural practices are only transitory measures. Even with Green Revolution technologies, 41 000 a day die of starvation. In the next two to four generations we will have to produce as much food as in the entire 12 000-year history of agriculture (Freeman, 1989-90). Many authors call on science and technology to help feed a ballooning human population (Ruttan, 1989, Saxena etal., 1989; Plucknett, 1993). Part of that increase will have to come from reducing pest losses, without destroying the Earth's capacity to keep growing food. The Green Revolution was based on: (1) the rapid spread of new HYVs of rice and wheat in developing countries; (2) the nine-fold increase in fertilizer use between 1952 and 1983; (3) the great expansion of irrigation; and (4) the use of high amounts of pesticides (Freeman, 1989-90). Worldwide grain production increased from 623 million tons in 1952 to 1447 million tons in 1983. Most of this increase was due to high amounts of fertilizers and pesticides applied to the HYVs planted in large-scale monocultures. But, the HYVs of rice, wheat and maize produce high yields only in response to high inputs. HYVs need between 70 and 90 kg of N ha-1, when the average amount available in most developing countries is only one third of that (Freeman, 1989-90). Thanks to the new HYVs, many countries in Asia and Latin America are still self-sufficient in rice and wheat, but for how long? There is a maximum yield that any land can support and there is a finite (and even decreasing) amount of farm land. Rice, wheat and maize are the three leading food crops in the world, together providing more than half of all calories consumed by the entire human population (FAO, 1987). Most rice is grown in south, southeast, and east Asia from Pakistan to Japan. Of the 26 leading rice-producing nations, which include only two nations of Latin America (Brazil and Colombia), 18 are in Asia (Huke and Huke, 1990). Rapid population growth puts increasing pressure on the already strained food-producing resources. The rate of population growth in those developing countries where rice is the most important food is well above the world average. The following statistics given by Huke and Huke are amazing: worldwide, 100 million people are added every year, of which 60 million depend on rice. It is predicted that Asia will be one of the continents more affected by starvation. The main concern is that more than 90% of the riceconsumers live in Asia where 60 % of the world' s people live. The world' s population will reach 6200 million by the year 2000 and 8400 million by the year 2025. This implies more people to feed on less agricultural land. The challenge is enormous. While academics debate the definition of 'sustainable', our interest should be less words and more actions that contribute to sustainability. While we write sympathetically about traditional agriculture, we do not believe that sustainable agriculture is merely traditional or that no elements of modern agriculture are

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sustainable. We cannot be certain of the sustainability of new practices, but many modern practices seem unsustainable (e.g. most synthetic pesticide use, conventional tillage practices, irrigation leading to salinization). Only very old farming systems have had the opportunity to prove their sustainability (e.g. the rice terraces of southeast Asia, European peasant farms, or the chinampas of Mexico). Old farming systems have survived by evolving, not by being static. A system can fail for biological, technical or human reasons (see also Denevan, Chapter 2, this volume). While future historians (if there are any) will be the only ones who really know if today's pest control techniques are sustainable, all of us must use our best judgement now to decide if our crop protection techniques can feed the people without ruining the resources of future generations. Pathogen and pest management in sustainable agriculture includes: 1. Giving local or indigenous technical knowledge a place of honor in the activity of scientific learning. 2. Stopping genetic erosion. 3. Giving up ecologically destructive technologies, especially those based on chemicals. 4. Preserving the soil. 5. Stabilizing and then slowly reducing the human population. Crop diseases cause an annual worldwide loss of 13-20%, worth US$50 000 million (James, 1981). Since the beginning of agriculture 12 000 years ago, plant diseases have affected human welfare, sometimes catastrophically. Perhaps the first well-documented disaster was the famine provoked by potato late blight Phytophthora infestans (Mont) de Bary in Ireland in the late 1840s; about 1 million people starved to death and another 3-4 million migrated to North America. That epidemic was only the beginning. In 1943, in Bangladesh, another fungus, Bipolaris- (Helminthosporium) oryzae (Breda de Haan) Waksman & Henrici, the causal agent of brown leaf spot of rice, caused a terrible famine. The disease took half of the rice harvest and about 2 million people starved to death (Padmanabhan, 1973). In 1970, another Helminthosporium species, H. maydis Nisik & Miyake, the causal agent of the southern corn leaf blight, destroyed about 15 % of the United States' maize crop, worth $1000 million (Fry and Thurston, 1980). Even though epidemics in food crops have been known for centuries, they were uncommon until the extensive cultivation of HYVs starting in the 1960s. Traditional agroecosystems had high genetic diversity. The genetic uniformity of modern crop varieties offer short-lived resistance to insect pests and pathogens (Bramble, 1989). HYVs, the high use of nitrogen fertilizers, more intensive management practices and extensive monoculture increased the severity of many diseases. Many practices of modern agriculture have increased plant disease problems. Cultivating large areas with genetically similar plants in dense monoculture selects for pathogens that thrive on that host-genotype. Nevertheless, modern

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intensive agriculture will probably continue planting extensive areas with little genetic variability (Fry and Thurston, 1980). Unfortunately, we know relatively little about tropical plant production and still less about tropical plant pathology and entomology. For example, 90% of the insect species of Britain have been described (LaSalle and Gauld, 1991), while perhaps half of the Earth's 50 million insect species are in the tropical rain forests, in danger of becoming extinct before being described (Erwin, 1988; Wilson, 1988).

II. CHEMICAL CONTROL A N D SUSTAINABILITY

Arthropod pests (mainly insects and mites) are controlled by chemicals, cultural practices, host-plant resistance and biological control. Eleven arthropods a year will probably be added to fauna of the USA about seven becoming pests (Hoy, 1988). There is no reason to assume that other countries, especially tropical ones, are any less susceptible to pest invasion than the USA. The rapid introductions of pests to new areas will challenge our creativity for the rest of our careers. Developing countries consume only 25% of the world's pesticides (Anon, 1979). Total volume of pesticide use is highest on maize (Zea mays L.) followed by rice (Oryza sativa L.), cotton (Gossypium spp.), soybean [Glycine max (L.) Merr.], and wheat (Triticum aestivum L.). These five crops use 56 % of all insecticides, fungicides and herbicides, equivalent to approximately $6100 million (Dekker and Georgopoulos, 1982). Field tests with foliar fungicides to control diseases such as rice blast can produce yield increases from 1 to 2 t ha-~ (Castafio-Zapata and GNvez, 1972; Montoya, 1983; Yanuar etal., 1985; Nasrun etal., 1989), which suggests that fungal diseases can destroy up to 25 % of the potential crop. By 1985, over 370 000 t of pesticides were produced annually (Jewell, 1987). Preventative measures include resistance breeding and cultural practices; curative measures are mostly chemical (Plucknett, 1993).

A. Insecticides

Few argue for more insecticides. Almost everyone writing about insect pest control assumes that conventional insecticides are not sustainable. Ironically they are still the backbone of pest control. Freeman (1989-90) argues that the careful and appropriate use of insecticides is necessary to save harvests to feed the hungry. Some people write about improved application techniques for insecticides, like new 'ultra-low volume' sprayers (which spray ultra-high concentrations of chemicals) for use by small farmers (Matthews, 1990). McKenzie and Byford (1993) support insecticides for pests of cattle. In their experiments, horn flies (Diptera: Muscidae) developed resistance to all insecticides tested, but mixes

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and rotations of insecticides slowed resistance by one to seven generations. Most authors still supporting insecticides recognize the need to reduce their use. Sechser (1989) mildly defends insecticides, but calls for more sampling and improved application styles that kill fewer natural enemies. Advanced chemical technologies may be more benign than older ones. Semiochemicals, the stuff of insect communication, are less or non-toxic, and can be used in small amounts to attract or confuse insects. Hoy (1988) suggests that semiochemicals could be used to enhance control by natural enemies. Most of the hard-core advocates of insecticides must be spending their time making and applying pesticides rather than writing about them. Gore (1992) claims that 13 000 times more pesticides are produced now than when 'Silent Spring' was published. This seems unfathomable in the IPM (integrated pest management) era, but IPM often increases and justifies pesticide use (Luna and House, 1991). IPM has continued to support pesticides and now even the agrochemical companies have no trouble espousing IPM. A 1993 paper by ACRE, an organization that is supported by 'the makers of America's crop protection chemicals' cynically urged pesticide dealers to advocate IPM because 'those who would further regulate you and your customers have fallen in love with IPM, or what they think is IPM, as a solution to the perceived environmental problems of agriculture'. The paper went on to stress that IPM uses chemicals. It is time to question IPM's pesticide connection. According to the World Health Organization (WHO), in developing countries approximately 750 000 people are injured and up to 14 000 die every year from pesticide poisoning (Chengappa, 1989). Pesticides are the major force destroying natural enemies. In conventional agriculture many species have reached pest status only because their natural enemies have been eliminated. That was the case in Latin America with whitefly (Bemisia tabaci Genn.), the vector of bean golden mosaic virus (BGMV). In developing countries pesticides constitute over 40 % of all purchased inputs in farming compared with only 6% for developed countries (Adam, 1977, cited in Pollard, 1991). Despite a 234 % increase in insecticide inputs, 548% increase in fungicides and 5414 % increase in herbicides over the period of 15 years (1964-79) in Brazil, there was only a 16.8% increase in production of the 15 major crops (FAO, 1986). Current losses to pests in agricultural systems that use pesticides are from 20 to 50 %, as much as before the chemical era (Hobbelink, 1991). The Brundtland report called for no new agrochemicals to be used (Hinrichsen, 1987). There is no evidence that reducing pesticide use lowers yields in developing countries (van Veldhuizen and Hiemstra, 1993). On-farm experiments in the Philippines showed no increase of pest damage in rice plots without pesticides (Fujisaka et al., 1992). The notion that insecticides help produce higher crop yields is based on a common, but flawed, experimental design that uses small test plots of dubious validity. In pesticide trials, pesticide drift and the movement of herbivorous insects from one small plot to another cloud the results (Sterling etal., 1992).

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Unfortunately, intercropping and host-plant resistance experiments are also commonly done on plots so small that the results should not be extrapolated to commercial fields. Many cases could be cited of environmental contamination caused by insecticides. For example, because of agricultural runoff into estuaries on the west coast of Mexico, clams and other commercial seafood species contain lindane and aldrin above levels permitted by the FWPCA (US Federal Water Pollution Control Administration) (Galindo-Reyes etal., 1992). One argument against the sustainability of insecticides is the danger of residues in food. However, there is little evidence that pesticide residues damage health in the US (Ehrlich and Ehrlich, 1990). Lewis (1990) argues that traffic accidents are the only important mortality risk from any modern technologies. However, medical diagnoses in the developing world do not reveal how many people die from applying pesticides. Deaths diagnosed as strokes in the Cabanatuan area of the Philippines for men aged 15-34 years rose 291% after the insecticide endrin was adopted, rising from 4.59 to 18.0 deaths per 100 000 people. The rate of death only increased for young adult males, the ones applying insecticides, suggesting that millions of pesticide deaths worldwide may be misdiagnosed (Loevinsohn, 1987). While chemists may be able to develop newer, safer insecticides, Darwinian evolution guarantees that any pesticide will select for resistant arthropods (Quiroz, 1983; Simms, 1987; Sechser, 1989; Luna and House, 1991; McKenzie and Byford, 1993; Groeters etal., 1993). This is perhaps the greatest argument against the sustainability of insecticides. Insects inevitably evolve resistance to them. Gould's brilliant paper on the evolutionary potential of crop pests describes weeds, plant pathogens and insect pests as masters of surviving the farmers' assaults. 'Many of the short-triumphs of pest control have carried within them the seeds of longer-term failure' (Gould, 1991). The history of the war between farmer and pest teaches us not to underestimate the capacity of any pest species to resist attempts to destroy it, whether it be a weed, a pathogen or an insect (Gould, 1991). The solution is not just to keep inventing new insecticides in a chemical arms race with bugs. Insects resistant to one toxin are preadapted to be resistant to others (Simms, 1987). Five hundred arthropod pests are now resistant to chemical control (Dover and Croft, 1984; Georghiou, 1986, cited in Whitten and Oakeshott, 1991; Eckert, 1988). Only 230 were resistent in 1971 (Quiroz, 1983). Ironically, bees and other beneficial pollinators are among the insects most seriously decimated by insecticides (Kevan etal., 1990). Few farmers have escaped the impact of resistant pests, especially on intensively treated crops like rice, maize, sugarcane, cotton, fruits, vegetables and several greenhouse crops. Anywhere cotton is grown, the pests that attack the crop (over 25 species of beetles, caterpillars, bugs and mites in 36 countries) have become resistant (Georghiou and Mellon, 1982).

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Insecticides are also not sustainable because they create major pests from secondary ones by destroying their natural enemies (Luna and House, 1991). For example, in Brazil insecticides made the tobacco budworm (Heliothis virescens) (F.) a major pest, more important than the boll weevil (Anthonomus grandis Boheman) in some areas (Ramalho etal., 1990). Insecticides made whitefly a major pest in cotton in the Sudan (Eveleens and Rahman, 1993). Insecticides can also increase weeds by killing their natural enemies (Smith, 1982, cited in Luna and House, 1991). Much of the abuse of insecticides is connected to profit motives. For example, in Trinidad and Tobago, pesticide salesmen encourage farmers to use an average of $1526 worth of insecticides per hectare, even though social wasps (Polistes spp.) and other natural enemies can control the insect pests on tomatoes (Pollard, 1991). Insecticides have provoked serious crop losses in some countries. Cotton yields in the Sudan were lowest where insecticide use is highest (Eveleens and Rahman, 1993). In Indonesia in the 1976-1977 season, 500000ha of rice fields were heavily damaged by brown planthoppers (Nilaparvata lugens) (Stap.), which ruined 350 000 t of rice, enough to feed 3 million people. Government pesticide subsidies of 70-80% encouraged massive pesticide applications. Pesticides not only failed to control the planthoppers, but also killed vertebrates, beneficial insects and people. I P M was adopted as government policy in 1979. The program included training extension agents and some farmers and prohibited 57 insecticides. Only a few narrow spectrum ones were allowed. By 1987, pesticide subsidies were withdrawn. Since then rice production has increased more than the human population and there have been no more planthopper problems. Trained farmers did not need to use insecticides on rice. The government saved $100-150 million per year on insecticides (Oka, 1991; see also Pearce etal., 1990). From 1985 to 1988 the Sandinista government subsidized 95-98% of pesticide costs in Nicaragua. Pesticides were applied as often as time allowed. Some people even bought pesticides and poured them out, just to keep the bottle (Hruska, 1990). Once subsidies were dropped so did pesticide use. Interest in biocontrol is now high.

B. Fungicides The discovery of the Bordeaux mixture 100 years ago was the first important landmark in the history of chemical control of plant diseases. Commercial production of many crops, including Green Revolution ones, would be difficult or impossible without chemicals to control diseases. The discovery of the dithiocarbamate fungicides 50 years ago, and the introduction of several systemic fungicides in the late 1960s, are the two most important events in the history of chemical control of diseases (Anon, 1979). Vine crops use most of the world's fungicides, followed by rice, vegetables,

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deciduous fruits, potatoes and small grain cereals (Schwinn, 1982a). About 70% of all fungicides are used on the above crops, almost exclusively against foliar diseases. Vines and rice use about 50% of the fungicides. Rice and small grain cereals have the highest potential for using more fungicides (Schwinn, 1982b). For several types of diseases, chemical control is still weak or not possible at all. Even for those diseases that can be controlled, the major fungicides are technically out-dated; most of them are good for preventative use only. They are neither systemic or curative. Technical progress since the late 1960s in systemic and curative fungicides is amazing. However, it has led to the new problem of resistance (Schwinn, 1982b). Furthermore, most of the fungicides available are protectants. The farmer has to apply them following a prophylactic schedule, when the probability of infection has reached a certain threshold level. The new action systemic fungicides, even though they have a significant curative action, are used erroneously as if they were protectants. Chemicals to control plant disease select for resistant strains of the pathogenic species. In general, cases of insecticide resistance have been better documented than those involving other pest groups, but costly crop failures due to fungicide resistance is causing considerable concern. Over 150 crop plant pathogens are known to be fungicide resistant (Dover and Croft, 1984). First, resistance appeared to the pyrimides, later to the benzimidazoles, and most recently, to the acylalanine metalaxyles (Schwinn, 1982b). Resistance was practically unknown in plant pathogens as long as only inorganic chemicals were used to control plant diseases. Traditional European farmers still get good results from the old Bordeaux mix (Bentley, 1992a). Resistance was observed in isolated cases, with few of the organic protectants, but became a major problem after the introduction of the specific-acting systemic fungicides and antibiotics (Anon, 1979). Resistance has forced farmers to think more carefully about pesticides. In the United States, a recent study by the National Academy of Sciences found that of 4500 samples taken from fruit and vegetables, 80% contained hazardous residues (Anon, 1993). The situation in developing countries could be worse (FAO, 1986).

C. Reducing Synthetic Pesticides with Seed Treatments Even those who support pesticides usually agree that less is better. Pesticide use can be reduced by seed treatment with systemic pesticides. Seed treatment is effective against seed-borne and root diseases, especially in tropical areas with optimum conditions for disease development. Seed treatment with fungicides can control seedling blast of rice (Ahn, 1981; Castafio-Zapata and Klap, 1991), seedborne and root diseases of beans (Trutmann et al., 1992) and seed treatment with insecticides can control beanfly (Ophiomyia spencorella) on beans (Trutmann et al.,

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1992) and aphids in winter barley, reducing the incidence of barley yellow dwarf virus (Leclercq-le and Dedryver, 1992). Chemical treatments of infected seeds reduce infection caused by several pathogens, increase germination, emergence, vigor and sometimes yield (Papavizas and Lewis, 1975; Segura and Dfaz, 1975; Ellis et al., 1976; Willis, 1983; CastafioZapata, 1985; Pedersen etal., 1986; Wright and Hughes, 1987; Castafio-Zapata and Zepeda, 1990; Trutmann et al., 1992). Chemical seed treatments in an IPM program help increase crop production, but require training programs to ensure that users understand them. Chemical seed treatments are not a new concept; but, surprisingly, their use as a technology for resource-poor farmers has been a neglected area of research.

III. CULTURAL CONTROL A N D SUSTAINABILITY

Cultural control is more than mechanical operations, such as tillage and burning. It involves many aspects of crop and soil management, including crop rotation, time of planting and harvesting, seed storage, fertilizer rates and cropping system diversification (Palti, 1981 ; Mabbett, 1982; Prasad et al., 1983; Page and Bridge, 1993; Qu6n6herv6, 1993). Although some cultural control practices, such as crop rotation, are general practices that affect a variety of pests, many cultural controls are relatively pest-specific, requiring knowledge of the life history and habits of the target pest (Luna and House, 1991). Altieri (1992) devotes a short book to the idea that increased biodiversity reduces pests. He cites dozens of studies that show that more plant species in a field lead to more natural enemies and fewer pests. Traditional farmers have often grown several crops together and it is refreshing to see intercropping being legitimized by agricultural scientists. Most of the experiments cited by Altieri compare insect populations on monocrops with those on mixed crops of two or three species. For example, intercropping sunhemp and cowpea with cassava on C I A T (Centro lnternacional para Agricultura Tropical) experiment station trials in Colombia lowered insect pest damage to economically acceptable levels (Gold et al., 1989). Experiments are valuable for showing the value of intercropping for crop protection, but a natural history approach that looked at the insect populations and yields in traditional farmers' fields, where 20 plant species are sometimes grown together, might be even better. Increasing demands for food can lead to new, unsustainable cultural practices. In Nigeria, African rice gall midge damage was exacerbated by, among other things, more land planted to rice and by a wider range of planting dates which allowed rice pests to build up (Umeh et al., 1992). The Balinese water temple networks evolved to regulate irrigation over large areas. The temple networks scheduled a fallow period which helped reduce pests. In the 1970s when farmers ignored the fallow and planted continuously, rice losses to planthoppers reached 50%. In 1988, the fallow was observed and pest losses were less than 1%. Now

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development agencies intend to do away with the temple system (Lansing and Kremer, 1993). In Africa, the staple food crops, sorghum, maize and cowpea, are attacked by stemborers, leading to 30-80 % crop loss. The International Center of Insect Physiology and Ecology (ICIPE) in Kenya recognizes that stemborers are difficult to control by insecticides. ICIPE's researchers see intercropping as the most promising control strategy for stemborers (Saxena et al., 1989). Intercropping in India has also been shown to give farmers higher profits (Gupta and Aggarwal, 1992). To combat pests successfully in a sustainable agriculture, it seems less risky to apply the old practices of ancient farmers. As Gould says: 'if one were to dream of control measures to which insect pests truly could not adapt, food deprivation might be the most evident candidate'. The age-old practice of crop rotation is based on this approach; farmers alternate planting of a pest's host plant with a plant that it cannot feed on, and the pests die of starvation. This strategy has proved effective for centuries. The 12-year civil war in E1 Salvador helped show the value of organic amendments. La Providencia co-operative, in San Agustln, Usulut~in, could not buy agrochemicals during the war. The farmers used coffee pulp as fertilizer and used vegetal residues and wild plants to repel insect pests. Coffee yields at La Providencia range between 300 and 400 kg ha-1, a sustainable, higher value production with minimum inputs (Henrfquez, 1993). Organic agriculture seeks to minimize insect pest problems by creating conditions favorable to naturally occurring sources of mortality such as parasites, predators and by helping plants become more pest resistant. Pesticides, concentrated fertilizers and large-scale monocultures must be avoided (Van Driesche, 1989). Organic producers do not use synthetic pesticides. However, some chemicals approved for use in organic agriculture still have the potential to cause outbreaks by destroying natural enemies. Sulfur, for example, is used on fruit to control plant diseases but is very damaging to predaceous mites and entomopathogenic fungi (Van Driesche, 1989). Cultural practices have one of the highest potentials for reducing yield loss due to plant diseases. They can be manipulated to minimize inoculum production, survival and dissemination, as well as infection of many pathogens and disease development, yet this area of disease control receives the least attention among the major control measures.

IV. HOST-PLANT RESISTANCE AND SUSTAINABILITY Speaking for the C G I A R system of international research centers in the developing world, Plucknett (1993) writes that the system has now adopted sustainability as part of its mandate and favors breeding resistant plants as an alternative to

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pesticides. When host-plant resistance cannot be achieved, the centers 'must turn to other measures, including biocontrol'. This bias in favor of plant breeding comes from the C G I A R ' s older role of breeding the modern, high yielding crop varieties of the Green Revolution. Host plant resistance is the cheapest and safest method of controlling plant disease (Plucknett, 1993). Before 1960, rice yields per hectare in much of the world were extremely low. By 1966, IRRI had produced a variety with yields ranging from 6 to 10 t ha-1. The I R R I varieties were taken to various countries of Asia and Latin America for adaptive research and propagation. By 1969 the HYVs were covering about 23 % of the Intensification Program Area of Indonesia. As a result, rice production doubled from 13.7 million tonnes in 1966 to 26.3 million tonnes in 1979 (Suhardjan and Iman, 1980). The first group of introduced HYVs had a narrow genetic base. Those varieties were more vulnerable to devastation by insect pest and diseases. In 1975, the yield losses caused only by the brown planthopper (Nilaparvata lugens (Stap.) were estimated to be about 0.7 million tonnes of rough rice (Suhardjan and Iman, 1980). Similarly, in Korea the HYV Tongil was released in 1972 (IRRI, 1976) and yielded 30% more than the common varieties. By 1977, Tongil and its derivatives were grown on 54 % of the rice-growing areas of Korea. Due to the intensive monoculture, the fungus Pyricularia o~zae Cav., the causal agent of rice blast, broke the resistance of Tongil, provoking epidemics of blast and heavy losses of Korean rice production (Kiyosawa and Cho, 1980). The selection of genotypes adapted to acid soils in the humid tropics is the most successful example of the use of plant breeding to reduce the need for inputs. Acidtolerant varieties are being planted over large areas that previously could not be planted without heavy lime applications, favoring resource-poor farmers. Acid soils are distributed over extensive areas of the humid tropics and subtropics, where they represent an important but fragile resource covering more than 1510 million ha in tropical Latin America, Africa and Asia (Rao et al., 1993). Differential aluminum tolerance of genotypes within species has been reported for rice, maize, wheat, oat, sorghum, bean, soybean and sugar cane, among others (Foy, 1992), suggesting that this potential can be used to improve acidsoil adaptation in high-yielding varieties. In 1982, the CIAT Rice Program started a project to develop upland rice lines adapted to depleted soils and resistant to diseases (particularly rice blast and the hoja blanca virus) and insects pests (especially planthoppers and spittlebugs). The rices were also selected for good yield potential and high lodging resistance under favorable conditions (Sarkarung, 1986). More than 1300 lines were acquired, many adapted to high A1, low-nutrient conditions, besides being resistant to rice blast disease and brown leaf spot (Sarkarung, 1986). Castafio-Zapata (1991a) introduced 200 of those lines from CIAT to Sumatra, Indonesia. More than 60% of the lines, in addition to being highly tolerant to A1 toxicity, were resistant to blast disease, the most important limiting factor of upland-rice production in acid soils. A similar successful approach has been followed for cassava (E1-Sharkawy, 1993).

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Methods have been developed for screening and testing host-plant resistance and for tolerance to several biotic and abiotic stresses. In rice, for instance, the International Network for Genetic Enhancement of Rice (INGER), IRRI, Philippines, organized nurseries for finding and testing resistance to several major diseases. The program has identified many disease-resistant rices. The same has been achieved at CIAT, Colombia, for several biotic and abiotic constraints of upland rice production (Rao etal., 1993), cassava (E1-Sharkaway, 1993), and common beans (Pachico and Schoonhoven, 1989). The CIAT Bean Program decided to concentrate on a low input strategy of resistance instead of breeding for yield because beans are susceptible to many insect pests and pathogens and because poor farmers did not have access to chemical control (Pachico and Schoonhoven, 1993). Although plant breeders are incorporating resistance into commercial varieties, good sources of stable resistance have not been found for many important diseases. Varieties resistant to one disease are often susceptible to others. Breeding must emphasize varieties that resist a wider complex of diseases (Castafio-Zapata, 1991b). Incorporating multiple resistance into commercial varieties had been a long undertaking and the so-called 'pyramiding of resistant genes' has had only limited success. The most important disadvantage has been the breakdown of resistance due to new physiological races of the pathogens, especially obligate parasites such as those that cause rusts and downy mildews and facultative parasites such as the causal agent of rice blast. In wheat, many rust races that were prevalent in the past are insignificant today because of breeding that incorporated specific resistances into modern wheats. However, new rust races continually appear to threaten production because of the pathogen's capacity for mutation and sexual reproduction (Wiese, 1987). Downy mildew is one of the world's worst agricultural diseases because it attacks many crops (Moffat, 1992). The causal agent of rice blast, P. oryzae, is highly variable and the rice varieties having race-specific resistance are rapidly overcome in the tropics. A few commercial varieties have been highly resistant to the pathogen but only for a short time (Ahn, 1981; Castafio-Zapata, 1991b). Hopefully, however, this drawback is expected to be overcome by using other breeding strategies such as multilines, gene deployment, varietal diversification, or concentration of slow blasting components (Castafio-Zapata, 1981). In addition, recent advances in understanding both plant defense mechanisms and pathogen action are opening the door to designing new strategies for helping plants turn aside infections (Moffat, 1992). Recent advances in biotechnology now allow the DNA of genes to be isolated chemically and transferred via cell and tissue culture into whole plants. Plant breeders have made little effort to work with farmers. This is ironic since breeding is one of the things that farmers and scientists both do. For example, the Lenca of Honduras keep a red maize for the disease resistance it gives to other varieties (Ard6n-Mejia, 1993). Early experiences with farmers and breeders have been positive. Ashby et al. (1989) helped farmers and CIAT work together;

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researchers benefited from knowing the qualities farmers select for. The bean varieties chosen by farmers for early release were grown for more years than finished varieties, saving breeders time and money while giving farmers more acceptable lines (Sperling etal., 1994). Genetic erosion is perhaps the greatest threat to the sustainability of plant breeding. US vice-president A1 Gore thinks it is the greatest threat to the global food system (Gore, 1992). Plant breeders depend on genetic material from wild plants and from landraces. Both are disappearing fast. Habitat destruction extinguishes many wild congenerics of crops. Although some farmers continue to grow a mix of HYVs and traditional varieties (Bellon, 1991), many landraces are lost as farmers adopt plant breeders' varieties. A few private organizations are working to save landraces. Native Seed Search helps organize farmers in the US southwest who raise traditional crops (Soleri et al., 1991). Saving seeds on-farm is becoming more important in light of the limitations of seedbanks. A seedbank in a revolution is more vulnerable than a shopping center in a riot. Since 1989, two seedbanks have been destroyed in the former USSR, one in Georgia and another in Azerbaijan (Gillis, 1993). Shining Path guerrillas blew up the CIP (International Potato Center) buildings in Peru (Gore, 1992). Plant breeding for pest management is probably not sustainable. Insects overcome the resistance of new plant varieties as easily as they develop resistance to insecticides (Simms, 1987). The HYVs in general were bred for high yield, and tend to be more susceptible to insect damage, as shown by a study of maize in Ecuador (Evans and Zambrano, 1991). Harms (1992) admits that HYVs have less pest and disease resistance than landraces, but claims that by paying more attention to resistance and by using new tools (including genetic engineering) plant breeders can breed genetic resistance into many crops (Harms, 1992). Biotechnology may well help breed pest resistance into plants, although pests will probably evolve their way around the resistance just as fast as they adapt to pesticides or conventionally bred crop varieties (Walgate, 1990). Reducing losses to pests may be the plant breeders only option, if it is true that we have already reached the yield potential of the HYVs and chemical fertilizer (Byerlee and Husain, 1993). E1-Sharkawy (1993) is hopeful that cassava breeding can still double farmers' yields, but there is more potential for plant breeding of cassava than other crops, because scientists have studied cassava less than others.

V. BIOLOGICAL CONTROL AND SUSTAINABILITY Biocontrol is a possible alternative to intensive pesticide use. Even though synthetic fertilizers and pesticides produce high crop yields, environmental balances have been disrupted and considerable crop damage by insects and pathogens still prevails. According to Waage and Greathead (1988), most reviews on biological control

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begin with a defensive list of the successes of biocontrol. This is probably because the public still has a negative view ofbiocontrol because of some early experiences with vertebrate predators (what we call mongoose paranoia): people think that once an introduced natural enemy has eliminated the pest, it will become a nuisance itself. The Organization of African Unity almost failed to accept the mealybug project because of such fears (Waage and Greathead, 1988). Biocontrol is becoming so well established that even chemical giants like CibaGeigy are getting involved, researching parasitic wasps and entomopathogens (Sechser, 1989). Although classical biocontrol has been tried on about 300 pests, only about 120 attempts have worked. However, the biocontrol successes are impressive because once a natural enemy of a pest is established no further investments are needed and the introduced species pose no environmental risks (Cate, 1990; Pimentel, 1991; Scott, Chapter 7, this volume). Parasitoids have been successfully established in too many places to mention. Some successes include control of citrus blackfly (Aleurocanthus woglumt) in Oman (Al-Mjeni and Sankaran, 1991), Florida (Tefertiller et al., 1991) and Central America (Quezada, 1990) and control of cereal aphids in Chile with four parasitic hymenoptera (Quiroz, 1983). Control of cassava mealybug (Phenacoccus manihott) in Africa has been the biggest biocontrol project and has saved billions of dollars annually in crop losses (Mwanza, 1993; Plucknett, 1993). Conserving native natural enemies is also important (Pollard, 1991). Examples include rearing dragonfly larvae (Odonata: Libellulidae) and releasing them in water supplies in Burma to control mosquitoes Aedes aegypti (Diptera: Culicidae) (Sebastian et al., 1990). In Bangladesh some farmers have maintained rice yields without pesticides by cultivating insectivorous fish in their rice fields (Kamp et al., 1993). Kgdnay reports taking charge of a cane plantation in Argentina in 1967. Previous management had been 'fighting ants just because they were ants'. Once they stopped killing ants, other insect pests disappeared, as the native ants began to fulfill their role as pest predators (Kgdnay, 1987). Experiments in Nicaragua showed that insecticides killed ants and increased insect pest populations (Perfecto, 1991). Ants are among the best pest control agents in the tropics. They recruit other workers to prey, have large populations, and can survive even when pest populations are low (Way and Khoo, 1992). The most important way to conserve native natural enemies is to stop using insecticides, as the Indonesian case has shown (Oka, 1991; van de Fliert and Winarto, 1993). Hoy (1988) supports genetic improvement of natural enemies to make them pesticide resistant. Entomopathogens are being used increasingly in the developing world, including Thailand, Egypt and Brazil (Jones, 1988; Jahn, 1992). It remains to be seen if entomopathogens are much of an improvement over chemical insecticides. While less toxic to humans and other vertebrates, pests develop resistance to biological insecticides (Simms, 1987; Groeters etal., 1993). One important difference between known biological agents and synthetic chemicals is that biologicals are almost always protectants, while many modern

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insecticides and fungicides are systemic and also may be used once infection has started (Jacobsen and Backman, 1993). Exciting developments in biological control of plant diseases have occurred during the past 20 years (Lewis and Papavizas, 1991). Only five biocontrol products are now registered for use by the US Environmental Protection Agency (EPA) for control of plant diseases (Jacobsen and Backman, 1993). There are few products because biological control research for product development has been done for only 15-20 years, while synthetic fungicides have been under development for more than 60 years. Pest resistance has not been reported for biological agents, except in Galltrol-A for control of crown gall (Agrobacterium tumefasciens) (Smith & Townsend) Conn. (Ryder and Jones, 1990) and Bacillus thuringiensis Berliner for control of diamondback moth (PluteUa xylosteUa L.) (Groeters etal., 1993). Nevertheless, this may reflect the limited development of biocontrol products instead of an inherent low potential for development of resistance to biological control products. IPM programs need more biocontrol products for controlling diseases. These products have to be as efficient as common pesticides. Micro-organisms will probably assume an increasingly prominent role as pest control agents as we look forward to new environmentally responsible technologies. To control many pests in the future, biological control may be the technology of choice, and scientific interest and reallocation of resources towards using live fungi, bacteria or virus for agricultural pest control has increased significantly (Jacobsen and Backman, 1993).

Vl. WEEDS

We have neither the expertise nor the space to address weeds properly. This is unfortunate because weeds are potentially the most damaging pest (Hoy, 1988). Genetically engineered crops, bred to be resistent to herbicides, are an ecological menace, encouraging herbicide use and damaging the environment (Simms, 1987; Gore, 1992). Forty-one weed species are now resistant to herbicides (50 according to Dover and Croft, 1984) and 32 diseases of crop plants are caused by herbicides. Reduction in levels of soil organic matter, degradation and contamination of groundwater, human cancers and general impoverishment of the ecosystem have all been associated with herbicide use (Kloppenburg, 1988). There has been some work with biological control of weeds, especially by using plant diseases (Strobel, 1991). Despite their other disadvantages, weeds may be sources of flowers for beneficial insects, and encourage neutral insects which may serve as alternative food for predators or parasites (Altieri et al., 1977).

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VII. SOIL HEALTH A N D SUSTAINABILITY

The basis of sustainable plant protection is plant health, and soil fertility is crucial. Chemical fertilizers are not sustainable (Stinner and House, 1987; Crews and Gliessman, 1991). A tonne of fertilizer increases yields less each year it is applied (Ehrlich and Ehrlich, 1990). Potassium and phosphorus are minerals. They have to be mined. Like fossil fuel, one day they will be exhausted. The best way to improve and restore soil quality and productivity is by proper and regular additions of organic matter, especially by crop rotations, cover crops, crop residues, animal manures, composts and reduced tillage (Papendick and Parr, 1992). Plant health depends on the biostructure of the soil (Kgtlnay, 1987). Beneficial micro-organisms recycle nutrients, decompose organic waste and protect plants from pests. These micro-organisms thrive on organic matter, which also detoxifies soil (Parr etal., 1992). Adding green manure controls soil pathogens by increasing the amount of saprophytes such as Trichoderma spp. In India, green manure and crop rotation to control common scab of potatoes (Streptomyces scabies (Thaxter) Waksman & Henrici) has been known for 60 years (Millerd, 1922, 1923, cited by Trehan and Grewal, 1980). A startling 0.7 % of the world's topsoil is lost annually (Brown and Wolf, 1984; cited in Parr etal., 1992; see also Gore, 1992, chapter 6; Hobbelink, 1991, chapter 1). Agriculture has become like a business rushing towards bankruptcy by eating away its own capital assets. Again, there is no easy solution. Canadian agriculture of the 1930s was low-input, but had higher rates of soil erosion than now (Gracey, 1990). There were problems with soil erosion in ancient Mexico (Garcfa-Cook and Merino-Carri6n, 1990). Maintaining soil fertility also means keeping the soil fr,~m washing and blowing away and from becoming loaded with salt and other toxic minerals. Soil conservation is one of sustainable agriculture's greatest needs. Chemical fertilizer hurts soil structure by depriving soil of organic matter (Mountjoy and Gliessman, 1988). Chemical fertilizers build up toxins in soil (Janzen, 1973; Parr etal., 1992). In India, continuous use of fertilizers has deteriorated soil fertility and reduced crop yields (Perumal, 1993). In Tanzania farmers adopted a chemical approach and their maize yields went from 4 t down to 1 t. Fertilizer use lowered production, increased pests and damaged the softs (Warden, 1993). Sometimes chemical fertilizers improve plant growth and increase yields, but they also predispose plants to diseases and insect pests. Different kinds and amounts of fertilizers affect the development of plant diseases. In rice, the supply of nitrogen is essential for plant growth, helping to increase yields everywhere rice is planted. Nevertheless, high doses of nitrogen can reduce yields if rice blast attacks either foliage or panicles (Montoya, 1983). Special attention must be given when recommending nitrogenous fertilizers at seedling and panicle stages, when rice plants are more susceptible to P. oryzae. In general, more nitrogen

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fertilizer induces greater severity of rice blast (Castafio-Zapata, 1991a). Similarly, high nitrogen fertilizer rates favor higher brown planthopper (N. lugens) populations (Suhardjan and Iman, 1980). Rice farmers have to use less nitrogen fertilizer on HYVs to avoid serious outbreaks of either blast disease or brown planthopper. Nitrogen increases plant vigor and rate of growth, which make plants more susceptible to pathogens. Vigorously growing crops are generally more susceptible to obligate parasites, such as rusts and powdery mildews of wheat as well as virus diseases, such as tobacco mosaic virus (Palti, 1981). Some important facultative parasites also benefit from high crop vigor, including P. oyzae, Thanatephorus cucumeris (Frank) Dork. and Sclerotium rolfsii Sacc. on rice (Ou, 1981), and Stenocarpella maydis (Berk) Sutton and Helminthosporium turcicum Pass. on maize (Schurtleff, 1980; Palti, 1981), among many others. From the crop protection perspective, nitrogen fertilization has to be based on information about the pathogens likely to attack the crop and the frequency and severity of the expected attack (Palti, 1981). Nevertheless, this may not be possible in developing countries where most farmers have limited access to this kind of information. It is not necessarily true that chemical fertilizers are required to maintain high yields. One study of farmers in the Philippines showed that using less pesticides and chemical fertilizer led to fewer pest problems, good harvests and lower costs (Garcia-Padilla and Padilla, 1993). Gupta and Aggarwal (1992) report some experiments with intercropping and organic matter in which organic fertilizers mixed with chemical N provided acceptable yields. Crews and Gliessman (1991) show that high-yielding raised fields in Tlaxcala, Mexico have supported dense human populations since pre-Colombian times by recycling organic matter. In a thoughtful paper on nitrogen fertilizer, Greenwood (1990) stresses the importance of N to sustain high yields and concludes that N runoff probably is a very small threat to human health and the environment. N has the disadvantage of creating more greenhouse gasses. With N fertilizer, farmers can raise more fodder and more cattle. Cows are poor recyclers of N. They urinate more N in one spot than the soil can absorb, so much of the N is lost to leaching (Greenwood, 1990). Greenwood argues in favor of continued chemical N and dismisses recycling of organic manure. ' M a n simply does not know how to recycle nutrients when he grows the crops he needs for food' (Greenwood, 1990). Greenwood is wrong; farmers do know how to recycle soil nutrients. Traditional European farmers learned to overcome that problem by keeping cattle in stalls. Stall bedding of gorse and other forest plants absorbs urine and manure, which are spread onto the fields each spring (Bentley, 1992a). Greenwood's attitude is typical of the agricultural establishment's antagonism to recycling organic matter. This was not always so. In 1908, the former Chief of the Division of Soil Management for the US Department of Agriculture, F. H. King traveled through Asia, marveling over the highly evolved farming systems that recycled everything from crop residues to night soil (King, 1911). Chinese farmers had successfully used these techniques for over 40 centuries. King was struck by the sustainability

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of intensive Chinese agriculture decades before the word 'sustainable' became popular. In his insightful book on how to manage an agricultural research center, John Nickel complains that 'too much talk about minimum inputs will lull uninformed policy makers into complacency by leading them to think that there is an easy way out; that agricultural development can somehow be accomplished by a combination of peasant wisdom and organic farming' (Nickel, 1989). On p. 117 he says bluntly that organic farming is a 'non-starter'. We sympathize with Nickel; there is no easy way out of the challenge of feeding the world' s billions without stripping the planet bare. 'In spite of all the positive characteristics of traditional African agriculture, and its success in supporting the population for generations, it seems unable to cope with greatly increased population densities and changing social and economic conditions (Cleveland, 1990)'. However, the only farming systems with demonstrated sustainability, the ones that have existed for centuries, are all based on peasant wisdom and organic farming. Some recent technical advances, like classical biocontrol, may also be sustainable, although that has not yet been proven. We suggest either building on organic farming, carefully, or for those already committed to chemical-intensive agriculture, work back away from heavy chemical use. Dismissing organic agriculture out of hand is not scientific. The value of organic inputs, and of peasant wisdom, must be tested empirically before being discarded.

VIII. SOCIAL SYSTEMS AND SUSTAINABLE AGRICULTURE Ecological entomologists who would never dream of writing about a pest without discussing its natural enemies are often content to ignore soil and water. Many who write about agriculture leave out the farmers, or else include them as twodimensional, cardboard people with no culture, no social, political or economic environment. People have to be seen as the most important part of agriculture. Plucknett (1993) boasts about the achievements of agricultural research (especially the C G I A R system) in bringing about the Green Revolution and averting mass starvation. He chides Ehrlich (1967) for predicting hundreds of millions of famine deaths in the 1970s and 1980s. Unfortunately, Ehrlich may still have the last word, if not the last laugh. We now worry about new problems that Ehrlich didn't dream of in the 1960s: the extinction crisis, rainforest destruction, AIDS, acid rain, a hole in the ozone, a run-away greenhouse effect that could drown the most populous parts of the planet and throw the Earth's climate out of kilter (Ehrlich and Ehrlich, 1990). Famine and disease are already with us (Gore, 1992), but Homer-Dixon etal. (1993) claim that mass violence linked to land shortage could replace starvation as a leading cause of death and disruption. They cite several examples, including the case of 1700 Bangladesh settlers in India who were massacred in 5 h by Lalung Tribespeople claiming settlers were taking the best land (Homer-Dixon etal., 1993). Civil war could threaten the existence

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of international agricultural research centers spread out over the developing world. Big agriculture is killing the Earth to make money. Chemical companies are buying seed companies and biotechnology companies to breed seeds that maximize chemical use (Kloppenburg, 1988; Gore, 1992). The IARCs and private companies have collected seed from farmers, which was used to breed new varieties, which the private companies increasingly sell back to small farmers (Kloppenburg, 1988, 1990). It is one of the social inequities with no easy solution. Increasingly known as 'farmers' rights', the idea that local people should be paid for germplasm taken from them is flawed by the difficulty of deciding exactly who should get the money and how (governments? NGOs (non-government organizations)? hundreds of millions of isolated peasant farmers? new bureaucracies?). Biotechnology promises to bring many of the same kinds of equity and environmental problems as the Green Revolution. An important difference is that the Green Revolution was headed by the IARCs working with a few crops. Biotechnology could work with hundreds of species, is led by private companies in the industrial north and they are being bought out by the largest chemical companies (Hobbelink, 1991). Biotechnology is now getting more funds from the USDA, while biological control gets less, even though biotechnology has not yet solved any pest problems (Luna and House, 1991). Sustainable agriculture requires more knowledge about ecological processes than high input farming (Stinner and House, 1987). There are few journals like ILEIA Newsletter, CIKARD News, Honey Bee or Indigenous Knowledge and Development Monitor that actively seek to document the knowledge and experiments of traditional farmers. Peasant farmers do not know everything. They often know nothing of causal agents of disease, of insect metamorphosis, of parasitoids or even of arthropod predators (Yabar, 1990; Bentley, 1991, 1993; Mata, 1991; Heong et al., 1992). A study of small farmers in Costa Rica showed that they had little idea that pesticides were dangerous either to people or the natural environment (Meir, 1990b). But their knowledge is nothing to sneer at. Traditional knowledge is a priceless store of information about how things were done in the past, when people were fed successfully without eroding the very base of farming. Not all old farming systems were sustainable; the Classic Maya, the Anasazi and ancient Mesopotamia are just three examples of crashed agroecosystems (see also Denevan, Chapter 2, this volume). Nor is all modern technology unsustainable; classical biocontrol, nitrogen fertilizer, Bordeaux mix and semiochemicals may all be. Sustainable techniques mimic natural ecological processes. Classical biocontrol and soil antagonists both work because they subject pests to the pressure of natural enemies. Cultural practices are sustainable when they imitate natural patterns of soil formation or biodiversity. Host-plant resistance that is based on many lines of resistance is probably sustainable because it is similar to the complex protection that plants evolve under natural selection; pest resistance based on one line will be easily overcome by the pests. Most synthetic pesticides are at odds with nature

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and unsustainable. However, some of the recent popular alternatives are no more natural nor sustainable. Bombarding a field with an entomopathogen is unlike any ecological process, and insects rapidly evolve resistance to insecticides based on Bacillus thuringie~is, for example. Botanical pesticides are pseudonatural placebos. A plant's native protection chemicals are meant to be used in the plant, not concocted for spraying on other species. We expect that if any botanical pesticides are effective, pests will quickly evolve resistance to them. The fact that much of traditional information pertains to a world of lower population density is no excuse to disregard it. So far, there has been a lack of an ecological, traditional agricultural system perspective in formal tropical agricultural research (Ehdich and Ehrlich, 1990). Traditional technical knowledge is more dynamic than we usually give it credit for. British anthropologist-geographer Paul Richards has described numerous farmer experiments in Sierra Leone; some farmers select new rice varieties (1985, 1986, 1989, 1991). The Chilean entomologist Miguel Altieri (1984, 1986, 1987, Chapter 10, this volume) has consistently argued that farmer practices be taken seriously in pest control. The term 'farmer participation' has been coined to refer to scientists and farmers working together. So far the idea has generated few technologies and has been too vaguely defined to be of much use in overcoming scientists' reluctance and inability to collaborate with small farmers (Tripp, 1989; Bentley, 1991). This is unfortunate, because farmers also experiment, and scientists could learn more by working with them. Few people know that the most successful fungicide ever, the Bordeaux mix, was invented by a nineteenth-century French farmer who first devised it to keep people from eating his ripe grapes. A scientist (Millardet) recognized its value as a fungicide (Lang and Clutterbuck, 1991). We have encouraged Central American farmers to invent sustainable pest control technology by systematically filling in the gaps in their knowledge, while validating and respecting much of what they already know. This helps the campesinos create a fresh perspective on pest control. Farmer graduates of our training have moved wasp and ant nests, lured wasps and ants onto crops with sugar and invented traps and botanical herbicides for pests (Bentley, 1992b,c, 1993; Bentley a al., 1993, 1994). Until now, farmers have been missing from much of scientists' work in biocontrol; farmers are especially important allies for conserving and manipulating native natural enemies (Andrews a al., 1992). Traditional knowledge is not the whole answer, but it is part of the solution rather than part of the problem of today' s agriculture. One of the most promising signs in recent years has been the publication of David Thurston's (1992) book on traditional management of plant diseases by small farmers. Thurston documents practices farmers have used to control and especially to prevent plant diseases. Cultural practices have adaptive value; existing technology is the product of a long evolution and would not exist for long if it were grossly maladaptive. Thurston is a plant pathologist who has gained respect for traditional farmers. David Cleveland and Daniela Soleri are anthropologists who have taken the trou-

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ble to learn agronomy. Their book on dryland gardens is an unusual blend of respect for traditional peoples and practices with a good technical background (Cleveland and Soleri, 1991). As the American geographer Gene Wilken said after describing the ingenious farm technology of traditional Mexican farmers: 'It is also condescending to view traditional farmers as sagacious husbandmen, imbued with infallible folk wisdom, in mystic harmony with the environment' (Wilken, 1987). The bases of a sustainable pest control in the developing world are the traditional practices of small farmers, combined with creative modern technologies to come up with pragmatic techniques to save our crops from pests and disease without destroying the soil and the Earth. We will need everything from manure to biotechnology to survive into the twenty-first century.

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14 THE DIVERSITY OF FUNGI ASSOCIATED WITH VASCULAR PLANTS: THE KNOWN, THE UNKNOWN AND THE NEED TO BRIDGE THE KNOWLEDGE GAP P.F. Cannon and D. L. Hawksworth International Mycological Institute, Bakenham Lane, Egham, Surrey T W 2 0 9TY, UK

I. Introduction II. The Number of Species of Fungi A. Known and Estimate Species Numbers B. Species Concepts and Individuality III. Range of Associations with Vascular Plants IV. Ecology and Site Inventory V. Distribution VI. Fungi on Different Plant Families A. Trends in Species Description B. Comparison of Fungi on Gramineae and Cyperaceae C. Comparisons of Fungi Associated with Other Plant Families D. Emphasis on Fungi of Economic Importance E. Fungi Associated with Cactaceae VII. Conclusions Acknowledgements References

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I. I N T R O D U C T I O N T h e last 10 years have witnessed an immense and unprecedented surge in interest in, and concern for, the diversity of life on Earth. T h e prime focus for this concern has been the macro-organisms, particularly vertebrates and vascular plants. However, only during the last 3 years have those concerned with the enumeration, cataloguing, monitoring and conservation of biodiversity started to appreciate the extent and significance of microbial diversity. T h e fungi comprise a major part of this hidden realm. W h e n a long-neglected or previously unrecognized subject area suddenly comes to the fore, there is inevitably a dearth of informed znd contemporary reviews. This contribution is an attempt to redress that situation with respect to ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 Academic Press Limited All rights of reproduction in anyform reserved

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the major portion of fungal diversity, that associated with vascular plants. We have endeavoured to assess what is known, the extent of the unknown, and explain why there is a need to bridge some of the knowledge gaps so identified. These questions are asked with respect to the numbers of fungi associated with plants, the range of associations, ecology and distribution, and differences between host families. In this chapter, the term 'host' is used in its social rather than pathological sense, without necessarily implying either dependency or antagonism in interrelationships.

II. THE NUMBER OF SPECIES OF FUNGI A. Known and Estimated Species Numbers The world's fungi are known most inadequately. The number of known species was estimated to be in the order of 70000 by Hawksworth (1991), and this number is increasing at a rate of around 1700 per year. On the basis of the substratum indices in the standard catalogues of fungal names, particularly the 'Index of Fungi', we judge the number on or directly associated with vascular plants or plant products to be at least 80 % (currently about 60 000 species). This proportion is likely to be conservative, as most fungi reported to be associated with such substrata as air, water and soil in fact derive their nutrition directly from plant material. Such figures necessarily remain estimates as no world checklist of accepted fungal species exists. Assessing the total number of species of fungi on Earth is problematic. However, three independent lines of argument have led to a conservative working estimate of 1.5 million species (Hawksworth, 1991). This suggests that: (1) we know only about 5 % of the fungi on Earth; (2) there are around six times as many fungi as vascular plants; and (3) the fungi are the largest major group of organisms apart from the arthropods, with the possible exception of the 'unculturable' bacteria (Triiper, 1992). The 1.5 million estimate has not been seriously challenged. Questions raised by May (1991) with regard to the proportions of new taxa found on collecting trips being less than 95 % have been addressed elsewhere with additional data (Hawksworth, 1994). An admittedly conservative 'working figure' of 1 million was used by Hammond (1992) for the fungi in a critical review of the world's estimated biota. Large margins of error are inherent in all such estimates. The major uncertainties relate to the numbers of species obligately associated with insects in the tropics, and the degree of host specificity of fungi on tropical plants. In the latter context, as a result of studies especially on Acacia and Banksia in Australia, Pascoe (1990) estimated that there might be at least 10 times as many fungi as vascular plants (i.e. about 2.7 million species), and Smith and Waller (1992) considered 1.5 million too low as they felt there were probably 1 million undescribed fungi on tropical plants alone.

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Since the reviews of Hawksworth (1991, 1994), some additional examples of fungal diversity associated with particular host plants have caught our attention. Hyde (1992) discovered 43 fungi on Nypafruticans in Brunei. Kohlmeyer and Volkmann-Kohlmeyer (1993) described nine fungi from Juncus roanerianus on the east cost of the USA, and found it necessary to introduce four new ascomycete genera. In the case of ectomycorrhizal fungi in the tropics, R. Wading (unpublished) collected 148 such fungi along one 7.5-km trail in Cameroon of which 82 were new to science. Roberts et al. (1986) found no fewer than 98 species of fungi from symptomless, surface-sterilized sunflower fruits (achenes), although around half of these were only apparent in stored samples and it was not made clear what proportion was viable. Fisher and Petrini (1990) identified 89 fungal species as endophytes from wood of Alnus species from four sites in England and Switzerland. Bills and Polishook (1991) isolated as many as 69 fungal species of microfungi from bark of Carpinus r from a single locality in northeastern USA, and a total of 155 species from five sites in that region using only three standard media. Not all the fungi in these examples were novel, and a significant proportion proved difficult to characterize fully due to lack of proper comparative data and problems in assessing host ranges. Nevertheless, these studies serve to emphasize the often enormous diversity of fungal taxa associated with single plant species. There has not yet been any critical study carried out of the total fungal biota of an individual tropical tree growing in its native habitat. We know that these frequently support large numbers of novel species from the studies ofA. C. Batista and coworkers, who described about 3500 species from Brazilian forests in the period 1954-1972, but we lack precise information about fungal host ranges. Batista's studies (which did not include research into endophytes) showed that a single leaf may simultaneously support 10-12 fungi, including three to five new to science, but we have no evidence that such leaves are representative of the total number belonging to the individual tree, or indeed to what extent the proportion of novel species will decline upon successive examination of further leaves from the same tree. We also do not know whether adjacent trees of different species have identical species, or a completely different array of fungi; knowledge of host specificity for most tropical fungi is rudimentary indeed. Mycological succession as leaves develop, senesce and decay will result in further diversity.

B. Species Concepts and Individuality Difficulties in assessing species numbers are exacerbated by the lack of consensus as to what type and degree of discontinuity is appropriate between fungal species. No unified species concept exists, though it is questionable if one is desirable in such an ecologically and genetically diverse group. Species have traditionally been based on discontinuities in morphological features, or in some cases merely occurrences on particular hosts. The relative merits of morphological, as opposed to biological and phylogenetic, species concepts are only starting to be debated

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by mycologists. Since the review of Burnett (1983) there has been remarkably little informed discussion upon this subject, though there has been a gradual trend away from morphology towards phylogenetic species concepts (Blackwell, 1993); but see also Vishniac (1992) and Vilgalys and Hibbett (1993). For most of the described fungi such debates are academic, as apart from well-known crop pathogens and spoilage organisms, few species are studied in adequate detail. We estimate that about 25 % of fungal species are known only from a single, often fragmentary, collection, with a usually inadequate description. Only about 17 % are represented in the world's culture collections (Hawksworth, 1991), and are thus in practice available for critical analysis. Were species concepts to be based on intersterility, the figure of 1.5 million would have to be considerably inflated. Although such an approach is clearly both problematic and in most cases impractical, it is becoming clear that many recognized 'species' include large numbers of non-outcrossing populations which propagate clonany, either on an apparently permanent basis or oscillating between outcrossing and non-outcrossing breeding systems (Rayner, 1990, 1992). Brasier (1987) documents numerous instances where traditional morphologically based taxa have been recently subdivided, largely using genetically based differences. More recent examples of this trend include the differentiation of European and North American taxa within the morphological 'species' Heterobasidion annosum (Otrosina et al., 1990), and within species of Laccaria previously assumed to have cosmopolitan distributions (MueUer, 1991). Five separate mating populations have been identified within the widespread 'species' Gibberellafujikuroi (anamorph Fusarium moniliforme; Klittich and Leslie 1992). Anderson et al. (1992) suggest that degrees of interfertility are affected by geographical isolation, sympatric taxa showing a higher level of mutual sterility than separated populations. The absence or comparative rarity of sexual reproduction in many fungal species makes interpretation of intersterility data particularly difficult when considering species delimitation. The number of vegetative compatibility groups within species is sometimes very large; at least 50 have been identified from a sample of only 100 strains of GibbereUafujikuroi (Anderson etal., 1992), and 25 were found in 31 isolates of Sclerotinia sclerotiorum (Kohn et al., 1990). The systematic and evolutionary significance of such a plethora of vegetative compatibility groups needs careful interpretation (P. D. Bridge, pers. comm.). A further problem area, about which there has been more debate recently, is the large number of fungal species which either lack the ability or choose not to undergo meiosis during their life cycle. Historically, it was considered that most if not all of these mitotic fungi would be found to have sexual stages, but there is now general agreement that many mitotic species have diverged irrevocably from their meiotic ancestors. There is now much interest in removing these fungi (often referred to as deuteromycetes or fungi imperfecti) from their historical taxonomic limbo and integrating them into a general fungal classification. The proceedings of a recent conference on this subject edited by Reynolds and Taylor (1993) contains much valuable information. Molecular divergence is used widely

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in species definition in yeasts (Kurtzman, 1987, 1993), and such evidence will be increasingly useful both in characterization of f'damentous fungal taxa and linking mitotic species with their meiotic relatives. Much work remains also in the refinement of species concepts in biotrophic groups suGh as the Erysiphales and Phyllachorales, most or all of which cannot be grown in pure culture using current techniques (Braun, 1987; Cannon, 1991). This means that it is very difficult to assess morphological distinctions between taxa in the absence of variation caused by physical and chemical differences of their hosts. Clearly, host ranges cannot be properly determined in the absence of this information. The recent development of P C R techniques (Foster et al., 1993) and in particular methods for analysis of the DNA contained in dried specimens (Bruns et al., 1990) will be of considerable practical help in isolating fungus variation from host influences, but many problems remain in obtaining samples in which DNA has not deteriorated (Haines and Cooper, 1993). Almost all experimental studies on the variation within morphologically defined fungus species have been carried out on economically important taxa, usually agricultural or forest pathogens. The selection pressures and therefore speciation processes which gave rise to these are clearly not typical of the fungi as a whole. It is clear for these organisms that in many instances very rapid speciation is taking place, in order to colonize new, man-made ecosystems. It is very likely, for example, that the host-specific varieties of Gaeumannomyces graminis have evolved recently (O'Dell etal., 1992), and that differences at isozyme level between strains of Puccinia striiformis taken from wheat and barley (Newton et al., 1985) represent the beginnings of divergence. While the presence of widespread monoculture and genetically similar host cultivars may increase the rate of parasite speciation, it is not unreasonable to speculate that fungi in natural ecosystems are undergoing similar patterns of evolutionary development. Alternatively, strongly aggressive forms may be present at low levels in natural ecosystems, their effect being mediated by genetic variability present within naturally occurring populations or other competitive factors (including natural biocontol by mycoparasites). Even the definition of an individual is fraught with difficulty for the mycologist. In practice, individual fruit-bodies produced by underground mycelia, or produced on different parts of a plant, tend to be processed as separate items even though they may in reality be connected by hidden hyphae. A graphic example is the recognition of an apparently genetically homogeneous mycelium of ArmiUaria bulbosa in Michigan, which extended over at least 15 ha and weighed an estimated 10 t (Smith et al., 1992). Although the interpretation of that and similar claims is open to question in several details (Brasier, 1992), and barriers between different individuals can be developed in wood (Boddy, 1992, 1993), the general thesis is inescapable. Taking the other extreme, it is tempting to consider that as in most fungal species almost all individual cells are capable of both independent survival and reproduction, these should all be regarded as separate entities, especially noting the widespread incidence of heterokaryons in fungal hyphae. In

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groups where coenocytic hyphae are commonly encountered, even nuclei might be considered as separate individuals.

III. RANGE OF ASSOCIATIONS WITH VASCULAR PLANTS The great majority of fungal species are dependent on vascular plants for their existence. A large proportion obtain the carbohydrates and other nutrients they require directly from vascular plants, utilizing either dead tissue in nutrient recycling, or cells and nutrients from living plants, in antagonistic or mutualistic associations. However, the interdependence extends further. Many animals, including insects, which directly (e.g. herbivores, pests) or indirectly (e.g. carnivores, parasitoids) feed on plants or plant products, are also dependent on vascular plants for their survival, as are fungi which have direct relationships with those animals. In addition, the large number of lichen-forming fungi restricted to bark, leaves or wood are dependent on plants for physical support and exposure to sunlight, if not for other nutrients (Hawksworth, 1988). Fungi are essential components of all ecosystems on Earth (Trappe and Luoma, 1992), and all plants are dependent upon them in return. In ecological terms, the popular image of fungi as agents of disease and decay is positive rather than negative. Fungi are one of the most important groups of plant tissue decomposers (Cromack and Caldwell, 1992), releasing nitrogen and other essential compounds for recycling by plants. Most phanerogams have intimate associations with fungi, in mutualistic and often also antagonistic relationships. Christensen (1989) has provided an excellent review of the role of fungi in ecosystems, identifying 20 separate functions. These include organic matter decomposition, release of elements, transport of elements and water, soil modification and detoxification, and the instigation of antagonistic and mutualistic symbioses. The associations between fungi and plants take various forms, and there are few clear dividing lines separating the types of relationship. The nature of the association frequently varies according to the position of the partners in their life cycles. Our definitions alter depending on the position from which we view the association (Janzen, 1985), and are coloured by our preoccupation with croppathogen associations. For example, Lophodermium seditiosum is regarded by forest pathologists as a serious pathogen of Pinus sylvestris, especially in nurseries producing Christmas trees in North America (Staley, 1975; Minter etal., 1978). From the standpoint of an individual infected tree, the fungus has a deleterious effect upon growth, but as it usually will not kill it completely, the tree's unsightly appearance makes it less likely to be felled for an ornament. In such circumstances, the fimgus and plant unexpectedly have a mutually beneficial relationship. This fomn of association may be not uncommon in natural ecosystems, and is probably almost essential for the continued existence of both plant and fungus. The fact that disease epidemics in undisturbed natural ecosystems are rare, suggesting steady states for most associations, supports this hypothesis.

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Taking a more long-term point of view, a relationship with Lophodermium seditiosum may still be advantageous for Pinus sylvestris as a species. Although individuals entering into this particular association (i.e. those regarded by plant pathologists as susceptible) will be less likely to be propagated for further stocks of Christmas trees, such propagation is irrelevant from the point of view of gene conservation; Christmas trees are rarely allowed to grow large enough to set seed. In these circumstances, the species is dependent on foresters being less than totally efficient at eliminating 'disease' reservoirs. The interrelationships between fungi and plants are very poorly known, except in the restricted cases of major crops and their most significant pathogens. It is very common for a fungus which occurs within living plant tissue as an endophyte or a biotrophic parasite to switch to saprobic nutrition once the plant tissue has died or become moribund, often only producing spores to form the next generation once the plant is dead. Similar abilities are usually essential to continued survival and offspring generation for necrotrophic parasites (Webber et al., 1987). Such well-known aggressive pathogens as ArmiUaria species may persist for decades in decaying root systems before attacking new hosts (Anderson et al., 1992). Many fungi which are Uncritically regarded as necrotrophic parasites, especially those causing leaf spots or stem dieback rather than systemic disease, may not significantly hasten the death of the plant or plant part in which they reside, and indeed in some instances the sacrifice of this tissue may be compensated for by contributions by the fungus to the plant of metabolic products. There has been a recent surge of interest in endophytic associations between fungi and plants. The diversity of fungi even within individual plant parts can be considerable (see above, and Carroll, 1988, 1992). There must be many physiological and biochemical similarities between endophytic fungal species, which usually only become apparent upon death of the plant, and biotrophic parasites, which also occur symptomlessly within plant tissue, but subsequently produce spores from within still-living plant tissue. The endophytic species Rhabdodine parkeri is closely allied to two other pathogenic species (Sherwood-Pike etal., 1986), which in some circumstances at least behave biotrophically (Minter, pers. comm.). The links between necrotrophic and endophytic fungi are also poorly researched. A recent case where a single mutation altered an isolate of a Colletotrichum species from an aggressive necrotroph into an endophyte which protected its plant partner by competition with the pathogenic strain (Freeman and Rodriguez, 1993) underlines the delicacy of plant-fungus interactions. The fragility of the relationship between biotrophic fungi, such as the Erysiphales, Meliolales and most members of the Phyllachorales (Ascomycota), and their plant partners can be appreciated by the great diversity of fungicolous fungi which obtain their nutrition from them, compared with those found on saprobes or necrotrophs (Hawksworth, 1981; Cannon, 1991). It is likely that biotrophic fungi cannot develop resistance to infection by other fungi without disrupting their relationship with the plant.

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Mycorrhizal associations are very widespread, Occurring with roots of perhaps as many as 90% of terrestrial plant species (Harley and Smith, 1983). Benefits to plants include increased growth and seed production, increased water and nutrient uptake, and increased drought tolerance (Allen and Allen, 1990). The fungi involved are frequently not strongly host-specific, but most are obligate mutualists (Lewis, 1973). The ability of ectomycorrhizal trees in particular to form associations with a range of fungi (and vice versa) is ecologically advantageous, adding resilience to the ecosystem (Perry et al., 1989). There has been very little research into interactions between endophytic and mycorrhizal fungi. In that the fungal components of endophytic and mycorrhizal associations in many cases have similar roles, it might be expected that endophytes would be less prevalent in mycorrhizal plants, and that fungi from the two groups would compete for resources within the plant. No detailed information is available, although Chu-Chou et al. (1990), Clay (1992) and Guo et al. (1992) have observed recently that endophytes of grasses belonging to the Clavicipitaceae are sometimes antagonistic to mycorrhizal fungi. Clay suggested that endophytes might be at a competitive advantage compared to mycorrhizal fungi due to their closer proximity within the plant to the regions of sugar production. Mutualistic interactions such as those identified between the Gramineae and Clavicipitaceae may be much more common than is currently realized; it seems to be rare for phytochemists to consider the possibility of fungal endophytes contributing to the metabolite prof'des involved in defence against herbivores that they identify from plant tissues. There is evidence that some species of Baccharis (Compositae) produce trichothecene toxins which were originally derived from associated soilborne fungi (Jarvis etal., 1987; Carroll, 1992), and that the anticancer drug taxol harvested from bark of Taxus brevifolia (Taxaceae) is produced also by the novel endophytic fungus Taxomyces andreanae (Stierle et al., 1993; Strobel et al., 1993). Although we are not confident that the possibility of synthesis of these compounds by endophytic fungi rather than the plants themselves can yet be completely ruled out, it is tempting to speculate that these products, and even plant growth substances like IAA and gibberellins, might have once originated from the fungal partners of plant-fungus associations by horizontal gene transfer (Pirozynski, 1988, 1991; Atsatt, 1991). While there is an immense amount of information on interactions between fungal pathogens and crop plants, the importance of pathogens in the maintenance of natural ecosystems through the limitation of species that would otherwise predominate is hardly explored. The ability of such fungi to control non-crop weeds outside their normal geographic ranges is well known and increasingly exploited (Templeton and Heiny, 1989), and clearly indicates that supression of vigour is an integral part of the role of fungi in natural ecosystems. Harper (1990) raises a number of pertinent issues in connexion with plant-pathogen dynamics in natural ecosystems which still have not been fully addressed, and there is a pressing need for experimental work on fungus-plant interactions in native plant communities.

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IV. ECOLOGY AND SITE INVENTORY

Fungi may adopt very restricted ecological niches, adding considerably to the work necessary in making complete inventories of the fungal species in given areas. Examples involving vascular plants include an undescribed species of Lophodermium which is apparently confined to galls on Juniperus caused by the midge Hormomyiajuniperina, and is clearly distinct from the common (presumably endophytic) species L. juniperinum (Cannon and Minter, unpublished). There is an extensive range of yeast species (mostly belonging to the genus Pichia), which occur only in necrotic lesions of cacti, originally bacterial in origin, and which are dependent for transmission on individual species of the fruit-fly genus Drosophila (Starmer et al., 1982). A wide range of saprobic, often ecosystem-specific fungi are known from dead wood and bark in mangrove communities, where extreme fluctuations in salinity and constant drying and wetting cycles require considerable physiological specialization for survival (Hyde et al., 1990). The existence of most fungi as hidden mycelium with ephemeral fruit-bodies, many of which are small or otherwise inconspicuous, and which may appear only irregularly, makes survey work aimed at the production of inventories very difficult, even for fungi associated with plants. Indeed, no site on Earth yet has a fungal catalogue that adequately represents the diversity present. Even where intensive sampling of a small, well-known area over an extended period of time has occurred, undiscovered species come to light at a surprising rate. For example, at the 211-ha Slapton Ley National Nature Reserve in Devon, England, around 2350 species of fungi had been recorded by June 1994 (Hawksworth, 1986, unpublished), of which 1048 have been added after an intensive study from 1969-1975 (Hawksworth, 1976). Sporadic collecting in the site continues to yield around 30 additional species every year. Many microhabitats in this site are as yet not or scarcely sampled, almost no cultural work or soil isolations have been carried out, and it now seems probable that the actual number of fungi in this single site is not less than 2500 (interestingly, 5.1 times that of the number of vascular plant species in the Reserve; see above) and could well be more. After almost 25 years of study, involving a considerable number of experts and also major field meetings and onsite courses, a complete inventory for one lowland UK site has not been possible. The Slapton study demonstrates that many years of regular observations, recognizing the diversity of ecological niches and microenvironments, are essential to obtain even a rough estimate of the number of fungal species present in a defined area. Even within apparently homogeneous substrata such as soil, the variety of nutritional needs of the constituent fungi means that a wide range of collection and isolation methods is necessary. Specialized fungi such as thermophilous and psychrophilous species are often not amenable to standard isolation methods (Carreiro and Koske, 1992), and although basidiomycetes form a considerable proportion of the soil mycoflora (Frankland, 1982), few species can easily be identified at present using cultural techniques alone. Such work is clearly expensive to carry out.

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New techniques are being developed which may allow diversity assessments in varied habitats of fungi which cannot be cultured using traditional means, or which do not readily spore. Preliminary research using molecular probes shows a considerable range of such organisms (Liesack and Stackebrandt, 1992). Similar research, along with extensions of traditional culture methods such as the use of naturally-occurring germination stimulators (French, 1992) and physical adaptions of growth conditions (e.g. Boasson and Shaw, 1982), should both identify large numbers of new taxa and allow much more detailed assessments of the interrelationships of currently-known groups, such as biotrophic parasites, which cannot at present be grown in culture. Biotrophic fungi may also be cub turable in association with plant callus tissue grown aseptically in vitro, or at least preservable in conjunction with living plant tissue (Dahmen et al., 1983; Molot etal., 1987).

V. DISTRIBUTION

There has been considerable disagreement in the past as to assessments of the extent of geographical distribution of fungal species. Cooke (1975)emphasized the ubiquity of fungi, suggesting that though most fungi are not cosmopolitan, many have wide distributions over areas which are often significantly geographically separated. This thesis has been repeated recently by Gams (1992), who stated that 'microfungi are usually cosmopolitan and have an enormous potential for dispersal'. However, this hypothesis only holds for around 5% of the known fungi, primarily belonging to one or both of two categories: (1) easily cultured saprobic soil organisms; and (2) abundantly sporing and easily transported moulds associated with humans, their habitations and foodstuffs. The contrast can be illustrated even within a single family. For example, in the Trichocomaceae, while some Penicillium species (e.g.P. chrysogenum, P. citrinum) are amongst the most widespread fungi on Earth, those with Eupenicillium teleomorphs tend to be known only from particular regions, often from undisturbed desert or woodland soils (Pitt, 1980). Between 1980 and 1990 new soil fungi were being published at a rate of one per week, suggesting that we only know a fraction of a very rich biota. Fungi restricted to particular plants or animals are necessarily limited by their host ranges, and many lichen-forming species in particular (which have been more intensively studied than most non-lichenized taxa) have well-defined patterns related to paleogeography and climatic parameters (Pirozynski and Weresub, 1979; Galloway, 1994). However, fungal species are not always coextensive with their hosts due to constraints such as differing climatic requirements, and contrasting nutritional or competitive pressures. Many apparent anomalies are caused by lack of data, or insufficiently rigorous analysis of host preferences. Fungi may also be absent from some areas of their partner's distribution due to difficulties in dispersal. Phyllachora lespedezae, for example, occurs on North

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American but not Asiatic species of Lespedeza, and has also spread onto the related plant genus Kurnmerowia, introduced into North America from eastern Asia (Cannon, 1991, in press). There is little doubt that P. lespedezaeis a North American fungus which has not had the opportunity to colonize Old World host species. The thesis that most fungal species have relatively restricted distributions is supported through studies of diaspore dispersal (Malloch and Blackwell, 1992). These suggest that the dispersal propagules of most fungi are rarely able to travel more than a few metres, restricting the opportunities for spreading between separated plant populations. Limited powers of dispersal of lichenized fungi on trees mean that they have applications as monitors of environmental disturbance (Rose, 1992) and this phenomenon will doubtless be found to apply to many other large-spored wood- and bark-inhabiting ascomycetes. Documented cases of long-distance dispersal which are not directly humanassociated are relatively rare, and are mainly confined to parasites of cultivated plants with large areas of monoculture, which provide large target areas for the dispersing spores. The importance of introductions in overcoming such geographical barriers is well-known to plant pathologists and quarantine officers and need not be elaborated on here, but it is not so widely appreciated that this same phenomenon applies to mycorrhizal associates of introduced cultivated trees (Pegler, 1977, 1986). Two important general statements made by Christensen (1981) with regard to fungal ecology and distribution have not been challenged seriously by subsequent workers: (1) there is an extremely high species diversity among the fungi in any given ecosystem; and (2) habitat specificity for individual species and guilds of species appears to be the rule. Probably all fungal species, including the most widespread, exhibit some degree of host or substrate specialization, which in itself limits their distribution ecologically if not geographically.

VI. FUNGI ON DIFFERENT PLANT FAMILIES A. Trends in Species Description In the exploratory phases of natural history in the eighteenth and nineteenth centuries, major resources were deployed in the collection and description of fungi present in natural ecosystems. The golden age for exploratory mycology was in the period 1880-1940. Since the crucial watershed of the Second World War, there has been a major shift in studies towards fungi of economic importance, and to more detailed studies of species and species groups. Table I shows that the number of newly described species in selected families was at a maximum in 1920-1940, the decadal value being 30-60 % higher than figures in all subsequent decades, and that the rate of discovery of novel taxa continues to decline. We are convinced that this decline is due to a decrease in research time rather than a lack of species to describe.

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Table I. Number of newly described species of fungi associated with selected plant families, 1920-1990. ,. . . .

19201939 Araliaceae Cactaceae Capparidaceae Compositae Cruciferae Cyperaceae Gesneriaceae Gramineae Scrophulariaceae Umbelliferae All families (estimate)

19401949

19501959

19601969

19701979

19801989

66 27 19 913 171 259 9 1205 149 232

20 4 17 236 31 90 0 412 46 61

38 9 34 385 59 117 6 730 42 92

43 3 13 340 76 92 2 679 52 101

21 20 18 203 66 91 1 468 35 70

25 19 9 192 23 148 3 605 28 41

20 500

4000

7500

7500

6500

6000

,,

Total 213 82 a 110 2269 426 797 22 4009 352 597 52 000 ,,,

a 39 of the 82 fungal species associated with the Cactaceae are yeasts described by a single research group. The data in Tables 1-4 are abstracted from the host indices of the Index of Fungi, a twice-yearly publication prepared at the International Mycological Institute since 1940, which records new taxa and other nomenclatural actions associated with fungi.

The change in research emphasis away from studies of natural ecosystems is demonstrated by the numbers of newly described fungi associated with important crop plants increasing more quickly than those linked to plant species with no direct recognizable benefits to man. Table II shows that newly described fungi associated with the Gramineae increased as a proportion of all species described from 5.9 to 8.6% between 1920-1940 and 1970-1990. In contrast, those associated with the Compositae, a similarly very large plant family but with relatively limited economic significance, decreased in the same period from 4.5 to 3.2 % of all described species.

B. Comparison of Fungi on Gramineae and Cyperaceae The emphasis in taxonomic research towards crop-associated species has certainly constrained the limited mycological community's ability to collect and describe fungal species. This thesis is evidenced by a comparison of the number of fungi associated with related plant groups of differing economic importance (Table III). The Gramineae is undoubtedly the most important plant family in economic terms; its products are the staple diet of almost all human groups. Wheat, barley, oats, rice, sugar cane, sorghum and maize are all grass products. In contrast, the Cyperaceae, though widely distributed, are of almost negligible economic value (Mabberley, 1987). Table III shows that the number of newly described fungal species relative to the total number of species of Gramineae is more than twice the level in the

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Table II. Interest by taxonomists in fungi associated with selected plant families - expressed as percentages of total new species described for all families.

Araliaceae Cactaceae Capparidaceae Compositae Cruciferae Cyperaceae Ges neriaceae Gramineae Scrophulariaceae Umbelliferae

1920-1940

1970-1990

0.32 0.13 0.09 4.45 0.83 1.26 0.04 5.88 0.73 1.13

0.37 0.31 0.22 3.16 0.71 1.91 0.03 8.58 0.50 0.89

Table III. Number of plant species compared with fungal associates described between 1920 and 1990.

Araliaceae Cactaceae Capparidaceae Compositae Cruciferae Cyperaceae Gesneriaceae Gramineae Scrophulariaceae Umbelliferae

Plant species

Fungal species

Proportion

800 1650 675 21 000 3000 3600 2400 7950 4500 3100

213 92 110 1969 426 797 22 4099 352 597

3.8:1 17.9:1 6.1:1 10.7:1 7.0:1 4.5:1 109.1 : 1 1.9:1 12.3:1 5.2:1

Cyperaceae. One clear indication that this disparity is contributed to by underrecordirlg is the discovery of no less than 10 ascomycetes new to science amongst 38 associated with the single species Carexfirma in the eastern Alps (Nograsek, 1990). The most important reason for the difference in fungus-plant species ratios is certainly economic, but several other factors related to the characteristics of the two families need to be considered.

1. Biochemistryand Endophytism Coughenaur (1985) regarded the evolution of grass-dominated savannah vegetation and large herbivores as at least partially mutualistic, the grasses being adapted to grazing by having well-protected basal meristems and benefiting from the discouragement of competitor plants with more vulnerable growing points. He considered that these mutualisms had led to a relative dearth of biochemical defences against herbivory, particularly alkaloids. Clay (1986) has speculated that the lack of these compounds has encouraged associations with fungi, particularly endophytes of the Clavicipitaceae. He considered that mutualisms with endophytic fungi have benefited grasses by discouraging herbivory (both mammalian and invertebrate), by the production of toxic alkaloids by fungi (Clay, 1988a, b);

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these are presumably effective against native herbivores as well as farmed species on which most of the research has been done. There is little information on whether the toxins discouraging herbivory produced by endophytes are also effective against other fungi, whether parasitic or saprobic, though work by White and Cole (1985) and Bayaa etal. (1987) indicate that this is sometimes the case. The Cyperaceae have associations with related fungi, although the diversity of fungal endophytes associated with this family appears to be smaller (Clay, 1990). This impression is perhaps caused partly by lack of research. The Gramineae and Cyperaceae each have a characteristic flavonoid profile, and the two patterns differ significantly (Williams and Harborne, 1988). The concept that flavonoid compounds play a role in disease resistance is an old one, but links are very tenuous and there is no evidence to suppose that the chemical group as a whole has a widespread function in preventing infection (Harborne and Ingham, 1978). Some flavonoid compounds do function as phytoalexins, and there has been some research to indicate that fungi pathogenic to the plants that produce them are able to break them down into non-toxic substances (de Wit, 1987; Weltring, 1992). Grasses are known to produce induced antifungal compounds, refuting earlier theories that these were lacking (Kuhn and Hargreaves, 1987). Some of these have been documented by Overeem (1976), Deverall (1976) and Kuhn and Hargreaves (1987). Some active substances are formed specifically in response to infection, while others appear to be permanently resident in host tissues, though sometimes at lower levels in the absence of infection. These disparate pieces of information, when taken together, suggest that the case for fungal diversity associated with the Gramineae being greater due to the biochemical characteristics of their plant partners is not proven, though our knowledge base is woefully restricted.

2. Morpholog~ and Anatomy The Gramineae are morphologically and anatomically more diverse than the Cyperaceae, which may be expected to result in a more varied fungal biota. This is most obviously illustrated by the extensive development of woody structures by bamboos. In the Cyperaceae woody tissue broadly similar to that found in the Gramineae is formed in a few genera, but is restricted to small perennial shoot bases. The development of perennial tissues in the Gramineae must have contributed to the diversity of fungal associates, providing long-term physical support and nutrition.

3. Taxonomic Diversity There is some suggestion that the Gramineae are taxonomically more diverse than the Cyperaceae, judging from the genus:species ratios of the two families. The Gramineae has 737 genera and around 8000 species, while the Cyperaceae has 115 genera and about 3600 species (Mabberley, 1987). This gives genus: species ratios of about 1 : 11 for the Gramineae and 1 : 31 for the Cyperaceae. The

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reasons for this difference are undoubtedly complex, but the inclination of taxonomists to subdivide further groups of major importance must be one of them (Waiters, 1986). Such effects are unlikely to be totally compensated for by similar tendencies amongst students of the associated fungi, as mycologists frequently employ outmoded species concepts when referring to host taxa. 4. Mycorrhizal Associations The Gramineae forms a significant component of vegetation in a much wider range of ecosystems than the Cyperaceae, and this probably also contributes to the diversity of associated fungi. Only about 25% of British Cyperaceae are known to have mycorrhizal associations, compared with about 50% for the Gramineae (Harley and Harley, 1987). The water-logged habitats typical of the Cyperaceae preclude, or at least markedly discourage, mycorrhizal synthesis (Tester et al., 1987).

C. Comparisons of Fungi Associated with Other Plant Families In addition to the Gramineae and Cyperaceae example, some other pairs of families demonstrate the historical bias of taxonomic research towards temperate rather than tropical groups. In Table III, the Gesneriaceae is a tropical counterpart of the Scrophulariaceae. New fungal associates of the Scrophulariaceae were described at a rate of one fungal species per 12.3 plant species between 1920 and 1990, but only one per 109.1 for the Gesneriaceae. The roughly similar figures for the Cruciferae and Capparidaceae, the former temperate and economically important and the latter mostly semitropical and with limited economic importance, may at first seem to be contrary to the above example. However, this result may be explained by the much higher proportion of woody species in the latter family, with greater opportunities for fungal association due to greater physical and chemical variation. The Umbelliferae and Araliaceae are a roughly analagous family pair to the Cruciferae and Capparidaceae, the temperate distribution of the former being offset by the higher incidence of woodiness in the latter.

D. Emphasis on Fungi of Economic Importance Table 4 documents the emphasis of taxonomic studies on fungi associated with economically important genera of the Gramineae. Between 1920 and 1990, the number of newly described fungi at species level and below was about half the total number of grass species. This ratio of 0.5 : 1 can be contrasted with figures of more than 4 : 1 for almost all of the cereal genera, and 35 : 1 for Zea. For the economically important groups, the figures in practice refer to fungi occurring on single species or close aggregates; rather few fungi have been described from wild

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Table IV. Number of fungal species described between 1920 and 1990 associated with selected grass genera.

Number of species Genus

Host

Fungi

A vena

12 300 20 19 600 4 250 30 3 24 20 4

49 60 36 107 112 87 80 129 37 70 161 140

7950

4099

Festuca Hordeum Oryza Panicum Phragmites Poa Saccharum Secale

Sorghum Triticum

Zea

Total Gramineae

Fungi: host 4.1 : 1 O. 5:1 1.8:1 5.6:1 O. 2:1 21.2:1 O.3:1 4.3:1 12.3:1 2.9:1 8.1 : 1 35.0:1 0.5:1

relatives of major cereals. Owing to the confused nomenclature of crop species, accurate figures for individual grass species are difficult to obtain. The imbalance of research towards fungi associated with crop species is almost certainly greater than these figures suggest; fungi associated with cereal crops are likely to have been described earlier than those with plant partners with no economic importance. Cereal grasses not grown in temperate regions, such as Sorghum, have a relatively low fungus:species count, reflecting the continuing emphasis on research into temperate rather than tropical agriculture. Of the grass genera surveyed, Phragmites (a genus of very restricted economic importance) had the second highest number of fungal associates relative to species, 21.2 : 1. There are at least four reasons for this: (1) the principal species, P. australis, is extremely widespread and common; (2) it is a large grass, thus harbouring a wide range of ecological niches and physical environments; (3) the small size of the genus distorts the ratio; and (4) the fungi associated with P. australis have been the object of several critical postgraduate studies. The genus So~charum, with the large physical size of its principal species and considerable economic importance, shows a fungus-species ratio of only 4.3" 1 using the criteria described above, and its exclusively tropical distribution suggests that fungal associates of the genus are probably under-recorded. The study by Sivanesan and Waller (1986) on Saccharum is the only recent assessment of known fungal diversity associated with an economically important grass genus. Their list of 378 fungal associates gives a rather larger fungus-plant species ratio of 12.6 : 1, reflecting the inclusion both of close associates described before 1920 and a large number of saprobic species which are not confined to Saccharum. There is no reason to suppose that the figures for other crop genera would not increase by similar margins using complete inventories of known fungal associates.

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E. Fungi Associated with Cactaceae The Cactaceae is a very distinctive group of angiosperms, in natural conditions occupying very restricted ecological niches. The group is also of very considerable economic importance to the horticultural trade. An investigation of the fungi associated with the family underlines the emphasis on research into associates of plant species in the developed world. Table V shows that the ratio of the number of fungal species to native cactus species in North America is of the order of 20 times greater than in either Central America or South America. The data are necessarily tentative, owing to the difficulty of abstracting information from widely disparate sources, few of which are adequately indexed. Many of the fungi recorded as associated with species of Cactaceae in the USA are probably wide-spectrum pathogens and saprobes of plants in cultivated conditions, but there is no reason to suppose that such fungi would not be found associated with cacti from other regions in native habitats if the conditions were correct. Almost half the number of new fungal species associated with Cactaceae described since 1920 are the products of a singleresearch group (e.g. Starmer etal., 1978, 1979, 1982; Miranda etal., 1982; Phaff etal., 1985), which has investigated the yeast flora associated with necrotic lesions originally caused by Erwinia species (Bradbury, 1986). The co-evolutionary relationship of these fungi with flies belonging to the genus Drosophila, which are distribution vectors, has been extensively investigated. The yeasts appear to be evolving rapidly and are often strongly host-specific, and the diversity identified by studies of a relatively restricted number of cactus species (almost all work has concentrated on the large columnar types) from a rather small number of sites suggests that the number of yeast species occupying similar habitats worldwide is very large indeed. Molecular taxonomic studies of yeast species in particular will probably identify a very much larger diversity than is currently evidenced, as current species concepts, at least for most non-pathogenic taxa, are largely based on a relatively small number of very crude physiological tests. Unrelated species may be grouped into one because of physiological adaptations to similar ecological niches. Some types of molecular data can also reflect ecology rather than evolution, if they are interpreted carelessly (Cannon and Minter, 1992). Table V also reflects emphasis on research into weed pests, in this case the noxious adventive species of Opuntia. We have found reports of 135 species of fungi from this one genus, four times as many as from any other cactus genus.

VII. CONCLUSIONS Considering the large and rapidly increasing awareness of the economic potential of fungi, especially in the pharmaceutical and biotechnology industries, but also in relation to ecosystem function and maintenance, there is a pressing need to enhance our knowledge of the Earth's fungi.

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Table V. Number of fungi recorded from genera of Cactaceae in various geographical

regions.

Cactus genus

Astrophytum Carnegiea Cephalocereus Cereus Coryphantha Cryptocereus Echinocactus Echinocereus Echinopsis Epiphyllum Espostoa Ferocactus Hylocereus Lemairocereus Lophocereus Mammillaria Melocactus Myrtillocactus Nopalea Opuntia Pachycereus Pereskia Rathbunia Rhipsalidopsis Rhipsalis Schlumbergera Selenicereus Trichocereus Numbers of fungi Numbers of cacti Fungi: cacti

N o . of

spp.

6 1 48 36 64 2 16 44 30 16 4 23 18 26 2 168 36 1 10 300 5 2 2 2 50 3 20 25

No. of fungi NAm

CAm

SAm

3 24 1 17 3 5 8 3 4 8 1 1 6 2 2 9 0 0 1 61 0 0 0 1 0 18 1 2

0 5 3 2 0 0 0 0 0 0 0 1 0 8 4 0 1 1 0 10 7 0 2 0 0 0 0 0

0 0 0 4 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 10 0 1 0 0 1 0 0 0

N Am 105 145 1 : 1.4

CAm 22 591 1:26.9

Elsewhere

Worldwide

0 0 0 13 0 0 2 1 1 5 0 1 0 0 0 4 1 0 0 57 0 1 0 0 0 3 1 0

3 25 4 34 3 5 10 4 5 12 1 3 6 10 6 13 2 1 1 135 7 2 2 1 1 18 2 2 SAm 17 521 1:30.6

Plants : fungi 2.0:1 0.04:1 12.0:1 1.1 : 1 21.3:1 0.4:1 1.6:1 11.0:1 6.0:1 1.3:1 4.0:1 7.7:1 3.0:1 2.6:1 0.3:1 12.9:1 18.0:1 1.0:1 10.0:1 2.22:1 0.7:1 1.0:1 1.0:1 2.0:1 50.0:1 0.2:1 10.0:1 12.5:1 Elsewhere 85 1 1:0.01

Fungus sources: Farr et al. (1989); 'Index of Fungi' and its predecessors (1920-1990); IMI herbarium; Oudemans (1919-1924); Revista Mexicana de Micologia; International Journal of Systematic Bacteriology. Numbers of species of Cactaceae in major regions abstracted from Hunt (1992); only definitely accepted species counted. NAm, North America (USA and Canada); CAm, Central America as far south as Panama (including Mexico and the Caribbean); SAm, South America.

At present, our knowledge base is grossly inadequate, with not less than 95 % of fungal species present remaining unknown to science. Recognizing the impracticality of collecting, isolating and describing these in a realistic time-frame, there is a need to target available and new resources to maximum effect. The assessment of biodiversity and research priorities in relation to fungi is encompassed in a separate report (Hawksworth and Ritchie, 1993), the detailed conclusions of which are not reiterated here. Economic stringencies and pressures on land use mean that widespread

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production of critical fungal inventories must be replaced by standardized sampling protocols tested against known areas with similar ecosystems, in order to assess the diversity and thus the conservation potential of sites. This is envisaged in the D I V E R S I T A S model developed by I U B S - S C O P E - U N E S C O (Di Castri etal., 1992). Plans for All Taxa Biodiversity Inventory (ATBI) sites including fungi, which would provide calibrations for such sampling methods, are currently being prepared (Yoon, 1993). At the scientific level, we see a need to adopt an increasingly rigorous approach in relation to issues such as species numbers. Claims concerning extinction rates, based on world estimates of species numbers and annual habitat losses, are already drawing criticism because of the absence of robust data (Simon and Wildavsky, 1993). Some significant steps towards rectifying this situation have been taken as a part of the D I V E R S I T A S programme, in that a series of provocative null hypotheses have been proposed for testing (Solbrig, 1991). In developing research agendas aimed at disproving these hypotheses, in the best traditions of science, data in which we can start to have real confidence will emerge. In order to develop the knowledge base with respect to the diversity of fungi associated with vascular plants, we wish to encourage strongly focused research and discussion in the following subjects: 1. Comparison of host specificity of defined fungal groups in the tropics with their relatives in broadly similar ecosystems in temperate regions. 2. Comparison of the total fungal inventory of a range of tropical forest sites with the number of vascular plants present. 3. Intensive collection of fungi from one or more defined tropical sites carried out over at least 3-5 years (and perhaps much longer) by a team of specialists, with the aim of a statistical estimation of the total species count based on the decline in reporting of novel taxa in specific ecological niches and/or using defined methods over time. 4. Investigation of the bias in sampling caused by physical size differences in higher taxa of fungi. 5. Study of the variation in numbers of fungal associates between pairs of genera of the same plant family which include similar numbers of species and which share similar life forms, but which occur in different climatic zones. 6. Analysis of the variation in numbers of fungi (including associated fungicolous and lichenized species) living on the surfaces of individual perennial tropical leaves, and the specificity of these fungi towards their hosts. 7. Research into molecular variation within isolates of morphologically identical or near-identical fungi occurring on different host-plant genera. 8. Analysis of species concepts in a range of fungus groups using morphological, intersterility and molecular techniques, with the aim of reaching consensus as to the most reliable criteria (or combination of criteria) on which to base ranks, particularly species and infraspecific taxa, and also the extent to which universal species concepts should be applied.

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9. The refinement of methods of DNA analysis in dried fungal material, in order to clarify species concepts and host ranges in biotrophic fungi which cannot be cultured. Such research is not a matter to be shelved in view of the acute and declining numbers of mycological systematists able to undertake such work (Burdsall, 1990; Pascoe, 1990; Hawksworth and Ritchie, 1993; Hawksworth, 1994), and also the often inadequately resourced and consequently ill-maintained dried and living collections (i.e. herbaria and culture collections respectively) in which systematic knowledge is rooted. Fungi associated with plants, and other substrata, merit a higher profile in future research programmes related to the understanding, management and sustainable use of biodiversity at a level appropriate both to their numbers and economic and environmental importance.

ACKNOWLEDGEMENTS We are indebted to Dr D. W. Minter for stimulating discussions and for making some of his hitherto unpublished observations available to us, and for the helpful comments of Drs P. D. Bridge and B. C. Sutton (IMI). Dr D. Simpson and Mr N. P. Taylor (both of the Royal Botanic Gardens, Kew) made useful contributions from botanic angles.

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Bacteriology 2 8, 318- 325. Starmer, W.T., Phaff, H.J., Miranda, M., Miller, M. W. and Barker, J. S. F. (1979). Pichia opuntiae, a new heterothallic species of yeast found in decaying cladodes of Opuntia inermis and in necrotic tissue of cereoid cacti. InternationalJournal of Systematic Bacteriology 29, 159-167. Starmer, W. T., Phaff, H.J., Miranda, M., Miller, M. W. and Heed, W. B. (1982). The yeast flora associated with the decaying stems of columnar cacti and Drosophila in North America. Evolutionary Biology 14, 269-295. Stierle, A., Strobel, G. and Stierle, D. (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of pacific yew. Science 260, 214-216. Strobel, G., Stierle, A., Stierle, D. and Hess, W. M. (1993). Taxomyces andreanae, a proposed new taxon for a bulbilliferous hyphomycete associated with Pacific yew (Taxus brevifolia). Mycotaxon 47, 71-80. Templeton, G. E. and Heiny, D. K. (1989). Improvement of fungi to enhance mycoherbicide potential. In 'Biotechnology of Fungi for Improving Plant Growth' (J. M. Whipps and R.D. Lumsden, eds), pp. 127-151. Cambridge University Press, Cambridge. Tester, M., Smith, S. E. and Smith, F. A. (1987). The phenomenon of'nonmycorrhizal' plants. CanadianJournal of Botany 65, 419-431. Trappe, J. M. and Luoma, D. L. (1992). The ties that bind: fungi in ecosystems. In 'The

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15 ADVENTURES OF A ROSE PATHOLOGIST Charlene Harwood Bear Creek Gardens Inc., P.O. Box 9100, Medford, Oregon 97501, USA

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I. The Adventure Begins II. Industry versus Academia III. Roses and Rose Pathology A. Powdery Mildew B. Downy Mildew C. Virus and Virus-like Diseases D. Blackspot E. Rust F. Crown Gall G. Herbicide Damage H. Dehydration IV. Plant Pathology of the Future References

I. THE A D V E N T U R E BEGINS M y career as a rose pathologist began in graduate school, but my adventures were not to begin until later! W h e n I left academia, I chose a non-traditional career move. I went to work in industry, something considered rather shameful at the time, certainly not top drawer. And, m y e m p l o y m e n t was not even with a pesticide company. At least those jobs in industry were respected for being stable and well paid, if viewed as being limiting and boring. I went to work for a rose nursery. I r e m e m b e r a colleague asking, in all seriousness, what I would do when, having solved all of the c o m p a n y ' s disease problems, I worked myself out of a job. T h e r e is no conceit to match that of a scientist. Fifteen years later, I find that m y training in plant pathology has served me well in preparation for a satisfying, challenging career. M y intent is to use this forum and my e m p l o y m e n t as an example to provide a perspective on the science of plant pathology, and the opportunities it provides.

ADVANCES IN PLANT PATHOLOGYmVOL. 11 ISBN 0-12-033711-8

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II. INDUSTRY VERSUS A C A D E M I A There are trade-offs with every employment option. Let us examine those involved in a decision to work in industry. The lament most frequently mentioned is the lack of freedom to pursue any avenue of research. It is true that in industry, money rules. Businesses expect to maximize profits. To that end, they are reluctant to pay for knowledge gained for its own sake. Research must be goaloriented, with the goal being reduced production costs and/or higher sales achieved by marketing angles or improved quality of goods. The scientist choosing a career in industry should be the kind of person who derives great satisfaction in practical results. However, within that context, creativity is not stifled; it is encouraged. And, if the scientist proposes a project of probable benefit to the business, funding is more readily available. How m a n y interesting avenues of basic research have languished from lack of funding, while academicians have struggled to compete for limited grant funds? Research is never cheap. In the final analysis, there must always be someone willing to pay for it. Another benefit to working in industry is the probability of seeing one's work implemented. Most often the scientist is given the opportunity to have some control over the implementation. Of course, the scientist is directly held accountable for failures. In contrast, for academicians, it must be frustrating to have solved a problem and not have the solution put into practice, or to watch it fail because of improper implementation. But, there is the comfort of not having one' s livelihood directly connected with the success or failure of that implementation. Negative results, those experiments where the results failed to support the theory, or worse, where the experimental design was inadequate to allow a conclusion to be drawn, are not often recorded in publications of academic research. In my experience in industry, all efforts are documented so that learning can take place and mistakes not be repeated. I have viewed this approach as a distinct advantage. There is no pressure to publish. O n the contrary, there may be discouragement from doing so, as the business may view research it has paid for as proprietary. While it may be a blessing not to be anxiously counting publications as tenure review approaches, there is a loss also. It is through publication and participation in meetings that scientists achieve recognition, prestige, and build a fellowship with those studying similar disciplines. This loss and isolation is perhaps the most serious disadvantage to working in industry. Accompanying the restriction on publication is the lessened opportunity for peer review of work, especially if the research staff is small, as it is in many nontraditional industry employment opportunities. There have been times, both when I was right and wrong in my direction, when my work would have benefited from peer review. While there may not be pressure to publish, there is pressure to produce results. All positions in industry must be seen as paying for themselves. With no tenure

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system, research staff is always somewhat at the mercy of the economic situation of the business. It is a wise enterprise that sacrifices research last, recognizing that it is innovation that will enable it to pull ahead of competition; wise, but not common. Finally, there is the issue of corporate politics. I can think of no more rigorous training ground for gaining skill at political manoeuvring than the academic setting.

III. ROSES A N D ROSE PATHOLOGY Rose diseases affect rose growers at all levels. Working for a primary producer, I have had the opportunity to interact with most of these levels, as most were, in some sense, customers. My area of greatest responsibility has been to improve the health, and thus the production, of field-grown rose plants, or to achieve the same yield at a reduced cost. That health needs to be maintained through harvest, storage, delivery, and on the store shelf. Therefore, I have been called upon to study post-harvest treatments as well as growing problems. In the United States, about 70% of field-grown roses are produced in the southern San Joaquin Valley of California, about 25 % are grown in the Phoenix area of Arizona, and about 5 % in the Tyler, Texas area. Sales from these primary producers total about $300000000 per year (Omer Schneider, Bear Creek Gardens, Medford, Oregon, personal communication). The method of production in these areas is similar. Hardwood rootstock cuttings are taken from plants in the field in the fall. All but the top two nodes on the leafless cuttings are removed by hand, using knives. The cuttings are then planted, again by hand (Fig. 1). Also during late fall, cuttings are taken from flowering cultivars in the field. These cuttings are stripped of their leaves and stored nearly frozen. In the spring, these cuttings are removed from storage, and their nodes are used to T-bud graft the rootstock cuttings which by then will have rooted. This grafting is done by crews of two persons using carts which enable them to work just 2.5 cm above the soil line on the cutting (Fig. 2). The first member of the pair makes the cut and inserts the node of the flowering cultivar; the second wraps the graft with a grafting rubber. The top of the rootstock is left in place for the remainder of the growing season. However, it may be partially severed-to force the graft to produce a shoot during the first season. Even if the top is cut in this manner, the grafted plant can provide a source of rootstock cuttings that fall. In the winter, crews remove the rootstock just above the graft union, and trim the scion shoots to 7.6 cm in length (Fig. 3). The following growing season, the flowering cultivar top grows out (Fig. 4). Growth is often arrested by pruning or mechanical sawing to stimulate bottom branching. By fall, the plants are a source of budwood cuttings and are ready for harvest.

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Fig. 2. Use of a budding cart to allow grafter to make the graft on rose cuttings 2.5 cm from the ground.

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Fig. 4. Field-grown rose plants during their second summer season, showing growth of the flowering scion cultivars.

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Fig. 5. Tractor pulling rubber-fingered rose leaf stripper.

The plants are prepared for digging by mowing them to about 33-41 cm high. Tractors pull rotating drums, with rubber fingers attached, through the field to strip off the leaves (Fig. 5). Then, a U-shaped blade is drawn under the crop, severing the roots and lifting the plants out of the ground. The soil is shaken off and the plants are piled on trailers for transport to sheds where they are graded, pruned, and labelled. Finally, they are placed in cold storage pending delivery to customers. The above described production cycle is for the typical gardenrose. Variations on that procedure are used to produce miniature roses, roses destined for greenhouse growers, tree roses, and own-root shrub roses. These plants are sold throughout the United States, and may be exported to Canada, Central America, South America, the Caribbean, and Japan. Our customers include individual gardeners; garden centres, which sell either dormant stock or potted plants; and greenhouse growers for cut-flower production. I have provided customer service by addressing disease problems in all of these situations. These challenges have given me the opportunity for travel across the United States and to a few other countries. I have had exposure to many types of businesses, from small single proprietorship garden centres to large cut-flower co-operatives. Perhaps my favourite trip was to visit fledgling greenhouse rose growers in Jamaica, to help them with their fertilization and pest control

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programmes. Being a rarity, an industry scientist in a specialized field, the opportunity to interact with so many facets of the rose business has afforded me some of the recognition and prominence lost through the inability to publish. Being the only scientist on staff for several years, I have been called upon to interpret disease in the broadest sense: soil compaction, water quality, fertilization regimes, sanitation during propagation, statistical analysis of quality control sampling, and cold storage conditions, among others, have been my domain. This variety of responsibilities has suited me. My original attraction to plant pathology was because it required multidisciplinary study. As such, it can uniquely prepare students to respond to numerous employment demands. Industry would do well to hire more plant pathologists. As an example of the challenges, once I was called upon t~ explain why some of our roses sent to greenhouse growers were dying. The roots were infected with Rhizoctonia, a pathogen which does not usually cause a problem on roses. The plants had started to grow quickly, but collapsed. We were able to show that they had been predisposed to infection prior to harvest, by defoliation late in the growing season, when starch was being stored in the roots. Defoliation from any cause--mites, rust, mechanical disturbance--at that time of year would lower the starch levels found in the roots, although differences in starch levels found in the stems wou|d not be apparent. The defoliation also would stimulate nodes to begin to break. So when the roses were planted by the customer, they would start to leaf out especially quickly, having already begun the process. We were able to develop a quality test for starch in the roots to monitor our crop at harvest. Given that my audience is primarily interested in plant pathology, I describe below some of the rose diseases I have encountered, and experiences I have had with them in the various phases of the industry. Two good references on this subject are by Horst (1983) and Langhans (1987).

A. Powdery Mildew Rose powdery mildew is caused by Sphaerotheca pannosa var. rosae. The fungus can infect immature foliage and canes, and flowers. Starting as a small red spot, the colonies form the typical white powdery covering of mycelium and spores. Severe infection causes leaves to desiccate and fall. Stem infections frequently turn into unsightly, superficial, rough, brown cankers. The disease is favoured by mild temperatures and humidity. Mycelial growth is optimal at 18-20~ with conidium germination optimal at 21 ~ Shading also promotes disease development, and infection is usually more prevalent on the abaxial leaf surfaces. Infection starts in the spring from shoots produced from nodes that were infected the previous growing season. The infections are protected over the winter by rudimentary leaves and bud scales. The incidence of such infections is low, so as the mildew season unfolds patches of infection can be seen with these characteristic shoots as infection foci at the centre of each.

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For the producer of field-grown plants and greenhouse rose growers, this disease is the most costly. During periods of conducive weather, typically spring and fall, the plants must be protected with a fungicide every 7-14 days. Efforts to assure continued registration of materials on our small acreage, high value, specialized crop, have led us to co-operate with both university and pesticide manufacturer researchers to evaluate new products. Over the years, depending on the political climate, manufacturers have both rejected and wooed us. Those concerned with the risk and low profit potential of a small, high value crop have done the rejecting; those interested in getting a product to market quickly have seen our non-food status as attractive. In order to facilitate production decisions on whether spraying is economically justifiable, we have evaluated the effects of intensity and duration of infection on a range of cultivars. Of particular interest was the interaction between powdery mildew and the cultivar 'Dr Huey'. This cuhivar serves as the rootstock for most of the garden roses produced in the United States. It is extremely susceptible to powdery mildew. When sterol-inhibiting fungicides became available, it was possible for the first time to reduce the infection level in this rootstock to moderate levels. However, we discovered that the resultant increase in vigour caused the rootstock, when budded, to reject the grafts. Yet, if left unchecked, powdery mildew would cause defoliation on plants budded late in the season. The consequence of defoliation is that the bark tightens, and grafting becomes impossible. O u r challenge thus has been to manage the disease for the greatest grafting success and, therefore, the highest yield. Faced with the more rapid loss of fungicides than gain of newly registered compounds, and increased environmental awareness, we have worked on nonchemical mildew control. M a n y powdery mildews are inhibited by simply washing the leaves with water. Rose powdery mildew is no exception. The water physically disrupts spore production, washes the normally aerially dispersed spores down to the ground, and causes the spores to lyse on the leaf surfaces thereby reducing infection. O u r work has focused on timing sprinkler irrigation with spore release to achieve control. Greenhouse rose growers also depend heavily on fungicides. Having more control over the growing environment, greenhouse growers have more options. The enclosed structures allow for sulphur fumigation treatments. Curtains can be used to reduce the fluctuations in light intensity and humidity which promote spore release. Homeowners and garden centres do not have the control over the growing environment that greenhouse growers do, but they can control site selection. We encourage them to pick sunny locations with good air movement. Use of mid-day sprinkler irrigation is an option that works well. Cultivar selection also can be recommended, as many cultivars are quite resistant. However, a cultivar

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resistant in one area may be susceptible in another, so customers are encouraged to visit their local municipal rose gardens to evaluate selections.

B. Downy Mildew Downy mildew, the most feared disease of roses, is caused by Peronospora sparsa. Under favourable environmental conditions, this fungus causes irregular, magenta-coloured spots which may become necrotic and papery. Leaf tissue between the spots may be chlorotic. Tender shoots may appear scorched. Defoliation may occur overnight, with few other warning symptoms. I call this the disease of a thousand faces. If conditions are just right, i.e. cool temperatures and high humidity, a thick, grey mat of sporangiophores and sporangia may form on the abaxial leaf surface. Often, however, sporulation is sparse, hence the species epithet. Despite the fact that most of the field rose production in the United States is in hot arid climates, this fungus is able to survive the hot, dry summers and cause sometimes spectacular defoliation during the brief spring and fall periods when weather conditions are favourable for the disease. The overwintering/ oversummering mechanisms are not fully understood. The same species causes systemic infection of blackberry, and overwinters as root infections in this host (Ellis et al., 1991). It is not known if the blackberry pathogen also infects roses. Infected blackberry shoots, produced from such systemic infections, are symptomatic in the spring. Such symptomatic shoots have not been seen on roses. We have observed that fields most likely to be affected are those that are held over for a third growing season, but it is unknown whether this manifestation is due to oospores in living tissue or debris, mycelial colonies, system;.c infection, and/or the fact that these plants leaf out earlier and have a denser canopy during the time infection is most likely to occur. Great variability is seen in cultivar susceptil~ility, but no studies have been done to screen cultivars for resistance. In field production, control of the disease depends on knowledge of favourable weather conditions and diligence in applying protective fungicide applications during such periods. Given the potentially rapid spread of the disease, protection cannot be breached during any of the time during which disease-conducive weather conditions exist. Greenhouse growers have much less dread of this organism. While it can be truly devastating, the pathogen is so dependent on humidity that maintaining humidity below 85 %, which can be easily achieved by manipulating the enclosed environment, gives effective control. Producers of potted roses for sale in bloom often must contend with this disease, especially if they are located in high rainfall climates, or grow plants in poorly ventilated plastic hoop houses. Often a person will have successfully grown roses using the same techniques for a decade, only to be surprised by downy mildew in a year when conditions are just right. Potted plant producers are encouraged

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to space plants, that is not to put them pot-to-pot, to irrigate when foliage will dry quickly after irrigation, to encourage air movement through venting if growing them indoors, and to use a preventative spray schedule. Home gardeners rarely see this disease. Plant spacing, fewer plants, and less likelihood of groupings of susceptible cultivars mean there is less opportunity for this disease to get started.

C. Virus and Virus-like Diseases Virus and virus-like diseases of rose include rose mosaic, caused primarily by prunus necrotic ringspot, apple mosaic and arabis mosaic, rose streak, rose ringpattern, rose spring dwarf, and rose rosette. They cause a range of symptoms from leaf patterns to growth deformations. None of these diseases is spread mechanically from rose to rose, and only rose rosette is known to have a vector in roses. The others are believed to be spread in roses only through grafting. Thus, these diseases are primarily a concern for rose producers. It is possible, with diligence, attention to detail, and a clean stock programme, to produce rose crops free of these vectorless diseases. The key is to have unbudded mother blocks to break the potential infection cycle inherent in taking cuttings from budded stock. If a cultivar is unknowingly infected, and rootstock cuttings are taken from plants budded with this cultivar, then the cuttings will be infected. When those cuttings are planted and other cultivars are budded to them, infection will spread. Thus, the disease agent can quickly contaminate many cultivars thought to be free of infection, and the cycle repeats, ever widening. Recently, many United States growers have focused attention on such clean stock programmes. Growers in other parts of the world often use seedling rootstocks. With no evidence of seed transmission, there is a natural break in the cycle, and e msequently a much lower incidence of the diseases. Recently, the development of reliable, commercially available, ELISA testing for the most common mosaic viruses has facilitated operation of such clean stock programmes. An initial, rapid determination can be made on the virus status of a given plant, and its progeny can be increased in numbers or discarded while results from the traditional long-term biological indices are pending. With regard to purchasers of plants from primary producers, the main emphasis is on educating them to know that their best guarantee of growing healthy plants is to buy healthy plants from a producer with an effective clean stock programme. Many buyers need reassurance that the virus and virus-like diseases will not be spread through pruning. Part of my responsibility has been to educate the sales and customer service staff of our company, so they can in turn counsel the customers. Rose rosette is a North American endemic disease of suspected virus etiology. It is spreading eastward from the middle of the country on wild Rosa multiflora hedges. This is a lethal disease to most rose species, but there is controversy over how large a threat it poses to cultivated roses and rose production. This debate

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is especially heated given the proposal to use the pathogen as a biological control agent for the R. multiflora hedges, which have been classified as noxious weeds. I have had the opportunity to represent my industry on this issue.

D. Blackspot No discussion of rose diseases would be complete without mention of blackspot, caused by Diplocarpon rosae, the most important disease of roses worldwide. Wherever roses are grown in moderate climates with precipitation or high humidity, it is prevalent. The black spots on the foliage are often ringed by chlorotic tissue, and the edges of the black spot are diagnostically feathered. Conidia produced in these lesions are spread by water and insects. Leaf infection leads to defoliation, with some cultivars defoliating much more readily than others. The fungus overwinters in the leaf debris. The subsequent poor growth of defoliated plants is a major reason for a lack of interest in planting roses in many parts of the world. It is because of this disease that roses have the reputation of being hard to grow and requiring frequent spraying. Because of the arid climate in California, blackspot is only a minor nuisance in field production. Even when weather conditions are conducive, the disease does not spread rapidly enough to build up to a significant extent. In Arizona, however, late summer rains are common, and growers must apply fungicides to prevent defoliation. Likewise, garden centres and home gardeners must rely on fungicide applications, although the importance of sanitation, and cultural programmes to keep leaves dry, are stressed. In greenhouse operations, where leaves can be kept dry, there is not a problem.

E. Rust There are nine species of Phragmidium reported to cause rust of roses. All are autoecious and form pycnial, aecial, uredial, telial and basidial stages on roses. Most frequently the orange-spored uredial stage is seen. Chlorotic flecking of the abaxial leaf surface, opposite an adaxial uredium, is common. Towards fall, teliospores may be produced in the uredia. Both the teliospores and urediospores enable the fungus to overwinter. Rust infection causes leaf drop. Similar to blackspot, rust spores require several hours of leaf moisture for infection. Rust is most prevalent in climates with mild temperatures and rainfall, heavy dew formation, or high humidity. Despite the arid conditions found in most rose production areas, rust can be a problem, especially in the fall. The cultivar 'Manetti', used as an understock for greenhouse roses, is especially susceptible. Control centres on sanitation of crops carried over through a winter, and fungicide applications. Knowledge of which cultivars are most susceptible aids in fidd monitoring during weather periods conducive to infection.

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With enclosed structures and climate control, rust rarely is a problem for greenhouse growers. Home gardeners and garden centre growers are encouraged to practice sanitation, keep leaves dry by arranging for optimal location, spacing and ventilation of plants, and follow a preventative fungicide programme.

F. Crown Gall Crown gall, caused by Agrobacterium tumefaciens, can be a nasty surprise at harvest time. Plants which appear normal above ground may be found to have the typical cauliflower-like growths, most frequently where the roots meet the stem (hence the name of the disease), but also on the roots themselves. For infection to occur, this soft-borne bacterium requires a wound which stays moist. Given that roses are grafted, in the field, just above the soil line, and that the plants are flooded with irrigation water just after grafting, it is perhaps surprising that there is essentially no infection found at the graft union. This disease is primarily of concern to propagators. During propagation many plants are wounded when they are small, so there is greatest opportunity for infection, and galled plants cannot be sold by the propagators. Contamination during this process can lead to serious losses. The key to crown gall control is sanitation. Plant materials, tools, and work surfaces must be disinfested. There was a good sanitation programme in place when I arrived, which had been successful in minimizing crown gall infection, even before soil fumigation was practised. If the cuttings could be sanitized, trimmed, and allowed to heal before planting, little infection took place, even though the organism might be present in the soil. O u r research efforts have focused on comparing the effects of soil solarization versus fumigation with methyl bromide on A tumefaciens populations, and the use of the bacterial antagonist K84. Repeatedly, we have been taught how easy it is to allow a chink in the wall of sanitation to occur. K84 dip solutions are effective in reducing crown gall infections, but they can also be a source of inoculum if the solution becomes contaminated while dipping plants. Thus, we apply the biological agent as a spray. Similarly, wash water from the process of cleaning plants at harvest can contaminate fields, irrigation pipelines and sumps, resulting in more nasty surprises at harvest. Plant purchasers, including greenhouse growers, garden centres, and home gardeners have less worry with crown gall. Generally they are planting in soil with a low level of inoculum, either clean potting soil, treated beds, or soil which has not been repeatedly cropped to crown gall hosts. Also, since the wounding that may occur at planting is most likely to be on the roots, if infection occurs it is likely to be on a root. An infection on a root is much less debilitating than a crown or stern infection, which may interfere with translocation of water and nutrients.

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G. Herbicide Damage Herbicides are widely used at all levels of rose growing to save labour. Hence there have been opportunities to diagnose symptoms of herbicide damage from many sources. We have worked to establish which herbicides are safe and useful in field production. Bioassay techniques have been useful in diagnosis and in achieving optimal herbicide placement. We have also investigated problems caused by herbicide drift from applications in nearby fields. Volatilization of herbicides in enclosed structures is a particular problem for potted rose growers in greenhouses and plastic hoop houses. Home gardeners and nurserymen alike have found that roses have little tolerance for exposure to glyphosate. O u r role in serving these customers has been one of education as well as diagnosis.

H. Dehydration During harvest and storage the bare root plants are susceptible to dehydration. Loss of water is the single most important post-harvest threat to quality of the product. As bare root dormant rose plants lose moisture, their appearance initially does not change. The first symptom of water loss is an increased brittleness of roots. We have been able to quantify this loss using root segments and a pressure bomb. Water loss beyond a certain level results in plants being slow to start growing when they are planted. Soaking plants in water after such dehydration only partially improves the speed at which the plants leaf out. Speed in leafing out is important to potted rose growers, who often try to time first flowering with spring holidays or peak sales periods. As dormant rose plants lose more water, the bark begins to shrivel and show faint vertical lines. Roses damaged to this degree will exhibit some cane death when planted, as well as being slow to start growing. However, death will not ensue unless roses are almost completely dried out. Desiccated roses may die back and show no growth for months, and then start producing new growth from the bud union. Roses with roots packaged in wood shavings enclosed in plastic bags have about a 2-week shelf life before they begin to exhaust the moisture in the shavings. Products packaged in containers meant to be planted are designed to be watered while on the shelf. Again our role has been one of education. Frequently garden centre staff think that the plants will remain viable indefinitely, without any water, until planted. To reduce water loss and prolong viability, we have tested many antitranspirant coatings. Recent technology has provided improved products, but the best coating for water loss prevention is still melted wax. Unfortunately, in hot climates the wax melts and burns the canes, and so it cannot be used.

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Charlene Harwood

IV. PLANT PATHOLOGY OF THE FUTURE The above comments of disease problems affecting rose growers and my perspective as a scientist in industry show how the science of plant pathology can prepare people for diverse, challenging careers. It seems important to qualify that endorsement with a concern for the direction of plant pathology education. Advances in biotechnology and molecular biology have been amazing in the last decade. Plant pathologists need a working knowledge of these developments. There should be university staff who specialize in that aspect of the science. Perhaps certain campuses should devote themselves to that area of the discipline. However, there should be room for continued emphasis on generalists. There should be some schools which choose a broad-based, multidisciplinary approach to educating the prospective plant pathologist, with abundant opportunity for field experience, laboratory experience, diagnostic experience, and classes taught by experts in other agricultural fields. I am grateful I had such an education. As I review the titles of publications in plant pathology journals, the nature of presentations at professional meetings, and the advertisements for employment opportunities in the discipline, I cannot help but worry that our profession is moving away from such training. Finally, I would like to make a case for the importance of research experience to a prospective industry scientist. The ability to design experiments, analyse results, and draw conclusions will be put to use in almost any enterprise. Many agricultural operations run tests only to fail to follow through as production demands overshadow interest in the results, or to find that when the test is complete it was not set up in a way to answer the question originally posed. The ability to be an experimentalist is more important than knowing everything about everything. With research ability as a tool, the industry scientist can get the background knowledge needed as problems arise, and be able to handle a variety of challenges.

References Ellis,M. A., Converse," R. H., Williams, R. N. and Williamson, B. (1991). 'Compendium of Raspberry and Blackberry Diseases and Insects'. The American Phytopathological Society, St Paul, Minnesota. Horst, R. K. (1983). 'Compendium of Rose Diseases'. The American Phytopathological Society, St Paul, Minnesota. Langhans, R. W. (1987). 'Roses. A Manual of Greenhouse Production'. Roses Incorporated, Haslctt, Michigan.

Index

actinomycetes 134, 230 additives, organic 31 adjacent vegetation 196, 204

Agrobacterium tumefaciens 314 agroecology 104 agroecosystem 48, 51, 192, 202 management 51-2 agroforestry 6, 25-6 agronomic practices 118-19 alleles resistance 76-7, 79 virulence 78, 81 allelochemicals 160 allodeposition 93 amoebas 134 angiosperms 293 Animal and Plant Health Inspection Service of the USDA 70 antagonistic organisms 134, 159-60, 173-5, 239 anthracnose 110 antibiosis 123 antibiotics 122, 160 ArmiUaria 283 Arthropoda 10, 159, 173, 192, 252 Australian cotton industry 10-11 avocado 136, 137

Bacillus thuringiensis (Bt) 11, 12, 117, 263, 268 bacterial antagonists 122-3, 134 barley mildew 83, 90 bees 183-5 biocides 12 biocontrol 3, 14, 63, 117-24, 148, 159-61, 162, 252, 261-63 agents, registration 174-5 with bees 183-5 ecological basis of 121 biofertilizers 60, 63 bioherbicides 60, 67

BioMalTM 60, 72 Blackspot 313 boom-and-bust cycle 76-9 Bordeaux mix 255, 267, 268 Botrytis cinerea 173-87 breeding research 113 brown leaf spot 251,259 buffer crops 11 burning crop residues 159

C Gactaceae 293-4 canal systems 51 canola 71-2 carbamate 10 carboxyalkenyl hydrazinium 216 cereal yields 8 Ceylon 35 chemical fertilizers 45, 52 pesticides 66, 203 chemicals as inducers 216-20 chestnut blight fungus 135 China, North 35 chloropicrin 53 Ghlorosufuron 9 chlorothalonil 177, 183 Golca Valley 34 GollegoTM 60, 64, 72 Colorado beetle 12 Common Agricultural Policy 8 companion cropping 8 compound fertilizers 15 conidia 176-7, 181, 184 Consultative Group on International Agricultural Research (CGIAR) 3, 258-9, 266 control strategies 14 cost of goods 65 cotton industry, Australian 10-11 crop diversification 195, 201 domestication 22

318

inoculation 59 management 241 mixed 158 -pathogen associations 282 perennial 159, 201 residues, burning 159 rotation 119, 148, 157-8, 159, 162, 173, 241, 257-8 trap 159 variety choice 77-80 -weed-insect interaction 196 cropping systems 147,257 Crown Gall 314 cultivars plant 235 resistant 152, 155, 162, 211 rotation of 156 tolerant 150, 155 cultivation ephemeral 37-8 landscaped 37-8 cultural controls 14 customer demand 61-2 cyanobacteria 231, 243 Cylindrocarpon 54 cyclodeine 10 Cyperaceae 288-91 biochemistry and endophytism 289-90 morphology and anatomy 290 mycorrhizal associations 291 taxonomic diversity 290-1 D DDT 10, 203 decrue farming 26 deforestation 25, 38 detritus food webs 234 detritus pathway 46 DeVine T M 60, 64-6, 72 diamondback moths 12, 263 dichlorocyclopropane 216

Diplocarpon rosae 313 disease management, nonchemical 106-7, 113 diseases foliar 256 vector-borne 3 diversification schemes 96 DNA 2, 82, 113, 243, 281 of genes 260 hybridization 114-15 recombinant technology 119-21

Index

downy mildew 81,216, 260 of lettuce 90-1 drained fields 29-31 Drosophila 285, 293 dryland farming 26 durable resistance 85-7, 96 durability and genetics 86 Dutch elm disease 135 dynamic equilibrium 48-50

ecological theory 104 ecosystem foundation 46-8 enemies hypothesis 193-4 energy flow 46-7, 48-9 energy loss 105 entomopathogens 262, 268 Environmental Protection Agency (EPA) 70 Erysiphales 281 E~ysiphe graminis 80, 82-4, 86, 88, 93-5 Eucalyptus marginata 136 eyespot 88

F family planning 249

Federal Insecticide, Fungicide and Rodenticide Act, The 70 fermentation 63 fertilizers 38 nitrogen 265, 267 rates 257 Fertilizers Act, The 70 field experimentation 68-9 external 69 floodwater farming 26 Food and Agriculture Organization 3 forest clearance 24 fumigant 10, 52 fungal distribution 286-7 diversity 277-96 ecology 285-6 economic importance 291-93 pathogens 3, 9 fungi 134, 137, 173, 277-96 biotrophic 283, 286 ectomycorrhizal 279 endophytic 283, 284 meiotic 280

Index

mitotic 280 mycorrhizal 232-3, 237-8, 284 necrotrophic 283 psychrophilous 285 thermophilous 285 fungicides 80, 177, 211 foliar 252 phenylamide 91 systemic 255-6 Fusarium 54 G gametic disequilibrium 84, 88 General Agreement on Tariffs and Trade (GATT) 8 genes conservation 283 pyramiding of resistant 260 genetic engineering 115, 117, 177 erosion 261 genetics, plant 59, 113 genomes 114 genotype frequencies 95 germplasm 16, 109-10, 267 Gliocladium roseum 186- 7 glucan elicitors 217 Gramineae 288-90 biochemistry and endophytism 289-90 morphology and anatomy 290 mycorrhizal associations 291 taxonomic diversity 290 gray mold 176-7 green manuring 32, 38 revolution 7, 249-50, 255, 266 guano 32 H

specificity 132, 138, 281 human population 249, 251

inoculation 211 fungal 238 liquid 66 microbial 63 with Rhizobium 59-60, 64, 66, 71, 235-6 insecticides 252-5 organophosphorus 203 insects dynamics 196 herbivorous predatory 3 integrated pest management 10, 147, 161, 191-206, 211, 241-42, 253, 257, 263 intercropping 254, 257-8, 265 International Agricultural Research Centers (IARCs) 249, 267 International Board of Plant Genetic Resources (IBPGR) 3 International Centre for Improvement in Wheat and Maize 10 International Center of Insect Physiology and Ecology 258 International Convention on Biodiversity 2, 4 International Network for Genetic Enhancement of Rice 260 Intravalley Canal 34-5 irrigation farming 27 isozyme surveys 2

J jarrah 136, 140 jointvetch, northern 60, 67

Helicoverpa armiga 7, 10

herbicide resistance 9 herbivores 196 heterogenous cropping 91 high yielding varieties (HYVs) 250-51, 259, 261, 265 hitch-hiking selection 84 host -plant attributes 205 -plant resistance 155-7, 252, 254, 258-61, 267 resistance 152

319

K K84, bacterial antagonist 314 K-selection 104 K-strategy 13-14 L Lake Titicaca 34 land-race cultivation 75

320

Index

leaf disc assay 180-82, 186 fungal disease 13 pests 16 legume root nodules 236 Lolium rigidum 9

nitrogen fertilizer 265, 267 fixation 235-7 North China 35 nutrient cycles 47, 48-9, 233-5 nutrition, plant-symbiont 4

M

O

manual irrigation 27 Maris Piper 155, 156 Maris Tricorn 12 market potential 62 mating control 14 Meloidogyne incognita 151 Mesopotamia 36 methyl bromide 52-5 microbes 116 microbial antagonism 119-22 micro-organism diversity in soil 230-1 mildew barley 77 downy 311-12 powdery 309-11 mixtures control of disease in 92-3 pathogen fitness in 94-5 pathogen populations in 93-4 performance prediction 95 molecular biology 113-17 monoculture 75-6, 85, 96, 159, 191, 192, 194, 201, 251 intensification 9 mulches 110-11 multicropping 33 multiple-species introduction strategy (MSI) 203 mycorrhizal fungi 231-3, 237-8 mycoparasites 122, 135, 137, 138

organic additives 31 Organization of Economic Co-operation and Development (OECD) 70 Organization of African Unity 262 organophosphate 10 organophosphorus insecticides 203

N natural defence systems 211-24 natural selection ~:3 nematodes 230 -crop damage 149-50 -host interactioJls 148-50 management 1z..7-62 plant-parasitic 147-8, 156-7 population change 150, 153-4 quarantine 155 Nitragin T M 59-60

P parasitic hymenoptera 202-3 parasitoid populations 193-195 pathogens control 4, 122 -derived resistance 116 fungal 3, 53 as inducers 212-16 soil-borne 4, 52, 122, 221 viral 9 pathosystems 50-1 peasant agriculture 107-13 PeniciUium bilaii 60-67 Peronospora sparsa 311 Pest Control Products Act, The 70 pesticides 4, 14, 45, 52, 66 and environment 241-42 synthetic 256-7 pests 32-3 alien 3 exogenous 3 phanerogams 291 phosphonates 216 Phragmidium spp. 313 PhyUachorales 281 Phytophthora spp. 216- 7 cinnamomi 9, 132-42 palmivora 60 phytotoxicity 216 piperonyl butoxide 11 plant diversification 202, 204 growth-promoting rhizobacteria (PGPR) 238-9, 243 residues 234

Index

root diseases 239-40 planthopper 259 plant-symbiont nutrition 4 plows 24-5 polymerase chain reaction (PCR) 114-15, 281 population regulating mechanisms 47-9 potato common scab 264 late blight 86-7, 95, 251 powdery mildew 12, 76, 80, 81-2 predator populations 193, 195 prehistoric agriculture 21-39 probenazole 216 producer subsidies 7 product efficacy 70-1 prokaryotes 173 PROVIDE T M 60-1, 64-7, 71-2 applicator 66 pseudomonads 137 Pucinnia spp. 9, 76, 83, 89 pyramiding of resistant genes 260 pyrethroid 10 Pythium spp. 9, 51-4

Rosa multiflora 312 rose

pathology 303-17 production in USA 305 rose leaf stripper 308 rose pathology blackspot 313 careers in 303-17 Crown Gall 314 dehydration 315 downy mildew 311-12 herbicide damage 315 powdery mildew Rhizoctonia 309 Rust 313-14 viruses and virus-like diseases 312 Rose rosette 312 round-leaved mallow 60-1 rust epidemics 9, 10, 81 brown 95 fungus 213 of poplars 135 of rose 313-14 stem 76, 83, 84, 85, 87 yellow in wheat 81

R r-selection 104 r-strategy 13-14 rainfed cultivation 24-5 raised fields 29, 30, 51 regulatory requirements 69-70 resistance breeding 4, 14 durable 84, 85-7 genes 77-80, 85, 88, 89, 91 pyramiding 87-8 herbicide 9, 13 host-plant 11 ineffective 80-1 multiple-gene 11 pesticide 10 systemic 211-13 restriction fragment-length polymorphism (RFLP) analysis 117 rhizobial inoculants 59-60, 64, 66-7, 71 Rhizoctonia 309 Rhizoctonia solani 52, 54 rhizosphere 235 rice blast 264 production 249-50, 259 root pests 16

S saprophytes 264 screening organisms 180-82 seed treatments 256-7 semiochemicals 205-6, 253,267 shifting cutivation 23-4 siderophore production 123, 240 slash/mulch practices 110-11 smuts 81 social systems 266-9 soil 229-44 conservation 264 fertility 31-2, 264 fumigation 158 health 264-6 microbiology 229-44 pest management 31-3 quality 243 solar heating 158 radiation 46-7 Sphaerotheca pannosa var. rosae 309 stemborers 258 stranglervine 60 strawberries black root rot 55

321

322

and BotEvtis cinerea 173-87 Californian 52-5 cropping systems 173-4 and methyl bromide 52-5 subsidies 8 producer 7 sulphonylurea herbicides 241 swidden fields 23-4 systemic induced resistance 212-13

T tachninid fly 133 take-all 120 terracing 27-9 bench 27-8 sloping-field 27-8 tillage methods 173 tomato 88, 157 endophytic fungus in 213 toxicology 70 transgenic crops 114 resistance 114 trap crops 159 Trichoderma 54 Triticum aestivum 60 trophic interactions 53

Index

U United Nations Conference on Environment and Development 2

V vascular plants and fungi 277-96 Verticillium 54, 138 Victoria blight 76 village-garden agriculture 4 virulence genes 83 selection for 81-5

W water harvesting 26 water primrose 67 weeds 261 control 3 Western science 107-10, 112, 119 whitefly 253, 255 wintermoth 133 World Commission on Environment and Development 1 World Health Organization (WHO) 253