Horticultural Reviews, Volume 22

HORTICULTURAL REVIEWS Volume 22

Horticultural Reviews is sponsored by: American Society for Horticultural Science

Editorial Board, Volullle 22

Judith A. Abbott A. R. Ferguson Freddi Hammerschlag

HORTICULTURAL REVIEWS Volume 22

edited by

Jules Janick Purdue University

John Wiley 8' Sons, Inc. NEW YORK / CHICHESTER / WEINHEIM / BRISBANE / SINGAPORE / TORONTO

A NarB TO nIEREA.DER=

This boot bas been electtoDlcally reproduced from di,ital information stored at JobIl Wile,. et SOIlS. Inc. We are pleued tbat !he use of this new teebllololY will eUble us to keep works of eadurill, scholarly value in print as 10111 as there i. a reasonable demmcl for them. The content of this book is ideDticaI to previous priatiap.

This book is printed on acid-free paper.


Copyright © 1998 by John Wiley & Sons, Inc. All rights reserved. Published simultaneously in Canada. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning or otherwise, except as permitted under Sections 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, 222 Rosewood Drive, Danvers, MA 01923, (978) 750-8400, fax (978) 750-4744. Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 605 Third Avenue, New York, NY 10158-0012, (212) 850-6011, fax (212) 850-6008, E-Mail: PERMREQ @ WILEY.COM. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold with the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional person should be sought.

Library of Congress Cataloging-in-PubJication Data: Library of Congress Catalog Card Number: 79-642829 ISBN 0-471-25444-4 ISSN 0163-7851 Printed in the United States of America. 1098765432

Contents List of Contributors Dedication: Frank G. Dennis, Jr.

ix

x

John F. Kelly 1.

Banksia: New Proteaceous Cut Flower Crop

1

Margaret Sedgley I. II. III. IV. V. VI. VII.

Introduction Taxonomy Breeding Systems Plant Improvement Physiology Production Conclusions Literature Cited

2. Leucospermum: Botany and Horticulture

2 3 5

10 14 19

21 22

27

Richard A. Criley I. II. III. IV.

Introduction Botany Horticulture Crop Potential and Research Needs Literature Cited

3. Postharvest Heat Treatments of Horticultural Crops Susan Lurie 1.

II. III.

Introduction Heat Treatments Commodity Responses

28

32 42 77 81

91 92 93

96 v

CONTENTS

vi

IV. V. VI.

Fungal Pathogen Response Insect Response Conclusions Literature Cited

103 106 110 111

4. Modified and Controlled Atmospheres for Tropical

Frulls

123

Elhadi M. Yahia I.

II. III. IV. V.

Introduction Modified (MA) and Controlled (CA) Atmospheres Potential Problems and Hazards of MA and CA Fruit Review Conclusions Literature Cited

124 127

135 135 164 168

5. Nitrogen Use in Vegetable Crops in Temperate

Climates

185

M. K. Shenk

I. II. III. IV. V.

Introduction Factors Influencing Fertilizer Needs Determination of Fertilizer Requirement Nitrogen Management Conclusion Literature Cited

186 190 196 205 211 212

6. Origin and Dissemination of Apricot Miklos Faust, Dezso Suranyi, and Ferenc Nyujto

225

I. II. III. IV. V. VI.

Introduction Classification Linguistic Evidence Origin Dissemination Conclusions Literature Cited

225 226 241 244 248

259 263

CONTENTS

vii

7. Tea: Botany and Horticulture L. Manivel I. II. III. IV.

Introduction Botany Horticulture Future Prospects Literature Cited

267 268 271 277 289 290

Subject Index

296

Cumulative Index

298

Cumulative Contributor Index

320

Contributors Richard A. Criley, Department of Horticulture, University of Hawaii, Honolulu, Hawaii 96822 Miklos Faust, Fruit Laboratory, Beltsville Agricultural Research, Agricultural . Research Service, Beltsville, MD 20705 John F. Kelly, Michigan State University Susan Lurie, Department of Postharvest Science, ARO, The Volcani Center, Bet Dagan, Israel L. Manivel, Tocklai Tea Research Association and UPASI Tea Research Institute, India Ferenc Nyujto, Fruit Research Station, Cegled, Hungary M. K. Schenk, Institute of Plant Nutrition, Department of Horticulture, University of Hannover, Herrenhauser StraBe 2, 30149, Hannover, Germany Margaret Sedgley, Department of Hort~ulture, Viticulture & Oenology, Waite Agricultural Research Institute, The University of Adelaide, Glen Osmond, South Australia 5064, Australia Dezso Suranyi, Fruit Research Station, Cegled, Hungary Elhadi M. Yahia, DIPA, Facultad de Qufmica, Universidad Autonoma de Queretaro, Queretaro, Mexico 76010

Frank G. Dennis, Jr.

Dedication: Frank G. Dennis, Jr. Frank George Dennis, Jr. was born in Lyons, New York, a stone's throw from Geneva and Ithaca. He established himself early in high school as a versatile student, scholar, and athlete and upon graduation entered Cornell University. His undergraduate education was interrupted when he returned to the family farm when his father became ill. He later reenrolled at Cornell and completed his B.S. degree in agriculture in 1955. Following graduation, he worked as an orchard manager before returning to Cornell, where he earned his doctorate in pomology in 1961. He established himself during graduate school as a future leader in growth regulator physiology. As a National Science Foundation Post-doctoral Fellow, he spent a year in the laboratory of J.P. Nitsch in France. Upon his return to the United States in 1962, he joined the pomology faculty at Geneva, where he conducted research and published important work on fruit development, flower-bud initiation, and the roles of gibberellin and auxin in fruit and seed development. In 1968, Frank joined the Department of Horticulture faculty at Michigan State University, where he continued his career as a teacher, scholar, researcher, cooperator, mentor, adviser, pomologist, poet, historian, and friend. Frank officially retired in 1996, but he remains active in his department, his profession, and in his service as the Editor for HortScience. Dr. Dennis's scholarly contributions are evidenced by his extensive publications, nearly all produced in collaboration with his students and scientists at institutions in several countries. Their work has included research on growth regulator assays, seed and bud dormancy, fruit quality and yield, growth regulator metabolism, chemical thinning, pollination, fruit set, frost avoidance, and many practical studies in direct response to the needs of fruit growers. His expertise in these areas has been shared in Central and South America, Jamaica, Mexico, Ethiopia, Malaysia, Cameroon, Morocco, Romania, Spain, France, Italy, United Kingdom, and in several of the United States. He has hosted visiting scholars from Italy, Australia, Hungary, and China. As a teacher and mentor, at both the undergraduate and graduate levels, he has been formally recognized with awards, but more importantly xi

xii

DEDICATION: FRANK G. DENNIS,

JR.

he is remembered by many former students as the person who played a major role in their professional and personal development. They remember his "class within the class," his trips around the state with students tagging along, his impromptu and challenging questions, and his genuine interest in students' learning. He believes that it is important to have a full appreciation of the classical work in horticultural research. His relationship with his students was clearly stated by one of his former advisees who said, "He played an active role in my development as a researcher all through my graduate career (after leaving Michigan State University) by playing the devil's advocate when I became overconfident with research results. He kept me thinking that the final experiment had not been done, and probably never would be." Frank's extensive knowledge of the plant sciences, his in-depth capabilities in pomology, and his uncanny ability to recall literature appropriate to a current discussion or paper, in combination with his exceptional skill as an editor, have made him a valued reviewer of scientific papers and popular applied articles. All who have had their papers subjected to his red pen have seen their work markedly improved by his suggestions and criticisms, and few, if any, were made to feel offended by his sharp, incisive criticism. In fact, many have returned deliberately to him for additional critical reviews. We are fortunate that he has chosen to serve as Editor for one of the major journals of the American Society for Horticultural Science. So many of us who have known Frank Dennis professionally can state that he is also a friend and colleague. We equate his crew-cut haircut, his tenor voice, and his humorous and warm poetry with his always youthful approach to life and the world and his always-upbeat demeanor. We appreciate his concern for and involvement with current social and political issues, and we often look to him for conscienceguided insights. We can be proud that this volume is dedicated to Frank Dennis, an outstanding horticulturist and a wonderful person. John F. Kelly Michigan State University

1 Banksia: New Proteaceous Cut Flower Crop* Margaret Sedgley Department of Horticulture, Viticulture, and Oenology Waite Agricultural Research Institute The University of Adelaide Glen Osmond, South Australia, 5064 Australia

I. Introduction II. Taxonomy III. Breeding Systems A. Reproductive Structure B. Breeding Biology C. Genetic Variability IV. Plant Improvement A. Controlled Pollination B. Selection C. Interspecific Compatibility D. Cultivars V. Physiology A. Flowering B. Propagation C. Water and Nutrient Uptake D. Postharvest Physiology VI. Production A. Culture B. Diseases and Pests *Research conducted by M. Sedgley was supported by the Australian Research Council. the Rural Industries Research and Development Corporation, the Horticultural Research and Development Corporation, the Australian Flora Foundation, the Society for Growing Australian Native Plants New South Wales. and the International Protea Association. Thanks to Andrew Dunbar. Jennie Groom, Michelle Wirthensohn, and Meredith Wallwork for the photographs.

Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc.

M. SEDGLEY

2

VII. Conclusions Literature Cited

I. INTRODUCTION

Banksia species (Plate 1) have been cultivated for the international cut flower market for only 20 to 30 years, but there is increasing interest in areas other than the native home, Australia, with production in Israel, South Africa, Hawaii, and California (Ben-Jaacov 1986; Sedgley 1996). Within Australia, Banksia is one of the four most widely planted commercial native genera, but production is based on seedling material and between plant variability is high. Banksia species for the fresh cut flower market must fulfill strict commercial criteria, which include terminal blooms and long stem length (Fig. 1.1), and further research is needed

Fig. 1.1.

Inflorescence and foliage of Banksia 'Waite Orange'. Bar represents 4 em.

1. BANKSIA: NEW PROTEACEOUS CUT FLOWER CROP

3

into all aspects of Banksia biology and production. In addition to the fresh cut flower market, Banksia stems are traded as dried and dyed blooms, and a wide range of species is used in environmental horticulture, for the attractive inflorescences and foliage, and to attract birds and other wildlife. Although there has been little work conducted so far on the use of Banksias as pot plants, recent developments with related genera suggest that such an approach may be productive (Ben-Jaacov et a1. 1989). Banksia wood and cones are turned or incorporated into ornaments, and the timber of some species has been used for furniture. Other genera from the Proteaceae that are important horticulturally include the Australian Grevillea, Dryandra, Isopogon, TeJopea, and Macadamia, and the South African Protea, Leucadendron, Leucospermum, and Serruria. Horticultural aspects of Banksia production have been reviewed by Sedgley (1996), and recent research reviews on related genera include leaf blackening in cut Protea flowers (Jones et a1. 1995), while Leucospermum will be covered by Criley in this volume. The objective of the present paper is to review research activity that underpins the current development of Banksia as a floricultural crop.

II. TAXONOMY The Banksia genus includes 76 taxa, which are currently grouped into two subgenera, three sections, and 13 series (Table 1.1) (George 1981, 1988, 1996, 1997; Maguire et a1. 1996). The most widely cultivated species for floriculture belong to the subgenus Banksia sections Banksia and Coccinea, and are characterized by terminal flowering of large showy inflorescences. These include the scarlet Banksia, B. coccinea, the pink B. menziesii (Fig. 1.2), the green/yellow B. Baxteri and B. speciosa, and the orange species B. ashbyi, B. prionotes, B. hookeriana, B. burdettii, and B. victoriae. B. ashbyi is mainly cultivated in Israel, whereas the others are grown in most Banksia production areas. Others cultivated to a lesser extent for cut flowers or foliage include the yellowflowered species B. grandis, B. sceptrum, and B. integrifoJia, the brown B. soJandri and B. brownii, and the orange B. ericifolia. Many other species of Banksia produce axillary blooms that are obscured by foliage and have short stems, but some terminal flowering forms of otherwise axillary-bearing species, such as the red B. occidentaJis, have recently been identified and used for cut flower production. The most important commercial species is B. coccinea, and this is also the most problematic taxonomically. It has a number of unique features, and no obvious close relatives in the genus. A recent cladistic analysis

4 Table 1.1.

M. SEDGLEY Systematic sequence in Banksia (after George 1997).

Subgenus Banksia Section Banksia Series SaJicinae: B. dentata L.f., B. aquiJonia A.S. George, * B. integrifoJia LJ., B. pJagiocarpa A.S. George, B. obJonglfolia Cav., B. robur Cavanilles, B. conferta A.S. George, * B. paJudosa RBr., * B. marginata Cav., B. canei J.H. Willis, B. saxicola A.S. George. Series Grandes: * B. grandis Willd., B. soJandri RBr. Series Banksia: B. serrata LJ., B. aemuJa RBr., * B. ornata F. MueH. ex Meissn., *B. baxteri RBr., * B. speciosa RBr., * B. menziesii RBr., * B. candolJeana Meissn., B. sceptrum Meissn. Series Crocinae: * B. prionotes Lindley, * B. burdettii E.G. Baker, * B. hookeriana Meissn., B. victoriae Meissn. Series Prostratae: B. goodii RBr., * B. gardneri A.S. George, B. chamaephyton AS. George, * B. bJechnifoJia F. Muell., * B. repens Labill., * B. petioJaris F. MueH. Series Cyrtostylis: * B. media RBr., * B. praemorsa Andrews, B. epica AS. George, B. piJostyJis C. Gardner, * B. attenuata RBr., * B. ashbyi E.G. Baker, B. benthamiana C. Gardner, B. audax C. Gardner, B. Jullfitzii C. Gardner. * B. eJderiana F. MueH & Tate, * B. Jaevigata Meissn., B. eJegans Meissn., B. lindJeyana Meissn. Series Tetragonae: * B. Jemanniana Meissn., B. caJeyi RBr., B. acuJeata A.S. George. Series Bauerinae: * B. baueri RBr. Series Quercinae: * B. quercifoJia RBr., B. oreophiJa A.S. George. Section Coccinea: * B. coccinea RBr. Section Oncostylis Series Spicigerae: B. spinuJosa A.S. George, * B. ericifoJia LJ., B. verticillata RBr., B. seminuda (AS. George) B. Rye, B. JittoraJis RBr., *B. occidentalis RBr., * B. brownii Baxter ex RBr. Series Tricuspidae: * B. tricuspis Meissn. Series Dryandroideae: B. dryandoides Baxter ex Sweet. Series Abietinae: * B. sphaerocarpa RBr., * B. micrantha AS. George, B. grossa A.S. George, * B. telmatiaea AS. George, B. JeptophylJa AS. George, B. Janata A.S. George, B. scabrella A.S. George, B. vioJacea C. Gardner, B. incana A.S. George, * B. Jaricina C. Gardner, * B. puJchelJa RBr., B. meisneri Lehmann, * B. nutans RBr. Subgenus IsostyJis: B. ilicifoJia RBr., B. oJigantha AS. George, * B. cuneata AS. George.

* Species tested for interspecific compatibility.

of the genus failed to clarify its status (Thiele and Ladiges 1996), and it is hoped that molecular systematics will provide the answer (Maguire et al. 1997d; Mast 1997). It is important to know the taxonomic affinities of the major commercial species, so that attempts at interspecific hybridization can be directed toward the most closely related and hence productive crosses.

1. BANKSIA: NEW PROTEACEOUS CUT FLOWER CROP

Fig. 1.2.

5

Inflorescence and foliage of Banksia menziesii. Bar represents 2 em.

III. BREEDING SYSTEMS A. Reproductive Structure

Banksia species range from prostrate forms to trees, and all are evergreen woody perennials (Fig. 1.3), some of which regenerate from lignotubers following fire. Many flowers are crowded into showy inflorescences, which are followed by infructescences, often called cones, in which relatively few seeds develop in large woody follicles. The most common flower colors are yellow, orange, green, brown, and red. Banksia violacea produces purple flowers, and although the blooms are too small and obscured by foliage to be used in floriculture, it may provide a useful character for plant breeding. Foliage may be fine and needle-like or coarsely serrated. Banksia floral structure conforms to the typical proteaceous pattern of large numbers of individual flowers grouped together

6

Fig. 1.3.

M. SEDGLEY

Tree of Banksia baxteri. Post is 14 inches.

to form conspicuous inflorescences (Fig. 1.2). In B. coccinea and B. menziesii, the flowers are produced spirally on the inflorescence, with 13 separate genetic spirals initiating simultaneously (Fuss and Sedgley 1990). The flowers develop in pairs, with each flower subtended by a floral bract and the pair of florets and their floral bracts subtended by a common bract. These bracts are inconspicuous, and the floral display is provided by the colored perianths and styles. Each Banksia flower has four tepals, with a single bilobed anther attached by a short filament to the distal region of the perianth. The pistil consists of an ovary with two ovules, and a long style with a small pollen-receptive stigmatic area in the apical region. In some species, the

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

7

style elongates more quickly than the perianth during floral development, and arches beyond the corolla tube by protruding between two perianth members. An unusual feature of the genus is that the Banksia floral display is contributed entirely by the perianth and the style. In B. coccinea, for example, the inflorescence is gray prior to anthesis from the gray color of the perianths, and red following anthesis from the red color of the styles. The distal portion of the Banksia style is specialised for pollen presentation, and its structure varies between species (Fig. 1.4) (Sedgley et al. 1993). The receptive stigmatic cells are located in a groove toward the tip of the pollen presenter, which in most species is located longitudinally and obliquely terminal, although in a few it is transverse or lateral. In B. menziesii, the pollen presenter has a complex internal structure, as observed by light microscopy, with the transmitting tissue enclosed by transfer cells, which may serve to maximize water and nutrient supply to the growing pollen tubes (Clifford and Sedgley 1993). The transfer cells are not present in the rest of the style, and the number of transmitting tissue cells declines over the approximately 2 em length of the style, with only 11 cells present atthe junction with the ovary. The Banksia style is a robust wiry structure with lignified sclerenchyma tissue located in the outer cortex. After flowering, the inflorescence develops into a woody infructescence, and successfully fertilised ovaries develop into follicles, each with one or two seeds. In most species the infructescence does not increase in size after flowering, and the mature follicles are much larger than the ovaries at anthesis, resulting in spatiallimitations to fertility (Fuss and Sedgley 1991a,b). An exception is B. grandis in which the axis, common bracts, and floral bracts enlarge around the follicles and become lignified, such that the mature infructescence can be used for cutting and turning into craft objects. Most species do not release their seeds until after fire (Zammit and Westoby 1987). B. Breeding Biology As in many other proteaceous genera, the flower of Banksia exhibits protandry, with the anthers dehiscing prior to flower opening to deposit their pollen on the pollen presenter (Sedgley and Fuss 1995). This generally occurs about one day before the flower opens, and following anthesis the pollen is collected by foraging fauna. At this stage the stigma papilla cells are not receptive to pollen. and peak stigma receptivity is attained three days after flower opening. This has been determined by increase in the width of the stigmatic groove and by increase in pollen germination on the stigma in B. menziesii (Fuss and Sedgley

8

M. SEDGLEY

(a)

(b)

Fig. 1.4. lmm.

Pollen presenter of (a) Banksia serrata and (b) Banksia grandis. Bar represents

1991a), and in B. coccinea by increase in stigmatic secretion (Fuss and Sedgley 1991b). In the natural habitat all of the flower's own pollen has been removed by insect, bird, or mammal pollinators by the time the stigma is receptive, and the flower may be cross pollinated by a foraging animal that has visited another plant.

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

9

Outcrossing is a feature of the genus (Carthew et a1. 1988; Sedgley 1995d; Goldingay and Carthew 1997), and most species of Banksia that have been studied produce less seed following self pollination than following cross pollination. The self incompatibility is only partial, however, as controlled hand pollination of B. menziesii resulted in 80% infructescence set following crossing compared with 33% following selfing, and 6 follicles per crossed inflorescence compared with 1.3 after selfing (Fuss and Sedgley 1991c). In B. coccinea all pollinated inflorescences set some seed, but the crossed infructescences had 40.7 seeds compared with 27.9 after selfing (Fuss and Sedgley 1991b,c). Further information was obtained from a 5 by 5 diallel experiment, with the results measured by pollen tube growth, observed using fluorescence microscopy (Fuss and Sedgley 1991b). Pollen tubes had reached the base of the styIe by six days after pollination, but self pollination generally resulted in poorer tube growth. Statistical analysis showed that some plants were more successful parents than others, that some genotype combinations were better than others, and that some crosses were more fertile when conducted in one direction than in the other. These results indicate that Banksia has a mixed mating system with complex genetic interactions. Most species are characterised by relatively low seed yields (Ayre and Whelan 1989), and this has been attributed to a wide range of possible causes, including breeding system constraints, pollinator limitation, insect and bird predation, and poor nutrition.

c.

Genetic Variability

Outcrossing plants generally show high levels of morphological variability, and this is true of the Banksia genus. For example, there are four distinct geographically isolated forms of B. canei reported (Salkin and Hallam 1978). More subtle variation is found in most species, including variability in yield, bloom quality and color, time of flowering, and disease tolerance (Fuss and Sedgley 1991a; Sedgley 1995c,d). In addition to morphological characters, biochemical methods are increasingly used to measure genetic variation. Isozyme analysis has demonstrated high levels of genetic diversity in B. attenuata, B. menziesii (Scott 1980), and B. cuneata (Coates and Sokolowski 1992), and this has been confirmed in the latter species using RAPD-PCR analysis (Maguire and Sedgley 1997c). A further application of RAPD-PCR is to compare plants in wild populations with those in cultivation. This approach has demonstrated that for B. coccinea, variability is lower between cultivated than between natural populations, indicating that the cultivated populations studied are closely related to each other and

10

M. SEDGLEY

suggesting that the germplasm in cultivation may not represent the full variability available in the wild (M. A. Rieger and M. Sedgley unpublished). This is not the case for B. menziesii, which appears to be wellrepresented in cultivation. Using RAPD-PCR, it is also possible to identify which natural and cultivated populations are the most closely related, so that wild populations that are already represented in cultivation do not need to be sampled further. IV. PLANT IMPROVEMENT

Variability is a disadvantage to the grower because it leads to inconsistency in product, but it means that there is ample scope for selection and breeding of new improved cultivars. For Banksia the method of preserving desirable characteristics is single plant selection followed by vegetative propagation. The population subjected to selection may be wild populations in the native habitat, open pollinated populations under cultivation, or cultivated populations derived from controlled pollination. A. Controlled Pollination

Research into the Banksia breeding system has been used to develop controlled hand pollination methods (Fuss and Sedgley 1991c). Inflorescences of the seed parent are covered with a bag to exclude pollinating fauna, after the removal of all open flowers. One day later, the bag is opened, pollen is removed from all newly-opened flowers using a looped synthetic pipe-cleaner, all unopened flowers are removed, and the bag is replaced. Three days later, at peak receptivity of the stigma, pollen is transferred to the stigma, using the pollen-laden pollen presenter from the pollen parent as a paint brush to insert the pollen into the stigmatic groove. The bag is replaced for a few days, to prevent any further pollen transfer, after which it is removed during the remainder of the seed development period, which varies with species from five to sixteen months (Sedgley et a1. 1994). Seed set following controlled hand pollination is around 3.5% (Sedgley et a1. 1996), and mature seed are collected and germinated for subsequent selection. Pollen storage and viability testing are important adjuncts to a breeding program. B. menziesii pollen was stored at 20, 4, -20, -80, and -196°C, and assessed using a semi-solid medium of 1 % agar, 150/0 sucrose, 0.01 % boric acid, 0.03% calcium nitrate, 0.02% magnesium sulphate, 0.01 % potassium nitrate, with an incubation temperature of

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

11

25°C (Maguire and Sedgley 1997a). Germination after six months remained constant at around 70% in all treatments, except 20°C storage, which gave only 25% germination. Pollen viability was assessed using fluorescein diacetate, but the results did not reflect the loss of germinability at 20°C and correlation with in vitro results were variable. There was no effect of floret position on the inflorescence on germination, but pollen viability varied over the flowering period with maximum germination mid-season. B. Selection

Strict criteria based upon commercial requirements must be applied to the population under selection (Sedgley 1995c,d). These include size, number, quality and color of blooms, stem length, time of flowering, length of the flowering period, vase life, disease tolerance, and ease of vegetative propagation. Quality is a very complex set of characteristics, comprising stem length and straightness, with minimal leaf damage and abnormal florets (Fuss and Sedgley 1991a). Adequate testing of superior selections is required, as some characters, such as bloom color, may alter during the flowering season (Bickford and Sedgley 1994,1995). In the red, pink, apricot, yellow, and bronze variants of B. menziesii, the overall inflorescence color derives from the combination of style and perianth, which may comprise different hues. Where anthocyanin pigments are responsible for the color, intensity may vary with temperature and thus with season and location. Selection for color stable variants is an important aim of B. menziesii improvement. RAPD-PCR can be used to generate fingerprints specific for each new cultivar of Banksia, to aid in identification and registration (Maguire et al. 1994; Sedgley 1995a,b). There is also potential to use the method in marker-aided selection, to accelerate progress, as plants do not need to be grown to maturity from seed before they can be assessed horticulturally. C. Interspecific Compatibility

For most horticultural crops, significant gains in productivity, quality, and novelty have resulted from chance or deliberate interspecific hybridization, and research on Banksia has addressed this aspect of reproductive biology. Experimentation has focussed on the commercial cut flower species, with interspecific sexual compatibility investigated in B. prionotes, B. hookeriana, B. menziesii, and B. coccinea (Tables 1.1, 1.2). Some species supported no germination of interspecific pollen, some supported normal pollen tube growth, and others produced pollen tube abnormalities, including thickened walls, bulbous swellings,

12

M. SEDGLEY

Table 1.2. Banksia interspecific combinations with pollen tube growth to the base of the style or with viable seed set (Sedgley et al. 1994.1996; Maguire and Sedgley 1997b). Female parent

B. menziesii

B. prionotes

B. hookeriana B. coccinea

Male parent

Pollen tube growth

Viable seed set

B. baxteri B. speciosa B. candolleana B. prionotes B. burdettii B. tricuspis B. baxteri B. speciosa B. eJderiana B. coccinea B. brownii B. tricuspis B. prionotes B. ericifolia B. micrantha B. sphaerocarpa

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

No No No No No No No No No No No No Yes

No No No

directionless growth, burst tips, and branched tubes (Sedgley et al. 1994, 1996; Maguire and Sedgley 1997b). Control of pollen tube growth in the pistil was imposed in the pollen presenter and upper style. A number of species combinations showed pollen tube growth to the base of the style, but only the B. hookeriana by B. prionotes cross has so far resulted in seed set (Table 1.2). Given that intraspecific seed set of Banksia is very low, in the order of 3.50/0 (Sedgley et al. 1996), it is important to repeat the crosses that showed pollen tube growth to the base of the style, with higher numbers of pollinations. Natural interspecific hybrids have occurred, both in the wild and under cultivation (Taylor and Hopper 1988), including crosses between B. hookeriana and B. prionotes. One such putative hybrid with horticultural merit, registered as the cultivar 'Waite Orange' (Sedgley 1991), was studied using morphological, sexual, and biochemical characters (Sedgley et al. 1994, 1996). Hybrid status of 'Waite Orange' was confirmed using morphological characters, and controlled pollination showed that the hybrid was fertile following controlled selfing and backcrossing to both parental species, as well as following open pollination, but that seed set was lower than for the parental species. In addition, interspecific hybridization between B. hookeriana and B. prionotes was investigated via pollen tube growth, seed set, and morphological measurements. Pollen tube growth to the ovary was observed following self

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

13

and cross intraspecific pollination of both species and following interspecific hybridization to B. hookeriana as the seed parent, but not in the reciprocal cross. All crosses resulted in seed set, except for self pollination of B. prionotes and interspecific pollination to B. prionotes as the seed parent. Mortality of hybrid seedlings was high. RAPD analysis of hybrid seedlings from two families showed the presence of paternal B. prionotes bands in all 11 seedlings tested. Leaf length or width of nine hybrid seedlings that survived to the ten leaf stage was intermediate between that of intraspecific seedlings of both parents at the same age. It was concluded that hybridization between B. hookeriana and B. prionotes is unilateral, with interspecific seed set of B. hookeriana comparable to that following intraspecific pollination. Isozyme and AP-PCR analysis confirmed that the two parent species were closely related. D. Cultivars

Banksia species are relatively new to the cut flower industry, and there has been little emphasis placed on cultivar development. There are seven named cultivars of Banksia for amenity use, but only three for cut flower production, and all are propagated vegetatively to perpetuate their superior varietal characteristics. The ten named cultivars were derived from open pollinated populations under cultivation, and none so far has resulted from controlled hybridization. Of the seven cultivars for environmental horticulture, three are prostrate forms. 'Celia Rosser' is derived from an open-pollinated seedling of B. canei. It has deeply lobed leaves, a prostrate growth habit, and yellow inflorescences. 'Austraflora Pygmy Possum' is a coastal low-growing form of B. serrata, and 'Roller Coaster' is a prostrate variant of B. integrifolia. The other four cultivars have the more usual upright habit of Banksia species. 'Limelight' is a sport of B. ericifolia with lime green foliage, 'Giant Candles' is an interspecific hybrid between B. ericifolia and B. spinulosa var. spinulosa that arose in cultivation, 'Lemon Glow' is a yellow-flowered form of B. spinulosa var. cunninghamii, and 'Birthday Candles' is a dwarf form of B. spinulosa var. spinulosa. All of these varieties are for garden use, with 'Birthday Candles' for pot and garden cultivation. There are three terminal-flowering cultivars for cut flower production. 'Waite Orange' (Fig. 1.1) is a natural interspecific hybrid between B. hookeriana and B. prionotes, that flowers between the peak period of the two parental species and so extends the season for production of orange Banksia blooms (Sedgley 1991, 1995c,d). 'Waite Crimson' is a mid-season dark red selection of B. coccinea (Sedgley 1995a), and 'Waite

14

M. SEDGLEY

Flame' is an early season orange-red selection, also of B. coccinea (Sedgley 1995b). V. PHYSIOLOGY

A. Flowering Floral intitation of the species B. coccinea, B. menziesii, B. hookeriana, and B. baxteri occurs between October and December, the southern hemisphere late spring and early summer (Fuss et al. 1992; Rohl et al. 1994). Although floral initiation occurs at roughly the same time of year in all four species, flowering does not, and the main difference between them is in the rate of development of the initiated inflorescences. This is very important commercially, as it means that pruning must be carried out prior to October, even in the late-flowering species such as B. coccinea, or the grower risks removing intitated blooms for the next year's harvest (Sedgley and Fuss 1992). Only the thickest shoots will initiate an inflorescence, and the likelihood of a shoot producing a bloom is correlated with shoot age and shoot size. The age of a shoot is determined from the number of bud scar rings, with two-year-old shoots having a ring of bud scale scars at the base, and another ring half way along the shoot. Most blooms are produced on shoots that are two years old, with only a minority produced on one- or three-year-old shoots. Thus, each shoot must be allowed to develop for two years before a bloom can be expected, and some shoots never produce blooms. These are thin and weak compared with those that do, and there is a minimum shoot diameter, measured at the bud scar ring at the base of the current flush growth, which must be achieved for a shoot to flower. The critical diameter is 4.5 mm for B. coccinea, 6 mm for B. menziesii, 8 mm for B. hookeriana, and 11 mm for B. baxteri, and the information has been used to develop a pruning strategy for Banksia (Sedgley and Fuss 1992). High light intensity is also important for successful flowering of Banksia, with pruning to prevent shading an important consideration. Floral initiation in the southern hemisphere late spring or early summer indicates that the environmental cues of increasing temperature and daylength may be important. This has been confirmed by experiments in which plants of B. coccinea and B. hookeriana were grown in environmental growth chambers, with full control of temperature and daylength (Rieger and Sedgley 1996). Four sets of conditions were imposed, with 8 and 16 h daylength, each with two temperature regimes of 15/10 oe (day/night) and 25/20 oe. For B. coccinea, most floral initiation occurred at 16 h 25/20 oe and 16 h lS/10oe, with less initiation at 8 h 15/1o oe and none at 8 h 25/20 oe. This indicates that long daylength

1.

BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

15

may be the environmental trigger for flowering in this species. For B. hookeriana, both the 16 and 8 h 25/20°C treatments stimulated flowering, with no floral initiation at 15/10°C with either 16 or 8 h daylength. This indicates that for B. hookeriana temperature has the major control over floral initiation. Manipulation of Banksia flowering, to induce early or late flowering or to extend the production season, is not currently practised, but these research results introduce the possibility for extension of the flowering period of B. coccinea. By using supplementary lights to increase the natural daylength during winter, it may be possible to induce the plants to initiate earlier, and so possibly to flower earlier. Extension of the flowering period by inducing late initiation is more of a problem, as the plants would need short days at a time when natural daylength is increasing. While this is difficult in the field, it may be possible under protection. Manipulation of temperature, as required for B. hookeriana, could also be achieved under cover. The Banksia bloom is an inflorescence comprising many hundreds of individual flowers; if initiation is incomplete, it can result in uneven or truncated blooms. Low temperature effects appear to be particularly common, correlating with abnormal blooms of B. coccinea (Fuss and Sedgley 1991a) and B. menziesii (Fuss et al. 1992). Careful site selection and provision of windbreaks or shelter are the most effective means of controlling the problem. B. Propagation

Banksia seeds are encased by woody follicles in cone-like infructescences. The follicles of most species are adapted to open only after fire (Elliot and Jones 1992), although there are exceptions to this rule, including B. marginata and B. integrifolia (Wardrop 1983). Heat generated during a wildfire melts adhesive material sealing the follicle, and the effect can be simulated in a fire or oven. A period of rain after the wildfire is important in some species, and this can be simulated by submerging the infructescences in cold water for between one and three days, followed by sun drying (Elliot and Jones 1992). In contrast to some other genera of Proteaceae, the seeds of Banksia species require no germination pretreatment. They are generally large and rich in nutrients (Pate et al. 1986), and so tend to have high germination success rates. The temperature optimum for germination varies with species, from 18-23°C for B. integrifolia to 28-32°C for B. aemula (Heslehurst 1979), with 10-25°C the best range for B. coccinea (Bennell and Barth 1986a). For germination of B. coccinea, B. aculeata, and B. ornata, 15°C is the optimum temperature,

M. SEDGLEY

16

with 70% germination of B. aculeata seed at 25°C as compared with 100% at 15°C. Germination rate is slow, with first emergence after about three weeks, but taking up to three months for complete germination. Following germination, seedling growth is fastest at 25°e. Propagation of Banksia species by rooted cuttings is variable (Bennell and Barth 1986a), and is based on semi-hardwood material collected following the spring growth flush, during the cooler months of the year. Some species will produce roots with no auxin treatment (George 1984), although better results are achieved with 3,500 ppm indolebutyric acid (IBA) for most species. The highest strike rates for B. coccinea were achieved with 8,000 to 12,000 ppm IBA (Bennell and Barth 1986a), and although some cuttings produced roots at all concentrations tested, root development was better with IBA than without. Genotype also influences rooting, with variation from to 80% success for different individuals of B. hookeriana and B. prionotes (Sedgley 1995c,d). Success with micropropagation has resulted in culture establishment of B. coccinea, B. ericifoJia, B. lemanniana, B. marginata, B. menziesii, B. ornata, B. prionotes, B. serrata, and B. spinulosa var. collina from nodal segments and shoot tips (K. M. Tynan, E. S. Scott, and M. Sedgley unpublished). Murashige and Skoog medium with benzyladenine resulted in slow growth and multiplication rates; with shoot formation on cultures of B. coccinea and B. spinulosa var. collina. Roots were induced on excised shoots of B. coccinea using filter paper bridges over liquid medium, but there has been little success so far in hardening off rooted explants. There has been little consistent success with grafting and budding of Banksia species. Rootstocks used for experimentation are generally seedlings of B. integrifolia, B. spinulosa, and B. marginata that are tolerant of heavy soils and of the root rot fungus Phytophthora cinnamomi Rands (McCredie et aI. 1985a). Bennell and Barth (1986b) used a wedge graft for field-grown scions of B. coccinea and B. menziesii, which had been girdled four weeks prior to grafting. The overall success rate for both species was between 30 and 400/0 at 20 weeks, but a further complication is that grafts may survive for a number of years, with the union failing under conditions of stress (Elliot and Jones 1992). At present the success rate does not justify commercial use of grafting for Banksia, and further research is needed into graft compatibility.

°

C. Water and Nutrient Uptake

Most species of Banksia are native to the Mediterranean climate areas of south-western Australia, with some from south-eastern Australia and

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

17

one tropical species that extends into New Guinea and the Aru Islands (George 1987). All species grow best in light sandy soils of acid pH, and the south-western Australian species are particularly intolerant of heavy soils. Most are adapted to a hot, arid summer prone to bushfires, and have developed strategies to cope with these conditions (Cowling and Lamont 1986). They are adapted to poor soils of low nutritional status, particularly phosphorus, and develop proteoid roots for increased nutrient absorption (Lamont 1986; Low and Lamont 1986). Proteoid roots are specialisations for solubilization of soil phosphates (Grierson and Attiwill 1989), and to increase the root surface area for absorption. In the native habitat they are major exporters to other parts of the plant of phosphate, potassium, and amino acids during the wet winter season (Jeschke and Pate 1995). The Banksia root system is dimorphic, with proteoid root-bearing shallow lateral roots in the top 15 em, and a single tap or sinker root extending down to 7 m, or to the water table if located higher than this depth (Low and Lamont 1990; Dodd and Bell 1993; Pate et a1. 1995). Proteoid roots die during the arid summer, and regenerate during the wet winter of the native habitat, while shoot growth patterns are the reverse, with extension during summer. The amount of water required by Banksia plants of different ages has not been determined, but water stress can be a limitation to seedling establishment in the wild (Burgman and Lamont 1992; Enright and Lamont 1992). Investigation of xylem and phloem sap of B. prionotes indicates that lateral root xylem sap is more concentrated in virtually all solutes than that of sinker roots, even during the dry summer following senescence of the proteoid roots (Jeschke and Pate 1995). Gradients in xylem sap concentration suggest lateral abstraction and storage of incoming phosphate in basal stem parts during winter with subsequent release to the xylem in summer for the growing period. Phloem sap is more concentrated than xylem sap in nutrient ions and amino acids. Under cultivation, phosphorus toxicity can be a problem for Banksia species, with symptoms reported in cut flower plantings with soil levels of greater than 40 ppm. In a detailed study, interactive effects between phosphorus and iron have been reported in B. ericifolia subsp. ericifolia grown in soilless potting medium (Handreck 1991). As the phosphorus level was increased, iron deficiency symptoms increased, indicating preferential translocation of phosphorus over iron. The ideal ratio of phosphorus to iron in the medium was around 20, in media containing less than 3 mglL phosphorus and 1.5 gIL iron. An important feature of Banksia biology is that high levels of nutrients are concentrated

18

M. SEDGLEY

in the seeds to give seedlings an advantage in the poor native soils of Australia (Groves et al. 1986; Pate et al. 1986).

D. Postharvest Physiology Relatively little research has been conducted on preservative or pulsing solutions for fresh Banksia cut blooms, but sucrose pulsing generally does not enhance quality or longevity, and concentrations above 2 % are detrimental. Work with B. coccinea found no effect of sucrose pulsing, with blooms having a vase life of 15 days in water plus 0.01 % chlorine (Delaporte et al. 1997). Hydroxy quinoline sulphate is detrimental, as it causes reduction in vase life and accelerated opening of the florets. Cold dry storage is possible at 2°e and 100% relative humidity in darkness for 14 days, after which there is a 10-day vase life. Research aimed at postharvest insect removal has tested a range of measures (Seaton and Joyce 1992, 1993). Conventional disinfestation methods involving chemical control have no phytotoxic effects on B. hookeriana blooms, but there is a need to develop alternative methods for safety reasons. Gamma irradiation is unsuitable because it damages Banksia blooms (Seaton and Joyce 1992), as do volatiles such as acetaldehyde, although to a lesser extent. Low temperature and high carbon dioxide treatments show promise for Banksia stems, as all test insects are killed by 10 to 14 days storage at l°e, with a reduction to seven days if 45-60% e0 2 is combined with the low temperature treatment (Seaton and Joyce 1993). B. hookeriana has an acceptable vase life following treatment of up to 28 days at l°e. Hot water dips are less successful, with Banksia blooms damaged by all treatments that kill insects. Lower-quality blooms unsuitable as fresh stems are often dried. For natural drying the blooms are hung, and the process can be accelerated by solar heating, hot air dryers, dehumidifiers, microwaving, freezing, and dehydration using silica gel. The colors of both flowers and leaves fade under these conditions, and sulfuring to preserve color is achieved either by burning elemental sulfur or by using sulfur dioxide gas in an enclosed area. The orange Banksia species and B. menziesii respond well to sulfuring. Stems can be bleached using hypochlorite, chlorite, peroxide, or hydrosufite (Dubois and Joyce 1992), or preserved by placing in 10% glycerine for 24 h before drying. This latter treatment gives a shiny gloss to the dried product, which retains flexibility. It is not suitable for cut blooms, as these damage easily when treated with glycerine. Dyed Banksia blooms are popular for some markets. Blooms of palecolored species such as B. baxteri, B. speciosa, and the unopened buffcolored flowers of the orange species are dipped into aniline or

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

19

water-soluble dyes. These impart a wide range of bright, vibrant colors, including blue, purple, orange, red, and green, or combinations. Uptake dyes produce more subtle colors but are not much used.

VI. PRODUCTION A. Culture

Banksia species are cultivated almost exclusively without protection and planted directly into soil. There has been little attempt at protected cultivation, although B. menziesii can be grown experimentally in nutrient solution (Avidan et al. 1983 cited by Ben-Jaacov et al. 1989). Between-plant spacings vary from 2 m for the more compact species such as B. coccinea to 3.5 m for the more spreading B. speciosa and B. prionotes, with between-row spacings of between 3 and 6.5 m (Sedgley 1996). Windbreaks, weed removal, and rabbit protection are often used, and a mulch of a freely-draining medium such as gravel or coarse sand aids in protection of the roots from extremes of temperature. Drippers or microjets are the most efficient for irrigation, and tensiometer studies indicate that in Australia irrigation of 4 litres per plant per day is advisable in all except the winter months. Application of nitrogen, potassium, and iron are important, but high levels of phosphorus are generally avoided, with slow-release low-phosphorus fertilizer used in most nurseries. Healthy growth has been recorded with 0.5 g urea plus 0.5 g potassium chloride applied per plant through the irrigation system every six weeks, with 1 g ammonium nitrate and 1 g potassium sulfate per week during the active growth and flowering period. Iron chelate is also applied when chlorosis is a problem. B. Diseases and Pests The most important disease of Banksia species, both in the wild and under cultivation, is root rot caused by the pathogen Phytophthora cinnamomi. The disease is soil borne, and is readily transmitted on feet, vehicles, tools, and by water. In the nursery, the disease causes damping off of seedlings. In the field, poor growth is followed by drying and wilting of the foliage, because by the time above-ground symptoms are visible, the root system has been heavily colonised. In addition to dead roots, there is often collar rot at ground level. It has been recorded that a number of other Phytophthora species infect Banksia plants, particularly in nurseries. These include P. dreshsleri Tucker, P. nicotianae

20

M. SEDGLEY

Waterhouse, P. cactorum Schrot., and P. citricola Sawada (Hardy and Sivasithamparam 1988; Tynan et a1. 1995). Control of Phytophthora is very difficult. Introduction of the disease to a new nursery or planting should be avoided, as it is impossible to eradicate the disease once it is established, and it can survive in soil without a host for many years. The development of Phytophthoratolerant cultivars may be possible (Tynan et a1. 1995), as there is both between and within species variability (Cho 1981, 1983; McCredie et a1. 1985a,b). Tolerance screening requires an effective non-destructive method (Dixon et a1. 1984), and an excised root assay appears to be the most reliable (Tynan et a1. 1995). Another promising approach is the use of antagonistic biological control agents; the bacterium Pseudomonas cepacia Burkh. has been used to suppress the effects of the disease in the nursery (Turnbull et a1. 1992). Grafting of susceptible types onto tolerant species has been suggested as an alternative control measure for the field (McCredie et a1. 1985a), but grafting success to date has not reached commercial levels. Chemicals can be used to combat Phytophthora, but eradication of the fungus from infected land is difficult, and there may be phytotoxic effects. Banksia species are attacked by relatively few pests, and most are insects that cause damage to the blooms or seeds (Scott 1982; Zammit and Hood 1986; Wallace and O'Dowd 1989; Woods 1988; Vaughton 1990). Tunnelling moth larvae (Arotrophora spp.) are the most common of the Banksia flower caterpillars, both under cultivation and in the wild. The adult moth lays eggs on immature blooms and the larvae move into the center of the inflorescence stem and kill large numbers of flowers by feeding on the soft tissue. The larvae pupate in the flower stem, and control is difficult because they are protected within the inflorescence rachis. Larvae of a number of Lepidopteran genera may cause damage by feeding on flowers, including Cryptophasa sp., Peraglyphis idiogenes Common, and Xyloryctis spp. The Coleopteran Myositta has been reported on B. menziesii flowers in the wild, and leaf damage can be caused by the chewing snout beetle, Catasarcus sp. In contrast to the small number of flower predators, a wide range of insect genera has been recorded feeding on seeds within the Banksia infructescence. These include Lepidopterans of the genera Arotrophora, Chalarotona, Scieropepla, Xyloryeta, Xyloryctis, Brachmia, and Carposina, the Coleopterans Alphitopis nivea Pascoe, Cechides amoenus Pascoe, and Myositta spp, and unidentified Coleopteran weevils. Banksia seeds form part of the natural diet of parrots and cockatoos, and cones are often predated in cultivated plantings and in the wild (Vaughton 1990; Witkowski et a1. 1991). Predators include the crimson

1. BANKSIA: NEW PROTEACEOUS CUT FLOWER CROP

21

rosella, Platycereus elegans Gmelin, and the yellow-tailed black cockatoo, Calyptorhynchus funereus Shaw. Open blooms are often removed from the plant, as well as cones with developing seeds.

VII. CONCLUSIONS

Banksia species are already established as cut flower crops, and are amongst the most readily identifiable of Australian native plants (Plate I). They are accepted on international markets and demand currently exceeds supply. This situation will not continue indefinitely, and while lesser quality may be acceptable in a sellers' market, this will not be the case as supply increases. Considerably more research is needed into all aspects of Banksia production so that stems can compete with the high standard expected of established cut flower crops such as rose and carnation. In addition to making good commercial sense, there are strong environmental reasons why further research into Banksia biology is essential. Until the early 1980s, most Banksia stems for the cut flower market were bush picked from the native habitat, particularly in south-western Australia (Pegrum 1988), and Banksia is still the second largest bush picked genus in Australia. This has resulted in major damage to natural ecosystems via disturbance, introduction of disease, and depletion of seed reserves. Soil and plant destruction is caused by access vehicles, and soil-borne diseases are spread on tires and footwear. The root rot fungus Phytophthora cinnamomi attacks a wide range of native genera, including Banksia, and is very readily distributed (Shearer et al. 1991). The aerial canker diseases Diplodina sp., Zythiostroma spp., and Botryosphaeria ribis Gossenb. & Dugger are spread via infected secateurs, and have been the cause of more recent concern. Diplodina cankers girdle branches and eventually kill the plant, the disease being most prevalent in stands aged over 12 years. Removal of blooms depletes the seed bank and has implications for continued regeneration. Legislation is now in place to prevent bush picking of B. coccinea and B. baxteri from crown land, and this has resulted in an increase in Banksia plantings for cut flower production. The visual appeal of Banksia blooms is unquestioned, but there are other features that will ensure continued popularity, including long shelf life and variety of color and form. Continued research input into production problems is needed to ensure stability of the international industry in a new but increasingly popular cut flower commodity.

22

M. SEDGLEY

LITERATURE CITED Avidan, A., I. Wallerstein, and Y. Chen. 1983. Growing Banksia menziesii in nutrient solution: the essentiality of the proteoid roots. Hassadeh 63:2626-2632. Ayre, D. J., and R J. Whelan. 1989. Factors controlling fruit set in hermaphroditic plants: studies with the Australian Proteaceae. Tree 4:267-272. Ben-Jaacov, J. 1986. Protea production in Israel. Acta Hort. 185:101-110. Ben-Jaacov, J., A. Ackerman, S. Gilad, and Y. Shchori. 1989. New approaches to the development of Proteaceous plants as floricultural commodities. Acta Hort. 252:193199. Bennell, M., and G. Barth. 1986a. Propagation of Banksia coccinea by cuttings and seed. Proc. Int. Plant Prop. Soc. 36:148-152. Bennell, M., and G. Barth. 1986b. Selection and grafting studies of Banksia coccinea and Banksia menziesii. Proc. Int. Plant Prop. Soc. 36:220-224. Bickford, S. A., and M. Sedgley. 1994. Colour variation of Banksia menziesii blooms for cut flower production. J. Hart. Sci. 69:993-997. Bickford, S. A., and M. Sedgley. 1995. Banksia menziesii: the chameleon banksia. Austral. Hart. 93(2):43-46. Burgman, M. A., and B. B. Lamont. 1992. A stochastic model for the viability of Banksia cuneata populations: environmental, demographic and genetic effects. J. Appl. Ecol. 29:719-727. Carthew, S. M., D. J. Ayre, and R J. Whelan. 1988. High levels of outcrossing in populations of Banksia spinuJosa RBr. and Banksia paludosa Smith. Austral. J. Bot. 36:217-223. Cho, J. J. 1981. Phytophthora root rot of Banksia: host range and chemical control. Plant Dis. 65:830-833. Cho, J. J. 1983. Variability in susceptibility of some Banksia species to Phytophthora cinnamomi and their distribution in Australia. Plant Dis. 67:869-871. Clifford, S. c., and M. Sedgley. 1993. Pistil structure of Banksia menziesii RBr. (Proteaceae) in relation to fertility. Austral. J. Bot. 41:481-490. Coates, D. J., and R E. S. Sokolowski. 1992. The mating system and patterns of genetic variation in Banksia cuneata A.S. George (Proteaceae). Heredity 69:11-20. Cowling, R M., and B. B. Lamont. 1986. Population ecology of Western Australian Banksia species: implications for the wildflower industry. Acta Hort. 185:217-227. Criley, R. A. 1998. Developmental Research for Proteaceaous Cut Flower Crops: Leucospermum. Hort. Rev. 21:00. Delaporte, K. L., A. Klieber, and M. Sedgley. 1997. To pulse or not to pulse? Improving the vase life of Banksia coccinea by postharvest treatments. Austral. Hart. 95(8),79-84. Dixon, K., W. Thinlay, and K. Sivasithamparam. 1984. Technique for rapid assessment of tolerance of Banksia spp. to root rot caused by Phytophthora cinnamomi. Plant Dis. 68:1077-1080. Dodd, J., and D. T. Bell. 1993. Water relations of the canopy species in a Banksia woodland, Swan coastal plain, Western Australia. Austral. J. Bot. 18:281-293. Dubois, P., and D. C. Joyce. 1992. Bleaching ornamental plant material: a brief review. Austral. J. Expt. Agr. 32:785-790. Elliot, W. R, and D. L. Jones. 1992. Encyclopaedia of Australian Plants Suitable for Cultivation. Volume 2. Lothian Publishing Company Pty. Ltd., Melbourne, Austral. Enright, N. J., and B. B. Lamont. 1992. Survival, growth and water relations of Banksia seedlings on a sand mine rehabilitation site and adjacent scrub-heath sites. J. Appl. EcoL 29:663-671.

1. BANKSIA: NEW PROTEACEOUS CUT FLOWER CROP

23

Fuss, A. M., S. J. Pattison, D. Aspinall, and M. Sedgley. 1992. Shoot growth in relation to cut flower production of Banksia coccinea and Banksia menziesii (Proteaceae). Scientia Hort. 49:323-334. Fuss, A. M., and M. Sedgley. 1990. Floral initiation and development in Banksia coccinea RBr. and B. menziesii RBr. (Proteaceae). Austral. J. Bot. 38:487-500. Fuss, A. M., and M. Sedgley. 1991a. Variability in cut flower production of Banksia coccinea RBr. and Banksia menziesii R Br. at six locations in southern Australia. Austral. J. Expt. Agr. 31:853-858. Fuss. A. M., and M. Sedgley. 1991b. Pollen tube growth and seed set of Banksia coccinea RBr. (Proteaceae). Ann. Bot. 68:377-384. Fuss, A. M., and M. Sedgley. 1991c. The development of hybridisation techniques for Banksia menziesii for cut flower production. J. Hort. Sci. 66:357-365. George, A. S. 1981. The genus Banksia LJ. (Proteaceae). Nuytsia 3:239-473. George, A. S. 1984. The remarkable banksias. Wildflowers of great potential. Austral. Hort. 82(10):16-21. George. A. S. 1987. The Banksia Book. Kangaroo Press. Austral. George, A. S. 1988. New taxa and notes on Banksia L.f (Proteaceae). Nuytsia 6:309-317. George, A. S. 1996. Notes on Banksia LJ. (Proteaceae). Nuytsia 11:21-24. George, A. S. 1997. Banksia. In: Proteaceae 2. Flora of Australia Volume 17. Australian Biological Resources Study. Commonwealth Scientific and Industrial Research Organisation. Canberra. Goldingay R L., and S. M. Carthew. 1997. Breeding and mating systems of Australian Proteaceae. Austral. J. Bot. (in press). Grierson, P. F., and P. M. Attiwill. 1989. Chemical characteristics of the proteoid root mat of Banksia integrifolia L. Austral. J. Bot. 37:137-143. Groves, R H., P. J. Hockin, and A. McMahon. 1986. Distribution of biomass, nitrogen, phosphorus and other nutrients in Banksia marginata and B. ornata shoots of different ages after fire. Austral. J. Bot. 34:709-725. Handreck, K. A. (1991). Interactions between iron and phosphorus in the nutrition of Banksia ericifolia L.f. var. ericifolia (Proteaceae) in soil-less potting media. Austral. J. Bot. 39:373-384. Hardy, G. E., and K. Sivasithamparam. 1988. Phytophthora spp. associated with containergrown plants in nurseries in Western Australia. Plant Dis. 72:435-437. Heslehurst. M. R 1979. Germination of some Banksia species. Austral. Plants 10:176-177. Jeschke, W. D., and J. S. Pate. 1995. Mineral nutrition and transport in xylem and phloem of Banksia prionotes (Proteaceae), a tree with dimorphic root morphology. J. Expt. Bot. 46:895-905. Jones. R B., R McConchie. W. G. van Doorn, and M. S. Reid. 1995. Leaf blackening in cut Protea flowers. Hort. Rev. 17:173-202. Lamont, B. B. 1986. The significance of proteoid roots in proteas. Acta Hort. 185:163-170. Low, A. B., and B. B. Lamont. 1986. Nutrient allocation in winter rainfall proteaceous heathlands in relation to nutrient losses through wildflower picking and fire. Acta Hart. 18: 889-899. Low, A. B., and B. B. Lamont. 1990. Aerial and below-ground phytomass of Banksia scrub-heath at Eneabba, South-western Australia. Austral. J. Bot. 38:351-359. Maguire, T., G. Collins, and M. Sedgley. 1994. Extraction of DNA from plants from the family Proteaceae using a modified CTAB method. Plant Molec. BioI. Reptr. 12:106-109. Maguire, T. L., J. G. Conran, G. G. Collins, and M. Sedgley. 1997d. Molecular analysis of interspecific and intergeneric relationships of Banksia using RAPDs and non-coding chloroplast DNA sequences. Theor. App!. Genet. 95:253-260.

24

M. SEDGLEY

Maguire, T. L., J. G. Conran, and M. Sedgley. 1996. Banksia Sect. Coccinea (AS. George) T. Maguire et al., (Proteaceae). A new section. Austral. Syst. Bot. 9:887-891. Maguire, T. L., and M. Sedgley. 1997a. Storage temperature affects viability of Banksia menziesii pollen. HartSeL 32:916-917. Maguire, T. L., and M. Sedgley. 1997b. Interspecific and intergeneric hybridisation with Banksia coccinea RBr (Proteaceae). Austral. J. Bot. (in press). Maguire, T. L., and M. Sedgley. 1997c. Genetic diversity in Banksia and Dryandra (Proteaceae) with emphasis on Banksia cuneata, a rare and endangered species. Heredity 79:394-401. Mast, A R. 1997. A molecular phylogeny of Banksia and the tribe Banksieae based on ITS and cpDNA sequence data: implications for systematics, biogeography, and character evolution. Austral. Syst. Bot. (in press). McCredie, T. A, K. W. Dixon, and K. Sivasithamparam. 1985a. Grafting banksias to avoid root rot. Austral. Hart. 83(4):75-79. McCredie, T. A, K. W. Dixon, and K. Sivasithamparam. 1985b. Variability in the resistance of Banksia LJ. species to Phytophthora cinnamomi Rands. Austral. J. Bot. 33:629-637. Pate, J. S., E. Rasins, J. Rullo, and J. Kuo. 1986. Seed nutrient reserves of Proteaceae with special reference to protein bodies and their inclusions. Ann. Bot. 57:747-770. Pate, J. S., W. D. Jeschke, and M. J. Aylward. 1995. Hydraulic architecture and xylem structure of the dimorphic root systems of south-west Australian species of Proteaceae. J. Expt. Bot. 46:907-915. Pegrum, J. 1988. Making the most of our floral resources. J. Agr. Western Austral. 29: 115-118. Rieger, M. A, and M. Sedgley. 1996. Effect of daylength and temperature on flowering of the cut flower species Banksia coccinea and Banksia hookeriana. Austral. J. Expt. Agr. 36:747-753. Rohl, L. J., A. M. Fuss, J. A. Dhaliwal, M. G. Webb, and B. B. Lamont. 1994. Investigation of flowering in Banksia baxteri RBr. and B. hookeriana Meissner for improving pruning practices. Austral. J. Expt. Agr. 34:1209-1216. Salkin, A, and N. D. Hallam. 1978. The topodemes of Banksia canei J. H. Wills (Proteaceae). Austral. J. Bot. 26:707-721. Scott, J. K. 1980. Estimation of the outcrossing rate for Banksia attenuata RBr. and Banksia menziesii RBr. (Proteaceae). Austral. J. Bot. 28:53-59. Scott, J. K. 1982. The impact of destructive insects on reproduction in six species of Banksia LJ. (Proteaceae). Austral. J. Zool. 30:901-921. Seaton, K. A, and D. C. Joyce. 1992. Gamma irradiation for insect disinfestation damages native Australian cut flowers. Scientia Hart. 52:343-355. Seaton, K. A., and D. C. Joyce. 1993. Effects of low temperature and elevated CO 2 treatments and of heat treatments for insect disinfestation on some native Australian cut flowers. Scientia Hart. 56:119-133. Sedgley, M. 1991. Banksia (Banksia hookeriana hybrid). Plant Varieties J. 4(2):9-11. Sedgley, M. 1995a. Banksia coccinea 'Waite Crimson'. Plant Varieties J. 8(2):8-9; 18. Sedgley, M. 1995b. Banksia coccinea 'Waite Flame'. Plant Varieties J. 8(2):9; 18-19. Sedgley, M. 1995c. Cultivar development of ornamental members of the Proteaceae. Acta Hort. 387:163-169. Sedgley, M. 1995d. Breeding biology of Banksia species for floriculture. Acta Hart. 397:155-162. Sedgley, M. 1996. Banksia. p. 20-37. In: K. A Johnson and M. D. Burchett (eds.), Australian Native Plants-Horticulture and Uses. University of New South Wales Press, Sydney, Austral.

1. BANKS/A: NEW PROTEACEOUS CUT FLOWER CROP

25

Sedgley, M., and A. M. Fuss. 1992. Correct pruning lifts banksia yields. Austral. Hort. 90:50-53.

Sedgley, M., and A.M. Fuss. 1995. Reproductive biology of Banksia. Acta Hort. 387:187-190.

Sedgley, M., M. G. Sierp, and T. L. Maguire. 1994. Interspecific hybridization involving Banksia prionotes Lind. and B. menziesii R.Br. (Proteaceae). Int. J. Plant Sci. 155:755-762.

Sedgley, M., M. Sierp, M. A. Wallwork, A. M. Fuss, and K. Thiele. 1993. Pollen presenter and pollen morphology of Banksia LJ. (Proteaceae). Austral. J. Bot. 41:439-464. Sedgley, M., M. G. Wirthensohn, and K. 1. Delaporte. 1996. Interspecific hybridization between Banksia hookeriana Meisn, and B. prionotes Lindl. (Proteaceae). Int. J. Plant Sci. 157:638-643. Shearer, B., R. Wills, and M. Stukey. 1991. Wildflower killers. Landscope 7:28-34. Taylor, A., and S. Hopper. 1988. The Banksia Atlas. Australian Flora and Fauna Series, no. 8, Australian Government Publishing Service, Canberra, Austral. Thiele, K., and P. Y. Ladiges. 1996. A cladistic analysis of Banksia (Proteaceae). Austral. Syst. Bot. 9:661-733. Turnbull, 1. V., H. J. Ogle, A. M. Stirling, and P. J. Dart. 1992. Preliminary investigations into the influence of Pseudomonas cepacia on infection and survival of proteas in Phytophthora cinnamomi infected potting mix. Scientia Hort. 52:257-263. Tynan, K. M., E. S. Scott, M. Sedgley, K. Dixon, and K. Sivasithamparam. 1995. Phytophthora dieback in banksias: screening for resistance. Acta Hort. 387:159-162. Vaughton, G. 1990. Predation by insects limits seed production in Banksia spinulosa var. neoanglica (Proteaceae). Austral. J. Bot. 38:335-340. Wallace, D. D., and D. J. O'Dowd. 1989. The effect of nutrients and inflorescence damage by insects on fruit-set by Banksia spinulosa. Oecologia 79:482-488. Wardrop, A. B. 1983. The opening mechanism of follicles of some species of Banksia. Austral. J. Bot. 31:485-500. Witkowski, E. T. F., B. B. Lamont, and S. J. Connell. 1991. Seed bank dynamics of three co-occurring banksias in south coastal Western Australia: the role of plant age, cockatoos, senescence and interfire establishment. Austral. J. Bot. 39:385-397. Woods, W. 1988. Pests of native flowers. J. Agr. Western Austral. 29:119-121. Zammit, C., and C W. Hood. 1986. Impact of flower and seed predators on seed-set in two Banksia shrubs. Austral. J. Ecol. 11:187-193. Zammit, C, and M. Westoby. 1987. Population structure and reproductive status of two Banksia shrubs at various times after fire. Vegetatio 70:11-20.

2 Leucospermum: Botany and Horticulture * Richard A. CrUey Department of Horticulture University of Hawaii Honolulu, Hawaii 96822

I. Introduction II. Botany A. Origin and Ecology B. Morphology C. Taxonomy D. Floral Physiology 1. Flowering 2. Pollination Biology E. Genetics III. Horticulture A. Propagation 1. Seed 2. Cuttage 3. Grafting 4. Tissue Culture B. Environmental Responses 1. Light 2. Temperature 3. Cold Tolerance 4. Soils C. Cultural Practices 1. Spacing 2. Pruning 3. Disbudding 4. Irrigation *Published as Journal Series No. 4303 of the College of Tropical Agriculture and Human Resources, University of Hawaii, Honolulu, HI. Acknowledgment is made to Dr. Philip E. Parvin and Dr. Gert J. Brits for their assistance in the preparation of this review.

Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 27

R. CRILEY

28 5. Nutrition and Fertilization 6. Production Period 7. Growth Regulator Studies

D. Plant Protection 1. Diseases 2. Nematodes 3. Insect Pests 4. Weeds E. Postharvest Studies 1. Handling and Storage 2. Insect Eradication 3. Grades and Standards F. Genetic Improvement G. Leucospermum as a Pot Plant 1. Production 2. Postproduction IV. Crop Potential and Research Needs Literature Cited

I. INTRODUCTION

The Proteaceae embrace 82 genera, of which the most important cut flower genera are Protea, Leucospermum, Leucadendron, Banksia (Sedgley 1998), and Grevillea (Joyce et a1. 1997), all of which also have species used as cut foliages (Parvin 1991a) and landscape material. The nut crop, Macadamia, is one of the other prized members of the Proteaceae. In this review, the noun protea (proteaceous when used as an adjective) is used in a general sense for the cut flower members of the family, while a genus name is used where it was clearly identified in a citation. Venkata Rao (1971) noted, perhaps incorrectly, that the family Proteaceae contains very few plants of economic importance but that most are rich nectar producers and of value to apiarists. Indeed, it is the copious nectar production in some ornithophilous species of Protea that may lead to the black leaf disorder of the cut flower (Dai and Paull 1995; Jones et a1. 1995). Many proteaceous species are adapted to pollination by birds, and the large solitary inflorescences of these have also attracted the interest of humans because of their ornamental qualities. Brits et a1. (1983) reviewed the development of proteas as cultivated crops in South Africa. In his introduction to the first newsletter of the International Protea Association, G. J. Brits (1984) noted that many South African flowering plants were developed as horticultural crops in Europe, but despite early attempts to cultivate proteas in Europe their specialized horticultural requirements prevented them from incurring

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

29

a similar fate. The distribution of the Proteaceae is linked to the occurrence of acid soils that are extremely deficient in plant nutrients. This linkage continues to frustrate horticulturists who are used to nurturing their plants with fertilizers. Proteas were first cultivated seriously in the early 1900s at the National Botanic Gardens at Kirstenbosch in the Cape province of South Africa, but they had been gathered from mountain veld even earlier and marketed in Cape Town, where an appreciation and acceptance of these cut flowers developed. Following public concern about the pressure that wild flower harvesting was having on the habitat, in 1920 the Kirstenbosch Botanical Gardens encouraged the founding of the "Society for the Protection of Wild Flowers," whose early emphasis was the planting of veld flowers to protect the native flora, a "planting brigade rather than a plucking brigade" according to their original brochure (Brits 1984; Rourke 1980). The progression of proteas in their development as a commercial crop is illustrated in Table 2.1. The use of plantings of selected clonal material is still expanding, while the last stage, use of clonal materials from genetic manipulation, has not begun. The first South African publication on the cultivation of proteas appeared in 1921 (Matthews 1921). This historic, but almost forgotten, article was the forerunner of the vast popular literature available today. Some cultural guides of more recent standing include publications by Vogts (1958,1960,1962,1979,1980,1982), Watson and Parvin (1970), Furuta (1983), Harre (1988b, 1995), Matthews (1993), and McLennan (1993). The foundations for commercial protea cultivation in the Western Cape of South Africa were established during the 1940s to the 1970s by Frank C. Batchelor, who conducted the first breeding efforts, collected natural hybrids and established vegetatively propagated plants, set standards of quality, marketed cultivated proteas overseas, founded the forerunner of South African Protea Producers and Exporters Association (SAPPEX), and identified production research needs. During the 1950s, Marie Vogts gathered the known information about proteas and published it (Vogts 1958). She also identified areas needing more research (Vogts 1960) and played a key role in limiting the damage to wild populations by publishing cultural methods (Vogts 1962, 1979; Vogts et a1. 1972). By the 19608, a small number of managed "flower orchards" were producing flowers of better quality than most of those gathered from the wild, and the introduction of refrigeration facilities in the 1980s improved keeping quality prior to long-distance shipment. Flower importers in the northern hemisphere wanted continuous supplies of the same species throughout the year, whereas most of the proteas being

R. CRILEY

30

Table 2.1. Development of proteas as commercial cut flowers from harvesting in the wild to selection and development of clonal materials. Adapted from: Matthews and Matthews 1994.

Stage Harvesting from naturally occurring proteas in the wild

Characteristics

Quantity & quality

No control of production, weather-dependent, no disease control, high picking costs

Quality and quantity unreliable

2. Plantations raised from seed

Efficient layout, disease control possible, use of irrigation, high replacement rate

Improved reliability and quality, but flower forms variable

3. Plantations from

Stock improved by selection from best seedling materials

Improved reliability and quality, quantities a function of plant numbers

Selection from breeding programs for: flower and leaf life, stem length, disease resistance, packing and shipping qualities, flowering time, productivity

Reliable supplies, premium flower quality. uniform product, high productivity

Rapid response to market requirements for color, vaselife, stem length. Rapid response to disease problems

Premium quality flowers that exactly meet market needs, uniform product, high productivity, and highly competitive with other flower crops

1.

vegetatively propagated material 4. Plantations of

selected clonal material

5. Clonal materials from genetic manipulation and propagation by tissue culture

shipped were highly seasonal. A partial solution to this problem has been to gather early- and late-flowering variants to lengthen the season. More recently, the Fynbos Unit of the South African Agricultural Research Council has been breeding in the important genera of proteas to develop a longer flowering period (Brits 1978, 1992a, 1992b; Littlejohn et a1. 1995; van Vuuren 1995). During the 20th International Horticultural Congress (1978) in Sydney, Australia, growers and researchers from South Africa, Hawaii, Israel, New Zealand, and Australia proposed the concept of an international organization to disseminate the information being generated in different parts of the world. The International Protea Association (IPA) was established in 1981 in Melbourne, Australia, by delegates to the first IPA Conference. The IPA initially represented the interests of growers and shippers, while

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

31

the researchers formed the International Protea Working Group (IPWG) during 1984 meetings in Stellenbosch, South Africa, under the auspices of the Ornamental Section of the International Society for Horticultural Science. Recognizing a need to keep records on new cultivars as they were developed and released, the IPA supported establishment of the International Registration Authority for Proteas in Stellenbosch, South Africa ([email protected]). It has recently published (lnt. Reg. Auth. 1997) the fourth edition of the International Protea Register. Biennial meetings of the IPA and occasional concurrent meetings of the IPWG and IPA have been productive venues for the exchange of information between scientists and the commercial growers. Each produced its own publication for many years before they were merged in 1994, with the Protea News of IPWG now being published as part of the Journal of the International Protea Association. Four volumes of Acta Horticulturae (185, 254, 316, 387, and 453) present some of the most readily available information on proteas, but the newsletters and journals of the two organizations are largely unavailable outside the membership base. This review includes a generous sampling of information shared in these resources. The principal protea production areas initially were South Africa, California and Hawaii in the USA, Australia, and New Zealand. Israel's floriculture industry joined them in the mid-1970s following a visit and talks by California's leading protea grower, Howard Asper. Since then, interest in the production of proteas has spread to many other countries, and nascent production for export is underway in Spain (Canary Islands), Zimbabwe, France, Mexico, San Salvador, and Chile. Worldwide, there may be about 900 protea growers. Verifiable figures of the numbers of growers of Leucospermum are not possible to obtain, and even the figures on numbers of growers of Proteaceae are, at best, estimates. South Africa counts over 300 producers affiliated with SAPPEX, while Australia has over 150 affiliated with the Australian Flora and Protea Growers Association. The sources for both figures estimate that perhaps twice as many smaller growers are not affiliated. Elsewhere, estimates are 40 growers for New Zealand, 30 for Hawaii, 90 for California, and 55 for Israel. In 1983, at the founding of the IPA, it was estimated that a little over 800 ha were planted to cultivated proteas, while in the early 1990s, the area was 5 times greater (Parvin 1991b). South Africa registered the greatest increase in cultivated area as a result of pressures to reduce harvesting from the wild. A recent report (Malan 1997) estimated that 173,000 Leucospermum species and hybrid plants were established on 66 ha in intensive cultivation as of 1996 and a harvest of 1.3 million stems was projected for 1997-98. In 1992, Zimbabwe was estimated to

32

R. CRILEY

have about 240 ha of protea plantings (Harre 1992). Australia's native plant industry began to expand in the 1980s, reaching about 63 ha of cultivated Leucospermum in 1993 out of more than 945 ha devoted to native and introduced proteas (Turnbull 1997). Israel had about 20 ha of proteas (1.5 ha in Leucospermum) in 1992 (Meltzer 1992), with only 85,000 Leucospermum stems sold at auction in 1995-96 (J. Ben-Jaacov, personal communication). The cultivated area for all proteas in Hawaii in 1996 was 66 ha (Hawaii Agr. Stat. Servo 1997) and in California 192 ha (Karen Robb, personal communication). Figures for the economic value of Leucospermum are hidden in the overall category of proteas, although figures from the Dutch auctions showed a per stem price for imported Leucospermums ranging from 0.75 to 0.70 (US$) in 1994-95. The per stem price for L. patersonii at auction in Israel was 76 cents in 1995-96 and 103 cents in the first three-quarters of the 1996-97 season (J. Ben-Jaacov, personal communication). In the USA, proteas are combined into the category of "other cut flowers" except for Hawaii, where the return to protea growers was $1.2 million in 1996 and in San Diego County of California where farm gate value (1996) was $3.57 million (Karen Robb, personal communication). A mid-90s figure for the farm gate value of Leucospermum in Australia was about one million dollars from 20 ha (David Matthews, personal communication). A figure of $12 million was estimated for the worldwide value of cut proteas in the late 1980s, and this may represent less than 1/2% of the world's annual expenditure for flowers (Parvin 1991b). The proportion of this figure that Leucospermum represents is undetermined, although reports suggest it is about 10% (Forsyth 1992). II. BOTANY A. Origin and Ecology Before Australia, Antarctica, South America, and Africa drifted apart, they shared a zoological and botanical ancestry. Africa parted from the ancestral landmass about 120 million years ago, whereas South America and Australia separated about 70 million years ago. Sir Joseph Hooker (cited in Venkata Rao 1971) observed in 1860, that the many bonds of affinity between the three southern floras, the Antarctic, Australian and African, indicate they have been members of one great vegetation which may once have covered as large a southern area as Europe now does the northern. The geographical changes that have resulted in its dismemberment into isolated groups scattered over a southern ocean must have been great indeed.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

33

The Proteaceae presently occur across the three temperate southern hemisphere continents (Australia, Africa, South America) that formerly were connected as Gondwanaland (Gondwana). The success of the dispersed members of the family has been attributed to inherent genetic plasticity (Dixon 1987). The concentration of Proteaceae in Australia (45 genera, 800+ species) argues for their origin there but endemism also exists in the African Proteaceae (16 genera, Rourke 1997), and no genera are common between the continents. South Africa presents great diversification in the subfamily Proteoideae (Vogts 1982). Proteaceous fossils dating from the early Tertiary period have been found in Victoria (Australia) as well as in Antarctica. The South American genera are evolutionarily closer to the eastern Australia taxa. Venkata Rao (1971) suggested that Proteaceae evolved in the mountainous rainforest conditions of eastern Australia in the Cretaceous period before spreading out into the lowlands and adapting to more xerophytic conditions. Western Australia and Africa are, in his view, secondary centers of diversification. The Proteaceae are largely distributed on soils of low nutrient content, often with acidic pH values. B. Morphology

Leucospermum species are evergreen woody perennials with growth habits that range from small trees to spreading shrubs to prostrate ground covers. Some species produce a thickened lignotuber at ground level which contribute to vegetative regeneration of the plant following fires. The root systems are profusely branched with clusters of rootlets of limited growth appearing on the main roots. These are known as proteoid roots (Purnell 1960; Lamont 1986). Venkata Rao (1971) and Lamont (1986) state that proteoid roots are not mycorrhizal but may require a biological stimulus for their development. The leaves are simple, smooth to hairy, with entire to toothed margins. The inflorescences are manyflowered and resemble compositaceous clusters with short, thick receptacles subtended by involucral bracts. The flowers are simple with three basic whorls, the perianth, androecium, and gynoecium. The flowers are 4-merous, hermaphroditic, and perigynous (Venkata Rao 1971). Although the flowers are structurally regular, three posterior tepals are fused and the anterior one remains free so that the perianth is bilabiate. The style emerges through this discontinuity, and the tepals reflex to show reds, oranges, and yellows. Stamens are adnate to the tepals with the anther fused to the tepal midrib. Pollen grains are triporate and are shed before the stigma is receptive. The pistil has a long, curved style with a lateral stigma subtended by a pollen collecting apparatus.

34

R. CRILEY

Rourke (1972) and Jacobs (1985) describe the inflorescence as a capitulum that develops from an axillary rather than a terminal bud, but that appears to arise distally. Inflorescences may be solitary, as in 1. cordifolium, 1. lineare, and L. vestitum, or in clusters (conflorescences), as in L. oJeifoJium, L. tottum, and 1. mundii. The individual florets consist of a perianth formed by four fused perianth segments, one of which separates from the other three as the flower opens. The perianth curls back to display a prominent style; the striking appearance of the whole inflorescence of open flowers resembles a pincushion-thus one of the common names is pincushion protea. The styles, perianth, and involucral bracts may be white, yellow, pink, orange, or red and the combinations are responsible for the popularity of the pincushion proteas as cut flowers. The fruit of the Leucospermum is an indehiscent achene with a gelatinous pericarp (functionally, an elaiosome) and a tough seed coat consisting of several layers of sclerified cells. A reinterpretation of the pericarp-testa interface suggests that a crystalliferous layer found at this boundary is part of the testa outer integument rather than the pericarp (Manning and Brits, 1993). The embryology of Proteaceae has received considerable study by Venkata Rao (1971). The ovule is solitary and orthotropous and develops into a large (c. 8 mm), rounded seed, nonendospermic with mainly oily and proteinaceous food rt3serve. The species name, Leucospermum, which means "white seed," refers to the elaiosomes, which dry out to become pale and papery in herbarium specimens, but which are fatty, juicy coverings attractive to native ant species that drag the seed to shallow underground nests in the fynbos habitat. This may enable dispersal and germination (Brits 1987). C. Taxonomy The Proteaceae consists of more than 1700 species in 82 genera, all of which occur in the southern hemisphere. The genus Leucospermum consists of 48 species (Table 2.2, Plate 2) confined to southern Africa (Rourke 1972). Only a few species have been utilized as cut flowers (1. cordifolium, L. patersonii, L. lineare, L. conocarpodendron, L. vestitum), but natural and manmade interspecific hybrids exist as clonal selections that are grown commercially (Jacobs 1985). Other species are being examined for their potential to contribute disease resistance, foliage traits, and extended flowering seasons. Chromatographic analyses of 267 species and subspecies of all genera in the Proteaceae have contributed to an understanding of the evolutionary relationships within this family (Perold 1984, 1987). The phenolic compounds, leucodrin and its hydroxylated analogue, leudrin,

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

35

Table 2.2. Leucospermum species and derivation of the species name (Rourke 1972, SAPPEX 1990, Rebelo 1995). Species

Authority

arenarium bolusii calligerum catherinae

Rycroft Gandoger (Gandoger) Gandoger & Schinz Compton

conocarpodendron cordatum cordifolium cuneiforme erubescens formosum fulgens gerrardii glabrum gracile grandiflorum guenzii hamatum harpagonatum heterophyllum hypophyllocarpodendron innovans lineare muirii mundii oleifolium parile

(L.) Buek Phillips (Salisb. Ex Knight) Fourcade (Burm. F.) Rourke Rourke (Andr.) Sweet Rourke Stapf Phillips (Salisb. Ex knight) Rourke (Salisdb.) R. Br. Meisn. Rourke Rourke (Thunb.) Rourke (L.) Druce Rourke R. Br. Phillips Meisn (Berg.) R. Br. (Salisb. Ex Knight) Sweet

patersonii pedunculatum pluridens praecox praemorsum profugum prostratum reflexum rodolentum royenifolium saxatile saxosum secundifolium spathulatum tomentosum

Phillips Klotzsch in Krauss Rourke Rourke (Meisn.) Phillips Rourke (Thunb.) Stapf Buek ex Meisn. (Salisb. Ex Knight) Stapf (Salisb. Ex Knight) Rourke (Salisb. Ex Knight) Rourke S. Moore Rourke R. Br. (Thunb.) R. Br.

Derivation of name Of sandy places After H. Bolus Bearing beauty After Mrs. Catherine van der Byl and its catherine wheel appearance Cone-fruit-tree Heart-shaped Heart-shaped leaf Wedge-shaped Reddening Beautiful Shiny After W. T. Gerrard Hairless Slender Large/noble flower After W. Guenzius Crooked Sickle-shaped Various-leaved Under-Ieaf-fruit-tree Novelty Linear After J. Muir After J. L. L. Mund Olive-leaf Equal (similar to other species) After H. W. Paterson? Having a stalk Many-teeth Flowering early With end bitten off Fleeing outwards Lying on the ground Bent backwards Smelling like a rose Wild-coffee (Royena)-leaf Of the rocks Occurring among rocks Unidirectional leaves Spoon-shaped Woolly (continues)

R. CRILEY

36

Table 2.2.

(Continued)

Species

Authority

tottum

(1.) R. Br.

truncatum truncatuJum utricuJosum vestitum winterii wittebergense

(Buek ex Mesin.) Rourke (Salisb. Ex Knight) Rourke Rourke (Lam.) Rourke Rourke Compton

Derivation of name Native to the Cape (Hottentot) Cut off at tip Small, cut off at tip Having a bladder Clothed After J. Winter of the Wittenberg mountains

A number of synonyms and botanical varieties have been collected under the above species by Rourke (1972).

and the diastereoisomer conocarpin and its ring-opened methyl ester, reflexin, have been used to distinguish between Leucadendron and Leucospermum. Perold (1988) further demonstrated that the presence or absence of these phenolic compounds could be used in the characterization of Leucospermum hybrids. Both leucodrin and conocarpin are absent in 1. cordifolium, 1. lineare, and 1. tottum, while leucodrin occurs in 1. patersonii and its hybrids and conocarpin occurs in 1. glabrum and its hybrids. D. Floral Physiology

Leucospermum was summarized in The Handbook of Flowering III (Jacobs 1985). He proposed that Leucospermum was a day-neutral plant in which flower initiation was evoked in response to high light intensity in conjunction with intraplant factors such as cessation of shoot growth and release of axillary buds from correlation inhibition. Jacobs et al. (1986) later separated flower growth and development into four stages: pre-floret (inflorescence bud initiation phase), floret initiation (floret primordium initiation phase), floret differentiation, and inflorescence enlargement. Plants grow vegetatively in spring and summer, with floret initiation commencing after shoot extension growth has ceased in fall. The pre-floret phase is characterized by slow growth and the development of bracts without florets in their axils. These bracts make up the involucre that covers the peduncle. In later-formed bracts, florets develop (the timeframe being mid-to-Iate fall), until ce.ssation of floret initiation during the shortest days of winter (see also Criley et al. 1990). 1. Flowering. Knowledge on flower initiation and development in

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

37

Inflorescences develop slowly through the winter months, then more rapidly as the days become longer and light intensity increases. Depending upon cultivar, flowering occurs in late winter through early spring or even into summer. For a period after cessation of shoot extension, pinching can induce vegetative growth from the upper axillary buds, indicating, according to Jacobs (1980, 1983), that the plants have not yet entered an induced state. By late fall, an induced state is achieved in a distal axillary bud, and other axillary buds are inhibited. Induction is relatively strong for the more distal buds and decreases basipetally. The developing inflorescence correlatively inhibits axillary buds below it (Jacobs 1980, 1983; Malan et a1. 1994a,b). Any of the top 6 to 10 lateral buds on a decapitated plant are capable of developing as an inflorescence. The 6 to 10 buds below the developing inflorescence develop to about 5 mm in diameter as secondary inflorescence buds composed primarily of bract-like leaves and perianth initials, but they do not develop further unless the primary inflorescence is removed. Removal of the primary inflorescence bud during inductive short days leads to inflorescence initiation in 1 or 2 lateral buds, with a weaker effect the later in the season (Malan 1986). The developmental period of the secondary inflorescence buds becomes shorter the later in the spring that the primary inflorescence is removed due to more rapid accumulation of heat units in the ensuing spring and summer (Jacobs and Honeyborne 1979), however, the ability of a secondary bud to develop a flower declines the later the removal of the primary inflorescence (Jacobs and Honeyborne 1978; Malan et a1. 1994b). The induced state is maintained for about 2 months (in the Cape Province of South Africa) and the plant gradually returns to the noninduced vegetative state by early spring. Secondary inflorescence buds will abscise when the plant returns to a vegetative growth phase. Buds below the secondary inflorescence buds do not develop and remain correlatively inhibited, but they will grow out vegetatively if the shoot is cut back. A key concept is that the buds entering the bract initiation phase must achieve a certain size (characterized as 20 mg DW) or they do not continue to develop (Malan 1986). Jacobs' (1985) concept that inflorescence initiation was not a response to photoperiod, as it does not occur during the long days (LD) of summer and the induced state is lost during short days (SD) of winter, changed as evidence mounted for a new interpetation. Jacobs' laboratory studied a number of factors, including timing of inflorescence initiation; influence of growth regulators, shading, and photoperiod; effects of defoliation, decapitation, and other manipulations of the shoots to determine how they influenced flowering.

38

R. CRILEY

Jacobs et a1. (1986) reported that long days delayed onset of the induced state and that flower initiation in Leucospermum required high light intensities during vegetative growth followed by SD. The induced state is lost more rapidly under shade than full sunlight or when the plant is sprayed with GA or ethephon (Napier 1985). Napier's studies showed that a decrease in leaf starch was associated with the diminished capacity to form flowers. Later work (Malan and Jacobs 1987, 1990) demonstrated that LD (3.7 /-lmol . S-l . m- 2 provided from incandescent lamps throughout the night period) could prevent flower initiation on upper axillary buds on shoots decapitated at various times from summer through winter, while similarly handled shoots under natural daylengths initiated and developed inflorescences. Night break lighting (2 to 6 hr depending on length of dark period) was also effective in preventing flowering (Malan and Jacobs 1990). Since the transition from vegetative to induced state occurred at the same time every year, Malan and Jacobs (1987, 1990) suggested that photoperiod might playa key role in the induction of Leucospermum. The low level of light energy needed to prevent initiation also argued for the participation of photoperiod in the process. Jacobs and Minnaar's (1980) observations of simultaneous reproductive development also supported the idea of a photoperiod switch. Malan and Jacobs (1990) stated that 'Red Sunset' was a qualitative SD plant that required at least 42 SD inductive cycles (>12 hr dark) for normal flowering. Such conditions prevail at Stellenbosch, South Africa (33 0 , 54'S) from April to September. Inflorescence development can occur between May and September; however bud responsiveness is weaker after June. Leaf removal and shading prevented flower initiation in the interspecific hybrid 'Red Sunset' (1. cordifolium xL. lineare) (Jacobs 1980). Heavy shading applied during summer reduced the number of stems forming an inflorescence (Jacobs 1983), but long stems were less responsive to the inhibition of flowering at low light intensities. The question may be posed, "Must a shoot reach a certain size or achieve a threshold leaf area, or simply cease elongation to begin to accumulate carbohydrates in order to be receptive to an inductive short day?" The appearance of an inflorescence on short stems of recent origin following a late pinch argues against shoot age or a threshold leaf area as necessary for induction (Jacobs 1980, 1983). Jacobs and Minnaar (1980) reported that production of bracts with florets in their axils commenced simultaneously on all shoots regardless of variations in the time of shoot growth cessation. Cessation of shoot growth on old plants occurred in mid-summer, while shoot growth extended into fall on

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

39

young plants (Jacobs 1985). Jacobs (1985) noted that early cessation of shoot growth could also be induced by water stress for plants growing under dry land conditions. Malan and Jacobs (1987) stated that buds that had developed a number of bract-like leaves would develop as vegetative shoots if the plants were stimulated into shoot extension growth by rainfall after growth cessation and concluded that shoot growth cessation is not a reliable indicator that the plants had reached an induced state for reproductive development. Cessation of shoot elongation certainly seems implicated, but the question of whether it is a necessary condition is not clear. The correlative inhibition of primary inflorescence bud upon secondary inflorescence buds was thought due to its IAA production and export (Malan et a1. 1994a). Diffusable plant growth substances from primary inflorescence buds were collected in agar receiver blocks and analyzed by radioimmunoassay and by HPLC. IAA content and its export from the primary inflorescence bud did not differ significantly from that of inhibited buds nearby, but the developmental patterns favored the primary inflorescence. Since all buds exported IAA, they concluded that it was not the IAA concentration of a single organ or its inherent ability to export IAA that is responsible for inhibition, but the total amount of IAA moving down the shoot that determined the extent of inhibition. During floret initiation and differentiation, auxin production and export were low, but at the end ofthe floret initiation stage, IAA and ABA peaked, while GA was present until floret initiation was complete, and cytokinins were high in the pre-floret stage and first half of the initiation stage, but declined during later stages of development (Malan et a1. 1994b,c). GA export peaked just before lateral axillary buds lost their responsiveness to inductive short days. Since exogenous application of GA also reduced the responsiveness of axillary buds to short days (Napier and Jacobs 1989), Malan et a1. (1994b) proposed that GA export from the primary inflorescence bud was responsible for the correlative inhibition of the axillary buds. The GAs could be either GA 1 or GA 3 or both, as both were detected by the antiserum and had similar polarities and HPLC retention times. Malan et a1. (1994c) determined that benzyladenine (BA) applied to decapitated shoots prior to floret development in the secondary inflorescence buds increased the dry mass of the inflorescence and number of florets per inflorescence. The results were similar to those of Napier et a1. (1986a). Extra bracts were initiated on the peduncle, but precocious floret development (in these bracts) did not occur and the loss of responsiveness to short days in winter time was not affected by the cytokinin

40

R. CRILEY

compared to untreated buds. Malan et al. (1994c) concluded that BA did not interact with the gibberellins that were apparently inhibiting lateral bud responsiveness to short days. To sum up the role of growth regulating substances in floral development, it appears that auxin does not playa major role in inhibiting bud responsiveness to short days. Gibberellins from more distal buds, especially the primary inflorescence bud, may play the role of correlative inhibitors of lower buds on the shoot. The more developed the inflorescence bud, the more strongly the lateral buds are inhibited in responding to inductive SD, presumably because of high GA levels (Malan et al. 1994b). Cytokinins are involved in quantitative roles such as increasing the meristem diameter, number of bracts and florets, and number of inflorescences per stem. In L. patersonii, LD were required for floret induction, but SD accelerated floret initiation (Wallerstein 1989; Wallerstein and Nissim 1988). The LD effect quantitatively influenced the number of axillary buds that initiated inflorescences. The most distal axillary buds were the most sensitive. Stem thickening was concurrent with the cessation of stem elongation under SD, but if the axillary meristems failed to develop into inflorescence buds, stem thickening ceased. 2. Pollination Biology. Species of Proteaceae are frequently pollinated by various honey-seeking birds, bats, and small animals. The flowers are grouped in capitula consisting of 30-300 florets. The florets shed pollen over a period of 7 to 14 days, generally before the pistil of the same flower is receptive (protandry). Fresh pollen remains viable for up to six days when stored at room temperature and up to six weeks when stored at 5°C (Brits and van den Berg 1991). The small stigmatic groove (30-300 /-lm long) opens within 24 hours and attains maximum receptivity two to five days after anthesis, as shown in Fig. 2.1 (Brits and van den Berg 1991). Pollen viability can be tested by germinating in 12% sucrose plus 100 mg boron/L (Fig. 2.2) (Brits 1992a). Shchori et al. (1992) reported that better germination was achieved using Taylor's medium in a hanging drop. Ito et al. (1978, 1990) have described their pollination technique. Since pollen is shed before the stigma is receptive, emerging styles (hooked stage) are gently released from the perianth, and the stigmas are examined for the presence of pollen. The anthers are removed from flowers that do not show pollen on the stigma. Pollen from fully open flowers of selected male parents is applied to the slotted tip of the stigmatic area two days after emasculation and again two days later. The

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

~

80

.~

~

Cl:l

E

.S?

en

e;e.

Stigmatic grooves

-+-

100

7

\

60

\

"

\

40

\

\

\

x

I

I

I

I

41

I

7

·X·· Seed set

Go) (,,)

c

Go)

x

(,,)

Co?

\\

Go)

]

5 \

\

.5

en

\.

x

"'C

3

Go) Go)

Co?

en «>

20 0 7

8

Fig. 2.1. Average percentage of stigmatic grooves open and number of seed set following artificial pollination on successive days after anthesis in Leucospermum cordifoJium. Source: Brits and van den Berg 1991.

50

700

40 c

.S:? C;; c

/

30

'§

t/

20

/

10

ri

Germination·8 600 Germination + B Tube length ·8 500 E -s- Tube length + B .3-

,,""*,

-+-

\

/

Go)

C7)

'CJi'!.

"\ ~

-,

5

10

15

20

25

.s

C7)

c

.s: Go)

300

"" 30

.Q

:::l

I-

200

.* .... *.. ...*.... * ......*..........*

a 0

400

0

100 0 35

Sucrose concentration (%1 Fig. 2.2. Effect of sucrose and boron (100 mg H3B0 3 /L) on pollen germination percentage and pollen tube growth in L. cordifoJium. Source: Brits 1992a.

42

R. CRILEY

emasculated and pollinated flower is covered to prevent contamination and labelled to identify the cross. E. Genetics Chromosome numbers are constant within the genus at 2n = 24, x = 12 (Rourke 1972; Van der Merwe 1985). A wide range of interspecific hybrids have been collected and introduced to cultivation (Brits and van den Berg 1991). In addition, directed crosses are being made among species in efforts to produce later flowering, improve color and shape, and introduce tolerance to Phytophthora cinnamomi (Brits 1992a). Brits (1992a) noted that self-incompatibility is present to a moderate degree in Leucospermum and that interspecific crosses are often highly heterotic. Cross pollination is apparently favored; as only 3 to 4% of selfed flowers set seed as compared to 6 to 8% for cross-pollination (Brits 1992a). Horn (1962) reported even lower percentages of seed set among open pollinated flower heads. Thus, a strong degree of self-incompatibility and interspecies incompatibilities were proposed (Brits and van den Berg 1991). Resources allocation, insufficient pollinators, and predation are possible alternative explanations for low seed yields. III. HORTICULTURE The most widely grown Leucospermum species are floriferous, spreading shrubs on which relatively short-stemmed inflorescences are borne in the spring. Horticulturists have had to develop management practices to improve stem length and straightness for their use as cut flowers. Their potential as flowering potted plants was recognized when budded cuttings flowered after rooting; stock plants are being manipulated to achieve stronger branches for this use. A. Propagation 1. Seed. Poor seed (or more properly, achene) germination in Leu-

cospermum has posed problems for both horticulturists and plant breeders. Much of the early research to overcome this problem has been conducted in the laboratories of Johannes van Staden of the Department of Botany, University of Nata!. In preliminary studies (Brown and Van Staden 1973; Van Staden and Brown 1973), removal of the pericarp and seed coat increased germination, as did increasing the oxygen concentration around intact seed. The outer layer of the achene (the peri-

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

43

carp proper) becomes gelatinous upon imbibition and is presumed to interfere with gaseous exchange. Based on a report (Van Staden and Brown 1977) that oxygen promoted embryo cytokinin levels, Brits and Van Niekerk (1976) used hydrogen peroxide to improve germination. However, the effect was applicable only to proteaceous species with nut-like achenes, as 13 out of 15 serotinous species did not respond to the hydrogen peroxide treatment (Brits 1986b). Brits (l986c) noted that achenes harvested slightly prematurely germinated better than naturally matured achenes and suggested that dormancy was due to restricted oxygen uptake attained during the final stages of seed maturation, and that dormancy probably resides in the outer layer(s) of the seed coat. The hydrogen peroxide treatment was not always successful, which led Brown et al. (1986) to examine a range of other treatments successful on seed of other plants. Following imbibition, the pericarp was removed, and the seeds were incubated under alternating temperatures of looe for 8 hand 20 0 e for 16 h with light (11 W1m) provided during the high temperature period from cool white fluorescent lamps. Emergence of the radicle was used as the criterion of germination. Germination was on moist filter papers to which various growth regulators were added. Some growth regulators were supplied as soaks prior to placing the achenes on moist filter paper. Germination improved from 11 % for controls to 44-50% with GA 3 concentrations of 25 to 500 mg/L. With the commercial product, Promalin (mixture of GA 4 , GA 7 , and benzyladenine), a 24 h soak improved germination from 10% for the control to 26 to 46% for Promalin concentrations of 50 to 400 mg/L. Achenes germinated on filter paper to which a range of ethephon concentrations had been added also slightly improved germination over that of the control, while incubating achenes in an atmosphere of ethylene gas similarly improved germination. In the same series of experiments, hydrogen peroxide (10% v/v) soaks improved germination to 24%, compared to 12% for controls. They concluded that the gibberellins are the most active group of hormones in stimulating germination of Leucospermum achenes and suggested that GA in combination with other treatments needed investigation. Brits (1986a,c) placed a fluctuating diurnal temperature requirement for germination in an ecological context. An optimum high of 24°e and low of 9°e as determined from controlled experiments promoted germination. In burnt mesic conditions of their natural habitat, Leucospermum seeds germinated during the winter when water was most likely to be available, rather than in the warm, dry summer. The daily surface temperatures of this sun-warmed soil in winter paralleled those of the

44

R. CRILEY

controlled experiment, while temperature conditions of unburnt, or lightly or heavily shaded, soils did not meet the temperature requirements for germination. Brits concluded that Leucospermum was closely adapted to its environment with regard to germination temperature requirements. He also recorded temperatures at depths of 30 to 45 mm, where seeds buried by ants were found. Daily temperature fluctuations during early winter were of the same order as the known temperature requirements of L. cordifolium seeds. The ecological approach to germination was also evident in a more recent report that desiccation, such as that due to fire, breaks the exotesta, and the endotesta as well when wetted, to permit oxygen diffusion and hydration of the embryo (Brits et a1. 1993). Brits et a1. (1997) propose that Leucospermum has at least one adaptive strategy for each stress or disturbance factor operating in nature: ant dispersal, desiccationscarification by fire, alternating temperature requirement, and ecologically related temperature requirements. Phasic changes of gibberellins and cytokinins are also believed to control germination through an inductive threshold, mobilization of lipid and protein reserves, cotyledon expansion, and radicle growth (Brits et a1. 1995). Although complicated schema involving sulfuric acid scarification, Promalin (a gibberellin + benzyladenine preparation), pure oxygen, and alternating temperatures work to improve germination to 95% in the laboratory and are effective on a number of species (Brits 1990d), Brits (1991) proposed a simple treatment for commercial seedling production. Dry achenes are soaked in a 1% solution of hydrogen peroxide for 24 hours, the gelatinous pericarp is removed, and the achenes are sown in open seedbeds in autumn when daily temperatures vary from the optimum low at night to the optimum high by day. Satisfactory germination percentages (not reported, but presumed from other reports by the same author to be about 60%) were the result. This procedure was used successfully for L. cuneiforme and L. tottum by Rodriguez-Perez (1993). While most propagators agree on the importance of fresh seed for high germination percentages, commercial germination practices for proteaceous seed has been subject to many variations. Parvin (1974) recommended 3 parts of finely screened cinders to 1 part peatmoss as a germination medium with 21°C bottom heat, and "plenty of moisture" leaching through 15 cm of medium. Harre (1986) reported his best successes came from sowing seed in a 1 loam: 1 pumice mixture or 5 loam: 2 coarse sand: 3 pumice during the falling temperatures of autumn, treating with captan to reduce fungal attack, and awaiting germination. The hard-shelled seeds of Leucospermum are slow and erratic to germinate, taking 3 to 15 months. Harre soaked seed in 60°C hot water for 30 mins

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

45

prior to sowing, but did not clearly state whether this practice improved germination. Perry (1987) suggested a hot water soak to minimize seedborne diseases followed by dusting with a fungicidal powder. Once seedlings have reached the first true leaf stage, they are hardened off for potting. Harre also advocated "wrenching," a technique whereby the seedlings are disturbed a week before transplanting to induce lateral root formation. The diversity of successful practices does not lend itself to a single recommendation. Brits' hydrogen peroxide treatment has broad applicability while Harre's practical nurseryman's approach (Harre 1988b) suffices for media, containers, transplanting, and environmental considerations. While uneven germinatioh may be the reason that growers prefer to transplant rather than direct seed to tubes or pots, improvements in seed quality should speed the use of direct seeding in containers suitable for transplanting. 2. Cuttage. Leucospermum cutting propagation offers few challenges because most plant material roots readily. Brits (1986d) compared terminal and sub-terminal cuttings and found that recently matured terminals taken in autumn rooted best. Harre (1988a) rooted leaf (or possibly a leaf-bud) cuttings of many protea species, but noted that they did not produce plants. His observations suggest, however, that leafbud cuttings might be examined as a means of rapid increase for new cultivars. However, in other trials, rooting and shoot elongation of leaf-bud cuttings were poor, and up to 32 weeks was required for transplantable cuttings (Rodriguez-Perez 1992). While Leucospermum cuttings can be rooted at almost any physiological stage of development, a preferred cutting is the recently matured new growth, known as a semi-hardwood cutting (Malan 1992). This type of material is gathered in autumn after shoot growth terminates. Harre (1988a) recommended removing the tip about a week before taking the cutting because rooting was improved, and vegetative growth resumed readily following rooting. Manipulation of cuttings on the stock plants before harvest as well as after the collection of cuttings was suggested as a means to improve rooting (Harre 1989). Cuttings (type and maturity not specified) of 1. cordifolium 'Riverlea' were harvested fully turgid in early morning and held under mist for varying periods before being treated with 2000 ppm IBA and placed under automatic mist (cycle not given). Delays of 3 and 5 days before sticking the cuttings yielded rooting in excess of 90 % , while a delay of 7 days reduced rooting to 77%. The cuttings were deemed well enough rooted that hardening could begin after 44 days and potting up after 50 days.

46

R. CRILEY

Another aspect to manipulating the future cutting was developed for the production of potted Leucospermum plants (Brits et al. 1992). Wellbranched cuttings induced by spraying a primary elongating shoot with 960 mg/L ethephon rooted easily in 6 to 8 weeks. Yoshimoto (1982) proposed that air-layering of branched cuttings was another technique that could be used to produce larger plants for pots or for field planting. As a result of practical experiments, Harre suggested that rooting under 35-50% shade is superior to lower light intensities; that a wellaerated medium leads to superior root quality (his examples included better rooting in cracked tubes and tubes with holes and when cuttings were placed down the side of a tube); and that initial propagation under automated intermittent mist, then shifting onto capillary watering beds as roots initiate, provided excellent results (Harre 1988a, 1989). Cuttings from well-nurtured stock plants 2 to 5 years old are his preferred propagules. He also recommends pinching and cutting back the stock plants to yield more cuttings of a uniform diameter and quality.

Rooting Compounds. While Leucospermum cuttings often root without the aid of auxins, most nurseries use auxin treatment to enhance rooting. Rousseau's early report (1968) suggested IBA solutions of 0.2 to 0.4% were adequate and mixtures of IBA/NAA in the same range gave about the same results. McKenzie (1973) used a quick dip in 0.3% IBA, noting the results were better than with Seradix No.2 powder. A range of 0.2-0.3% IBA was recommended by Parvin (1974), while Parvin (1982) later reported improved rooting of two South African Leucospermum hybrids over untreated controls when liquid IBA-NAA (2:1) formulations were used, and total auxin concentrations were in the range of 1300 (1:10 dilution) to 2500 (1:5 dilution) parts per million. A talc dust of 0.80/0 IBA (as Hormex #8) yielded somewhat lower rooting percentages than did the liquid formulations, while Yoshimoto (1982) recommended 0.65% IBA in talc powder. Jacobs and Steenkamp (1976) reported on the results of a series of IBA treatments (from 0 to 8000 ppm) and recommended 4000 ppm as either a quick dip solution or talc dust for 1. cordifolium semi-hardwood cuttings. Asper (1984) routinely used 5000 ppm IBA as a dip treatment to induce rooting. Propagation Medium and Bottom Heat. Rousseau (1968) used a sandpeat mixture for rooting, while Yoshimoto (1982) found a 1 peat: 2 perlite medium produced the best results. Interestingly, Harre (1988a,b) avoids peatmoss in his post-rooting medium and instead includes scoria, sand, or pumice with soil. He suggests that proteoid roots, which develop in the peat-based medium, do not contribute to the establish-

Z. LEUCOSPERMUM: BOTANY AND HORTICULTURE

47

ment of liners when they are transplanted to the field. A lengthy exchange of opinions concerning the use of peat or bark suggested there was no good biological basis for avoiding peat, as many proteaceous plants were grown well in media containing peat (Blake 1987). For example, McKenzie (1973) used a 1 peat:1 sand medium for propagation and 2 soil:1 peat:1 sand as a potting mix. Jacobs and Steenkamp (1976) evaluated several rooting media for 1. cordifolium and recommended a 2:1 or 1:1 mixture of peat and polystyrene grains over mixtures of 2:1, 1:1, or 1:2 peat and sand, because the former clung to the new roots better than did the heavier sand-based medium. Brits (1986d) reported that bottom heat (23 ± a.BOC) greatly improved rooting over no bottom heat (12 ± 2°C) under mist, and that the use of IBA-based rooting compounds improved rooting at the cooler temperature but not at the warmer. Cultivar differences were important, with 75% rooting for 'Caroline' and only 30% for 'Hybrid T 75 11 24.' Subterminal cuttings did not root as well as terminal cuttings of the same cultivar given bottom heat, but were nearly equal to or outperformed terminal cuttings without bottom heat. Brits also observed that misting at long intervals, and allowing the leaves to dry off between on cycles did not influence cutting mortality, perhaps because the xerophytic character of Leucospermum may impart some tolerance to drier rooting conditions. These results suggest the potential to develop simpler, cheaper, and healthier rooting technology than conventional frequent-misting systems (Brits 19B6d). 3. Grafting. Grafting is often viewed as a solution to problems of root system adaptation to low or high pH soils, salinity, or soil-borne diseases. Grafting on lime-tolerant rootstocks has been recommended as an approach to problems of protea production on soils of neutral to slightly basic pH (Brits 1984b). A lime-tolerant species such as L. patersonii was recommended. Moffat and Turnbull (1993) evaluated rootstocks resistant to Phytophthora cinnamomi, and although none were found in the genus Leucospermum, they found a variety of grafting techniques that worked well on either rooted cuttings or on cuttings to be rooted under mist (cutting grafts). The standard grafting technique is wedge-grafting of leafy semihardwood scions onto seedling rootstocks (Rousseau 1966; Vogts et a1. 1976), but the requirement of a mist system during wound healing increased costs and stimulated a look at other techniques. Approach grafts are also successful but more time-consuming to execute, and required more aftercare. During 1976 to 1980, G. J. Brits of the Vegetable and Ornamental Plant

48

R. CRILEY

Research Institute (Riversonderend, South Africa) conducted 40 grafting and budding experiments to determine rootstock production methods, grafting and budding techniques, potential understocks, and to evaluate the effectiveness of grafting (Brits 1990b, 1990c). Rooted cuttings of Leucosperm um were superior to seedling rootstocks because of necessary thickness requirements, uniformity, and clonal selection possibilities. The wedge graft, using a 2-bud scion with 0.5 cm 2 leaf blade subtending each bud, yielded 80 to 95% take on rooted cuttings, while chip budding onto unrooted cuttings yielded a 93 % success rate. Prior to planting out in the field, the scion should be allowed to produce at least 5-cmlong shoots in the nursery. As to time of year, Brits expressed a preference for early autumn, although he noted that grafts made in the spring had the benefit of producing growth during the same growing season. The use of cutting grafts, where the graft union develops while the cutting roots, is also recommended (Brits 1990b). Cutting grafts were evaluated using four Leucospermum cultivars (Ackerman et al. 1995). In the second year after planting established liners into the field, the grafted plants significantly out-yielded the same cultivars on their own roots. Ackerman and his colleagues concluded that there was significant advantage to using resistant rootstocks selected for their suitability to the local soil types. Brits (1995b) has reported that budding onto a cutting and rooting it was more economical than grafting. The choice of rootstock was important, because 'Vlam' roots with difficulty while hybrid rootstocks could be selected with 100% capacity to root (Brits 1990b). Brits (l990c) evaluated 19 Leucospermum species with rootstock potential and found great variability in capacities to root as cuttings, support vigorous scion growth when used as rootstocks, and produce a shoot of graftable diameter (Table 2.3). None of the species exhibited great tolerance to Phytophthora cinnamomi, although a hybrid of L. formosum x 1. tottum designated as 'T75 11 02,' and another of 1. conocarpodendron ssp. viridum xL. cuneiforme, designated 'T75 11 24,' performed well in one field experiment. Selection of rootstock plays a significant role in improving adaptability and yield of Leucospermum. Van der Merwe (1985, and references cited therein) produced a number of intergeneric grafts, and suggested close genetic relationships as a result of compatibilities he found. One important result was that Serruria may be grafted onto Leucospermum conocarpodendron and grown in sites where Serruria on its own roots would not survive. Malan (1990) compared an interspecific hybrid (1. tottum x L. formosum) and 'Sue Ellen' understocks for cuttings wedge-grafted with scions of 'Sue Ellen' (a hybrid of 1. cordifolium x 1. lineare). While graft union rates were only 12.2% and 23.8% for 'Sue

Table 2.3. General characteristics of 19 Leucospermum species with rootstock potential for species of the section Brevifilamentum Rourke, determined from horticultural data or deduced from ecological data (ex Rourke 1972). Real or expected compatibility is based on grafting results with 6 exceptional candidates and on taxonomic relationships, respectively. A = excellent; B = good; C = average/normal; D = unsatisfactory relative to 1. cordifolium. Rooting values (except those in parentheses) ex Jacobs 1982 (Brits 1990c).

Horticultural Data

Leucospermum sp.

.J:>

to

Graft compatibility

catherinae conocarpodendron ssp. conocarpodendron ssp. viridum (Durbanville) cordifolium cuneiforme erubescens formosum fulgens grandiflorum guenzii patersonii pluridens praecox praemorsum reflexum rodolentum saxosum truncatum utriculosum vestitum

Rooting ability

Ecological Tolerances

Vigor of rooted cuttings

Plant size/stern diameter

Longevity

pH 6.5-8.5

ReI. high salts

Drought

Cold

Wet soils

(B)

61

C

C

C

C

C

D

B

A

B B

(70)

71

D D

A A

A A

B B

B B

B C

C C

C C

100 50 (60) 56 78 66 (60) (100) 14 100 56 (66) 51 (60) 61 29 42

C C C B C

C C C B B B

C

C

C

B C

A

C C C B B

C B

B A A B A B

B

C

C

B

B A

C D D C C

C D D C C

C D C

B A B A C C A B A

B

B B B

B A B B A B

D C B D C

C C C C D C C 0

C

C C C

C C

C C

A

(C) (C) B (B) (B) (B) A B (B) (B)

C (C)

(C) (CI

(C) (A)

B

C A

C

B

C B

B

B B B B C

C B B B C

C

B

C C C

C B

C

D

B B

C C

C C B C C B

C C C C B

C C C

C C

50

R. CRILEY

Ellen' on itself and the hybrid, respectively, due to the inexperience of the laborers, rooting was faster for the hybrid understock cuttings and growth of the scion shoots was better than for the 'Sue Ellen' understock cuttings. Malan also noted that new growth of 'Sue Ellen' scions was less affected by Phytophthora cinnamomi root rot when grafted on the hybrid than on its own roots. Brits (1995b) reported that budding onto 'Spider' cuttings in the fall, followed by LD during winter, produced marketready plants six months later. Moffat and Turnbull (1994) recommended additional investigation of L. saxosum as a potential rootstock with low susceptibility to Phytophthora. Root rot resistant understocks have the potential to increase plantings of Leucospermum where Phytophthora root rot is a problem. 4. Tissue Culture. Leucospermum cordifolium callus culture without

organogenesis was reported by Van Staden and Bornman (1976). BenJaacov and Jacobs (1986) reported success in bud sprouting from semihardwood shoot segments of 'Red Sunset,' an interspecific hybrid of L. cordifolium xL. lineare,' on filter paper bridges immersed in liquid Anderson medium with 2 ppm BA. Kunisaki (1989,1990) achieved proliferation from axillary bud explants in half-strength MS inorganic salts, 2% sucrose and 0.2 mg BAper liter. Round, green proliferating bodies were induced to form shoots after transfer to filter paper bridges. After 4 to 6 leaves developed, the propagules with their shoots were transferred to agar medium, then, at 5 to 10 mm in height, they were separated from the propagules and grown on to greater length. Rooting was achieved by soaking the basal 2 to 4 mm stem in 50 or 100 mg IBA/L solutions for 4 days (later modified to a 10-min dip in 150 mg IBA/L). The microcuttings were rooted in an agar-based half-strength MS medium with activated charcoal and 2% sucrose. Kunisaki (1990) reported greater success with a modified composition of the agar rooting medium, but also noted that rooting could be achieved in sterile perlite. A "feeder leaf" technique was employed successfully by Rugge et a1. (1990), in which a leaf blade on an explant was inserted into the culture medium. Axillary bud sprouting above the feeder leaf was substantially improved over the bud subtended by the feeder leaf or buds proximal to the feeder leaf in this technique. Tal et a1. (1992a) showed that cytokinins and GA 3 had strong effects on multiplication, but that a medium containing BA was better than zeatin. GA 3 at 1 to 2 mg/L was essential for rapid proliferation and elongation of the shoots, providing nearly double the shoot increase of BA alone. GA 3 also enhanced shoot .length, an important consideration in handling shoots during subculturing. Light intensities of the level of 230

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

51

Ilmol . m- 2 . S-l enhanced in vivo rooting compared to lower intensities. The auxins, IAA, IBA, and NAA, all improved rooting over the use of no auxin, but the best rooting was with 1 mg IBA/L. Hardening off was successfully accomplished using plantlets with 3 to 5 nodes, fog (delivering 0.25 mm water/h), and high levels of light (14,000 lux). In conclusion, research results have laid the groundwork for commercial micropropagation of Leucospermum, but conventional systems of vegetative propagation are more widely used. B. Environmental Responses 1. Light. Jacobs and Minnaar (1980) determined that light intensity reductions of up to 50% did not slow the rate of flower development, but flower quality, as assessed by the number of styles per flower head, receptacle length and diameter, and inflorescence dry weight, decreased with decreasing light intensity. Jacobs (1983) proposed that there was a quantitative response to light intensity because heavy shading prevented flower initiation. Napier (1985) found that shading plants when they had been induced led to reduced carbohydrate in the leaves and a loss of the induced state. The reduced capacity of deheaded shoots to initiate an inflorescence during winter may be more related to low light energy relationships than to a short photoperiod (Jacobs 1980). Jacobs and Minnaar (1980) ruled out a major role for light intensity and stated that the main factors affecting rate of flower development in pincushion were temperature and shoot size. 2. Temperature. In the areas of South Africa where Leucospermum spp. are native, the mean annual temperatures are 13 to 16°C and the monthly mean is below 20°C (Ben-Jaacov 1986). Leucospermums are frostsensitive, and growers have observed plant loss in severe frosts. Diverse protea-growing areas such as Israel, western Australia, and California achieve greater extremes (Ben-Jaacov 1986). In the commercial production area of Hawaii, the range is from a monthly minimum daily mean of about 13°C during winter to a maximum daily mean of 25°C in late summer, but the daily mean seldom exceeds 20°C. The protea-producing area of the island of Madeira at 500 m above sea level has winter/summer ranges of 10-18/15-25°C (Blandy 1996). Prior to establishing that flowering was under photoperiodic control, Jacobs (1976) and Jacobs and Honeyborne (1979) proposed that the accumulation of heat units (from 4.4°C to the average daily temperature beginning 1 May onwards in South Africa) controlled the rate of floral development. Following removal of a primary inflorescence bud, about

52

R. CRILEY

925 heat units above a 5.8°C base temperature were required to mature 90% of secondary flower buds that began to develop. Fewer days were required in late spring than early spring as a response to greater heat unit sums per day, about 8.5 early on to about 20 by mid-summer. Jacobs (1976) also suggested that the exploitation of warm and cool growing regions could extend the production period from August into January. Criley et a1. (1990) reported a 120-day development period for inflorescences of 'Vlam' once floret initiation began in the fall, with about onefourth of the heat units accumulated in the last month of development. Heat unit accumulation (from a base of 6°C to the mean daily temperature from 1 September) was uneven, varying from 14 units/day in midfall to 10 in mid-winter under Hawaii conditions, with an average of 12.8 heat units per day over the period of development. The heat unit total was 1536 units from floret initiation until 50% bloom was achieved. They concluded that under short photoperiods with high light intensities, floral development could be rapid if temperatures were not limiting. Application of the light and temperature results may be difficult to achieve for field-grown pincushion plants, but possibilities exist for potted plants. One scenario would impose 12 hr SD during the high light period of the year on potted plants grown at 18-20°C. Flowering could be expected about 4 months after the development of a 1 em bud. 3. Cold Tolerance. In South Africa, most Leucospermum species are indigenous to frost-free areas of the Cape (Ackerman 1995) (Table 2.4). When grown outside their natural habitats, they experience both warmer and cooler temperatures. As a general statement, they will tolerate brief exposure to temperatures as low as -3°C. L. cordifolium is affected by severe frost, while species from higher elevations, such as L. tottum and L. vestitum, are more cold tolerant (Vogts 1980). L. lineare, from elevations of 300 to 1000 m, is another cold-tolerant species. Research on cold acclimation has not been reported, but growers have shared knowledge about plant survival during episodic cold periods through the newsletter of the IPA. 4. Soils. Most of the Leucospermums are indigenous to nutrient-poor, coarse, acidic, sandstone-derived soils. A few species are indigenous to soils derived from limestone and with a high pH. Vogts (1980) and Matthews and Carter (1993) have described the native locales of several important commercial species, including L. cordifolium, L. vestitum, and L. tottum. The weathered Table Mountain sandstone soils (pH 4.5 to 6.5) of the Caledon and Bredasdorp districts support populations of

Plate 1

Banksia serrata painted by Celia Rosser. Courtesy of Monash University.

Leucospermum cordifolium 'Vlam' Plate 2 Leucospermum species that have contributed to the commercial assortment of pincushion cut flowers or potted plants (L. oleifolum). Photos by P.E. Parvin and R. A. Criley. (Continues on next page)

Leucospermum tottum

Leucospermum conocarpodendron subsp. conocarpodendron

Leucospermum lineare Plate 2 Leucospermum species that have contributed to the commercial assortment of pincushion cut flowers or potted plants (L. oleifolum). Photos by P.E. Parvin and R. A. Criley. (Continues on next page)

Leucospermum vestitum

Leucospermum oleifolum

Leucospermum patersonii Plate 2 Leucospermum species that have contributed to the commercial assortment of pincushion cut flowers or potted plants (L. aleifolum). Photos by P.E. Parvin and R. A. Criley. (Continues on next page)

Leucospermum reflexum var. luteum

Leucospermum reflexum

Leucospermum glabrum Plate 2 Leucospermum species that have contributed to the commercial assortment of pincushion cut flowers or potted plants (L. oleifolumj. Photos by P.E. Parvin and R. A. Criley.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

53

Table 2.4. Origin and altitudinal distribution of some of the Leucospermum species grown in commercial cultivation (Rebelo 1995).

Leucospermum sp. conocarpodendron ssp. conocarpodendron cordifolium glabrum lineare patersonii reflexum tottum var. tottum vestitum

Habitat

Elevation (m)

Granite and sandstone soils

to 160

Sandstone soils Cool, southern slopes on peaty soils Granite-derived clays Restricted to limestone soils Near streams on sandstone soils Sandstone slopes Varied, on rocky sandstone slopes

30 to 500 150 to 500 300 to 1000 50 to 300 1000 to 2000 300 to 2000 60 to 1350

L. cordifolium, while L. vestitum is found on similarly acidic soils in

mountainous areas of the West Cape north to the Cedarsburg range. Weathered sandstone soils support 1. tottum in mountainous areas of the Cape. 1. lineare is found on gravelly clay soils derived from granite in mountains of the southern Cape. The Leucospermums seem adaptable to a variety of soil types within a narrow range of pH and fertility levels, as evidenced by their culture in Hawaii and the Canary Islands (volcanic soils), southern California and Israel, Australia, and several regions of southern Africa. Soilless culture has also been successful using either 10 cm slabs of rockwool or crushed volcanic rock (Cala 1986). C. Cultural Practices 1. Spacing. Planting densities are governed by two considerations: the ultimate size of the plant and the method of maintenance. One commercial grower recommended that Leucospermum be planted 3 m apart in rows (Matthews 1982). An Australian recommendation is 1. 7 m inrow and 3.5 m between rows (Matthews and Matthews 1994). A South African grower reported a spacing of 1.75 x 0.75 m (7580 plants/hal. but planting distances would change with changes in pruning method (Steenkamp 1993). As good drainage is required, hardpan should be broken up and the soil rototilled. If posts and wire supports are used, the height ofthe lowest wire will depend on the size of bush being planted, but may be as low as 15 cm from the ground. Additional wires are installed later. The main leaders of the plants are fastened to the wire by clips of the type used in the culture of various vining fruits.

R. CRILEY

54

2. Pruning. Management of proteas began with minimal attention to the

plant structure. However, as with many other woody plants, pruning was found beneficial because heading back increased lateral shoot production and controlled plant height and shape for ease of harvest and to facilitate spraying. Brits et al. (1986) pointed out that a balance between thinning and heading'back is necessary to stimulate vegetative growth while minimizing production of nonmarketable short flowering branches. Brits et al. (1986) distinguished between proteas with a lignotuber and ordinary non-lignotuberous species. Some Leucospermum species (L. saxosum, 1. cuneiforme) are lignotuberous, which means they produce an enlarged base consisting of thickened wood and bark on which numerous axillary and adventitious buds are visible. The lignotuber provides a source of new shoots when veld fires damage the higher parts of the plant. Both fire and pruning down to the lignotuber serve to rejuvenate the plant. In contrast, older shoots of the non-lignotuberous species tend to die back to the base, and pruning is used to remove old, nonproductive shoots or to stimulate lateral breaks on young (1- or 2year-old) wood. Leucospermum is pruned differently from Protea (Brits et al. 1986;' Matthews and Matthews 1994) (Fig. 2.3). Strong flowering branches of the current season are headed back to 7-15 cm during or soon after flower harvest to produce bearing branches for the ensuing season. The

~\

\ '- \ A \

,

\

\

Fig. 2.3. Schematic representation of four types of shoots borne on productive Leucospermum plants and suitable pruning sites. A: strong flowering branch. the base of which is left when the flower is cut; B: weak flowering branch of marketable length; C: Weak, non-marketable flowering branch-both Band C are cut flush with the parent branch (thinning cuts); D: thin, vegetative shoot that is left to develop in another growing season. b = flower; M = parent branch. Source: Brits et al. 1986.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

55

early cutback permits a longer growing season and, potentially, a longer stem. Thinner, later-flowering branches are cut to their origins, as new shoots that might sprout from a short, thin stub result in a cycle of short branches, which again produce short branches. Producers normally thin the non-marketable flowering branches in a separate operation at the end of the flowering season. Strong flowering branches of lignotuberous species are headed back to within 30 em of the base of the plant at a point just above well-developed buds. Other aspects of pruning of Leucosperm um parallel practices followed in managing other woody plants (Brits et al. 1986). Old flower heads and seed heads are removed during postharvest follow-up pruning. Vigorous shoots of 10 to 15 em length that developed during flowering are allowed to remain. Young, actively growing dominant shoots should be pruned back to 20 to 40 em. Poorly branching and short, thin shoots and dead and diseased shoots are removed. Seedling plants and rooted terminal cuttings of Leucospermum are headed back during vegetative growth flushes to improve plant shape and remove horizontal branches lying on the ground (Matthews and Matthews 1994). Flower heads that form on rooted cuttings should be removed to encourage lateral shoot growth. The prevalence of disease in the aerial portions of the plant will dictate the use of disinfectant on the pruning shears and protective sealants on pruning wounds 1.5 em diameter or greater. Matthews and Matthews (1994) distinguish between 1. cordifolium and other species of Leucospermum in recommending that the number of flowers per bush of the cordifolium types be strictly limited by pruning during the early years of bush development to achieve a more upright bush habit and longer stems. Yr 1: 0 Flw; Yr 2: 4 Flw; Yr 3: 10 Flw; Yr 4: 25 Flw; Yr 5: 50 Flw; Yr 6: 60 Flw. In their program, pruning is done at flowering and for a month or so afterwards. Pruning is also used to influence flowering, principally to delay it. Early fall pruning to leave 10 to 15 shoots of 10 to 15 em length was evaluated by Malan and Jacobs (1994) as a means to delay flowering through the production of shoots physiologically incapable of responding to short day inductive conditions. Night break lighting between 20:00 and 04:00 and supplemental irrigation were additive in prolonging stem growth. Naturally short daylengths in spring were expected to result in reproductive development and an extended flowering season. The system was unsuccessful, however, because changes in growth habit during the cool, reduced-light-intensity days of winter resulted in few marketable stems. This study should be repeated, however, with other cultivars or in warmer regions to determine if temperature or light intensity were truly limiting.

56

R. CRILEY

3. Disbudding. Following up on work by Jacobs and Honeyborne (1978), Brits (1986e) and Jacobs et al. (1986) demonstrated that removal of the primary inflorescence bud about two months prior to normal flowering led to the development of secondary inflorescence buds and a later harvest. Brits (1977) had previously demonstrated that application of ethephon to the branches prevented development of the primary inflorescence and activated the secondary inflorescence buds; later flowering was the result. Timing, however, was important, as late treatments caused loss of yield and decreased flower quality. Brits (1986e) suggested that it was necessary to select cultivars that would respond favorably to deheading or ethephon treatments. Both normally flowering and lateflowering cultivars were responsive. Although all buds on a shoot have a potential to develop as flowers, normally the first bud to develop inhibits reproductive development of other buds. In a few species such as 1. erubescens and 1. saxosum more than one flower develops, but on most large-flowered species, this is uncommon and undesirable for packing and shipping. Malan and Roux (1997) note that the characteristic of producing multiple flower buds does permit extension of the production season by removing the primary bud and allowing a secondary bud to develop. Since the second bud was suppressed in its initial development, it flowers later (Jacobs 1983, 1985). Malan and Jacobs (1990) had previously observed that decapitation of the terminal 5 cm of a growing shoot caused axillary bud break that was vegetative during natural or artificial long days but that resulted in development of an inflorescence in the uppermost axillary bud during the shorter daylengths of fall. The capacity of these axillary buds to develop as inflorescences was lost as days lengthened in the spring. Between 42 and 56 SD cycles were necessary for inflorescence development and late winter decapitation provided too few SD for reproductive development. Cultivar differences exist in the responsiveness of axillary buds to develop as inflorescences (Jacobs and Honeyborne 1978; Jacobs 1980, 1983). Disbudding ofthe primary inflorescence of 'Golden Star' in South Africa as late as October 15 was possible without crop loss (Jacobs and Honeyborne 1978), but 'Red Sunset' buds regenerated as vegetative shoots. September 15 was considered as the latest date at which disbudding would still provide a crop. Malan and Roux (1997) stated that the flowering time of early-flowering cultivars such as 'Ballerina' and 'Starlight' could be delayed better using disbudding techniques than later-flowering cultivars (Table 2.5). The disbudding operation is more complex than merely delaying flower production because it impacts upon the next year's crop as well.

Table 2.5. The period of delay from normal peak flowering time, at Eisenburg, South Africa, following disbudding of Leucospermum cultivars during the period indicated (Malan and Roux 1997). Disbudding Period

Cultivar

Normal flowering

Late April

Tested on most vigorous shoots (mostly 60 to 80 em long) 3-4 Sunrise late July 3 month distribution early Sept. Luteum of disbudded shoots 2-3 Gold Dust early Sept. mid Sept. 0 Scarlet Ribbons 0 Flamespike mid Sept. Helderfontein late Sept. 0 Yellowbird late Sept. 0 early Oct. 0 Ballerina early Oct. 0 Caroline early Oct. 0 Red Sunset mid Oct. 0 Gold Star Vlam late Oct. 0 late Oct. 0 Goldie Tested on average shoots (40 to 60 em long) Succession I early Sept. Succession II early Oct. early Oct. High Gold early Nov. Starlight

--

(Jl

'J

Late May

Late June

Late July

Late August

Weeks delay 7-8

13-14

16-17

16-17

4-5 1-2 0-1 2-4 0-1 0-3 0-1 0 0 0

6-7 3-4 0-2 6-7 1-2 2-4 0-2 0-3 0 0-1 0

8-10 5-6 4

0-1

11-12 6-10 6-7 4-8 7-11 4-7 4-7 2-6 5-7 0-1

4-5 1-4 3-5 1-4

5-7 4-6 5-6 1-7

5-8 5-7 8-10 3-8

4-5 0-1 1-3 0-2

-

4-6 4-7 1-4 3-4 0-3 2

58

R. CRILEY

Malan and Roux (1997) caution that the most vigorous shoots should not be disbudded, as these will be the early harvest of flowers and from their stubs develop the shoots for the next season's crop. Shoots of average vigor may be disbudded to produce a late crop, while weak shoots «40 em) do not respond well to disbudding. Disbudding can be done in groups to time the later crops for demand peaks. The practice of disbudding should only be applied to plants under a well-managed regime of pruning, fertilizing, and irrigating in which the vigor of the plant allows a predictability of the later production. 4. Irrigation. Water requirements for most Proteaceae have not been

determined. In the mountainous regions of the Cape where many Leucospermum species are found, rainfall (@ 400 to 1000 mm) is concentrated in the winter months, while a few species are found in the summer rainfall (600 to 1000 mm) regions inland and further north. In the western Cape province, pincushions are cultivated without supplemental irrigation, relying on natural winter rainfall of 600 to 700 mm. Malan and Jacobs (1994) reported that shoot growth cessation could be prevented during the dry fall by weekly irrigation at the rate of 27 L/m 2 (calculated from the author's description oftheir methodology), but night break lighting was required to continue the effect through winter. They concluded that water stress was the main cause of cessation of shoot growth prior to inductive SD in the autumn. However, many shoots were incapable of uninterrupted apical growth, and the development of distal axillary shoots rendered the shoots unmarketable as flower stems. Winter shoot production through the use of night break lighting and irrigation was not an effective approach to delay flowering until summer in 'Red Sunset' pincushion. In a typic eutrandept, medial isothermic soil, commonly denoted as a loam at the Maui Agricultural Research Station (Kula, island of Maui, Hawaii, USA), where an average annual rainfall of 45 to 100 cm rainfall occurs, an irrigation rate of 5.5 to 7.5 L per plant per day was determined optimum (Wu et al. 1978). Less water was used in fumigated fields where the stress of root-knot nematodes was absent. The presence of root-knot nematodes increased water requirements by nearly 2 L per day. A rate of 3.8 L per day could achieve 80% of optimum yield during drought situations. The latter rate is similar to Malan and Jacobs (1994) rate of 27 L/m 2 , but is less than the 35 L per week recommendation of Furuta (1983). 5. Nutrition and Fertilization. Unique to the Proteaceae are clusters of finely branched even-length rootlets occurring throughout the shallow

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

59

root system of most species (Purnell 1960). The rootlets are crowded together along the axis of the lateral roots and are covered with long root hairs. They do not appear to have mycorrhizal associations, but it is reported that they are microbially induced (Malajczuk and Bowen 1974). The masses have a lifespan of about 6 months before shrivelling and disappearing. Such root masses are known as proteoid roots, and through their large surface areas they are thought to be responsible for K and P absorption (Lamont 19a6; Vorster and Jooste 19a6a). Grierson and Attiwill (19a9) found increased H+ ion concentrations in leachates of proteoid roots, but also found increased levels of reduced manganese, and suggested that unidentified chelating compounds were released as well, since high amounts of aluminum have been found in leaves of Proteaceae. Lamont (19a6) cautions that management practices such as cultivation will damage proteoid roots, and weed control is essential to reduce competition between the shallow proteoid roots and shallow-rooted weeds. Since the proteoid roots are concentrated in the leaf litter and surface layers of the soil, proteaceous species tend to be sensitive to chemical treatments, whether they be fertilizer, nematicides, or fungicides. Phosphorus absorption in proteoid roots of Protea compacta showed a peak between pH 4 and 5.5 (Vorster and Jooste 19a6a). Analyses also showed that proteoid roots were more effective in absorbing potassium than were ordinary roots. However, proteoid roots also accumulated their P, acting as sinks, while ordinary roots readily translocated P to the aerial parts (Vorster and Jooste 19a6b). Inclusion of sucrose in experimental solutions stimulated the translocation of P from the proteoid roots, suggesting an energy-dependent mechanism for translocation from proteoid roots to the aerial parts. Proteoid roots were metabolically more active in P absorption at 35°C than at lower temperatures, while ordinary roots increased their rate of P absorption over the range of 15 to 35°C (Smith and Jooste 19a6). Proteoid roots also displayed a higher oxygen uptake than did ordinary roots. Grierson and Attiwill (l9a9) demonstrated that proteoid roots can acidify their immediate environment. pH values of 4.2 to 4.4 were reported in the leachates of proteoid roots of Banksia integrifolia, while associated leaf litter and soil 5 cm away had pH values of 7.1 and 5.5 to 6.5, respectively. They concluded that nutrient uptake is enhanced by lower pH and the release of organic chelating compounds from the roots. With Protea cynaroides, periods of active growth of proteoid roots immediately precede bud differentiation and bud development (Hanekom et al. 1973) and thus correlate with periods requiring high nutrient uptake. Although the above results were obtained with Protea compacta,

60

R. CRILEY

P. cynaroides, and Banksia integrifolia, the principles may be extended to Leucospermum. The mass of fine proteoid roots permits greater diffusion of oxygen around them. Their sugar and oxygen requirements and greater metabolic activity in both ion absorption and translocation suggest proteoid roots playa unique role in the nutritional status of these plants. The proteoid roots die off during the dry summers and are replaced each winter with the return of winter rains, a period when inflorescence development takes place. Both numbers and mass of proteoid roots increased during L. parile seedling development (Jongens-Roberts and Mitchell 1986). Mobilization of P to the canopy occurred in 1- to 2-year-old plants, while in 5to 6-year-old flowering plants, P level declined in the non-reproductive parts of the plant. In young plants, root production and foliar phosphorus content increased during the winter, but there was a marked decline in both in older plants. The phosphorus-phobia vis-a-vis the Proteaceae is widely circulated in the commercial literature [c.f., "Provided phosphate is totally withheld, average pH levels of 5 will be acceptable ... " (Riverlea Nursery undated)] and has received attention from researchers (Allemand et a1. 1995; Malan 1996). Rates of fertilization considered normal for other woody plants often caused phytotoxicity to proteas, and Munro (1990) related that growers were advised not to supply P in their fertilizer programs. Nichols (1981) classified L. cordifolium among the highly sensitive proteas as a result of experiments providing young plants with 1 to 2 kg P/M3 of soilless potting medium. Sanford (1978) reported very little effect of phosphorus addition (as treble superphosphate) of up to 400 kg P/ha in field culture, although there was a slight increase in marketable yield. Foliar content of P was not correlated with yields of flowers per plant. One Australian grower (Bowden 1987), however, reported that his proteaceous plants responded to low levels of slow-release forms of P. His account suggests a need to examine the form in which P is applied. Trials of 0.1 % potassium dihydrogen phosphite as a foliar spray for Phytophthora cinnamomi control showed no trace of phytotoxicity in several proteaceous species, including L. reflexum, while providing a high degree of control of the pathogen (Wood 1987; Turnbull and Crees 1995). Similar effectiveness was observed on four Leucadendron species (Marks and Smith 1989). Matthews (1982) suggested that soils used for Leucospermum culture should have a pH of 5 to 5.5, K and P levels below 20, Ca below 10, and Mg below 30. On the basis of New Zealand Ministry of Agriculture and Forestry soil analysis, the following nutrients levels (units not specified) were considered suitable for Proteaceae: Ca, 6; P, 4 to 6; K, 4 to 6; and

61

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

Mg, 8 to 12 (Salinger 1985). In Hawaii, a minimum soil content of 32 ppm (PzOs)' 0.117 meq K, and a pH of 5.5 to 6.1 were recommended (Munro 1990). In soilless culture using rockwool slabs or crushed volcanic rock, satisfactory growth of L. tottum and L. reflexum was achieved using a fertility regime of 50 ppm N, 15 ppm P, 25 ppm K, and 1 ppm microelements. The pH was maintained between 5.5 and 6.5 by addition of sulfuric acid (Calo 1986). In pine bark and sand, root development, plant height, and branching of containerized L. cordifoJium plants were satisfactory with N levels of 50 and 100 ppm and P levels of 4.5 and 9 ppm in twice-weekly liquid feeding (Matthews 1993). Parvin (1986) reported on the application of tissue analysis to understanding the nutritional requirements of Leucospermum. Samples of recently matured leaves from the most recently matured vegetative flush of growth were collected from healthy green, field-grown plants. The analyses (Table 2.6) were used to define a baseline against which abnormal plants could be compared. Seasonal variation existed, but only calcium and magnesium showed large differences between the vegetative growing period of summer and the inflorescence development period of late fall, with higher values for the former than the latter. Sanford (1978) found little relationship between amounts ofN, P, and K applied as fertilizer and foliar levels of the same nutrient. In his study, foliage N ranged from 1.27 to 1.38%, P was in the range of 0.14 to 0.16%, and K ranged from 0.62 to 0.67% in recently expanded leaves. Using sand culture, Claassens (1986) determined that Leucospermum

Table 2.6. Foliar and flower head tissue analyses of Leucospermum cordijoJium (Parvin 1986 and Claassens 1986). Content (% Dry Weight) Flower Head z

Foliage Element N P K Mg Ca S

Parvin Y

Claassens

Veld

Sand culture

1.18 0.09 0.49 0.22 0.53 0.14

0.86 0.12 1.39 0.20 1.05

0.50 0.08 1.40 0.60 0.20

2.00 0.15 1.60 0.60 0.25

ZClaassens 1986. YContent for microelements (ppm): Al (190), Cu (6), Fe (118), Mn (248) and Zn (30).

62

R. CRILEY

cordifolium responded better to ammonium than nitrate forms of N, although this species tolerated nitrate better than did the genus Protea. Analyses for the highest dry matter yield showed somewhat higher tissue concentrations for P, K, and Ca and lower N than did Parvin's fieldgrown plants (Table 2.6). He also analyzed the flower heads of unfertilized veld plants and his fertilized sand culture plants and found trends to be similar except for nitrogen. Claassens concluded that higher N levels contributed to higher yields as well as to a higher nutrient content, and that N in the ammonium form is the predominant element that needs to be managed in culture. Witkowski (1989, 1990) reported that L. parile stored N in leaves and twigs and used it during inflorescence production during the next year. Claassens's (1986) study was cited by Brits (1990c), with the additional information that certain ecotypes originating on calcareous soils tolerated higher concentrations ofN0 3 , NH 4 , P, alkalinity, and total salts than ecotypes originating from more acidic soils. Brits suggested that such characteristics might be a useful guide to selecting rootstocks. Malan (1996), on the other hand, offered the opinion that fertilization may be so dependant upon variety and site characteristics that recommendations would need tailoring to specific conditions. 6. Production Period. Although there are nearly 100 Leucospermum

cultivars available, the exporters see a need only for a few lines that cover the entire marketing period. Since a cultivar typically blooms for only 4 to 6 weeks, approximately 6 to 8 cultivars flowering in succession would cover the late winter to late spring marketing period (Brits 1992b). These would include the basic color lines and early, mid-season, and late production periods. Parvin (1974) reported that 65-75% of the total crop of L. cordifolium 'Hawaiian Sunburst' was harvested during the December through February time period in Hawaii. During a three-year study, beginning with 6-year-old plants, the per plant yields averaged 600 to 650 flowers. Approximately three years transpires under Hawaii conditions from initial seeding or rooting of cuttings before commercial levels of flower harvesting develop (Parvin 1974). Jacobs (1976) suggested that the flowering season could be extended by developing clonal selections from early- and late-flowering seedling populations (Fig. 2.4). His data showed that 500/0 of the crop could be harvested in 14 to 29 days, but through suitable selections, the marketing season could be extended over four to five months. Leucospermum releases of the ARC Fynbos Unit extend the season from mid-August (late winter) to mid-November (mid-spring) (Table 2.7).

Figures above horizontal bar indicate percentage of crop harvested. Figures below horizontal bar indicate number of days. Fig. 2.4. Distribution of flowering in a seedling population of Leucospermum cordifolium in South Africa. Source: Jacobs 1976.

7. Growth Regulator Studies. Long, strong stems are desired by the cut flower growers, but some Leucospermum species and hybrids produce stems too short to be of commercial value. Napier et al. (1986a,b) investigated the influence of single and multiple sprays of GA at 1000 mg/L on a hybrid of L. conocarpodendron x L. cordifolium during the summer vegetative growth stage. They noted that GA applications were ineffective in causing elongation when shoots were reproductive, but internodes between basal bracts of the shoot were elongated. Multiple

64

R. CRILEY

Table 2.7. Color and flowering periods in the western Cape (South Africa) for 17 Leucospermum cultivars released by the Fynbos Unit of the Agricultural Research Council of South Africa (Brits 1992b). Flowering Period Color

Earlyz

Yellow

Red

Pink/Pastel! Novelty

'Sunrise'L. cordifolium x L. patersonii 'Succession l' !ineare-type 'Helderfontein' L. glabrum

Mid-season Y

Latex

'Yellow Bird' 1. 'Goldie'L. cordifolium cuneiforme 'Luteum' L. reflexum 'High Gold' L. cordifolium x 1. patersonii 'Flamespike' 'Vlam' L. cordifolium L. cordifolium 'Fire Dance' 1. cordifolium 'Scarlet Ribbon' 'Pink Star' 1. cordifojium 1. glabrum x 1. tottum 'Tango' 'Caroline' 1. glabrum x 1. lineare 1. cordifolium x L. tottum 'Starlight' lineare-type 'Succession 2' Uneare-type 'Ballerina' jineare-type

zMiddle August to end of September YMiddle September to end of October XLate September to mid-November

applications of GA caused a marked increase in stem length without affecting shoot diameter. The dry weight per unit length of shoot was decreased because of smaller leaves. In a concentration comparison, GA at 750 mg/L applied five times at three-week intervals provided optimal shoot elongation, while higher concentrations caused damage to the leaves and shoot tip, and shoot diameter was thinner. In a similar field study on a L. conocarpodendron x L. cordifolium hybrid, Malan and Jacobs (1992) reported that a single GA a spray at 500 mg/L, when shoots resulting from pruning were 10 to 17 cm long, markedly increased the number of shoots longer than 30 cm when compared to control plants. Pruning was done in late winter to leave a stub about 20 cm in length, and the GA application was made 10 to 12 weeks later. Their study included multiple applications, but only up to 3, a month apart, and shoot length increased with multiple applications, as in Napier's study. Internode length was affected only

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

65

slightly (no data presented), but node count was increased significantly. Their final recommendation of 500 mg GA 3 /L was based on the economics of GA application, higher concentrations being uneconomic in their opinion. Application of the cytokinin benzylaminopurine (BA) to developing inflorescences of 'Red Sunset' increased the number of florets in the inflorescence as well as dry weight, but also caused abnormal peduncle growth (Napier et al. 1986b). A single application made early in the development of the inflorescence increased floret number by 45%, while multiple applications added only slightly more, although dry weight of the inflorescence increased as the number of BA applications increased to four. Malan et al. (1994c) reported that apices ofBA-treated shoots were larger than those of untreated shoots and more bract and flower initials were produced as a result, thus confirming the observations of Napier et al. (1986a). Spray applications of BA after inflorescence initiation stimulated the development of several inflorescence buds on the same branch, a process that ended in the abortion of the inflorescence buds (Wallerstein and Nissim 1988). Dupee and Goodwin (1990) reported that application of gibberellin (GA 4 +7 or GA 3 ) or paclobutrazol to initiated flower buds enhanced flowering by 3 to 9 days. Terminal bud removal delayed flowering, while terminal bud removal and treatment of the next bud with GA 4 + 7 hastened the development of the secondary bud. Spray applications of GA to initiated inflorescences accelerated development, but also caused flower bud abortion (Wallerstein and Nissim 1988). Ethephon (960 mg/L) is also being usedon mother plants to induce multiple branches on shoots to be harvested and used as cuttings for potted plant production (Brits et al. 1992). The use of auxins for rooting of cuttings is treated under propagation. Ethephon application (500 mg/L) to decapitated shoots reduced their responsiveness to inductive short days (Napier and Jacobs, 1989). Ethephon also enhanced the loss in responsiveness to short days when the plants were grown under shade. It is not clear how ethephon interacts with the lowered carbohydrate status of the shoot to reduce flower initiation. D. Plant Protection 1. Diseases. Among the important diseases affecting Leucospermum are root and collar rots caused by Phytophthora cinnamomi Rands and P. nicotianae Breda de Haan, leaf spots and stem cankers caused by DreschsJera dematioidea (Bubak and Wrobl.) Subramanian and P. C.

66

R. CRILEY

Jain, and D. biseptata (Saci and Roum) M. J. Richardson and E. M. Fraser, a stem and leaf scab caused by a Sphaceloma (= Elsinoe telomorph) sp., and a canker and dieback caused by Botryosphaeria dothidea (Moug:Fr) Ces and De Not. (Von Broembsen 1985,1989; Von Broembsen and Van der Merwe 1985; Knox-Davies et a1. 1988; Kent 1989; Nagata and Ferreira 1991, 1993). Botrytis cinerea Pers.:Fr also colonizes young shoot tips and buds of Leucospermum (Cho 1977). The aerial diseases are favored by conditions where dew or fog persist in the mornings and are transmitted by splashing water and cuts caused by pruning and flower harvest. The Dreschlera group and Sphaceloma (Elsinoe) require free water for conidial germination (Benic and Knox-Davis 1983; Kent 1989). The first report of verticillium wilt on any protea species appeared in 1991 (Koike et a1. 1991), when affected plants of L. cordifolium collapsed and died. Symptom expression included terminal shoot wilting, fading of foliage to light green, and eventual collapse and browning of the entire plant. Brown flecking and streaking were apparent in the stem xylem tissue. Verticillium dahliae Kleb was isolated and its pathogenicity confirmed by inoculation into and reisolation from cuttings of 1. cordifolium cv. Firewhee1. In the long term, breeding for disease resistance is a desirable alternative to fungicide use, but with the past emphasis on breeding for flower qualities, little progress has been made. Some progress has been reported in breeding for Phytophthora tolerance and Dreschlera resistance (Von Broembsen and Brits 1985,1990), but all species evaluated lacked resistance. Good tolerance was shown for several hybrids and species selections and some tolerance appeared to be expressed within 1. cordifolium (Von Broembsen and Brits 1990). Leonhardt et a1. (1995) reported some resistance to Sphaceloma (Elsinoe scab disease) in 1. conocarpodendron and L. reflexum. They have also found some interspecific hybrids with resistance to Sphaceloma, Botrytis, and Dreschlera. Matthews (1988) reported that 1. patersonii showed some resistance to pincushion scab with a cultivar 'Goldie' completely resistant. Protective fungicides (e.g., mancozeb, iprodione, chlorothalonil) are recommended, as well as regular sanitation to remove diseased or dead plant parts. Control of canker and dieback was achieved by a single spray application of benomyl immediately after pruning. Since Leucospermum is extremely susceptible to Phytophthora (Von Broembsen and Brits 1985), control measures include avoiding poorly drained sites, planting disease-free nursery material, and fumigating the soil with methyl bromide prior to planting. Soil solarization has also been recommended (Knox-Davies 1988). Systemic fungicides have given inadequate control or are phytotoxic.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

67

Control measures for many foliar diseases include roguing, sanitation, disinfection of pruning shears, and application of fungicides. Overreliance on broad-spectrum fungicides such as benomyl has fostered resistance among some pathogens (Cho 1977). Due to the ever-changing spectrum of chemical controls, it is impractical to attempt to list effective materials, but useful resources include Protea Diseases (Von Broembsen 1989), Protea Diseases and Their Control (Forsberg 1993), and the occasional publication of The Protea Disease Letter (Nagata and Ferreira 1991, 1993) by the University of Hawaii. An interesting biological control approach against Phytophthora cinnamomi utilized selected strains of Pseudomonas cepacia (Turnbull et a1. 1989). Among the Proteaceae, Leucospermum was still susceptible to the root rot when inoculated with Pseudomonas cepacia, but plant mortality was slightly reduced. The promise of biological control, at least for Leucospermum, remains unfulfilled. 2. Nematodes. Root-knot nematodes can severely limit growth and productivity of Leucospermum (Cho and Apt 1977). Heavily infected plants show stunting and chlorosis, followed by death of the plant. Treatments with phenamiphos and the fumigant dibromochloropropane (DBCP) increased shoot growth and flower production (Cho et a1. 1976). The root-knot nematode [Meloidogyne incognita (Kofoid and White) Chitwood] decreases cut flower yields by at least 25 % in infected fields compared to fumigated fields with an optimal irrigation regime (Wu et a1. 1978). Under drought conditions or with minimal irrigation however, yields were comparable. 3. Insect Pests. Three general categories of insect pests that damage proteas are (1) flower visitors, which mayor may not damage the flowers but which are quarantine problems because the flowers must be marketed insect-free; (2) leaf feeders, leaf miners, and sap suckers, which cause aesthetic damage to the foliage of exported cut flowers; and (3) borers, which use protea stems and flowers as their hosts (Coetzee 1987a, 1987b). Occasionally centipedes and snails are found in the flower heads. A "Witches Broom" stem proliferation condition in protea may be caused by a mite (Aceria proteae) (Coetzee 1987a). Seed predation is a problem both in the wild and for propagators of proteas from seed (Coetzee and Giliomee 1987). Effective registered pesticides exist for some of the pests, but differ from country to country.

4. Weeds. Nishimoto (1975) reported little or no injury from high rates of dichlobenil and oxadiazon (Ronstar) on trickle-irrigated Leucosper-

68

R. CRILEY

mum planted 8 months prior to treatment. However, slight to severe injury was reported from simazine, ametryne, and diuron, especially at high rates. Weed control from all treatments was good. DeFrank and Rauch (1988) achieved acceptable weed control from pre-emergent sprays of oxadiazon and oxyflurofen 2% + oryzalin 1 % , but noted that a black plastic woven ground cover suppressed all weed growth, which has since become an accepted weed control practice in Hawaii. For grass weed control, DeFrank (1990) recommended the post-emergent herbicides: fluazifop-butyl (Fusilade), sethoxdim (Poast), DPX 6202 (Assure), and RE-36290 (Selectone). DeFrank and Rauch (1988) achieved satisfactory post-emergence grassy weed control with the manufacturer's recommended rate of fluazifop-P, but noted that a 4X rate could damage Leucospermum flower buds. E. Postharvest Studies 1. Handling and Storage. Except in southern California, proteas tend to be grown in areas far distant from their markets. As most proteaceous flowers are heavy and/or bulky, air shipment is expensive, and shippers have investigated slower shipment methods, including seafreight. Pincushions are normally harvested with at least the first row of styles open, but this varies with the cultivar and destination. For packing into boxes, inflorescences with too many open styles are not desired because of tangling. On average, about 50% of the styles are open (Matthews and Matthews 1994). Research on postharvest handling practices has shown that the pincushion protea will tolerate cool, dry, long-term storage and still provide a useful vaselife. 1. cordifolium flowers that were cooled and hydrated at 1°C in water, wrapped in newsprint and bagged in plastic film withstood periods of three and four weeks of 1°C storage, and after rehydration, possessed an average vaselife of 8 days, versus 9 days for untreated controls (Jones and Faragher 1990). Haasbroek et al. (1973) successfully stored L. cordifolium at 1. 7°C for 3 and 4 weeks without significant deterioration in vaselife. Downs and Reihana (1986) found significant varietal differences in vaselife following a period of simulated transport, with the New Zealand cultivar Harry Chittick at 35.5 days, a Hawaii hybrid of 1. lineare x L. cordifoJium at 29.7 days, and a South African hybrid (1. glabrum xL. conocarpodendron) Veldfire at 16.9 days. Parvin (1978) improved vaselife of Leucospermum cordifolium by 44 to 48% through the use of a 2 to 4% sucrose plus 200 to 600 ppm hydroxyquinoline citrate "preservative" solution. Silver nitrate at 1000 ppm was not beneficial for the cultivars of L. cordifolium but improved

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

69

vaselife for the L. conocarpodendron x L. cuneiforme hybrid, 'Hawaii Gold' (Parvin and Leonhardt 1982). Since the mature, expanded pincushion flower occupies as much room in a shipping carton as a standard chrysanthemum, investigations were undertaken into the revival of wilted flowers with extruded styles, which could be packed more tightly. Flowers pulsed with a preservative prior to partial dehydration (20% loss of FW) and storage (24 h at 13°C) could be revived, although vaselife was not as long as with fresh cut flowers (Criley et al. 1978a, 1978b). Leucospermum flowers cut in bud (7 em diameter) offered better promise, however, with full development and less loss of vaselife than flowers cut at a younger stage (Criley et al. 1978a; Parvin and Leonhardt 1982). 2. Insect Eradication. A variety of approaches has been used to eradicate insects from the flower heads before shipping. Maughan (1986) reported that fumigation of various Protea spp. with methyl bromide, carbon dioxide, nitrogen, sulfur dioxide, dichlorvos, pyrethrum, and combinations killed varying amounts of insects, but often damaged the flowers or decreased vaselife. Treatments combining carbon dioxide with pyrethrum or diclorvos required exposures up to 30 h for 100 % kill, but did not produce marked damage. Magnesium phosphide gas plus dichlorvos also has given excellent control (Wright and Coetzee 1992), as has a pressurized aerosol of dichlorvos (Coetzee 1987b; Wright 1992). Vapor heat treatments of 10 min at 56°C or 66°C decreased vaselife of cut Banksia prionotes by 21 % and 49%, respectively, while hot water dips of 30 min at 46°C or 10 min at 56°C damaged the inflorescences and reduced vaselife by 25% and 37%, respectively (Seaton and Joyce 1993). Gamma irradiation of protea flowers effectively killed earwigs, spiders, weevils, millipedes, and ants after 50 minutes of exposure (0.1 to 2.9 megaRads) without serious leaf blackening, but the experiments did not include Leucospermum (Wright and Coetzee 1992). At a dose required to kill insects (10k Gy), flowers and leaves of Banksia were damaged (Seaton and Joyce 1992). In the only similar work mentioning Leucospermum, inflorescences with 500/0 of the styles reflexed were subjected to 30 Krads of gamma irradiation (Haasbroek et al. 1973). Evaluation of the flowers and foliage after irradiation, 36 h storage at 15°C, and rehydration in a preservative solution showed little or no damage and a vaselife of 28 days versus 23 days for blooms with no irradiation treatment. Since corroborating data is lacking, it is not clear whether Leucospermum is more tolerant to gamma irradiation than other proteaceous flowers or whether the conditions of this experiment were unique.

R. CRILEY

70

3. Grades and Standards. For many years, harvest of pincushions from

natural stands in the veld resulted in mixed quality and lack of uniformity of the product (Littlejohn et al. 1995). This situation improved as pincushions moved to more distant cultivation areas and seedlings and selections were planted out. Little effort was made to manage the plants for longer, straighter sterns. Initially, the wholesale and retail florists accepted mixed qualities, but the existence of standards for most floricultural crops stimulated a similar request for the proteaceous cut flowers as well. An early attempt to gain approval for grades and standards for cut pincushion flowers (Hawaii Dept. Agr. 1980; Table 2.8) failed to

Table 2.8. Standards proposed for Leucospermum cordifolium by the Hawaii Department of Agriculture (1980).

Class (Grade) Standard

Extra fancy

Fancy

Stem length from cut end to base of flower head Flower

> 23 cm

15 to 23 cm

Full head, well-formed and symmetrical, well developed, more than 1/2 styles reflexed, well colored, and typical of the species. Clean, properly trimmed, free from injury. Angle of flower head not more than 90° to the stem. Leaves stripped from lower 3/4 of stem. Slight defect or blemish permitted. Curvature not to exceed 2.5 em from a straight line. Not more than 2% by count may fail to meet the requirements of the grade or the stem length.

Full head, well-formed and symmetrical, well developed, more than 1/2 styles reflexed, well colored, and typical of the species. Clean, properly trimmed, free from injury. Angle of flower head not more than 90° to the stem. Leaves stripped from lower 3/4 of stem. Slight defect or blemish permitted. Curvature not to exceed 2.5 cm from a straight line. Not more than 2% by count may fail to meet the requirements of the grade or the stem length.

Foliage

Stem straightness Tolerances for defects and offsize

71

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE Table 2.9. Flower Export Council of Australia proposed standards (1992) for cut Proteaceae (Leucospermum). Class (Grade) Standard

Extra class

Class 1

Minimum length Flower

60

cm Well formed.

40cm Reasonably wellformed. Sound, clean, uniform, of good color and size, no abnormal external moisture, fresh in appearance, insect- and diseasefree. Proportion of reflexed styles < 5%. Flowers not hidden by leaves. 90% of leaves intact on not less than 50% of stalk below flower head. Flowers typical of the variety. Typical of species.

Foliage

Clonal

Single bloom Tolerance for defects and blemishes

Sound, clean, uniform, of good color and size, no abnormal external moisture, fresh in appearance, insect- and diseasefree. Proportion of reflexed styles < 5%. Flowers not hidden by leaves. 90% leaves intact on not less than 50% of stalk below flower head. Flowers of clonal origin. Typical of variety and species. Stems straight (no more than 10° bend). 5%

Straight stem with flower head no more than 45° bend. 10%

enlist grower support. A major deficiency of this proposal was acceptance of short stem flowers. The Flower Export Council of Australia (1992) circulated a draft grades and standards proposal (Table 2.9). Where they languish, grades and standards need to be implemented, if only to improve communication in the overseas flower markets that exporters have targeted. The IPA itself should develop a set of standards for stem length and straightness; flower shape and freedom from defects, insects, and diseases; and descriptions for single- and multiple-headed stems. Tables 2.8 and 2.9 present a platform from which to start.

72

R. CRILEY

F. Genetic Improvement One of the first Leucospermum hybrids to be registered was a red hybrid named 'Mars,' selected in 1969 by the late F. C. Batchelor on his Protea Heights farm from a Leucospermum cordifolium population after five generations of mass selection (Brits 1984a, 1985a). As of the fourth edition of the International Protea Register (International Registration Authority: Proteas 1997), 30 cultivar names have been registered and another 58 have been noted but not registered for selections and interspecific hybrids of Leucospermum. Breeding objectives for proteas have mostly focussed on new flower colors, improved productivity, and a longer season of bloom, but characteristics such as improved postharvest life, disease resistance, and slender, longer, and straighter stems, reduced leaf pubescence, and smaller leaves have also received attention (Brits 1992a, 1992b; Ito et al. 1990; Leonhardt et a1. 1995).1. Jineore has been used to contribute slender, light-weight stems with narrow, pubescence-free foliage, all qualities sought by flower exporters (Leonhardt et al. 1995). 1. lineore contributes earliness to hybrids with 1. cordifolium, while 1. tottum contributes a later flower season (Jacobs 1976). Interspecific hybrids of 1. Jineore with L. cordifolium have been selected that markedly extend the normal flowering season in South Africa (Brits 1992b). Active breeding programs are being conducted at the Fynbos Research Station, Elsenburg, South Africa (Brits 1992a, 1992b; Littlejohn et al. 1995) and at the Maui Research Station of the University of Hawaii (Ito et aI. 1978, 1979, 1990,1991; Leonhardt et a1. 1995), and in Israel (Shchori et a1. 1995). Breeding and selection require 10 to 15 years, although some hybrids have been produced in less than 10 years (Ito et a1. 1990). In Israel, evaluation of hybrids between L. potersoni and 1. conocarpodendron yielded four high-yielding cultivars tolerant of high pH soils and a rootstock cultivar in only four years after planting out (Shchori et al. 1995). Ackerman et a1. (1995) selected plants tolerant to high pH, calcareous soils, from seedlings of 1. patersoni. One selection, designated 'Nemastrong,' was also tolerant to nematodes. A cross between 1. patersonii and 1. conocorpodendron, designated 'CarmeH,' also demonstrated excellent resistance to high pH and calcium. Both selections root well from cuttings and have good grafting characteristics. G. Leucospermum as a Pot Plant While a number of the Proteaceae may be grown as potted plants, the Leucospermums, with their relative ease of rooting and attractive floral display, have the greatest potential (Sacks and Resendiz 1996). Plants for sale

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

73

need to be offered with several buds open. High light intensity is necessary for flowering (Jacobs and Minnaar 1980; Napier and Jacobs 1989; Ackerman et al. 1995) as well as for rapid rooting of cuttings. Research on the photoperiod responsiveness of Leucospermum (Wallerstein 1989; Malan and Jacobs 1990) indicates that daylength manipulation may have implications for potted flowering plant production as well. Leucospermum species suitable for potted plants are of two types: those having a single large inflorescence, such as L. cordifoJium, L. lineare, and L. tottum; and those with small multiple inflorescences (conflorescences) such as L. oleifolium, L. muirii, and L. mundii (Ackerman et al. 1995; Brits et al. 1992; Brits 1995a). It is important to select material that will root rapidly and support flower initiation and development on a young root system (Ackerman and Brits 1991; Brits et al. 1992). 1. Production. Some pinchusions do not respond well to a short production cycle and must be grown on a longer cycle of 18 to 24 months (Ackerman et al. 1995). These include the multiple-headed species and some single-headed types. Branched cuttings are produced on the mother plant, rooted in late autumn, and kept under production an extra year to flower in the second season. Sacks and Resendiz (1996) use a 20-month production program, rooting cuttings in the summer, transplanting to 10-cm pots, and pinching to induce branching the following spring and potting up to 16-cm pots. Salable pots with 5 to 6 buds per plant are produced a year later. The growing medium should be lightweight but capable of holding sufficient water and nutrient cations (Brits et al. 1992). A medium of 10 peat:40 pine bark:50 river sand supplied with a liquid feed at each irrigation (77 ppm N, 5 ppm P, 63 ppm K, 23 ppm Ca, 8 ppm Mg, 1.8 ppm Fe, and a microelement complex) proved satisfactory (Ackerman et al. 1995), while Ben-Jaacov et al. (1989) reported successful cultivation in media of 4 coarse peat:4 fibrous peat:2 vermiculite No.6 or 3 volcanic tuff (8 mm):l peat in 10-cm pots. Brits (1990a) provided a rapid production method using cuttings that had set buds on the mother plant (Fig. 2.5). Following rooting, the inflorescences developed, producing a marketable potted plant within 6 to 8 months after harvesting of the original cuttings. As one single flowering stem, the plants were not marketable because of weak stems and lack of fullness, but several single-stem cuttings per pot is feasible (Brits et al. 1992). Branched, budded cuttings are useable, but cultivar selection for the capacity to continue inflorescence development is necessary to avoid bud abortion during or following rooting. Alternative protocols for rapid pot plant production are illustrated in Fig. 2.6. Brits et al. (1992)

74

R. CRILEY

LATE SPRING

WINTER

AUTUMN

Harvest Rooting 'I

15 em

I'

"

Fig. 2.5. Original concept of rapid production of flowering Leucospermum potted plants from semi-hardwood cuttings rooted while bearing a flower bud. Source: Brits et a1. 1992.

POT PLANT PRODUCTION SYSTEMS Month of activity

SON D J F A. Harvest cuttings during flower initiation. Select for shoots of at least 3.5 nun diameter. Select for multiple branched cuttings with desirable angle to main stem and short enough to be proportional to final pot size.

B. Shoot tips of mother plants are pinched and headed back, and branch-stimulating compounds such as BA and ethephon are applied. Harvest cutting early during active growth. Root during late summer and allow flower initiation at normal time.

M

A

· Flower · initiation · in the · field

M

J

J

A

S

o

· Rooting period . Resume ·-----------------------. flower · Harvest Root . devel· cuttings growth. opment

N

Flowering

8 months

.Rooting Flower. Flower . Flowering · period . initiation . development ---------------. on own · Harvest roots Root . growth. 10 months

Fig. 2.6. Alternative rapid production systems for Leucospermum potted plants in the southern hemisphere using cuttings harvested in different physiological stages. Source: Brits et a1. 1992.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

75

suggested that taking the cuttings in late summer (earlier than the semihardwood stage) would overcome the problem of abortion of the primary flower bud and allow rooting to occur before initiation of flower buds. They suggested heading back soft terminals to harder subterminal wood. Yoshimoto (1982) successfully rooted cuttings with branches stimulated by removing 6 to 10 cm of tip during spring and summer, but he was not successful in forcing flowering in the next season. At that time, the application of high light and photoperiod requirements was unknown. A significant advance in production of potted Leucospermum 'Ballerina' was reported by Brits et al. (1992). Branched shoots (Fig. 2.7) produced by spraying 960 mg ethephon/L on strongly elongating primary shoots about 10 cm long on the mother plant were rooted and manipulated as potted plants. The resulting shoots had a wider angle to the primary shoot compared to hand-pinched controls and produced a

Fig. 2.7. A shoot of Leucospermum treated with ethephon to induce multiple laterals. Photo: CrUey.

R. CRILEY

76

more desirable shape for marketing. Observations from other studies (Brits et a1. 1986; Jacobs and Minnaar 1980; and Napier 1985) suggested that shoot diameter was important for good flower initiation, and that cultivars should be selected for their capacity to produce flowers on relatively thin stems (c. 3.5 mm diam.). Flowers were initiated on stem diam. of 4 to 5 mm in cut flower types, but on stems too long for wellproportioned potted plants. Species producing multiple inflorescences, such as 1. mundii and 1. oleifoJium, were also recommended. The 1. Jineare x L. tottum hybrid 'Ballerina' has been shown to have a high propensity to develop flowers even after cutting back (Brits et a1. 1992; Ackerman et a1. 1995) (Fig. 2.8). In one experiment in which primary shoots on mother stock plants were tip-pinched, BA was applied, and the resulting shoots shaped on the mother plant before taking the shoot as a cutting. Following treatment with 4000 ppm KIBA, noninduced, branched cuttings of two cultivars rooted well in 4 to 5 weeks. 'Ballerina' tolerated the manipulations better than did 'Tango' (a hybrid of 1. glabrum xL. lineare) with 80% of the rooted plants flowering on several branches the next spring versus a very low proportion for 'Tango.' Growth regulators are being used to induce branching (Brits et a1. 1992) and improve compactness, increase leaf number, and increase shoot diameter, with a concomitant improvement in the capacity to ini-

Jan 19

May 25

Sept 16

Dee

Flowers

10 em

+ BA

New infl. buds initiate

Fig. 2.8. Diagram of sequential manipulations performed on 'Ballerina' Leucospermum lineare xL. tottum shoots, followed by rooting in early spring and resulting in branched potted plants flowering in December in the southern hemisphere. Source: Brits et aI. 1992.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

77

titate inflorescences (Ackerman and Brits 1991; Ben-Jaacov et al. 1990; Brits 1995a). These uses may apply to cutting manipulations on the stock plant as well as to plants already growing in containers. Brits et al. (1992) proposed a scheme for the rapid production of potted Leucospermum using paclobutrazol and BA on the mother plants (Figure 2.9). Ethephon may cause some shoot length reduction and is additive with paclobutrazol (Brits 1995a). 2. Postproduction. Budded Leucospermum plants abort their young flowering buds if moved into low indoor light conditions. Ackerman et al. (1995) recommend that the first row of styles be released on the inflorescence as the minimum developmental stage. Following storage in darkness for up to 8 days at 4°C and 90% RH, budded plants of 'Ballerina' continued to flower without damage or reduction in quality. Under similar conditions, L. oleifoJium and L. mundii suffered some bud damage and leaf discoloration and flowered for 17 and 7 to 10 days, respectively (Ackerman et al. 1995).

IV. CROP POTENTIAL AND RESEARCH NEEDS

As developing nations seek sources of foreign currency to support development and improve conditions for rural peoples, the export of flower crops has been an important component. However, such nations do not support research into the new floral crops, and the sources of knowledge will be the very nations whose growers will lose market share to the new competition. Nonetheless, a 1997 listing of IPA members revealed only 13 different nations and did not include any from Asia or Central/South America. The same impetus that moved rose, carnation, and chrystanthemum production to Colombia, Ecuador, Mexico, and Kenya will also drive Leucospermum production to suitable climatic regions in nations with low land and labor costs. Interest is being shown in areas as diverse as Taiwan, China, Korea, southern France, Corsica, Chile, and El Salvador. Development of new protea-producing regions will come from joint ventures with existing growers. Since the market for proteas of all types is not yet saturated, particularly in terms of year-round availability, there is still room for both domestic and foreign production to increase. The few researchers involved with production of cut flowers and potted proteaceae have much work ahead of them before crop production practices reach the levels of sophistication attained by roses or carnations, for example. The challenge for producers is to identify and prioritize where to put limited financial resources in support of long-term as well as short-term needs.

78

R. CRILEY SPRING

... > (,) 0 o 2 TREATMENT

oW

Z


WINTER SPRING

AUTUMN

SUMMER

(,)

Z ::;) -

CXl W

..,

LI.

Shoot growth period

I

a.

- _. -'W

CIl

I-

(,)

o

> o

z

uw

Q

l

Period of flower induction Inflorescence buds develop

1

Control

2 Decapitate

3 Decapitate + PBZ

4 Decapitate + PBZ + headback

5 Decapitate

+ PBZ + headback + BA

Fig. 2.9. Diagrams of basic rapid production systems of Leucospermum in the southern hemisphere. Seasonal manipulations are done on the mother plant primary shoots and on rooted cuttings and include. progressively. 1: control; 2: branching treatment; 3: growth retardation with pac1obutrazol (PBZ); 4: shaping of pot plant by heading back laterals; 5: benzyladenine treatment to increase number of inflorescence buds in types bearing conflorescences. Source: Brits et al. 1992

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

79

At the Sixth Biennial Conference of the IPA, Parvin (1991b) observed that the first decades of protea production were producer-driven: the novelty value was high, the supply was low, and almost any protea brought to market could be sold. He ventured that as wholesalers, retailers, and the ultimate consumer begin to appreciate quality, the markets will be driven by consumer preferences. Education of the consumer, determining consumer preferences, and controlling production to grow what the consumer wants are the future for the industry. The research needs of Leucospermum, as separate from other Proteaceae, are not so distinct, and there is a great deal of overlap in such lists (Brits et al. 1992; Brits 1995c; Malan 1995). The categories for needed research range from gaining a better understanding of the biology and physiology of the subject plant to learning about marketing opportunities and requirements. Gathering and learning more about the varied germplasm is a high priority, especially with South African flora threatened by wild gathering, land clearance for crops and animals, and other forces inflicting loss of habitat. In the Leucospermum collections at the Fynbos Unit of the South African Agricultural Research Council, some forms can no longer be found in the wild. The germplasm base is especially valuable for breeding and crop improvement (Littlejohn 1995). Plant breeders have much to learn about the genetic bases for productivity, disease resistance, flower color, ease of propagation, and possibilities for manipulating flowering time. Nutrition remains an area of concern because of off-color foliage disorders, interactions with soil pH and soil type, and inadequate standards for tissue analysis and their interpretation as a guide to fertilization. Malan (1996) notes that the interaction of substrates, growing techniques, and nutrition on proteoid root development is unknown. The suggestion that ammonium nitrogen is favored by Proteaceae should be followed up, as well as alternative forms of phosphorus for fertilization. Development of Leucospermum as potted plants also requires an understanding of the fertilizer regime. The interactions of major and minor elements with the flowering process is not known, and this could be important in the timing of fertilizer application on growth and flowering. Increasingly, attention is being turned toward practices that spread seasonal production over longer periods, improve quality, and permit better management of the plants. Other culture and management issues requiring research include: salinity tolerance, irrigation frequency and amount, pruning for optimal flower production and plant growth habit, and the interaction of nutrition with vegetative and reproductive phases of growth. The culture of Leucospermum under protected cultivation

80

R. CRILEY

and soilless culture systems is receiving attention in areas where the climate is marginal for outdoor culture (Allemand et al. 1995; Montarone and Allemand 1995). While vegetative propagation is not the problem with Leucospermum that it is with other Proteaceae, research continues to find more efficient and less costly systems. Bringing tissue culture from a laboratory level to commercial production volumes also represents a challenge, if not to research, then to the ingenuity of commercial laboratories. The introduction of rootstocks, such as 'Spider,' (Van der Merwe et al. 1991) and 'Nemastrong' and 'Carmeli' (Ackerman et al. 1997) that are tolerant to diseases, easy to root as well as suitable for the technique of cutting grafting, and compatible with other species and hybrids, may accelerate plantings of Leucospermum in previously inhospitable sites. Israeli research has proven the value of adaptability testing in the development of rootstocks suitable to local soil types. Pest control remains an on-going problem area, not only for new insects, but also because of diminishing availability of registered chemical controls. Insect presence in cut flowers limits their use and export and is the impetus for finding improved practices to prevent their presence, remove them, or kill them (Seaton and Woods 1991; Wright and Coetzee 1992). Ants, while not damaging pests on their own, are well known for "managing" colonies of other insects that they bring into the inflorescences, and effective control measures need to be developed. The practices of Integrated Pest Management (IPM) have not been elaborated for Leucospermum, although the principles developed for other crops will certainly apply (Wright 1995). Control of diseases and nematodes faces the same problem of diminished availability of registered chemicals. The stem and collar rots caused by Phytophthora spp. are particularly difficult because the most effective fungicide, metalaxyl, is not registered for field use in protea. At present, use of Phytophthora-tolerant rootstocks offers the best approach, while the traditional breeding approach will require many years to implement and may still find no genes for resistance in the species. The technologies of genetic engineering may yield useful results once resistance genes are identified. The minor crop designation under which all protea fall is a deterrent to rapid advances in finding herbicides that can be used among proteas, but progress can be expected here, especially when registrations permit a broad designation for ornamental use. Specific weeds may still pose a problem, however. The use of groundcover or sod-crops that can be mowed and managed to reduce their competition with the shallowrooted proteas offers some promise, especially when other advantages

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

81

may accrue, such as nematode-repelling properties, reservoirs for predaceous insects, and nutrition (through the use of nitrogen-fixing legumes). Postharvest research is needed to determine optimum storage conditions, vaselife following pre-conditioning and storage treatments, hybrids with good vaselife, packing and shipping conditions, management of diseases, and disinfestation of insects. The post-production characteristics of potted Leucospermum and the production practices that influence them are also in need of elaboration. Marketing research is high on the list of priorities of commercial growers in all parts of the world. The needs range from product selection to identification of consumer wants, from postharvest handling and storage to packaging, and from identifying seasonal sources to the markets requiring the products available at any given time. At the Seventh Biennial IPA Conference in Harare, Zimbabwe, Kobus Steenkamp, Farm Manager of Protea Heights near Stellenbosch, recounted the story of a farmer who had won a million Rand in a lottery. Asked what he would do with the money, he replied, "I will just carry on farming until the money is finished." Mr. Steenkamp added, "I think one can run a sound business with proteas, but not easily get rich." LITERATURE CITED Ackerman, A 1995. IPA workshop report on problems of protea growing and IPA panel discussion. Introduction to the workshop. J. Int. Protea Assoc. 29:6-8. Ackerman, A., J. Ben-Jaacov, G. J. Brits, D. G. Malan, J. H. Coetzee, and E. Tal. 1995. The development of Leucospermum and Serruria as flowering potted plants. Acta Hort. 387:33-46.

Ackerman, A, and G. J. Brits. 1991. Research and development of protea pot plants for export under South African and Israeli conditions. Protea News 11:9-12. Ackerman A, S. Gilad, B. Mechnik, Y. Shchori, and J. Ben-Jaacov. 1997. "Cutting grafts" for Leucospermum and Leucadendron-a method for quick propagation by simultaneous rooting and grafting. Acta Hort. 453:15-27. Ackerman, A, Y. Shchori, S. Gilad, B. Mitchnik, K. Pinta, and J. Ben-Jaacov. 1995. Development of Leucospermum tolerant to calcareous soils for the protea industry. J. Int. Protea Assoc. 29:24-29. Allemand, P., M. Montarone, and R. Brun. 1995. Problems in soilless greenhouse cultivation of Proteaceae in French Mediterranean region. Acta Hort. 408:63-71. Asper, H., Sr. 1984. Propagation of proteas. Proc. Int. Plant Prop. Soc. 34:168-169. Ben-Jaacov, J. 1986. Protea production in Israel. Acta Hort. 185:101-110. Ben-Jaacov, J., A Ackerman, S. Gilad, R. Carmeli, and A. Barzilay. 1990. Development of Leucospermum as potted plant-control of vegetative growth with paclobutrazol on L. 'Tomer'. Intern. Workshop on intensive protea cultivation, Neve-Han, Israel, Sept. 1990. (Abstr.) Ben-Jaacov, J., A. Ackerman, S. Gilad, and Y. Shchori. 1989. New approaches to the development of proteaceous plants as floricultural commodities. Acta Hort. 252:193-199.

82

R. CRILEY

Ben-Jaacov, J., and G. Jacobs. 1986. Establishing Protea, Leucospermum, and Serruria in vitro. Acta Hort. 185:39-52. Benic, 1., and P. S. Knox-Davies. 1983. Scab of Leucospermum cordifohum and other Proteaceae caused by an Elsinoe species. Phytophylactica 15:95-107. Blake, G. J. 1987. Peat or bark or folklore. J. Int. Protea Assoc. 13:45-48. Blandy, A. 1996. Area reports to the 8th Biennial IPA Conference, Israel, March 1996. 4. Madeira. J. Int. Protea Assoc. 31:11-12. Bowden, A. 1987. Application of phosphorus to proteaceous plants. Proc. Int. Plant Prop. Soc. 37:138-141. Brits, G. J. 1977. Manipulation of flowering time in Leucospermum cordifolium with ethephon. Agroplantae 9:127-130. Brits, G. J. 1978. Genetic and cultural improvement of Leucospermum cordifolium (Proteaceae). Proc. XXth Int. Hort. Congr. (Australia) Abstr. 1877. Brits, G. J. 1984a. South African proteas historical review. Protea News 1:7-9. Brits, G. J. 1984b. Protea production in the United States of America. Protea News 1:10-11. Brits, G. J. 1985a. International cultivar registration system and checklist. Protea News 2:3-8. Brits, G. J. 1985b. The influence of genotype, terminality, method of auxin application, and temperature on the rooting of Leucospermum cuttings. Acta Hort. 185:23-30. Brits, G. J. 1986a. Influence of fluctuating temperatures and H20 2 treatment on germination of Leucospermum cordifolium and Serruriaflorida (Proteaceae) seeds. S. Afr. J. Bot. 52:286-290. Brits, G. J. 1986b. The effect of hydrogen peroxide treatment on germination in proteaceae species with serotinous and nut-like achenes. S. Afr. J. Bot. 52:291-293. Brits, G. J. 1986c. Horticultural and ecological aspects of seed germination in Leucospermum cordifohum (Proteaceae). M.S. Thesis, Univ. Stellenbosch, Stellenbosch, RSA. (Abstracted in Protea News 5:9-10.) Brits, G. J. 1986d. The influence of genotype, terminality and auxin formulation on the rooting of Leucospermum cuttings. Acta Hort. 185:23-30. Brits, G. J. 1986e. Extension of harvesting period in Leucospermum by means of manual and chemical pruning methods. Acta Hort. 185:237-240. Brits, G. J. 1987. Germination depth vs. temperature requirements in naturally dispersed seeds of Leucospermum cordifohum and 1. cuneiforme (Proteaceae). S. Afr. J. Bot. 53:119-124. Brits, G. J. 1990a. Protea pot plants are the latest. J. Int. Protea Assoc. 19:10-11. Brits, G. J. 1990b. Rootstock production research in Leucospermum and Protea: 1. Techniques. Acta Hort. 264:9-25. Brits, G. J. 1990c. Rootstock production research in Leucospermum and Protea: II. Gene sources. Acta Hort. 264:27-40. Brits, G. J. 1990d. Techniques for maximal seed germination of six commercial Leucospermum R.Br. species. Acta Hort. 264:53-60. Brits, G. J. 1991. Improvement of seed germination in pincushion proteas. J. Int. Protea Assoc. 21:67. Brits, G. J. 1992a. Breeding programmes for Proteaceae cultivar development. Acta Hort. 316:9-18. Brits, G. J. 1992b. The VOPI diversifies its protea cultivar releases. J. Int. Protea Assoc. 24:19-25. Brits, G. J. 1995a. Selection criteria for protea flowering potted plants. Acta Hart. 387:47-54. Brits, G. J. 1995b. Leucospermum budding in South Africa gets underway. J. Int. Protea Assoc. 29:23-24.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

83

Brits, G. J. 1995c. IPA workshop report on problems of protea growing and IPA panel discussion. Introduction to the workshop. J. Int. Protea Assoc. 29:8-9. Brits, G. J., N. A. C. Brown, and J. Van Staden. 1997. Eco-hormonal and structural aspects of the complex seed dormancy in Leucospermum RBr. (Proteaceae) in fynbos. Austral. J. Bot. (in press). Brits, G. ]., F.]. Calitz, N. A. C. Brown, and]. C. Manning. 1993. Desiccation as the active principle in heat-stimulated seed germination of Leucospermum R Br. (Proteaceae) in fynbos.New Phytol. 125:397-403. Brits, G. ]., J. G. M. Cutting, N. A. C. Brown, and J. Van Staden. 1995. Environmental and hormonal regulation of seed dormancy and germination in Cape fynbos Leucospermum RBr. (Proteaceae) species. Plant Growth Reg. 17:181-193. Brits, G. J., G. Jacobs, and J. C. Steenkamp. 1986. The pruning of proteas for cut flower production. Protea News 4:9-16. Reprinted from Pamphlet Series Flowers and Ornamental Shrubs B.15, 1986. Dept. Agr. Water Supply, Pretoria, S. Afr. Brits, G. ]., G. Jacobs, and M. M. Vogts. 1983. Domestication offynbos Proteaceae as a floricultural crop. Bothallia 14:641-646. Brits, G. ]., E. TaL]. Ben-Jaacov, and A. Ackerman. 1992. Cooperative production of protea flowering pot plants selected for rapid production. Acta Hort. 316:107-118. Brits, G. ]., and G. C. van den Berg. 1991. Interspecific hybridization in Pratea, Leucospermum, and Leucadendron (Proteaceae). Protea News 10:12-13. Brits, G. T., and M. N. Van Niekerk. 1976. Breaking of seed dormancy in Leucospermum cordifolium (Proteaceae). Agroplantae 8:91-94. Brits, G. ]., and M. N. Van Nierkerk. 1986. Effects of air temperature, oxygenating treatments, and low storage temperature on seasonal germination responses of Leucospermum cordifolium (Proteaceae) seeds. S. Afr. ]. Bot. 52:207-211. Brown, N. A. c., and ]. Van Staden. 1973. Studies on the regulation of seed germination in the South African Proteaceae. Agroplantae 5:111-116. Brown, N. A. c., ]. Van Staden, and G. Jacobs. 1986. Germination of achenes of Leucospermum cordifolium. Acta Hort. 185:53-59. Calo, 1. 1986. Growing proteas in artificial media in Israel. J. Int. Protea Assoc. 10:2-3. Cho, ]. J. 1977. Shoot and flower blight of Leucospermum cordifolium incited by a benomyl-tolerant strain of Botrytis cinerea. Phytopathology 67:124-127. Cho, J. J., and W. ]. Apt. 1977. Susceptibility of proteas to Meloidogyne incognita. Plant Dis. Rptr. 61:489-492. Cho,]. ]., W.]. Apt, and O. V. Holtzmann. 1976. The occurrence of Meloidogyne incognita on members of the Proteaceae family in Hawaii. Plant Dis. Rptr. 60:814-817. Claassens, A. S. 1986. Some aspects of the nutrition of proteas. Acta Hort. 185:171-179. Coetzee, ]. H. 1987a. Control of protea insects in the summer rainfall regions. ]. Int. Protea Assoc. 11:21-24. Coetzee, ]. H. 1987b. Control of protea flower insects and mites. ]. Int. Protea Assoc. 11:24-27. Coetzee,]. H., and J. H. Giliomee. 1987. Seed predation and survival in the infructescences of Pratea repens (1.) (Proteaceae) in the western Cape. S. Afr. J. Bot. 53:61-64. Criley, R A., P. E. Parvin, and S. Lekawatana. 1990. Flower development in Leucospermum cordifolium 'Vlam' Acta Hort. 264:61-70. Criley, R A., P. E. Parvin, and C. Williamson. 1978a. Keeping quality of Leucospermum cordifolium. First Ann. Om. Sem. Proc. Univ. Hawaii, CES Misc. Publ. 172:34-36. Criley, R A., C. Williamson, and R. Masutani. 1978b. Vaselife determination for Leucospermum cordifolium. Flor. Rev. 163(4228):37-38,80-81. Dai, J., and R. E. Paull. 1995. Source-sink relationship and Pratea postharvest leaf blackening. J. Am. Soc. Hort. Sci. 120:475-480.

84

R. CRILEY

DeFrank, J. 1990. Systems of weed control in protea. Proc. Third Fert. and am. Short Course. Coop. Ext. Servo ColI. Trop. Agr. Human Resources, Univ. Hawaii. HITAHR 01.01.90. p. 94-95. DeFrank, J., and F. D. Rauch. 1988. Weed control strategies for Hawaiian grown protea. Hort. Dig. (Hawaii) 88:5-9. Dixon, K. 1987. Proteaceae of western Australia. Proc. 4th IntI. Protea Conf. Proteaflora Enterprises, Melbourne, Australia. p. 59-72. Downs, c., and M. Reihana. 1986. The quality of Leucospermum cultivars after simulated transport. J. Int. Protea Assoc. 10:5-8. Dupee, S. A., and P. B. Goodwin. 1990. Effect of temperature, daylength and growth regulators on flowering in Pratea, Telopea, and Leucospermum. Acta Hort. 264:79-86. Flower Export Council of Australia. 1992. Draft copy of standards for fresh cut flowers. Austral. Protea Grower 4(2). (Cited in J. lnt. Protea Assoc. 24:16-18.) Forsberg, L. 1993. Protea diseases and their control. Dept. Primary Ind., Brisbane, QLD, Australia. Forsyth, T. 1992. The marketing of proteas in Australia. J. lnt. Protea Assoc. 22:13-18. Furuta, T. 1983. Protea culture. Univ. Calif. Coop. Ext. Servo Leaflet 21333. Grierson, P. F., and P. M. Attiwill. 1989. Chemical characteristics of the proteoid root mat of Banksia integrifolia L. Austral. J. Bot. 37:137-143. Haasbroek, F. J., G. G. Rousseau, and J. F. de Villiers. 1973. Effect of gamma rays on cut blooms of Pratea compacta R. Br., Protea longiflora Lamarck and Leucospermum cordifolium Salisb. ex Knight. Agroplantae 5:33-42. Hanekon, A. N., J. Diest, and K. L. J. Blommaert. 1973. Seasonal uptake of 32phosphorus and 86rubidium by Protea cynaraides. Agroplantae 5:107-110. Harre, J. 1986. Propagation of South African Proteaceae by seed. Proc. lnt. Plant Prop. Soc. 36:470-476. Harre, J. 1988a. Proteaceae propagation. J. Int. Protea Assoc. 14:23-33. Harre, J. 1988b. Proteas, the propagation and production of Proteaceae. Riverlea Promotions, Feilding, NZ. Harre, J. 1989. Delayed propagation technique. Protea News 8:2-3. Harre, J. 1991. Profit from proteas. Riverlea Nurseries, Feilding, NZ. Harre, J. 1992. Zimbabwe. J. lnt. Protea Assoc. 22:6. Harre, J. 1995. Protea growers handbook. Riverlea Nurseries, Feilding, NZ. Hawaii Agricultural Statistics Service. 1997. Hawaii flowers and nursery products. Annual summary. Haw. Dept. Agr., Honolulu, HI. Hawaii Department of Agriculture. 1980. Proposed standards for protea cut flowers. Section 4-42-36. Haw. Dept. Agr., Honolulu, HI. Horn, W. 1962. Breeding research on South African plants. II. Fertility of Proteaceae. J. S. Afr. Bot. 28:259-268. Int. Registration Authority: Proteas. 1997. The international protea register. 4th Ed. Elsenburg, S. Afr. Ito, P. J., K. W. Leonhardt, P. E. Parvin, T. Murakami, and D. W. aka. 1991. New hybrid Leucospermum (Proteaceae) introductions. The Hawaii Tropical Cut Flower Industry Conference March 29-31, 1990. ColI. Trop. Agr. & Human Resources, Univ. Hawaii, Res.-Ext. Ser. 124:164-165. Ito, P. r., T. Murakami. D. aka, and P. E. Parvin. 1990. New protea hybrids developed by breeding. p. 91-92. Proc. Third Fert. and am. Short Course. Coop. Ext. Servo ColI. Trop. Agr. Human Resources, Univ. Hawaii. HITAHR 01.01.90. Ito, P. r., T. Murakami, and P. E. Parvin. 1978. Protea improvement by breeding. First Ann. Om. Sem. Proc. Coop. Ext. Servo ColI. Trop. Agr. Human Resources, Univ. Hawaii. Misc. Pub. 172:1-4.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

85

Ito, P. J., T. Murakami, and P. E. Parvin. 1979. New Leucospermum hybrids. Seventh Ann. Protea Workshop Proc. Coop. Ext. Servo ColI. Trop. Agr. Human Resources, Univ. Hawaii. Misc. Pub. 176:1-4. Jacobs, G. 1976. Proteaceae-production planning for the export market. SAPPEX News!' 14: 23-26. Jacobs, G. 1980. Aspects of flower initiation and development of pincushion Leucospermum cv. Red Sunset. Crop. Prod. 9:175-177. Jacobs, G. 1983. Flower initiation and development in Leucospermum cv. Red Sunset. J. Am. Soc. Hort. Sci. 108:32-35. Jacobs, G. 1985. Leucospermum. p. 283-286. In: A. H. Halevy (ed.), Handbook of flowering. CRC Press, Boca Raton, FL. Jacobs, G., and G. E. Honeyborne. 1978. Delaying flowering time of Leucospermum cv. Golden Star by deheading. Agroplantae 10:13-15. Jacobs. G., and G. E. Honeyborne. 1979. The relationship between heat unit accumulation and the flowering date of Leucospermum cv. Golden Star. Agroplantae 11:83-85. Jacobs. G., and H. R. Minnaar. 1980. Light intensity and flower development of Leucospermum cordi/olium. HortScience 15:644-645. Jacobs, G., D. R. Napier. and D. G. Malan. 1986. Prospects of delaying flowering time of Leucospermum. Acta Hort. 185:61-65. Jacobs, G.. and J. C. Steenkamp. 1976. Rooting of stem cuttings of Leucospermum cordifolium and some of its hybrids under mist. Farming in South Africa Ser.: Flowers, Ornamental Shrubs, and Trees, B.7. Jones. R, and J. Faragher. 1990. The viability of transporting selected cutflower species by seafreight. J. Int. Protea Assoc. 19:43-44. Jones, R B.• R. McConchie, W. G. van Doorn, and M. S. Reid. 1995. Leaf blackening in cut Pratea flowers. Hort. Rev. 17: 173-201. Jongens-Roberts, S. M., and D. T. Mitchell. 1986. The distribution of dry mass and phosphorus in an evergreen fynbos shrub species, Leucospermum pariJe (Salisb. ex J. Knight) Sweet (Proteaceae), at different stages of development. New Phytol. 103:669683. Joyce, D. C., P. Beal, and A. J. Shorter. 1997. Vase life characteristics of selected Grevillea genotypes. J. Int. Protea Assoc. 33:23-28. Kent. H. 1989. Pincushion leaf spot and blight. J. Int. Protea Assoc. 17:15-19. Knight, J. 1809. On the cultivation of the plants belonging to the natural order ofProteeae, with their generic as well as specific characters and places where they grow wild. William Savage. London. Knox-Davies, P. S. 1988. Report on protea disease survey in Zimbabwe. J. Int. Protea Assoc. 16:55-56. Knox-Davies, P. S., P. S. van Wyk, and W. F. O. Marasas. 1988. Diseases of proteas and their control in the south eastern cape. J. Int. Protea Assoc. 16:50-54. Koike. S. T., J. H. Nelson, and D. K Perry. 1991. Verticillium wilt of protea (Leucospermum cordifolium) caused by V. dahliae. Protea News 12:11. Kunisaki, J. T. 1989. In vitro propagation of Leucospermum hybrid. 'Hawaii Gold.' HortScience 24:686-687. Kunisaki, J. 1990. Micropropagation of Leucospermum. Acta Hort. 264:45-48. Lamont, B. 1985. The comparative reproductive biology of three Leucospermum spp. (Proteaceae) in relation to fire responses and breeding system. Austral. J. Bot. 33:139-145. Lamont, B. 1986. The significance of proteoid roots in proteas. Acta Hort. 185:163-170. Leonhardt. K, S. Ferreira, N. Nagata, D. Oka. J. Kunisaki. P. Ito. and P. Shingaki. 1995. Hybridizing Leucospermum (Proteaceae) for disease resistance and improved horti-

86

R. CRILEY

cultural characteristics. p. 76-77. Proc. Third Multicommodity Cutflower Industry Conf. College Trop. Agr. Human Resources, HITAHR 03.04.95. Littlejohn, G. 1995. The Fynbos genebank project. ]. Int. Protea Assoc. 30:6-7. Littlejohn, G. M., 1. D. van der Walt, G. C. van der Berg, W. G. de Waal, and G. J. Brits. 1995. 'Marketable product' approach to breeding proteaceae in South Africa. Acta Hort. 387:171-175. Malajczuk, N., and G. D. Bowen. 1974. Proteoid roots are microbially induced. Nature 251:316-317. Malan, D. G. 1986. Growth and development of Leucospermum. M.Sc. thesis, Univ. of Stellenbosch, Stellenbosch, RSA. Malan, D. G. 1990. Rooting and graft compatibility of hybrid Leucospermum cuttings. J. Int. Protea Assoc. 20:65-66. Malan, D. G. 1992. Propagation of Proteaceae. Acta Hort. 316:27-34. Malan, D. G. 1995. Crop science of Proteaceae in southern Africa: Progress and challenges. Acta Hort. 387:55-62. Malan, D. G. 1996. Fertilizing proteas.]. Int. Protea Assoc. 31:32-33. Malan, D. G., 1997. Report from South Africa-Status of industry development.]. Int. Protea Assoc. 34:29-35. Malan, D. G., J. G. M. Cutting, and G. Jacobs. 1994a. Correlative inhibition of inflorescence development in Leucospermum 'Red Sunset.' J. S. Afr. Soc. Hort. Sci. 4:26-31. Malan, D. G., J. G. M. Cutting, and G. Jacobs. 1994b. The role of the developing inflorescence in the loss of responsiveness to flower inducing short days in Leucospermum 'Red Sunset.' J. S. Afr. Soc. Hort. Sci. 4:32-36. Malan, D. G., J. G. M. Cutting, and G. Jacobs. 1994c. Inflorescence development in Leucospermum 'Red Sunset': effect of benzyladenine and changes in endogenous cytokinin concentrations. J. S. Afr. Soc. Hort. Sci. 4:37-41. Malan, D. G., and G. Jacobs. 1987. The influence of photoperiod on flower induction of Leucospermum cv. Red Sunset. Protea News 6:12-13. Malan, D. G., and G. Jacobs. 1990. Effect of photoperiod and shoot decapitation on flowering of Leucospermum 'Red Sunset.' ]. Am. Soc. Hort. Sci. 115:131-135. Malan, D. G., and G. Jacobs. 1992. Effect of gibberellic acid on shoot growth of Leucospermum R. Br. Acta Hort. 316:99-105. Malan, D. G.• and G. Jacobs. 1994. Influence of day length. irrigation and pruning on shoot growth of Leucospermum 'Red Sunset.' J. S. Afr. Soc. Hort. Sci. 4:24-25. Malan, D. G., and R. D. Ie Roux. 1997. Disbudding Leucospermum for better crop distribution. J. Int. Protea. Assoc. 33:17-18. Manning. J. C., and G. J. Brits. 1993. Seed coat development in Leucospermum cordifolium (Knight) Fourcade (Proteaceae) and a clarification of the seed covering structures in Proteaceae. Bot. J. Linn. Soc. 112:139-148. Marks, G. C.. and L. W. Smith. 1989. Effect of foliar applications on Phytophthora Ginnamomi root and stem infection. J. Int. Protea Assoc. 17:20-23. Matthews, A. 1993. Protea stock plant nutrition. Proc. Int. Plant Prop. Soc. 43:48-54. Matthews, D. 1988. Pincushion scab disease-a follow up. J. Int. Protea Assoc. 16:48. Matthews. D., and A. Matthews. 1994. Proteas: an Australian growers guide. Proteaflora Enterprises Pty Ltd., Monbulk, Australia. Matthews, J. W. 1921. The cultivation of Proteas and their allies. J. Bot. Soc. S. Afr. 7:15-16. Matthews, L. J. 1982. Culture of Proteaceae. p. 27-33. In: Fourth Proc. Flower Growers' Seminar (Nelson). J. P. Salinger (ed.), Dept. Hort. and Plant Health, Massey University, Palmerston North, NZ.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

87

Matthews, L. J. 1993. The protea growers handbook for New Zealanders. David Bateman Ltd., Auckland, New Zealand. Matthews, 1. J., and Z. Carter. 1993. Proteas of the world. Timber Press, Portland, OR Maughan, J. 1986. Post harvest treatments of protea cut flowers to eradicate arthropods. ]. Int. Protea Assoc. 10:10-13. McKenzie, B. 1. 1973. Propagation of Proteaceae by cuttings. Proc. Int. Plant Prop. Soc. 23:380. McLennan, R 1993. Growing proteas. Kangaroo Press Pty Ltd., Kenthurst, NSW, Australia. Meltzer, C. 1992. Protea production in Israel. J. Int. Protea Assoc. 22:10-12. Moffat, J., and 1. Turnbull. 1993. Grafting proteas. Publ. by the author: Nanju Protea Nursery, Mail centre 582, Toowoomba, QLD 4352, Australia. Moffat, J., and 1. Turnbull. 1994. Production of Phytophthora tolerant rootstocks: II. Grafting compatibility studies and field testing of grafted proteas. J. Int. Protea Assoc. 27:14-22. Montarone, M., and P. Allemand. 1995. Growing Proteaceae soilless under shelter. Acta Hort. 387:73-83. Munro, R J. 1990. Feeding phosphate to proteas. J. Int. Protea Assoc. 19:48-49. Nagata, N. M., and S. Ferreira. 1991. Survey of Protea diseases in Hawaii. Univ. Hawaii, Maui Agr. Res. Ctr., Protea Disease Letter 1(1):1-4. Nagata, N. M., and S. Ferreira. 1993. The Protea Disease Letter 2:1-5. Univ. Hawaii, Maui Agr. Res. Ctr. Napier, D. R 1985. Initiation, growth, and development of Leucospermum cv. Red Sunset inflorescences. M.Sc. thesis. Univ. Stellenbosch, Stellenbosch, South Africa. Napier, D. R, and G. Jacobs. 1989. Growth regulators and shading reduce flowering of Leucospermum cv. Red Sunset. HortScience 24:966-968. Napier, D. R, G. Jacobs, J. van Staden, and C. Forsyth. 1986a. Cytokinins and flower development in Leucospermum. J. Am. Soc. Hort. Sci. 111:776-780. Napier, D. R, D. Malan, G. Jacobs, and J. W. Bernitz. 1986b. Improving stem length and flower quality of Leu cosperm um with growth regulators. Acta Hort. 185:67-73. Nichols, D. 1981. The phosphorus nutrition of proteas. First Int. Conf. Protea Growers. Proteaflora Enterprises Pty Ltd., Melbourne, Australia. Nishimoto, R K. 1975. Weed control in established Proteaceae with soil residual herbicides. Proc. Fourth Protea Workshop. Univ. Hawaii Coop Ext. Servo Misc. Publ. 139:4-12. Parvin, P. E. 1974. Project: Proteas-Hawaii. Proc. Int. Plant Prop. Soc. 24:41-42. Parvin, P. E. 1978. The influence of preservative solutions on bud opening and vase life of selected Proteaceae. Proc. 1st Ann. Orn. Sem. UHCES Misc. Publ. 173:29-33. Parvin, P. E. 1982. Comparison of rooting materials on Leucospermum cuttings. Proc. Int. Plant Prop. Soc. 32:336-338. Parvin, P. E. 1986. Use of tissue and soil samples to establish nutritional standards in Protea. Acta Hort. 186:145-153. Parvin, P. E. 1991a. Potential cut flower, cut foliage production of Australian and South African flora in Florida. Proc. Fla. State Hort. Soc. 104:296-298. Parvin, P. E. 1991b. Trends, the decade ahead. p. 137-142. In: Proc. Sixth Biennial Conf. Int. Protea Assoc. Int. Protea Assoc., Monbulk, Australia. Parvin, R E., R A. CrHey, and R M. Bullock. 1973. Proteas: developmental research for a new cut flower crop. HortScience 8:299-303. Parvin, P. E., and K. W. Leonhardt. 1982. Care and handling of cut protea flowers. Proc. 8th and 9th Ann. Protea Workshop. Univ. Hawaii, HITAHR Res.-Ext. Ser 018:20-23. Perold, G. W. 1984. Phenolic lactones as chemotaxonomic indicators in the genera Leucodendron and Leucospermum (Proteaceae). S. Afr. J. Bot. 3:103.

88

R. CRILEY

Perold, G. W. 1987. Chemical contribution to the taxonomy of the Proteaceae in South Africa. Protea News. 6:3-4. Perold, G. W. 1988. Variability of phenolic metabolites in some Leucospermum spp. and hybrids. Protea News 8:5-6. Perry, D. K. 1987. Successfully growing Proteaceae. Proc. Int. Plant Prop. Soc. 37:112-115. Purnell, H. M. 1960. Studies on the family Proteaceae I. Anatomy and morphology of the roots of some Victorian species. Austrl. ]. Bot. 8:38-50. Rebelo, A. G. 1995. SASOL Proteas: A field guide to the Proteas of Southern Africa. Fernwood Press, Vlaeberg, S. Afr. Rebelo, A. G., and J. P. Rourke. 1986. Seed germination and seed set in South African Proteaceae: ecological determinants and horticultural problems. Acta Hort. 185:75-88. Riverlea Nurseries, (undated). Complete master catalogue and cultural guide of Proteaceae. Riverlea Nursies, P.O. Box 69, Feilding, NZ. Rodriguez-Perez,]. A. 1992. Propagation by leaf bud cuttings of Leucadendron 'Safari Sunset', Leucospermum cordifolium, Leucospermum patersonii, and Protea obtusifolia. Acta Hort. 316:35-45. Rodriguez-Perez, J. A. 1993. Effects of treatments with hydrogen peroxide, gibberellic acid and both products in sequence on germination of Leucospermum cuneiforme and 1. tottum (Proteaceae). rSpanish] Actas del II Congreso Iberico de Ciencias Horticolas, Saragoza Spain. April 1993:559-564. Rourke,]. P. 1972. Taxonomic studies on Leucospermum R. Br. S. Afr.]. Bot. (Suppl.) 8:1-194. Rourke, ]. P. 1980. The Proteas of South Africa. Purnell & Sons (S.A.) Pty Ltd., Cape Town, Rep. S. Afr. Rourke, ]. P. 1997. The systematics of the African Proteaceae. J. Int. Protea Assoc. 33:20. (Abstr.) Rousseau, G. G. 1966. Proteas can be grafted. Farming in S. Afr. 42(6):53-55. Rousseau, G. G. 1968. Propagation of Proteaceae from cuttings. Fruit and Food Technology Inst., Pretoria, South Africa. Dept. Agr. Tech. Serv., Tech. Comm. 70. Rugge, B. A., G. Jacobs, and K. I. Theron. 1990. Factors affecting bud sprouting in multinodal stem segments of Leucospermum cv. Red Sunset in vitro. J. Hort. Sci. 65:55-58. Sacks, P. V., and I. Resendiz. 1996. Protea pot plants: production, distribution and sales in Southern California. J. Int. Protea Assoc. 31:34. Salinger, J. P. 1985. Commercial flower growing. Butterworth of New Zealand, Wellington, NZ. Sanford, W. G. 1978. Response of pincushion protea to nitrogen, phosphorus, and potassium fertilizers. First Ann. Orn. Sem. Proc. Coop. Ext. Servo Call. Trop. Agr. Human Resources, Univ. Hawaii. Misc. Pub. 172:21-28. SAPPEX. 1990. Meaning of scientific names: 2. Leucospermum. J. Int. Protea Assoc. 20:85. Seaton, K. A., and D. C. Joyce. 1992. Effects of low temperature and elevated CO 2 and of heat treatments for insect disinfestation of some native Australian cut flowers. Scientia Hort. 52:343-355. Seaton, K. A., and D. C. Joyce. 1993. Gamma irradiation for insect disinfestation damages native Australian cut flowers. Scientia Hart. 56:119-133. Seaton, K. A., and W. M. Woods. 1991. Review of field and postharvest control of insects in Proteaceae. p. 67-76. Proc. 6th Biennial Conf. Int. Protea Assoc. Int. Protea Assoc., Monbulk, Australia. Sedgley, M. 1998. Developmental research for Proteaceous cut flower crops: Banksia. Hort. Rev. 22:1-22. Shchori, Y., T. Goern, and J. Ben-Jaacov. 1992. Pollen germination and storage in Banksia and some other proteaceae plants. Acta. Hart. 316:19-22.

2. LEUCOSPERMUM: BOTANY AND HORTICULTURE

89

Shchori, Y., J. Ben-Jaacov, A. Ackerman, S. Gilad, and B. Metchnik. 1995. Horticultural characters of intraspecific hybrids of Leucospermum patersonii x 1. conocarpodendron. J. Int. Protea Assoc. 30:10-12. Smith, A. J., and J. H. Jooste. 1986. Phosphate absorption by excised ordinary and proteoid roots of Protea compacta R. Br. S. Afr. J. Bot. 52:549-551. Steenkamp, K. 1993. Protea production at Protea Heights, Stellenbosch, SA. J. Int. Protea Assoc. 26:30-31. Tal, E., H. Solomon, J. Ben-Jaacov, and A. A. Watad. 1992a. Micropropagation of selected Leucospermum cordifolium: effect of antibiotics and GA3. Acta Hort. 316:55-58. Tal, E., J. Ben-Jaacov, and A. A. Watad. 1992b. Hardening and in vivo establishment of micropropagated GreviJIea and Leucospermum. Acta Hort. 316:63-67. Turnbull, L. V. 1997. Some statistics on the production of Proteaceae in Australia. J. Int. Protea Assoc. 34:10. Turnbull, L. V., and 1. R. Crees. 1995. Field studies on the effectiveness of phosphonate suppression of Phytophthora root rot in proteas. J. Int. Protea Assoc. 30:18-27. Turnbull, L. V., H. J. Ogle, and P. J. Dart. 1989. Biological control of Phytophthora cinnamomi in proteas. J. Int. Protea Assoc. 18:26-29. Van der Merwe, P. 1985. The genetic relationship between the South African Proteacea [sic]. Protea News 3:3-5. Van der Merwe, E. K., D. C. de Swardt, J. F. Ferreira, and G. J. Brits. 1991. Evaluation of a Leucospermum tottum x 1. formosum hybrid as Phytophthora cinnamomi tolerant rootstock. Protea News 11:15-17. Van Staden, J., and C. J. Bornman. 1976. Initiation and growth of Leucospermum cordifolium callus. J. s. Afr. Bot. 42:17-23. Van Staden, J., and N. A. C. Brown. 1973. The role of covering structures in the germination of seed of Leucospermum cordifolium (Proteaceae). Austral. J. Bot. 21:189-192. Van Staden, J., and N. A. C. Brown. 1977. Studies on the germination of South African Proteaceae: a review. Seed Sci. Technol. 5:633-643. Van Vuuren, P. J. 1995. New ornamental crops in South Africa. Acta Hort. 397:71-84. Venkata Rao, C. V. 1971. Proteaceae. Bot. Monogr. No.6. Council of Scientific and Industrial Research, New Delhi, India. Vogts, M. M. 1958. Proteas, know them and grow them. Afrikaanse pers-Boeklandel BPK, Johannesburg. Vogts, M. M. 1960. The South African Proteaceae: the need for more research. S. Afr. J. Sci. 56:297-305. Vogts, M. M. 1962. The cultivation of the Proteaceae. J. Bot. Soc. S. Afr. 48:8-11. Vogts, M. M. 1979. Proteas: intensive cut-flower cultivation. Leucospermum species. Farming in S. Afr. Ser.: Flowers and Ornamental Shrubs. B.12. Vogts, M. M. 1980. Species and variants of protea. Farming in South Africa Ser.: Flowers and Ornamental Shrubs B.1. Dept. Agr. Water Supply. Vogts, M. M. 1982. South Africa's Proteaceae, know them and grow them. C. Struik Pty Ltd., Cape Town. Vogts, M. M., K. J. 1. Blommart, 1. Ginsburg, J. T. Meynhardt, A. C. Myburgh, G. G. Rousseau, D. J. Rust, G. Schliemann, W. F. S. Schwabe, and J. H. Terblanche. 1972. F.F.T.R.I. Information bulletin series on the commercial cultivation of proteas. Dept. Agr. Fish., Fruit, Fruit. Technol. Res. Inst. Bulletin nos 8, 18, 24, 28, 34,45,76,86,89, 98. Vogts, M. M., G. G. Rousseau, and K. L. J. Blomrnart. 1976. Propagation of proteas. Farming in South Africa Ser.: Flowers, Ornamental Shrubs, and Trees, B.2. Dept. Agr. Water Supply.

90

R. CRILEY

Von Broembsen, S. L. 1985. Dreschlera blight of pincushions in South Africa. Protea News 3:27. Von Broembsen, S. 1. 1986. Blight of pincushions (Leucospermum spp.) caused by Dreschlera dematioidea. Plant Dis. 70:33-36. Von Broembsen, S. 1989. Handbook of diseases of cut-flower proteas. Int. Protea Assoc., Monbulk, Victoria, Australia. Von Broembsen, S. 1., and G. J. Brits. 1985. Control of root rot of proteas in South Africa. Protea News 3:19. Von Broembsen, S. 1., and G. J. Brits. 1990. Evaluation of the resistance of pincushion (Leucospermum spp.) breeding lines to root rot caused by Phytophthora Ginnamomi. Acta Hort. 264:115-121. Von Broembsen, S. 1.., and J. A. Van der Merwe. 1985. Control of Botryosphaeria canker and die-back of proteas in South Africa. Protea News 3:27. Vorster, P. W., and J. H. Jooste. 1986a. Potassium and phosphate absorption by excised ordinary and proteoid roots of the Proteaceae. S. Afr. J. Bot. 52:277-281. Vorster, P. W., and J. H. Jooste. 1986b. Translocation of potassium and phosphate from ordinary and proteoid roots to shoots in the Proteaceae. S. Afr. J. Bot. 52:282-285. Wallerstein, 1. 1989. Sequential photoperiodic requirement for flower initiation and development of Leucospermum patersonii (Proteaceae). Israel J. Bot. 38:24-34. Wallerstein, 1., and A. Nissim. 1988. Flowering control in Leucospermum patersonii [in Hebrew]. Hassadeh 64:714-717. Watson, D. P., and P. E. Parvin. 1970. Culture of ornamental proteas. Univ. Hawaii., Haw. Agr. Expt. Sta. Res. Bui. 147. Witkowski, E. T. F. 1989. Nutrient limitation of inflorescence production of Leucospermum parile in Cape fynbos. Protea News 8:10. Witkowski, E. T. F., D. T. Mitchell, and W. D. Stock. 1990. Response of a cape fynbos ecosystem to nutrient additions: shoot growth and nutrient contents of a proteiod (Leucospermum parile) and an ericoid (Phylica cephalanthe) evergreen shrub. Acta Oecologia 11:311-326. Wood, P. 1987. Results of initial tests with potassium dihydrogen phosphite against P. Ginnamomi. J. Int. Protea Assoc. 13:29-30. Wright, M. G. 1992. Disinsectation of fynbos cut flowers and greens-a progress report to the South African Protea Producers and Exporters Association. SAPPEX News 76:8-10. Wright, M. G. 1995. Integrated pest management-concepts and potential for the control of borers on proteas. Acta Hort. 387:153-157. Wright, M. G., and J. H. Coetzee. 1992. An improved technique for disinsectation of Pratea cut flowers. J. S. Afr. Soc. Hort. Sci. 2:92-93. Wu, I.-P., J. J. Cho, and P. E. Parvin. 1978. Response of Sunburst protea to irrigation inputs and root knot nematode infections. First Ann. Om. Sem, Proc. Coop. Ext. Servo ColI. Trop. Agr. Human Resources, Univ. Hawaii. Misc. Pub. 172:16-20. Yoshimoto, S. 1982. A progress report on protea research. Proc. 8th and 9th Ann. Protea Workshop. Univ. Hawaii, HITAHR, Res.-Ext. Ser 018:1-5.

3 Postharvest Heat Treatments of Horticultural Crops* Susan Lurie Department of Postharvest Science ARO, The Volcani Center Bet Dagan, Israel

I. Introduction II. Heat Treatments A. Hot Water Dips and Sprays B. Vapor Heat C. Hot Air III. Commodity Responses A. Fruit Ripening B. Thermotolerance C. Tolerance to Chilling Injury D. Heat Damage IV. Fungal Pathogen Response A. Sensitivity of Different Growth Stages B. Host-pathogen Interactions: Defense Reactions of the Host V. Insect Response A. Effect on Insect Life Stages B. Probit 9 or Not C. Thermotolerance: Combined Treatments VI. Conclusions Literature Cited

*The ideas expressed and experience reflected in this review are the result of research partially funded by the United States-Israel Binational Research Development Authority, the United States Cooperative Development Foundation, and the Ministry of Economic Cooperation of Germany. This is a contribution from the Agricultural Research Organization. The Volcani Center, Bet Dagan, Israel No. 2061-E, 1997.

Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 91

92

S. LURIE

I. INTRODUCTION

In a time of increased awareness among consumers that many of the chemical treatments of fruits and vegetables to control insects, diseases, and physiological disorders are potentially harmful to humans, there is a need to develop effective, non-damaging physical treatments for insect disinfestation and disease control in fresh horticultural products. High or low temperature treatments, anoxia, and irradiation are some of the possibilities being explored. This review will discuss in detail the methods being employed for high temperature treatments and their effects both on the commodities treated and on pathogens and insects of these commodities. High temperature treatments are being very actively pursued for postharvest treatments of fresh produce, to control both insect pests and fungal pathogens. In part, this is because of the deregistration of a number of chemical treatments that had previously been used for effective control. In addition, there is increased demand for produce that is chemically free, or has had the minimum amount of treatments possible. Heat has fungicidal and as well as insecticidal action, but treatment conditions that are optimal for insect control may not be optimal for disease control, and, in some cases, may even be detrimental. Also, whether a high temperature treatment is developed for fungus or insect control, it should not damage the commodity being treated. This review will discuss the damage that high temperature can cause to commodities, but will also present in detail beneficial responses of commodities to heat treatments. These include the slowing of ripening of climacteric fruit and vegetables, sweetening of commodities, either by increasing sugars or decreasing acidity, and prevention of storage disorders, such as superficial scald on apples and chilling injury on subtropical fruits and vegetables. What is known concerning the mode of action of high temperature on these processes will be described. The effects of high temperature on fungi and insects at different stages of development will also be discussed, and related back to the interrelationship among these three living organisms (plant, fungus, insect) in response to heat. There have been a number of previous reviews of specialized aspects of heat treatments (Paull 1990; Couey 1989; BarkaiGolan and Phillips 1991; Klein and Lurie 1991, 1992a; Coates and Johnson 1993; Paull 1994). This review will try to extend those earlier reviews to provide an overview of the field.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

93

II. HEAT TREATMENTS

A. Hot Water Dips and Sprays There are three methods used to heat commodities: hot water, vapor heat, and forced hot air. Hot water treatment was originally used for fungal control, but its use has been extended to disinfestation of insects. Vapor heat treatment was developed specifically for insect control, while forced hot air has been used for both fungal and insect control and to study the response of commodities to high temperature. Hot water dips have generally been utilized for fungal pathogen control, since fungal spores and latent infections are either on the surface or in the first few cell layers under the peel of the fruit or vegetable. Postharvest dips to control decay are often applied for only a few minutes, and temperatures used are higher than those for hot air or vapor heat because only the surface of the commodity is heated. Many fruits and vegetables tolerate hot water temperatures of so to 60°C for up to 10 min, but shorter exposure at these temperatures can control many postharvest plant pathogens (Barkai-Golan and Phillips 1991). Low concentrations of fungicides can be applied as part of the hot water treatment, thus allowing more effective fungal control with a reduction in chemicals. This has been particularly effective on citrus with the fungicides thiabendazole and imazalil (McDonald et al. 1991; Wild 1993; Schirra and Mulas 1995a, 1995b). In addition, compounds generally recognized as safe (GRAS) have been applied in hot water to improve the efficiency of their antifungal action. Heated solutions (45°C) of sulfur dioxide, ethanol, and sodium carbonate have been used to control green mold (Penicillium digitatum Sacc.) on citrus fruits (Smilanick et al. 1995; Smilanick et al. 1997). These compounds were as effective as imazalil in controlling artificial inoculations of the fungus (Smilanick et al. 1995). A recent innovation in hot water treatment has been the development of a hot water spray machine (Fallik et al. 1996a). This is a technique designed to be part of a sorting line, whereby the commodity is moved by means of brush rollers through a pressurized spray of hot water. By varying the speed of the brushes and the number of nozzles spraying the water, the commodity can be exposed to high temperatures for 10 to 60 sec. The water is recycled, but because of the temperatures used (50 to 70°C), organisms that are washed off the product into the water do not survive. This type of machine is currently used in Israel both to clean and to reduce pathogen presence on a number of fruits and vegetables, such as mangos (Prusky et al. 1997). Packers get a bonus for using the

94

S. LURIE

spray machine on mangoes as well as on melons and corn and it is required for export of these commodities. Hot water dips have been tested for efficacy in disinfesting insects as well (Couey 1989). Hot water is a more efficient heat transfer medium than hot air, and when it is properly circulated through a load of fruit, uniform temperature profile is established. For disinfestation, a longer treatment is necessary than for fungal control, because the total fruit, and not just the surface, has to be brought to the proper temperature. Procedures have been developed to disinfest a number of subtropical and tropical fruits, including bananas (Armstrong 1982), papayas (Couey and Hayes 1986), and mangos (Sharp 1986; Animal and Plant Health Inspection Service 1987; Sharp et al. 1989a, b; Sharp and Picho-Martinez 1990), from various species of fruit fly. In addition, hot water dips are being investigated for insect control in avocados (Jessup 1991), citrus (McGuire 1991), guava (Gould and Sharp 1992), persimmons (Lester et al. 1995; Lay-Yee et al. 1997a), and stone fruit (Sharp 1990; McLaren et al. 1997). The times of immersion can be 1 h or more at temperatures below 50°C, in contrast to many antifungal treatments that require only minutes at temperatures above 50°C. However, for disinfestation of surface insects such as thrips (Thrips obscuratus Crawford), effective times of immersion may be similar to those used for fungal treatments. Stone fruits (apricot, nectarine, and peach) can be cleared of thrips by 2 or 3 min in water at 48 or 50°C (McLaren et al. 1997).

B. Vapor Heat Vapor heat is a method of heating fruit with warm air saturated with water vapor at temperatures between 40 and 50°C to kill insect eggs and larvae as a quarantine treatment before fresh market shipment (APHIS 1985). Heat transfer is by condensation of hot water vapor on the cooler fruit surface. This procedure was first used to kill Mediterranean (Ceratitis capita to Wiedemann) and Mexican (Anastrepha Judens Loew) fruit fly (Baker 1952; Hawkins 1932). However, once ethylene dibromide and methyl bromide came into use as inexpensive chemical fumigants, vapor heat treatment was abandoned. With the ban on use of ethylene dibromide in 1984, and the imminent removal of methyl bromide from use in 2001, vapor heat has again come into use (Gaffney et al. 1990). Commercial facilities operate in many countries, mainly to process subtropical fruits, particularly mango and papaya (Paull 1994). In addition, numerous studies have been conducted to develop a protocol for disinfestation of many fruits and vegetables from various insect pests. The treatment consists of a period of warming (approach time), which

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

95

can be faster or slower depending on a commodity's sensitivity to high temperatures. The warming period is followed by a holding period, when the interior temperature of the produce reaches the desired temperature for the length of time required to kill the insect. The last phase is the cooling period, which can involve air cooling (slow) or hydrocooling (fast). Thus, there are a number of components of the treatment that can be manipulated to find the best combination for elimination of the insect pest without damaging the commodity. Vapor heat treatments have been developed against the oriental fruit fly (Dacus dorsalis Hendel) in papayas (Seo et al. 1974) and green pepper (Sugimoto et al. 1983); against the melon fly (Dacus cucurbitae Coquillet) in eggplant (Furusawa et al. 1984) and mango (Sunagawa et al. 1987); against the Caribbean fruit fly (Anastrepha suspensa Loew) in grapefruit (Hallman et al. 1990) and carambola (Hallman 1990a); and against codling moth (Cydia pomonella L.) in apple and pear (Neven et al. 1996). C. Hot Air Hot air can be applied by placing fruit or vegetables in a heated chamber with a ventilating fan, or by applying forced hot air, during which the speed of air circulation is precisely controlled. This method heats more slowly than hot water or vapor heat, although forced hot air will heat produce faster than a regular heating chamber. The latter method has mainly been utilized to study physiological changes in fruits and vegetables in response to heat (Klein and Lurie 1991; Klein and Lurie 1992a). Forced hot air, however, has been used to develop quarantine procedures (Gaffney and Armstrong 1990). One reason for opting for this method is that the high humidity in vapor heat can sometimes damage the fruit being treated, and the slower heating time and lower humidity with forced hot air cause less damage. A high temperature forced air quarantine treatment to kill Mediterranean fruit fly, melon fly, and oriental fruit fly on papaya has been developed (Armstrong et al. 1989; Hansen et al. 1990). This procedure requires rapid cooling after the heat treatment to prevent fruit injury, as does the forced hot air treatment for citrus (Sharp and Gould 1994; Sharp and McGuire 1996). Recently, the heat treatment for papaya has been modified so that hydrocooling is unnecessary (Armstrong et al. 1995), and this method is under investigation for other commodities, such as persimmon (Dentener et al. 1996). Hot air can also decrease fungal infections. Heating can reduce decay caused by Botrytis cinerea Pers.:Fr. and Penicillium expansum Link in apple fruit (Fallik et al. 1996c; Klein et al. 1997b) and Botrytis cinerea

96

S. LURIE

Pers.:Fr. in tomato (Fallik et al. 1993). The treatments used in these cases are long-term heating, from 12 to 96 h at temperatures ranging from 38 to 46°C, and are unlikely to become a commercially viable treatment because of the time involved and the cost of the energy expenditure. However, the potential use of hot air treatment as a means of beneficially affecting commodity physiology and at the same time preventing both insect and fungal invasion justifies the further development of this technology.

III. COMMODITY RESPONSES A. Fruit Ripening Ripening of most climacteric fruit is characterized by softening of the flesh, an increase in the sugar:acid ratio, enhanced color development, and increases in respiratory activity and ethylene production. Exposing fruit to high temperatures attenuates some of these processes while enhancing others. This anomalous situation results in heated fruit being more advanced in some ripening characteristics than nonheated fruit while maintaining their quality longer during shelf life at 20°C. The inhibition of ripening by heat may be mediated by its effect on the ripening hormone, ethylene. Heat treatment inhibits ethylene synthesis within hours in both apple and tomato (Biggs et al. 1988; Klein 1989). Elevated temperatures can cause ACC to accumulate in apple and tomato tissue concomitantly with the decrease in ethylene production (Yu et a1. 1980; Atta Aly 1992), though raising the temperature further or holding the fruit longer in heat will cause the disappearance of ACC as well (Klein 1989; Atta Aly 1992). A rapid loss of ACC oxidase activity occurs in many fruit exposed for short periods to high temperatures (Chan 1986a, b; Dunlap et al. 1990; Paull and Chen 1990), due primarily to a decrease in ACe oxidase mRNA and cessation of enzyme synthesis (Lurie et al. 1996b). ACC synthase is also sensitive to high temperatures (Biggs et a1. 1988), but most studies indicate that it is less heat sensitive than ACC oxidase (Klein 1989; Atta Aly 1992). The inhibition of ethylene formation is reversed when the fruits are removed from heat (Field 1984; Biggs et a1. 1988; Dunlap et a1. 1990; Paull and Chen 1990; Chan 1991), and often ethylene rises to higher levels than in nonheated fruits (Klein and Lurie 1990; Lurie and Klein 1992b). This recovery requires protein synthesis (Biggs et a1. 1988), and studies showed that both mRNA and protein of ACC oxidase accumulate during recovery from heat treatment (Lurie et a1. 1996b).

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

97

During the heating period, not only is endogenous ethylene production inhibited, but fruits will not respond to exogenous ethylene (Seymour et a1. 1987; Yang et a1. 1990). This indicates either a loss or inactivation of ethylene receptors, or the inability to transfer the signal to initiate the subsequent series of events leading to ripening. No information is available on the response of ethylene receptors to heat, but it has been shown that the expression of tomato ripening genes is inhibited by high temperature (Picton and Grierson 1988). Specific mRNAs connected with ripening processes were found to disappear during a heat treatment of tomato and reappear during recovery from heat (Lurie et a1. 1996b). These mRNAs included those encoding ACe oxidase, polygalacturonase, and lycopene synthase. Heated fruits often soften more slowly than nonheated fruits. A number of researchers have described the effect of continuous storage at elevated temperatures on fruit firmness. Plum (Tsuji et a1. 1984), pears (Maxie et a1. 1974), avocado (Eaks 1978), and tomato (Biggs et a1. 1988) softened more slowly when held continuously at temperatures between 30 and 40°C than at 20°C. The rate of softening increased when heated fruits were returned to 20°C, but it was still less than that of nonheated fruits. Even after 6 months of storage at O°C and subsequent shelf life at 20°C, apples that had been held at 38°C for 3 or 4 days prestorage were 10 N firmer than nonheated fruit (Porritt and Lidster 1978; Klein and Lurie 1990; Klein et a1. 1990; Sams et a1. 1993; Conway et a1. 1994). The texture of heat-treated apples after storage was different quantitatively and qualitatively from that of nonheated fruit. Conway et a1. (1994), using compression tests, found the heated apples to be tougher, while Lurie and Nussinovitch (1996), using Instron compression and shearing measurements, found heated apples to be crisper than nonheated. Cell wall studies of apple fruit found less soluble pectin and more insoluble pectin in heated compared to nonheated fruits, an indication of inhibition of polyuronide degradation (Klein et a1. 1990; Ben Shalom et a1. 1993, 1996). In addition, in heated apples there was less calcium in the water-soluble pectin and more was bound to the cell wall compared to nonheated fruit (Lurie and Klein 1992a). It was thought that this was the result of the activity of pectin esterase creating more sites for calcium binding, but a study of heated and nonheated fruits showed a similar degree of pectin esterification in both (Klein et a1. 1995). During the heating period, arabinose and galactose content decreased with no accompanying decrease in uronic acids (Ben Shalom et a1. 1993). It is possible that loss of neutral sugar side chains during the heat treatment may lead to closer packing of the pectin strands, and in turn hinder enzymic cleavage during and after storage, resulting in firmer fruit.

98

S. LURIE

The decrease in the rate of softening may be due to inhibition of the synthesis of cell wall hydrolytic enzymes such as polygalacturonase (Chan et al. 1981; Yoshida et al. 1984; Lazan et al. 1989) and (X- and rJgalactosidase (Sozzi et al. 1996). In tomato, mRNA for polygalacturonase was absent in fruit during a heat treatment and appeared after the fruit was removed from heat (Lurie et al. 1996b). Depending on the length of treatment, heated tomato fruit may recover and soften to the same extent as nonheated fruit (Lurie and Klein 1992b), or remain firmer than nonheated fruit (Mitcham and McDonald 1992). In the former study tomato fruits were held for 3 days at 38°C and in the latter for 4 days at 40°C. Flavor characteristics of fruits can be affected by a heat treatment. Titratable acidity declines in apples, while soluble solids concentration is unaffected by heat treatment (Liu 1978; Porritt and Lidster 1978; Klein and Lurie 1990). The same was found after heat treatment of nectarine for insect disinfestation (Lay-Yee and Rose 1994), and hot water immersion of strawberry for decay control (Garcia et al. 1995a). In tomato (Lurie and Klein 1991, 1992b; Lurie and Sabehat 1997) and grapefruit (Miller and McDonald 1992), neither titratable acidity nor soluble solids content was affected by heat. However, in other studies, these same fruits showed reduction in titratable acidity (D'hallewin et al. 1994; Garcia et al. 1995b; Shellie and Mangan 1996). The disparate results may be due to cultivar differences or differences in the heat treatment. In some commodities, sugar content is favorably affected by heat treatment. Three hours of 45°C water before cool storage of muskmelons prevented the loss in sucrose that occurred in nonheated fruit during storage (Lingle et al. 1987). Squash sucrose content can also be raised by holding them at 30°C before storage (Bycroft et al. 1997). These heat-treated squash were perceived as sweeter than nonheated squash by a taste panel. Heated tomato fruits were not distinguished from nonheated by a taste panel, but heated Golden Delicious apples were perceived as crisper, sweeter, and overall more acceptable than nonheated fruit (Klein et al. 1997a). Volatile production is also affected by a heat treatment (McDonald et al. 1996). Volatile production in apples is enhanced during the heat treatment, is inhibited immediately following the treatment, and recovers afterward (S. Lurie and E. Fallik unpublished). The profile of the apple volatiles is also changed, with some being enhanced more than others by the heat. In tomato, the highest volatile levels in ripe fruit were from fruit heated at the mature green stage and then stored at 13°C before ripening (McDonald et al. 1996). Heat treatment leads to an accelerated rate of degreening in apples (Liu 1978; Klein et al. 1990; Whitaker et al. 1997). Chlorophyll content in apple peel, plantain peel, and tomato pericarp decreased during heat

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

99

treatment (Seymour et al. 1987; Lurie and Klein 1990; Lurie and Klein 1991). Heat treatment can also lead to yellowing of cucumbers (Chan and Linse 1989) and zucchini (Jacobi et al. 1996), although color changes in papaya skin or flesh were unaffected (Paull and Chen 1990) and it delayed yellowing of broccoli (Forney 1995; Tian et al. 1996, 1997). The difference in responses of different commodities may be an indication of whether or not new enzymes must be synthesized to effect the color changes. In the case of apples, chlorophyll degradation reveals the yellow of the underlying carotenoids already present (Hulme 1971), although for full yellowing some carotenoid synthesis occurs, while other fruits may require synthesis of carotenoids. For example, it has been found that heat treatment inhibits lycopene synthesis in tomato (Cheng et al. 1988). This is due to the inhibition of transcription of the gene for lycopene synthase, a key enzyme in the pathway, and transcription recommences after removal from heat (Lurie et al. 1996b). In banana, the inhibition of degreening during the heat treatment appears to be due to the absence of the chlorophyll oxidase enzyme activity resulting in the retention of chlorophyll in the peel (Blackbourn et al. 1989). It is unknown if this inhibition is at the level of gene expression. Respiration rate is initially enhanced by high temperatures (Lurie and Klein 1990, 1991), but after extended time at high temperatures the rate decreases (Cheng et al. 1988; Inaba and Chachin 1989; Lurie and Klein 1991). With increasing time at high temperature a greater proportion of the respiration is from the cyanide insensitive pathway (Inaba and Chahin 1989). When heated fruits are returned to ambient temperature, often their respiration rate is lower than that in nonheated fruits (Klein and Lurie 1990). A heat treatment, depending on temperature and length of exposure, can decrease or increase the climacteric respiration peak as well as advance or delay it after treatment (Eaks 1978; Klein and Lurie 1990). The response of a particular fruit or vegetable will result from a combination of factors, including the physiological age of the commodity, the time and temperature of exposure, whether the commodity is removed from heat to storage or to ripening temperature, and whether the heat treatment causes damage. B. Thermotolerance

The mechanism by which a heat treatment causes changes in fruit ripening, such as inhibition of ethylene synthesis and cell wall degrading enzymes, may be tied to changes in gene expression and protein synthesis. During a high temperature treatment the mRNAs of fruit ripen-

100

S. LURIE

ing genes disappear and those of heat shock proteins (HSP) accumulate (Picton and Grierson 1988; Lurie et a1. 1996b). An immediate response to high temperature is disassociation of polyribosomes, followed by a reassociation of some ribosomes into polyribosomes that preferentially translate the mRNAs of HSP (Ferguson et a1. 1994). This response both downregulates normal protein synthesis, even without degradation of the existing mRNAs, and upregulates HSP synthesis. The synthesis of HSP is part of the response of all organisms to heat stress, from bacteria to humans (Lindquist, 1986). Studies with many organisms have demonstrated that exposure to elevated, sublethal temperatures induces thermotolerance, which protects them from a second exposure to a normally lethal temperature. A correlation between the development of thermotolerance and the synthesis of HSP has been found (Li et a1. 1982; Vierling 1991), as well as a correlation between the loss of thermotolerance and the disappearance of HSP (Landry et a1. 1982). In addition, the development of thermotolerance is dependent on protein synthesis; pepper discs treated with protein synthesis inhibitors before high temperature treatments did not develop thermotolerance (Liu et a1. 1996). Development ofthermotolerance is dependent on the incubation temperature; it must be high enough to initiate the synthesis of HSP. Temperatures ranging from 35 to 40°C have been found to be effective, depending upon the commodity. At 42°C or higher, HSP synthesis is attenuated, and commodities are more likely to suffer heat damage (Ferguson et a1. 1994). The propensity of a moderate heat stress to protect against an extreme heat stress has been used to develop treatments to prevent commodity damage while killing the fungal pathogens or insect pests. A two-stage hot water treatment, 30 min at 42°C followed by hot water at 49°C, was developed for papaya disinfestation (Couey and Hayes 1986). This treatment also controls postharvest fungal diseases (Akamine and Arisumi 1953). Induction of heat tolerance in papaya has been found by Paull and coworkers (1986) and Paull and Chen (1990). Conditioning in 37° or 39°C air before a 46° or 47°C hot water disinfestation reduces heat damage on avocados and mangos (Joyce and Shorter 1994; Jacobi et a1. 1995a, 1995b). Similar benefits of prior temperature conditioning have been found for avocados by Woolf and Lay-Yee (1997) and for cucumbers by Chan and Linse (1989). C. Tolerance to Chilling Injury

The correlation between HSP and thermotolerance has been established in many organisms, but only recently has it been found that a heat stress

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

101

can condition plants to low temperature. Salveit and coworkers found that prior high temperature exposure affected chilling sensitivity of tomato discs (Saltveit 1991), mung bean hypocotyls (Collins et a1. 1993), and cucumber cotyledons and seeds (Lafuente et al. 1991; Jennings and Saltveit 1994). When a heat treatment was administered to tomato fruit, their sensitivity to low temperature was reduced and they could be stored for up to a month at zoe without developing chilling injury (Lurie and Klein 1991; Sabehat et a1. 1996; Lurie and Sabehat 1997). This resistance to low temperature injury was found to be contingent on the presence ofHSP (Lafuente et a1. 1991; Sabehat et a1. 1996). Once this response was demonstrated in tomato fruit, it was found to occur in other fruits and vegetables, including avocado (Woolf et a1. 1995), citrus (Schirra and Mulas 1995a; Rodov et al. 1995; Wild 1993), cucumber (McCollum et a1. 1995), mango (McCollum et a1. 1993), pepper (Mencarelli et a1. 1993), persimmons (Burmeister et a1. 1997; Lay-Yee et a1. 1997a), and zucchini (Wang 1994). However, the response may in some cases be cultivar specific. For example, Whitaker (1994) found no benefit in heating 'Rutgers' tomato fruit, and we have been unable to induce resistance to chilling injury in cherry tomatoes by heat treatment (S. Lurie unpublished). A heat treatment has been used together with a cold quarantine treatment to disinfest avocado from fruit fly. The cold treatment, which followed the heat treatment, did not induce chilling injury (Sanxter et a1. 1994; Nishijima et al. 1995). When the heat treatment was given as a fungicidal hot water dip, rots were also controlled (Jessup 1991). In a study with avocado discs, maximal HSP production was found after 4 h at 3BOC and heating provided a significant degree of protection from chilling injury (Florissen et a1. 1996). The reduction of sensitivity to chilling injury in fruits may not be due solely to the presence of HSP. Chilling injury has long been thought to begin with membrane damage (Lyons 1973), and the heat treatment may cause membrane alterations. High temperature increases membrane leakage (Inaba and Crandall 19BB; Lurie and Klein 1990, 1991), but after removal from heat stress the tissue recovers (Lurie and Klein 1990). Using membrane leakage as a measure of chilling injury, Saltveit (1991) found that conditioning tomato fruit discs at 37°C reduced leakage at low temperature. An examination of the lipid composition of apple plasma membrane or tomato total tissue lipids showed that after heat treatment and subsequent cold storage there were more phospholipids and greater fatty acid unsaturation than in nonheated fruits (Lurie et al. 1995; Lurie et a1. 1997b). Whitaker et a1. (1997) examined total apple lipids, and found greater fatty acid unsaturation, though not greater phospholipid

102

S. LURIE

content, in heated fruit. This would indicate more fluid membranes in the heated fruit, and correspond with reduced indiscriminate leakage from the tissues of heated fruits and vegetables. These changes in lipid composition were found in tomato fruit treated for 2 days at 38°C with hot air, and also in 46° and 48°C hot water dips of 2 to 3 min, an indication that even short exposure to heat can instigate processes leading to tissue adaptation to low temperature (Lurie et al. 1997b). Apples are normally thought to be fruits that are insensitive to low temperature, but superficial scald is a physiological storage disorder that is a form of chilling injury (Bramlage and Meir 1990). It is an oxidative process causing peel browning, and has been correlated with the oxidation of a-farnesene, a component of the apple wax (Huelin and Coggiola 1970). A prestorage heat treatment of apples controls this disorder during the first months of O°C storage by inhibiting the accumulation of a-farnesene and consequently decreasing its oxidation products (Lurie et al. 1990). The inhibitory effect allows for 3 to 4 months of air storage without scald development (Lurie et al. 1990; Combrink et al. 1994). Part of the overall reduction in a-farnesene may be due as well to a thinner wax layer and changes in structure of the wax surface after the heat treatment (Roy et al. 1994; Lurie et al. 1996a). a-farnesene is a volatile and conditions that facilitate its dissipation from the fruit (such as wrapping in waxed paper) will reduce scald. The heat treatment causes the fruit wax layer to become thinner and may allow faster volitalization of the a-farnesene and therefore less accumulation of oxidation products. D. Heat Damage

Although this review has focused on the positive response of commodities to a heat treatment, there is always a danger of tissue damage. This is one reason why there is such a multitude of treatments, which is the result of efforts to find a time-temperature regime that will produce the desired effect (disinfestation, fungal control) without damaging the commodity. Damage can be both external and internal. External damage generally appears as peel browning (Kerbel et al. 1987; Klein and Lurie 1992b; Lay-Yee and Rose 1994; Woolf and Laing 1996), pitting (Miller et al. 1988; Jacobi and Gowanlock 1995), or yellowing of green vegetables such as zucchini (Jacobi et al. 1996) or cucumber (Chan and Linse 1989). Tissue damage caused by heat will also result in increased decay development (Jacobi and Wong 1992; Jacobi et al. 1993; Lay-Yee and Rose 1994). Internal damage can evidence itself in mango and papaya as poor color development, abnormal softening, the lack of starch

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

103

breakdown, and the development of internal cavities (An and Paull 1990; Jacobi and Wong 1992; Mitcham and McDonald 1993; Paull 1995). Internal damage on other fruits can include flesh darkening in avocado, citrus, lychee, and nectarine (Jacobi et al. 1993; Shellie et al. 1993; LayYee and Rose 1994; Shellie and Mangan 1994, 1996). If the produce is stored at low temperature after the heat treatment, the heat damage can be confused with chilling injury, which has similar symptoms.

IV. FUNGAL PATHOGEN RESPONSE A. Sensitivity of Different Growth Stages The efficacy of a heat treatment on a fungal pathogen is usually measured by the reduction in viability of the organism, either in spore germination or mycelliar growth. The response of a pathogen to heat can be influenced by the moisture content of the spores, metabolic activity of the pathogen, the concentration and age of the inoculum, and the chemical composition and water activity of the treatment medium. Even the culture medium on which the fungus is grown after the heat treatment can influence its apparent viability. Genetic differences among fungi are expressed as considerable variation in sensitivity to high temperature (Barkai-Golan and Phillips 1991). A dry heat treatment at 38°C of tomato prevented decay by Botrytis cinerea Pers.:Fr., but was ineffective for Alternaria alternata Keissler (Fallik et al. 1993). For a given fungal species, spore inactivation increases with both temperature and duration of the treatment. Spores of Alternaria alternata Keissler may be inactivated equally by 2 min at 4BoC or 4 min at 46°C (Barkai-Golan and Phillips 1991). Water relations of the pathogen can markedly effect transfer of heat and the effectiveness of the treatment. A comparison of dehydrated or moist conidia of Penicillium digitatum Sacco found that 100/0 of the dry and 90% of the moist spores were killed by the same heat regime. Germinated spores are also more sensitive than dormant spores. For Alternaria alternata Keissler, germinated but not dormant spores can be inactivated by 42°C water. The LD so temperature for germinating and dormant spores of Rhizopis stolonifer Lind exposed to hot water for 4 min was 39°C and 49°C, respectively (Barkai-Golan and Phillips 1991). Extensive research on heat treatment to control pathogens was conducted in the past. A list of the pathogens controlled and commodities treated is presented in the reviews of Barkai-Golan and Phillips (1991)

104

S. LURIE

and Coates and Johnson (1993). There is still considerable effort carried out on citrus, particularly since adding fungicides to a hot water dip often gives better protection than either treatment alone (Couey 1989), and on vegetables such as tomato and pepper, for which there are no approved postharvest chemicals for decay control (Fallik et al. 1993, 1996b). Botrytis cinerea Pers.:Fr. is a fungus that is very sensitive to high temperature; heat treatments have been reported for its control on apples (Klein et al. 1997b), flowers (Elad and Volpin 1991), pepper (Fallik et a1. 1996b), tomato (Fallik et al. 1993), and strawberry (Garcia et al. 1996). As discussed earlier, these treatments often have the added benefit of reducing the sensitivity of the commodity to chilling injury, thus extending the storage life by preventing both pathological and physiological disorders. Some of the quarantine treatments developed for insect pests have been investigated for effectiveness against fungal decay. The vapor heat treatment used for disinfestation of 'Carabao' mango in the Philippines was found to significantly reduce the incidence of anthracnose and stem end rot in fruit, although the onset of decay was not delayed by the treatment (Esquerra and Lizada 1990). In stone fruits, a hot water dip to kill thrips also reduced brown rot (McLaren et al. 1997). In 'Kensington Pride' mango disinfected with vapor heat, there was good control of anthracnose (Colletotrichum gJoeosporioides Penz), but variable control of stem end rot (DothiorelJa dominicana Sacco and LasiodipJodia theobromae L.) (Coates et al. 1993). Stem end rot was probably more difficult to control using heat than anthracnose because of the location of the fungus at the time of treatment. Quiescent infection structures of C. gJoeosporioides Penz are located in the cuticular region of mango peel, whereas hyphae of the stem end rot fungi are located within the pedicel tissue of fruit (Johnson et al. 1992). In this location, stem end rot fungi would be less vulnerable to the heat treatment. In addition, C. gJoeosporioides is more heat-sensitive than D. dominican a or L. theobromae (Rappell et al. 1991). Other studies have shown that disinfestation treatments may not control pathogens and may even encourage their development. Fruit rot caused by Penicillium sp. was increased in grapefruit as a result of hot water treatment for the control of Caribbean fruit fly (Miller et al. 1988). Vapor heat treatment of grapefruit could also increase storage decay in some cases (Hallman et al. 1990). A hot air treatment of papaya fruit against fruit flies was ineffective in controlling postharvest disease in comparison with fungicides or hot water treatment (Nishijima et al. 1992). However, when hot air treatment was combined with thiabendazole application or hot water immersion, the incidence of postharvest diseases was reduced (Nishijima et al. 1992).

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

105

B. Host-pathogen Interactions: Defense Reactions of the Host

Heat treatment is a stress and as such the plant tissue responds by trying to alleviate and/or repair the damage caused by the stress. The most studied of the responses to heat is the production of HSP. There is no evidence that HSP can have antifungal or anti-insecticidal properties. However, heat treatment, just as it inhibits ripening, may delay the breakdown and disappearance of preformed antifungal compounds that are present in unripe fruits (Prusky 1996). In addition, heat treatment may induce synthesis of compounds such as phytoalexins or pathogenesis related (PR) proteins, particularly if the commodity heated has wounds from harvest or postharvest handling. These compounds may be present only in a local area around the wound rather than throughout the tissue. Heat treatment of film-wrapped citrus fruit at 36°C accelerated healing of fruit wounds and markedly reduced decay caused by Penicillium digitatum Sacco (Ben-Yehoshua et al. 1987; Ben-Yehoshua et al. 1989; D'hallewin et al. 1994). Seal packaging provided a water saturated atmosphere and protected the fruit from high temperature injury (BenYehoshua et al. 1987). The heated citrus were found to have a high concentration of the phytoalexin scoparone and the concentration was correlated with antifungal activity in the fruit extract (Kim et al. 1991). Different citrus species (lemon, orange, grapefruit, lime, kumquat) varied in their capacities to produce scoparone as a result of inoculation with Penicillium digitatum Sacco followed by heat treatment (BenYehoshua et al. 1992; Rodov et al. 1994). PR proteins were also detected by Western blot around wounded areas of heated but not nonheated fruit (Rodov et al. 1996). Also the heating induced the biosynthesis of fungitoxic aromatic aldehydes and deposition of lignin-like polymers that were strongly bound to walls of cells adjacent to wound sites in the fruit peel (Eckert et al. 1996; Rodov et al. 1996). There are indications that heat treatment of apples induces a phytoalexin compound, and wounding plus heat enhances the production of this compound (Fallik et al. 1996c). Penicillium expansum Link inoculated into apple tissue before a heat treatment failed to develop after the treatment, but if reisolated from the wound and plated out on agar, the spores were viable. Thus, there was an interaction between the heated fruit tissue and the pathogen that prevented germination of the spores in the wounded fruit. Avocado contain an antifungal diene that disappears as the fruits ripen and concomitantly allows the development of quiescent infections of Colletotrichum gJoeosporioides Penz. A 10 min hot water dip caused

106

S. LURIE

faster decrease of this compound and the earlier appearance of disease symptoms compared to nonheated fruit (Plumbley et a1. 1993). However, a dry heat treatment of the fruit delayed the development of decay (Lurie et a1. 1997c), highlighting the necessity for the proper time-temperature treatment for each commodity. Mature green tomato fruit are refractory to pathogen invasion and as ripening proceeds they lose this resistance. Loss of resistance has been correlated with the disappearance of mRNA for an anionic peroxidase (Sherf and Kolattukudy 1993). Heating mature green fruit delayed the loss of the anionic peroxidase mRNA and maintained antifungal resistance in the fruit tissue (Lurie et a1. 1997a). Thus, in addition to the possible lethal effect of high temperature on the pathogen, there are a number of host-pathogen interactions that can be exploited to decrease fungal decay,

V. INSECT RESPONSE

A. Effect on Insect Life Stages In insects, thermal tolerance and heat induced mortality are dependent on time and temperature exposures and involve a complex interaction of physiological and biochemical changes. Although heat causes many changes, the thermal mortality death data developed by Jang (1986, 1991) suggest that thermal responses of both fruit fly eggs and larvae are almost identical to first order kinetics used to describe monomolecular chemical reactions. Thermal death of fruit fly eggs and larvae follows a logarithmic function, so that the final number of survivors of any timetemperature treatment is dependent on the initial number of insects. Rates of heating depend on the heat transfer characteristics of the fruit, size and shape of the fruit, type of container holding the fruit, and characteristics of the heat treatment. The time and temperature effects on different life stages of fruit fly eggs and larvae under various heating regimes have been measured (Jang 1986; Sharp and Chew 1987; Hallman 1990b; Heard et a1. 1991; Jang 1991; Moss and Jang 1991; Hanson and Sharp 1994), as well as other insects such as moths (Yokayama and Miller 1987; Ydkayama et a1. 1991). These studies on insects divorced from the fruit help to predict the thermal response of the insects in the fruit. As with fungal pathogens, various insects have different sensitivities to high temperature. If a commodity is infected with more than one pest, the disinfestation procedure must be aimed at the most resistant species. For example, persimmon can be hosts for both apple moth (Epiphyas

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

107

postvittaca Walker) and mealy bug (Pseudococcus longispinus 1.), and mealy bugs are more tolerant to hot water immersion (Lester et al. 1995) or hot air treatment (Dentener et al. 1996) than the apple moth. In addition, the position of the insect on the fruit, whether on the surface or inside the flesh or calyx, will affect its exposure to heat and consequently its mortality. Larvae in the seed cavity are the most difficult to kill because they are insulated by the fruit pulp and are farthest from the warming fruit surface. A further consideration is the suitability of the commodity as a host. In many cases there is significant mortality of the insects (up to 50%) in a fruit even without any disinfestation treatment (Jang 1996). Some insects, such as the longtailed mealy bug, show no difference in response to heat at different life stages (Hansen et al. 1992). However, for most fruit flies the larvae are less resistant to high temperature than the eggs (Hansen et al. 1990). A study of hot air disinfestation treatment on papaya for three species of fruit fly found Mediterranean fruit fly (Caratitis capitata Wiedemann) to require higher temperatures for eradication than melon fly (Dacus cucurbitae Coquillet) or oriental fruit fly (Dacus dorsalis Hendel), and in all three species the first and third instars were more susceptible to heat than the eggs (Armstrong et al. 1989,1995). Some species of moth, such as the light brown apple moth (Epiphyas postvittana Walker) show more tolerance to heat than others (e.g., Ctenopseustis obliquana or Planotortrix octo), and the eggs ofthese insects are also more tolerant to heat than larvae at different stages of development (Jones et al. 1995). In heat treatments of insects, there appears to be a threshold between 41° and 43°C (Moss and Chan 1993; Hansen and Sharp 1994). Below 43°C, the insects exhibit chronic mortality, where death occurs during metamorphoses. Cell tolerance to heat is dependent on developmental stage, with the G1 phase (between mitosis and the synthetic phase) the most resistant and the M (mitosis) stage the most sensitive (Mackey and Roti Roti 1992). Heat treatments may interfere with the production of proteins essential for development and tissue differentiation, and in this manner cause death. Jang (1992) observed that in Mediterranean fruit fly, HSPs were produced between 37° and 41°C, while normal protein synthesis was reduced. A temperature greater than 43°C may cause acute mortality with nb survivors. All protein synthesis, including HSP, ceases above 42° or 43°C (Tomasovic and Koval 1985; Jang 1992), and membrane components are disrupted. This is similar to what was found in plant tissue (Ferguson et al. 1994). Therefore, most disinfestation protocols involve raising the fruit temperature above 43°C for a period of time, often to 46

108

S. LURIE

or 47°C, long enough to kill the insect but less than the time needed to cause tissue damage to the commodity. B. Probit 9 or Not For insect pests of fresh horticultural products, statistical analyses are used to estimate the probability of success of a treatment. To evaluate this, first laboratory bioassays are performed, followed by large-scale confirmatory tests. Until adoption of the maximum pest limit concept in New Zealand (Baker et al. 1990), successful treatment in quarantine entomology was defined as probit 9. Stated for the first time in 1939, this probit represents a mortality of 99.99683%, or a survival of 32 out of 1,000,000 insects (Baker 1939). This recommendation assumed that 99.99683% mortality would ensure that the risk of accidental introduction of an exotic pest would be nonexistent. The assumptions inherent in the probit 9 requirement are: (1) 99.99683% effectiveness is the minimum level necessary for quarantine security, (2) the probit model is always suitable for analyses of data from cOlllmodity treatment bioassays, and (3) only the probability of death is relevant to the future establishment of the pest in a new environment. As convenient as these assumptions are for regulatory agencies, they have a limited scientific basis. Indeed, knowledge of insect pests and their responses to quarantine treatments, specifically heat, has increased substantially since 1939, and a growing body of evidence suggests that mortality (particularly 99.99683% mortality) is far too narrow a criterion upon which to evaluate treatment efficacy (Landolt et al. 1984; Robertson et al. 1984; Armstrong and Couey 1989; Baker et al. 1990; Vail et al. 1992). However, "probit 9 security" is still the requirement of the US Department of Agriculture, and comparable regulatory agencies of other nations, for importation of fresh horticultural products that might be contaminated with exotic pests. In 1990, Baker et al. described the concept of setting maximum pest limits for produce imported into New Zealand. This method consists of setting limits on the maximum number of fruit flies imported into the port of Auckland at a given time, assuming that a single male and a single female would not emerge, mate, and establish a new population. The maximum limit concept is derived from the suggestion of Landolt et al. (1984) that quarantine efficacy should be evaluated on the basis of the probability of successful reproduction and not on mortality. Factors such as mating, dispersal, feeding, and finding hosts in a new location should be considered. These factors are collectively considered to constitute risk, and are variables that should be defined. In addition,

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

109

Worner (1988) indicated that the climatic suitability of the new environment is also an important factor. This new concept replaces the exclusive use of mortality (probit 9) as the criterion for treatment efficacy, with the use of probability of introduction and establishment of pests. It remains to be seen how successful these ideas will be in replacing probit 9 as the official guidelines in most countries. C. Thermotolerance: Combined Treatments

Just as commodities exposed to moderately high temperatures can develop thermotolerance and resistance to low temperature injury, so can insects. Brief exposure to high temperature (30 min at 40°C) elicits a protective response in flies that prevents injury when they are subjected to lethal temperature of 45°C (Chen et a1. 1991). This response was found in all developmental stages of the fly, and has obvious implications for strategies of disinfestation. The same type of thermal acclimation has recently been found for the light brown apple moth (Epiphyas postvittana Walker), and may well be true for all insects (Beckett and Evans 1996). Studies with heating rates by Neven and Rehfield (1995) demonstrated that a longer exposure of coddling moth to slower heating rates is needed to provide the same level of mortality as more rapid rates (Neven 1994; Neven and Mitcham 1996). Obviously, slower heating rates allow for larvae to adjust to temperature extremes. Hallman (1994) found that larvae reared at 30°C were more likely to tolerate immersions at 43°C than larvae reared at 20°C. One of the recent developments in disinfestation research is the use of combinations of more than one treatment. Other shocks or abiotic stresses to which an insect can be exposed and which a commodity can withstand include low temperature and controlled atmosphere. A number of studies have used these together with high temperature to eliminate insect pests. For treatment of temperate fruits, such as apple or pear, a combination of prestorage heat treatment with cold storage has been found to be more effective for control of codling moth (Cydia pomelJa L.) than the heat treatment alone (Neven and Rehfield 1995). Citrus fruits are often subjected to cold storage quarantine for control of fruit flies. A prestorage heat treatment, or a 50°C fungicide dip before cold storage, has led to insect control without fruit chilling injury (Wild and Hood 1989; McDonald et a1. 1991). The same regime of a 50°C dip in fungicide followed by cold storage at 1°C for 'Hass' avocado was found to control

110

S. LURIE

Queensland fruit fly (Bactrocera tryoni Froggatt) without causing fruit damage (Jessup 1994), while the cold quarantine alone caused chilling injury (Jessup 1991). Giving a heat treatment in the presence of controlled atmosphere allows for shortening of the period of time the commodity is held at a high temperature. All six of the leafroller species that constitute the primary pest complex of kiwifruit in New Zealand could be controlled by exposure to 0.40/0 02' 5% CO 2 with the most resistant species requiring 32 h for total mortality (Whiting et al. 1995). The same atmosphere at 40°C eliminated the pests in less than 5 h (Whiting et al. 1996). Another kiwifruit pest, the two spotted spider mite (Tetranychus urticae Koch) could be controlled by incubation at 40°C and 0.4% 02' 200/0 CO 2, It took 8.1 h for the diapausing stage and 5.4 h for the nondiapausing stage to be killed (Lay-Yee and Whiting 1996). Decreasing the concentration of O2 has a greater effect than increasing the concentration of CO 2 ; high mortality occurred more rapidly when the concentration of O 2 was lower, especially at 0.4 % (Whiting et al. 1991; Whiting and van den Heuvel 1995). A similar treatment of heat and controlled atmosphere controlled insect pests of apples, including various species of moth, leafroller, wheatbug, and mealybug (Whiting et al. 1992; Lay-Yee et al. 1997b; Whiting and Hoy 1997). Using a triple combination of prestorage heat with controlled atmosphere, followed by weeks of cold storage, controlled both the moths and fruit flies that infest pear and apple (Chervin et al. 1997a, 1997b). In this case, 30°C was used, because 35° or 40°C caused skin scalding on pear fruit. These combined treatments may circumvent the development of insect tolerance to high temperatures, and allow substantial shortening of the treatment period. VI. CONCLUSIONS

There has been intensive research during the past few years on heat treatment of commodities, particularly for insect eradication. However, the work has been for the most part empirical, that is, a matrix of timetemperature treatments was tried in order to find a combination that kills the insect pest with minimal damage to the commodity. What has been missing is modeling work to predict the commodity response, similar to what has been done previously for insects. This kind of research direction might advance the field faster than it is now progressing. In addition, a better understanding of the molecular and biochemical processes occurring in the fruit and vegetable tissue during and following the heat

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

111

treatment should aid in developing successful treatments. It is tempting to envision an integrated treatment that would control both insect and fungal pests, beneficially affect commodity quality, and be economically attractive. Thus far, no such treatment has been developed. LITERATURE CITED Akamine, E. K., and T. Arisumi. 1953. Control of postharvest storage decay of fruits of papaya (Carica papaya 1.) with special reference to the effect of hot water. Proc. Am. Soc. Hort. Sci. 61:270-274. An, J. F., and R E. Paull. 1990. Storage temperature and ethylene influence on ripening of papaya fruit.]. Am. Soc. Hort. Sci. 115:949-953. Animal and Plant Health Inspection Service. 1985. Section III, 9 and section VI-T106. Plant protection and quarantine manual. U.S. Dept. Agr., Hyattsville, MD. Animal and Plant Health Inspection Service. 1987. Section IV-T102, (c). Plant protection and quarantine treatment manual. U.S. Dept. Agr., Hyattsville, Md. Armstrong, J. W. 1982. Development of a hot-water immersion quarantine treatment for Hawaiian grown 'Brazilian' bananas. ]. Econ. Entomol. 75:787-790. Armstrong, ]. W., and H. M. Couey. 1989. Fumigation, heat and cold. p. 411-424. In: A. S. Robinson and H. Hooper (eds.), Fruit flies, their biology, natural enemies and control. Elsevier, Amsterdam. Armstrong, ]. W., J. D. Hansen, B. K. S. Hu, and S. A. Brown. 1989. High-temperature, forced-air quarantine treatment for papayas infested with Tephritid fruit flies (Diptera: Tephritidae). J. Econ. Entomol. 82:1667-1674. Armstrong, ]. W., B. K. S. Hu, and S. A. Brown. 1995. Single-temperature forced hot-air quarantine treatment to control fruit flies (Diptera: Tephritidae) in papaya. J. Econ. Entomol. 88:678-682. Atta Aly, M. A. 1992. Effect of high temperature on ethylene biosynthesis by tomato fruit. Postharv. BioI. Technol. 2:19-24. Baker, A. G. 1939. The basis for treatment of products where fruit flies are involved as a condition for entry into the United States. USDA Cir. 551, Washington, DC. Baker, A. G. 1952. The vapor-heat process. U.S. Dept. Agr. Yearbook, U.S. Govt. Printing Office, Washington, DC. Baker, R T.,]. W. Cowley, D. W. Harte, and E. R Frampton. 1990. Development of a maximum pest limit for fruit flies (Diptera: Tephritidae) in produce imported from New Zealand. J. Econ. Entomol. 83:13-17. Barkai-Golan, R, and D.]. Phillips. 1991. Postharvest heat treatment of fresh fruits and vegetables for decay control. Plant Dis. 75:1085-1089. Beckett, S. ]., and D. E. Evans. 1996. The effects of thermal acclimation on immature mortality in the Queensland fruit fly Bactiocera tryoni and the light brown apple moth Epiphyas postvitta at a lethal temperature. Entomol. Exper. Appl. 81:1-7. Ben Shalom, N., ]. Hanzon, ]. D. Klein and S. Lurie. 1993. A postharvest heat treatment inhibits cell wall degradation in apples during storage. Phytochemistry 34:955-958. Ben Shalom, N., J. Hanzon, R Pinto, and S. Lurie. 1996. Cell wall changes and partial prevention of fruit softening in prestorage heat treated 'Anna' apples. ]. Sci. Food Ag. 72:231-234. Ben-Yehoshua, S., ]. J. Kim, and B. Shapiro. 1989. Elicitation of resistance to the development of decay in citrus fruit by curing of sealed fruit. Acta Hort. 258:623-630.

112

S. LURIE

Ben-Yehoshua, S., V. Rodov, J. J. Kim, and S. Carmeli. 1992. Preformed and induced antifungal materials of citrus fruits in relation to the enhancement of decay resistance by heat and ultraviolet treatments. J. Ag. Food Chern. 40:1217-1221, Ben-Yehoshua, S., B. Shapiro, and R. Moran. 1987. Individual seal-packaging enables the use of curing at high temperatures to reduce decay and heat injury of citrus fruits. HortScience 22:777-783. Biggs, M. S., W. R. Woodson, and A. K. Handa. 1988. Biochemical basis of high temperature inhibition of ethylene biosynthesis in ripening tomato fruits. PhysioL Plant. 72:572-578. Blackbourn, H., P. John, and M. Jeger. 1989. The effect of high temperature on degreening in ripening bananas. Acta Hart. 258:271-278. Bramlage, W., and S. Meir. 1990. Chilling injury of temperate crops. p. 37-53. In: C. W. Wang (ed.) Chilling Injury of Horticultural Crops, CRC Press, Boca Raton, FL . Burmeister, D., S. Ball, S. Green, and A. B. Woolf. 1997. Interaction of hot water treatments and controlled atmosphere storage on quality of 'Fuyu' persimmons. Postharv. BioI. TechnoI.,12:71-82. Bycroft, B., V. Corrigan, and G. Boulton. 1997. Sweetening squash with heat treatments. Acta Hort., in press. Chan. H. T. 1986a. Effects of heat treatments on the ethylene forming enzyme system in papaya. J. Food Sci. 51:581-583. Chan, H. T. 1986b. Heat inactivation of the ethylene forming enzyme system in cucumber. J. Food Sci. 51:1491-1493. Chan. H. T. 1991. Ripeness and tissue depth effects on heat inactivation of papaya ethylene forming enzyme. ]. Food Sci. 56:996-998. Chan, H. T., and E. Linse. 1989. Conditioning cucumbers for quarantine heat treatments. HortScience 24:985-989. Chan, H. T., S. Y. T. Tam, and S. T. Seo. 1981. Papaya polygalacturonase and its role in thermally injured ripening fruit. J. Food Sci. 46:190-197. Chen. C. P., R. E. Lee, and D. L. Denlinger. 1991. Cold shock and heat shock: a comparison of the protection generated by brief pretreatment at less severe temperatures. Physiol. Entomoi. 16:19-26. Cheng, T. S., J. D. Floros, R. L. Shewfelt, and C. J. Chang. 1988. The effect of high temperature stress on ripening of tomatoes (Lycopersicon escuJentum). J. Plant Physioi. 132:459-464. Chervin, C.• S. Kulkarni, S. Kreidl, F. Birrell. and D. Glenn. 1997a. A high temperature/low oxygen pulse improves cold storage disinfestation. Postharv. BioL Technol., 10:239-246. Chervin, C., A. Jessup, A. Hamilton, S. Kreidl, S. Kulkarni, and P. Franz. 1997b. Nonchemical disinfestation: combining the combination. Acta Hort.: 464. In press. Coates, L. M., and G. 1. Johnson. 1993. Effective disease control in heat-disinfected fruit. Postharv. News Infor. 4:35N-40N. Coates, L. M., G. 1. Johnson, and A. Cooke. 1993. Postharvest disease control in mangoes using high humidity hot air and fungicide treatments. Ann. AppI. BioI. 123:441-448. Collins, G. G., X. Nie, and M. E. Saltveit, Jr. 1993. Heat shock increases chilling tolerance of mung bean hypocotyl tissue. Physioi. Plant. 89:117-124. Combrink, J. c., L. B. Benie, E. Lotz, and A. B. Truter. 1994. Integrated management of postharvest fruit quality. Acta Hart. 368:657-666. Conway, W. S., C. E. Sams, C. Y. Wang, and J. A. Abbott. 1994. Additive effects of postharvest calcium and heat treatment on reducing decay and maintaining quality in apples. J. Am. Soc. Hort. Sci. 119:49-53.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

113

Couey, H. M. 1989. Heat treatment for control of postharvest diseases and insect pests of fruits. HortScience 24:198-201. Couey, H. M., and C. F. Hayes. 1986. A quarantine system for papayas using fruit selection and a two stage hot water treatment. J. Econ. Entomol. 79:1307-1314. Dentener, P. R, S. M. Alexander, P. J. Lester, R J. Petry, J. H. Maindonald, and R M. McDonald. 1996. Hot air treatment for disinfestation of lightbrown apple moth and longtailed mealy bug on persimmons. Postharv. BioI. Technol. 8:143-152. D'hallewin, G., G. Arras, T. Castia, and A. Piga. 1994. Reducing decay of Avana mandarin fruit by the use of UV, heat and thiabendazole treatments. Acta Hort. 368:387-394. Dunlap, J. R, S. E. Lingle, and G. E. Lester. 1990. Ethylene production in netted muskmelon subjected to postharvest heating and refrigerated storage. HortScience 25:207-209. Eaks, 1. 1. 1978. Ripening, respiration, and ethylene production of 'Hass' avocado fruits at 20° to 40°C. J. Am. Soc. Hart. Sci. 103:576-578. Eckert, J. W., M. Ratnayake, J. R Sievert, and R R Strange. 1996. Curing citrus fruits to control postharvest diseases. p. 48. VIII Congress of the Intntl Soc. of Citriculture, Abstracts, Sun City, South Africa. Elad, Y., and H. Volpin. 1991. Heat treatment for the control of rose and carnation gray mould (Botrytis cinerea). Plant Pathol. 40:278-286. Esquerra, E. B., and M. C. C. Lizada. 1990. The postharvest behaviour and quality of 'Carabao' mangoes subjected to vapor heat treatment. ASEAN Food J. 5:6-11. Fallik, E., Y. Aharoni, O. Yekutieli, A. Wiseblum, R Regev, H. Beres, and E. Bar Lev. 1996a. A method for simultaneously cleaning and disinfecting agricultural produce. Israel Patent Application No. 116965. Fallik, E., S. Grinberg, S. Alkalai, and S. Lurie. 1996b. The effectiveness of postharvest hot water dipping on the control of gray and black moulds in sweet red pepper (Capsicum annuum). Plant Pathoi. 45:644-649. Fallik, E., S. Grinberg, M. Gambourg, J. D. Klein, and S. Lurie. 1996c. Prestorage heat treatment reduces pathogenicity of PenicjJJium expansum in apple fruit. Plant Pathoi. 45:92-97. Fallik, E., J. D. Klein, S. Grinberg, E. Lomaniec, S. Lurie, and A. Lalazar. 1993. Effect of postharvest heat treatment of tomatoes on fruit ripening and decay caused by Botrytis cinerea. Plant Dis. 77:985-988. Ferguson,!. B., S. Lurie, and J. H. Bowen. 1994. Protein synthesis and breakdown during heat shock of cultured pear (Pyrus communis 1.) cells. Plant Physioi. 104:1429-1437. Field, R J. 1984. The effect of temperature on ethylene production by plant tissue. p. 47-69. In: J. A. Roberts and G. A. Tucker (eds.). Ethylene and plant development. Butterworths, London. Florissen, P., J. S. Ekman, C. Blumenthal, W. B. McGlasson, J. Conroy, and P. Holford. 1996. The effects of short heat treatments on the induction of chilling injury in avocado fruit (Persea americana Mill). Postharv. BioI. Technol. 8:129-141. Forney, C. F. 1995. Hot water dips extend the shelf life of fresh broccoli. HortScience 30:1054-1057. Furasawa, K., T. Sugimoto, and T. Gaja. 1984. The effectiveness of vapor heat treatment against the melon fly, Dacus cucurbitae Coquillett, in eggplant and fruit tolerance to treatment. Res. Bull. Plant Port. Servo Japan 20:17-24. Gaffney, J. J., and J. W. Armstrong. 1990. High-temperature forced-air research facility for heating fruits for insect quarantine treatments. J. Econ. EntomoI. 83:1959-1964. Gaffney, J. J., G. J. Hallman, and J. 1. Sharp. 1990. Vapor heat research unit for insect quarantine treatments. J. Econ. Entomol. 83:1965-1971.

114

S. LURIE

Garcia, J. M., C. Aguilera, and M. A. Albi. 1995a. Postharvest heat treatment on Spanish strawberry (Fragaria x ananassa cv. Tudla). J. Ag. Food Chern. 43:1489-1492. Garcia, J. M., C. Aguilera, and A. M. Jimenez. 1996. Grey mold in and quality of strawberry fruit following postharvest heat treatment. HortScience 31 :255-25 7. Garcia, J. M., J. M. Ballesteros, and M. A. Albi. 1995b. Effect of foliar applications of CaCl z on tomato stored at different temperatures. J. Ag. Food Chern. 43:9-12. Gould, W. P., and J. L. Sharp. 1992. Hot water immersion quarantine treatment for guava infested with Caribbean fruit fly (Diptera: Tephritidae). J. Econ. EntomoI. 85:1235-1239. Hallman, G. J. 1990a. Vapor-heat treatment of carambolas infested with Caribbean fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 83:2340-2342. Hallman, G. J. 1990b. Survival and reproduction of Caribbean fruit fly (Diptera: Tephritidae) adults immersed in hot water as third instars. J. Econ. EntomoI. 83:2331-2334. Hallman, G. J. 1994. Mortality of third instar Caribbean fruit fly (Diptera: Tephritidae) reared at three temperatures and subjected to hot water immersion or cold storage. J. Econ. EntomoI. 87:405-408. Hallman, G. J., J. J. Gaffney, and ]. L. Sharp. 1990. Vapor heat treatment for grapefruit infested with Caribbean fruit fly (Diptera: Tephritidae). J. Econ. EntomoI. 83:1475-1478. Hallman, G. J., and J. 1. Sharp. 1990. Hot-water immersion quarantine treatment for carambolas infested with Caribbean fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 83:1471-1474. Hansen, J. D., J. W. Armstrong, B. K. S. Hu, and S. A. Brown. 1990. Thermal death of oriental fruit fly (Diptera: Tephritidae) third instars in developing quarantine treatments for papayas. J. Econ. EntomoI. 83:160-167. Hansen, J. D., A. H. Hara, and V. 1. Tenbrink. 1992. Vapor heat: a potential treatment to disinfect tropical cut flowers and foliage. HortScience 27:139-143. Hansen, J. D., and J. L. Sharp. 1994. Thermal death in third instars of the Caribbean fruit fly: time-temperature relationships. J. Econ. EntomoI. 87:736-740. Hawkins, L. A. 1932. Sterilization of citrus fruit by heat. Citriculture 9:21-22. Heard, T. A., N. W. Heather, and R. J. Corcoran. 1991. Dose-mortality relationships for eggs and larvae of Bactiocera tryoni (Diptera: Tephritidae) immersed in hot water. J. Econ. EntomoI. 84:1768-1770. Huelin, F. E., and I. M. Coggiola. 1970. Superficial scald, a functional disorder of stored apples. V. Oxidation of a-farnesene and its prevention by diphenylamine. J. Sci. Food Agric.21:44-48. Hulme, A. C. 1971. Pome fruits. p. 333-374. In: A. C. Hulme (ed.), The Biochemistry of Fruits and Their Products, Volume 2, Academic Press, NY. Inaba, M., and K. Chachin. 1988. Influence of and recovery from high temperature stress on harvested mature green tomatoes. HortScience 23:190-192. Inaba, M., and K. Chachin. 1989. High-temperature stress and mitochondrial activity of mature green tomatoes. ]. Am. Soc. Hort. Sci. 114:809-814. Inaba, M., and G. Crandal., 1988. Electrolyte leakage as an indicator of high temperature injury to harvested mature green tomatoes. J. Amer. Soc. Hort. Sci. 113:96-99. Jacobi, K. K., J. Giles, E. MacRae, and T. Wegrzyn. 1995a. Conditioning 'Kensington' mango with hot air alleviates hot water disinfestation injuries. HortScience 30:562-565. Jacobi, K. K., and D. Gowanlock. 1995. Ultrastructural studies of 'Kensington' mango (Mangifera indica Linn.) heat injuries. HortScience 30:102-103. Jacobi, K. K., and L. S. Wong. 1992. Quality of 'Kensington' mango (Mangifera indica Linn.) following hot water and vapour-heat treatments. Postharv. BioI. Techno!. 1:349-359. Jacobi, K. K., L. S. Wong, and J. E. Giles. 1993. Lychee (Lichi chinensis Sonn.) fruit quality following vapour heat treatment and cool storage. Postharv. BioI. Techno!. 3:111-119.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULrURAL CROPS

115

Jacobi, K. K., L. S. Wong, and J. E. Giles. 1995b. Effects of fruit maturity on quality and physiology of high humidity hot air treated 'Kensington' mango (Mangifera indica Linn.). Postharv. BioI. TechnoI. 5:149-159. Jacobi, K. K., L. S. Wong, and J. E. Giles. 1996. Postharvest quality of zucchini (Cucurbita pepo L.) following high humidity hot air disinfestation treatments and cool storage. Postharv. BioI. TechnoI. 7:309-316. Jang, E. B. 1986. Kinetics of thermal death of eggs and first instar larvae of three species of fruit flies (Diptera: Tephritidae). J. Econ. Entomol. 79:700-705. Jang, E. B. 1991. Thermal death kinetics and heat tolerance in early and late third instars of the oriental fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 84:1298-1303. Jang, E. B. 1992. Heat shock proteins and thermotolerance in a cultured cell line from the Mediterranean fruit fly, Ceratitis capitata. Arch. Insect Biochem. Physiol. 19:93-103. Jang, E. B. 1996. Systems approach to quarantine security: postharvest application of sequential mortality in the Hawaiian grown 'Sharwil' avocado system. J. Econ. Entomol. 89:950-956. Jennings, P., and M. E. Saltveit. 1994. Temperature and chemical shocks induce chilling tolerance in germinating Cucumis sativus (cv. Poinsett 76) seeds. PhysioI. Plant. 91:703-707. Jessup, A. J. 1991. High temperature dip and low temperatures for storage and disinfestation of avocados. HortScience 26:1420. Jessup, A. J. 1994. Quarantine disinfestation of 'Hass' avocados against Bactrocera tryoni (Diptera: Tephritidae) with a hot fungicide dip followed by cold storage. J. Econ. Entomol. 87:127-130. Johnson, G. 1., A. J. Mead, A. W. Cooke, and J. R. Dean. 1992. Mango stern end rot pathogens-fruit infection by endophytic colonization of the inflorescence and pedicel. Ann. AppI. BioI. 120:225-234. Jones, W. M., B. C. Waddell, and J. H. Maindonald. 1995. Comparative mortality responses of three tortricid (Lepidoptera) species to hot water. J. Econ. EntomoI. 88:1356-1360. Joyce, D. C., and A. J. Shorter. 1994. High temperature conditioning reduces hot water treatment injury of 'Kensington Pride' mango fruit. HortScience 29:1047-1051. Kerbel,E. L., G. Mitchell, and G. Mayer. 1987. Effect of postharvest heat treatment for insect control on the quality and market life of avocados. HortScience 22:92-94. Kim, J. J., S. Ben-Yehoshua, B. Shapiro, Y. Henis, and S. Carmeli. 1991. Accumulation of scoparone in heat-treated lemon fruit inoculated with Penicillium digitatum Sacco Plant Physiol. 97:880-885. Klein, J. D. 1989. Ethylene biosynthesis in heat treated apples. pp. 184-190. In: H. Clijsters, M. de Proft, R. Marcelle and M. van Pouche (eds.). Biochemical and physiological aspects of ethylene production in lower and higher plants. Kluwer, Dordrecht, The Netherlands. Klein, J. D., J. A. Abbott, D. Basker, W. S. Conway, E. Fallik, and S. Lurie. 1997a. Sensory evaluation of heated and calcium treated fruits. Acta Hort.: 464. In press. Klein, J. D., W. S. Conway, B. D. Whitaker, and C. E. Sams. 1997b. Botrytis cinerea decay in apples is inhibited by postharvest heat and calcium treatments. J. Am. Soc. Hort. Sci. 122:91-94. Klein, J. D., J. Hanzon, P. L. Irwin, N. Ben-Shalom, and S. Lurie. 1995. Pectin esterase activity and pectin methyl esterification in heated Golden Delicious apples. Phytochemistry 39:491-494. Klein, J. D., and S. Lurie. 1990. Prestorage heat treatment as a means of improving poststorage quality of apples. J. Am. Soc. Hort. Sci. 115:256-259. Klein, J. D., and S. Lurie. 1991. Postharvest heat treatment and fruit quality. Postharv. News and Info. 2:15-19.

116

S. LURIE

Klein, J. D., and S. Lurie. 1992a. Heat treatments for improved postharvest quality of horticultural crops. HortTechnology 2:316-320. Klein, J. D., and S. Lurie. 1992b. Prestorage heating of apple fruit for enhanced postharvest quality: interaction of time and temperature. HortScience 27:326-328. Klein, J. D., S. Lurie, and R. Ben Arie. 1990. Quality and cell wall components of 'Anna' and 'Granny Smith' apples treated with heat, calcium and ethylene. J. Am. Soc. Hort. Sci. 115:954-958. Lafuente, M. T., A. Belver. M. G. Guye, and M. E. Saltveit, Jr. 1991. Effect of temperature conditioning on chilling injury of cucumber cotyledons. Plant Physiol. 95:443-449. Landolt, P. J., D. L. Chambers, and V. Chew. 1984. Alternative to the use of probit 9 as a criterion for quarantine treatments of fruit fly (Diptera: Tephritidae) infested fruit. J. Econ. Entomol. 77:285-287. Landry, J., D. Bernier, P. Chretien, L. M. Nicole, R. M. Tanguay, and N. Marceau. 1982. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res. 42:2457-2461. Lay-Yee, M., S. Ball, S. K. Forbes, and A. B. Woolf. 1997a. Hot water treatment for insect disinfestation and reduction of chilling sensitivity of 'Fuyu' persimmon. Postharv. BioI. Technol. 10:81-88. Lay-Yee, M., and K. J. Rose. 1994. Quality of 'Fantasia' nectarines following forced air heat treatments for insect disinfestation. HortScience 29:663-666. Lay-Yee, M., and D. C. Whiting. 1996. Response of 'Hayward' kiwifruit to high-temperature controlled atmosphere treatments for control of two-spotted spider mite (Tetranychus urticae). Postharv. BioI. Technol. 7:73-81. Lay-Yee, M., D. C. Whiting, K. J. Rose, and K. J. Spooner. 1997b. Response of apples to hightemperature controlled atmosphere disinfestation treatments. Acta Hort., 464 in press. Lazan, H., Z. M. Ali, K. S. Liang, and K. L. Yee. 1989. Polygalacturonase activity and variation in ripening of papaya fruit with tissue depth and heat treatment. Physiol. Plant. 77:93-98. Lester, P. L., P. R. Dentener, R. J. Petry, and S. M. Alexander. 1995. Hot-water immersion for disinfestation of lightbrown apple moth (Epiphyas postvittana) and longtailed mealy bug (Pseudococcus longispinus) on persimmons. Postharv. BioI. Technol. 6:349-356. Li, G., N. S. Peterson, and H. K. Mitchell. 1982. Induced thermal tolerance and heat shock protein synthesis in Chinese hamster ovary cells. Int. J. Radiat. Oncol. BioI. Phys. 8:63-67. Lindquist, S. 1986. The heat shock response. Annu. Rev. Biochem. 55:1151-1191. Lingle, S. E., G. E. Lester, and J. R. Dunlap. 1987. Effect of postharvest heat treatment and storage on sugar metabolism in polyethylene-wrapped muskmelon fruit. HortScience 22:917-919. Liu, F. W. 1978. Modification of apple quality by high temperature.}. Am. Soc. Hort. Sci. 103:730-732. Liu, X., J. A. Anderson, N. O. Maness, and B. Martin. 1996. Protein synthesis inhibitors block high temperature acclimation in bell pepper. HortScience 31:160-161. Lurie, S., E. Fallik, and J. D. Klein. 1996a. The effect of heat treatment on apple epicuticular wax and calcium uptake. Postharv. BioI. Technol. 8:271-277. Lurie, S., E. Fallik, A. Handros, and R. Shapira. 1997a. The involvement of peroxidase in resistance to Botrytis cinerea in heat treated fruit. Physio!. Molec. PlantPathoi. 50:141-149. Lurie, S., A. Handros, M. Ackerman, R. Shapira, and G. Zauberman. 1997c. Prestorage heat treatments of avocados. p. 31-37. In: S. Gazit (ed.), Proceedings of World Avocado Congress, Tel Aviv, Israel.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

117

Lurie, S., A. Handros, E. Fallik, and R. Shapira. 1996b. Reversible inhibition of tomato fruit gene expression at high temperature. Plant Physiol. 110:1207-1214. Lurie, S., and J. D. Klein, 1990. Heat treatment ofripening apples: differential effects on physiology and biochemistry. Physiol. Plant. 78:181-186. Lurie, S., and J. D. Klein, 1991. Acquisition of low temperature tolerance in tomatoes by exposure to high temperature stress. J. Am. Soc. Hort. Sci. 116:1007-1012. Lurie, S., and J. D. Klein. 1992a. Calcium and heat treatments to improve storability of 'Anna' apple. HortScience 27:36-39. Lurie, S., and J. D. Klein. 1992b. Ripening characteristics of tomatoes stored at 12°C and 2°C following a prestorage heat treatment. Scientia Hort. 51:55-64. Lurie, S., J. D. Klein, and R. Ben Arie. 1990. Postharvest heat treatment as a possible means of reducing superficial scald of apples. J. Hort. Sci. 65:503-509. Lurie, S., M. Laamim, Z. Lapsker, and E. Fallik. 1997b. Heat treatments to decrease chilling injury in tomato fruit. Effects on lipids, pericarp lesions and fungal growth. Physiol. Plant. 100:297-302. Lurie, S., and A. Nussinovich. 1996. Compression characteristics, firmness, and texture perception of heat treated and unheated apples. Int. J. Food Sci. Technol. 31 :1-5. Lurie, S., S. Othman, and A. Borochov. 1995. Effects of heat treatment on plasma membrane of apple fruit. Postharv. BioI. Techno!. 5:29-38. Lurie, S., and A. Sabehat. 1997. Prestorage temperature manipulations to reduce chilling injury in tomatoes. Postharv. BioI. Technol. 11:57-62. Lyons, J. M. 1973. Chilling injury in plants. Annu. Rev. Plant Physiol. 24:445-466. Mackey, M. A., and J. L. Roti Roti. 1992. A model of heat induced clonogenic cell death. J. Theor. BioI. 156:133-146. Maxie, E., G. Mitchell, N. Sommer, G. Snyder, and H. Rae. 1974. Effects of elevated temperatures on ripening of 'Bartlett' pear. J. Am. Soc. Hort. Sci. 99:344-349. McCollum, T. G., S. D'Aquino, and R. E. McDonald. 1993. Heat treatment inhibits mango chilling injury. HortScience 28:197-198. McCollum, T. G., H. Doostdar, R. T. Mayer, and R. E. McDonald. 1995. Immersion of cucumber fruit in heated water alters chilling-induced physiological changes. Postharv. BioI. Technol. 6:55-64. McDonald, R. E., T. G. McCollum, and E. A. Baldwin. 1996. Prestorage heat treatments influence free sterols and flavor volatiles of tomatoes stored at chilling temperature. J. Am. Soc. Hort. Sci. 121:531-536. McDonald, R. E., W. R. Miller, T. G. McCollum, and G. E. Brown. 1991. Thiabendazole and imazalil applied at 53°C reduce chilling injury and decay of grapefruit. HortScience 26:397-399. McGuire, R. G. 1991. Market quality of grapefruits after heat quarantine treatments. HortScience 26:1393-1395. McLaren, G. F., R. M. McDonald, J. A. Fraser, R. R. Marshall, K. J. Rose, and A. J. Ford. 1997. Disinfestation of New Zealand flower thrips from stonefruit using hot water. Acta Hort.: 464. In press. Mencarelli, F., B. Ceccantoni, A. Bolini, and G. Anelli. 1993. Influence of heat treatment on the physiological response of sweet pepper kept at chilling temperature. Acta Hort. 343:238-243. Miller, W. R., and R. E. McDonald. 1992. Postharvest quality of early season grapefruit after forced air vapor heat treatment. HortScience 27:422-424. Miller, W. R., R. E. McDonald, T. T. Hatton, and M. Ismail. 1988. Phytotoxicity to grapefruit exposed to hot water immersion treatment. Proc. Florida State Hort. Soc. 101:192-195.

118

S. LURIE

Mitcham, E. J., and R. E. McDonald. 1992. Effect of high temperature on cell wall modifications associated with tomato fruit ripening. Postharv. Bio!. Techno!. 1:257-264. Mitcham, E. J., and R. E. McDonald. 1993. Respiration rate, internal atmosphere, and ethanol and acetaldehyde accumulation in heat treated mango fruit. Postharv. Bio!. Techno!. 3:77-86. Moss, J. 1., and H. T. Chan. 1993. Thermal death kinetics of Caribbean fruit fly. J. Econ. Entomo!' 86:1162-1166. Moss, J. 1., and E. B. Jang. 1991. Effects of age and metabolic stress on heat tolerance of Mediterranean fruit fly (Diptera: Tephritidae) eggs. J. Econ. Entomo!. 84:537-541. Neven, L. G. 1994. Effects of combined heat treatments and cold storage on fifth instar codling moth (Lepidoptera: Tortricidae) mortality. J. Econ. Entomo!' 87:1262-1265. Neven, L. G., and E. Mitcham. 1996. CATTS: controlled atmosphere/temperature treatment system. A novel tool for the development of quarantine treatments. Am. Entomo!' 42:56-59. Neven, L. G., and 1. M. Rehfield. 1995. Comparison of prestorage heat treatments on fifth Instar codling moth (Lepidoptera: Tortricidae) mortality. J. Econ. Entomo!' 88:1371-1375. Neven, 1. G., L. M. Rehfield, and K. C. Shellie. 1996. Moist and vapor forced air treatments of apples and pears: effects on the mortality of fifth instar codling moth (Lepidoptera: Tortricidae). J. Econ. Entomo!' 89:700-704. Nishijima, K. A., H. T. Chan, S. S. Sanxter, and E. S. Linse. 1995. Reduced heat shock period of 'Sharwil' avocado for cold tolerance in quarantine cold treatment. HortScience 30:1052-1053. Nishijima, K. A., K. Miura, J. W. Armstrong, S. A. Brown, and B. K. S. Hu. 1992. Effect of forced, hot-air treatment of papaya fruit on fruit quality and incidence of postharvest diseases. Plant Dis. 76:723-727. Paull, R. E. 1990. Postharvest heat treatments and fruit ripening. Postharv. News and Info. 1:355-363N. Paull, R. E. 1994. Response of tropical horticultural commodities to insect disinfestation treatments. HortScience 29:988-996. Paull, R. E. 1995. Preharvest factors and the heat sensitivity of field grown ripening papaya fruit. Postharv. BioI. Technol. 6:167-175. Paull, R. E., and N. J. Chen. 1990. Heat shock response in field grown ripening papaya fruit. J. Am. Soc. Hort. Sci. 115:623-631. Paull, R. E., N. J. Chen, and H. van Gorsel. 1986. Ripening response of papaya fruit previously exposed to high temperatures. HortScience 21:811. Picton, S., and D. Grierson. 1988. Inhibition of expression of tomato ripening genes at high temperature. Plant Cell Envir. 11 :265-272. Plumbley, R. A., D. Prusky, and 1. Kobiler. 1993. The effect of hot-water treatment on the levels of antifungal diene and quiescence of Colletotrichum gloeosporioides in avocado fruits. Plant Path. 42:116-120. Porritt, S. W., and P. D. Lidster. 1978. The effect of prestorage heating on ripening and senescence of apples during cold storage. J. Amer. Soc. Hort. Sci. 103:584-587. Prusky, D. 1996. Pathogen quiescence in postharvest diseases. Ann. Rev. Phytopath. 34:413-434. Prusky, D., E. Fallik, 1. Kobiler, Y. Fuchs, G. Zauberman, E. Pesis, M. Ackerman, 1. Roth, A. Weksler, O. Yekutiely, A. Waisblum, A. Keinan, and G. Ofek. 1997. Hot water brush: a new method for the control of postharvest disease caused by Alternaria rot in mango fruits. Phytoparasitica 25:52. Rappel, 1. M., A. W. Cooke, K. K. Jacobi, and 1. A. Wells. 1991. Heat treatments for postharvest disease control in mangoes. Acta Hart. 291:362-371.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

119

Robertson, J. L., K. S. Smith, N. E. Savin, and R. J. Lavigne. 1984. Effects of dose selection and sample size on the precision of lethal dose estimates in dose-mortality regression. J. Econ. Entomol. 77:833-837. Rodov, V., S. Ben-Yehoshua, O. Fang, G. O'hallewin, and T. Castia. 1994. Accumulation of phytoalexins scoparone and scopoletin in citrus fruits subjected to various postharvest treatments. Acta Hort. 381:517-523. Rodov, V., S. Ben-Yehoshua, R. Albagli, and O. Q. Fang. 1995. Reducing chilling injury and decay of stored citrus fruit by hot water dips. Postharv. BioI. Technol. 5:119-127. Rodov, V., P. Burns, R. Fluhr, N. Ben Shalom, and S. Ben-Yehoshua. 1996. Induced local disease resistance in citrus mesocarp (albedo): accumulation of phytoalexins and PRproteins. p. 108. VIII Congress of Intntl. Soc. Citriculture, Abstracts, Sun City, South Africa. Roy, S., W. S. Conway, A. E. Watada, C. E. Sams, E. F. Erbe, and W. P. Wergin. 1994. Heat treatment affects epicuticular wax structure and postharvest calcium uptake in 'Golden Delicious' apples. HortScience 29:1056-1058. Sabehat, A., O. Weiss, and S. Lurie. 1996. The correlation between heat-shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol. 110:531-537. Saltveit, M. E. Jr. 1991. Prior temperature exposure affects subsequent chilling sensitivity. Physiol. Plant. 82:529-536. Sams, C. E., W. S. Conway. J. A. Abbott, R. J. Lewis, and N. Ben-Shalom. 1993. Firmness and decay of apples following postharvest pressure infiltration of calcium and heat treatment. J. Am. Soc. Hort. Sci. 118:623-627. Sanxter, S. S.. K. A. Nishijima, and H. T. Chan Jr. 1994. Heat treating 'Sharwil' avocado for cold tolerance in quarantine cold treatments. HortScience 29:1166-1168. Schirra, M.. and M. Mulas. 1995a. Influence of postharvest hot-water dip and imazalilfungicide treatments on cold-stored 'Oi Massa' lemons. Adv. Hort. Sci. 1:43-46. Schirra, M., and M. Mulas. 1995b. Improving storability of 'Tarocco' oranges by postharvest hot-dip fungicide treatments. Postharv. BioI. Technol. 6:129-138. Seo. S. T .. B. K. S. Hu, M. Komura, C. Y. Lee. and E. J. Harris. 1974. Dacus dorsalis: vapor heat treatment in papayas. J. Econ. Entomol. 67:240-242. Seymour, G. B., P. John, and A. K. Thompson. 1987. Inhibition of degreening in the peel of bananas ripened at tropical temperatures. II. Role of ethylene. oxygen and carbon dioxide. Ann. Appl. BioI. 110:153-161. Sharp. J. L. 1986. Hot-water treatment for control of Anastrepha suspensa (Diptera: Tephritidae) in mangos. J. Econ. Entomol. 79:706-708. Sharp. J. L. 1990. Immersion in heated water as a quarantine treatment for California stone fruit infested with the Caribbean fruit fly (Oiptera: Tephritidae). J. Econ. Entomol. 83:1468-1470. Sharp, J. L., and V. Chew. 1987. Time/mortality relationships for Anastrepha suspensa (Diptera: Tephritidae) eggs and larvae submerged in hot water. J. Econ. Entomol. 80:646-649. Sharp. J. L., and W. P. Gould. 1994. Control of Caribbean fruit fly (Diptera: Tephritidae) in grapefruit by forced hot air and hydrocooling. J. Econ. Entomol. 87:131-133. Sharp, J. L.. and R. G. McGuire. 1996. Control of Caribbean fruit fly (Diptera: Tephritidae) in navel orange by forced hot air. J. Econ. Entomol. 89:1181-1185. Sharp, J. L., M. T. Ouye. W. Hart. S. Ingle. G. Hallman, W. Gould, and V. Chew. 1989a. Immersion of Florida mangos in hot water as a quarantine treatment for Caribbean fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 82:186-188. Sharp, J. L., M. T. Ouye, S. J. Ingle. W. G. Hart, W. R. Erkerlin, H. H. Caledonia. J. Toledo, L. Stevens. E. Quintero, J. Reyes. and A. Schwarz. 1989b. Hot-water quarantine treat-

120

S. LURIE

ment for mangos from the state of Chiapas, Mexico infested with Mediterranean fruit fly and Anastrepha serpentina. J. Econ. EntomoI. 82:1663-1666. Sharp, J. L., and H. Picho-Martinez. 1990. Hot-water quarantine treatment to control fruit flies in mangoes imported into the United States from Peru. J. Econ. Entomo!. 83:1940-1943.

Shellie, K. c., M. J. Firko, and R. L. Mangan. 1993. Phytotoxic response of 'Dancy' tangerine to high temperature, moist, forced air treatment for fruit fly disinfestation. J. Am. Soc. Hort. Sci. 118:481-485. Shellie, K. C., and R. L. Mangan. 1994. Postharvest quality of 'Valencia' orange after exposure to hot, moist forced air for fruit fly disinfestation. HortScience 29:1524-1527. Shellie, K. C., and R. L. Mangan. 1996. Tolerance of red fleshed grapefruit to a constant of stepped temperature, forced air quarantine heat treatment. Postharv. Bio!. Techno!. 7:151-159.

Sherf, B. A., and P. E. Kolattukudy. 1993. Developmentally regulated expression of the wound and pathogen-responsive tomato anionic peroxidase in green fruits. Plant J. 3:829-833. Smilanick, J. L., B. E. Mackey, R. Reese, J. Usall, and D. A. Margosan. 1997. Influence of concentration of soda ash, temperature, and immersion period on the control of postharvest geen mold of oranges. Plant Dis. 81:379-382. Smilanick, J. L., D. A. Margosan, and D. J. Henson. 1995. Evaluation of heated solutions of sulfur dioxide, ethanol, and hydrogen peroxide to control postharvest green mold of lemons. Plant Dis. 79:742-747. Sozzi, G. 0., O. Cascone, and A. A. Fraschina. 1996. Effect of a high temperature stress on endo-f}-mannanase and a- and ~-galactosidase activities during tomato fruit ripening. Postharv. BioI. Techno!. 9:49-63. Sugimoto, T., K. Furusawa, and M. Mizobuchi. 1983. The effectiveness of the vapor heat treatment against the oriental fruit fly, Dacus dorsalis Hendel, in green pepper and fruit tolerance to the treatment. Res. Bu!. Plant Prot. Servo Japan 19:81-88. Sunigawa, K, K Kume, and R. Iwaizumi. 1987. Effect of vapor heat treatment against the melon fly, Dacus cucurbitae Coquillett, in mango and fruit tolerance to the treatment. Res. BuI. Plant Prot. Japan 23:13-20. Tian, M. S., T. Islam, D. G. Stevenson, and D. E. Irving. 1997. Color, ethylene production, respiration, and compositional changes in broccoli dipped in hot water. J. Am. Soc. Hort. Sci. 122:112-116. Tian, M. S., A. B. Woolf, J. H. Bowen, and 1. B. Ferguson. 1996. Changes in color and chlorophyll fluorescence of broccoli florets following hot water treatment. J. Am. Soc. Hort. Sci. 121:310-313. Tomasovic, S. P., and T. M. Koval. 1985. Relationship between cell survival and heat stress protein synthesis in a Drosophila cell line. Int. J. Radiat. BioI. 48:635-650. Tsuji, M., H. Harakawa, and Y. Komiyama. 1984. Changes in shelf life and quality of plum fruit during storage at high temperatures. J. Japan. Soc. Hort. Sci. 52:469-473. Vail, P. V., J. S. Tebbets, B. E. Mackey, and C. E. Curtis. 1992. Quarantine treatments: a biological approach to decision-making for selected hosts of codling moth (Lepidoptera: Tortricidae). J. Econ. EntomoI. 86:70-75. Vierling, E. 1991. The roles of heat shock proteins in plants. Annu. Rev. Plant Physio!. Plant Mo!. Bio!. 42:579-620. Wang, C. Y. 1994. Combined treatment of heat shock and low temperature conditioning reduces chilling injury in zucchini squash. Postharv. BioI. TechnoI. 4:65-73. Whitaker, B. D. 1994. A reassessment of heat treatments as a means of reducing chilling injury in tomato fruit. Postharv. BioI. TechnoI. 4:75-83. Whitaker, B. D., J. D. Klein, W. S. Conway, and C. E. Sams. 1997. Influence of prestorage heat and calcium treatments on lipid metabolism in 'Golden Delicious' apples. Phytochemistry. 45:465-472.

3. POSTHARVEST HEAT TREATMENTS OF HORTICULTURAL CROPS

121

Whiting, D. c., S. P. Foster, and J. H. Maindonald. 1991. The effects of oxygen, carbon dioxide, and temperature on the mortality responses of Epiphyas postvittana (Lepidoptera: Tortricidae). J. Econ. Entomol. 84:1544-1549. Whiting, D. c., S. P. Foster, J. van den Heuvel, and J. H. Maindonald. 1992. Comparative mortality responses of four Tortricid (Lepidoptera) species to a low oxygen-controlled atmosphere. J. Econ. Entomol. 85:2305-2309. Whiting, D. C., and L. E. Hoy. 1997. High temperature controlled atmosphere and air treatments to control obscure mealybug (Hemiptera: Pseudococcidae) on apples. J. Econ. Entomol.,90:546-550. Whiting, D. c., G. M. O'Connor, and J. H. Maindonald. 1996. First instar mortalities of three New Zealand leafroller species (Lepidoptera: Tortricidae) exposed to controlled atmosphere treatments. Postharv. BioI. Technol. 8:229-236. Whiting, D. c., G. M. O'Connor, J. van den Heuvel, and J. H. Maindonald. 1995. Comparative mortalities of six Tortricid (Lepidoptera) species to two high-temperature controlled atmospheres and air. J. Econ. Entomol. 88:1365-1370. Whiting, D. C., and J. van den Heuvel. 1995. Oxygen, carbon dioxide, and temperature effects on mortality responses of diapausing Tetranychus urticae (Acari: Tetranychidae). J. Econ. Entomol. 88:331-336. Wild, B. L. 1993. Reduction of chilling injury in grapefruit and oranges stored at 1°C by prestorage hot dip treatments, curing, and wax application. Austral. J. Expt. Ag. 33:495-498. Wild, B. L., and C. W. Hood. 1989. Hot dip treatments reduce chilling injury in long term storage of 'Valencia' oranges. HortScience 24:109-110. Woolf, A. B., and W. A. Laing. 1996. Avocado fruit skin fluorescence following hot water treatments and pretreatments. J. Am. Soc. Hort. Sci. 121:147-151. Woolf, A. B., and M. Lay-Yee. 1997. Pretreatments at 38°C of 'Hass' avocado confer thermotolerance to 50°C hot water treatments. HortScience. 32:705-708. Woolf, A. B., C. B. Watkins, J. H. Bowen, M. Lay-Yee, J. H. Maindonald, and I. B. Ferguson. 1995. Reducing external chilling injury in stored 'Hass' avocados with dry heat treatments. J. Am. Soc. Hort. Sci. 120:1050-1056. Worner, S. P. 1988. Ecoclimatic assessment of potential establishment of exotic pests. J. Econ. Entomol. 81:973-983. Yang, R. F., T. S. Cheng, and R. L. Shewfelt. 1990. The effect of high temperature and ethylene treatment on the ripening of tomatoes. J. Plant Physiol. 136:368-372. Yokoyama, V. Y., and G. T. Miller. 1987. High temperature for control of oriental fruit moth (Lepidoptera: Tortricidae) in stone fruits. J. Econ. Entomol. 80:641-645. Yokoyama, V. Y., G. T. Miller, and R. V. Dowell. 1991. Response of codling moth (Lepidoptera: Tortricidae) to high temperature, a potential quarantine treatment for exported commodities. J. Econ. Entomol. 84:528-531. Yoshida, 0., H. Nakagawa, N. Ogura, and T. Sato. 1984. Effect of heat treatment on the development of polygalacturonase activity in tomato fruit during ripening. Plant Cell Physiol. 25:505-509. Yu, Y. B., D. O. Adams, and S. F. Yang. 1980. Inhibition of ethylene production by 2,4dinitrophenol and high temperature. Plant Physiol. 66:286-290.

4 Modified and Controlled Atmospheres for Tropical Fruits* Elhadi M. Yahia DIPA, Facultad de Quimica, Universidad Aut6noma de Queretaro, Queretaro, 76010, Mexico.

1. Introduction II. Modified (MA) and Controlled (CA) Atmospheres A. CA Storage B. MA/CA for Transport C. MA Packaging (MAP) D. Low Pressure (LP. Hypobaric) Atmospheres E. Insecticidal Atmospheres (IA) F. Additional Treatments III. Potential Problems and Hazards of MA and CA IV. Fruit Review A. Avocado B. Banana and Plantain C. Cherimoya D. Durian E. Feijoa F. Guava G. Lanzon H. Loquat (Japanese plum, Japanese medlar) 1. Longan J. Lychee (litchi, litchee) K. Mango L. Mangosteen M. Papaya N. Passion fruit (yellow) o. Pineapple P. Rambutan

*1 thank Drs. Robert E. Paull. Jeffrey K. Brecht. Jules Janick, and two anonymous reviewers for their helpful reviews and comments. Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 123

124

E. YAHIA

Q. Sapodilla R. Sugar apple (custard apple, sweetsop)

S. Waxapple V. Conclusions Literature Cited

I. INTRODUCTION Until recently many tropical fruits were only grown in home gardens and small farms, primarily for local consumption. Currently several of these fruits are among the most important horticultural crops, and the market for these fruits has increased significantly in the last two decades. This is due to several factors, including changes in diet habits, demand for exotic articles, and improved technologies such as storage and transport. Although prices of agricultural commodities have been steadily declining in the last 20 years, tropical fruit prices have been rising (Buchanan 1994). The higher prices, improved technologies, and increased demand is resulting in increased plantings of many tropical fruits in several regions of the world. Tropical fruits are chilling sensitive (Wang 1990). Some types of avocado, as well as banana, breadfruit, cherimoya, jackfruit, marney, mango, mangosteen, papaya, pineapple, rambutan, sapota, soursop, white sapote, and yams are very sensitive to chilling injury (eI). Some types of avocados, as well as carambola, durian, feijoa, guava, sugar apple, and tamarillo are moderately sensitive (Table 4.1). The chilling sensitivity of tropical fruits does not permit their maintenance in low temperature, and as a consequence all these crops have a relatively short postharvest life compared to many temperate and subtropical fruits (Table 4.1). Most tropical fruits have a postharvest life of only a few weeks at the most. Modified (MA) and controlled atmospheres (CA) have been shown to ameliorate chilling sensitivity in several crops, including those of tropical origin (Wang 1990). The tropics are characterized by high temperature and relative humidity that favor the spread of insects and diseases. Some of the most important diseases that infect tropical fruits and cause major losses inClude anthracnose (caused by Colletotrichum gloeosprioides Penz.) and stem end rot (caused by Diplodia natalensis P. Evans). Anthracnose is the major postharvest problem in avocado, banana, guava, mango, and papaya, and contributes to most of their losses. MA/CA can control some decay either directly or indirectly by delaying ripening and senescence ofthe commodity, and thus maintaining the resistance to pathogen attack (EI-Goorani and Sommer 1981). Effective control of pathogens is

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

125

Table 4.1. Chilling sensitivity, recommended postharvest storage temperature, and postharvest life of some tropical fruits.

Fruit Avocado Carambola Banana Cherimoya Durian Feijoa Guava Loquat Lychee Mango Mangosteen Papaya Passion fruit Pineapple Rambutan Sapodilla Sugar apple ZN

Chilling sensitivityz

Ideal temp.

I-V y

4-13 5 12-16 8-10 4-6 5-10 5-10

V V

I

I-V I-V N N V

V

V I

I-V I-V V

I

(0C)

o 1

10-15 13 7-13 7-10 7-12 7-12 12-16 5-7

Postharvest life at optimum conditions (days) 14-28 21-28 7-28 14-28 21-49 14-21 14-21 21 21-35 14-28 14-28 7-21 14-21 7-21 7-21 14-21 28-42

= Not sensitive, I = Intermediate, V = Very sensitive.

essential for the postharvest maintenance of these crops, and for the successful application of MA/CA. Many insects infect tropical crops. Some of the most important include various species of fruit flies, such as the genus Ceratitis in several regions of the world, several Anastrepha species in South and Central America and the West Indies, and the genus Dacus in Africa and Asia. Quarantine treatments are needed in order to distribute tropical fruits around the world. Traditionally, chemical fumigants (mainly ethylene dibromide and methyl bromide) have been the principal treatments used for this purpose. However, ethylene dibromide has been banned (Federal Register 1984) because of health risks. Methyl bromide is still used for some crops, but with restrictions due to concerns about being a class Y ozone depleter. Several alternative physical treatments have been tested for disinfestation purposes. Low temperatures (0-2.2°C for 10 to 16 days) can be used for control of the Mediterranean fruit fly (Paull and Armstrong 1994). However, these temperatures cannot be used for most tropical fruit. Hot water treatments are being used in several countries to control fruit flies in mangoes (46.1°C for 65 to 90 min)

126

E. YAHIA

and papayas (2-stage heating process with temperatures of 42 for 30 min and 49°C for 20 min, fruit core temperature of 47.3°C) (Paull and Armstrong 1994). Vapor heat treatments have been developed and used (Fons 1990). Injuries have been reported in both mango and papaya fruits treated with heat (Paull and Armstrong 1994). Irradiation has proved potentially applicable for insect control in some tropical fruits such as mango and papaya (Paull and Armstrong 1994), however, no commercial application has been developed yet for this purpose due to several problems, including possible injury to the fruit, high costs, and consumer concerns. MA and CA (::; 1.0% O 2 and/or ~ 500/0 CO 2 ) have insecticidal and fungistatic effects, and the potential to be developed as disinfestation treatments (see below). Despite their postharvest problems (chilling sensitivity, disease and insect infestations, and short postharvest life), tropical fruit must be shipped to distant markets, usually by air or sea. Shipping times are long; for example, the minimum time required for sea freight from Eastern Australia is 21 days to South East Asia, 28 days to Japan and North America, and 42 days to Europe (McGlasson 1989). Minimum shipping time from Mexico is 18 days to Europe and 21 days to Japan (Yahia 1995). Therefore, it is essential to assure a sufficiently long postharvest life for these fruits to be able to be distributed in distant markets. Prolonged postharvest life requires adequate postharvest handling systems, such as optimum harvesting time, control of insects and diseases, and the use of ideal postharvest temperature management. MA and CA can be of major benefit to preserve the quality of these fruits and to prolong their postharvest life. There have been several excellent books and reviews on MA and CA emphasizing temperate (especially pome) fruits (Dewey et a1. 1969; Dewey 1977; Isenberg 1979; Smock 1979; El-Goorani and Sommer 1981; Richardson and Meheriuk 1982; Blankenship 1985; Kader 1986; Fellman 1989; Calderon and Barkai-Golan 1990; Blanpied 1993). In contrast, little research has been carried out on MA/CA of tropical fruits. For example, out of 5441 articles published on MA/CA of fruits and vegetables until May 1997 (Kader and Morris 1977; Kader and Morris 1981; Kader 1985; Zagory and Kader 1989,1993, Kader et a1. 1997), only about 60/0 (340 articles) were on tropical fruits and vegetables. The few reviews which have included information on MA/CA of tropical fruit (Hatton and Spalding 1990; Kader 1993) have been largely limited to mango, avocado, banana, pineapple, and papaya. Information on many of the minor tropical crops is either missing or dispersed in local journals and reports. The objective of this review article is to review published research data on MA/CA of tropical crops and to make valid conclusions and recom-

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

127

mendations on the appropriate commercial use of MA/CA. Suggestions for future research needs will be listed for each fruit in order to improve the application of MA/CA. II. MODIFIED (MA) AND CONTROLLED (CA) ATMOSPHERES

MA refers to atmospheres that differ from ambient air, whereas CA refers to strictly controlled atmospheres (Smock 1979; Kader 1986). MA and CA have several potential benefits for tropical fruit. These include retardation of maturation, ripening, and senescence (Hatton and Spalding 1990), alleviation and/or control of CI (Wang 1990), control of some pathogenic disorders (EI-Goorani and Sommer 1981), physiological disorders (Hatton and Spalding 1990), and insects (Shetty et al. 1989; Jang 1990; Ke and Kader 1992). Optimum gas composition for different products is very variable, and depends on many factors, such as type of product, physiological age, temperature, and duration of treatment (Isenberg 1979; Smock 1979). Exposure of horticultural products to Ozlevels below and/or COzlevels above their optimum tolerable range can cause the initiation and/or aggravation of certain physiological disorders, irregular ripening, increased susceptibility to decay, development of off-flavors, and could eventually cause the loss of the product (Kader 1986). Optimum levels of Oz and COz for long-term storage of some tropical fruits are listed in Tables 4.2 and 4.3. Most horticultural crops can tolerate extreme levels of gases when stored for only short periods (Table 4.4). MA and CA are not used during storage of tropical fruit, but are used for their transport, especially by sea. MA has been used for more than

Table 4.2. Classification of some tropical fruits according to their tolerance to low O2 during transport and/or storage for relatively long periods at optimum temperature and relative humidity. Minimum O 2 concentration tolerated (%) 2.0 3.0 5.0

Fruit Avocado, banana, mangosteen, papaya, pineapple Durian, mango, rambutan, sweetsop Cherimoya, lanzones, lychee, sapodilla, sugar apple

Source: Hatton and Spalding 1990; Kader 1993; Kader and Ke 1994; Yahia et a1. 1997; Yahia and Paull 1997.

128

E. YAHIA

Table 4.3. Classification of some tropical fruits according to their tolerance to high CO 2 during transport and/or storage for relatively long periods at optimum temperature and relative humidity. Maximum CO 2 concentration tolerated (%)

Fruit Lanzones Banana, mango Avocado, cherimoya mango, mangosteen, papaya, pineapple, sapodilla, sugar apple Rambutan Durian, lychee

0.0 5.0 10.0 12 20

Source: Hatton and Spalding 1990; Kader 1994; Kader and Ke 1994; Yahia et a1. 1997; Yahia and Paull 1997.

Table 4.4. Classification of some tropical fruits on the basis of their tolerance to extreme (insecticidal) atmospheres. Gases (%)

Temp (OC)

O2

CO 2

Tolerance (days)

Avocado

20 20

0.1-0.44 5-7.5

50-75 20-50

1 2

Guava Feijoa Mango

20 20 20

0.5

0.0 98

1 1

0.1-0.2

Papaya

20 20 20

2.0 0.5 0.2-0.4

Fruit

5

50 70-80

5

4 2

References Yahia 1993b; Yahia 1997; Yahia and Carrillo-Lopez 1993 Yahia 1997 Pesis et a1. 1991 Yahia 1993b; Yahia and Tiznado 1993; Yahia and Vazquez 1993 Yahia et a1. 1989; Yahia et a1. 1992

30 years during banana transport from Central America to the rest of the world. In the last few years, the use and interest in MA and CA has increased for many other tropical fruits.

A. CA Storage

CA storage technology does not seem to be as promising for many tropical fruits when compared to temperate fruits. This is due to several reasons, including those related to crop availability and quantity,

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

129

preharvest and postharvest handling, and availability of technology. Except for bananas, tropical crops cannot be stored for prolonged periods that would justify the use of CA. Although several reports (Hatton and Spalding 1990) indicate that MA/CA might have some beneficial effects for tropical crops, some of these positive results might be due to humidity rather than to MA/CA. Many factors should be considered when evaluating the potential application ofMA/CA; among them are fruit quantity and value, reason for the use of MA/CA (control of metabolism, control of pathogens, control of insects, etc.), availability of alternative treatments, competition with other production regions, type of market (local, distant, export), and type of preharvest and postharvest technology available in the region. Lougheed and Feng (1989) suggested that for a fruit to be compatible with the use of CA it should preferably be characterized by: (1) a long postharvest life; (2) resistance to CI; (3) a large range of non-injurious atmospheres; (4) resistance to fungal and bacterial attack; (5) adaptation to a humid atmosphere; (6) a climacteric fruit that can be ripened during or after storage; (7) absence of negative CA residual effect; and (8) the possibility that CA can reduce the production and effects of ethylene. Apple, a fruit very compatible to the use of CA, is a high valued fruit, produced in large quantities, and characterized by a climacteric respiration and a long postharvest life. In addition, the production and action of ethylene is controlled by CA, there exists a large variation in the tolerance levels for O2 and CO 2 , CA permits the use of lower storage temperatures in some cultivars, the fruit is relatively less infected by pathogens and insects compared to other fruits, especially those of tropical origin, some physiological disorders can be alleviated by CA, fruit can be harvested and stored in bulk, and a great deal of MA/CA research has been carried out. No tropical fruit, except banana, meets these qualifications. B. MA/CA for Transport MA/CA for transport has not been adequately covered in previous reviews. The many advances that have been accomplished in recent years indicate that transport in MA/CA is much more promising for tropical fruits than CA storage. Since transport periods of tropical crops can be relatively long (up to several weeks), MA/CA can be very helpful in maintaining fruit quality. The use of MA/CA can encourage the use of sea transport, since it is cheaper than air transport. Atmospheres for transport can be developed passively, semi-actively, or actively. Passive systems are MA regimes where the atmosphere is

130

E. YAHIA

modified by fruit respiration and the permeability of a barrier material. In the semi-active systems, one or more gases is/are added or withdrawn, most commonly at the beginning, but no strict control is carried out. Active systems imply a strict control of the atmosphere during the entire transport period. The most common systems for transport in the last 30 years have been developed on a semi-active basis. These systems are used for transport of bananas (Woodruff 1969a,b) and strawberries (Harvey 1977); though usually less efficient, they are less expensive than active systems. The use of CA for transport has been contemplated for several decades, however, several problems have hindered its success, including the unavailability of adequate gas-tight containers, suitable systems for gas control and analysis, and adequate CA-generating systems. Existing systems and companies before the late 1980s were unable to deliver on promised applications and benefits of CA transport. Liquid N z and pressure swing adsorption (PSA) systems were tried first to create and maintain CA systems in sea containers but were unsuccessful. The disadvantage of the PSA systems is the susceptibility of the carbon sieve to deterioration in high vibration environments (Malcolm 1993). Liquid N z has high boil-off rate and can run out in the middle of the ocean, making it difficult to refill, and thus the CA would be lost. In the late 1980s, the concept of CA transport became more practical due to the availability of gas-tight containers, adequate gas control systems, and the ability to establish and maintain controlled gas mixes. The use of air separation technologies in the late 1980s, especially the introduction of membrane technology in 1987, made CA transport practical and feasible (Malcolm 1989). The use of CA for transport of perishable commodities is now a practical reality. A CA container has the same features as that of a refrigerated container, in addition to a higher level of gas tightness, O2 and CO 2 control systems, and perhaps systems for control of ethylene and relative humidity (RH). CA systems for transport should be used when transport periods are long and/or fruit is very perishable. The "Oxytrol system," which was the first commercially available MA system (Lugg 1977), was developed by Occidental Petroleum Corporation, California. It is a self-contained system designed to be used as an adjunct in refrigerated transport vehicles. The main components of the system are an oxygen sensor, electronic analyzer-controller, liquid nitrogen storage tank, liquid nitrogen vaporizer, gas discharge nozzle, and peripheral equipment (White 1969). The liquid nitrogen tank can be filled before, during, or after loading. Liquid N2 is vaporized and warmed prior to injection into the transport vehicle. CO 2 is controlled using

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

131

hydrated lime. This system has been used for highway and sea shipments of lettuce, celery, papaya, and pineapple. "Tectrol" (total environment control) was developed and first used by Transfresh Corporation, California in 1969. For transport, tight refrigerated transport units (railroad, highway, or sea) are flushed with the desired pre-mixed gas blend and then sealed. The "Tectrol" unit consists of nitrogen tanks that are controlled to correct for the deviation of oxygen. This system was only satisfactory when oxygen was the only gas to be controlled, and the trip was short (Lugg 1969, 1977). Lime and magnesium sulfate are used to lower the concentration of CO 2 and C2 H4 , respectively. Some of the crops transported in this system include lettuce, strawberry, mango, and avocado. A newer Tectrol system includes a controller that monitors, controls, and records O2 and CO 2 , An interface system allows the controller to manage the container environment without external interference. The "CONAIR-PLUS" system (G+H Montage GmbH, Hamburg, Germany) can create a CA system through the introduction ofN 2 (generated under pressure) by means of a membrane from the ambient air to the container (Idler 1993). This system can also control CO 2 and ethylene. It has been used to transport apple, avocado, melon, and mango. The Maritime Protection division of Permea, Inc. (St. Louis, Missouri) developed the first membrane-based CA system (PRISM CAl in 1987. This system contains gas analyzers and computer microprocessors for establishing and maintaining the CA system. It was designed to be installed on the weather deck of a refrigerated ship, and to establish, monitor, and control CA conditions. After completion of the voyage, the system can be flown back to the port of origin in the cargo hold of a 747 aircraft (it is designed to occupy the same space as an LD-29 aircraft cargo container). The system was first used by the New Zealand Apple and Pear Board, then by Cool Carriers to transport apples (Malcolm 1993), and lately was used in some other ships (Parker 1993). Other systems such as Freshtainer (Maidstone, England) and NITEC (Spokane, Washington, USA) have been developed in the last few years.

c.

MA Packaging (MAP)

MAP refers to the development of a modified atmosphere around the product through the use of permeable polymeric films (Kader et al. 1989). MAP has been reported to maintain the quality of several tropical fruits (Macfie 1956; Scott and Roberts 1966; Scott et al. 1970; Oudit and Scott 1973; Scott 1975; Olorunda 1976; Salazar and Torres 1977; Scott and Chaplin 1978; Stead and Chithambo 1980; Brown et al. 1985;

132

E. YAHIA

Chaplin et al. 1986; Miller et al. 1986; Paull and Chen 1987; Mohamed and Othman 1988; Paull and Chen 1989; Sonsrivichai et al. 1989; Gonzalez et al. 1990; Ketsa and Leelawatana 1992; Satyan et al. 1992a; 1992b). MAP has also been reported to be advantageous in maintaining some minimally processed tropical fruits such as durian, jackfruit, mangosteen, papaya, and pineapple (Powrie et al. 1990; Siriphanich 1994). Reported results for MAP are very variable (Kader et al. 1989). Some of the reported beneficial effects of MA may be due to maintaining a humid atmosphere around the commodity, and not to gas modification. Variable results are due to the lack of experimental control. Many different types of polymers are used, although the most common are different types of polyethylene. Different thicknesses of the same type of film or different conditions (temperature and RH) surrounding the package result in different permeabilities and therefore different in-package atmospheres. Strict experimental control is essential in order for the different results to be compared adequately. Research reported on sealed polyethylene packages was carried out with one or more fruits, with different size packages, and without suitable experimental controls, all of which led to high variability in results. Some researchers assumed, without much basis, that packaging in sealed polyethylene bags can substitute for the use of ideal low storage temperatures (Chaplin et al. 1982). MAP is an inexpensive method compared to CA storage and transport, and therefore it has been suggested as an alternative to shipping in MA/CA (McGlasson 1989). MAP may not be appropriate during transport, especially during long-term sea transport, due to variation in temperature that would lead to water condensation inside the packages, changes in the permeability of packaging films, and thus changes in the package atmosphere. Many factors must be considered when trying to develop a MAP system, including type, thickness, and method of fabrication of film; package size; temperature; humidity; length of storage; type, quantity, and physiological stage of fruit; and tolerance of each fruit to the different gases (Oz, CO z, CZH 4 ). Water-saturated atmosphere around the commodity favors the development of decay pathogens. In addition, there is usually an accumulation of ethylene inside packages (Gonzalez et al. 1990; Yahia and Rivera-Dominguez 1992). Films used for tropical crops should be characterized by a relatively higher permeability to gases and to water vapor. There is a need for effective disease control treatments (Yahia and Rivera-Dominguez 1992), and practical and effective methods for absorbing water and ethylene in the packages (Yahia and Rivera-Dominguez 1992, Kader et al. 1989). MAP should be used properly and only as a complement to ideal postharvest handling, including optimum storage temperature. Very active research is being car-

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

133

ried out, and commercial interest is rising, especially for minimally processed products. More theoretical research is still needed to study gas exchange characteristics of different crops, and ideal packaging materials with respect to gases and to water vapor permeabilty for tropical crops.

D. Low Pressure (LP, Hypobaric) Atmospheres LP refers to holding the commodity under a reduced pressure, generally less than 200 mm Hg. In this system, the O 2 concentration is reduced proportionately with the atmospheric pressure. LP has been reported to extend the storage and shelf life of several crops (Gemma et a1. 1989), including mango (Burg and Burg 1966; Burg 1975; Apelbaum et a1. 1977c; Spalding 1977a; Spalding and Reeder 1977; Ilangantileke and Salokhe 1989), avocado (Burg and Burg 1966; Burg 1975; Spalding and Reeder 1976a; 1976b; Apelbaum et a1. 1977b; Spalding 1977a), banana (Burg and Burg 1966; Burg 1975; Apelbaum et a1. 1977a), papaya (Alvarez 1980; Chau and Alvarez 1983), and cherimoya (Plata et a1. 1987). LP systems were used commercially for a short period in the 1970s for the transport of some food products, including meats, flowers, and fruits (Burg 1975; Byers 1977). However, this system is more expensive than the traditional MA/CA systems. Furthermore, some fruits require other gases that cannot be administered during low pressure storage. For example, CO 2 is an important component in an adequate atmosphere for avocado (Spalding and Reeder 1976a; Spalding 1977a), but cannot be easily increased in a LP system. Currently, this system is not used commercially for tropical fruits and vegetables.

E. Insecticidal Atmospheres (IA) Atmospheres with very low O2 content ($ 1.0 0/0) and/or very high CO 2 levels (~50%) have insecticidal effects (Kader and Ke 1994; Yahia et a1. 1997). Insect control with MA and CA depends on the O2 and CO 2 concentration, temperature, RH, insect species and development stage, and duration of the treatment. The lower the O 2 concentration, the higher the CO 2 , the higher the temperature, and the lower the RH, the shorter the time necessary for insect control (Kader and Ke 1994). MA and CA have several advantages in comparison with other means used for insect control. These are physical treatments that do not leave toxic residues on the fruit, and are competitive in cost with chemical fumigants (Soderstrom et a1. 1984). MA and CA do not accelerate fruit ripening and

134

E. YAHIA

senescence as compared to the use of high temperatures, and have better consumer acceptance than irradiation. Wrapping of fruits in semipermeable shrink-wrap films for 3 to 6 days was reported to control some fruit flies (Shetty et al. 1989; lang 1990). Shetty et al. (1989) reported that shrink-wrap significantly reduced survival of oriental fruit fly (Dacus dorsalis Hendel) eggs and first instar larvae in infested papaya in 96 hours, and larvae of Drosophila melanogaster in mango in 72 h. However, fruit remain infested if not properly wrapped. In order to establish quarantine insect treatments for short periods of times, extreme gas concentrations (~0.5% Oz and/or ~ 50% COz) should be implemented at high temperatures (~ 20°C). Some fruits do not tolerate these treatments. For example, 'Hass' avocado are injured when exposed to these atmospheres for more than one day at 20°C (CarrilloLopez and Yahia 1990; Yahia 1997; Yahia and Kader 1991; Yahia and Carrillo-Lopez 1993; Ke et al. 1995). The basis for sensitivity or tolerance of fruit to insecticidal atmospheres is still unknown (Ke and Kader 1992; Yahia 1993b; Kader and Ke 1994; Ke et al. 1995). Differential scanning calorimetry did not show any differences between sensitive (avocado) and tolerant (mango) tissues (Yahia and Rivera-Dominguez (1995). Application of insecticidal atmospheres at high temperatures can accelerate the mortality of insects. 'Manila' and 'Oro' mangos treated with a combination of dry-forced heat at 44°C and insecticidal CA (0.7 % Oz and 67% CO 2) for 160 min resulted in 100% mortality of eggs and third instar larvae of Anastrepha ludens and A. obliqua without causing fruit injuries (Yahia et al. 1997). There is no current commercial use of insecticidal atmospheres for horticultural crops. However, treatments with MA/CA alone or in combination with other treatment(s) (such as cold or heat) are now being evaluated as a means of commercial insect control for tropical fruits (Kader and Ke 1994). F. Additional Treatments

Carbon monoxide added to MA and CA provide several advantages for the control of pathogenic diseases and insects (Woodruff 1977; ElGoorani and Sommer 1981), and tissue browning and discoloration (Kader 1986). The potential use of CO with tropical fruits is dependent upon the development of safe methods of application before any commercial use can be considered. CO increases the production of CZH4 at low but not at high concentrations (Woodruff 1977). CO appears to be more effective for fruits that tolerate elevated CO 2 ,

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

135

Ethylene removal during transport and storage of tropical crops can be beneficial in delaying ripening. Further studies are needed to investigate the potential benefits and feasibility of ethylene removal.

III. POTENTIAL PROBLEMS AND HAZARDS OF MA ANDCA Despite the long list of potential benefits and advantages of MA and CA for tropical fruit, there are several potential problems and hazards. Inadequate atmospheres can aggravate or initiate physiological disorders and fermentation in intact fruit (Kader 1986), and can increase microbial growth on minimally processed products. MA and CA can be injurious and even deadly to humans entering a room or a container without proper safety equipment or before the room or container has been properly ventilated. MA and CA can cause structural damage to rooms and containers that lack proper pressure relief systems or as the result of improper combustion of gases such as propane used to generate the atmosphere.

IV. FRUIT REVIEW A. Avocado (Persea americana Mill) The avocado is a climacteric fruit rich in energy. There are three ecological races including Mexican (subtropical), Guatemalan (semitropical), and West Indian (tropical). The most important cultivars are 'Hass', a Guatemalan self-fertile cultivar, and 'Fuerte', a hybrid between the Mexican and Guatemalan races. Anthracnose and CI are the most important causes of postharvest losses. Postharvest life is about 2 to 4 weeks at 4 to 13°C (depending on cultivar). Extensive work has been done on MA/CA of avocado, both to extend the storage life and to characterize responses to MA/CA. Avocado has been a favorite system to use in studying the physiological and metabolic effects of MA/CA on fruit (Young et a1. 1962; Biale and Young 1981; Kanellis et al. 1989a; b; c; Yahia and Carrillo-Lopez 1993; Ke et a1. 1995). Very early research by Overholser (1928) reported that the storage life of 'Fuerte' avocados was prolonged one month in an atmosphere of 4 to 5% O 2 and 4 to 5% CO 2 at 7.5°C compared to air storage. Brooks et al. (1936) reported that fruit could be held in atmospheres containing 20 to 50% CO 2 at 5 to 7.5°C for 2 days without causing any injury. Atmos-

136

E. YAHIA

pheres with CO 2 levels below 3% prolonged the storage life of Florida avocado at all temperatures, and reduced the development of brown discoloration of the skin (Stahl and Cain 1940). Extensive studies performed on 'Fuerte' at the University of California at Los Angeles indicated that the time for the fruit to reach the climacteric is extended in proportion to the decrease in O 2 concentration from 21 to 2.5% (Biale 1942; 1946). In later years, Young et a1. (1962) demonstrated that the delay of the climacteric could also be achieved by 100/0 CO 2 in air, and the combination of low O2 and high CO 2 further suppresses the intensity of fruit respiration. Hatton and Reeder (1965, 1969b, 1972) and Spalding and Reeder (1972, 1974) found that a CA of 2% O 2 plus 10% CO 2 at 7.5°C doubled the storage life of the cultivars 'Lula', 'Fuch', and 'Booth 8'. The percentage of acceptable fruit after storage increased by absorption of ethylene during CA storage (Hatton and Spalding 1974). 'Hass' fruits can be stored for up to 2 months, and 'Reed' for up to 3 months in CA (Sive and Resnizky 1989a). 'Hass' fruits remained firm and unripe for 7 to 9 weeks in CA of 2-100/0 O 2 plus 4-10% CO 2 at 7°C (Jordan and Smith 1993). Below 40/0 CO 2 storage life was 5 to 6 weeks. A mixture of 2% O 2 plus 10% CO 2 extended the shelf life and reduced the gray pulp and virtually eliminated pulp spot of 'Fuerte', 'Edranol', and 'Hass', but increased anthracnose (Truter and Eksteen 1987a,b). Metzidakis and Sfakiotakis (1995) observed two physiological disorders in 'Hass' fruit after storage for 10 days in 20/0 or 1% 02' The first was characterized by white specks in the outer layer of the epidermis, with no flesh damage, and the second appeared as brown areas in the epidermis near the stem that formed cavities in the flesh and caused abnormal ripening. Truter and Eksteen (1987b) found that a 25% CO 2 shock treatment applied one day after harvest reduced physiological disorders without any increase in anthracnose. Ripening of 'Fuerte' fruit was delayed using a 25% CO 2 shock treatment applied in pulses three times every 24 h (Allwood and Wolstenholme 1995). Intermittent exposure to 20% CO 2 of 'Hass' fruit stored in air delayed senescence at 12°C, reduced CI at 4°C, and controlled decay at both temperatures (Marcellin and Chavez 1983). CA delays the softening process, and thus maintains the resistance of the fruit to fungal development (Spalding and Reeder 1975). Prusky et a1. (1991b, 1993) reported that 30% CO 2 (with 15% 02) for 24 h increased the levels of the antifungal compound l-acetoxy-2-hydroxy-4-oxo-heneicosa-12, 15-diene in the peel and flesh of unripe avocado fruits, and delayed decay development. This diene has been suggested as the basis for decay resistance in unripe avocados (Prusky et a1. 1982,1988, 1991a). Prusky et a1. (1993) reported that treatment with 0.75 % O 2 and 30% CO 2

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

137

induced a two-peak increase similar to that observed after treatment with 30% COz and 15% 0z, and thus concluded that high COz, and not low 0z' is the cause of the sequence of events leading to the diene increase. The high concentration of COz increased the activity of phenylalanine ammonia lyase (PAL) in the fruit peel, enhanced the messenger RNA expression of the gene encoding for PAL activity, and increased the concentration of the soluble phenolic epicatechin (Prusky et al. 1985, 1988,1993). High (20%) COz can be tolerated by thick-skinned avocados such as 'Hass' and 'Lula', but causes browning of the skin in thinskinned cultivars such as 'Ettinger' (Collin 1984). High concentrations of CO (5 to 10%) added to CA can reduce decay development (EIGoorani and Sommer 1981). Moderately high concentrations of COz (up to 10%) ameliorate CI in 'Taylor' avocado (Vakis et al. 1970). Spalding and Reeder (1972) found less internal and external CI in CA than in air storage of 'Booth 8' and 'Lula' fruits. Intermittent high COz treatment (three treatments during 21 days) reduced CI symptoms (Marcellin and Chaves 1983). 'Fuerte' fruits have less pulp spot and blackening of cut vascular bundles after storage in 2% Oz plus 100/0 COz at 5.5°C for 28 days, or after a "shock" treatment of 25% COz at 5.5°C for 3 days and an additional 28 days at normal atmosphere at 5.5°C (Bower et al. 1990). Fruit receiving the shock treatment tended to have a lower activity of polyphenol oxidase and total phenol content. Spalding (1977a) concluded that the COz must be kept below 15% to prevent other fruit injury. Prestorage of 'Fuerte' fruit in 3% Oz (balance N z) for 24 h at 17°C significantly reduces CI symptoms after storage at 2°C for 3 weeks, with fruit having lower respiration and ethylene production, lower ion leakage, higher reducing power (expressed as SH groups, mainly cysteine and glutathione), and longer shelf life than the untreated fruit (Pesis et al. 1993, 1994a). The authors suggested that N 2 reduces CI by maintaining a higher antioxidant defense and membrane integrity. 'Booth 8' and 'Lula' avocados can be held for up to 8 weeks in 2% Oz with 10% CO 2 at 4 to 7°C and 98 to 100% RH. Removal of ethylene further improved the keeping quality of the 'Lula' fruit (Spalding and Reeder 1972). Fruit of 'Booth 8' had slight CI at 4.5°C. 'Fuerte' and 'Anaheim' fruit were stored in Brazil for up to 38 days in 6% O 2 plus 10% CO 2 at 7°C, but only for 12 days in air (Bleinroth et al. 1977a). Storage of 'Waldin' and 'Fuchs' fruit in 2% O 2 plus 10% CO 2 at 7°C for up to 4 weeks prevented development of anthracnose and CI (Spalding and Reeder 1974, 1975). 'Hass' fruit could be stored for up to 60 days in atmospheres of 2% O 2 plus 5% COz (Faubion et al. 1992; Jordan and Barker 1992; McLauchlan et al. 1992). Four commercial CA rooms were

138

E. YAHIA

constructed in Florida in the 1972/73 season for storage of 'Lula' fruit in bulk bins (Spalding and Reeder 1974). The rooms were run at 20/0 oz plus 10% COz at 7.2°C and 95% RH, and fruit were marketed in excellent condition after 5 weeks of storage, except for some fruit with rind discoloration (due to CI) where the temperature dropped below 4.4°C. In South Africa, Bower et a1. (1989) suggested that even though fruit stored in CA (2% Oz plus 10% COz) are superior to those in other storage systems, CA storage of avocados is not economical and does not fit logistically in the current marketing system. 'Hass' avocados sealed in polyethylene bags of unknown characteristics and stored at 20 or 30°C for 4 to 11 days stayed firmer and apparently did not ripen while in the bags (Chaplin and Hawson 1981). Atmospheres developed in the bags were 2.4 to 6.2% 0z, 6.5 to 8.9% COz, and 0.1 to 12.7 ppm of ethylene. The presence ofKMn0 4 in the bags had no effect on Oz and CzH4 1evels, but significantly decreased the COz levels. The COz is absorbed by the activated alumina (AI z0 3 ) used as the KMn0 4 support. The failure of the KMn0 4 to reduce the CzH4 concentration is probably due to high temperature. Abnormal ripening was observed when the storage temperature was high and the period exceeded 8 days. 'Hass' and 'Fuerte' fruit individually sealed in polyethylene bags (0.05 mm thickness) and stored at 4 or 7.5°C showed little or no CI symptoms compared to control fruit (Scott and Chaplin 1978). The atmosphere inside these bags had 3 to 70/0 COz, 2 to 6% 0z, and up to 2.5 ppm of CzH4 • Oudit and Scott (1973) reported a considerable extension in the storage life of 'Hass' avocados sealed in polyethylene bags. 'Hass' fruit sealed in polyethylene bags (0.015 to 0.66 mm) ranging in permeance from 111 to 605 cc Oz . m Z • hr z . atm- 1 , and from 0.167 to 0.246 gr HzO . m- z . hr- 1 . atm- 1 and stored at 5°C for up to 4 weeks lost less weight and firmness compared to unsealed fruits (Gonzalez et a1. 1990). Bags with the lowest permeance maintained the lowest 0z, the highest COz atmosphere, and resulted in the least loss in firmness. Initial modification ofthe atmosphere by introducing COz and N z into the packages immediately after sealing reduced the accumulation of CZH4 , but had no significant additional benefits due to the short period in which the initially modified atmosphere was maintained. Decay development in fruit sealed in polyethylene bags is considered to be a problem by some researchers (Aharoni et a1. 1968), but not by others (Thompson et a1. 1971). Fruit halves of 'Fuerte' packaged in 10 x 25 em nylon polyethylene laminate bags (permeance 0.5-0.6 g HzO . 635cm- z . 24h-1 at 38°C and 100% RH, and 3-6 Oz cm 3 . m-z . 24h- 1 at 3°C and 0% RH) with air, vacuum, or a gas mix containing 50/0 CO, 15% Oz and 80% COz for 21 days at 7.2°C had no differences in mesocarp

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

139

browning, and the gas mix had the highest anaerobic and psychotrophic plate counts (Gerdes and Parrino-Lowe 1995). Fruit of 'Booth 7' coated with "NatureSeal," a polysaccharide-based edible film, and stored at 20°C ripened 2 days later than the control, even when treated with 100 ppm ethylene for up to 3 days, but treatment with ethylene for 4 days overcame the ripening delay (Bender et al. 1993). The internal atmosphere of uncoated fruit was 15.2% O 2 and 3.7% CO 2 , while it was 10.2% O2 and 10.1 % CO 2 in coated fruit. Coating with "NatureSeal" is ineffective once the onset of ethylene production occurs. Coating 'Fuerte' avocados with a 12% water emulsion of polyethylenebased wax and storage for 14 days at 5°C did not significantly modify the internal 0z, CO 2 , and C2H4 concentrations, and had little effect on fruit softening (Durand et al. 1984). The storage life of avocado fruit held in low pressure storage depends on their susceptibility to decay and to CI. LP, especially below 100 mm Hg, markedly prolonged the storage life of 'Hass' fruit (Apelbaum et al. 1977b). For example, fruit stored in 60 mm Hg at 6°C remained unripe for 70 days, showed no adverse effects, and ripened normally after transfer to normal atmospheric pressure at 14°C. However, storage of fruit in 50 mm Hg caused substantial fruit desiccation. Optimum conditions for low pressure storage of Florida avocado is 20 mm Hg at 4.5°C (Spalding and Reeder 1976a; Spalding 1977a). Fruits held in these conditions for up to 3 weeks were firmer and had less decay and CI than fruit held in 76 or 760 mm Hg. However, gases such as CO 2 and CO cannot be added when a LP system is used. CO 2 is considered to be essential for control of decay and to ameliorate CI in avocados. This limitation is considered to be the main impediment for the commercialization of LP for 'Booth 8', 'Lula', and 'Waldin' (Spalding and Reeder 1975). Spalding (1977a,b) concluded that the LP system should not be recommended commercially for avocado contrary to the results of Burg (1975) and Apelbaum et al. (1977b). Fruit of several cultivars (Taylor, Booth 7, Booth 8, Hickson, Lula, Waldin) stored in 2% O2 plus 10% CO 2 at 4.5 to 7.2°C for up to 7 weeks had less pectinesterase (PE) activity (Barmore and Rouse 1976). The authors suggested that PE activity could be used to monitor changes in softening time during CA storage. Storage of 'Hass' avocados in 2.5% O 2 suppressed the cellulase activity, and produced an alteration in the profile of fruit total protein, causing no effect, suppression, enhancement or induction of various new polypeptides (Kanellis et al. 1989b). Storage of 'Hass' avocados in 2.5-5.0% 0z, suppressed the activity of ripening enzymes such as cellulase and polygalacturonase at the protein level as well as at the mRNA level, and induced the synthesis of new isoen-

140

E. YAHIA

zymes of alcohol dehydrogenase (ADH) (Kanellis et a1. 1991). Low Oz levels (0, 1, 3, 5, and 10%) for 48 h induced the appearance of new, as well as an increase in staining intensity of pre-existing polypeptides in both preclimacteric and propylene-initiated 'Hass' fruit, but suppressed polypeptides in ripening fruit (Kanellis et a1. 1993). Low Oz (0 to 5%) caused a suppressive effect on pre-existing mRNA in preclimacteric or initiated fruit, but caused an evident repressive effect on newly synthesized ripening mRNA (Kanellis et a1. 1993). Induction of specific protein synthesis and gene expression take place in 'Hass' fruit stored in 0 to 5% Oz (Kanellis et a1. 1993). ADH, lactate dehydrogenase (LDHJ, and glucose phosphate isomerase (GPI) isoenzymes are expressed in low Oz in both preclimacteric and initiated avocado fruit, and the increase in ADH protein corresponds to elevated ADH-mRNA levels. 'Hass' fruit maintained in MA (0.1 to 0.44% 0z, 50 to 75% CO z, balance N z) for up to 5 days at 20°C had higher CO z production compared to fruit stored in air, most likelyreflecting anaerobiosis (Carrillo-Lopez and Yahia 1990; Yahia 1993b; Yahia and Carrillo-Lopez 1993). Fruit stored in this MA and then ripened in air had mesocarp and exocarp injury after 2 days. Storage for 2 days in MA decreased the concentration of glucose 3-phosphate, fructose 3-phosphate, and 2-phosphoglycerate, while the concentration of glyceraldehyde 3-phosphate, 1,3-bisphosphoglycerate decreased after storage for 5 days. Cross-over plots for changes in the concentration of the glycolytic intermediates between air and MA did not show significant effects of MA on control sites (Carrillo-Lopez and Yahia 1990). On the basis of these results, Yahia (1993b) and Yahia and Carrillo-Lopez (1993) concluded that 'Hass' fruit is very sensitive to insecticidal atmospheres, tolerating only one day at 20°C. These findings were confirmed later by Yahia and Kader (1991) and Ke et a1. (1995). Biale and Young (1981) stated that avocado is very sensitive to anaerobic conditions, unlike other fruits that can switch to fermentative metabolism when deprived of Oz. CA injury in avocado is aggravated by the combining effect of low Oz and high CO z' For example, rind injury in 'Lula' appeared in fruits held for 3 days in 0.5% Oz plus 25% CO 2 , was very slight in 0.5% Oz plus 0% CO z, and absent in 21 % Oz plus 250/0 CO z (Spalding and Marousky 1981). 'Hass' fruit kept in 0.25% Oz alone or in combination with 80% CO 2 for 3 days at 20°C had higher concentrations of acetaldehyde and ethanol, increased NADH, and decreased NAD levels than the control (Ke et a1. 1995). 'Hass' fruit has a cytoplasmic pH of 6.9 in air, while storage in 0.25% 0z, 80% COz, or the combination of both, decreased the pH value to 6.7, 6.3, and 6.3, respectively (Hess et a1. 1993). The optimum pH for pyruvate decarboxylase (PDC) is about 6.0-6.5 (Ke et a1. 1995),

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

141

and thus the decrease in cytoplasmic pH reported by Hess et al. (1993) would activate this enzyme. The decrease in pH would also inhibit pyruvate dehydrogenase (PDH), and affect the activity of LDH and ADH (Ke et al. 1995). Exposure of the fruit to 0.25% O2 ,80% CO 2 , or a combination of both reduced ATP level by 20%,22%, and 63%, respectively (Hess et al. 1993). Exposure of 'Hass' fruit to 25% or 75% CO 2 for up to 105 h at 25°C enhanced the capacity of their mitochondria to restore energy-linked functions, whereas exposure to 100% N2 causes irreparable damage (Moriguchi and Romani 1995). Ke et al. (1995) proposed a mode of action for the effects of very low O2 stress on fermentative metabolism in avocado fruit. Low O 2 substantially reduces NADH flux through the electron transport system, and as a result NAD and ATP levels decrease and NADH level increases. Cytoplasmic pH is decreased to the level where PDH activity is decreased or inhibited, and pyruvate flux through the TCA cycle is decreased. PDC activity is increased due to changes in cytoplasmic pH leading to an increase in pyruvate concentration. A new ADH isoenzyme is induced, and thus acetaldehyde and ethanol are produced from pyruvate. LDH activity is increased due to the increase in pyruvate and NADH concentrations, and the decrease in NAD and ATP levels, and thus lactate is accumulated. The accumulation of fermentative products (ethanol, acetaldehyde, and lactate), the energy shortage, and the modification of normal metabolism may be the cause of injury in fruits exposed to low O2 stress. MA has been used during marine shipment of avocado from several countries, including Mexico, South Africa, and Chile (Spalding and Marousky 1981; Eksteen and Truter 1985; 1989; Eksteen et al. 1992; Yahia 1995). Some shipments have failed in the past. The recent improvement in MA and CA during transport has solved some problems and the quantity of fruit shipped in these systems is increasing. Optimum atmosphere composition for long-term storage and for transport is about 2 to 5% O 2 and 3 to 10% CO 2 , These atmospheres delay ripening and reduce CI. Avocados are, however, very sensitive to insecticidal atmospheres. Further research is needed to investigate the potential benefits and applications of CA for storage of avocado. Studies are still needed to reveal the basis of avocado sensitivity to insecticidal atmospheres and to find ways to ameliorate this effect. B. Banana and Plantain (Musa spp)

Bananas and plantain are climacteric fruits and among the most important in world trade. Postharvest life is about 4 weeks at 12-16°C. Crown

142

E. YAHIA

rot, anthracnose (caused by Colletotrichm musae), "cigar end" stylar rot, and CI are the major causes of postharvest losses. MA/CA can extend the storage life of green bananas (Mapson and Robinson 1966; Scott and Roberts 1966; Smock 1967; Badran and Lima 1969; Woodruff 1969b; Liu 1970; Quazi and Freebairn 1970; Scott et a1. 1970; Fuchs and Temkin-Forodeiski 1971; Scott 1971; Duan et a1. 1973; Scott and Gandanegara 1974; Burg 1975; Scott 1975; Liu 1976a; 1976b; Scott and Chaplin 1978; Brown 1981; Shorter et a1. 1987; Satyan et a1. 1992a, 1992b; Banks 1984a; Hesselman and Freebairn 1986; Kanellis et a1. 1989a). Bananas are most responsive to MA/CA when the fruit are in the preclimacteric stage (Smock 1979). Optimum atmospheres differ for different cultivars ranging from about 2 to 5% O 2 plus 2 to 5% CO 2 at the optimum of 13°C (Woodruff 1969b). Plantains (cooking bananas) have similarCA requirements (Satyan et a1. 1992b). An atmosphere containing 5% O2 plus 5% CO 2 was found to be suitable for 'Gras Michel' fruit held for 20 days at 12°C (Wardlaw 1940). 'Lacatan' and 'Dwarf Cavendish' fruit were kept for 3 weeks in 6 to 8% CO 2 plus 2% O2 at 15°C (Smock 1967). The recommended atmosphere for two Malaysian cultivars at 20°C and 80% RH was 5 to 10% CO 2 with a continuous removal of ethylene (Broughton and Wu 1979). An atmosphere with 10/0 O 2 inhibits ripening in green bananas and is considered to be the low limit at 15.5°C (Parsons et a1. 1964). Concentrations of O 2 less than 1% cause fruit injury, symptoms of which include dull yellow to brown skin discoloration, failure to ripen, flaky gray flesh, and off-flavor (Parsons et a1. 1964). However, 1% O 2 was reported by other researchers (Mapson and Robinson 1966; Chiang 1970) to result in poor quality and more stalk rot. Hesselman and Freebairn (1986) found that O 2 levels less than 2.5% affect the taste of 'Valery' fruit. A CO 2 concentration higher than 5% was reported to result in undesirable flavor and texture after fruit ripening (Woodruff 1969b), though 10% is considered to be the upper limit for 'Gros Michel' (Gane 1936). Experiments were conducted with s.torage of bananas in sealed CA rooms (Woodruff 1969b). The rooms were flushed with N 2 to reduce the O 2 level and supplemental CO 2 was added. A CO 2 scrubber (water scrubbing system) was used to control the CO 2 concentration. Purifiers containing brominated, activated carbon were used to absorb volatiles (including ethylene). CA markedly reduced the crown rot. Woodruff (1969b) listed four advantages ofCA storage of bananas: (1) fruit can be held for long periods without significant ripening or turning; (2) decreases incidence of rots and molds; (3) maintains a fresher appearance of the fruit; and (4) more flexibility in coping with glutted markets. However, there has been no commercial CA storage for bananas. Bananas

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

143

are available all year around, and therefore there is no need for long-term storage. Gas-tight CA chambers would have to be built aboard marine ships, since most of the postharvest life of bananas is maintained in transit. In the past, CA in transit has not been technologically feasible, however, the recent advances in CA technology and marine containers facilitates the application of CA aboard marine ships that can provide a postharvest life as long as 2 months. MA has been used commercially for the last 3 decades during marine shipments of banana (Woodruff 1969a,b). In this system, green fruit are usually packed in polyethylene bags of about 0.04 mm (1.5 mil) thickness, and then the bags are evacuated (usually using a vacuum cleaner) and sealed (Woodruff 1969a). High temperatures at the time of evacuation accelerate the establishment of the desirable atmosphere (Woodruff 1969b). The atmosphere in these bags usually averages about 2.5% O2 (1 to 4.5%) and 5.2% CO 2 (4 to 6%) after 3 to 4 weeks. This system has been called "Banavac" by United Fruit Company (Smock 1979; Woodruff 1969b). Bananas can be held for 30 days using this method, and can be maintained green for up to 60 days. However, rots increase and quality declines after 30 days (Woodruff 1969b). Fermentation problems have occurred in up to 1% of fruit shipped in this system (Woodruff 1969a). Only green fruits should be used, and it is essential to avoid the use of punctured bags. Punctured bags do not allow the development of the appropriate atmosphere. Ripe fruit increase the accumulation of ethylene inside the bags and further stimulate fruit ripening. An ethylene concentration of 10 ppm accelerated the ripening of 'Valery' fruit (Woodruff 1969b). A concentration of 10 ppm or more of ethylene can also stimulate the softening of green fruit (Chiang 1968; Chiang 1970), a condition known as "soft-green" (Woodruff 1969b) or "green ripeness" (Scott 1975). High temperature, high CO 2 , and low O 2 in the storage atmosphere were suggested to be the main factors causing this disorder, though the exact mechanism is not fully understood (Zhang et al. 1993). The use of ethylene absorbents such as potassium permanganate absorbed on aluminum silicate or vermiculite in the bags can prevent this disorder and prolong the postharvest life of the fruit (Scott et al. 1968; Liu 1970; Scott 1975). Ethylene removal with brominated carbon was found to extend the storage life of 'Lacatan' and 'Cavendish' fruit held in 2 to 3% Oz plus 8% CO z (Smock 1967), and is more effective than using molecular sieve 5A in a continuous air and CzH4 stream (Chiang 1968). MA can prolong banana storage life even at ambient temperatures (Scott and Gandanegara 1974). Sealed polyethylene bags (0.1 mm thickness) containing 100 g vermiculite impregnated with a saturated solution of KMn0 4 , allowed a

144

E. YAHIA

storage life of 'Williams' fruit for up to 6 weeks at 20 to 28°C and 16 weeks at 13°C (Satyan et a1. 1992a,b). 'Latundan' fruit were stored in 0.08 mm thick polyethylene bags for up to 13 days at 26-30°C (Agillon et a1. 1987). Green mature 'Cavendish' stored in low density polyethylene bags (0.05 mm thickness) for up to 30 days at 8°,11° and 14°C developed an in-package atmosphere of 3 to 11 % O2 and 3 to 5% CO 2 (Hewage et al. 1995). However, these storage conditions did not affect ripening and sensory quality, nor did they alleviate CI symptoms developed at 8 and 11 cC. 'Emas' fruit stored in polyethylene bags (0.04 mm thickness) for 6 days at 24°C generated an atmosphere of up to 30/0 CzH 4 , 14.6% COz, and as low as 2.9% O2 (Tan et a1. 1986). Accumulation of 10% COz or more, especially from day 3 to day 6, and an O2 concentration below 2% in the bags caused abnormal ripening when the fruit were later ripened in air. Fruit had skin and pulp darkening, and softening of the inner portion of the pulp, with the outer portion remaining hard. The waterinsoluble protopectins decreased, and water-soluble pectins and pectates increased in wrapped fruit. A minimum of 10% CO 2 for a few days is required to cause injury to 'Emas' fruit, and injury at 10% COz was also reported for 'Mas' bananas (Abdullah et a1. 1987). Several cultivars of plantains (Bluggoe, Pacific Plantain, Blue Lubin, and Pisang Awak) behaved similarly to 'Cavendish' banana when stored in polyethylene bags (0.1 mm) with or without an ethylene absorbent (potassium permanganate on aluminum oxide) at 7°,13°,20°, and 28°C (Satyan et a1. 1992b). The storage life is increased by a factor of two in the absence of an ethylene absorbent and a factor of three in the presence of the ethylene absorbent. CO 2 concentration inside the packages increased up to 15%, and concentrations as high as 32% were reported at the end of storage. Packaging with or without ethylene absorbent had no effect on the incident of CI either in the cooking banana cultivars or in 'Cavendish'. The authors further suggested that this method of sealing in polyethylene bags "appears to be an alternative method to refrigeration" (1). Bananas were packed in 0.038 mm polyethylene bags and transported at ambient temperature for up to 2,575 km (Scott et a1. 1971). After 18 days packed fruit were still in the hard green condition whereas the unpacked (control) had ripened. Packaging also reduced weight loss and mechanical injury. Liu (1976a) suggested pretreatment of the fruit with ethylene at the production or packing site before storage or shipping to avoid post shipping treatment and thus reducing costs and stimulating even ripening. 'Dwarf Cavendish' banana pretreated with ethylene and stored for 28 days in 1 % O 2 or in 0.1 atmospheric pressure at 14°C remained green and firm until the end of the storage period, and started to ripen almost

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

145

immediately after being placed in air at 21°C, without additional ethylene treatment. However, the period of ethylene pretreatment is critical and should not exceed a "threshold length of time (TLT)." The TLT is defined as the minimum time required for a fixed concentration of ethylene treatment to induce banana ripening response (Liu 1976b). Only bananas that had been pretreated with ethylene for a period equal to the TLT were successfully stored in CA (Liu 1976a). Neither CA nor LP could prevent the ripening of bananas pretreated with ethylene for a period longer than TLT. Fruit are usually not uniform in their TLT. Commercially mature bananas may have TLT between 4 and 20 h, and a test for TLT takes 1 to 2 days (Liu 1976b). The author concluded that it would be extremely difficult to select large lots of fruit with uniform TLT, and thus the potential hazard of fruit ripening during storage or shipping after excessive ethylene pretreatment jeopardizes the commercial applicability of this method. Pro-long (a mixture of sucrose esters of fatty acids and sodium salt of carboxymethylcellulose) extends the shelf-life of bananas (Lowings and Cuts 1982; Banks, 1984a; 1984b). The commercial wax "Decco Luster 202" (1:2 wax:water, v/v) delayed the ripening of 'Saba' fruit (Pastor and Pantastico 1984), but other formulations ("Carbowax" and "Prima Fresh") had no effect. The action of "Pro-long" has been attributed to increased resistance to CO z and Oz diffusion, creating an internal atmosphere with reduced Oz and elevated CO z levels (Lizada and Noverio 1983). 'Gros Michel' fruit held in a LP (150 mm Hg) at 15°C were maintained in a better quality than those held at normal pressure (Burg and Burg 1966). Fruit held in LP of 760, 250, and 80 mm Hg at 14°C were maintained for 30,60, and at least 120 days, respectively, with an acceptable texture, taste, and aroma, and suffering no injury. The quality of green bananas was unaffected when fruit were held for up to 7 days in 100% Nz at 15.5°C, but had dark-brown to black skin blemishes when held for 10 days (Parsons et al. 1964). After 4 days in 100% Nz at 15.5°C, the fruit ripened to a normal color and flavor in 13 days at 20°C. However, the fruit failed to ripen in air, and developed decay, brown skin discoloration, and off-flavor after storage in 100% N z for 7 days. The fruit ripened normally in air at 20°C after being held in 99% Nz and 1% Oz at 15.5°C for 10 days. Ripening banana fruit held for 24 h in 60% CO z at 25°C had a 74% decrease in the rate of Oz uptake and a 10-fold increase in CZH 4 (Kubo et al. 1990). Fruit of 'Berangan' (Musa acuminata) stored for 6 weeks at 12°C and 95% RH had a respiratory quotient close to unity when maintained in 2% Oz or higher, and higher than one when maintained in 0.5% 0z, indicating anaerobic metabolism (Abd.Rahman et al. 1997).

146

E. YAHIA

Low Oz (2.5%) suppressed the activity of acid phosphatase, and the addition of ethylene to the low Oz atmosphere did not reverse this suppression (Kanellis and Solomos 1985; Kanellis et a1. 1989a). However, this atmosphere either alone or in combination with ethylene prevented the decline in the activity of pectin methyl esterase. Kanellis et a1. (1989a) suggested that there were differential effects of low Oz on metabolic processes since the accumulation of sugars increased gradually for 4 days in low 0z, but acid phosphatase did not increase throughout the duration of the low O2 treatment. Low Oz (3 % ) limited the operation of the Krebs cycle in fruit of Musa paradisiaca L., but high CO 2 showed no rate limiting steps in this cycle (McGlasson and Wills 1972). Ali Azizan (1'988) reported that high CO 2 suppressed the activities of ADH, LDH, PDC, and phosphofructokinase (PFK), but not malic enzyme and phosphoenol pyruvate carboxylase in 'Pisang Mas' fruit. Optimum atmospheres for bananas are 2 to 5% O2 plus 2 to 50/0 CO 2 , These atmospheres delay fruit ripening without causing any deleterious effects. CA can maintain the fruit for a longer period in good quality, although a recent report (Blankenship 1996) indicated that bananas that have ripened under CA conditions had poorer quality than those ripened in air in terms of visual appearance. MA, sometimes in combination with ethylene-absorbent agents, is commonly used during long-distance marine transport. LP can also maintain fruit quality for a longer period with very acceptable quality. However, due to year-around availability of the fruit and because of cost considerations, CA is not commonly used and LP is not commercially used. There is, however, potential for the use of CA on marine ships. Research needs for this fruit include investigation of the cost and technological feasibility of establishing and using CA, especially on board ships. C. Cherimoya (Annona cherimola Mill.) The cherimoya is a subtropical fruit with an active metabolism and a climacteric respiratory behavior. Rapid peel browning, loss of firmness, and CI are the main causes of postharvest losses. Postharvest life is about 2 to 4 weeks at 8 to 1DoC. Fruit of 'Fino de Jete' stored in air and in CA (3% O 2 in combination with 0,3,6, and 9% CO 2 ) at 8°C (Alique and Oliveira 1994) showed an additive effect of CO 2 and low O2 atmospheres on reducing ethylene production and fruit softening, but did not significantly affect sugars and citric acid. A combination of 3% O 2 with 3 or 6% CO 2 increased the storage life of 'Fino de Jete' fruit held at 9°C by 2 weeks over that of fruit stored in air. There were no differences between 3 and 6% CO 2 , Earlier

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

147

studies by De La Plaza (1979) and De la Plaza et a1. (1979) also found that CA (2% O 2 + 10% CO 2 at 9°C) retards fruit softening and prolongs the storage life of 'Fino de Jete' and 'Campa' by one week compared to storage in air. This study found that CA has no effect on reducing sugars and titratable acidity in either cultivar, and the high CO 2 increased the respiration rate in 'Fino de Jete'. 'Fino de Jete' and 'Campa' fruit have a higher maximum climacteric in CA (2% O2 plus 10% CO 2 ) than in air (De la Plaza 1980). Palma et a1. (1993) concluded that 'Concha lisa' fruit can be maintained in 5% O2 at 10°C for up to 43 days and still ripen normally after 4 days at room temperature. In this cultivar, 10% and 15% O 2 delayed the climacteric, but at 5% O2 there was no detectable climacteric or ethylene production for up to 43 days. 'Fino de Jete' fruit held in a combination of 10% O 2 and 10, 15 or 20% CO 2 at 8°C and 98% RH for 3, 6 or 9 days, ripened later than those held in air (Alique 1995). Fruit held in 20% CO 2 for 9 days showed unacceptable quality due to bitterness, while 200/0 CO 2 for 3 days delays fruit softening, retards the accumulation of polygalacturonase-related protein, and maintains chlorophyll content of the peel (Del Cura et a1. 1996). Ethylene absorption using KMn0 4 -sepiolite extruded round rods ("Green Keeper") from fruit of 'Fino de Jete' packed in polyethylene films and stored at 8.5°C and 98% RH is beneficial at a dose of 3.5g/kg (De La Plaza et a1. 1993). This dose was efficient in reducing respiration and ethylene production, and kept the fruit in good quality for 18 days. Optimum atmospheres of about 2 to 5% O2 plus 3 to 10% CO 2 can be beneficial during marine transport of fruit. D. Durian (Durio zibethinus Murray) The durian is a climacteric fruit native to southeast Asia that can weigh up to 5 kg, and has thick fibrous skin and short sharp spines. Thailand is the biggest producer and exporter of durian. 'Chanee' and 'Monthong' are the two most popular cultivars. The fruit is eaten fresh, and prepared as candy, paste, dehydrated powder, or frozen. Postharvest life is about 3 to 7 weeks at 4 to 6°C. Reduction of the O2 level in the atmosphere to 10% caused a significant reduction in respiration and ethylene production in fruit of the cultivars 'Chanee', 'Kan Yao', and 'Man Tong', but did not delay fruit ripening (Tongdee and Suwanagul 1988a,b; Tongdee and Neamprem 1989; Tongdee et a1. 1990a). The same authors reported that ripening is delayed in fruit stored in 5% or 7.50/0 O2 for up to 7 days at 22°C, and fruit ripened normally upon transfer to air. However, fruit stored in 2% O 2 are injured and fail to ripen even when transferred to air. High CO 2

148

E. YAHIA

(10 to 20%) caused only a slight reduction in ethylene production and did not affect fruit ripening, having a greater effect on the aril condition when combined with low Oz. The effect of low Oz and/or high CO 2 on durian ripening is influenced by the stage of maturity at harvest (Suwanagul and Tongdee 1989; Tongdee et a1. 1989). Fruit that were allowed to begin their ripening process before storage in CA had a slightly longer shelf life (Siriphanich 1996). Waxing of 'Chanee' and 'Mon Tong' fruit with different "FMC SF" formulas restricted gas movement through the rind, resulting in higher internal CO z, lower 0z, and CZH 4 concentrations and delayed fruit ripening (Tongdee et a1. 1990b). Sriyook and Siriphanich (1989) reported that sucrose ester coating delayed ripening for 1 to 3 days at 25°C. Storage of minimally processed fruit in an atmosphere of 10% CO z in air inhibits fungal growth for a week at room temperature (Siriphanich 1994). Optimum atmospheres are about 5% Oz with up to 20% CO 2 , More studies are still needed to further define the most appropriate atmosphere and the feasibility of MA/CA applications.

E. Feijoa(Feijoa sellowiana Berg.) The feijoa is a climacteric fruit related to guava, originated in Brazil, and is grown in several countries. Postharvest life is about 2-4 weeks at 5-10°C. Treatment of hand-picked feijoa with 98% N z or CO z for 24 h at 20°C increased the accumulation of acetaldehyde, ethanol, ethyl acetate, and ethyl butyrate, and improved aroma and flavor for up to 13 days of storage (Pesis et a1. 1991). CA-stored fruit were judged to be sweeter than the control, but there were no differences in total soluble solids or acidity. Treatment with N z for 24 h is the most effective in increasing volatile production and in maintaining the best appearance. Work is needed to identify the ideal atmosphere composition and potential benefits of MA/CA. F. Guava (Psidium guajava L.) The guava is a climacteric fruit native to tropical America and commercially grown throughout the tropics and subtropics. Anthracnose and CI are the most important causes of losses. Postharvest life is about 2-3 weeks at 5-10°C. The postharvest life of guava is extended by packaging it in 300 gauge polypack film bags (Khedkar et a1. 1982). Wrapped fruit had less mass loss, greater vitamin C retention, and higher organoleptic scores, and no

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

149

adverse effects. The effects noted might be due to high humidity rather than to gas modification. Coating of mature-green fruit with cellulose- or carnauba-based emulsions delays ripening and slows softening, but causes less coloring and more surface blackening (McGuire and Hallman 1995). Coating with 2% or 4% hydroxypropylcellulose slows softening by 35% and 45%, respectively, compared to uncoated fruit. Coating with 5% carnauba formulation slowed softening by 10 to 30%, and is effective in reducing mass loss. Studies are required to investigate the ideal atmosphere composition and potential benefits of MA/CA.

G. Lanzon (Lansium domesticum Correa) The fruit, 2 to 5 em and ellipsoid to round, is native to the southeastern Malay archipelago. It is consumed mostly fresh but can be candied. CA atmospheres containing 5% O 2 with no CO 2 at 14.4°C increase the storage life of 'Paete type' lanzon to 16 days compared to 9 days in air, and also reduces skin browning (Pantastico et a1. 1969). Increasing the CO 2 from 0 to 5%, regardless of the O 2 concentration, did not increase the acidity of the fruit, but increased surface browning, especially at 10% 02' Waxing with Johnson's Prima Fresh Wax emulsion reduces mass loss, but aggravates the browning effect after only 5 days of storage. Waxed fruit were sweeter than the control, indicating that waxing does not impair the ripening process to offset the normal reduction in acidity. Optimum atmosphere for storage of lanzon was 5% O 2 with zero CO 2 , Holding fruit in polyethylene bags (27 x 22 em, 0.08 mm thick) with 16, 32 and 64 holes for 4 days at 28°C reduces mass loss but increases surface browning (Brown and Lizada 1984). Atmospheres (%Oz/CO z) developed in the bags are 15.2/4.4, 10.9/7.6, and 8.818.4, respectively. Browning is thought to be caused by the increased concentration of CO 2 , Further research is still needed to investigate the potential benefits of MA/CA for lanzon.

H. Loquat (Japanese plum, Japanese medlar) (Eriobotrya japonica L.) The loquat, originating in China, is grown in several parts of the world. Postharvest life is about 3 weeks at O°C. Fruit of four cultivars (Acco 1, Acco 13, Tanaka, and Tsrifine B) stored with and without polyethylene wraps at 0, 6, and BOC and 90% RH for 4 weeks and then for 4 days at 20°C had better appearance and less mass loss, but more internal browning and postharvest rotting, and poorer fla-

150

E. YAHIA

vor and quality in the wrapped than in the unwrapped fruit (GuelfatReich 1970). Further research is needed to investigate the ideal gas composition and the potential benefits of MA/CA. I. Longan (Dimocarpus longana Lour.) A small fruit (1.5-3.0 em in diameter), longan originated either in subtropical China or in the area between Burma and India. Diseases are the major causes of losses, and postharvest life is about 5 weeks at 10°C and 90% RH. MAP consisting of 1 % or 3% O 2 were effective in delaying browning of the peel, reducing respiration, maintaining soluble solids and vitamin C, and partially inhibiting the activity of polyphenoI oxidases in 'Shixia' fruit (Zhang and Quantick 1997). Further research is needed to investigate the ideal atmosphere and potential application of MA/CA.

J.

Lychee (litchi, litchee) (Litchi chinensis Sonn.)

The lychee is a non-climacteric fruit native to Southern China. Postharvest life is about 3-5 weeks at 1°C. Loss of bright cherry red color, desiccation, and decay are the major causes of postharvest losses. Lychee fruit begins to loose its bright red color soon after harvest and turn dull brown (Paull and Chen 1987). The storage life of lychee is extended very significantly (up to 5 weeks) by storage in polyethylene bags at 2°C (Macfie 1955a; Macfie 1955b; Thompson 1955; Singh 1957; Campe1l1959; Akamine 1960). Packaging in polyethylene bags and storage at 10°C also extended the postharvest life of the fruit and reduced the incidence of decay (Macfie 1955a, b). Storage of 'Hei Ye' (Groff or Hak yip) and 'Chen Zi' (Brewster) fruits in polyethylene bags (0.25 mm thickness) at 2 or 22°C delayed the onset of pericarp browning (Paull and Chen 1987). Decay is a problem in fruit packaged in polyethylene bags for 6 days at 22°C, or after about 20 days in bags held at 2°C. 'Mauritius' fruits at 5°C in 3 or 4% O 2 with 5, 10 or 15% CO 2 showed negligible incidence of black spot and lesser incidence of stem-end decay when compared with control fruits (Vilasachandran et al. 1997). The rate of fruit darkening is reduced by storage in plastic bags (Akamine 1960; Scott et al. 1982). Browning of 'Mauritius' fruit is controlled for 28 days at 1°C and 200/0 CO 2 in N z (Lonsdale 1993). However, Chen et al. (1986) reported that concentration of COz higher than 5% caused off-flavors. Browning in pericarp of 'Brewster' is delayed significantly by applying polysaccharide coatings, but the effect is insufficient to warrant commercial application (York

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

151

1995). In South Africa, Lonsdale (1993) suggested an alternative treatment to S02 which included "Vitafilm" wrapping, a gas mixture of 20% COz in N z and irradiation (0.75 or 1.5 kgy). Bleaching of the pericarp is noted to be due to low levels of O2 (Akamine 1960). MAP with high CO 2 atmosphere (up to 20%) is beneficial in maintaining the quality of lychee. However, further research is needed to identify the most adequate atmosphere conditions for MAP. K. Mango (Mangifera indica L.) The mango, a climacteric fruit, is one of the most important tropical fruits in world trade. Anthracnose and CI are the most important causes of postharvest losses. Postharvest life of mature-green fruit is about 2-4 weeks at 10-15°C. A very early study by Singh et a1. (1937) suggested that mangos (cultivar unspecified) could be kept in an atmosphere of 9.2% O 2 to prolong the ripening period. Kapur et a1. (1962) reported that fruit of 'Alfonso' were kept satisfactorily in 7.5% CO 2 at 8.3-10.0°C for 35 days, and fruit of 'Raspuri' in 7.5% COz at 5.5-7.2°C for 49 days. Maekawa (1990) concluded that it is possible to maintain 'Irwin' fruits for up to 4 weeks in 5% CO 2 plus 50/0 CO 2 with 12°C and the use of an ethylene absorbent (activated charcoal/vanadium oxide catalyst). In addition, the author reported that temperature can be safely reduced to 8°C. 'Rad' fruits can be successfully kept for up to 25 days in 6% Oz plus 4% CO 2 at 13°C and 94% RH (Noomhorm and Tiasuwan 1995). In Brazil, 'Haden' fruits were held for 30 days and 'Carlota', 'Jasmin', and 'Sao Quirino' were held for 35 days in 6% O 2 and 10% CO 2 at 8°C plus 90% RH (Bleinroth et a1. 1977b). In France, 'Amelie' fruits stored for 4 weeks in 5% O 2 plus 5% CO 2 at 10 to 12°C had less decay, and fruit were reported to be more acceptable after CA than after air storage (Kane and Marcellin 1979). Sive and Resnizky (1989b) maintained 'Tommy Atkins' and 'Keitt' fruits treated with prochloraz (to control Alternaria alternata) in CA for up to 10 weeks at 13°C. The Philippines Council for Agriculture and Resource Research (1978) reported that 'Caraboa' fruits can be kept for 28 days in 50/0 O2 and 5% CO 2 at 10°C, however, this cultivar was reported to be very susceptible to MA injury by other researchers in the Philippines (Gautam and Lizada 1984; Nuevo et a1. 1984a, 1984b). Gautam and Lizada (1984) reported that storage in MA using polyethylene bags for more than one day causes ripening abnormalities. It has been suggested that CA is not, or is only slightly beneficial for mango (Hatton and Reeder 1966,1967, 1969a; Spalding and Reeder 1974). The best atmosphere for 'Keitt' was reported to be 5% O2 plus 5% CO 2 at 13°C, how-

152

E. YAHIA

ever, quality was not significantly better than in air storage (Hatton and Reeder 1966; Spalding and Reeder 1977). A 10% COz atmosphere alleviated chilling symptoms in fruit of the 'Kensington', but higher concentrations were injurious, while low Oz (5%) had no significant effect (O'Hare and Prasad 1993). Higher concentrations of COz (more than 10%) were found to be ineffective in alleviating CI at 7°C, and tended to cause tissue injury and high levels of ethanol in the pulp. 'Rad' fruits had internal browning and off-flavor in atmospheres containing 6 or 8% COz (Noomhorm and Tiasuwan 1995). The presence of starchy mesocarp in 'Carabao', which is characteristic of internal breakdown, increases in this cultivar during storage in MA (Gautam and Lizada 1984). Fruit stored for 4-5 days exhibited severe symptoms that included air pockets in the mesocarp resulting in spongy tissue (Nuevo et al. 1984a, 1984b). Parenchyma cells of affected tissues had an average of 18 starch granules per cell, compared to an average of two starch granules in healthy adjacent cells. However, no difference in starch granule shape was detected between the two tissues. The spongy tissue, which usually occurs in the inner mesocarp near the seed and becomes evident during ripening, had almost 10 times the starch content compared to the healthy tissue in the same fruit. External symptoms of the internal browning due to MA consist of failure of the peel to· develop color beyond the halfyellow stage. 'Carabao' fruit stored in polyethylene bags (0.04 mm thickness) had a faint fermented odor that disappeared during ripening (Gautam and Lizada 1984). The fermented odor was stronger the longer the storage duration, and persisted throughout ripening when fruit were kept for 2 to 5 days in polyethylene bags. The respiratory quotient of this cultivar ranged from 0.59 at 21 % Oz to 6.03 at 2.4% 0z, indicating a progressively anaerobic metabolism (Sy and Mendoza 1984). COz production decreased as the Oz level was decreased from 21 to 3%, but increased at Oz concentrations below 3%. Fermented odor is explained as a possible indication of fermentative decarboxylation as is reported in 'Alfonso' fruit subjected to elevated concentrations (more than 15%) ofCO z (Lakshrninarayana and Subramanyam 1970). Injury in 'Kensington' fruit caused by higher levels of CO 2 appeared to be more severe at lower temperatures (O'Hare and Prasad 1993); that could be due either to compounding injury (chilling + CO 2 ) or to greater sensitivity of unripe fruits to CO 2 , Diseases, especially anthracnose and stem-end rot, are the principal limiting factors for mango storage. Moderate O 2 (~ 5%) and CO 2 (~ 5%) atmospheres do not control these diseases. Pronounced decay incidence appeared after storage of 'Rad' fruit for 20 days in atmospheres containing 4-60/0 O 2 plus 4-8% CO 2 at 13°C and 94% RH, and severe inci-

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

153

dence appeared after 25 days (Noomhorm and Tiasuwan 1995). Greater incidence of decay (stem-end rot and anthracnose) was observed in 'Carabao' fruit stored in MA for 2 to 5 days at 25 to 31°C (Gautam and Lizada 1984). The enrichment of CA with 5 to 10% CO has been suggested for better disease control (Woodruff 1977). However, CO is potentially toxic and explosive, and should not be used unless safe measures for application are developed. Mango fruit wrapped in 0.08 mm thick polyethylene bags, with and without perlite-KMn0 4 , and stored for 3 weeks at 10°C before treatment with ethylene, ripened to normal color, texture, and flavor (Esguerra et al. 1978). 'Keitt' fruit individually sealed in low density (LDPE) and high density (HDPE) polyethylene films for 4 weeks at 20°C delayed ripening, reduced weight loss, and did not result in any off-flavors (Gonzalez et al. 1990). The LDPE had a thickness of 0.010 mm and permeabilities of 700 ml Oz . m- z . h- I . atm- I , and 0.257 g HzO . m-z . hr i . atm- I . The HDPE film had a thickness of 0.020 mm and permeabilities of 800 ml Oz . m-z . hr-1 . atm-I, and 0.166 g HzO . m- z . hr i . atm- I . The combined effect of hot benomyl (1000 ppm) solution at 55°C for 5 min, and seal packaging in 0.01 mm PVC, extended the storage life of mature-green 'Nam Dok Mai' mango stored at 13°C (Sornsrivichai et al. 1992). Fruit quality was unaffected by film packaging after 4 weeks, but was inferior to the control after 6 weeks of storage. The inhibition of carotene pigment development in the peel ofthis variety is suggested by Yantarasri et al. (1994) to be related to Oz concentration inside the package and not to CO z concentration. The authors suggested that a concentration of at least 16% Oz is essential to develop peel color to the marketable stage (greenish). 'Tommy Atkins' fruit individually sealed in heat shrinkable films and stored for 2 weeks at 12.8°C and then ripened at 21°C had less mass loss, but did not show differences in firmness, skin color development, decay development, or time to fruit ripening, and had more off-flavors than unwrapped fruit (Miller et al. 1983). Polyethylene films used were: Clysar EH-60 film of 0.01 mm nominal thickness, Clysar EHC-50 copolymer film of 0.013 mm nominal thickness, and Clysar EHC-l00 copolymer film of 0.025 mm nominal thickness. Individual mature fruit of the same cultivar were later sealed in Clysar EHC-50 copolymer film with 0.013 mm thickness, and Cryovac D955 with 0.015 thickness, and stored at 21°C and 85-90% RH (Miller et al. 1986). Oz permeance of the films was 620 cc 3 . m- z . 24h- I . atm- I and 9833 cc 3 . m- z . 24h- 1 . atm- I , respectively. Water transmission was 1.5 g . m-z . 24 h- I and 2.0 g . m-z . 24 h-1 at 23°C, respectively. Fruit had less weight loss, but higher incidence of decay and off-flavor at soft-ripeness than unsealed fruit. The authors concluded that there were no practical benefits associated with

154

E. YAHIA

wrapping this cultivar in these films and storing them at 21°C or even at lower temperatures. They even suggested that "film wrapping mangos at various stages of ripeness after harvest is not a technique which will improve the maintenance of mango quality during storage for ripening." 'Kensington' mango treated with heated benomyl (0.5 g . L-l at 51.5°C for 5 min) and sealed in polyethylene bags (0.04 mm thickness) for various durations at 20°C, had off-flavor and lacked normal skin color when ripened, but ripened satisfactorily when held in perforated bags (Chaplin et a1. 1982). The postharvest life of this fruit was not consistently longer than the control. The concentration of CO 2 in the bags exceeded 200/0 and that of O 2 was lower than 5%. The incidence of offflavors was reduced by inclusion in the bags of C2 H4 absorbent blocks (KMn04 on vermiculite/cement block). The authors concluded that mangos cannot be stored satisfactorily at ambient temperature using such a technique. However, Stead and Chithambo (1980) reported that fruit ripening at 20 to 30°C is delayed 5 days by sealing in polyethylene bags (0.02 mm thickness) containing potassium permanganate, without any abnormal flavor, but gas composition in the bags was not reported. 'Tommy Atkins' and 'Keitt' mangos were individually sealed in shrinkable Cryovac polyolefin films (15 or 19 /lm thickness), either nonperforated (MD film) or perforated with 8 holes of 1.7 mm diam.l6.75 cm 2 (MPY) or 8 holes of 0.4 mm diam/6.75 cm 2 (SM60M) (Rodov et a1. 1994). After 2-3 weeks storage at 14°C and an additional week at 17°C, mango packaged in perforated polyolefin films ripened normally, and the best results were achieved when film with 0.4 mm perforations is combined with increased free volume inside the package by sealing the fruit within polystyrene trays. After 3 weeks of storage and one week of shelf life, sealed 'Keitt' fruit was inferior in quality to the control for being less ripe, but beyond 4 weeks (up to 6 weeks) sealed fruit had better quality scores because they were less overripe. Sealing did not reduce decay of fruit stored for long periods. Non-perforated PVC film packaging of 'Nam Dork Mai' fruit was not sufficiently permeable for O2 exchange to allow proper ripening (Yantarasri et a1. 1995). Therefore, a so-called "perforated MA" was used where fruit were wrapped in polystyrene trays (three fruit/pack) at 20°C with a perforation area of:?: 0.004 cm 2 • Fruit were reported to ripen normally and with no production of off-flavors. Color development in the peel is reported to require a higher concentration of O 2 than the flesh, and a film of pore area:?: 0.008 cm 2 allowed fruit color to develop after 3 weeks while a pore area of:?: 0.39 cm 2 allowed the fruit to color within 2 weeks. Chaplin et a1. (1986) reported that symptoms of CI are reduced in 4 cultivars of mango stored in sealed polyethylene bags for up to 15 days at 1°C.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

155

Treatment of 'Julie' mango with a 0.75% w/v aqueous solution of Prolong (a mixture of sucrose esters of fatty acids and sodium salt of caboxymethylcellulose) and stored at 25°C and 85-95% RH reduced mass loss, retarded ripening, and increased storage life (6 days longer) without causing any adverse effects on quality (Dhalla and Hanson 1988). A treatment with 1.0% Pro-long increased ethanol concentration in the pulp of some fruit. Treatment with 0.8-2.4% Pro-long delayed ripening of 'Haden' fruit (Carrillo-Lopez et al. 1996). Mango fruit were artificially infested with larvae of Drosophila melanogaster, and individually wrapped with a Cryovac D-955 crosslinked, 60-gauge polyolefin shrink film (Shetty et al. 1989). None of the insects survived in fruit wrapped for 72 h or more. Gould and Sharp (1990) reported a 99.95% mortality of the Caribbean fruit fly in filmwrapped fruit for 15 days, but fruit deteriorated after only 6 days. Storage of 'Keitt' mangos in an insecticidal MA (0.03-0.26% 0z, 72-79% CO z, balance Nz)' and CA (0.2% 0z, balance Nz or 2% Oz + 50% CO z, balance N z) for up to 5 days at 20°C delayed fruit ripening as indicated by respiration, flesh firmness, and color development (Yahia et al. 1989; Yahia 1993b; Yahia and Tiznado 1993; Yahia and Vazquez 1993). These atmospheres increased the activity of phosphofructokinase, ADH, and PDC, but did not affect the activity of pyruvate kinase, succinate dehydrogenase, and a-keto-glutarate dehydrogenase. Although these atmospheres caused changes in glycolisis and tricarboxylic acid cycle, there was no indication of injury and the fruit ripened normally after exposure to air. Sensory evaluation conducted after fruit ripening showed no presence of off-flavors, and there were no differences between fruit maintained in MA/CA and those maintained in air. On the basis of these results, 'Keitt' mango is considered to be very tolerant of insecticidal atmospheres. It is assumed that the 5 days tolerated by mango are sufficient to control many insects (Kader and Ke 1994; RojasVillegas et al. 1996). Atmospheres containing 0.7% Oz and/or 67% CO z at 44°C for 160 min caused 100% mortality of eggs and third instar larvae of Anastrepha ludens and A. obliqua (Yahia et al. 1997). Storage of 'Keitt' and 'Tommy Atkins' fruit for 21 days at 12°C in atmospheres containing 25, 45,50, or 70% CO z plus either 3% Oz or air induced the production of 0.18 to 3.84 ml ethanol kg- 1 . h- 1 after transfer to air at 20°C for 5 days (Bender et al. 1995). Atmospheres containing 50 and 70% CO 2 caused fruit injury, and resulted in the highest ethanol production rates. The enclosure of 'Haden' and 'Tommy Atkins' fruit in sealed 20-L jars with initial atmospheres of 90% CO z in air or 97% Nz + 3% Oz for 24 h prior to storage delayed ripening (Pesis et al. 1994b). Burg (1975) reported that 'Haden' mango ripen four times slower at

156

E. YAHIA

150 mm Hg than in air. Several cultivars including 'Irwin', 'Keitt', 'Kent', and 'Tommy Atkins' were found to be firmer after storage for 3 weeks in 76 or 152 mm Hg at 13°C and 98-100% RH (Spalding and Reeder 1977). These fruit ripened normally after storage, had less decay, and a higher percentage of acceptable fruit. A pressure of 76 mm Hg results in the greenest fruit, however, this LP caused splitting. Therefore, a pressure of 152 mm Hg is considered as the optimum LP. Mango shipped experimentally in LP (80 mm Hg at 10°C) from Mexico to Japan arrived in satisfactory condition after 28 days from picking (Spalding 1977a). LP (152 mm Hg) is reported to be suitable for shipping or storage of mango, together with banana and lime (Spalding 1977a, 1977b). '0 Krong' mango precooled at 15°C and waxed were maintained in 60-100 mm Hg at 13°C for up to 4 weeks, and then ripened normally (Ilangantileke and Salokhe 1989). 'Rad' fruit were kept in 100 mm Hg at 15°C for 30 days (Chen 1987). However, due to cost considerations, no commercial use of LP is reported at the present. There is no current use of CA storage for mango, however, long-term marine shipping in MA has been commercially used on a very limited basis from several countries including Mexico (Yahia 1993a). The recent use of CA during transport will most probably improve the quality of shipped fruit. Research results are still very contradictory due to the different cultivars of mangos used, different atmospheres implemented, and the common lack of experimental control. The optimum atmosphere composition for prolonged shipping or storage of mango are reported to range between 3-5% O2 plus 5-10% CO 2 at optimum temperature and RH. These atmospheres can delay ripening, but benefits are minor. CA and MA would most probably be beneficial in delaying fruit ripening during longdistance marine transport for 2 weeks or more. The tolerance of mango to insecticidal atmospheres suggests a potential commercial application, especially in combination with other treatments such as heat. The research needs for improved mango storage are diverse; they include: Establishment of ideal atmospheres and potential applications for the different cultivars in different regions, and the potential feasibility of MAP and CA storage. 2. Establishment of the tolerance/sensitivity of different mango cultivars to insecticidal atmospheres. 3. Determination of mortality of different insects in MA and CA, in combination with other treatments such as heat, and the development of MA/CA as a quarantine treatment. 1.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

4.

157

Determination of the basis for tolerance/sensitivity to insecticidal atmospheres.

L. Mangosteen (Garcinia mangostana L.)

The mangosteen is a non-climacteric fruit native to the Malay archipelago. The fruit is 5 to 10 em, round, thick shelled, and eaten mostly fresh but can also be made into paste and candy. The postharvest life is about 2-4 weeks at 13°C and 85-90% RH. Fruit have been stored at 5°C in 5% O 2 plus 5% COz for one month (Godfrey and Davis 1994). Mangosteen stored at the stage of initial color development in low Oz (1, 3, 5, or 10%) and/or high COz (5 or 10%) at 15°C and 85-90% RH had delayed peel color development and calyx deterioration for up to 7 weeks (Rattanachinnakorn et al. 1996). Atmospheres containing 5% Oz plus 10% COz showed the best results in maintaining both external appearance and internal quality for up to 4 weeks, with an extra 5 days of shelf life. Atmospheres with 1% Oz induced fermentation of the fruit, and increased the incidence of disease development. Packaging in polyethylene bags (not characterized) reduced mass loss and postharvest diseases (Daryono and Sabari 1986), but it is unknown whether the effect was due to humidity and/or gas modification. Further research is needed to establish the most adequate atmospheres and to investigate the real potential of MA/CA. M. Papaya (Carica papaya L.)

The papaya is a climacteric fruit native to Central America. Anthracnose is the major fungal problem in postharvest. The postharvest life of the fruit is about 1-3 weeks at 7-13°C. 'Solo' papaya in Hawaii held for 6 days in 10% CO 2 at 18°C developed less decay than fruit stored in air or in higher concentrations of COz (Akamine 1959; 1969). Chen and Paull (1986) reported that ripening of 'Kapaho Solo' papaya was delayed by storage in 1.5 to 5% Oz with or without 2 or 100/0 COz, but CI symptoms were not reduced. In Florida, papaya held in 1% Oz plus 3% CO 2 at 13°C for 3 weeks and then ripened at 21°C was 90% acceptable, with fair appearance, slight or no decay, and good flavor (Hatton and Reeder 1969c). The storage life of 'Bentong' and 'Taiping' papaya in Malaysia was extended by maintaining the fruit in 5% COz at 15°C and removal of ethylene (Nazeeb and Broughton 1978). CA storage of papaya can be beneficial only when the O2 concentration is kept under 1%, and when it is used along with low temperature, hot water treatment, and ethylene dibromide (EDB) (Akamine

158

E. YAHIA

and Goo 1969). EDB was banned in 1984 (Federal Register 1984). Arriola et a1. (1980) concluded that MA raised handling costs but did not maintain better quality fruit. Spalding and Reeder (1974) concluded that CA is not beneficial to prolong the storage life of papaya. Md. Yon and Abd.Rahman (1997) reported recently on the successful shipment of about 6350 kg of 'Eksotica' fruit from Malaysia to Dubai (13 days) at 12.5°C in MA containing 2-8% O2 and 6-13% CO 2 with an undetectable amount of ethylene. Akamine and Goo (1969) reported that the shelf life of papaya held in 1% O 2 at 13°C for 6 days was only one day longer than fruit held in air. However, Hatton and Reeder (1969c) reported that fruit were held for 21 days with an acceptable quality in an atmosphere containing 1% O 2 plus 5% CO 2 , Optimum maturity for CA-stored fruit is mature green or 10% yellow (Akamine and Goo 1969). CA was suggested to supplement the hot water treatment for a potential storage or shipping period of up to 12 days (Akamine and Goo 1969). Sankat and Maharaj (1989) and Maharaj and Sankat (1990) reported that fruit of 'Known You No. l' and 'Tainung No. l' at the color break stage treated with hot water (48°C for 20 min) and dipped in heated (52°C for 2 min) Benlate (1.23-1.50 gil) were maintained for up to 29 days in 1.5-2.0% O 2 plus 5% CO 2 at 16°C, compared to 17 days in air. Akamine and Goo (1968) suggested that it is feasible to use CA during the shipment of hot-water treated or irradiated papayas when shipping period is from 6 to 12 days. 'Kapoho' and 'Sunrise' fruit individually sealed in RDPE (0.18 mm thickness) had less CI symptoms than unsealed fruits, but developed offflavor (Chen and Paull 1986). Seal packaging of 'Backcross Solo' papayas in three layers of low-density polyethylene (0.0125 mm thickness) and storage at 24-28°C for 18 days retarded development of peel color and fruit softening, and reduced the increase in titratable acidity (Lazan et a1. 1990). In addition, seal packaging alleviated water stress and modified internal and external atmospheres. Internal CO 2 increased to 2.2%, and O2 decreased and was maintained at 1.2%. The retardation in fruit softening is attributed partly to a decrease in polygalacturonase activity, and to polyuronide solubilization. MAP (using 0.05 mm shrinkable polyethylene films) at 15°C retarded the firmness loss in 'Exotica' papaya fruit (Lazan et a1. 1993). 'Sunset', 'Sunrise', and 'Kapoho Solo' papayas had a double hot water treatment, were dipped in 0.65 giL thiabendazole, and either dipped in various wax solutions or shrink wrapped with various films (Paull and Chen 1989). Films used were Cryovac MPD-2055, Cryovac D-955, Dupont 75ERC, Dupont 60ERC, and Dupont 50ERC. The type of wax solutions used were Brogdex 505-20 (1 :11), FMC-7051 (1:9), FMC 560 (1:4), FMC-219B (1:4), Decco-261 (1:4), Agric Chern 93-8510078 (1:0), Prima Fresh-30 (1:3), Wax-On shellac (1:4), and

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

159

Wax-On polyethylene (1:4). After holding the fruit for up to 2 weeks at 10°C, mass loss is reduced by 14 to 40% by waxing, and 90% by shrink wrapping. Some treatments delayed ripening by 1 to 2 days after the fruit were ripened in air, however, some off-flavor was also developed. The CO 2 concentration that caused off-flavor was found to be 7 to 8%; no offflavor was developed at 6% CO 2 , Applying a cellulose-based film to papaya altered the internal gas concentration, retarded ripening, and extended fruit shelf life (Baldwin et a1. 1992). 'Kapoho' and 'Sunrise' papayas treated with Sta-Fresh 7051 wax solution (1:10 v/v) and stored at 2°C for 14 days or 10°C for 24 days had less CI symptoms (Chen and Paull 1986). Fruit infested with eggs or first instar larvae of the Oriental fruit fly (Dacus dorsalis Hendel), wrapped in a Cryovac D-955 cross-linked, 60gauge polyolefin shrink film, and stored at 24 to 25°C showed a reduction in the number of insects that survived after 96 hours (Shetty et a1. 1989). Eggs and first instar larvae survived when the wrap was present for less than 48 hours. The authors suggested that the shrink wrap may have affected the survival of the eggs and larvae by creating a modified environment due to the depletion or accumulation of certain gases, but gas analysis in the packages was not reported. lang (1990) infested 'Solo' papayas with eggs or one of three larval stages of Ceratitis capitata or Dacus cucurbitae, and individually wrapped the fruit in the same film (Cryovac, D-955) used by Shetty et a1. (1989). The fruit were held at 22 to 24°C for 72 to 144 h. Fruit infestation significantly decreased as the storage period increased, especially after 96 h. Infestation with eggs of Ceratitis decreased about 80% between 72 and 120 h, and larval infestation was also reduced, but some infestation remained even after 6 days of wrapping. Dacus larvae were found to be more resistant than Ceratitis eggs and larvae. The author reported that more than 90% of the infestation found after 120-144 h was due to loosely wrapped fruit or holes in the wrap. Larvae were observed to exit the fruit onto the fruit surface within 30 to 60 min, and often die between the fruit surface and the wrap. The author suggested that this might be due to modification of gases or altered metabolism inside the fruit, however, gas monitoring was not reported. Papaya fruit shipped in LP containers from Hawaii to Los Angeles and New York (20 mm Hg, 10°C, and 90-98% RH) for 18 to 21 days had longer postharvest life, developed less diseases, and mostly ripened normally after removal from the containers (Alvarez 1980). Fruit held in hypobaric storage had 63% less peduncle infection, 55% less stem end rot, and 45% less fruit surface lesions than those held in normal atmospheric pressure. Fruit stored for 21 days at 10 mm Hg and 10 0 e imme-

160

E. YAHIA

diately after being inoculated with Colletotrichum gJoesporioides and then ripened for 5 days at room temperature had less anthracnose than the control fruit (Chau and Alvarez 1983). However, LP only retarded pathogen and disease development and thus will only be effective if disease programs are used to reduce fruit infection. 'Sunrise' papayas stored in an insecticidal atmosphere (0.17 to 0.35% 0z, balance N z) for up to 5 days at 20°C had less firmness loss than the control, and no apparent external or internal injury (Yahia et al. 1989; Yahia 1991; Yahia et al. 1992; Yahia 1993b). However, about 30% ofthe fruit had very weak fermentative odor after 3 days, and the odor increased in intensity as the exposure period to low O 2 was prolonged. The activity ofLDH and PDC increased after 3 and 5 days, respectively, while concentrations of pyruvate and lactate did not change. On the basis of off-flavor development, papaya was suggested to tolerate these insecticidal atmospheres for less than 3 days. Decay was evident after one day of storage in low O 2 , indicating that low O 2 alone is not sufficient for decay control, and there is a necessity for an antifungal treatment (Yahia et al. 1989). Powrie et al. (1990) patented a preservation procedure for cut and segmented fruit pieces where they claimed to store papaya pieces in MAP for up to 16 weeks at 1°C with little loss in taste and texture. This was done in a high gas barrier package (DuPont LP 920™) consisting of polyethylene/tie/ethylene vinyl alcohol/tie/polyethylene plastic laminated pouches. Papaya fruit were cut into pieces of 10-25 g, dipped in 5% citric acid, and the package was flushed with 15-20% Oz and 3% helium before sealing. The ratio of gas to fruit volume was 1 :4. No commercial use for MA/CA storage has been reported for papaya. Ideal atmospheres are not yet fully defined, but range between 2-5% O 2 plus 5-8% CO z' It is unknown if MA/CA have potential application. Further controlled studies are still required to establish the potential applications and ideal atmospheres. N. Passion fruit (yellow) (Passiflora edulis (Sims)

f. flavicarpa Deg.) The passion fruit is a climacteric fruit native to the tropical regions of North and South America. Postharvest life is about 2-3 weeks at 7-10°C. The yellow passion fruit is the basis of almost all the industry, although some purple passion fruit are also marketed. Passion fruit placed in polystyrene trays, overwrapped with plasticized PVC film (VF-60), and stored for 15 to 30 days at 10°C had less

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

161

mass loss and better external appearance, although the film did not effectively modify the O 2 or CO 2 levels (Arjona et al. 1994). The CO 2 concentration within the packages never exceeded 0.5% and that of O2 never dropped below 13% throughout the 30 days of the experiment. Based on the slight increases in CO 2 and decreases in O 2 concentrations in the packages, most of the beneficial effect is obviously due to humidity control rather than to gas control. Wrapping did not affect fruit sugar and juice pH. About 80% of the yellow passion fruit were judged marketable after storage in polyethylene bags (bags were not characterized) for 14 days at 23°C (Salazar and Torres 1977). The authors recommended that fruit should be treated with fungicides before packaging. Fruit sealed in polyethylene bags and stored at 6 to 10°C had less shriveling for 3 to 4 weeks (Cambell and Knight 1983). Fruit stored in polyethylene bags or treated with paraffin wax and stored at 7.2°C and 85 to 90% RH remained marketable for up to 30 days (Cerrada et al. 1976). Coating of purple passion fruit with either 1.0 and 1.5% Semperfresh reduced weight loss and extended the shelf life by 4 days (Bepete et al. 1994). There were no differences between the effect of 1 and 1.5% Semperfresh. The potential benefits and feasibility of MA/CA for passion fruit is still unclear, and an ideal atmosphere for this fruit has not been established.

o.

Pineapple (Ananas comsus L., Merrill.)

The pineapple is a non-climacteric fruit native to Brazil and widely distributed throughout the tropics. Fruit flies attack the fruit but do not survive inside the flesh. Postharvest life of the fruit is about 1-5 weeks at 7-13°C. Internal breakdown caused by low temperature is a major disorder during storage and transport. Dull (1971) concluded that decreased O2 and increased CO 2 concentrations had no obvious effect on pineapple fruit quality, and therefore no major advantage of quality maintenance was to be gained by manipulation of the concentration of these two gases. However, in a previous report Dull et al. (1967) found that CA extended fruit storage life by 1 to 3 days. Akamine (1971) and Akamine and Goo (1971) concluded that CA storage (2% O2 and 98% N2 ) at 7.2°C had no effect on the crown of the fruit, mass loss, decay, or on the incidence of indigenous brown spot, but delayed shell color development, improved fruit appearance by reducing superficial mold growth on the butt of the fruit, and extended shelf life, indicating a potential for shipping pineapple in CA. The optimum O 2 concentration is suggested to be 2%. CA storage (3% O2 and 7%

162

E. YAHIA

CO 2 at 10°C) did not alleviate the expression of black heart symptoms in 'Mauritius' fruits when harvested in the morning, but decreased the incidence of the disorder when fruit were harvested in the evening and held for 2 weeks at 10°C in 7% CO 2 and 3% O 2 (Wilson Wijeratnam et al. 1997). Haruenkit and Thompson (1994) stored 'Smooth Cayenne' fruit imported to England from Mexico in CA of 1 to 2% O 2 plus 0 to 10% CO 2 at 4, 8, or 12°C, and then ripened the fruit at 22°C for 3 and 6 days. Fruit stored in 1 or 2% O2 plus 10% CO 2 showed a delay in the development of internal browning. The authors concluded that pineapples could be stored in these conditions for up to 3 weeks. However, Paull and Rohrback (1985) reported that internal browning of 'Smooth Cayenne' pineapple is not reduced by storage in 3% 02' with or without 5% CO 2 at 8°e. Fruit stored in 3% O 2 at 22°C for one week and followed by one week at 8°C had reduced symptoms. Hypobaric storage is reported to extend the storage life of pineapples by up to 30 to 40 days (Staby 1976). Packaging of 'Mauritius' pineapple in polyethylene bags for 2 weeks at 10°C resulted in an atmosphere of 10% O 2 plus 7% CO 2 and resulted in black heart development (Hassan et al. 1985). However, Abdullah et al. (1985) reported that the same cultivar packaged in 0.07 mm thick polyethylene bags and stored at 10°C for up to 4 weeks followed by one week at 28°C developed less black heart than the control. The atmosphere in these bags had 5-10% O 2 plus 7-13% CO 2 , Waxing 'Smooth Cayenne' fruit with a polyethylene-paraffin mixture (20-50% v/v) increased the concentration of CO 2 in the internal atmosphere, reduced the loss in pH and ascorbic acid in the juice, and delayed the appearance and severity of internal browning after storage for up to 4 weeks at 8°C (Paull and Rohrback 1982; Rohrback and Paull 1982). Powrie et al. (1990) patented a preservation procedure claiming to maintain pineapple pieces for up to 10 weeks in MAP at 1°C, without chilling injury and loss of taste or texture. The fruit is sliced and cut into pieces of 6 to 15 g and packed in DuPont LP 920 plastic pouches. The packages were flushed with a gas mixture containing 15 to 20% O2 and 3% argon, sealed and immediately cooled to 1°C. The ratio of gas to fruit volume was 1.0 to 3.3. Reports on effects of MA/CA on pineapple are contradictory. Ideal atmospheres are not fully defined, but are about 2% O 2 plus 5-10% CO 2 , Very little research has been done on LP and MAP. Currently, no commercial storage in CA is conducted. Research is still needed in a controlled manner to better determine the potential benefits of MA/CA, and to fully define the ideal atmospheres.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

163

P. Rambutan (Nephelium lappaceum L.) Ramhutan is a non-climacteric fruit native to the rain forest of Malaysia. The fruit has a leathery skin covered with fleshy pliable spines called spinterns. Desiccation, loss of red peel color, browning, and drying of spintern are the principal causes of deterioration. Storage life is about 1-3 weeks at 7-12°C (depending on cultivar). Beneficial atmospheres for rambutan are 3-5% O 2 plus 7-12% CO 2 (Kader 1993). These atmospheres delay senescence, retard red color loss, and extend postharvest life to about one month if water loss is controlled. Storage of the cultivar 'R162' in 9 to 120/0 CO 2 retarded color loss and extended shelf life by 4 to 5 days, while 3% 0z, 5 ppm C2 H 4 , or the inclusion ofC zH4 absorbents did not significantly affect the rate of color loss (O'Hare et al. 1994; O'Hare 1995). No further retardation of skin color deterioration was observed with CO 2 levels beyond 12%. The shelf life is increased from 13 to 17 days at 9% CO 2 , Decay was not observed until at least 22 days of storage. The authors suggested that MA/CA is effective through an elevation of the CO 2 concentration and not through a decrease in 02' No deleterious CO 2 effects were observed at concentrations of up to 12%. Storage of rambutan in sealed polyethylene bags (Mendoza et al. 1972; Lam and Ng 1982; Lee and Leong 1982; Inpun 1984; Ketsa and Klaewkasetkorn 1995) or plastic containers (Mohamed and Othman 1988) retarded skin color loss, ameliorated CI, and extended shelf life. The storage life of 'Lebak bulus' fruit packed in 0.03 and 1.0 mm thick polyethylene or polypropylene bags at 10°C is extended to 10 days (Harjadi and Tahitoe 1992). Wax skin coatings were reported to be less effective than polyethylene wrapping in extending storage life (Mendoza et al. 1972; Brown and Wilson 1988). MA/CA containing high concentrations of CO 2 (up to 12%) are beneficial to retard quality loss in rambutan. Research is needed to investigate the beneficial effects of low O2 atmospheres, and the economic feasibility of MA/CA application. Q. Sapodilla (Manilkara achras L., syn. Achras sapota L.)

Sapodilla is a climacteric fruit native to the Yucatan peninsula of Mexico and the province of Peten in Guatemala, and is grown in several tropical regions. The fruit is also known by several other names, such as chiku, dilly, nasberry, sapodilla plum, chico zapote, or nespero. It is a spherical, ellipsoidal fruit ranging from 100 to 500 g in nut. The postharvest life is about 2-3 weeks at 12-16°C and 85-90% RH.

164

E. YAHIA

The storage life of sapodilla is increased by removing ethylene and adding 5-10% CO 2 to the storage atmosphere (Broughton and Wong 1979). A concentration of 20% CO 2 is deleterious. The storage life is also increased when fruit are maintained in an atmosphere with 5 to 10% O2 at 20°C and e 2 H4 is removed (Hatton and Spalding 1990). 'Kalipatti' fruit treated with 60/0 Waxol or 250 or 500 ppm Bavistin, or hot water (50 0 e for 10 min), and wrapped in 150 gauge polyethylene film with 1 % ventilation ripened later than those of the control, but fungal rot was high (Bojappa and Reddy 1990). This is most probably due to high humidity rather than to atmosphere modification. 'Jantuang' fruit were stored inMAP for 4 weeks at 10 0 e or 3 weeks at 15°e, one week longer than fruit without MAP (Mohamed et al. 1995). Further research is still needed to identify optimum atmospheric composition and potential benefits of MA/CA. R. Sugar apple (Custard apple, Sweet sop) (Annona squamosa L.)

The sugar apple is a climacteric fruit indigenous to South America. The storage life is about 4-6 weeks at 5-7°C and 85-90% RH. Ripening of sugar apple was delayed by addition of 10 or 15% CO 2 or removal of O 2 (Broughton and Guat 1979). A concentration of 5% CO 2 did not cause any effect, while 15% CO 2 caused abnormal ripening. The absence of O 2 inhibited fruit ripening and the climacteric rise in respiration. Babu et al. (1990) reported that fruit dipped in 500 ppm Bavistin and kept in polyethylene bags containing KMn0 4 can be maintained for up to 9 days. The recommended atmosphere for sugar apple is 10% CO 2 at 15-20o e and 85- 90% RH. Further research is still needed to investigate the potential benefits of MA/CA. S. Waxapple (Syzygium samarangense) Waxapple fruit are sensitive to CI at 2-10 o e. Sealed polyethylene packaging reduced CI and fruit rotting (Horng and Peng 1983). There is no indication of whether the effect is due to gas or to humidity control. Research is still needed to determine optimum gas concentrations and potential use of MA/CA. V. CONCLUSIONS Tropical fruit are grown in conditions that favor pathogens and insect infestations, far from important markets, and frequently in locations

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

165

that lack adequate technology. These crops are chilling sensitive and most are characterized by a short postharvest life. MA and CA technology can provide major benefits for preserving the quality of these crops, especially during long-term sea transport. About 70% of the published reports on MA/CA of tropical crops has been on avocado, bananas, mango, and papaya; about 25% on cherimoya, durian, lychee, pineapple, rambutan, and sweetpotato; and about 5% on cassava, feijoa, guava, lanzon, loquat, mangosteen, passion fruit, sapodilla, sugar apple, and waxapple. No research has been reported on atemoya, birba, breadfruit, cacao, cashew, coconut, jackfruit, langsat, longan, macadamia, mammee-apple, marney, mountain apple, starfruit, tomatillo, pulsan, white sapote, soursop, tamarind, and yam. Studies on the mode of action of MA/CA have been almost exclusively on avocado and banana, with very little or no attention given to other tropical crops. Potential benefits ofMA and CA for tropical crops (Table 4.5) depend on such factors as the type of crop, the handling methods during pre- and postharvest, and the length of the shipping period. Adequate handling systems, including temperature management, humidity control, avoidance of mechanical damage, sanitation, and ethylene removal treatment (for some crops) are essential for the successful application of MA/CA. The future research needs are listed below in order of priority. 1.

2. 3.

4.

5. 6. 7.

Specify benefits and establish ideal MA/CA for intact and lightly processed tropical fruits, especially those for which little or no information is available. Resolve the fungistatic effect and the mode of action of the antifungal effects of MA/CA. Clarify insecticidal atmospheres, especially in combination with other treatments such as heat. Information that is needed includes tolerance of different fruits to these atmospheres, mortality of different species of insects, ideal gas compositions, temperatures, and duration of treatment. Resolve the mechanism(s) of insect mortality during film wrapping. Elucidate the mode of action of MA/CA in alleviating or augmenting physiological disorders. Clarify the behavior of the fruit after MA/CA and implement methods for handling MA/CA-treated fruits. Investigate the potential use of LP for transport of tropical fruits, especially those with high sensitivity to ethylene that do not require the addition of other gases (such as CO 2 and CO), and develop inexpensive LP technology.

....

O'l O'l

Table 4.5.

Conclusions and recommendations on the use of MA/CA for some tropical fruits. Atmosphere %C0 2

Transport, MApz Insect control

2-5 $0.5

~

3-10 50

Good Poor

Banana

Transport, MAP, storage

2.5

2.5

Excellent

Cherimoya

Transport, storage

2-5

3-10

Good

Durian

Transport

3-5

10-20

Fair

Feijoa

Transport

Not very defined Fair

Guava

Transport

Not defined

Avocado

Intended use

Degree of benefits

%02

Fruit

Comments Among most studied fruits. System is most used to study basis of MA/CA effects. MA/CA very adequate for transport, possible use during storage, but uncertain for use to control insects. Research needed to establish CA for storage and to investigate possible use for insect control. Among most studied fruits. Excellent for transport (used), and for storage (not used yet). Research needed to investigate feasibility of use for storage. MA/CA with ethylene removal has good potential for use during transport. Research needed to define most appropriate MA/CA conditions and potential use. Optimum MA/CA conditions and potential applications not defined. Fruit is tolerant to anaerobic atmospheres. MA/CA conditions and potential applications are not defined. Fruit is sensitive to anaerobic (insecticidal) atmospheres.

Lanzon

Transport

5

0

Fair

Loquat

Undetermined

?

?

?

Lychee

Packaging, transport

5

20

Good

Mango

Transport Insect control

3-5 $0.5

~

5-10 50

Good Excellent

Mangosteen

Transport

2

10

Fair

Papaya

Transport Insect control

2-5 $ 0.5

~

5-8 50

Fair Fair

Passion fruit

Undetermined

?

?

?

Pineapple

Transport

2-5

5-10

Not determined

Sapodilla

Undetermined

5

10

Fair

Sugar apple

Undetermined

5

10

Fair

zModified atmosphere packaging.

~

O'l 'J

Further research needed to establish optimum MA/CA conditions and potential use. Research needed to establish optimum MA/CA conditions and potential application. Research needed to determine optimum MA/CA conditions. Research results are contradictory and further controlled experimental work needed. Excellent potential for insect control especially in combination with high temperature. Further research is needed to determine potential application. Further controlled studies needed to determine adequate MA/CA conditions and potential applications. Research needed to determine adequate MA/CA conditions and potential applications. Reports are contradictory and controlled studies needed to define ideal MA/CA conditions and potential use. Research needed to fully identify ideal MA/CA conditions and potential applications. Research needed to determine optimum MA/CA conditions and potential applications.

168

E. YAHIA

8. Evaluate the potential use of CO and other bioactive gases in combination with MA/CA, especially during transport, and develop safer exposure techniques. 9. Determine the mode of action of MA/CA in order to increase the commercial use of the technology. These studies should contribute further to our understanding of the mechanism by which low 02/high CO 2 control fruit ripening/senescence or cause tissue injury. Very little is known about the protein turnover and gene expression in fruits held in MA/CA. Molecular studies are needed to identify clones for genes that are switched on or off in response to low Oz/high CO 2, to identify molecular markers to monitor responses of fruits to MA/CA, and to manipulate tissue responses. LITERATURE CITED Abd.Rahman, A., N. Maning, and O. Dali. 1997. Respiratory metabolism and changes in chemical compositions of banana fruit after storage in low oxygen atmosphere. Proc. 7th. Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. In press. Abdullah, H., A. R. Abd Shukor, M. A. Rohaya. and P. Mohd Salleh. 1987. Carbon dioxide injury in banana (Musa sp. cv Mas) during storage under modified atmosphere. MARDI Annual Senior Staff Conference, Univ. Malaysia, Kuala Lampur, Jan. 14-17, 1987.

Abdullah, H., M. A. Rohaya, and M. Z. Zaipun. 1985. Effect of modified atmosphere on black heart development and ascorbic acid contents in 'Mauritius' pineapple (Ananas comosus cv 'Mauritius') during storage at low temperature. ASEAN Food J. 1:15-18. Agillon, A. B., N. L. Wade, and M. C. C. Lizada. 1987. Wound-induced ethylene production in ripening. ASEAN Food J. 3(3 & 4):145-148. Aharoni, Y., M. Nadel-Schiffmann, and G. Zaubermann. 1968. Effects of gradually decreasing temperature and polyethylene wraps on the ripening and respiration of avocado fruits. Israel J. Agr. Res. 18:77-82. Akamine E. K. 1959. Effects of carbon dioxide on quality and shelf life of papaya. Hawaii Agr. Expt. Sta. Tech. Prog. Rep. 120. Akamine, E. K. 1960. Preventing the darkening of fresh lychee prepared for export. Hawaii Agr. Expt. Sta. Tech. Prog. Rep. 127. Akamine, E. K. 1969. Controlled atmosphere storage of papayas. Hawaii Univ. Ext. Misc. Publ. 64:23-24. Akamine, E. K. 1971. Controlled atmosphere storage of fresh pineapple. Univ. Hawaii Ext. Publ. Akamine, E. K., and T. Goo. 1968. Controlled atmosphere storage for shelf life extension of irradiated papayas (Carica papaya L. var. Solo). Annu. Rpt. 1967-68. Div., Isotopes U.S. Atomic Energy Comm. p. 63-111. Akamine, E. K., and T. Goo. 1969. Effects of controlled atmosphere storage of fresh papayas (Carica papaya L., var. Solo) with special reference to shelf-life extension of fumigated fruits. Res. Bul. Hawaii Agr. Expt. Sta. 144 (BF). Akamine, E. K., and T. Goo. 1971. Controlled atmosphere storage of fresh pineapple (Ananas cosmos L. 'Smooth cayenne'). Res. Bul. Hawaii Agr. Expt. Sta. 152.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

169

Ali Azizan, M. 1988. Effects of carbon dioxide on the process of ri pening and modified atmosphere storage of 'Mas' bananas. Ph.D. Thesis, Univ. Kebangsaan, Malaysia. Alique, R 1995. Residual effects of short-term treatments with high CO 2 on the ripening of cherimoya (Annona cherimola Mill) fruit. J. Hort. Sci. 70:609-615. Alique, R, and G. S. Oliveira. 1994. Changes in sugars and organic acids in cherimoya (Annona cherimola Mill.) fruit under controlled-atmosphere storage. J. Agr. Food Chern. 42:799-803. Allwood, M. E., and B. N. Wolstenholme. 1995. Modified atmosphere shock treatment and an orchard mulching trial for improving Fuerte fruit quality. Yearbook South African Avocado Grower's Assoc. 18:85-88. Alvarez, A. M. 1980. Improved marketability of fresh papaya by shipment in hypobaric containers. HortScience 15:517-518. Apelbaum, A., Y. Aharoni, and N. Temkin-Gorodeiski. 1977a. Effects of subatmospheric pressure on the ripening processes of banana fruit. Trop. Agr. (Trinidad) 54:3946. Apelbaum, A., G. Zauberman, and Y. Fuchs. 1977b. Prolonging storage life of avocado fruits by subatmospheric pressure. HortScience 12:115-117. Apelbaum, A., G. Zauberman, and Y. Fuchs. 1977c. Subatmospheric pressure storage of mango fruits. Scientia Hort. 7:153-160. Arjona, H. E., F. B. Matta, and J. O. Garner, Jr. 1994. Wrapping in polyvinyl chloride film slows quality loss of yellow passion fruit. HortScience 29:295-296. Arriola, M. C., J. F. Calzada, J. F. Menchu, C. Rolz, R. Garcia, and S. de Cabrera. 1980. Papaya. p. 316-340. In: S. Nagy and P. E. Shaw (eds.). Tropical and subtropical fruits. Avi, Westport, CT. Babu, K. B., Md. Zaheeruddin, and P. K. Prasad. 1990. Studies on postharvest storage of custard apple. Acta Hort. 269: 299. Badran, A. M., and L. Lima. 1969. Controlled atmosphere storage of green bananas. US Patent 3,450,542. Baldwin, E., M. Nispero-Carriedo, and C. Cambell. 1992. Extending storage life of papaya with edible coating. HortScience 27:679. (Abstr.) Banks, N. H. 1984a. Some effects of TAL Pro-long coating on ripening bananas. J. Expt. Bot. 35:127-137. Banks, N. H. 1984b. Studies on the banana fruit surface in relation to the effects of TAL prolong coating on gaseous exchange. Scientia Hort. 24:279-286. Barmore, C. R, and A. H. Rouse. 1976. Pectinesterase activity in controlled atmosphere stored avocados. J. Am. Soc. Hort. Sci. 10:294-296. Bender, R. J., J. K. Brecht. and C. A. Campbell. 1995. Responses of 'Kent' and 'Tommy Atkins' mangoes to reduced O2 and elevated CO 2 , Proc. Florida State Hort. Soc. 107:274-277. Bender, R J., J. K. Brecht, S. A. Sargent, J. C. Navarro, and C. A. Campbell. 1993. Ripening initiation and storage performance of avocado treated with an edible-film coating. Acta Hort. 343:184-186. Bepete, M., N. Nenguwo, and J. E. Jackson. 1994. The effect of sucrose coating on ambient temperature storage of several fruits. p. 427-429. In: B. R. Champ, E. Highley, and G. 1. Johnson (eds.), Postharvest handling oftropical fruits. Proc. Int. Conf., Chiang Mai, Thailand, 19-23 July 1993. ACIAR Proc. 50. Biale, J. B. 1942. Preliminary studies on modified air storage of the Fuerte avocado fruit. Proc. Am. Soc. Hort. Sci. 41:113-118. Biale, J. B. 1946. Effect of oxygen concentration on respiration of 'Fuerte' avocado fruit. Am. J. Bot. 23:363-373.

170

E. YAHIA

Biale, J. B., and R. E. Young. 1981. The avocado pear. p. 1-63. In: A. C. Hulme (ed.), The biochemistry of fruits and their products. Vol. 2. Academic Press, New York. Blankenship, S. M. (ed.). 1985. Controlled atmospheres for storage and transport of perishable agricultural commodities. Proc. 4th Nat. CA Res. Conf., July 23-26, 1985, Raleigh, NG. Blankenship, S. M. 1996. The effect of ethylene during controlled-atmosphere storage of bananas. HortScience 31:638. (Abstr.) Blanpied, G. D. (ed.). 1993. CA'93. Proc. 6th Intl. CA Res. Conf. Northeast Region Agricultural Engineering Service, Cornell Univ., Ithaca, NY, NRAES-71, Vols. 1 & 2. Bleinroth, E. W., J. L. M. Garcia, I. Shirose, and A. M. Carvalho. 19na. Storage of avocado atlow temperature and in controlled atmosphere (in Portuguese). Coletanea lnst. Teenol. Aliment. (Brazil) 8(2):587....:622. Bleinroth, E. W., J. L. M. Garcia, and Y. Yokomizo. 1977b. Low temperature, controlled atmosphere conservation of four varieties of mango. Coletanea Inst. Tecnol. Aliment. (Brazil) 8(1):217-243. Bojappa, K. K. M., and T. V. Reddy. 1990. Postharvest treatments to extend the shelf life of sapota fruit. Acta Hort. 269:391. (Abstr.) Bower, J. P., J. G. M. Cutting, and A. B. Truter. 1989. Modified atmosphere storage and transport of avocados-what does it mean? South African Avocado Growers' Association Yearb. 12: 17-20. Bower, J. P., J. G. M. Cutting, and A. B. Truter. 1990. Container atmosphere, as influencing some physiological browning mechanisms in stored 'Fuerte' avocados. Acta hort. 269:315-321. Brooks, G., C. O. Bratley, and L. P. McColloch. 1936. Transit and storage diseases of fruits and vegetables as affected by initial carbon dioxide treatments. USDA Tech. Bul. 519. Broughton, W. J., and T. GuaL 1979. Storage conditions and ripening of the custard apple (Annona squamosa L.). Scientia Hort. 10: 73-82. Broughton, W. J., and H. C. Wong. 1979. Storage conditions and ripening of chiku fruits Achras sapota L. Scientia Hort. 10:377-385. Broughton, W. J., and K. F. Wu. 1979. Storage conditions and ripening of two cultivars of banana. Scientia Hort. 10:83-93. Brown, B. 1., and P. R. Wilson. 1988. Exploratory study of postharvest treatments on rambutan (Nephelium (sic) lappaceum) 1986/1987 season. Rare Fruit Counc. Austral. NewsI. 48:16-18. Brown, B. I., L. S. Wong, and B. I. Watson. 1985. Use of plastic film packaging and low temperature storage for postharvest handling of rambutan, carambola and sapodilla. p. 272-286. In: Proc. Postharvest Hort. Workshop, Melbourne, Victoria. Brown, D. J. 1981. The effects of low O 2 atmospheres and ethylene and CO 2 production, and l-aminocyclopropane-1-carboxylic acid concentration in banana fruits. MS Thesis, Univ. Maryland, College Park. Brown, E. 0., and M. C. C. Lizada. 1984. Modified atmospheres and deterioration in Ianzones (Lansium domesticum Correa). Postharvest Res. Notes 1(2):36. Buchanan, A. 1994. Tropical fruits: the social, political, and economic issues. p. 18-26. In: B. R. Champ, E. Highley, and G. 1. Johnson (eds.), Postharvest handling of tropical fruits. Proc. Intl. Conf., Chiang MaL Thailand, 19-23 July 1993. ACIAR Proc. 50. Burg, S. P. 1975. Hypobaric storage and transportation of fresh fruits and vegetables. p. 172-188. In: N. F. Haard and D. K. Salunkhe (eds.), Postharvest biology and handling of fruits and vegetables. Avi, Westport, CT. Burg, S. P., and E. A. Burg. 1966. Fruit storage at subatmospheric pressures. Science 153:314-315.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

171

Byers, B. 1977. The Grumman Dormavac system. p. 82-85. In: D. H. Dewey (ed.), Controlled atmospheres for the storage and transport of perishable agricultural commodities. Proc. 2nd Nat. CA Res. Conf., Hort. Rpt. 28, Dept. Hort., Mich. State Univ., East Lansing. Calderon, M., and R. Barkai-Golan (ed.). 1990. Food preservation by modified atmospheres. CRC Press, Boca Raton, FL. Cambell, C. W. 1959. Storage behavior of fresh "Brewster" and "Bengal"lychees. Proc. Fla. State Hort. Soc. 72:356. Campbell, C. W., and R J. Knight, Jr. 1983. Produci6n de granadilla. Comunicaci6n XIII Congreso NORCOFEL. Minesterio de Agricultura, Pesca y Alimentaci6n, Canary Islands, Spain, p. 223-231. Carrillo-Lopez, A., R Rojas-Villagas, and E. M. Yahia. 1996. Ripening and quality of mango fruit as affected by coating with "Semperfresh." Acta Hort. 370:206-216. Carrillo-Lopez, A. y E. M. Yahia. 1990. Tolerancia del aguacate var. Hass a niveles insecticidas de O 2 y CO 2 Y el efecto sobre la respiraci6n anaerobica. Tecnologia de Alimentos (Mexico) 25(6):13-18. Cerrada, E., M. P. eerrada, and M. A. M. Brasil. 1976. Concerva9ao do maracuja amarelo para utiliza9ao in natura. Acta Hort. 57:145-151. Chaplin, G. R, D. Graham, and S. P. Cole. 1986. Reduction of chilling injury in mango fruit by storage in polyethylene bags. ASEAN Food J. 2:139-142. Chaplin, G. R, and M. G. Hawson. 1981. Extending the postharvest life of unrefrigerated avocado (Persea americana Mill) fruit by storage in polyethylene bags. Scientia Hort. 14:219-226. Chaplin, G. R, K. J. Scott, and B. 1. Brown. 1982. Effects of storing mangos in polyethylene bags at ambient temperature. Singapore J. Pri. Ind. 10:84-88. Chau, K. F., and A. M. Alvarez. 1983. Effects of low-pressure storage on Colletotrichum gJoeosprioides and postharvest infection of papaya. HortScience 18:953-955. Chen, J. N., and R. E. Paull. 1986. Development and prevention of chilling injury in papaya fruit. J. Am. Soc. Hort. Sci. 111:639-643. Chen, R C. 1987. Effect of precooling and waxing treatment on mango under hypobaric storage. M.Sc. Thesis, AIT, Bangkok, Thailand. Chen, W. S., M. X. Su, and F. W. Li. 1986. A study on controlled atmosphere storage of lychee. p. 87-88. In: K. M. Chau (ed.), Selection from the Symposium on Litchi Research Papers (1981-1985), Beijing. Chiang, M. N. 1968. Studies on the removal of ethylene from CA-storage of bananas. Spec. PubI. ColI. Agr. Nat. Taiwan. Univ. 20, Taipei, Taiwan. Chiang, M. N. 1970. The effect of temperature and the concentration of O 2 and CO 2 upon the respiration and ripening of bananas, stored in a controlled atmosphere. Spec. Publ. ColI. Agr. Nat. Taiwan Univ. 11:1-13, Taipei, Taiwan. Collin, M. N. 1984. Conservation de l'avocat por chocs CO 2 , Fruits 39:561-566. Daryono, M., and S. Sabari. 1986. The practical method of harvest time on mangosteen fruit and its characteristics in storage. Bul. Penelitian-Hortikultura Indonesia 14(2):3844. De la Plaza, J. L. 1979. Controlled atmosphere storage of cherimoya. p. 701-712. Proc. XV Int. Congr. Refrig., Venice, Italy, Instituto per la Tecnica del Freddo del CNR, Italy, Vol. III. De la Plaza, J. L. 1980. Controlled atmosphere storage of cherimoya. Proc. 15th Int. Congr. Refrig., Venice, 1979, Vol. 3, p. 701-712. De la Plaza, J. L., L. Munoz-Delgado, and C. Iglesias. 1979. Controlled atmosphere storage of cherimoya. Bul. l'institut International du Froid 59(4):1154.

172

E. YAHIA

De la Plaza, J. L., S. Rossi, and M. L. Calvo. 1993. Inhibitory effects of the ethylene chemisorption on the climacteric of cherimoya fruit in modified atmosphere. Acta Hart. 343:181-183. Del Cura, B., M. I. Escribano, J. P. Zamorano, and C. Merodio. 1996. High carbon dioxide delay postharvest changes in RuBPCase and polygalacturonase-related protein in cherimoya peel. J. Am. Soc. Sci. 121:735-739. Dewey, D. H. (ed.). 1977. Controlled atmospheres for the storage and transport of perishable agricultural commodities. Proc. 2nd Nat. CA Res. Conf., Hart. Rpt. 28, Dept. Hart., Michigan State Univ. East Lansing. Dewey, D. H., R C. Herner, and D. R Dilley (eds.). 1969. Controlled atmospheres for the storage and transport of horticultural crops. Proc. Nat. CA Res. Conf., Hart. Rpt. No.9, Dept. Hart., Michigan State Univ. Dhalla, R, and S. W. Hanson. 1988. Effect of permeable coatings on the storage life of fruits. II. Pro-long treatment of mangoes (Mangifera indica L. cv. Julie). Int. J. Food Sci. Technol. 23:107-112. Duan, H., S. G. Gilbert, Y. Ashkenazi, and Y. Hening. 1973. Storage quality of bananas packaged in selected permeability films. J. Food Sci. 38:1247-1250. Dull, G. G. 1971. The pineapple: General. p. 303-324. In: A. C. Hulme (ed.), The biochemistry of fruits and their products. Academic Press, London. Dull, G. G., R E. Young, and J. B. Hiale. 1967. Respiratory patterns in fruit of pineapple, Ananas comosus detached at different stages of development. Physiol Plant. 20:1059-1065. Durand, B. J., L. Orcan, U. Yanko, G. Zauberman, and Y. Fuchs. 1984. Effect of waxing on moisture loss and ripening of 'Fuerte' avocado. HortScience 19:421-422. Eksteen, G. J., and A. B. Truter. 1985. Effect of controlled and modified atmosphere storage on quality of eating ripe avocados. Yearb. South African Avocado Growers Assn. 9:33. Eksteen, G. J., and A. B. Truter. 1989. Transport simulation test with avocados and bananas in controlled atmosphere containers. Yearb. South African Avocado Growers Assn. 12:26-32. Eksteen, G. J., A. B. Truter, and L. L. Vorster. 1992. Long-distance controlled atmosphere transport of avocados. p. 463-466. In: C. Lovatt et a1. (eds.), Proc. 2nd World Avocado Congr., April 21-26, 1991, Orange, CA. EI-Goorani, M. A., and N. F. Sommer. 1981. Effects of modified atmospheres on postharvest pathogens of fruits and vegetables. Hort. Rev. 3:412-461. Esguerra, E. B., D. B. Mendoza, Jr., and E. R. B. Pantastico. 1978. II. Use of perlite-KMn04 insert as an ethylene absorbent. Phillip. J. Sci. 107:1-2. Faubion, D. F., F. G. Mitchell, G. Mayer, and M. L. Arpaia. 1992. Response of "Hass" avocado to postharvest storage in controlled atmosphere conditions. p. 467-472. In: C. Lovatt et a1. (eds.), Proc. 2nd World Avocado Congr., April 21-26, 1991, Orange, CA. Federal Register. 1984. Ethylene dibromide; amendment of notice to cancel registrations of pesticide products containing ethylene dibromide. 49:14182-14185. Fellman, J. K. (ed.). 1989. Proc. 5th Intl. CA Res. Conf. (June 14-16, 1989), Wenatchee, WA, Vols. 1 and 2. Fans, J. F. 1990. Quarantine barriers treatments as a means to facilitate trade. Acta Hart. 269:435-439. Fuchs, Y., and N. Temkin-Forodeiski. 1971. The course of ripening of banana fruits in sealed polyethylene bags. J. Am. Soc. Hort. Sci. 96:401-402. Gane, R 1936. A study of the respiration of bananas. New Phytol. 35:383.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

173

Gautam, D. M., and M. C. C. Lizada. 1984. Internal breakdown in 'Carabao' mango subjected to modified atmospheres. Storage duration and severity of symptoms. Postharvest Res. Notes 1(2):28. (Postharvest Hart. Training and Res. Center, Dept. Hart., Univ. Philippines, Los Banos). Gemma, H., C. Oogaki, M. Fukushima, T. Yamada, and Y. Nose. 1989. Preservation of some tropical fruits with an apparatus of low pressure storage. J. Japan. Soc. Food Sci. Technol. 36:508-518. Gerdes, D. 1., and V. Parrino-Lowe. 1995. Modified atmosphere packaging (MAP) of Fuerte avocado halves. Lebensm.-Wiss.-u.-Technol. 28:12-16. Godfrey Lubulwa, A. S., and J. S. Davis. 1994. An economic evaluation of postharvest tropical fruit research: some preliminary results. p. 32-49. In: B. R Champ, E. Highley, and G. I. Johnson (eds.), Postharvest handling of tropical fruits. Proc. IntI. Conf., Chiang Mai, Thailand, 19-23 July 1993. ACIAR Proc. 50. Gonzalez, G.. E. M. Yahia, and I. Higuera. 1990. Modified atmosphere packaging of mango and avocado fruit. Acta Hart. 269:335-344. Gould, W. P.. and J. L. Sharp. 1990. Caribbean fruit fly (Diptera: Tephritidae) mortality induced by shrink-wrapping infested mangoes. J. Econ. Entomoi. 83:2324-2326. Guelfat-Reich, S. 1970. Storage of loquats (in French). Fruits Outre Mer. 25:169. Harjadi, S. S., and D. Tahitoe. 1992. The effects of plastic film bags at low temperature storage on prolonging the shelf-life of rambutan (Nephelium lappaceum) cv. Lebak bulus. Acta Hort. 321:778-785. Haruenkit. R, and A. K. Thompson. 1994. Storage of fresh pineapples. p. 422-426. In: B. R Champ, E. Highley, and G. I. Johnson (eds.), Postharvest handling of tropical fruits. Proc. IntI. Conf., Chiang Mai, Thailand, 19-23 July 1993. ACIAR Proc. 50. Harvey, J. M. 1977. In-transit atmosphere modification. Effects on quality of fruits and vegetables. p. 71-78. In: D. H. Dewey (ed.), Controlled atmospheres for the storage and transport of perishable agricultural commodities. Proc. 2nd Nat. CA Res. Conf., Hart. Rpt. No. 28, Dept. Hort., Michigan State Univ., East Lansing. Hassan, A., R T. Atan, and Z. M. Zaino 1985. Effect of modified atmosphere on black heart development and ascorbic acid contents in 'Mauritius' pineapples (Ananas comosus cv. 'Mauritius') during storage at low temperature. ASEAN Food J. 1(1):15-18. Hatton, T. T., Jr., and W. F. Reeder. 1965. Controlled atmosphere storage of Lula avocados-1965 tests. Proc. Caribbean Reg. Am. Soc. Hort. Sci. 9:152-159. Hatton, T. T. and W. F. Reeder. 1966. Controlled atmosphere storage of Keitt mangoes, 1965. Proc. Carib. Reg. Amer. Soc. Hort. Sci. 10:114-119. Hatton, T. T., Jr., and W. F. Reeder. 1967. Controlled atmosphere storage of Keitt mangoes, 1965. Proc. Am. Soc. Hort. Sci. (Caribbean Region) 10:114-119. Hatton, T. T., Jr., and W. F. Reeder. 1969a. Responses of Florida avocados, mangos and limes in several controlled atmospheres. Proc. Nat. CA Res. Conf., Michigan State Univ. Hort. Rpt. 9. East Lansing. p. 72-73. Hatton, T. T., and W. F. Reeder. 1969b. Maintaining market quality of Florida avocado. In: Proc. Conf. Tropical Subtropical Fruits. Tropical Products Instit. Conf., Univ. of London. England. Hatton, T. T., Jr., and W. F. Reeder. 1969c. Controlled atmosphere storage of papayas (1968). Proc. Trap. Reg. Amer. Soc. Hort. Sci. 13:251-256. Hatton, T. T., Jr., and W. F. Reeder. 1972. Quality of 'Lula' avocados stored in controlled atmospheres with and without ethylene. J. Am. Soc. Hart. Sci. 97:339-341. Hatton, T. T., Jr., and D. H. Spalding. 1974. Maintenance of market quality in Florida avocados. In: ASHRAE Trans. Part I. Vol. 80.

174

E. YAHIA

Hatton, T. T., Jr., and D. H. Spalding. 1990. Controlled atmosphere storage of some tropical fruits. p. 301-313. In: M. Calderon and R. Barkai-Golan (eds.), Food preservation by modified atmospheres. CRC Press, Boca Raton, FL. Hess, B., D. Ke, and A. A. Kader. 1993. Changes in intracellular pH. ATP, and glycolytic enzymes in 'Hass' avocado in response to low O 2 and high CO 2 stresses. p. 1-9. Proc. 6th Int. CA Res. Conf., Cornell Univ., Ithaca, NY. Hesselman, G. W., and H. T. Freebairn. 1986. Rate ofripening of initiated bananas as influenced by oxygen and ethylene. J. Am. Soc. Hort. Sci. 94:635-637. Hewage, S. K., H. Wainwright, S. W. Wijerathnam, and T. Swinburne. 1995. The modified atmosphere storage of bananas as affected by different temperatures, p. 172-176. In: A. Ait-Oubahou and M. EI-Otmani (eds.), Postharvest physiology and technologies for horticultural commodities: Recent advances. Institut Agronomique & Veterinaire Hassan II, Agadir, Morocco. Horng, D., and C. Pengo 1983. Studies on package, transportation and storage of waxapple fruits (Syzygium samarangense) (in Japanese). NCHU Horticulture 8:31-39. Idler, L. 1993. Employment of CA on board seagoing vessels in porthole containers. p. 252-291. In: CA'93. Proc. Sixth CA Res. Conf., Cornell Univ., Ithaca, NY, June 15-17, 1993. Ilangantileke, S., and V. Salokhe. 1989. Low-pressure storage of Thai mango. p. 103-117. In: Fifth Proceedings. Vol. 2. Other commodities and storage recommendations. Fifth CA Res. Conf., Wenatchee, WA, June 14-16, 1989. Inpun, A. 1984. Effect of temperature and packaging materials (polyethylene bags, plastic baskets) on postharvest quality and storage life of rambutan (NephiJium Jappaceum L.) var. Seechompoo. (in Thai). Monograph, Dept. Hortic., Kasetsart Univ., Bangkok. Isenberg, F. M. R. 1979. Controlled atmosphere storage of vegetables. Hort. Rev. 1:337-394. Jang, E. B. 1990. Fruit fly disinfestation of tropical fruits using semipermeable shrink-wrap film. Acta Hort. 269:453-458. Jordan, R. A., and L. R. Barker. 1992. Controlled atmosphere storage ofHass avocado. HPG Biennial Rev., QDPI, 4-5. Jordan, R. A., and L. G. Smith. 1993. The responses of avocado and mango to storage atmosphere composition. p. 629-638. In: CA'93. Proc. Sixth CA Res. Conf., Cornell Univ., Ithaca, NY. Kader, A. A. 1985. Modified atmospheres. An indexed reference list with emphasis on horticultural commodities, supplement No.4 (Jan. 1, 1981 to May 31, 1985). Postharvest Horticulture Series 3, Univ. California, Davis. Kader, A. A. 1986. Biochemical and physiological basis for effects of controlled and modified atmospheres on fruits and vegetables. Food Technol. 40(5):100, 102-104. Kader, A. A. 1993. Modified and controlled atmosphere storage of tropical fruits. p. 239-249. In: B. R. Champ, E. Highley, and G. 1. Johnson (eds.), Postharvest handling of tropical fruits. Proc. Int. Conf., Chiang MaL Thailand, 19-23 July 1993. ACIAR Proc.50. Kader, A. A., and D. Ke. 1994. Controlled atmospheres. p. 223-236. In: R. E. Paull and J. W. Armstrong (eds.), Insect pests and fresh horticultural products: Treatments and responses. CAB Int., Wallingford, UK. Kader, A. A., and L. 1. Morris. 1977. Modified atmospheres. An indexed reference list with emphasis on horticultural commodities, supplement No.2 (May 1, 1974 to Feb. 28, 1977). Vegetable Crops Series 187, Univ. California, Davis. Kader, A. A., and L. 1. Morris. 1981. Modified atmospheres. An indexed reference list with emphasis on horticultural commodities, supplement No.3 (March 1, 1977 to Dec. 31, 1980). Vegetable Crops Series 213, Univ. California, Davis.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

175

Kader, A. A, M. S. Olds, P. V. Moyer, and D. Zagory. Modified atmospheres. An indexed reference list with emphasis on horticultural commodities. Postharvest Horticultural Series 14, Dept. Pomology, U.c. Davis, CA Kader, A. A, D. Zagory, and E. 1. Kerbel. 1989. Modified atmosphere packaging of fruits and vegetables. CRC Crit. Rev. Food Sci. Nutr. 28(1):1-30. Kane, 0., and P. Marcellin. 1979. Effects of controlled atmosphere on the storage of mangoes (varieties Amelie and Julie) (in French). Fruits 34(2): 123-129. Kanellis, A K, M. M. Hassan, K A Loulakakis, and K A Roubelakis-Angelakis. 1993. Biochemical and molecular aspects of the low oxygen action on fruit ripening. p. 117-122. In:]. C. Pech, A Latche, and C. Balague (eds.), Cellular and molecular aspects ofbiosynthesis and action of the plant hormone ethylene. Kluwer Academic Publ., Dordrecht. Kanellis, A. K, and T. Solomos. 1985. The effect oflow oxygen on the activities of pectinmethyl esterase and acid phosphatase during the course of ripening of bananas. p. 20-26. In: S. M. Blankenship (ed.), Proc. 4th Nat. CA Res. Conf., Hort. Rpt. 126, Dept. Hort. Sci., North Carolina State Univ., Raleigh. Kanellis, A. K, T. Solomos, and A. K Mattoo. 1989a. Changes in sugars, enzymic activities and acid phosphatase profiles of bananas ripened in air or stored in 2.5% O 2 with and without ethylene. Plant Physio!. 90:251-258. Kanellis, A K, T. Solomos, and A K Mattoo. 1989b. Hydrolytic enzyme activities and protein pattern of avocado fruit ripened in air and in low oxygen, with and without ethylene. Physiol. Plant. 90:259-266. Kanellis, A K., T. Solomos, A M. Mehta, and A K Mattoo. 1989c. Decreased cellulase activity in avocado fruit subjected to 2.5% O 2 correlates with lower cellulase protein and gene transcript levels. Plant Cell Physiol. 30:829-834. Kanellis, A. K., T. Solomos, and K A. Roubelakis-Angelakis. 1991. Suppression of cellulase and polygalacturonase and induction of alcohol dehydrogenase isoenzymes in avocado fruit mesocarp subjected to low oxygen stress. Physiol. Plant. 96:269-274. Kapur, N. S., K S. Rao, and H. S. Srivastava. 1962. Refrigerated gas storage of mangoes. Food Sci. 11:228-231. Ke, D., and A A Kader. 1992. Potential of controlled atmospheres for postharvest insect disinfestation of fruits and vegetables. Postharvest News and Information 3(2):31N-37N. Ke, D., E. Yahia, B. Hess, 1. Zhou, and A Kader. 1995. Regulation of fermentative metabolism in avocado fruit under oxygen and carbon dioxide stress. J. Am. Soc. Hort. Sci. 120:481-490. Ketsa, S., and O. Klaewkasetkorn. 1995. Effect of modified atmosphere on chilling injury and storage life of rambutan. Acta Hort. 398:223-231. Ketsa, S., and K Leelawatana. 1992. Effect of precooling and polyethylene film liners in corrugated boxes on quality of lychee fruits. p. 742-746. In: S. Subhadrabandhu (ed.), Frontier in tropical fruit research. Int. Soc. Hort. Sci., Wageningen, Netherlands. Khedkar, D. M., K W. Ansarwadkar, R. S. Dabhade, and A. L. Ballal. 1982. Extension of storage life of guava (var. 1.-49). Indian Food Packer 35(2):49. Kubo, Y.. A. Inaba, and R. Nakamura. 1990. Respiration and ethylene production in various harvested crops held in CO 2 -enriched atmospheres. ]. Am. Soc. Hort. Sci. 115:975-978. Lakshminarayana, S., and H. Subramanyam. 1970. Carbon dioxide injury and fermentative decarboxylation in mango fruit at low temperature storage. J. Food Sci. Technol. 7(3):148-152. Lam, P. F., and K H. Ng. 1982. Storage of waxed and unwaxed rambutan in perforated and sealed polyethylene bags. Proc. Workshop on mango and rambutan, Univ. Philippines, Los Banos, p. 190-210.

176

E. YAHIA

Lazan, H., Z. M. Ali, and M. K. Selamat. 1993. The underlying biochemistry of the effect of modified atmosphere and storage temperature on firmness decrease in papaya. Acta Hort. 343:141-147. Lazan, H., Z. M. Ali, and W. C. Sim. 1990. Retardation of ripening and development of water stress in papaya fruit seal-packaged with polyethylene film. Acta Hort. 269:345-358. Lee, S. K, and P. C. Leong. 1982. Storage studies on the rambutan in Singapore. p. 172-175. Proc. Workshop on mango and rambutan, University of the Philippines, Los Banos. Liu, F. W. 1970. Storage of bananas in polyethylene bags with an ethylene absorbent. HortScience 5:25-27. Liu, F. W. 1976a. Storing ethylene-pretreated bananas in controlled atmosphere and hypobaric air. J. Am. Soc. Hort. Sci. 101:198-201. Liu, F. W. 1976b. Correlation between banana storage life and minimum time required for ethylene response. J. Am. Soc. Hort. Sci. 101:63-65. Lizada, C. c., and V. Noverio. 1983. The effect of Pro-long on patterns of physico-chemical and physiological changes in the ripening of bananas. Laguna: PHTRC, 1983, Annu. Rep., The Philippines. Lonsdale, J. H. 1993. Maintaining market quality of lychee overseas without S02' South African Litchi Growers Assoc. Yearb. 5:25-28. Lougheed, E. C., and S. Q. Feng. 1989. Pragmatic assessment of the potential of CA. p. 217-223. In: Fifth Proceedings. Vol. 2. Other commodities and storage recommendations. Proc. 5th CA Res. Conf., Wenatchee, Wash., June 14-16, 1989. Lowings, P. H., and D. F. Cuts. 1982. The preservation of fresh fruits and vegetables. IFST Proc. 15:52-54. Lugg, J. R 1969. The Transfresh system of atmospheres for produce transportation. In: Controlled atmospheres for the storage and transport of horticultural crops. Proc. Natl. CA Res. Conf., Mich. State Univ., Hort. Rep. 9:58-59, East Lansing. Lugg, J. R 1977. The Transfresh system for transportation of perishables. p. 79-81. In: D. H. Dewey (ed.), Controlled atmospheres for the storage and transport of perishable agricultural commodities. Proc. 2nd Nat. CA Res. Conf., Hort. Rpt. 28, Dept. Hort., Michigan State Univ., East Lansing. Madie, G. R, Jr. 1955a. Wrapping and packaging of fresh lychee. Fla. Lychee Growers Assoc. Yearb. 1:25. Madie, G. R, Jr. 1955b. Packaging and storage of lychee fruits, preliminary experiments. Fla. Lychee Growers Assoc. Yearb. 1:44. Madie, G. R, Jr. 1956. Packaging and handling of fresh lychee fruit. Fla. Lychee Growers Assoc. Yearb. 2:15. Maekawa, T. 1990. On the mango CA storage and transportation from subtropical to temperate regions in Japan. Acta Hort. 269:367-374. Maharaj, R., and C. K. Sankat. 1990. Storability of papayas under refrigerated and controlled atmosphere. Acta Hort. 269:375-385. Malcom, G. L. 1989. Controlled atmospheres: Now a reality with membranes. Proceedings of the Cargo Systems Containers & Intermodal Conference, Nov. 28-30, 1989, Hamburg, Germany. Malcom, G. L. 1993. Impact of advanced air separation technology on controlled atmosphere equipment markets. p. 307-313. In: CA'93. Proc. 6th CA Res. Conf., Cornell Univ. Ithaca, NY, June 15-17,1993. Mapson, L. W., and J. E. Robinson. 1966. Relation between O2 tension, biosynthesis of ethylene, respiration and ripening changes in banana fruit. J. Food Technol. 1:215-225. Marcellin, P., and A. Chavez. 1983. Effects of intermittent high CO 2 treatment on storage

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

177

life of avocado fruits in relation to respiration and ethylene production. Acta Hort. 138:155-163. McGlasson, W. B. 1989. MA packaging. A practical alternative to CA shipping containers. p. 235-240. In: Fifth Proceedings. Vol. 2. Other commodities and storage recommendations. Proc. 5th Int. CA Res. Conf., Wenatchee, WA, June 14-16, 1989. McGlasson, W. B., and R. B. H. Wills. 1972. Effects of oxygen and carbon dioxide on respiration, storage life, and organic acids of green bananas. Austral. J. BioI. Sci. 25:35-42. McGuire, R. G., and G. J. Hallman. 1995. Coating guavas with cellulose- or carnauba-based emulsions interferes with postharvest ripening. HortScience 30:294-295. McLauchlan, R. L., S. N. Ledger, and L. R. Barker. 1992. Simulated export of avocado by sea under controlled atmosphere. HPG Biennial Rev. 1992. Md.Yon, R, and A. Abd. Rahman. 1997. MA shipment of papaya (Carica papaya L.) cv. Eksotica to Dubai. Proc. 7th. Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press) Mendoza, Jr., D. B., ER. B. Pantastico, and F. B. Javier. 1972. Storage and handling of rambutan (Nephelium lappaceum L.). Philippines Agr. 55:322-332. Metzidakis,1. T., and E. M. Safkiotakis. 1995. Physiological disorders induced by low oxygen on avocado fruits. Acta Hort. 379:397-403. Miller, W. R, P. W. Hale, D. H. Spalding, and P. Davis. 1983. Quality and decay of mango fruit wrapped in heat-shrinkable film. HortScience 18:957-958. Miller, W. R, D. H. Spalding, and P. W. Hale. 1986. Film wrapping mangoes at advanced stages of postharvest ripening. Trop. Sci. 26:9-17. Mohamed, S., and E. Othman. 1988. Effect of packaging and modified atmosphere on the shelf life oframbutan (Nephelium lappaceum). Pertanika 11 :217-228. Mohamed, S., B. Taufik, and M. N. A. Karim. 1995. Effects of modified atmosphere packaging on the physiological characteristics of ciku (Arcas sapota L.) at various storage temperatures. J. Sci. Food Agr. 70:231-240. Moriguchi, T., and R. Romani. 1995. Mitochondrial self-restoration as an index to the capacity of avocado fruit to sustain stress at two climacteric states. J. Am. Soc. Hort. Sci. 120:643-649. Nazeeb, M., and W. J. Broughton. 1978. Storage conditions and ripening of papaya "Bentong" and "Taiping". Scientia Hort. 9(3):265-277. Noomhorm, A., and N. Tiasuwan. 1995. Controlled atmosphere storage of mango fruit, Mangifera indica L. cv. Rad. J. Food Proc. Preserv. 19:271-281. Nuevo, P. A., A. U. Cua, and M. C. C. Lizada. 1984a. Internal Breakdown in 'Carabao' mango subjected to modified atmospheres. III. Starch in the spongy tissue. Postharvest Res. Notes 1(2):63. (Postharvest Hart. Training and Res. Center, Dept. Hart., Univ. Philippines, Los Banos). Nuevo, P. A, ER. B. Pantastico, and D. B. Mendosa. 1984b. Gas diffusion factors in fruits. 1. Anatomical structure in mango fruit. Postharvest Res. Notes 1(1):1. (Postharvest Hort. Training and Res. Center, Dept. Hort., Univ. Philippines, Los Banos). O'Hare, T. J. 1995. Postharvest physiology and storage of rambutan. Postharvest BioI. TechnoI. 6:189-199. O'Hare, T. J., and A Prasad. 1993. The effect of temperature and carbon dioxide on chilling symptoms in mango. Acta Hort. 343:244-250. O'Hare, T. J., A. Prasad, and A W. Cooke. 1994. Low temperature and controlled atmosphere storage of rambutan. Postharvest BioI. TechnoI. 4:147-157. Olorunda. A. a. 1976. Effect of ethylene absorbent on the storage life of plantain packed in polyethylene bags. Nigerian J. Sci. 10(1/2):19-26. audit. D. D., and K. J. Scott. 1973. Storage of Hass avocados in polyethylene bags. Trop. Agr. (Trinidad) 50(3):241-243.

178

E. YAHIA

Overholser, E. L. 1928. Some limitations of gas storage of fruits. Ice Refrig. 74:551. Palma, T., D. W. Stanley, ]. M. Aguilera, and ]. P. Zoffoli. 1993. Respiratory behavior of cherimoya (Annona cherimola Mill) under controlled atmospheres. HortScience 28:647-649. Pantastico, ER. B., D. B. Mendoza, ]r., and R. M. Abilay. 1969. Some chemical and physiological changes during storage of lanzones (Lansium domesticum Correa). Philippine Agr.52:505-517. Parker, S. 1993. Controlled atmospheres can reduce cargo losses. The Motor Ship 74(870):16-20. Parsons, C. S.,]. E. Gates, and D. H. Spalding. 1964. Quality of some fruits and vegetables after holding in nitrogen atmospheres. Proc. Am. Soc. Hort. Sci. 84:549-566. Pastor, R. L., and ER. B. Pantastico. 1984. Storage characteristics of waxed cooking bananas. Postharvest Res Notes 1:23-24. (Postharvest Hart. Training and Res. Center, Dept. Hort., Univ. Philippines, Los Banos). Paull, R. E., and ]. W. Armstrong (eds.). 1994. Insect pests and fresh horticultural products. Treatments and responses. CAB Int., Wallingford, UK. Paull. R. E., and ]. N. Chen. 1987. Effect of storage temperature and wrapping on quality characteristics of litchi fruit. Scientia Hart. 33:223-236. Paull, R. E., and ]. N. Chen. 1989. Waxing and plastic wraps influence water loss from papaya fruit during storage and ripening. ]. Am. Soc. Hort. Sci. 114:937-942. Paull, R. E., and K. G. Rohrback. 1982. Juice characteristics and internal atmosphere of waxed 'Smoth Cayenne' pineapple fruit. ]. Am. Soc. Hart. Sci. 107:448-452. Paull, R. E., and K. G. Rohrback. 1985. Symptoms development of chilling injury in pineapple fruit. ]. Am. Soc. Hart. Sci. 110:100-105. Pesis, E., R. Marinansky, G. Zauberman, and Y. Fuchs. 1993. Reduction of chilling injury symptoms of stored avocado fruit by prestorage treatment with high nitrogen atmosphere. Acta Hort. 343:252-255. Pesis, E., R. Marinansky, G. Zauberman, and Y. Fuchs. 1994a. Prestorage low-oxygen atmosphere treatment reduces chilling injury symptoms in 'Fuerte' avocado fruit. HortScience 29:1042-1046. Pesis, E., R. Marinansky, I. Rot, and A. Weksler. 1994b. Effect of postharvest application of acetaldehyde or a short period of anaerobiosis on fruit senescence. Proc. Royal Soc. Edinburg 102B:473-478. Pesis, E., G. Zauberman, and 1. Avissar. 1991. Induction of certain aroma volatiles in feijoa fruit by postharvest application of acetaldehyde or anaerobic conditions. ]. Sci. Food Agr. 54(3):329-337. Philippines Council for Agriculture and Resource Research. 1978. The Philippines recommendations for mango. PCARRD Tech. Bul., Ser. 38, Los Banos, Laguna. Plata, M. C., L. S. de Medina, M. Martinez-Cayuela, M. J. Faus, and A. Gil. 1987. Changes in texture, protein content and polyphenoloxidase and peroxidase activities in cherimoya induced by ripening in hypobaric atmospheres or in presence of sulfite (in Spanish). Rev. Agroquimica Tecnol. Alim. 27:215-224. Powrie, W. D., R. Chiu, H. Wu, and B. ]. Skura. 1990. Preservation of cut and segmented fresh fruit pieces. U.S. Patent 4,895,729. Prusky, D., L. Karni, 1. Kobiler, and A. A. Plumbley. 1991a. Induction of the pre-formed antifungal diene in unripe avocado fruits: effect of challenge inoculation by Colletotrichum gJoeosporioides. Physiol. Molec. Plant Patho!' 37:425-435. Prusky, D., N. T. Keen, ]. ]. Sims, and S. Midland. 1982. Possible involvement of an antifungal compound in latency of CoJ1etotrichum gJoeosporioides in unripe avocado fruit. Phytopathology 72:1578-1582.

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

179

Prusky, D., 1. Kobiler, R. Ardi, and Y. Fishman. 1993. Induction ofresistance of avocado fruit to ColJetotrichum gloeosporioides attack using CO 2 treatments. Acta Hort. 343:325-330. Prusky, D., 1. Koliber, andB. Jacoby. 1988. Involvement of epicatechin in cultivar susceptibility of avocado fruits to Colletotrichum gJoeosporioides by CO 2 treatment. Physio!. Molec. Plant Pathol. 39:325-334. Prusky, D., 1. Kobiler, B. Jacoby, J. J. Sims, and S. L. Midland. 1985. Inhibitors of avocado lipoxygenase: their possible relationship with the latency of Colletotrichum gJoeosporioides. Physiol. Plant Pathol. 27:269-279. Prusky, D., R. A. Plumbley, and 1. Kobiler. 1991b. Modulation of natural resistance of avocado fruits to Colletotrichum gJoeosprioides by CO 2 treatment. Physiol. Molecul. Plant PathoI. 39:325-334. Quazi, M. G., and H. T. Freebairn. 1970. The influence of ethylene, oxygen and carbon dioxide on the ripening of bananas. Bot. Gaz. 131:5-14. Rattanachinnakorn, B., J. Phumhiran, and S. S. Nanthachai. 1996. Controlled atmosphere storage of mangosteen (in Thai). Annu. Tech. Conference Proc., Hort. Res. Inst., Dep. Agr., Bangkok, Thailand. Richardson, D. G., andM. Meheriuk (eds.). 1982. Controlled atmospheres for storage and transport of perishable agricultural commodities. Timber Press, Beaverton, OR. Rodov, V., S. Ben-Yehoshua, S. Fishman, S. Gotlieb, T. Fierman, and D. Q. Fang. 1994. Reducing decay and extending shelf life of bell-peppers and mangoes by modified atmosphere packaging. p. 416-418. In: B. R. Champ, E. Highley, and G. 1. Johnson (eds.), Postharvest handling of tropical fruits. Proc. Int. Conf., Chiang Mai, Thailand, 19-23 July 1993. ACIAR Proc. 50. Rohbrach, K. G., and R. E. Paull. 1982. Incidence and severity of chilling induced internal browning of waxed 'Smooth Cayene' pineapple. J. Am. Soc. Hort. Sci. 107:453-457. Rojas-Villegas, A., A. Carrillo-Lopez, M. Silveira, R. Avena-Bustillos, and E. Yahia. 1996. Effects of insecticidal atmospheres on the mortality of fruit flies in mango. Acta Hort. 370:89-92. Salazar, R. y R. Torres. 1977. Almacenamiento de frutos de maracuya en bolsas de polyetileno. Revista ICA-Bogota, Colombia 12(1):1-11. Salunkhe, D. K., and S. S. Kadam (eds.). 1995. Handbook of fruit science and technology. Production, composition, storage, and processing. Marcel Dekker, New York. Sankat, C. K., and R. Maharaj. 1989. Controlled atmosphere storage of papayas. Proc. 5th Int. CA Res. Conf. (June 14-16,1989), Wenatchee, WA, p. 161-170. Satyan, S. H., K. J. Scott, and D. Graham. 1992a. Storage of banana bunches in sealed polyethylene tubes. J. Hort. Sci. 67:283-287. Satyan, S. H., K. J. Scott, and D. J. Best. 1992b. Effects of storage temperature and modified atmospheres on cooking bananas grown in New South Wales. Trop. Agr. 69:263-267. Scott, K. J. 1971. Polyethylene bags and ethylene absorbent for transporting bananas. Agr. Gaz. N.S.W. 82: 267-269. Scott, K. J. 1975. The use of polyethylene bags to extend the life of bananas after harvest. Food Technol. Austral. 27:481-482. Scott, K. J., J. R. Blake, G. Strachan, B. L. Tugwell, and W. B. McGlasson. 1971. Transport of bananas at ambient temperature using polyethylene bags. Trop. Agr. (Trinidad) 48:245-254. Scott, K. J., B. 1. Brown, G. R. Chaplin, M. E. Wilcox, and J. M. Bain. 1982. The control of rotting and browning of litchi fruit by hot benomyl and plastic film. Scientia Hort. 16:253-262.

180

E. YAHIA

Scott, K. J., and G. R. Chaplin. 1978. Reduction of chilling injury in avocados stored in sealed polyethylene bags. Trop. Agr. (Trinidad) 55(1):87-90. Scott, K. J., and S. Gandanegara. 1974. Effect of temperature on the storage life of bananas held in polyethylene bags with ethylene absorbent. Trop. Agr. (Trinidad) 51 :23-26. Scott, K. J., W. B. McGlasson, and E. A. Roberts. 1968. Ethylene absorbent increase storage life of bananas packed in polyethylene absorbent. Agr. Gaz. N.S.W. 79:52. Scott. K. J., W. B. McGlasson, and E. A. Roberts. 1970. Potassium permanganate as an ethylene absorbent in polyethylene bags to delay ripening of bananas during storage. Austral. ]. Expt. Agr. Anim. Husb. 10:237-240. Scott, K. J., and E. A Roberts. 1966. Polyethylene bags to delay ripening of bananas during transport and storage. Austral. J. Expt. Agr. Anim. Husb. 6:197-199. Shetty, K. K., M. J. Klowden, E. B. Jang, and W. Koshan, 1989. Individual shrink wrapping technique for fruit fly disinfestation in tropical fruits. HortScience 24:317-319. Shorter, A. J., K. J. Scott, and D. Graham. 1987. Controlled atmosphere storage of bananas in bunches at ambient temperatures. CSIRO Food Res. Q. 47:61-63. Singh, B. N., P. V. V. Seshagiri, and S. S. Gupta. 1937. The response of the respiratory system in mango and guava to alteration in the concentrations 'of oxygen and nitrogen. Ann. Bot. (London) 1(2):31l-323. Singh, R. 1957. Improvement of packaging and storage of litchi at room temperature. Ind. ]. Hort. 14:205. Siriphanich, J. 1994. Minimal processing of tropical fruits. p. 127-137. In: B. R. Champ, E. Highley, and G. I. Johnson (eds.), Postharvest handling of tropical fruits. Proc. Int. Conf., Chiang Mai, Thailand, 19-23 July 1993. ACIAR Proc. 50. Siriphanich, J. 1996. Storage and transportation of tropical fruits: A case study of Durian. p. 439-451. In: S. Vijaysegaran, M. Pauziah, M. S. Mohamed, and S. Ahmed Tarmizi (eds.), Proc. Int. Conf. Trap. Fruits. Kuala Lumpur, Malaysia, 23-26 July 1996. Sive, A, and D. Resinsky. 1989a. Storage as a solution to a number of problems in the avocado industry (in Hebrew). Alan Hanotea 44(1):39-46. Sive, A, and D. Resinsky. 1989b. CA storage trials of mangoes. Report 1988 season (in Hebrew). Alon Hanotea 44(1):53-56. Smock, R. 1979. Controlled atmosphere storage of fruits. Hort. Rev. 1:301-·336. Smock, R. M. 1967. Methods of storing bananas. Philippine Agr. 51:501-517. Soderstrom, E. L., and D. G. Brandl. 1983. Modified atmospheres for postharvest insect control in tree nuts and dried fruits. p. 487-497. Proc. 3rd. Int. Working Conf. StoredProduct Entomol., Kansas State Univ., Manhattan, Kansas, Oct. 23-28, 1983. Soderstrom, E. L., P. D. Gardner, J. L. Baritelli, K. N. de Loza, and D. G. Brandl. 1984. Economic cost evaluation of a generated low-oxygen atmosphere as an alternative fumigant in the bulk storage of raisins. J. Econ. Entomol. 77:457-461. Sonsrivichai, J., P. Anusadorm, C. Oogaqki, and H. Gemma. 1989. Storage life and quality of mango (Mangifera indica L. cv Keaw Sawoey) fruits stored in seal-packaging by plastic films and under low pressure at different temperatures. Japan J. Trop. Agr. 33(11):6-17. Sornsrivichai, S., S. Gomolmanee, D. Boonyakiat, ]. Uthaibutra, P. Boon-Long, and H. Gemma. 1992. Seal packaging by plastic film as a technique for limiting fungal decay of mangoes. Acta Hort. 296:23-32. Spalding, D. H. 1977a. Low pressure (hypobaric) storage of avocados, limes, and mangos. p. 156-164. In: D. H. Dewey (ed.), Controlled atmospheres for the storage and transport of perishable agricultural commodities. Hort. Rpt. 28, Michigan State Univ., East Lansing. Spalding, D. H. 1977b. Current recommendations of atmospheres for transport and storage of tropical fruits. p. 242-249. In: D. H. Dewey (ed.), Controlled atmospheres for the

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

181

storage and transport of perishable agricultural commodities. Hort. Rpt. 28, Michigan State Univ., East Lansing. Spalding, D. H., and F. J. Marousky. 1981. Injury to avocados by insufficient oxygen and excessive carbon dioxide. Proc. Fla. State Hort. Soc. 94:299-301. Spalding, D. H., and W. F. Reeder. 1972. Quality of "Booth 8" and "Lula" avocados stored in a controlled atmosphere. Proc. Fla. State Hort. Soc. 85:337-341. Spalding, D. H., and W. F. Reeder. 1974. Current status of controlled atmosphere storage of four tropical fruits. Proc. Fla. State Hort. Soc. 87:334-337. Spalding, S. H., and W. F. Reeder. 1975. Low oxygen, high carbon dioxide controlled atmosphere storage for control of anthracnose and chilling injury of avocados. Phytopathology 65:458-460. Spalding, D. H., and W. F. Reeder. 1976a. Low pressure (hypobaric) storage of avocados. HortScience 11 :491-492. Spalding, S. H., and W. F. Reeder. 1976b. Low pressure (hypobaric) storage of several fruits and vegetables. Proc. Fla. State Hort. Soc. 92:201. Spalding, S. H., and W. F. Reeder. 1977. Low pressure (hypobaric) storage of mangos. J. Am. Soc. Hort. Sci. 102:367-369. Sriyook, S., and J. Siriphanich. 1989. The use of surface coating to prolong the shelf life of Durian cv Chanee. Paper presented at the Workshop on the use of surface coatings for fruit and vegetables for export (in Thai). Institute of Scientific and Technological Research, Bangkok, Thailand. Staby, G. L. 1976. Hypobaric storage-an overview. Combined Proceedings of the Int. Plant Prop. Soc., 26:211-215. Stahl, A. L., and J. C. Cain. 1940. Storage and preservation of miscellaneous fruits and vegetables. Fla. AgI. Sta. Ann. Rpt. 1940, 88. Stead, D. E., and G. S. G. Chithambo. 1980. Studies on the storage of tropical fruits in polyethylene bags. Luso. J. Sci. Tech. (Malawi) 1:3-9. Suwanagul, A., and S. C. Tongdee. 1989. Effect of controlled atmosphere storage on internal ethylene content and ripening of durian. p. 46-54. Proc. Durian Workshop (in Thai), Thailand Institute of Scientific and Technological Research, Bangkok, Thailand. Sy, D. A., and D. B. Mendoza JI. 1984. Respiratory responses of 'Caraboa' mango to different levels of oxygen. Postharvest Res. Notes 1(1):3. (Postharvest Hort. Training and Res. Center, Dept. Hort., Univ. Philippines, Los Banos). Tan, S. c., P. F. Lam, and H. Abdullah. 1986. Changes of the pectic substances in the ripening of bananas (Musa sapientum, cv. Emas) after storage in polyethylene. ASEAN food J. 2:76-77. Thompson, A. K., G. F. Mason, and W. S. Halkon. 1971. Storage of West Indian seedling avocado fruits. J. Hort. Sci. 46:83-88. Thompson, B. D. 1955. The effect of pre-packaging and cold storage on the quality of fresh lychees. Fla. Lychee Growers Assoc. Yearb. 1:22. Tongdee, S. C, A. Chayasombat, and S. Neamprem. 1989. Effects of harvesting maturity on respiration, ethylene production, and the composition in the internal atmospheres of Durian (DurioZebethinusMurray) (in Thai). Proc. Durian Workshop, Thailand Institute of Scientific and Technological Research, Bangkok, Thailand, p. 31-36. Tongdee, S. C, and S. Neamprem. 1989. Effects of low oxygen atmospheres on ripening in Durian (Durio Zebethinus Murray) (in Thai). Proc. Durian Workshop, Thailand lnst. Sci. Technol. Res., Bangkok, Thailand. p. 37-45. Tongdee, S. C, and A. Suwanagul. 1988a. Effects of low oxygen atmospheres on ripening in durian (Durio zibethinus Murray). Seminar on Durian Proc., Thailand Inst. Sci. Techno!. Res., Bangkok, Thailand, p. 37-45.

182

E. YAHIA

Tongdee, S. C., and A. Suwanagul. 1988b. Effects of controlled atmosphere storage on internal ethylene content and ripening of durian fruits. Seminar on Durian Proceedings, Thailand Inst. Sci. Technol. Res., Bangkok, Thailand, p. 46-54. Tongdee, S. c., A. Suwanagul, and S. Neamprem. 1990a. Durian fruit ripening and the effect of variety, maturity stage at harvest, and atmospheric gases. Acta Hort. 269:323-324. Tongdee, S. c., A. Suwanagul, S. Neamprem, and U. Bunruengsri. 1990b. Effect of surface coatings on weight loss and internal atmosphere of durian (Durio zibethinus Murray) fruit. ASEAN Food J. 5:103-107. Truter, A. B., and G. J. Eksteen. 1987a. Controlled atmosphere storage of avocados and bananas in South Africa. Frigair'86 3(20):5. Truter, A. B., and G. J. Eksteen. 1987b. Controlled and modified atmospheres to extend the storage life of avocados. S. African Avocado Grower's Association Yearb. 10:151-152. Vakis, N., W. Grierson, and J. Soule. 1970. Chilling injury in tropical and subtropical fruits. III. The role of CO2 in suppressing chilling injury of grapefruit and avocados. Proc. Trop. Reg. Am. Soc. Hort. Sci. 14:89-100. Vilasachandran, T., S. A. Sargent, and F. Maul. 1997. Controlled atmosphere storage shows potential for maintaining postharvest quality of fresh litchi fruits. Proc. 7th Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press) Wang, C. Y. (ed.). 1990. Chilling injury of horticultural crops. CRC Press, Boca Raton, FL. Wardlaw, C. W. 1940. Preliminary observations on the refrigerated gas storage of 'Gros Michel' bananas. Trop. Agr. (Trinidad) 17:103-105. White, T. G. 1969. The oxytrol system-function, commercial use, and commodity research. Controlled atmospheres for the storage and transport of horticultural crops. Proc. Natl. CA Res. Conf., Michigan State Univ., East Lansing. Hort. Rept. 9:55-57. Wilson Wijertnam, R. S., M. Abeyesekere, and 1. G. N. Hewajulige. 1997. The response of two varieties of pineapples to CA storage and observations on calcium levels in the fruits. Proc. 7th Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press) Woodruff, R. E. 1969a. Overseas transport of bananas. p. 54. In: Controlled atmospheres for the storage and transport of horticultural crops. Proc. Nat!. CA Res. Conf., Mich. State Univ., East Lansing. Hort. Rept. 9:54. Woodruff, R. E. 1969b. Modified atmosphere storage of bananas. p. 80-94. In: Controlled atmospheres for the storage and transport of horticultural crops. Proc. Natl. CA Res. Conf., Mich. State Univ., East Lansing. Hort. Rept. 9:80-94. Woodruff, R. E. 1977. Use of carbon monoxide in modified atmospheres for fruits and vegetables in transit. p. 52-54. In: D. H. Dewey (ed.), Controlled atmospheres for the storage and transport of perishable agricultural commodities. Proc. 2nd Natl. CA Res. Conf., Dept. Hort., Mich. State Univ., East Lansing. Hort. Rpt. 28. Yahia, E. M. 1991. Respuestas de papaya (Carica papaya L.) a atm6sferas insecticidas. Proc. Interam. Soc. Trop. Hort. 35:84-100. Yahia, E. M. 1993a. Modified/controlled atmosphere storage in Mexico. p. 570-579. In: CA'93, Proceedings of the Sixth lnt. CA Res. Conf., Ithaca, NY, June 14-16, 1993. Yahia, E. M. 1993b. Responses of some tropical fruits to insecticidal atmospheres. Acta Hort. 343:371-376. Yahia, E. M. 1995. Postharvest handling of horticultural crops in Mexico. p. 1-10. In: A. Ait-Oubahou and M. EI-Otmani (eds.), Postharvest physiology, pathology and technologies for horticultural crops: recent advances. Institut Agronomique & Veterinaire Hassan II, Agadir, Morroco. Yahia, E. M. 1997. Avocado and guava fruits are sensitive to insecticidal atmospheres and/or heat. Proc. 7th lnt. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press) Yahia, E. M., and A. Carrillo-Lopez. 1993. Tolerance and responses of avocado fruit to

4. MODIFIED AND CONTROLLED ATMOSPHERES FOR TROPICAL FRUITS

183

insecticidal O 2 and CO 2 atmospheres. Food Sci. Technol. (Lebensm. Wiss. u-Technol.) 26:42-48. Yahia, E. M., and A. A. Kader. 1991. Physiological and biochemical responses of avocado fruits to O2 and CO 2 stress. Plant Physiol. 96 (Suppl.):96. (Abstr.) Yahia, E. M., F. Medina, and M. Rivera. 1989. The tolerance of mango and papaya to atmospheres containing very high levels of CO 2 and/or very low levels of O 2 as a possible insect control treatment. Proc. 5th Int. CA Res. Conf. (June 14-16, 1989), Wenatchee, WA, Vol. 2, p. 77-89. Yahia, E. M., D. Ortega, P. Santiago, and L. Lagunez. 1997. Responses of mango and maturity of Anastrepha ludens and A. obliqua to modified atmospheres at high temperature. Proc. 7th Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press) Yahia, E. M., and M. Rivera-Dominguez. 1992. Modified atmosphere packaging of musk melons. Food Sci. Technol. (Lebensm. Wiss. u-Technol.) 25:38-42. Yahia, E. M., and M. Rivera-Dominguez. 1995. Application of differential scanning calorimetry in the study of avocado and mango fruit responses to hypoxia. p. 206-209. In: A. Ait-Oubahou and M. EI-Otmani (eds.), Postharvest physiology, pathology and technologies for horticultural crops: recent advances. Institut Agronomique Veterinaire Hassan II, Agadir, Morocco. Yahia, E. M., M. Rivera, and O. Hernandez. 1992. Responses of papaya to short-term insecticidal oxygen atmospheres. J. Am. Soc. Hort. Sci. 117:96-99. Yahia, E. M., and M. Tiznado-Hernandez. 1993. Tolerance and responses of harvested mango to insecticidal oxygen atmospheres. HortScience 28:1031-1033. Yahia, E. M., and L. Vazquez-Moreno. 1993. Responses of mango to insecticidal oxygen and carbon dioxide atmospheres. Food Sci. Technol. (Lebensm. Wiss. u-Technol.) 26:42-48. Yahia, E. M., and R. Paull. 1997. The future for modified atmosphere (MA) and controlled atmosphere (CA) uses with tropical fruits. Chronica Horticulturae, December 1997. p. 18-19. Yantarasri, T., S. Ben-Yehoshua, V. Rodov, W. Kumpuan, J. Uthaibutra, and J. Sornsrivichal. 1995. Development of perforated modified atmosphere package for mango. Acta Hort. 398:81-91. YantarasrL T., J. Uthaibutra, J. Sornsrivichai, W. Kumpuan, V. Sardsud, and N. KanaThurn. 1994. Modified atmosphere packaging by perforated polymeric film and its effect on physical properties of mango fruit. p. 438-440. In: B. R. Champ, E. Highley, and G. I. Johnson (eds.), Postharvest handling of tropical fruits. Proc. Int. Conf., Chiang MaL Thailand, 19-23 July 1993. ACIAR Proc. 50. York, G. M. 1995. An evaluation of two experimental polysaccharide nature seal coatings in delaying the postharvest browning of the lychee pericarp. Proc. Florida State Hort. Soc. 107:350-351. Young, R. E., R. J. Romani, and J. B. Biale. 1962. Carbon dioxide effects of fruit respiration. II. Response of avocados, bananas, and lemons. Plant Physiol. 37:416-422. Zagory, D., and A. A. Kader. 1989. Modified atmospheres: An indexed reference list with emphasis on horticultural commodities, Suppl. 5 (June 1, 1985 to March 31, 1989). Postharvest Horticulture Series 6, Univ. California, Davis. Zagory, D., and A. A. Kader. 1993. Modified atmospheres. An indexed reference list with emphasis on horticultural commodities, Suppl. 6 (April 1, 1989 to April 3D, 1993). Postharvest Horticulture Series 7, Univ. California, Davis. Zhang, D., B. Y. Huang, and K. J. Scott. 1993. Some physiological and biochemical changes of "green ripe" bananas at relative high storage temperatures. Acta Hort. 343:81-85. Zhang, D., and P. C. Quantick. 1997. Preliminary study on effects of modified atmosphere packaging on postharvest storage of longan fruit. Proc. 7th Int. CA Res. Conf., Davis, Calif., 12-18 July, 1997. (In press)

5 Nitrogen Use in Vegetable Crops in Temperate Climates M. K. Schenk Institute of Plant Nutrition Department of Horticulture University of Hannover Herrenhauser StraBe 2 30149 Hannover Germany

I. Introduction II. Factors Influencing Fertilizer Needs A. Mechanisms of N Uptake 1. Nitrate 2. Ammonium 3. Field Conditions B. Nitrogen Demand 1. Inflow Rate 2. Growth Rate C. N Uptake from the Soil 1. Transport 2. Root System III. Determination of Fertilizer Requirement A. Soil Tests 1. Inorganic N Soil Content 2. Net Mineralization during Crop Growth 3. Timing of Soil Analysis 4. Limitations of the Soil Test B. Plant Tests 1. Sap Nitrate Test 2. Restrictions of Sap Nitrate Test 3. Critical Range 4. Rapid Tests

Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 185

M. SCHENK

186

IV. Nitrogen Management A. Fertilizer Application Techniques 1. Split Application 2. N Placement B. N Fertilizer Type 1. Nitrification Inhibitors and Slow Release Fertilizers 2. Chloride C. Crop Management 1. Irrigation 2. Organic Matter 3. Catch Crops V. Conclusion Literature Cited

List of Common and Botanical Plant Names

azalea broccoli brussels sprouts cabbage carrot cauliflower chicory cucumber kohlrabi leek lettuce maize oilseed radish potato radish rape spinach sugar beet tobacco tomato wheat

Rhododendron-simsii-hybrid Brassica oJeracea L. (Italica group) Brassica oJeracea L. (Gemmifera group) Brassica oJeracea L. (Capitata group) Daucus carota L. Brassica oJeracea L. (Botrytis group) Cichorium intybus L. Cucumis sativus L. Brassica oJeracea L. (Gongylodes group) Allium ampeloprasum L. var. porrum Lactuca sativa L. Zea mays L. Raphanus sativus L. var. oleiformis Solanum tuberosum L. Raphanus sativus L. var. sativus Brassica napus L. Spinacia oleracea L. Beta vulgaris L. Nicotiana tabacum L. Lycopersicon esculentum Mill. Triticum aestivum 1.

1. INTRODUCTION

The mineral nutrient N is needed in large amounts by plants because it is a constituent of macromolecules such as protein. However, only some plants living in association with Nz-fixing bacteria can use the

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

187

dinitrogen gas contained in the air. The majority of plants rely on ammonium and nitrate that originate from decomposition of organic material and are taken up from the soil. Thus the availability of N often limits plant growth. The breakthrough in the improvement of N nutrition and plant production was the invention of technical ammonia synthesis in 1913 by Haber and Bosch who were awarded the Nobel prize for chemistry in 1918. The main N forms contained in fertilizers are ammonium, nitrate, and urea. In horticulture, organic N forms releasing N slowly are also used (Maynard and Lorenz 1979). Organically bound N is transformed by soil microorganisms to ammonium, which is readily nitrified. Thus, plants mostly absorb N in the form of nitrate. The nitrate taken up is reduced by nitrate reductase and nitrite reductase to ammonia, which is fixed into glutamate to produce glutamine (Oaks 1992). The understanding of the structure and regulation of the related enzymes has been improved by molecular biological analysis of nitrate assimilation (Crawford 1995; Bachmann et al. 1996; Campbell 1996; Su et al. 1996). The glutamine provides the amino group for synthesis of amino acids, which are constituents of proteins. The nutrition of animals and man relies on protein synthesized by plants. Human beings need about 50 g protein per day (WHO 1990), which is equivalent to 8 g of N. Thus, the N amount cycling from the soil to the plants, to the animals, to humans, and finally back to the soil, which is necessary for adequate nutrition, increases with the population, which estimates predict will double during the next century (Todaro 1994). Feeding the population is a challenge to agriculture and horticulture. It requires the increased use of N fertilizers, whose use amounted to 76 megatonnes in the world in 1996. Fertilizer N consumption in the developed countries is down to 28 megatonnes/year from nearly 40 megatonnes late in the 1980s, which is mainly due to reduced N use in the former states of the Soviet Union. In developing countries, however, fertilizer N consumption doubled in the last 15 years, reaching 48 megatonnes/year (Wodsack 1997). The fertilizer N is the biggest source for increasing the amount of freely available N in the N cycle. Other factors are the increased cultivation of crops living in association with N2-fixing bacteria and the burning of fossil fuels (Mlot 1997). Increased use of N for plant production, besides its beneficial effects, creates serious problems. The anion nitrate, the N form mainly occurring in the soil, is not bound to the solid phase in the soil and it is very mobile in the soil solution. Thus it can be leached easily. Calculations reveal that in developed countries about 100 kg / ha annually are potentially exposed to the danger of leaching into the groundwater or lost via drainage, leading to eutrophication of rivers, lakes, and coastal areas

188

M. SCHENK

(Bach 1985; Power and Schepers 1989; Wendland et al. 1993). Further, nitrate losses are caused by denitrification. This microbial process is induced by oxygen deficiency in the soil, which is often due to precipitation or irrigation. In such situations, soil bacteria optionally use nitrate instead of oxygen as electron acceptors for respiration. The products of this process are N 2 • N 20, and NO. The proportion of these gases depends on soil and environmental factors. In addition, NH 3 volatilization may occur from ammonia or urea fertilizer application. NH 3 losses from senescing leaves of plant residues in the field are also reported. Gaseous losses from physiologically active and vital leaves are negligible (Schjorring et al. 1989; Glasener and Palm 1995). However, NH 3 losses from these sources are minor compared to those emerging from animal production sites and farmyard manure or slurry application (Sommer and Olesen 1991; Sommer et al. 1993). Nitrate level in the groundwater, which is used as a source of drinking water, must be low. The maximum allowable level is set in the range of 10 mg to 11.3 mg nitrate-N per liter in the United States and the European Community (EEC 1980; Power and Schepers 1989). Reports clearly indicate that land management has a considerable impact on the nitrate load of groundwater. Horticulture generally involves the risk of overusing N and leaching nitrate into the aquifers because fertilizer costs are minor compared to the economic value of products (1-2 % of production costs). High fertilizer input is considered a requirement for high yield and quality of the marketable product. However, not all commodities are involved. For example, fruit production only needs low N input, whereas vegetable production requires high N fertilization (Schrage 1990; Hochmuth 1992). However, fruit crops were not always produced in low N input systems. In the 1960s, annual fertilizer recommendations were as high as 200-400 kg N / ha and today it is only a tenth of that amount. One reason for this drastic change was the observation that N excess enhances the calcium deficiency of apples. In vegetable production, it is still a common practice to fertilize crops excessively with N in order to achieve high yield and quality, which often means green color. Growers fertilize twice as much as recommended by extension services (Schrage 1990; Hochmuth 1992). This results in annual residual nitrate amounts of up to 700 kg N I ha in the soil at the time of harvest of a crop (Schrage 1990). Nursery production is another sector of high N input. Up to 250 kg N/ ha was found in the soil profile at the end of the vegetation period, of which most was lost through leaching by the next spring (Alt et al. 1989; Dierend and Spethmann 1994a,b). The quality of the produce, however, is not necessarily beneficially

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

189

affected by high N application. One concern is that vegetables may contain large amounts of nitrate and therefore pose health hazards to consumers (Maynard et a1. 1976). Depending on the diet, up to 80% of nitrate intake is due to vegetable consumption (White 1975). Generally, leafy vegetables (but also radish and kohlrabi) may contain large concentrations of nitrate, whereas generative parts like curds of cauliflower or tomato fruits have less. The nitrate content is low during summer compared to other seasons with less radiation (Temperli et a1. 1978; Drews et a1. 1995). To protect the consumer, maximum levels allowable in the produce were imposed. The very first restrictions were for vegetables used for baby food. In the last few years, levels for vegetables were also set. To meet these levels, excess N fertilization must be omitted, especially during the time of the year when low light conditions exist. Other drawbacks of excess N supply are also reported. Cauliflower grown at high N levels is said to develop a bad odor during cooking, which also holds true for other brassica species, whereas the typical flavor constituents are diminished (Fischer 1992). Carrots grown at high N levels are less sweet and storage quality is poor (Bottcher et al. 1969). There are also indications that tipburn of lettuce is enhanced by high N supply (Brumm and Schenk 1993). Land management practices contribute to manmade NzO emissions globally. NzO is an important greenhouse gas in the troposphere leading to global warming, and it is involved in the depletion of ozone in the stratosphere (Graedel and Crutzen 1994). From ice core studies, it can be concluded that nitrous oxide concentrations increased from about 280 ppb v before the year 1700 to 310 ppb v today. The main increase was observed since the middle of the 20th century. The annual increase of 0.2 to 0.3% of NzO concentration represents an annual world increase of about 3 to 4.5 megatonnes NzO-N, which is about 50% of the natural background emission of 9.5 megatonnes NzO-N. The predominant sources of manmade increase of nitrous oxide emissions are cultivated soils and biomass burning. Furthermore, part of the NzO emissions from natural ecosystems such as from forests, rivers, and coastal areas may also be caused by agricultural activities. In total, about 0.5-2% of N fertilizer input is estimated as nitrous oxide losses to the atmosphere. The subject of nitrous oxide in the atmosphere and agriculture is discussed in detail by Bowman (1989), Graedel and Crutzen (1994), and Granli and B0ckmann (1994). NzO arises from both biological nitrification and denitrification. Denitrification is considered to be the more significant process (Poth and Focht 1985; Freitag et a1. 1987; Bock et a1. 1991; Williams et a1. 1992; Granli and B0ckmann 1994). The requirements for both processes are particularly present in horticultural production,

190

M. SCHENK

where plenty of ammonium, nitrate, and easily decomposable C-skeletons are available. Under these conditions, lack of oxygen in the soil after heavy rain or irrigation may induce considerable losses to the atmosphere (Ryden and Lund 1980; Schloemer 1991). In summary, N fertilization in horticulture has to consider not only farm economy but also the environment and human health. Appropriate procedures to integrate these objectives were developed during the last 20 years. A previous review is on the prediction of N fertilizer needs of arable crops (Greenwood 1986). Other reviews cover the utilization of controlled-release fertilizers (Maynard and Lorenz 1979), ammonium and nitrate nutrition (Barker and Mills 1983), as well as fertilization of ornamental greenhouse crops (Joiner et a1. 1983), fruit trees (Atkinson 1986), and blueberry and other calcifuges (Korcak 1988). This contribution will review the current state of methodology for applying proper N levels, focussing on vegetable crops grown under humid and subhumid climatic conditions of the temperate Northern hemisphere.

II. FACTORS INFLUENCING FERTILIZER NEEDS

A. Mechanisms of N Uptake Plants actively absorb not only ammonium and nitrate, but also amino acids (Schobert et a1. 1988; Jones and Darrah 1994), whereas urea uptake is not metabolically driven. The predominant N forms taken up from soil are nitrate and to a certain extent ammonium, depending on N fertilization and soil conditions. Normally ammonium will immediately be nitrified within a few days after application, except when soil temperature or pH is low or nitrification inhibitors are used. 1. Nitrate. Nitrate uptake is driven by transmembrane electrical potential differences created by proton pumps. There are indications that uptake occurs via cotransport of N0 3-/H+ as proposed by Ullrich and Novacky (1981). However the N0 3-/OH- (HC0 3-) antiport that was suggested by Thibaud and Grignon (1981) is still being discussed. There is evidence for three different nitrate uptake systems: a constitutive high affinity transport system (CHATS), an inducible high affinity transport system (lHATS) that is responsible for nitrate uptake at low concentrations (below 1 mM), and a constitutive low affinity transport system operating at concentrations higher than 1 mM nitrate (CLATS) (Behl et a1. 1988; Aslam et a1. 1992). The induction ofIHATS by providing nitrate to nitrate-starved plants and the decline after withdrawal of nitrate is

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

191

interpreted as de novo synthesis of nitrate transporters. Min Ni and Beevers (1994) reported that in maize roots three polypeptides in the tonoplast fraction and two polypeptides in the plasma membrane fraction were induced as integral proteins. The IHATS for nitrate is saturable, having low km in the range of 10-100 I..lM (Doddema and Telkamp 1979; Siddiqi et al. 1990; Glass et al. 1992; Aslam et al. 1992). In contrast, the CLATS is characterized by a first-order response to N0 3- concentration (Siddiqi et al. 1990; Glass et al. 1992). The second factor controlling the induction of nitrate transporters seems to be the cellular amino acid concentration. Padgett and Leonard (1993) showed that synthesis of nitrate transporters in a cell suspension culture of Zea mays was depressed by a mixture of aspartic acid, arginine, glutamine, and glycine. Only after depletion of amino acids in the cell-culture media was a pronounced induction observed. Similarly, it was found that some amino acids supplied to the root or to cotyledons of seedlings inhibited nitrate uptake (Muller and Touraine 1992). These findings support the idea that nitrogen assimilation products must be involved in the regulation of nitrate uptake, as was suggested by the experiments of Breteler and Siegerist (1984). The proposed mechanisms to control nitrate transport are similar to those suggested for regulation of sulfate uptake. Sulfate uptake of excised tobacco roots was also depressed by the end products of SOl- assimilation, S-containing amino acids (Herschbach and Rennenberg 1991). Furthermore, the point is being discussed that supply of organic acids to the root enhances nitrate uptake (Touraine et al. 1992). However, it has to be questioned whether this is a direct effect on nitrate uptake or the result of an improved supply of carbohydrates to root metabolism leading to higher nitrate uptake. In the last year, genes of HATS nitrate transporters have been identified for fungi and algae, but not for higher plants. However, it is suggested that higher plants may have similar genes because they are conserved between fungi and algae. In contrast, LATS nitrate transporters have been identified for higher plants (Crawford 1995). 2. Ammonium. Ammonium uptake is considered to depend on transmembrane electrical potential differences and uptake can be distinguished in a saturable HATS operating at low ammonium concentrations up to 1 mM and a first order kinetic LATS working between 1 and 40 mM (Wang et al. 1993,1994). 3. Field Conditions. The biological significance of LATS for nitrate and ammonium uptake in natural ecosystems is questionable since concentrations in soil solution are not likely to exceed 1 mM in the bulk soil and

192

M. SCHENK

will even be lower at the root surface (Barber 1984). This means that in field conditions saturable HATS is usually operating and nitrate and ammonium uptake depending on the concentration at the root surface can be described by Michaelis-Menten kinetics. Most reports on the uptake of intact plants are based on depletion studies in nutrient solution or on use of 15N, which do supply information on net uptake but not on total uptake. The latter can be determined by the use of 13N, an isotope of short half-life in short-time studies (Wieneke and Nebeling 1990). Thus, for situations when net uptake (inflow) is being considered, the term Imax has been suggested (Barber 1984). The HATS is defined by saturation at 1 mM NO a-. However, maximum nitrate inflow has been reported even at concentrations of 3 to 100 ~M (Olsen 1950; Edwards and Barber 1976a; Heins and Schenk 1987). The investigations revealed that the average inflow of nitrate in soil culture was of the same order of magnitude as the maximum inflow observed in nutrient-solution cultures (Heins and Schenk 1987). There are indications that kohlrabi must take up nitrate at the maximum rate to achieve highest yield, whereas spinach could compensate for low N supply by means of increased root hair surface (Steingrobe and Schenk 1991). The physiology of N uptake is reviewed by Clarkson (1986), Glass (1988), Clarkson and Hawkesford (1993), Imsande and Touraine (1994), and Crawford (1995). B. Nitrogen Demand 1. Inflow Rate. It is well established that the maximum inflow rate is

dependent on environmental and plant factors. Low root temperature decreases both nitrate and ammonium uptake but it seems that nitrate uptake is more sensitive to temperature (Frota and Tucker 1972; Clarkson and Warner 1979). Plants suffering from nitrate deficiency accelerate the inflow rate after restoring the supply. Root parts sufficiently supplied are able, by enhanced inflow rate, to compensate for roots suffering from N deficiency (Kuhlmann and Barraclough 1987). This reaction was also observed on older roots, indicating that decline of Imax with plant age is probably not caused by reduced capacity (Edwards and Barber 1976a; Pitman and Cram 1976) but by lower demand that has to be covered by a unit of root (White 1973; Edwards and Barber 1976b; Nye and Tinker 1977). The N demand is induced by the new growth and also reflects changes in the Nt content of the whole plant during ontogenesis. Thus, it could be shown that changes in maximum nitrate inflow rates were closely related to relative growth rates of wheat and butterhead lettuce (Rodgers and Barneix 1988; Steingrobe and Schenk 1993,

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

193

1994a). Also, for P uptake, a close correlation between relative growth rate and maximum inflow rate was observed (Wild and Breeze 1981). The maximum inflow rate is an average over the whole root system and variation along the root has not been considered. Nitrate and ammonium uptake rates are at their maximum at the first cm of root tips and drastically decline towards basal parts. However, the average inflow rate is reflected well by the uptake capacity of the root zone 2 cm behind the tip, because the contribution of root tips to total N uptake is low (Cruz et a1. 1995; G. Reidenbach pers. commun.). 2. Growth Rate. Increase in the dry matter of plants causes N demand, as was shown for butterhead lettuce (Kiisters 1996). However, the relationship between dry matter production and N uptake might not be linear if the Hcriticallevel" of N in plant dry matter changes during crop development or if retranslocation of N from older leaves to meristematic tissue occurs (Kiisters 1996). Regarding the signalling of N demand from the shoot to roots, the weight of opinion supports the hypothesis that circulation of amino acids via phloem and xylem is involved (Glass and Siddiqi 1984; Cooper and Clarkson 1989; Muller and Touraine 1992). In addition, Touraine et a1. (1992) also discuss the possibility that translocation of organic acids is related to regulation of nitrate uptake.

C. N Uptake from the Soil 1. Transport. Transport of nitrate and ammonium in the soil solution to plant roots occurs through mass flow and diffusion. N reaches the root surface mostly as nitrate since ammonium is easily nitrified under normal conditions. This explains why nitrate transport has been extensively investigated. The proportion of nitrate or ammonium reaching the root surface via mass flow increases with the concentration of the respective nutrient in the soil solution. For ammonium, mass flow is not significant since the concentration in the soil solution is low. For nitrate, the contribution of mass flow is more important than for ammonium because up to 50% of total N uptake may be from mass flow, as was shown for wheat (Strebel et a1. 1980). The contribution of mass flow is potentially large after fertilization when nitrate concentration in the soil solution is high, whereas toward the end of a culture course diffusion predominates. Hahndel and Wehrmann (1986a) calculated for spinach shortly before harvest a daily N uptake of 17 kg / ha, of which 4 kg were attributed to mass flow and 13 kg to diffusion.

194

M. SCHENK

Diffusion is driven by the concentration gradient between bulk soil and root surface (Barber 1984). The nitrate concentration in the bulk soil solution necessary to meet the uptake rate of roots was calculated for an optimally supplied spinach crop as low as 2 mM (Heins and Schenk 1987) or less (Burns 1980). This finding is in contrast to the observation that the actual nitrate concentration in soil solution of an optimally supplied spinach crop was about four times higher (Heins and Schenk 1987). Similar results were obtained for other crops (Robinson et al. 1991; Wiesler and Horst 1994). It was speculated that this depended on a non-homogeneous distribution of roots and nitrate in the soil, an incomplete root-soil contact, or non-uniform uptake capacity along roots (Heins and Schenk 1987; Robinson et al. 1991; Noordwijk et al. 1993; Wiesler and Horst 1994). However, the non-uniform uptake capacity along roots seems less relevant, although the uptake capacity changes along roots, but the average uptake rate, which was used for the cited calculations, reflected fairly well the uptake capacity of the root proportion mostly contributing to uptake (Cruz et al. 1995; G. Reidenbach, pers. commun.). 2. Root System. Root length densities of vegetable crops in the plough layer, 0-30 cm, lie mostly in the range of 2-4 cm / cm 3 soil (Heins and Schenk 1987; Jackson and Bloom 1990; Schenk et al. 1991; S0rensen 1993; Steingrobe and Schenk 1994b; Smit et al. 1996), which is low compared to cereals having more than 10 cm / cm 3 soil (De Willigen and Noordwijk 1987; Barraclough et al. 1989). From this a half-distance of 3-4 mm between vegetable roots can be calculated assuming homogeneous distribution. Nitrate ions are quite mobile in the soil solution and may travel about 6 mm per day at an effective diffusion coefficient of De = 10-6 cm 2 . sec- 1 (Barber 1984). This is twice the half-distance between roots and means that competition between roots for nitrate ions easily occurs. Therefore, roots should be able to exhaust soil nitrate nearly completely. But, it was shown for spinach, kohlrabi, and lettuce that crops were unable to deplete soil solution concentration below about 1.5 mM nitrate (Heins and Schenk 1987; Schenk et al. 1991; Brumm and Schenk 1993). This suggests that the whole root length does not contribute uniformly to N uptake because of inhomogenity of root and nitrate distribution as well as root-soil contact. Robinson et al. (1991) calculated for wheat that just 3.5 to 11 % of the whole root length was effective in nitrate absorption. This is in agreement with Burns (1980), who speculated that 10% of the root system would be enough to satisfy the nitrate demand of cereals, whereas vegetable crops would need 22-44% of their root system. Nevertheless, it could be shown for

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

195

maize that nitrate depletion in deeper soil layers was enhanced by an increase in root length density (Wiesler and Horst 1994). Similarly, we observed for cauliflower genotypes the tendency for an increase in root length density from 0.2 to 1.5 em / cm 3 soil in the lower 45-60 em layer to result in a decrease in residual nitrate from 30 to 10 kg / ha in this layer. Although these results suggest that root length density might be effective with regard to N exhaustion, if root length density level is low, it has to be kept in mind that the amount of N involved is small compared to the N absorption of a crop. Another fact is that the inhomogenous distribution of both roots and nitrate in the soil does not allow complete exhaustion of nitrate even during suboptimal N supply. The residual nitrate in the soil after butterhead lettuce was not significantly lower compared to the optimum (Brumm and Schenk 1993). The effective root depth is an important factor in the characterization of crop root systems. Vegetable crops generally have shallow root systems, which is reflected in a low dry matter production per ha (Burns 1980; Heins and Schenk 1987; S0rensen 1993). Long-lasting brassicas such as cabbage, brussels sprouts, and cauliflower have deeper root systems than lettuce crops or spinach (Smit et a1. 1996). Nursery plants are very diverse, depending on species, age, and management practice. Rooting depth of spinach and kohlrabi was not increased during N deficiency, even if the deeper soil layers contained large amounts of nitrate (Schenk et a1. 1991). This is in contrast to observations of winter wheat (Barraclough et a1. 1989). It was suggested that winter wheat can adapt to low N supply by rooting more deeply because of a longer growing period compared to that of the vegetable crops (Schenk et a1. 1991).

Another mechanism of adaptation is an increase in the root: shoot ratio in cases of N deficiency. This is often due to a decrease in shoot matter, whereas root growth is less reduced. However, for spinach it was shown that total root length also significantly increased (Heins and Schenk 1987). A further adaptation mechanism is an increased length of root hairs during N deficiency. Again, this mechanism seems to be species specific, since it was observed for spinach and rape but not for tomato and kohlrabi (Foehse and Jungk 1983; Steingrobe and Schenk 1991). It is speculated that both increased length of roots and root hairs may help to meet shoot demand by extensive exploration of nitrate-rich soil zones if parts of the root system are insufficiently supplied with nitrate. Under these conditions it was shown that branching of roots is stimulated at nitrate supply sites (Drew 1975). This morphological reaction could be related to an increased inflow of assimilates from the shoot and a simultaneously enhanced auxin flow (Sattelmacher and Thoms 1995).

196

M. SCHENK

III. DETERMINATION OF FERTILIZER REQUIREMENT Horticultural soils contain large amounts of organically bound N, whereas the proportion associated with the mineral fraction is comparatively low. The organic N becomes available to the plant by ammonification and nitrification. The N supply from the soil resulting from mineralization and desorption from soil minerals has to be supplemented by fertilizer N to meet the demand of the crop. Therefore, the N supply from the soil has to be estimated for accurate fertilization. A. Soil Tests 1. Inorganic N Soil Content. Studies of King and Whitson (1901,1902), Soper and Huang (1963), Giles et al. (1973) and Carter et al. (1974) suggested that the quantity of inorganic N (nitrate and ammonium) in the rootable soil layer becomes available to the crop and can be used for forecasting fertilizer needs. This approach was adapted by others for the development of fertilizer recommendation systems. For maize, a pre-sidedress N0 3 test (PSNT) was developed, by which the nitrate concentration in the 0-30 cm layer is determined just prior to high N demand of the crop (Magdoff et al. 1984). The PSNT proved to be quite accurate in identifying situations if the soil supplies sufficient N but it offered only little help in making fertilizer rate predictions (Heckman et al. 1995). However, studies of Wehrmann and Scharpf (1979) and Ris et al. (1981) demonstrated that consideration of inorganic N content in the whole soil depth effectively rooted by the specific crop allows reliable fertilizer recommendations at planting. In contrast to other soil tests the inorganic N content is not expressed as a concentration but as a quantity in kg N/ha. Depending on the precrop, use of slurry, organic manure, soil type, and rainfall, the N quantity considerably differed from about 20 to 340 kg N / ha in 0-90 cm depth in spring before planting the next crop (Jungk and Wehrmann 1978). Generally inorganic N content of the soil is higher after sugar beet, rape, and vegetables and lower after cereals. Application of slurry or manure also results in higher inorganic N quantity (Kuhlmann et al. 1989). Soils having a high water holding capacity store more inorganic N. High rainfall leaches nitrate out of the soil, resulting in low inorganic N levels (Strebel et al. 1989). Under subhumid conditions in Northern Europe, the inorganic N quantity in the 0-30 cm layer is generally lower than in the layers 30-60 cm and 60-90 cm in spring due to leaching in winter (Jungk and

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

197

Wehrmann 1978). Thus, analysis of the surface layer would not be sufficient if plants have an effective rooting depth exceeding this layer. Cereals, sugar beet, maize, long-lasting vegetable crops such as cabbage and brussels sprouts, and a number of nursery plants have the potential to explore the soil to a depth of 90 cm (De Willigen and Noordwijk 1987; Barraclough et al. 1989; Wiesler and Horst 1994; Smit et al. 1996). Potato and leek are able to exhaust N down to about 60 cm (Vos and Groenwold 1986; Smit et al. 1996). A large number of vegetable crops having a short culture course only use the upper 0-30 cm layer. Examples are butterhead lettuce, kohlrabi, and spinach (Heins and Schenk 1987; Schenk et al. 1991; Sorensen 1993). However, rooting depth depends on site conditions. Generally, it can be stated that effective rooting depth decreases during unfavorable climatic and soil conditions (Mohr 1978,1980; Barber 1984). For reliable fertilizer recommendations, the effective rooting depth has to be considered for soil analysis.

N Form in the Soil. The inorganic N content in the soil mainly consists of nitrate. Only under specific conditions, after slurry application or impaired nitrification because of low temperature or low pH, may soils contain considerable quantities of ammonium (Jungk and Wehrmann 1978; Wehrmann and Scharpf 1979; Ris et al. 1981). There was some controversy about the contribution of non-exchangeable ammonium to nutrition of crops. However, plants are unable to use the native nonexchangeable ammonium of clay minerals but only the recently fixed ammonium (Col dewey zum Eschenhoff 1985; Wehrmann and Coldewey zum Eschenhoff 1986). The authors suggest that considerable fixation of ammonium will not occur under most conditions. Therefore, extraction procedures for plant available inorganic N have to include nitrate and the exchangeable ammonium, which is achieved by use of 1 M KCl, for example. Soil Sampling. Soil has to be sampled according to the effective rooting depth of the specific crop. It is suggested that 16-20 cores per site be taken to get a valid mean value because variability of inorganic N in the soil can be considerable (Scharpf 1977; Dahnke and Johnson 1990). ThIS takes place especially after incorporation of harvest residues, as is usual in vegetable production (Schrage 1990). Soil samples have to be kept cool until analysis in the laboratory in order to avoid additional mineralization, which would be an artifact (Scharpf 1977). Mostly, the fresh soil is analysed because fertilizer recommendations have to be supplied immediately within some days.

198

M. SCHENK

However, it is also possible to dry the soil quickly within 24 h at moderate temperatures (60°C) without influencing the inorganic N content (Dahnke and Johnson 1990).

Optimum N Fertilizer Level. The pre-sidedress N0 3- test, as developed for maize and sweet maize, allows a decision as to whether N dressing is necessary or not (Magdoff et al. 1984; Heckmann et al. 1995). The critical value is in the range of 20-30 mg inorganic N / kg soil. Like other soil tests characterizing nutrient availability as a concentration, calibration in field trials is necessary to establish the relationship between soil test value and optimum N fertilization (Schenk et al. 1989). The approach to express soil inorganic N as a quantity in kg N / ha is based on the observation that crops are able to deplete inorganic N in the rootable soil layer during the culture course and fertilizer trials showed that soil inorganic N affects plants like fertilizer N (Scharpf 1977). A target level for optimum N supply in kg N / ha to reach the desired yield goal could be defined as the sum of both soil inorganic N and fertilizer N. Thus, the recommended fertilizer rate is obtained by deduction of soil inorganic N from the target level for optimum N supply (Dahnke and Johnson 1990). Today the important parameters, effective rooting depth and target level for optimum N supply, are available for a large number of arable and vegetable crops grown in countries of Northern Europe (Scharpf 1977; Schenk et al. 1991; Brumm and Schenk 1993; S~nensen 1993; Smit et al. 1996). However, it has to be kept in mind that the target level for optimum N supply depends on the respective yield goal (Dahnke and Johnson 1990; Schenk et al. 1991), which might vary considerably. This is particularly significant for nurseries because of the different age levels of crops and the ecological conditions ofthe'production site affecting the growth rate (Alt et al. 1995; Dierend and Spethmann 1996). As a rule of thumb it can be said that lOt of fresh matter of vegetables contain 30 kg Nand 10 t of fresh matter of new growth of nursery crops contain 60 kg N (Obermayr and Alt 1992; Alt et al. 1995). 2. Net Mineralization during Crop Growth. The soil inorganic N analysis at planting or at a later stage of crop development is not suitable to predict net mineralization during the culture course. However, both the critical values of the pre-sidedress N0 3- test (Magdoff et al. 1984) and the target levels for optimum N supply (Scharpf 1977; Jungk and Wehrmann 1978; Wehrmann and Scharpf 1979) are determined in field experiments where net mineralization occurs. Thus, these parameters consider a net mineralization occurring on average in the field because

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

199

they were determined as the mean of several field experiments on different sites. However, net mineralization may vary considerably between sites. Fields with high application rates of slurry and organic manure have a higher mineralization potential. The same holds true for sites with extensive vegetable production and recycling of harvest residues (Schrage 1990; Engels 1993). In addition to the quantity of easily decomposable organic matter, the soil conditions affect microbial activity. Low soil temperature and water content reduce net mineralization. Several chemical and biological methods were proposed for the estimation of potentially mineralizable N. The biological methods, aerobic or anaerobic incubation, deliver a reliable estimation of net mineralization under controlled conditions but fail in the field (Keeney 1982; Stanford 1982; Kohler 1983). Furthermore, they are less suitable for routine analysis in soil test labs. From this point of view chemical methods are more convenient and several of them, including electro-ultrafiltration, were investigated (Keeney 1982; Nemeth et al. 1979; Smith and Shengxiu Li 1993). Additionally, methods for fractionation of organic N in crop residues were developed to characterize the proportion that is readily available for microbial decomposition (Vanlauwe et al. 1994; De Neve et al. 1994). Fox et al. (1993) proposed near-infrared reflectance spectroscopy for assessment of net mineralization and suggested a physical fractionation according to the density of organic matter. For some of these N availability indices it was shown that taken for themselves they only have minor capacity to predict N net mineralization in the field (Kohler 1983; Kuhlmann et al. 1986; Schrage 1990), as was stated for the biological methods. In horticultural field production, soil temperature is the most determining factor of net mineralization of the potentially available organic N because crops will generally be irrigated. Posterior calculations considering temperature revealed a high correlation to net mineralization in the field (Richter et al. 1980; Honeycutt et al. 1991; Kiisters 1996). An increase of mean air temperature from 10 to 20°C measured at 1m above the soil enhanced the daily net mineralization rate four-fold from 0.2 to 1.1 kg N / ha. For a lettuce crop, this difference adds up to about 40 kg N / ha, which is nearly half of the N demand (Kiisters 1996). Net mineralization at optimum N supply not only depends on site characteristics but also on the specific crop. For cereals at optimum N supply, virtually no net mineralization occurred, whereas for sugar beet considerable amounts were supplied from soil organic matter (Engels and Kuhlmann 1993). For vegetable crops, net mineralization was also observed (Heins and Schenk 1987; Schenk et al. 1991; Kiisters 1996). The

200

M. SCHENK

results of Engels and Kuhlmann (1993) indicated a decline in net mineralization in cropped fields with increased N fertilization. It could be shown that this was probably due to immobilization by microorganisms feeding on carbohydrates excreted from the root into the soil (Blankenau et al. 1996). This underlines the fact that the calculation of the target level for optimum N supply from the amount contained in the crop at the respective yield goal (Dahnke and Johnson 1990), assuming an average net mineralization, is a first approach that has to be validated in field experiments. The organic matter content of horticultural soils is generally higher than in arable soils because large amounts of crop residues in vegetable production and organic manure in nurseries are incorporated. Thus, net mineralization rate in horticultural soils is comparatively high. Additionally, N becomes available from decomposition of fresh crop residues having a favorable C/N-ratio for net mineralization. It was shown for several vegetable residues that about 100% of organic N may become available within 6-10 weeks after incorporation in the soil (Scharpf and Schrage 1988). If crops are planted in the mulch of harvested residues or green manure, the mineralization rate is about half of that after incorporation in the soil (Schrage 1990). The amount of inorganic N resulting from decomposition of crop roots is low compared to that coming from mineralization of crop shoot material, because generally the amount of N contained in roots may be estimated to be up to 10% of that contained in the shoot. The N quantity in harvest residues varies considerably between species. Lettuce crops have only 20-30 kg N I ha in harvest residues, whereas brassicas leave up to 150 kg N behind (Schrage 1990). Chemical extraction procedures failed to characterize mineralizable N on sites where easily decomposable residues of precrops were incorporated (Schrage 1990; McTaggart and Smith 1993). Schrage (1990) developed a calculation table to estimate net mineralization from harvest residues. In nurseries it is common practice to use farmyard manure for soil preparation. According to a survey of German nurseries by Alt et al. (1989), 90-200 kg N I ha are applied annually with farmyard manure, which will become available through net mineralization at equilibrium conditions in addition to mineralization of soil organic matter. These large amounts resulting from mineralization of harvest residues and farmyard manure have to be taken into account for the calculation of N fertilizer rate. Schrage (1990) suggested considering the estimated net mineralization as available to the crop such as soil inorganic N. This means that the fertilizer rate calculated by deduction of soil N supply from the target level for optimum N supply is accordingly lower.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

201

3. Timing of Soil Analysis. Generally, soil tests are done prior to planting. This is also applicable to the soil nitrate test, as shown for a scale of arable and horticultural crops (Scharpf 1977; Bohmer 1980; Ris et al. 1981). However, net mineralization after soil sampling may be considerable, especially if harvest residues or organic manure were incorporated. This uncertainty can be reduced by delaying soil sampling until the beginning of the linear growth phase, when highest N demand ofthe crop starts. Also the influence of temperature on net mineralization is taken into account for the time elapsed. Another aspect is that leaching of nitrate to the unrooted soil depth during the early growth phase is considered. This is particularly significant for shallow rooting crops, on soils with low water-holding capacity and in regions of high rainfall. Thus, fertilizer recommendation systems based on an in-culture course soil test were developed for vegetables and arable crops (Magdoff et al. 1984; Lorenz et al. 1986; Ministerie van Landbouw en Visserij 1989). In this system, a low N fertilizer rate at planting guarantees optimum N supply until sidedressing after the in-culture course soil test. This timing of the soil test will also be useful in nurseries because significant N uptake does not occur during bud burst but later, when dry matter production is high (Brumm and Schenk 1992; Dierend and Spethmann 1994c). The N necessary for the early growth of woody species is derived from storage pools in wooden parts of the plant (Kramer and Koslowski 1979). 4. Limitations of the Soil Test. The soil test on inorganic N in the soil

allows a good forecast of N fertilizer needs on average conditions. However, strongly divergent gains or losses after soil sampling may have an impact on its quality, which is particularly important in horticulture. Various kinds of information on factors influencing net mineralization (temperature, quantity of harvest residues, for example) and nitrate transport in the soil (water-holding capacity of the soil, rainfall and irrigation, for example) as well as production goal have to be considered to determine the fertilizer rate. This requires broad knowledge. Computerbased decision support systems were developed for application in practice (Fink and Scharpf 1993; Alt and Rimmek 1994; Rahn et al. 1994; Alt 1996). Computerization additionally allows weather conditions to be taken into account during the specific culture course. Another restriction in the application of a soil test is the high labor input for taking soil samples down to 90 em depth if this is required by the crop. The precondition is that the soil allow auger sampling below the plow layer. In addition, efficient laboratory facilities are required for rapid processing of soil samples because the time span between soil sampling and fertilization is short during the growing season. To overcome

202

M. SCHENK

the latter problem, a rapid nitrate test based on Merckoquant strips read by a reflectometer is available (Jemison and Fox 1988). Handling requires some routine and well-trained staff. However, the main problem of taking soil samples remains. The inorganic N content in soils can be described by simulation models that are quite complex and need a range of input data (De Willigen and Neeteson 1985; Addiscott and Whitmore 1987; Gysi 1990a,b; Kersebaum and Richter 1991; Riihlmann and Geyer 1993). Adaptation of simulation models to the smaller set of data regularly available for the farmer~s field resulted in considerable deviations of predictions from measured values (Otter-Nacke and Kuhlmann 1991). In Germany (Bavaria) an extensive network including weather stations was installed to improve N fertilizer recommendations of the extension service by means of simulation models. The program is not yet finished, but it seems that simulation models need too much input data for reliable simulation-data that are not available under standard situations on farms. B. Plant Tests

The increase in N availability in the soil is reflected in the N content of plants and in yield level. The quantitative knowledge of the relationship between N content of plants and yield can be used to determine the necessity to fertilize. However, plant analysis is a diagnostic tool to evaluate the actual nutritional status of plants but does not supply information on the rate to be applied because of the following reasons. First, N content of plants reflects the inorganic N availability in the soil depth that the plant has reached at the time of analysis. However, crops will not have penetrated the soil down to the potential effective rooting depth at the beginning of linear growth phase when sidedressing has to be done to meet the increasing demand of crops. Thus, the plant N content cannot reflect the inorganic N in deeper soil layers that becomes available to the crop in the culture course. Second, the relationship between available inorganic Nand N content in plants can be described by a saturation function. Hence, it is not possible to estimate at saturation the quantity of available inorganic N in soil from N content in plants. Therefore, attempts to estimate quantitative N fertilizer need from the N content of young plants were not successful (Scaife and Turner 1987). 1. Sap Nitrate. It has been shown for cereals that stem sap nitrate analy-

sis is helpful for the characterization of actual N flow from soil to plants during later stages of crop development when roots explore the effective rooting depth (Wehrmann et a1. 1982; Wollring and Wehrmann 1990).

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

203

Under these conditions, plant analysis has the potential to estimate inorganic N availability for short forecast periods. N nutritional status is better reflected in nitrate content than in total N content (Olsen and Lyons 1994). For analysis, generally plant sap is taken from petioles or stems because nitrate is stored in parenchyma cells of the xylem. Furthermore, nitrate content is less dependent on actual radiation compared to leaf lamina. Investigations on potato, butterhead lettuce, and winter wheat showed a diurnal variation of nitrate content (Jakob et a1. 1986; Schrage 1990; McKerron et a1. 1995), whereas this was not observed with cucumber (Schacht and Schenk 1994). In addition to the time of day, the plant part has to be standardized. McKerron et a1. (1995) reported a three-fold increase of sap nitrate concentration from the younger to the older leaves of potato and similar effects were also observed for cucumber (Schacht and Schenk 1994). The reason might be that nitrate assimilation in older leaves is reduced because less amino acids are required in the fully expanded leaves or activity of nitrate reductase is limited due to reduced radiation reaching the lower leaves. Generally it can be stated that sampling should be done early in the morning when nitrate content of sap is little affected by actual radiation and the potential is high to reflect nitrate availability most sensitively. Petioles of fully expanded young leaves are usually taken (Coltman 1987; Gardner and Roth 1990; Westcott et a1. 1991; Hartz et a1. 1993; Lewis and Love 1994; Olsen and Lyons 1994; Schacht and Schenk 1994; McKerron et a1. 1995; Pritchard et al. 1995). 2. Restrictions of Sap Nitrate Test. Nitrate taken up by plants is re-

duced to nitrite by nitrate reductase in the cytoplasm. Nitrite is translocated to the chloroplast in leaves or the plastid in the roots where it is reduced to ammonia. The ammonia originating from nitrate reduction or from ammonium uptake is introduced into the amino acid metabolism via fixation of NH 3 to glutamate forming glutamine (Oaks 1992). In most plants nitrate as such is transported via the xylem to the leaves of the plant, where nitrate reduction occurs. However, some species such as legumes, begonia-elatior hybrids, and woody species have a high potential to reduce nitrate in the roots (Andrews 1986; Schenk 1988; Oaks 1992). Ammonium coming from nitrate reduction in the roots or taken up is assimilated in the roots and translocated to the shoot in the form of amino acids, amides, and ureides. For plants reducing nitrate already in roots, the nitrate sap test is less applicable because of low concentrations in petiole sap (Schenk 1988). In these cases the amino-acid test as proposed by Schulz and Marschner (1987) might be superior, as was shown for azaleas (Bettin and Schenk 1988). However, this test was unsuitable for cucumber after the onset of fruiting because concentrations in petiole

204

M. SCHENK

sap drastically declined (Schacht and Schenk 1994), since cucumber fruits are a strong sink for amino acids (Schapendonk and Challa 1980). The N form of fertilization probably has to be considered only if transformation of urea and ammonium is impaired, because it was shown that, even with continuous fertilization of pot plants, nitrate concentration of petiole sap was unaffected by variation of N0 3- /NH 4 + ratio (Schenk 1988). However, low temperature may restrict the reliability of the nitrate test, because it was observed that nitrate concentration decreases although the soil contained sufficient nitrate (Schrage 1990). This can be explained by temperature sensitivity of the nitrate uptake mechanism (Frota and Tucker 1972; Clarkson and Warner 1979). Also, nitrification inhibitors which are used to increase N efficiency by blocking the transformation of ammonia to the mobile nitrate ion (see Section IV B 1) may restrict the applicability of the sap nitrate test. Finally, it has to be mentioned that Maier et al. (1994) observed a negative correlation between nitrate and chloride concentration in the petiole sap of potato. This corresponds to other reports indicating that chloride supply decreases nitrate content of plants (Kafkafi et al. 1982 for tomato; Hahndel and Wehrmann 1986b for spinach and butterhead lettuce) and might be significant for interpretation of sap nitrate tests if higher quantities of chloride are supplied via irrigation water or fertilization. 3. Critical Range. A general problem of using the nitrate sap test is the availability of valid critical levels or critical ranges. The latter might be more convenient since variability of sap nitrate is quite high. Critical ranges are available for a scale of vegetables (Hochmuth 1994). Numerous papers report a decline in the critical level during the culture course. It is questionable whether this reflects changes of physiological needs during ontogenesis or reduced nitrate availability in the soil, since fertilizer was applied once at planting or split in rates. The work of McKerron et al. (1993) on potato suggests that nitrate concentration of optimum treatment does not change much during crop development if the very earliest stage is not considered. This was also observed in greenhouse-grown cucumber (Schacht and Schenk 1994). The conclusion would be that a single level of petiole sap nitrate could be used during the culture course of a crop, as proposed by Westermann and Kleinkopf (1985) for potato. McKerron et al. (1995) raise the question of whether the nitrate sap test has the potential to optimize N application. This has to be affirmed since it was shown for winter wheat in the field (Wollring and Wehrmann 1990), for tomato and cucumber in the greenhouse (Coltman 1988; Schacht and Schenk 1994), and for pot plants (Schenk 1988) that plant sap nitrate concentration was suitable to control fertil-

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

205

ization. However, it has to be emphasized that this applies to cases where plant roots explored the complete potentially rootable soil layer. 4. Rapid Tests. The N-status of plants can be rapidly evaluated by semiquantitative determination of nitrate in plant press sap. For nitrate concentrations up to 3000 mg / liter, the diphenylamine-method proved to be useful, as shown for winter wheat (Wollring and Wehrmann 1990). For higher nitrate concentrations as they occur in vegetable crops, it was suggested that the rapidity of coloration of Merckoquant test strips be measured after application of undiluted plant sap. The reproducibility is unsatisfactory. Much better results are obtained after dilution of plant sap and measurement by means of a hand-held reflectometer. Another possibility is the measurement ofN0 3- in fresh petiole sap by a portable, battery-operated nitrate selective electrode (Hartz et a1. 1993). The rapid nitrate tests described are comparatively simple but still some manipulations are necessary that are time consuming and need continuous practice for proper application. This problem could be overcome by using a chlorophyllmeter (SPAD-502 from Minolta) that is portable and can be operated in the field. The method is based on the fact that chlorophyll content reflects the N status of plants (Takebe et a1. 1990). It was shown that chlorophyll measurements indicate the N nutritional status of arable crops, including potato (Wood et a1. 1992; Minotti et a1. 1994). A definition of critical values has to consider the specific coloration of the cultivar. Respective data are available for N fertilizer recommendations in cereals in Germany (J. Wollring, pers. commun.). Such calibration work cannot be realistically done for a large number of species and cultivars such as are grown in horticultural production. However, a N deficiency strip receiving (depending on daily crop uptake) 20 to 50 kg N / ha less at the first application could serve as an internal reference. The decline of chlorophyll readings in the deficient reference strip compared to the well-fertilized field will indicate the beginning of a shortage of N in the soil before growth of the crop is affected and sidedressing can be done in time. This method, called fertilizer window, would also consider other environmental factors potentially influencing chlorophyll readings-for example, radiation, water supply, and availability of other nutrients.

IV. NITROGEN MANAGEMENT To characterize the efficiency of fertilizer application, recovery of 15N labelled fertilizer is often measured. This approach, however, has the

206

M. SCHENK

disadvantage that mineralization-immobilisation turnover is not considered. 15N will be incorporated into the soil organic N pool and diluted, resulting in an underestimation of subsequent mineralization. Thus, recovery measured by the 15N method is generally lower than by the difference method (Harmsen and Moraghan 1988). The apparent recovery fraction (ARF) according to the difference method is calculated from: ARF = NP-NPo x 100

NF

where NP o is the amount of N taken up by an unfertilized crop and NP is the amount of N taken up by a fertilized crop. NF stands for the fertilizer rate. The precondition for this approach is that net mineralization be independent of N fertilization which, however, is doubtful, as discussed in Section III A. In order to achieve a high apparent recovery fraction, the applied fertilizer has to be kept available for the crop. Thus, losses due to volatilization or leaching have to be minimized and the application technique must ensure that N can be reached by the crop. A. Fertilizer Application Techniques 1. Split Application. N fertilizer applied in large amounts prior to planting or early during crop growth is exposed to the risk of leaching or denitrification. This risk can be reduced by splitting up N fertilization into small portions. In addition, top dressing rates can be adapted to actual N supply from mineralization of organic matter. Such a recommendation system based on measurement of soil inorganic N was developed and is practiced in a vegetable growing region of Germany (Lorenz et a1. 1989). The use of granulated N fertilizers for top dressing may be restricted to early growth stages depending on the crop. The injection of N fertilizer in the irrigation water, however, allows top dressing during the entire growth cycle. This technique, which is known as fertigation, allows precise timing of nitrogen in very short time intervals (weeks, days, or even shorter) according to the demand of the crop. For proper management of fertilization, N uptake during crop development has to be known. Such N uptake data are available for a range of crops (Ministerie van Landbouw and Visserej 1989; Hochmuth 1992). They may depend on climatic conditions and yield level of the specific site. Modeling growth and N uptake of butterhead lettuce revealed that the N amount contained in the fresh matter increases with dry matter content, which follows an optimum-shaped

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

207

curve during the year. Crops growing in spring and autumn take up about 20% less N (Schenk 1996). Fertigation also requires a monitoring of soil inorganic N in order to adjust fertilizer rates to net mineralization and crop N uptake at the specific site. However, in drip irrigation systems, which often are used for fertigation, soil testing has to be adapted because N is supplied punctually and only a portion ofthe whole soil volume stores the N for plant uptake. The N amount may be small since it is replenished in short intervals. In such situations, characterization of available inorganic N as a quantity in the rootable soil layer is of limited use. It might be more appropriate to characterize N availability as inorganic N concentration in the soil or soil solution (Hartz and Hochmuth 1996). N0 3 -N concentrations> 75 mg / L indicate sufficient availability (Hartz and Hochmuth 1996) and the lower boundary is about 20 mg / L since plants are unable to deplete the soil solution further (Section 2 C 2). There is evidence that concentrations below 75 mg N0 3 -N / L may be sufficient to meet N demand of the crop (Hartz and Hochmuth 1996; Kiisters 1996). To avoid overfertilization, inorganic soil N concentration has to be monitored, since inorganic N accumulation exceeding the optimum is not reflected in the sap nitrate test (Section III B). But petiole N0 3 concentration is a reliable indicator of plant N status (Hochmuth 1994; Hartz and Hochmuth 1996), especially in fertigation systems where even low nitrate concentrations in the soil solution are sufficient to supply plants because of continuous supply ofN via fertigation. In such situations, soil N test might be unsuitable for the characterization of N supply from the soil to plants (Schenk 1988). However, instead of the laborious soil test, easy-to-handle plant tests such as measurement of chlorophyll might become available to support the fertilizer decision. Benefits from splitting N application only occur if losses are prevented and/or net mineralization deviates from the average. Because of these conditions, mixed results are reported in the literature. Welch et al. (1985), for instance, observed considerable yield increases. Kiisters (1996), in contrast, found no influence on fresh matter yield at optimal fertilizer rate in any of 12 experiments, although in 2 of the experiments leaching out of the rootable soil layer (0-30cm) was prevented. This highlights the aspect that chances to prove positive effects of splitting increase if sharp optimum or slightly suboptimum treatments are included in the experimental design. Potentially, beneficial effects can be expected (1) on soils having low water-holding capacity, (2) with shallow rooting crops, (3) in regions of heavy rainfall with the risk of nitrate leaching.

208

M. SCHENK

2. N Placement. For P that is relatively immobile in the soil, it is well established that banding of P fertilizers can improve P efficiency, and so farmers use this technique. Placement of a N fertilizer dose on the plant could improve spatial availability for crops at large planting distances during early growth stages when plant roots have not yet penetrated the whole potentially rootable soil volume. Accordingly, it was observed that N placement supported initial growth of lettuce, potato, and maize (Steingrobe and Schenk 1994b; Himken 1995). However, this was reflected in a less pronounced manner in the final yield of potato and maize and not with lettuce. The reason might be that growing conditions improved during the culture course, thus reducing the initial effects (Steingrobe and Schenk 1994b). With cauliflower, no effect ofN placement on plant development occurred (Everaarts et al. 1996). N recovery was on average only slightly (ca. 5%) enhanced, but sites differed considerably (Himken 1995). This indicates that plants are able to use the broadcast applied N fertilizer as well. Results obtained by Himken (1995) confirm a homogeneous depletion of N in the soil independent of the distance to the plant with optimum or suboptimum N supply. Root length densities decreased with distance to the plant but were still at a level sufficient to exhaust nitrate from the soil in between plants (Steingrobe and Schenk 1994b; Himken 1995). However, only at supraoptimum N supply was higher residual inorganic N observed in the middle of the rows. Thus, other reasons have to be discussed to explain the improved N recovery. Results obtained by Himken (1995) suggested that both leaching losses as well as N immobilization are potentially less. It was speculated that availability of C-sources limited the N immobilization in case of N placement. There are other factors positively influencing plant growth in addition to improved N recovery. First, in the case of NH 4 + application, a large portion of ammonium should be provided early in the crop cycle because nitrification is inhibited at higher NH 4 + concentrations in the placement zone (Malhi and Nyborg 1985; Hofman et al. 1993; Himken 1995). The larger NH/ proportion of N taken up by plants may significantly stimulate plant growth (Merkel 1973; Schenk and Wehrmann 1979; Alexander et al. 1991; Barber et al. 1992; CaO and Tibbits 1993). Second, it is well known that NH 4 + placement improves P nutrition and mobilization of Mn or Zn could also occur. Another aspect of N placement is that root branching will be enhanced in the supply zone, as described in Section II C. This effect could be used for the production of nursery plants with compact root stocks, which is especially interesting for those traded with root balls. However, root branching in the

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

209

placement zone will only be stimulated if the site is N deficient (Brumm and Schenk 1992). B. N Fertilizer Type It is well established that volatilization of NH 3 gas can occur after application of ammonium salts or urea on the soil surface, which is prevented by placement or incorporation. Losses from urea are higher than from ammonium fertilizers and increase with soil pH (Vlek et a1. 1981). 1. Nitrification Inhibitors and Slow Release Fertilizers. In addition to split application and fertilizer placement, the use of nitrification inhibitors or slow release fertilizers has the potential to increase N efficiency. Nitrification inhibitors inhibit the oxidation of ammonium. As a cation, it is bound to soil exchange sites and protected from leaching. The results of Welch et a1. (1985) and Hahndel et a1. (1994) reveal that indeed nitrapyrin (N-serve) and dicyandiamide (didin), respectively, improved yield of a range of vegetable crops. But these effects were mainly restricted to situations with high rainfall during the culture course (Hahndel et a1. 1994). However, partial nutrition with ammonia by itself also has the potential to stimulate growth, as discussed in Section IV A 2 (N Placement). On the other hand, predominant absorption of N in the form of ammonium may result in yield reductions, depending on the crop. Hahndel and Wehrmann (1986a) reported a yield decrease for spinach but not for butterhead lettuce. Nitrate acts as osmoticum in the plants and cannot be replaced in this function by ammonium (Hahndel and Wehrmann 1986a,b). Furthermore, ammonium nutrition may be conflicting with crops tending to Ca deficiency because of the antagonistic action of ammonium (Wilcox et a1. 1973). Slow release fertilizers are also being discussed as a way to increase N efficiency by preventing losses, especially in nurseries, but detailed studies are not yet available.

2. Chloride. For species where nitrate plays an important role as osmoticum, the N requirement can be partially substituted by chloride. Hahndel and Wehrmann (1986b) report that the N target level for maximum yield of spinach and butterhead lettuce could be reduced by 50 and 30 kg N / ha, respectively, if the total chloride supply from the soil and fertilization amounted to 350 or 150 kg / ha. They suggested a fertilization of 150 or 50 kg / ha in the form of KCI prior to planting, if elsoil test values are unavailable. However, exceeding the abovementioned levels of chloride supply bears the risk of yield reductions.

210

M. SCHENK

C. Crop Management 1. Irrigation. In horticultural field production, irrigation is common practice. It has been the general experience that crops are excessively irrigated, which leads to N losses. For appropriate irrigation, timing and rate must be scheduled. This can be done by models based on evapotranspiration or measuring soil water tension (Pier and Doerge 1995). This issue will not be discussed further in the review, but it is clear that efficient N use can only be achieved if water application is limited to plant demand, as shown by Cook and Sanders (1990) and Thompson and Doerge (1996). Considering the fact that natural precipitation cannot be predicted and that horticultural crops often have a shallow root system, frequent application of small amounts of water would be the best way to optimize water application (Jackson et a1.). Furthermore, the irrigation technique must ensure a homogeneous distribution of water so that no excess irrigation to compensate inhomogenity is required. 2. Organic Matter. During the last decades, soil fertility was improved by increasing the plow layer, as described for Germany (Nieder and Richter 1986). Together with the general practice of applying large amounts of farmyard manure, this may result in a net mineralization exceeding the demand of the crop, as was shown for nurseries, because many nursery crops have low annual N demand, frequently less than 50 kg N / ha (AIt et a1. 1989; Dierend and Spethmann 1994a,b). The residual mineral N is in danger of escaping into the environment, a problem that has to be considered in the management of soil organic matter. Another important N source is the residues of the preceding crop remaining in the field, which applies above all to vegetable production. A survey by Schrage (1990) and Titulaer (1995) showed a wide range of 20-30 kg N / ha for crops like butterhead lettuce and chicory and up to 160 kg N / ha for cauliflower, broccoli, and brussels sprouts. The organically bound N is turned over to inorganic N within 6-10 weeks and thus is available for the following crop (Schrage 1990), and has to be taken into account by appropriate deduction from the target level for optimum N supply (Schrage 1990). Computer-based decision systems include this important aspect (Fink and Scharpf 1993; Rahn et a1. 1994). Furthermore, planning of crop rotation has to take into account the fact that the subsequent crop should be able to use the amount of N contained in crop residues so that the residual N remaining in the soil at the end of the vegetation period is low enough to meet ecological standards. Crop residues remaining in the field at the end of the vegetation period are problematic. Depending on the climate, soil temperatures may allow a

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

211

more or less significant mineralization (Engels and Kuhlmann 1993, e.g.) and subsequent leaching of N0 3 • Mulching is a probable way to delay mineralization, but may not be sufficient. 3. Catch Crops. Not only residual inorganic N but also nitrate originat-

ing from decomposition of crop residues can easily be leached during winter on bare fallow fields. Cover crops planted at the harvest of the last crop have a large potential to absorb N and to save it from leaching for the next vegetation period (Shennan 1992; S0rensen 1992; S0rensen and Thorup-Kristensen 1993). In the literature, up to 150 kg N / ha are reported (Jackson et al. 1993). Factors having a strong impact on the capacity of the catch crop are species, climatic conditions, and duration of the planting window. It was demonstrated that N contained in the plant matter becomes potentially available for the next summer crops (Elers and Hartmann 1988; Jackson et al. 1993; S0rensen and ThorupKristensen 1993). The choice of the appropriate catch crop will depend on the specific conditions (climate, planting window) as well as on interactions with soil-borne plant diseases or pests. Oilseed radish, for example, is unsuitable for crop rotation (including brassicas) because the risk of club root infestation (Plasmodiophora brassicae) is increased. V. CONCLUSION Economic considerations governed N application in the past, aiming to minimize the risk of yield losses by means of a supraoptimum fertilizer rate. The reasons for this attitude were the low price of N fertilizer and the lack of appropriate methods for reliable determination of optimal fertilizer rate. The review outlines the considerable increase in the knowledge ofN dynamics in the soil-plant system during the last two decades, which has led to various tools for the characterization of N fertilizer needs. Full application of current knowledge would allow farmers today to improve N fertilizer dosage without the risk of yield losses. It is a challenge for extension services to encourage adoption of new methodology by growers. Horticultural production systems are quite variable depending on the crop, climate, soil, and farming technique. Mulching with plastic, for example, has an impact on water and temperature regime of the soil as well as on gas exchange, thus influencing net mineralization (Ruppel and Makswitat 1996). The analysis ofN dynamics in such specific conditions and appropriate adoption of methodology for N management would allow a further step towards ecological friendly production.

212

M. SCHENK

Special attention has to be given to management of N contained in crop residues remaining in the field at the end of the growing period because of the leaching hazard. This risk is especially high for brassicas that leave large amounts of crop residues in the field. Irrigation scheduling and techniques have to be integrated into strategies to improve N fertilizer efficiency in order to avoid nitrate leaching as well as denitrification losses. However, horticultural field production remains an open system and even the best handling of the components of N management will not completely prevent migration of N to other eco-systems. The risk of losses increases with the amount of N circulating in the production system, which consequently should be kept as low as possible. For nursery production, for example, where large amounts of farmyard manure are used, it is necessary to analyze relationships between organic matter supply and crop requirements in order to define critical levels and to prevent supraoptimum N application contained in organic matter (Bohne et al. 1996). Another approach to efficient use of N would be to breed for cultivars having high N efficiency (Barker 1989). Seed companies have integrated this goal into their strategy by selecting at suboptimum N supply. For brassica, for example, cultivars are required that leave less harvest residues behind. Finally, it seems worthwhile to investigate whether cultivation at reduced growth rates during supraoptimal N supply has the potential to achieve the set yield and quality goal (Schenk et al. 1991). First results on lettuce indicate that accepting a few days' delay of the harvest allows a halving of the target level for N supply. However, it is clear that the applicability of this strategy depends on the respective crop. LITERATURE CITED Addiscott, T. M., and A. P. Whitmore. 1987. Computer simulation of changes in soil mineral nitrogen and crop nitrogen during autumn, winter and spring. J. Agr. Sci. (Camb.) 109:141-157. Alexander, K. G., H. M. Miller, and E. G. Beauchamp. 1991. The effect of an NH/-enhanced nitrogen source on the growth and yield of hydroponically grown maize (Zea mays L.). J. Plant Nutr. 14:31-44. Alt, D. 1996. Calculation of fertilizer demand for vegetable crops in private gardens. Acta Hort.428:165-170. Alt, D., B. Bloem, and V. Langeloh. 1995. Niihrstoffentziige durch den Neutrieb von Baumschulgeh61zen. Gartenbauwissenschaft 60:73-76. Alt, D., H. Kohlstall. C. Bierreth, M. Hegge, and A. Bier-Kumotzke. 1989. Stickstoffversorgung von Baumschulgeh6lzen. Gartenbauwissenschaft 54:123-128. Alt, D., and J. Rimmek. 1994. Grundziige eines EDV-Programms fur die Diingung von Garten. Gartenbauwissenschaft 59:186-190.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

213

Andrews. M. 1986. The partitioning of nitrate assimilation between roots and shoot of higher plants. Plant Cell Environ. 9: 511-519. Aslam. M.. R. L. Travis. and R. C. Huffaker. 1992. Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiol. 99:1124-1133. Atkinson, D. 1986. The nutrient requirements of fruit trees: some current considerations. Adv. Plant Nutr. 2:93-128. Bach. M. 1985. Stickstoff-Bilanzen der Kreise der Bundesrepublik Deutschland als Grundlage einer Abschatzung der moglichen Nitratbelastung des Grundwassers durch die Landwirtschaft. Mitteilgn. Dtsch. Bodenkundl. Gesellschaft 431II:625-630. Bachmann. M.. N. Shiraishi. W. H. Campbell. B.-C. Yoo. A. C. Harmon. and S. C. Huber. 1996. Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8:505-517. Baker. A. V.• and H. A. Mills. 1983. Ammonium and nitrate nutrition of horticultural crops. Hort. Rev. 5:317-413. Barber. K. L.. L. D. Muddux. D. E. Kissel, G. M. Pierzynski, and B. R Bock. 1992. Corn responses to ammonium- and nitrate-nitrogen fertilization. Soil Sci. Soc. Am. J. 56:1166-1171. Barber. S. A. 1984. Soil nutrient bioavailability. Wiley. New York. Barker. A. V. 1989. Genotypic responses of vegetable crops to nitrogen nutrition. HortScience 24:256-591. Barraclough. P.. H. Kuhlmann. and A. H. Weir. 1989. The effect of prolonged drought and nitrogen fertilizer on root and shoot growth and water uptake by winter wheat. J. Agron. Crop Sci. 163:352-360. Behl. R. R. Tischner. and K. Raschke. 1988. Induction of a high-capacity nitrate-uptake mechanism in barley roots prompted by nitrate uptake through a constitutive lowcapacity mechanism. Planta 176:235-240. Bettin. A.. and M. Schenk. 1988. Stickstoff-Bestimmung bei Azaleen. Deutscher Gartenbau 42:342-343. Blankenau. K.. H. W. Olfs. and J. Lammel. 1996. The effect of increasing N supply on net N mineralisation in soils under barley and fallow. Transaction of 9th Nitrogen Workshop. Technical Univ. Braunschweig. Germany. p. 193-196. Bock. E.. H. P. Koops. H. Harms. and B. Ahlers. 1991. The biochemistry of nitrifying organisms. p. 171-200. In: J. M. Shively and L. L. Barton (eds.). Variations in autotrophic life. Academic Press. London. Bohmer. M. 1980. Der Mineralstickstoffgehalt von Boden mit Feldgemiisebau und seine Bedeutung fUr die Stickstoffernahrung der Pflanze. Diss. Univ. Hannover. Germany. Bohne, H.. Th. Daum. and C. Schuh. 1996. Einflul3 von Biokompost und Stallmist auf Bodeneigenschaften und Wachstum von Acer pseudoplatanus. Gartenbauwissenschaft 61:53-59. Bottcher. H.. G. Ziegler, and F. Diwisch. 1969. Einflul3 iiberh6hter Stickstoffdiingung auf Haltbarkeit und Qualitatserhaltung bei der Lagerung von Gemiise. Archiv Gartenbau 17:43-60. Bowman. A. F. 1989. Soils and greenhouse effect. Proc. Intern. Conference Soils and the Greenhouse Effect. Wiley. New York. Breteler, H.. and M. Siegerist. 1984. Effect of ammonium on nitrate utilization of dwarf bean. Plant Physiol. 75:1099-1103. Brumm. 1., and M. Schenk. 1992. N-Ernahrung und Wachstum von Pinus sylvestris L. Gartenbauwissenschaft 57:101-106.

214

M. SCHENK

Brumm, 1., and M. Schenk. 1993. Influence of nitrogen supply on the occurrence of calcium deficiency in field grown lettuce. Acta Hort. 339:125-136. Burns, J. G. 1980. Influence of the spatial distribution of nitrate on the uptake of N by plants: a review and a model for rooting depth. J. Soil Sci. 31:155-173. Campbell, W. H. 1996. Nitrate reductase biochemistry comes of age. Plant Physiol. 111:355-361CaO, W., and T. W. Tibbits. 1993. Study of various NH 4 +/N0 3- mixtures for enhancing growth of potatoes. ]. Plant Nutr. 16:1691-1704. Carter, J. N., M. E. Jensen, and S. M. Bosma. 1974. Determining nitrogen fertilizer needs for sugar beets from residual soil nitrate and mineralizable nitrogen. Agron. J. 66:319-323. Clarkson, D. T. 1986. Regulation of the absorption and release of nitrate by plant cells: a review of current ideas and methodology. p. 3-27. In: H. Lambers,J. ]. Neeteson, and I. Stulen (eds.), Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Martinius Nijhoff Publ., Dordrecht, The Netherlands. Clarkson, D. T., and M. J. Hawkesford. 1993. Molecular approaches to plant nutrition. p. 23-33. In: J. Barrow (ed.), Plant nutrition-from genetic engineering to field practice. Kluwer Academic Publ., Dordrecht, The Netherlands. Clarkson, D. T., and A. J. Warner. 1979. Relationships between root temperature and the transport of ammonium and nitrate ions by italian and perennial ryegrass (Lolium multiflorum and Lolium perenne). Plant Physiol. 64:557-561. Coldewey z. Eschenhoff, H. 1985. Der Einflufi von Pflanzen und Mikroorganismen auf den Gehalt an nicht-austauschbarem NH 4 + in Lossboden. Diss. Univ. Hannover, Germany. CoHman, R. R. 1987. Yield and sap nitrate offresh market field tomatoes to simulated fertigation with nitrogen.]. Plant Nutr. 10:1699-1704. CoHman, R. R. 1988. Yields of greenhouse tomatoes managed to maintain specific petiole sap nitrate levels. HortScience 23:148-151. Cook, W. P., and D. C. Sanders. 1990. Fertilizer placement effects on soil nitrogen and use by drip-irrigated and plastic-mulched tomatoes. HortScience 25:767-769. Cooper, H. D., and D. T. Clarkson. 1989. Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals. A possible mechanism integrating shoot and root in the regulation of nutrient uptake. J. Expt. Bot. 40:753-762. Crawford, N. M. 1995. Nitrate: Nutrient and Signal for Plant Growth. Plant Cell 7:859-868. Cruz, C., S. H. Lips, and M. A. Martins-Lou<;ao. 1995. Uptake regions of inorganic nitrogen in roots of carrot seedlings. Physiol. Plant 95:167-175. Dahnke, W. c., and G. V. Johnson. 1990. Testing soils for available nitrogen. In: R. L. Westerman (ed.), Soil testing and plant analysis. 3rd ed. SSSA, Madison, Wisconsin. De Neve, S., J. Dannier, and G. Hofman. 1994. Fractionation of vegetable crop residues in relation to in situ N mineralization. Env. J. Agron. 3:267-272. De Willigen, P., and]. J. Neeteson. 1985. Comparison of six simulation models for the nitrogen cycle in the soil. Fert. Res. 8:157-171. De Willigen, P., and M. Van Noordwijk. 1987. Roots, plant nutrition and nutrient use efficiency. Ph. D. Thesis. Agr. Univ. Wageningen, The Netherlands. Dierend, W., and W. Spethmann. 1994a. Der Mineralstickstoffgehalt in Boden von Baumschulen. I. Veranderungen der Nmin-Gehalte des Bodens wahrend der Vegetationsperiode. Gartenbauwissenschaft 59:1-5. Dierend, W., and W. Spethmann. 1994b. Der MineralstickstoffgehaH in Boden von Baumschulen. II. Nmin-Gehalte des Bodens im Herbst und Nitratauswaschung tiber Winter. Gartenbauwissenschaft 59:62-66.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

215

Dierend, W., and W. Spethmann. 1994c. N-Aufnahme von GehOlzen im Verlauf der Vegetationsperiode. Gartenbauwissenschaft 59:121-125. Dierend, W., and W. Spethmann. 1996. Einflufi der N-Diingung auf das Wachstum von Apfelunterlagen und einjiihrigen Apfelbiiumen. Erwerbsobstbau 38:90-93. Doddema, H., and G. P. Telkamp. 1979. Uptake of nitrate by mutants of Arabidopsis thaJiana, disturbed in uptake or reduction of nitrate. II. Kinetics. Physiol. Plant. 45:332-338. Drew, M. C. 1975. Comparison of the effect of localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system and the shoot in barley. New Phytol. 75:479-490. Drews, M.,]. Schonhof, and A. Krumbein. 1995. Nitrat-, Vitamin Co, fi-Carotin- und Zuckergehalt von Kopfsalat im Jahresverlauf beim Anbau im Gewiichshaus (Lactuca sativa L.). Gartenbauwissenschaft 60:180-187. Edwards, J. H., and S. A. Barber. 1976a. Nitrogen uptake characteristics of corn roots at low N concentration as influenced by plant age. Agron. J. 68:17-19. Edwards, J. H., and S. A. Barber. 1976b. Nitrogen influx into corn roots as influenced by shoot requirement. Agron. J. 68:471-473. EEC 1980. Council directive on the quality of water for human consumption. Official issue No. 801778, EECL 229,111 European Economic Community, Brussels. Elers, B., and H. D. Hartmann. 1988. Modellversuche zur Mineralisation von Griindiingungspflanzen. Landwirtsch. Forschung 41:246-252. Engels, T. 1983. Nitratauswaschung aus Getreide- und Zuckerriibenfliichen bei unterschiedlichem N-Angebot. Diss. Univ. Hannover, Germany. Engels, T., and H. Kuhlmann. 1993. Effects of the rate of N fertiliser on apparent net mineralisation of N during and after cultivation of cereal and sugar beet crops. Z. Pflanzenerniihr. Bodenk. 156:149-154. Everaarts, A. P., C. P. de Moel, and M. Van Noordwijk. 1996. The effect of nitrogen and the method of application on nitrogen uptake of cauliflower and on nitrogen in crop residues and soil at harvest. Neth. J. Agr. Sci. 44:43-56. Fink, M., and H.-C. Scharpf. 1993. N-Expert-a decision support system for vegetable fertilization in the field. Acta Hort. 339:67-74. Fischer, J. 1992. The influence of different nitrogen and potassium fertilisation on the chemical flavour composition of kohlrabi (Brassica oleracea vaf. gongylodes L.). ]. Sci. Food Agr. 60:456-463. Foehse, D., and A. Jungk. 1983. Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74:359-368. Fox, R. H., J. S. Shenk, W. P. Piekidek, M. O. Westerhaus, J. D. Toth, and K. E. Macneal. 1993. Comparison of near-infrared spectroscopy and other soil nitrogen availability quick tests for corn. Agron. J. 85:1049-1053. Freitag, A., M. Rudert, and E. Bock. 1987. Growth of Nitrobacter by dissimilatoric nitrate reduction. FEMS Microbiol. Lett. 48:105-109. Frota, J. N. E., and T. C. Tucker. 1972. Temperature influence on ammonium and nitrate absorption by lettuce. Soil Sci. Soc. Am. Proc. 36:97-100. Gardner, B. R, and R. L. Roth. 1990. Midrib nitrate concentration as a means for determining nitrogen needs of cauliflower. J. Plant Nutr. 13:1435-1451. Giles,]. F.,]. D. Reuss, and A. E. Ludwick. 1973. Prediction of nitrogen status of sugar beets by soil analysis. Agr. Abstr. Am. Soc. Agron. Annual Meetings 98:11-16. Glasener, K. M., and C. A. Palm. 1995. Ammonia volatilization from tropical legume mulches and green manures on unlimed and limed soils. Plant Soil 177:33-41. Glass, A. D. M. 1988. Nitrogen uptake by plant roots. lSI Atlas of Plant Science. Plants Animals 1:151-156.

216

M. SCHENK

Glass, A. D. M., J. E. Shaft, and L. V. Kochian. 1992. Studies on the uptake of nitrate in barley. IV. Electrophysiology. Plant Physio!. 99:456-463. Glass, A. D. M., and M. Y. Siddiqi. 1984. The control of nutrient uptake in relation to the inorganic composition of plants. p. 103-147. In: P. B. Tinker and A. Liiuchli (eds.), Advances in plant nutrition 1. Praeger Pub!., New York. Graedel, T. E., and P. J. Crutzen. 1994. Chemie der Atmosphare. Spektrum Akademischer Verlag. Heidelberg, Germany. Granli, T., and O. C. Backmann. 1994. Nitrous oxide from agriculture. Norweg. J. Agr. Sci., Supp!. 12:7-128. Greenwood, D. J. 1986. Prediction of nitrogen fertilizer needs of arable crops. Adv. Plant Nutr. 2:1-61. Gysi, C. 1990a. Modelling and measurement of the nitrogen cycle in a vegetable field in Switzerland. 1. A soil-plant model for the nitrogen cycle. Z. Pflanzenernahr. Bodenk. 153:181-187. Gysi, C. 1990b. Modelling and measurement of the nitrogen cycle in a vegetable field in Switzerland. II. Validation of the nitrogen model with field data. Z. Pflanzenerniihr. Bodenk. 153:189-196. Hahndel, R, H. Lang, and P. Hermann. 1994. Wirkung von Ammonium-stabilisierten Diingern auf Ertrag und Qualitat von Gemiise. Agribio!. Res. 47:101-108. Hahndel, R, and J. Wehrmann. 1986a. Einflufi der N0 3- bzw NH4 -Ernahrung auf Ertrag und Nitratgehalt von Spinat und Kopfsalat. Z. Planzenerniihr. Bodenk. 149:290-302. Hahndel, R, and J. Wehrmann. 1986b. Einflufi der CI-Ernahrung auf Ertrag und Nitratgehalt von Spinat und Kopfsalat. Z. Pflanzenerniihr. Bodenk. 149:303-313. Harmsen, K., and J. T. Moraghan. 1988. A comparison of the isotope recovery and difference methods for determining nitrogen fertilizer efficiency. Plant Soil 105:55-67. Hartz, T. K., and G. J. Hochmuth. 1996. Fertility management of drip-irrigated vegetables. HortTechnology 6:168-172. Hartz, T. K., M. Le Strange, and D. M. May. 1993. Nitrogen requirements of drip-irrigated peppers. HortScience 28:1097-1099. Heckmann, J. R, W. T. Hlubik, D. J. Prostak, and J. W. Paterson. 1995. Pre-sidedress soil nitrate test for sweet corn. HortScience 30:1033-1036. Heins, B., and M. Schenk. 1987. Root growth and nitrate uptake of vegetable crops. J. Plant Nutr.1O:1743-1751. Herschbach, c., and H. Rennenberg. 1991. Influence of glutathion on sulphate influx, xylem loading and exudation in excised tobacco roots. J. Expt. Bot. 42:1021-1029. Himken, M. 1995. Einflufi plazierter N-Diingung in Mais und Kartoffeln auf die N-Effizienz und das Sprofi- und Wurzelwachstum. Diss., Univ. Hannover, Verlag U. Grauer, Stuttgart, Germany. Hochmuth, G. J. 1992. Concepts and practices for improving nitrogen management for vegetables. HortTechnology 2:121-125. Hochmuth, G. J. 1994. Efficiency ranges for nitrate nitrogen and potassium for vegetable petiole sap quick test. HortTechnology 4:218-222. Hofman, G., P. Verstegen, P. Demyttenaere, M. van Meirvenne, P. Delanote, and G. Ampe. 1993. Comparison ofrow and broadcast N application on N efficiency and yield of potatoes. p. 359-365. In: M. A. C. Fragoso, and M. 1. van Beusichem (eds.), Optimization of plant nutrition. Kluwer Academic Pub!. Honeycutt, C. W., 1. J. Potaro, and W. A. Halteman. 1991. Predicting nitrate formation from soil, fertilizer, crop residue and sludge with thermal units. J. Environ. Qual. 20:850-856. Imsande, J., and B. Touraine. 1994. N demand and the regulation of nitrate uptake. Plant Physio!. 105:3-7.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

217

Jackson, 1. E., and A. J. Bloom. 1990. Root distribution in relation to soil nitrogen availability in field-grown tomatoes. Plant Soil 128:115-126. Jackson, L. E., and 1. J. Stivers. 1993. Root distribution oflettuce under commercial production: implications for crop uptake of nitrogen. BioI. Agr. Hort. 9:273-293. Jackson, 1. E., 1. J. Wyland, and 1. J. Stivers. 1993. Winter cover crops to minimize nitrate losses in intensive lettuce production. J. Agr. Sci. (Camb.) 121:55-62. Jakob, F., H.-P. Vielemeyer, and W. Podlesak. 1986. Untersuchungen zur Eignung des Nitratgehaltes von Winterweizen zur Diagnose des N-Ernahrungszustandes in Feldbestanden. Arch. Pflanzenbau Bodenk. 30:607-612. Jemison, J. M., and R. H. Fox. 1988. A quick-test procedure for soil and plant tissue nitrates using test strips and a hand-hold reflectometer. Commun. Soil Sci. Plant Anal. 19:1569-1582. Joiner, J. N., R. T. Poole, and C. A. Conover. 1983. Nutrition and fertilization of ornamental greenhouse crops. Hort. Rev. 5:317-403. Jones, D. 1., and P. R. Darrah. 1994. Influx and efflux of amino acids from Zea mays L. roots and its implications in the rhizosphere. Plant Soil 163:1-12. Jungk, A., and ]. Wehrmann. 1978. Determination of fertilizer requirements by plant and soil analysis. Proc. 8th Intern. ColI. on Plant Analy. Fert. Problems. Auckland, New Zealand. A.R. Kafkafi, U., N. Voloras, and J. Letey. 1982. Chloride interaction with nitrate and phosphate nutrition in tomato (Lycopersicon esculentum L.). J. Plant Nutr. 5:1369-1385. Keeney, D. R. 1982. Assessment of soil nitrogen availability. p. 651-688. In: A. L. Page, R. H. Miller. and D. R. Keeney (eds.), Methods of soil analysis Part 2, 2nd edn. Am. Soc. Agron., Madison, WI. Kersebaum, K. C., and J. Richter. 1991. Modelling nitrogen dynamics in a plant-soil system with a simple model for advisory purposes. Fert. Res. 27:273-281. King, F. H., and A. R. Whitson. 1901. Development and distribution of nitrate and other soluble salts in cultivated soils. Univ. Wisconsin Agr. Expt. Sta. Bul. 85. King. F. H., and A. R. Whitson. 1902. Development and distribution of nitrates in cultivated soils. Univ. Wisconsin Agr. Expt. Sta. Bul. 93. Kohler, J. 1983. Eignung von Methoden der Bodenanalyse zur Erfassung der N-Nachlieferung von Lofiboden und zur Bemessung der Stickstoffspatgaben zu Winterweizen. Diss. Univ. Hannover. Korcak, R. F. 1988. Nutrition of blueberry and other calcifuges. Hort. Rev. 10:183-227. Kramer, P., and T. Koslowski. 1979. Physiology of woody plants. Academic Press, New York. Kuhlmann, H., and P. B. Barraclough. 1987. Comparison between the seminal and nodal root system of winter wheat in their activity for Nand K uptake. Z. Pflanzenernahr. Bodenk. 150:24-30. Kuhlmann, H., P. B. Barraclough, and A. Weir. 1989. Utilization of mineral nitrogen in the subsoil by winter wheat. Z. Pflanzenernahr. Bodenk. 152:291-295. Kuhlmann, H., J. Kohler, and J. Wehrmann. 1986. Eignung der EUF-Methode zur Ermittlung der K- und N-Versorgung von Lofiboden in Niedersachsen. Landw. Forsch. 39:87-96. Kiisters, J. 1996. Entwicklung eines Simulationsmodells zur Steuerung der Stickstoffdungung von Kopfsalat (Lactuca sativa L.) im Freiland. Diss. Univ. Hannover, Verlag U. Grauer, Stuttgart, Germany. Lewis, R. J., and S. 1. Love. 1994. Potato genotypes differ in petiole nitrate-nitrogen concentrations over time. HortScience 29:175-179. Lorenz, H. P., ]. Schlaghecken, and G. Engl. 1986. Gezielte Stickstoffversorgung im

218

M. SCHENK

Gemiisebau nach dem kulturbegleitenden Nmin Sollwerte (KNS)-System. Neustadter Hefte 26, Germany. Lorenz, H. P., J. Schlaghecken, G. Engl, A. Maync, and J. Ziegler. 1989. Regulated nitrogen fertilization in field vegetable production according to the 'Guided cultivation Nmin target value (KNS)-system'. p. 85. Min. Agr. Vitic. Rheinland-Pfalz, Mainz, Germany. Magdoff, F. R, D. Ross, and J. Amadon. 1984. A soil test for nitrogen availability to corn. Soil Sci. Soc. Am. J. 48:1301-1304. Maier, N. A., A. P. Dahlenburg, and C. M. J. Williams. 1994. Effect of nitrogen, phosphorus and potassium on yield and petiolar nutrient concentration of potato (Solanum tuberosum 1.) cvu. Kennebec and Atlantic. Austral. J. Expt. Agr. 34:825-834. Malhi, S. S., and M. Nyborg. 1985. Methods of placement for increasing the efficiency of N fertilizers applied in the fall. Agron. J. 77:27-32. Maynard, D. N., A. V. Barker, P. L. Minotti, and N. H. Peck. 1976. Nitrate accumulation in vegetables. Adv. Agronomy 28:71-118. Maynard, D. N., and 0. A. Lorenz. 1979. Controlled-release fertilizers for horticultural crops. Hort. Rev. 1:79-140. McKerron, D. K. L., M. W. Young, and H. U. Davies. 1993. A method to optimize Napplication in relation to soil supply of N and yield of potato. Plant Soil 155:139-144. McKerron, D. K. L., M. W. Young, and H. V. Davies. 1995. A critical assessment ofthe value of petiole sap analysis in optimizing the nitrogen nutrition of the potato crop. Plant Soil 172:247-260.

McTaggart, I. P., and K A. Smith. 1993. Estimation of potentially mineralisable nitrogen in soil by KCI extraction II. Comparison with soil N uptake in the field. Plant Soil 157:175-184.

Merkel, D. 1973. EinfluB des N0 3 :NH4 -Verhaltnisses in der Nahrlosung auf Ertrag und Gehalte an organischen und anorganischen Ionen in Tomatenpflanzen. Z. Pflanzenernahr. Bodenk. 134:236-246. Min Ni, and L. Beevers. 1994. Nitrate-induced polypeptides in membranes from corn seedling roots. J. Expt. Bot. 45:353-356. Ministerie van Landbouw en Visserij. 1989. Stikstofbijmestsysteem voor enige Vollegrondsgroentegewassen. Consulentschap voor Bodem-, water- en bemestingszaken in de Akkerbouw en Tuinbouw, Wageningen, The Netherlands. Minotti, P. L., D. E. Halseth, and J. B. Sieczka. 1994. Field chlorophyll measurements to assess the nitrogen status of potato varieties. HortScience 29:1497-1500. Mlot, C. 1997. Tallying nitrogen's increasing impact. Sci. News 151:100. Mohr, H. D. 1978. Die Durchwurzelung von Boden in Abhangigkeit von wichtigen Bodeneigenschaften. Kali-Briefe (Btintehof) 14:103-113. Mohr, H. D. 1980. EinfluB von Bodeneigenschaften auf das Wurzelwachstum. Kali-Briefe (Biintehof) 15:305-316. Muller, B., and B. Touraine. 1992. Inhibition of N0 3 - uptake by various phloemtranslocated amino acids in soybean seedlings. J. Expt. Bot. 43:71-74. Nemeth, K, M. I. Makhdum, K. Koch, and H. Berringer. 1979. Determination of categories of soil nitrogen by electro-ultrafiltration (EUF). Plant Soil 53:445-453. Nieder, R, and J. Richter. 1986. C- und N-Festlegung in Boden Stidostniedersachsens nach Krumenvertiefung. Z. Pflanzenernahr. Bodenk. 149:189-201. Noordwijk, M. v., G. Brouwer, and K Harmanny. 1993. Concepts and methods for studying interactions ofroots and soil structure. Geoderma 56:351-375. Nye, P. H., and P. B. Tinker. 1977. Solute movements in the soil-root system. Studies in ecology. Vol. 4. Blackwell Scientific Publications, Oxford. Oaks, A. 1992. A re-evaluation of nitrogen assimilation in roots. Bioscience 42:103-111.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

219

Obermayr. A.. and D. Alt. 1992. Moglichkeiten und Schwierigkeiten bei der Ermittlung des Frischsubstanz-Ertrages von Baumschulgeholzen als Basis einer sachgerechten Stickstoff-Diingung. Gartenbauwissenschaft 57:11-14. Olsen. C. 1950. The significance of concentration for the rate of ion absorption by higher plants in water culture. Physiol. Plant. 3:152-164. Olsen.]. K, and D. ]. Lyons. 1994. Petiole sap nitrate is better than total nitrogen in dried leaf for indicating nitrogen status and yield responsiveness of capsicum in subtropical Australia. Austral. ]. Expt. Agr. 34:835-843. Otter-Nacke. S.• and H. Kuhlmann. 1991. A comparison of the performance of N simulation models in the prediction ofN min on farmer's field in spring. Fert. Res. 27:341-347. Padgett. P. E.. and R. T. Leonard. 1993. Regulation of nitrate uptake by amino acids in maize cell suspension culture and intact roots. p. 173-176. In: ]. Barrow (ed.), Plant nutrition. From genetic engineering to field practice. Kluwer Academic Publishers. Dordrecht. The Netherlands. Pier. ]. W.. and T. A. Doerge. 1995. Nitrogen and water interactions in trickle irrigated watermelon. Soil Sci. Soc. Am. ]. 59:145-150. Pitman. M. G., and W. J. Cram. 1976. Regulation of ion content in whole plants. Symp. Soc. Expt. Bot. 31:391-424. Poth. M.• and D. D. Focht. 1985. 15N kinetic analysis of NzO production by Nitrosomonas europae: an examination of nitrifier denitrification. Appl. Environ. Microbiol. 49:1134-1191. Power.]. F., and]. S. Schepers. 1989. Nitrate contamination of groundwater in North America. Agr., Ecosyst. Environ. 26:165-187. Pritchard, K H., T. A. Doerge. and T. L. Thompson. 1995. Evaluation of in-season nitrogen tests for drip irrigated leaf lettuce and romaine lettuce. Commun. Soil Sci. Plant Anal. 26:237-257. Rahn, C. R., D. J. Greenwood. and A. Draycott. 1994. Prediction of nitrogen fertilizer requirement with HRI Well-N computer model. In: O. van Cleemput, G. Hofmaan. and A. Vermoesen (eds.), Progress in nitrogen cycling. Proc. 8th Nitrogen Workshop, Univ. Ghent. Belgium. Reidenbach. G. 1996. Institut fur Pflanzenerniihrung. Univ. Hannover. Germany. Richter,]. A.. A. Nuske, M. Boehmer. and]. Wehrmann. 1980. Simulation of nitrogen mineralisation and transport in loess-parabrownearthes plot experiments. Plant Soil 54:329-337. Ris, ]., K W. Smilde, and G. Wignen. 1981. Nitrogen fertilizer recommendations for arable crops based on soil analysis. Fert. Res. 2:21-32. Robinson. D., D. J. Linehan, and S. Caul. 1991. What limits nitrate uptake from soil? Plant. Cell Environ. 14:77-85. Rodgers. C. 0., and A. J. Barneix. 1988. Cultivar differences in the rate of nitrate uptake by intact wheat plants as related to growth rate. Physiol. Plant. 72:121-126. Riihlmann. J., and B. Geyer. 1993. Validation of a simulation model for carbon and nitrogen dynamics in soil in a field trial. Acta Hort. 339:75-84. Ruppel. S., and E. Makswitat. 1996. Einflu13 von schwarzer Mulchfolie auf den N-Umsatz beimAnbau von Einlegegurken (Cucumis sativus L.). Gartenbauwissenschaft 61:230-237. Ryden. ]. c.. and L. ]. Lund. 1980. Nature and extent of directly measured denitrification losses from some irrigated crop production units. Soil Sci. Soc. Am. ].44:505-511. Sattelmacher, B., and K Thoms. 1995. Morphology and physiology of the seminal root system of young maize (Zea mays L.) plants as influenced by a locally restricted nitrate supply. Z. pflanzenerniihr. Bodenk. 158:493-497.

220

M. SCHENK

Scaife, M. A., and M. K. Turner. 1987. Field measurement of sap and soil nitrate to predict nitrogen top-dressing requirements of brussels sprouts. J. Plant Nutr. 10:1705-1712. Schacht, H., and M. Schenk. 1994. Steuerung der Diingung von Gewachshausgurken (Cucumis sativus L.) in geschlossenen erdelosen Kultursystemen mit Hilfe von Nitratund Amino-N-Gehalt im Blattstielprefisaft. Gartenbauwissenschaft 59:97-102. Schapendonk, A. H. C. M., and H. Challa. 1980. Assimilate requirements for growth and maintenance of the cucumber fruit. Acta Hort. 118:73-82. Scharpf, H.-C. 1977. Der Mineralstickstoffgehalt des Bodens als Mafistab fur den Stickstoffdiingerbedarf. Diss. Univ. Hannover, Germany. Scharpf, H.-C., and R. Schrage. 1988. Grofienordnung und Einflufifaktoren der Freisetzung von Stickstoff aus Ernteriickstanden im Gemiisebau. VDLUFA-Schriftenreihe 28, Kongrefiband Teil II:81-95. Schenk, M. K 1988. N-status of pot plants as evaluated by measurement of substrate and plant sap nitrate. Acta Hort. 221:253-260. Schenk, M. K 1996. Regulation of nitrogen uptake on the whole plant level. Plant Soil 181:131-137.

Schenk, M., D. Alt, and H. Kuhlmann. 1989. Vorschliige zur Anlage und Auswertung von Diingungsversuchen fur die Eichung von Bodenanalysen. Landw. Forsch. 42:253-264. Schenk, M., B. Heins, and B. Steingrobe. 1991. The significance of root development of spinach and kohlrabi for N fertilization. Plant Soil 135:197-203. Schenk, M., and J. Wehrmann. 1979. The influence of ammonia in nutrient soil solution on growth and metabolism of cucumber plants. Plant Soil 52:403-414. Schj0rring, J. K, N. E. Nielsen, H. E. Jensen, and H. Gottschau. 1989. Nitrogen losses from field grown spring barley plants as affected by the rate of nitrogen application. Plant Soil 116:167-175. Schloemer, S. 1991. Denitrifikation eines gemiisebaulich genutzten Bodens in Abhangigkeit von der Einarbeitung frischer Erntereste. Z. Pflanzenernahr. Bodenk. 154:265-269.

Schobert, C., W. Kockenberger, and E. Komor. 1988. Uptake of amino acids by plants from the soil: a comparative study with castor bean seedlings grown under natural and axenic soil conditions. Plant Soil 109:181-188. Schrage, R. 1990. Methoden zur Bestimmung des Stickstoff-Diingerbedarfs von Gemiisekulturen mit geringem analytischen Aufwand. Diss. Univ. Hannover, Germany. Schulz, R., and H. Marschner. 1987. Vergleich von Nitrat- und Amino-N-Schnelltest zur Charakterisierung des Stickstoffversorgungsgrades von Winterweizen. Z. Pflanzenernahr. Bodenk. 150:348-353. Shennan, C. 1992. Cover crops, nitrogen cycle, and soil properties in semi-irrigated vegetable production systems. HortScience 27:749-753. Siddiqi, M. Y., A. D. M. Glass, T. J. Ruth, and T. W. Rufty. 1990. Studies on the uptake of nitrate in barley. I. Kinetics of 13N0 3 - influx. Plant Physio!. 93:1426-1432. Smit, A. L., R. Booij, and A. Van der Werf. 1996. The spatial and temporal rooting pattern of Brussels sprouts and leeks. Neth. J. Agr. Sci. 44:57-72. Smith,.K. A., and Shengxiu Li. 1993. Estimation of potentially mineralisable nitrogen in soil by KCl extraction 1. Comparison with pot experiments. Plant Soil 157:167-174. Sommer, S. G., B. T. Christensen, N. E. Nielsen, and J. K. Schj0rring. 1993. Ammonia volatilization during storage of cattle and pig slurry: effect of surface cover. J. Agr. Sci. (Camb.) 121:63-71. Sommer, S. G., and J. E. Olesen. 1991. Effects of dry matter content and temperature on ammonia losses from surface-applied cattle slurry. J. Environ. Qual. 20:679-683.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

221

Soper, R. J., and P. M. Huang. 1963. The effect of nitrate nitrogen in the soil profile on the response of barley to fertilizer nitrogen. Can. J. Soil Sci. 43:350-358. S0rensen, J. N. 1992. Effects of catch crops on the content of soil mineral nitrogen before and after winter leaching. Z. Pflanzenernahr. Bodenk. 155:61-66. S0rensen, J. N. 1993. Use of the Nmin-method for optimization of vegetable nitrogen nutrition. Acta Hort. 339:179-192. S0rensen, J. N., and K. Thorup-Kristensen. 1993. Nitrogen effects of non-legume catch crops. Z. Pflanzenernahr. Bodenk. 156:55-59. Stanford, G. 1982. Assessment of soil nitrogen availability. p. 651-688. In: F. J. Stevenson (ed.), Nitrogen in agricultural soils. Am. Soc. Agron., Madison, WI. Steingrobe, B., and M. K. Schenk. 1991. Influence of nitrate concentration at the root surface on yield and nitrate uptake of kohlrabi (Brassica oleracea gongyloides 1.) and spinach (Spinacia oleraeea 1.). Plant Soil 135:205.-211. Steingrobe, B., and M. K. Schenk. 1993. Simulation of the maximum nitrate inflow (1max of lettuce Laetuca sativa 1.) grown under fluctuating climatic conditions in the greenhouse. Plant Soil 155/156:163-166. Steingrobe, B., and M. K. Schenk. 1994a. A model relating the maximum nitrate inflow (I max ) of lettuce to the growth of roots and shoots. Plant Soil 162:249-257. Steingrobe, B., and M. K. Schenk. 1994b. Wurzelverteilung von Kopfsalat und Moglichkeiten der Diingerplazierung sowie N-Bevorratung des Pflanzballens zur Erhohung der Diingereffizienz. Gartenbauwissenschaft 59:167-172. Strebel, 0., W. H. M. Duynisfeld, and J. Bottcher. 1989. Nitrate pollution of groundwater in Western Europe. Agr. Ecosyst. and Environ. 26:189-214. Strebel, 0., H. Grimme, M. Renger, and H. Fleige. 1980. A field study with nitrogen -15 of soil and fertilizer nitrate uptake and of water withdrawal by spring wheat. Soil Science 130:205-210. Su, W., S. C. Huber, and N. M. Crawford. 1996. Identification in vitro of a post-translational regulatory site in the hinge 1 region of arabidopsis nitrate reductase. Plant Cell 8:519-527. Takebe, M., T. Yoneyama, K. Inada, and T. Murakami. 1990. Spectral reflectrance ratio of rice canopy for estimating crop nitrogen status. Plant Soil 122:295-297. Temperli, A., U. Kiinsch, F. Keller, and H. Knijpenga. 1978. Zum Nitratgehalt in Kopfsalat. Schweiz. Landw. Forsch. 17:75-88. Thibaud, J. B., and C. Grignon. 1981. Mechanism of nitrate uptake in corn root. Plant Sei. Lett. 22:279-289. Thompson, T. 1., and A. T. Doerge. 1996. Nitrogen and water interactions in subsurface trickle-irrigated leaf lettuce: I. Plant response. Soil Sci. Soc. Am. J. 60:163-168. Titulaer, H. 1995. In: Control of N supply and irrigation of field grown vegetable crops by computer model and fertigation. p. 42-61. In: Final report EC-project Nil 8001-CT 9120115. European Community, Brussels. Todaro, M. P. 1994. Economic development. Longman, New York. Touraine, B.. B. Muller, and C. Grignon. 1992. Effect of phloem-translocated malate on N0 3 - uptake by roots of intact soybean plants. Plant Physio!. 93:1118-1123. Ullrich, W. R., and A. Novacky. 1981. Nitrate-dependent membrane potential changes and their induction in Lemna Gibba G1. Plant Sci. Lett. 22:211-217. Vanlauwe, B., 1. Dendooven, and R. Merckx. 1994. Residue fractionation and decomposition: the significance of the active fraction. Plant Soil 158:263-274. Vlek, P. 1. G., I. R. D. Fillery, and J. R. Burford. 1981. Accession, transformation and loss of nitrogen in soils of the arid region. Plant Soil 58:133-175.

222

M. SCHENK

Vos, J., and J. Groenwold. 1986. Root growth of potato crops on a marine-clay soil. Plant Soil 94:17-33. Wang, M. Y., A. D. M. Glass, J. E. Shaff, and L. V. Kochian. 1994. Ammonium uptake by rice roots. III. Electrophysiology. Plant Physiol. 104:899-906. Wang, M. Y., M. Y. Siddiqi, T. J. Ruth, and A. D. M. Glass. 1993. Ammonium uptake by rice roots. II. Kinetics of 13NH4 + influx across the plasmalemma. Plant Physiol. 105:1259-1267. Wehrmann, J., and H. Col dewey z. Eschenhoff. 1986. Distribution of nitrate, exchangeable and non-exchangeable ammonium in the soil-root interface. p. 447-450. In: H. Lambers, J. J. Neeteson, and I. Stulen (eds.), Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Martinius Nijhoff Publishers, Dodrecht, The Netherlands. Wehrmann, J., and H.-C. Scharpf. 1979. Der Mineralstickstoffgehalt des Bodens als Mafistab fUr den Stickstoffdiingerbedarf (Nmin-Methode). Plant Soil 52:109-126. Wehrmann, J., H.-G. Scharpf, M. Bohmer, and J. Wollring. 1982. Determination of nitrogen fertilizer requirements by nitrate analysis of the soil and the plant. p. 702-709. In: A. Scaife (ed.), Proc. 9th Intern. Plant Nutr. Coil., Warwick, England. Commonw. Agr. Bur., Farham, Royal Bucks. Welch, N. C., K. B. Tyler, and D. Ririe. 1985. Nitrogen rates and nitrapyrin influence on yields of brussels sprouts, cabbage, cauliflower and celery. HortScience 20: 111 0-1112. Wendland, F., H. Albert, M. Bach, and R. Schmidt. 1993. Atlas zum Nitratstrom in der Bundesrepublik Deutschland. Springer Verlag, Berlin. Westcott, M. P., V. R. Stewart, and R. E. Lund. 1991. Critical petiole nitrate levels in potato. Agron. J. 83:844-850. Westermann, D. T., and G. E. Kleinkopf. 1985. Nitrogen requirements of potatoes. Agron. J. 77:616-621. White, J. N. 1975. Relative significance of dietary sources of nitrate and nitrite. J. Agric. Food Chern. 23:886-891. White, R. E. 1973. Studies on mineral ion absorption by plants. II. The interactions between metabolic activity and the rate of phosphorus uptake. Plant Soil 38:509-523. WHO 1990. Diet, nutrition, and the prevention of chronic diseases. World Health Organization Technical Report Series 797. Wieneke, J., and B. Nebeling. 1990. Improved method for 13N-application in short-term studies on N0 3- fluxes in barley and squash plants. Z. Pflanzenernahr. Bodenk. 153:117-123. Wiesler, F., and W. J. Horst. 1994. Root growth and nitrate utilization of maize cultivars under field conditions. Plant and Soil 163:267-277. Wilcox, G. E., J. E. Hoff, and C. E. Jones. 1973. Ammonium reduction of calcium and magnesium content of tomato and sweet corn leaf tissue and influence on the incidence of blossom end rot of tomato fruit. J. Am. Soc. Hort. Sci. 98:86-89. Wild, A., and V. G. Breeze. 1981. Nutrient uptake in relation to growth. p. 331-340. In: D. E. Johnson (ed.), Physiological processes limiting plant productivity. Butterworth, London. Williams, E. J., G. L. Hutchinson, and F. C. Fehsenfeld. 1992. NO x and NO z emissions from soil. Global Biogeochem. Cycl. 6:351-388. Wodsack, H.-P. 1997. Der Weltmarkt rur stickstoffhaltige Diingemittel. Ernahrungsdienst 51:issue 52 (in press). Wollring, J. 1996. Centre for Plant Nutrition and Environmental Research Hanninghof, DUlmen, Germany.

5. NITROGEN USE IN VEGETABLE CROPS IN TEMPERATE CLIMATES

223

Wollring, J., and J. Wehrmann. 1990. Der Nitratgehalt in der Halmbasis als Mafistab fur den Stickstoffdungerbedarf bei Wintergetreide. Z. Pflanzenernahr. Bodnek. 153:47-53. Wood, C. W., D. W. Reeves, R. R. Duffield, and K. 1. Edmisten. 1992. Field chlorophyll measurements for evaluation of corn nitrogen status. J. Plant Nutr. 15:487-500.

6 Origin and Dissemination of Apricot Miklos Faust Fruit Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, Beltsville, Maryland 20705 Dezso Suranyi and Ferenc Nyujto Fruit Research Station, Cegled, Hungary I. Introduction II. Classification A. Botanical B. Horticultural III. Linguistic Evidence IV. Origin V. Dissemination of Apricot A. European B. Worldwide VI. Conclusion Literature Cited

I. INTRODUCTION

Apricot is considered by many to be one of the most delicious of temperate tree fruits. It has been appreciated and grown for thousands of years on the slopes of mountains in Asia and at least two thousand years in Europe. There are many uses of apricot (Davidson and Knox 1993). It is enjoyed as fresh fruit, but a large portion of the worldwide production is preserved primarily by drying. In China, from the 7th century, apricots were not only dried, but also preserved by salting and even smoking. The black smoked apricots of Hubei were famous. Apricot jam is an important ingredient for the confectioner. It is used as a sweet adhesive in cakes such as Sachertorte and in diluted form as a Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 225

226

M. FAUST, D. SURANYI AND F. NYUJT6

glaze that finishes many confections. In Middle Eastern cookery, apricots are used in sweetmeats, especially in dishes with lamb, such as the so-called mishmishia. Apricots are also pitted and stuffed with almonds or almond paste. In China, the most common apricot grown is thinfleshed-cultivars produced for their seeds. Apricot seeds give the character of the Italian" amaretti di Saronno" and the character of macaroons and biscuits. Dried apricots from Hunza are small but famous, because the Hunza people enjoy remarkable health and longevity and attribute both in part to this fruit. Turkey also produces the so-called apricot leather, dried apricot flesh in the form of thin sheets, which is melted down for its highly concentrated flavor. The flowers ofthe Japanese apricot, mume, are revered for their beauty and mume trees have been increasingly used as ornamentals in Japan since the Nara era (7th-8th century). The use ofmume for medicinal purposes began in the 19th century with the making of a special pickle, ume-boshi, from the fruit, which is believed to be conductive to health. Recently, mume is being used as a drink, the ume-shu, and as juice (Yoshida 1994). Although the apricot is a desirable fruit, apricot production is severely restricted by ecological conditions. Consequently, although apricots are widespread geographically, they have not become pomologically important except in areas where the required ecological conditions (uniformly cold winters, frostless spring, and hot summers) exist (Bailey and Hough 1975; Layne et al. 1996). Relatively few people have worked in apricot research compared with other deciduous fruit crops and few comprehensive reviews have been produced. Notable reviews include those of Kostina (1936), Loschnig and Passecker (1954), Forte (1971), Bailey and Hough (1975), Nyujt6 and Suninyi (1981), Baldini and Scaramuzzi (1982), Mehlenbacher et al. (1990), and Layne et al. (1996).

II. CLASSIFICATION A. Botanical

Apricots occupy a place between plums and peaches. They are graftable onto peach and plum and can hybridize with both species. For more than 17 centuries apricots were considered a form of early peach. Crescentius (1518) described apricot as part of the peach group and not as a separate fruit. Hieronymus Bock (1595) in his Kriiuterbuch wrote about apricots as gelben Sommerpfirsiche (yellow summer-peaches), Turner (1551) called apricot a "hasty peche tre," and according to Loeschnig and Passecker (1954), Maaler, in 1561, referred to apricots as "kleine,

6. ORIGIN AND DISSEMINATION OF APRICOT

227

fruhzeitige Pfersich" (small, early peach). Bauchin (1560-1624) in his Krauterbuch, published in 1687, well after his death, was the first to designate apricot as a separate fruit species. Tournefort (1700), court botanist to Louis XIV and creator of Latin names for almost 200 well known fruit cultivars, separated apricot from peach and classified it as a separate genus, naming it Armeniaca. Linnaeus (1737), even before establishing his binomial system, included apricot with cherries and plums in the genus Prunus. For apricot he used the name Prunus foliis ovato-cordatis, but recognizing Tournefort's prior use of Armeniaca, listed Malus armeniaca and Armeniaca malus as synonyms. Today, we consider that apricots belong to the Rosaceae, subfamily Prunoideae, genus Prunus L., subgenus Prunophora (Neck.) Focke, section Armeniaca (Mill.) Koch (Rehder 1940). Prunophora (apricots and plums) is the subgenus in which leaves in the bud are rolled up, convolute, showing well as the leaves begin to emerge from the bud (Bailey 1927). In the apricot section, there were several species recognized in earlier classifications, but recent taxonomists reduced the number of species, indicating that the differences between some previously described species and P. armeniaca are insufficient to maintain their species status. Thus, Wilson, during his exploration in China in 1907-1909, found it impossible to separate species by the shape or pubescence of the leaves. Leaves were more densely pubescent in young plants of P. sibirica, P. armeniaca and P. mume than in older plants in which the pubescence more or less disappeared (Sargent 1988). Consequently, several former species have became classified as botanical varieties within P. armeniaca (Bailey 1927). Presently, recognized species in this group are: P. armeniaca, P. mume, P. brigantica, P. dasycarpa, and P. holocericea. The existence of P. holocericea is still questioned, and P. brigantica may belong to plums. The brief descriptions of these species are as follows: 1. P. armeniaca, L. [Syn. Armeniaca vulgaris Lam.; P. armeniaca var typica Maxim.; P. tiliaefolia Salisbury) is known as common apricot (Fig. 6.1). Small tree with reddish bark up to 10-15 m in height. It is drought resistant and if dormant it is winter hardy. Leaves are large, ovate or round-ovate, sometimes slightly cordate at base, abruptly pointed, glabrous, closely serrate, the petioles are stout and gland bearing. Flowers are white or pink, solitary, appearing from lateral buds of last year's shoot. They open before the leaves. Fruit are variable, somewhat flattened, mostly yellow or whitish, overlaid more or less with red. The fruit of wild specimens ranges from 3 to 20 g, cultivated selections produce fruit 40 to 50 g, and exceptionally large types have fruit up to 100 g. The stone is somewhat flattened and smooth, ridged and sulcate on the edge.

228

Fig. 6.1.

M. FAUST, D. SURJ\NYI AND F. NYUJT6

P. armeniaca, wild specimen (from L6schnig and Passeker 1954).

Throughout the years there was some controversy about types closely related to P. armeniaea. As indicated above, the differences appear to be limited or inconsistent for clear definition and Bailey (1927) reduced the number of species and retained the previously described species as botanical varieties. P. armeniaea var. sibiriea Koch; [Syn. P. sibirea L.; Armeniaea sibiriea, Pers.; Armeniaea sibiriea (L.) Lamark; Armeniaea var. sibiriea Koch.; Armeniaea davidiana Carriere] is known as Siberian apricot (Fig. 6.2). Bush or small tree. Leaves are small and glaborous, sometimes sparingly bearded beneath, ovate or rounded, long pointed, unequally crenateserrate. Flowers are white or pink, appearing early in the spring and usually in great profusion. Fruit is rarely more than 12 mm in diameter, yellow with a reddish cheek, practically inedible. Stone is smooth and very sharp edged. P. armeniaea var. mandshuriea Maxim. [Syn. P. mandshuriea Koehne; P. mandshuriea (Koehne) Skvortzoff; Armeniaea var. mandshuriea Maxim.; Armeniaea mandshuriea (Maxim.) Skvorzt.: P. mandshuriea (Maxim.) Koehne] is known as Manchurian apricot (Fig. 6.3). Large tree,

6. ORIGIN AND DISSEMINAnON OF APRICOT

Fig. 6.2.

229

P. armeniaca var. sibirica (Kostina 1936).

up to 20 m high. Shoots are smooth, green or light brown. Leaves are large, subcordate or cuneate at base, at apex long-cuspidate and acute, margin strongly double toothed, the serrations sharp and twice longer than wide. Flowers are large, white or pink, open before the leaves. Fruit nearly globular, about 25 mm long, yellow, red-spotted, succulent and sweet, stone small and smooth, the margin obtuse, the seed is sweet. The tree is very hardy. Its flowering period is extended, with the earliest flowers subject to spring frosts. P. armeniaca var. ansu (Maxim.) Kost. [Syn. P. ansu (Maxim.) Komarov; Armeniaca ansu (Maxim.) Kost.; P. armeniaca var. ansu Maxim.] is known as Ansu apricot (Fig. 6.4). Tree is bush-like. Leaves are broadelliptic, at base short-cuneate, at apex acuminate, very glabrous, the margins crenate-serrate. Flowers are twin, pink, open very early. Fruit is subglobose, deeply umbilicate or sulcate, red, tomentose, the flesh is

230

Fig. 6.3.

M. FAUST, D. SUMNYI AND F. NYUJT6

P. armeniaca var. mandshurica (Kostina 1936).

grayish brown and sweet and free from minutely reticulated stone which has only one sharp edge. Its wild form is not known. Cultivated in China, Japan, and Korea in areas where the winter is mild.

2. P. mume Sieb. & Zucco (Syn. Armeniaca mume, Sieb; P. mume var. typica Maxim.; P. armeniaca Thunb.). Japanese apricot (Fig. 6.5). Tree of dimensions of common apricot but the bark greenish or gray and the foliage is duller in color. Leaves are relatively small, narrow-ovate to nearly round-ovate, long-pointed, finely and sharply serrate, more or less scabrous, and lighter colored beneath. Flowers are sessile or nearly so and fragrant. Fruit is smaller than of P. armeniaca, yellow or greenish, the dry flesh adhering to the pitted stone.

6. ORIGIN AND DISSEMINATION OF APRICOT

Fig. 6.4.

231

P. armeniaca var. ansu (Kostina 1936).

3. P. brigantica VilI. [Syn. Armeniaca brigantica (VilI.) Persoon; P. Armeniaca subsp. brigantica Dipp.] is known as alpine plum. Small thornless tree or shrub, with mostly small leaves and small smooth subacid fruit the size of small green-gage plum. Leaves are broad-oval or ovate, the blade 50-75 mm long, abruptly short and pointed, very sharply serrated, above glabrous or essentially so, beneath lighter colored. Flowers are light pink, they appear in clusters of 2-5, blooms after leafing. Flesh is white. The fruit is round, yellow and plum-like but scarcely edible. In France, the kernels were used to produce the huille des marmottes, an oil considered superior to olive oil (Downing 1862). It is native in Gallia (France) in a very small area on the south-western slopes ofthe Alps. 4. P. dasycarpa Ehrh. [Syn. P. armeniaca var. dasycarpa Koch.; Armeniaca dasycarpa (Ehrh.) Pers.; Armeniaca dasycarpa Ehrh.; Armeniaca

232

Fig. 6.5.

M. FAUST, D. SURANYI AND F. NYUJTO

P. mume (Kostina 1936).

dasycarpa Borkh.; Armeniaca nigra Desfon.; Armeniacafusca Tourp. & Rit.; Armeniaca atropurpurea Loison; Armeniaca persifolia Loison.J, known as purple or black apricot, produces a small tree. Leaves are small and narrow, mostly elliptic-ovate, finely and closely serrated, thin and dark green. Petioles are slender, and nearly or quite glandless. Flowers are large and long stalked, showy. Fruit is globular and plum-like, dark purple, the flesh is tart and soft, stone is fuzzy. This apricot with dark purple velvety fruit is cultivated in Kasmir, Afghanistan, Baluchistan, and in Europe (Brandis 1874; Kostina 1936; Loschnig and Passeker 1952). It is considered a generic hybrid between apricot and plum (P. armeniaca x P. cerasifera) (Kostina and Riabov 1959) and as a result it has been also named as Armenoprunus ]anchen. It is mostly self sterile (Nyujt6 and Suranyi 1981). 5. P. holocericea Batal. [Syn. Armeniaca holocericea Batal.; Armeniaca holocericea (Batal.) Kost.; Prunus armeniaca var. holocericea (Batalin)] is known as Tibetian apricot (Fig. 6.6). Tree is 4-5 m tall, leaves are large, its short petioles and veins are pubescent. Fruit is pubescent, stone is round and seed is bitter. Few trees of this species were found by a Russian explorer in the 19th century between Batang and Litang in the west-

6. ORIGIN AND DISSEMINATION OF APRICOT

Fig. 6.6.

233

P. holocericea (Kostina 1936).

ern part of Sichuan Province of China. Its existence as a species should be questioned. Some morphological variants of apricots have ornamental values and have been given the subspecific designation of forma (t). These are summarized by Terpo (1974) as: f. pendula Dipp. or pendula (Jag.) Rehd. with hanging or pendulous twigs; f. variegata Hart. or variegata Schneid. with variegated leaves; f. ovalifolia ser. with egg-shaped leaves; and f. cordifolia ser. with heart-shaped leaves. Botanists also recognized the variability of the fruit of P. armeniaca and distinguished several subgroups based on fruit characteristics as convariants (Conv.). These are: Conv. minor Schub!. & Mart., fruit is small, bitter and acidic, seed is mostly bitter; Conv. vulgaris Schubl. & MarL, fruit is large, with sweet mesocarp, juicy, seed is bitter or sweet; Conv. dulcis Schub!. & Mart., fruit is large and wide with red cheek, seed is sweet;

234

M. FAUST, D. SURANYI AND F. NYUJT6

Conv. persicoides Pers., fruit is flat, seed is bitter. This botanical classification has only limited usefulness as it was based merely on fruit size and sweetness or bitterness of the seed and does not take into account the ecological conditions, tree types, chilling requirements of the tree, adaptation to dry conditions and other important considerations. Among the apricot types one has to mention the apricot plum, the cotplum, and the plumcot. Apricot plum P. Simonii Carr (Syn. Persica Simonii Decne), was named for Eugene Simon, who sent pits from China to France prior to 1872. Botanical position on the genus is doubtful, as it has some characters of apricot and those of plums (Bailey 1927). King (1939) studied several cotplums that were supposedly hybrids of P. armeniaca and P. salicina. Based on chromosomal configuration, he accepted these as true hybrids. Rolin and Blanet reported P. cerasifera hybrids with apricot in 1755 (Loschnig and Passecker 1954). Giorgio Gallesio in his Pomona Italiana illustrated an albicocca susina (cotplum) in 1817 (Baldini and Tosi 1994), which is probably the first illustration of such hybrids (Fig. 5.7D). Luther Burbank produced plumcots by crossing P. salicina and P. armeniaca. In 1909, he had as many as 55 to 75 thousand plumcot seedlings, and in a letter to V.P. Hedrick, indicated that there were no pure apricots or pure plums among the seedlings, but every possible variety and every possible combination was observed and all qualities were strongly expressed (Hedrick 1911). The first plumcot introduced from Burbank's crosses was 'Ruthland', introduced by George C. Roeding in 1907. The fruit was the size of an ordinary apricot with a deep purple-velvety skin, with brilliant red flesh and a pleasant sub-acid apricot-plum flavor (Wickson 1914). There are also hybrids between P. mume and apricot, the Bungo-ume, or between P. mume and plum, called Sumomo-ume (Yoshida 1994). Mehlenbacher et a1. (1990) list several other species combinations, apricot x almond, several plum species x apricot, and peach x apricot. B. Horticultural

A large percentage of the world's wild apricots have a very thin flesh, and because of this the fruit is not eaten and only the seed is utilized. In contrast' some types have thick flesh and are highly desirable as fruits. In addition, the color and consistency of the fruit varies along with its shape. Because of the varied character of the fruit, apricot types have been classified from the horticultural point of view. The first known horticultural classification was done by Gian Battista Della Porta about 1500. He divided the apricots into two groups: bericocche and chrisomele (Forte 1971). The bericocche fruit was round, with soft, whitish flesh, and

6. ORIGIN AND DISSEMINATION OF APRICOT

A

235

8

D

Fig. 6.7. Illustrations of apricots in Giorgio Gallesio's Pomona ItaJiana, 1817. (A) 'AlbicDcca di Germania', note the large size and the dark yellow color of the fruit compared with the pale color of C, and the small size of Band C. Fruit sizes can be compared because leaf sizes in all three pictures are about the same. (B) Albicocca lucente, (C) Albricocca di Sardegna, (D) AlbicDcca susina plum-like leaves typical of cotplum hybrids. Compare the leaves with apricot leaves shown in A, B, or C. The fruit is intense red.

236

M. FAUST, D. SURANYI AND F. NYUJTO

OJ the


J brttock! tree.

J L/.fmuni4c.• m,tl~! maior.

Thegrcl1tcr Apiccocke Hce.

Fig. 6.8.

2 Armm;414m4Imm;'w'.

The letTer Aprecocke tree.

Apricots illustrated in Gerard's Herball, 1633.

its seed tasted somewhat like almond. The chrisomele group had yellow aromatic fruit, firm flesh, and sweet seeds. The name mele d'oro (golden fruit) was also used for this group. Gerard (1633) also distinguished two groups, the greater and lesser abrecocke trees (Fig. 6.8), which differed in fruit size and quality. Later, Dochnahl (1860) classified the apricot cultivars into 4 groups: (1) Dasycarpa, red fruit, bitter seed, long pointed leaf; (2) Alberga, small yellow fruit, early, bitter seed, small leaf; (3) Chrisomera, large fruited, yellow fruit with some red, bitter seed, large leaves; and (4) Marilla almost like Chrisomera but with sweet seed. The Royal Horticultural Society also attempted to classify the apricots. This classification was based on (1) the size of the flower (small or large); (2) color of the fruit (pale, deep yellow, red, orange, or magenta); (3) pores on the suture of the seed (pore size is smaller or larger than a needle can go through); and (4) taste of the seed (sweet or bitter) (Nyujto and Suninyi

6. ORIGIN AND DISSEMINAnON OF APRICOT

237

1981). Hogg (1875) reworked the previous classifications with minor modifications, but his system has never been accepted. During this century' Kostina (1936), Mandy (1949), and Loschnig and Passecker (1954) also made attempts to classify apricot cultivars. From 1928 to 1938, Kostina and others made an effort to collect apricots from all geographical regions. After examining 700 accessions, Kostina (1936) developed a classification system based on the following characteristics: (1) seed is sweet or bitter; (2) fruit skin is smooth or pubescent; (3) fruit is freestone or clingstone; (4) fruit flesh is white to cream colored, or yellow to orange; and (5) fruit is small, medium size, or large. From these she identified 48 basic combinations. Kostina (1969, 1970) also distinguished four major eco-geographical groups within the common species of P. armeniaca. These are: (1) Central Asian group including areas around Fergana, the Zerevshan mountains, Samarkand, and the Kopet-dag (a mountain range in northern Iran). This group is the oldest and the richest in diversity of forms. It includes selections from central Asia, Xinjiang (China), Afghanistan, Baluchistan, Pakistan, and northern India. Trees are vigorous, long-lived, and late blooming. Trees are adapted to a dry atmosphere but are sensitive to lack of soil moisture. Fruit is small, has a sweet kernel, and is excellent for drying. Cultivars ripen from May to September. The succeptibility of trees to diseases limits their planting in humid areas (Bailey and Hough 1975). (2) frano-Caucasian group comprised of the Irano-Caucasian area and Dagestan (western shore of the Caspian Sea) and includes local selections from Armenia, Georgia, Azerbaijan, Dagestan, Iran, Syria, Turkey, and North Africa. Trees of this group are not as vigorous and long lived as those of the Central Asian Group. Trees are less winter hardy and begin to grow earlier in the spring. The kernels are sweet. Fruit is larger than of those of the Central Asian Group and the flesh is often white or light colored. (3) European group including types in Western Europe, Eastern Europe, and zerdeJi or Ukrainian type. This group is the youngest in origin and the least variable. It originated from relatively few forms which, in the opinion of Kostina, were brought to Europe from Armenia, Iran, and the Arab countries during the past 2000 years. (4) Dzhungar-Zailij group, which is considered the most primitive group and located north of Almaty (Alma Ata) and the Tien-Shan mountains. This group includes selections from Panfilov (Dzharskent), Taldy-Kurgan, and Almaty (Alma Ata) regions of Kazakhstan and from Ining (Kuldja) of Xinjiang. These trees have great winter hardiness, withstanding -30°C and are small fruited types. Kostina (1970) further subdivided the European group into WestEuropean (most western European and North American cultivars belong

238

M. FAUST, D. SURANYI AND F. NYUJT6

here), East-European (cultivars of Bulgaria, Romania, Moldavia, and south Ukraine belong here), and North-European (mostly zerdely type seedlings adapted to the northern area of apricot production). Thus, Kostina made a definite distinction between the West-European types and any other apricots. This distinction seems to be important and will be discussed later. Paunovic (1970) modified Kostina's classification, creating five groups: (1) Central Asian, (2) Asian-European, (3) European, (4) American, and (5) African groups. His reasoning was that the international use of cultivars in the case of apricot is not uniform compared with the more uniform use in other fruits because the adaptability of apricots to environmental conditions is much less compared with other fruits. Bailey and Hough (1975) also proposed that a North African group should be added to Kostina's grouping, including types grown in North Africa, Tunisia, and in the oases south of the Atlas Mountains. Apricots in these areas have low chilling requirements and are well adapted to climates with mild winters, which makes them a distinct group. It is relatively easy to classify those groups of cultivars that were introduced from a closed production area and grown in a distinct valley or an oasis. It is more difficult to classify the European cultivars that have varied origin and have been selected for the best performance in a given area (Nyujto and Suninyi 1981). The difficulty in classifying the European types is clearly manifested in all classifications concerning this group. The classification somewhat reflects the origin of these cultivars. Kovalev (1970) considered only two ecotypes of the European apricot: (1) the southern European and (2) the east European types. Nyujto and Suranyi (1981) divided the European group into southern or Mediterranean and continental types. From these classifications it is clear that most authors separated the southern and northern type European cultivars, and separated these from the other apricot groups. None of the classifications was concerned with the P. armeniaca forms of China, especially those found in Shaanxi and Gansu Provinces. In these provinces, apricot fruit varies from small to medium, the flesh from whitish to intense yellow, the ripening period from early June to the end of August and the kernel generally sweet. Yuan and Du (1983) described 86 forms from Shaanxi. Some of these are illustrated in Fig. 6.9. and show the remarkable variability of the species. Zhang and Liu (1995) recorded that wild types may have large fruits up to 71 g in the same geographic region. Because classification based on fruit characteristics frustrated horticulturists, Mandy (1949) attempted to classify apricots based on their leaves and found larger differences based on leaves than on fruits. He

6. ORIGIN AND DISSEMINATION OF APRICOT

Fig. 6.9.

Types of apricots found in Shaanxi Province of China.

239

240

M. FAUST, D. SURANYI AND F. NYUJT6

considered the length of the petiole (20-40, 41-55, or 56-70 mm long); the shoulder of the leaf, the size of the leaf «40,41-60, or 61-80 cm 2 ), serration of the leaf edge, and the tip of the leaf (short <10, medium 11-15, and long 16-20 mm). Nyujto and Suranyi (1981) used this system to identify 43 cultivars. During the Turkish occupation of Central Europe (1510-1680), many apricots were brought into the region and most of them were propagated by seed. As a consequence, cultivar groups somewhat similar to land races have developed. These cultivar groups or land races, common in Hungary, are the basis of Nyujtb's classification (Nyujt6 and Suranyi 1981), as shown in Table 6.1. Even in relatively recent times, apricot breeders have found horticultural classification useful because each group carries certain adaptability characteristics. Smikov (1983) attempted to fit 853 existing apricot cultivars according to the major classification groups of Kostina. He found that 416 cultivars belonged to the middle Asian subgroup, of which 110 were clearly Fergana types and 72 were types found in Kopet Dag. Only 5 cultivars belonged to the Irano-Caucasian group, while 232 cultivars belonged to the European group, of which 152 were West European, 40 East European, and 30 were zerdeli types. About 200 local cultivars belonged to the Dzungar-Zaily group. Finally, Mehlenbacher et al. (1990) list cultivars with characteristics important to apricot producers and apricot breeders. Their list of cultivars is not a classification but merely a recognition of cultivars with climatic adaptation, resistance to various diseases, suitability for processing, tree growth habit, and harvest time. From the above discussion, it is obvious that it is not simple to classify diverse groups of apricot cultivars. In fact, Tomcsanyi (1979) recognized that with the introduction of new cultivars, derived from diverse groups, conventional thinking in terms of established categories in apricot classification is no longer possible. Even though there are several groups of apricots, only a few cultivars are broadly adapted in each ecological area. Mehlenbacher et al. (1990) listed cultivars with wider adaptation only as exceptions: 'Canino', that grows in several Mediterranean countries, and 'Hungarian Best', that grows throughout central and eastern Europe under various names. In addition, the authors consider 'Nancy', a Hungarian type, and its descendants ('Royal', 'Blenheim', and 'Moorpark') are adapted well beyond their place of discovery in California and at the Cape of South Africa. Local adaptation, which has been, and still is, the major concern for each breeding program, makes classification not only difficult, but pointless, because the ecological adaptation overrides any other characteristics of the fruit when large-scale production is concerned.

6. ORIGIN AND DISSEMINATION OF APRICOT Table 6.1.

241

Characteristics of Hungarian apricot cultivar groups. (Nyujt6 and Suranyi

1981.)

Cultivar group (land race) "Hungarian" apricot Rose apricot

Characteristics Favorable

Unfavorable

High quality fruit, yellow flesh color, adaptable to poor soils, self fertile Hardy, excellent transportability, productive, machine harvestable, firm flesh, self fertile

Short winter dormancy, alternating production, extended maturity, apoplexia z and Monolinia sensitive Tends to overcrop and produce small fruit, flesh is often mealy, not precocious, sensitive to MonoJinia Poor self fertility, blooms too early, sensitive to frost, sensitive to MonoJinia, flesh softens quickly Short dormant period, blooms too early, bloom is frost sensitive, develops blind wood, occasionally sensitive to apoplexia z and Monilinia Small, soft fruit, extended maturity period, self sterile Occasionally produces small fruit, Monolinia sensitive, occasionally sensitive to apoplexia z Frost sensitive, fruit softens slowly, fruit remains green at suture Elongated, almond shaped fruit, trunk is sensitive to canker

Giant apricot

Large fruit, good fresh fruit quality, precocious, early maturing

Cardinal apricot

High quality, large attractive fruit, excellent productivity, produces fruit also on secondary shoots

Early Red

Very early maturity, productive, relatively resistant to apoplexia, long dormancy, tolerant to cold Productive, well shaped and high quality fruit, attractive color, well developed canopy, self fertile Large, attractive fruit, uniform productivity. small canopy, self fertile Attractive fruit, very firm flesh, excellent for machine harvesting, long rest period

Rakovszky

Cegledi Dawn-Red Almondapricot

ZDisorder involving sudden wilting and death.

III. LINGUISTIC EVIDENCE The name of apricot (albicocco, albericocco, albricooco) was apparently derived from the combination of Arbor precox from the latin praecocia ("precocious") because of its earliness (Guerriero 1982). Columella

242

M. FAUST, D. SURANYI AND F. NYUJT6

(about 50 A.D.), the first who mentioned apricot, used the expression Armenian apple, Armeniisque, in his work De Re Rustica. Pliny (79 A.D.) used the word praecocia in his Historia naturalis as an occasional designation for Pomum armeniaum or armeniaca arbor. Praecoquum, a variant of praecox pI. praecocia, means ripen early, ripe in summer, premature, precocious. Discorides (around 60 A.D.) called it maiJon or armeniacon (De Candolle 1886). Several authors (Kostina 1936; Loschnig and Passecker 1954; Blaha et al. 1966; Goor and Nurock 1968) assumed that the English word apricot was derived from praecocia. Distinction has been made between the early ripening "fruit," apricot, and the later ripening "fruit," peach. Turner (1551) called apricot "abrecock or hasty peche tre." He remarked: "The hasty peche tre hatch much broader leves then the peche tre and hys fruite is a greate tyme sonner rype then the peche is." Groups of words used for naming P. armeniaca include: (1) kaysi (Turkish), (2) zerdeli (Persian), (3) Arbor-precox (Latin), and (4) Marille (German). Depending on the dissemination of apricot, a given language may use the derivatives of more than one of the basic words depending on whether the apricot is seed propagated or grafted. Kaysi is an Ottoman-Turkish word that originated from Pontus (Roman territory in northern Turkey). The local name of apricot in Ukraine is zserdelj or zerdeli, which stems from the Persian word zardalju meaning yellow plum. The Turkish and Persian words are occasionally mixed and include Turkish kaysi (grafted cultivars), kuruk (dried halved fruit), kuraga (dried fruit with seed); Tatar: kajszi (grafted cultivars), zerdaJe (propagated by seed); Bulgarian: kajszija (grafted cultivars), zalazar, or zalzar (propagated by seed); Romanian: cais, caisi, caisa; Croatian: kajsija; Albanian: kajsi; and Hungarian: kajszi. Apparently the seed-propagated apricot was not the same quality as the grafted trees, and was so recognized by the Persian word in Tatar and Bulgarian designation of seed-propagated apricots. The names derived from the Latin Arbor-precox include the Arabic: al-barquq (tree), al-bareue, albarquq, and mish-mish (fruit); Italian: albicocco, albericocco; Spanish: albaricoque; Portugese: albricoque; French: abricot (fruit), abricotier (tree); German: Aprikose (fruit) and Apricosebaum (tree); Dutch: abrios; Danish/Swedish/Norwegian: abrikos; Finnish: aprikoosi; Russian: abrikos; and the English: apricot, and apricot-tree. The Italian albicocco and the English apricot were used in many forms in the past. The Italian forms include for the tree: albicocco comune, albercocco, pesco armenico, meliaco, umiliaco, armellino; and for the fruit: albicocca, albercocce, armeniache, pesche armeniche, meliache, armellini, umiliache, moniaca, biricoccola (Tamaro 1901). The

6. ORIGIN AND DISSEMINATION OF APRICOT

243

past English forms include: abrecok, aprecox, abrecock, apricok, aprecock, abricot, abrycot, abricoct, apricote, and aprecott. Murray (1888) gives a number of various uses of the word apricot. Some of his examples are notable and repeated here because they illustrate the use of apricot in the 16th to 18th centuries. In 1551, Turner wrote "Abrecockes ... are less than the other peches"; in 1573-80, Tusser remarked "Of trees or fruites to be set or removed: apple trees ... apricockes."; in 1578, Lyte recorded that "There be two kindes of peaches.... The other kindes are soner ripe, wherefore they be called abrecox or aprecox"; in 1601, Holland reported that "Abricots are ready to be eaten in summer"; in 1617, Rider remarked about "an abricot apple"; and in 1718, Chamberlayne gave instruction: "If an abricot be grafted upon a plumb ... " The word "apricot" was used since Richard Bradley's time in 1739 (Bradley 1739). Names derived from South-GermanIAustrian include Marille or Malede; Czech: merunka; Slovanian: marulica; Polish: morela; Slovakian: marhule. Kluge and Gotze (1934) remarked that old expressions of Marille included Morling, Morich, Mollelein, or Molleten. He also thought that the Schwabish Mollele originated from ammarelle. Guerriero (1982) mentions that the Latin name of apricot, albicocco, was not generally used throughout Italy in Roman times. The Roman dialect used maniaga or magnaga and a Tuscan dialect armelliano, all probably stemming from the word armeniaca. Thus it is conceivable that the basis of the German Marille or Malede originated from armeniaca through linguistic transformations. A lengthy discussion on this word can be found in Loschnig and Passecker (1954). The Chinese xing or hszin, the Japanese anzu, and the Armenian Giran (reddish-yellow) or sziranen are different and do not correspond to any of the above words. According to Lindqvist (1991), the Chinese symbol, 4', is composed of idioms of an open mouth under a tree, which can be found in many names indicating locations (Fig. 6.10). The identity of the fruit known by the Hebrews as tappuah (Proverbs 25:11; Song of Solomon 2:3,7:8,8:5) is unclear. In most English translations of the Bible tappuah is translated as "apple" since linguistically it corresponds closely to the Arabic tuffah (apple). According to Hepper (1992), the other candidate for tappuah is the apricot. Apricots could have been grown in the area and tappuah was used as a place-name for localities where the fruit must have been important. The fragrance of tappuah is referred to in the Song of Solomon 7:8 and its sweetness in 2:3, both characteristics attributable to apricot. Hepper (1992) thinks that when Solomon wrote that "A word fitly spoken is like apples ofgold in a setting of silver" (Proverbs 25:11) the king was referring to apricot.

244

M. FAUST, D. SURANYI AND F. NYUJT6

Fig. 6.10. Locations in China with apricot in their name: (a) Xingzsen. (b) Xinghaj, (c) Xinghxinghxia, (d) Xingtaj, (e) Xinglung, (f) Xinghajlien, (g) Ansu (North Korea), (h) Xinghua. (i) Xingan, (j) Xingji.

IV. ORIGIN The history of apricot goes back at least 5000 years in China and 2000 years in the western world. De Candolle (1886) places the origin of apricot in China. According to an account attributed to Emperor Yu (2205-2198 B.C.), the apricot was cultivated in China in his time (Roach 1985). However, Sun et a1. (1983) remarked that the Book of Odes ("Shii Ching," an anthology of verses written between the 11th and 6th centuries B.C., does not mention apricots but contains poems about peaches, plums, pears, hazelnuts, chestnuts, and jujubes. Nevertheless, apricot was known in China in 658 B.C. and superior apricot orchards existed there in the period 406-250 B.C. (Nyujt6 and Suranyi 1981). Later books not only mention apricot but verses were written about this fruit by Li taj-po (701-762) and Po Csii-ji (772-846). Chinese painters used apricot as a favorite subject (Fig. 6.11). Grafting of apricots began in China about 600 A.D. and defined cultivars developed after this time (Nyujt6 and Suranyi 1981). Laufer (1919) identified Sogdiana (ancient name for the area around Samarkand) as the place apricot was native. Jeszejan (1977), an Armenian, naturally described Armenia as the native location of apricot. He based his conclusions on the fact that apricot culture had a long history in Armenia, especially in the area of Yerevan. Apricot seeds from about

6. ORIGIN AND DISSEMINATION OF APRICOT

245

Fig. 6.11. Apricot blossoms painted by a Southern Song Dynasty academic painter, Ma Yuan (ca. 1160-1225). Painting exemplifies the "broken branch" convention focusing on a corner of nature rather than on a broader landscape. In upper right is the writing of Empress Yang Mei-tzu-"meeting the wind, they offer their artful charm; moist with dew, they boast their pink blossom."

3000 B.C. have been discovered at Sengevit and at Garni (both near Yerevan), but in the opinion of Aralkeljan (1951), a noted archeologist, the fruit form that these seeds have originated was brought into Armenia rather than produced there. De Candolle (1886), reviewing the available data on wild apricots in Armenia, stated that several qualified travelers, including Karl Koch, who traveled extensively in Armenia and the Caucasian mountains, did not find wild apricots there. The apricots these travelers found were all cultivated or escapes from cultivation. Based on this information, De Candolle concluded that apricot was not native in Armenia. Apricot seeds were found from a later period at the excavation of Karmir Blur (a fort near Yerevan) from the 8th century B.C. (Arzumanjan 1970). Still later, in the first century A.D., large apricot

246

M. FAUST, D. SURANYI AND F. NYUJT6

plantations existed around Echmiadzin (near Yerevan) that were cultivated by Armenian monks (Timko 1971). Vavilov (1992) included the cultivated apricot into three of his centers of origin. The centers important for apricots are: (1) the Chinese Center, including northeastern, central, and western China as far as Gansu Province, and northeastern Tibet; (2) the Central Asian Center, the mountain area extending from the Tien-Shan south, through the Hindu Kush to Kashmir; it includes Afganistan, Tajikistan, and Uzbekistan; (3) the Asia Minor Center, the mountains of north-eastern Iran to the Caucasus and Central Turkey and Turkmenistan. Vavilov considered the Asia Minor Center to be the secondary center of origin of cultivated forms. Crossa-Raynaud (1960) and Guerriero (1982) placed the origin of apricot in middle Asia, which corresponded to Vavilov's Central Asian Center and thought that apricot moved both east and west (Fig. 6.12). Consequently, if one accepts this theory, the Chinese Center of Vavilov also would become a secondary center of origin for apricot similar to the Near Eastern Center. However, the Siberian and Manchurian apricots are sufficiently different from the common apricot so that the Chinese Center of origin, as Vavilov contemplated it, may be the actual one. The geographic area of each apricot type, as far as the botanical variety is concerned, is well described. The common apricot, P. armeniaca, is native in the Fergana area, the Hindu Kush, Kopet dag, and Armenia extending to Dagestan to the west and across the Tarim basin to Shaanxi and Gansu to the east (Fig. 6.13).

~

ft

'\

\. ...

Fig. 6.12.

,-

Distribution of apricot from the Central Asian Center of Vavilov.

6. ORIGIN AND DISSEMINATION OF APRICOT

247

Fig. 6.13. Geographic distribution of apricot species in Eastern Asia. (1) P. armeniaca; (2) P. armeniaca var. sibirica; (3) P. mume; (4) P. armeniaca var. mandshuriaca; (5) P. holocericea.

The Siberian apricot, P. armeniaca var. sibirica Koch, is located in northern China. Its northern limit is around the 50° latitude. It can be found in eastern Siberia in the valley of the Ussuri River, on the steep slopes of the Kinghan mountains dividing China and Siberia and on the slopes of mountains extending as far south as Beijing. The Siberian apricot extends westward across Manchuria and continues north and south of the Gobi desert; to the north, it occurs as far west as the valley of the Selenge River, while to the south, it extends through the mountains of Inner Mongolia and northern China as far west as the northern loop of the Yellow River (Fig. 6.13). Its native area is the largest compared to the other apricot types, and can be found in the second canopy level of the forest together with rhododendrons, mespilus, and Siberian apple. The Manchurian apricot, P. armeniaca var. mandshurica Maxim, is found in eastern Manchuria and Korea, essentially east of the Siberian apricot (Fig. 6.13). It occurs on sunny slopes in groups of trees or mixed among other tree species. The ansu apricot, P. armeniaca var. ansu (Maxim.) Kost., is a species that is cultivated in warm, humid areas of east China. There is approx-

248

M. FAUST, D. SURANYI AND F. NYUJT6

imately 1000 mm of rain and high (30°C) temperatures in this area (Gu Mo 1988). The Japanese apricot, P. mume, is also a native of China. It was introduced to Japan approximately 2000 years ago, utilized as a garden tree since the Nara era (7th to 8th century), and its breeding for ornamental use began in the Edo era (17th to 19th century). It is the southernmost species of apricots. It can be found in southern Gansu, Hubei, Sichuan, and Hunan provinces (Fig. 6.13). It is a relatively lowland species, at home in gravelly soils up to 200 m elevation. Wherever native, apricot is considered a fruit of mountainous areas (Layne et a1. 1996), with the exception of the ansu apricot. In China, Middle Asia, or the Caucasian region, apricot trees are always native on high mountains. Wild forms of P. armeniaca are found on the western slopes of the Tien Shan mountains and on the north-western slopes of the mountains around Fergana in dry, stony soil, up to 1200 to 1400 m, in the Shigar valley 2500 to 2800 m high, and near Ascole at 3650 m (Casini and Neri 1964). Frank Meyer, an American plant explorer also collected apricots at 1400 m altitude in the Tien Shan mountains (Vavilov 1992). In Turkestan, apricot is found between 1200 and 2200 m and in Manchuria near the south-eastern Mongolian border at 3000 m above sea level (Forte 1971). The origin of apricot in mountainous regions may have a special significance. In general, chilling requirement, as an evolutionary attribute, is believed to have developed to prevent premature sap flow and dehardening processes in climates with fluctuating winters. Species that originated in very cold climates, occurring usually at high mountain tops, or on the fringes of fruit growing to the north, had no need to develop a high chill requirement as a protective system because most of the winter was cold enough to compel dormancy throughout the freezing period. Therefore, it is likely that the medium-chill-requiring apricot types developed on mountain tops in the Fergana or other sufficiently cool areas, and were subsequently moved to Africa, creating the low-chillrequiring types of apricots.

IV. DISSEMINATION OF APRICOT A. European The name armeniaca may indicate that apricot came to the western world from Armenia. Unger (1859) thought that Alexander the Great (356-323 B.C.) brought the apricot from Armenia to Greece and Epirus (Albania), from which countries it reached Italy. However, apricot appar-

6. ORIGIN AND DISSEMINATION OF APRICOT

249

ently was unknown to the Greeks at the time of Theophrastus (327-287 B.C.), a contemporary of Alexander the Great (De Candolle 1886). Similarly, Roman authors including Cato (234-149 B.C.), Varro (116-27 B.C.), and Vergilius (70-19 B.C.), writing about agricultural subjects, did not mention apricot (L6schnig and Passecker 1954). However, it was mentioned as Mela armeniaca (Armenian apple) by later authors, such as Discorides (around 50 A.D.) and Columella (around 50 A.D.) indicating that it may have arrived in Roman territories during the first century B.C. (L6schnig and Passecker 1954). Pliny (23-79 A.D.), in his Historia naturalis, used the names of pomum armeniacum or armeniaca arbor and occasionally the expression praecoqua, meaning early. Koch (1869) indicated that Lucullus and Pompeius may have learned about apricots in the war in which they attacked Armenia from Syria during 69-63 B.C. Lucullus had a villa and a garden to which he retired in 63 B.C. that was located on the Pincian Hill above the Spanish steps in Rome, and there he cultivated apricots (Hobhouse 1992). Thus, it is possible that the apricot arrived in Italy during the first century B.C. directly from Armenia and not through Greece. Apricot was cultivated throughout Asia and it is difficult to know where it may have come from to Europe. Harlan (1861) described P. armeniaca as native from around Kabul (Afghanistan) and bearing yellow, acid, and inferior fruit. He also encountered five sorts grown in production, one of which was especially luscious. It required careful manipulation in gathering, because it was so delicate that if one should fall to the ground, the shape would be destroyed. In Ladakh (Pakistan), according to Moorcroft (quoted by Darwin 1893), there were 10 kinds cultivated, all raised from seed except one, which was propagated by budding. Apricot was known in Islamic gardens; al-Biruni in 1050 provides us a list of fruits, among which he mentions apricot (Harvey 1975). Erman (quoted by Pumpelly 1871) mentions it as a "wild peach" of Nerchinsk, Siberia, as a true apricot, containing a very agreeable kernel in a fleshless envelope. According to Sturtevant's notes (Hedrick 1919), apricot was cultivated throughout the entire East, in Kashmir and northern India, in China and Japan, northern Africa and southern Europe. Around Damascus it was cultivated extensively and a marmalade was made from the fruit. Because of its widespread occurrence and use in Africa, Regnier and Sickler (quoted by McIntosh 1855) assigned a native area to apricot between the Niger and the Atlas. In the oases of Upper Egypt, the fruit of "mish-mish" is dried in large quantities for the purpose of commerce. Regnier saw wild apricot grown in upper Egypt, but in the opinion of De Candolle, they must have been grown from discarded cultivated stones (De Candolle 1886).

250

M. FAUST, D. SURANYI AND F. NYUJTO

The apricot arrived in Europe and was distributed there in various ways. Loschnig and Passacker (1954), based on word usage, describe three different routes of entry into Europe: (1) the northern route from China to the Balkans; (2) the southern route from Armenia through Syria, Arabia, Greece, Italy, and northern Africa; later it was also spread into Russia; and (3) middle route distribution from the Danube valley to Germany. The Roman soldiers played a major role in this distribution pattern, carrying the seeds/plants from place to place. Crossa-Raynaud (1960) assigned a different set of routes for apricot dissemination from its origin in Middle Asia: (1) to the Middle East, into Egypt and North Africa. This branch produced the cultivars 'Klabi', 'Beladi', 'Luzi', 'Bedri', and 'Amor Leuch' in Tunis, and the apricots of the oases, 'Mich-mich'. These African types are noted for their low cold requirement. (2) To Greece, middle and southern Europe extending north from the Mediterranean Sea. According to him, this group is represented by the cultivars 'Nancy', 'Royal', 'Luizet', 'Ampuis', and 'Rouge du RoussHon'. These cultivars require a considerable amount of chilling, their fruit is large, and essentially this is the group that disseminated into California, South Africa, and Australia. (3) To the East. Cultivars of P. armeniaca var. sibirica belong here. These cultivars are distinguished for their very high chilling requirement and their exceptional winter hardiness. According to Crossa-Raynaud (1960), the apricot entered into Russia from the west during the 17th century, but into Ukraine, Crimea, the Caucasian area, and Turkestan directly from the Middle East. The local name of apricot in Ukraine, zerdeli, indicates a direct entry from Persia. Possible distribution routes of apricot from its native areas to the modern production areas are illustrated in Fig. 6.12. Regardless of the original entry into Europe, a major entry of apricot to Central Europe directly from Turkey must be considered. Early archeological evidence indicates that apricot was in Pannonia (Hungary) in Roman times. At Budapest, in Aquincum (a Roman settlement), apricot seeds were found dating from approximately the first century (Suftlnyi 1985). An apricot seed was found in a 9th century grave at Balatonszentgyorgy (Sagi and Fuzes 1967) and from the 14th century, apricot seeds were unearthed from a well located at Disz Square 10, Budapest (Hartyanyi and Novaki 1975). The first mention of apricot in the Hungarian language occurs in the 14th century "Besztercei Dictionary." This indicates that apricot existed in Hungary well before the 16th century. However, the Turkish occupation of Hungary (1526-1680) greatly increased apricot plantings in the Hungarian planes. Even today, in Hungary, the present centers of apricot production clearly overlap with

6. ORIGIN AND DISSEMINATION OF APRICOT

251

the 16th-century location of Turkish estates of the Sultan (Nyujto and Suranyi 1981). The Hungarian word for apricot, kajszi, has a Turkish origin and did not appear in the word list of Szikszai Fabricious Balazs in 1590, but was used after 1600. This is an indication that the Turks brought the apricots with them. The Turkish apricots were apparently superior compared to the existing European cultivars and were desirable for planting. Consequently, propagation material was exchanged between interested parties. For example, Miklos Olah, Archbishop of Augsburg, Germany, requested budwood from Tamas Nadasdy's garden in Hungary in 1551. Boldizsar Batthyanyi requested budwood from Job Kavasy's garden in Hungary. Gessner, a Swiss horticulturist, in his 1561 book, Horti Germaniae, mentions Hungarian apricots as "magna et optima" (largest and best) (Nyujt6 and Suranyi 1981). Apparently the influence of Hungarian apricots increased apricot production in western Europe. Turner (1551) indicated that at that time there were still very few apricots in England but apricots were commonly grown in Germany around Cologne. Nevertheless, the importation from Turkey continued. During the 17th century, Cardinal Peter Pazmany imported apricot nursery stock directly from Turkey, and propagated them himself by grafting. From this period on, there is ample evidence described by Nyujto and Suranyi (1981) that apricot was grown in Hungary. In 1664, Janos Lippay, the gardener of the Archbishop of Pozsony (Bratislava), described four distinct cultivars, but at the end of the 18th century, Samuel Tessedik, a well known horticulturist, still used seedlings because grafted apricot trees did not survive on his high-sodium soils along the rivers of Tisza and Koros. Thus, development of land-race-type populations in the area dominated by the Turks, including Hungary, Serbia, and Croatia, was entirely possible. These cultivar groups (perhaps land races) are the basis of Nyujt6's classification described previously. There was an upsurge in production of apricots in the early 1800s in Hungary. In 1792 there was only two square miles of blowing sand in the area of Kecskemet (central Hungary), but this increased three-fold by 1805 and soon there was blowing sand everywhere. The increase in blowing sand was due to years of severe drought and increased sheep production that devastated the meager grass cover over the sandy areas. Expanding agriculture demanded more land, and consequently the sad over the sand was broken up. The Hungarian Congress discussed the danger of blowing sand in 1807 and encouraged the planting of apricots and plums, which were known to be able to establish themselves in sandy soils. The effort was successful, and there are records that

252

M. FAUST, D. SURANYI AND F. NYUJT6

beginning in 1855, Lipot Asz6dy and Sons, and from 1858, the Herz Brothers exported apricots from Kecskemet to Krakkow, Warsaw, Vilnia, and St. Petersburg (Nyujto and Suranyi 1981). In Italy, in the 7th century, apricots were grown south of Naples along with other fruits (Hobhouse 1992). In 1552, Girolamo Fiorenzuola in his La grande arte della agricola recommended apricots as one of the fruits that are suited to make spalliere or hedges growing against the low lattice fences (Hobhouse 1992). Matthioli (1500-1577) described three apricot cultivars (Martini 1988). A rare inventory taken at Villa Lante at Bagnaia north of Rome after the death of Cardinal Gambara in 1587 describes several fruits, including an orchard of apricots (Hobhouse 1992). Also in the 16th century, Tebaldi's Discorso sull' agricultura described the production of almonds, apricots, and peaches, while the work of Francesco Carletti (1573-1636) spoke about preservation of peaches and apricots by addition of sucrose (Forte 1971). In 1699, Bartholomeo Bimbi, an Italian painter of the Medicis, painted a large canvas with 9 apricots and 36 peaches. Eight of the apricot cultivars were identified by Cristoferi and Faccioli (1982) as 'Albicocca Grossa di Germania', 'Alessandrine 0 di Malta', 'Bianche di Genova', 'Di Padova', 'Di Venezia Del Padre Napoli', 'Mikliache', 'Nostrale', 'Tardive', and 'Tardive Del Padre Napoli'. He also painted a smaller canvas of 'Albricocche di Germania'. In 1758 Giorgio Gallesio in his Pomona Italiana describes five cultivars, including 'Albicocca di Germania' (Fig. 6.7A), a cultivar obviously originated in Germany, and 'Lucente 0 Alessandrina' (Fig. 6.7B) (Baldini and Tossi 1994). Alexander Bracci (ca. 1480) listed 100 plant species planted in the Medici villa Poggio a Caiano, outside Florence, which included several fruit and nut species-among them apples, pears, plums, peaches, figs, elderberries, mulberry, walnuts, and chestnuts (Emboden 1987). Apricot was not among the fruits listed. This may mean that apricots were not good enough or luscious enough to be included in the outstanding garden of the Medici the Magnificent. In 1676, Cause published a book in Amsterdam containing a chapter on how to grow apricots (Janson 1996). The baroque gardens at Het Loo (The Netherlands) were constructed around 1685 for William of Grange (1650-1702). In the reconstruction of this garden, based on contemporary descriptions, peaches, apricots, and nectarines grew on the sunniest walls. Thus, apricot was grown in Holland in the middle ages (Hobbhouse 1992). Langley in 1729 also wrote about apricots and illustrated the Roman and Turkish types (Fig. 6.14). The fact that apricots were grown throughout Europe is also indicated by archeological research, which discovered apricot seeds in Austria. Werneck (1955) found large apricot seeds (24.4 x 16.7 x 9.6 mm) at

6. ORIGIN AND DISSEMINATION OF APRICOT

Retl'll"

Ar,.;e.t. ,.il"

253

,r"ll/ .J•• r.Z. ,,-n/l, 2.P.:LJ'111

-m,

;'1,,;' .71,.,,,,,,,1t Z .. -It/"'r" 2J,jrn""". J~I,.,,.nl A~;IJJ br -1 ;,~.,'r')I'~'. 1),.",/~r' 1"1t'lI" 1'1I,'#' .n,:.?/I·~/tllfJ".

Fig. 6.14.

Il'lnr f"!;

r1r'"

nl" 011 ,1/'

.li·,,,

Illustration of Turkish and Roman apricots from Langley's Pomona, 1729.

Linz that dated to the 1st century. The interest in Europe in apricots was also expressed in 1819, when the Carlowitz nursery of Dresden in its sales catalog offered 13 apricot cultivars. A similar list of cultivars was produced in 1813 by J. L. Christ in his book, Vollstaendige Pomologie, published in Frankfurt. It was about stone fruit production and described 16 apricot cultivars (Janson 1996). Apricots were introduced to the Roussillon area of France by the Arabs prior to 1000 and into the Loir valley by Renato I d'Aragona, Duke of Lorena, in 1442 (Forte 1971). Because ofthe relatively late move

254

M. FAUST, D. SURANYI AND F. NYUJT6

of apricot to northern France, it is not surprising that apricots were not included in Charlemagne's Capitulare, written in 800. Apricots were planted at Versailles in the garden designed and built for Louis XIV by Jean de la Quintinye (1626-1688) (Tukey 1964). Why did apricots not move to the north of France until 440 years after their introduction into country? The answer probably lies in the fact that the southern types, introduced by the Arabs, were unsuitable to the north and the northern types arrived through an entirely different route. We suspect that import of Turkish types through Hungary was the origin of the great France cultivars that became important worldwide. In 1777 Andrieux described nine apricot cultivars (Janson 1996). 'Nancy', the cultivar to which a number of excellent cultivars can be traced, was noticed near Nancy and was originally described as 'De Nancy' in 1755. In 1889, Mathieu described 32 synonyms for this cultivar, including the name 'Pecheapricose' (Loschnig and Passacker 1954), which name was carried to England and is believed to be the predecessor of 'Moor Park'. In 1767, the sales catalog of nurseries operated by Carthusian monks at Paris described 10 apricot cultivars (Janson 1996). 'Royal', an important cultivar, was found as a distinct tree among the seedlings obtained from the seed of 'Nancy' and sent to Michel Harrey, director of the Luxemburg Gardens in Paris in 1808. The name was given to this exceptional plant after the King, Louis XVIII, had expressed his delight with a box of fruit given to him in 1815 (Stander 1983). 'Rouge du Roussillon' appeared around 1830 in the eastern Pyrenees area. It is a good producer, grown in the area of Roussillon, but carries the limited adaptability common to most apricot cultivars. Another important cultivar, 'Luizet', was discovered by Gabriel Luizet, owner of a nursery, among his seedlings in 1838. This cultivar was spread into almost every country of Europe and North Africa (Got 1958). The authors believe that 'Luizet' inherited its adaptability from the 'Hungarian Best', rare among apricots for its adaptability to a wide range of environments, but unfortunately 'Luizet' is a relatively shy producer. Yet another cultivar, 'Pavio!', was found in Lyon by Paviot near the end of the 19th century and soon spread to the rest of Europe. The last great cultivar of France that needs to be mentioned is 'Bergeron', found among a group of seedlings in Saint-Car au Mont d'Or in 1920 by M. Bergeron. Apricots were introduced into Spain by the Arabs, likely during the regime of the Umayyads (661-750), who conquered Spain between 711 and 719. Three manuscripts written in Spain in the 11th and 12th centuries mention apricots. The book of agriculture compiled by Ibn Bassal in about 1080 describes many fruits, including apricots (Hobhouse 1992). The second book, describing Andalusian agriculture, written by

6. ORIGIN AND DISSEMINATION OF APRICOT

255

Ibn al-'Awwam (1190) one hundred years later, also mentions apricots as one of the fruits suitable to the Andalusian hillsides and describes ways to care for them along with a considerable list of other fruits. Ibn al Baitar (1220) produced an encyclopedia of medicinal values of plants in which he describes the values of apricots and about 20 other fruits. Production of apricots slowly increased and the importance of apricots was enhanced. The major cultivar of Spain, 'Bulida', was discovered in Murcia between 1920 and 1930. The other important cultivars are 'Canino' (Syn. in France 'Bulida du Roussilon'), discovered as a chance seedling at Sagunto, near Valencia, by General Canino between 1910 and 1920, 'Monique', and 'Paviot'. Planting of apricots especially increased during the period from 1955 to 1967, from 4.5 to 20.8 thousand hectares (Ministerio de Agricultura 1975). Apricot production extended as far north as England. Thomson (1848) said that it was brought to England from Italy in 1524, while McIntosh (1855) gives the date of introduction to England as 1548. Roach (1985) reports that John Tradescant in 1620 sailed to North Africa as a voluntary passenger on a naval vessel rounding up pirates and brought back a cultivar named 'Algar' from Algiers. Gerard (1633) in his HerbaJI mentions the aprecocke or abrecoke trees and illustrates the greater and lesser aprecocke trees (Fig. 6.8). He describes the two types as almost identical, with the exception that the lesser apricot bears inferior fruit. Parkinson (1629) described four different cultivars, adding the 'White' and 'Masculine' to Gerard's greater and lesser aprecockes, and his friend Mr. Millen had five sorts: the 'Common', the 'Long and great', the 'Muske', the 'Barbary', and the 'Early aprecocke'. In 1688, Leonard Meager increased the cultivars offered for sale by the Brompton Park Nursery to seven. He offered the 'Algar, 'Civet', 'Masculine', 'Orange', 'Roman', 'Ordinary' and 'Great Turkey'. According to Roach (1985), the 'Roman' was synonymous with the 'Common' and it was a very old cultivar that may have gone back to Roman times and was the most widely grown apricot until the introduction of 'Moor Park'. 'Moor Park' was introduced by Admiral Lord Anson, and was fruited at Moor Park, near Watford in Heresfordshire in 1760 and was superior to all previous cultivars. In 1777, Richard Weston, in his nursery catalog, offered 'Temple', which was a synonym for 'Moor Park'. Driver (1788) thought that 'Moor Park' was synonymous with the so called "peach-apricot," which probably had been brought over from France at the beginning of the 18th century. Switzer, in 1724, reported a very large apricot cultivated in Berkshire, which was as large as a large peach and was called "French apricot" (Roach 1985). Later Hogg, based on graft-compatibility evidence, decided that 'Moor Park' was probably a seedling of the peach-apricot

256

M. FAUST, D. SURANYI AND F. NYUJTO

(Roach 1985). In those days apricot was recommended more than it was before. Reverend John Lawrence, Rector of Yelvertoft in Northamptonshire, in the 1723 edition of his book "The gentlemans recreation" offered an engraved plan of a fruit garden planted with 84 trees (Janson 1996). Lawrence recommended planting three apricot trees among apples, pears, cherries, plums, peaches, and nectarines. Apricots represented 3.5% of the orchard, about twice their proportion in the gardens of Versailles (Tukey 1964). Brookshaw produced two books, the Pomona Britannica and The Horticultural Repository, listing the best varieties of English fruits in 1817 and 1823, respectively. In these books, he describes five apricot cultivars (Janson 1996). In 1835, there were 17 cultivars in England according to Sturtevant (Hedrick 1919), but Hooker (1818) in his Pomona Londoniensis named only 'Moor Park', which may indicate its superior quality. 'Blenheim', another great English cultivar, originally called 'Shipley's', was introduced by Miss Shipley, the daughter of a gardener to the Duke of Marlborough at Blenheim, some time before 1830 (Roach 1985). This cultivar was exported to California and became widely planted. B. Worldwide

The Spaniards apparently took the apricot to the New World and established it in their earliest settlements. It thrived in the drier parts of Mexico (Magness 1951). The English also established apricots in Virginia where Capt. John Smith reported that it was grown in 1629 (Magness 1951). Manning reported that it was grown abundantly in Virginia in 1720 (Hedrick 1919). Thomas Jefferson planted apricots at Monticello and noted in his garden book in 1769 that he planted peach stocks for budding ("inoculating,j) apricots and field planted apricots in 1771 and future years. Jefferson remarked in 1809 that he planted apricot stones sent to him by Mrs. Hackley from Cadiz, Spain, and in 1810 that he planted Bordeaux apricots. Cultivar names are rarely mentioned in his record but he definitely had two cultivars: 'Angelic' and 'Large Early' in addition to seedlings raised from the seeds of 'Meliache' and' Albicocche' (Baron 1987). Regardless of early plantings, apricot has never proved well adapted to the climate ofthe eastern United States and apricot growing remained confined to the area west of the Rocky Mountains, largely in California, with some commercial quantities also grown in Washington, Oregon, and Utah. In 1817, Coxe described six apricot cultivars (Janson 1996). During fruit exhibits of the Massachusetts Horticultural Society apricots were regularly shown. In 1830, more apricots were shown than before, but

6. ORIGIN AND DISSEMINATION OF APRICOT

257

only one cultivar, 'Moorpark', was represented at the exhibit. Some of the 'Moorpark' fruit were large. Specimens of E. Phinney on 27th July measured 15cm in circumference. Nevertheless, the number of cultivars grown increased (Manning 1880). In 1862, A. Downing described 20 cultivars with 86 synonyms. In 1871, C. Downing reported 12 cultivars that included some old types: 'De Nancy', 'Royal', 'Moorpark', 'Kaisha', 'Apricot Peche', and 'Mush-Mush'. In 1875, Thomas listed 20 cultivars that included the same favorites ('Nancy', 'Royal', 'Blenheim', and 'Moorpark'). In 1879, the American Pomological Society recommended 11 cultivars (Hedrick 1919). At the beginning of this century, apricots were grown in the Eastern United States, but apricot growing was unsuccessful because the early frosts destroyed the flowers. The favorite cultivars in the East were 'Moorpark' and 'Peach Royal' (Hedrick 1950). Apricot was introduced into California by the Mission Fathers. Vancouver found apricots at the Santa Clara Mission in 1792 (Wickson 1927). Later, when the best English and French cultivars were introduced, the area of cultivation greatly increased. The number of trees reported in California in 1899 was about 3 million, occupying nearly 16,000 ha. Fruit was dried and canned. The shipment of fresh apricots from California was 290 carloads in 1910 (Wickson 1927). In 1920, there were 25,600 ha of apricots in the United States and 96% of this area was located in California (Wellman 1927). Production increased between 1909 and 1920 by 3,000 t per year. In the early 1920s most of the crop was dried (67%) or canned (29.5%) and only a small fraction utilized as fresh fruit (1.3%) (Wellman 1927). The California area increased steadily until about 1940, reaching the 32,000 ha level, and decreased afterward. By 1965, apricot area in California was at about the same level as at the turn of the century, with yield at a corresponding level. Production was 141,000 t during the early 1920s, increased to 250,000 t by 1940, and decreased again to 181,000 t by the early 1960s (Foytik 1961). Around 1876, Russian Mennonites introduced apricots directly from Russia and propagated the plants from seed in Nebraska. The Russian strain was the subspecies sibirica (Hedrick 1950). They only had a few named cultivars, which included 'Budd', 'Gibb', and 'Alexander'. According to Professor Budd, the Russian apricots were hardy in Iowa but did not bear well and blossomed too early. He recommended only the 'Shense' apricot (syn. 'Acme'), which was a cultivar introduced from northern China (Bailey 1894). Apricots, unlike peaches, underwent relatively little improvement in North America. Two of the major apricot cultivars of California are 'Royal', imported from France, and 'Blenheim', introduced from England, both at an early date (Hesse 1951). These two cultivars are almost

258

M. FAUST, D. SURANYI AND F. NYUJT6

identical at most locations and even experienced growers have difficulty identifying them. In contemporary descriptions they are listed as 'Royall Blenheim' (Hesse 1951). Another imported cultivar is 'Moorpark', originally called 'Moor Park', which was imported from England. It was excellent for drying, not so good for canning, and too late for shipping (Hesse 1951). In 1885, J. E. Tilton discovered a seedling on his estate at Hanford, Kings County, California, which he named 'Tilton' and it became one of the most important cultivars in California (Foytik 1961). No apricot introductions from Asia have been made that were comparable to the introduction of the 'Chinese Cling' peach. The two old cultivars, 'Royal/Blenheim' and 'Tilton', remain the mainstay of the California apricot industry. Melenbacher et a1. (1990) estimated that 'Royal/Blenheim' produced 41 % and 'Tilton' 39% of the California apricot crop. In 1890 and 1891, some apricots were planted in Arizona. At Phoenix, 'Blenheim', 'Moorpark', and 'Royal' were planted to test their productivity (Devol 1895), but the apricot industry never became important. In Canada, production in British Columbia nearly mirrored the apricot situation of the United States. In the Okanagan and Similkameen valleys, apricot plantings increased from 51,000 trees in 1925 to 201,000 trees in 1955, and decreased to 70,000 trees by 1967. The decrease was caused by the decreased demand for fresh market fruit (Trumpour 1969). Apricots are also grown on a small scale in Ontario and were introduced by Russian settlers. They thrive best near the shores of Lake Ontario and Lake Erie. In Australia, apricot has been popular ever since the first settlers occupied the land. Production has been concentrated in the Murray River irrigated area of South Australia. Jan van Riebeeck, commander of the first European settlement at the Cape (1652-1662), planted the first apricots in South Africa sometime between 1659 and 1662, and their descendant, known simply as the "Cape apricot," was the most common type for a long time (Stander 1983). At the end of the 19th century, Harry Pickstone imported a cultivar, 'Royal', from France that became the leading cultivar of South Africa until the 1980s. Another important cultivar of South Africa, 'Bulida', was imported from Spain in the 1930s, and the third important cultivar, 'Peeka', was the first locally bred apricot released to the industry in 1966. Cape apricots are harvested in November and December. They were exported beginning in the 1930s to Europe. In 1938, 100,000 5-kg packages were exported and this figure increased to 153,000 in 1954. Beginning in the 1960s, demand for Cape apricots declined, but increased again in the 19808 (Stander 1983).

6. ORIGIN AND DISSEMINATION OF APRICOT

Table 6.2.

259

Production of apricot worldwide. Production (1000 t)

Europe

N&S America

Asia

Africa

Oceania

Total

1948-52

230

206

145

50

35

666

1975-77

590

166

397

146

62

1361

1985-87 1993

745 783

129 200

624 941

213 244

37 31

1748 2199

Year

Reference Nyujto and Suranyi (1981) Nyujto and Suranyi (1981) Layne et a1. (1996) FAO (1994)

Apricot production worldwide is slightly over 2 million t, but still constitutes less than 1 % of the total fruit production. Nearly half of the crop is produced in Europe, followed by Asia. World production increases slowly at about 3 % per annum. During the last 50 years, production increased in Asia, Europe, and Africa and remained level in America and Oceania. The production during the last half of this century is given in Table 6.2. The 10 largest producers (1,000 t) in 1993 (FAG 1994) were Turkey (400), Spain (199), Italy (192), France (156), USA (144), Pakistan (140), Iran (118), Hungary (80), Tajikistan (65), and China (60). It is unknown whether apricot production for seed is included in the Chinese total.

VI. CONCLUSION Apricot and peach have similarities in their origin, but differ in their dissemination and development. Both species originated in Asia and were brought to Europe by the Romans. However, dissemination of apricot was much slower in Europe than that of peach. Both are excellent desert fruits, but peach has become a foremost fresh fruit while apricot has remained largely a dried product. The difference manifested itself early. According to Fischer and Benson (quoted by Loschnig and Passecker 1954), between the 3rd and 15th centuries apricot was considered to be an early peach and was not considered a separate species by Crescentius (1518), written in 1304-1309, or Hieronymus Bock (1595). Apricots were disseminated only slowly in France. In the 17th century, only 1500 m 2 ofthe king's fruit garden at Verailles were planted to apricot as compared to 27,500 m 2 for peach. One possible reason could be the size ofthe fruit; apricot was much smaller than peach, which made it less desirable. The

260

M. FAUST, D. SURANYI AND F. NYUJTO

Table 6.3. Size of apricot fruits at Fergana and Samarkand as determined by Kostina. Fruit Distribution (%) Location

Large

Medium

Small

3

55 57

42

Fergana Samarkand

21

22

Source: Guerriero 1982.

reference to small size was expressed in 1561 by Maaler, who called apricots "kleine, friihzeitige Pfersich" (small, early peach) (Loeschnig and Passaker 1954). Where did the large-fruited apricots originate? Large-fruited apricots may have entered into Europe from Middle Asia through Greece, as proposed by Crossa-Raynaud (1960). There are occasional large-fruited types both in the Samarkand area and in China. Kostina determined fruit sizes in the Fergana and Samarkand apricots (Guerriero 1982). There were more large-fruited types at Samarkand than at Fergana (Table 6.3). A comparison of average fruit sizes is 'Royal' (35-50 g), 'Rouge de Rousillon' (38 g), 'Canino' (50 g), 'Luizet' (55 g), and 'Peche de Nancy' (55 g) (Couranjou 1977). Gu Mo (1988) described the size of fruit in a number of Chinese apricot cultivars and reported some exceptionally large fruit (Table 6.4). However, these large types apparently were not imported into Europe, because the West-European types were different from the Asiatic types. Thus, Crossa-Raynaud's (1960) proposal may not, after all, be the explanation for the appearance of large-type apricots. It is clear that apricots were in Europe from the first century B.C., but did not become important until the 17th century. The increase in appreTable 6.4. Size of apricot fruit in selected Chinese cultivars, described by Gu Mo (1988). Fruit Size (g) Cultivar Most cultivars Luotaoxhuang Chuanling Hongjingzhen Huaxianajiexing

Average

Largest

30 50

50 78 75 120 150

45

71 100

6. ORIGIN AND DISSEMINATION OF APRICOT

261

dation of apricots during the 17th century coincides with the Turks bringing apricots to Hungary. A special quality and/or considerable size advantage is required to make this an important fruit crop. However, the Turkish apricots were, and still are, relatively small. Of 57 Turkish apricot cultivars described by Giilcan (1988), all but two had smaller fruit than 60 g and most of them were under 40 g. Therefore, it is difficult to imagine that the present West-European cultivars appeared in Europe as a simple Turkish import. In most apricot growing nations, including Turkey, apricots are preserved by drying, and for this purpose mediumto small-size fruit is preferred. The Hungarians, because their climate is not warm enough, could not dry apricots but used them instead as fresh fruit. For fresh fruit consumption, the large-fruited types are the most suitable. Thus, the imported Turkish types must have undergone a selection process for size in Hungary during the development of the eight Hungarian land races identified in Nyujt6's classification. It is conceivable that members of these improved land races were carried further west, becoming the ancestors of the West-European group of cultivars. The evidence for this theory is scant. The French apricots, introduced from the south by the Arabs did not move north likely because of adaptation difficulties. The French apricot culture was augmented only when 'Nancy', a northern type, was discovered in 1755. 'Nancy', according to L6schnig and Passecker's (1954) illustration, and Tomcsanyi's (1979) description, is very close to, and perhaps a descendant of the 'Hungarian apricot' group. It is possible, considering the time of appearance of 'Nancy' and the previously described geographic movement of apricot material in the 18th century, that seed from the Turkish/Hungarian group was carried to France and was the origin of this cultivar. 'Royal', in turn, originated as a seedling of 'Nancy'. 'Blenheim', another important cultivar, indistinguishable from 'Royal', may be another seedling of 'Nancy'. 'Moorpark' also can be described as a descendant of 'Nancy', the "peach-apricot" as it was named in England. 'Albicocca di Germania' (Fig. 6.7A) illustrated by Gallesio (1817) is considered to be the peach-apricot, 'Nancy', by Tamaro (1901). Finally, 'Tilton', likely to be a seedling of the major California cultivars, 'Royal', 'Blenheim', or 'Moorpark', is the latest addition to the West-European group among the major cultivars. These major cultivars, forming the West-European group of Kostina, point to the influence of the Hungarian apricots in the development of the European cultivars. Such reasoning also distinguishes the other major line of apricot cultivars, the descendants of 'Canino'. These likely stem from the low-chilling type from North Africa and may form the basis of the Mediterranean group, thought to be separate from the West-European group by several classifiers.

262

M. FAUST, D. SURANYI AND F. NYUJT6

Modern analysis, involving DNA markers, might answer where and how the high-quality, large-fruited apricots originated. At present, we must consider the 17th century as the time and Central Europe (Hungary, Croatia, Serbia, and perhaps Romania) as the location where the ancestors of the present apricot cultivars were selected and 'De Nancy' the mother cultivar from which the modern line of apricots originated. This view also points to the narrow genetic origin of apricots and explains the slow progress in apricot improvement in recent times. Throughout this review, we referred often to the special ecological conditions apricots require. We have done this because several other authors made this point. However, the adaptability of apricots should be reexamined. 'Hungarian apricot' and all its indirect descendants'Royal', 'Blenheim', 'Moorpark', 'Albicocca di Germania', and even 'Luizet'-are well adapted in many conditions where chilling is satisfactory and winters are not too harsh. 'Canino', representing the other line of apricots, is also well adapted. However, its adaptation area includes low chilling and mild winter locations. It is used extensively as a parent in breeding programs in Africa. In the last 10 years in Europe there has been an increased use of new cultivars developed recently in the United States ('Orange Red', 'Goldbar', 'Goldstrike', 'Tomcat') and Canada ('Hargrand', 'Harval', 'Haroblush', 'Harojoy', 'Harostar'). These cultivars also appear well adapted. Thus, one cannot make a blanket statement about the local adaptation requirement in apricots. Apricot is a low-chillingrequiring species. Low-chilling-requiring types may start sap flow early in fluctuating winter climates, with the result that the tree is injured by relatively moderate levels of subsequent cold. Injured bark is sensitive to diseases. In addition, apricots have varying heat requirement for spring bud break. Types with low heat requirement bloom very early and are extremely sensitive to spring frost during or after bloom. Considering these factors, it is not surprising that there are many climates in which apricot cultivars do not do well. A better understanding is needed of the factors that limit cultivar adaptation and lead to better breeding and selection methods for improved cultivar adaptation. Apricot are best for eating when the fruit is completely ripe. Apricot fruit softens fast when ripening is initiated. Apricots readied for the fresh market must be harvested relatively early to prevent softening during marketing. The use of fresh apricots decreased when the fresh fruit had to be harvested early and was transported over long distances because of significant losses in flavor quality and losses caused by brown rot following harvest. This resulted in limited market potential for fresh fruit. Apricots would be a good candidate for genetic transfer of traits that keep the fruit firm. If a non-softening type, or non-melting

6. ORIGIN AND DISSEMINATION OF APRICOT

263

flesh equivalent to processing peach is created, we consider apricot to be a fruit whose time is still to come as a fresh market fruit. More mention should be made of the unique and varied flavors of apricot (more so than peach). The problem is that most consumers have never tasted a tree-ripened apricot and have no idea what an excellent, aromatic flavor is waiting for them to discover.

LITERATURE CITED Arakeljan, V. N. 1951. Garni 1. Izd. Agrik. Yerevan. Arzumanjan, P. R. 1970. Kultura abrokosza v Armjanszki SSR. Sbornic materialov. Izd. Ajastan, Yerevan. Bailey, C. H., and 1. F. Hough. 1975. Apricots. p. 367-383. In: J. Janick and J. M. Moore (eds.), Advances in fruit breeding. Purdue Univ. Press. West Lafayette, Indiana. Bailey, L. H. 1894. Apricot growing. Cornell Univ. Agr. Expt. Sta. Bul. 71. Bailey, L. H. 1927. The standard cyclopedia of horticulture. Macmillan, New York. Baldini, E.. and F. Scaramuzzi. 1982. L'Albicocco. Reda, Conegliano. Baldini, E., and A. Tosi. 1994. Scienza e Arte nella Pomona Italiana di Giorgio Gallesio. Accad. GeorgofiIi, Firenze. Baron, R. C. 1987. The garden and farm books of Thomas Jefferson. Fulcrum Inc., Golden, Colorado. Bauchin. C. 1687. Krauterbuch. Basel. Blaha, J., L. Luza, and J. Kalasek. 1966. Apricots (in Czech). p. 227-414. In: J. Blaha (ed.), Peaches, apricots. almonds. Czechoslovak Acad. Sc. Prague. Bock. H. 1595. Krauterbuch. Strasbourg. Bradley, R. 1739. New improvements of planting and gardening. London. Brandis, D. 1874. The forest flora of North-West and Central India. London. p. 192. Casini, E., and M. Neri. 1964. L'Albicocco. Edagricole. Bologna. Columella. 1st century A.D. De Re Rustica I-XII. Trans. L. E. S. Foster and E. H. Heffner. London, 1979. Couranjou, J. 1977. Varieties d'abricotier. INVUFLEC, INRA, Paris. Crescentius. P. 1518. (Opus ruralium commodorum) Von dem nutz der ding gie in Aecker gebaut werden. Strassburg. (There were earlier editions, Latin 1471, Italian 1478, German 1493, but the original work was written earlier.) Cristoferi, G., and F. Faccioli. 1982. Albicocce. p. 45-49. In: E. Baldini (ed.), Agrumi, frutta e uva e nella Firenze di Bartolomeo Bimbi pittore Mediceo. Cons. Nazion. Del. Richerhe, Bologna. Crossa-Raynaud, P. H. 1960. Problems d'arboriculture fruitiere en Tunise. Abricotiers. Ann. L'Institut National de la Recherche Agronomique de Tunisie 33:39-63. Darwin, C. 1893. The variation of animals and plants under domestication. 2nd ed. London. Vol. 1, p. 366. Davidson, A, and C. Knox. 1993. Fruit. A connoisseur's guide and cookbook. Simon & Schuster, London. De Candolle, A 1886. Origin of cultivated plants. 2nd ed. Reprinted in 1964. Hafner, New York. Devol, W. M. S. 1895. Notes on apricots at Phoenix Station. Univ. Arizona Agr. Expt. Sta. Bul. 16.

264

M. FAUST, D. SURANYI AND F. NYUJTO

Dochnahl, F. }. 1860. Der siechere Fuhrer in der Obstkunde oder systematische Beschreibung alier Obstorten, Vol. 3. (Quoted by Loschnig and Passecker 1954) Downing, A. J. 1862. The fruits and fruit trees of America. Revised by C. Downing. Wiley, New York. Downing, C. 1871. Selected fruits from Downing's fruits and fruit trees. Wiley, New York. Driver, W. 1788. Pomona Britannica. London. Emboden, W. A. 1987. Leonardo Da Vinci on plants and gardens. Discorides Press, Portland. FAO. 1994. Yearbook, annual production. 48:162-163. Forte, V. 1971. L'Albricocco. Edagricole, Bologna. Foytik,}. 1961. California apricot industry. Trends and outlook. Calif. Agr. Exp. Bta. Ext. Servo Circ. 495. Galiesio, G. 1817. Pomona Italiana. Bologna. Gerard, J. 1633. HerbalI. Enlarged edition by T. Johnson. (facimile ed. 1975). Dover Pub!., New York. GOOf, A., and M. Nurock. 1968. The peach, the apricot, the plum, and the pear. In: Fruits of the Holy Land. p. 202-227. Israel Univ. Press., Jerusalem. Got, N. 1958. L'abricotier. Paris. Gu Mo. 1988. Apricot cultivars in China. Acta Hort. 209:63-67. Gueirriero, R. di. 1982. Cultivar. p. 9-19. In: E. Baldini and F. Scaramuzzi (eds.), L'AIbicocco. Reda, Conegliano. Giilcan, R. 1988. Apricot cultivars in near east. Acta Hort. 209:49-54. Harlan, K. L. 1861. Reports of the Agricultural Section of the United States Patent Office. Washington, D.C. 1837-1861. p. 529. Hartyanyi, P., and Gy. Novaki. 1975. NovEmyi mag as termasleletek Magyarorszagon az ujkortol a XVIII szazadig. p. 23-71. In: Magyar Mezogazd. Muz. EVk6nyve 1973-1974. Harvey, J. 1975. Gardening books and plant lists of Moorish Spain. Garden History 3:10-21. Hedrick, U. P. 1911. The plums of New York. Dep. Agriculture, State of New York. Albany. Hedrick, U. P. 1919. Sturtevant's notes on edible plants. Albany. Hedrick, U. P. 1950. A history of horticulture in America to 1860. Oxford Univ. Press, New York. Hepper, F. N. 1992. Baker encyclopedia of bible plants. Baker Book House, Grand Rapids, MI. Hesse, C. O. 1951. Apricot culture. Univ. Calif. Agr. Expt. Sta. Cir. 412. Hobhouse, P. 1992. Gardening through ages. Simon and Schuster, New York. Hogg, R. 1875. The fruit manual. London. Hooker, W. 1818. Pomona Londoniensis. London. Ibn al-'Awwam. 1190. Libro de agricultura, Facs. edit. Madrid, 1988. Ibn al Baitar. 1220. Djami el moufridat. Translated by J. Sontheimer, Stuttgart 1840-1842. Janson, H. F. 1996. Pomona's harvest. Timber Press, Portland, OR. Jeszejan, G. S. 1977. KuItura abricosza Armenii. p. 3-147. Abrikos. Ajastan, Yerevan. King, J. R. 1939. Cytological studies on some varieties frequently considered as hybrids between plum and the apricot. Proc. Am. Soc. Hart. Sci. 37:215-217. Kluge and Gotze. 1934. Etymologisches Worterbuch. 11th ed. Geugter, Berlin. (Quoted by Loschnig and Passeker 1954) Koch, K. 1869. Dendrologie. Die Deutsche Obstgeh6lze. Band I-II. Enke, Stuttgart. Kostina, K. F. 1936. Abrikos. BuI. App!. Bot. Gen. Plant Breeding SuppI. 83. Inst. Plant Industry, Leningrad. Kostina, K. F. 1969. The use of varietal resources of apricots for breeding. Trud. Nikit. Bot. Sad. 40:45-63. Kostina, K. F. 1970. Selekcionnoe iszpolzovanie sortuv fondov abrikosa. p. 177-189. In: V. J. Ajzenberg (ed.), Abrikos. Ajastan, Yerevan.

6. ORIGIN AND DISSEMINATION OF APRICOT

265

Kostina, K F., and I. N. Riabov. 1959. An experiment on distant hybridization of fruit trees (in Russian). Trud. Nikit. Bot. Sad. 29:113-137. Kovalev, N. V. 1970. Ustojcivost abricosa k klajsterosporiozu v svjazi s geograficskim I geneticeskim proishozsdeniem. p. 169-172. In: V. ]. Ajzenberg (ed.), Abrikos. Ajastan. Yerevan. Langley, B. 1729. Pomona: or the fruit garden illustrated. London. Laufer, B. 1919. Sino Iranica: Chinese contributions to the history of civilization in ancient Iran. Field Mus. of Nat. Hist. Anthropol. Ser. 15,3. Chicago. Layne, R. E. c., C. H. Bailey, and L. F. Hough. 1996. Apricots. p. 79-111. In: J. Janick and J. N. Moore (eds.), Fruit breeding. Vol. 1. Wiley, New York. Undqvist. C. 1991. China, empire of living symbols. Addison-Wesley Publ., New York. Unnreo, C. 1737. Hortus Cliffortanus. Reprinted in 1968. Verlag Cranier, New York. Loschnig, J., and F. Passecker. 1954. Die Marille und ihre Kultur. Ost. Agrarverlag, Wienna. Magness,]. R. 1951. How fruit came to America. Vol. C:325-377. Mandy, Gy. 1949. A kajszilevel alakulasanak fajtameghatarozo jelentOsege. Borbasia 9:6-10. Manning, R. 1880. History of Massachusetts Horticulture Society. 1829-1878. Boston. Martini, S. 1988. History of pomology in Europe. Wadenswill. Mcintosh, C. 1855. The book of the garden. Edinburgh, Vol. 2:517. Mehlenbacher. S. A., V. Cociu, and L. F. Hough. 1990. In: J. N. Moore and J. R. Ballington, Genetic resources of temperate fruit and nut crops. Acta Hart. 290:65-107. Intern. Soc. Hart. Sci.. Wageningen. Ministerio de Agricultura (Spain). 1975. Produccion y demanda de albaricoquue. Madrid. Murray, ]. A. H. 1888. A new English dictionary on historic principles. Clarendon Press, Oxford. Nyujto, F., and D. Suranyi. 1981. Kajszibarack. Mezogazd. Kiad6. Budapest. Parkinson, J. 1629. A garden of pleasant flowers (Paradisi in sole-paradisus terrestris). Republished in 1976. Dover Publ. Inc., New York. Paunovic. A. S. 1970. Vrste i sorte kajsija i njihovo gajenje. Glasnik poljoprivrede i zadrugarstva 4:26-33. Pliny. 79 A.D. Natural History VIII-XIX (trans. H. Rackham and W. H. S. Jones, 1938-1956). Harvard Univ. Press, Cambridge. Pumpelly, R. 1871. Across America, Asia. 5th ed. New York. Rehder, A. 1940. Manual of cultivated trees and shrubs hardy in North America. Macmillan, New York. Roach, F. A. 1985. Cultivated fruits of Britain. Their origin and history. Blackwell, Oxford. Sagi, K, and F. M. Fuzes. 1967. Regeszeti adatok a Pannoniai kontinuitashoz. AgrartOrt. Szemle 9:79-98. Sargent, C. S. (ed.) 1988. Plantae Wilsonianeae. Reprinted by Discorides Press, Portland. Smikov, K K 1983. Abricos. Dostizhenia selekcii plodovich kultur I vinograda. Kolos. Stander, S. 1983. Tree of life. The story of Cape fruit. Saayman and Weber, Cape Town. Sun, Y. W., S. Thu, and K Yao. 1983. History of fruit culture and resources of fruit trees in China. Shanghai Publ. House of Science and Techn., Shanghai. Suranyi, D. 1985. Kerti novemyek regenye. Mezogazdasagi Kiado, Budapest. Szikszai-Fabricius, B. 1590. Nomenclatura dictionarium. Latino-Ungaricum. Csaktornyai, Debrecen. Tamaro, D. 1901. Trattato di frutticoltura, Vol. 2:117-133. Ulrico Hoepli, Milan. Terpo, A. 1974. Taxonomy and geographical distribution of fruit producing plants. p. 145-213. In: F. Gyuro (ed.), A gyumo1cstermesztes alapjai. Mezogazdasagi Kiado, Budapest.

266

M. FAUST, D. SURANYI AND F. NYUJT6

Theophrastus. 300 B.C. De causis plantarum I (trans. B. Einarson and G. K. K. Link in 1967). London. Thomas, J. J. 1985. American fruit culturist. Part 2. Wood & Co., New York. Thomson, R. A. 1848. Report upon the varieties of apricots. Hort. Soc., London. Timko, 1. 1971. Keleti keresztenyseg, keletiegyhazak. Szent Istvan Tarsulat, Budapest. Tomcsanyi, P. 1979. Gyiimo1csfajtaink. Mezogazdasagi Kiado, Budapest. Tournefort de, J. P. 1700. Institutiones rei herbariae. Paris. Trumpour, M. P. D. 1969. Commercial apricot production in British Columbia. Publ. Branch, Dep. Agr. Canada. Tukey, H. B. 1964. Dwarfed fruit trees. Macmillan Co., New York. Turner, W. 1551. A new herbal!. London. Unger, F. 1859. Reports of the Agricultural Section of the United States Patent Office. Washington D.C., 1837-1861. Vavilov, N. 1. 1992. Origin and geography of cultivated plants (tr. L. Storr-Best). Cambridge Press, Cambridge. Wellman, H. R. 1927. Apricots. Univ. California Agr. Expt. Sta. Bul. 423. Werneck, H. L. 1955. Die Obstweihefund im Vorraum des Mithraeums zu Linz Donau. Oberosterreich. Naturkundl. Jahrb. Stadt Linz. p. 41-54. Wickson, E. J. 1914. California fruits. 7th ed. Pacific Rural Press, San Francisco. Wickson, E. ]. 1927. Apricot. In: L. H. Bailey (ed.), The standard cyclopedia of horticulture. Macmillan, London. Yoshida, M. 1994. Mume, plum and cherry. In: K. Konishi, S. Iwahori, H. Kitagawa, and T. Yakura (eds.), Horticulture in Japan. Asakura Publ. Co., Tokyo. Yuan W. Z., and S. Du. 1983. Germplasm of fruit trees in Shaanxi. Shaanxi People Pub!. House, Xian. Zhang, ]., and W. Liu. 1995. Preliminary report on identifying and selecting plum and apricot germplasm resources. Acta Hort. 403:74-77.

7

Tea: Botany and Horticulture* 1. Manivel Former Plant Physiologist Tocklai Tea Research Association and UPASI Tea Research Institute, India

1. Introduction A. Economic Importance B. Historical Summary II. Botany A. Systematics B. Origin and Evolution C. Anatomy and Morphology 1. Vegetative 2. Floral D. Physiology E. Genetics and Cytogenetics F. Crop Improvement III. Horticulture A. Crop Establishment B. Training and Pruning C. Crop Management 1. General 2. Agro-inputs D. Growth Regulators in Crop Management 1. Growth Retardants 2. Biostimulants 3. Antitranspirants E. Water Management F. Plant Protection 1. Insects

*The help and assistance rendered by my colleagues, R. Raj Kumar and S. Marimuthu, in preparing the manuscript is gratefully acknowledged. I am grateful to the Tea Research Association ofIndia and the United Planters' Association of Southern India for providing information incorporated in their publications for the benefit of the industry at large. Horticultural Reviews, Volume 22, Edited by Jules Janick ISBN 0-471-25444-4 © John Wiley & Sons, Inc. 267

268

1. MANIVEL

2. Disease 3. Weed Control

G. Harvest and Mechanization H. Processing and Marketing 1. Processing 2. Packing, Forwarding, and Marketing IV. FUTURE PROSPECTS Literature Cited

I. INTRODUCTION

A. Economic Importance Tea is one of the world's most popular beverages. Tender shoots of the tea plant (Camellia sinensis (1.) O. Kuntze) comprising two to three leaves and a bud are used for making the commercial black (fermented) or green tea (unfermented). Popularity ofthe beverage cannot be ascribed to anyone component or a group of components. The therapeutic value of tea arises from its unique combination of a large number of constituents, including carbohydrates, amino acids, lipids, vitamins, minerals, alkaloids, and phenolics. Proteins present in the leaf are rendered insoluble during the process of manufacture and tea infusions contain hardly any protein and only negligible amounts of carbohydrates and fat. They do, however, possess a few water-soluble vitamins, notably riboflavin, niacin, pantothenic acid, inositol, and some quantities ofthiamine, biotin, and folic acid (Krishnamoorthy 1987). Tea by-products have received attention in recent years mainly as sources of pigment, polyphenols, and caffeine, all derived from low-quality manufactured tea. Antioxidant properties of tea extracts have been exploited for preservation in the food industry (Zongmao 1994). Caffeine and the polyphenols present in tea act as mild stimulants and help to keep the body and mind agile (Marks 1992; Mulky 1993). These are said to be somewhat more stimulating to the muscular system than to the cerebrum and, taken in moderation, tea relieves body fatigue. Infusions of tea leaves are used to treat conjunctivitis because of their astringent characteristics. Saponin from tea seeds finds a place in medicine preparation because of its high surface activity, and is used also in the cosmetic and chemical industries (Zongmao 1994). A glycoside, camellin, used as a cardiac stimulant in endocarditis and pericarditis, has been isolated from the seeds of C. japonica, a tea relative usually grown as an ornamental.

7. TEA: BOTANY AND HORTICULTURE

269

Tea seeds yield about 17.3% oil, which is very low compared with 58% from C. sasanqua and 66% from C. japonica. Tea seed oil is of the non-drying class and resembles the oil of C. sasanqua in its properties and characteristics. Extraction of oil from tea seed is not economically viable, although the oil is used as a lubricant (Wealth of India 1950). Tea seed cake contains saponin and is unfit for animal feed. As a fertilizer, it has poor value on account of its low nitrogen, phosphorus, and potassium content. It has been utilized in the manufacture of a nematocide useful in horticulture (Wealth of India 1950). Tea is an important crop that determines the economy of many countries where commercial tea is an important export crop. World tea productivity statistics are presented in Table 7.1. Millions of workers, particularly women, are employed in the tea industry, especially for harvest. Management practices in the field and the incidence of pests and diseases vary with topography and the environment, while manufacturing the component depends on demand and consumer preference. In the past three decades, a number of books have been devoted to tea, including Harler (1964), Eden (1976), Barua (1989), Willson and Clifford (1992), Banerjee (1993), and Arunachalam (1995). This review summarizes recent developments in plant husbandry, manufacturing, scientific innovations, and trends in the field of plant improvement, nutrient management, and stress physiology, with emphasis given to developments in India. B. Historical Summary

The word "tea" originated from the Amoy pronunciation of the Chinese word t'e (pronounced tay), while cha was derived from Cantonese. Tea was first mentioned in a Chinese dictionary published in 350 B.C. However, the first detailed reference to this beverage was made in the 4 th century when Kien-Lung described its medicinal effects and methods of preparation. Tea drinking became very popular in China at the time of the Tang Dynasty (618-907) (Harler 1964; Eden 1976). The British collected the seeds from China for introduction into their colonies in India and Sri Lanka. However, later wild types of "Assam" and "Cambod " tea were found in Assam and Indochina. The origin of tea is supposed to be near the Irrawaddy River in Indochina, although this is in dispute. China type tea is believed to have originated in China, while the Assam and Cambod types may have originated in Indochina (Wight 1959). The Dutch introduced tea to Indonesia and began the trade with Europe. Later the British East India Company entered the tea

270

Table 7.1.

L. MANIVEL Global scenario on area, production, and export: 1994 (Dwibedi 1995).

Country

Area under cultivation (ha)

Production (Mkg)

Export (Mkg)

Export (% of production)

Asia Bangladesh China India Indonesia Iran Japan Malaysia Myanmar Sri Lanka Taiwan Thailand Turkey Vietnam

47888 1170800 418331 129231 4000 55700 3005 58662 221836 23087 6574 89330 63000

52 588 744 130 45 86 6 38 244 22 8 134 36

24 180 147 85 1

46.2 30.6 19.8 65.4 2.2

224 4

91.8 18.2

5 12

3.7 33.3

6

85.7

184 35 4 5

85.7 100.0 80.0 83.3

19 2

79.2 84.6 66.7

Africa Burundi Cameroon Kenya Malawi Mauritius Rwanda S.Africa Tanzania Uganda Zaire

8750 1531 104864 18705 3151 12566 6164 19415 20500 9000

7 4 209 35 5 6 N.A 24 13 3

11

Europe Georgia

81400

18

3425

6

3

50.0

41406 6000 4000

46 10

43 8

93.5 80.0

Oceania Papua New Guinea

South America Argentina Brazil Peru

Others

3

16

5.4

33.4

trade and popularized the drink in Western Europe and in North America. The Boston tea party (1773) was an incident preceding the American War of Independence in which rebellious colonists in disguise destroyed a valuable shipment of tea owned by the British East India Company by throwing it into Boston Harbor.

7. TEA: BOTANY AND HORTICULTURE

271

Initially tea was propagated by seeds; later vegetative propagation through single nodal cuttings was standardized (Tunstall 1931) and widely adopted for clonal propagation. Currently, both asexual and sexual methods of propagation are used to ensure the perpetuation of desired traits and utilization of hybrid vigor. II. BOTANY A. Systematics

Tea belongs to the Theaceae (syn. Camelliaceae) and is a member of the genus Camellia, which contains approximately 82 species (Ellis 1995). Sealy (1958) considered commercial tea plants as a single species designated Camellia sinensis (L.) O. Kuntze, with two well-marked variants: C. sinensis var. sinensis, to which the China types were assigned, and C. sinensis var. assamica, the Assam type. Sealy described C. sinensis var. sinensis f. parviflora (Miq.) Sealy and C. sinensis f. macrophylJa as "fixed variants." A less conservative treatment was applied by Wight (1962), who recognized three distinct species: Camellia sinensis (L.) O. Kuntze, the China type; C. assamica ssp. assamica (Masters) Wight, the Assam type; and C. assamica ssp. lasiocalyx (Planch. ex Watt) Wight, the Cambod type of tea. Barua (1963) provided the morphological and anatomical description of the three taxa, which were later supported by Bezbaruah (1971). The most recent treatment (Chang and Bartholomew 1984) recognizes three varieties of one species: C. sinensis L. var. sinensis (China type), C. sinensis var. assamica (Mast.) Kitamura (Assam type), and C. sinensis var. waldenae (S.Y. Hu) Chang (Cambod type). The three basic tea types are described as follows:

• China types: Shrubs 1 to 3 m tall with numerous suckers originating from the base of the plant, near the ground. Leaves are comparatively small, leathery, dark green in color and erect posture. Flowers occur year around. • Assam types: Small trees, 10 to 15 m tall, possessing a robust branch system with thin, glassy large leaves and semierect to horizontal posture. Flowers arise singly or in pairs from cataphyllary leaf axils. • Cambod types: Small trees measuring about 6 to 10 ill tall with several upright, equally developed branches. Leaves intermediate in size, pale yellow in color with pink tinge at the base. Floral characters resemble mostly the Assam type (Banerjee 1992).

272

L. MANIVEL

Tea grows well in locations with an annual precipitation ranging from 1150 to 8000 mm, ambient temperatures between -8 and 35°C, and daylength of 9.4 to 15.0 h. It flourishes well on acidic soils with pH ranging from 4.5 to 5.5, and from sea level to an altitude of2,300 m (Eden 1976). B. Origin and Evolution The origin of China type sinensis has not yet been established, since no wild type has been located. However, the other two types, assamica and lasiocalyx, were believed to have originated in the basin of the Irrawaddy River in Indochina (Barua 1989). The narrow region of Wenshan and Honghe, located at 22° 40' to 24° 10' Nand 103° 10' to 105° 20' E in Tan province, China, just south of the Tropic of Cancer, is the center of origin of the tea plant. This plant is indigenous to a vast fan-shaped area bordered at the northwest by Assam, at the northeast by the China coast, and at the south by southern Cambodia and Vietnam. However, Chang and Bartholomew (1984) maintain that both C. sinensis var. sinensis and C. sinensis var. assamica are endemic to China. From the primary sites of origin, the three types moved eastward and westward to spread through much of southern Asia and westward to Europe. Species of tea are largely self incompatible, with China types being the most self incompatible and the Cambod types the least (Wight 1956), hence cross breeding is the rule. Self incompatibility is welcome to an extent in complex hybrids (Bezbaruah and Saikia 1977). Present-day cultivars are the natural hybrids between the three types, predominantly "assamica" in character. C. irrawadiensis, a distinct species, has also contributed to the evolution of botanical varieties. Due to the interaction of these species and the growing environment, distinct tea variants with specific tea qualities arose (Barua and Dutta 1959; Wight and Gilchrist 1961a,b). From seed populations, selections were made and clones emerged. Combination of clones through natural or controlled hybridization gave rise to numerous cultivars all over the world. A continuous process of evolution and stabilization ofthe desirable traits for modernday tea cultivars has involved combining productivity, quality, and tolerance to abiotic and biotic stresses. C. Anatomy and Morphology 1. Vegetative

Foliar Anatomy. At the gross anatomical level, the cross section of tea leaf is typical of any other dicot. Between two epidermal layers, the

7. TEA: BOTANY AND HORTICULTURE

273

parenchymatous mesophyll tissue is differentiated to form palisade and spongy layers. Scattered in the mesophyll are the veins, oriented in such a way that the phloem is abaxial and xylem is adaxial. Anatomical features differ in some clones (Raman and Cheng 1981). Presence of sclereids and their shape, particularly of lumen and constrictions, are identifying features for the three types (Barua and Dutta 1959). The presence of sclereids is a distinct feature of assamica and lasiocalyx types but conspicuously absent in China type cultivars (Barua and Dutta 1959). The types of tea differ in their quality parameters of manufactured tea; assamica being known for the strong liquor (Wight and Gilchrist 1961b), while the China type is known for its flavor and aroma. A large number of calcium oxalate crystals are found in different organs of the tea plant. The number of crystals varies significantly between clones. Based on crystal frequency, an "agro-type index" has been evolved and this has been used for identification of clones with differing genetic bases (Wight 1958).

Foliar Morphology. Tea leaf size varies significantly among the cultivars. In general, tea leaves are elliptic to oblong in shape with a rugose to smooth upper surface. These are pale to dark green in color, with lamina sparsely appressed, pubescent or silvery villose; serrate, having a wavy to flat margin with acute to accuminate apex, with acute to rounded base. They are horizontal to erect in their posture. Saw-like, sharp serrations are typical of China types, while the broad droopy leaves with bulliform ripples is typical of the Assam type. A pink tinge of the petiole and purple pigmentation of the newly emerging flush are associated with Cambod cultivars. Leaves of the China type are hard, thick and leathery when compared to Assam cultivars. Lamina of Cambod jats are intermediate and resemble those of the Assam type (Wight 1962). Interveinal chlorosis due to magnesium deficiency during stress periods is unique to Cambod type cultivars. 2. Floral

Morphology. Flowers are borne in cataphyllary axils, singly or in pairs. The pedicel is 6 to 10 mm long, clavate; the caducous bractioles 2 to 5 mm long; the persistent sepals are 5 to 6 in number; 3 to 6 mm long, leathery, green, glabrous. The ovate/orbicular sepals are imbricate. The shallow/cup-shaped petals are 7 to 8 in number, measure about 1.5 to 2.0 em long, and are generally white in color. Numerous stamens are arranged in two whorls, the inner one shorter, 8 to 13 mm long, united at the base with the corolla lobes. The ovary is creamy white, densely

274

1. MANIVEL

hairy, trilocular with ovules 3 to 5 in each locule and with axile placentation. The styles are generally three, free with apical stigmas; the capsule contains 1 to 3 spherical seeds. Floral biology. Flowers initiate during May-June and bloom three months later depending on the climatic conditions. Flowering begins toward the end of December and continues to the end of March, attaining its peak during February under south Indian conditions. However, occasional flowers do appear in the trees, particularly on the China type, all through the year. Bezbaruah (1975) reported that no fixed time was observed in northeastern India for the opening of tea flowers, while under south Indian conditions anthesis commenced from 0600 hand continued up to 1130 h (Sharma et a1. 1981). The time of anther dehiscence varies in relation to anthesis. The calyx is persistent in tea flowers, whereas the corolla and androecium start withering by 24 h from anthesis. The stigma is green even after 24 h, while at the end of 48 h the style withers (Sharma et a1. 1981). Tea fruits take almost a year to develop; fruits set in September or October and become ready for harvest in the subsequent year. Capsules are harvested when ripe lest the seeds dehisce and fall. Unfilled seeds float in water and are normally rejected while sorting. The seeds possess a hard, impervious seed coat. The cotyledons are creamy white, with a high content of oil. Seeds are recalcitrant in nature and lose moisture in storage, which in turn affects their viability. Forthis reason, the seeds are stored in refrigerated conditions (4-9°C) in moist sand and charcoal (Barman 1988).

D. Physiology Rhythmic growth of tea shoots has been well documented (Bond 1942, 1945; Barua and Das 1979; Sharma 1979). Growth periodicity of shoots and roots is governed by management practices in tea plantations. Shoots complete up to 7 flushes in a year, alternating with the interflush rest C'banji") periods. In the course of development, the preformed initial produces in succession two scale leaves (janam) and an unserrated leaf (fish leaf) followed by a series of three to four normal foliage leaves. The plucking (harvesting) standards are named after these types of leaves; thus janam plucking, fish leaf plucking, and mother leaf plucking. The growth rate of these shoots and unfolding rate of new leaves depend on plant vigor and the growing environment. Growth rate has been found to correlate with the heat units accumulated during the formative as well as the growth period (Murthy and Sharma 1989).

7. TEA: BOTANY AND HORTICULTURE

275

Besides the interflush dormancy, dormancy during winter months has been recognized in temperate areas such as Assam, China, and Japan (Arunachalam 1995). However, winter dormancy does not occur in regions nearer the equator such as southern India and Sri Lanka. Bud dormancy during the interflush and winter dormancy has been attributed to many factors, such as lack of vascular connections, deficiency in nutrients, stresses, and finally the endogenous promoter and inhibitor level (Raj Kumar 1995). Aperiodic shoots, when tipped (first harvest after pruning), give rise to secondary and tertiary branches producing an order of laterals. Complexity in the order of laterals results in vascular bundle constriction and discontinuity or obstruction in sap flow; this could be the reason for the slow growth and weaker shoots, forcing the buds to go dormant. In a given year, tea shoots complete up to seven orders of branching, contributing the new shoots that are harvested periodically for production of the tea of commerce (Das 1977). Periodicity is maintained in regular plucking fields, whereas it is broken in the pruned tea bush that produces aperiodic shoots. Periodicity of shoot growing is attributed to the combination of internal and external factors that are yet to be investigated. Besides the periodicity of shoot growth, proliferation of feeder roots below the ground level occurs (Barua 1989; Fordham 1972) and alternates with the growth or dormancy of the shoots. Interdependency of roots and shoots has been associated with growth substances produced by the leaves and roots. Cytokinins produced in roots are utilized for the initiation, development, and growth of new shoots, while proliferation and growth of root is governed by the assimilates and hormones contributed by leaves (Kulasegaram 1969). Root growth and depth of roots are determined by soil type and water availability. In Assam, where the water table is high, roots are limited to the top 45 em of the soil, whereas in southern India, Sri Lanka, and African plantations, thick roots are spread up to 5 m depth or more, exploring for minerals and water in deeper layers (Carr 1971). However, the effective absorbing roots and feeder roots are restricted to the top layer of the soil (Barua and Dutta 1961). Mycorrizae may be associated in the mobilization of P. Initiation, development, and anthesis of flowers occur in an orderly sequence, determined by the phasic growth of the apical bud (Barua 1989). The phenomenon of growth periodicity, interflush dormancy, winter dormancy, alternation of growth of roots and shoots can be correlated with endogenous promoters and inhibitors which in turn are influenced by the environment. Being a C3 plant, tea is not photosynthetically efficient and a major

276

1. MANIVEL

part of photosynthates are lost in respiration (Roberts and Keys 1978). Tea is cultivated principally in rainfed conditions; the water requirement for sustaining the assimilation is not adequately met during part of the year. The harvest index is further reduced due to periodic pruning and perennial plucking. Introduction of longer pruning cycles with lighter cuts in between regular pruning has enhanced the harvest index and productivity (Dutta 1969). Growing shoots are strong sinks due to intensive metabolic activity in the bud mediated by the accumulated assimilates and hormones. During the peak growing season, the entire maintenance leaves of the canopy contribute photosynthates toward growth of the shoots, as documented by the upward movement of radioactive carbon (Manivel and Hussain 1982a,b). However, during rest periods, bidirectional movement or downward movement of the photosynthates have been observed due to the reduced sink capacity of the banji shoots or stronger growth activity of the roots. Seasonal change in the direction of movement of photosynthates due to the changing sink capacity mediated by the endogenous growth substance has been documented in Assam (Manivel and Hussain 1982a,b). Recent studies in southern India revealed that the promoter level fluctuates depending on the environment, although the inhibitor level remains more or less constant. The balance between promoters and inhibitors plays a vital role in deciding the movement of photosynthates and therefore whether the types of shoots will be flush or banji (Raj Kumar 1995). Radiotracer studies also revealed that flowers drain photosynthates competing with the growing shoots (Marimuthu et al. 1994). E. Genetics and Cytogenetics Most of the cultivated tea types are diploids, with 2n == 30 (Bezbaruah 1971; Ellis 1995). The chromosomes oftea vary in size and have median to submedian centromeres. Clones belonging to the three types of tea do not reveal any major difference in their karyotype, although minor differences were correlated with morphological features of the plants (Bezbaruah 1967). Natural tetraploids have been detected and there are some triploid cultivars. Aneuploids have also been reported. Tetraploids were found to be vigorous but lacking in quality. Breeding on the tetraploid level and selecting elite triploids have been suggested as a breeding strategy (Bezbaruah 1971). UPASI-3, a natural triploid, combines the vigor and quality (Venkataramani and Sharma 1975); while TV-29 is a triploid with good vigor but average quality. Crosses between China and Assam types have displayed heterosis

7. TEA: BOTANY AND HORTICULTURE

277

(Wu and Shyu 1966). Heterosis in tea has been exploited in the production of seed-propagated rootstocks (Bezbaruah 1968). There are few genetic studies in tea. Wu (1964) found that length and density of hair on the undersurface of young tea leaves are quantitatively inherited. Size of tea seed has been shown to be a maternal character (Barua 1961). F. Crop Improvement The objectives of genetic improvement programs are to improve productivity. The plant is highly heterozygous and self incompatible. Clonal selection from heterogenous seedling populations has resulted in many productive, high-quality clones in all the tea-growing countries (Venkataramani and Sharma 1975; Bezbaruah and Singh 1980). Genetic improvement by recombination of selected clones has increased productivity by 40 % • Mutation breeding using chemical and physical mutagens have not yielded tangible results and there are no reports of progress through biotechnology. Tolerance to biotic and abiotic stress are the major traits in which improvement is required.

III. HORTICULTURE A. Crop Establishment

Tea is a water-dependent crop, and one of the prerequisites for tea cultivation is well-distributed rainfall. The second most important factor is the acidity (pH) of the soil. High humidity and high irradiation are required for rank growth. Tea-growing areas in India are confined to the river valleys in Assam or the hills in southern India and Sri Lanka, which benefit from monsoon showers and acidic soil. In India, at present, clonal scions are grafted to clonally propagated rootstocks (Satyanarayana et a1. 1992). Generally, grafts are grown in nursery beds and later transferred to polyethylene sleeves for easy transport and planting. Cultural practices are governed by environment and availability of raw materials. For example, bamboo frames are used as shade in Assam, while coir mat is used in southern India. In southern India, polythene cloches are used to increase humidity to hasten rooting of cuttings. Good rooting of cuttings without any malformation such as club-callus requires attention to media pH and water status (Eden and Bond 1941; Wight 1955). A staggered double hedge triangular system of 60 x 60 x 105 or 60 x

278

L. MANIVEL

60 x 135 cm spacing (60 cm between plants and 105 or 135 cm between rows) accommodates about 13,000 to 15,000 plants/ha. Planting time varies with rainfall distribution. In Assam, planting is done at the end of the monsoon, while in southern India and Sri Lanka, planting is done throughout the monsoon. Planted areas are mulched with dried twigs and trash to minimize evapotranspirationallosses and to restrict weed growth. Sprinklers or drip irrigation are employed for better survival of plants during dry months wherever an adequate water source is available and resources permit. Provision for temporary and permanent shade is made at the planning stage. The shade trees, Grevillea robusta A. Cunn. in the south and Albizzia odoratissima Benth. in the north, are preferred for permanent shade (Hadfield 1974). Removal of shade in certain Indian and African plantations proved costly and inflicted permanent damage. Initially the trees are planted at 6 x 12 m and later thinned to 12 x 12 m spacing. Tephrosia sp., Indigofera teysmanii Miq., and Crotalaria sp. are planted as temporary shade. These trees or shrubs are pruned regularly to regulate the shade for three to five years. At the time of formative pruning, these temporary shade species are uprooted because some of the surface feeders compete with tea for moisture and nutrients and at times serve as alternate hosts for pests and diseases.

B. Training and Pruning

The foundation for sustained productivity of the tea plant as a perennial bush requires a balanced shoot to root ratio and a lowset frame with an adequate number of primary, secondary, and tertiary branches. Weed control and nutrient feeding promote plant growth. Pruning is a critical operation (Dutta 1956). Apical dominance is overcome by different pruning measures. This distributes adequate branches all around the trunk at the pre-determined height. Desired bush architecture is achieved through centering, cut-across, and structural pruning in the first 3 to 5 years after planting (Bezbaruah and Barbara 1983). Plant height is maintained to facilitate harvest. Pruning also stimulates vegetative growth. The formative pruning after planting is made at 45 or 55 cm from the ground level, at the end of the fifth year or earlier, depending upon growth. This forms the permanent frame on which the canopy is built. Normally, pruned bushes require 60 to 90 days to recover before harvest, depending on the cultivar and thickness of the stems. The canopy is maintained by tip pruning the leaves in such a way that three to five leaves are left. All the terminal growth from aperiodic shoots is removed

7. TEA: BOTANY AND HORTICULTURE

279

by tipping, and dormant axillary buds are allowed to grow into laterals and secondary shoots. As a result of this process, the height of the plucking table rises and shoots become smaller. Different degrees of severity are required in pruning to obtain optimal productivity, quality, and managerial convenience (Dutta 1960a; Venkataramani and Venkataram 1968). In northern India, a milder kind of cut known as skiffing is carried out between regular pruning cycles. Normal pruning is done once in three or four years. In skiffing (described as deep skiff, medium skiff, and light skiff according to the severity of the cut) a part of the canopy is retained. As a result, bud break is quick and crop loss due to pruning is minimal compared to regular pruning. This type of pruning is continued for three or four cycles. When too many knots (the base of a branch buried in a later growth of wood) are formed, hindering the sap flow, a kind of deep cut known as height reduction or medium pruning is performed. It takes 2 to 3 months for the latent buds to break in cases of medium or rejuvenation pruning, resulting in about 30% crop loss during that year. In order to minimize crop loss during the pruned year by hastening budbreak, chemicals such as hydrogen cyanamide at 0.5% are applied to the pruned frame within three days of cut. This treatment has advanced budbreak by about a month compared to untreated plants; buds were set and gave a good early and total crop without any adverse effect on quality oftea or health of the bush (Table 7.2). It also promoted an increase in leaf area index (Marimuthu et a1. 1993). When the plantations ages, frames may be adversely affected due to pests such as termites and diseases such as poria (Poria hypolateritia Berk.) and canker (Phomopsis theae Petch). Corrective surgery of the affected frame at a low level is known as rejuvenation pruning. This is carried out once in 50 years or more, depending on the health of the frame (Barua 1971, 1972). In southern India and Sri Lanka, pruning is carried out once in four or five years. Pruning is done either pre-monsoon (April/May) or postmonsoon (August/September), whereas in northern India, tea bushes are Table 7.2. Effect of hydrogen cyanamide (Dormex. SKW) on budbreak, and productivity in seedling tea. Treatment Control HCN (0.5%)

No. of buds emerged

No. of shoots tipped

Early crop (%)

Pruned year crop (kg made tea/hal

207 236*

104 118*

100 117*

2351 2709*

*Significantly higher at 5% level.

280

L. MANIVEL

pruned during winter months (December/January) when there is no growth due to bud dormancy. Height reduction or rejuvenation pruning are practiced according to need in south Indian plantations (Venkataramani and Venkataram 1968). In Sri Lanka, pruning practices are similar to those of southern India (Kulasegaram 1986). Practices in Africa are similar to those in India. Mechanical pruning has been achieved in Georgia and Japan. C. Crop Management 1. General. Tea exhibits distinct annual growth peaks and troughs. Depending on the locations, 5 to 7 flushes are obtained, causing uneven crop distribution. There is an interflush bud dormancy (banji) and a winter dormancy for three months (December to February) in northeastern India. As soon as the terminal shoot is plucked, apical dominance is broken, inducing the growth of the axillary buds. The growth rate of shoots and the unfolding of new leaves depend mainly on the ambient environment, which influences the internal constituents ofthe shoots (Barua 1989; Rahman 1977a; Rahman and Barua 1980). The plucking interval can be predicted by leaf expansion (Murthy and Sharma 1989). The growth rate of shoots is faster and greater in higher latitudes where the bushes undergo dormancy (Barua and Barua 1969). Two types of shoots are harvested at periodic intervals for the manufacture of commercial tea. Wherever quality is given priority, shoots comprising two leaves and a bud are harvested, while three leaves and a bud are harvested for the purpose of increasing the quantity, even though there is a slight compromise in quality. There are also variations in harvesting based on the type of leaf of the shoot retained on the stub. Scale leaves (Janam), fish leaf, or mother leaf may be left on the stub. This practice varies with seasons and territories (Jain and Tamang 1988; Watson 1986). Mechanical shear harvesting is done at longer intervals.

2. Agro-inputs

Fertilizers. Nutrients comprise one of the major inputs in tea plantations. Their level of application is dependent on several factors that include soil fertility, terrain, and annual precipitation as well as its distribution, geographical locations, and finally the productivity. NPK are the major nutrients applied every year. Nand K are combined for efficiency in utilization as well as to minimize the toxic effect of high N. Level of N ranges anywhere from 180 to 200 kg in Assam, 300 kg in southern India, and 1000 kg in Japan (Jain 1988). In northern India, young field-grown tea plants are fertilized every

7. TEA: BOTANY AND HORTICULTURE

281

month with 10 g of 10N:2P:8K, whereas in the South 180 kg N combined with Kat 1:0.8 ratio is applied by eyebrow method (placing the fertilizer in a curved arch around the plant) in four split doses each at the rate of 17 g/plant (Ranganathan and Natesan 1987). As the bushes grow, fertilizer level is increased based on productivity as well as the nutrient status of the soil. Productive mature tea fields receive 180 to 200 kg of N balanced with K in northern India, whereas in south India N level varies with yield level. For 2000 kg made tea/ha level, 240 kg of N is recommended for low organic matter (OM), 200 kg for medium OM, and 180 kg for high OM status in tea soils. Tea fields yielding more than 2000 kg of manufactured tea/ha receive an additional allowance of 5 kg of N for every 100 kg of made tea for low and medium OM status and 4 kg of N for high OM status. N-K ratio varies depending on height of the pruning in the pruned year and according to the sources of N in other years of pruning. Soil is tested for available P in alternate years and rock phosphate is applied by placement based on soil test values at the rate of 34 to 43 kg of P/ha (Verma 1997). In order to minimize loss from runoff, nutrients are applied in portions at intervals of three to six weeks. The level of the enzyme nitrate reductase in feeder roots of tea plants can be used as an index to determine the interval between two fertilizer applications. Nitrogen accumulates in roots as theanin, especially when the assimilation capacity of the canopy is limited through imbalance ofN:K ratio (Dev Choudhury et al. 1985). It has been found that soil pH decreases rapidly due to higher N levels; zinc deficiency increases rapidly with the depletion of starch reserves in the roots. Unless these deficiencies are corrected, the response to other agro-inputs decreases (Manivel et al. 1997). In addition to NPK applications, micronutrients such as Zn, Mn, B, and Mg are applied as foliar sprays to overcome the deficiency of these nutrients, and for better utilization of other inputs. About 12 to 15 kg of zinc sulphate and an equal amount of magnesium sulphate and urea are applied as foliar sprays in four to five portions. The addition of S is now emphasized in Assam plantations. In addition to the foliar application of micronutrients, urea and KCI, each at 1%, are applied at monthly intervals, particularly as an ameliorative measure against drought. Foliar spray of urea and KCI is an effective measure of manuring during adverse soil moisture conditions (Manivel 1993). The absolute minimal requirement of N for sustained tea production lies around 120 kg/ha, which is equivalent to 300 kg N per ha per year based on the absorption efficiency and runoff losses. If all other conditions are favorable, crop yields beyond 7000 kg/ha can be achieved with

282

1. MANIVEL

the optimum annual level of N of 300 kg/ha (Manivel et al. 1997). It is essential to recognize the importance of organic fertilizers in place of inorganic fertilizers such as pruning residues and vermicompost to ensure ecological stability and to maintain a sustainable crop environment (Bonheure and Willson 1992; Manivel et al. 1994a). D. Growth Regulators in Crop Management Plant growth regulators have been recognized as potential tools in tea management after a decade of research (Manivel et al. 1995). 1. Growth Retardants. Uneven crop distribution is one of the problems faced in north Indian tea plantations, putting undue pressure on crop and factory management. During the peak period, tea gardens face a shortage of workers for harvest and of floor space for manufacture. A smoother crop distribution can be achieved using growth retardants such as paclobutrazol and (2-chloroethyl) phosphonic acid (ethephon), which temporarily suppress the crop without affecting the annual crop or quality of manufactured tea (Manivel 1986). Another novel use of growth retardants is to enrich the starch reserve in roots so that the bushes can be pruned in different seasons for smoother crop distribution. This would be beneficial in the Darjeeling hills, where the seasonal variation in price based on quality is important. Paclobutrazol and ethephon break apical dominance in young tea, induce more uniform vigorous laterals from the lower part of the main stem, acting to improve the canopy architecture and harvest index. Proliferation of feeder roots is a spinoff additional benefit from use of growth retardants in young tea in addition to the promotion of lateral growth (Venkatesalu et al. 1994). In addition to the application of growth retardants for lateral promotion in young tea, polymer-based antitranspirants such as Green Miracle, an emulsion of long-chain alcohols (Stanes India Ltd), have been found to impart drought tolerance. Time of application and dosages of these chemicals in Indian tea plantations have been standardized and are being used successfully (ManiveI1987; Manivel et al. 1994b). 2. Biostimulants. During peak seasons, growth promoters, based on triacontanol and/or seaweed extract that consists of hydrolysed proteins, auxins, cytokinins, and enzyme precursors with vitamins, hasten budbreak and growth rate (Table 7.3), so that a higher crop is harvested in favorable periods (Barman and Manivel1989; Manivel1988; Manivel et al. 1994b). Crop distribution pattern is also smoothed. These bioregula-

7. TEA: BOTANY AND HORTICULTURE

283

Table 7.3. Influence of biostimulants on growth and productivity of mature seedling and clonal teas.

Treatment

Pn Psi shoot (mg CO 2 , dm- 2 • h- 1 ) (- bars)

Yield (kg made tea/hal

Seedling tea Control Biozyme Z (1000 ppm) TRIAY (2 ppm) LSD P = 5%

7.6 10.3 9.1 1.1

12.1 10.3 10.5 1.2

3621 3889 3854 157

Clonal tea Control Biozyme (1000 ppm) TRIA (2 ppm) LSD P = 5%

8.8 10.1 10.8 0.4

12.7 10.6 11.2 1.2

3932 4143 4245 170

Assimilate translocated (%)

Root CHO

11.2 22.8 23.0

10.6 13.8 13.2

(%)

ZBiozyme is a seaweed extract. YTRIA is a formulation based on triacontanol.

tors improve productivity through enhanced photosynthesis: favorable partitioning of assimilates, and improved water use. Application of these bioregulators for south Indian conditions has been standardized and recommended for use by plantations during the peak growing seasons (Manivel et a1. 1995). In the case of northern India, the first and second flushes fetch premium prices and therefore these biostimulants are used to enhance the productivity of the first and second flush. 3. Antitranspirants. During dry months, antitranspirants are used to minimize the impact of drought. Antitranspirants during the dry months in conjunction with NK foliar (Table 7.4) have proved effective in mitigating the drought effect as ameliorants in tea plantations of both north and south India for young and mature tea (Manivel et a1. 1994c; Venkatesalu et a1. 1993). In order to sustain productivity, the presence of a mature leaf on top of the canopy before the onset of drought is a recommended practice (Barua 1989; Sharma et a1. 1992). Foliar fed NK has served as an ameliorant as well as a source of nutrients during unfavorable soil moisture conditions (Manivel 1993). Moisture stress during winter, dry periods, and frost in high elevations are major stresses that plants go through almost every year. Although limited success has been achieved in drought management through use

L. MANIVEL

284

Table 7.4. Effect of antitranspirants and NK foliar application on health and productivity of drought susceptible tea clone.

Treatment

Psi shoot Pn (mg CO 2 , dm- 2 • h- 1) (- bars)

Control Antistress Z (350 ppm) Humipic Y (1000 ppm) Green Miracle x (1000 ppm) Urea + KCI 1 % each L.S.D. P =5%

Yield (kg made tea/hal

Assimilate translocated

Root CHO

(%)

(%)

7.2 9.5 9.6

12.9 10.7 9.9

3736 4048 3951

21.0 23.0 13.0

10.6 12.3 13.0

9.2 8.7 0.9

10.3 9.9 0.8

4035 3958 165

32.0 38.0

12.3 13.4

Antistress based on amines. based on long chain polymer of glycol. x Green Miracle based on emulsion of long chain alcohols. Z

Y Humipic

of antitranspirants and sprinkler irrigation, effective steps are not yet available for frost protection. E. Water Management Tea is a rainfed crop; geographical crop distribution explains the requirement of annual precipitation and its distribution. In most tea-growing nations, tea plants experience three to five months of soil moisture stress. Supplemental irrigation either by sprinkler or drip is adopted to preserve bush health and to sustain productivity through maintaining a favorable microclimate at bush level (Krishnapillai et a1. 1992). Sprinkler irrigation is adopted wherever an adequate water source is available, while drip is preferred where water is limiting but clean. Initial overhead cost is larger for drip than for sprinkler irrigation. Fertigation is possible through drip emitters. Supplemental irrigation during dry periods can increase production up to 30% (Singh 1988). Higher vapor pressure deficits are directly correlated with reduced photosynthesis. A similar relationship exists between high rate of transpiration, soil temperature, and root reserve. Excess water during the monsoon period results in waterlogging. As the water table is high in the Brahmaputra valley or northeast India, roots are submerged during the monsoon, which hinders absorption of nutrients. Plants with shallow root systems in turn become susceptible during moisture stress in winter months. Hence, provision of open or underground drains to remove excess water during the monsoon is an

7. TEA: BOTANY AND HORTICULTURE

285

advantageous practice. Open drains were in vogue in the past. Buried drains seem to be superior to open drainage systems that occupy much land. Although the initial investment is high, tea plantations in Assam and the Brahmaputra valley have started switching over to pipe drains because of the reduced recurring cost as well as the availability of additionalland for planting (Singh 1978, 1979; Singh et a1. 1980; Ghosh and Dey 1983; Banerjee 1993). Wherever feasible, pumping of water into the river from the drains is being adopted in Assam plantations. The beneficial effects of irrigation in dry months have been amply demonstrated. Judicious water management during stress periods can improve root system and canopy functions, nutrient utilization, and reduce competition from weeds (Singh 1988). Drainage is not advocated in very steep slopes (>30°) because of the hazard of erosion and landslides. F. Plant Protection 1. Insects. Insecticides are essential for tea crop management. Insect

control measures have been reviewed for south India (Muraleedharan 1991; 1992) for north India (Banerjee 1983), and for Sri Lanka (Senaratne 1986).

Arthopod pests can be categorized as cold weather sucking insects, peak season worms, and chewing insects. Special insects such as termites and shot hole borers (Euwallacea fornicatus Eichhoff) are activated during dry months in exposed areas. Mites (acarids) are one of the major pests in tea plantations. Their life history and ecology had been reviewed and elucidated by Banerjee (1965). Both north and south Indian tea plantations, as well as Sri Lanka, experience mites during dry winter months in areas where the shade is inadequate. All these categories of pests can be controlled by different insecticides. Quinalphos, Endosulphan, and monocrotophos are the pesticides commonly used against most sucking insects, caterpillars, and bugs. Chlorpyriphos is used for the control of termites. Dicofol, Ethion, and sulphur are proven acaricides against all types of mites. Shot hole borers are controlled by resorting to Fenvalerate, a synthetic pyrethroid formulation. Of late, due to indiscriminate use of pesticides (particularly pyrethroids), an epidemic outbreak of tea mosquito (Helopeltis sp.) has occurred, disastrously affecting productivity. Environmental consciousness has contributed to the idea of integrated pest management (IPM) through judicious use of biopesticides. Neem based formulations and Bacillus thuringiensis are being tested (Muraleedharan 1992). Maximum residue level of different pesticides in the

286

L. MANIVEL

product has been specified by the tea importing countries, and the Food and Agriculture Organisation (FAO) has proposed residues regulations at the international level (Muraleedharan 1994). 2. Disease. Two categories of diseases are encountered in tea plantations, depending on the terrain and agroclimatic conditions. Root diseases are predominant in low-lying waterlogged areas like the Assam plains, whereas in hills and cooler areas, blister blight (Exobasidium vexans Massee) is the principal disease affecting the tender leaves. Prolonged chronic waterlogging depletes the root reserve, which promotes the incidence of root diseases. Various root diseases and their control measures have been reviewed by Agnihothrudu (1963a,b). Chemical disease control and phytosanitation measures are suggested for northeastern tea plantations (Agnihothrudu 1957; Das et a1. 1959). Some ofthe diseases such as branch canker (Plasmapara sp.) and Poria (UstuJina sp.) (Phomopsis and Poria sp.) are caused by faulty management and agronomic practices, including exposure to sun scorch and defective pruning. Soil-borne root diseases are controlled by soil fumigants or systemic fungicides, whereas canopy diseases such as black rot (Corticium theae Bernard) and blister blight are controlled by copper fungicides and triazoles (Chandra Mouli 1993; Satyanarayana 1977,1981). Oflate, a unique symbiosis of a fungus with an insect pest, thorny stem-blight (Tunstallia aculeata (Petch) Agnihothrudu), earlier reported in northern India (Agnihothrudu 1961), has been found in south Indian plantations, especially in certain clones growing in particular agroclimatic situations. 3. Weed Control. A wide spectrum of weeds, including monocots and

dicots, are reported in tea plantations (Rahman 1977b; Rao and Rahman 1978). Some of the pernicious weeds are rhizomiferous (Rao 1978). Preemergent herbicides such as simazine are commonly used before planting to suppress weed growth. Rhizomiferous weeds like Imperata cylindrica (1.) Beauv, nutgrass (Cyperus rotundifoJia 1.) and ferns are controlled by use of glyphosates (Rao and Rahman 1978). Contact herbicides such as paraquat (Gramaxone, leI India Ltd) are frequently used to control the dicot herbaceous weeds. Some weeds such as Conyza ambigua DC., Crassocephalum crepododes (Benth) Moore, and Borreria latifolia AubI. are not controllable by any single herbicide. Therefore, cocktails of a few herbicides, such as glyphosate and 2,4-D, are used (Satyanarayana et a1. 1994). Another problematic creeper weed in the fields of north Indian plantations is Mikania cordata (Burm. f.) B.1. Robinson. It is controlled by judicious application of translocated herbicides like 2,4-D and glyphosate, or uprooted by hand. Some weeds

7. TEA: BOTANY AND HORTICULTURE

287

(Mikania) are suspected to be hosts for pests like the tea mosquito, Helopeltis sp. (Sandanam 1986).

G. Harvest and Mechanization

Tender current-season, succulent, vegetative shoots comprising two to three leaves and a bud are harvested for manufacturing commercial tea. While shoots with two leaves and a bud are preferred for product quality, shoots with three leaves and a bud are harvested wherever size of crop is the consideration. Selective plucking of growing two and a bud, or three and a bud, sparing the one leaf and a bud, as well as the bud, is known as standard or fine plucking. Plucking or removal of all the shoots, including the buds above the predetermined level of plucking table, is known as black plucking. Regeneration of shoots takes a long time and weight of shoots is reduced due to black plucking, which ultimately results in crop loss. Sink induced photosynthetic advantage is lost due to the absence of adequate sinks on the plucking table which are essential to sustain the high rate of photosynthesis of the maintenance leaves (Rahman 1977a; Willson and Clifford 1992). The interval between harvests is determined by the growth rate of shoots, which depends upon ambient conditions. On an average, about 30 to 35 pluckings are made in India. Harvested crop shoots are used for black tea manufacture. Longer intervals and high N application are adopted in order to harvest succulent shoots with high amino acids for the manufacture of green tea in Japan and China (Jain 1988). Selective hand plucking is slow and inefficient and to improve production per plucker, mechanical harvest with motorized or hand shears has been adopted by many plantations. Planning the planting design to accomodate mechanization is a factor in new plantations. Shoot regeneration and growth behavior of tea cause many problems in harvest. One of them is the production of dormant shoots. Removal of banji shoots is advocated while harvesting, even though they may not meet the fixed standard of two to three leaves and a bud. Systems of harvest, standard of shoots, and interval of plucking, which vary with the regions, terrain, and climate, have been investigated and refined in recent decades (Rahman 1977a; Dutta 1960b; Sarronwala 1980; Sharma 1987; Sharma et al. 1992; Watson 1986). Automation has lagged in the tea industry as it has in other beverage crops such as coffee and cacao. Global efforts are underway to design the pruning and harvesting machines in the field for manpower saving. The first harvesting/pruning machines were developed in the Republic of Georgia in the former Soviet Union. Japan is now taking the lead.

288

L. MANIVEL

Topography and design of planting in old plantations are the principal hurdles in the use of machines. Unless the planting accomodates tractor-drawn equipment, the scope for field mechanization is limited. Motorized harvesters are increasing in India. Hand-operated as well as motorized shears are used with advantage to cope with labor demand during rush seasons. Thus, worker productivity has been improved without affecting quality. Automation of handling harvested leaves has been achieved through conveyors and maintenance of temperature; fiber removal and sorting are achieved through on-line mounted electronic equipment in many tea factories. Mechanization of field management and automation of the factories is increasing rapidly (Hara 1996). H. Processing and Marketing 1. Processing. The principle and technology involved in tea processing have been described by Roberts (1986) and Samaraveera (1986). Manufactured tea may be classified as green or black tea. In green tea, shoots are steamed to inactivate the enzymes and processed. Green tea is more popular in far Eastern Asian countries. "Sencha" of Japan is the best grade of green tea; it is produced primarily out of spring shoots that are the first harvest of the year. Black tea is popular in the rest of the world. The basic steps involved in its manufacture are withering, rolling or cutting, fermention, drying, sorting, and packing (Roberts 1949). Second flush orthodox tea in India is world renowned for liquor and flavor. Tea flavor is unique to China type growing in high elevations such as Darjeeling (2200 m) in India, and Nuwaraeliya in Sri Lanka, while liquor strength is attributed to the broad leaved assam type growing in the plains of the Brahmaputra River. In addition to the leaves, the growing conditions and management techniques also contribute to quality. Attempts to duplicate Darjeeling flavor in Assam and vice versa in the same cultivar were unsuccessful, confirming the complexity of the factors responsible for the quality of the marketable black tea. An intermediate product is oolong tea, which is partially fermented. Withering is achieved by blowing warm air over the shoots spread on troughs lined with wire mesh, which reduces water content in cells to 30 to 40% of the original. Depending on the season and moisture content of the shoots, withering takes about 12 to 16 h. Thickness of leaf spread and/or the temperature of the air blown are regulated to maintain the withering period. Rolling involves initiation of the oxidation process. Either the shoots are rolled gently (orthodox) or cut, torn, and curled (GTC) depending on the type of tea manufactured. Once the tis-

7. TEA: BOTANY AND HORTICULTURE

289

sues are ruptured, oxidation of the phenolics is allowed to proceed during fermentation for about 40 to 75 min depending on the environment (Hampton 1992). During fermentation a desired balance between the flavanols, theaflavins, and thearubigins is achieved, which ultimately determines product quality. Once the desired balance (1:10 to 1:12 of theaflavin :thearubigin) is achieved, the enzyme action is terminated by firing at a temperature of 100°C for a period of about 30 min. The manufactured tea is sorted into different grades that are primarily based on size of the particles, ranging from broken pekoe to super fine dust. In eTC black tea, fibers are removed by employing on-line electrostatic fiber extractors, and other foreign bodies, iron pieces or nails, if any, are removed by magnets. The warm manufactured tea is heaped in storage bins for a cool-off (curing/maturity) before packing. Moisture content of tea at time of packing is restricted to 3 to 4%. 2. Packing, Forwarding, and Marketing. Tea is principally packed in plywood boxes of standard size, lined with foil to facilitate transport and prevent the entry of moisture; alternative packing materials such as foillined paper sacks or jute bags are also used. Filled boxes weigh 30-40 kg depending on grade and bulk density. Tea is typically marketed in pooled auction centers through brokerage firms. Export of tea is regulated by the Tea Board in India, a government agency. Amount to be exported is decided based on the production, domestic requirement, and obligations through forward contracts. Quality and value of auction price is dictated by tasters appointed by the brokerage firms and warehouses.

IV. FUTURE PROSPECTS Tea is an international beverage crop cultivated in varying agroclimatic conditions crossing geographical and ecological barriers. The tea industry is a developed agroindustry employing millions of workers directly and indirectly, generating wealth that influences the economy of teagrowing nations. The number one priority during the twenty-first century should be breeding for elite types with specific traits such as tolerance to stresses, pernicious pests, and diseases as well as increased productivity. A comprehensive germplasm collection and preservation technology is essential for this purpose. Basic research on gene mapping is necessary to develop genetically engineered plants with the desirable traits. In order to increase mechanization, new bush architectures have to be

290

L. MANIVEL

evolved. Simultaneously, new machines for pruning and harvesting need to be developed, but the social consequences of the technology also need to be considered. Developing machines to improve processing and to reduce in cost of production is of paramount importance for the viability of the industry. Value-added new products such as cold water soluble instant tea and blended beverages, coupled with strategic marketing, will help to stabilize the price of tea. New processing techniques and the addition of enzymes to improve the cuppage and quality of tea can be adopted, bearing in mind statutory obligations and consumer interest. Intensive research on the pharmaceutical effects of tea drinking is needed to take full advantage of the potentialities. Tea seed oil is a good lubricant and a base that is used in the cosmetic industry and it, too, needs exploration. Tea, being a health product, could be a basis for different ancillary industries such as caffeine, tannins, and amino acids. In spite of the hundred years of research in tea production, processing, and machinery, there is ample scope for further improvement and refinement of all aspects of tea husbandry. A global effort in this direction has been organized through the initiatives of FAG.

LITERATURE CITED Agnihothrudu, V. 1957. Chemotherapy of fungal diseases of plants. Two Bud 4(2):2-7. Agnihothrudu, V. 1961. Notes on fungi from North East India VII. Tunstallia genus caus· ing thorny stem blight of tea (Camellia sinensis (L.) O. Kuntze). Phyto Pathologische Z. 40:277-282. Agnihothrudu, V. 1963a. Some important root diseases, red rust and poria. Two Bud 10(2):9-12. Agnihothrudu, V. 1963b. A concise key for the identification of commoner primary root rot of tea in N.E. India. Two Bud 10:31-32. Annual Report, 1994. p. 106-117. United Planters' Association of Southern India Tea Sci· entific Department, Valparai, India. Arunachalam, K. 1995. A handbook on Indian tea. Standard Literature Company Limited, Calcutta 700 014, India. Banerjee, B. 1965. Daily activity rhythm of some tea pests and its importance in control operations. Two Bud 12:31-42. Banerjee, B. 1983. Pests of tea. p. 261-276. Agricultural Entomology. II. AISWA Pub!., New Delhi, India. Banerjee, B. 1992. Botanical classification oftea. p. 25-52. In: K. C. Willson and M. N.Clifford (eds.), Tea cultivation to consumption. Chapman and Hall, London. Banerjee, B. 1993. Tea production and processing. Oxford and IBH Pub!. Co. Private Limited, New Delhi, India. p. 188-225. Barman, T. S. 1988. Maturation, germination and storage of tea seeds. Proc. 30th Tocklai Conf. p. 102-105.

7. TEA: BOTANY AND HORTICULTURE

291

Barman, T. S. and L. Manivel. 1989. Effect of growth regulators on mature tea. Indian J. Plant Physiol. 32:151-152. Barua, D. N. 1961. The significance of seed size in cultivated tea (Camellia sinensis L.). ]. Expt. Agr. 29:143-152. Barua, D. N. 1963. Characteristics of Tocklai released clones. Two Bud 10:26-28. Barua, D. N. 1971. Rejuvenation of old tea. Two Bud 18:22-28. Barua, D. N. 1972. Rejuvenation of old tea. Part II. Two Bud 19:10-13. Barua, D. N. 1989. Tea: culture science and practice. Tea Research Assoc., ]orhat, India. Barua, D. N., and S. C. Barua. 1969. Seasonal dormancy. Two Bud 16:41-45. Barna, D. N., and S. C. Das. 1979. Mechanism ofgrowth periodicity in tea. Two Bud 26:36-40. Barua, D. N., and A. C. Dutta. 1959. Leaf sclereids in the taxonomy of Thea camellias II. Camellia sinensis L. Phytomorphology 9:372-382. Barua, D. N., and K. N. Dutta. Root growth of cultivated tea in the presence of shade trees and nitrogenous manure. Emp.J. Exp. Agr. 29:287-298. Bezbaruah, H. P. 1967. Tea chromosomes. Two Bud 14:96. Bezbaruah, H. P. 1968. Genetic improvement of tea in North-East India-its problems and possibilities. Ind. J. Genet. 28:126-34. Bezbaruah, H. P. 1971. Cytological investigation in the family Theaceae. I. Chromosome number in some Camellia sps. and allied genera. Caryologia 24:4. Bezbaruah, H. P. 1975. Development of flower, pollination and seed set in tea in N.E. India. Two Bud 22:25-30. Bezbaruah, H. P. and B. C. Barbara. 1983. Recent developments in bringing up of young tea into bearing some theoretical and practical considerations. Two Bud 30:29-37. Bezbaruah, H. P. and L. R. Saikia. 1977. Variation in self and cross compatibility in tea (Camellia sinensis L.)-a summary of 40 years pollination results at Tocklai. Two Bud 24:21-26. Bezbaruah, H. P., and I. D. Singh. 1980. Characteristics of Tocklai released planting materials. Two Bud 27:6-8. Bond, T. E. T. 1942. Studies in the vegetative growth and anatomy of the tea plant (Camellia thea Link.) with special reference to the phloem. I. The flush shoot. Ann. Bot. 6:607-630. Bond, T. E. T. 1945. Studies in the vegetative growth and anatomy of the tea plant (Camellia thea Link.) with special reference to the phloem. II. Further analysis of flushing behaviour. Ann. Bot. 9:183-216. Bonheure, D., and K C. Willson. 1992. Mineral nutrition and fertilizers. p. 269-330. In. KC. Willson and M.N. Clifford (eds.), Tea cultivation to consumption. Chapman and Hall, London. Carr, M. K. V. 1971. An assessment of some ofthe results oftea/soil/water studies in southern Tanzania. p. 21-47. In: M. K. V. Carr and Susan Carr (eds.), Water and the tea plant. Proc. TRIBA, Kenya. Chandra Mouli, B. 1993. Blister blight control: new recommendations. p.5. In: Handbook of tea culture. Sect. 13. UPASI Tea Research Inst., Valparai, India. Chang, H., and B. Bartholomew. 1984. Camellias. Timber Press, Portland, Oregon. [An edited translation of Hung-ta Chang. 1981. A taxonomy of the genus Camellia. Acta Sci. Nat. Univ. Sunyatseni, monograph ser.l:1-180.] Das, G. M., K C. Sarmah, and V. Agnihothrudu. 1959. Phytosanitary measures in tea during dormant season. Two Bud 6:14-19. Das, S. 1977. The endogenous factors reponsible for dormancy in the tea bush with particular reference to environmental conditions in North East India. Ph.D. Thesis. Gauhati Univ., Assam, India.

292

L. MANIVEL

Dev Choudhury, M. N., S. D. Ravindranath, M. R. Goswami, K. C. Thakur and N. K. Jain. 1985. Metabolic response of tea (Camellia sinensis) to excess nitrogen. Indian J. Plant Nutrn.4:7-22. Dutta, S. K. 1956. Results of pruning experiments. Two Bud 3:3-9. Dutta, S. K. 1960a. Experiments on pruning and tipping in relation to plucking. Two Bud 7:9-21. Dutta, S. K. 1960b. The tea bush and long term agricultural operations. Two Bud 7:8-11. Dutta, S. K. 1969. Pruning times and types and crop distribution. p. 39-46. Proc. 24th Conf. Tocklai Expt. Sta. Tea Res. Assn., India. Dwibedi, H. N. (ed.). 1995. Tea statistics 1993-94. p. 242. Tea Board ofIndia, Calcutta 700 001, India. Eden, T. 1976. Tea. 3rd edition. Longman Group Limited, London. p. 236. Eden, T., and J. Bond. 1941. The technique of vegetative propagation of tea. Tea Q. 14:102-105. Ellis, R. T. 1995. Tea. p. 22-27. In: J. Smartt and N.W. Simmonds (eds.), Evolution of crop plants. Longman Scientific & Technical, Essex, England. Fordham, R. 1972. Observations on the growth of roots and shoots of tea (Camellia sinensis L.) in southern Malawi. J. Hort. Sci. 47:221-229. Ghosh, P., and S. K. Dey. 1983. Designing field drainage system. Two Bud 30:9-12. Hadfield, W. 1974. Shade in North-East India tea plantations. I. The shade pattern. J. Appl. Ecol. 11: 151-176. Hampton, M. G. 1992. Production of black tea. p. 459-512. In: K. C. Willson and M. N. Clifford (eds.), Tea cultivation to consumption. Chapman and Hall, London. Hara, Y. 1996. Tea in Japan. Proc. Global advances in tea science (in press). Harler, C. R. 1964. The culture and marketing of tea. 3rd edition. Oxford Univ. Press, London. p. 126. Jain, N. K. 1988. Rationalization offertilizer recommendations in tea agro-technology. p. 31-44. In: Proc. Regional Tea (Sci.) Con£. Tea Research Inst., Sri Lanka. Jain, N. K., and M. B. Tamang. 1988. Physiological basis of tea management practices. Proc. Int. Congr. Plant Physio!., New Delhi, India. p. 460-479. Krishnamoorthy, K. K.1987. Value of tea nutritionally and therapeutically. Planters' Chron. 81:203-206. Krishnapillai, S., D. Palamulla, and S. Navaratne. 1992. Studies on tea and drought. 1. Some observations on drought effects on physiology of tea. Sri Lankan J. Tea Sci. 61:59-67. Kulasegaram, S. 1969. Studies on the dormancy of tea shoots. 2. Roots as the source of stimulus associated with the growth of dormant buds. Tea Quart. 40:84-92. Kulasegaram, S. 1986. Pruning. p. 82-87. In: P. Sivapalan, S. Kulasegaram, and A. Kathiravetpillai (eds.), Handbook of tea. Tea Research Institute, Sri Lanka. Manivel, L. 1986. Growth regulators in mature tea. Tocklai Advisory Leaflet 16. Tocklai Expt. Sta., Jorhat, Assam, India. Manivel, L. 1987. Lateral promotion in young tea. Tocklai Advisory Leaflet 17. Tocklai Expt., Sta., Jorhat, Assam, India. Manivel, L. 1988. Triacontanol in tea. p.157-164. In: P. Sivapalan and A. Kathiravetpillai (eds.), Proc. Regional Tea (Sci) Conf. Tea Research Inst., Sri Lanka. Manivel, L. 1989. Physiology of productivity in tea ofN.E.India. p. 211-215. In: S. M. Karmarkar (ed.), Strategies in physiological regulation of plant productivity. Proc. ISPP National Seminar, Bombay, India. Manivel, L. 1993. NK foliar spray to induce drought tolerance in mature tea. Handbook of tea culture. Sec. 24. UPASI Tea Research lnst., Valparai, India.

7. TEA: BOTANY AND HORTICULTURE

293

Manivel, 1., and S. Hussain. 1982a. Photosynthesis in tea. 1. Contribution ofphotosynthates to pluckable shoots by maintenance leaves. Two Bud 29:13-16. Manivel, 1., and S. Hussain. 1982b. Photosynthesis in tea. II. Direction of movement of photosynthates. Two Bud 29:49-52. Manivel, 1., S. Marimuthu, and R. Raj Kumar. 1997. Physicochemical studies on nutrition of tea. Sci. BuI. 9. Tea Board, India. p. 13. Manivel, 1., S. Marimuthu, V. Venkatesalu, and R. Raj Kumar. 1994b. Effect of potassium nutrition and growth regulators on photosynthesis and assimilate translocation in tea. p. 217-223. In: Proc. Int. Seminar on integrated crop management in tea towards higher productivity. Int. Potash Institute, Switzerland and Tea Research Institute, Sri Lanka. Manivel, 1., R. Raj Kumar, and S. Marimuthu. 1994a. Spent mushroom compost as an amendment in tea. Planters' Chron. 89:69-72. Manivel, 1., R. Raj Kumar, S. Marimuthu, and V. Venkatesalu. 1994c. Foliar application of potassium for increasing drought tolerance in tea. J. Potassium Res. 11(1):81-87. Manivel, L., R. Raj Kumar, S. Marimuthu, and V. Venkatesalu. 1995. Plant growth regulators for crop management in tea. HortScience. 30(4):802. (Abstr.) Manivel, 1., R. Raj Kumar, and V. Venkatesalu. 1993. Biostimulants in tea for crop productivity. J. Plantation Crops 21 (suppl):322-327. Marimuthu, S., 1. Manivel, and R. Raj Kumar. 1993. Hydrogen cyanamide for bud break in pruned tea. J. Plantation Crops 21 (suppl.):372-376. Marimuthu, S., R. Raj Kumar and 1. ManiveI. 1994. Factors affecting partitioning of assimilates in tea. J. Nuclear Agr. BioI .23:219-223. Marks, V. 1992. Physiological and clinical effects of tea. p. 707-740. In: K. C. Willson and M. N. Clifford (eds.), Tea cultivation to consumption. Chapman and Hall, London. Mulky, M. J. 1993. Chemistry and pharmacology of tea. p. 83-96. In: M. J. Mulky and V.S. Sharma (eds.), Tea culture, processing and marketing. Oxford and IBH Publishing Company Private Limited, New Delhi, India. Muraleedharan, N. 1991. Pest management in tea. p. 130. United Planters' Association of Southern India, Scientific Department, Tea Research Inst., Valparai, Coimbatore District, India. Muraleedharan, N. 1992. Bioecology and management of tea pests in southern India. J. Plantation Crops 20:1-20. Muraleedharan, N. 1994. Pesticide residues in tea: problems and prospects. Planters' Chron.89:371-375. Murthy. R. S. R., and V. S. Sharma. 1989. Rationalisation of plucking intervals in tea: forecasting systems. UPASI Scientific Dept. BuI. 43:6-15. Rahman, F. 1977a. Plucking of mature tea. Two Bud 24:4-7. Rahman, F. 1977b. Chemical weed control in tea. Two Bud 24:33-35. Rahman, F., and D. N. Barua. 1980. Plucking. In: Tea Encyclopaedia. 201. Tea Research Assoc., Jorhat, Assam, India. Raj Kumar, R. 1995. Influence of plant growth regulators on developmental, physiological and biochemical features of tea (Camellia sinensisjL.) O. Kuntze). Ph.D. Thesis. Bharathiar Univ., Coimbatore, India. Raman, K., and P. C. Cheng. 1981. Comparative foliar anatomical studies of clonal teas. p. 413-424. In: S. Vishveshwara (ed.-in-chief), Genetics, plant breeding and horticulture. PLACROSYM-IV. Printers India Ltd., Bangalore, India. Ranganathan, V., and S. Natesan. 1987. Manuring oftea. Revised recommendations. Handbook of tea culture. Sec. 11. UPASI Tea Research Inst., India. Rao, V. S. 1978. Herbicide mixtures in tea. Two Bud 25:15-16. Rao, V. S., and F. Rahman. 1978. Weed control in tea with glyphosate. Two Bud 25:71-73.

294

L. MANIVEL

Roberts, E. A. H. 1949. Tea manufacture. 7th Ann. Conf., Tocklai Expt. Sta., ]orhat, Assam, India. Roberts, G. E., and A.J. Keys. 1978. Mechanism of photosynthesis in tea plant (Camellia sinensis L.). J. Expt. Bot. 29:1403-1407. Roberts, G. R. 1986. Principles of tea manufacture. p. 154-158. In: P. Sivapalan, S. Kulasegaram, and A. Kathiravetpillai (eds.), Handbook of tea. Tea Res. Inst., Sri Lanka. Samaraveera, D. S. A. 1986. Technology of tea processing. p. 158-207. In: P. Sivapalan, S. Kulasegaram, and A. Kathiravetpillai (eds.), Handbook of tea. Tea Res. Inst., Sri Lanka. Sandanam, S. 1986. Cultural operations. p. 45-62. In: P. Sivapalan, S. Kulasegaram, and A.Kathiravetpillai (eds.), Handbook of tea. Tea Res. Inst., Sri Lanka. Sarronwala, B. K. 1980. The planters' handbook. Tea Research Assn., Calcutta, India. Satyanarayana, G. 1977. Important diseases of mature tea in N.E. India. p .54-55. In: 28th Ann. Conf., Tocklai Expt. Sta., Jorhat. Assam, India. Satyanarayana, G. 1981. Silent maladies of tea. p. 19-20. In: 29th Annual Conf., Tocklai Expt. Sta., Jorhat, Assam, India. Satyanarayana, N., S. Cox, and V. S. Sharma. 1992. Field performance of grafts made on fresh tea clonal cuttings. J. Plantation Crops (suppl.) 20:151-156. Satyanarayana, N., R. V. J. Hango, Ch. Sreedhar, and V. S. Sharma. 1994. Weeds in tea fields multidimensional management programme. Planters' Chron. 89:527-531. Sealy, J. B. 1958. A revision of the genus Camellia. Royal Hort. Soc., London. Senaratne, K. A. D. W. 1986. Insect and mite pests of tea. In: P. Sivapalan, S. Kulasegaram, and A. Kathiravetpillai (eds.). Handbook of tea. Tea Res. Inst., Sri Lanka. Sharma, V. S. 1979. Growth rhythm of tea shoots. DPASI Tea Sci. Dept. Bull. 36:9-11. Sharma,V. S. 1987. Harvesting in tea. Planters' Chron. 81:261-266. Sharma, V. S., M. Mohanan, and A.T. Selvan. 1981. Biology of flower in some tea (Camellia spp.) clones of southern India. p. 375-383. In: S. Vishveshwara (ed.-in-chieO, Genetics, plant breeding and horticulture. PLACROSYM-IV. Printers India Ltd., Bangalore, India. Sharma,V. S., N. Satyanarayana, C. P. D. Joseph, V. Govindarajulu. M. Surendra Mohan, and J. B. Hudson. 1992. Productivity in relation to severity of plucking of tea. J. Plantation Crops 20(suppl.):260-266. Singh. B. 1978. Prediction of drainage and irrigation requirement of tea, based on meteorological data. Two Bud 25:75-79. Singh, B. 1979. Problems of open drainage in flat lands. Two Bud 26:26-31. Singh, B. 1988. Diagnosis and investigation of drainage problems. p. 1-16. In: B.Singh (ed.), Drainage for tea. Tocklai Expt.Sta., Assam. Singh, B., D. S. Phukan, and B. P. Sakia. 1980. Water table behaviour with pipe drainage in tea soils. Two Bud 27:24-30. Tunstall, A. C. 1931. A note on the propagation of tea by green shoot cuttings. Quart. J. Ind. Tea Assn. 49-51. Venkataramani, K. S., and V. S. Sharma. 1975. Notes on the DPASI tea clones approved by Tea Board and released for commercial planting. Planters' Chron. 70:119-121. Venkataramani, K. S., and C. S.Venkataram. 1968. Rejuvenation pruning. Planters' Chron. 63:156-157. Venkatesalu, V., L. Manivel, and R. Raj Kumar. 1993. Effect of antitranspirants in tea. J. Plantation Crops 21 (suppl.):366-371. Venkatesalu, V., R. Raj Kumar, L. Manivel, and S. Marimuthu. 1994. Growth regulators in bringing up of young tea. J. Plantation Crops 24(suppl.):643-646. Verma, D. P. 1997. Balanced fertilizer for sustainable productivity of tea. Fertilizer News 42 (4):113-125.

7. TEA: BOTANY AND HORTICULTURE

295

Watson, M. 1986. Plucking. p. 78-81. In: P. Sivapalan, S. Kulasegaram, and A. Kathiravetpillai (eds.), Handbook of tea. Tea Research Institute, Sri Lanka. Wealth of India. 1950. A directory of Indian raw materials and industrial products. Vol. II. S. S. Bhatnagar. Chairman, Editorial Committee, Council of Scientific and Industrial Res., New Delhi, India. p. 26-51. Wight, W. 1955. Commercial propagation of Camellia sinensis in India. Am.Camellia Yearb.88-100. Wight, W. 1956. Commercial selection and breeding of tea in India. World Crops 8:263-268. Wight. W. 1958.The agrotype concept in tea taxonomy. Nature 181:893-895. Wight, W. 1959. Nomenclature and classification ofthe tea plant. Nature 183:1726-1728. Wight, W. 1962. Tea classification revised. Curro Sci. 31:298-299. Wight, W., and R. C. J. H. Gilchrist. 1961a. The concept of kind of tea. Nature 191:14-16. Wight, W., and R. C. J. H. Gilchrist. 1961b. Concerning the quality and morphology oftea. Rep. ITA, TES for 1959. p. 69-86. Willson, K. c., and M. N. Clifford (eds.). 1992. Tea cultivation to consumption. Chapman and Hall, London. Wu, C. T. 1964. Studies on heredity. variation and morphology ofpubesence on the young shoots of tea plant. Bul. Pinchen Tea Exp. Sta. 20:1-23. Wu, C. T., and I. S. Shyu. 1966. Studies on the utilization of heterosis in tea plant. Bul. Pinchen Tea Exp. Sta. 32:1-17. Zongmao, C. 1994. Tea science in the year 2000 with special reference to China. p. 51-59. In: Proc. International Seminar on integrated crop management in tea: towards higher productivity. Int. Potash Res. Inst., Switzerland and Tea Res. Inst., Sri Lanka.

Subject Index

A

H

Apricot, origin and dissemination, 225-266 Avocado, CA and MA, 135-141

Heat treatment (postharvest), 91-121 L

Lanzon, CA and MA, 149; 150

B

Leucospermum, 27-90

Banana, CA and MA, 141-146 Banksia, 1-25

Loquat, CA and MA, 149-150 Lychee, CA and MA, 150

C

M

CA for tropical fruits, 123-183 Cherimoya, CA and MA, 146-147 Custard apple, CA and MA, 164

Mango, CA and MA, 151-157 Mangosteen, CA and MA, 157 Modified atmosphere for tropical fruits, 123-183

D N

Dedication: Dennis, F. G., xi-xii Durian, CA and MA, 147-148 F

Feijoa, CA and MA, 148 Floricultural crops: Banksia, 1-25 Leucospermum, 27-90

Flower and flowering: Banksia, 1-25 Leucospermum,27-90

Fruit Crops: Apricot, origin and dissemination, 225-266 CA and MA for tropicals, 123-183

296

Nitrogen, vegetable crops, 185-223 Nutrition (plant), nitrogen in vegetable crops, 185-223

o Ornamental plants: Banksia, 1-25 Leucospermum, 27-90

p

Papaya, CA and MA, 157-160 Passion fruit, CA and MA, 160-161 Pineapple, CA and MA, 161-162

SUBJECT INDEX

Plantain, CA and MA, 141-146 Postharvest physiology: CA for tropical fruit, 123-183 Heat treatment. 91-121 MA for tropical fruit, 123-183 Protaceous flower crop: Banksia, 1-25 Leucospermum, 27-90 R

297

Sugar apple, CA and MAt 164 Sweet sop, CA and MA, 164 T

Teat botany and horticulture, 267-295

v

Rambutan, CA and MA, 163

Vegetable crops, N nutrition, 185-223

s

w

Sapodilla, CA and MAt 164

Wax apple, CA and MA, 164

Cumulative Subject Index (Volumes 1-22) A

Abscisic acid: chilling injury 15:78-79 cold hardiness, 11 :65 dormancy, 7:275-277 genetic regulation, 16:9-14,20-21 mechanical stress, 17:20 rose senescence, 9:66 stress, 4:249-250 Abscission: anatomy and histochemistry, 1:172-203

citrus, 15:145-182, 163-166 flower and petals, 3:104-107 regulation, 7:415-416 rose, 9:63-64 Acclimatization: foliage plants, 6:119-154 herbaceous plants, 6:379-395 micropropagation, 9:278-281, 316-317

A c tinidia , 6:4-12 Adzuki bean, genetics, 2:373 Agaricus, 6:85-118 Agrobacterium tumefaciens, 3:34 Air pollution, 8:1-42 Almond: bloom delay, 15:100-101 in vitro culture, 9:313 postharvest technology and utilization, 20:267-311 Alocasia, 8:46, 57, see also Aroids Alternate bearing: chemical thinning, 1:285-289 fruit crops, 4:128-173 298

pistachio, 3:387-388 Aluminum: deficiency and toxicity symptoms in fruits and nuts, 2:154 Ericaceae, 10:195-196 AmorphophalJus, 8:46, 57, see also Aroids Anatomy and morphology: apple flower and fruit, 10:273-308 apple tree, 12:265-305 asparagus, 12:71 cassava, 13:106-112 citrus, abscission, 15:147-156 embryogenesis, 1:4-21, 35-40 fig, 12:420-424 fruit abscission, 1:172-203 fruit storage, 1:314 ginseng, 9:198-201 grape flower, 13:315-337 grape seedlessness, 11:160-164 heliconia, 14:5-13 kiwifruit, 6:13-50 magnetic resonance imaging, 20:78-86, 225-266

orchid, 5:281-283 navel orange, 8:132-133 pecan flower, 8:217-255 petal senescence, 1:212-216 pollution injury, 8:15 Androgenesis, woody species, 10:171-173

Angiosperms, embryogenesis, 1:1-78

Anthurium. See also Aroids, ornamental fertilization, 5:334-335

299

CUMULATIVE SUBJECT INDEX

Antitranspirants, 7:334 cold hardiness, 11 :65 Apical meristem, cryopreservation, 6:357-372

Apple: alternate bearing, 4:136-137 anatomy and morphology of flower and fruit, 10:273-309 bitter pit, 11:289-355 bioregulation, 10:309-401 bloom delay, 15:102-104 CA storage, 1 :303-306 chemical thinning, 1:270-300 fertilization, 1:105 fire blight control, 1:423-474 flavor, 16:197-234 flower induction, 4:174-203 fruit cracking and splitting,

Artemisia, 19:319-371 Artemisinin, 19:346-359 Artichoke, CA storage, 1:349-350 Asexual embryogenesis, 1:1-78; 2:268-310; 3:214-314; 7:163-168, 171-173,176-177, 184,185-187,187-188, 189, 10:153-181, 14:258-259, 337-339

Asparagus: CA storage, 1:350-351 fluid drilling of seed, 3:21 postharvest biology, 12:69-155 Auxin: abscission, citrus, 15:161, 168176

bloom delay, 15:114-115 citrus abscission, 15:161, 168-176 dormancy, 7:273-274 flowering, 15:290-291, 315 genetic regulation 16:5-6, 14,

19:217-262

fruiting, 11 :229-287 in vitro, 5:241-243; 9:319-321 light, 2:240-248 maturity indices, 13:407-432 mealiness, 20:200 nitrogen metabolism, 4:204-246 replant disease, 2:3 root distribution, 2:453-456 stock-scion relationships, 3:315-375

summer pruning, 9:351-375 tree morphology and anatomy, 12:265-305

vegetative growth, 11 :229-287 watercore, 6:189-251 yield, 1 :397-424 Apricot: bloom delay, 15:101-102 CA storage, 1:309 origin and dissemination, 22:225-266

Aroids: edible, 8:43-99; 12:166-170 ornamental, 10:1-33 Arsenic, deficiency and toxicity symptoms in fruits and nuts, 2:154

21-22

geotropism, 15:246-267 mechanical stress, 17:18-19 petal senescence, 11:31 Avocado: CA and MA, 135-141 flowering, 8:257-289 fruit development, 10:230-238 fruit ripening, 10:238-259 rootstocks, 17:381-429 Azalea, fertilization, 5:335-337 B

Babaco, in vitro culture, 7:178 Bacteria: diseases of fig, 12:447-451 ice nucleating, 7:210-212, 11:69-71

pathogens of bean, 3:28-58 tree short life, 2:46-47 wilt of bean, 3:46-47 Bacteriocides, fire blight, 1:450-459 Bacteriophage, fire blight control, 1:449-450

CUMULATIVE SUBJECT INDEX

300

Banana: CA and MA, 22:141-146 CA storage, 1:311-312 fertilization, 1:105 in vitro culture, 7:178-180 Banksia, 22:1-25 Bean: CA storage, 1 :352-353 fluid drilling of seed, 3:21 resistance to bacterial pathogens, 3:28-58

Bedding plants, fertilization,

Brassicaceae, in vitro, 5:232-235 Breeding, see Genetics and breeding Broccoli, CA storage, 1:354-355 Brussels sprouts, CA storage, 1:355 Bulb crops. See a/so Tulip genetics and breeding, 18:119123 in vitro, 18:87169 micropropagation, 18:89113 root physiology, 14:5788 virus elimination, 18:113-123

c

1:99-100; 5:337-341

Beet: CA storage, 1:353 fluid drilling of seed, 3:18-19 Begonia (Rieger), fertilization, 1:104 Biochemistry, petal senescence, 11:15-43

Biennial bearing, see Alternate bearing Bioregulation. See a/so Growth substances apple and pear, 10:309-401

Bird damage, 6:277-278 Bitter pit in apple, 11 :289-355 Blackberry harvesting, 16:282-298 Black currant, bloom delay, 15:104 Bloom delay, deciduous fruits, 15:97 Blueberry: developmental physiology, 13:339-405

harvesting, 16:257-282 nutrition, 10:183-227 Botanic gardens, 15:1-62 Boron: deficiency and toxicity symptoms in fruits and nuts, 2:151-152 foliar application, 6:328 nutrition, 5:327-328 pine bark media, 9:119-122 Bramble, harvesting, 16:282-298 Branching, lateral apple, 10:328-330 pear, 10:328-330

CA storage, see Controlledatmosphere storage Cabbage: CA storage, 1:355-359 fertilization, 1:117-118 Cactus: crops, 18:291-320 reproductive biology, 18:321-346 Caladium, see Aroids, ornamental Calcifuge. nutrition, 10:183-227 Calciole, nutrition, 10:183-227 Calcium: bitter pit, 11 :289-355 cell wall, 5:203-205 container growing, 9:84-85 deficiency and toxicity symptoms in fruits and nuts, 2:148-149 Ericaceae nutrition, 10:196-197 foliar application, 6:328-329 fruit softening, 10:107-152 nutrition, 5:322-323 pine bark media, 9:116-117 tipburn, disorder, 4:50-57 Calmodulin, 10:132-134, 137-138 Carbohydrate: fig, 12:436-437 kiwifruit partitioning, 12:318-324 metabolism, 7:69-108 partitioning, 7:69-108 petal senescence, 11: 19-20 reserves in deciduous fruit trees, 10:403-430

301

CUMULATIVE SUBJECT INDEX

Carbon dioxide, enrichment,

Chlorosis, iron deficiency induced,

7:345-398, 544-545 Carnation, fertilization, 1:100; 5:341-345

Chrysanthemum fertilization,

Carrot: CA storage, 1:362-366 fluid drilling of seed, 3:13-14 Caryophyllaceae, in vitro, 5:237-239 Cassava, 12:158-166; 13:105-129 Cauliflower, CA storage, 1:359-362 Celeriac, CA storage, 1:366-367 Celery: CA storage, 1:366-367 fluid drilling of seed, 3:14 Cell culture, 3:214-314 woody legumes, 14:265-332 Cell membrane: calcium, 10:126-140 petal senescence, 11:20-26 Cellular mechanisms, salt tolerance, 16:33-69

Cell wall: calcium, 10:109-122 hydrolases, 5:169-219 ice spread, 13:245-246 tomato, 13:70-71 Chelates, 9:169-171 Cherimoya, CA and MA, 22:146147

Cherry: bloom delay, 15:105 CA storage, 1:308 origin, 19:263-317 Chestnut: blight, 8:281-336 in vitro culture, 9:311-312 Chicory, CA storage, 1:379 Chilling: injury, 4:260-261,15:63-95 pistachio, 3:388-389 Chlorine: deficiency and toxicity symptoms in fruits and nuts, 2:153 nutrition, 5:239

9:133-186 1:100-101; 5:345-352

Citrus: abscission, 15:145-182 alternate bearing, 4:141-144 asexual embryogenesis, 7:163-168 CA storage, 1:312-313 chlorosis, 9:166-168 cold hardiness, 7:201-238 fertilization, 1:105 flowering, 12:349-408 honey bee pollination, 9:247-248 in vitro culture, 7:161-170 juice loss, 20:200-201 navel orange, 8:129-179 nitrogen metabolism, 8:181 rootstock, 1:237-269 Cloche (tunne}), 7:356-357 Coconut palm: asexual embryogenesis, 7:184 in vitro culture, 7:183-185 Cold hardiness, 2:33-34 apple and pear bioregulation, 10:374-375

citrus, 7:201-238 factors affecting, 11:55-56 herbaceous plants, 6:373-417 injury, 2:26-27 nutrition, 3:144-171 pruning, 8:356-357 Colocasia, 8:45, 55-56. See also Aroids Common blight of bean, 3:45-46 Compositae, in vitro, 5:235-237 Container production, nursery crops, 9:75-101

Controlled environment agriculture, 7:534-545. See also Greenhouse and greenhouse crops; hydroponic culture; protected culture Controlled-atmosphere (CA) storage: asparagus, 12:76-77,127-130

302

Controlled-atmosphere (CA) storage (cont'd) chilling injury, 15:74-77 flowers, 3:98, 10:52-55 fruit quality, 8:101-127 fruits, 1:301-336; 4:259-260 pathogens, 3:412-461 seeds, 2:134-135 tropical fruit, 22:123-183 tulip, 5:105 vegetable quality, 8:101-127 vegetables, 1:337-394; 4:259-260 Copper: deficiency and toxicity symptoms in fruits and nuts, 2:153 foliar application, 6:329-330 nutrition, 5:326-327 pine bark media, 9:122-123 Corynebacterium flaccumfaciens, 3:33,46 Cowpea: genetics, 2:317-348 U.S. production, 12:197-222 Cranberry: botany and horticulture, 21:215-249 fertilization, 1:106 harvesting, 16:298-311 Cryphonectria parasitica, see Endothia parasitica Cryopreservation apical meristems, 6:357-372 cold hardiness, 11:65-66 Crytosperma, 8:47, 58. See also Aroids Cucumber, CA storage, 1:367-368 Currant, harvesting, 16:311-327 Custard apple, CA and MA, 22:164 Cytokinin: cold hardiness; 11:65 dormancy, 7:272-273 floral promoter, 4:112-113 flowering, 15:294-295, 318 genetic regulation, 16:4-5, 14, 22-23 grape root, 5:150, 153-156 lettuce tipburn, 4:57-58

CUMULATIVE SUBJECT INDEX

petal senescence, 11:30-31 rose senescence, 9:66

D Date palm: asexual embryogenesis, 7:185-187 in vitro culture, 7:185-187 Daylength, see Photoperiod Dedication: Bailey, L. H., l:v-viii Beach, S. A., l:v-viii Bukovac, M. J., 6:x-xii Campbell, C. W., 19:xiii Cummins, J. N., 15:xii-xv Dennis, F. G., 22:xi-xii Faust, Miklos, 5:vi-x Hackett, W. P., 12:x-xiii Halevy, A. H., 8:x-xii Hess, C. E., 13:x-xii Kader, A. A., 16:xii-xv Looney, N. E., 18:xiii Magness, J. R., 2:vi-viii Moore, J. N., 14:xii-xv Pratt, c., 20:ix-xi Proebsting, Jr., E. L., 9:x-xiv Rick, Jr., C. M., 4:vi-ix Sansavini, S., 17:xii-xiv Sherman, W. B., 21:xi-xiii Smock, R. M., 7:x-xiii Weiser, C. J., 11:x-xiii Whitaker, T. W., 3:vi-x Wittwer, S. H., 10:x-xiii Deficiency symptoms, in fruit and nut crops, 2:145-154 Deficit irrigation, 21:105-131 Defoliation, apple and pear bioregulation, 10:326-328 'Delicious' apple, 1:397-424 Desiccation tolerance, 18:171-213 Dieffenbachia, see Aroids, ornamental Dioscorea, see Yam Disease: and air pollution, 8:25 aroids, 8:67-69; 10:18; 12:168-169

CUMULATIVE SUBJECT INDEX

bacterial, of bean, 3:28-58 cassava, 12:163-164 control by virus, 3:399-403 controlled-atmosphere storage, 3:412-461 cowpea, 12:210-213 fig, 12:447-479 flooding, 13:288-299 hydroponic crops, 7:530-534 lettuce, 2:187-197 mycorrhizal fungi, 3:182-185 ornamental aroids, 10:18 resistance, acquired, 18:247-289 root, 5:29-31 stress, 4:261-262 sweet potato, 12:173-175 tulip, 5:63, 92 turnip mosaic virus, 14:199-238 yam (Dioscorea), 12:181-183 Disorder. See also Postharvest physiology bitterpit, 11:289-355 fig, 12:477-479 pear fruit, 11:357-411 watercore, 6:189-251; 11:385-387 Dormancy, 2:27-30 blueberry, 13:362-370 release in fruit trees, 7:239-300 tulip,5:93 Drip irrigation, 4:1-48 Drought resistance, 4:250-251 cassava, 13:114-115 Durian, CA and MA, 22:147-148 Dwarfing: apple, 3:315-375 apple mutants, 12:297-298 by virus, 3:404-405 E

Easter lily, fertilization, 5:352-355 Embryogenesis, see Asexual embryogenesis

Endothia parasitica, 8:291-336 Energy efficiency, in greenhouses, 1:141-171; 9:1-52

303

Environment: air pollution, 8:20-22 controlled for agriculture, 7:534-545 controlled for energy efficiency, 1:141-171,9:1-52 embryogenesis, 1:22,43-44 fruit set, 1:411-412 ginseng, 9:211-226 greenhouse management, 9:32-38 navel orange, 8:138-140 nutrient film technique, 5:13-26 Epipremnum, see Aroids, ornamental

Erwinia: amylovora, 1:423-474 lathyri, 3:34 Essential elements: foliar nutrition, 6:287-355 pine bark media, 9:103-131 plant nutrition 5:318-330 soil testing, 7:1-68 Ethylene: abscission, citrus, 15:158-161, 168-176 apple bioregulation, 10:366-369 avocado, 10:239-241 bloom delay, 15:107-111 CA storage, 1:317-319, 348 chilling injury, 15:80 citrus abscission, 15:158-161, 168-176 cut flower storage, 10:44-46 dormancy, 7:277-279 flowering, 15:295-296, 319 flower longevity, 3:66-75 genetic regulation, 16:6-7, 14-15, 19-20 kiwifruit respiration, 6:47-48 mechanical stress, 17:16-17 petal senescence, 11:16-19, 27-30 rose senescence, 9:65-66 F Feed crops, cactus, 18:298-300 Feijoa, CA and MA, 22:148

304

Fertilization and fertilizer: anthurium, 5:334-335 azalea, 5:335-337 bedding plants, 5:337-341 blueberry, 10:183-227 carnation, 5:341-345 chrysanthemum, 5:345-352 controlled release, 1:79-139; 5:347-348 Easter lily, 5:352-355 Ericaceae, 10:183-227 foliage plants, 5:367-380 foliar, 6:287-355 geranium, 5:355-357 greenhouse crops, 5:317-403 lettuce, 2:175 nitrogen, 2:401-404 orchid,5:357-358 poinsettia, 5:358-360 rose, 5:361-363 snapdragon, 5:363-364 soil testing, 7:1-68 trickle irrigation, 4:28-31 tulip, 5:364-366 Vaccinium, 10:183-227

Fig: industry, 12:409-490 ripening, 4:258-259 Filbert, in vitro culture, 9:313-314 Fire blight, 1:423-474 Flooding: fruit crops, 13:257-313 Floricultural crops. See also individual crops Banksia, 22:1-25 fertilization, 1:98-104 growth regulation, 7:399-481 heliconia, 14:1-55 Leucospermum, 22:27-90

postharvest physiology and senescence, 1:204-236; 3:59-143; 10:35-62; 11:1543 Florigen, 4:94-98 Flower and flowering: alternate bearing, 4:149

CUMULATIVE SUBJECT INDEX

apple anatomy and morphology, 10:277-283 apple bioregulation, 10:344-348 aroids, ornamental, 10:19-24 avocado, 8:257-289 Banksia, 22:1-25

blueberry development, 13:354-378 cactus, 18:325-335 citrus, 12:349-408 control, 4:159-160,15:279-334 development (postpollination), 19:1-58 fig, 12:424-429 grape anatomy and morphology, 13:354-378 honey bee pollination, 9:239-243 induction, 4:174-203; 254-256 initiation, 4:152-153 in vitro, 4:106-127 kiwifruit, 6:21-35; 12:316-318 Leucospermum, 22:27-90

orchid, 5:297-300 pear bioregulation, 10:344-348 pecan, 8:217-255 perennial fruit crops, 12:223-264 phase change, 7:109-155 photoperiod, 4:66-105 pistachio, 3:378-387 postharvest physiology, 1:204-236; 3:59-143; 10:35-62; 11:15-43 postpollination development; 19:1-58 protea leaf blackening, 17:173-201 pruning,8:359-362 raspberry, 11:187-188 regulation in floriculture, 7:416-424 rhododendron, 12:1-42 rose, 9:60-66 senescence, 1:204-236; 3:59-143; 10:35-62; 11:15-43; 18:1-85 sugars, 4:114 thin cell layer morphogenesis, 14:239-256

CUMULATIVE SUBJECT INDEX

tulip, 5:57-59 water relations, 18:1-85 Fluid drilling, 3:1-58 Foliage plants: acclimatization, 6:119-154 fertilization, 1:102-103; 5:367-380 Foliar nutrition, 6:287-355 Freeze protection, see Frost protection Frost: apple fruit set, 1:407-408 citrus, 7:201-238 protection, 11:45-109 Fruit: abscission, 1:172-203 abscission, citrus, 15:145-182 apple anatomy and morphology, 10:283-297

apple bioregulation, 10:348-374 apple bitter pit, 11 :289-355 apple flavor, 16:197-234 apple maturity indices, 13:407-432

apple ripening and quality, 10:361-374

avocado development and ripening, 10:229-271 bloom delay, 15:97-144 blueberry development, 13:378-390

cactus physiology, 18:335-341 CA storage and quality, 8:101-127 chilling injury, 15:63-95 cracking, 19:217-262 diseases in CA storage, 3:412-461 drop, apple and pear, 10:359-361 fig, 12:424-429 kiwifruit, 6:35-48; 12:316-318 maturity indices, 13:407-432 navel orange, 8:129-179 nectarine, postharvest, 11 :413-452 nondestructive postharvest quality evaluation, 20:1-119 peach, postharvest, 11:413-452 pear, bioregulation, 10:348-374 pear, fruit disorders, 11:357-411

305

pear maturity indices, 13:407-432 pear ripening and quality, 10:361-374

pistachio, 3:382-391 quality and pruning, 8:365-367 ripening, 5:190-205 set, 1:397-424; 4:153-154 set in navel oranges, 8:140-142 size and thinning, 1:293-294; 4:161

softening, 5:109-219, 10:107-152 splitting, 19:217-262 strawberry growth and ripening, 17:267-297

texture, 20:121-224 thinning, apple and pear, 10:353-359

tomato parthenocarpy, 6:65-84 tomato ripening, 13:67-103 Fruit crops: alternate bearing, 4:128-173 apple bitter pit, 11:289-355 apple flavor, 16:197-234 apple fruit splitting and cracking, 19:217-262

apple growth, 11:229-287 apple maturity indices, 13:407-432

apricot, origin and dissemination, 22:225-266

avocado flowering, 8:257-289 avocado rootstocks, 17:381-429 berry crop harvesting, 16:255-382 bloom delay, 15:97-144 blueberry developmental physiology, 13:339-405 blueberry harvesting, 16:257-282 blueberry nutrition, 10:183-227 bramble harvesting, 16:282-298 cactus, 18:302-309 carbohydrate reserves, 10:403-430 CA and MA for tropicals, 22:123-183

CA storage, 1:301-336 CA storage diseases, 3:412-461 cherry origin, 19:263-317

CUMULATIVE SUBJECT INDEX

306

Fruit crops (cont'd) chilling injury, 15:145-182 chlorosis, 9:161-165 citrus abscission, 15:145-182 citrus cold hardiness, 7:201-238 citrus flowering, 12:349-408 cranberry, 21:215-249 cranberry harvesting, 16:298-311 currant harvesting, 16:311-327 deficit irrigation, 21:105-131 dormancy release, 7:239-300 Ericaceae nutrition, 10:183-227 fertilization, 1:104-106 fig, industry, 12:409-490 fireblight, 11:423-474 flowering, 12:223-264 foliar nutrition, 6:287-355 frost control, 11:45-109 grape flower anatomy and morphology, 13:315-337 grape harvesting, 16:327-348 grape nitrogen metabolism, 14:407-452 grape pruning, 16:235-254, 336-340 grape root, 5:127-168 grape seedlessness, 11:164-176 grapevine pruning, 16:235-254, 336-340 honey bee pollination, 9:244-250, 254-256 jojoba, 17:233-266 in vitro culture, 7:157-200; 9:273-349 irrigation, deficit, 21:105-131 kiwifruit, 6:1-64; 12:307-347 longan, 16:143-196 lychee, 16:143-196 muscadine grape breeding, 14:357-405 navelorange,8:129-179 nectarine postharvest, 11 :413-452 nondestructive postharvest quality evaluation 20:1-119 nutritional ranges, 2:143-164

olive salinity tolerance, 21:177-214 orange, navel, 8:129-179 orchard floor management, 9:377-430 peach origin, 17:331-379 peach postharvest, 11 :413-452 pear fruit disorders, 11 :357-411 pear maturity indices, 13:407-432 pecan flowering, 8:217-255 photosynthesis, 11:111-157 Phytophthora control, 17:299-330 pruning, 8:339-380 rambutan, 16:143-196 raspberry, 11:185-228 roots, 2:453-457 sapindaceous fruits, 16:143-196 short life and replant problem, 2:1-116 strawberry fruit growth, 17:267-297 strawberry harvesting, 16:348-365 summer pruning, 9:351-375 Vaccinium nutrition, 10:183-227 water status, 7:301-344 Fungi: fig, 12:451-474 mushroom, 6:85-118 mycorrhiza, 3:172-213; 10:211-212 pathogens in postharvest storage, 3:412-461 truffle cultivation, 16:71-107 Fungicide, and apple fruit set, 1:416 G

Garlic, CA storage, 1:375 Genetic variation: alternate bearing, 4:146-150 photoperiodic response, 4:82 pollution injury, 8:16-19 temperature-photoperiod interaction, 17:73-123 Genetics and breeding:

CUMULATIVE SUBJECT INDEX

aroids (edible), 8:72-75; 12:169 aroids (ornamental), 10:18-25 bean, bacterial resistance, 3:28-58 bloom delay in fruits, 15:98-107 bulbs, flowering, 18:119-123 cassava, 12:164 chestnut blight resistance, 8:313-321

citrus cold hardiness, 7:221-223 cranberry, 21:236-239 embryogenesis, 1:23 fig, 12:432-433 fire blight resistance, 1:435-436 flowering, 15:287-290, 303-305, 306-309,314-315

flower longevity, 1:208-209 ginseng, 9:197-198 in vitro techniques, 9:318-324; 18:119-123

lettuce, 2:185-187 muscadine grapes, 14:357-405 mushroom, 6:100-111 navel orange, 8:150-156 nitrogen nutrition, 2:410-411 pineapple, 21:138-164 plant regeneration, 3:278-283 pollution insensitivity, 8:18-19 potato tuberization, 14:121-124 rhododendron, 12:54-59 sweet potato, 12:175 sweet sorghum, 21:87-90 tomato parthenocarpy, 6:69-70 tomato ripening, 13:77-98 tree short life, 2:66-70 Vigna, 2:311-394

woody legume tissue and cell culture, 14:311-314 yam (Dioscorea), 12:183 Geophyte, see Bulb, tuber Geranium, fertilization, 5:355-357 Germination, seed, 2:117-141, 173-174

Germplasm preservation: cryopreservation, 6:357-372 in vitro, 5:261-264; 9:324-325

307

pineapple, 21:164-168 Germplasm resources: pineapple, 21:133-175 Gibberellin: abscission, citrus, 15:166-167 bloom delay, 15:111-114 citrus, abscission, 15:166-167 cold hardiness, 11:63 dormancy, 7:270-271 floral promoter, 4:114 flowering, 15:219-293, 315-318 genetic regulation, 16:15 grape root, 5:150-151 mechanical stress, 17:19-20 Ginseng, 9:187-236 Girdling, 4:251-252 Glucosinolates, 19:99-215 Graft and grafting: incompatibility, 15:183-232 phase change, 7:136-137, 141-142 rose, 9:56-57 Grape: CA storage, 1:308 chlorosis, 9:165-166 flower anatomy and morphology, 13:315-337

harvesting, 16:327-348 muscadine breeding, 14:357-405 nitrogen metabolism, 14:407-452 pollen morphology, 13:331-332 pruning, 16:235-254, 336-340 root, 5:127-168 seedlessness, 11:159-187 sex determination, 13:329-331 Gravitropism, 15:233-278 Greenhouse and greenhouse crops: carbon dioxide, 7:357-360, 544-545

energy efficiency, 1:141-171; 9:1-52

growth substances, 7:399-481 nutrition and fertilization, 5:317-403

pest management, 13:1-66 vegetables, 21:1-39

CUMULATIVE SUBJECT INDEX

308

Growth regulators, see Growth substances Growth substances, 2:60-66. See also Abscisic acid, Auxin, Cytokinins, Ethylene, Gibberellins abscission, citrus, 15:157-176 apple bioregulation, 10:309-401 apple dwarfing, 3:315-375 apple fruit set, 1:417 apple thinning, 1:270-300 aroids, ornamental, 10:14-18 avocado fruit development, 10:229-243 bloom delay, 15:107-119

H

Halo blight of beans, 3:44-45 Hardiness, 4:250-251 Harvest: flower stage, 1:211-212 index, 7:72-74 lettuce, 2:176-181 mechanical of berry crops, 16:255-382

Hazelnut, see Filbert Heat treatment (postharvest), 22:91-121

Heliconia, 14:1-55 Herbaceous plants, subzero stress,

CA storage in vegetables, 1:346-348 cell cultures, 3:214-314 chilling injury, 15:77-83 citrus abscission, 15:157-176 cold hardiness 7:223-225; 11:58-66 dormancy, 7:270-279 embryogenesis, 1:41-43; 2:277-281 floriculture, 7:399-481 flower induction, 4:190-195 flowering, 15:290-296 flower storage, 10:46-51 genetic regulation, 16:1-32 ginseng, 9:226 grape seedlessness, 11:177-180 in vitro flowering, 4:112-115 mechanical stress, 17:16-21

meristem and shoot-tip culture, 5:221-227

navel oranges, 8:146-147 pear bioregulation, 10:309-401 petal senescence, 3:76-78 phase change, 7:137-138, 142143

raspberry, 11 :196-197 regulation, 11:1-14 rose, 9:53-73 seedlessness in grape, 11:177-180 triazole, 10:63-105

6:373-417

Herbicide-resistant crops, 15:371-412

Histochemistry: flower induction, 4:177-179 fruit abscission, 1:172-203 Histology, flower induction, 4:179-184. See also Anatomy and morphology Honey bee, 9:237-272 Horseradish, CA storage, 1:368 Hydrolases, 5:169-219 Hydroponic culture, 5:1-44; 7:483-558

Hypovirulence, in Endothia parasitica, 8:299-310 I

Ice, formation and spread in tissues, 13:215-255

Ice-nucleating bacteria, 7:210-212; 13:230-235

Industrial crops, cactus, 18:309-312 Insects and mites: aroids, 8:65-66 avocado pollination, 8:275-277 fig, 12:442-447 hydroponic crops, 7:530-534 integrated pest management, 13:1-66

CUMULATIVE SUBJECT INDEX

lettuce, 2:197-198 ornamental aroids, 10:18 tree short life, 2:52 tulip, 5:63, 92 Integrated pest management: greenhouse crops, 13:1-66 In vitro: abscission, 15:156-157 apple propagation, 10:325-326 artemisia, 19:342-345 aroids, ornamental, 10:13-14 bulbs, flowering, 18:87-169 cassava propagation, 13:121-123 cellular salinity tolerance,

309

grape root growth, 5:140-141 lettuce industry, 2:175 navel orange, 8:161-162 root growth, 2:464-465

J Jojoba, 17:233-266 Juvenility, 4:111-112 pecan, 8:245-247 tulip, 5:62-63 woody plants, 7:109-155 K

16:33-69

cold acclimation, 6:382 cryopreservation, 6:357-372 embryogenesis, 1:1-78; 2:268-310; 7:157-200; 10:153-181

Kale, fluid drilling of seed, 3:21 Kiwifruit: botany, 6:1-64 vine growth, 12:307-347

environmental control, 17:123-170

flowering, 4:106-127 flowering bulbs, 18:87-169 pear propagation, 10:325-326 phase change, 7:144-145 propagation, 3:214-314; 5:221-277; 7:157-200; 9:57-58, 273-349; 17:125-172

thin cell layer morphogenesis, 14:239-264

woody legume culture, 14:265-332

Iron: defiCiency chlorosis, 9:133-186 defiCiency and toxicity symptoms in fruits and nuts, 2:150 Ericaceae nutrition, 10:193-195 foliar application, 6:330 nutrition, 5:324-325 pine bark media, 9:123 Irrigation deficit, deciduous orchards, 21:105-131

drip or trickle, 4:1-48 frost control, 11:76-82 fruit trees, 7:331-332

L

Lamps, for plant growth, 2:514531

Lanzon, CA and MA, 22:149 Leaves: apple morphology, 12:283-288 flower induction, 4:188-189 Leek: CA storage, 1:375 fertilization, 1:118 Leguminosae, in vitro, 5:227-229; 14:265-332

Lemon, rootstock, 1:244-246. See also Citrus Lettuce: CA storage, 1:369-371 fertilization, 1:118 fluid drilling of seed, 3:14-17 industry, 2:164-207 tipburn, 4:49-65 Leucospermum, 22:27-90 Light: fertilization, greenhouse crops, 5:330-331

flowering, 15:282-287, 310-312

CUMULATIVE SUBJECT INDEX

310

Light (cont'd) fruit set, 1:412-413 lamps, 2:514-531 nitrogen nutrition, 2:406-407 orchards, 2:208-267 ornamental aroids, 10:4-6 photoperiod, 4:66-105 photosynthesis, 11:117-121 plant growth, 2:491-537 tolerance, 18:215-246 Longan, see Sapindaceous fruits CA and MA, 22:150 Loquat, CA and MA, 22:149-150 Lychee. See also Sapindaceous fruits CA and MA, 22:150 M

Magnesium: container growing, 9:84-85 deficiency and toxicity symptoms in fruits and nuts, 2:148 Ericaceae nutrition, 10:196-198 foliar application, 6:331 nutrition, 5:323 pine bark media, 9:117-119 Magnetic resonance imaging, 20:78-86, 225-266

Male sterility, temperaturephotoperiod induction, 17:103-106

Mandarin, rootstock, 1:250-252 Manganese: deficiency and toxicity symptoms in fruits and nuts, 2:150-151 Ericaceae nutrition, 10:189-193 foliar application, 6:331 nutrition, 5:235-326 pine bark media, 9:123-124 Mango: alternate bearing, 4:145-146 asexual embryogenesis, 7:171-173 CA and MA, 22:151-157 CA storage, 1:313 in vitro culture, 7:171-173 Mangosteen, CA and MA, 22:157

Mechanical harvest, berry crops, 16:255-382

Mechanical stress regulation, 17:1-42

Media: fertilization, greenhouse crops, 5:333

pine bark, 9:103-131 Medicinal crops: artemisia, 19:319-371 poppy, 19:373-408 Meristem culture, 5:221-277 Metabolism: flower, 1:219-223 nitrogen in citrus, 8:181-215 seed, 2:117-141 Micronutrients: container growing, 9:85-87 pine bark media, 9:119-124 Micropropagation. See also In vitro; propagation bulbs, flowering, 18:89-113 environmental control, 17:125-172

nuts, 9:273-349 rose, 9:57-58 temperate fruits, 9:273-349 tropical fruits and palms, 7:157-200

Microtus, see Vole Modified atmosphere (MA) for tropical fruits, 22:123-183 Moisture, and seed storage, 2:125-132

Molybdenum nutrition, 5:328-329 Monocot, in vitro, 5:253-257 Monstera, see Aroids, ornamental Morphology: navel orange, 8:132-133 orchid, 5:283-286 pecan flowering, 8:217-243 Moth bean, genetics, 2:373-374 Mung bean, genetics, 2:348-364 Mushroom: CA storage, 1:371-372 cultivation, 19:59-97

CUMULATIVE SUBJECT INDEX

spawn, 6:85-118 Muskmelon, fertilization, 1:118119 Mycoplasma-like organisms, tree short life, 2:50-51 Mycorrhizae: container growing, 9:93 Ericaceae, 10:211-212 fungi, 3: 172-213 grape root, 5:145-146 N

Navel orange, 8:129-179 Nectarine: bloom delay, 15:105-106 CA storage, 1:309-310 postharvest physiology, 11:413-452 Nematodes: aroids, 8:66 fig,12:475-477 lettuce, 2:197-198 tree short life, 2:49-50 NFT (nutrient film technique), 5:1-44 Nitrogen: CA storage, 8:116-117 container growing, 9:80-82 deficiency and toxicity symptoms in fruits and nuts, 2:146 Ericaceae nutrition, 10:198-202 fixation in woody legumes, 14:322-323 foliar application, 6:332 in embryogenesis, 2:273-275 metabolism in apple, 4:204-246 metabolism in citrus, 8:181-215 metabolism in grapevine, 14:407-452 nutrition, 2:395, 423; 5:319-320 pine bark media, 9:108-112 trickle irrigation, 4:29-30 vegetable crops, 22:185-223 Nondestructive quality evaluation of fruits and vegetables, 20:1-119

311

Nursery crops: fertilization, 1:106-112 nutrition, 9:75-101 Nut crops: almond postharvest technology and utilization, 20:267-311 chestnut blight, 8:291-336 fertilization, 1:106 honey bee pollination, 9:250-251 in vitro culture, 9:273-349 nutritional ranges, 2:143-164 pistachio culture, 3:376-396 Nutrient: concentration in fruit and nut crops, 2:154-162 film technique, 5:1-44 foliar-applied, 6:287-355 media, for asexual embryogenesis, 2:273-281 media, for organogenesis, 3:214-314 plant and tissue analysis, 7:30-56 solutions, 7,:524-530 uptake, in trickle irrigation, 4:30-31 Nutrition (human): aroids, 8:79-84 CA storage, 8:101-127 Nutrition (plant): air pollution, 8:22-23, 26 blueberry, 10:183-227 calcifuge, 10:183-227 cold hardiness, 3:144-171 container nursery crops, 9:75-101 cranberry, 21:234-235 embryogenesis, 1:40-41 Ericaceae, 10:183-227 fire blight, 1:438-441 foliar, 6:287-355 fruit and nut crops, 2:143-164 ginseng, 9:209-211 greenhouse crops, 5:317-403 kiwifruit, 12:325-332 mycorrhizal fungi, 3:185-191 navel orange, 8:162-166 nitrogen in apple, 4:204-246

CUMULATIVE SUBJECT INDEX

312

Nutrition (plant) (cont'd) nitrogen in vegetable crops,

flowering bulb roots, 14:57-88 flowering bulbs in vitro,

22:185-223

18:87-169

nutrient film techniques, 5:18-21,

foliage acclimatization, 6:119-154 heliconia, 14:1-55 Leucospermum, 22:27-90 orchid pollination regulation,

31-53

ornamental aroids, 10:7-14 pine bark media, 9:103-131 raspberry, 11:194-195 slow-release fertilizers, 1:79-139

19:28-38

poppy, 19:373-408 protea leaf blackening, 17:173-201 rhododendron, 12:1-42

o Oil palm: asexual embryogenesis, 7:187-188 in vitro culture, 7:187-188 Okra: botany and horticulture, 21:41-72 CA storage, 1:372-373 Olive: alternate bearing, 4:140-141 salinity tolerance, 21:177-214 Onion: CA storage, 1:373-375 fluid drilling of seed, 3:17-18 Opium poppy, 19:373-408 Orange. See also Citrus alternate bearing, 4:143-144 sour, rootstock, 1:242-244 sweet, rootstock, 1:252-253 trifoliate, rootstock, 1:247-250 Orchard and orchard systems: floor management, 9:377-430 light, 2:208-267 root growth, 2:469-470 water, 7:301-344 Orchid: fertilization, 5:357-358 physiology, 5:279-315 pollination regulation of flower development, 19:28-38 Organogenesis, 3:214-314. See also In vitro; tissue culture Ornamental plants: Banksia, 22:1-25 chlorosis, 9:168-169 fertilization, 1:98-104, 106-116

p

Paclobutrazol, see Triazole Papaya: asexual embryogenesis, 7:176177

CA and MA, 22:157-160 CA storage, 1:314 in vitro culture, 7:175-178 Parsley: CA storage, 1:375 drilling of seed, 3:13-14 Parsnip, fluid drilling of seed, 3:13-14

Parthenocarpy, tomato, 6:65-84 Passion fruit: in vitro culture, 7:180-181 CA and MA, 22:160-161 Pathogen elimination, in vitro, 5:257-261

Peach: bloom delay, 15:105-106 CA storage, 1:309-310 origin, 17:333-379 postharvest physiology, 11:413-452

short life, 2:4 summer pruning, 9:351-375 wooliness, 20:198-199 Peach palm (Pejibaye): in vitro culture, 7:187-188 Pear: bioregulation, 10:309-401 bloom delay, 15:106-107

313

CUMULATIVE SUBJECT INDEX

CA storage, 1:306-308 decline, 2:11 fruit disorders, 11:357-411 fire blight control, 1 :423-474 in vitro, 9:321 maturity indices, 13:407-432 root distribution, 2:456 short life, 2:6 Pecan: alternate bearing, 4:139-140 fertilization, 1: 106 flowering, 8:217-255 in vitro culture, 9:314-315 Pejibaye, in vitro culture, 7:189 Pepper (Capsicum): CA storage, 1:375-376 fertilization, 1:119 fluid drilling in seed, 3:20 Persimmon: CA storage, 1:314 quality, 4:259 Pest control: aroids (edible), 12:168-169 aroids (ornamental), 10:18 cassava, 12:163-164 cowpea, 12:210-213 fig, 12:442-477 fire blight, 1:423-474 ginseng, 9:227-229 greenhouse management, 13:1-66 hydroponics, 7:530-534 sweet potato, 12:173-175 vertebrate, 6:253-285 yam (Dioscorea), 12:181-183 Petal senescence, 11:15-43 pH:

container growing, 9:87-88 fertilization greenhouse crops, 5:332-333

pine bark media, 9:114-117 soil testing, 7:8-12, 19-23 Phase change, 7:109-155 Phenology: apple, 11 :231-237 raspberry, 11:186-190 Philodendron, see Aroids, ornamental

Phosphonates, Phytophthora control, 17:299-330 Phosphorus: container growing, 9:82-84 deficiency and toxicity symptoms in fruits and nuts, 2:146-147 nutrition, 5:320-321 pine bark media, 9:112-113 trickle irrigation, 4:30 Photoautotrophic micropropagation, 17:125-172

Photoperiod, 4:66-105, 116-117; 17:73-123

flowering, 15:282-284, 310-312 Photosynthesis: cassava, 13:112-114 efficiency, 7:71-72; 10:378 fruit crops, 11:111-157 ginseng, 9:223-226 light, 2:237-238 Physiology. See also Postharvest physiology bitter pit, 11 :289-355 blueberry development, 13:339-405

cactus reproductive biology, 18:321-346

calcium, 10:107-152 carbohydrate metabolism, 7:69-108

cassava, 13:105-129 citrus cold hardiness, 7:201-238 conditioning 13:131-181 cut flower, 1:204-236; 3:59-143; 10:35-62

desiccation tolerance, 18:171-213 disease resistance, 18:247-289 dormancy, 7:239-300 embryogenesis, 1:21-23; 2:268-310

flower development, 19:1-58 flowering, 4:106-127 fruit ripening, 13:67-103 fruit softening, 10:107-152 ginseng, 9:211-213 glucosinolates, 19:99-215

314

Physiology (cont'd) heliconia, 14:5-13 juvenility, 7:109-155 light tolerance, 18:215-246 male sterility, 17:103-106 mechanical stress, 17:1-42 nitrogen metabolism in grapevine, 14:407-452 nutritional quality and CA storage, 8:118-120 olive salinity tolerance, 21:177-214 orchid,5:279-315 petal senescence, 11:15-43 photoperiodism, 17:73-123 pollution injury, 8:12-16 polyamines, 14:333-356 potato tuberization, 14:89-188 pruning, 8:339-380 raspberry, 11:190-199 regulation, 11:1-14 root pruning, 6:158-171 roots of flowering bulbs, 14:57-88 rose, 9:3-53 salinity hormone action, 16:1-32 salinity tolerance, 16:33-69 seed,2:117-141 seed priming, 16:109-141 subzero stress, 6:373-417 summer pruning, 9:351-375 thin cell layer morphogenesis, 14:239-264 tomato fruit ripening, 13:67-103 tomato parthenocarpy, 6:71-74 triazole, 10:63-105 tulip, 5:45-125 vernalization, 17:73-123 volatiles, 17:43-72 watercore, 6:189-251 water relations cut flowers, 18:1-85 Phytohormones, see Growth substances Phytophthora control, 17:299-330 Phytotoxins, 2:53-56

CUMULATIVE SUBJECT INDEX

Pigmentation: flower, 1:216-219 rose, 9:64-65 Pinching, by chemicals, 7:453-461 Pineapple: CA and MA, 22:161-162 CA storage, 1:314 genetic resources, 21:138-141 in vitro culture, 7:181-182 Pine bark, potting media, 9:103-131 Pistachio: alternate bearing, 4:137-139 culture, 3:376-393 in vitro culture, 9:315 Plantain: CA and MA, 22:141-146 in vitro culture, 7:178-180 Plant protection, short life, 2:79-84 Plum, CA storage, 1:309 Poinsettia, fertilization, 1:103-104; 5:358-360 Pollen, desiccation tolerance, 18:195 Pollination: apple, 1:402-404 avocado, 8:272-283 cactus, 18:331-335 embryogenesis, 1:21-22 fig, 12:426-429 flower regulation, 19:1-58 fruit crops, 12:223-264 fruit set, 4:153-154 ginseng, 9:201-202 grape, 13:331-332 heliconia, 14:13-15 honey bee, 9:237-272 kiwifruit,6:32-35 navel orange, 8:145-146 orchid,5:300-302 petal senescence, 11:33-35 protection, 7:463-464 rhododendron, 12:1-67 Pollution, 8:1-42 Polyamines, 14:333-356 chilling injury, 15:80 Polygalacturonase, 13:67-103

CUMULATIVE SUBJECT INDEX

Postharvest physiology: almond, 20:267-311 apple bitter pit, 11:289-355 apple maturity indices, 13:407-432 aroids, 8:84-86 asparagus, 12:69-155 CA storage and quality, 8:101127 CA for tropical fruit, 22:123-183 cut flower, 1:204-236; 3:59-143; 10:35-62 foliage plants, 6:119-154 fruit, 1:301-336 fruit softening, 10:107-152 heat treatment. 22:91-121 lettuce. 2:181-185 low-temperature sweetening. 17:203-231 MA for tropical fruit, 22:123-183 navel orange, 8:166-172 nectarine, 11:413-452 nondestructive quality evaluation, 20:1-119 pathogens, 3:412-461 peach,11:413-452 pear disorders, 11:357-411 pear maturity indices, 13:407432 petal senescence, 11:15-43 protea leaf blackening. 17:173201 quality evaluation, 20:1-119 seed,2:117-141 texture in fresh fruit, 20:121-244 tomato fruit ripening, 13:67-103 vegetables, 1:337-394 watercore, 6:189-251; 11:385387 Potassium: container growing. 9:84 deficiency and toxicity symptoms in fruits and nuts, 2:147-148 foliar application. 6:331-332 nutrition, 5:321-322

315

pine bark media, 9:113-114 trickle irrigation, 4:29 Potato: CA storage. 1:376-378 fertilization. 1:120-121 low temperature sweetening, 17:203-231 tuberization, 14:89-198 Propagation. See also In vitro apple, 10:324-326; 12:288-295 aroids, ornamental, 10:12-13 cassava, 13:120-123 floricultural crops, 7:461-462 ginseng. 9:206-209 orchid, 5:291-297 pear, 10:324-326 rose, 9:54-58 tropical fruit, palms 7:157-200 woody legumes in vitro, 14:265-332 Protaceous flower crop. See also Protea Banksia, 22:1-25 Leucospermum, 22:27-90 Protea, leaf blackening, 17:173201 Protected crops, carbon dioxide, 7:345-398 Protoplast culture, woody species, 10:173-201 Pruning, 4:161, 8:339-380 apple, 9:351-375 apple training, 1:414 chemical, 7:453-461 cold hardiness. 11:56 fire blight, 1:441-442 grapevines. 16:235-254 light interception, 2:250-251 peach,9:351-375 phase change, 7:143-144 root, 6:155-188 Prunus. See also Almond; Cherry; Nectarine; Peach; Plum in vitro, 5:243-244; 9:322 root distribution, 2:456

CUMULATIVE SUBJECT INDEX

316

Pseudomonas: phaseolicola, 3:32-33, 39,44-45 solanacearum, 3:33 syringae, 3:33,40; 7:210-212

Q Quality evaluation: fruits and vegetables, 20:1-119, 121-224 nondestruGtive, 20:1-119 texture in fresh fruit, 20:121-224 R

Rabbit,6:275-276 Radish, fertilization, 1:121 Rambutan, CA and MA, 22:163. See also Sapindaceous fruits Raspberry: harvesting, 16:282-298 productivity, 11:185-228 Rejuvenation: rose, 9:59-60 woody plants, 7:109-155 Replant problem, deciduous fruit trees, 2:1-116 Respiration: asparagus postharvest, 12:72-77 fruit in CA storage, 1:315-316 kiwifruit, 6:47-48 vegetables in CA storage, 1:341-346 Rhizobium, 3:34,41 Rhododendron, 12:1-67 Rice bean, genetics, 2:375-376 Root: apple, 12:269-272 cactus, 18:297-298 diseases, 5:29-31 environment, nutrient film technique, 5:13-26 Ericaceae, 10:202-209 grape, 5:127-168 kiwifruit, 12:310-313 physiology of bulbs, 14:57-88

pruning, 6:155-188 raspberry,11:190 rose, 9:57 tree crops, 2:424-490 Root and tuber crops: aroids, 8:43-99; 12:166-170 cassava, 12:158-166 low-temperature sweetening, 17:203-231 minor crops, 12:184-188 potato tuberization, 14:89-188 sweet potato, 12:170-176 yam (Dioscorea), 12:177-184 Rootstocks: alternate bearing, 4:148 apple, 1:405-407; 12:295-297 avocado, 17:381-429 citrus, 1:237-269 cold hardiness, 11:57-58 fire blight, 1:432-435 light interception, 2:249-250 navel orange, 8:156-161 root systems, 2:471-474 stress, 4:253-254 tree short life, 2:70-75 Rosaceae, in vitro, 5:239-248 Rose: fertilization, 1:104; 5:361-363 growth substances, 9:3-53 in vitro, 5:244-248

s Salinity: air pollution, 8:25-26 olive, 21:177-214 soils, 4:22-27 tolerance, 16:33-69 Sapindaceous fruits, 16:143-196 Sapodilla, CA and MA, 22:164 Scoring, and fruit set, 1:416-417 Seed: abortion, 1:293-294 apple anatomy and morphology, 10:285-286 conditioning, 13:131-181

CUMULATIVE SUBJECT INDEX

desiccation tolerance, 18:196-203 environmental influences on size and composition, 13:183-213 flower induction, 4:190-195 fluid drilling, 3:1-58 grape seedlessness, 11:159-184 kiwifruit,6:48-50 lettuce, 2:166-174 priming, 16:109-141 rose propagation, 9:54-55 vegetable, 3:1-58 viability and storage, 2:117-141 Secondary metabolites, woody legumes, 14:314-322 Senescence: cut flower, 1:204-236; 3:59-143; 10:35-62; 18:1-85 petal, 11 :15-43 pollination-induced, 19:4-25 rose, 9:65-66 whole plant, 15:335-370 Sensory quality CA storage, 8:101-127 Shoot-tip culture, 5:221-277. See also Micropropagation Short life problem, fruit crops, 2:1-116 Small fruit, CA storage, 1:308 Snapdragon fertilization, 5:363-364 Sodium, deficiency and toxicity symptoms in fruits and nuts, 2:153-154 Soil: grape root growth, 5:141-144 management and root growth, 2:465-469 orchard floor management, 9:377-430 plant relations, trickle irrigation, 4:18-21 stress, 4:151-152 testing, 7:1-68; 9:88-90 Soilless culture, 5:1-44 Solanaceae, in vitro, 5:229-232 Somatic embryogenesis, see Asexual embryogenesis

317

Sorghum, sweet, 21:73-104 Spathiphyllum, see Aroids, ornamental Stem, apple morphology, 12:272-283 Storage. See also Postharvest physiology, Controlledatmosphere (CA) storage cut flower, 3:96-100; 10:35-62 rose plants, 9:58-59 seed, 2:117-141 Strawberry: fertilization, 1:106 fruit growth and ripening, 17:267-297 harvesting, 16:348-365 in vitro, 5:239-241 Stress: benefits of, 4:247-271 climatic, 4:150-151 flooding, 13:257-313 mechanical, 17:1-42 petal, 11 :32-33 plant, 2:34-37 protection, 7:463-466 salinity tolerance in olive, 21:177-214 subzero temperature, 6:373-417 Sugar. See also Carbohydrate allocation, 7:74-94 flowering, 4:114 Sugar apple, CA and MA, 22:164 Sugar beet, fluid drilling of seed, 3:18-19 Sulfur: deficiency and toxicity symptoms in fruits and nuts, 2:154 nutrition, 5:323-324 Sweet potato: culture, 12:170-176 fertilization, 1:121 Sweet sop, CA and MA, 22:164 Symptoms, deficiency and toxicity symptoms in fruits and nuts, 2:145-154 Syngonium, see Aroids, ornamental

318

CUMULATIVE SUBJECT INDEX

T

Taro, see Aroids, edible Tea, botany and horticulture, 22:267-295

Temperature: apple fruit set, 1 :408-411 bloom delay, 15:119-128 CA storage of vegetables, 1:340-341

chilling injury, 15:67-74 cut flower storage, 10:40-43 cryopreservation, 6:357-372 fertilization, greenhouse crops, 5:331-332

fire blight forecasting, 1:456-459 flowering, 15:284-287, 312-313 interaction with photoperiod, 4:80-81

low temperature sweetening, 17:203-231

navel orange, 8:142 nutrient film technique, 5:21-24 photoperiod interaction, 17:73-123

photosynthesis, 11:121-124 plant growth, 2:36-37 seed storage, 2:132-133 subzero stress, 6:373-417 Texture in fresh fruit, 20:121-224 Thinning, apple, 1 :270-300 Tipburn, in lettuce, 4:49-65 Tissue. See also In vitro culture, 1:1-78; 2:268-310; 3:214-314; 4:106-127; 5:221-277; 6:357-372; 7:157-200; 8:75-78; 9:273-349; 10:153-181 dwarfing, 3:347-348 nutrient analysis, 7:52-56; 9:90

Tomato: CA storage, 1:380-386 chilling injury, 20:199-200 fertilization, 1:121-123 fluid drilling of seed, 3:19-20 fruit ripening, 13:67-103

galacturonase, 13:67-103 parthenocarpy, 6:65-84 Toxicity symptoms in fruit and nut crops, 2:145-154 Transport, cut flowers, 3:100-104 Tree decline, 2:1-116 Triazole, 10:63-105 chilling injury, 15:79-80 Trickle irrigation, 4:1-48 Truffle cultivation, 16:71-107 Tuber, potato, 14:89-188 Tuber and root crops, see Root and tuber crops Tulip. See also Bulb fertilization, 5:364-366 in vitro, 18:144-145 physiology, 5:45-125 Tunnel (cloche), 7:356-357 Turfgrass, fertilization, 1:112-117 Turnip, fertilization, 1:123-124 Turnip Mosaic Virus, 14:199-238

u Urd bean, genetics, 2:364-373 Urea, foliar application, 6:332

v Vaccinium, 10:185-187. See also Blueberry; Cranberry Vase solutions, 3:82-95; 10:46-51 Vegetable crops: aroids, 8:43-99; 12:166-170 asparagus postharvest, 12:69-155 cactus, 18:300-302 cassava, 12:158-166; 13:105-129 CA storage, 1:337-394 CA storage diseases, 3:412-461 CA storage and quality, 8:101-127 chilling injury, 15:63-95 fertilization, 1:117-124 fluid drilling of seeds, 3:1-58 greenhouse management, 21:1-39 greenhouse pest management, 13:1-66

CUMULATIVE SUBJECT INDEX

honey bee pollination, 9:251-254 hydroponics, 7:483-558 low temperature sweetening, 17:203-231 minor root and tubers, 12:184-188 mushroom cultivation, 19:59-97 mushroom spawn, 6:85-118 N nutrition, 22:185-223 nondestructive postharvest quality evaluation, 20:1-119 okra, 21:41-72 potato tuberization, 14:89-188 seed conditioning, 13:131-181 seed priming, 16:109-141 sweet potato, 12:170-176 tomato fruit ripening, 13:67-103 tomato parthenocarpy, 6:65-84 truffle cultivation, 16:71-107 yam (Dioscorea), 12:177-184 Vegetative tissue, desiccation tolerance, 18:176-195 Vernalization, 4:117, 15:284-287; 17:73-123 Vertebrate pests, 6:253-285 Vigna. See also Cowpea genetics, 2:311-394 U.S. production, 12:197-222 Virus: benefits in horticulture, 3:394-411 elimination, 7:157-200; 9:318; 18:113-123 fig, 12:474-475 tree short life, 2:50-51 turnip mosaic, 14:199-238 Volatiles, 17:43-72 Vole, 6:254-274

w Walnut, in vitro culture, 9:312 Water relations: cut flower, 3:61-66; 18:1-85 deciduous orchards, 21:105-131 desiccation tolerance, 18:171-213 fertilization, greenhouse crops, 5:332

319

fruit trees, 7:301-344 kiwifruit, 12:332-339 light in orchards, 2:248-249 photosynthesis, 11:124-131 trickle irrigation, 4:1-48 Watercore, 6:189-251 pear, 11:385-387 Watermelon, fertilization, 1:124 Wax apple, CA and MA, 22;164 Weed control, ginseng, 9:228-229 Weeds: lettuce research, 2:198 virus, 3:403 Woodchuck,6:276-277 Woody species, somatic embryogenesis, 10:153-181

x Xanthomonas phaseoJi, 3:29-32,41, 45-46 Xanthophyll cycle, 18:226-239 Xanthosoma, 8:45-46,56-57. See also Aroids Sugar. See also Carbohydrate allocation, 7:74-94 flowering, 4:114 y

Yam (Dioscorea), 12:177-184 Yield: determinants, 7:70-74; 97-99 limiting factors, 15:413-452

z Zantedeschia, see Aroids, ornamental Zinc: deficiency and toxicity symptoms in fruits and nuts, 2:151 foliar application, 6:332, 336 nutrition, 5:326 pine bark media, 9:124

Cumulative Contributor Index (Volumes 1-22)

Abbott,]. A., 20:1 Adams III, W. W., 18:215 Aldwinckle, H. S., 1:423; 15:xiii Anderson, 1. C., 21:73 Anderson, ]. L., 15:97 Anderson, P. C., 13:257 Andrews, P. K., 15:183 Ashworth, E. N., 13:215 Asokan, M. P., 8:43 Atkinson, D., 2:424 Aung, L. H., 5:45 Bailey, W. G., 9:187 Baird, L. A. M., 1:172 Banks, N. H., 19:217 Barden, ]. A., 9:351 Barker, A. V., 2:411 Bass, L. N., 2:117 Becker,]. S., 18:247 Beer, S. V., 1:423 Behboudian, M. H., 21:105 Bennett, A. B., 13:67 Benschop, M., 5:45 Ben-Ya'acov, A., 17:381 Benzioni, A., 17:233 Bewley, J. D., 18:171 Binze!, M. L., 16:33 Blanpied, G. D., 7:xi Bliss, F. A., 16:xiii Borochov, A., 11:15 Bower, J. P., 10:229 Bradley, G. A., 14:xiii Brennan, R., 16:255 Broschat, T. K., 14:1 Brown, S. 15:xiii Buban, T., 4:174 320

Bukovac, M. J., 11:1 Burke, M. J., 11:xiii Buwalda, J. G., 12:307 Byers, R. E., 6:253 Caldas, L. S., 2:568 Campbell, L. E., 2:524 Cantliffe, D. J., 16:109, 17:43 Carter, G., 20:121 Carter,]. V., 3:144 Cathey, H. M., 2:524 Chambers, R. J., 13:1 Charron, C. S., 17:43 Chin, C. K., 5:221 Clarke, N. D., 21:1 Cohen, M., 3:394 Collier, G. F., 4:49 Collins, W. L., 7:483 Compton, M. E., 14:239 Conover, C. A., 5:317; 6:119 Coppens d'Eeckenbrugge, G., 21:133 Coyne, D. P., 3:28 Crane, J. C., 3:376 Criley, R. A., 14:1; 22:27 Crowly, W., 15:1 Cutting, J. G., 10:229 Daie, J., 7:69 Dale, A., 11:185; 16:255 Darnell, R. L., 13:339 Davenport, T. L., 8:257; 12:349 Davies, F. S., 8:129 Davies, P. J., 15:335 Davis, T. D., 10:63 DeGrandi-Hoffrnan, G., 9:237 De Hertogh, A. A., 5:45; 14:57; 18:87

CUMULATIVE CONTRIBUTOR INDEX

321

Deikman, J., 16:1 DellaPenna, D., 13:67 Demmig-Adams, B., 18:215 Dennis, F. G., Jr., 1:395 Doud, S. L., 2:1 Duke, S. 0., 15:371 Dunavent, M. G., 9:103 Duval, M.-F., 21:133 Diizyaman, K, 21:41 Dyer, W. K, 15:371

Goszczynska, D. M., 10:35 Grace, S. c., 18:215 Graves, C. J., 5:1 Gray, D., 3:1 Grierson, W., 4:247 Griffen, G. J., 8:291 Grodzinski, B., 7:345 Gucci, R, 21:177 Guest, D. 1., 17:299 Guiltinan, M.J., 16:1

Early, J. D., 13:339 Elfving, D. c., 4:1; 11:229 EI-Goorani, M. A., 3:412 Esan, E. B., 1:1 Evans, D. A., 3:214 Ewing, K K, 14:89

Hackett, W. P., 7:109 Hallett, I. C., 20:121 Halevy, A. H., 1:204; 3:59 Hammerschmidt, R, 18:247 Hanson, E. J., 16:255 Harker, F. R, 20:121 Heaney, R K., 19:99 Heath, R R, 17:43 Helzer, N. L., 13:1 Hendrix, J. W., 3:172 Henny, R J., 10:1 Hergert, G. B., 16:255 Hess, F. D., 15:371 Heywood, V., 15:1 Hogue, K J., 9:377 Holt, J. S., 15:371 Huber, D. J., 5:169 Hunter, K L., 21:73 Hutchinson, J. F., 9:273

Faust, M., 2:vii, 142; 4:174; 6:287; 14:333; 17:331; 19:263; 22:225 Fenner, M., 13:183 Fenwick, G. R, 19:99 Ferguson, A. R, 6:1 Ferguson, 1. B., 11:289 Ferguson, L., 12:409 Ferree, D. c., 6:155 Ferreira, J. F. S., 19:319 Fery, R L., 2:311; 12:157 Fischer, R. L., 13:67 Flick, C. K, 3:214 Flore, J. A., 11:111 Forshey, C. G., 11:229 Fujiwara, K., 17:125

Isenberg, F. M. R, 1;337 Iwakiri, B. T., 3:376

Geisler, D., 6:155 Geneve, R L., 14:265 George, W. L., Jr., 6:25 Gerrath, J. M., 13:315 Giovannetti, G., 16:71 Giovannoni, J. J., 13:67 Glenn, G. M., 10:107 Goffinet, M. C., 20:ix Goldschmidt, K K, 4:128 Goldy, R G., 14:357 Goren, R, 15:145

Jackson, J. E., 2:208 Janick, J., 1:ix; 8:xi; 17:xiii; 19:319; 21:xi Jarvis, W. R, 21:1 Jensen, M. H., 7:483 Jeong, B. R, 17:125 Jewett, T. J., 21:1 Joiner, J. N., 5:317 Jones, H. G., 7:301 Jones, J. B., Jr., 7:1 Jones, R B., 17:173

322

Kagan-Zur, V., 16:71 Kang, S. -M., 4:204 Kato, T., 8:181 Kawa, L., 14:57 Kawada, K., 4:247 Kelly, J. F., 10:ix; 22:xi Khan, A. A., 13:131 Kierman, J., 3:172 Kim, K. -W., 18:87 Kinet, J. -M., 15:279 King, G. A., 11:413 Kingston, C. M., 13:407-432 Kliewer, W. M., 14:407 Knight, R J., 19:xiii Knox, R B., 12:1 Kofranek, A. M., 8:xi Korcak, R F., 9:133; 10:183 Kozai, T., 17:125 Krezdorn, A. H., 1:vii

CUMULATIVE CONTRIBUTOR INDEX

Maynard, D. N., 1:79 McConchie, R, 17:173 McNicol, R J., 16:255 Merkle, S. A., 14:265 Michailides, T. J., 12:409 Michelson, K, 17:381 Mika, A., 8:339 Miller, S. S., 10:309 Mills, H. A., 2:411; 9:103 Mills, T. M., 21:105 Mitchell, C. A., 17:1 Mizrahi, Y., 18:291, 321 Molnar, J. M., 9:1 Monk, G. J., 9:1 Monselise, S. P., 4:128 Moore, G. A., 7:157 Mor, Y., 9:53 Morris, J. R, 16:255 Murashige, T., 1:1 Murray, S. H., 20:121 Myers, P. N., 17:1

Lakso, A. N., 7:301; 11:111 Lamb, R C., 15:xiii Lang, G. A., 13:339 Larsen, R P., 9:xi Larson, R A., 7:399 Leal, F., 21:133 Ledbetter, C. A., 11:159 Li, P. H., 6:373 Lill, R E., 11:413 Lipton, W. J., 12:69 LHz, R E., 7:157 Lockard, R. G., 3:315 Loescher, W. H., 6:198 Lorenz, O. A., 1:79 Lu, R, 20:1 Lurie, S., 22:91-121 Lyrene, P., 21:xi

O'Donoghue, K M., 11:413 Ogden, R J., 9:103 O'Hair, S. K., 8:43; 12:157 Oliveira, C. M., 10:403 Oliver, M. J., 18:171 O'Neill, S. D., 19:1 Opara, L. D., 19:217 Ormrod, D. P., 8:1

Manivel, L., 22:267 Maraffa, S. B., 2:268 Marangoni, A. G., 17:203 Marini, R P., 9:351 Marlow, G. c., 6:189 Maronek, D. M., 3:172 Martin, G. G., 13:339 Mayak, S., 1:204; 3:59

Palser, B. F., 12:1 Papadopoulos, A. P., 21:1 Pararajasingham, S., 21:1 Parera, C. A., 16:109 Pegg, K. G., 17:299 Pellett, H. M., 3:144 Perkins-Veazil, P., 17:267 Ploetz, R C., 13:257

Nadeau, J. A., 19:1 Neilsen, G. H., 9:377 Nerd, A., 18:291,321 Niemiera, A. X., 9:75 Nobel, P. S., 18:291 Nyujto, F., 22:225

CUMULATIVE CONTRIBUTOR INDEX

Pokorny, F. A., 9:103 Poole, R T., 5:317;6:119 Poovaiah, B. W., 10:107 Portas, C. A. M., 19:99 Porter, M. A., 7:345 Possingham, J. V., 16:235 Pratt, c., 10:273; 12:265 Preece, ]. E., 14:265 Priestley, C. A., 10:403 Proctor, J. T. A., 9:187 Quamme, H., 18:xiii Raese, J. T., 11:357 Ramming, D. W., 11:159 Reddy, A. S. N., 10:107 Redgwell, R. J., 20:121 Reid, M., 12:xiii, 17:123 Reuveni, M., 16:33 Richards, D., 5:127 Rieger, M., 11:45 Roper, T. R, 21:215 Rosa, E. A. S., 19:99 Roth-Bejerano, N., 16:71 Roubelakis-Angelakis, K. A., 14:407 Rouse, J. L., 12:1 Royse, D. J., 19:59 Rudnicki, R M., 10:35 Ryder, E. J., 2:164; 3:vii Sachs, R, 12:xiii Sakai, A., 6:357 Salisbury, F. B., 4:66; 15:233 San Antonio, J. P., 6:85 Sankhla, N., 10:63 Saure, M. c., 7:239 Schaffer, B., 13:257 Schenk, M. K., 22:185 Schneider, G. W., 3;315 Schuster, M. L., 3:28 Scorza, R, 4:106 Scott, J. W., 6:25 Sedgley, M., 12:223; 22:1 Seeley, S. S., 15:97 Serrano Marquez, c., 15:183 Sharp, W. R., 2:268; 3:214

323

Shattuck, V. I., 14:199 Shear, C. B., 2:142 Sheehan, T. J., 5:279 Shipp, J. L., 21:1 Shirra, M., 20:267 Shorey, H. H., 12:409 Simon, J. E., 19:319 Sklensky, D. E., 15:335 Smith, G. S., 12:307 Smock, R M., 1:301 Sommer, N. F., 3:412 Sandahl, M. R, 2:268 Sopp, P. I., 13:1 Soule, ]., 4:247 Sparks, D., 8:217 Splittstoesser, W. E., 6:25; 13:105 Srinivasan, C., 7:157 Stang, E. J., 16:255 Steffens, G. L., 10:63 Stevens, M. A., 4:vii Stroshine, R. L., 20:1 Struik, P. c., 14:89 Studman, C. J., 19:217 Stutte, G. W., 13:339 Styer, D. J., 5;221 Sunderland, K. D., 13:1 Suranyi, D., 19:263; 22:225 Swanson, B., 12:xiii Swietlik, D., 6:287 Syvertsen, J. P., 7:301 Tattini, M., 21:177 Tetenyi, P., 19:373 Tibbitts, T. W., 4:49 Timon, B., 17:331 Tindall, H. D., 16:143 Tisserat, B., 1:1 Titus, J. S., 4:204 Trigiano, R. N., 14:265 Tunya, G. 0.,13:105 Upchurch, B. L., 20:1 van Doorn, W. G., 17:173; 18:1 Veilleux, R. E., 14:239 Vorsa, N., 21:215

324

Wallace, A., 15:413 Wallace, D. H., 17:73 Wallace, G. A., 15:413 Wang, C. Y., 15:63 Wang, S. Y., 14:333 Wann, S. R, 10:153 Watkins, C. 8., 11:289 Watson, G. W., 15:1 Webster, B. D., 1:172; 13:xi Weichmann, J., 8:101 Wetzstein, H. Y., 8:217 Whiley, A. W., 17:299 Whitaker, T. W., 2:164 White, J. W., 1:141 Williams, E. G., 12:1 Williams, M. W., 1:270 Wismer, W. V., 17:203

CUMULATIVE CONTRIBUTOR INDEX

Wittwer, S. H., 6:xi Woodson, W. R, 11:15 Wright, R. D., 9:75 Wutscher, H. K., 1:237 Yada, R Y., 17:203 Yadava, U. L., 2:1 Yahia, E. M., 16:197; 22:123 Yan, W., 17:73 Yarborough, D. E., 16:255 Yelenosky, G., 7:201 Zanini, E., 16:71 Zieslin, N., 9:53 Zimmerman, R H., 5:vii; 9:273 Zucconi, F., 11:1