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Home , Rhynchophorus palmarum, Stenomesius, Trigona amalthea, Trissolcus, Unaspis citri

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Tropical Fruit Pests and Pollinators

Biology, Economic Importance, Natural Enemies and Control

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Dedication

To my nieces, Dalia Lucia and Carmen Yomaira, and nephews, Jario Alberto and Jorge Eduardo and to my adopted children Christina and Matthew. To Luz-Stella Cobo-Martinez for encouraging me to become an entomologist.

Acknowledgements

Extensive thanks to my co-editors, authors and co-authors for their willingness to participate in this endeavour. Dr Richard E. Litz for encouraging me to edit this book. Drs Richard Jones and William Brown for their support. Ms Elvia Esparza for the superb art work on the book cover. Ms Rita E. Duncan and Dr Diviina Amalin for their help. To the different reviewers of the book chapters.

J.E. Peña

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Tropical Fruit Pests and Pollinators

Biology, Economic Importance, Natural Enemies and Control

Edited by

J.E. Peña

Tropical Research and Education Center University of Florida, Florida USA

J.L. Sharp

USDA-ARS, Miami, Florida USA

and

M. Wysoki

ARO, The Volcani Center Bet Dagan Israel

CABI Publishing

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CABI Publishing is a division of CAB International

CABI Publishing CABI Publishing CAB International 10 E 40th Street Wallingford Suite 3203 Oxon OX10 8DE New York, NY 10016 UK USA

Tel: +44 (0)1491 832111 Tel: +1 212 481 7018 Fax: +44 (0)1491 833508 Fax: +1 212 686 7993 E-mail: [email protected] E-mail: [email protected] Web site: www.cabi-publishing.org

©CAB International 2002. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners.

A catalogue record for this book is available from the British Library, London, UK.

Library of Congress Cataloging-in-Publication Data Tropical fruit pests and pollinators : biology, economic importance, natural enemies, and control / edited by J.E. Peña, J.L. Sharp, and M. Wysoki. p. cm. Includes bibliographical references (p. ). ISBN 0-85199-434-2 (alk. paper) 1. Tropical fruit--Diseases and pests. 2. Tropical fruit--Diseases and pests--Control. 3. Insect pollinators--Control. I. Peña, Jorge E., 1948-II. Sharp, Jennifer L. III. Wysoki, M. SB608.F8 T75 2002 634′.6--dc21 2002001303

ISBN 0 85199 434 2

Typeset by AMA DataSet Ltd, UK Printed and bound in the UK by Cromwell Press, Trowbridge

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Contents

Contributors vii

1 Introduction 1 J.E. Peña

2 Pests of Banana 13 C.S. Gold, B. Pinese and J.E. Peña

3 Tropical Citrus Pests 57 D. Smith and J.E. Peña

4Pests and Pollinators of Mango 103 G.K. Waite

5 Pests of Papaya 131 A. Pantoja, P.A. Follett and J.A. Villanueva-Jiménez

6 Pests of Pineapple 157 G.J. Petty, G.R. Stirling and D.P. Bartholomew

7 Pollinators and Pests of Annona Species 197 J.E. Peña, H. Nadel, M. Barbosa-Pereira and D. Smith

8 Pests and Pollinators of Avocado 223 M. Wysoki, M.A. van den Berg, G. Ish-Am, S. Gazit, J.E. Peña and G.K. Waite

9 Pests of Guava 295 W.P. Gould and A. Raga

10 Pests of Minor Tropical Fruits 315 P.A.C. Ooi, A. Winotai and J.E. Peña

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vi Contents

11 Pests of Litchi and Longan 331 G.K. Waite and J.S. Hwang

12 Passion Fruit 361 E.L. Aguiar-Menezes, E.B. Menezes, P.C.R. Cassino and M.A. Soares

13 Quarantine Treatments for Pests of Tropical Fruits 391 J.L. Sharp and N.W. Heather

Index 407

The colour plates can be found following p. 56

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Contributors

E.L. Aguiar-Menezes, Empresa Brasileira de Pesquisa Agropecuaria, Centro Nacional de Pesquisa de Agrobiologia, BR 465, Km 7, Caixa Postal 74505, Seropedica, RJ 23890-000 Brazil. M. Barbosa-Pereira, Department of Entomology, ESALQ-USP, Piracicaba, São Paulo, Brazil. D.P. Bartholomew, Department of Agronomy and Soil Science, University of Hawaii at Manoa, 1910 East-West Road, Honolulu, Hawaii 96822, USA. P.C.R. Cassino, Universidade Federal Rural do Rio de Janeiro, Centro Integrado de Manejo de Pragas, ‘Cincinnato Rory Goncalves’, BR 465, Km 7, Seropedica, RJ 23890-000 Brazil. P.A. Follett, USDA-ARS, Pacific Basin Agricultural Research Center, PO Box 4459, Hilo, Hawaii 96720, USA. S. Gazit, Department of Horticulture, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel. C.S. Gold, International Institute of Tropical Agriculture, ESARC, PO Box 7878, Kampala, Uganda. W.P. Gould, USDA-ARS, Subtropical Horticulture Research Station, 13601 Old Cutler Road, Miami, FL 33158, USA. N.W. Heather, School of Land and Food, The University of Queensland, Gatton College, Queensland 4345, Australia. J.S. Hwang, Taiwan Agricultural Chemicals and Toxic Substances Research Institute, 189 Chung-Cheng Road, Wufeng, Taichung Hsien, Taiwan 413, Republic of China. G. Ish-Am, Department of Horticulture, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel. E.B. Menezes, Universidade Federal Rural do Rio de Janeiro, Centro Integrado de Manejo de Pragas, ‘Cincinnato Rory Goncalves’, BR 465, Km 7, Seropedica, RJ 23890-000 Brazil. H. Nadel, International Centre for Insect Physiology and Ecology (ICIPE), PO Box 30772, Nairobi, Kenya. A. Pantoja, Department of Crop Protection University of Puerto Rico, Mayaguez Campus, PO Box 9030 Mayaguez, Puerto Rico 00681-9030. J.E. Peña, Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, FL 33031, USA. G.J. Petty, Institute for Tropical and Subtropical Crops, Agricultural Research Council, Private Bag X1, Bathurst 6166, Republic of South Africa. B. Pinese, Queensland Department of Primary Industries, PO Box 1054, Mareeba, Queensland 4880, Australia. P.A.C. Ooi, FAO Regional Office for Asia and the Pacific, 39 Phra Atit Road, Bangkok 1022, Thailand. A. Raga, Instituto Biologico, Caixa Postal 70, 13.001-970, Campinas, SP, Brazil.

vii

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viii Contributors

J.L. Sharp, USDA-ARS, 13601 Old Cutler Road, Miami, FL 33158, USA. D. Smith, Department of Primary Industries, Maroochy Horticultural Research Station, Nambour, Queensland 4560, Australia. M.A. Soares, Universidade Federal Rural do Rio de Janeiro, Centro Integrado de Manejo de Pragas, ‘Cincinnato Rory Goncalves’, BR 465, Km 7, Seropedica, RJ 23890-000 Brazil. G.R. Stirling, Biological Crop Protection (Pty) Ltd, 3601 Moggill Road, Moggil, Queensland 4070, Australia. M.A. van den Berg, Institute for Tropical and Subtropical Crops, Private Bag X11208, Nelspruit 1200, South Africa. J.A. Villanueva-Jiménez, Colegio de Postgraduados, Campus Veracruz, Apartado Postal 421, CP 91700 Veracruz, Veracruz, Mexico. G.K. Waite, Queensland Horticulture Institute, Maroochy Research Station, PO Box 5083, SCMC, Nambour, Queensland 4560, Australia. A. Winotai, Biological Control Group, Division of Entomology and Zoology, Department of Agri- culture, Chatuchak, Bangkok 10900, Thailand. M. Wysoki, Department of Entomology, ARO, Institute of Plant Protection, The Volcani Center, PO Box 6, Bet Dagan 50250, Israel.

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1 Introduction

Jorge E. Peña Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, FL 33031, USA

Tropical Fruit have modifying effects on these crops. Tree phenology (flushing, quiescence, flowering, Tropical fruit form a large and diverse com- fruiting and leaf fall) is much more dramatic in modity group, that ranges from perennial the tropics than at high latitudes, where win- to herbaceous species (Alexander and ter confines growth and development largely Possingham, 1984; Akora, 1998). The herba- to one season each year (Verheij and Coronel, ceous group comprises important crop plants 1992). Day length in the tropics varies too such as banana, pineapple, and papaya while little to noticeably affect the annual course of the woody or perennial plants may include radiation or temperature. Thus, most climatic tree species, shrubs, and vines (Verheij cues of plant development are not as firmly and Coronel, 1992). In this book we have tied to calendar months as is the case at higher attempted to record and summarize what latitudes. The phenological cycle in the tropics is known regarding pests and pollinators may shift a few months from one year to the of tropical fruit from the major tropical fruit next. This complicates phenological studies, producing areas: South and South-East Asia, but should make it easier to detect which Australia, Africa, South and Central America environmental factor (e.g. dry season) triggers and the Caribbean region. We have focused a certain growth and development response on tropical citrus, avocado, mango, pine- (e.g. flowering). Because of their diversity, not apple, banana, passion fruit, litchi, guava, all tropical fruit follow the same strategy Annona spp., durian, mangosteen, acerola, for growth and development. Strategies are and carambola. The reader will notice that the based on differences in tree form and branch- amount of information is extensive for citrus, ing habits. For instance, single-stemmed avocado and pineapple, whereas relatively plants such as pineapple, papaya, and banana little has been compiled for durian, mango- are contrasted with freely branching fruit steen, passion fruit, acerola, and carambola. trees (Verheij and Coronel, 1992). Most This reflects the worldwide importance, con- tropical fruit are considered as perennial sumer acceptance, and production margins of plants which persist for several years without these fruit crops. abrupt, major changes other than seasonal leaf Tropical fruits are regularly grown in a formation, flowering, and fruit development variety of climates from latitude 23°27′ Nto (Bennett et al., 1976). However, pineapple, 23°27′ S of the equator, while some are grown papaya, and passion fruit are grown for up to approximately 37° N in Spain. Proximity shorter periods of time and arthropod to the sea, sea currents, altitude, direction of management on these crops is influenced by prevailing winds, rainfall, and humidity all their duration in the field (Ch. 6).

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 1

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2 J.E. Peña

Traditionally, tropical fruits were pro- Major Asian producers are India, China, the duced in the greatest quantity, and with the Philippines, Indonesia, Thailand, and Paki- best quality, at or near the original centres stan. In the western hemisphere the leading of each species’ distribution. As examples, producers of tropical fruit are Brazil, Mexico, the range and quality of mangoes is high in Ecuador, Colombia, Costa Rica, and Cuba India, but other countries, such as Mexico, (FAO, 2001) (Table 1.3). Tropical fruit pro- Guatemala and Israel, are seeking to optimize duction in Africa is apparently concentrated production. Litchis are traditional in southern in Nigeria, Burundi, South Africa, Congo, China, but as a result of considerable pro- Cameroon, Egypt, and Angola. duction research, are now grown in the USA, Australia, and elsewhere. On the other hand, Table 1.2. Trends in the global production of mangosteen, durian, and salak remain largely minor tropical fruit crops (Annona, guava, passion confined to their centres of origin, in the fruit, etc.) (source: FAO, 2001). Malaya–Indonesia region. Pineapples, commonly those of the cayenne type, bananas, Years Tropical fruit production (t) Increase (%) mainly of the dwarf Cavendish variety, and 2000 15,331,309 24 papayas of the ‘Solo’ type, are now almost 1990 11,653,889 29 ubiquitous in the tropics. A surprisingly wide 1980 8,374,428 29 range of tropical fruits including bananas, 1970 6,004,759 14 papayas, and pineapples are grown in 1961 5,165,192 high altitude areas (2000–2500 m) near the equator in countries such as Kenya, Colombia, Ecuador, Peru, Indonesia, and India. In nearly Table 1.3. Rank order of 15 countries with major tropical fruit production (source: FAO, 2001). all cases, these fruits flourish in unusual environmental niches which are frost free and Country Fruit production (’000 t) receive a high level of solar radiation. According to FAO (2001), world produc- 1. India 35,142 tion of tropical fruit (avocado, banana, citrus, 2. Brazil 34,122 3. China 20,093 mango, papaya, and pineapple) increased by 4. Mexico 9,800 36–54% from 1975 to 2000 (Table 1.1), and 5. Philippines 9,123 production of minor crops (Annona, guava, 6. Indonesia 8,343 passion fruit, etc.) increased by 24–29% during 7. Thailand 7,941 this period (Table 1.2). However, Verheij and 8. Ecuador 5,000 Coronel (1992) caution that these figures 9. Colombia 4,725 could be misleading, because most fruit comes 10. Pakistan 3,743 from trees scattered in home gardens, making 11. Costa Rica 2,101 it difficult to compile reliable statistical data. 12. Nigeria 1,629 According to FAO (2001), India is the leading 13. Burundi 1,514 14. South Africa 1,433 tropical fruit producing country, followed by 15. Bangladesh ,720 Brazil, China, Mexico, and the Philippines.

Table 1.1. Trends in global production of various tropical fruits (source: FAO, 2001).

Commodity Production 1975 (t) Production 2000 (t) Increase (%)

Avocados 1,232,763 2,336,765 52 Bananas 31,688,547 58,687,214 54 Citrus 51,736,565 104,966,628 50 Mangoes 12,774,918 24,975,204 51 Papayas 1,944,494 5,363,167 36 Pineapples 7,219,688 13,455,362 53 Tropical fruit 6,894,951 15,331,309 45

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Introduction 3

Few tropical fruits are grown in Europe Subtropical Entomology, which continues to be and only relatively small amounts in the USA, cited as an essential reference for students and Australia, and Israel. In the USA, tropical researchers of tropical and subtropical fruit fruits are grown in Florida and California, entomology. However, tropical crop produc- where the availability of suitable soils and tion has undergone major changes since occasional below-freezing temperature limit the book was published. Several other texts production. Hawaii grows a wide range of dealing with pest management systems for tropical fruits, but has an unusual maritime tropical crops (Lamb, 1974; Hill, 1975; Swaine tropical climate that is modified by altitude. et al., 1985; Braga et al., 1998; Tandon, 1998; For this reason varieties of papaya and maca- Mariu, 1999) have since been written. These damia developed in Hawaii have complex publications are in response to substantial environmental requirements, and are grown growth of tropical fruit production and elsewhere with only limited success. Small increased concern for food safety. Many books quantities of tropical fruit for European dealing with integrated pest management markets are grown in Israel, generally with have concentrated on field crop IPM with the the support of irrigation in low-lying, saline occasional exception of temperate fruits, such desert areas with low relative humidity. Many as pear and apple (Boethel and Eikenbary, equatorial tropical countries including those 1979), citrus (Anonymous, 1991) or nuts and in Africa, the Americas, India, and South- almonds (Anonymous, 1985). East Asia are beginning to strengthen Because production of tropical fruit research programmes on propagation, genetic ranges from sophisticated plantation type improvement, control of flowering, control crops to rudimentary backyard production, of pathogens and arthropods, irrigation and coupled with economic solvency and produc- nutrition, postharvest handling, and storage. tion purpose, internal vs. export production, it is difficult to generalize on a single method of crop protection. For instance, Verheij and Coronel (1992) maintain that tropical fruit Integrated Pest Management (IPM) for crop protection or the use of commercial Tropical Areas pesticides is limited to commercial cropping systems, i.e. orchards and corporate planta- Pest management has as its goal the control tions. Entwistle (1972) supports the idea that of agricultural pests to benefit society as a the application of the concept of integrated whole (Pimentel, 1981). Therefore, successful control often marks a stage in the evolution of pest control strategies must take into account research where information accrued in fields the complexities of society and the entire of study originally treated largely as separate ecosystem (Pimentel, 1981). According to a has expanded into a dynamic study of definition proposed by FAO in 1972, IPM is the interacting whole. This case may have happened for some crops such as pineapple, a system which primarily takes into account citrus, and banana but not for others. Again, the milieu and the population dynamics of the species under consideration and uses the diversity of the tropical crops treated in appropriate techniques and methods in a this book makes it difficult to make a single compatible manner in order to restrict the assessment, as can be done for temperate fruit pest populations below the threshold of crops such as apple or pear. The diversity of economic damage. Application of such a tropical fruit farmers ranges from those with method mandates not only a thorough wide financial support to those with mini- knowledge of the biology of the pest, i.e. mum resources. Small farmers in the tropics all the biotic factors which can affect it need an arsenal of various pest management and the effect of abiotic factors on the crop tools (e.g. chemical, biological, cultural, etc.) ecosystem, but also its market goals (export in order to have a successful IPM programme vs. internal consumption). (Goodell, 1984). Farmers in less developed Fifty-one years have passed since the countries lack resources and monetary sup- appearance of W. Ebeling’s (1950) book, port to build up an effective IPM farm-level

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4 J.E. Peña

implementation programme, while farmers region, while this pest is completely unknown in developed countries have well funded in China and Asia (see Ch. 3). research and extension institutions (Goodell, Commercial production of tropical crops 1984). regularly starts on or near areas with little Integrated control of a pest or pest com- agricultural development. The constitution of plex in a tropical crop requires a full investiga- arthropod fauna that exist in unexploited tion of relationships and interactions within areas would be likely to invade new plants the whole ecosystem (Entwistle, 1972). Because when any disturbance occurs, creating condi- of the specifically complex society of plants tions for colonization of the new introduced and arthropods inhabiting the area where plants. Such situations may occur when the tropical fruits originate, tropical fruits may fruit tree is planted on land prepared by clear have a greater diversity of trophically associ- felling or beneath the shade of secondary ated arthropods than any temperate crop. For forest. In such circumstances, the arthropod instance, Entwistle (1972) maintains that the fauna may still reflect that of the local primary 1400 arthropod species listed for cocoa can and secondary plant communities of the area only be the skeleton crew of the total cocoa (Entwistle, 1972). Attempts should be made fauna. Thus, information on tropical fruit ento- to bring together existing data into cohesive mology is regionally uneven both in quantity studies of insect communities in these impor- and quality; this being the result of national tant plant associations. Until these data are policies or the absence of them, and the domi- available, tropical fruit entomology will in nant nature of certain pest problems. More- many ways lack a fundamental perspective. over, few authors have yet taken an integrated Tropical fruit crops provide a relatively attitude to arthropods of tropical fruit crops. long-term and stable environment, offering Globalization of tropical fruit and rapid continuing habitats for both pests and natural expansion of export markets has resulted in enemies. This environment provides excellent exotic plants grown outside of their centres of opportunities for biological control and origin. For instance, citrus originated in Asia alternative pest management programmes and is grown in the Neotropics while papaya (Bennett et al., 1976). However, the extensive and passion fruit originated in the Neotropics use of broad spectrum pesticides disrupts this and now are grown in Asia, Australia, etc. stable environment, and leads to instability of Thus, upon arrival in their new area of domes- arthropod densities (Hoyt and Burts, 1974). tication, exotic fruit plants are populated by an According to Hoyt and Burts (1974) any indigenous regional arthropod fauna, and by attempt to develop integrated control pro- exotic arthropods that have also migrated grammes in fruit crops must take into account from the crop’s centre of origin. Thus, arthro- the following: (i) knowledge of native or resi- pod systems (pollinators, pests, and natural dent arthropod fauna; (ii) arthropod fauna enemies) for introduced plant species will affecting the tree crop in its area of origin or be somewhat different from those observed domestication; and (iii) the presence of natural in the crop’s area of origin. For instance, the enemies. The basis for integrated pest man- European honeybee Apis mellifera did not agement includes the pest’s biology and ecol- co-evolve with avocado but it is used as a ogy, sampling and monitoring techniques, pollinator of avocado in Israel and Australia. economic thresholds, and the application of Original pollinators from the area of origin management tactics, i.e. chemical, biological, of avocado in Mexico and Guatemala could autocidal, plant resistance, etc. be other more efficient hymenopteran species (see Ch. 8). In the Neotropics several insects have adapted to introduced plant species, such as citrus. For instance, the Neotropical, Biology and ecology Diaprepes abbreviatus (Coleoptera: Curculion- idae) has adopted citrus as one of its preferred The botanical diversity of tropical fruit is host plants. D. abbreviatus is considered a key enormous and their arthropod fauna is pest for citrus in Florida and the Caribbean probably more complex than we suspect.

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Introduction 5

There is climatic and geographical variation Sampling and monitoring within the range of tropical fruit cultivation which is known to affect the composition Sampling populations to determine kinds of insects on each tropical crop. For and to estimate numbers of living species are instance, Bephratelloides spp. (Hymenoptera: the most fundamental research activities in Eurytomidae) are the most common insects ecology and the primary basis of integrated affecting Annona crops in the Neotropics. pest management (Pedigo, 1994). The basic Within this group, Bephratelloides cubensis, aims of IPM are most effectively accom- a key pest species present in Florida, has plished by employing preventive tactics such a female-biased sex ratio, while a similar as biological control, plant resistance and cul- species, B. pomorum, dominant in Annona- tural activities to maintain pest populations growing regions of Brazil, has an almost below the economic injury level. However, 50 : 50 sex ratio. In the same way, the moth if these tactics fail, other curative methods, Cerconota annonella is found affecting Annona i.e. chemical or microbial control, are applied. in the warmer regions of South America and The use of the latter methods calls for a prac- the Caribbean but is absent from subtropical tical sampling programme that will help to Florida. Insects can be classified as define pest density as well as the appropriate autochthonous species with a more local decision rules such as economic threshold distribution, or as inter-regional species and use of a curative method. Hare (1994) which may affect crops in different areas suggests that for pest management decisions either by exceptional powers of dispersal it is necessary to rapidly and economically coupled with the host and environmental determine where the pest population is tolerance, or as homophylous, i.e. tending relative to its treatment threshold. to distribution by man. These classifications Sampling programmes for fruit trees are are not necessarily mutually exclusive and inherently more complex than for annual, it may be difficult, as for example with herbaceous plants because of the wide variety such mealybugs as Maconellicoccus hirsutus of habitats that trees offer (Hare, 1994). For and the aphid Toxoptera aurantii, to dis- instance, in fruit trees substantial heterogene- tinguish the main agents of dispersal ity in pest populations can exist even within (Entwistle, 1972). different parts of the leaf canopy, some Most arthropods affecting tropical fruit pests are direct (fruit feeding) but can also be are polyphagous (mites, fruit flies, scales, indirect (affecting shoot, wood, foliage, roots) whiteflies, and thrips) and studies on their (Hare, 1994). Beers et al. (1994) suggest that for biology have been published extensively. fruit trees, sampling is better directed toward Thus readers requiring more detail should indirect pests because they have a greater consult, among others, the books edited probability of being present at non-damaging by White and Elson-Harris (1994) (fruit levels. Sampling and monitoring methods for flies); Jeppson et al. (1975), Helle and Sabelis tropical fruit are well established for some (1985a,b) (mites); Rosen (1990a,b) (armoured direct pests such as fruit flies, fruit borers scales); and Parker et al. (1995) (thrips). (Ch. 4) as well for some indirect pests (i.e. In order to apply IPM concepts to tropical banana weevil) (Ch. 2), leafminers (Ch. 3), fruit, we must better understand the biology mites (Keenan, 1997; see also Ch. 3) and defoli- and ecology of these arthropods particularly ators (Ch. 8). However, the inability to corre- in their relationship with tropical fruit. This late sampling data to infestation levels of the book reviews the biology of the most impor- fruit at the time of harvest is still a problem tant pest species and pollinators affecting (Chs 2 and 4). While attempts have been made tropical fruit, but may not include some to develop sampling techniques for several regionally important pests. Although base- pests of citrus, mango, avocado, and banana line information is provided, this book (Smith et al., 1997; see also Chs 2, 3 and 4), ade- demonstrates that there are several gaps of quate sampling techniques are not available information pertaining to these arthropods. for some pests and crops (Chs 10 and 12).

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6 J.E. Peña

Of course, the availability or allocation Chemical control of resources for sampling, research and monitoring is a function of the place where the The choice of toxicants and availability of crop is grown, the purpose of fruit production spraying equipment differs among tropical (export vs. internal consumption), and the fruit producing countries. Verheij and economic solvency of growers. Thus, grower Coronel (1992) maintain that in Asian organizations in Australia, the USA, South countries, traditional tropical fruit crop pro- Africa, and Israel are able to fund research for tection measures such as chemical control are tropical fruit, while tropical fruit growers in occasionally practised, being largely limited many developing countries cannot. to small plants and nursery work, while in Australia, the USA, and Israel, there are few constraints regarding availability of equipment and pesticides to be used for Economic thresholds tropical fruit. The use of pesticides in some areas is limited by tree size, since spraying of Pest management of fresh fruit focuses more large trees is impossible with the equipment upon preserving the appearance of the fruit most small growers can afford. The scattered rather than upon maximizing fruit pro- plantings in backyards, on field borders and duction. While several additional factors along watercourses impede access of equip- may complicate determination of the actual ment. Moreover, the tree population may economic status of pests, the level of damage consist of many seedling trees, and factors tolerated by consumers and packers varies such as biennial bearing would make it diffi- and complicates pest management decisions. cult to establish an annual spraying routine. Therefore, some confusion still exists regard- Because of a variety of issues, including ing economic thresholds, economic injury toxic residues, etc., spraying should be based levels, and economic damage with respect to on sound investigation. Ad hoc spraying may temperate fruit (Hoyt and Burts, 1974), and well be uneconomic and counter-productive. this confusion is even greater for tropical For instance, in the case of defoliators that are fruit. For instance, there are insufficient data usually only numerous in periods of maximal on the economic consequences of arthropods leaf production, application timing is critical of tropical fruit and when available these for cost effective spraying. Secondly, spraying data are often approximate. As export com- may disturb the balance between phyto- modities, tropical fruit crops command con- phagous insects and their natural enemies, sistently high prices, with highest prices leading to increasing numbers of secondary for undamaged fruit of premium quality. pests. Thirdly, the toxicants used may not Therefore the lack of knowledge of economic always be those considered suitable to thresholds, and/or the non-existence of pollinating insects. Verheij and Coronel (1992) economic thresholds, prevent control pro- suggest that developed countries, which grammes from focusing on the prevention were the first to rely heavily on commercial of damage to tropical fruit by pests. This biocides for fruit growing, are now adopting factor, together with the paucity of sampling integrated crop protection systems that were techniques for tropical fruit pests, suggests implemented by small farmers in developing that little effort has been focused on deter- countries. Nevertheless, pesticides have been mining economic treatment levels (Chs 2, 3 associated with significant successes in pro- and 6). Consequently, pesticides continue to tecting tropical fruit from insect attack and be widely applied as prophylactic measures. increasing tropical fruit productivity. Thus, Another source of insect-associated loss is the control of fruit and foliar insect pests pollination, which in several crops is thought continues to depend on the use of chemical to limit production. Objective studies are insecticides/acaricides (Chs 3 and 6). required to substantiate the value of Information regarding proper timing, pollinators and their effect on yield. spray volumes and knowledge of the pest

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Introduction 7

complex differs among tropical fruit. While tropical fruit pests. Use of feeding and sexual solid information is available for some crops attractants (secondary pheromones) in tropi- like pineapple (Ch. 6), it is disregarded for cal fruit has been largely limited to fruit flies others, e.g. papaya (Ch. 5). In Chapter 5 Pan- (Chs 5 and 9). Few species-specific attractants toja et al. report that most papaya producers are available for other insect groups such apply insecticides on a calendar basis. Such as weevils (Curculionidae) (Gold et al., 2002) routine heavy use of sprays for controlling and Lepidoptera (Ch. 8; see also Bailey et al., fruit flies and leafhoppers in papaya can cause 1988). heavy outbreaks of mites and other pests. Moreover, pesticidal procedures for controlling pests for some crops (e.g. citrus), when Biological control applied to other crops without reliable knowledge of the effects of these chemicals on the Biological control has great potential as a crop in question may exacerbate crop losses major tactic for regulating pest populations because of phytotoxicity, induced explosion in fruit orchards (Hoyt and Burts, 1974). The of population densities of other pests, reduc- ability to apply biological control effectively tion of natural enemy populations, etc. has increased in recent decades because of Widespread use of non-selective pesti- greater knowledge of the arthropod fauna cides continues to be the rule (Chs 6, 10 and of some tropical fruits (citrus, avocado, 12), but currently there is a trend towards pineapple, and mango) (Chs 3, 4, 8 and 9) but evaluating a new generation of pesticides concentrated efforts to use biological control (Ch. 8), adoption of selective spraying (Ch. 7), agents have rarely been made for most pests proper timing of spray applications (Ch. 6), of various tropical fruit crops (Chs 2, 7, 10 and and determining the effect of pesticides on 12). For instance, efforts towards developing predators and parasitoids (Ch. 8). systems for biocontrol of the pink hibiscus In contrast to the extensive information mealybug, Maconellicoccus hirsutus, and the on effects of pesticides on pests, there is very carambola fruit fly, Bactrocera carambolae, little (Ch. 12) information on their effects in the Caribbean were not initiated until on pollinators (Chs 4, 7 and 8). For instance, after these pests had become major threats Aguiar-Menezes et al. suggest in Chapter 12 to valuable crops (Ch. 10). Generally, if a that the deleterious effects on pollinators can stenophagous insect (i.e. avocado weevils, be averted by proper timing of spray applica- papaya fruit fly, avocado thrips, and Annona tions in passion fruit, according to the cultivar. fruit moths) is the major constraint to produc- Purple passion, whose flowers open during tion of a single commodity, then efforts to the morning hours, should be sprayed during develop biological control are pursued half- late afternoon, while the yellow cultivar, heartedly (Chs 5 and 8). The exceptions to this whose flowers open in the afternoon, should rule are the current strong efforts towards be sprayed in the morning. biocontrol of banana weevil (Ch. 2), and the search for natural enemies of avocado thrips (Ch. 8). Efforts also differ among countries. Attractants – pheromones For instance, in Australia and Israel biological control is an important component of Non-selective traps such as black light and Annona pest management (Ch. 7), while other bait traps are commonly used in tropical fruit Annona-producing countries, i.e. Brazil, Ecua- because they can provide useful information dor, Venezuela, Colombia, and Mexico, rely for monitoring purposes. Furthermore, on chemical pest control. development of selective traps (baited with It is likely that with time the use of attractants or pheromones) often to the pest biological control agents for tropical fruit species level, has been a tremendous boost to protection will increase extensively. The IPM of temperate fruit (Beers et al., 1994) and main constraints on this trend are the lack of it may provide the same benefit available for commitment and money. Currently, very few

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8 J.E. Peña

people in tropical countries are researching (1990) reported that field sanitation did these areas, and very few specialists receive not reduce infestation by the mango nut adequate financial support. While major weevil, Sternochetus mangiferae (Coleoptera: emphasis has been given to staple crops Curculionidae) in Hawaii, while in the (i.e. rice and cassava), with the exception of Neotropics, removal of Annona spp. fruit banana, little or no emphasis has been given to infested with the seed borer Bephratelloides fruit crops. cubensis is considered to be a regular practice Scattered through this book are several to avoid future infestations (Ch. 7). Untreated references to microorganisms such as fungi, backyard trees and neglected plantings are bacteria, and viruses pathogenic to insects. considered to be major sources of pests such However, most pathogens of tropical fruit as fruit flies. Thus, in Australia, hygiene and pests are virtually unknown. Apart from attention to alternative host plants that can fungal and bacterial control of insects on increase pest pressure on the Annona (custard citrus, avocado, and banana, there have been apple) orchard, are important (Ch. 7). Mature few studies into applied aspects of this very fruit infested with yellow peach moth or with promising area. In general, it may be said that the Queensland fruit fly should be collected with the exception of citrus and avocado, the and destroyed. Preferred fruit fly hosts like biological control of tropical fruit arthropods guava and loquat should not be planted as has been much neglected and that there is a trap crops in or near the Annona orchard. great need for further work. According to Hoyt and Burts (1974), cultural practices generally do not offer a direct means for controlling pests but, when used Host plant resistance properly, they can enhance natural enemy activity or retard pest population growth to a Host plant resistance offers considerable degree that is important in integrated control promise as a tactic in pest management. Even programmes. With polyphagous insects, the though it appears that most efforts are wild host plants may be so numerous that concentrated in developing genetic resistance special eradication would be impracticable, to plant pathogens, use of this tactic merits yet removal of related wild host plants may attention for numerous crops against numer- be very beneficial where insect pests have ous arthropod pest species. Evaluation of restricted host ranges. Gold et al. in Chapter 2 tropical fruit germplasm collections for describe crop sanitation as an important factor resistance to arthropod pests should become for maintaining low banana weevil densities a high priority. Most efforts are directed at in banana plantings. However, crop sanitation insect vectors (citrus, papaya, and pineapple), has not been firmly established for controlling and pests of mango, avocado, and guava (Chs important pests of avocados (i.e. weevils) 4, 8 and 9). By contrast several valuable fruits, (Ch. 8), Annona (annona seed borer) (Ch. 7), i.e. durian and acerola, continue to be largely and mango (mango seed weevil) (Ch. 4). unnaturalized and selections for improved traits have rarely been made. Pollination

Cultural practices Interest in pollination is as ancient as civilized culture. Farmers have always shown a keen Cultural control concerns the employment of interest in the reproductive biology of plants cultural management methods to minimize and some mechanisms of fruit production insect damage. The use of trap crops, host (Real, 1983) and while most of the studies plant removal, removal of pests, and the have focused on the temperate zone, there is reduction of pests’ habitats are considered an expanding emphasis on investigations of beneficial by some and controversial by oth- tropical forests and plant ecosystems. Several ers. For instance, Hansen and Amstrong studies of tropical plant pollination have

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Introduction 9

been conducted in diverse natural habitats in other countries. For example, Mexico and (i.e. Beach, 1984; Valerio, 1984; Gottsberger, Brazil must respond to standards imposed by 1989) and this information has been applied the USA or Japan that require fruit that is free to agricultural systems. Yet, it is necessary of any cosmetic blemishes, and often this can to remember that agroecosystems may lack be only be achieved by use of agrochemicals some of the complex interactions observed or quarantine treatments (Sharp and Heather, in natural habitats. Young (1982) pointed out 2002). that for trees of tropical forests such as cacao, Standard IPM methodologies, involving production of mature fruit is influenced by a number of control alternatives used alone or factors other than pollinator abundance. It is in combination (such as orchard sanitation, interesting to note that cacao originated as an monitoring, early harvesting, parasitoid understorey tree in Amazonian rainforests, release and wild host removal) have achieved where there was probably a well established some success in controlling pests such as equilibrium between pollinator abundance fruit flies for individual growers (Hendrichs, and abundance of flowers in the tree. Young 1996). However, because these various tactics (1982) concludes that successful pollination are usually implemented in a helter-skelter or in a tropical crop depends in part upon the uncoordinated manner, their effectiveness is floristic complexity of the tree and the effects compromised. Therefore, many commercial of surrounding habitats on the influx of producers are forced to regularly apply insects influencing pollination within the insecticide-bait sprays to protect fruit in agricultural habitat. The authors in this book their orchards from flies dispersing from provide different approaches to these issues. neighbouring orchards and other hosts. In Chapter 8, Wysoki et al. trace the different Since very important polyphagous pests, theories of pollination of avocado. While one i.e. fruit flies, weevils, lepidopterans, etc., school advocates the role of pollinators and affect similar tropical fruit species, the concept the influence of native species of pollinators of area-wide pest control can be applied effec- of avocado, another school asserts the theory tively in large geographical areas, where the that insect pollinators are not needed. A same fruit crops are exploited (Klassen, 2000; similar controversy exists with respect to Lindquist, 2000). When fruit growers pursue a mango (Ch. 4). Peña et al. in Chapter 7 review concerted ‘total pest population management the flowering plant evolution of Annona spp., strategy’ over a substantial area, the number and discuss the methodologies for improving of individual pests produced is reduced pollination mechanisms. In Chapter 12 progressively with time, and the number Aguiar-Menezes et al. summarize studies moving between neighbouring orchards is on passion fruit pollination and discuss largely reduced. Under these area-wide those insect species that could be effective conditions, which require an effective pollinators and tactics that limit their organization of growers, and in some effectiveness. instances increasing technical sophistication, IPM becomes much more effective. Malavasi et al. (1994) discuss this approach for the creation of pest-free areas to facilitate Conclusions exporting of fruit. A pest-free area is one that lacks a quarantine-significant pest species, According to Aluja (1994) there are two major and is separated from infested areas by natu- and opposing forces that drive the dynamics ral or artificial barriers. There are two types of of pest management from a worldwide pest-free areas: (i) pest-free zones are large perspective: trends toward globalization of geographic areas, such as the entire country of markets versus trends toward sustainability Chile, that are certified free of tropical fruit of agricultural practices and conservation flies of economic importance; and (ii) pest-free of biodiversity. Aluja (1994) demonstrated production groves that require the demon- that market forces compel several countries strated suppression of quarantine pests to to comply with quality standards established non-detectable levels. Florida is able to export

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10 J.E. Peña

grapefruit to Japan by creating Caribbean Courses, 18–31 May 1997, Bangalore, India, fruit-fly-free grapefruit groves in about 22 pp. 42–53. counties. Requirements to establish pest-free Alexander, D.McE. and Possingham, J.V. (1984) fields of crop production include a sensitive Potential for fruit growing in tropical Australia. In: Page, P.E. (ed.) Tropical Tree detection programme, suppression of the Fruits of Australia. Queensland Department quarantine-significant pest to non-detectable of Primary Industries, Brisbane, pp. 1–19. levels, strict control of the fields, and safe- Aluja, M. (1994) Bionomics and management of guards to prevent infestation during packing Anastrepha. Annual Review of Entomology 39, and transit to the port of export. 155–178. In conclusion, for better management of Anonymous (1985) Integrated Pest Management for tropical fruit, pests’ habits, importance of their Almonds. University of California, Division of damage and action levels should be known Agriculture and Natural Resources, Oakland, as the foundation for any programme. For California, Publication 3308, 156 pp. the tropical crop in question, more emphasis Anonymous (1991) Integrated Pest Management for Citrus, 2nd edn. University of California, Divi- should be devoted to improved knowledge of sion of Agriculture and Natural Resources, pollinators and ways to improve their effec- Oakland, California, Publication 3303, 144 pp. tiveness; these will be determined by research Bailey, J., Hoffman, M. and Olsen, K. (1988) Black and by practical experience. After these steps light monitoring of two avocado insect pests. are taken, development of better monitoring California Agriculture 42, 26–27. techniques for pests and natural enemies Beach, J.H. (1984) The reproductive biology of the should follow as well as the evaluation of peach or ‘pejibaya’ palm (Bactris gasiapaes) and a feasible biological control (requirements and a wild congener (B. porschiana) in the Atlantic impact of biocontrol agents) programme. lowlands of Costa Rica. Principes 28, 107–119. These are not merely research tools, but Beers, E., Hull, L. and Jones, V. (1994) Sampling pest and beneficial arthropods of apple In: Pedigo, should also be a set of techniques and data L. and Buntin, D. (eds) Handbook of Sampling with practical value for scouts and growers. Methods for Arthropods in Agriculture. CRC Lastly, development of IPM packages for the Press Boca Raton, Florida, pp. 383–415. whole pest complex should consider that all Bennett, F.D., Rosen, D., Cochereau, P. and Wood, B. these arthropods inhabit the same universe. (1976) Biological control of pests of tropical Some of them can be controlled with pesti- fruits and nuts. In: Huffaker, C.B. and cides, others can be controlled by biological Messenger, P.S. (eds) Theory and Practice of agents, cultural methods or by any means that Biological Control. Academic Press, New York, are less harmful to the whole system. pp. 359–387. Boethel, D. and Eikenbary, R. (1979) Pest Manage- ment Programs for Deciduous Tree Fruits and Nuts. Plenum Press, New York, 256 pp. Acknowledgements Braga, R., Cardoso, J.E. and das Chagas, F. (1998) Pragas de Fruteiras Tropicais de Importancia Agroindustrial. Empresa Brasileira de Pesquisa I thank W. Klassen, C. Mannion and R. Agropecuaria, Centro Nacional de Pesquisa Giblin-Davis for comments to improve an Agrodindustria Tropical, Brasilia, 209 pp. earlier version of this manuscript. Ebeling, W. (1950) Subtropical Entomology. Lithotype Process Co, San Francisco, 747 pp. Entwistle, P. (1972) Pests of Cocoa. Longmans, London, 779 pp. References FAO (Food and Agriculture Organization) (2001) FAO Statistical Data Base. http://appsl.fao. Akora, R.K. (1998) Genetic resources of native org/servlet/Xte.FAOStat Data Base. tropical fruits in Asia: diversity, distribution Goodell, G. (1984) Challenges to international pest and IPGRI’s emphasis on their conservation management research and extension in the and use. In: Akora, R.K. and Ramanatha Rao,V. third world: do we really want IPM to work? (eds) Tropical Fruits in Asia, Diversity, Main- American Entomologist 30, 18–26. tenance, Conservation and Use. Proceedings of Gottsberger, G. (1989) Beetle pollination and flower- the IPGRI-ICAR-UTANET Regional Training ing rhythm of Annona spp. (Annonaceae) in

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Introduction 11

Brazil. Plant Systematics and Evolution 167, Technique. CRC Press, Boca Raton, Florida, 165–187. pp. 165–180. Hansen, J.D. and Armstrong, J.W. (1990) The failure Mariu, D. (1999) Integrated Pest Management of of field sanitation to reduce infestation by the Tropical Perennial Crops. CIRAD, France, and mango nut weevil, Cryptorhynchus mangiferae Science Publishers, Enfield, New Hampshire, (F.) (Coleoptera: Curculionidae), in Hawaii. 167 pp. Tropical Pest Management 36, 359–361. Parker, B.L., Skinner, M. and Lewis, T. (1995) Thrips Hare, D.J. (1994) Sampling arthropod pests in Biology and Management. Plenum Press, New citrus. In: Pedigo, L. and Buntin, D. (eds) York, 636 pp. Handbook of Sampling Methods for Arthropods in Pedigo, L. (1994) Introduction to sampling Agriculture. CRC Press, Boca Raton, Florida, arthropod populations. In: Pedigo, L. and pp. 417–432. Buntin, D. (eds) Handbook of Sampling Methods Helle, W. and Sabelis, M.W. (1985a) Spidermites, for Arthropods in Agriculture. CRS Press, Boca Their Biology, Natural Enemies and Control, Raton, Florida, pp. 1–14. Vol. 1A. Elsevier, Amsterdam, 405 pp. Pimentel, D. (ed.) (1981) CRC Handbook of Pest Helle, W. and Sabelis, M.W. (1985b) Spidermites, Management in Agriculture, Vol. I. CRC Press, Their Biology, Natural Enemies and Control, Boca Raton, Florida, 597 pp. Vol. 1B. Elsevier, Amsterdam, 458 pp. Real, L. (1983) Introduction. In: Real, L. (ed.) Hendrichs, J. (1996) Action programs against Pollination Biology. Academic Press, New York, fruit flies of economic importance: session pp. 1–5. overview. In: McPheron, B. and Steck, G. (eds) Rosen, D. (1990a) Armored Scale Insects: Their Biology, Fruit Fly Pests: a World Assessment of Their Natural Enemies and Control, Vol. 1A. Elsevier, Biology and Management. St Lucie Press, Delray Amsterdam, 384 pp. Beach, Florida, pp. 513–519. Rosen, D. (1990b) Armored Scale Insects: Their Biology, Hill, D. (1975) Agriculture Pests of the Tropics and Natural Enemies and Control, Vol. 1B. Elsevier, Their Control. Cambridge University Press, Amsterdam, 687 pp. New York, 516 pp. Smith, D., Beattie, G. and Broadley, R. (1997) Citrus Hoyt, S.C. and Burts, E.C. (1974) Integrated control Pests and Their Natural Enemies: Integrated of fruit pests. Annual Review of Entomology 19, Pest Management in Australia. Queensland, 231–252. Department of Primary Industries, Brisbane, Jeppson, L.R., Keifer, H. and Baker, E. (1975) Mites Australia, 272 pp. Injurious to Economic Plants. University of Swaine, G., Ironside, D.A. and Yarrow, W. H. (1985) California Press, Berkeley, 614 pp. Insect Pests of Tropical Fruit and Vegetables. Keenan, M. (1997) Foreword. In: Smith, D., Beattie, Queensland Department of Primary Indus- G. and Broadley, R. (eds) Citrus Pests and Their tries, Information Series QI83021, Brisbane, Natural Enemies. Department of Primary Australia, 350 pp. Industries, QI97030, Brisbane, Australia, Tandon, P.L. (1998) Management of insect pests 272 pp. in tropical fruit crops. In: Akora, R.K. and Klassen, W. (2000) Area-wide approaches to insect Ramanatha Rao, V. (eds) Tropical Fruits in pest management: history and lessons. In: Asia, Diversity, Maintenance, Conservation and Tan, K.H. (ed.) Proceedings of International Use. Proceedings of the IPGRI-ICAR-UTANET Conference in Area-wide Control of Insect Pests. Regional Training Courses, 18–31 May 1997, 28 May–2 June 1998, Penang, Malaysia, Bangalore, India, pp. 235–245. Penerbit Universiti Sains Malaysia, pp. 21–38. Valerio, C. (1984) Insect visitors to the inflorescence Lamb, K.P. (1974) Economic Entomology in the Tropics. of the aroid Diffenbachia oerstedii (Araceae) in Academic Press, New York, 1995 pp. Costa Rica. Brenesia 22, 139–146. Lindquist, D.A. (2000) Pest management strategies: Verheij, E.W. and Coronel, R.E. (1992) Plant area-wide and conventional. In: Tan, K.H. (ed.) Resources of South-east Asia. Edible Fruits and Proceedings of International Conference in Area- Nuts. Prosea Foundation, Bogor, Indonesia, wide Control of Insect Pests. 28 May–2 June 1998, 446 pp. Penang, Malaysia, Penerbit Universiti Sains White, F. and Elson-Harris, M. (1994) Fruit Flies of Malaysia, pp. 13–19. Economic Significance: Their Identification and Malavasi, A., Rohwer, G. and Campbell, D.S. Bionomics. CAB International, Wallingford, (1994). Fruit fly free areas: strategies to develop UK, 601 pp. them. In: Calkins, C.O., Klassen, W. and Young, A. (1982) Population Biology of Tropical Insects. Liedo, P. (eds) Fruit Flies and the Sterile Insect Plenum Press, New York, 511 pp.

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2 Pests of Banana

C.S. Gold,1 B. Pinese2 and J.E. Peña3 1International Institute of Tropical Agriculture, ESARC, PO Box 7878, Kampala, Uganda; 2Queensland Department of Primary Industries, PO Box 1054, Mareeba, Queensland 4880, Australia; 3Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, Florida 33031, USA

Bananas and plantains (Musa spp.) are among western Africa, Latin America and the Carib- the most important crops in tropical and sub- bean. Dessert bananas, especially Cavendish tropical climates. The genus Musa evolved in clones (AAA), are important export crops in South-East Asia (Stover and Simmonds, 1987) Latin America and the Caribbean, Africa, Asia where numerous undomesticated Musa spe- and the Pacific, and Australia. cies still grow as ‘opportunistic weeds’ (Price, In terms of gross value of production, 1995). Edible bananas (Musa spp., Eumusa bananas and plantains are the fourth most series) originated within this region from two important global food crop. World production wild progenitors, Musa acuminata and M. is calculated to be 87,934,558 t (INIBAP, 2001). balbisiana, producing a series of diploids, trip- Export bananas are the developing world’s loids and tetraploids through natural hybrid- fourth most important commodity and most ization. Additionally, man has selected for important fruit crop (INIBAP, 2001). Bananas parthenocarpy (development of fruit without grown for export are almost exclusively of one pollination or seeds). Simmonds and Shep- variety, ‘Cavendish’; this cultivar accounts herd (1955) provided a key by which these for little more than 10% of global production. naturally hybridized bananas may be divided Most banana production consists of a wide into six genome groups (i.e. AA, AAA, AAB, range of locally adapted clones that are AB, ABB, ABBB) based on the relative contri- consumed within the region (INIBAP, 2001). butions of M. acuminata and M. balbisiana. Banana production systems range from Domesticated bananas include a wide range low input kitchen garden and small-scale of dessert, cooking and brewing cultivars subsistence stands to large-scale, high input (Stover and Simmonds, 1987). The most export banana plantations. Some commercial extensively grown bananas are triploids. plantations of dessert bananas or plantains are Plantains (AAB) evolved in southern replanted annually. By contrast, well-managed India with a secondary centre of Musa banana stands have produced stable yields diversity in West Africa. East Africa has also for 30–100 years, even under low input condi- evolved as a secondary centre of Musa diver- tions. At the same time, an extended harvest sity with numerous, locally evolved highland period ensures resource-poor farmers with cooking and brewing clones (denoted AAA- food and income throughout the year. How- EA). Cooking banana is the primary staple ever, insect pests can cause reduced yields and crop in the Great Lakes region of eastern shortened plantation life (Rukazambuga et al., Africa, while plantain is an important food in 1998; Gold et al., 1999d).

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 13

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14 C.S. Gold et al.

Phenology Pests

Bananas are rhizomatous herbaceous plants Pest and disease pressures have increased ranging in height from 0.8 to 15 m (Turner, considerably in recent years, and yield loss 1994). A mat (= banana stool) consists of an due to pests and/or disease attack is now underground corm (rhizome) from which one considered the most significant factor affect- or more plants (shoots) emerge. Adventitious ing banana and plantain production world- roots spread extensively 4–5 m from the par- wide (INIBAP, 2001). The status of specific ent and down to 75 cm or more (Nakasone pests and diseases reflects, in part, the banana and Paull, 1998); however, most roots are clone and the management system. At a near the soil surface. Plants represent a single global level, diseases are considered the shoot (pseudostem, stem, leaves, flower and major threat, followed by nematodes and bunch). Yield is normally expressed in kg/ insects and mites. Nakasone and Paull (1998) area/year reflecting both number and size suggest that the continuous nature of banana of bunches harvested. The banana shoot production makes pests such as nematodes consists of a pseudostem bearing the leaves more important than insects and mites; and a true stem bearing the flower and fruit however, Pinese and Piper (1994) argue that (bunch). The apparent stem or pseudostem is management of insect pests is a key operation actually composed of leaf sheaths. New in banana production in Australia. Gold and leaves emerge from the centre of the pseudo- Gemmill (1993) reported that pest problems stem. A single plant produces 25–50 leaves in banana and plantain significantly reduce in its lifetime and normally supports 10–15 yields in all tropical regions, and particularly functional leaves at any one time (Nakasone in Africa. and Paull, 1998). The true stem arises from Detailed information on banana pests the apical meristem after leaf production has has been presented by authors in different terminated and grows through the centre of parts of the world (Ostmark, 1974; Gold the pseudostem (Stover and Simmonds, 1987; and Gemmill, 1993; Pinese and Piper, 1994; Turner, 1994; Karamura and Karamura, 1995). Fancelli and Martins, 1998). Integrated pest One terminal inflorescence emerges from management tactics have been developed for the true stem and bends downward after several pests; in general, chemicals are widely extrusion. After the fruit matures, the stem used in some systems, although these are dies back to the corm. Farmers normally cut beyond the means of many growers. Environ- harvested plants between ground level and mental degradation and the development 1 m. Crop residues may be used for weevil of insect resistance have highlighted the traps (Gold, 1998). limitations of chemically based control New plants (ratoons) are produced by strategies and the need for integrated pest suckers emerging from lateral buds in the management, including host plant resistance, corm. These can be left in situ or serve as cultural control and biological control. a source of planting material, in which case In this chapter we will address manage- they are removed and planted elsewhere. ment of the most common arthropod pests of Normally, a banana mat consists of three banana in tropical areas. or more plant generations (= ratoons or crop cycles) at any one time. Plant density is controlled by the farmer through desuckering. As banana stands age, mats ‘divide’ and the Pests of Rhizome and Pseudostem relationship between plants (e.g. sharing of a common corm) becomes more tenuous; Banana weevil, Cosmopolites sordidus thus, in older stands, mat definition becomes (Germar) unclear. Suckers used to establish new fields are called the ‘mother plant or plant crop’ The banana weevil, Cosmopolites sordidus (Stover and Simmonds, 1987; Turner, 1994). (Germar), is an important pest of banana,

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Pests of Banana 15

plantain and ensete (Plate 1). Damage to the unclear how long the weevil has been present banana plant is entirely the result of larval in most areas. feeding. Weevil attack can prevent crop The banana weevil is an oligophagous establishment, cause significant yield reduc- pest with a narrow host range, attacking tions in ratoon cycles and contribute to short- wild and cultivated clones in the genera Musa ened plantation life. For example, the weevil (banana, plantain, abaca) and Ensete. Reports has been implicated as a primary factor con- of alternative hosts appear to be in error. tributing to the decline and disappearance Nevertheless, L. Traore (personal communi- of East African highland cooking banana cation) was able to maintain larvae through (Musa spp., genome group AAA-EA) from its several instars using a factitious host (pro- traditional growing areas in central Uganda cessed Xanthasoma saggittifolium), while Pavis (Gold et al., 1999b) and western Tanzania (1988) and Schmitt (1993) had modest success (Mbwana and Rukazambuga, 1999). Banana rearing larvae on artificial diets. weevil pest status may reflect ecological conditions, banana types, cultivar selection, Banana weevil biology and management systems. ADULTS Longevity, tropisms, and distribution. The Taxonomy, morphology, distribution banana weevil displays a classical ‘K’ selected and host range life cycle (Pianka, 1970) with long life span and The banana weevil was first identified by low fecundity. Adults may live up to 2 years Germar in 1824 from specimens collected in (Froggatt, 1925; Treverrow et al., 1992), Java and given the name Calandra sordida.In although mean longevity under field condi- 1885, Chevrolat changed this to its currently tions is not known. The adult is nocturnally recognized name Cosmopolites sordidus active and characterized by negative photo- (Germar). The genus Cosmopolites belongs tropism, strong hygrotrophism, thigmo- to the subfamily Rhynchophorinae of the tactism, gregariousness and death mimicry family Curculionidae (weevils and snout (Delattre, 1980; Ittyeipe, 1986; Tsai, 1986). The beetles). Taxonomic keys are presented by adults favour moist environments and are Zimmerman (1968a); adult morphology has closely associated with banana mats (being been described by Moznette (1920), Beccari primarily in the leaf sheaths, around the base (1967), Zimmerman (1968b), Viswanath of the mat or, occasionally, in larval galleries) (1976) and Nahif et al. (1994); reproductive or with detached residues (Gold et al., 1999d) system morphology by Cuille (1950), (Plate 2). The weevils feed on rotting banana Beccari (1967), Uzakah (1995) and Nahif tissue and are not pests (Budenberg et al., (1998); and larval morphology by Moznette 1993b). Under field conditions, the weevil can (1920) and Viswanath (1976). Males can survive for 3 to 6 months once all banana be separated from females by curvature material is removed (Froggatt, 1924; Peasley and punctuation of the rostrum and by and Treverrow, 1986; Allen, 1989; Mestre and curvature of the last abdominal sternite Rhino, 1997). (Roth and Willis, 1965; Longoria, 1968). The sex ratio is 1 : 1. Daily and seasonal activity periods. Banana The banana weevil originated within weevil adults are active between 1800 and the Indo-Malayan region (Simmonds, 1966; 0600 h (Cuille, 1950; Uzakah, 1995) with great- Zimmerman, 1968b; Waterhouse, 1993), coin- est activity between 2100 and 0400 h (Uzakah, cident with the area of origin of bananas 1995). A substantial proportion of the popula- (Stover and Simmonds, 1987). Spread of the tion may be inactive for extended periods of weevil is presumed to have been through the time (S. Lux, personal communication). The movement of infested planting material. The weevils are sedentary during daylight hours. weevil is currently found throughout Asia, Seasonal differences in trap captures of Oceania, Australia, sub-Saharan Africa and adult weevils have been reported by many the Americas (Cuille and Vilardebo, 1963). It is authors. Trap captures may reflect activity

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16 C.S. Gold et al.

patterns, but do not provide meaningful esti- plants, conspecifics and/or mates. Cuille mates of population density (Vilardebo, 1973) (1950) was the first to propose and test which require mark and recapture methods ‘chemotropisms’ of banana weevil. He con- (Price, 1993; Gold and Bagabe, 1997). Higher cluded that olfactory cues were most impor- trap captures have been found in dry seasons tant in host location, while chemoreception (Yaringano and van der Meer, 1975), rainy played the predominant role in host accep- seasons (Cuille, 1950; C.S. Gold et al., unpubli- tance. Cuille concluded that chemoreception shed), or unrelated to climatic factors (Oliveira is probably more important than olfaction for et al., 1976; Delattre, 1980; Pavis, 1988). These a sedentary insect like banana weevil. Further conflicting results provide an unclear picture work by Budenberg and Ndiege (1993) and of when adults are most active and, hence, Budenberg et al. (1993b) found that males and most vulnerable to control interventions. females were both attracted to plant volatiles (i.e. kairomones); they suggested the weevils Dispersal and movement. Dispersal of the used these volatiles for attraction to food weevil may be by walking, occasional flight sources rather than oviposition sites. Buden- and dissemination of infested planting berg et al. (1993a) also demonstrated the pres- material. The maximum observed distance ence of an aggregation pheromone (sordidin) moved by walking was 35 m in 3 days (Gold produced in the male hindgut and attractive and Bagabe, 1997) and 60 m in 5 months to both sexes. It is likely that weevils are (Delattre, 1980). Gold et al. (1999d) found only attracted to their host plants by plant volatiles a small percentage of weevils moved > 25 m and that the aggregation pheromone then in 6 months. This suggests that dispersal serves as an arrestant from further movement. by walking may contribute to invasion of The use of pheromones and attractive neighbouring fields but not much beyond. plant volatiles (i.e. kairomones) as a means The nocturnal habit of the weevil has of controlling banana weevil through mass largely precluded direct observations on trapping and/or in baits for delivery of weevil flight under field conditions. Although B. bassiana was first proposed by Budenberg the banana weevil has functional wings, most et al. (1993a) and Kaaya et al. (1993). observers believe the weevil rarely flies (e.g. Jayaraman et al. (1997) also suggested that Gordon and Ordish, 1966; Pinese and Piper, semiochemical-enhanced mass trapping 1994; Sponagel et al., 1995). In contrast, Cuille could overcome the low reproductive and Vilardebo (1963) reported the weevil capacity of the insect and lead to successful to be a good flyer and suggested that this control. Chemtica International SA in Costa may explain wider dissemination than a few Rica has begun commercial production of kilometres. banana weevil pheromones (enhanced with The banana weevil’s narrow host range kairomones) in a product called Cosmolure+ and limited dispersal capability mitigate (C. Oehlschlager, personal communication). against immigration of adults into isolated or newly planted banana stands by walking or Oviposition. Female weevils are sexually flying (Gold et al., 1999d). It has been widely immature upon emergence with first ovi- recognized that dispersal of banana weevil is position occurring 4–6 weeks later (Uzakah, primarily through infested planting material 1995). Mean oviposition rates of 1–11 eggs (e.g. Froggatt, 1925; Pinese and Piper, 1994). week−1 have been recorded in the laboratory Banana suckers may contain adults in the (Cuille, 1950; Delattre, 1980; Koppenhofer, leaf sheaths or immature stages within the 1993a; Abera, 1997; Gold, Kagezi and Nemeye, rhizome. This suggests that the use of clean unpublished) and 0.5–1.2 eggs week−1 in the planting material is an important factor in field (Abera, 1997). Oviposition is believed establishing healthy banana stands. to be greatly reduced in dry seasons (Cuille, 1950; Nonveiller, 1965). Semiochemicals. Olfactory cues may be Eggs (0.5 × 2 mm) are deposited singly in utilized by banana weevils in locating host the base of the host plant (i.e. leaf sheaths, leaf

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Pests of Banana 17

scars, rhizome) in orifices (1–2 mm deep) thermal requirement of 538 degree-days. The excavated by the female weevil with her non-feeding prepupal stage is 3–4 days rostrum. Oviposition occurs on plants of any (Mesquita et al., 1984; Gold et al., 1999c). age and on crop residues (Abera et al., 1999). Pupation is in a bare chamber excavated by The weevils have been variously reported to the larvae near the rhizome surface of the host prefer young plants (Cuille, 1950), preflow- plant (Vilardebo, 1960). The developmental ered plants (Treverrow and Maddox, 1993), threshold for the pupal stage is 10.1°C with flowered plants (Vilardebo, 1973; Mesquita a thermal requirement of 121 degree-days and Caldas, 1986; Abera et al., 1999) and crop (Traore et al., 1996). Under tropical conditions, residues (Treverrow and Maddox, 1993; Gold the larval stage probably lasts 4–6 weeks, and Bagabe, 1997; Abera et al., 1999). while the pupal stage is 1 week.

IMMATURES Banana weevil developmental Sampling methods for estimating adult rates under ambient temperatures (reviewed population density and larval damage by Schmitt, 1993; Traore et al., 1993) show wide variability in stage duration: 3–36 days for The most common sampling methods for eggs, 12–165 days for larvae (Plate 3), 1–4 days banana weevil include trapping of adults for prepupae, 4–30 days for pupae and 24–220 and estimates of larval damage in recently days from egg to adult. The longest stage harvested plants. Trapping as a means of durations were found in Australia where assessing banana weevil population levels seasons are pronounced and the range in has been employed since 1912 (Knowles and weevil development times large; under these Jepson, 1912) and continues to be widely conditions, development rates were up to used. A variety of traps (described by four times as long as recorded anywhere else. Castrillon, 1989) are made out of crop While temperature is certainly the most criti- residues (i.e. recently harvested rhizomes cal factor in determining developmental rates, and pseudostems). Those using rhizome relative humidity, cultivar, age of plant, food material are generally more attractive to quality and population density may also be banana weevils than those made from involved (Mesquita et al., 1984; Schmitt, 1993). pseudostems. Trap quality and climatic Traore et al. (1993) determined a develop- factors can influence trap catches, making mental threshold for the egg stage of 12°C interpretation of results difficult (Vilardebo, and a thermal requirement of 89 degree-days. 1973; Bakyalire, 1992). Under tropical conditions, the egg stage Weevil populations can be more accu- is commonly 7–8 days. Field eclosion rately estimated using standard mark and rates probably exceed 90% in the field. recapture methods including trapping, mark- Koppenhofer and Seshu Reddy (1994) found ing, releasing and subsequent retrapping lower hatchability for eggs in pseudostems, (Delattre, 1980; Price, 1993; Gold and Bagabe, possibly due to higher water content or 1997; Gold et al., 1997). In Cameroon, Delattre metabolites. Kiggundu (2000) suggested that (1980) estimated weevil densities in two fields viscosity and metabolites of plant sap in to be 2600 ha−1 and 15,600 ha−1, respectively. resistant clones may also reduce egg success. In a single watershed in Ntungamo district, Upon hatching, first instar larvae Uganda, Gold et al. (1997) found weevil densi- bore directly into the plant. The larvae feed ties to range from 1600 to 149,000 ha−1 with a throughout the rhizome and will also enter median population of 9300 ha−1 (= 15 per mat). the true stem (i.e. after flowering). In severe This within-site variability suggests that man- attacks, the larvae may move from the mother agement plays an important role in regulating plant into young suckers (Vilardebo, 1960; weevil populations. Champion, 1975). The number of instars has Unfortunately, estimates of weevil popu- been variously reported to range from five to lations are only poorly related to damage eight (reviewed by Gold et al., 1999c). Traore levels (Shillingford, 1988; Gowen, 1995). For et al. (1996) found a developmental threshold example, Gold et al. (1997 and unpublished) for the larval stage of 8.8°C with a total found a weak relationship between estimates

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18 C.S. Gold et al.

of weevil adult density and damage (r = 0.11). Pest status This suggests that, all other things being equal, control methods targeting adult The pest status of banana weevil remains weevils may be less effective than those controversial, with yield loss estimates against the immature stages, and may also ranging from 0 to 100% (e.g. Sengooba, 1986; require a considerable lag time before pop- Sponagel et al., 1995; Mestre and Rhino, 1997) ulation reductions are translated into reduced (Table 2.1). It is often unclear how many yield damage and increased yields. loss estimates were derived and whether they Vilardebo (1960) proposed that visual purport to represent single fields or regional observations on larval damage are a better estimates. Moreover, some of these studies indicator of weevil pest status than trap failed to partition damage effects of weevils counts and recommended counting the and nematodes and yield loss estimates are, number of galleries exposed on the rhizome thus, confounded. Farmers are well aware periphery. Vilardebo (1973) then proposed that weevil damage is more important in a coefficient of infestation (CI) in which the older stands and on-station trials have shown rhizome is pared below the collar to a depth of increasing yield losses over time (Rukazam- 1–2 cm and the proportion of rhizome surface buga, 1996). Thus, single cycle yield loss trials (i.e. 0–100%) with weevil galleries is esti- may be misleading. In addition, the weevil’s mated. Although the CI has been widely used, importance may be influenced by banana the scoring system is not clearly defined and clone and management system. Weevil remains highly subjective. To standardize the damage levels are likely to be very different scoring system, Mitchell (1978) developed on Cavendish bananas (AAA) grown in a percentage coefficient of infestation (PCI) commercial plantations than on highland in which the upper rhizome is pared and cooking bananas (AAA-EA) or plantains presence/absence of peripheral weevil dam- (AAB) grown in smallholdings. Pest status age is recorded for each of ten sections, each within genome groups is also in dispute. For covering 18° of the rhizome surface. example, recommended action thresholds on Internal damage within the rhizome Cavendish banana vary from two weevils per probably has a greater impact on banana trap in Brazil (Moreira, 1979) to 15–25 weevils growth and bunch filling than damage to per trap in Central America (Anonymous, the rhizome periphery. Damage to the central 1989; Sponagel et al., 1995). cylinder is likely to affect nutrient transport Ecological factors and management prac- and stem growth while damage to the cortex tices may also influence yield loss. The weevil may adversely affect root development and is absent (Lescot, 1988) or in low numbers lead to snapping and toppling (Taylor, 1991; (Castrillon, 2000; Gold and Okech, unpub- Gold et al., 1994b). Moreover, the ability of lished) above 1600 m above sea level. As a the weevil to penetrate the rhizome may be result, it is unimportant in much of the Ensete cultivar related; as such, the CI and PCI serve growing regions of Ethiopia (M. Bogale et al., as poor estimates of internal rhizome damage unpublished) and part of the highland banana (Ogenga-Latigo and Bakyalire, 1993; Gold growing region of eastern Africa. In Ghana, et al., 1994b). Therefore, Gold et al. (1994a,b) low levels of weevil damage in plantain may proposed a scoring method in which two result from the short crop cycle (one or two cross-sections were made in the rhizome ratoons) before replanting (Schill, 1996). (at the collar and 10 cm below the collar). In Yield losses to banana weevil have been each section they estimated the percentage of associated with sucker mortality, plant loss, surface area taken up in galleries in the central reduced bunch weights and shorter stand life. cylinder and in the outer cortex. Rukazam- Newly planted stands in or near previously buga (1996) reported a stronger relationship infested fields may suffer high levels of plant between damage to the central cylinder and loss (Ambrose, 1984; Price, 1994) as a sucker yield, than with damage to the cortex and can be killed by a single larva if it attacks rhizome periphery. the growing point (C. Gold, personal observation). Moreover, ovipositing weevils are

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Pests of Banana 19

Table 2.1. Reported yield losses to banana weevil.

Continent/country Yield loss Clone Methods Reference

Latin America Brazil 30 Moreira, 1971 20–50 Gallo et al., 1978 Abandoned Observ. Arleu and Neto, 1984 Colombia up to 80a Marcelino and Quintero, 1991 Cuba 22–34 Trials Reinecke, 1976 > 19> Trials Calderon et al., 1991 20 Trials Masso and Neyra, 1997 Ecuador 20–40 Champion, 1975 Honduras 8–26 Roberts, 1955 0 Trials Sponagel et al., 1995 Peru a48a Liceras et al., 1973 Puerto Rica a30–70a Ingles and Rodriguez, 1989 b90b Trials Roman et al., 1983 Africa Cameroon 20–90 Lescot, 1988 Congo up to 90 Ghesquiere, 1925 Ghana 25–90 AAB Gorenz, 1963 Kenya 24–90 AAA-EA Trials ICIPE, 1991 %16–53% AAA-EA Trials Ngode, 1998 up to 100% AAA-EA Koppenhofer, 1993 %22–76% AAA-EA Trials Musabyiamana, 1999 Tanzania Kagera 30 AAA-EA Walker et al., 1983 ab30ab AAA-EA Sikora et al., 1983 15 Trials Uronu, 1992 Uganda 5–44 AAA-EA Trials Rukazambuga et al., 1998 b40–50b AAA-EA Trials Gold et al., 1998 Central 20–60 AAA-EA Damagec Gold et al., 1999 Masaka up to 100a AAA-EA Observ. Sengooba, 1986 Rakai up to 100a AAA-EA Observ. Sengooba, 1986 > 50% AAA-EA Observ. Sebasigari and Stover, 1988 West Africa %35–40% AAB Sery, 1988 Asia/Pacific India b35b Trials Job et al., 1986 Tonga < 10< Damageb Crooker, 1979 30–60 Damageb Englberger and Toupu, 1983 up to 80a Observ. Pone, 1994

aPlant loss due to toppling and snapping attributable to weevils. bComposite weevil and nematode. cEstimated from Rukazambuga et al. (1998).

attracted to cut rhizomes, making newly of weevil attack and low levels of nematode detached suckers especially susceptible to damage. Snapping (i.e. breaking of the attack. Toppling is often attributed to plant rhizome) may also occur on plants with parasitic nematodes that attack the root severe weevil damage (Gowen, 1995). In cen- system, thereby reducing anchorage (Gowen, tral Uganda, banana weevils have contributed 1995). However, it appears likely that weevil to the decline in stand life from > 30 years to damage reduces root number and can also less than 4 years (Gold et al., 1999b). contribute to toppling. For example, in Ugan- In a yield loss trial on highland banana in dan field trials, Rukazambuga (1996) found Uganda, Rukazambuga et al. (1998) related extensive toppling in mats with high levels levels of weevil damage in the central cylinder

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20 C.S. Gold et al.

(cf. Gold et al., 1994b) to plant growth, unfavourable to pest build-up. For banana maturation rates and yield over four crop weevil, habitat management includes the cycles. (Nematode damage was low (root use of clean planting material, management necrosis index < 3%) suggesting that effects of crop residues (i.e. sanitation) and trapping. were attributable only to weevils.) Damage rose from 4% in the plant crop to 17% in CLEAN PLANTING MATERIAL IN CLEAN FIELDS The the third ratoon (N.D.T.M. Rukazambuga, use of clean planting material can reduce unpublished), while yield loss to weevils initial banana weevil infestations and retard increased from 5% in the plant crop to 44% pest build-up for several crop cycles. At the in the third ratoon. In the third ratoon, plant same time, it can protect new banana stands loss and reduced bunch size were equally against nematodes and some diseases. responsible for lower yields. Suckers used as planting propagules often Weevil pressure has been widely believed contain weevil eggs, larvae and, occasionally, to be associated with ‘poor’ (i.e. low levels of) adults. This provides the principal entry management, stressed plants, bad drainage, point of banana weevils into newly planted acid or low fertility soils, weedy fields, inade- fields. Removing these weevils from planting quate sanitation, extended droughts and material eliminates the most important source nematode infestations (e.g. Froggatt, 1925; of infestation in new plantations. The insect’s Ostmark, 1974; Speijer et al., 1993; Gowen, low fecundity and slow population growth 1995; Sponagel et al., 1995). In Uganda, higher further suggest that a reduction in initial levels of weevils have been attributed to infestation level will impede population reduced crop sanitation and other manage- build-up and provide extended protection to ment practices (Gold et al., 1999b). newly planted fields. As a result, the use of In contrast, Rukazambuga (1996) found clean planting has been widely recognized similar percentages of yield loss (27%) in and promoted. stressed (i.e. intercropped with finger millet) A number of methods have been and vigorous (i.e. mulched monoculture) proposed for freeing planting materials from banana. This translated into a 2.5 t ha−1 loss weevils. These include tissue culture, paring in the intercrop and a loss of 6.3 t ha−1 in the and hot-water treatment. With all methods, mulch. These data suggest that banana weevil reinfestation remains a critical concern. can be an important constraint in well- Froggatt (1925) advocated the use of clean managed banana stands. planting material and recommended against planting near infested fields or in previously Integrated pest management of banana weevil infested sites. Previously infested fields can be rid of weevils by crop rotation or fallowing. Current research results suggest that no The use of tissue culture plantlets for single control strategy will be likely to banana weevil control has been recommen- provide complete control for banana weevil. ded by Peasley and Treverrow (1986). Unlike Therefore, a broad integrated pest manage- other methods, tissue culture plants are likely ment (IPM) approach might provide the best to be 100% free of banana weevils and nema- chance for success in controlling this pest. todes at the time of planting. However, tissue The components of such a programme culture plantlets are not universally available include habitat management (cultural con- or affordable (Seshu Reddy et al., 1998). trol), biological control, host plant resistance Paring, or removal of the outer surface and (in some cases) chemical control. of the rhizome, has also been widely recommended (e.g. Froggatt, 1925; Sein, 1934; Seshu Habitat management (cultural control) Reddy et al., 1998). Paring can expose weevil galleries and allow the farmer to reject heavily Habitat management can reduce herbivore damaged suckers. Removal of all of the leaf levels by creating an environment that sheaths and paring of the entire rhizome will reduces pest movement, promotes host eliminate most weevil eggs and first instar plant tolerance of pest attack and/or is larvae. Many later instar larvae are likely to be

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Pests of Banana 21

deeper within the rhizome and not removed CROPPING SYSTEMS AND CROP MANAGEMENT by paring. The use of multiple cropping systems for Hot water treatment to kill weevil eggs the control of banana weevil may be limited. and larvae was first recommended in the Mixed cropping systems often result in lower 1920s (Ghesquiere, 1924) and continues to be insect pressure by reducing immigration promoted (Seshu Reddy et al., 1993, 1998). rates, interfering with host plant location Ordinarily, the rhizomes are pared and then and increasing emigration rates (Altieri completely submerged in hot water. Sein and Letourneau, 1982; Risch et al., 1983). (1934) reported that placing suckers in boiling However, banana weevils are sedentary water for 1 min killed all weevil eggs and sur- insects that live in perennial systems in the face larvae. The use of some hot water treat- presence of an abundant supply of hosts. ment regimes (e.g. 52°C for 27 min or 54°C Kehe (1985) found much lower incidence for 20 min) is also a highly effective control of weevil attack (CI = 6%) in plantains mixed against banana nematodes (Seshu Reddy et al., with older coffee stands (i.e. > 5 years) than 1993, Speijer et al., 1995). These temperatures in those mixed with younger coffee plants have been suggested for concurrent manage- (CI = 91%), with cacao (CI = 88%) or with ment of weevils and nematodes (Seshu Reddy annual crops (CI = 79%). He postulated that et al., 1993, 1998). However, Gold et al. (1998a) caffeine produced by older coffee plants found less than 33% mortality of banana served as an insecticide or feeding inhibitor. weevil larvae for similar temperature regimes. By contrast, Uronu (1992) tested a series of Larval survival was greater in the central cyl- intercrops and failed to find a viable crop inder than in the cortex. Arroyave (1985) also mixture that would both reduce weevil reported that hot water baths are not effective numbers and produce satisfactory banana at killing larvae deep within the rhizome. yields. Gold and McIntyre (unpublished) Gold et al. (1998b) found lower weevil found no effect of green manures numbers for 11–27 months in plots planted with reported insecticidal properties (i.e. from (i) pared or (ii) pared and hot water Canavalia, Mucuna, Tephrosia) either on weevil treated rhizomes than in plots planted with adult numbers or on damage. untreated suckers (controls). Weevil damage Weeding, removal of trash from the base levels in controls were 70–200% higher than of the mat, deleafing, and desuckering have all in plots grown from treated planting material been reported as means of eliminating shelters for the plant crop. However, all treatments for weevils or making the environment at the displayed similar levels of weevil damage in base of the mat less favourable (Wallace, 1938; the first ratoon. Hot water treatment had little Seshu Reddy et al., 1998). However, few data advantage over paring for controlling weevil are available to demonstrate possible effects but afforded excellent nematode control for of these practices on weevil levels. Recent the duration of the trial. work has demonstrated that grass mulches However, paring to remove weevil eggs may increase weevil damage by creating and expose larval damage has not been widely a more favourable environment (i.e. cool, adopted by farmers in East Africa. Many moist conditions) for adult weevils (Price, farmers believe that suckers will not perform 1994; Rukazambuga, 1996; Braimah, 1997). In well following removal of most or all of the Tanzania and Uganda, some farmers mulch root system. In Tanzania, for example, Taylor away from the base of the mat as a means (1991) reported that farmers viewed the of reducing weevil infestations (Varela, 1993; recommendation of rhizome paring with Ssennyonga et al., 1999). ‘extreme disbelief’. Implementation of hot Deep planting and earthing up have been water baths for the control of banana weevils recommended to render the rhizome inacces- and nematodes requires investment in a sible to ovipositing females and prevent high hot water tank and a heating source (e.g. mat. Seshu Reddy et al. (1993) planted cooking electricity, gas burner, wood). As a result, bananas at depths of 15, 30, 45, and 60 cm adoption by resource-poor farmers may be in drums and reported that shallow planted limited (c.f. Ssennyonga et al., 1999). suckers were more prone to attack, although

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22 C.S. Gold et al.

some weevils were able to find the deepest weevil population dynamics and related planted suckers. However, Abera (1997) damage. showed that weevils freely oviposit in leaf sheaths, while M. Masanza (unpublished) TRAPPING ADULT WEEVILS The use of trap- found greater levels of subterranean ovi- ping adults to control banana weevils has position during dry seasons. been controversial. Knowles and Jepson (1912) noted the attraction of banana weevils CROP SANITATION Following harvest, crop to crop residues (i.e. harvested rhizomes and residues may serve as shelters for adults (Gold pseudostems) and proposed trapping adults et al., 1999d) and oviposition sites for females. with these materials. Since then, trapping For example, Gold et al. (1999d) found > 35% has been widely recommended as a banana of adult weevils to be associated with crop weevil control by many workers (e.g. Sein, residues. Banana weevils readily oviposit on 1934; Hargreaves, 1940; Ndege et al., 1995; residues for extended periods after harvest Seshu Reddy et al., 1995). Enhanced trapping (Abera, 1997; M. Masanza, unpublished). For with the addition of chemicals, biopesticides some clones, attack on residues may be more and/or semiochemicals has also been pro- extensive than that against growing plants posed (Veitch, 1929; Yaringano and van der (e.g. Gros Michel in Ecuador; Cavendish Meer, 1975; Schmitt et al., 1992; Budenberg in Australia and Latin America, Kisubi et al., 1993a; Kaaya et al., 1993). For example, in Uganda (Vilardebo, 1960; Treverrow Jayaraman et al. (1997) and Alpizar et al. (1999) and Bedding, 1993; Gold and Bagabe, 1997; suggested that mass trapping with semio- H.E. Ostmark, personal communication). chemicals could overcome the weevil’s low Crop sanitation has been widely recom- fecundity and slow population build-up, and mended to eliminate weevil refuges and lead to successful control. Similarly, Braimah breeding sites (Ghesquiere, 1924; Hargreaves, (1997) suggested that the use of pseudostem 1940; Waterhouse and Norris, 1987; Smith, traps, enhanced by semiochemicals and 1995). Methods include cutting residues at combined with other compatible control or below the soil surface and chopping methods (e.g. entomopathogens), holds the or splitting old rhizomes and pseudostems. key to banana weevil control. In contrast, However, the value of sanitation as a means Mestre (1997) concluded that the weevil is of weevil control has been disputed. For a poor candidate for mass trapping with example, Peasley and Treverrow (1986) and semiochemicals because it is soil dwelling, Treverrow et al. (1992) suggest that crop sedentary and rarely flies. hygiene (i.e. sanitation) is the long-term key to The effect of trapping on weevil popu- weevil control and that without it all other lations will, in part, reflect the intensity of control measures are pointless. Nanne and trapping (i.e. frequency and density) and the Klink (1975) report that sanitation can drasti- types of materials used. Inclusion of rhizome cally reduce weevil populations. Farmers in material increases a trap’s attractivity to central Uganda felt that abandonment of weevils. Thus disc-on-stump traps tend to sanitation practices was an important factor have higher weevil catches than pseudostem in increasing weevil problems on their farms traps (see Castrillon, 1989, for description). (Gold et al., 1999b). In contrast, Jones (1968) However, pseudostem trapping is most often felt that sanitation required too much labour, recommended for systematic trapping studies while Gold (1998) suggested that it is possible because a single harvested plant can only sup- that crop residues might act as ‘trap crops’ port one disc-on-stump trap (fixed in space), drawing gravid female weevils away from while the same plant can provide material for growing plants. Much of this debate is specu- many pseudostem traps (placed where the lative, based on perceptions of weevil pest farmer deems most useful. In addition, it is status, intuitive beliefs on population dynam- likely that trapping in established fields will ics and on-farm observations. Unfortunately, result in a gradual decline in weevil numbers there have been virtually no data from con- with a lag time required before effects are trolled studies on the role of crop sanitation in manifested in reduced damage.

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Weevil reductions due to trapping have there were no significant treatment effects. been reported by Masanza (1995), Ndege et al. Moreover, there was only a weak relationship (1995), Seshu Reddy et al. (1995), Vilardebo between the number of weevils removed and (1950), Yaringano and van der Meer (1975), the change in population density. The results Arleu and Neto (1984), Arleu et al. (1984), suggest that intensive trapping can, but does Koppenhofer et al. (1994), and Ngode (1998). not always, reduce weevil numbers. For example, Yaringamo and van der Meer The use of enhanced trapping with (1975) reported a 50% population reduction semiochemicals could result in higher rates of from 4 months of rhizome trapping, but weevil removal at lower trap densities and the means by which this reduction was with reduced labour. Chemtica International determined is not clear. Seshu Reddy et al. SA, in Costa Rica, tested lures with male (1995) also found a 50% reduction in weevils aggregation pheromones and found that a captured following systematic trapping. formulation, Cosmolure+ (containing a mix- Koppenhofer et al. (1994) implemented three ture of the four sordidin isomers plus plant trapping studies and found reductions of volatiles) was most attractive to both male 33–67% over periods of time ranging from and female banana weevils (C. Oehlschlager, 7 weeks to 1 year. personal communication). Using interference In each of these studies, comparisons studies by collecting weevils from pheromone- were made with initial populations and, thus, baited pitfall traps placed at different dis- the trials lacked proper controls, making the tances, Oehlschlager (personal communica- results inconclusive. For example, reported tion) determined that the optimum spacing of weevil reductions in the Seshu Reddy et al. traps was 20 m. Current recommendations are (1995) study and two Koppenhofer et al. (1994) to place 4 traps ha−1. These traps are replaced trials were interpreted from trap capture rates, monthly and systematically moved through which may have reflected weather conditions the field. and trap efficiency (Vilardebo, 1973). In a third Alpizar et al. (1999) reported that pitfall trial, Koppenhofer et al. (1994) released a traps with Cosmolure+ collected 12 times known number of weevils and then estimated as many weevils as unbaited sandwich populations using mark and recapture meth- traps. Through interference studies, they ods. However, weevil population declines estimated the effective radius of trap of the same magnitude as that reported in attractivity at 2.5–7.5 m. They then tested Koppenhofer et al.’s (1994) third trial have Cosmolure+ in three plantain fields and in one been found for field populations of marked Grand Enano (AAA) stand using Chemtica and released weevils in trials where trapping recommendations on trap placement. In the was not conducted (Rukazambuga, 1996; plantain systems, weevil capture rates in Gold and Night, unpublished). treated plots remained at initial levels for Controlled studies to determine the 9 months and steadily decreased thereafter, efficacy of pseudostem trapping in reducing while trap captures remained steady in con- weevil populations were conducted under trol plots. Over 18 months, damage levels, farmer conditions in Ntungamo district, measured by Vilardebo’s (1973) coefficient of Uganda. Twenty-seven farms were then infestation, decreased from 15% to 12% in the stratified on the basis of weevil population treated plots, while increasing from 15% to density and divided among three treatments: 34% in controls. This resulted in a 25% yield (i) researcher-managed trapping (one trap/ gain for the first 18 months. Similar results mat/month); (ii) farmer-managed trapping were found in the Grand Enano field, where (trap intensity at discretion of farmer); and treated plots had less damage and a 32% yield (iii) controls (no trapping). After one year, advantage. weevil populations had declined by 61% in researcher-managed fields, by 43% where Biological control with arthropods farmers managed trapping and by 23% in controls (Gold et al., 2002). Effects were highly Biological control efforts against banana variable among farms within treatments and weevil have included the use of exotic natural

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24 C.S. Gold et al.

enemies (classical biological control), endemic of even partial control (Waterhouse and natural enemies, secondary host associations Norris, 1987). Although these results are and microbial control (e.g. entomopathogens, discouraging, Neuenschwander (1988) rec- endophytes, entomophagous nematodes). ommended additional searches that might Microbial control agents may require repeated focus on parasitoids (especially of the applications as biopesticides, although they relatively vulnerable egg stage). Such natural lack the toxic side effects of chemical insec- enemies tend to more host specific and ticides. As such, they may entail periodic more effective biological control agents than application costs on the part of the farmer. opportunistic predators such as P. javanus. An intensive search for natural enemies CLASSICAL BIOLOGICAL CONTROL Classical of banana weevil carried out in 2001 in biological control of banana weevil may be Sumatra, Indonesia failed to reveal the possible. Introduced pests, unimportant in presence of either egg or larval parasitoids their native habitats, often reach damaging (A. Aberu, personal communication). levels when released from the control of coevolved natural enemies. The banana ENDEMIC NATURAL ENEMIES Endemic natural weevil appears to fit this pattern. Therefore, enemies reported in Latin America, Africa exploration for banana weevil natural ene- and Asia (reviewed by Beccari, 1967; Schmitt, mies in Asia followed by selection, quarantine 1993; Koppenhofer, 1993b,c; Seshu Reddy and release of suitable species could establish et al., 1998) include nabids, cydnids, capsids, an herbivore equilibrium below economic reduviids, mirids, thrips, rhagionids, sarco- thresholds. phagids, histerids, carabids, hydrophilids, The first searches for natural enemies staphylinids, dermaptera, curculionids, in Asia were undertaken by Muir in 1908 scarabaeids, tenebrionids, and formicids. (Froggatt, 1925), Jepson (1914) and Froggatt Very little information is available on the (1928). They identified a histerid Plaesius efficacy of these natural enemies and most javanus Erichson, the staphylinids Belonuchius appear to be of limited importance. ferrugatus Erichson and Leptochirus unicolor Koppenhofer et al. (1992) listed 12 preda- Lepeletier, a cucujid Canthartus sp. and a tors of banana weevil in western Kenya. These leptid (rhagionid) fly Chrysophila ferruginosa included three staphylinids, three histerids, (Wied) as being predacious on the banana one hydrophilid, one carabid, one tene- weevil and banana stem weevil (Odoiporus brionid, two labiids, and one carcinophorid longicollis Oliv.). Later searches revealed the earwig. In laboratory studies, these predators presence of other histerids (e.g. Hololepta spp.) variously searched rhizomes of living plants and a hydrophilid (Dactylosternum hydrophil- and pseudostem and rhizome residues. oides MacLeay). All of these are opportunistic Eleven predators attacked the banana weevil predators that feed on a range of prey. The egg stage, ten attacked the first two larval most important appeared to be P. javanus instars, nine attacked the third and fourth whose larvae and adults both attack banana instar, while four attacked later stages. Using weevil immatures. This predator is most high predator densities under experimental commonly found in deteriorating banana conditions, two of these predators reduced residues and rarely enters weevil galleries in weevils by up to 50% in suckers, 39% in living plants. stumps and 40–90% in residue pseudostems, Between 1913 and 1959, 45 attempts were T. interocularis reduced weevil densities in made to introduce eight natural enemies from spent pseudostems by 42%, while the other Asia to other banana growing regions in the predators were unimportant (Koppenhofer world. These introductions tended to be done and Schmutterer, 1993; Koppenhofer, 1995). with small predator consignments. In most However, the number of natural enemies cases, the natural enemies either failed to used in these experiments far exceeded field establish following introduction or were inef- densities, suggesting that the impact of these fective (Waterhouse and Norris, 1987). Only in predators in banana stands is likely to be Fiji and Jamaica has there been any suggestion limited (Koppenhofer and Schmutterer, 1993).

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Pests of Banana 25

Hargreaves (1940) was the first to suggest One concern, however, is that these ants may that ants might have potential as biological also protect homopteran pests of other crops control agents of banana weevil in Africa, (A.M. Varela, personal communication). although no studies were ever conducted. During the 1970s, Cuban researchers began SECONDARY HOST ASSOCIATION Neuensch- a biological control programme using the wander (1988) suggested that natural enemies myrmicine ant Pheidole megacephala (Fabricius) of closely related hosts offer the promise for against sweet potato weevils (Perfecto, 1994). efficient secondary associations with banana Roche (1975) suggested that Tetramorium weevil. Traore (1995) investigated the possible guineense (Mayr) might be capable of sup- use of the mymarid egg parasitoid Anaphes pressing banana weevil populations. Both victus Huber against banana weevil in Benin. P. megacephala and T. guineense will enter A. victus is an important parasitoid of weevil crop residues and remove eggs and larvae eggs in the Americas. This parasitoid was (S. Rodriguez, personal communication). selected for study because it searches near T. guineense was also observed to nest in the soil level, is habitat-rather than species- leaves and crop residues. specific and because it effectively suppresses Roche and Abreu (1982, 1983) began the populations of carrot weevil (Listronotus propagation and dissemination of T. guineense oregonensis (LeConte)) (Boivin, 1993). colonies. Colonies with up to 22 queens and In the laboratory, A. victus readily accep- 62,000 workers and immatures were collected ted banana weevil eggs, but parasitoid and liberated in new fields (Perfecto and emergence was negligible (0–2%) (Traore, Castineiras, 1998). Ant establishment was 1995). In contrast, A. victus immatures success- followed by the rapid appearance of new fully emerged from water hyacinth weevil, colonies. At the onset of one trial, weevil Neochetina eichorniae Warner, demonstrating trap catches were greater than ten per mat. that the parasitoid could successfully com- Liberation of ants on 8% and 50% of the mats plete its development within a new host. provided total field coverage in 6 and 2 Traore (1995) attributed failure to emerge months, respectively (Roche and Abreu, from banana weevil eggs to its larger size and 1983). Eighteen months later, weevil trap the fact that the larvae of A. victus failed to catches were 56–65% lower. Based on consume all of the banana weevil egg con- these results, Roche and Abreu (1983) recom- tents, with decomposition of uneaten material mended releasing ants on 25–30% of the area contributing to pupal failure. for ‘complete control’ in 3–4 months. The potential of myrmicine ants to Microbial control control banana weevil has also been demonstrated by Castineiras and Ponce (1991). They Microbial agents tested against the banana released 9 and 15 P. megacephala colonies ha−1 weevil include entomopathogenic fungi (e.g. into plantain plots (separated by 200 m alleys) Beauveria bassiana and Metarhizium anisopliae) 6 months after planting. During the first (Plate 4), entomopathogenic nematodes (e.g. crop cycle, weevil trap captures and damage Steinernema spp. and Heterorhabditis spp.) indices were similar in plots where ants had (Plate 5) and endophytes (e.g. non-pathogenic been released, in carbofuran-treated plots and Fusarium spp.). Entomopathogenic fungi and controls. In the second cycle, ants reduced nematodes are mostly used to kill adult wee- weevil trap captures by 54–69% and damage vils, while endophytes target the immature by 64–66%, with a corresponding yield stages. Although a number of strains have increase of 15–22%. The level of control shown promise in the laboratory and in pre- provided by ants was similar to that of the liminary field studies, efficient and economi- pesticide. cally viable delivery systems still need to be Myrmicine ants in the genera Tetramor- developed. Only in a few sites have entomo- ium and Pheidole are widespread (e.g. Walker pathogens been reported to establish follow- and Dietz, 1979; Varela, 1993). Their control ing applications in banana fields. Without potential in other banana systems is unknown. adequate establishment, entomopathogens

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26 C.S. Gold et al.

will require repeated applications as a effects), while weevil mortality was negligible biopesticide. This will entail continued pro- in solutions with 10% oil. Using a 15% oil solu- duction, distribution, and storage costs that tion, he found mortality to range from 10% at will be passed on to the farmer. 1 × 107 spores ml−1 to 97% at 5 × 108 ml−1. Nankinga (1994) allowed weevils to ENTOMOPATHOGENIC FUNGI Entomopatho- walk on PDA cultures and found five isolates genic fungi have been tested against banana of B. bassiana produced > 96% mortality after weevil since the 1970s (Ayala and Monzon, 21 days. Topical applications of the same iso- 1977; Delattre and Jean-Bart, 1978). Numerous lates in water suspensions produced 73–100% strains have been screened against adult mortality. Nankinga (1994) also found mortal- banana weevils in Africa and the Americas, ity rates to be directly related to spore dose for employing diverse formulations, spore three strains of B. bassiana. Higher doses killed concentrations and application methods almost all weevils, while females were more (reviewed in part by Nankinga, 1999; susceptible than males to lower doses of the Nankinga et al., 1999). These strains, isolated pathogen. Topical applications by dispersion from a wide range of insects, as well as from or immersion caused much higher rates of Galleria baits, were predominantly B. bassiana mortality than spraying pathogen solutions and, secondarily, M. anisopliae. Additional on to soil or pseudostem traps. research has been conducted on mass pro- Although it is difficult to compare the duction on a range of substrates (e.g. maize, results of different studies because of the wide rice), spore viability and storage, formulations range of methods used, it is clear that the most (powders, water solutions, mineral oils), effective strains were capable of causing high doses, application methods and mortality mortality in the laboratory at lower spore rates after varying time intervals. In spite of concentrations and in shorter periods of time. the variability in methods, laboratory studies In general, promising isolates of B. bassiana conducted in many different banana-growing were more effective than those of M. anisopliae regions have consistently demonstrated high (Delattre and Jean-Bart, 1978; Batista Filho levels of weevil mortality (often exceeding et al., 1987; Mesquita, 1988; Busoli et al., 1989; 95%) to a large number of strains. Kaaya et al., 1993; Nankinga, 1994). Mineral For example, Brenes and Carballo (1994) oils used in formulations often affected screened 24 isolates of B. bassiana (from Hemi- mortality of weevils independent of entomo- ptera, Lepidoptera, ants and other weevils) pathogens, but tended to be more expensive by shaking the insects in conidial powder. The than other substrates. six most promising isolates were selected for Under field conditions, naturally occur- further testing. Mortality of weevils dipped in ring infection rates (determined for trapped water suspensions containing 1 × 109 spores weevils) tended to be between 0 and 6% −1 ml ranged from 73 to 100% with a LT50 (Mesquita et al., 1981; de Souza et al., 1981; Van of 7–10 days. Using a range of spore concen- den Enden and Garcia, 1984; Gomes, 1985; × 9 −1 trations, an LT90 of 2.67 10 spores ml was Peña et al., 1993; C.M. Nankinga, unpublished; calculated for the most promising isolate. C.S. Gold, personal observation). This sug- Carballo and de Lopez (1994) then found gests that entomopathogens may have to be 31–63% adult mortality when B. bassiana periodically applied as biopesticides. How- conidial powder or spores on rice substrate ever, few studies have addressed delivery were applied to pseudostem traps. systems and efficacy under field conditions. Contreras (1996) screened five strains Delattre and Jean-Bart (1978) were of B. bassiana in the laboratory in oil-based unsuccessful in reducing weevils by spraying formulations and found 65–95% weevil B. bassiana spores on to the base of mats, while mortality in 15 days, with an LT50 of 2.5–8 Mesquita (1988) obtained 5% infection after days. Carballo (1998) tested water-based and immersing pseudostem traps in B. bassiana oil-based formulations of B. bassiana. Formula- spore solutions. Following applications of tions with > 20% oil caused high levels of B. bassiana spores to pseudostem traps in mortality in the weevil (independent of fungal rice paste and oil-based formulations, Batista

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Pests of Banana 27

Filho et al. (1991, 1995, 1996) found 61% and and Schoeman, 1999), but it is unclear how 20% fewer weevils, respectively, in treated important this is under field conditions, traps. Contreras (1996) suggested applications where weevil density is relatively low. might be better placed on disc-on-stump traps that, in his studies, captured 3–4 times as ENDOPHYTES A wide variety of endophytic many weevils as pseudostem traps. He found fungi have been isolated from nearly all exam- higher infection rates in oil formulations than ined plants (ranging from grasses to trees) and in rice-based substrates of B. bassiana immedi- plant tissues (Carroll, 1991). Many of these ately after application, but the reverse was have developed mutualistic relationships true 8 days after application. Nankinga (1999) with plants and some act as antagonists to found 50–60% infection rates for weevils pests and diseases. Endophytes can enhance collected in disc-on-stump and pseudostem resistance to specialist herbivores that have traps treated with B. bassiana spores in maize evolved mechanisms to circumvent the culture, 55–61% for traps treated with spores plant’s normal defences (Carroll, 1991; in oil suspension, 23–44% for traps treated Breen, 1994). with spores in water suspension and 0% in oil The use of endophytes in banana to give and water controls. Pathogenicity decreased extended protection to tissue culture planting in treated soils after 2 weeks, although 15% of material is currently under study. Griesbach weevils collected from treated soils showed (2000) obtained 200 isolates of endophytic signs of infection 5 months after treatment. fungi from 64 recently harvested highland Nankinga (1999) also monitored weevil trap bananas (AAA-EA) and Pisang awak (ABB). catches for 8 months in a trial with two Spore suspensions of 12 isolates (eight B. bassiana applications. Mean weevil counts Fusarium spp., three Acremonium spp., one were lowest in plots treated with maize Geotrichium sp.) caused 80–100% mortality formulation (40) followed by plots receiving in weevil eggs, while 74 additional isolates soil formulation (54), oil formulation (68) and caused 60–79% mortality. Screening of the controls (81). The incidence of field mortality 12 most promising isolates against banana of weevils observed in traps was low, with a weevil larvae gave 0–48% mortality, with the maximum of 5% and often under 1%. Maize- best two strains being F.cfconcentricum (48%) based formulations also tended to reduce and F. oxysporum (32%). Griesbach (2000) was weevil damage levels in the central cylinder also able to successfully inoculate tissue cul- and cortex. These reductions in weevil dam- ture plants with endophytes. Preliminary pot age suggest that infected weevils may not trials on the effects of inoculated endophytes have been attracted to pseudostem traps and on weevil damage in tissue culture plants that actual mortality was higher. produced some positive but largely inconsis- Disc-on-stump and pseudostem traps tent results. Current research efforts concern may aggregate weevils at delivery sites pathogenicity testing of candidate isolates, for entomopathogens (Kaaya et al., 1993; distribution and persistence within the host Contreras, 1996; Nankinga, 1999). Budenberg plant and efficacy in reducing weevils in et al. (1993a) further suggested that semio- potted plants. chemicals might increase weevil attractivity of entomopathogen-baited traps. Currently, ENTOMOPATHOGENIC NEMATODES The use of pheromones are exploited in pitfall traps. This entomopathogenic nematodes (EPNs) for would require a modification of the current insect control and their potential use against pitfall trap design for use of pheromone banana weevil has been reviewed by such that the weevils become infected rather Treverrow et al. (1991), Parnitzki (1992) and than drown. Such a method would only be Schmitt (1993). The most commonly used advantageous over standard pitfall trapping species are within the genera Steinernema if infected adults were able to transmit the and Heterorhabditis. These have received wide pathogen to other weevils. Preliminary labo- attention as biological control agents because ratory experiments suggest that such transmis- of their wide host range and ability to kill sion does occur (Nankinga, 1994; Schoeman the host rapidly with no adverse effects on

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the environment (Schmitt, 1993). Five species Host plant resistance of Xenorhabdus bacteria are mutualistically associated with EPNs. Infective juvenile The literature on susceptibility of Musa clones nematodes enter through the host’s natural to banana weevil attack is largely frag- orifices (Steinernema) or interskeletal mem- mentary, with highly variable and often con- brane (Heterorhabditis) (Treverrow et al., 1991). tradictory findings (Pavis and Lemaire, 1997; After entering the host, the nematodes Kiggundu et al., 1999). Most often, reported penetrate mechanically into the haemocoel results reflect comparisons among a small and release Xenorhabdus which causes septi- number of clones used in field trials. Fogain caemia and insect death within 1–2 days and Price (1994), Ortiz et al. (1995), Anitha (Schmitt, 1993). et al. (1996) and Kiggundu (2000) conducted EPNs may be more effective against screening trials to identify existing clones banana weevil larvae than against weevil displaying resistance to banana weevil. adults (Figueroa, 1990; Peña and Duncan, The variability in findings may reflect, 1991). However, the cryptic habitat of weevil in part, differences in sampling methods in larvae within living plants makes delivery assessing weevil damage. For example, in a difficult (Treverrow and Bedding, 1993; screening trial, Kiggundu (2000) found that Treverrow, 1994). In addition, it is difficult to Nsowe (AAA-EA) scored highest among know which plants are infected with larvae. highland banana clones in damage to the Therefore, applications cannot be restricted to rhizome surface but among the lowest in those plants with high weevil numbers. internal rhizome damage. Pavis and Lemaire Treverrow et al. (1992) and Treverrow (1997) and Mestre (1997) noted the need for and Bedding (1993) developed a delivery standard screening methods and reference system for EPNs, capitalizing on the weevil’s cultivars. Kiggundu (2000) recommended attraction to cut rhizomes and damaged the use of total cross-section damage (cf. Gold plants. Two conical shaped cuts were made in et al., 1994a) as this measure has a high level residual rhizomes. These cuts attracted adult of heritability and is well correlated with weevils and provided thigmotactic stimuli other indices of weevil damage. In contrast, that encouraged them to remain at the Rukazambuga et al. (1998) suggested the use infection sites. The holes also buffered the of damage to the central cylinder, as this delivery site against temperature extremes damage appeared to have the greatest impact and provided excellent conditions (high on plant growth and yield. humidity, moderate temperatures, protection against ultraviolet light) for nematode per- RESISTANCE ACROSS GENOME GROUPS Edible sistence. The nematodes were released at a bananas (Musa spp., Eumusa series) origi- density of 250,000 per hole in a formulation nated within South-East Asia from two wild including a polyacrylic gel (to reduce water diploid progenitors, Musa acuminata and build-up and incidence of nematode drown- M. balbisiana, producing a series of partheno- ing) with an adjuvant of 1% paraffin oil (to carpic diploids and triploids through natural encourage the weevils to raise their elytra, hybridization. Both M. acuminata and M. exposing the first spiracle for nematode balbisiana escaped attack in a screening trial in entry). The nematodes persisted for up to Cameroon (Fogain and Price, 1994). 50 days and attacked both adults and larvae Plantains (AAB) appear to be more (Treverrow et al., 1991; Treverrow, 1994). At susceptible to banana weevil attack than moderate weevil infestation levels, nematode other clonal groups (Ghesquiere, 1925; Fogain baits performed as well as or better than and Price, 1994; Gold et al., 1994a; Price, 1994; insecticides (Treverrow, 1993; Treverrow and Kiggundu, 2000). Highland cooking bananas Bedding, 1993), but were not as effective (AAA-EA) also appear susceptible to banana as pesticides in heavily infested fields weevil (Sikora et al., 1989; Gold et al., 1994a; (Treverrow, 1994). However, controls based Kiggundu, 2000). Reports on susceptibility on EPNs were not economically competitive of AAA dessert bananas (e.g. Gros Michel, with pesticides (Treverrow, 1993, 1994). Cavendish, Williams, Valery) have ranged

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Pests of Banana 29

from resistant to susceptible (e.g. Mesquita fitness). Host plant resistance may be et al., 1984; Fogain and Price, 1994; Gold et al., attributed to antixenosis (non-preference), 1994a; Stanton, 1994; Sponagel et al., 1995; antibiosis and/or host plant tolerance Kiggundu, 2000). Sponagel et al. (1995) sug- (Painter, 1951). For banana weevil, available gest that weevils favour crop residues of AAA data suggest that antibiosis is the most impor- dessert bananas over developing plants and tant factor conferring host plant resistance, are thus unimportant. AB and ABB bananas while antixenosis is of little importance. Little are often considered among the most resistant has been reported on host plant tolerance to Musa clones to banana weevil (Mesquita et al., banana weevil damage, as such work would 1984; Seshu Reddy and Lubega, 1993; Gold require yield loss studies over several crop et al., 1994a; Ortiz et al., 1995; Abera et al., 1999; cycles. Kiggundu, 2000). In germplasm collections in Cameroon and Nigeria, ensete appeared Antixenosis. Antixenosis suggests that to be highly susceptible to banana weevil resistant clones avoid pest attack by reducing (Pavis and Lemaire, 1997; C.S. Gold, personal rates of host plant location (i.e. attraction) observation). However, in Ethiopia, where and/or host plant acceptance; the combined the crop is most widely grown, ensete largely effects of these two processes would be escapes attack because most production is reduced oviposition. Pavis and Lemaire above the weevil’s upper elevational thresh- (1997) suggested that antixenotic factors old (M. Bogale et al., unpublished). might also deter adult feeding. The data on the relative attraction of CLONAL RESISTANCE In screening trials in banana weevils to susceptible and resistant Cameroon (Fogain and Price, 1994) and clones is equivocal. Budenberg et al. (1993b) Nigeria (Ortiz et al., 1995), all plantain clones and Pavis and Minost (1993) reported appeared susceptible to banana weevil. In that females were equally attracted to cut contrast, Chavarria-Carvajal (1998) evaluated rhizomes and volatiles from resistant and eight plantain clones and found the common susceptible cultivars. In contrast, Minost dwarf plantain and a Lacknau clone to have (1992) found that Burmanica (AA) was most less than 20% of the damage occurring in attractive to adult weevils, followed by Pisang Sin Florescencia and Rhino Horn plantains. awak (ABB), Borneo (AA) and French Clair Irizarry et al. (1988) and Fogain and Price (AAB), while Petit Naine (AAA) and Rose (1994) also found Lacknau clones less suscep- (AA) were much less attractive. However, tible than other plantains. clonal attraction was not related to subsequent As part of a larger screening trial, Kig- weevil damage. Similarly, Musabyimana gundu (2000) evaluated 26 highland bananas (1995), Abera (1997) and Kiggundu (2000) for susceptibility to banana weevil. Cluster found some differences among trap captures analysis suggested that 7 clones were highly at the base of different clones, but these differ- susceptible to weevil attack (mean damage ences were not related to damage at harvest. 9%), 13 clones were intermediate in suscepti- These studies suggest that resistance mecha- bility (6%) and 6 clones were resistant (4%). nisms must be related to oviposition and/or Among the more resistant cooking clones larval development rather than to host plant were Mbwazirume and Nakyetengu, which attraction. are both widely grown. One brewing clone Little work has been done on host plant was considered susceptible, three were inter- acceptance. Abera (1997) found field ovi- mediate in susceptibility and two appeared position on Kayinju (ABB) to be similar to relatively resistant. that on highland banana clones, even though the latter displayed much higher levels of MECHANISMS CONFERRING RESISTANCE Success- weevil damage. Kiggundu (2000) looked at ful attack of bananas by banana weevils oviposition on resistant and susceptible clones involves host plant location, host plant accep- in both choice and no-choice experiments. tance (oviposition) and host plant suitability There was very little mean separation and the (larval survival, developmental rate and lower levels of oviposition occurred on clones

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(Atwalira, Nakyetengu, Muvubu) that were high mortality rates. Rhizome extracts from not considered resistant. Kayinju applied to susceptible rhizome The banana weevil is a relatively seden- material inhibited larval feeding, while tary insect living in perennial systems with an extracts from susceptible clones did not. abundance of host plants. Kiggundu (2000) Pavis and Minost (1993) found a negative argued that it is unlikely that banana weevils correlation (r = −0.47) between rhizome hard- might walk far looking for a suitable host. ness and infestation rate and hypothesized Most likely, tenure time at the base of any mechanical resistance to oviposition or larval given mat and oviposition may be more development. However, Ortiz et al. (1995) related to environmental factors such as found no relationship between rhizome hard- soil moisture. Available data indicate that the ness and weevil damage scores in segregating weevil will freely oviposit on both susceptible progenies, suggesting that other resistance and resistant clones, suggesting that antibiosis mechanisms may be more important. plays the most important role in host plant resistance (Abera, 1997; Kiggundu, 2000). Tolerance. Tolerance suggests that the host plant can sustain high levels of insect Antibiosis. Antibiotic factors are those damage without yield reduction. Cuille and which negatively influence larval perfor- Vilardebo (1963) argued that Gros Michel mance (i.e. poorer survivorship, slower devel- (AAA) was resistant because the large size opment rates, reduced fitness). These factors of the rhizome conferred tolerance to weevil may range from physical (e.g. sticky sap and attack. Kiggundu (2000) also found that latex, rhizome hardness) to nutritional quality rhizome size can reduce the proportion of and deficiencies to toxic secondary plant damaged tissue. Pavis (1993) suggested that substances. the vigorous growth of Pisang awak allowed In a mixed cultivar trial, Abera (1997) it to tolerate moderate levels of attack. How- found weevil damage to the interior of the ever, no studies have compared damage rhizome to be 5–25 times higher in five thresholds and related yield losses for highland banana clones than in Kayinju. different Musa clones. Banana weevil attraction and oviposition on Pisang awak was similar to that on the BREEDING FOR RESISTANCE To date, there highland bananas, while larval survivorship have been no attempts to breed bananas or was estimated as 10–23 times higher in plantains for resistance to banana weevil. highland bananas than in Kayinju. From these Breeding for resistance depends upon sound data, Abera (1997) concluded that antibiosis knowledge of resistance mechanisms, resis- explained why Kayinju was resistant to tance markers and the genetics of resistance banana weevil. Mesquita and Alves (1983), (Kiggundu et al., 1999). As a foundation, it Mesquita et al. (1984) and Mesquita and is important to determine whether there are Caldas (1986) found that banana weevil useful sources of resistance within the avail- immatures developed faster and had fewer able germplasm. Kiggundu (2000) observed ecdyses on some clones than on others. that the wild diploid Calcutta-4 and the clones Lemaire (1996) reported slower larval devel- Yangambi-Km5 and FHIA-03 showed high opment and higher larval mortality on the levels of resistance and might be exploited resistant clone Yangambi-Km5. Kiggundu in breeding programmes. Lemaire (1996) (2000) found that two resistant clones, and Mestre and Rhino (1997) also found FHIA-03 and Kayinju, increased larval Yangambi-Km5 to be highly resistant to developmental time. Larval mortality ranged banana weevil. Calcutta-4 has already been from 5 to 100%, with highest levels occurring successfully used in conventional breeding in resistant clones such as Kayinju (100%) programmes in Nigeria and Uganda, while and Kabula (AAA-EA) (90%). Larvae reared the male/female fertility of Yangambi-Km5 on Mbwazirume (AAA-EA), FHIA-03, Ndiizi and FHIA-03 still needs to be determined (AB), and Yangambi-Km5 (AAA) also had (Kiggundu, 2000).

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Pesticides outbreaks of banana weevil in the mid-1980s were attributed to pest resurgence following Chemical pesticides for control of banana development of resistance to dieldrin (Sen- weevil may be applied to protect planting gooba, 1986; Sebasigari and Stover, 1988; Gold material (through dipping of suckers or et al., 1999a) leading to loss of confidence in applications in planting holes), periodically chemical control by some farmers. applied at the base of the mat after crop establishment, and/or applied to pseudostem Botanicals traps to increase trap catches. Since the first recommendation in 1907 for the use of chemi- In Kenya, Musabyimana (1999) conducted cals (i.e. Bordeau mixture) to control banana a detailed study on the effects of neem weevil (Gravier, 1907), there have been (Azadirachta indica) seed derivatives on numerous studies on the relative efficacy of banana weevil adult activity, success of different insecticides under different formu- immatures and resulting damage. This lations and application rates, persistence and research, including both laboratory and the appearance of insecticide resistance in field trials, employed different formulations banana weevils. Chemicals remain an impor- of neem seed powder (NSP), neem kernel tant part of banana weevil control although powder (NKP), neem cake (NC) and neem oil costs often make them prohibitive for subsis- (NO). The azadirachtin content was deter- tence farmers. mined as 4000 p.p.m. for NSP, 5500 p.p.m. In 1951, the use of chemicals gained fur- for NKP, 5800 p.p.m. for NC and 850 p.p.m. ther importance with the advent of synthetic for NO. Musabyimana’s (1999) results insecticides that largely replaced labour- suggest that neem derivatives can reduce demanding cultural controls such as trapping weevil damage by interfering with each stage or sanitation. As with many other pests, the of attack: (i) fewer adults will locate or remain introduction of chemicals in the 1950s for the at the host plant; (ii) females locating the control of banana weevil was greeted with host plant will have reduced oviposition; optimism. Braithwaite (1958) suggested that (iii) eclosion rates will be lower; (iv) an eradication of the banana weevil might be antifeedant effect will delay and reduce larval achieved with aldrin and dieldrin. feeding; and (v) larval fitness (developmental A wide range of chemicals, encompass- rates, size, survivorship) will be reduced. ing all major classes of insecticides, have been Direct application of NC and NSP to the tested and recommended as effective for the soil was much more cost effective than appli- control of banana weevil (reviewed, in part, by cations of aqueous solutions. Overall, NSP Sponagel et al., 1995 and Seshu Reddy et al., appeared to be the preferred derivative as it 1998). Many once recommended chemicals was easier to produce and had better effects. have been banned or otherwise fallen out of From these results, Musabyimana (1999) favour because of their high levels of mamma- recommended application rates of 60–100 kg lian toxicity, environmental concerns and/or ha−1 once every 4 months. the development of resistance. Nevertheless, In laboratory studies in Cameroon, insecticides can often achieve high levels of Messiaen (2000) had results consistent with control in short periods of time. those of Musabyimana (1999): neem had Insecticide resistance in banana weevil a repellent effect on adults and reduced has been documented in Australia, Latin oviposition levels and eclosion rates. How- America and Africa (reviewed by Gold et al., ever, in field studies, Messiaen et al. (2000) 1999a) for a range of chemicals including found limited advantage in weevil control cyclodienes (aldrin, BHC, heptachlor, diel- from applications of neem dips (i.e. aqueous drin), organophosphates (chlorpyrifos, etho- solution of concentrated NSP) and no benefits prophos, pirimiphos-ethyl and prothiophos), from granular applications of NSP (30–100 g and carbamates (carbofuran). Cross-resistance per plant). In two trials, neem treatments has also been demonstrated (Edge, 1974; did not influence weevil adult populations, Collins et al., 1991). In Uganda and Tanzania, although damage was reduced in one

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32 C.S. Gold et al.

experiment. However, neem dips reduced and stem of banana plants, although they sucker mortality by 73–85% and total plant will occasionally feed within the rhizome. mortality by 50%. This contrasts with the banana weevil, which From his results in Kenya, Musabyimana attacks the rhizome and will rarely enter (1999) concluded that NSP and NC soil the pseudostem. As such, pseudostem borer applications are effective enough to do away damage may be clearly visible, while banana with paring and hot water treatment of suck- weevil damage can only be observed by ers to be used as planting material. His data dissection of the rhizome. The pseudostem suggest that extended protection under field borer will attack both living plants and conditions is possible. However, the largely harvested stumps (Pinto, 1928). In some sites, negative results obtained by Messaien et al. the weevil may show a preference for crop (2000) in Cameroon were inconsistent with residues (B. Pinese, personal observation). those of Musabyimana (1999) and show that it The colour of the adult weevil varies with would be useful to conduct further studies age from reddish brown to black (Dutt and at additional sites. Also, the availability of Maiti, 1972). The weevil is characterized by neem products, their economic viability and long life span, negative phototropism, thig- their acceptance by farmers need to be motropism, gregariousness, hydrotropism, determined. and death mimicry (Kung, 1955). Most adults live 6–10 months, although some can survive for more than 2 years (Pinto, 1928). In contrast Banana pseudostem borer, Odoipurus to the banana weevil, the adult readily flies, longicollis (Olivier) although it has been described as a ‘poor’ flyer (Dutt and Maiti, 1972). In spite of being The banana pseudostem borer or pseudostem negatively phototropic, diurnal flight may weevil is considered a minor to important occur (C.S. Gold, personal observation). pest of banana and Manila hemp in parts Oviposition is in the leaf sheaths of living of India, Nepal, Burma, Sri Lanka, Thailand, plants or residues (Pinto, 1928). The weevils Indonesia, China and elsewhere in Asia are especially attracted to and readily oviposit (Froggatt, 1928; Pinto, 1928; Kung, 1955; in cuts in banana material (Kung, 1955). Kung Dutt and Maiti, 1972; Waterhouse, 1993). (1955) suggested that ovipositing females The weevil bears a superficial resemblance prefer stressed plants, while Pinto (1928) to the banana weevil, Cosmopolites sordidus observed greater oviposition in residues than (Germar), but is slightly larger and its elytra in living plants. Dutt and Maiti (1972) found do not completely cover the abdomen (Pinto, greatest oviposition in pseudostems with a 1928; Dutt and Maiti, 1972). The morphology girth of 25–50 cm, with little oviposition in of the adult and the immature stages have plants < 25 cm or > 75 cm in girth. The eggs been described by Dutt and Maiti (1972). are placed singly in chambers made with Sexing of adults is based on punctuation of the female’s rostrum. Pinto (1928) found ovi- −1 the rostrum. Males also tend to be smaller position rates of 1–6 eggs day and observed than females. Observations on sex ratio range two weevils to produce 103 and 185 eggs, from 1 : 1.45 (male : female) (Kung, 1955) to respectively, in 4.5 months. The egg stage has 1 : 1.17 (Dutt and Maiti, 1972). been reported as 3–4 days (Pinto, 1928) and 5–12 days (Kung, 1955). Life history, habits, pest status The larvae pass through four (Kung, 1955) or five (Dutt and Maiti, 1972) instars. The The life cycle of the banana pseudostem borer first instar remains in the same leaf sheath has been described by Pinto (1928), Kung where the egg was placed. Subsequent instars (1955) and Dutt and Maiti (1972). The adult bore into the inner leaf sheaths or pseudostem weevils feed on living and decomposing (Dutt and Maiti, 1972). The mature larvae may banana leaf tissues, but eat little and are not be twice the size of those of banana weevil considered pests. Damage is done by the lar- (Pinto, 1928). The larval stage has been val stage. The larvae attack the pseudostem reported as 14 days (Pinto, 1928), 3–6 weeks

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Pests of Banana 33

(Kung, 1955) and 26–68 days (Dutt and Maiti, germplasm and found six varieties to be 1972). severely infested, three heavily infested, four The prepupa forms a pupal chamber moderately infested and 27 lightly infested. within the host plant. Pupation is within a cocoon formed out of plant fibres. The prepupal stage lasts 3–9 days, while the pupal period has been reported as 3–20 days (Pinto, West Indian sugarcane borer, (Olivier) 1928; Kung, 1955; Dutt and Maiti, 1972). Metamasius hemipterus sericeus Following emergence, the adults may pass extended periods and even mate within the The West Indian sugarcane borer, Metamasius host plant. Normally, there is a preoviposition hemipterus sericeus (Olivier), also known as period of 1 month (Pinto, 1928; Dutt and Maiti, ‘the rotten stalk borer of sugarcane’ in Puerto 1972). Rico and ‘picudo rayado’ in South America, Tunnelling by the weevil larvae can is an important pest of palms, sugarcane, lead to the rotting of pseudostem tissues and pineapple, and bananas in the West breakage in the wind (Dutt and Maiti, 1972). Indies, Mexico, Central South America and Although the weevil has been described as Florida, USA (Vaurie, 1966; Woodruff and an important pest, there has been no quantifi- Baranowski, 1985; Giblin-Davis et al., 1994). cation of plant loss and/or yield reductions. Further work in this area seems a prerequisite Life history and habits for the development of any integrated pest management programme. The adult stage of M. hemipterus sericeus is free-living within banana pseudostems, palm Control measures fronds and sugarcane sheaths. This weevil is distinguished from other species by the Little information is available on the control colour (red to yellow and black) and size of banana pseudostem weevil. Pinto (1928) (9–14 mm), but can be confused with recommended selecting new and clean sites Metamasius callizona, which infests bromeli- (Pinto, 1928), the use of clean planting mate- ads. Sometimes the colour pattern of M. rial, crop sanitation (e.g. burying infested hemipterus sericeus is variable, causing some residues), rogueing of infested plants, crop confusion. The colours of the elytra are rotation (to rid fields of weevils), and trap- one-half to one-third red and the remainder ping by placement of residue slices on the mostly black; the pronotum and venter are ground. Zhou and Wu (1986) and Mathew black to red and black. Adult females of et al. (1997) suggested removing dead leaves M. h. sericeus lay eggs in cracks or damaged to eliminate hiding places for the adults. areas of the host plant or in petioles or crown Whereas the weevil flies and its dispersal shafts of certain species of healthy palms. The capacity has not been determined, it is adult can live up to 60 days. The female can unclear how effective the use of these cultural deposit approximately 500 eggs (Castrillon methods might be. Kung (1955) collected and Herrera, 1980). The egg is 1.5 mm in more than 2 million weevils in traps over a length, oval, and hatches between 3 and 4-month period, but did not provide informa- 7 days after oviposition. tion on the effect of this trapping programme The yellowish larvae are typical legless on weevil populations. weevil grubs and similar in most aspects to Chemical control and host plant resis- other members of the Rhynchophorinae. The tance have also been suggested. Mathew average size of the larvae is 1.3 to 1.9 cm. The et al. (1996, 1997) found swabbing of the larvae bore and feed in the host tissue, causing pseudostem and borer holes to be effective in extensive physical damage which can lead reducing weevil infestations. In India, Ishaque to the death of the host (Giblin-Davis et al., (1978) found one variety to be completely 1994). The larval stage lasts between 50 and 60 free of the weevil, while two others appeared days. Then a fibrous pupal case is constructed resistant; Charles et al. (1996) screened banana (similar to that of the giant palm weevil,

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34 C.S. Gold et al.

Rhynchophorus palmarum (L.)). The pupal stage disc traps. Giblin-Davis et al. (1994) tested dif- is spent in this cocoon for about 10–20 days. ferent trap designs and the response of adults to semiochemicals and concluded that weevil Damage counts increased with combinations of ethyl acetate, sugarcane and/or the aggregation Generally, the West Indian cane weevil is pheromone metalure, compared with the use considered a secondary pest of sugarcane of any compound alone (ethyl acetate, sugar- (Simmonds, 1966; Sosa et al., 1997) and it is cane or metalure). attracted to damaged or rotting plant mate- Population assessment of M. h. sericeus is rial. In sugarcane, Sosa et al. (1997) consider problematic. Trapping of adults is often used that the weevil is attracted to cane damaged to monitor weevil numbers. Viladerbo (1973) by either mechanical cultivation, harvesting and later Castrillon and Herrera (1980) equipment, rats, borers, disease or natural suggested the use of a ‘sandwich trap’ using growth cracks. Raigosa (1974) considers that banana pseudostem as an attractant. Using Metamasius females prefer to deposit eggs on the same trapping method, Peña et al. (1995) canes that have been damaged by Diatraea.In determined that population build-up of the Colombia this type of damage is known as weevil increased during spring, summer and the complex Diatraea-Metamasius. Metamasius early autumn in Florida, but warned that the has also been observed infesting canes used number of weevils collected at these traps as seedpieces (Raigosa, 1974). In Florida, was consistently low. Giblin-Davis et al. Sosa et al. (1997) observed infestation levels (1994) have determined major aggregation ranging from 8% to 32% of the stalks of CP pheromone compounds that can be used 85–1382. Sosa et al. (1997) found little or no for trapping and for monitoring weevil infestation in other cultivars growing next to populations in the field. CP 85–1382. Larvae of M. hemipterus sericeus can seriously affect ornamental palms, Sampling Phoenix canariensis, Ptychosperma macarthurii, Ravenia rivularis, Roystonia regia, destroy Sosa et al. (1997) surveyed sugarcane fields in banana and plantain, Musa spp., and inter- Florida, by two or three people walking the specific hybrids of Saccharum (Vaurie, 1966; field looking for infested stalks for 30 min. Giblin-Davis et al., 1994; Peña et al., 1995). If damaged cane was found, the field was Larval tunnelling in palms starts in the considered infested. Later Sosa et al. (1997) petioles, wounds in petioles, crown, stem sampled by walking along the aisle for and then extends into healthy leaf or stem ~80 m, moving inside the field and marking tissue. Affected palms are often characterized off the first 3 m of row, alternating between by the production of an amber-coloured and 2 centre rows and by striping leaves of the gummy exudate in the stem, crown shaft or bottom half of stalks for external symptoms petioles, and galleries in the leaves, petioles, of infestation such as lodging or cracked and stems (Giblin-Davis et al., 1994). rinds with frass extruding. Then they deter- In banana the larvae feed in the upper mined the number of larvae, pupae or adults part of the pseudostem. The first symptoms per sample. Sosa et al. (1997), determined a are yellowing of lower leaves and consequent mean of 2.4 weevils per stalk, suggesting that rotting of the pseudostem. this pest should be monitored closely.

Trapping Seasonality

Raigosa (1974) captured an average of 30 Densities of M. h. sericeus were low in Florida weevils per trap using pieces of bamboo filled when a banana disc trap was used to with pieces of fermenting cane. Peña et al. assess population density. Population build- (1995) captured a maximum of ten weevils up was observed from April through to June per trap per week using banana pseudostem and between November and December.

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Pests of Banana 35

Chemical control PARASITOIDS Surveys for biological control agents (predators, parasites) of M. h. sericeus Chemically based pest controls, currently have been unsuccessful (J.E. Peña, unpub- recommended by some control programmes, lished). Thus, very little is known about effec- represent a short-term and questionable tive biocontrol agents of M. h. sericeus in the strategy for resource farmers in Florida and Americas and the Caribbean. Siqueira et al. the Caribbean region with accompanying (1996) identified predators of Metamasius at health and environmental concerns for the the family level and stated that they were entire area. Giblin-Davis et al. (1996) demon- more abundant in Brazil than parasitoids. The strated that adults of M. h. sericeus were killed predacious families included Labiduridae, by labelled rates of acephate, carbofuran, Histeridae, Staphylinidae, Carabidae, Cicin- chlorpyrifos, cyfluthrin, disulfoton, imidach- delidae, Formicidae, Reduviidae, and Tachi- loprid, isofenphos, lindane and vydate. nidae. Search of host-specific parasitoids in Raigosa (1974) and Rossignoli (1972) exam- one of the areas of origin has not provided ined the use of sugarcane poisoned traps and any positive results (J.E. Peña, unpublished). determined that this method was adequate However, Cave and Alvarez del Hierro for control of M. h. sericeus while Nogueira (1997) found that the tachinid Admontia spp., (1976) and Sarah (1990) demonstrated that which was observed in Honduras parasitizing chemical control is not always possible Metamasius quadrilineatus, could be tested against M. h. sericeus. as a possible parasitoid of other species of Metamasius. Natural enemies Lixophaga sphenophori (Villeneuve), a successful parasitoid of a related sugarcane wee- ENTOMOPATHOGENS The use of entomo- vil species (Rhabdoscelus obscurus (Boisduval)), pathogens provides a promising but is currently considered as a candidate for bio- expensive means of control of M. h. sericeus. logical control of M. h. sericeus. L. sphenophori Entomogenous fungi, Beauveria bassiana was collected in New Guinea parasitizing the (Balsamo) Vuillemin and Metarhizium sugarcane weevil Rhabdoscelus obscurus and anisopliae (Metchnikoff) Sorokin, have gained was successfully introduced into Hawaii for considerable attention as potential control for control of the same weevil species in sugar- weevils (Mesquita et al., 1981; Peña et al., 1995; cane in 1910 (Waggy and Beardsley, 1972). The Giblin-Davis et al., 1996). For example, a study biology and behaviour of L. sphenophori is undertaken by Peña et al. (1995) demonstrated similar to another successfully introduced that naturally occurring B. bassiana was tachinid, Lixophaga diatreae, which is a parasite an important mortality factor to adults of of lepidopterous borers in sugarcane. L. M. h. sericeus in Florida. B. bassiana infection diatreae is larviparous and the complete life increased up to 70% between March and April stage lasts 20.5 to 32 days (Scaramuza, 1930). 1991, when more than ten weevils were The mode of entry by the parasitoid into the captured per trap (Peña et al., 1995). However, weevil larva and the ‘symptoms’ of para- more information was needed on the effect of sitized larvae have been described by Olson this fungus before pest management decisions (1970a,b). Topham and Beardsley (1973) have could be made. Giblin-Davis et al. (1996) studied the behaviour of L. sphenophori flies in demonstrated that the nematode Steinernema the field. These authors found a high correla- carpocapsae was efficacious against larvae tion between presence of flies and number of but not against adults of M. h. sericeus and nectar source plants. Leeper (1972) reported concluded that because of the high potential that Euphorbia hirta, Ricinus communis, Crotala- for high weevil production in Florida and ria incana and C. mucromata were the most the cyptic habitat of the boring stages of important sources for adult fly feeding. The this weevil, chemical insecticides and entomo- first two plant species are widely found in pathogenic nematodes will need to be applied Florida and could provide the nutritional frequently and over a long period of time for requirements of the fly upon its introduc- effective management. tion. Ota and Mitchell (1971) reported

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36 C.S. Gold et al.

that application of several insecticides in (Plates 6 and 7) are the most important sugarcane did not adversely affect parasitism peel-blemishing insects, producing a range of of L. sphenophori on Rhabdoscelus larvae. damage symptoms on immature fruit. Most of these species are found in the inflorescences or between fruits (Gallo et al., 1988). The skin Other pests of roots and rhizomes of severely infested fruit may crack, allowing secondary invasion of pathogens. The banana rust thrips Chaetanaphothrips signipennis, Roots and rhizomes are also attacked by apparently native to north Queensland, scarab beetle larvae, mealybugs, Chavesia sp., Australia, was originally described from and cydnid bugs of the genus Scaptcoris Sri Lanka. It has also been recorded in whose exudations inhibit growth of soil fungi Fiji, Panama, Trinidad, Brazil, Honduras, (Ostmark, 1974). Costa Rica, and Florida. In Brazil, injury by Tryphactothrips lineatus is regularly observed on 30-day-old fruits, or on fruits > 32 mm in Pests of Flowers and Fruits diameter (Martinez and Palazzo, 1971). In Mexico, Frankliniella parvula prefers to Thrips: Chaetanaphothrips orchidii oviposit in the epidermis of young banana (Moulton), C. signipennis (Bagnall), fruits and less frequently in the flower parts. Caliothrips bicinctus Bagnall, In Yemen, Scirtothrips aurantii and Thrips Frankliniella parvula Hood, Heliothrips pusillus cause fruit spotting on bananas. Small haemorrhoidalis (Bouché), Hercinothrips circular spots first appear on the surface of the bicinctus (Bagnall), Thrips hawaiiensis fruit, gradually enlarge, blacken and develop (Morgan), Tryphactothrips sp. into oily, water-soaked lesions (Childers and Achor, 1995). Thrips cause superficial skin blemishes on In Australia, T. hawaiiensis causes a immature and developing banana fruit. Dam- superficial skin injury locally referred to age is primarily cosmetic although severe as ‘corky scab’. Adults are attracted to the attacks may result in splitting of the peel emerging inflorescence. Female oviposition with subsequent development of secondary and subsequent nymphal and adult feeding roots. Usually only fruit grown commercially cause damage on the developing fruit while requires treatment with prophylactic pesti- the bunch is wrapped closely in the bracts. cides. In Australia, chemical treatments are Oviposition punctures result in localized routinely applied to prevent the rusty brown raised ‘pimples’ which disappear as the fruit discoloration caused by the pantropical develops, while the superficial grazing by the banana rust thrips Chaetanaphothrips signi- thrips develops into the slightly raised silvery pennis. The closely related C. orchidii grey areas of ‘corky scab’. This damage is (Moulton) causes similar damage in Central more prevalent during dry periods and is and South America. The banana flower thrips more commonly associated with fruit fingers Thrips hawaiiensis (Morgan), a widespread on the lower bunch hands, the rachis and and polyphagous flower feeder in Oriental attacked cushion (Pinese and Piper, 1994). and Pacific regions, damages fruit at flowering as it oviposits and feeds on fruit during Typical life history and immediately after emergence of the inflorescence. The slightly raised silvery grey Eggs are inserted into the plant tissues lesions caused by this thrips are locally including fruit, pseudostem and leaf petioles, referred to as ‘corky scab’. depending on species. Surfaces that are in Banana thrips Hercinothrips bicinctus close contact are preferred for oviposition (Bagnall), Caliothrips bicinctus, Chaetanapho- and development. The eggs hatch in 1 to 2 thrips orchidii, C. signipennis, Thrips hawaiiensis weeks. Nymphs are clear to straw-coloured and Tryphactothrips lineatus (Ostmark, 1974; and, like the adults, shun sunlight, quickly Reis and Souza, 1986; Pinese and Piper, 1994) dispersing when disturbed from their cryptic

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Pests of Banana 37

hiding places between adjacent fruit or from chlorpyrifos-impregnated ribbon to the upper under leaf bracts on the pseudostem. Pupa- bunch stalk also provides extended protection tion takes place on the plant or in the soil near against C. signipennis. Untreated polythene the base of the plants, depending on species. bunch covers significantly reduced damage Banana rust thrips may spend part of their compared to uncovered fruit while bunch life cycle in the soil, while banana flower covers impregnated with 1% chlorpyrifos pro- thrips stages all occur on the host plant vided almost total protection (Pinese, 1987). (Pinese and Piper, 1994). For example, in Australia, the entire life cycle of T. hawaiiensis is spent on the fruit Banana fruit scarring beetles, or other parts of the plant. During summer Colaspis hypochlora Lefevre months, the period from egg to adult for this species is 3 weeks. Colaspis hypochlora has been reported from Mexico, Central America, Colombia and Brit- Monitoring ish Guyana (Simmonds, 1982). It appeared Monitoring methods for rust and flower first as a banana pest in Colombia in 1922; thrips and their damage have been developed the outbreak reached a peak 3 years later and are used in Australia (Pinese and Piper, and declined in subsequent years. Eggs are 1994). most commonly placed in cavities gnawed by the female beetle in the sheath or root of the Management banana plant; however, they may also be laid in the soil to a depth of up to 1 cm. Eggs may Cultural methods of control, such as clean be placed singly or in groups of up to 45. cultivation and removal of trash, promote the The larvae remain in the soil, feeding on the exposure of pupae to desiccation, but do not roots of grasses, especially those of Paspalum provide effective control (Simmonds, 1966). conjugatum. The larvae are sensitive to soil In Brazil, Gallo et al. (1988) recommended the moisture and will move downwards in dry use of chemical control as soon as the flowers soils. If the soil remains dry for long periods, are formed, elimination of flowers after the the larvae may die. Pupation occurs in the fruits are formed, removal of alternative host soil, the depth depending on the moisture plants, and covering banana bunches with a present. bag impregnated with insecticides. Martinez On emergence, the adults leave the soil and Palazzo (1971) recommend harvesting feed on the leaves of various weeds as well as fruits with 34 mm diameter. According to on the young leaves and fruits of banana. The Simmonds (1966) no useful natural enemies adult beetle is nocturnal in habit. Following of the banana thrips are known. Pinese (2001) emergence, the beetles live for 9 to 12 days. In also reported a lack of beneficials for C. Colombia, breeding occurs only during the signipennis in north Queensland, Australia, wet season, which allows production of four although Pinese and Piper (1994) found that broods (April, June, August and October/ a number of generalist predatory bugs, November). coccinellids and chrysopids feed on flower The adult beetles feed on the unfurled thrips and can reduce their numbers. leaves of the banana, on the skin of the fruits, Chemical control methods consist of marking the fruit in such a way as to render enclosing the bunch inside an insecticide- it unsaleable. Most of the scarring occurs on treated bag. This practice, once widespread, is the lower proximal surfaces of the fingers, still recommended in South America. A single reflecting the fact that the beetle chooses the pesticide injection into the emerging inflores- most sheltered spots for feeding. The scars are cence, a treatment specifically aimed at the mostly oval in shape, and their damage banana scab moth, is also efficacious against can be confused with that caused by the T. hawaiiensis and helps protect from early fruit-scarring bee Melipona (Trigona) amalthea C. signipennis infestation. Attaching a piece of (Olivier). Scarring is worst on banana fruits

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growing in close proximity to drainage canals, rufivena occassionally inflicts damage to or grassy-weedy patches in the fields and young fruit adjacent to rainforest. or near grassy roadsides, thus reflecting O. sacchari belongs to a group of species the larval ecology of the insect. that are detritus feeders and rarely feed on living plant tissue. The eggs are minute and Control laid singly on the banana fruit (Pinese and Piper, 1994). The egg stage is 10 days at 18°C Cutting grasses selectively around infested (Martin, 1983). The larva has seven instars areas has been recommended for reducing with total stage duration of 50–90 days, while Colaspis infestations. Natural enemies of the the pupal stage is 21 days (Martin, 1983; Davis beetle in Colombia do little to reduce the and Peña, 1990). The lowest larval tempera- population, though predation by frogs, ture threshold is −5°C. The pupa is found lizards and spiders has been observed under a tough silken cocoon and adults rest (Simmonds, 1966). Chemical control is not with their wings folded on banana leaves. The recommended. life cycles of O. glycyphaga and T. rufivena have not been studied.

Irapua bee, Trigona spinipes Fabricius Damage

O. sacchari prefers to oviposit on fresh inflo- The ‘Irapua’ bee Trigona spinipes Fabricius rescences as opposed to dry flowers (Moreira, visits the inflorescences of banana and some- 1979a,b). The larvae may feed on bunches, times causes damage to young fruits. Injury pseudostems and sometimes even attacks appears as dark, very well defined spots on the rhizome (Martin, 1983). The most serious the fruit and, in cases of heavy bee infesta- damage occurs to the banana inflorescence. tion, the damage appears along the angles The larvae burrow into the substratum and of the fruit (Silva and Fancelli, 1998). Silva seldom feed on exposed material. Their pres- and Fancelli (1998) recommend as control ence is usually indicated by the accumulation measures to harvest fruits early or to protect of frass and other debris entangled in larval fruits with polythene bags impregnated with silk over the surface of the injury. In Brazil, insecticides. larval galleries cause rotting of fruits (Moreira, 1979a,b). In Florida, there are ten generations per year with adult populations highest bet- Banana moths, Opogona glycyphaga ween the spring and early autumn months. Meyrick, Opogona sacchari Bojer, Adult activity is observed between 01:00 h Tirathaba rufivena (Walker) and 04:00 h (12L : 12D) before the end of scot- ophase. Martin (1983) recomended the use of The banana moth Opogona sacchari Bojer (= O. black light traps for collection of adults. subcervinella (Walker); Tinea subcervinella O. glycyphaga causes superficial scarring (Walker), Gelichia sanctae-helenae Mellis) has predominantly near the flower ends or at con- been recognized as a pest of bananas and tact points between the lower flowers and the row crops in both tropical and temperate fruits. Thus damage is mostly limited to areas environments. O. sacchari has been reported where larvae can feed under the protection of from Mauritius, Canary Islands, Madagascar, spent floral parts. Presence of copious black Italy, Belgium, The Netherlands, Great Brit- frass pellets attached to webbing is indicative ain, Brazil, Peru, Barbados, and the United of attack by this pest. States. O. sacchari is highly polyphagous T. rufivena larvae feed deep into the and attacks at least 42 plant species, among pulp, in contrast to the superficial feeding by them Musa paradisiaca and Musa sapientum. O. glycyphaga. This moth is most damaging The sugarcane bud moth, O. glycyphaga is in bunches near rainforests, suggesting that a significant banana fruit pest in Australia rainforest plants are their preferred food and (Pinese and Piper, 1994) and Tirathaba bananas are an incidental host.

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Pests of Banana 39

Control Damage

The best control method for banana fruit Larval feeding on young banana fruits, moths is prevention. This can be done by primarily on the outer curve, causes super- cleaning debris from banana plantations ficial scarring. As the fruit develops, lesions (Martin, 1983). In Brazil, Cintra (1975) recom- turn into black scabs from which the insect’s mends manual removal of affected inflor- common name is derived. Severe feeding can escences. Chemical control has also been extend to cover the majority of the finger, recommended (Moreira, 1979b) and the lar- preventing normal fruit development and vae of O. sacchari are known to be susceptible causing fruit distortion. The scab moth is to carbamates and organophosphates. How- most active during wet, humid and hot con- ever, insecticide efficacy in controlling fruit ditions when, if left untreated, total bunch moths drops rapidly after 8 days (Peña et al., damage is possible. Banana is the preferred 1990a,b). commercial host but feeding has been The entomopathogenic nematodes observed on Heliconia, Nipa and Pandanus and Steinernema carpocapsae and Heterorhabditis these hosts can provide suitable breeding heliothidis provided 16–23% larval mortality sites during periods when bananas are not during the first 2 weeks following application available. (Peña et al., 1990a,b). In Australia, treatment of bunches with entomopathogenic nematodes Biology for of control banana scab moth and rust thrips provided effective control of both The adult female lays dorsoventrally flattened O. glycyphaga and T. rufivena. scale-like eggs singly or, more commonly, in small clusters of up to 20 overlapping eggs. Eggs are placed on the smooth bracts of the inflorescence, the bases of the adjacent leaves Banana scab moth, Nacoleia octasema and, uncommonly, the upper pseudostem. (Meyrick) Females live for 4–5 days and lay 80–120 eggs (Simmonds, 1966). Egg laying is confined to The banana scab moth, Nacoleia (Notarcha, the period immediately prior to and during Lamprosema) octasema is known from emergence of the inflorescence, a period Indonesia, New Guinea, the Solomon spanning about 7 days. After emergence, the Islands, New Caledonia, Fiji, Tonga, Samoa, young larvae migrate under the upper bunch and Queensland (Simmonds, 1982) (Plate 8). bracts to feed on the immature fruit of the In Queensland its distribution is confined basal (upper) hands. As the bracts and under- to coastal areas north of Townsville. Sibling lying fruit hands lift, the larvae migrate pro- species or biotypes may be present as host gressively to the nearest lower unlifted hand preference varies markedly in different to feed in the protected area between the fruit locations between what appear to be mor- and the bunch stalk until they reach the distal phologically similar insects. For example, (bottom) hands. Although not naturally gre- bananas are not attacked on mainland New garious, limitations on suitable feeding sites Guinea or parts of Indonesia or Malaya can lead to crowding (Paine, 1964). By the where the moth feeds on Pandanus and Nipa. time the last hand lifts, the larvae have com- This may indicate the presence of non- pleted five instars and are usually fully banana-feeding races being present in these grown. areas (Paine, 1964). While a valid explanation The larvae grow and feed more vora- for this anomaly has not been put forward, ciously as they move down the bunch. Thus, taxonomic clarification to determine if damage tends to increase in severity from the distinct races are present in geographically top to the bottom hands. During hot summer separate areas is required before meaningful conditions, when fruit and bunch develop- attempts at the introduction of biological ment is rapid, the larvae complete their controls can progress. development under the bracts of the male

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40 C.S. Gold et al.

bud among the upper male flowers or migrate that limitations of food and climate are more back up the bunch, feeding between fruit important than parasites in the regulation of fingers. Pupation occurs primarily within a this pest. frail silken cocoon covered by frass on the In commercial plantations, pesticide bunch or among the trash near the base applications to the ‘throat’ of plants which of the plant, or within dry leaf petioles on are approaching inflorescence emergence by the lower pseudostem. The entire life cycle aerial or ground-based cover sprays or by from egg hatch to egg laying is completed in dusting individual plants have been replaced aproximately 28 days during summer. Cooler by a single targeted injection into the inflores- and drier winter periods are not suitable for cence. Diluted organophosphates or carba- scab moth, when development periods are mates (20–40 ml) are injected into the upper greatly increased. In Australia, its restricted third of the inflorescence to prevent damage to climatic range has prevented its spread into fruit (Pinese and Piper, 1994). This treatment the drier and cooler environments outside has to be applied to the vertical inflorescence, of the wet coastal tropical regions of north requiring at least weekly selection and Queensland. treatment of inflorescences. All adult behaviour is crepuscular with adult emergence and mating occurring from 30 to 60 min after sunset (B. Pinese, personal Fruit flies: Banana fruit fly, Bactrocera musae observation). Adults are very cryptic by day (Tryon); Queensland fruit fly, and are seldom observed and, if disturbed, fly Bactrocera tryoni (Froggatt) short distances before seeking shelter. Both the banana fruit fly, Bactrocera musae Control (Tryon), and the Queensland fruit fly, Bactrocera tryoni (Froggatt), are pests of Chemical treatments remain the most impor- banana grown in north Queensland (Austra- tant control tactic for commercial production. lia) the Torres Strait, Papua New Guinea and As the entire life cycle is completed on the nearby islands. B. musae is primarily a pest plant, cultural control is not practical against of cultivated and wild banana and will sting this pest (Simmonds, 1982; Waterhouse and and oviposit in very immature fruit, but its Norris, 1987) and biological control has very eggs may fail to develop unless oviposition limited potential (Paine, 1964). Franzmann occurs in fruit approaching maturity (climac- (1979) recorded only nine larval parasites and teric). B. tryoni has an extensive host range no egg parasites from extensive field collec- but will only sting ripe or ripening banana tion of eggs and larvae. These included two fruit. Commercial bananas harvested at the species of tachinid fly parasite, Bacromyiella mature ‘hard green’ stage (preclimacteric) ficta and Argyrophylax proclinata Crosskey, are not considered hosts of either species and one elasmid wasp, Elasmus sp. Although for quarantine purposes. Waterhouse and Norris (1987) list 12 species Eggs are laid in the pulp just below the which were introduced into Fiji, Java, and skin. As fruit ripens, they hatch and the mag- Western Samoa from 1929 to 1964, only one, gots feed on the soft flesh and, when fully Chelonus sp., established in Fiji where it exerts developed, fall to the ground to pupate. The variable control. Poor efficiency has also been complete life cycle takes about 2.5 weeks dur- noted from naturally occurring parasites. In ing the hot summer months. north Queensland, high populations of the ants Tetramorium bicarinatum (Nylander) and Control Pheidole megacephala appeared to significantly reduce the incidence of damage and T. Control relies on good plantation manage- bicarinatum was observed attacking larvae. ment to prevent ‘mixed ripe’ bunches which However, the generally poor level of bio- can attract and act as breeding sites for fruit logical control of N. octasema in bananas fly. Harvesting at the ‘hard green’ stage, prior led Paine (1964) to the pessimistic conclusion to fruit becoming susceptible, is the main

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Pests of Banana 41

method of ensuring damage-free fruit. Insec- and grow within the rolls, commencing a new ticide treatments are not necessary. roll once the midrib is reached. The second and subsequent three instars are covered in a white waxy powder that provides protection Pests of Foliage from drowning during high rainfall. The larval stage lasts between 20 and 30 days Banana skipper, Erionota thrax (Linnaeus) depending on temperature. Pupation occurs within the leaf roll and lasts from 8 to 12 days. The banana skipper, Erionota thrax (Linnaeus), Adults emerge in the afternoon and are most is a minor to severe pest of bananas and Musa active in the evening and early morning when textilis in South-East Asia (Kalshoven, 1981) they actively fly around banana plants to mate and, since 1986, Papua New Guinea (Sands and oviposit. et al., 1988). Damage is also recorded from bamboo, coconut and a range of palms Control including oil and nipa (Waterhouse and The banana skipper is adequately controlled Norris, 1989) although it has been suggested by a range of beneficial insects such that that other species may be responsible for the other control measures are seldom required. records on palms and bamboo (Sands et al., If unusually heavy outbreaks occur, the 1988; Waterhouse and Norris, 1989). Banana collection and destruction of leaf rolls is clumps in isolated villages in Java had a helpful. In Indonesia, egg parasitoids, includ- very patchy damage distribution, ranging ing Ooencyrtus erionotae, Agiommatus sp. and from severe defoliation to nil on clumps Anastatus sp., can parasitize 50–70% of the growing within close proximity (B. Pinese, eggs (Kalshoven, 1981). Young larvae are personal observation). Heavy rainfall and attacked by Apanteles erionotae while older strong winds are unsuitable for banana third instar larvae are preferred by skipper. Entry of water into the leaf rolls Scenocharops sp. (Waterhouse and Norris, drowns the larva (particularly the first instar) 1989). The pupal parasitoids Brachymeria sp., and wind-torn leaf laminae are unsuitable for Xanthopimpla sp. and Pediobius sp. also con- the production of leaf roll shelters. For these tribute to biological suppression of E. thrax. reasons, outbreaks in Malaysia and Indonesia are more common after a drought and in wind-protected areas (Kalshoven, 1981). Direct fruit production losses would only Bagworm, Oiketicus kirbyi Guilding be significant following heavy defoliation, since banana plants can withstand at least 20% The bagworm Oiketicus kirbyi Guilding is leaf lamina loss before production is affected a polyphagous insect (Costa Lima, 1945; (Ostmark, 1974). None the less, bananas in Martorell, 1945; Ebeling, 1959) that became a South-East Asia are grown for aesthetic value leaf-feeding pest of bananas in Costa Rica (Hoffmann, 1935) and for culinary purposes in 1958 (Stephens, 1962) and later caused where even minor infestations would be some damage in plantations of banana in detrimental. Colombia (Garcia, 1987). The maggot-like The adult butterfly lays bright yellow female deposits eggs in the posterior portion eggs singly or in groups of up to 25. These are of the pupal case that remains as a secured laid at dusk or at night, preferentially on the ‘bag’. Eggs hatch in 27 to 32 days and the lower leaf lamina midway between the midrib larval stage may range from 207 to 382 days and the outer edge. Eggs turn bright red and (Stephens, 1962). The female pupal period the pale green larvae hatch after about 5 to 8 lasts 10 to 33 days while the male pupal stage days. The larvae move to the outer leaf lamina lasts 11 to 39 days. The larvae-female adult where they commence feeding and then pro- can live 14 days during which time she may duce loose rolls by cutting the leaf and rolling deposit up to 6700 eggs. The males live only the lamina towards the midrib. Larvae feed 3 to 5 days.

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Control spp. (Hymenoptera: Scelionidae), Calocarcelia sp. (Diptera: Tachinidae), Meteorus spp. Two dipterous parasitoids, Sarcophaga (Sarco- (Hymenoptera: Braconidae) (Fancelli and dexia) lambens Wiedemann and Achaotoneura Martins, 1998). sp., attack medium and large bagworms. A braconid, Iphiaulax sp. parasitizes all larval sizes, whereas Psychidosmicra sp. (Hymen- optera: Chalcidae) attacks only small larvae. Sucking insects – Banana aphid, Pentalonia Other hymenopterous parasites found by nigronervosa Coquerel Stephens (1962) are Casinaria sp., Phobetes sp., and Carinodes sp. Predacious ants frequently The banana aphid, Pentalonia nigronervosa attack larvae of all sizes. A microsporidiam, Coquerel, is the sole vector of banana bunchy Nosema sp., and a fungus, Beauveria bassiana top disease, one of the serious viral diseases (Balsamo) Vuillmen, infect all larval stages of Musaceae (Magnaye, 1959). Although the (Stephens, 1962) in Costa Rica. In Colombia, disease was observed as early as 1915 and small larvae are attacked by Psychidosmicra became serious in 1923 (Ocfemia, 1930), this sp., Spilochalcis sp., Iphiaulax sp., and Brachy- aphid gained importance only when the meria sp. (Garcia, 1987). first proof of its ability to transmit bunchy Cultural control is recommended by top virus from diseased to healthy abaca removing all larvae from infested plantations. was established (Ocfemia, 1930). Other Microbial control, using Bacillus thuringiensis, researchers claim that only this species and is recommended in Colombia as an effective the subspecies, O. nigronervosa f. caladii, are control (Garcia, 1987). capable of transmitting the disease (Espino and Ocfemia, 1948). The banana aphid is a widely distributed tropical and subtropical species. Distribution records include the Phil- Caterpillars, Caligo spp., Opsiphanes spp., ippines, Ellice Island, Malaya, Fiji, Samoa, Antichloris spp. Papua, Sabah, India, Ceylon, Mauritius, Africa (including Malawi and Rwanda), Several caterpillars sporadically, cause Egypt, Sierra Leone, Zanzibar, Australia, damage to the foliage of bananas. Often their Central America, and Bermuda. In some presence is the result of disruptions to the cases (e.g. Uganda) the aphid is present, but ecosystem that surround banana plantations the bunchy top virus is not. (Mesquita and Alves, 1984). For example, Both alate and apterous forms of Pent- Caligo spp., Opsiphanes spp., and Antichloris alonia nigronervosa coexist in dense colonies spp. can become pests of banana when their on banana plants and breed continuously natural enemies are reduced. At such times, throughout the year (Varma and Capoor, 1958). these have been reported as key pests of P. nigronervosa populations increase at moder- banana in Brazil (Tourner and Viladerbo, ate humidity and temperature and decrease 1966; Tourner et al., 1966). during drought and heavy rainfall (Kolkaila and Soliman, 1954; Varma and Capoor, 1958; Control Kung, 1963; Menon and Christudas, 1967; Gavarra, 1968). In Egypt, the greatest aphid In Brazil larvae of Caligo spp. are parasitized activity occurs from December to February, by Hemimasipoda sp. (Diptera: Tachinidae), with the population being at its lowest from Spilochalcis spp. (Hymenoptera: Chalcidae); March to May (Kolkaila and Soliman, 1954). In Opsiphanes spp. is parasitized by Apanteles the warmer regions the aphid is most abundant spp. (Hymenoptera: Braconidae), Horismenus during winter from May to July (Goddard, spp. (Hymenoptera: Eulophidae), Spilochalcis 1929; Ayyar, 1954; Varma and Capoor, 1958; spp. (Hymenoptera: Chalcidae) and by Kung, 1963; Menon and Christudas, 1967). Xanthozoma melanopyga (Diptera: Tachinidae); Besides the Musaceae, this species can be Anthocloris spp. is parasitized by Telenomus found feeding on species in the families

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Pests of Banana 43

Araceae, Zingiberaceae, Cannaceae; however, resistance of the hybrids to the aphid vector their main hosts are abaca and banana. may partly explain their resistance to banana bunchy top disease. Biology

The banana aphid reproduces parthenogenetically throughout the year and no males Mites have been observed. It is also entirely viviparous as eggs are unknown. From 21 to 26 Mites are considered minor pests of banana, overlapping generations have been recorded but can erupt into epidemics, causing dam- throughout the year with no hibernation age to leaves (Ostmark, 1974) and less often (Kung, 1963). The average fecundity of one to fruit. Mite outbreaks are usually due to apterous female is 31.5 (Johnson, 1963; Kung, insecticide-induced disruption and some 1963; Magnaye, 1959). Threshold development mite epidemics have been triggered by road in degree-days ranged from 287 to 330°d dust inhibiting the action of predators at 22–31°C and 69–72% relative humidity (Ostmark, 1974). (Lomerio and Calilung, 1993). There are four Most of the mites are oligophagous to five nymphal instars and the total develop- species with restricted distribution. For mental period ranges from 8 to 21 days with instance, the banana rust mite Phyllocoptruta an average of 14.5 days (Kung, 1963). musae Keifer is reported to cause spotting on The preferred sites for P. nigronervosa are bananas in Queensland (Jeppson et al., 1975), within the whorl of the growing shoot and but it is not reported in other parts of the between the leaves on young suckers and world. Mites of the genus Tetranychus are most growing plants and on immature fruit. During commonly reported as pests of banana. The rainy months, the aphids are found around banana spider mite (also known as the straw- the base of the pseudostems at soil level or berry spider mite) (Plate 9) T. lambi Pritchard several centimetres below (Calilung, 1978). and Baker and the twospotted spider mite Colonies sometimes infest flowers and fruits T. urticae Koch are common pests of a broad (Kolkaila and Soliman, 1954). The aphids range of crops and are widely distributed colonize the roots and corms of abaca but (Pinese and Piper, 1994). are rarely found on roots of banana (Magee, 1927; Ocfemia and Garcia, 1947; Wardlaw, Damage 1972). In Australia, heavy bunch infestations, which result in sooty mould development on Mite damage in banana is confined to the fruit, are infrequent due to effective biological underside of the leaves; however, in severe control from a complex of beneficial insects. outbreaks the mites can move to bunches Outbreaks are associated with cooler weather and damage the fruit. Leaf damage appears at in autumn and spring and disruption of natu- first as isolated bronzed rusty patches, which ral control from broad specrum pesticides. later coalesce along the leaf veins as the infes- Dispersal can be by flight (Magee, 1927; tation increases. Fruit damage by T. lambi is Goddard, 1929) or assisted by the ants found mainly at the cushion end of the Ragiolepsis longipes Gord. and Dolichoderus fingers. Feeding in this area causes a red to bituberculatus Mayr. purple-black discoloration of the fruit surface that may later dry out and crack (Pinese and Host plant resistance Piper, 1994). T. urticae damages the tips of fingers mostly on the top hands, giving the Facundo and Sumalde (1998) determined that affected fruit a dull silvery grey appearance. the abaca cultivars Itoalus × Magsarapong The main impact of mite damage is on yield, No. 7 and Pacol × CES III-2 were resistant to where loss of phytosynthetic capacity results P. nigronervosa, compared with the develop- in slower plant growth and fruit filling. The ment observed in the resistant cultivar impact is most noticeable if plants are Tinauagan Pula (TP). They consider that stressed by other factors such as drought or

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nematode and banana weevil borer damage References to roots and corms. In experimental trials, where mite pressure and plant response were Abera, A.M.K. (1997) Oviposition preferences and assessed, an arbitrary ‘medium’ leaf damage, timing of attachment by the banana weevil where bronzing damage was readily visible (Cosmopolites sordidus Germar) in East African on leaves, caused a 2 week extension to the highland banana (Musa spp.). MSc thesis, Makerere University, Kampala, Uganda. fruit filling period from bunch emergence to Abera, A.M.K., Gold, C.S. and Kyamanywa, S. harvest (B. Pinese, unpublished). (1999) Timing and distribution of attack by the banana weevil (Coleoptera: Curculionidae) in Biology East African highland banana (Musa spp.). Florida Entomologist 82, 631–641. The life cycles and appearance of T. lambi and Allen, R.N. (1989) Control of Major Pests and Diseases T. urticae are similar. The main distinguishing of Bananas. Department of Agriculture New feature between them is the relative lack South Wales, 10 pp. of fine webbing in infestations of T. lambi, Alpizar, D., Fallas, M., Oehlschlager, A.C., whereas high populations of T. urticae are Gonzalez, L. and Jayaraman, S. (1999) always associated with webbing (Pinese and Pheromone-based mass trapping of the banana Piper, 1994). weevil, Cosmopolites sordidus (Germar) and the West Indian sugarcane weevil Metamasius hemipterus L. (Coleoptera: Curculionidae) in Monitoring and control plantain and banana. Memorias XIII Reunion ACORBAT, 23–27 November 1998. Guayaquil, Pinese and Piper (1994) recommended pp. 515–538. fortnightly monitoring during periods of Altieri, M.A. and Letourneau, D.K. (1982) hot dry weather when mite development and Vegetation management and biological activity is highest. Five plants are selected control in agroecosystems. Crop Protection 1, and mite damage to leaves is assessed using 405–430. three categories: (i) low or few scattered Ambrose, E. (1984) Research and development in discrete mite colonies; (ii) medium or mite banana crop protection (excluding Sigatoka) colonies scattered but numerous and coal- in the English speaking Caribbean. Fruits 39, escing between the interveinal areas; and 234–247. Anitha, N., Rajamony, L. and Radhakrishnan, T.C. (iii) high, or mite colonies coalescing, with (1996) Reaction of banana clones against major bronzing damage over most of the leaves. biotic stresses. Planter 72, 315–321. Miticide treatments are required only Anonymous (1989) Guia Educativa No. 1: Trampeo when mean damage to leaves reaches the Para el Picudonegro en Platano. Fundacion ‘medium’ level. Other considerations relate Hondureña Investigaciones Agricolas, La to the presence or absence of mite predators, Lima, 14 pp. particularly the mite-eating ladybird beetle, Arleu, R.J. and Neto, S.S. (1984) Broca da Stethorus fenestralis (Coleoptera: Coccinellidae), bananeira Cosmopolites sordidus (Germ., 1824) plant vigour and anticipated weather condi- (Coleoptera: Curculionidae). Turrialba 34, tions. To achieve maximum benefit from miti- 359–367. Arroyave, F.P. (1985) Control del picudo negro cide treatments, high volume cover sprays −1 Cosmopolites sordidus Germar en semilla using a minimum of 500 l ha must be applied vegatativa de platano (Musa AAB Simmonds). when leaves are turgid to ensure good spray Ingeniero Agronomo thesis, Universidad de cover under the leaves where the mites are Caldas, Manizales, Colombia. present. A second application, 14 days later, is Ayala, J.L. and Monzon, S. (1977) Ensayo sobre usually required to control mite carryover. diferentes dosis de Beauveria bassiana para el control del picudo negro del platano (Cosmopolites sordidus) (Germ.). Centro Agricultura, Revista Ciencias de Facultad de Acknowledgement Ciencias Agricolas 4, 19–24. Ayyar, G.R. (1954) Unrecorded host plant of This is Florida Agricultural Experiment Pentalonia nigronervosa Coq. Current Science 23, Station’s Journal Series No. R-08408. 408–409.

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Sikora, R.A., Bafokuzara, N.D., Mbwana, A.S.S., R.V., Davide, R.G., Stanton, J.M., Treverrow, Oloo, G.W., Uronu, B. and Seshu Reddy, K.V. N.L. and Roa, V.N. (eds) Proceedings of Banana (1989) Interrelationship between banana Nematode/Borer Weevil Conference, Kuala weevil, root lesion nematode and agronomic Lumpur, 18–22 April 1994. INIBAP, Los Baños, practices, and their importance for banana pp. 48–56. decline in the United Republic of Tanzania. Stephens, C.S. (1962) Oiketicus kirbyi (Lepidoptera: Food and Agriculture Organization Plant Protec- Psychidae) a pest of bananas in Costa Rica. tion Bulletin 37, 151–157. Journal of Economic Entomology 55, 381–386. Silva, C.G. and Fancelli, M. (1998) Banana insect Stover, R.H. and Simmonds, N.W. (1987) Bananas, pests. In: Galan S.V. (ed.) Proceedings of 3rd edn. John Wiley & Sons, New York, an International Symposium of Banana in the 469 pp. Subtropics. Tenerife, Spain, pp. 385–393. Taylor, B. (1991) Research field work on upland Simmonds, N.W. (1966) Bananas. Longman, bananas, Musa spp., principally acuminata London, UK, 512 pp. triploid AAA types in the Kagera region of Simmonds, N.W. (1982) Bananas, 2nd edn. Tanzania. With observations on growth and Longman, Harlow, UK. causes of decline in crop yield. Rivista di Simmonds, N.W. and Shepherd, K. (1955) The Agricultura Subtropicale e Tropicale 85, 349–392. taxonomy and origins of the cultivated Topham, M. and Beardsley, J. (1973) Influence of bananas. Linnean Society of Botany 55, 302–312. nectar source plants on the New Guinea sugar- Simmonds, N.W. and Simmonds, F.J. (1953) cane weevil parasite, Lixophaga sphenophori Experiments on the banana borer, Cosmopolites (Villeneuve). Proceedings of the Hawaiian sordidus in Trinidad, BWI. Tropical Agriculture Entomological Society 22, 145–154. 30, 216–223. Tourner, J.C. and Viladerbo, A. (1966) Lepidopteres Siqueira, H.A., Barreto, R., Cavalcante, T. and defoliateur du bananaier en Equateur: morph- Picanco, M. (1996) Conrole biologico de ologie et biologie. II Opsiphanes tamarindi, var. Cosmopolites sordidus e Metamasius sp. corrosus Stitchel. Fruits 21, 159–166. (Coleoptera: Curculionidae) em bananeoira Tourner, J.C., Viladerbo, A., and Stomayor, B. (1966) por predadores e parasitoides. V Siconbiol, Faz Lepidopteres defoliateurs du bananier en de Iguacu, Brasil, 9–14 June, p. 161. Equateus: morphologie et biologie. I Caligo Smith, D. (1995) Banana weevil borer control in eurilochus Stich. (Brassolidae). Fruits 21, south-eastern Queensland. Australian Journal of 55–56. Experimental Agriculture 35, 1165–1172. Traore, L. (1995) Facteurs biologiques de mortalite Sosa, O., Shine, J. and Tai, P. (1997) West Indian cane de Curculionidae en mileux tempere et tropi- weevil (Coleoptera: Curculionidae): a new pest cal. PhD thesis, McGill University, Montreal, of sugarcane in Florida. Journal of Economic Canada. Entomology 90, 634–638. Traore, L., Gold, C.S., Pilon, J.G. and Boivin, G. Speijer, P.R., Budenberg, B. and Sikora, R.A. (1993) (1993) Effects of temperature on embryonic Relationships between nematodes, weevils, development of banana weevil, Cosmopolites banana and plantain cultivars and damage. sordidus Germar. African Crop Science Journal 1, Annals of Applied Biology 123, 517–525. 111–116. Speijer, P.R., Gold, C.S., Kajumba, C. and Karamura, Traore, L., Gold, C.S., Boivin, G. and Pilon, J.G. E.B. (1995) Nematode infestation of ‘clean’ (1996) Developpement postembryonnaire du banana planting material in farmers fields in charancon du bananier. Fruits 51, 105–113. Uganda. Nematologica 41, 344. Treverrow, N. (1993) An integrated management Sponagel, K.W., Diaz, F.J. and Cribas, A. (1995) El program for banana weevil borer. Final Report. Picudo Negro del Platano, Cosmopolites sordidus HRDC. Project Number: Fr/0012/RO. Wollong- Germar. Fundacion Hondureña Investigacion bar Agricultural. Institute, Wollongbar NSW, Agricola. La Lima, Honduras, 35 pp. Australia, 40 pp. Ssennyonga, J.W., Bagamba, F., Gold, C.S., Treverrow, N. (1994) Control of the banana weevil Tushemereirwe, W. K., Ssendege, R. and borer, Cosmopolites sordidus (Germar) with Katungi, E. (1999) Understanding Current entomopathogenic nematodes. In: Valmayor, Banana Production with Special Reference to R.V., Davide, R.G., Stanton, J.M., Treverrow, Integrated Pest Management in Southwestern N.L. and Roa, V.N. (eds) Proceedings of Banana Uganda. International Center of Insect Physiol- Nematode/Borer Weevil Conference, Kuala ogy and Ecology, Nairobi, Kenya, 47 pp. Lumpur, 18–22 April 1994. International Stanton, J.M. (1994) Status of nematode and weevil Network for Improvement of Banana and borer problems in Australia. In: Valmayor, Plantain, Los Baños, pp. 124–138.

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Pests of Banana 55

Treverrow, N. and Bedding, R.A. (1993) Develop- Vaurie, P. (1966) A revision of the Neotropical ment of a system for the control of the banana genus Metamasius (Coleoptera: Curculionidae, weevil borer, Cosmopolites sordidus, with ento- Rhynchophorinae). Species groups I and II. mopathogenic nematodes. In: Bedding, R., Bulletin American Museum Natural History 131, Akhurst, R. and Kaya, H. (eds) Nematodes 213–337. and the Biological Control of Insect Pests. CSIRO, Veitch, R. (1929) The banana weevil borer. In: Veitch, Melbourne, pp. 41–47. R. and Simmonds, J.H. (eds) Pests and Diseases Treverrow, N. and Maddox, C. (1993) The of Queensland Fruits and Vegetables. Octaro, distribution of Cosmopolites sordidus (Germar) Brisbane, pp. 255–263. (Coleoptera: Curculionidae) between various Vilardebo, A. (1950) Conditions d’un bon rende- types of banana plant material in relation to ment du peigeage de Cosmopolites sordidus. crop hygiene. General and Applied Entomology Fruits 5, 399–404. 23, 15–20. Vilardebo, A. (1960) Los insectos y nematodos de Treverrow, N., Bedding, R., Dettmann, E.B. and las bananeras del Ecuador. Instituto Franco- Maddox, C. (1991) Evaluation of entomo- Euaotiano de Investigaciones Agromicas, pathogenic nematodes for the control of Paris, 78 pp. Cosmopolites sordidus Germar (Coleoptera: Vilardebo, A. (1973) Le coefficient d’infestation, Curculionidae), a pest of bananas in Australia. critere d’evaluation du degre d’attaques Annals of Applied Biology 119, 139–145. des bananeraies par Cosmopolites sordidus Treverrow, N., Peasley, D. and Ireland, G. (1992) Germ. le charancon noir du bananier. Fruits Banana Weevil Borer: A Pest Management 28, 417–431. Handbook for Banana Growers. Banana Industry Viswanath, B.N. (1976) Studies on the biology, Committee. NSW Agriculture, 28 pp. varietal response and control of banana Tsai, Y.P. (1986) Major insect pests of banana. rhizome weevil, Cosmopolites sordidus In: Plant Protection in the Republic of China (Germar) (Coleoptera: Curculionidae). PhD (1954–1984), 6 pp. thesis, Bangalore, India. Turner, D.W. (1994) Bananas and plantains. In: Waggy, S. and Beardsley, J. (1972) Biological studies Schaffer, B. and Andersen, P.C. (eds) Handbook on two sibling species of Lixophaga (Diptera: of Environmental Physiology of Fruit Crops, Tachinidae) parasites of the New Guinea sug- Vol. III, Subtropical and Tropical Crops. CRC arcane weevil, Rabdoscellus obsucrus Press, Boca Raton, Florida, pp. 37–61. (Boisduval). Proceedings of the Hawaiian Ento- Uronu, B.E.M.A. (1992) The effect of plant resistance mological Society 21, 485–494. and cultural practices on the population Walker, A.K. and Dietz, L.L. (1979) A review of densities of banana weevil Cosmopolites entomophagous insects in the Cook Islands. sordidus (Germar) and on banana yield. PhD New Zealand Entomology 7, 70–82. thesis, Kenyatta University, Kenya. Wallace, C.R. (1938) Measurement of beetle borer Uzakah, R.P. (1995) The reproductive biology, migration in banana plantations. Journal of the behaviour and pheromones of the banana Australian Institute of Agricultural Sciences 4, weevil, Cosmopolites sordidus Germar 215–219. (Coleoptera: Curculionidae). PhD thesis, Wardlaw, C.W. (1972) Diseases of the Banana and of University of Ibadan, Nigeria. the Manila Hemp Plant. Macmillan, London, Van den Enden, H. and Garcia, E.A. (1984) 615 pp. Reconocimiento del control natural del Waterhouse, D.F. (1993) The Major Arthropod Pests picudo negro del platano (Cosmopolites and Weeds of Agriculture in Southeast Asia. Aus- sordidus) Germar en la zona del gran Caldas. tralian Centre for International Agricultural Universidad Nacional Facultad de Agronomia, Research, Canberra, 141 pp. Manizales, Colombia, 114 pp. Waterhouse, D.F. and Norris, K.R. (1989) Cosmo- Varela, A.M. (1993) Report on a trip to Bukoba polites sordidus (Germar). In: Waterhouse, D.F. and Muleba districts (Kagera region) to assess and Norris, K.R. (eds) Biological Control: Pacific the possibility for biological control of banana Prospects. Inkata Press, Melbourne, Australia, weevil with ants. Unpublished manuscript. pp. 152–158. Agriculture Research Institute, Maruku, Woodruff, R.E. and Baranowski, R.M. (1985) Tanzania, 15 pp. Metamasius hemipterus (Linnaeus) recently Varma, P.M. and Capoor, S.P. (1958) Mosaic disease established in Florida (Coleoptera: Curcul- of cardamon and its transmission by the ionidae). Florida Department of Agriculture and banana aphid. Pentalonia nigronervosa Coq. Consumer Services Division of Plant Industry, Indian Journal of Agricultural Science 28, 97–107. Entomology Circular No. 272, 4 pp.

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56 C.S. Gold et al.

Yaringano, C. and Van der Meer, F. (1975) (Olivier). Acta Phytophylactica Sinica (China) 13, Control del gorgojo del platano, Cosmo- 195–199. polites sordidus Germar, mediante Zimmerman, E.C. (1968a) The Cosmopolites banana trampas diversas y pesticidas granulados. weevils (Coleoptera: Curculionidae; Rhyncho- Revista Peruana de Entomologia 18, phorinae). Pacific Insects 10, 295–299. 112–116. Zimmerman, E.C. (1968b) Rhynchophorinae of Zhou, S.F. and Wu, X.Z. (1986) Monitoring and southeastern Polynesia. Pacific Insects 10, control of banana borer Odoiporus longicollis 47–77.

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5. 6.

Banana Plate 1. Damage by banana weevil to banana corm (J. Peña). Plate 2. Cosmopolites sordidus, adult (R. Duncan). Plate 3. Banana weevil, larva (R. Duncan). Plate 4. Banana weevil adult infected with Beauveria bassiana (R. Duncan). Plate 5. Banana weevil larva infected by nematodes (R. Duncan). Plate 6. Severe damage to banana by banana rust thrips (B. Pinese). 7. 8.

10.

12.

11.

Banana Plate 7. Typical damage to mature banana by rust thrips (B. Pinese). Plate 8. Banana scab moth larva feeding on immature fruit (B. Pinese). Plate 9. Damage to banana by banana spider mite (B. Pinese). Citrus Plate 10. Citrus rust mite, Phyllocoptruta oleivora (J. Peña). Plate 11. Broad mite, Polyphagotarsonemus latus (DPI-Queensland). Plate 12. Oriental spider mites (DPI-Queensland). 13. 14.

15. 16.

18.

17.

Citrus Plate 13. Citrus leaves damaged by oriental spider mite (DPI-Queensland). Plate 14. Red scale Aonidiella aurantii on fruit (DPI-Queensland). Plate 15. Green coffee scale along midrib (DPI-Queensland). Plate 16. Longtailed mealybug (DPI-Queensland). Plate 17. Anagyrus fusciventris, a wasp parasite of longtailed mealybug (DPI-Queensland). Plate 18. Citrus blackfly Aleurocanthus woglumi (R. Duncan). 19. 20.

21. 22.

24. 23.

Citrus Plate 19. Citrus planthopper (DPI-Queensland). Plate 20. Citrus leafminer, adult (R. Duncan). Plate 21. Citrus leaves damaged by citrus leafminer (R. Duncan). Plate 22. Fruit piercing moth (DPI-Queensland). Mango Plate 23. Queensland fruit fly (G. Waite). Plate 24. Damage by mango seed weevil (G. Waite). 25. 26.

28.

27.

30.

29.

Mango Plate 25. Red-banded thrips (G. Waite). Plate 26. Mango scale (G. Waite). Plate 27. Pink wax scale, Ceroplastes rubens (G. Waite). Papaya Plate 28. Papaya fruit fly, Toxotrypana curvicauda, female (R. Swanson). Plate 29. Damage to green fruit by papaya fruit fly (J. Peña). Plate 30. Papaya scale, Philephedra tuberculosa (M. Shepard). 31. 32.

33.

36.

35. 34.

Papaya Plate 31. Damage to papaya leaves by two-spotted mite (J. Peña). Plate 32. Papaya leafhopper (R. Duncan). Pineapple Plate 33. Damage to pineapple roots by Meloidogyne (R. Bradley). Plate 34. Damage to pineapple by leathery pocket mite (G. Petty). Plate 35. Leathery pocket mite (G. Petty). Plate 36. Thrips affecting pineapple (G. Petty). 37. 38.

39. 41.

40.

42.

Pineapple Plate 37. Thrips damage to pineapple (G. Petty). Plate 38. Mealybug wilt to pineapple (G. Petty). Plate 39. Asthenopholis subfasciata, stages of white grub damaging pineapple (G. Petty). Plate 40. Symptoms of white grub injury to pineapple. Annona sp. Plate 41. Atemoya flower (H. Nadel). Plate 42. Carpophilus freemani, pollinating nitidulid (H. Nadel). 43. 46.

45. 44.

47.

48.

Annona sp. Plate 43. Annona montana flower (J. Peña). Plate 44. Annona muricata pollinating scarabs (J. Peña). Plate 45. Annona seed borer Bephratelloides cubensis (H. Nadel). Plate 46. Annona seed borer damage to atemoya (J. Peña). Plate 47. Cerconota anonella, adult (F. Garcia). Plate 48. Damage to fruit by Cerconota anonella (J. Peña). 49. 50.

52.

51.

54.

53.

Annona sp. Plate 49. Cratosomus bombinus, adult (Monica Barbosa-Pereira). Plate 50. Damage to branches by Heilipus velamen (Monica Barbosa-Pereira). Avocado Plate 51. Protopulvinaria pyriformis (M. Wysoki). Plate 52. Avocado lacebug, Pseudacysta perseae (J. Peña). Plate 53. Retithrips syriacus (M. Wysoki). Plate 54. Heliothrips haemorrhoidalis (M. Wysoki). 55.

56.

58. 57.

59. 60.

Avocado Plate 55. Heliothrips haemorrhoidalis damage (M. Wysoki). Plate 56. Conotrachelus perseae (N. Bautista). Plate 57. Heilipus laurii (N. Bautista). Plate 58. ‘Hass’ male flower at first dehiscence (stage D2). The stigma is dry, the nectaries secreting nectar (E. Lahav). Plate 59. ‘Reed’ female flower (stage B2). Field picture (A. Shuv). Plate 60. Honeybee collecting nectar from ‘Ettinger’ male flower (stage D2). Pollen accumulates on the ventral thorax. Field picture x 3.4 (A. Shuv). 61. 62.

64.

63.

65.

Avocado Plate 61. ‘Ettinger’ pollen grains organized into a honeybee’s pollen load. The pollen is not well packed and the pollen load tends to disintegrate. SEM x 50, the bar represents 100 µm (G. Ish-Am). Plate 62. The stingless bee Geotrigona acapulconis collecting nectar from ‘Hass’ female flower stage (stage B2), and holding the stigma by a leg. Field picture x 6.2 (G. Ish-Am). Plate 63. Avocado pollen packed to form pollen load on a Geotrigona acapulconis pollen basket. SEM x 50, the bar represents 100 µm (G. Ish-Am). Plate 64. The Mexican honey wasp Brachygastra mellifica collecting nectar from a male flower before dehiscence (stage D1). The anthers touch the wasp’s lateral thorax, ventral abdomen and legs. Field picture x 6.0 (G. Ish-Am). Plate 65. The fly Lucilla sericata (Calliphoridae) collecting nectar from ‘Reed’ female flower (Stage B2). Field picture x 7.0 (G. Ish-Am). 66. 67. 69.

68. 71.

70.

Guava Plate 66. Anastrepha suspensa, adult (R. Duncan). Plate 67. McPhail trap (W. Gould). Plate 68. Diachasmimorpha longicaudata (H. Glenn). Plate 69. Guava fruit protected against Caribbean fruit fly (R. Duncan). Minor fruits Plate 70. Hypomeces squamosus (A. Winotai). Plate 71. Conogethes punctiferalis (A. Winotai). 72. 73.

74.

76. 75.

Minor fruits Plate 72. Mudaria luteileprosa (A. Winotai). Plate 73. Durian mealybug infestation (A. Winotai). Plate 74. Phyllocnistis sp. mining rambutan leaf (A. Winotai). Plate 75. Conopomorpha spp. (A. Winotai). Plate 76. Conopomorpha damage (A. Winotai). 77. 78.

80.

79.

81.

Minor fruits Plate 77. Hyperaeschrella sp. (A. Winotai). Plate 78. Bactrocera sp. (A. Winotai). Plate 79. Aphids infesting carambola fruitlets (J. Peña). Plate 80. Acerola weevil (A. Hunsberger). Plate 81. Acerola weevil larva (A. Hunsberger). 82. 83.

84.

85.

86.

87.

Litchi, longan Plate 82. Damage to litchi by nut borer (G. Waite). Plate 83. Cryptophlebia adult (G. Waite). Plate 84. Green shield scale (G. Waite). Plate 85. Fruitspotting bug causing fruit fall (G. Waite). Plate 86. Erinose mite (G. Waite). Plate 87. Damage by erinose mite to flowers (G. Waite). 88.

89.

90. 91.

92. 93.

Passion fruit Plate 88. Pollination of Passiflora edulis yellow passion fruit by the carpenter bee, Xyolocopa spp. (E. Aguiar-Menezes). Plate 89. Adult of Agraulis vanillae vanillae (Lepidoptera: Nymphalidae) (E. Aguiar-Menezes). Plate 90. A. vanillae caterpillar feeding on leaves of yellow passion fruit (E. Aguiar-Menezes). Plate 91. Coreidae. Left: adult of Veneza zonatus; right: adult of Leptoglossus gonagra (E. Aguiar-Menezes). Plate 92. Anastrepha spp., a pest of passion fruit (E. Aguiar-Menezes). Plate 93. Immature yellow passion fruit damaged by fruit fly larvae (E. Aguiar Menezes). Color profile: Disabled Composite 150 lpi at 45 degrees

3 Tropical Citrus Pests

D. Smith1 and J.E. Peña2 1Department of Primary Industries, Maroochy Horticultural Research Station, Nambour, Queensland 4560, Australia; 2Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, FL 33031, USA

Introduction (major, occasionally important or minor) is used by Smith et al. (1997). Every citrus region Citrus is host to a large number of pests has an even more select group of key pests worldwide. Ebeling (1959) lists about 875 – three or four major pests dominating the insects and mites, albeit less than 10% are whole pest monitoring programme. Some of major importance. Talhouk (1975) lists 144 insects are key pests because they are vectors well known species. Warmer temperatures of serious diseases like greening or tristeza. and higher humidities usually result in there Major pests are those that occur most fre- being up to three times as many pests in quently (usually each season) and can the tropics in comparison with the higher seriously affect fruit yield or quality or tree latitude and Mediterranean climatic areas. health. They can have limited potential for Southern China, for example, has over 120 biological control. A grading of occasionally species of some significance (Anonymous, important means the pest occurs more 1975) as has India (Ghosh, 1990), while Japan sporadically, or causes less damage, while a has about 40 (Anonymous, 1981). Warmer pest of minor importance has the potential areas of South Africa have about 100 species to cause problems but is usually present in (Bedford et al., 1998) while Morocco has about small numbers. Secondary or induced pests 30 (Papacek, 1997). Northern and north east- are normally kept at a minor level by natural ern Australia also have about 100 species. Dry enemies but flare up when there is too much southern inland regions of Australia have disruption from broad spectrum pesticides. about 30 (Smith et al., 1997). Hemipterous pests (scales, mealybugs, aphids, whiteflies, leafhoppers) constitute 30–60% of the pests, Differences between tropical and higher followed by lepidoptera (fruit boring and latitude citrus growing areas and practices piercing moths, leafrollers, and leafminers), mites, beetles, bugs, flies, and thrips. Citrus A major difference between tropical citrus pests are classified according to the severity and citrus grown in high latitudes is the effect and frequency of attack and whether they of climate on tree phenology. Citrus growth attack fruit or other parts of the tree (Nasca in semitropical (latitude 26° N) to inter- et al., 1981). Some pests have a greater poten- tropical (23° N) areas is mostly governed by tial for control by natural enemies. Talhouk the amount of precipitation between winter (1975) classes the pests as major, occasional and summer and the alternance between pre- or of little importance and a similar system cipitation between the wet and the dry season

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 57

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58 D. Smith and J.E. Peña

rather than by changes in temperature, such losses, small farms cannot afford this type as those observed in the Mediterranean and of management (Verheij and Coronel, 1992). California, USA (Cassin, 1984). Tropical and Postharvest treatments, waxing, grading and intertropical citrus growing areas show major packing are less developed and more fruit differences among themselves in citrus is sold on domestic markets. Disease control varieties (Murata, 1997). In South-East Asia has an important role in all citrus areas but sweet orange, grapefruit and lemon are of even more so in the tropics and particularly little importance, while tangerines play a the Asian tropics where Asian greening is relatively large role in the region (Verheij and transmitted by the citrus psylla Diaphorina Coronel, 1992). In other tropical areas, there citri Kuwayama. For instance, because of are more oranges (many produced for juice) the marcotting system of propagation, many and pomelos and limes produced for both trees are already infested with greening even processing and fresh fruit (Ghosh, 1990). before planting out. Integrated pest manage- Tropical citrus production has grown, from ment (IPM) systems in the tropics have to 71 million t in 1980 to approximately 78 contend with control of important vector million t year−1 (FAO, 2000). In the tropics, pests such as citrus psylla. flowering and fruiting is less seasonally defined than in subtropical and temperate areas. In the latter, citrus species (other than Key Pests lemons) usually flower once a year except when stressed (e.g. by lack of water). Shoot Mites growth of most varieties in cooler areas occurs in distinct flushes with 50% of more in At least a dozen species of mites attack tropi- the spring flush. Autumn flushes produce cal citrus (Jeppson et al., 1975; Cermeli, 1983; vigorous shoots with large, wide leaves. In Atachi, 1991; Quiros-Gonzalez, 1996) (Table summer these shoots do not carry flowers 3.1). The species are classified within the except on lemons, or when it results in an Eriophyidae, Tarsonemidae, Tetranychidae out-of-season crop that is often of no eco- and Tenuipalpidae. nomic value. Management practices such as irrigation and fertilizer application can be Eriophyidae used to minimize summer/autumn vegetative growth. In the tropics, flushing is less DESCRIPTION, BIOLOGY, DAMAGE The citrus defined and is almost continual on some rust mite (CRM), Phyllocoptruta oleivora varieties. In some tropical areas, trees are (Ashmead), is the most important arthropod even encouraged to have several flowerings citrus pest worldwide (Browning et al., 1995). per season and the constant presence of Knapp et al. (1996a) report that this mite is a young fruit can make pest control much serious pest of citrus in most humid regions more difficult. Citrus farming practices also of the world. Other significant eriophyids on differ between the tropics and higher lati- citrus are: citrus bud mite, Eriophyes sheldoni tudes. Often there are more small orchards (Ewing) (worldwide); citrus grey mite, of 1–10 ha managed by a single family. Calacarus citrifolii Keifer (Transvaal, South Subsequently there is less mechanization and Africa); brown citrus rust mite, Tegolophus spraying equipment is less efficient. Financial australis Keifer (Queensland, Australia); and risk can pressure smaller growers into using the pink citrus rust mite, Aculus pelekassi chemical rather the biological options for pest Keifer (Japan). control. Propagation techniques for nursery According to Knapp (1983), the adult stock tend to be less stringent with regard to citrus rust mite is a yellow or light brown rootstock and budwood selection and nurs- mite and has an elongated, wedge-shaped ery production. Pest monitoring is practised body about three times as long as wide (Plate on an increasing number of larger orchards 10). The mite has two pairs of short anterior but less so in the many small orchards. While legs and a pair of lobes on the posterior end larger orchards need daily care to prevent which assist in moving and clinging to plant

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Tropical Citrus Pests 59

continued acuminata

signipennis

orientalis latus

aonidium viridis

fellis bella oleivora floridensis citri purchasi spiniferus citrella pests citricidus smithi Colgaroides bibax

citri spp. rubens viridis becki armigera citri

longulus albomaculatus spp., Icerya

Nipaeoccus Othreis sheldoni Eutetranychus Coccus important

Toxoptera Unaspis Ceroplastes Biprorulus Penthimeola Empoasca Chrysomphalus Planococcus Chaetanaphothrips scale Phyllocnistis Bruchophagus Phyllocoptruta Coccus Ceroplastes

Panonychus mite Helicoverpa Aleurocanthus Siphanta scale bug moths

Lepidosaphes spp. scale aphid scale Scirtothrips Polyphagotarsonemus scale mite thrips wasp mite mealybug mealybug scale

Eriophyes scale spider cushion citrus red wax scale coffee mite mite gall rust red mealybug leafhopper mealybug leafhopper leafminer rust snow occasionally blackfly citrus soft earworm piercing wax mite mite or Citrus Bud Citrus Citrus Oriental Broad Citrus Spherical Florida Cottony Spiny Black Citrus Long Green Pink Purple Citrus Spherical Planthoppers Citrus Spined Citrus Corn Fruit Scirtothrips Citrus Florida Broad Bud Citrus Iridomyrmex • Major • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

australis leucotreta world.

tryoni capitatia the of

aurantii

Ceratitis Tegolophus rosa

areas aurantii

Bactrocera erythreae

fly Cryptophlebia mite fly mite fruit moth

tropical Ceratitis Trioza rust Scirtothrips fruit

Aonidiella mite fly and spider citrus thrips psylla rust codling fruit scale scale pests Citrus Citrus Mediterranean Natal False Citrus Brown Oriental Red Red Queensland Key • • • • • • • • • • • subtropical in citrus of African), pests Territory phytophthora, Swaziland, phytophthora, melanose, mite (South scab, and Northern Transvaal, blackspot, lemon and greening blackspot, insect – – region spot, spot, Natal, – Important diseases diseases brown brown Mozambique Queensland leprosis Africa – 3.1. e l b alternaria tristeza, Important tristeza Important alternaria a Zimbabwe, Southern T Subtropical/tropical Australia

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60 D. Smith and J.E. Peña

articulatus floccosus

banksii neglecta

spp. sexmaculatus urticae coffeae citricidus

pests aurantii

pelikassi

hesperidum

praelonga

spp. Saissetia cinerea Selenaspidus oleae Aleurothrixcis

Saissetia spiraecola spp. Aculus

important Toxoptera

Paraleyrodes Toxoptera Tetranychus Eutetranychus Coccus scale

scale Eutetranychus scale

Orthezia mite scale Aphis whitefly mite aphid mite mite red scale

Saissetia aphid Parlatoria mite scale scale scale scale black rust mite mite Brevipalpus

Solenopsis cushion aphid whiteflies red red scale citrus citrus citrus mite mite snow orthezia woolly red red occasionally citrus scale scale Indian citrus scale scale brown spp. brown mite ants mites or Caribbean Soft Red Purple Florida Black Pink Chaff Red Citrus Citrus Six-spotted Broad Flat Two-spotted Florida West Black Soft Hemispherical Cottony Citrus Nesting Spiraea Brown Fire Citrus Texas Bud Broad Texas Citrus Atta • • • • • • • • • • • • • • • Major • • • • • • • • • • • • • • • • • • spp. spp.

phoenicis humile Diaprepes borer fly

Brevipalpus Homalodisca fruit

Linepithema aphid scale spp. rootstalk e.g. mite mite ant scale citrus rust snow leafminer leafminer rust mites, pests Argentine Sugarcane Citrus Citrus Citrus Brown Citrus Purple Mediterranean Sharpshooters Citrus Flat Anastrepha • • • • • • Key • • • • • • • brown scab, phytophthora xyloporosis citrus States variegated alternaria Colombia Gulf canker, melanose, and Peru, tristeza, leprosis, . – – phytophthora, citrus spot, region Florida Brazil, –

Continued greasy diseases diseases tristeza, America, xyloporosis, America 3.1. e l b Important exocortis, spot, Important chlorosis, a Central South T Subtropical/tropical

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Tropical Citrus Pests 61

continued

chinensis

citrifolii

cervinus

woglumi

cendani viridis citri dorsalis spp. zizyphus

Anoplophora

Dialeurodes spp. e.g. Asynonychus Coccus Othreis

Parlatoria Bactrocera whitefly Aleurocanthus Dialeurodes scale Eutetranychus moth aphid fly beetle borers, fly fly aphid scale aphid whitefly mite scale scale Adoxophyes scale fruit mite aphid rose scale wax red whitefly scale citrus coffee aphid mite mealybug mealybug whitefly black black mealybug whitefly citrus parlatoria citrus spiny parlatoria scale borer piercing wax brown mite mite Chaff Purple Pink Black Cerambycid Citrus Florida Citrus Citrus Cloudy-winged Woolly Citrus Melon Spiraea Fuller’s Florida Citrus Oriental Fruit Mussel Black Green Soft Citrus Brown Black Black Citrus Fruit Bud Six-spotted Black Broad Bud Oriental • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

citri dorsalis yanonensis

Unaspis

Diaphorina whitefly Scirtothrips mite mite mite mite scale psylla leafminer red rust spiny leafminer rust red psylla thrips scale scale Citrus Chilli Citrus Citrus Citrus Yanone Red Citrus Citrus Red Citrus Citrus Citrus • • • • • • • • • • • • • wilt, Bangladesh, citrus blackspot, gummosis Malaysia, sudden (Asian melanose, Burma, scab, greening, Thailand, spot, citrus Satsuma tristeza phytophthora, Asian yellowshoot black Indonesia, – – canker, Vietnam, Taiwan – exocortis, scab, tristeza, melanose, citrus diseases diseases Asia citrus Philippines, China, Pakistan Important canker, anthracnose, greening), anthracnose, phytophthora, Important Sarawak, India, South-East Southern

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62 D. Smith and J.E. Peña

dictyospermi

cryptus

squamosus humeralis pests

philippinensis neri rusci

occipitalis

Chrysomphalus sagittiferella important Hypomyces

Agrilus Pseudococcus scale citri

Rhynchocoris scale Aspidiotus Bactrocera

Ceroplastes gnidiella whitefly mite aphid fly fly scale aphid weevil bug borer Citripestis scale Prays scale fruit scale cushion aphid scale fruit spp. wax scale citrus mite mealybug mealybug bark stink whitefly woolly occasionally scale citrus scale borer eating brown moth mite wax or Citrus Citrus Cottony Chaff Oriental Papaya Leaf Citrus Citrus Yanone Oleander Purple Black Florida Soft Fig Citrus Citrus Brown Black Spiraea Bud Fruit Bud Dictyospermum Achaea Broad Two-spotted Cryptoblabes • • • • • Major • • • • • • • • • • • • • • • • • • • • • • • • fly fruit mite mite red leafminer rust scale pests Mediterranean Red Citrus Citrus Citrus Key • • • • • septaria phytophthora, . – region xyloporosis Mediterranean

Continued – diseases secco, mal 3.1. Africa e l b spot, Important a T Subtropical/tropical North

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Tropical Citrus Pests 63

surfaces. Egg deposition begins within a day 2–3 weeks throughout the fruit season. Fruit or two of the female reaching maturity and should be sampled at random representing continues throughout her life, about 20 days. the four quadrants of the tree (Bullock et al., The eggs hatch in about 3 days during sum- 1999). In Brazil, Gravena and Trevizoli (1984) mer months and immature mites undergo two found that a density of more than 70 mites moults, with each nymphal stage lasting from per cm2 was the threshold injury level for the 1 to 3 days during the summer (McCoy et al., citrus rust mite. An action level of 5–10% of 1988). young and old fruit infested with CRM could The citrus rust mite is found on leaves, be considered the action level in Australia fruits and young branches. Affected leaves (Smith et al., 1997). Knapp et al. (1996a) exhibit shallow yellow punctures, giving reported that the amount of citrus rust mite them a pale appearance similar to that blemish acceptable for fresh fruits varies in produced by Eutetranychus banksi McGregor Florida, generally it must not exceed 5% of (Ochoa et al., 1994). Various types of damage the surface area. However, citrus grown for can be seen in fruits according to whether processing can withstand up to 75% surface they were attacked early or late (McCoy and area damage before reduced fruit size and Albrigo, 1975). Attacks of P. oleivora on Citrus juice content and increased fruit drop become sinensis result in blackening or darkening evident. In Florida, USA, six CRM cm−2 is of the fruit. When the attack is early the fruit considered the threshold where pesticide is also smooth and opaque, whereas in late intervention would be required and ten CRM attack the blackening is shiny. The surface of cm−2 would be the action threshold where attacked fruit in C. limon, C. limettoides and treatment would be required as soon as C. aurantifolia takes on a smooth yellow brown possible (Bullock et al., 1999). to white appearance which is opaque in early attacks and shiny in late attacks. Occasionally, BIOLOGICAL CONTROL According to Brown- C. limon shows fine cracking. Effects of citrus ing et al. (1995) citrus rust mite is attacked by mite on fruit drop and tree growth have a complex of natural enemies, but generally been reported by Allen (1979). P. oleivora under Florida, USA conditions, beneficial population densities can fluctuate depending organisms are unable to consistently maintain on weather conditions or phenological tree rust mites below damaging levels. In Mexico, conditions, but some studies in the Neotropics an unidentified cecidomyiid appears to be indicate that temperature around 24.5°C and the major biological control agent (Ruiz, 1997) 30–90% RH favour its development. of P. oleivora and densities of the phytoseiid, Euseius mesembrinus (Dean) appear also to MONITORING AND ECONOMIC THRESHOLDS be correlated with increased densities of Monitoring methods for CRM have been P. oleivora and E. banksi (Ruiz-Cancino et al., developed by different authors (Yothers 1996). In Benin, the exotic phytoseiids and Miller, 1934; Allen and Stamper, 1979; (Amblyseius aerealis (Muma), Euseius concordis Hall et al., 1991, 1994; Peña and Baranowski, (Chant), Galendromus annectens (De Leon)) 1992; Smith et al., 1997). Action levels depend introduced against the cassava mite, Mono- on fruit size, percentage of fruit infested nychelus tanajoa (Bondar), are thought to have and predatory mite activity (Smith et al., potential against P. oleivora and E. sheldoni 1997). Nascimento et al. (1982) suggest that (Ewing) (Atachi, 1991). In Australia, Smith P. oleivora population levels can be estimated et al. (1997) and Smith and Papacek (1991) by collection of five leaves per plant. They report as the most important predators of can be assessed by counting the total number CRM the phytoseiids Euseius victoriensis of mites per leaf, counting the number of (Womersley), Euseius elinae Schicha, mites on 2.5 cm2 or using a brushing machine. Amblyseius herbicolus (Chant) and A. lenti- The efficacy of these three methods is similar ginosus Denmark and Schicha as well as (Oliveira et al., 1982). In Florida, CRM the pathogen, Hirsutella sp. Samson et al. monitoring should be initiated as soon as (1980) described the taxonomy of Hirsutella populations are detected and continue every thompsonii Fisher in Florida. Applications of

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64 D. Smith and J.E. Peña

H. thompsonii at 1010 conidia per plant are rec- processes, changes in growth intensity, flow- ommended in Cuba, when more than 25% of ering and yield may be observed. The most the fruits are infested (Otero et al., 1994). common change is a retardation of the growth of the organs of damaged plants. P. latus Tarsonemidae reduced the total leaf area and leaf water content of damaged lime and sour orange The broad mite, Polyphagotarsonemus latus plants in Florida (Peña and Bullock, 1994). (Banks) is an important pest of tropical citrus (Jeppson et al., 1975; Gerson, 1992) (Plate 11). INJURY LEVELS TO FRUIT Under greenhouse ± The broad mite has a longevity of 13.4 1.0 conditions, limes began to show damage 4–6 ± days for females and 12.0 2.4 days for days after infestation and severe damage males. The intrinsic rate of increase (rm)is to the fruit epidermis appears 12 days after 0.359, with a mean generation time of 10.34 infestation (Peña, 1990) or when lime fruits and net reproductive rate (Ro) 41.0 (Jones and are two-thirds mature (Smith et al., 1997). Brown, 1983; Vieira and Chiavegato, 1999). The potential for damage caused by P. latus ECONOMIC INJURY LEVELS Despite the econo- has become evident during the last two mic importance of P. latus, very few authors decades (Gerson, 1992). Attacks tend to be have determined the relationship between concentrated on the young leaves, and some- P. latus density and injury to citrus. Estimates times cause damage to specific plant parts, of economic injury levels can be obtained e.g. stems, flowers, fruitlets or tips of shoots using equations that describe the relationship (Nucifora, 1961; Costilla, 1980). Hot, humid between lime fruit surface damaged and weather during exposure to broad mite feed- broad mite days, and between percentage of ing seems to intensify the symptoms of dam- fruits damaged per tree and broad mite days. age (Brown and Jones, 1983). The principal Smith et al. (1997) recommend an action level symptoms of attack consist of deformation of 5% of the fruit infested, particularly in of the leaves and suberization of the floral coastal areas of Australia, or where predators buds, growing tips and fruit. Apparently, are absent. Peña (1990) uses the term broad P. latus mouthparts are unsuitable for effec- mite days and reported that in Florida the tive penetration of renitent tissues (Jeppson economic injury level per lime tree will fluctu- et al., 1975). Broad mite damage can be similar ate between 42 and 45 broad mite days for the in appearance to that caused by citrus spring and summer harvest, respectively. rust mite. The broad mite damage on citrus appears as a thin, silver-grey skin that can be easily scratched off (Smith et al., 1997). Its CHEMICAL CONTROL The economic injury feeding appendages are suitable for penetrat- level, as mentioned earlier, is extremely low. ing succulent tissues, but are quite incapable In particular, the rapid injury caused to fruits, of penetrating thick-walled, lignified, and leaves and flowers necessitates a treatment at often varnished tissues, such as are found in an early stage in population development to mature stems and leaves. Toxins injected dur- prevent excessive injury. Several acaricides, ing feeding, presumably of salivary origin, including cyclocompounds (e.g. propargite), cause alteration of normal tissue ontogeny in diphenyl compounds (e.g. dicofol), organic the host plant (Aubert et al., 1980). On limes, phosphates (e.g. carbophenothion) and natu- larger numbers of P. latus are found on ral avermectins have been found to be shaded parts of the fruit compared to the effective against broad mites (Bullock, 1978; stylar, peduncle and sunlit regions. This Schoonhoven et al., 1978; Peña, 1988). pattern may be due to the propensity of the mites to avoid sunlight, or to avoid parts of BIOLOGICAL CONTROL the fruit with low relative humidity (Peña Predators. Few studies have been conduc- and Baranowski, 1992). ted to investigate the suitability of broad mites As a consequence of damage to plant as targets for biological control. The potential tissue and disturbance of plant physiological of phytoseiid mites as predators has been

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Tropical Citrus Pests 65

reported for different areas and crops 100%. Since development of P. latus is (Moutia, 1958; Badii and McMurtry, 1984; positively related to relative humidities McMurtry et al., 1984; Hariyappa and between 75% and 90%, and development of Kulkarni, 1989). In Florida, six species of entomopathogenic fungi require between 90 predacious mites (four Phytoseiidae, one and 100% RH, fungi might offer another possi- Bdellidae and one Ascidae) were observed on ble way to reduce broad mite populations. lime fruits (Peña et al., 1989a; Peña, 1992a,b). Peña et al. (1996a) compared the toxicity of Typhlodromalus peregrinus (Muma) accounted Beauveria bassiana, Paecilomyces fumosoroseus for 72.4% of the predacious mites and and Hirsutella thompsonii and confirmed that outnumbered Typhlodromis dentilis (DeLeon), all isolates tested were able to infect P. latus Amblyseius aerelis (Muma), Galendromus under laboratory conditions. Under green- helveolus (Chant), Bdella distincta Baker and house conditions, despite significant mortal- Balock and Asca muma Hurlbutt. In Australia, ity of P. latus, a fungal epizootic was variable Euseius victoriensis is considered effective among performed tests. Failures of this nature in subcoastal areas as well as the are not uncommon when attempts are made ladybird Scymnus sp. The effectiveness of to use fungi as mycoacaricides. In this mite predators for controlling broad mite instance, the failure is most probably populations was demonstrated by Peña et al. related to fluctuation of relative humidity (1989a). In an exclusion experiment, popula- and temperature differences between envi- tion densities of P. latus increased in plots ronments where fungi are tested. The relative treated with pyrethroids immediately after humidities were very high (approaching the first insecticide application. During the 100%) in the Petri dish bioassay, but variable dry season, the percentage of damaged fruits (50–90%) in the whole-plant experiments. per tree was 3.2 and 3.65 times higher in predator-free plots than in plots with preda- Tenuipalpids tors. During the humid season, however, there were no significant differences between the Brevipalpus spp. feed on the exposed surface percentage of fruits injured per tree in the of citrus fruit, but are also found on the predator-free plots and plots with predators. undersides of leaves and green twigs (Smith Several factors could be responsible for this. et al., 1997). In Citrus aurantifolia, the fruit Since most of these mites are facultative shows off-white, irregular cracking, covering predators, the presence of other preferred up to 80% of the epidermis. In Honduras, prey species or food substrates might influ- this mite is associated with the citrus scab ence the predator mite response. Also, since pathogen Elsinoe fawcettii in the same host the broad mite has a short generation time (Ochoa et al., 1994). Ochoa et al. (1994) found (Jones and Brown, 1983), and fruit injury is attacks by Brevipalpus in conjunction with observed in 4 to 6 days (Peña, 1990), the ratio P. oleivora and the fungus Sphaceloma fawcettii. of predator to broad mite populations may Brevipalpus phoenicis (Geijskes) is consid- need to be higher than that observed. ered a key pest of citrus in Brazil (Gravena et al., 1995), particularly for the transmission of Pathogens. Pathogens have potential as virus-like leprosis to fruits and twigs. Gravena control agents of phytophagous mites, or et al. (1995) considered that adult mites are contribute to the natural regulation of mite the best transmitters of the virus, while young populations. Fungi infecting Tetranychidae forms are less efficient. Action thresholds and Eriophyidae have been documented by for tenuipalpids are higher than for other different researchers, but field applications mites. For instance, Smith et al. (1997) of fungi against mites have been carried out recommended an action threshold of 20% by few investigators, which indicates that fruit infested. the major constraints are the germination of spores and penetration of the fungus into the BIOLOGICAL CONTROL The predator Euseius mite, which are very poor at humidities below citrifolius is considered effective against B.

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66 D. Smith and J.E. Peña

phoenicis in Brazil (Gravena et al., 1995) and E. africanus produces fine stippling on E. victoriensis is important in Australia. the leaves, causing them to drop prematurely Amblyseius citri Vande-Merme and Ryke is a without turning brown. Heavy rain is a limit- predator in South Africa (Bedford et al., 1998). ing factor in the distribution of the species. Other species are citrus flat mite Injury by the Texas citrus mite is similar to that Brevipalpus californicus (Banks), ornamental produced by P. citri (Jeppson et al., 1975). Eggs flat mite Brevipalpus obovatus Donnuadic and of this species are found throughout the year Brevipalpus lewisi (McGregor) (Bedford et al., in Texas and low relative humidity and 1998). temperatures above 27°C are favourable for the development of the species (Jeppson et al., Tetranychids 1975). The oriental red mite feeds on the upper leaf surfaces, producing grey spots, and later Citrus red mite Panonychus citri (McGregor) is leaves have a chlorotic appearance. Infested a cosmopolitan species. Injury is character- leaves weaken and finally drop; twigs die, ized by light coloured (etched) areas called which results in bare trees. Injury is more stippling, which give a greyish or silvery severe in the autumn, especially under low appearance to the leaves or fruit (Knapp et al., soil water and humidity conditions. The lon- 1996a). P. citri densities on limes grown in gevity of adults is about 12 days in summer, southern Florida increase during spring and 14–18 days in the spring and autumn, and up early autumn (Peña and Baranowski, 1992). to 21 days during the winter (Jeppson et al., In Florida, the combined influence of 1975). The time of year populations peak undetermined numbers of citrus red mites and most injury occurs is largely determined and weather may result in heavy leaf drop, by prevailing temperatures and humidity. twig dieback and fruit drop (Knapp et al., This species seems to prefer sour lemon 1996a). However, the citrus red mite is not stock to sweet lemon, mandarin and orange. considered a problem during extremely hot, As with P. citri, phytoseiids are vital in dry weather in Australia (Smith et al., 1997). controlling many tetranychid species. In P. citri occurs throughout eastern and South- Australia the dominant phytoseiid is East Asia (Beattie, 1997; Beattie and Watson, E. victoriensis (Smith et al., 1997). In South-East 1997). In China, damage levels to the leaf of Asia species such as Amblyseius largoensis 20–30% resulted in yield losses. In the Guangz- (Muma) and Amblyseius longispinus (Evans), hou area, the economic injury level is reached Amblyseius deleoni (Muma and Denmark), in spring when 21 mites are recorded per ten- Amblyseius cinctus Corpuz and Rimando and der leaf (Tan et al., 1989). The predators, Ambly- Phytoseius hongkongensis Swirski and Shecter, seius newsami Evans and A. nicholsi Evans are are important. considered to respond to population build- up of P. citri in China. Phytoseiids are vital for biocontrol of P. citri wherever it occurs. Other significant tetranychids – Texas Scales citrus mite, Eutetranychus banksi (McGregor), African citrus mite, Eutetranychus africanus Scales are the most abundant and variable (Tucker), the oriental spider mite, Eutetrany- group of citrus pests (Bennett and Alam, chus orientalis Klein) (Plates 12 and 13) – are 1985; Quezada, 1989; Rose, 1990). They have important pests of citrus in the Americas, a tremendous host range and can settle on Africa and the Near East, Asia, Australia and citrus twigs, branches, trunk and fruits. South Africa, respectively (Charanasri et al., The families, Coccidae (soft scales) and 1988). The two-spotted mite Tetramychus Diaspididae (armoured scales) are the most urticae Koch occurs on citrus in some areas, important. Armoured scales tend to be more e.g. Australia (Smith et al., 1997). In the Philip- abundant on trees growing under adverse pines, Eutetranychus cendani Rimando appears conditions, or in situations unfavourable to be the most common tetranychid species to their natural enemies (see Tables 3.2 (Cendaña et al., 1984). and 3.3).

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Tropical Citrus Pests 67

Table 3.2. Common wasp parasitoids of soft scales on citrus (Prinsloo, 1984; Malipatil et al., 2000).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Coccophagus ceroplastae Ceroplastes rubens, Coccus viridis, Coccus Japan elongatus and Pulvinaria polygonata Taiwan C. lycimnia Coccus hesperidum and Coccus Unknown pseudomagnoliarum C. semicircularis C. hesperidum and C. pseudomagnoliarum (?) Europe C. pulvinariae C. hesperidum South Africa C. cowperi C. hesperidum Uganda C. catherinae Ceroplastes brevicauda South Africa Euryischomyia flavithorax C. hesperidum and C. viridis Unknown Encyrtidae Anicetus beneficus C. rubens Japan A. communis Ceroplastes destructor South and East Africa Anicetus C. destructor South Africa (= Paraceraptrocerus) nyasicus Diversinervus elegans C. hesperidum, C. destructor, Ceroplastes Ethiopia floridensis, Saissetia nigra and Saissetia oleae D. stramineus C. viridis Kenya Encyrtus aurantii C. hesperidum (?) Europe (= lecaniorum) E. infelix S. coffeae (?) Ethiopia Metaphycus lounsburyi S. oleae South Africa (= bartletti) M. helvolus C. hesperidum, S. oleae and South Africa C. pseudomagnoliarum Metaphycus sp. n. A S. oleae South Africa (Guerrieri & Noyes) (fomerly lounsburyi) M. varius C. rubens (?) Australia M. luteolus C. hesperidum California M. stanleyi C. hesperidum South Africa M. galbus C. hesperidum South Africa Microterys nietneri C. hesperidum South Africa Ceroplastes floridensis Unknown Eulophidae Aprostocetus ceroplastae C. destructor South Africa C. floridensis C. sinensis Pteromalidae Scutellista caerulea S. oleae (?) South/East Africa S. coffeae S. nigra C. rubens C. floridensis C. destructor C. sinensis Moranila california C. floridensis (?) Australia C. rubens Cryptochetidae Cryptochetum iceryae Icerya purchasi Australia

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68 D. Smith and J.E. Peña

Table 3.3. Common wasp parasitoids of armoured scales on citrus (Rosen and Debach, 1979; Prinsloo, 1984; Rosen, 1994; Noyes, 1998; Malipatil et al., 2000).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Aphytis chrysomphali Aonidiella aurantii and Aonidiella citrina Mediterranean A. columbi Chrysomphalus aonidum and Lepidosaphes beckii Australia A. holoxanthus C. aonidum China A. lepidosaphes Lepidosaphes beckii (?) China A. lingnanensis A. aurantii, L. beckii China/eastern Asia L. gloverii and Unaspis citri A. africanas A. aurantii South Africa A. yanonensis Unaspis yanonensis China Aphytis roseni Selenaspidus articulatus Kenya A. hispanicus Parlatoria pergandii ? Mediterranean A. proclia Chrysomphalus dictyospermi ? Mediterranean Encarsia citrina A. aurantii China/California A. citrina A. orientialis C. aonidum U. citri and L. beckii Chrysomphalus dictyospermi E. perniciosi A. aurantii (?) China U. citri Pteroptrix smithi C. aonidium China Encyrtidae Comperiella bifasciata A. aurantii China A. citrina China C. lemniscata A. orientalis China/South-East Asia Habrolepis rouxi A. aurantii South Africa

Armoured scales regions as citrus (Rose, 1990). Perhaps this is substantiated by the fact that many effective The most important armoured scale species parasitoids used against these scales are from attacking citrus have been listed by Ebeling those areas (DeBach, 1976). (1959). They are red scale Aonidiella aurantii (Maskell) (Plate 14), purple or mussel scale Red scale, Aonidiella aurantii (Maskell) Lepidosaphes beckii (Newman) and citrus snow scale Unapis citri (Comstock), also Florida red Red scale is a key pest in many subtropical scale Chrysomphalus aonidium (L.), dictyo- and temperate parts of the world, e.g. South spernum scale Chrysomphalus dictyospermi Africa, North Africa, Australia, California, (Morgan), Glovers scale Lepidosaphes gloverii Texas, Mexico and parts of South America (Packard), yanone scale Unaspis yanonensis (Bennett et al., 1976; Anonymous, 1984; Gill, Kuwana, West Indian red scale Selenaspidus 1988; Smith et al., 1997; Bedford et al., 1998). articulatus (Morgan), black parlatoria In the Asian tropics and subtropics (where Parlatoria zizyphi (Lucas), and chaff scale the scale originated) it is only occasionally Parlatoria pergandii (Comstock). Similarity of important and is usually controlled by armoured species caused some confusion and parasitoids – Aphytis spp., Comperiella misdirection at times in biological control bifasciata Howard and Encarsia spp. The main (Rose, 1990). The species of armoured scales Aphytis species in red scale are Aphytis in the genera Aonidiella, Chrysomphalus, melinus DeBach and A. lingnanensis Compere Lepidosaphes, Parlatoria, Pinnaspis and Unaspis and also A. africanus Quednow in South are believed to be native to the same Asian Africa (Luck et al., 1982; Dahms and Smith,

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1994; Smith et al., 1997). The key to obtaining parasitoids were introduced (Smith, 1978; control in these other regions has been the Rosen and DeBach, 1979; Rosen, 1994; introduction of these parasitoids. Chilocorus Browning et al., 1995). negritus has been a valuable predator in South Africa (Bedford et al., 1998). Purple scale, Lepidosaphes beckii (Newman)

LIFE CYCLE The adult female gives birth to Purple scale was the most abundant and 100–150 mobile young, called crawlers, at a injurious insect in Florida citrus prior to 1960 rate of two or three a day over a 6–8 week (Knapp et al., 1996a). It is troublesome where period. The crawlers emerge from under it has spread throughout the world, e.g. their mother’s scale cover, and search for a South Africa, Australia, California, Texas, suitable feeding site on leaves, shoots or fruit. Central and South America (Nasca et al., Crawlers wandering on the tree canopy can be 1981), but is a relatively minor problem in blown by the wind into neighbouring trees or eastern Asia, its probable centre of origin. orchards. Once a crawler settles, it inserts its Aphytis lepidosaphes Compere is the dominant mouthparts into the plant and starts feeding. It parasitoid and it appears also to have spread secretes a white waxy covering, and at this with its host worldwide (DeBach, 1971). stage is called a ‘whitecap’. After a period of It prefers a dense canopy, with infestations feeding and growth, the insect moults. The being heavier at the centre of the tree and on cast skin is attached to the scale cover, giving the north and northeast quadrants. the cover its typical red colour. The development stage and sex of red scale can be deter- Citrus snow scale, Unaspis citri (Comstock) mined by the shape and size of the scale cover. After the second stage, scales can be identified Citrus snow scale is the most economically as male or female. The scale cover of males is important pest in Florida since 1960 (Knapp elongated, while the scale cover of females et al., 1996b), but is considered of low is circular. importance in South America (Mosquera, The male develops through a prepupal 1979). It had a major pest ranking in and pupal stage under a scale cover, before Queensland, Australia (Smith et al., 1997). emerging as a delicate, winged insect. It is Citrus snow scale attacks the trunk and large attracted to the female by a pheromone, and limbs of the tree, leaves and fruits are infested dies after mating. In first-stage and second- only after the main branches. Natural stage females, and in third-stage (i.e. adult) enemies including Telsimia sp., Chilocorus unmated females, the scale cover is not cacti L. (Coccinellidae), Encarsia spp., Aphytis attached to the body of the scale. When first- lignanensis Comp. (Hong Kong strain) are stage and second-stage females are moulting, mentioned by several authors (Brooks, and when third-stage females have the scale 1964; Quezada, 1989; Browning et al., 1995). cover it is attached to the body of the scale. Coronado and Ruiz (1996) list Encarsia spp. In the tropics there are six or seven as the most important parasitoid of U. citri generations per year in comparison with two in Mexico. In southern China, Encarsia to four generations in higher latitudes. inquerenda (Silvestri) is an important parasitoid and Aphytis debachi De Bach also Florida red scale, Chrysomphalum occurs. Good biocontrol of the scale has been aonidum (L.) achieved in Queensland with the predator Chilocorus circumdatus Gylenhall (of Chinese Florida red scale is also normally a minor pest origin) (Smith et al., 1995). in eastern Asia (the centre of its origin) being controlled by Aphytis holoxanthus (DeBach) and also Pteroptrix smithi Compere. Trans- Yanone scale, Unaspis yanonensis Kuwana ported around the world it became a major pest in many areas, e.g. Israel, Australia, Yanone scale replaces U. citri as an occasion- Florida, Mexico, until one or both of these ally important pest in China, Taiwan and

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Japan but is normally controlled by Aphytis LIFE CYCLE Male soft brown scales are rare. yanonensis (Rosen and DeBach, 1979). Females can reproduce without mating, and give birth to a total of about 200 live young Glovers scale, Lepidosaphes gloveri (Packard) (crawlers). The life cycle takes approximately 2 months in summer. Development within Glovers scale is reported as a serious pest of generations is not synchronized, i.e. various limes in Cuba, particularly in areas with an stages are present at any given time, and the average temperature of 25–29°C and relative generations overlap. humidity fluctuating between 70 and 75%. In Mexico, the introduction of A. lepidosaphes SEASONAL HISTORY In eastern Australia, Compere in the 1950s reduced the levels of there are four or five generations per year but infestation of this species (Ruiz, 1997). three or four generations per year in southern Rufous scale is a serious pest of citrus in areas (Smith et al., 1997). Peru and occurs in the West Indies (Guerrero, 1969; Beingolea, 1994). The parasitoid Aphytis HABITS Adult soft brown scales infest roseni DeBach and Gordy was successfully leaves and twigs, and occasionally green introduced from Kenya in 1971. fruit. The scales produce large amounts of honeydew, resulting in the growth of sooty mould. The honeydew also attracts ants, Soft scales which can interfere with biological control. Newly hatched crawlers move on to younger The main soft scale pests occur in the growth and the stalks of fruit. Young scales following genera: (i) Coccus – soft brown scale move around until they are half-grown, and Coccus hesperidum L, green coffee scale Coccus then migrate towards leaves and small green viridis (Green) (Plate 15), citricola scales, twigs where they settle and reproduce. Coccus pseudomagnoliarum (Kuwana), long The main natural enemies in Australia are soft scale Coccus longulus (Douglas); (ii) Metaphycus spp., Coccophagus spp., Microterys Saissetia – black scale Saissetia oleae (Olivier) flavus and Diversinervus elegans. Predators and hemispherical scale Saissetia coffeae include ladybirds like Rhyzobius spp. and lace- (Walker); (iii) Ceroplastes – pink or red wax wings (Smith et al., 1997). scale Ceroplastes rubens Maskell, white wax Details on life cycle, characteristics, dis- scale Ceroplastes destructor Newstead, Florida tribution, economic importance and damage wax scale Ceroplastes floridensis Comstock, caused by these scales are reported in hard wax scale Ceroplastes sinensis Del Browning et al. (1995), Hammon and Williams Guercio, fig wax scale Ceroplastes rusci L., (1984) and Smith et al. (1997). Soft scales are citrus wax scale Ceroplastes brevicacuda soft-bodied and have no separate protective Hall, barnacle scale Ceroplastes cirripediformis covering, but the body is usually protected Comstock; (iv) Pulvinaria – soft green scale with a thick waxy or mealy secretion. Soft Pulvinaria aethiopica (De Lotto), cottony citrus scales produce large amounts of sugary honey- scale Pulvinaria polygonata Cockerell, green dew. The main economic damage caused by shield scale Pulvinaria psidii Maskell and soft scales is from downgrading of fruit qual- orange pulvinaria Pulvinaria aurantii ity due to sooty mould fungus growing on Cockerell; (v) Protopulvinaria – pyriform scale the honeydew (Smith et al., 1997). Soft scales Protopulvinaria pyriformis Cockerell; and (vi) usually infest fruits, leaves and young twigs. Icerya – cottony cushion scale Icerya purchasi Heavily infested plants can lose vigour and Maskell (Ben-Dov, 1993; Browning et al., 1995; become unproductive as foliage becomes cov- Smith et al., 1997). ered in sooty mould. The honeydew attracts ants which defend the scales against natural Soft brown scale, Coccus hesperidum L. enemies causing disruption and aggravating the scale problem. Soft brown scale typifies a species that has Natural enemies (particularly encyrtid become cosmopolitan in its distribution. parasitoids) are extremely important in

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biological control of soft scales. The main frequently applied to lime orchards (Peña and encyrtid genera involved are Metaphycus, Baranowski, 1992). In Australia, the spring Anicetus, Microterys and Diversinervus. The generation of crawlers of Pseudococcus calceo- pteromalids Scutellista caerulea and Moranila lariae migrate to young fruit in late November spp., the eulophid Tetrastichus ceroplastae and and early December (Smith et al., 1997). P. citri the aphelinid Coccophagus spp. are also impor- occurs at low levels due to the combined tant (Smith et al., 1997; Malipatil et al., 2000). actions of the ladybeetle predator, Crypto- Coccinellids and chrysopids also play an laemus montrouzieri (Mulsant), several para- important role, the most notable case being the sitic wasps and a fungal disease (Browning ladybird Rodolia cardinalis Mulsant for cottony et al., 1995). Besides the mealybug ladybird, cushion scale (Bennett et al., 1976). the encyrtid Leptomastix dactylopii Howard There are one or two orthezid citrus pests and the lacewings, Oligochrysa lutea (Walker), including Orthezia praelonga Douglas that are Micromus sp., and Mallada signata are con- found on the leaves, branches, flowers and sidered important as natural enemies of the trunk occurring in Central and South America citrus mealybug in Australia (Waterhouse, including Colombia (Garcia Roa, 1995). The 1988; Smith et al., 1997). The encyrtid wasps most effective natural control agents are Tetracnemoidea brevicornis (Girault) and the predators Hyperaspis sp. (Coccinellidae), Anagyrus fusciventris (Girault) are major Ambracius dufouri, Proba vittiscutis (Miridae) parasites of P. calceolariae in southeastern and Chrysopa sp. Use of oils and soap helps to Australia (Table 3.4), while the aphelinid reduce damaging populations. wasp Coccophagus gurneyi Compere is more important on the east coast of Australia (Smith et al., 1997). Members of the encyrtid genus Mealybugs Anagyrus (Plate 17) are important parasitoids of mealybugs, e.g. Anagyrus pseudococci (Girault) in P. citri and Anagyrus agraensis The main mealybug pests of citrus include Saraswat in N. viridis. Pseudaphycus flavidulus citrus mealybug Planococcus citri (Risso), citro- (Brethes) and Leptomastix epona Noyse philous mealybug Pseudococcus calceolarie parasitize P. viburni (Ripa and Rodriguez, (Maskell), longtailed mealybug Pseudococcus 1999). Coccidoxenoides peregrinus (Timberlake) longispinus (Targioni and Tozzetti) (Plate 16), attacks first instar P. citri. Pseudococcus cryptus Hempel, Pseudococcus citriculus Green, spherical mealybug Nipae- coccus viridis (Newstead), tuber mealybug Pseudococcus viburni (affinis) (Maskell), Citrus whiteflies and blackflies comstock mealybug Pseudococcus comstocki Kuwana and oleander mealybug Paracoccus About 30 species of citrus whiteflies and burnerae (Brain) (Knapp et al., 1996; Smith blackflies have been reported throughout the et al., 1997; Bedford et al., 1998). The life cycle world, out of which a number of species like of mealybugs is similar to that of soft scales, citrus spiny whitefly Aleurocanthus spiniferus feeding on plant sap, and excreting honey- Quantaince, citrus blackfly Aleurocanthus dew. woglumi Ashby (Plate 18), cloudy winged The citrus mealybug is often encountered whitefly Dialeurodes citrifolii (Morgan), citrus in sheltered locations on the citrus tree, such as whitefly Dialeurodes citri (Ashmead), Dial- cracks, folds in leaves, and in fruit clusters eurodes elongata Dozier and citrus woolly or under fruit buttons (Browning et al., 1995). whitefly Aleurothrixus floccosus (Maskell) are Citrus mealybug feeding on fruit surfaces considered important in several tropical cit- may result in discoloration and severe rus areas (Ghosh, 1990). The Australian citrus infestations may cause fruit drop. whitefly Orchamoplatus citri (Takahashi) is In Florida, increases of P. citri are a minor pest in Australia. Details on the observed during summer and autumn, often life history and damage of Dialeurodes citri corresponding to periods when pesticides are (Ashmead), D. citrifolii and Paraleyrodes spp.

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72 D. Smith and J.E. Peña

Table 3.4. Common wasp parasitoids of mealybugs on citrus (Prinsloo, 1984; Noyes, 1998; Malipatil et al., 2000).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Coccophagus gurneyi Pseudococcus calceolariae Australia Encyrtidae Anagyrus agraensis Nipaecoccus viridis (?) North Africa A. fusciventris Pseudococcus longispinus Australia P. calceolariae A. pseudococci P. citri Mediterranean Coccidoxenoides peregrinus P. citri China Leptomastidea abnormis P. citri Mediterranean Leptomastix dactylopii P. citri Brazil (or Africa?) Tetracnemoidea brevicornis P. calceolariae Australia P. longispinus T. peregrina P. longispinus (?) South America P. calceolariae T. sydneyensis P. longispinus Australia P. calceolariae Pseudaphycus flavidulus Pseudococcus viburni (affinis) Chile P. maculipennis P. viburni Europe Leptomastic epona P. viburni Europe Pteromalidae Ophelosia spp. P. calceolariae Unknown Platygasteridae Allotropa sp. P. calceolariae China

are given by Browning et al. (1995). Most months on the leaves, which, in turn, serves as adults of citrus whiteflies and blackflies an excellent refuge for scales (Watson, 1915). congregate on young leaves, where they lay A. floccosus is also considered to be a potential eggs on the underside of the leaves; nymphs vector of plant viruses and virus-like organ- are regularly found on older leaves on isms that cause plant diseases and associated the middle and bottom tree canopy. The life disorders (Bird and Maramorosch, 1978). history, seasonal abundance and host range of A. floccosus has been determined by Salinas BIOLOGICAL CONTROL The main parasites of et al. (1996) in the Philippines. This species whitefly occur in the Aphelinidae – Encarsia is known as the woolly whitefly, a name spp. and Eretmocerus spp. also Cales spp. and derived from the wool-like filaments that Amitus spp. (Platygasteridae) (Clausen, 1978) develop in the third nymphal instar of the (Table 3.5). Ladybirds, lacewings and fungi insect (Watson, 1915). The nymphs of this (Aschersonia) are also important. Encarsia species are smaller than Aleurodicus sp. More opulenta (Silvestri) is important on citrus D. citrifolli (Morgan) were observed in Florida blackfly, E. lahorensis (Howard) on citrus on new flushes than on the old ones. whitefly, E. variegata on nesting whitefly Common density peaks are observed from (Browning et al., 1995). The introduction of early autumn through early winter (Peña and Amitus hesperidum Silvistri and E. opulenta Baranowski, 1992). (Silvestri) to Florida is probably responsible for the reduction of A. woglumi (Ashmead) DAMAGE Whiteflies inflict their damage densities (Browning et al., 1995). by sucking sap, excreting honeydew, which A. spiniferus is a minor pest of citrus in favours the growth of sooty moulds that Taiwan, but it can also cause the reduction of interfere with photosynthesis, and producing yield when population is high. There are six a dense mat of woolly material that persists for generations of the spiny blackfly in a year.

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Table 3.5. Common wasp parasitoids of whiteflies and blackflies on citrus (Clausen, 1978; Browning et al., 1995).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Eretmocerus series Aleurocanthus woglumi and Aleurocanthus spiniferus Malaysia E. portoricensis Aleurothrixus floccosus E. haldemani A. floccosus Cales noaki A. floccosus, Paraleyrodes sp. and Orchamoplatus citri Encarsia smithi A. woglumi Japan A. spiniferus E. clypealis A. woglumi and A. spiniferus India E. opulenta A. woglumi and A. spiniferus South Asia E. merceti A. woglumi Encarsia spp. Orchamoplatus citri and Paraleyrodes sp. Australia E. lahoriensis Dialeurodes citri Pakistan Platygasteridae Amitus hesperidum A. spiniferus and A. woglumi India, Pakistan A. spiniferus A. floccosus

Three natural enemies of this blackfly are a raise their body upward. The nymphs are predacious drosophilid, Acletoxenus sp., and orange-yellow in colour, flattened and cir- two parasitic wasps, Encarsia smithi (Silv.) cular in shape. The eggs are anchored by and A. hesperidum; however, they were not means of a short stalk embedded in the plant considered very effective. Several entomo- tissues. Females can lay more than 800 eggs. pathogenic fungi infecting this blackfly, e.g. Nymphs pass through five instars. Total Aschersonia spp. and Aegerita webbneri Fawc., life cycle requires from 15 to 47 days, depend- were found in the wet season. The number of ing upon the season. Adults may live for eggs laid per female averaged 19 (Chien and several months. For more information on Chiu, 1986). life history see Husain and Nath (1927), Atwal et al. (1970), Catling (1970), Capoor Citrus psyllids et al. (1974). The eggs of T. eritreae are elongate pear The psyllid vectors of Asian greening disease shape, and about 0.3 mm long; yellow when Diaphorina citri Kuway and African greening first laid, turning brownish. They are usually Trioza eritreae (Del Guercio) are considered a laid on the edges, or main veins, of very young most important threat to citrus in different leaves, being anchored to the leaf blade by a tropical areas of the world (Aubert et al., 1980; short appendage. Hatching takes about 5–6 Nariani, 1981; Van den Berg et al., 1991). The days. There are five nymphal instars, and the citrus psyllid D. citri is widely distributed whole nymphal period occupies 2–3 weeks. and important in Asia (Atwal et al., 1970; Females may live for a month and lay about Broadbent et al., 1980; Aubert and Quilici, 600 eggs (Hill, 1975). The historical review of 1983; Beingolea, 1988; Tandom, 1997) while T. infestations of T. erytreae is provided by Van eritreae is indigenous to Africa, where it is Den Berg and Fletcher (1988). found in many countries as well as on the Islands of St Helena, Mauritius, Madagascar DAMAGE The damage is caused by the and Réunion (Mamet, 1955; Breniére and nymphs and adults sucking sap from buds Dubois, 1965; CIE, 1967; Moran and Brown, and leaves (Tandom, 1997) and transmitting 1973; Etienne, 1978). Diaphorina citri are the organism that causes greening disease brown to light brown (black in Trioza erytreae) (Mead, 1977). Greening was first considered a (Mead, 1977) actively flying insects and mea- viral infection, but later the causal agent was sure 3–4 mm in length. While at rest, they identified as a phloem-restricted intracellular

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bacterium (Evers and Grisoni, 1991). The two In Réunion, the impact of T. erytreae and strains of greening are associated with each D. citri was reduced through releases of the vector, the African and the Asian, and are not parasites Tetrastychus dryi Waterston, Tetra- adapted to the same range of temperature stychus radiatus Waterston, and the encyrtid (Bove et al., 1974). The mechanical damage by Diaphorencyrctus aligarhensis (Shafee, Alam these psyllids leaves the leaves conspicuously and Agarwal) (Aubert and Quilici, 1983). pitted, the pits opening to the lower leaf surface. In severe attacks the leaf blades are PLANT RESISTANCE In India, of 20 species and cupped or otherwise distorted and yellow in cultivars tested for their reaction to greening, colour, especially when young (Hill, 1975). sweet lime was resistant alone or as rootstock There is no systematic data available on extent for mosambi orange. Italian, Eureka and of damage; however, D. citri has been reported Lisbon lemon were tolerant and showed causing loss of US$1.04 million in India mild symptoms (Nariani, 1981). (Tandom, 1997). Trees severely affected by the South African or heat-sensitive race of the IPM STRATEGY In India, at the initiation of greening disease are badly stunted and new flush, sprays of monocrotophos (0.025%) produce crops of predominantly greened, or dimethoate (0.03%) are delivered at a 10–12 worthless fruit. These fail to ripen and cannot day interval (Bindra et al., 1974; Nariani, 1981; be used for processing as they impart an objec- Tandom, 1991b). For effective management, tionable flavour which may taint large vol- pruning infested shoots and their destruction, umes of juice (Van Den Berg and Fletcher, maintaining orchard sanitation, and applica- 1988). The importance of greening in South tion of 1% pongamia oil and 4% neem oil Africa was emphasized when approximately at 21 and 7 day intervals is recommended 100,000 sweet orange trees were rendered (Tandom, 1997). Careful integrated biological commercially unprofitable by the disease. and chemical suppression of the psylla vector The South African greening disease was also is considered the most practical entomological partly responsible for the collapse of citrus method for containing greening disease on production in Réunion and Mauritius (Van mature trees (Samways, 1987). Den Berg and Fletcher, 1988). Nariani (1981) suggests an integrated control schedule incorporating use of disease- MONITORING T. erytreae was found to be free or heat-treated budwood, injection with highly attracted to yellow surfaces, particu- tetracycline antibiotics, insecticide sprays and larly fluorescent yellow-green (about 530 nm) use of tolerant rootstocks to reduce disease in citrus orchards in South Africa (Samways, losses. On the other hand, Aubert et al. (1980) 1987). Water pan traps painted with yellow suggested the use of disease-free nursery are also used successfully to trap other stock, introduction of hymenopterous para- psyllids (Omole, 1980). Yellow cards were sitoids and use of antibiotics as the best action useful to detect immigrant infestations of against psyllids and the greening disease. T. erytreae from adjacent vegetation into citrus orchards (Van den Berg et al., 1991).

BIOLOGICAL CONTROL Several species of Aphids predators have been reported feeding on eggs and nymphs of citrus psylla. The spider, Worldwide, 16 species of aphids are reported Marpissa tigrina Tikader is considered one of to feed regularly on citrus (Halbert and the most important predators of this pest in Brown, 1996). Aphids infest citrus blossom India (Sadana, 1991). Besides these, four and young growth. Of these species, four species of parasitoids have been reported are found consistently in Florida groves, from India (Tandom, 1991a) and up to 15 including cowpea aphid Aphis craccivora from the Asian Pacific region (Etienne, 1978; Koch, cotton or melon aphid Aphis gossypii Waterhouse, 1998; Tang and Aubert, 1990) Glover, spiraea aphid Aphis spiraecola Patch, (Table 3.6). black citrus aphid Toxoptera aurantii (Boyer

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de Fonscolombe) and more recently brown provided by Michaud (1998). It is currently citrus aphid Toxoptera citricida (Kirkaldy). distributed in South-East Asia, Africa south The brown citrus aphid (BrCA), is the ofthe Sahara, Australia, New Zealand, the most important vector ofcitrus tristeza virus Pacific Islands, South America, the Caribbean (CTV) because of its high vector efficiency, Islands, Central America and, most recently, especially for severe strains (Meneghini, 1946; Florida (Carver, 1978; Yokomi et al., 1994; Costa and Grant, 1951; Yokomi et al., 1994). An Halbert and Brown, 1996). One ofthe most extensive bibliographical review ofBrCA is devastating citrus crop losses ever reported

Table 3.6. Common wasp parasitoids of psyllids, aphids, planthoppers and leafhoppers on citrus (Clausen, 1978; Prinsloo, 1984; Tang and Aubert, 1990; Smith et al., 1997; Waterhouse, 1998).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Aphelinus gossypii Toxoptera citricidus, T. aurantii Australia, Hawaii Aphis spireacola Aphis gossypii A. spireacola A. gossypii Centrodora scolypopae Scolypopa australis Australia C. penthimiae Penthimiola bella South Africa Braconidae Lysiphlebus testaceipes A. spireacola California T. aurantii A. gossypii and T. citricidus L. japonica T. citricidus Japan L. fabarus T. citricidus, T. aurantii and A. gossypii Turkey India Aphidus colemani T. citricidus, T. aurantii and A. gossypii Lepolexis scutellaris A. gossypii and A spireacola India Binodoxiys spp. A gossypii India Aphidius matricariae T. aurantii Platygasteridae Aphanomerus spp. Colgar peracutum, Colgaroides acuminata Australia and Siphanta spp. Eulophidae Tamarixia radiata Diaphorina citri India T. dryi Trioza erytreae South Africa Encyrtidae Achalcerinys spp. C. peracutum Australia Psyllaephagus pulvinatus T. erytreae South Africa Ooencyrtus spp. C. peractum Australia C. acuminata Siphanta spp. Diaphorencyrtus aligarhensis D. citri Southeastern Asia Mymaridae Stethynium nr. empoascae E. Smithi Australia Anagrus baeri Empoasca smithi Australia Chaetomymar lepidius P. bella South Africa C. gracile P. bella South Africa Elasmidae Elasmus zehntneri P. citrella Philippines, Java Braconidae Microbracon phyllocnistoides P. citrella Indonesia Bracon sp. P. citrella Philippines

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followed the introduction of BrCA into Brazil, and mango planthopper Colgaroides acuminata Argentina and Venezuela (Carver, 1978; Roca- (Walker) produce copious honeydew with Peña et al., 1995). BrCA is considered larger resulting sooty mould (Smith et al., 1997). The than the other species of aphids occurring jassids or leafhoppers, particularly Empoasca in citrus (Halbert and Brown, 1996) and its spp. and also (in South Africa) citrus leaf- identification is difficult because most adult hopper Penthimiola bella (Stal.), suck maturing wingless forms of aphids are shiny black, and fruit causing multiple oleocellosis-like spots nymphs are dark reddish brown. A field key (Smith et al., 1997; Anonymous, 1984; Bedford to adult wingless forms of BrCA is provided et al., 1998). by Halbert and Brown (1996). The life cycle of Mymarid wasp egg parasitoids are BrCA is anholocyclic, meaning that there is no important natural enemies of leafhoppers and sexual cycle in the autumn, and thus no males, the aphelinid Centrodora penthimiae Annecke no oviparae and no eggs (Komazaki, 1987); parasitizes P. bella. The encyrtids Alchalcerinys nymphs mature in 6–8 days at temperatures of sp., Ooencyrtus spp. and Aphanomerus spp. are 20°C or higher (Komazaki, 1987) and the total important egg parasitoids of planthoppers life cycle can take as little as 1 week (Smith and dryinid wasps and strepsiptera parasitize et al., 1997). the nymphs and adults (Smith et al., 1997). Citrus is propagated vegetatively, which greatly increases the possibility for spreading the phloem-limited virus because CTV is graft Lepidoptera pests transmissible. Thus, the first step in any management programme should be to ensure that budwood and nursery stock are free of disease The main groups of lepidopterous pests (Halbert and Brown, 1996). Another aspect are: fruit borers (mainly tortricids but also of cultural control is inoculum suppression, pyralids and blastobasid larvae); leafminers or destruction of abandoned or volunteer notably citrus leafminer Phyllocnistis citrella crop plants that become reservoirs of pests Stainton; leafrollers (mainly tortricids); fruit and disease (Bishop et al., 1992; Plumb and piercing or sucking moths (mainly Othreis Johnstone 1995). spp. and Oraesia spp.); citrus butterflies (Papilio spp.); and flower or bud moths (Prays spp.). The false codling moth Cryptophlebia NATURAL ENEMIES Aphid parasitoids include Aphidius spp. and Aphelinus spp. A wide range leucotreta Megre is important in South Africa of predators occur, e.g. in Australia (Smith (Bedford et al., 1998). The carob moth Ecto- et al., 1997). Chilomenes lunata (F) is important myclois ceratoniae (Zeller) is a minor pest in in South Africa (Bedford et al., 1998). A range the Mediterranean and in Africa. American of predators attack citrus aphids. These bollworm or corn ear worm Helicoverpa armi- include ladybirds, e.g. the transverse ladybird gera (Hubner) is a sporadic pest, e.g. in South (Coccinella transversalis), the common spotted Africa and eastern Australia and South-East ladybird (Harmonia conformis), Harmonia Asia. Citrus flower moth Prays citri (Milliere) testudinaria, the variable ladybird (Coelophora is distributed worldwide. Adoxophyes spp. inaequalisi), and the yellow-shouldered are occasional pests in South-East Asia ladybird (Scymnodes lividigaster); syrphid and Australia. Table 3.7 lists the important flies, e.g. the common hoverfly (Simosyrphus parasitoids of lepidopteran citrus pests. grandicornis); and lacewing larvae. Citrus leafminer

The citrus leafminer Phyllocnistis citrella was Planthoppers and leafhoppers first noted in South-East Asia in 1856 and slowly dispersed to Japan (1927), Korea, These include flatids and jassids (Plate 19). Philippines (1915), Australia (1918), East The flatids or planthoppers, e.g. Siphanta spp., Africa (1967) and West Africa (1970). Since citrus planthopper Colgar peracutum (Walker) 1993, this insect has infested most other citrus

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Table 3.7. Common wasp parasitoids of other lepidoptera on citrus (Smith et al., 1997).

Parasitoids Main hosts on citrus Origin of parasitoid

Encyrtidae Ooencyrtus spp. Papilio spp. and Othreis spp. Worldwide Braconidae Apanteles spp. Cryptophlebia leucotreta, Tortrix spp., Worldwide Papilio spp. Dolichogenidea arisanus Epiphyas postvittana Worldwide Microplitis spp. Helicoverpa armigera and H. punctigera Worldwide Trichogrammatidae Trichogramma spp., e.g. pretiosum H. armigera, Tortrix spp., C. leucotreta Worldwide and E. postvittana Chalcididae Brachymeria spp. Tortrix spp. Worldwide Pteromalidae Pteromalus puparium Papilio spp. Worldwide Eulephidae Euplectrus kurandaensis Tiracola plagiata Worldwide Scelionidae Telenomus spp. H. armigera and Othreis spp. Australia Ichneumonidae Phytodietus sp. Isotenes miserana Australia Xanthopimpla sp. E. postvittana Australia

producing areas of the world. The first infes- resistant species was mandarin and the most tation of the Americas occurred in Florida, susceptible was lime. USA, followed by Mexico and the Caribbean region, the Mediterranean region, Central RELATIONSHIP BETWEEN P. CITRELLA INJURY AND America, the Near East countries and lately PLANT PHENOLOGY P. citrella injury to the most countries of South America. It is a plant causes reduction of the leaf surface common pest on citrus in South-East and area responsible for capturing energy for eastern Asia and in some areas is heavily tree growth. In heavy populations, leafminer sprayed. It tends to aggravate injury from larvae prevent newly emerging leaves from citrus canker. expanding fully, causing leaves to remain curled and twisted (Plate 21). Very few studies BIOLOGY The biology of the leafminer is have addressed the relationship between typical of other species of leafmining moths P. citrella levels, damage and, ultimately, its (Plate 20). Small eggs are laid on young leaves, effect on yield reduction (Binglin and Mingdu, and hatching larvae produce serpentine 1996; Hunsberger et al., 1996). Most important, mines beneath the leaf epidermis, where they measurement of leafminer damage remains feed upon the liquid contents of leaf cells. Life an undefined term. Studies conducted by history of the leafminer has been studied by Schaffer et al. (1996) in lime determined that Badawy (1969), Batra et al. (1988) and Garrido visual damage estimates in percentage of area (1995). Total generation time can fluctuate damaged (underside and upperside of the between 13 and 52 days depending on leaves) tended to overestimate leaf damage by temperature. about 30%. Number of larvae per leaf and the Species, and hybrids of the genus Citrus number of days mining were correlated with and other species of the family Rutaceae leaf damage. appear to be the primary host plant group of Hunsberger et al. (1996) found that lime P. citrella. Published accounts (Sandhu and yield was significantly reduced (37.7%) by Batra, 1978a,b) indicate that some cultivars CLM damage levels in south Florida. are more susceptible than others. The most The same authors established relationships

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78 D. Smith and J.E. Peña

between fertilized trees and stressed fertilized The sex attractant (Z,Z)-7,11-hexadeca- trees and concluded that there was a positive dienyl acetate and (Z,E)-7,11-hexadecadien- correlation (r2 = 0.57) between leaf abscission 1-ol discovered originally from Pectinophora and leaf damage. gossypiella (Bierl et al., 1974) has been used Binglin and Mingdu (1996) reported to trap citrus leafminer. This commercially that no influence on growth, development available lure (Ando et al., 1985) failed to of flushes or yield would occur with under indicate male activity in Florida, Spain, China 20% damaged area in tender leaves. These and Korea (Du et al., 1989; Tongyuan et al., authors report that in southern China the 1989; Caleca and Lo Verde, 1996; Malausa functional relationship between the number et al., 1996; Ortu, 1996; Jacas and Peña, 2002). of larva (x) and the percentage of damaged Male catches in pheromone traps may help to area (y) in a tender leaf is: y = −1.005 + 23.246x predict leafminer density in orchards before (R = 0.98), giving an economic threshold of reaching outbreak densities. 0.74 larva/tender sweet orange leaf for the autumn generation. Peña et al. (2000) reported CHEMICAL CONTROL Many growers have economic injury levels in Florida to fluctuate relied on chemical control of P. citrella but between 16 and 23% and between 18 and effective chemical control of CLM is difficult 85% leaf area damaged for 15-year-old and to achieve and total reliance on chemical 5-year-old Tahiti lime trees, respectively. control has been demonstrated to be ineffective (Knapp et al. 1995, 1996a). Application SEASONALITY Field observations from of chemicals should take into consideration China, Australia and some areas of Florida flushing pattern, actual population present, indicate that in subtropical regions spring tree age (mature trees vs. young trees), flushes are the least damaged of seasonal production system (orchard vs. nursery), growth periods, while summer and autumn application method (foliar vs. soil applica- flushes suffer the most serious infestations tion), and presence of natural enemy (Knapp et al., 1995). Different seasonality is complex. observed for subtropical areas (Peña et al., Some selective materials such as aver- 1996b), tropical areas, the Mediterranean, mectin are useful to check infestations and North Africa and the Near East. For instance, petroleum oil sprays (at 0.25–0.5%) applied Smith and Beattie (1996) demonstrated that three or four times per flush are also effective infestation of the new growth begins in early (Rae et al., 1996; Liu et al., 1999, 2001). December in Queensland and 4–6 weeks later in southern Australian states. Up to 100% of BIOLOGICAL CONTROL The most important young leaves in a flush can be attacked from aspect of citrus leafminer management is January to April when infestation levels drop biological control. While in many cases the rapidly with increasing parasitism, reduced diversity of natural enemies of the leafminer new growth and cooler temperatures. Peak (hymenopterous parasitoids, predacious numbers of adults were caught throughout arachnids, ants, lacewings) accounts for sig- the year with peak numbers in spring, sum- nificant reduction of the leafminer population mer and autumn in south Florida (Peña, 1998). (Amalin et al., 1996; Binglin and Mingdu, 1996; The total number of moths trapped was 2.5 Browning, 1996; Browning et al., 1996; Cano times higher in 1994 than in 1995. Relation- et al., 1996; Castaño et al., 1996; Cave, 1996; ships were established between adult catch Hoy and Nguyen, 1997; Morakote and and egg deposition during the year in south Nanta, 1996; Peña et al., 1996b; Smith and Florida. Results also suggested that numbers Neale, 1996; Waterhouse, 1998), in other of moths trapped are not influenced by the cases, their presence and activity are low. amount of rainfall but might be influenced by In the area of origin of the citrus temperature (Peña, 1998). Huang and Huang leafminer, the parasitoid complexes are varied (1989) and Peña and Schaffer (1996, 1997) have (LaSalle and Schauff, 1996) (Table 3.8) and made some studies of egg and larva distribu- their value as mortality factors differs among tion patterns and sampling methodology. geographical areas. For example, in China,

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Table 3.8. Common wasp parasitoids of citrus Zaommomentedon brevipetiolatus Kamijo pro- leafminer on citrus (LaSalle and Schauff, 1996; duced high levels of parasitism. However, Hoy and Nguyen, 1997). Ujiye (1996) considered that these native parasitoids cannot give an adequate bio- Parasitoids Origin of parasitoid logical control of the leafminer. Encyrtidae In the western hemisphere, the current Ageniaspis citricola Thailand, Philippines biological control situation has been studied Indonesia by different researchers (Hoy and Nguyen, Asecodes delucchi Thailand 1994; Browning et al., 1996; Cano et al., 1996; Eulophidae Castaño et al., 1996; Cave, 1996; French and Cirrospilus quadristriatus China Legaspi, 1996; Peña et al., 1996b; Perales et al., Citrostichus phyllocnistoides China, Thailand Semielacher petiolatus Australia 1996). The seasonal occurrence of parasitoids Zaommomentedon Thailand, Japan of P. citrella was studied from 1993 through brevipetiolatus 1995 in Florida (Peña et al., 1996b). The Closterocerus trifasciatus Thailand parasitoids collected were identified as Stenomesius japonicus Japan, China Pnigalio minio, Cirrospilus sp., Closterocerus sp., Sympiesis striatipes Thailand, Japan Sympiesis sp., Horismenus sp., Zagrammosoma Kratosyma citri Thailand, PNG multilineatum (Ashmead), Oncophanes sp., and Elachertus sp. China Elasmus tischeriae Howard. Most of these Chrysocharis pentheus Japan, Taiwan parasitoids are eulophids. Levels of para- Quadrastichus sp. Thailand sitism in Florida indicated that, through Pnigalio flavipes Florida Diglyphus begini Florida parasitoid conservation, biological control of P. citrella by its native parasitoids could play an important role in leafminer management. The importance of more detailed studies Binglin and Mingdu (1996) demonstrated that to determine the role of the indigenous para- larvae and pupae are attacked by four or five sitoids has been emphasized by Browning species of parasitoids in Guangdong Province (1996). Perales et al. (1996) reported that and at least seven species against larvae and Cirrospilus sp. preferred second and third two species against pupae in Fujian Province. instar larvae, while Horismenus sp. was These authors considered that the dominant observed in prepupa or pupa and Elasmus species Tetrastychus phyllocnistoides Naraya- sp., was observed in pupa. Duncan and Peña nan and Cirrospilus quadristriatus (Subba Rao (2000) reported fecundity, and host stage pref- and Ramamani) in Guangdong province, and erences of Pnigalio minio. Much research is still Elachertus sp. in Fujian Province played an needed to determine the effect of the different important role in controlling the population chemicals on the beneficial entomofauna development of the leafminer. In Thailand, of Florida. However, preliminary data (Peña 13 species of hymenopterous parasitoids were et al., 1999) show that Agrimek might be found. Parasitism during 1991 through 1993 the least harmful pesticide to the native fluctuated between 36.73% and 72.05%. The parasitoid. average percentage parasitism by Ageniaspis citricola Logvinovskaya, Quadristriatus sp., CLASSICAL BIOLOGICAL CONTROL Introduc- Cirrospilus ingenuus Gohan, Teleopterus sp., tion of exotic species (e.g. A. citricola) from Eurytoma sp., C. itrifasciatus, Citrostichus phyl- the area of origin has proven to be successful locnistoides (Narayanan), Sympiesis striatipes for Australia and Florida (Hoy and Nguyen, Ashmead and undetermined species was 1994; Smith and Beattie, 1996). There is a clear 11.39, 8.77, 4.84, 2.25, 0.23, 0.19, 0.18, 0.13, and need for other parasitoid species adapted 29.32%, respectively. to different climatic areas. In Queensland In other Asiatic areas, e.g. Japan, where P. A. citricola can kill 80–90% of its host during citrella was introduced 60 years ago, the domi- January–April, resulting in much less attack nant parasitoids, Sympiesis striatipes, Chryso- on the late summer–autumn flushes. Long charis pentheus (Walker), C. phyllocnistoides and cool winters and extreme dry heat (up to

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80 D. Smith and J.E. Peña

45°C) in summer have a detrimental effect et al., 2001) by the indigenous natural enemies on parasitism levels. In southern Australian than by the introduced parasitoid, A. citrella. states, Semielacher petiolatus Girault can reach parasitism levels of 20–60% but not until Fruit piercing moths March–April. High rates of parasitism in March–April appear to have an important In India, fruit sucking or piercing moths influence on the rate of reinfestation in the belong to the genera Othreis, Achaea, Calpe, following season, possibly by reducing the Anua, Ophideres. In Brazil, Gymnadrosoma size of the overwintering leafminer popula- aurantium Costa Lima (Lepidoptera: Grapho- tions (Smith and Beattie, 1996). A classical bio- litidae) (Cermeli, 1983) causes damage by logical control project was initiated in Florida sucking juice of citrus. Quezada (1989) in February 1994 with the introduction of reports that Othreis scabellum (Guenee) and the parasitoid A. citricola from Australia (Hoy O. serpentifera Walker (Noctuidae) are a et al., 1996). Rearing methods were developed serious problem for citrus in Honduras. (Smith and Hoy, 1995) and releases began in Ripe fruits of sweet orange, mandarin orange May 1994. A. citricola established, dispersed and sweet limes are commonly attacked. The and overwintered in Florida during 1994/95. insects pierce the fruit rind and expose it Maximum dispersal of A. citricola was docu- to secondary infections (Plate 22). The fruit mented 25 km from an initial release site usually drops within a few days and thus (Pomerinke and Stansly, 1996). In some sites, becomes unmarketable. It is claimed that parasitism of pupae was found to be as high through elimination of alternative host plants as 99% and parasitism rates of 60–80% were from the vicinity of citrus orchards the insect common (Hoy et al., 1995). However, the suc- infestation could be reduced (Ghosh, 1990). cess of A. citricola in the humid Florida climate O. fullonia (Clerck), O. materna (L.) and (Hoy et al., 1996) has not been repeated in Eudocima salaminia (Cramer) are significant the dry areas of Texas (V. French, personal pests in northeastern Australia. communication). Parasitoid rearing has been improved and modified by different researchers (Argov Coleopteran pests and Rossler, 1996; Hoy et al., 1996; Johnson et al., 1996; Peña and Duncan, 1996; Smith and Beetle pests of citrus include the branch and Neale, 1996). Because there is no artificial diet trunk borers of the family Cerambycidae (e.g. available for citrus leafminer, rearing of Anoplophora chinensis Forster in China), leaf, parasitoids requires an understanding of the fruit and root eating weevils of the family biology of the leafminer and the parasitoid as Curculionidae, e.g. Fuller’s rose weevil well as the phenology and flushing patterns of Asynonychus cervinus Crotch and leaf eating the host plant (Smith and Hoy, 1995). chrysomelids (e.g. monolepta beetle Mono- lepta australis Jacoby, in Australia). PREDATORS Binglin and Mingdu (1996) reported that the predators Chrysopa Root weevils boninensis, C. sinica and the predacious bug Orius insidiosus and some ants and spiders are Several species of weevils (Curculionidae) reported to prey on larvae of the leafminer. affect citrus in Florida and the Caribbean Amalin et al. (1996) reported that arachnids, (Schroeder and Beavers, 1977). These are Chiracanthium inclusum, Clubiona sp., Trachelas the West Indian sugarcane rootstalk borer volutus, Hivana velox, Hentzia palmarum, were weevil, Diaprepes abbreviatus (L.); Fuller’s rose considered the most dominant predators beetle, Asynonychus cervinus (Boheman), the feeding on larvae of citrus leafminer in south citrus root weevil, Pachneus litus (Germar); Florida, followed by lacewings, coccinellids the northern citrus root weevil Pachneus and ants. In Florida, Amalin et al. (2002) opalus (Olivier); and the little leaf notcher reported that a higher percentage mortality of Artipus floridanus Horn (Otero et al., 1995; P. citrella was obtained by predation (Amalin Knapp et al. 1996b). Other species of weevils

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considered important citrus pests in Central (1968) and McCoy and Simpson (1994). and South America are Exopthalmus spp. and Current research for Diaprepes has focused Compsus spp. (Coto et al., 1995). Hypomeces on trapping, kairomones and pheromones, squamasus Fabricus occurs in South-East Asia use of mortality factors, e.g. entomopatho- and citrus snout weevil Sciobius marshalls genic nematodes and fungi (Beavers and Schoeman in South Africa. All weevil species Schroeder, 1980; Schroeder 1990; Adair 1994; are similar in biology and the damage they do McCoy and Simpson, 1994; J.E. Peña et al., to citrus trees (Knapp et al., 1996b). unpublished), determination of proteins to The adults feed on leaves, often leaving a reduce larval feeding, plant resistance characteristic pattern of notches around the (Shapiro et al., 1996) and use of audiographic edges. Except for Fuller’s rose weevil, which methods to determine larvae in the soil deposits its eggs beneath the calyx of the fruit (Shapiro and Gottwald, 1995). For a review (Knapp et al., 1999), female root weevils lay of the biology of Diaprepes abbreviatus see their eggs in clusters on leaves and, by secret- Schroeder and Beavers (1977). Distribution ing a sticky substance, cement leaves together and sampling have been investigated by around egg clusters. A single female may lay Beavers and Selhime (1975), while Adair et al. as many as 5000 eggs during her life of 3 to (1998) determined D. abbreviatus oviposition 4 months. In 7 or 8 days the eggs hatch; larvae preferences. A. Hunsberger et al. (unpub- leave the cluster and fall to the soil. After they lished) observed that D. abbreviatus prefers to enter the soil, they may stay there for 8–12 deposit eggs on sorghum rather than other months, feeding on plant roots. They pupate host plants. in the soil, and then adults emerge, come up out of the soil and start the cycle all over again INJURY CAUSED BY LARVAE The larvae girdle eating leaves and laying eggs. The costs of the taproot, destroying the tree’s ability to fighting an infestation of the insect in a citrus take up nutrients and causing it to die. This grove are considerable. Currently, it involves type of injury provides an avenue for root rot an autumn application of nematodes for larval infections. One larva can kill a young tree, and control, use of spring and autumn sprays several larvae can cause serious decline to to kill adults (McCoy and Simpson, 1994) established trees. and use of fungicides in the spring, summer and autumn to control Phytophthora. Lesions BIOLOGICAL CONTROL A new species of caused by the larvae increase susceptibility to entomogenous nematode, Steinernema rio- root rot. Adding up these costs could reach bravis, offers improved control (Schroeder, $912 per hectare. Factoring a theoretical loss 1990). Bullock (1995) found that S. riobravis of 10% of the citrus trees and a 25% decrease offers 89–90% control of Diaprepes. The benefi- in harvests, the estimated loss reaches cial nematodes enter weevil larvae and release $3140 ha−1 year−1. a plug of bacteria which multiply in the larva’s Whitwell (1990) reports that Diaprepes body cavity and digest its insides, creating a famelicus causes losses of $30,000 ha−1 in material which the nematodes feed upon. This citrus nurseries in the Caribbean. This author process kills the larvae within 24–48 h, and reported that the use of soil-applied insecti- the nematodes continue to grow and mate. cides did not reduce root damage to citrus The female nematode releases infective nursery beds in the Caribbean island of juveniles which then go out and find other Dominica, probably because larvae were too host larvae (Anonymous, 1995). In central deep in the soil. Whitwell (1990) considers that Florida citrus areas, nematodes are applied pesticides may have exacerbated the problem August–October and March and May by reducing natural enemies. (Rhodes, 1990). The current and past research on Diaprepes abbreviatus (Coleoptera: Curculionidae) was EGG PARASITOIDS The introduction into con- summarized by Hall (1995) and analysed by tinental USA of some species of parasitic McCoy and Simpson (1994). Its biology has wasps, e.g. Tetrastichus (Quadrastichus) haiti- been revised by Fennah (1942), Woodruff ensis Gahan (Armstrong, 1987) collected from

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82 D. Smith and J.E. Peña

Caribbean countries with a heavy Diaprepes Dirioxa, Monacrostichus and Rhagoletis. The population has not been considered effective biology of the most important fruit flies has (Anonymous, 1996; Beavers et al., 1980). been summarized by Christensen and Foote However, preliminary results by R. Franqui (1960), their ecology has been summarized (personal communication) report higher para- by Bateman (1972) and their management sitism rates of Quadrastichus haitiensis on eggs has been assessed by McPheron and Steck of D. abbreviatus. For several years, Etienne (1996). et al. (1990) reported that the egg parasite Ceratogramma etiennei (Hymenoptera: Tricho- Bactrocera spp. grammatidae) appeared to be specific to eggs of the genus Diaprepes and recommended its Bactrocera spp. are pests of major importance introduction into other Caribbean islands and in the eastern hemisphere. The Bactrocera spp. into the USA. C. etiennei has been successfully reported on citrus by White and Elson-Harris reared in the laboratory and its biology has (1992) include: B. aquilonis (May), B. caryeae been determined by Etienne et al. (1990). The (Kapoor), B. caudata (Fabricius), B. cilifer same authors observed a parasitism level (Hendel), B. correcta (Bezzi), B. cucurbitae of 30% of the egg population in the island (Coquillett), B. curvipennis (Froggatt), B. of Guadeloupe. Moreover, the population of diversa (Coquillett), B. dorsalis (Hendel), B. Diaprepes sp. in Guadeloupe appears to be facialis (Coquillett), B. frauenfeldi (Schiner), lower after parasitoid augmentation, com- B. jarvisi (Tryon), B. halfordiae (Tryon), B. kriki pared to the pest situation in other Caribbean (Froggatt), B. latifrons (Hendel), B. malgassa islands such as Dominican Republic and Munro, B. melanota (Coquillett), B. melas Puerto Rico (J. Etienne, personal communica- (Perkins & May), B. minax (Enderlein), B. tion). C. etiennei is now cultured at TREC- neohumeralis (Hardy), B. passiflorae (Froggatt), Homestead (Peña et al., 1998). B. psidii (Froggatt), B. quinaria (Bezzi), B. tau (Walker), B. tsuneonis (Miyake), B. trilineola PREDATORS Eggs and larvae of Diaprepes Drew, B. trivialis (Drew), B. tryoni (Froggatt), abbreviatus have been reported as prey of nine B. zonata (Saunders), B. umbrosa (Fabricius), predator species in Florida (Whitcomb et al., and B. xanthodes (Broun). Among these, 1982; Tryon, 1986). Predation by ants is B. minax is considered one of the most reduced during the afternoon, but increases destructive pests of citrus in China (Huasong during the evening. Richman et al. (1983) et al., 1998), being particularly damaging to concluded that predation by ants was less Citrus sinensis and C. aurantium. B. tryoni is important in neonate larvae than for eggs the major fruit fly pest of citrus in eastern and late instar larvae. Later Jaffe et al. (1990) Australia. B. papayae and B. dorsalis are demonstrated that first instar larvae appear important throughout South-East Asia and to produce repellents that reduce predation. the western Pacific – Philippines, Indonesia, Tryon (1986) reported that earwigs are effec- Pakistan (Allwood and Drew, 1996). tive night predators of first instar larvae in Florida. LIFE CYCLE AND DAMAGE Bactrocera spp. female fruit flies insert their eggs beneath the skin of citrus, especially in ripening fruit. Dipteran pests White banana-shaped eggs are deposited in clusters of about a dozen eggs. A total of The main dipterous pests are fruit flies 200–400 eggs are laid by Anastrepha fraterculus, and blossom midges. Fruit flies can be major 1200–1500 eggs by B. dorsalis and 50 eggs by pests, capable of causing near total fruit B. minax. The larvae tunnel into the fruit, con- loss and can be of major concern from a taminating the fruit with frass and providing quarantine standpoint in exported fruit entry for fungi and bacteria. Fully grown lar- (Vijaygasegaran, 1993). vae measuring ca. 7 mm drop to the ground Fruit flies affecting citrus belong to and enter the soil where they pupate. The egg the genera Anastrepha, Bactrocera, Ceratitis, period lasts from 2 to 20 days. There are three

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Tropical Citrus Pests 83

larval instars. Larval and pupal periods are Hawaii became established against B. dorsalis each 2–4 weeks. Pupal stage of B. minax in (Clancy et al., 1952); however, fruit flies China is 180 days (Huasong et al., 1998). directly damage produce that is to be mar- Studies conducted by Singh (1991) with keted. As a result, a small fruit fly population B. dorsalis in India indicated that pupal period can cause economic damage, reducing the was longest (18 days) at 15°C and shortest success of classical biological control pro- (6 days) at 35°C. After emergence, the females grammes. Biosteres arisanus (Sonan) has require a protein source for egg maturation. recently been considered to have some Warm, humid weather is considered to be promise for control of B. dorsalis in Hawaii favourable for Bactrocera fruit flies and pest (Harris et al., 1998). populations build up as citrus ripening occurs. Bactrocera populations decrease Ceratitis spp. during dry periods. OCCURRENCE AND DAMAGE Seven species of MONITORING Fruit fly activity has been Ceratitis, C. capitata (Wiedemann), C. catoirii monitored in Australia using Dakpot® fruit fly Guerin-Méneville, C. cosyra (Walker) C. traps hung beneath the tree canopy. Methyl discussa (Munro), C. malgassa Munro, C. eugenol is considered the most powerful male quinaria (Bezzi) and C. rosa Karsch attack citrus lure for oriental fruit flies. Methyl eugenol was species (White and Elson-Harris, 1992). The used successfully for control and eradication Mediterranean fruit fly C. capitata is the most of B. dorsalis in Oahu (Steiner and Lee 1955), important and a common polyphagous pest Rota Island (Steiner et al., 1965), Okinawa, in citrus growing areas of Hawaii, western Kume, Miyako and Uaekama Islands Australia, Mexico, Réunion and South Amer- (Iwahashi, 1984) and has also been used for ica (Etienne, 1966; Morin 1967). Ceratitis cosyra monitoring B. umbrosus in the Philippines occurs in Africa whereas C. catoirii Guer (Umeya and Hirao, 1975). Fruit flies of both occurs in Réunion (Etienne, 1968). The female species were controlled by mass trapping of can oviposit all over the fruit, with no males with methyl eugenol and infestations preference for any part. Later, when fruit were brought to sub-economic levels in becomes suitable for maggot development, Pakistan (Mohyuddin and Mahmood, 1993). the oviposition sites become light in colour Protein or yeast baits containing a toxi- and the tissue softens. The fully grown mag- cant such as malathion are commonly used gots leave the fruit and pupate in the soil. to control B. tryoni in Australia (Smith et al., The developmental period is approximately 1997). The bait mixture is applied as a course 3–4 weeks and 8–10 generations year−1 can spray on the tree skirt in quantities of 15 l ha−1 occur depending on temperature and other at 7–14 day intervals while fruit are suscept- factors intrinsic to the fly population (Hill, ible and flies active. The baits are very effec- 1975). tive and relatively non-disruptive to natural enemies. BIOLOGICAL CONTROL Several parasitoids, e.g. Opius fullawayi (Silvestri), O. humilis Sil- BIOLOGICAL CONTROL A good number of vestri, O. incisi Silvestri, O. kraussi Fullaway, braconid parasitoids are recorded from O. tryoni Cameron, O. bellus Gahan, Biosteres Bactrocera spp. (Waterhouse, 1993); however, longicaudatus Ashmead, B. tryoni (Couron) they give a low level of control. The and B. oophilus (Fullaway) have been reported parasitoids of B. zonata that have been found parasitizing C. capitata (Beardsley, 1961; in Pakistan include Opinus longicaudatus Wharton and Marsh, 1978). Bess et al. (1961) (Ashm.), Dirhinus giffardii Silv., and Bracon sp. reported that the most important parasitoids The parasitoids, O. longicaudatus, D. giffardii collected from C. capitata in Hawaii were O. and Spalangia grotiusi Girault are commonly vandenboschi, O. oophilus and B. longicaudatus. reported from B. dorsalis (Syed et al., 1970); The fungus Beauveria tenella is reported from however, their incidence is extremely low. pupae of B. manix in China (Huasong et al., Opius spp. introduced from Malaysia into 1998). Again control is usually inadequate.

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Anastrepha spp. some cases control Anastrepha populations are glass and plastic versions of the McPhail LIFE CYCLE AND OCCURRENCE Anastrepha spp. trap, which is baited with a mixture of protein are endemic to the western hemisphere and (occasionally hydrolysed cottonseed together their range extends from the southern United with borax, molasses or fermented juices)and States to northern Argentina and includes water (Balock and Lopez 1969). The McPhail the Caribbean islands (Aluja, 1994). Six trap, however, has several drawbacks. It is Anastrepha species (A. fraterculus (Wiede- expensive, breaks easily and is cumbersome to mann), A. ludens (Loew), A. ocresia (Walker), service. Colours such as yellow and orange, A. serpentina (Wiedemann), A. suspensa reflecting maximally within a narrow spectral (Loew), and A. striata (Schiner)are associated region, i.e. 500–590 nm, have proven to be with citrus (White and Elson-Harris, 1992). effective for capturing several Anastrepha Mexican fruit fly, Anastrepha ludens,is species, e.g. A. fraterculus, A. ludens and A. reported to be the most common fruit fly pest suspensa, when used in spherical, rectangular attacking citrus in the Americas. Abundance or cylindrical traps. In commercial grapefruit of Anastrepha populations has been positively orchards in Honduras, monitoring is prac- correlated with temperature and negatively tised in combination with chemical and cul- correlated with relative humidity. However, tural control practices (Sponagel et al., 1996). a study by Aluja et al. (1989)demonstrated Use of broad-spectrum pesticides with the lack of a clear relationship between hydrolysate protein baits has been the rule for rainfall and Anastrepha fly captures in mango control of Anastrepha species (Hentze et al., orchards in Mexico. The same authors caution 1993). Tests using cyromazine, a highly that differences in population fluctuations can specific growth regulator against Diptera, occur within the same orchard. Most of what against various Anastrepha species resulted in is known today is based on basic biology stud- reduction of infestation of fruits (Diaz et al., ies carried out between 1900 and 1944 (Aluja, 1996). 1994). The basic life cycle is very similar among all Anastrepha spp. for which the biol- BIOLOGICAL CONTROL Both classical bio- ogy is known. Caribbean fruit fly eggs are laid logical control and repeated augmentative in small groups just below the rind of citrus releases of mass-reared parasitoids have been fruit (Browning et al., 1995). Egg incubation used to suppress Anastrepha populations. of Mexican fruit fly (A. ludens), requires 3.8 Parasitoid species such as Diachasmimorpha days; larval development 14.2 days and pupal longicaudata, Doryctobracon crawfordi, Ganapis development 14.2 days at 27 ± 2°C (Leyva pelleranoi, Biosteres vandenboschi and Acerato- et al., 1991). In the majority of Anastrepha neuromya indica have been imported and species, the females deposit their eggs, e.g. released in the USA, Mexico, Costa Rica, c. 15–19 eggs per A. ludens female, in either Brazil and Peru for the control of A. suspensa, the epicarp or mesocarp of ripening fruit. A. ludens and A. fraterculus. Depending on the species, eggs are laid either singly or in clusters. Larvae pass through CULTURAL CONTROL Orchard sanitation, i.e. three instars before emerging from the fruit collection and destruction of all unwanted and burrowing into the ground to pupate. fruit on the trees and on the ground, contrib- Damage to grapefruit in Honduras can utes significantly towards reducing damaging reach 87%, and each fruit could yield 5.7 to 11 fruit fly populations (Vijaysegaran, 1993). larvae (Sponagel et al., 1996). However, orchard sanitation is difficult to implement and enforce (Vijaysegaran, 1993). TRAPPING McPhail traps has been a Early harvesting is a technique that is suc- standard procedure for controlling Anastrepha cessfully practised on other tropical fruits. spp. for 35 years even though such methods Uncontrolled breeding of fruit flies in poorly have been ineffective. The most widely used managed or abandoned orchards should be traps during the last 35 years to monitor and in avoided.

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PHYSICAL CONTROL Wrapping or bagging Thrips individual fruits is a method not recommended for citrus (Vijaysegaran, 1993). Moreover There are about six important thrips pests the shortage of labour appears to be the major of citrus worldwide. Scirtothrips is the most constraint to the widespread use of bagging damaging genus. Citrus thrips Scirtothrips for production of selected fruits. At maturity, citri Moulton is a key pest of areas like Cali- oranges and grapefruits are susceptible to fornia, Scirtothrips aurantii Favre is a key pest A. suspensa, whereas immature fruit are not in South Africa and chilli thrips Scirtothrips susceptible to attack (Browning et al., 1995). dorsalis is a key pest of South-East Asia. Other The plant growth regulator gibberellic acid significant species are citrus rust (or orchid) (GA3) reduces attack of A. suspensa on grape- thrips Chaetanaphothrips orchidii Moulton and fruits (Greany et al., 1987). The success of this greenhouse thrips Heliothrips haemorrhoidalis strategy has prompted the application of GA3 (Bouchel) (worldwide) Taenothrips sp. (South into a broadly based pest-free zone in Florida. Africa) Scirtothrips albomaculatus Bianchi (eastern Australia) and Megaleurothrips kellyanus (Bagnall) (Australia). Citrus midges Scirtothrips damage which occurs mostly at and shortly after fruit set, is characterized The citrus midge, Prodiplosis longifila Gagne, by grey scar tissue around the stem and/or a neotropical species, is present throughout between touching fruit. One of the major most of the lime production areas of Florida causes of fruit blemish and downgrading and has gained pest status since 1984 (Peña throughout the world is wind rub (40%) and and Mead, 1988; Peña et al., 1989b). Damage it is easy to confuse the two (Bedford, 1943). by P. longifila normally affects the flower Bedford et al. (1998) describe the life and sea- parts, including the ovary, stamens and sonal history of S. aurantii in South Africa. petals. After larval feeding, fungal infection by Colletotrichum gloeosporioides Penz, Clado- LIFE HISTORY The biology and habits of sporium herbarum LK ex Fr. var. citricola and S. aurantii in Zimbabwe were described in Penicillum sp., follows, causing the death of detail by Hall (1930). Bedford (1943) described flowers. P. longifila has been reported feeding the different stages at Rustenburg, South on wild cotton, lucerne, beans, tomatoes and Africa as follows: potatoes. • Egg. The egg is bean-shaped when first Eggs of this species are deposited indi- laid and swells with the development vidually or in groups of 12–59 on stamens or of the embryo. It is translucent with on the ovary. Lime flowers are susceptible to a smooth thin shell. The eggs are laid egg laying from the time the flower is approxi- separately within the soft tissues of small mately 4 mm in diameter until the flower is green fruit and the tender leaves and near petal break. The eggs hatch in c. 1–2 days shoots of new growth, and are invisible depending on the prevailing temperature to the naked eye. The egg measures conditions. Upon hatching, the larvae find 0.22 mm by 0.11 mm. Most eggs are their way to the stamens and to the lower found just beneath the upper surface of portion of the ovary on which they feed. the leaves. Larvae mature in about 10 days and drop from • First instar larva. When newly hatched the flower and burrow into the soil to pupate the larva is colourless and translucent (Peña et al., 1989b). If undisturbed by insecti- but soon becomes translucent white. cide applications, the parasitoid Synopeas As it matures and before moulting the spp. can maintain the population density larva becomes yellowish. Wing pads are at non-economic levels (Peña et al., 1990). not present. The mean larval length is The citrus blossom midge Cecidomyia sp. is a 0.32 mm. minor pest in eastern Australia (Smith et al., • Second instar larva. The body colour of 1997). the second instar larva progresses from

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white when newly moulted to a deep SEASONAL HISTORY The number of genera- orange-yellow. The mean length before tions per year is estimated to be 9.4 at Rusten- pupation is 0.75 mm. burg (Bedford, 1943). Scirtothrips aurantii At maturity the larvae drop to the numbers are generally highest during the ground after sunset and pupate beneath 6 months from September to February. the citrus trees. In this way lethal soil Diapause does not occur, presumably due to temperatures are avoided. Most larvae the mild climatic conditions which prevail in drop close to the tree trunk. Sometimes the citrus-producing areas of southern Africa. a larva will pupate under the calyx of Larvae and adults may therefore be found at a citrus fruit but this appears to occur any time of the year if suitable feeding areas only very rarely. Like the first instar larva, are available. wing pads are not present. The adults lay eggs on the first growth • Prepupa. The pale yellow prepupa pos- flush of the new season. First generation sesses short wing pads and can walk larvae develop to maturity on this flush about if disturbed. It is a non-feeding and then pupate in the soil beneath the tree. stage. The eyes are reddish while the The subsequent emergence of adults tends to antennae and legs are translucent. Mean coincide with the hardening-off of this flush length is 0.57 mm. Moulting to the pupa and the end of blossoming. The adults then takes place within the soil or leaf litter. begin to infest the small fruitlets as they begin • Pupa. In this stage the translucent to swell and become dark green, especially wing pads are longer and extend back to when they grow up against the protecting approximately segment VIII of the abdo- sepals. men. The antennae are folded back over the head. The colour is similar to that NATURAL ENEMIES The two most common of the prepupa. The overall body length predators of the citrus thrips at Rustenburg is 0.56 mm. Mortality during pupation is (Bedford, 1943) are Haplothrips bedfordi Jacot- estimated at 56.3% (Gilbert, 1992). Guillarmod, which is only common from • Adult female. The female is pale, orange- January to April, and an anthocorid bug, yellow, and like all thrips the wings Orius (= Thriphleps) thripoborus (Hesse), which are folded longitudinally over the body is only common on citrus trees from April to when at rest. July. These and other predators had no effect • Adult male. The male is smaller than the in controlling thrips populations which cause female at 0.6–0.7 mm in length and severe damage (up to 75% culls or more) in the abdominal markings are sometimes orchards left unsprayed for several years. inconspicuous. Grout and Richards (1992) and Grout and Stephen (1993), investigated the value of LIFE CYCLE The egg stage takes from 6 to 24 indigenous phytoseiid mites as predators of S. days, depending on the season. The combined aurantii. Two important species are Euseius duration of the two larval stages is an average addoensis (Van der Merwe and Ryke) and E. of 7.6 days in midsummer (December to Feb- citri (Van der Merwe and Ryke). The former is ruary) and 13.5 days in August. Hall (1930) especially important as an effective predator gives the larval stage as 5 days in Zimbabwe. in the Eastern Cape where it is very common. The duration of the prepupal stage from Table 3.9 lists the important parasitoids of October to December is 1 day and that of the citrus thrips. pupal stage 3 days, making a total of 4 days. The total duration of the life cycle is 18.4 days during summer and 44 days during winter. True bugs Hibernation does not take place in any stage. The mean number of eggs per female per day There are at least six significant bugs on is 1.2 during the summer and 0.43 during July. citrus: coreid bugs like the leaf-footed bug Hall (1930) estimates the pre-ovipositional Leptoglossus phyllopus (L.), shield bugs like period at about 2.5 days. green vegetable bug Nezara viridula (L.),

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Table 3.9. Common wasp parasitoids of bugs and thrips on citrus (Smith et al., 1997).

Parasitoids Main hosts on citrus Origin of parasitoid

Aphelinidae Centrodora darwini Biprorulus bibax Australia Scelionidae Trissolcus basalis Nezara viridula North Africa, USA T. oenone B. bibax Australia T. ogyges B. bibax Australia T. mitsukurii N. viridula Japan T. nakagawai N. viridula Japan Gryon spp. Amblypelta nitida and A. lutescens Australia Anoplocnemis curvipes South Africa Pteromalidae Acroclisoides tectacorisi B. bibax Australia Eupelmidae Anastatus biproruli B. bibax Australia Anastatus spp. Musgraveia sulciventris Australia Thripobius semiluteus Heliothrips haemorrhoidalis Australia Goethana shakespeari H. haemorrhoidalis Australia Trichogrammatidae Megaphragma mymaripenne H. haemorrhoidalis Australia

antestia bug Antestiopsis spp. and spined (Browning et al., 1995; Smith et al., 1997; citrus bug Biprorulus bibax Breddin Bedford et al., 1998). (Browning et al., 1995; Smith et al., 1997; Bedford et al., 1998). The fruit sucking Termites bug Rhynchocoris humeralis Thunber occurs commonly throughout South-East Asia. The giant northern termite Mastotermes darwinensis Froggatt is a formidable pest of Egg parasitoids citrus in the northern tropics of Australia (Smith et al., 1999) attacking even living The scelionid genus Trissolcus and the tissue. Sub-Saharan Africa has several genera eupelmid genus, Anastatus are important attacking citrus but mostly involving dead (Table 3.9). Assassin bugs like Pristhesancus branches (Bedford et al., 1998). Subterranean plagipennis are significant predators. termite Reticulitermes flavipes (Koler) occurs in Florida (Browning et al., 1995).

Other pests Ants and wasps Paper wasps Polistes spp. occasionally pose a Cicadas problem to pickers and pruners. The citrus A few cicadas are recorded as minor gall wasp Bruchophagus fellis (Girault) of east- pests, e.g. bladder cicadas Cytosoma schmeltzi ern Australia is an unusual pest, attacking the Distant in Australia and Cryptotympana atrata young twigs and causing severe galling. It is Fabricius in China. heavily parasitized by Megastigmus spp. The main threat from Hymenoptera comes from ants and their attraction to honeydew producing pests – soft scales, mealybugs, Orthopterans planthoppers, whiteflies and aphids. Serious Orthopteran pests include katydids, crickets pests include Argentine ant (Ripa and Rodri- and grasshoppers – all minor pests guez, 1999), Linepithema humilis (Mayer), and

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88 D. Smith and J.E. Peña

other Iridomyrmex spp., leafcutting ants Atta and their damage or improve the environment spp. and fire ants Solenopsis spp. for natural enemies) and selective use of pesticides. IPM needs as its basis a sound Other pests knowledge of the pests and their natural enemies, action levels and management strate- These include spiders, snails, slugs and gies. Systematic monitoring of both the pests nematodes. Spiders are more a problem for and the levels of their natural enemies is vital pruners and pickers. Several snail species are (Smith and Papacek, 1993; Papacek, 1997). important, e.g. the common brown garden The record of IPM implementation snail Helix aspersa (Miller) (Smith et al., 1997), worldwide is currently more impressive the dune snail Theba pisana (Muller) (South on paper than in practice. However, fruit Africa) and the slugs Urocyclis spp. (Bedford tree pest control systems based purely on et al., 1998) and Deroceras spp. (Chili) (Ripa pesticides are faced with major problems and Rodriguez, 1999). of resistance development, development of The most important and widespread secondary pests, rising costs and threats to nematode which parasitizes citrus is the citrus environmental and human health. Properly nematode (Tylenchulus semipenetrans). Others managed IPM systems in citrus can cost a which sometimes cause problems are the root fraction of full chemical programmes and lesion nematode (Pratylenchus spp.) and the give better quality and production of fruit stubby root nematode (Paratrichodorus sp.). (Hardman et al., 1993). Several other types of plant parasitic nema- In developing a successful IPM todes have been found in association with programme for citrus there are a number of citrus trees, but they have not been found to be important components: economic pests. These include Paratylenchulus sp., Xiphinema sp. and Hemicriconemoides sp. 1. Sound knowledge of the pests – their habits, (Smith et al., 1997). the importance of the damage caused and action levels. An action level is the point at which action should be taken to avoid Pest Management Practice economic loss. It is determined by research (looking at pest densities, the impact of Because of the greater number of pest and natural enemies, damage levels, economics of disease problems in the tropics and the greater production, costs of spraying and expected number of small farms with less emphasis on market returns) and by practical experience. monitoring, pesticide use can be heavy and Often the best means of determining an action up to 24 or more sprays are applied per level is to make a ‘good estimate’ based on season. Application, particularly for seden- experience and then to test the estimate in tary scales and mealybugs and also mites, can commercial practice. It is very important to be inefficient with poor coverage. Pesticides determine the real economic impact of a pest. tend to be broad spectrum and very disrup- Citrus leafminer, for example, is extensively tive to natural enemies. Citrus is a long-term sprayed in the tropics and subtropics but crop offering continuity of overwintering there is increasing evidence of a low economic sites and habitats for both pests and natural impact except on young trees (Schaffer et al., enemies, and some degree of stability. How- 1996). There is a tendency for growers to apply ever, extensive use of disruptive pesticides repetitive sprays (up to two dozen a year) in negates these factors. Hand-operated spray- South-East Asia because the damage to the ing machinery common on small farms also leaves is readily seen. Unless workable action gives little protection to the user. levels for pests in a complex are proposed Integrated pest management relies and adhered to, ‘management’ will soon heavily on the biological control of pests by degenerate into ‘calendar spraying’. their natural enemies (parasitoids, predators 2. Sound knowledge of biological control. The or pathogens) and integrates into the system natural enemies of pests, with some measure any useful cultural techniques (to reduce pests of their significance, must be known. Natural

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Tropical Citrus Pests 89

enemies may include native or introduced throughout the season. The data collected species with both often having a vital role. need to be accurate and repeatable. A random Where exotic pest species have been intro- number of trees e.g. ten per hectare, are duced, researchers should if necessary have assessed per block and fruit, leaves and/or access to ‘classical biological control’ allowing twigs assessed (Smith et al., 1997). It is impor- the introduction of natural enemies from the tant to record the data, initially on a small pest’s centre of origin to redress the imbal- orchard sample card and then, if possible, ance. Excessive bureaucratic impediments on a computer spreadsheet. The data then to the introduction of natural enemies is recorded allow a decision to be made on any counter-productive to good biological control. actions to take. Mass rearing and augmentative or 4. Development of complete IPM packages for a inundative release of natural enemies is a whole pest complex. Some key pests may have proven useful technique in many citrus areas. poor biological control and must be treated It is of most use where a natural enemy with pesticides. Biocontrol studies have been is checked by adverse conditions e.g. cold made on Scirtothrips spp. by Grout and winters, very hot dry periods in summer, Richards, 1992 and Grout and Stephen, 1993. discontinuity between host generations or Serious transmitters of disease are also a major disruption from pesticide application. Mass problem in the tropics, the most notable rearing and augmentation can be costly, how- being D. citri (transmitter of Asian greening ever, and should not be used unless clearly throughout South-East Asia). Control of such necessary and effective. Aphytis spp. for red a pest can dominate the whole programme. scale, are some of the most commonly used Biocontrol studies have intensified with mass reared beneficials in citrus (Papacek and D. citri in recent years (Mercado et al., 1991; Smith, 1985). Osman and Quilici, 1991; Tang and Huang, Attention also must be paid to cultural 1991; Tang and Wu, 1991) and the use of selec- practices that can be contrary to biological tive chemicals particularly petroleum spray control, e.g. excessive dust from roads, bare oils is also an option (Rae et al., 1997). Other soil inter-rows. Phytoseiid mite populations pests are very important because of quaran- in Queensland orchards are increased sixfold tine status, e.g. fruit flies. Fortunately, good by allowing some inter-row growth and selective baiting techniques exist for fruit flies flowering of the grass Chloris gayana kunth and also postharvest treatments. It is impor- (Smith and Papacek, 1991). tant for researchers to develop IPM packages 3. Simple and effective monitoring procedures that are complete and to demonstrate them in – both for pests and their natural enemies. display blocks or in key orchards within a Monitoring is a vital component of IPM. It is region. In spite of the seriousness of some key best done by a trained scout who is dedicated pests and the variety of pest species occuring to the task. Orchardists can perform it them- in the tropics, successful IPM has been imple- selves but are often too busy and too involved mented in many areas worldwide. with the crop to make impartial decisions on 5. Careful use of pesticides. Selective pesticides pest management. The large number of small can be a powerful tool in IPM programmes. orchardists in the tropics, however, practically The main problems in pesticide use are igno- demands that individual growers learn to reg- rance of the effect of the pesticides on natural ularly count their pests and natural enemies. enemies, inefficient spraying machinery and This means that IPM and monitoring must be practices, rapid development of resistance extended and demonstrated to such growers and off target spray drift, which can disrupt and backed up on a long-term basis with help natural enemies. on quality control and research needs. There is considerable information on Monitoring is not a research tool but must the toxicity of pesticides to natural enemies be quick and practical for the scout or grower. (Broadley and Thomas, 1995; Hattingh and An average block of trees (1 ha) should be Tate, 1995; Smith et al., 1997). Synthetic pyre- assessed in no more than 30 min and sampling throids such as deltamethrin are persistent repeated at regular intervals (7 to 28 days) and very disruptive when used on citrus,

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90 D. Smith and J.E. Peña

and most organophosphates and carbamate not only important on individual farms but insecticides are also disruptive. The last decade throughout continuous farming areas. has seen the development of a range of new pesticide groups with some characteristics that showed promise for selectivity (Sparkes, References 1998). These include systemic neo-nicotinoids, insect growth regulators, phenylpyrazols, Adair, R.C. (1994) A four-year field trial of entomo- avermectins and spinosyns. There are still pathogenic nematodes for control of Diaprepes unfortunately some problems with these abbreviatus in a flatwoods citrus grove. Proceed- materials, with the systemics causing mite ings of the Florida State Horticultural Society 107, outbreaks (G.A.C. Beattie, personal communi- 63–68. cation, 1999) and some of the IGRs showing Adair, R.C., Nigg, H., Simpson, S. and Lefebre, L. persistant toxicity to coccinellids (Hattingh (1998) Ovipositional preferences of Diaprepes and Tate, 1995; Smith et al., 1999). abbreviatus (Coleoptera: Curculionidae). Florida Inefficient spraying is a chronic problem Entomologist 81, 225–234. in citrus worldwide. Scale, mealybug and Allen, J.C. (1979) The effect of citrus rust mite damage on citrus tree growth. Journal of most mite infestations require spraying to Economic Entomology 72, 327–330. point of runoff with a high percentage of Allen, J.C. and Stamper, J.H. (1979) Frequency coverage to gain control. Carmen (1975, 1977) distribution of citrus rust mite damage on details operations of the oscillating boom, the citrus fruit. Journal of Economic Entomology 72, preferred sprayer for large citrus trees. Air 746–750. blast sprayers with and without towers are Allwood, A.J. and Drew, R.A.I. (1996) Management probably the most used sprayers in higher lati- of fruit flies in the Pacific. A regional sympo- tude areas. Rotary atomizers and high veloc- sium, Nadi, Fiji 28–31 October 1996. ACIAR ity sprayers with air shear nozzles have also Proceedings No. 76, 267 pp. been tried (Smith et al., 1997). Air blast spray- Aluja, M. (1994) Bionomics and management of Anastrepha. Annual Review of Entomology 39, ers decrease rapidly in efficiency when tree 155–178. height increases above 4 m and when spray Aluja, M., Cabrera, M., Guillen, J., Celedonio, H. and −1 volumes drop below 5000 l ha . Mature trees Azora, I. (1989) Behavior of Anastrepha ludens −1 5 m high normally require about 10,000 l ha and A. serpentina (Diptera: Tephritidae) on for thorough wetting for sedentary pests. The wild mango tree (Mangifera indica) harbouring top centre of the tree is the most difficult to three McPhail traps. Insect Science and its reach with spray. Air blasters with towers can Application 10, 309–318. cover trees this high but lower spray volumes Amalin, D.M., Peña, J.E. and McSorley, R. (1996) will reduce efficiency. In the many small Abundance of spiders in lime groves and orchards in the tropics, spraying is done more their potential role in suppressing the citrus leafminer population. In: Hoy, M. (ed.) Pro- by hand-held wands driven by small pumps ceedings of International Conference, Managing on a spray cart, or where there are canals, Citrus Leafminer. University of Florida, p. 72. in a boat in the canal. There tends to be Amalin, D.M., Reiskind, J., Peña, J.E. and McSorley, considerable exposure of operators to spray R. (2001) Predatory behavior of three species of drift. Resistance development to pesticides is sac spiders attacking citrus leafminer. Journal of a continual problem, notably with pests like Arachnology 29, 72–81. red scale, citrus rust mite, tetranychid mites, Amalin, D.M., Peña, J.E., Duncan, R.E., Browning, psyllids and citrus thrips (Bedford et al., 1998). H.W. and McSorley, R. (2002) Natural mortal- Spray drift can easily occur between adjacent ity factors acting on citrus leafminer, Phyllo- blocks of trees or between neighbouring cnistis citrella, in lime orchards in South Florida BioControl 47, 327–347. orchards or (in some circumstances) between Ando, T., Taguchi, K.Y., Uchiyama, M., Ujiye, T. orchards or farms several kilometres apart. and Kuroko, H. (1985) (7Z-11Z)-7,11- Levels of drift may be extremely low but if hexadecadienal: sex attractant of the citrus the pesticide is persistent and highly toxic to leafminer moth, Phyllocnistis citrella Stainton key parasitoids, e.g. Aphytis spp., serious dis- (Lepidoptera: Phyllocnistidae). Agricultural ruptions will occur. Careful use of pesticides is Biological Chemistry, Tokyo 49, 3633–3653.

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Tang, Y.Q. and Aubert, B. (1990) An illustrated Nuts. Prosea Foundation, Bogor, Indonesia, guide to the identification of parasitic wasps 446 pp. associated with Diaphorina citri Kuwayama Vieira, M.R. and Chiavegato, L.G. (1999) Biology in the Asian Pacific region. In: Proceedings of Polyphagotarsonemus latus (Banks) (Acari: of the 4th International Asian Pacific Conference Tarsonemidae) on lemon (Citrus limon Burm). on Citrus Rehabilitation. 4–10 February 1970, Annais Sociedade Entomologia Brasileira 28, Chiang Mai, Thailand, pp. 228–245. 27–33. Tang, Y.Q. and Huang, Z.P. (1991) Studies on the Vijaysegaran, S. (1993) Control of fruit flies in biology of two primary parasites of Diaphorina the tropical regions of Asia. In: Aluja, M. and citri Kuwayama (Homoptera: Psyllidae). In: Liedo, P. (eds) Fruit Flies: Biology and Manage- Chung, Ke and Osman, S.B. (eds) Rehabilitation ment. Springer-Verlag, New York. of Citrus Industry in the Asia Pacific Region. Pro- Waterhouse, D.F. (1993) Biological Control: Pacific ceedings of the 6th International Asia Pacific Work- Prospects. Supplement 2. Australian Centre for shop on Integrated Citrus Health Management. International Agriculture Research, Canberra, Kuala Lumpur, Malaysia, 24–30 June 1991. 138 pp. Tang, Y.Q. and Wu, M.X. (1991) Interspecific Waterhouse, D.F. (1998) Biological Control of Insect host discrimination between two primary par- Pests: Southeast Asian Prospects. Australian asites of Asian citrus psyllid Diaphorina citri Centre for International Agriculture Research, Kuwayama. In: Chung, Ke and Osman, S.B. Canberra, 118 pp. (eds) Rehabilitation of Citrus Industry in the Asia Watson, J.R. (1915) The woolly whitefly. Florida Pacific Region. Proceedings of the 6 International Agricultural Experimental Station Bulletin 126, Asia Pacific Workshop on Integrated Citrus Health 79–101. Management. Kuala Lumpur, Malaysia, 24–30 Wharton, R.A. and Marsh, P.M. (1978) New world June 1991. Opinae (Hymenoptera: Braconidae) parasitic Tongyuan, D., Jinjun, X., Zeshua, W. and Fanlei, K. on Tephritidae (Diptera). Journal of the Wash- (1989) 7Z, Z11-hexadecadienal:sex attractant ington Academy of Sciences 68, 147–165. of Phyllocnistis wampella Liu & Zeng. Kunchong Whitcomb, W H., Gowan, T. and Buren, W. (1982) Zhishi 3, 147–149. Predators of Diaprepes abbreviatus larvae sugar- Tryon, H. (1986) The striped earwing and ant cane rootstalk borer weevil in Florida. Florida predators of sugarcane rootstock borer in Entomologist 65, 150–158. Florida citrus. Florida Entomologist 69, 336–343. White, I.M. and Elson-Harris, M. (1992) Fruit Flies Ujiye, T. (1996) Parasitoid fauna of the citrus of Economic Significance. CAB International, leafminer in Japan, Taiwan and Thailand. In: Wallingford, UK. Hoy, M. (ed.) Proceedings of International Confer- Whitwell, A.C. (1990) Diaprepes spp. problems ence on Managing Citrus Leafminer. University in Dominica and some possible solutions. In: of Florida, p. 100. Pavis, C. and Kermarrec, A. (eds) Recontres Umeya, K. and Hirao, J. (1975) Attraction of the Caraibbes en Lutte Biologique. INRA, Paris. Les jackfruitfly, Dacus umbrosus F. (Diptera: colloques no. 58. pp. 529–541. Tephritidae) and lacewing, Chrysopa sp. Woodruff, R.E. (1968) The present status of a (Neuroptera: Chrysopidae) to lure traps baited West Indian weevil (Diaprepes abbreviatus)in with methyl eugenol and cue-lure in the Florida (Coleoptera: Curculionidae). Florida Philippines. Applied Entomology and Zoology Department of Agriculture and Consumer 10, 60–62. Services, Plant Industry Entomology 77, Van den Berg, M.A. and Fletcher, C.D. (1988) A Gainesville, Florida. bibliography of the citrus psylla, Trioza erytreae Yokomi, R.K., Lastra, R., Stoetzel, M.B., Damsteegt, (Del Guercio) (Hemiptera: Triozidae), up to V.D., Lee, R.F., Garnsey, S.M., Gotwald, T.R., 1987. Phytoparasitica 16, 47–61. Rocha-Peña, M.A. and Niblett, C.L. (1994) Van den Berg, M.A., Deacon, V.E. and Steenekamp, Establishment of the brown citrus aphid P.J. (1991) Dispersal within and between citrus (Homoptera: Aphididae) in Central America orchards and native hosts, and nymphal and the Caribbean basin and transmission mortality of citrus psylla. Trioza erytreae of citrus tristeza virus. Journal of Economic (Hemiptera: Triozidae). Agriculture, Ecosys- Entomology 87, 1078–1085. tems and Environment 35, 297–309. Yothers, W.W. and Miller, R. (1934) Methods for Verheij, E.W. and Coronel, R.E. (1992) Plant determining rust mite abundance. Florida State Resources of South East Asia: Edible Fruits and Horticultural Society 47, 53–55.

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4 Pests and Pollinators of Mango

G.K. Waite Queensland Horticulture Institute, Maroochy Research Station, PO Box 5083, SCMC, Nambour, Queensland 4560, Australia

The mango was supposed to have originated important fruit of Asia and ranks fifth world- in the Indo-Burma region (Verheij, 1991), wide in production after bananas, citrus, but Mukherjee (1997) concluded that it most grapes and apples. Mangoes form a regular likely originated in South-East Asia, particu- part of the diet of people in areas where the larly in the Malay Archipelago. However, fruit is easily grown; it may be eaten ripe or it was probably first grown as a food crop green. In addition, a proportion of the fruit is in India, where its cultivation is thought to juiced or processed into preserves, chutney, have commenced at least 4000 years ago. frozen purée and dried mango. The seeds Small fruit with thin flesh can still be found in yield a starch and the skins are a source of parts of India and these were probably the anacardic acid. World production of mangoes ancestors of today’s selections, which offer in 2000 was estimated to be about 24.5 million the greater size and flavour found in scores of t (FAOSTAT Database, 2001). cultivars grown worldwide. The arrival of the In its spread around the world, the Portuguese in India in the late 15th century mango has been accompanied by some of its apparently benefited the Indian mango original insect pests. The seed weevils have industry, as the knowledge concerning vege- an easy and free ride in fruit which escapes tative propagation was put to good use to quarantine restrictions. Other pests have fol- plant large orchards of superior selections. lowed mangoes to their new homes, but such The global spread of mango cultivation occurrences may not always be linked to man- followed as European explorers transported goes in the first instance, e.g. the Mediterra- the fruit to Africa, North and South America nean fruit fly, Ceratitus capitata (Wiedemann), and the Caribbean. The 19th and 20th centu- and some scale insects. Because the pests ries have seen its range expand even further. concerned are polyphagous, sooner or later, Mangoes are now grown as an important if mango is one of their hosts, they will find it crop all over the world, in both tropical and in the new land. Often, in the absence of the subtropical areas. natural enemies they left behind, these pests assume greater importance in their new range than at home. Every production area has its unique Importance of the Crop complex of pests, many individuals of which may be shared with other areas. Generally, The mango is a significant cultural and there are a few key pests against which religious symbol in India and is much specific management techniques must be revered there (Mukherjee, 1997). It is the most applied. Often, because there are no effective

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natural enemies present, or the pests breed on Bakera (Typhlocyba) nigrobilineata Melichar alternative hosts and are very mobile and fly accounting for the balance (Alam, 1994). The into orchards to damage the crop, chemical leafhopper causing most problems in Guangxi controls must be applied. There are usually Province, China, is Idioscopus incertus Baker. several minor pests which only occasionally In the Philippines, I. clypealis females lay cause a problem under normal circumstances, 100–200 eggs on flower buds and panicles, but which may become serious pests for and in the midrib of young leaves (Anony- various reasons. The indiscriminate use of mous, 1994). Eggs take 4–7 days to hatch and pesticides that disrupt natural enemies; the the nymphal period, occupied by only four introduction of new cultivars that are more instars, takes about 8–10 days. Adults live for susceptible to particular pests; and changing up to 315 days and reproduce only during the international export protocols, which may mango flowering period (Alam, 1994). Mango impose a nil tolerance on certain pests thus hoppers in India, including I. clypealis, are creating an artificial pest status, may elevate reported to pass through five nymphal instars, previously minor pests to the top rank. occupying from 5 to 20 days, and the adults survive from one flowering to the next (Sohi and Sohi, 1990). Populations are at a minimum Pests of Flowers in December–January and reach a peak in March–April, when the mangoes flower (Tandon et al., 1983). Peña et al. (1998) report Mango flowers are attacked by a variety of that the species complete varying numbers insects such as midges, leafhoppers, caterpil- of generations per year, depending on the lars and thrips, as well as mites. Excessive location e.g. 4–5 generations of A. atkinsoni in damage at this critical time has the potential the Punjab of Pakistan and 1–6 generations to limit production even before the fruit is set, throughout India, while I. clypealis has 1–4 though it should always be remembered that generations in the Philippines and 5–6 in most tree crops, including mangoes, produce India. Mohyuddin and Mahmood (1993) an excess of flowers which usually set more found that I. niveosparsus and A. atkinsoni in fruit than the tree can mature. Consequently, Pakistan moved up and down the tree at dif- some allowance for pest damage can be made ferent times of the year and were concentrated without detriment to the final crop. in the lower canopy during May. In 1998, I. niveosparsus was recorded for the first time on mangoes in Queensland, Mango hoppers (Homoptera: Cicadellidae) Australia. The infestation was confined to an area around a remote sea port through which DISTRIBUTION AND BIOLOGY Numerous spe- the pest apparently gained entry, and has cies of leafhoppers are reported infesting not yet spread to commercial production mango trees throughout Asia, but the most areas (B. Pinese, Mareeba, 1998, personal important are Idioscopus clypealis Lethierry, communication). Idioscopus niveosparsus Lethierry, Idioscopus magpurensis Pruthi and Amritodius atkinsoni DAMAGE Adult and nymphal leafhoppers Lethierry (Soomroo et al., 1987; Veeresh, 1988). damage the flowers by piercing the tissues Often all species occur together as in Bihar and with their proboscis and sucking on the plant south India, or with one or more being the sap. The concentrated feeding of hundreds, major pests in particular areas e.g. A. atkinsoni and sometimes thousands, of individuals per and I. clypealis in the Punjab, I. niveosparsus panicle, results in the flowers withering and in Gujarat, Maharashtra and Karnataka and dropping, and no fruit is set. In addition to A. atkinsoni in north India (Veeresh, 1988). the direct effect of their feeding, the hoppers In the Philippines the mango blossom hopper, produce honeydew on which sooty mould I. clypealis, was found to constitute about thrives. This interferes with photosynthesis 98% of the hopper population present on the and pollination, if the flowers have not flowers, with I. niveosparsus and occasionally already been destroyed by the hoppers’

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feeding (Anonymous, 1994; Peña and Verghese and Rao (1985) while others have Mohyuddin, 1997). Differential cultivar sus- set specific infestation levels at which control ceptibility has been reported in the Philip- should be initiated (Serrano and Palo, 1933; pines, with I. clypealis causing the most severe Shah et al., 1984). damage to cv. ‘Carabao’, while B. nigrolineata Many insecticides have been used against prefers the cv. ‘Kathmitha’ (Alam, 1994). mango hoppers including a variety of botanical concoctions, chlorinated hydrocarbons, BIOLOGICAL CONTROL Little information is organophosphates and synthetic pyrethroids available from the Philippines with respect to (Dakshinamurthy, 1984; Datar, 1985; Sohi and natural control of mango hoppers. However, Sohi, 1990). Most of these have been applied as Alam (1994) reported that the entomophagous cover sprays on a schedule basis (Cendana fungi Metarhizium sp. and Beauveria sp. caused et al., 1983). In recent years the synthetic 100% mortality in caged populations of pyrethroids have given excellent control, I. clypealis. B. bassiana Balsamo (Vuilllemin) as has imidacloprid, a systemic compound and Verticillium lecanii (Zimmerman) Viegas belonging to the nitroguanadine group of are known to infect I. clypealis in India chemicals (Verghese, 1998). The technique (Srivastava and Tandon, 1986). In Pakistan, of trunk injection with systemic organophos- Mohyuddin and Mahmood (1993) recorded phates such as monocrotophos, dimethoate the parasitoids Gonatocentrus sp., Mirufens sp. and vamidothion provided good control nr. mangiferae Viggiani and Hayat, Centrodora of hoppers for up to 7 weeks in India sp. nr. scolypopae Valentine, Aprostocetus sp. (Thontadarya et al., 1978; Shah et al., 1983), and Quadrastichus sp. from hopper eggs, and and imidacloprid used in the same way in the ectoparasitoid, Epipyrops fuliginosa Tames, the Philippines has shown promising results from adults. In India, Fasih and Srivastava (G.K. Waite, 1998, unpublished). (1990) noted the egg parasitoids Aprostocetus Several non-chemical procedures are sp., Gonatocerus sp. and Polynama sp. In recommended to control mango hoppers. addition, five species of predators, Chrysopa Planting resistant varieties is an obvious tactic lacciperda (Kimmins), Mallarda boninensis and Nachiappan and Baskaran (1984) noted (Okomote), Bochartia sp., a mantid and a that in India, the cultivars ‘Chinnarasam’, lygaeid were found to prey on the nymphs. ‘Bangalora’, ‘Khader’ and ‘Beneshan’ were Aprostocetus sp., Platygaster sp., Synopeas resistant to A. atkinsoni, while Singh (1997a) sp. and Zatropis sp. were recorded as egg listed a further ten Indian cultivars that are parasitoids in Dominica (Whitwell, 1993). resistant. Smoking orchards to deter hoppers E. fuliginosa parasitizes Idioscopus spp. in was suggested by Otanes and Toquero (1927), Thailand. and Serrano and Palo (1933) recommended that light traps set up with kerosene lanterns MONITORING AND CONTROL Because mango placed in the middle of a basin containing hoppers attack the flowers and are capable of soapy water could be used to reduce hopper completely preventing fruit set, there are few populations just before flowering. Hoppers options available for spray decisions based on are noted for their habit of seeking secluded monitoring. Most recommendations involve and sheltered areas to rest. A common recom- the application of effective insecticides before mendation is to prune large and dense trees to hopper populations become too intense, and open them up to sunlight and so discourage as the trees commence to flower (Khanzada the pests from remaining in the trees (Bondad, and Naqvi, 1985). Generally, the flowers 1989; Anonymous, 1994). For cultivars that are the target for the sprays applied, but respond to artificial flower induction, peak Mohyuddin and Mahmood (1993) recom- hopper infestations can be avoided, for mended that one spray be applied in May, and instance on cv. ‘Carabao’ in the Philippines, that it need only be applied to the lower 5 m by inducing the trees to flower early in of the trunk and canopy where the hoppers October–December (Anonymous, 1994). rested. A sequential sampling plan for moni- The literature on mango hoppers is exten- toring hopper populations was suggested by sive, especially from India and Pakistan, and

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the reader is referred to Veeresh (1988) and most damaging species of a complex that Sohi and Sohi (1990), for a listing of references also includes Pleuroprucha insulsaria (Gueneé) concerning the pests in those countries. (Geometridae), Tallula spp. (Pyralidae) and Racheospilla gerularia (Hubner) (Peña and Mohuddin, 1997). In the Philippines, the tip borer, Chlumetia transversa Walker Midges (Diptera: Cecidomyiidae) (Noctuidae), is second only to mango hoppers as a pest of flowers (Bondad, 1989). Whitwell DISTRIBUTION AND BIOLOGY The mango blis- (1993) mentions that 14 lepidopterous species ter midge or mango gall midge, Erosomyia infest mango flowers in Dominica, with the mangiferae Felt, infests mangoes in the West most common being the geometrids, Eupi- Indies. According to Barnes (1948) it was first thecia sp., Chloropteryx glauciptera Hampson recorded in St Vincent and later in Trinidad and Oxydia vesulia (Cramer). Caterpillars and St Lucia. Female midges lay their eggs in belonging to the families Geometridae, the developing flower and leaf buds. When Lymantriidae, Noctuidae, Pyralidae and the eggs hatch after 2–3 days, the larvae cause Tortricidae infest mango flowers in Australia the tissue in which they are feeding to swell (Cunningham, 1989). The larvae of all of these and form galls. Up to 70% of small fruit may species feed on the florets and the flower also be affected (Whitwell, 1993). After 10–14 stems. Many of them construct shelters by days the larvae leave the galls and pupate in webbing the destroyed flower parts together the soil. Adults emerge about 7 days later (Cunningham, 1989; Peña, 1993). Penicillaria (Callan, 1941; Barnes, 1948). The abundance jocosatrix Gueneé (Noctuidae) is a major pest of the pest has been noted to be favoured by in Guam, where it can consume all of the dry seasons that are unusually wet (Murray, flowers on a panicle (Schreiner, 1987). The 1991). female moth deposits eggs on or near new Five cecidomyiid species including leaves and inflorescences and frequently on Erosomyia indica Grover and Prasad, are spider webs. The larvae develop more quickly reported to attack mango flowers and to on these younger plant parts than on older cause severe damage in India (Kulkarni, leaves (Nafus et al., 1991). 1955; Prasad, 1966, 1972; Butani, 1979), while Dasyneura mangiferae (Felt) does the same in DAMAGE Feeding by the larvae on the Hawaii (USDA, 1981). various flower parts destroys the potential for maximum fruit set, and some of the BIOLOGICAL CONTROL Platygaster sp., Sys- species involved also damage young fruit tasis dasyneurae and Eupelmus sp. parasitize (Peña, 1993). In many cases infestation levels Dasyneura sp. in India, while Tetrastichus sp., and consequent damage are insignificant Aprostocetus sp. and Mirufens longifunculata compared to the total number of flowers Viggiani and Hayat attack Erosomyia indica produced, and the capacity of the tree to (Grover, 1986; Fasih and Srivastava, 1990). set and carry a full crop to maturity Pirene sp. has been recorded as an ecto- (Cunningham, 1989). parasitoid of Procystiphora mangiferae Felt.

BIOLOGICAL CONTROL In general, because of the lack of knowledge concerning the Lepidoptera individual species attacking mango flowers, little information is available regarding DISTRIBUTION AND BIOLOGY Numerous spe- their natural control. Peña (1993) noted that cies of Lepidoptera have been found to infest Macrocentrus delicatus Cresson parasitizes mango flower panicles in all production P. atramentalis in Florida. The hymenopterous areas, but in few cases have the species parasitoids, Aleiodes sp. nr. circumscriptus involved been identified. In Florida, Pococera (Nees) (Braconidae) and Euplectrus sp. nr. atramentalis Lederer (Pyralidae) and Platynota parvulus Ferriere (Eulophidae), along with the rostrana (Walker) (Tortricidae) are the two tachinid Blepharella lateralis Macquart, were

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introduced into Guam from India in 1986– Scirtothrips dorsalis Hood, chilli thrips, is 1987, for the control of P. jocosatrix. Although regarded as being an important pest of mango Aleiodes sp. failed to establish, the other flowers in Thailand. The thrips attack the parasitoids successfully reduced P. jocosatrix flowers, fruit, young shoots and new flush. populations by about 75%, and fruit produc- Populations reach a peak during hot dry tion increased substantially (Nafus, 1991). weather. In very dry springs in Australia the plague thrips, Thrips imaginis Bagnall, MONITORING AND CONTROL Cunningham may heavily infest mango flowers, but (1989) recommended weekly monitoring of they apparently cause little if any damage flower panicles for the presence of damaging (G.K. Waite, 1996, unpublished). Tandon and caterpillars in Australia. Webbed shelters Verghese (1987) recorded Thrips palmi Karny should be pulled apart in order to record infesting mango flowers in India, leaving the presence of larvae, with endosulfan being scab-like marks where they had fed, and applied when caterpillar infestation is signifi- retarding growth. cant. No actual infestation levels were stated for the initiation of such action. Peña (1993) DAMAGE Thrips feed on all parts of the made similar recommendations for mangoes mango flower panicle, including the petals, in Florida, so that potential problems can be anthers and pollen. They may destroy the detected early and chemical controls applied florets so that no fruit sets, and also reduce if they are necessary. On Guam, Schreiner the vigour of the panicle so that growth is (1987) found that Bacillus thuringiensis Berliner retarded. (Bt) could be used to control P. jocosatrix, but only if populations were carefully monitored, BIOLOGICAL CONTROL Loomans and van or regular sprays were applied to cover the Lenteren (1995) reviewed the biological con- overlapping periods of larval emergence. trol agents of thrips and considered that the predators Orius sp., Anystis agilis Banks and Hypoaspis aculifer (Canestrini) showed good potential in the biocontrol of F. occidentalis. Thrips (Thysanoptera: Thripidae) Ceranisus menes Walker attacks that species in Israel (Rubin and Kuslitzky, 1992). DISTRIBUTION AND BIOLOGY Frankliniella bispinosa (Morgan) and Frankliniella kelliae MONITORING AND CONTROL Thrips popula- (Sakimura) frequently infest mango blossoms tions can be monitored by regular inspection in Florida, where they feed on the nectaries of flower panicles and control decisions made, and anthers, presumably affecting fruit set based on predetermined economic injury (Peña, 1993). Sakimura (1981) described F. levels if they have been set (Peña, 1993). kelliae as a species distinct from F. difficilis Monitoring for the presence of the chilli thrips Hood, and noted that it had been collected in Thailand is carried out by shaking shoots, from a range of host plants from Florida and flush leaves or inflorescences over a container, the Caribbean area. The western flower thrips, and counting the number of insects dislodged. Frankliniella occidentalis (Pergande), damages Sampling units are selected from all four sides flowers and fruit in Israel (Wysoki et al., 1993). of the tree. When five thrips per sample are This species made a dramatic appearance in found, a spray of carbaryl is recommended. A countries all over the world during the 1990s, predatory mite, Amblyseius sp., and a Stethorus and given the Israeli experience it would not sp. have been found in association with be surprising to find that it has become a pest the thrips and are thought to prey on of mango flowers in at least some of these them (S. Krairiksh, Thailand, 1999, personal countries. Van Lenteren et al. (1995) report that communication). the life cycle of F. occidentalis takes from 14.8 Verghese et al. (1988) studied the spacial to 16.6 days at 25°C. The thrips Frankliniella distribution of the pests on the tree, and con- cubensis attacks mango flowers in Costa Rica sidered that a sample of 55 panicles from the during the dry season (Jirón, 1993). lower canopy provides a good estimate of the

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thrips population present on the whole tree. Elson-Harris (1992) reported that eight species However, they did not recommend at what of Anastrepha have been found in association infestation level controls should be applied. with mangoes. Anastrepha obliqua (Macquart) Peña (1993) quoted a formula for calculating is a pest of mango and other soft fruits in most the number of thrips in a panicle, based on the Caribbean countries except Grenada, St Vin- number caught on sticky traps. In the absence cent and the Grenadines. The Mexican fruit fly of reliable estimates of the true population Anastrepha ludens (Loew) is a serious pest size, the trap method has not been shown to in Belize, Anastrepha serpentina (Wiedemann) give an unbiased estimate of numbers. and Anastrepha striata Schiner occur in Guyana and Trinidad and Tobago, while A. suspensa (Loew) and Anastrepha ocresia Walker infest Pests of Fruit fruit in Jamaica (Rhodes, 1992). Segarra (1988) determined that only A. obliqua attacked man- Mango fruit are a very valuable commodity goes in Puerto Rico, despite a long-held belief in most areas of production, whether they are that the only other fruit fly species present in A. suspensa consumed locally, sent to central markets in the country, , was also a problem. A. ludens large cities, or exported. There are numerous is the major pest of mangoes grown A. obliqua alternative uses for inferior fruit such as juice, at high altitudes in Mexico, while et al purée and dried mango, but the price paid for dominates at lower altitudes (Aluja ., A. obliqua good quality fruit without imperfections of 1996). has been shown to be the any kind, especially insect-induced, usually major fruit fly pest in Costa Rica and Guate- provides the farmer with a better return. For mala (Jirón, 1996) and is responsible for up to this reason, the fruit needs to be protected 94% of damage attributed to fruit flies (Jirón et al from a range of insects that may cause and Hedström, 1988; Jirón ., 1988). In Peru, physical damage or loss, or merely affect its the important species attacking mango are Anastrepha distincta Anastrepha outward appearance. Greene, fraterculus Wiedemann, A. serpentina, A. striata and Anastrepha chiclayae Greene (Morin, 1967; Tijero, 1992). Fruit flies (Diptera; Tephritidae) Bactrocera tryoni (Froggatt), Bactrocera neohumeralis (Hardy), Bactrocera jarvisi Flies of the family Tephritidae, commonly (Tryon), Bactrocera zonata (Saunders), Bactro- known as fruit flies, are pests of mangoes in cera frauenfeldi Schiner and Bactrocera dorsalis most parts of the world (Hill, 1975; Veeresh, (Hendel) are all reported to attack mango 1988; Bondad, 1989; Cunningham, 1989; (Umeya and Hirao, 1975; Cunningham, 1989). Aluja, 1994). The female flies oviposit in The name oriental fruit fly, B. dorsalis, had maturing fruit and the larvae burrow for many years unwittingly been given to a through the flesh, feeding on it and initiating complex of flies attacking a variety of fruits rots. Fruit may fall prematurely or, if eggs throughout South-East Asia. Drew and are laid just before the fruit is harvested, Hancock (1994) separated the complex into spoilage in the package will occur as the fruit 52 separate species. Many of these were ripens and the eggs hatch. Ideally, adult flies described from specimens caught in should be prevented from laying in the fruit. pheromone traps and have no host records The biology and behaviour of fruit flies has associated with them, but B. dorsalis, Bactrocera been studied in detail by Christenson and carambolae Drew and Hancock, Bactrocera Foote (1960), Bateman (1972), and Aluja et al. occipitalis (Bezzi), Bactrocera papayae Drew and (1997). Hancock and Bactrocera philippinensis Drew and Hancock, have all been reared from DISTRIBUTION AND ECOLOGY Anastrepha spp. mango fruit (Plate 23). range from the southern USA through Central The Mediterranean fruit fly is the America and the Caribbean, to Argentina most widespread of a number of Ceratitis in South America (Aluja, 1994). White and spp. reported to attack mangoes throughout

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Pests and Pollinators of Mango 109

the world. C. capitata occurs in Israel, Spain, BIOLOGICAL CONTROL Numerous parasit- Mexico, Réunion, Mexico, South America and oids are known to attack fruit flies in all parts South Africa (Morin, 1967; Galan-Sauco, 1990; of the world, and while they undoubtedly Vayssieres, 1997; De Villiers and Steyn, 1998). have some effect on fly populations, they Ceratitis cosyra (Walker), the marula fruit fly, are unable to reduce numbers to levels and Ceratitis rosa Karsch, the Natal fruit fly, that prevent economic damage. Syed et al. also attack mangoes in South Africa (De (1970) indicated that Biosteres longicaudatus Villiers and Steyn, 1998) while C. rosa also (Ashmead), Dhirinus giffardii Silvestri and occurs in Réunion (Vayssieres, 1997), along Spalangia grotiusi Girault parasitize B. dorsalis, with Ceratitis catoirii Guer (Etienne, 1968). C. while B. longicaudatus, D. giffardii and Bracon cosyra is by far the most important fruit fly pest sp. attack B. zonata in Pakistan. of mangoes in South Africa, accounting for Opius and Biosteres spp., notably Opius about 99% of individuals emerging from humilis Silvestri, Opius fullawayi (Silvestri), infested fruit in a survey conducted by Opius kraussi Fullaway, Opius incisi Silvestri, Labuschagne et al. (1996a). Opius tryoni (Cameron), Opius bellus Gahan, The life cycle of all Anastrepha spp. Biosteres vandenboschi Fullaway, Biosteres studied is basically the same. Eggs are laid oophilus (Fullaway), B. longicaudatus and singly or in groups, mostly into the pulp Biosteres tryoni (Couron), are recorded as of the developing fruit. The larvae develop parasitoids of C. capitata (Beardsley, 1961; Bess through three instars, after which they leave et al., 1961; Wharton and Marsh, 1978). the fruit to pupate in the soil. The rate of devel- Diachasmimorpha longicaudata, Ganaspis opment is influenced by temperature and the pelleranoi, B. vandenboschi, Doryctobracon food medium. Adult flies spend much time crawfordi and Aceratoneuromya indica have exploring the surface of the leaves of plants, been released for the biocontol of Anastrepha even those which are not reproductive hosts. ludens, A. suspensa and A. fraterculus in Mexico, In doing this they appear to obtain food in Brazil, Costa Rica, Peru and USA (Peña and the form of yeasts and bacteria (Christenson Mohyuddin, 1997). and Foote, 1960). Leyva et al. (1991) found that the eggs of A. ludens took 4.6 days to hatch MONITORING AND CONTROL Fruit fly num- in mango, but only 3.8 days in grapefruit. bers are easily monitored with pheromone For the larval stage, this was reversed, with traps, although trap catches have not been development taking 27 days in citrus, but only related to the risk to the crop. In Australia, 23 days in mango. cuelure is used in Dakpot traps which Bactrocera spp. have a similar biology are monitored weekly to detect sustained and behave in a similar way to Anastrepha increases in fly numbers, rather than thresh- spp. Warm, humid weather favours fruit old catches (Cunningham, 1989). Sprays fly activity and in Queensland, Australia, of dimethoate or fenthion applied every populations increase rapidly as the summer 2 weeks, or bait sprays (protein autolysate rains increase and the mango maturation plus chlorpyrifos) applied at least weekly, season progresses (Cunningham, 1989). are recommended. These should commence 6 weeks before the anticipated harvest date, DAMAGE Female fruit flies often probe or as trapping indicates. immature fruit with their ovipositor, causing In South Africa, the use of traps for blind stings in which no eggs are laid. These monitoring fly numbers is recommended, stings may lead to later infection by disease with bait sprays being applied accordingly. organisms, but more often the sap which Protein hydrolysate combined with the insec- exudes from the puncture is of prime concern, ticides mercaptothion or trichlorfon is used as since it burns the skin of the fruit (Wysoki the bait, and the mixture is applied to small et al., 1993). Eggs laid closer to maturity hatch, areas of the canopy in volumes of 250–1000 ml and the larvae proceed to burrow through per tree. The elimination of potential breeding the flesh, making it inedible, and eventually hosts of the flies such as wild tobacco, Solanum causing the fruit to rot and fall. mauritianum Scop., wild guavas and bramble

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berries, as well as orchard sanitation, are also potassium nitrate sprays. This ensures that a measures that minimize the fruit fly risk (De uniform flowering will occur in individual Villiers and Steyn, 1998). orchards, but not all farmers in an area may McPhail traps are used to monitor decide to induce their trees at the same time. Anastrepha spp. numbers in Peru, and control Nevertheless, there is the possibility of reduc- measures are applied when individual trap ing exposure to fruit fly and mango hopper catches average two flies per week (Herrera infestation through the manipulation of flow- and Viñas, 1977). Bait sprays are applied ering to produce the major crop during the dry preferably from the ground, so that they can season. In addition, a common practice in the be restricted to small areas of individual trees, Philippines is to enclose the developing fruit thus minimizing their impact on natural ene- in newspaper envelopes, which are applied by mies. If applied from the air, the risk of upset- hand when the fruit is about 80 mm long. The ting natural controls is increased because of envelopes are secured with a skewer of bam- the reduced control over where the chemical boo. Reasonable protection from fruit flies is lands, and other pest problems may flare provided, but as the fruit expands the end of (Soto-Manatiu et al., 1987). Aluja et al. (1996) the envelope often opens to allow entry of the found that more flies were caught in McPhail flies (G.K. Waite, 1998, unpublished). While traps baited with hydrolysed protein, placed Manoto et al. (1984) considered this approach around the edges of orchards than within to be the most effective way of preventing orchards, and large trap catches were not cor- fruit fly damage, Bondad (1985) showed that related with high infestation levels in the crop. even with the most durable paper, only In other countries, methyl eugenol has 46% of the fruit was protected. Trapping, been used to control fruit flies and even fruit wrapping and the application of bait eradicate them. B. dorsalis was reported to sprays are all recommended procedures have been eradicated from Oahu (Steiner in Thailand (S. Krairiksh, Thailand, 1999, and Lee, 1955), Rota Island (Steiner et al., 1965) personal communication). and Okinawa, Kume, Miyako and Uaekama In the search for fruit fly controls that Islands (Iwahashi, 1984). Mass trapping of might be less damaging to the orchard ecosys- male flies with methyl eugenol reduced infes- tem, Robacker et al. (1996) examined the effect tations to subeconomic levels in Pakistan of 55 isolates of Bacillus thuringiensis (Berliner) (Mohyuddin and Mahmood, 1993). Balock on adults and larvae of A. ludens. While flies and Lopez (1969) report the trapping of which fed on agar pellets carrying the bacte- A. ludens in McPhail traps using a pelletized rium died, aqueous formulations, which are mixture of cottonseed hydrolysate and borax necessary for application to trees in the field, dissolved in water as the bait. Infestations in did not kill flies. mangoes were reduced by 98% when one to In areas that produce a variety of fruit five traps per tree were deployed, depending crops with differing maturity times, the fruit on tree size. fly problem in the late maturing crops will Jirón (1996) detailed a management strat- generally be worse than for the early maturing egy for fruit flies infesting mangoes in Central fruit. In Israel, mango orchards adjacent to America. This included cultural techniques citrus groves are often infested by flies which such as attempting to induce mangoes to have bred in the citrus fruits (Wysoki flower and fruit during the dry season when et al., 1993). The application of pesticides to fruit fly numbers were minimal, planting of mangoes to control fruit flies is effective cultivars with synchronous flowering, ‘live in Pakistan, but it has sometimes led to the fence’ management (avoiding known fruit fly development of damaging scale infestations hosts in the species composition of bordering due to the disruption of natural enemies vegetation), parasitoid introductions, moni- (Mohyuddin and Mahmood, 1993). toring fly numbers through trapping, and Cultivars which are resistant to fruit fly appropriate insecticide applications. attack have been identified in some areas. The cv. ‘Carabao’ in the Philippines can Carvalho et al. (1996) found that cv. ‘Espada’ be induced to flower by the application of was unaffected by A. obliqua, but cv. ‘Carlota’

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Pests and Pollinators of Mango 111

was extremely susceptible. Not only did the Females of S. mangiferae generally lay flies not attack the fruits extensively, but adult eggs in small green fruit, and the larvae tunnel flies which did develop from larvae feeding to the seed, where they feed and develop. on the resistant cultivar lived for a shorter Because the fruit are small and green when the time. egg hatches, the tunnel made by the small larva disappears as the fruit expands and ripens. Most infested mangoes are consumed in ignorance of the presence of the insect in the Seed weevils (Coleoptera: Curculionidae) seed. Shukla and Tandon (1985) found that in India during March–April, eggs took 6–7 days The mango seed weevil, Sternochetus to hatch and the larva passed through five mangiferae (F.) (Coleoptera: Curculionidae), is instars and a pupal stage over a period of 43.7 widely distributed in Africa, Asia, Australia, days. Female weevils lived for about 302 days the Pacific Islands (Cunningham, 1989) and and males for 267 days. Only one generation the Caribbean (McComie and De Chi, 1994). occurred per year. Adult weevils emerged in Sternochetus gravis (F.) and Sternochetus late May–early June and remained in a faculta- frigidus (F.) occur in India (Dey and Pande, tive diapause until the following season. In 1987) and Bangladesh (Alam, 1972). S. frigidus contrast to S. mangiferae, the larvae of S. gravis was first detected in the Philippines in 1987 and S. frigidus live and feed in the pulp as the (Basio et al., 1994) and has caused extensive fruit grows, and the former species has been damage to mangoes on the island of Palawan known to infest up to 100% of fruit in some to which it is presently restricted (Anony- orchards (Dey and Pande, 1987). Females of S. mous, 1994). These weevils are important frigidus lay eggs on mature green fruit and pests of mangoes partly because they infest cover them with a brown exudate. They then the seeds and may be present in otherwise chew a notch in the fruit, causing the sap sound fruit, which makes them a quarantine to flow and cover the eggs with an opaque concern (Yee, 1958; Dey and Pande, 1987; white film. A female lays about 15 eggs day−1 Cunningham, 1989) (Plate 24). They may and perhaps 175–300 eggs in a lifetime. The also be a nuisance to nursery staff wishing to period from egg to adult occupies 40–50 days propagate trees from infested seeds. In India, (Anonymous, 1994). the seeds are used as a source of starch and No natural enemies of S. mangiferae for animal and poultry food, oils, seed meal were recorded in India, and all commercial and organic manure, so that weevil infesta- cultivars were susceptible to infestation tion also affects production of these products (Bagle and Prasad, 1984; Shukla and Tandon, (Bagle and Prasad, 1984). Follett and Gabbard 1985). Field sanitation has been recommended (2000) found that mango seeds can withstand as a control measure (Van Dine, 1906), but substantial damage by seed weevils and Hansen and Armstrong (1990) found that it still germinate successfully, especially the failed to reduce the incidence of infestation polyembryonic cultivars. Germination of because the weevils are apparently able to damaged seeds in the single-seeded cultivar fly further than had been thought. The best ‘Haden’ still exceeded 70%, suggesting that insecticidal treatment was deltamethrin app- concerns with respect to a deleterious impact lied twice in 3 weeks, commencing in early on nursery industries are exaggerated. Follett March. In South Africa, the organophosphate and Gabbard (2000) also conclude that mango fenthion, the pyrethroids deltamethrin, fenva- seed weevils do not seriously affect mango lerate and esfenvalerate, along with the insect yields or marketability. Nevertheless, it is still growth regulator triflumuron, are registered regarded as a significant quarantine threat for weevil control. Recent trials have found and unsuccessful attempts have been made that endosulfan also gives good control to kill it using heat, cold and fumigation treat- (Joubert, 1997). Dispersal of the weevils may ments (Balock and Kozuma, 1964). Irradia- be by flying to trees or crawling up trunks tion may be a useful alternative disinfestation from overwintering sites, but humans play a treatment (Heather and Corcoran, 1992). major role in the movement of the pest in

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infested fruit over longer distances (Hansen, areas and so has only just become evident as a 1993). Newly matured weevils may remain in pest there. Van Mele et al. (2001) suggested the seed for long periods before they emerge, that damage caused by D. sublimbalis in the and because of this, movement into new areas Mekong Delta has been wrongly attributed to is facilitated in exported fruit. Quarantine fruit flies. procedures, which prohibit the movement of mango plants and fruit from the island BIOLOGICAL CONTROL In the Guimaras of Palawan to other parts of the Philippines, Islands of the Philippines, the vespid wasp, have been enforced to protect the valuable Rychium attrisimum, preys on the larvae as industry in the rest of the country from S. they leave the fruit to pupate. Larvae are used frigidus, so that exports to foreign countries to stock the wasps’ nests as food for their can be maintained (Anonymous, 1994). young. The egg parasitoids Trichogramma chilonis Ishii and Trichgramma chilotreae have been recorded attacking the pest in Luzon (Golez, 1991). Mango seed borer (Lepidoptera: Pyralidae)

MONITORING AND CONTROL Mango fruit DISTRIBUTION AND BIOLOGY Deanolis sublim- become susceptible to the seed borer at balis Snellen, the mango seed borer, which was about 60 days post-induction, and insecticide commonly referred to as Noorda albizonalis applications should commence then. Further Hampson in much of the literature (Water- sprays at 75, 90 and 105 days post-induction house, 1998), is an important pest of mangoes are required to fully protect the fruit. The most in the Philippines (Anonymous, 1994), Viet- effective chemicals were found to be delta- nam (Nguyen et al., 1998a; Van Mele et al., methrin and cyfluthrin (Golez, 1991). Other 2001), China (Li et al., 1997), Thailand, Indone- recommendations are to remove infested fruit sia and Papua New Guinea (Cunningham, from the tree before the larvae can leave them 1984). The oval white eggs are laid in groups at to attack neighbouring fruit, to wrap the fruit the fruit apex and take 3–4 days to hatch. in protective bags at 55–65 days after induc- The larvae develop through five instars in tion, and to destroy fallen fruit (Anonymous, 14–20 days and they pupate in cocoons in the 1994). soil. The period from egg to adult takes from 28 to 40 days. The insect apparently prefers mango, but other species of Mangifera have been recorded as hosts (Waterhouse, 1998). Fruitspotting bugs (Hemiptera: Coreidae)

DAMAGE The distinctive red-banded larvae The yellowish green coreid bugs, Amblypelta feed on and bore through the mango pulp to lutescens lutescens (Distant) and Amblypelta the seed, which is consumed. Up to 11 larvae nitida Stål occur along the coast of Queens- have been recorded in a single fruit, but land, and attack most of the tropical and usually there is only one. Infested fruit split subtropical fruit crops grown there (Waite and rot, and fall to the ground (Anonymous, and Huwer, 1998). They prefer to feed on 1994). In Guimaras, Philippines, Golez (1991) young, green fruit, but A. l. lutescens also recorded 12.5% fruit infestation and in serious damages the terminals of a number of hosts. outbreak years, 40–50% yield reductions are In tropical north Queensland, A. l. lutescens possible. Waterhouse (1998) considered that, is the dominant species and feeds on the since D. sublimbalis is capable of causing such young fruit, causing black lesions to develop levels of damage, it may be a more important and the fruit to fall. It also feeds on the termi- pest of mangoes than has generally been nals and leaf petioles, causing wilting and realized. Among several suggestions for this dieback (Cunningham, 1989). In the subtropi- status are that it may have been overlooked as cal south, both species attack mango, but A. a pest or that it has only recently spread to new nitida confines its attention to the fruit, while

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A. l. lutescens attacks fruit as well as terminal mango trees in South Africa. The bugs feed growth (G.K. Waite, 1995, unpublished). The on the new flush, leaf veins and flower stalks, bugs breed in natural rainforest areas, and causing the tissue to die where they have fed. fly into the orchards to feed on the fruit They breed on many alternative hosts such as and terminals. Female bugs lay individual, weeds, vegetables, ornamentals, granadillas opalescent green eggs under leaves. There are and citrus, as well as mangoes. The eggs are five nymphal instars and a generation takes laid in rows on the leaves, and adults and about 40 days. nymphs numbering ten or more may kill all The main predators of fruitspotting bugs of the new growth on a small mango tree, are spiders, particularly members of the leading to retardation of growth. As no chem- family Thomisidae. Several species of egg icals are registered for its control, the insects parasitoids have been recorded. In north must be collected by hand and destroyed (De Queensland, Ooencyrtus sp. (Encyrtidae), Villiers, 1998). Anastatus sp. (Eupelmidae) and Gryon sp. (Scelionidae) parasitized 37.5–91.6% of the eggs of A. l. lutescens (Fay and Huwer, 1994). In south Queensland, Anastatus sp. and Gryon Thrips (Thysanoptera: Thripidae) meridianum (Dodd) have been found to parasitize eggs of A. nitida and A. l. lutescens to a The South African citrus thrips, Scirtothrips similar degree (Waite and Petzl, 1994). aurantii (Sign.), has become an increasingly Because fruitspotting bugs continuously damaging pest in recent years. Nymphs and migrate into orchards, more than one adults feed on small green fruit and cause a insecticide spray may be required to protect blemish on the skin. The damage is only cos- the young fruit. However, the fruit are safe metic, but it is sufficient to downgrade fruit from attack once they have grown to a length and make it unsuitable for export. The lesions of about 50 mm, and two or three sprays of vary from silvering to skin cracking, and if endosulfan at intervals of 2 weeks are gener- high populations are present when the fruit is ally sufficient to protect them from the bugs. very small, the whole surface may be scarred. The coconut bug, Pseudotheraptus wayi The thrips can be monitored with yellow Brown, was first recorded on mangoes in sticky traps. Methamidophos is registered for South Africa in 1977, and now also attacks control of the pest and is used as an undiluted guavas, pecans, macadamias, avocados and trunk treatment, applied with a paint brush loquats. It causes damage similar to that of (Grové, 1998a). Amblypelta spp. (De Villiers, 1990). Helopeltis sp. (Miridae) are minor pests of mango fruit in the Philippines and in northern Fruit piercing moths Australia, where they feed on the fruit and (Lepidoptera: Noctuidae) cause superficial corky blemishes that detract from the fruit’s appearance. Cashew and The noctuid moths Eudocima (Othreis) fullonia cacao are alternative hosts. Insecticides can be (Clerck), Eudocima materna (Linnaeus) and used to control them but in the Philippines Eudocima salaminia (Cramer) are common bagging, which is carried out for protection pests of ripening fruit in Queensland. Litchis, from fruit fly, is also effective (Anonymous, carambolas and citrus are particularly 1994). susceptible (Fay and Halfpapp, 1999), but mangoes may also be attacked. The moths possess a barbed proboscis with which they Tip wilters (Hemiptera: Coreidae) bore into the fruit and suck the juice. No satisfactory control method has been found The tip wilter, Anoplocnemis curvipes apart from totally netting orchards to exclude (Fabricius), can be a serious pest of young them.

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Pests of Leaves and Buds Thrips (Thysanoptera: Thripidae)

Gall midges (Diptera: Cecidomyiidae) The red-banded thrips, Selenothrips rubrocinctus (Giard), has been recorded as a pest of Gall midges infesting the leaves of mango mango leaves from the Caribbean, Hawaii, have been recorded from the Caribbean, Australia, South Africa, Brazil and Florida Brazil, India, South Africa (Procontarinia (Plate 25). The thrips prefer to feed on the matteiana Kieffer and Cecconi), China leaf, especially adjacent to the midrib, where (Erosomyia spp.) and Guam (Procontarinia they cause a silvering that develops into schreineri Harris). Larvae of the latter species necrosis, leading to eventual leaf drop. When form blister galls on the young leaves. When infestations are severe, fruit may also be the larvae mature and leave the galls, the attacked and the silvering turns yellow to tissue is invaded by the anthracnose fungus, brown and is speckled with dark, dried faeces Colletotrichum gloeosporioides Penz. The galls (Cunningham, 1989). Eggs are inserted into dry up and fall out, leaving a typical the leaf tissue and covered with a drop of ‘shot-hole’ effect that was originally thought fluid that dries to form a black, disc-like to be caused solely by the fungus. Similar cover. The adult thrips are almost black, with symptoms have been noted in relation to a red band on the first abdominal segment. infestation by this species on mangoes in The nymphs are pale orange with the first Saipan (Marianas Islands), Belau and Yap two abdominal segments and the anal (Caroline Islands), and in the Philippines segment coloured bright red (Moznette, (Harris and Schreiner, 1992). Heaviest infes- 1922). Yee (1958) recommended malathion as tations of the midge were recorded during a control when necessary in Hawaii, while in the wet season, possibly because of the Australia, Cunningham (1989) recommended increased survival of the immature stages endosulfan. Bartlett (1938) stated that the encouraged by the high humidity. hymenopterous parasitoid, Goethana parvi- Amradiplosis echinogalliperada Mabi and pennis Gahan, attacks the thrips in Puerto P. matteiana have been reported from Uttar Rico. Pradesh (Mani, 1943) and the Punjab (Rao, The Mediterranean mango thrips, 1956). P. matteiana is considered to be indige- Scirtothrips mangiferae Priesner, is recognized nous to India where Jhala et al. (1987) studied as a major pest of mangoes in Israel. The thrips the susceptibility to it of 17 mango cultivars in feed on the young shoots and leaves, causing south Gujarat. The cultivars ‘Alphonso’ and the shoots to become stunted and the leaves ‘Kesar’ were most heavily infested, while to curl and drop (Wysoki et al., 1993). Low ‘Deshi Malgoba’ and ‘Benisan’ were least overwintering populations form the basis affected. Phosphamidon and monocrotophos for an increase in spring numbers that peak were found to give the best chemical control in summer. The pest’s abundance can be of the pest (Jhala et al., 1990). In Africa, monitored using yellow sticky traps. Good the cultivar ‘Heidi’ is very susceptible to control has been achieved with the application P. matteiana while ‘Sensation’ is resistant of fluvalinate or acephate when the economic (Githure et al., 1997). The eulophid, threshold of ten thrips per shoot had been Chrysonotomyia pulcherrima, parasitizes the reached (Ganz et al., 1990). larvae heavily, and De Villiers et al. (1987) considered that the midge was never a serious pest. However, Grové (1998b) noted that in Bud mites (Acari: Eriophyidae) some areas, parasitism was less effective and the midge can cause severe damage. Apart The mango bud mite, Eriophyes mangiferae from India and South Africa, P. matteiana now (Sayed) is reported to attack the buds of occurs in Mauritius, Kenya, Réunion, Oman terminals. The normal symptom is a pro- and Malaysia, having spread on imported liferation of shoots on the terminal, giving mango plants (Githure et al., 1997). rise to a witches’ broom effect. However, if

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Pests and Pollinators of Mango 115

the fungus Fusarium sp. is present the tree Spider mites (Acari: Tetranychidae) develops floral and foliar galls because the fungus causes necrosis of the hypertrophia A number of mites belonging to the genus that would normally result in witches’ Oligonychus feed on the upper surface of brooming (Ochoa et al., 1994). mango leaves. The mango mite, Oligonychus In Florida, E. mangiferae has been found mangiferae Rahman and Sapra, is a common in association with malformed mango pest in India, Egypt, Mauritius, Peru, Israel flowers (Peña, 1993) and there has been and some parts of Asia. Its biology has been conjecture that it may be implicated in the studied by Rai et al. (1988). The tea red spider vectoring of diseases that could be the real mite, Oligonychus coffeae (Nietner), is an cause of the malformation. There has been important pest of avocados and a sporadic difficulty proving this hypothesis, and some pest of mangoes in Australia, where high consider that tissue damage caused by the populations may cause leaf bronzing if mite allows infection by Fusarium sp. excessive pesticide use eliminates its main (Denmark, 1983). The life history of the predator, the coccinellid, Stethorus sp. mite has been described by Abou-Awad (Cunningham, 1989). A similar situation (1981). The life cycle is completed in 15 days occurs in Central America and the USA at 25–27°C, and high summer temperatures where the avocado brown mite, Oligonychus appear to have an adverse effect on the mite. punicae (Hirst), and the avocado red mite, The mango bud mite occurs in Australia Oligonychus yothersi McGregor, cause leaf but has never been a problem except bronzing and, in severe cases, necrosis and occasionally in backyard trees (Cunningham, leaf fall (Andrews and Poe, 1980). It is consid- 1989). Orozco Santos and Núñez (1988) ered there that the problem is exacerbated by reported that E. mangiferae had been found sprays directed at other pests. O. punicae also in Mexico, and that it was associated with attacks mango in Puerto Rico (Comroy, 1958). a disorder termed ‘achaparramiento’, the witches’ broom effect described above. The mite could be controlled with sulphur or Other mites (Acari: Tarsonemidae) dimethoate. Doreste (1981) reports that in Venezuela E. mangiferae is increasing in Broad mite, Polyphagotarsonemus latus (Banks), distribution and intensity. may occasionally infest trees in the field but E. mangiferae is considered to be a is more often associated with nursery trees major pest in the Punjab, Delhi and Uttar (Wolfenbarger, 1956). Symptoms of broad Pradesh in India, where it has threatened mite attack include stunting and crinkling the very existence of the mango industry of new leaves and rolling of leaf margins. (Singh and Mukherjee, 1989). Agrawal and The mites can be controlled with applications Singh (1988) reported that it becomes more of dicofol or sulphur (Yee, 1987). (See also abundant in April and gradually reaches a Chapter 3.) peak in June. Control of the mango bud mite has been achieved in Egypt with four sprays of dichlorvos (Osman, 1979). As with many Mango scale (Homoptera: Diaspididae) eriophyid pests, e.g. litchi erinose mite, infestations should be anticipated through moni- Scale insects, especially diaspidid scales, are toring and a knowledge of the phenology and among the most important pests of mangoes flushing behaviour of the trees, so that sprays in some parts of the world. In Australia can be applied to apparently uninfested buds and especially in South Africa, the mango (Rai et al., 1966). The phytoseiid, Amblyseius scale, Aulacaspis tubercularis (Newstead), is swirskii Athias-Henriot, has been found in regarded as a key pest mostly because when association with E. mangiferae (Abou-Awad, it infests the fruit, even though the scale can 1981). be brushed off, it may leave blemishes on the

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fruit (Plate 26). This results in their rejection infestations of Ceroplastes pseudoceriferus for the lucrative export market (Labuschagne Green in Bangladesh cause wilting of leaves, et al., 1995; Joubert, 1997). As well as infesting malformation of flowers and general malaise fruit, A. tubercularis infests mango leaves, of the tree, so that flowering is reduced (Ali, causing discoloured and necrotic areas 1978). It is also a serious pest in Taiwan which, in severe cases, may result in leaf where it undergoes three generations a year fall. In Queensland, the diaspidid Phenacaspis (Wen and Lee, 1986). A number of parasitoids dilitata (Green) produces similar symptoms control the pest in India (Sankaran, 1955), (Cunningham, 1989). The biology of A. Bangladesh (Ali, 1978) and Taiwan (Wen and tubercularis has been described by Van Lee, 1986). Halteren (1970). In north Queensland, breed- Milviscutulus mangiferae (Green), mango ing occurs throughout the year. Females lay shield scale, is reported to be a pest of the crop about 50 eggs under the protective scale cov- in a number of countries. Many detrimental ering. On hatching, female crawlers become effects are attributed to its feeding, including sedentary and secrete a circular scale cover, leaf fall, failure of buds to open, reduced tree while the male crawlers congregate, and each vigour, fruit drop and even death of trees. secretes a fine white filament that curls over Outbreaks of the pest in Israel have been the body. Older instars secrete a white rectan- attributed to interference with biological gular cover that has two distinct grooves. The control agents by exhaust fumes emitted adult male is winged and is capable of flight. by vehicles using nearby highways (Gerson, Labuschagne et al. (1995) studied the popula- 1975; Swirski et al., 1997). Many natural tion dynamics of the scale in South Africa enemies have been reported to attack and found that it was more abundant on M. mangiferae. In Israel, Microterys flavus the southern shaded sector of the mango tree (Howard) and Coccophagus eritreaensis where temperatures are more moderate. Compere are the most common parasitoids Sprays of methidathion, chlorpyrifos and (Avidov and Zaitzov, 1960) while in South Lo-Vis oil have been recommended for the Africa, Coccophagus pulvinariae Compere, control of A. tubercularis in Queensland. The Tetrastichus sp. and Marietta javensis insect growth regulator, buprofezin, has given (Howard) have been recorded (Kamburov, better control in field trials (De Faveri and 1987). Oil and malathion have been commonly Brown, 1995). In South Africa, Labuschagne recommended as chemical control measures et al. (1995) recorded the parasitoid, Encarsia (Ebeling, 1959; Avidov and Zaitzov, 1960). citrina (Crawford) and the predators Rhizobius Pulvinaria (Cloropulvinaria) psidii (Mas- lophanthae (Blaisdell), Chilocorus nigritus kell) is rated as a serious pest in India (Fabricius) and Aleurodothrips fasciapennis (Gopalakrishnan and Narayanan, 1989), but it (Franklin) attacking the scale. An aphelinid is apparently only a minor pest in Pakistan parasitoid, Aphytis sp., and the predatory where it is kept under control by natural nitidulid beetle, Cybocephalus binotatus enemies (Mahmood and Mohyuddin, 1986). If Grouvelle, were introduced into South Africa these are disrupted by chemical sprays, then from Thailand in 1995. They have been problems may be encountered. C. psidii can be released in the field and appear to have a serious pest of litchis in Australia (Waite and established (Labuschagne et al., 1996b; Daneel Elder, 1996) but does not affect mangoes there. and Dreyer, 1997). Pink wax scale, Ceroplastes rubens Maskell, is a common pest of mangoes in Australia, where severe infestations may develop as a result of natural enemy disruption through Soft scales (Homoptera: Coccidae) spraying (Plate 27). Heavy films of sooty mould cover the leaves and may also con- Swirski et al. (1997) noted that 63 species taminate the fruit. The introduced parasitoid, of soft scales have been recorded infesting Anicetus beneficus Ishii, can provide good mango, but of these only about six are con- control under unsprayed conditions, but sidered to be economically important. Heavy corrective applications of oil may be required

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in spring or late summer to coincide with the mango trees by spoiling their appearance presence of young scales (Cunningham, 1989). and changing social attitudes towards them This pest may also become a problem under (Agounké et al., 1988). similar circumstances in Florida, USA (Peña, 1993). BIOLOGICAL CONTROL In Benin, the coccinellid Chilocorus nigritis (F.) was the most common predator of R. invadens. Several other predators were found but there was no native Mealybugs (Homoptera: Pseudococcidae) parasitoid which attacked the newcomer. Narasimham and Chacko (1988) noted that DISTRIBUTION AND BIOLOGY Rastrococcus R. invadens was scarce in India. They deter- invadens Williams is a polyphagous mealybug mined that Anagyrus sp., later described which, in addition to mango, attacks a range as Anagyrus mangicola Noyes (Noyes, 1990), of hosts including citrus, breadfruit, banana, and an encyrtid, Gyranusoidea tebygi Noyes frangipani and Ficus spp. (Agounké et al., (Noyes, 1988), were worthy of further investi- 1988). The mealybug has been noted as a gation for the purpose of biological control serious pest of mango in Ghana since 1982, of R. invadens in West Africa. Detailed investi- and it has since spread to other West African gations, including host specificity studies, countries (Willink and Moore, 1988; Ivbijaro were carried out at the International Institute et al., 1992). It has been the subject of intensive for Biological Control (IIBC) in the UK. These study with respect to its biology and bio- showed that G. tebygi was unlikely to compete logical control. The adult females are pale with Epidinocarsis lopezi (De Santis), a green-yellow and covered with white wax, parasitoid being used for the biocontrol which extends in long filaments at the anterior of Phenacoccus manihoti Matile-Ferrero on and posterior ends. The first instars are cassava. It was introduced into Togo in 1987, yellow, and they prefer to settle along the and subsequently into Benin, Ghana, Nigeria, midrib of the leaf. Development takes 28–30 Gabon and Zaire, where it established easily days, with females living for 80–90 days and and effected good control (Neuenschwander, producing 160–190 young. Males are winged 1989). The dilemma of whether to introduce and they outnumber females by about six to A. mangicola into this successful biological one (Willink and Moore, 1988). control situation was solved when attempts Rastrococcus spinosus (Robinson) was to establish that parasitoid in the field failed reported to be a pest in southern Pakistan (Moore and Cross, 1993). (Mahmood et al., 1980) and in the Philippines (Morrill and Otanes, 1947), but more recent MONITORING AND CONTROL The spatial dis- literature from the Philippines (Bondad, 1989; tribution of the mealybug on mango trees was Anonymous, 1994) does not mention it as an studied by Boavida et al. (1992) who devel- economic pest. oped binomial sampling plans for estimating the pest’s population and the effect of natural DAMAGE The insect may infest leaves, flow- enemies. However, they considered the plans ers and fruits from which it sucks the sap, and were suitable only for estimating medium when it is present in large numbers, heavy to high populations of mealybugs, and that deposits of honeydew encourage the growth for low populations, selective sampling of of a thick film of sooty mould on the foliage, infested units would assist in determining which interferes with photosynthesis and what was happening with respect to natural reduces fruit yield. In Ghana, losses of more enemy populations. The only practical solu- than 80% have been reported and farmers, tion to the mealybug problem seems to rest desperate to rid themselves of the pest, have with biological control, which is making good resorted to cutting mango trees down (Willink progress. The application of chemical controls and Moore, 1988). Apart from the loss of pro- including neem extract and pirimiphos-ethyl duction of an important fruit, the mealybug has been to no avail, since the pest rapidly has affected the amenity aspect of community reinfests trees (Agounké et al., 1988) and, of

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course, any potential biological control agents midrib remaining. The weevils can be shaken are affected by this approach. from the tree and destroyed or, if necessary, Drosicha stebbingii (Green) (Margaro- they may be sprayed with carbaryl or didae) is an important pest in India and Paki- methamidaphos (S. Krairiksh, Thailand, 1999, stan (Prasad and Singh, 1976; Mohyuddin, personal communication). Deporus marginatus 1981; Mohyuddin and Mahmood, 1993). The Pascoe, the mango leaf-cutting weevil, feeds insect damages the shoots by feeding on them on the epidermis of young leaves, causing as they develop. The females lay their eggs in them to dry out and die (Tigvattnannont, the soil and the nymphs emerge to colonize 1988; Bondad, 1989). the shoots in December. Exclusion of nymphs Three species of weevil, Apoderus tranque- from the trees by banding the trunks with baricus F., Eugnamptus marginatus Pascoe gums, tar, grease, etc., and chemical control and Rhynchaenus mangiferae Marshall, are through soil treatment have been suggested recorded as damaging mango leaves in south by Lakra et al. (1980) and Srivastava (1981), but India. The larvae of R. mangiferae, the smallest none of these is particularly effective. of these, mine in the leaves. The adults are The mealybugs, Ferrisia virgata (Cock- unusual in that they have enlarged posterior erell) and Planococcus lilacinus (Cockerell), femurs and are able to jump like flea beetles. In are reported to be pests of mangoes in the severe outbreaks there may be 20–30 weevils Philippines (Anonymous, 1994). The red ant, on every leaf. The feeding by adults on the Oecophylla smaragdina (F.) is often associated leaves, as well as the mining by larvae, causes with them, protecting them from natural the leaves to dry out or become distorted, enemies. and the photosynthetic area can be severely reduced (Anantanarayanan and Subramanian, 1955). Weevils (Coleoptera: Curculionidae)

Over 100 species of citrus weevils have Whiteflies (Homoptera: Aleyrodidae) been recorded from the Caribbean (Wood- ruff, 1985) and many of these apparently feed Peña et al. (1998) state that Aleurodicus on the leaves of mango, though not all occur dispersus Russel and Aleurocanthus woglumi on every island (Murray, 1991). The adult Ashby, the citrus blackfly, are of economic weevils feed on the leaf margins, producing importance in mangoes in Venezuela and a characteristic jagged edge effect. Pachnaeus Florida. Damage to leaves may result in litus Germar and Pachnaeus citri Marshall defoliation and the honeydew produced are recorded from Cuba and Jamaica, encourages the growth of sooty mould respectively, where they may cause extensive (Angeles et al., 1971; Peña, 1993). Natural damage to the tree roots, and are thus known enemies in Florida include Encarsia opulenta as citrus root weevils (Van Whervin, 1968). (Silvestri) and Amitus hesperodum (Silvestri). Murray (1991) considered that the citrus weevils could increase in importance as the mango industry expanded in the Caribbean. Despite the presence of several natural Pests of the Trunk, Branches and Twigs enemies (Van Whervin, 1968), chemicals have generally been used to control the pests, Boring pests can kill a significant proportion but cultural methods should also play a of terminal branches on which the potential significant role. crop would be borne. While mango farmers In Thailand, the gold dust weevil, attempt to prevent such damage, the task is Hypomeces squamosus (Fabricius), often forms difficult because insecticide sprays must be clusters when feeding on mango leaves. applied before the eggs hatch and the larvae Under such circumstances the entire leaf commence to tunnel in the wood. To achieve lamina may be consumed, with only the this on large trees and especially with

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relatively primitive application equipment is control of leafhoppers in central Luzon almost impossible. appeared to have some effect on the shoot borer (G.K. Waite, 1998, unpublished).

Mango shoot borer (Lepidoptera: Noctuidae) Borers (Coleoptera: Cerambycidae) DISTRIBUTION AND BIOLOGY Chlumetia transversa Walker, the mango shoot borer, occurs In the Philippines the two species of longi- in Bangladesh (Shahjahan and Ahmad, 1978), corn beetle, Niphonoclea albata (Newman) and India (Tandon et al., 1975), Sri Lanka, Thai- Niphonoclea capito (Pascoe), known as twig land, Malaysia, Indonesia, Vietnam (Nguyen cutters, damage the twigs of mangoes. The et al., 1998b) and the Philippines (Bondad, eggs are laid singly in cavities created by the 1989). The eggs are laid singly on the shoot female beetle, which girdle the twig about or flower panicle and hatch in about 4 days. 400 mm from the tip. The beetle also removes They are described as being white in the most of the leaves from the twig so that their Philippines, while Chahal and Singh (1977) weight does not snap it from the tree before report that they are yellow in India. The larvae the developing larva has matured (Cendana mature in 9 days, at which time they are et al., 1983). The beetles are apparently never coloured purple on the dorsal surface and abundant, but one female can damage up light yellow on the ventral surface. The to 30 twigs. Control is mainly by removal of mature larvae drop to the ground to pupate in beetles when they are seen on the trees from the soil, the moth emerging after 14 days. June to September, cutting off infested twigs and destroying them, and smudging (smok- BIOLOGICAL CONTROL The larval para- ing) trees to drive the beetles away (Bondad, sitoids, Eurytoma sp. and Microbracon lefroyi 1989). DC., along with the fungus, Fusarium Longicorn beetles belonging to the genus oxysporum, are reported to attack the pest Batocera are considered to be a significant in Thailand (S. Krairiksh, Thailand, 1999, problem in India (Veeresh, 1988). The species personal communication). concerned are Batocera rufomaculata Degeer, Batocera rubus (L.), Batocera royilei (Hope) and DAMAGE The borer is a serious pest of Batocera numetor Newmann. Young trees may mango flowers as well as of the shoots be killed by larvae boring and feeding in the (Bondad, 1989). The larvae bore into the trunk (Sharma and Tandon, 1972). Natural shoots and the panicles, causing the tips to enemies are ineffective in preventing damage, wilt and often the whole branch some distance and there are no satisfactory chemical back from the tip to die. Damaged panicles controls. In Vietnam, Plocaederus ruficornis break or split and dry out, gradually shedding Newman is regarded as a serious pest of flowers (Shahjahan and Ahmad, 1978). mangoes because of the damage it causes by boring in branches and the trunks of trees MONITORING AND CONTROL Chemical con- (Nguyen et al., 1998b). trols need to be applied at a time when the Trees that have been weakened from eggs are laid and before the larvae bore into other causes, either pathological or environ- the plant tissues. Leafhopper sprays, particu- mental, are often subject to attack by larly of synthetic pyrethroids, suppress shoot particular species of ambrosia beetles. The borer infestations at flowering, but infesta- scolytid beetles, Hypocryphalus mangiferae tions on the vegetative flush require specific (Stebbing) and Xylosandrus compactus treatments. Anonymous (1994) suggests that (Eichoff) attack trunks and branches of the insecticides used in such sprays should be weakened mango trees in the Americas, systemic in nature to ensure contact with the where, once established in an orchard, they borer inside the shoot. Experimental trunk may initiate attacks on healthy trees (Peña and injections of imidacloprid applied for the Mohyuddin, 1997).

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Planthoppers (Homoptera: Flatidae) that at least some pollination is assisted by wind or gravity. The mango planthopper, Colgaroides acumi- There are numerous reports concerning nata (Walker), feeds on shoots, flowers and the insect fauna attending mango flowers and fruit in Queensland. Direct damage from its the effect on fruit set of their exclusion. Bhatia feeding activity is usually insignificant, but et al. (1995) found that on panicles that were the accumulation of sooty mould on the bagged to exclude insects fruit set was zero, honeydew secreted may affect fruit quality. compared with 4.3% set on unbagged panicles The eggs are laid in compact pods that are that allowed insects free access. Similarly, glued to the undersurface of mature leaves. Singh (1997b) recorded zero fruit set on Unidentified egg parasitoids normally keep bagged panicles and 1.6 fruits set on populations at low levels but occasionally unbagged panicles. Galán Saúco et al. (1997), infestations may require chemical control investigating the production of ‘Tommy (Cunningham, 1989). In Mexico, Aethalion Atkins’ mangoes under greenhouse cultiva- reticulatum (L.) causes similar problems. tion in the Canary Islands, found that when all insects were excluded no fruit was set but when bees were introduced and other insects had free access, there was a significant Termites (Isoptera: Termitidae) increase in fruit set. The make-up of the pollinating fauna of Several termite species are recorded as caus- mangoes has been studied in a number of ing damage to mangoes, mainly in Australia countries. Jirón and Hedström (1985), Bhatia and India. Mastotermes darwinensis Froggatt et al. (1995), Singh (1997) and Singh (1999) and Coptotermes acinaciformis (Froggatt) cause all report that Diptera, mostly belonging to severe damage to mangoes in northern Aus- the families Calliphoridae and Syrphidae, are tralia, while other species such as Neotermes the most common visitors to mango flowers insularis (Walker) and Nasutitermes graveolus in Costa Rica and India. Hymenoptera were (Hill) are less important. Odontotermes found to be more prevalent in terms of species lokanandi Chatterjee and Thakur, Odontoter- in Australia (Anderson et al., 1982), Israel (Dag mes gurdaspurensis Holmgren and Holmgren, and Gazit, 1996) and South Africa (Eardley Odontotermes wallonensis (Wassman), Odontot- and Mansell, 1994). Nevertheless, although ermes obesus (Rambur) and Odontotermes horai some species are probably more important Roonwal and Chotani along with Microtermes than others, there seems to be a consensus obesi Holmgren are all recorded as pests of that numerous species within the complex of mango in India (Peña and Mohyuddin, 1997). visiting insects contribute to the pollination of Termites attack the roots and trunks of trees, mango flowers. reducing their vigour and sometimes causing Experiments conducted by Anderson death. et al. (1982) in northern Australia showed that wasps and native bees, Trigona sp., were more effective pollinators than were large flies. Pollination Since mango flowers are generally considered to be unattractive to honeybees, Apis mellifera That pollination in mangoes is mediated Linnaeus (Free and Williams, 1976), and this by insects rather than wind was first pro- species is uncommon in northern Australia, posed and demonstrated by Popenoe (1917) Anderson et al. (1982) suggested that Trigona although Wester (1920), who has been sp. might be used in that part of the country supported by Davenport and Núñez-Elisea to augment the pollinating fauna, since it is (1997), maintained that wind may be more common and prevalent on mango blossom important than insects in some environments. and can be hived. Trigona spp. are also Free and Williams (1976) found that mangoes associated with mangoes in Costa Rica, and were able to set fruit even though insects had although they are regarded as important for- been excluded by bagging, thus suggesting est pollinators, they appear to be unimportant

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in pollinating mangoes. Rather, they are thus reduced, especially if the sprays that are regarded as a nuisance because they chew applied have some degree of selectivity for small pieces of bark from the trees to make the pests. their nests. There is also a suggestion that they In a perennial crop such as mango, may be vectors of the bacterium, Erwinia (Jirón orchard ecosystems are able to stabilize over and Lobo, 1995). the years, except for periodic seasonal disrup- In Thailand, A. mellifera is kept for large- tion due to the application of necessary pesti- scale honey production and pollinating cides during the cropping season. Crops that longans, but Apis cerana Fabricius is pre- are to be consumed locally may not require ferred for small-scale honey production and the intensity of pesticide application that is for pollinating mangoes (Wongsiri and Chen, required for fruit destined for central or urban 1995). Sharma et al. (1998) conducted studies markets, or for export. The latter must not only in India to develop in-tree rearing of flies that be sound and of good eating quality, it must would assist in mango pollination. Several also have good appearance. Unfortunately, species, the most numerous of which were the high standard demanded for the cosmetic Lucilia sp. (Calliphoridae) and Sarcophaga sp. appearance of the fruit often results in exces- (Sarcophagidae), were reared from natural sive spraying, which in turn leads to the populations infesting fish or mutton pieces outbreak of secondary pests. Van Mele et al. that were placed in mesh bags and hung in the (2001) have presented a thorough appraisal lower branches of mango trees. of mango farmers’ perceptions and pest management practices in the Mekong Delta of Vietnam. They found that mango farmers made control decisions based on damage Mango Pest Management symptoms and not on the identification of the causal agent. This often resulted in Insect pest control in food crops has moved the application of inappropriate chemicals, through the post-World War II phase of a practice that was exacerbated by recom- indiscriminate application of a range of mendations made by pesticide retailers. chemical pesticides, to a more enlightened It is important that research on specific era of integrated pest management (IPM). IPM systems is continuous, so that new non- The aims of IPM are to reduce pesticide disruptive tactics can be introduced into the usage, and therefore environmental contami- system as they become available, by research- nation and health effects on consumers and ers who are familiar with the operation and farm workers, while adequately protecting a requirements of the system. Adequate and crop from pests to ensure that the farmer is effective extension of research results or able to obtain a reasonable return. Through a transfer of technology (TOT) to the farmers, better understanding of orchard ecosystems is difficult to accomplish, even in developed and the dynamics of pests and their natural countries with universities and departments enemies, together with efficient monitoring of agriculture using sophisticated advisory of the populations of both groups, decisions systems. If necessary, a systems approach can be made as to whether chemical interven- should be adopted with the development of tion is necessary. With the aid of an effective sustainable farming systems, in which IPM monitoring system and a good understand- can play a pivotal role. Such an approach is ing of the interrelationships between pests discussed by Litsinger (1993), especially with and their natural enemies, the proper timing respect to developing countries. In addition, of fewer sprays for the control of key pests for farmer knowledge should not be ignored, which there are no alternative controls allows since farmers are innovative and often have the complex of beneficial species that attacks excellent knowledge concerning the habits all of the potential pests in an orchard to oper- and occurrence of certain pests, which can ate to near its maximum capacity. The chance save research personnel much time. Farmers that minor pests will flare up, which could should also be enlisted to assist in the research, precipitate the application of more sprays, is since learning in a participatory way allows

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them to see at first hand how ecosystems C.A. (eds) Progress in Acarology, Vol. 2. work, and what relationships exist between Oxford-IBH, New Delhi, pp. 109–114. pests, natural enemies and the crop. In addi- Alam, M.Z. (1972) Some Insect and Mite Pests of Fruit tion, they are able to inform the researchers in Trees in East Pakistan and Their Control (revised edition). Bangladesh Agricultural Research the early stages of development of particular Institute, Dacca, 120 pp. management approaches, what is and what Alam, S.N. (1994) Population dynamics, varietal is not acceptable from the practical farming reactions and microbial control of different point of view. The ‘farmer first’ approach has species of mango leafhoppers. MSc thesis, been found to provide a good basis not only University of the Philippines, Los Baños. for conducting research, but also for having Ali, M. (1978) A report on the wax scales, Ceroplastes the findings of that research adopted (Cham- ceriferus Green and Chloropulvinaria polygonata bers et al., 1989). A whole crop approach to (Ckll.) (Homoptera: Coccidae) on mango and technology transfer in mangoes that includes their natural enemies. Bangladesh Journal of information on pests has been adopted in Zoology 6, 69–70. Aluja, M. (1994) Bionomics and management of Queensland. Crop-specific information kits Anastrepha. Annual Review of Entomology 39, that are part of the Agrilink Series address 155–178. damage symptoms, the likely cause of the Aluja, M., Celedonio-Hurtado, H., Liedo, P., symptoms and the most appropriate control Cabrera, M., Castillo, F., Guillén, J. and Rios, E. strategies (Meurant et al., 1999). (1996) Seasonal population fluctuations and An examination of the mango industries ecological implications for management of throughout the world suggests that in most Anastrepha fruit flies (Diptera: Tephritidae) there are key pests for which the only practical in commercial mango orchards in southern control is to apply insecticides. When this is Mexico. Journal of Economic Entomology 89, 667. the case, monitoring for the presence of pests Aluja, M., Jiménez, A., Piñero, J., Camino, M., Aldana, L., Valdés, M.E., Castrejón, V., Jácome, assumes high importance. Strategies that rely I., Dávila, A.B. and Figueroa, R. (1997) Daily on calendar sprays can be replaced with man- activity patterns and within-field distribution aged spraying programmes if monitoring and of papaya fruit flies (Diptera: Tephritidae) threshold levels are well developed. While in Morelos and Veracruz, Mexico. Journal of there are very few effective pesticides avail- Economic Entomology 90, 505–520. able that are target-specific or generally ‘soft’ Anantanarayanan, K.P. and Subramanian, T.R. on beneficial species, it may be possible, (1955) A note on the unusual occurrence of the through the adjustment of dosage rates mango leaf-weevil (Rhynchaenus mangiferae, and timing, to ameliorate the side effects of Mshll.) at Coimbatore. Madras Agricultural necessary sprays. Journal 42, 373–376. Anderson, D.L., Sedgeley, M., Short, J.R.T. and Allwood, A.J. (1982) Insect pollination in mango in northern Australia. Australian References Journal of Agricultural Research 33, 541–548. Andrews, K. and Poe, S. (1980) Spider mites Abou-Awad, B. (1981) Ecological and biological of El Salvador, Central America (Acari: studies on the mango bud mite, Eriophyes Tetranychidae). Florida Entomologist 63, mangiferae (Sayed), with description of the 502–505. immature stages (Eriphyoidea: Eriophyidae). Angeles, N., Dedordy, N., Paredes, P. and Requena, Acaralogia 22, 145–150. J. (1971) Citrus blackfly in Venezuela. Agounké, D., Agricola, U. and Bokonon-Ganta, Agronomia Tropical 21, 71–75. H.A. (1988) Rastrococcus invadens Williams Anonymous (1994) Major insect pests and diseases (Hemiptera: Pseudococcidae), a serious exotic of mango and their control. In: The Mango Tech- pest of fruit trees and other plants in West nical Committee. The Philippines Recommends Africa. Bulletin of Entomological Research 78, for Mango. Los Baños, Laguna: PCARRD and 695–702. PARRFI, 124 pp. Agrawal, L. and Singh, J. (1988) Present status of Avidov, Z. and Zaitzov, A. (1960) On the biology Eriophyes mangiferae in eastern Uttar Pradesh. of the mango shield scale, Coccus mangiferae In: ChannaBasavanna, G.P. and Virakta-math, (Green), in Israel. Ktvim 10, 125–137.

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Singh, G. (1997b) Pollination, pollinators and Lepidoptera). Indian Journal of Horticulture 32, fruit setting in mango. Acta Horticulturae 455, 154–155. 116–123. Tandon, P.L., Lal, B. and Rao, G.S.P. (1983) Predic- Singh, J. and Mukherjee, I.N. (1989) Pest status of tion of mangohopper Idioscopus clypealis (Leth.) phytophagous mites in some northern states of population in relation to physical environ- India. In: Proceedings of The First Asia-Pacific mental factors. Entomon 8, 257–261. Conference of Entomology. Chiang Mai, Thai- Thontadarya, T.S., Viswanath, B.N. and Hiremath, land, pp. 192–203. S.C. (1978) Preliminary studies on the control Singh, K.P. (1999) Evaluation of the pollination of mango hoppers by stem injection with efficiency of different insects on mango systemic insecticides. Current Science 47, 379. (Mangifera indica). Indian Forester 125, Tigvattnannont, S. (1988) Biological and auto- 333–335. ecological studies of the mango leaf-cutting Sohi, A.S. and Sohi, A.S. (Snr.) (1990) Mango weevil, Deporaus marginatus Pascoe (Coleop- leafhoppers (Homoptera: Cicadellidae) – a tera: Attelabidae). Khon Kaen Agricultural review. Journal of Insect Science 3, 1–12. Journal 16, 51–62. Soomroo, A., Khuhro, R. and Ansari, H. (1987) Tijero, R.F. (1992) El cultivo del mango en el Perú. Status of insects associated with mango Ediciiones Fundeagro 3, 53–54. blossom. Proceedings V Pakistan Congress of Umeya, K. and Hirao, J. (1975) Attraction of Zoology. Karachi, Pakistan, pp. 123–125. the jackfruitfly, Dacus umbrosus F. (Diptera: Soto-Manatiu, J., Jirón, L.F. and Hernandez, R. Tephritidae) and lace wing, Chrysopa sp. (1987) Chemical control and ecological obser- (Neuroptera: Chrysopidae) to lure traps baited vations of fruit flies of the genus Anastrepha with methyl eugenol and cue-lure in the Schiner (Diptera: Tephritidae) on mango. Philippines. Applied Entomology and Zoology Turrialba 37, 145–251. 10, 60–62. Srivastava, R.P. (1981) Comparative efficacy of United States Department of Agriculture (USDA) various insecticidal dusts against mango (1981) Plant Pest News 1. mealybug eggs. Indian Journal of Entomology 43, Van Dine, D.L. (1906) The mango weevil, Cryptor- 225–229. hynchus mangiferae (Fabr.). Hawaii Agricultural Srivastava, R.P. and Tandon, P.L. (1986) Natural Experiment Station Bulletin No. 17, 1–11. occurrence of two entomophagous fungi Van Halteren, P. (1970) Notes on the biology of pathogenic to mango hopper, Idioscopus the scale insect Aulacaspis tubercularis Newst. clypealis Leth. Indian Journal of Plant Pathology 4, (Diaspididae, Hemiptera) on mango. Ghana 121–123. Journal of Agricultural Science 3, 83–85. Steiner, L.F. and Lee, R.K. (1955) Large area tests of Van Lenteren, J.C., Loomans, A.J., Tommasini, male annihilation method for oriental fruitfly M.G., Maini, S. and Riudavets, J. (1995) Biologi- control. Journal of Economic Entomology 48, cal Control of Thrips Pests. Wageningen Agri- 311–317. cultural University Press, Wageningen, 201 pp. Steiner, L.F., Mitchell, W.C., Harris, E., Kozuma, T. Van Mele, P., Cuc, N.T.T. and Van Huis, A. (2001) and Fujimoto, M. (1965) Oriental fruit fly Farmers’ knowledge, perceptions and prac- eradication by male annihilation. Journal of tices in mango pest management in the Economic Entomology 58, 961–964. Mekong Delta, Vietnam. International Journal Swirski, E., Ben-Dov, Y. and Wysoki, M. (1997) of Pest Management 47, 7–16. Mango. In: Ben-Dov, Y. and Hodgson, C.J. Van Whervin, L.W. (1968) Citrus weevils of Jamaica (eds) Soft Scale Insects – Their Biology, Natural and some of their parasites. Technical Bulletin Enemies and Control (7B), pp. 241–254. No. 1, Citrus Research Unit, UWI, St Augustine. Syed, R.A., Ghani, M.A. and Murtaza, M. (1970) Vayssieres, J.F. (1997) Enquête sur les arthropodes Studies on the trypetids and their natural ene- ravageurs et auxiliaires du litchi à la Réunion. mies in west Pakistan. IV. Further observations Réport au Département des Productions Fruitières on Dacus (Strumeta) dorsalis Hendel. Technical et Horticoles, CIRAD-FLHOR, Ile de la Rèunion, Bulletin of the Commonwealth Institute of Bio- 40 pp. logical Control 13, 17–30. Veeresh, G.K. (1988) Pest problems in mango Tandon, P.L. and Verghese, A. (1987) New insect – world situation. Acta Horticulturae 123, pests of certain fruit crops. Indian Journal of 551–565. Horticulture 44, 120–121. Verghese, A. (1998) Effect of imidacloprid on mango Tandon, P.L., Krishnaiah, K. and Prasad, V.G. hoppers, Idioscopus spp. (Homoptera: Cicadel- (1975) Chemical control of mango shoot lidae). Pest Management in Horticultural Eco- borer Chlumetia transversa Walker (Noctuidae: systems 4, 70–74.

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Verghese, A. and Rao, G.S.P. (1985) Sequential sam- Wharton, R.A. and Marsh, P.M. (1978) New pling plan for leafhoppers, Idioscopus clypealis world Opiinae (Hymenoptera: Braconidae) Lethierry. Entomon 10, 285–290. parasitic on Tephritidae (Diptera). Journal Verghese, A., Tandon, P.L. and Rao, G. (1988) Eco- of the Washington Academy of Sciences 68, logical studies relevant to the management of 147–165. Thrips palmi Karny on mango in India. Tropical White, I.M. and Elson-Harris, M. (1992) Fruit Flies Pest Management 34, 55–58. of Economic Significance: Their Identification and Verheij, E.W.M. (1991) Mangifera indica L. In: Bionomics. CAB International, Wallingford, UK Verheij, E.W.M. and Coronel, R.E. (eds) Plant 601 pp. Resources of South-East Asia, No.2, Edible Fruits Whitwell, A.C. (1993) The pest/predator/para- and Nuts. Pudoc, Waginingen, pp. 211–216. sitoid complex on mango inflorescences in Waite, G.K. and Elder, R.J. (1996) Lychee/longan Dominica. Acta Horticulturae 341, 421–432. insect pests and their control. In: Proceedings of Willink, E. and Moore, D. (1988) Aspects of the the Fourth National Lychee Seminar Including biology of Rastrococcus invadens Williams Longans. Yeppoon, Queensland, pp. 102–109. (Hemiptera: Pseudococcidae), a pest of fruit Waite, G.K. and Huwer, R.K. (1998) Host plants and crops in West Africa and one of its primary their role in the ecology of the fruitspotting parasitoids, Gyranusoidea tebygi Noyes bugs Amblypelta nitida Stål and Amblypelta (Hymenoptera: Encyrtidae). Bulletin of Ento- lutescens lutescens (Distant) (Hemiptera: mological Research 78, 709–715. Coreidae). Australian Journal of Entomology 37, Wolfenbarger, D.O. (1956) Controlling mango insect 340–349. pests. Florida Agricultural Extension Service Waite, G.K. and Petzl, N. (1994) A search for egg Circular 147, 1–14. parasites of Amblypelta spp. (Hemiptera: Wongsiri, S. and Chen, P.P. (1995) Effects of agricul- Coreidae) in south-east Queensland. In: tural development on honey bees in Thailand. Menzel, C. and Crosswell, A. (eds) Maroochy Bee World 76, 3–5. Research Station Report No. 7, pp. 13–14. Woodruff, R.E. (1985) Citrus weevils in Florida Waterhouse, D.F. (1998) Biological control of and the West Indies: preliminary report on sys- insect pests: Southeast Asian prospects. ACIAR tematics, biology and distribution (Coleoptera: Monograph No. 51, 548 pp. Curculionidae). Florida Entomologist 68, Wen, H.C. and Lee, H.S. (1986) Seasonal abundance 370–379. of the ceriferous wax scale (Ceroplastes pseudo- Wysoki, M., Ben-Dov, Y., Swirski, E. and Izhar, Y. ceriferus) in southern Taiwan and its control. (1993) The arthropod pests of mango in Israel. Journal of Agricultural Research of China 35, Acta Horticulturae 341, 452–466. 216–221. Yee, W. (1987) The mango in Hawaii. University of Wester, P.J. (1920) The Mango. Philippine Bureau of Hawaii Agricultural Extension Service Circular Agriculture Bulletin 18, 3–70. 388, 19–22.

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5 Pests of Papaya

Alberto Pantoja,1 Peter A. Follett2 and Juan A. Villanueva-Jiménez3 1Department of Crop Protection, University of Puerto Rico, Mayaguez Campus, PO Box 9030 Mayaguez, Puerto Rico, 00681-9030; 2USDA-ARS, Pacific Basin Agricultural Research Center, PO Box 4459, Hilo, Hawaii 96720, USA; 3Colegio de Postgraduados, Campus Veracruz, Apartado Postal 421, CP 91700 Veracruz, Veracruz, Mexico

Papaya Carica papaya L. is a major tropical after human intervention to control other fruit cultivated in frost-free areas. Papaya has pests, mainly fruit flies and leafhoppers. culinary, medical and industrial uses but Aphids and leafhoppers are important pests is mainly cultivated for its edible fruit. As due to their vector capacity, but rarely cause with most tropical fruits grown in diverse direct damage to the trees. geographical regions, papaya is affected by All species reported from papaya are pre- several arthropods. Fruit quality for the fresh sented in Table 5.1. Species that rarely attack market is important. Therefore, arthropods papaya, or species with unknown pest status that blemish the fruit skin, enter the fruit, or economic importance are only mentioned or feed on the pulp or seeds can cause briefly or are tabulated. Information on geo- high losses and are considered economically graphical distribution of the arthropod and important. the type of damage is provided. There are 134 species of arthropods that affect papaya (Table 5.1). Most of the species belong to the Hexapoda, while 12 belong to the Acarina. Twenty-six species are fruit flies Origin and Distribution of the Crop in the family Tephritidae. Eighty-seven species can potentially attack or damage the fruit, Papaya is cultivated in the tropical and but are mainly associated with the foliage neotropical regions of the world between 32° or the trunk. One species is a seed borer. Five North and South. Its origin in Central Amer- species affect the flowers, and three species ica and current distribution of the crop have are root feeders. At least 12 species are known been documented by Storey (1984), Campbell vectors of important papaya diseases. (1984), and Morton (1987). Although papaya In different papaya growing areas, fruit was probably cultivated by early civilizations, flies, leafhoppers, mites, and scale insects no botanical records are available prior to are considered key pests requiring frequent the arrival of Columbus in America (Morton, pesticide applications. Fruit flies are the most 1987). The wide and rapid dissemination of important papaya pests either due to their the crop from Central America to the Carib- direct effect on the fruit or for quarantine bean region, Asia, Africa, and the Pacific in related issues. Mites are usually secondary the 16th century is associated with its propa- pests causing economic damage especially gation by seed, aggressive growth, long-term

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 131

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132 A. Pantoja et al. b TR TR TR TR TR TR TR TR TR TR TR TR part FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, Plant FR FR FR FR FR FR FR FR FL FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, 1985 2000 2000 Gill, ., .,

al al and 1993 1993 1976 1976 et et 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 FAO, FAO, FAO, FAO, FAO, FAO, FAO, Martorell, Martorell, Ben-Dov FAO, FAO, FAO, FAO, Ben-Dov, Ben-Dov, FAO, FAO, FAO, Nakahara Ben-Dov References WI WI WI WI WI SA, SA, SA, SA, SA, WI PI, PI, PI, PI, PI., SA, WI WI WI NA, NA, NA, NA, NA, PI, SA, SA, a SA, NA, ME, ME, PI, ME, PI PI, ME, ME, EU, EU, EU, NA, EU, NA, NA, EU, EU, distribution CA, CA, CA, EU, CA, EU, EU, CA, CA, SA AU, AU, AU, CA, AU, CA, AU, AU, AU, PI ME AS, AS, AS, AS, AS, AS, AS, AS, AS, WI AF, AF, AF, CA,.NA, AF, AF, AF, AS, AF, AF, Geographical PI PI PI PI PI PI PI PI, WI AS, AF, Gill Duzee & L. (Distant) Van papaya. Guillou (Signoret) (Cockerell) (Green) Nakahara Brown Le China (Green) Lever

papuensis (Olivier) Cockerell

(F.) hesperidum

affecting szentivanyi (Nietner) (Green) Usinger (Walker) (Douglas)

chiton oleae

(L.) pyriformis tessellatus nigra mangiferae variegatus tuberculosa angraeci gossypii cocophaga costalis gallegonis lutescens theobromae

oleae coffeae

Arthropods discrepans hesperidum longulus angustatus viridula 5.1. Pentatomidae Tingidae

e Amblypelta Amblypelta Amblypelta Amblypelta Amblypelta Brachylybas Fulvius Nezara Corythucha Coccus Coccus Coccus Drepanococcus Eucalymnatus Milviscutulus Parasaissetia Philephedra Protopulvinaria Saissetia Saissetia Conchaspis l b Conchaspididae Coreidae Coccidae Miridae a T ORDER/Family HEMIPTERA HOMOPTERA

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Pests of Papaya 133 TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR TR

continued FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FR, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, FO, 1992 1999a,b 1999a,b 2000 2000 2000 2000 ., ., ., ., Granara, Franqui, Franqui, al al al al

et et et et and and and 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 FAO, FAO, Ben-Dov FAO, Ben-Dov Williams Ben-Dov Ben-Dov FAO, FAO, FAO, FAO, FAO, FAO, FAO, FAO, FAO, FAO, FAO, FAO, Medina Medina FAO, FAO, FAO, FAO, FAO, WI WI WI SA, SA, SA, PI, PI, PI, NA, NA, NA, ME, ME, ME, WI EU, EU, EU, SA, PI, CA, CA, CA, PI WI NA, PI AU, AU, AU AU AU AU AU, SA, PI CA, PI AS, AS, AS, AS, AS, AS, AS, ME, AS, AF, PI AS, PI AF, PI PI PI PI WI AF, PI AF, AF, AF, CA, PI AS, AF, PI PI PI AF, AS, PI PI AF, de Miller & Tozzetti) Watson Granara Watson & & & Gimpel (Morgan) (Targioni-Tozzetti) (Cooley) (Green) (Targioni Cockerell (Cockerell) Williams Morrison Williams Williams (Signoret) (Morgan) Signoret (Westwood) Mckenzie (Newstead) (Newstead) Mckenzie Green (Maskell) (Douglas) (Comstock) cockerelli pentagona ostreata (Risso)

dictyospermi pustulans Maskell

(Cockerell) jackbeardsleyi longispinus viburni

trilobitiformis samaraius nesophilus viridis citri

marginatus longispina destructor excisus macfarlanei aurantii comperei inornata orientalis biclavis

virgata

aegyptiaca purchasi seychellarum Willink

Dysmicoccus Ferrisia Nipaecoccus Paracoccus Planococcus Pseudococcus Pseudococcus Pseudococcus Aonidiella Aonidiella Aonidiella Aonidiella Aspidiotus Aspidiotus Aspidiotus Chrysomphalus Howardia Morganella Pseudaonidia Pseudaulacaspis Pseudaulacaspis Pseudoparlatoria Asterolecanium Icerya Icerya Icerya Steatococcus Asterolecaniidae Margarodidae Pseudococcidae Diaspididae

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134 A. Pantoja et al. b part VE VE VE VE VE VE VE VE VE VE VE FO, FO FO FO, FO, FO, FO FO FO FO FO FO FO FO FO FO FO FO, FO, FO FO, FO, FO, FO, FO, FO Plant 1994 1994 1994 1994 1994 Abreu, Abreu, Abreu, Abreu, Abreu, 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1999a; 1999a; 1999a; 1999a; 1999a; 1971 1971 1971 1971 Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Franqui, Namba, Namba, Namba, Namba, and and and and and and and and and and and and and and and and and and 2000 2000 2000 2000 and and and and Higa Medina Higa Higa Medina Medina Medina Medina Medina Medina Medina Medina Medina Medina Medina Medina FAO, FAO, FAO, FAO, Medina Higa Medina Medina Medina Medina References WI SA, P., NA, a ME, WI EU, WI SA, distribution PI, SA, CA, PI., NA, AU, NA, EU, WI AS, WI WI WI WI PI PI, PI WI WI PI PI, PI WI CA, PI CA, Geographical SA, WI WI WI WI WI PI, WI WI WI WI WI AF, Bruner Davidson & Fonscolombe) & de (Thomas) Ashby (Fitch) (Mackie) (Quaintance) Russell (Quaintance) Metcalf Long (Osborn) Fonscolombe Oman Young Oman DeLong Ball Caldwell (Boyer . DeLong Harris (Thomas) de (Thomas) Patch Koch

(Sulzer) maidis

woglumi Glover acaciae laticeps euphorbiae

variabilis destructor dispersus

papayae canavalia dilataria fabalis insularis stevensi solana fasciatus Boyer aurantii puertana

Continued complectus persicae coreopsidis craccivora gossypii middletonii nerii spiraecola 5.1.

e Empoasca Empoasca Empoasca Empoasca Emposaca Empoasca Empoasca Poeciloscarta Sanctanus Oliarus Omolicna Trialeurodes Aleurocanthus Aleurodicus Aleurodicus Tetraleurodes Aphis Aphis Aphis Aphis Aphis Aphis Macrosiphum Myzus Rhopalosiphum Toxoptera l b Derbidae Cixiidae Aleyrodidae Cicadellidae Aphididae a T ORDER/Family

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Pests of Papaya 135 VE VE FR, FR, FR FR

continued FL, FL, RO FL, FL, FO, FO, FO FO, FO RO TR FR RO FR FR FR FR FR FR FR FR FR FR FR FR FR FR FR FO, FO, 1999 .,

al 1992 1992 1992 1992 1992 1992 1992 1992 1992 1992

et Medina 1970 Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, 1972 1972 .,

al 1994; and and and and and and and and and and 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000

et White FAO, White White White White FAO, White White FAO, FAO, White FAO, White FAO, FAO, FAO, FAO, FAO, White FAO, Yee Sakimura, Sakimura, FAO, Abreu, WI PI SA, ME, NA WI PI WI NA, PI AS, PI PI PI CA, NA, PI AU AF, AS, AS, PI AU, AU PI PI PI PI PI PI PI PI PI PI NA, PI CA, Percheron) (Giard) (Hardy) & (Pergande) Fairmaîre (Boisduval) (Linnaues) Murray (L.) (Froggatt) (Schiner) (Coquillett) (Loew) (Coquillett) (Tyron) (French) (Hendel) Montr. (Loew) (Coquillett) (Gory (Coquillett) (Tryon) (Hinds) (Tryon) (Froggatt)

obscurus

rubrocinctus Lindeman occidentalis fusca hemipterus maculatus ludens suspensa bryoniae cucumis cucurbitae dorsalis diversa facialis frauenfeldi jarvisi kirki melanota musae neohumeralis passiflorae crassiusculus abbreviatus vieillardi

orientalis

tabaci

Selenothrips Thrips Frankliniella Frankliniella Acicnemis Diaprepes Rhabdoscelus Metamasius Araecerus Carpophilus Protaetia Anastrepha Anastrepha Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Scarabaeidae Anthribidae Curculionidae Tephritidae Thripidae Nitidulidae COLEOPTERA DIPTERA THYSANOPTERA

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136 A. Pantoja et al. b TR part FR FR, FR SE FR FR FR FR FR FR FR ? FR NR FR, FO FO FO, FO FO FO FO FO, FO FO, FO Plant 1992 1992 1992 1992 1992 1992 1992 1992 1992 1992 1999a,b 1999a,b 1999a,b 1999a,b 1999a,b 1992 Franqui, Franqui, Franqui, Franqui, Franqui, Chacín, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, Elson-Harris, 1969 and and and and and and and and and and and and and and and and 2000 2000 2000 2000 2000 White White White White White White White White White Weems, White Medina Medina FAO, FAO, Clavijo Medina Medina Medina FAO, FAO, FAO, References WI SA, PI, NA, a ME, EU, distribution WI WI CA, SA, SA, PI AU, NA, NA, NA PI PI ME WI AU, AS AS, WI AF AF, AF AS, AS, CA, WI PI, PI PI SA, CA, WI WI CA, PI PI Geographical PI AU, PI AS, AF, Grote Walker Gerstaecker (Guenee) Wals (Hering) (Broun) (Enderlein) Busck Drew (Saunders) . (Clerck) (Froggatt) (Wiedemann) (Walker) merianae (Bigot) Guérin-Méneville Hufnagel Dyar (Drury) Karsch orneodalis curvicauda fasciculana minuscula (L.) trilineola tryoni xanthodes zonata lemniscata fullonia

capitata catoirii rosa emigratella plagiata nigroscutellata Continued alope ello lassauxi carica ipsilon bivittatus 5.1.

e Bactrocera Bactrocera Bactrocera Bactrocera Ceratitis Ceratitis Ceratitis Dacus Euphranta Myoleja Toxotrypana Epitomiptera Agrotis Eudocima Tiracola Erynnis Erynnis Erynnis Davara Amorbia Adoxophyes Decadarchis l b Phycitidae Tortricidae Sphingidae Noctuidae a T ORDER/Family LEPIDOPTERA

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Pests of Papaya 137 VE America, FR FR FR FR FR FR FR FR FR, FO, FO, FO, FO, FO FO FO FO, FO, FO, FO, FO, South = SA 1994 1994 1994 Abreu, Abreu, Abreu, Islands, 1994 1999a; 1999a; 1999a; Pacific host. = Abreu, PI Franqui, Franqui, Franqui, 1970 1970 1970; doubtful ., ., ., 2000 2000 = and and and

1994 1994 al al al America, ? 2000 2000 , et et et North FAO, BIOSIS, Medina FAO, BIOSIS, Yee Yee Abreu, Medina Abreu, Medina Yee = recorded NA not = East, NR Middle WI = vector, = PI, ME VE SA, NA, WI WI trunk, Europe, = = PI, AF, PI, WI TR EU AS, SA, WI PI, ME, WI seed, WI WI AU, WI PI AF, SA, WI PI SA, PI, CA, = America, SE Central roots, = = CA RO (Banks) (Boisduval) flowers, Australia, Ewing =

latus = Ehara (Geijskes) (McGregor) (Banks) FL Koch Keifer AU Keifer (Tucker)

banski Caribbean. Asia,

cinnabarinus urticae tumidus truncatus & foliage, phoenicis =

ornata pavoniformis = citrifolli brionese distribution spp AS FO Indies fruits, affected Africa, West Calacarus Calacarus Polyphagotarsonemus Tydeus Eutetranychus Tetranychus Tetranychus Tretanychus Tetranychus Brevipalpus Tuckerella Tuckerella = = = Tenuipalpidae Tydeidae Tuckerellidae Eryophidae Tetranychidae Tarsonemidae Geographical Part WI ACARI a b FR AF

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138 A. Pantoja et al.

seed viability, high economic returns, and is used to tenderize meat, clarify beer, its adaptation to wide and diverse soil treat digestive disorders, degum natural silk, conditions and climates (Harkness, 1967; extract fish oil; it is also used in shampoos and Seelig, 1970; Campbell, 1984). face-lifting preparations, in leather and rayon This herbaceous plant is also known as industries, in the manufacture of rubber and papaw, paw paw, kapaya, kepaya, lapaya, chewing gum, in photography, etc. The value tapaya, papayao, papaya, papaia, papita, of papaya as a medicinal plant is well known lechosa, fruta bomba, mamon, mamona, (Quisumbing, 1951; Chopra, 1958; Nuñez, mamao, and tree melon, and belongs to the 1982). The United States Food and Drug dicotyledonous family Caricaceae. This small Administration (USDA-FDA) approved the botanical family, indigenous to tropical and use of chymopapain for treatment of lumbar subtropical America, is represented by 31 spe- hernia in humans (Duke, 1983, 1984). Seed cies. Carica papaya is the most economically extracts have bactericidal potential (Emeruwa, important and widely cultivated species, 1982). Sharma and Ogbeide (1982) suggested while Carica pubescens (A.D.C.) Solms-Laumb, the use of papaya as a renewable energy known as chamburro and babaco (C. heilbornii source for the production of alcohol fuels. Heilborn) are available in Latin American markets, but are of little economic importance. Even though C. pubescens and C. heilbornii Production have been studied for commercial production and as a potential source of resistance genes to According to FAO (2000), during 1998 more papaya viruses, their exploitation requires than 5.2 million t of papaya were produced further investigation and development in 47 countries. Brazil is the largest papaya (Campbell, 1984, 1996; Duke, 1985). producer with 32% of the total production (1,700,000 t). Nigeria (751,000 t), Mexico (498,000 t), Indonesia (489,948 t), and India Uses of Papaya (450,000 t) are among the top papaya producers. Brazil is the third country in area har- Papaya is mainly cultivated for its edible vested (35,000 ha), but has the highest yields fruit, but medical and industrial uses have (485,714 kg ha−1). During 1998, Nigeria har- been documented (Seelig, 1970; Morton, 1977, vested the largest area (90,000 ha) followed 1987; Duke, 1983, 1984; Yadava et al., 1990). by India (40,000 ha) (FAO, 2000). Most of the The intended use is important for pest control papain and papaya for industrial use come determinations, as fruit quality is a key factor from Africa. for fresh market consumption. Ripe fruits are In the USA, papaya is cultivated on all the mostly eaten fresh, but green fruits can be major islands of Hawaii and in Florida. The cooked as a vegetable or candied by cooking principal area of commercial production is on sugar. The leaves are used as greens Kapoho in the Puna district of the island of in tropical America, the flowers are eaten in Hawaii (Yee et al., 1970). Since the mid-1930s, Java, the bark is used for making ropes in the cultivar ‘Solo’ has been grown in Hawaii. Africa, and the tree is used as an ornamental The papaya ringspot virus-resistant variety plant (Duke, 1983). The foliage has also been ‘Rainbow’ is now replacing ‘Solo’ as the tested as green foliage to feed small mammals predominant variety in Hawaii and Oahu. (Aduku et al., 1989). Hawaii currently grows 1500 ha of papayas The latex of ripe fruits contains a proteo- with a farm gate value of approximately lytic enzyme, papain, used in industry and US$28 million in 1999 and production is for medical treatments. The industrial and increasing. medical uses of papain have been reviewed by Depending on the market and use, Duke (1984, 1985, 1990), Morton (1977, 1987), papayas are harvested green, ripe or unripe. Seelig (1970), Poulter and Cagygill (1985), In Hawaii papaya is harvested when the skin Nuñez (1982), and Yadava et al. (1990). Papain is 80% green. In Puerto Rico papaya to be

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candied in sugar is harvested green, while Pests Attacking the Fruit papaya for the local market is harvested when the skin is 20–25% yellow. Fruit quality for the Fruit flies market is very important. Fruits must be han- dled with extreme care to avoid scratching Fruit flies (Diptera: Tephritidae) are the only and bruising. group of insects that actually penetrate the pulp or seeds. In spite of their worldwide distribution, their economic status remains Arthropods Associated with Papaya unsolved. Twenty-six species from seven genera, Anastrepha (two species), Bactrocera As with most tropical fruits grown in varied (17 species), Ceratitis (three species), Dacus, geographical regions, papaya is affected by Euphranta, Myoleja, and Toxotrypana (one several arthropods that can be considered species each) attack papaya fruits (Martorell, key or secondary pests. No comprehensive 1976; Morton, 1987; White and Elson-Harris, worldwide list of papaya pests is available, 1992; Abreu, 1994; Medina and Franqui, but arthropods from specific regions have 1999a,b; FAO-GPPIS, 2000; Monzu et al., 2000). been reviewed by a few authors. Morton White and Elson-Harris (1992), McPheron (1987) reported 11 key arthropod pests and Steck (1996), and Thompson (1998) affecting papaya in a wide geographical provided information on the geographical area. FAO-GPPIS (2000) recorded 159 pests distribution, biology, natural enemies, and for papaya (71 species in the Arthropoda), synonyms of fruit flies. Most of the Dacus spp. but the list does not include many insects affecting papaya are now placed in the genus commonly found on papaya in the Americas Bactrocera. Only known from Africa, D. and the Caribbean region. Martorell and bivittatus (Bigot) is the only species in this Adsuar (1952) reviewed the insects associ- genus reported from papaya, but is consid- ated with papaya in the Antilles and Florida, ered a doubtful host (Wilson and Elson- while Wolcott (1933, 1948), Martorell (1976), Harris, 1992; Thompson, 1998). Medina et al. (1999), Medina and Franqui Tephritid fruit flies have been serious (1999a,b), and Abreu (1994) listed 32 species pests in Hawaii since the first species was of arthropods associated with papaya in found around 1895 (Harris, 1989). They are Puerto Rico. In Hawaii there are 26 species widespread, occurring from sea level to of insects and mites that attack papaya (Yee 2100 m elevation, and attack hundreds of et al., 1970; Anonymous, 2000; Follett, 2000). plants, including many crop species. Three In Australia fruit flies are a predominant species feed on papaya. The oriental fruit concern to papaya producers (Monzu et al., fly, Bactrocera dorsalis (Hendel), is the most 2000). common species and is found at all elevations. Table 5.1 provides a list of arthropods The Mediterranean fruit fly, Ceratitis capitata associated with papaya worldwide. The (Wiedemann), was once common at lower Hexapoda represent 91% of the total number elevations where papaya is primarily grown of species, and those remaining are in the but was displaced when the oriental fruit fly Acarina. Tephritid flies (Diptera) are the only appeared in 1945, and is now more frequent direct fruit and seed feeders with 26 species at higher elevations (Bess, 1953; Vargas (19%). Eighty-seven species of arthropods can et al., 1995). Melon fly, Bactrocera curcurbitae attack or damage the fruit under heavy infes- (Coquillett), also feeds on papaya at low tations. The majority of the species (93) attack elevations. the foliage or the trunk (42), five species affect the flowers, and three are root feeders. At least BIOLOGY Eggs of fruit flies are regularly 12 species are vectors of important papaya dis- laid below the skin of the ripening papaya eases and one mite species is vector of a fungal fruit and typically hatch in 1–4 days. Medflies pathogen. Homoptera is the largest group with and melon flies lay 10–15 eggs day−1, singly or 65 species (49% of the total) in 11 families. in clusters, whereas oriental fruit flies lay 130

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eggs per day usually in groups of ten, but not been reported as a pest of papaya on the sometimes as many as 100 or more (Messing, island (Martorell, 1976; Abreu, 1994; Medina 1999). Larvae will feed for 1–4 weeks, depend- and Franqui, 1999a,b; Medina et al., 1999). ing on temperature, and drop from the fruit to pupariate in the soil under the papaya Toxotrypana curvicauda Gerstaecker plant. Adults emerge in 1–2 weeks. Damage to papaya fruits is caused primarily by larval The papaya fruit fly, T. curvicauda, is consid- feeding. ered to be the most damaging insect pest of papaya (Abreu, 1994; Heath et al., 1996; Bactrocera spp. Medina et al., 1999) (Plate 28). This species is present in Central America, the Caribbean, This genus, native to Asia, Australia, and and in tropical and subtropical areas of North the South Pacific, can be found in Africa and and South America, including Florida, USA temperate Europe (White and Elson-Harris, (Wolcott, 1933; Peña, 1986; Peña et al., 1986; 1992). Guiana, French Guiana, and Surinam Abreu, 1994; Landolt, 1994a,b; Medina et al., are the only papaya producing areas of the 1999). Although it was originally reported as neotropics where Bactrocera spp. are reported an exclusive host of C. papaya (Knab and (Harris, 1989; White and Elson-Harris, 1992). Yothers, 1914; Wolfenbarger and Walker, Seventeen species of Bactrocera are known 1974; Castrejón and Camino, 1991), recent to affect papaya. Monzu et al. (2000) and studies have demonstrated a broader host Huxham (2000) list Bactrocera papayae (Drew range, including other species of Caricaceae and Hancock) as one of the most threatening (Jacavita mexicana (A.D.C.) = Pileus mexicanus pests to papaya in Australia. The Asian Johnston), four species of the family Asclepia- papaya fruit fly B. papayae, a major poly- daceae, and occasionally mango, Mangifera phagous species recorded from 193 species indica L. (Weems, 1969; Castrejón, 1987; (Allwood et al., 1999), is native to South-East Castrejón and Camino, 1991; Peña, 1993; Asia, invaded Queensland in 1995 (Hancock Landolt, 1994a). et al., 2000) and was subsequently eradicated. The adult T. curvicauda fly resembles a Females can lay eggs in green papayas and common Polistes wasp in behaviour, size, form citrus and young bananas. Female B. papayae and general coloration. A long, slender, curved has a long ovipositor, allowing it to penetrate ovipositor, exceeding the length of its body, is past the sap layer of green fruits. a distinctive characteristic of this fly (Knab and Yothers, 1914; Medina et al., 1999). The long Anastrepha spp. ovipositor allows the female to lay the eggs (about ten per fruit) inside young fruits. The This genus is native to the neotropics and has preferred fruit size for oviposition is between not established itself outside the Americas 5 and 12 cm in diameter (Aluja et al., 1997b). (White and Elson-Harris, 1992). Two species Upon emergence, the larva feeds on the seed from this genus attack papaya (Swanson and mass and lining of the seed cavity, damaging Baranowski, 1972; Nguyen et al., 1993): the the fruit (Plate 29). In Puerto Rico, 84% fruit loss Caribbean fruit fly, Anastrepha suspensa has been observed in semi-commercial plots (Loew) (Weems, 1966; Swanson and (Abreu, 1994). The grown larva exits the fruit Baranowski, 1972; Nguyen et al., 1993) can to pupate in the soil. Depending on the tem- develop on fully ripe papayas (Lara et al., perature and soil humidity, larval and pupal 1989), but green papayas are resistant to development requires 15–17 days and 2–6 attack. The reduced preference for green weeks respectively (Weems, 1969; Landolt papaya fruits is associated with the presence et al., 1985; Peña et al., 1986; Aluja et al., 1997b). of benzyl isothiocyanate in the latex of green fruits (Seo et al., 1982a,b, 1983; Liquido et al., Ceratitis spp. 1989; Liquido, 1991c; Nguyen et al., 1993). Although A. suspensa is a pest of several Three species, C. capitata (Wiedemann), C. crops in Puerto Rico (Martorell, 1976) it has catoirii Guerin-Meneville, and C. rosa Karsch,

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are known from papaya. The Mediterranean measures involve insecticides and toxic baits. fruit fly, C. capitata, is a polyphagous pest Unlike other tephritids attracted to protein in almost all papaya producing areas of the baits, T. curvicauda does not require protein world. The distribution of C. catoirii, and C. for ovarian maturation, therefore baits based rosa is restricted to Asia and Africa (White on brown sugar and insecticides are and Elson-Harris, 1992; Thompson, 1998). recommended for control (Landolt, 1984b; Sharp and Landolt, 1984). Other control FRUIT FLY SAMPLING AND MONITORING Most measures include destruction of infested reports on the papaya fruit fly T. curvicauda are fruits and removal of wild hosts. from the USA and Mexico. Knab and Yothers Population suppression in papaya fields (1914) reviewed records and distribution of can be achieved by several methods. Sanita- the pest. Detailed descriptions of eggs, larvae, tion is a first step; fruits should be removed pupae, and adults were provided in this early as they ripen, and all fallen or infested fruit work. Further studies have concentrated on should be destroyed (Liquido, 1991b, 1993). adult behaviour and the male sex pheromone In Hawaii, sanitation is usually insufficient (Landolt and Hendrichs 1983; Landolt, 1984a; by itself because fruit flies are abundant Landolt et al., 1985, 1988, 1991; Landolt and on alternative host plants and can fly in Heath, 1988, 1990; Landolt and Reed, 1990; from outside areas. Insecticide protection is Aluja et al., 1997a,b). Peña (1986) and Peña possible using cover or bait sprays (Messing, et al. (1986) studied oviposition and feeding 1999). Malathion is the most commonly used behaviour on papaya seeds. Aluja et al. (1997a) insecticide but the microbe-derived toxin quantified daily activity patterns and within- spinosad may soon become a widely accepted field distribution of the papaya fruit fly, and alternative to malathion (Peck and McQuate, advised that if papaya plantations are mixed 2000). Malathion can be combined with (papaya, mango, avocado, soursop), both protein hydrolysate to form a bait spray within-orchard distribution and daily (Roessler, 1989). With bait sprays, male and movement patterns differ when compared female fruit flies are attracted to a protein with those observed in papaya planted as a source from which ammonia emanates. Bait monocrop. Sampling methods and the use of sprays are preferred to cover sprays because pheromone traps for T. curvicauda have been they are applied as spot treatments and the studied by Chuman et al. (1987), Landolt and impact on natural enemies is minimal. Heath (1988, 1990), Landolt and Reed (1990), Biological control has been tried on fruit Landolt et al. (1985, 1991), and Heath et al. flies with little success, but the potential of (1996). inundative parasitoid releases (Bautista et al., In Hawaii, fruit flies are monitored using 1998), alone or with bait sprays, is being traps baited with male lures. Methyl eugenol studied (Wood and Hardin, 2000). The is used to attract oriental fruit flies, cuelure parasitoid, Doryctobracon toxotrypanae (Marsh) is used for melon fly, and trimedlure (most from Costa Rica has been reported from widely used) or ceralure for medfly (CABI and T. curvicauda. The most effective parasitoid EPPO, 1997). Fay et al. (1997) reported that enemy of medfly and oriental fruit fly in methyl eugenol trapping and regular host Hawaii is Fopius arisanus (Vargas et al., fruit surveys are recommended in Australia 1993). Petcharat (1997) reports that Diachasmi- to monitor B. papayae. morpha longicaudata Ashmead (Hymenoptera: Braconidae) is responsible for 42% reduction CONTROL Several methods have been of B. papayae densities in Thailand. Male reported for papaya fruit fly control. Cultural annihilation, using attraction of males to control methods were reported by Aluja et al. insecticide-laced lures (Vargas et al., 2000), (1997a,b) and Landolt (1984b), while chemical and sterile insect techniques, using releases control measures were provided by Mason of large numbers of sterile flies to disrupt (1922), Wolfenbarger (1962), Conover and reproduction, have been used elsewhere to Waddill (1981), Peña and Nagel (1988), Aluja eradicate fruit flies but these tactics are not (1993, 1994), and Abreu (1994). Traditional presently considered feasible in Hawaii.

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Harvesting early is an effective means to Quarantine regulations require papaya to avoid fruit fly damage. Papayas are usually be treated before export from Hawaii to the fruit-fly-free when picked less than one- USA mainland and Japan. Currently, papayas quarter ripe (Seo et al., 1982a,b; Liquido et al., for export from Hawaii receive a single- 1989; Liquido 1990, 1991a,c). Although fruit temperature vapour heat treatment devel- continues to ripen after harvest, harvesting oped to disinfest fruit of fruit flies. This too early to avoid fruit fly infestation can treatment requires fruits to be heated to a fruit result in diminished fruit flavour, as fruit will centre temperature of 47.2°C during a treat- not ripen fully. ment duration of not less than 4 h (Armstrong In Mexico, T. curvicauda incidence is et al., 1995). A recent study showed that all affected by altitude and precipitation. In the stages of white peach scale on the surface of State of Veracruz, a low incidence of papaya papaya fruit are also killed by this vapour heat fruit flies is reported on ‘Cera’ type and treatment (Follett and Gabbard, 1999). the ‘Maradol’ variety (Machain, 1983). How- ever, at higher altitudes in Morelos State (1400–1800 m), T. curvicauda is a serious Arthropods Affecting the Foliage problem. Differences in varietal susceptibility and the Trunk have been documented for the ‘Hawaiian’ and ‘Cera’ varieties (Aluja et al., 1994). It is not clear Most of the arthropods associated with whether the effects of aggressive predators, papaya affect the foliage, the trunk or both unfavourable meteorological conditions, or (Table 5.1). Under heavy infestations some specific T. curvicauda strains are responsible species of scale insects, thrips and mites for such differences in papaya susceptibility in can affect flowers and fruits, but are usually Mexico. The combination of orchard design, associated with the trunk or the foliage. The trap crops, and border trappings have been orders Hemiptera, Homoptera, Thysanop- proposed as a means to reduce T. curvicauda tera, Coleoptera, Lepidoptera, and Acarina damage in commercial orchards in Mexico are associated with the foliage or the trunk (Aluja et al., 1997a,b). A trap crop of 10 m and represent 7, 49, 3, 5, 9, and 9% of the total surrounding the main block of papaya trees number of species reported for the crop, can reduce the incidence of T. curvicauda respectively (Table 5.1). A few species of (Aluja et al., 1997a,b). Hemiptera, Thysanoptera and Acari can also attack the flowers and fruits. ERADICATION A continuous effort to eradicate and prevent C. capitata from invading new areas of southern Mexico, northern Scale insects Central America, and the USA has been successful based on the strategic geographic location, and a permanent cooperative effort Thirty-eight species (28%) from 24 genera among phytosanitary authorities in Mexico, and six families of scale insects affect papaya. Guatemala, and the USA. Most agricultural Two families, Diaspididae and Coccidae, regions of Mexico have been free of the medfly represent 66% of the scale insects reported for decades. However, with a highly diversi- and 19% of the total number of arthropods fied agroecological system and heterogeneous related to papaya. social and cultural population structure, the confronting political, military, migratory and White peach scale, Pseudaulacaspis civil disputes make possible recurrent medfly pentagona (Targioni-Tozetti) invasions from southern regions into Mexico and the USA. Pseudaulacaspis pentagona (Targioni-Tozetti) (Homoptera: Diaspididae) has a cosmo- QUARANTINE Hawaii serves as a reservoir politan distribution and is one of the most for the introduction of tephritid fruit flies and economically important scale insects in other regulatory pests into the USA mainland. southeastern USA where it is a serious pest of

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peaches and other fruit and ornamental crops et al., 1987; Abreu, 1994) (Plate 30). Three (Nakahara, 1982; Gill, 1997). The white peach types of damage by this scale insect have scale was collected for the first time in Hawaii been documented: distortion of the apical in September 1997 on papaya. In Hawaii, its point during the seedling stage; flower and distribution is presently limited to the east leaf drop occuring after heavy infestations side of the island of Hawaii, but is expected to (Peña et al., 1987); and cosmetic damage expand rapidly. occuring if the females attach to the fruits Females begin laying eggs about 2 weeks (Peña et al., 1986; Abreu, 1994; Medina and after mating and lay their full complement of Franqui, 1999a). Damage to fruits is of con- eggs within 8–9 days. Eggs hatch in 3–4 days siderable importance, as affected fruits are after oviposition (Bennett and Brown, 1958). unmarketable; however, the pest status of Crawlers settle and begin feeding within 2 this insect remains unsolved. days after hatching and complete develop- The life history, natural enemies and ment in about 1 week. Two subsequent moults behaviour of P. tuberculosa have been studied requiring about 3 weeks produce adult by Peña and McMillan (1986) and Peña et al. females. Second instar males construct an (1987). Life span is 24 and 59 days for males oblong armour and after three moults become and females, respectively. Females produce winged adults. Progeny is produced only 87 crawlers per day in a 7-day oviposition through mating. The white peach scale period. Important natural enemies include initially attacks the trunks of papaya plants ten arthropods and Verticillium lecanii near the base. Overcrowding causes spread of (Zimmenn.). the scale up the trunk, and in heavily infested trees scales move up on to fruit, preferring to settle in the calyx and peduncle regions. Mealybugs White peach scale is a potential threat to the Hawaiian papaya industry as a source of Papaya mealybug, Paracoccus marginatus tree stress and fruit downgrading, and as a Williams and Granara de Willink quarantine pest on fruit for export. California, an important destination for Hawaiian papa- Paracoccus marginatus Williams and Granara yas, has given P. pentagona a ‘Q’ rating, mean- de Willink is a pest of papaya, cassava ing that the pest is not found in the state, yet (Manihot esculenta Crantz), Hibiscus spp., has economic pest status where it is known to aubergine (Solanum melongena L.), avocado occur. If live white peach scales are detected (Persea americana Mill.), annona (Annona during inspection in California, plant quaran- spp.), and sweet potato (Ipomoea batatas (L.) tine officials could take action, and this Lam.). The insect has been reported from scenario could also occur at other overseas papaya in Baja, California and from cassava destinations for Hawaiian papayas. in the central valleys of Mexico. The papaya mealybug occurs in tropical and subtropical CONTROL Elsewhere, P. pentagona is climates, principally in the coastal states of attacked by parasites and predators (Bennett, Mexico (Williams and Granara, 1992). The 1956; Collins and Whitcomb, 1975), but chemi- papaya mealybug has been reported since cal control is often required to prevent severe 1994 in the Caribbean islands of Antigua, crop injury. Control in the field in Hawaii has Belize, British Virgin Islands, the Dominican been attempted using Sunoil sprays to the Republic, Guatemala, Haiti, Nevis, St Kitts, trunk of the papaya tree with limited success. Puerto Rico, the US Virgin Islands and Costa Rica, and from continental USA (Florida) Philephedra tuberculosa Nakahara and Gill since 1998 (Miller et al., 1999). The insects feed on leaves, stems, fruits This scale insect is a pest of papaya, and even on seedlings. Mealybugs cause sugar apple, Annona squamosa L., soursop, deformation, wrinkling and rolling of the leaf Annona muricata L. and several species of edges and early leaf drop (Miller et al., 1999). ornamentals (Nakahara and Gill, 1985; Peña Attack to unripe fruits causes sap running

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and blemishes, a source of fruit downgrading. papaya producers apply insecticides on a Papaya fruits can be heavily infested with calendar basis, disrupting the natural pest mealybugs, becoming white and essentially balance. In Hawaii, during early spring, inedible. Under heavy infestations, the abaxial when natural enemies are low and plants side of the lower leaves can be covered with are susceptible, mite populations can reach insects that congregate near the main vein. densities that trigger the use of disruptive In Mexico, heavy infestations occur rarely in acaricides (i.e. beneficial predatory mites commercial orchards, probably due to the and pest mites are killed), and a pesticide presence of natural enemies. However, major treadmill begins for the rest of the season. infestations in Veracruz, Mexico, occur in June Three species of pest mites feed on prior to the summer rainy season (Valencia, papaya in Hawaii: the carmine mite, Tetra- 1975). nychus cinnabarinus (a key pest); the red and Diagnostic characters are a yellowish black flat mite, Brevipalpus phoenicis (an occa- body colour, with a series of short waxy sional pest), and a newly invading species, the filaments around the margin, of less than papaya leaf edge roller mite, Calacarus brionese one-quarter the length of the body. The ovisac (an eriophyid mite introduced into Hawaii is produced ventrally only, but can be two or in 1990 and currently spreading between more times the length of the body of the adult islands). Most recently the papaya leaf edge female. When specimens are placed in alcohol, roller mite has become a primary concern. they become blue-black, which is characteris- Otherwise considered secondary pests, tic of the species in this genus (Williams, 1986). present mainly during the dry season, mites Miller et al. (1999) reviewed the morphological are currently considered the most persistent characters of the adult female. papaya pest in Mexico. As a result of a production expansion during the 1990s, Mexican CONTROL Biological control appears to be growers relied on chemical control to produce the main factor keeping the species under high quality fruits and triggered an outbreak control in Mexico, where the most important of mites. natural enemies are Anagyrus sp., Acerophagus sp., near texanus Howard, and Apoanagyrus Carmine spider mite, T. cinnabarinus sp. (González et al., 1999). Common predators (Boisduval) are Chrysopa sp. and Chilocorus cacti L. which are usually found in low densities. Due to its T. cinnabarinus is a cosmopolitan species potential pest status in the Caribbean region, considered a papaya pest in several countries a classical biological control programme (Hernández et al., 1995). Females have an oval against P. marginatus was initiated, involving shape with a red or green coloration and introduction of parasites from Mexico into the a body from 0.4 to 0.5 mm in length. In a Bahamas and Florida, USA (González et al., 3-week life span the female oviposits 200 eggs 1999). on the abaxial side of the leaf. Eggs are about 0.1 mm long with an incubation period of 4–7 days. Males are smaller than females. As with most mites, larvae have six legs, and their Mites bodies are light pink. Nymphal development requires 3–5 days. The protonymphal and Twelve species of mites in seven genera affect deutonymphal stages, characterized by a red papaya. Mites are probably the most persis- to green coloration and the presence of four tent arthropod pests of papaya (Plate 31). The pairs of legs, require 6–10 days to complete lack of basic information on mite biology development. and ecology on papaya has prevented the Carmine mites feed on epidermal cells, development of effective management causing leaf curling, chlorosis, and plant practices. Naturally occurring predators can stunting. Mites can also cause premature yel- suppress mite populations after pesticides lowing and leaf drop as well as direct damage are removed from the system. However, most on small fruits. Mites feeding on developing

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fruits can cause fruit downgrading. In Puerto of P. macropilis is common in papaya, but den- Rico up to 79% of commercial papaya trees can sities are too low to effectively control mites. be affected by T. cinnabarinus (Abreu, 1994). In In Mexico a coccinellid, Stethorus sp., feeds on addition to direct feeding damage, the pres- spider mites, but their impact on controlling ence of T. cinnabarinus on Puerto Rican papa- natural populations has not been established. yas is associated with infection by Oidium spp. (Abreu, 1994). The combined effect of mites and fungal damage causes severe chlorosis. Leafhoppers (Homoptera: Cicadellidae) Broad mite, Polyphagotarsonemus latus Nine cicadellid species from three genera (Banks) (Tarsonemidae) (Empoasca, Poeciloscarta and Sanctanus) can Polyphagotarsonemus latus (Banks) is a cosmo- affect papaya (Table 5.1). Leafhoppers cause politan polyphagous species, with a wide two types of damage: direct feeding and sec- host range. Affected leaves curl up and break ondary damage as vectors (Plate 32). Symp- easily. Under severe infestations the foliar toms of leafhopper feeding include tip burn, area is reduced and leaves are severely wrinkling and cupping of the leaves, burning deformed and chlorotic. Abundant webbing of leaf margins in large trees, and stunting on the foliage is characteristic of this species. of smaller plants (Ebesu, 1985; Medina et al., The damage caused by this mite, sometimes 1999). Leafhoppers are more important for confused with symptoms of papaya ringspot their vectoring ability than for the mechanical virus, can be distinguished by the absence of damage. aqueous spots and ring forms on stems and In the Caribbean region, papaya pro- fruits, which are characteristic of the virus duction is severely limited by papaya bunchy infection. top disease, transmitted by Empoasca papayae In Puerto Rico and Brazil, P. latus is an Oman, E. stevensi Young, and E. insularis important pest, attacking papaya seedlings in Oman (Baker, 1936; Adsuar, 1946; Sein and greenhouses, while in Chiapas, Mexico, dam- Adsuar, 1947; Martorell and Adsuar, 1952; age by P. latus is severe under field conditions Nielson, 1968; Haque and Parasram, 1973; (M. de Coss, personal communication). Severe Fletchman, 1983; Web and Davis, 1987; Davis, stunting to seedlings was documented by 1994; Brunner et al., 1996; Davis et al., 1996, Abreu (1994) in Isabela, Puerto Rico. The 1997). There has been controversy on the causal damage caused by this mite in Brazil has agent of papaya bunchy top (Bird and Adsuar, been confused with papaya bunchy top 1952; Pontis, 1953; Eugene et al., 1968; Nielson, (Fletchman, 1983). 1968; Story and Halliwell, 1969). Recently Davis et al. (1996, 1997) reported that a rickett- CONTROL Sulphur dusting and mineral oils sia and not a phytoplasm is associated with are commonly used for mite control in Mexico; papaya bunchy top disease. Although attempts however, pesticide resistance is suspected in to culture the rickettsia in axenic culture have the dry Pacific regions, where T. cinnabarinus been unsuccessful, if this rickettsia causes the is the most important pest of papaya. Hawaii disease it will be the first report of a leafhopper- growers typically apply sulphur or a synthetic transmitted, lactifer-inhabiting, plant patho- acaricide on a calendar basis to suppress genic rickettsia (Davis et al., 1996, 1997). mites. The most effective predator in Hawaii Empoasca spp. and Puerto Rico appears to be the predatory mite, Phytoseiulus macropilis (Banks) (Prasad, In Puerto Rico, where the papaya bunchy 1966; Abreu, 1994). Two other predatory mites top was first reported (Cook, 1931), seven also commonly occur in Hawaii, Euseius sp. leafhopper species, Empoasca canavalia and Phytoseiulus hawaiiensis, but their dynam- DeLong, E. dilitaria Delong and Davidson, E. ics are poorly understood at present (Prasad, papayae Oman, E. insularis Oman, E. fabalis 1966). According to Abreu (1994) the presence DeLong, Poeciloscarta laticeps Metcalf and

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Bruner, and Sanctanus fasciatus (Osborn) are Boyer de Fonscolombe, Aphis gossypii Glover, associated with papaya (Martorell, 1976; Aphis spiraecola Patch, Myzus persicae (Sulzer) Ramirez, 1997); however, only two species, and Toxoptera aurantii (Boyer de Fonscolombe) E. papayae (the predominant species) and can be found on papaya plants (Namba and E. fabalis (secondary species), are commonly Higa, 1981; Abreu, 1994; Medina et al., 1999) collected from papaya and are associated or collected on water pan traps in papaya with papaya bunchy top (Ramirez, 1997). fields (Villanueva-Jiménez and Peña, 1991; The principal vector of papaya bunchy Rabara et al., 1996). Aphids are considered a top, E. papayae, is not known to occur in serious threat to papaya production due to Florida or Hawaii where another species, their ability to transmit diseases, in particular E. stevensi Young, is present. However, E. papaya ringspot virus (PRSV) and the papaya stevensi is reported to be a papaya bunchy mosaic virus (Adsuar, 1947a,b; Pontis, 1953; top vector in Trinidad (Young, 1953; Haque Nariani, 1956; Ishii and Holtzmann, 1963; and Parasram, 1973). This species was Khurana and Bhargava, 1971; Becerra, 1987). identified for the first time in Hawaii in 1980 Papaya production is limited by PRSV in as the cause of phytotoxaemia to papaya many areas of the world including Brazil, (Ebesu, 1985). Hawaii, India, Philippines, Puerto Rico, Little is known about the population Mexico, and Malaysia. In a 7-year study, dynamics and natural enemies of E. fabalis and Abreu (1994) found no aphids colonizing E. papayae (Martorell, 1976; Ramirez, 1997). papaya plants in Puerto Rico. Furthermore the biology and development of Several aphid species (M. persicae, M. both species are unknown on papaya plants. euphorbiae, A. spiraecola (= A. citricola), A. In Puerto Rico, E. papayae is the principal vec- gossypii, A. craccivora, A. nerii, Rhopalosiphum tor of papaya bunchy top (Brunner et al., 1996) maidis, and T. auranti (Boyer de Fosc) are representing 90% of the Empoasca spp. associ- capable of transmitting PRSV to papayas in ated with papaya (Ramirez, 1997). Heavy E. Hawaii (Ishii and Holtzmann, 1963; Namba papayae infestations on papaya are related to and Kawanishi, 1966; Higa and Namba, 1971; the presence of weeds in the field. The critical Namba and Higa, 1981; Labonne et al., 1992), period of susceptibility to papaya bunchy top Mexico (García, 1987; Villanueva and includes the first 90 days after transplanting Villanueva-Jiménez, 1994), and Puerto Rico (Brunner et al., 1996; Ramirez, 1997). This sug- (Adsuar, 1946; Martorell and Adsuar, 1952; gests that management practices for E. papayae Schaefers, 1969). should focus on the early period of plant PRSV produces distinct ringspots on establishment to reduce the contact between fruits, stunting of plants, and leads to a reduc- the insect vector and the crop. The natural tion in fruit production. Control is difficult parasitoid fauna of E. papayae have not been because the virus is transmitted by aphids established. in a non-persistent manner (Namba and Symptoms of E. stevensi feeding are simi- Higa, 1981). This means that the virus can lar to the familiar ‘hopperburn’ associated be acquired during brief probes, retained for with feeding by other Empoasca species several hours, and transmitted to a new host (Ebesu, 1985). In Hawaii, egg incubation within minutes. Thus, PRSV can be trans- requires 7–14 days and the nymphal period is mitted by non-colonizing species, and insecti- approximately 12 days. Adult feeding results cides may not be effective at preventing trans- in more severe injury than nymphal feeding mission (Namba and Higa, 1981). (Ebesu, 1985). In the early 1960s on the island of Oahu and in the late 1980s on the island of Hawaii, the chief papaya production areas at the time Aphids (Homoptera: Aphididae) were abandoned due to infestation by a highly virulent strain of PRSV (Ishii and Holtzmann, Aphids do not colonize papaya plants 1963). Recently, through genetic transforma- and are considered minor pests, but several tion with PRSV, a PRSV-resistant variety of species, Aphis coreopsidis (Thomas), Aphis nerii papaya, ‘Rainbow’, has been developed (Fitch

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et al., 1992). Areas previously abandoned Defoliators (Lepidoptera, Coleoptera) on both islands are now in cultivation with the transgenic variety. Papaya has few defoliators. Grasshoppers, hornworms and a weevil are reported as CONTROL Refined oil sprays have been defoliators. Little information is available on suggested as physical barriers for viral trans- these defoliators. mission. However, inconsistent results and high control costs prevent wide adoption of Hornworms this technology (Bhargava and Khurana, 1969; Hernández et al., 2000a). Organophosphate Hornworms (Lepidoptera: Sphingidae), are and carbamate insecticides are not recom- papaya and cassava (Manihot esculenta) pests mended, as sublethal doses can accelerate (Clavijo and Chacín, 1992; Abreu, 1994; viral transmission by exciting probing activity Medina and Franqui, 1999b). In Veracruz, in aphids. Applications of neem (Azadirachta Mexico, Erinnys ello (L.) is considered the indica A. Juss.) extracts affect aphid probing, most important papaya defoliator. In North, but do not prevent PRSV transmission Central, and South America the larvae can be (Hernández et al., 2000b; Pérez et al., 2000). found year round, but it is more abundant Integrated crop management strategies during the summer months. Three species, for papaya aphids have been developed in E. alope (Drury), E. ello, and E. lassuxi merianae Veracruz, Mexico (Flores et al., 1995), and Grote are reported from papaya in Puerto in the Philippines (Opina and Tomines, Rico (Martorell, 1976; Medina and Franqui 1996) to manage the viral disease and the 1999b), but damage is sporadic (Abreu, 1994). vectors. Barrier crops have been proposed as Last instar E. ello larvae are 90–120 mm a way to interfere with aphid landing and in length. Body colour varies from green, searching behaviour. The use of companion red, grey, yellow, to dark green or black. The crops such as sorrel (Hibiscus sabdariffa L.) larva feeds on leaves, destroying seedlings planted around the fields 2 months before and small trees and defoliating larger trees transplanting papaya may reduce the virus in a short time, then drops to the ground incidence (Becerra, 1989). The deep red to for pupation. The larva has a dorsal horn at purple H. sabdariffa coloration is believed the end of the abdomen. The pupae have to repel aphids from landing on papaya a reddish brown to black coloration. Moths fields. Intercropping barriers of maize or are nocturnal and present reddish brown to sorghum are used as intermediate landing grey forewings. Males have longitudinal dark crops in the Philippines (Andrade et al., 1994; spots on the forewings. The hindwings are Opina and Tomines, 1996). Aphids, carrying reddish brown with a dark brownish red mar- non-persistent virus, clean their stylets after ginal band with two dorsal black dotted lines feeding on the companion crops, reducing on the abdomen. Wing span is 80–90 mm. the viral infection (Andrade et al., 1994). Destruction of plants with viral symptoms CONTROL Weed control practices and soil reduces the source of primarily inoculum preparation can reduce adult and pupal and delays development of the infection in populations, respectively. In Mexico, manual the field (Becerra, 1987; Arenas et al., 1992). removal of last instar larvae is a common Protecting the seedlings under polypropylene practice in smallholdings; however, carbaryl or anti-aphid covers is recommended to and malathion have been used on small reduce rapid field infestations (Andrade larvae in large plantings (Machain, 1983). The et al., 1994). gregarious and polyembryonic braconid Little is known about natural enemies wasp, Apanteles sp., parasitizes hornworn of aphids on papaya. A coccinellid Cycloneda larvae. After completing its development, sanguinea L. found on papaya plants feeds on the parasitic larvae emerge to pupate by cov- aphids (Machain, 1983), but the effect of this ering hornworms with white cocoons. These predator on natural aphid populations still cocoons are very often hyperparasitized has to be determined. as well. According to Abreu (1994) natural

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control keeps hornworm under control in on papaya, feeding on leaves, fruit and roots Puerto Rican papaya orchards. (J.E. Peña, personal observation).

Minor Pests of Papaya Fruitspotting bugs

Yee et al. (1970) listed all the insect pests Six species of coreids from the genera known to occur on papaya in Hawaii at the Amblypelta and Brachylybas affect papaya in time and labelled them as major, minor, Australia, New Guinea, and the South Pacific or occasional pests. Minor pests on the list Islands (Brown, 1958a,b; Waite, 1990). The included the cotton aphid, Aphis gossypii; genus Amblypelta includes 15 species that potato aphid, Macrosiphum euphorbiae; south- attack several fruits, nuts, and papaya. The ern green stink bug, Nezara viridula; southern most damaging species are A. cocophaga garden leafhopper, Empoasca solana; black China, A. theobromae Brown and A. lutescens cutworm, Agrotis ipsilon; coconut scale, papuensis Brown (Brown, 1958b; Waite, 1990; Aspidiotus destructor; mining scale, Howardia Waite and Huwer, 2000). Waite and Huwer biclavis; obscure mealybug, Pseudococcus (2000) reviewed the host records and the pest obscurus; onion thrips, Thrips tabaci; the Texas status of Amblypelta in Australia. citrus mite, Eutranychus banksi; and two A few species of the orders Coleoptera tukerellid mites, Tukerella ornata, and T. and Lepidoptera are reported from papaya pavoniformis. The spiralling whitefly, Aleuro- in the Pacific islands (Table 5.1), but little is dicus dispersus Russell, was discovered in known about their importance and damage to Hawaii in 1978 and reportedly became a papaya production. Furthermore, little infor- serious pest soon after its introduction. Two mation is available on papaya pests from thrips, Frankliniella occidentalis and F. fusca, the Pacific islands, except for Hawai and are present in Hawaii and are known to Australia. be vectors of tomato spotted wilt virus on papaya (Sakimura, 1972). The impact these minor pests have on papaya production in Discussion Hawaii is unknown. Papaya is cultivated in semi-permanent stands in frost-free areas in the tropics and Diaprepes abbreviatus (L.) (Coleoptera: subtropics. A large number of arthropods are Curculionidae) associated with papaya. Fruits for fresh consumption and quarantine issues are impor- Puerto Rico and Florida are the only papaya tant marketing factors. Therefore, farmers producing areas reporting D. abbreviatus implement some type of pest management defoliating papaya. The diaprepes weevil tactic to harvest high quality, blemish-free is a known sugarcane and citrus pest fruits. Traditionally, most papaya producers (Wolcott, 1948; Martorell, 1996) that has been apply insecticides on a calendar basis. Public documented as causing defoliation to papaya pressure regarding pesticide regulation, the (Abreu, 1994). Although the pest status or disruption of the natural pest balance, con- economic importance of D. abbreviatus on tamination, resurgence of secondary pests, papaya has not been defined, up to 99 and the need for the least possible disruption D. abbreviatus adults per papaya tree have of the environment encouraged the search for been observed in northern Puerto Rico in natural pest control mechanisms. orchards where 51% of the trees were Human intervention to control fruit flies defoliated by the weevil (Abreu, 1994). The and leafhoppers on papaya has triggered out- diaprepes weevil is present in Florida, USA, breaks of mites and scales that can become on citrus and ornamentals (Schroeder and persistent pests of papaya. Naturally occur- Beavers, 1977) and lately it has been observed ring predators can suppress secondary pest

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populations after pesticides are removed from Biological and cultural control tactics on the system, but the lack of basic information papaya-based systems need further attention. on secondary pest biology and ecology on Culturally based practices can provide a first papaya has prevented the development of line of defence against secondary pests and effective management practices, thereby such practices are available for other crops encouraging producers to use pesticides. in countries producing papaya. Research and A clear understanding of the pest extension protocols should emphasize biology, behaviour, population dynamics integrating cultural and biologically based and pest status is the foundation for the practices in order to develop IPM and development of integrated pest management integrated crop management programmes. (IPM) strategies. Unfortunately, in spite of the economic importance and wide geographical distribution of the crop, papaya pest control, with the exception of fruit flies, has been References poorly studied. Currently, no IPM programme is available, even for an insect Abreu, E. (1994) Insectos de la papaya y prácticas de control. In: Memorias Foro: Cultivo, Producción y complex such as fruit flies, where abundant Manejo. Estación Experimental Agrícola de information on behavioural responses to Puerto Rico, Recinto de Mayagüez, Univ. pheromone and host finding, trapping sys- Puerto Rico, Aguadilla, Puerto Rico, 20 May tems, habitat manipulation, orchard design, 1994, pp. 58–62. and sanitation practices is available. Current Adsuar, J. (1946) Transmission of papaya bunchy and recent developments in the integration of top by a leafhopper of the genus Empoasca. sampling, and the use of food attractants and Science 103, 316. insecticides has allowed a reduction in the Adsuar, J. (1947a) Studies on virus diseases of use of broad spectrum pesticides; however, papaya (Carica papaya) in Puerto Rico. I. Trans- farmers rely heavily on insecticide use and mission of papaya mosaic. Journal of the Agri- culture University of Puerto Rico 31, 248–256. postharvest treatments to manage fruit flies. Adsuar, J. (1947b) Studies on virus diseases of Research is needed on biologically and cultur- papaya (Carica papaya) in Puerto Rico. II. Trans- ally based practices to manage indirect pests mission of papaya mosaic by green citrus and to integrate all available tactics for insects aphid (Aphis spiraecola Patch). Journal of the damaging the fruit. Agriculture University of Puerto Rico 31, 257–259. Aphids and leafhoppers are important Aduku, A.O., Dim, N.I. and Hassan, W. (1989) pests of papaya in the Americas and the Evaluation of green forages for dry season Caribbean mainly due to their vectoring feeding of rabbits. Journal of Applied Rabbit capacity. Factors affecting host finding and Research 12, 113–115. colonization by aphids and leafhoppers need Allwood, A.J., Chiranajariwong, A., Drew, R.A., Hanacek, E., Hancock, D., Hengsawad, C., to be studied and integrated to existing Jinapin, C., Jirasurat, M., Kong Krong, C., cultural practices for other pests, mainly Kritsaneepaiboon, S., Leong, C. and Vijaygase- fruit flies. Virus-resistant papaya varieties garan, S. (1999) Host plant records for fruit flies are available, but further work is needed (Diptera: Tephritidae) in South-East Asia. The on aphid sampling, host finding, colonization Raffles Bulletin of Zoology 7, 99 pp. and insect–pathogen relationships. Papaya Aluja, M. (1993) Manejo integrado de las moscas de la bunchy top is still a limiting factor for papaya fruta. Editorial Tirillas, México, D.F. production in the Caribbean, but little work Aluja, M., Jiménez, A., Camino, M., Aldana, L., has been conducted on the vector biology, Castrejón, V. and Valdés, M.E. (1994) sampling, natural enemies and the pathogen– Determinación de la susceptibilidad de tres variedades de papaya (Carica papaya) al ataque insect–plant relationship. Only poor to de Toxotrypana curvicauda (Diptera: Tephriti- modest relationships have been shown dae). Folia Entomológica Mexicana 90, 33–42. between aphids and leafhopper vectors and Aluja, M., Jimenez, A., Piñero, J., Camino, M., the number of affected plants in a field. It Aldana, L., Valdes, M.E., Castrejon, V., Jacome, is therefore unclear how chemical control of I., Davila, A.B. and Figueroa, R. (1997a) Daily adults will reduce damage. activity patterns and within-field distribution

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of papaya fruit fly (Diptera: Tephritidae) Coccoidea: Pseudococcidae and Putoidae) with in Morelos and Veracruz, Mexico. Journal of Data on Geographical Distribution, Host Plants, Economic Entomology 90, 505–519. Biology and Economic Importance. Intercept, Aluja, M., Jimenez, A., Camino, M., Piñero, J., Andover, 686 pp. Aldana, L., Castrejon, V. and Valdes, M.E. Ben-Dov, Y., Miller, D.R. and Gibson, G.A.P. (1997b) Habitat manipulation to reduce (2000) ScaleNet. http://www.sel.barc.usda. papaya fruit fly (Diptera: Tephritidae) dam- gov/scalenet/scalenet/htm age: orchard design, use of trap crops and Bennett, F.D. (1956) Some parasites and predators of border trapping. Journal of Economic Entomol- Pseudaulacaspis pentagona (Targ.) in Trinidad, ogy 90, 1567–1575. British West Indies. Canadian Entomologist 88, Andrade, H., Avila, C., García, E., Mora, A., 704–705. Nieto, D., Téliz, D. and Villanueva, J.A. (1994) Bennett, F.D. and Brown, S.W. (1958). Life history La mancha anular del papayo en Veracruz, and sex determination in the diaspine scale, México, y su manejo integrado. Séptima reunión Pseudaulacaspis pentagona (Targ.) (Coccoidea). científica del sector agropecuario y forestal del Canadian Entomologist 9, 317–324. Estado de Veracruz. GIP Grupo Interdisciplin- Bess, H.A. (1953) Status of Ceratitis capitata in Hawaii ario del Papayo, Veracruz, México, pp. 87–92. following the introduction of Dacus dorsalis Anonymous (2000a) Hawaii, Crop Knowledge and its parasites. Proceedings of the Hawaiian Master Papaya. http://www.extento.hawaii. Entomological Society 15, 221–234. edu/kbase/crop/crops/papaya.htm Bhargava, K.S. and Khurana, S.M.P. (1969) Papaya Anonymous (2000b) SCALENET. http://www.sel. mosaic control by oil spray. Phytopathologische barc.usda.gov/scalenet Zeitshrift 64, 338–343. Arenas, L., Avila, C., Cárdenas, E., Etchévers, J., BIOSIS (2000) http://www.york.biosis.org/triton/ Flores, C., García, E., González, V., Matheis, L., indexfm.htm Mora, A., Mora, G., Nieto, D., Riestra, D., Bird, J. and Adsur, J. (1952) Viral nature of papaya Téliz, D., Velázquez, J. and Villanueva, J. (1992) bunchy top. Journal of the Agriculture University La virosis del papayo en Veracruz: etiología y of Puerto Rico 36, 5–11. control. Quinta Reunión Científica del Sector Brown, E.S. (1958a) Revision of the genus Amblypelta Agropecuario y Forestal del Estado de Veracruz. Stal (Hemiptera: Coreidae). Bulletin of Entomo- Resultados y Avances de Investigación, at logical Research 49, 509–541. Veracruz. GIP (Grupo Interdisciplinario del Brown, E.S. (1958b) Injury to cacao by Amblypelta Papayo). Veracruz, México, pp. 62–71. Stal (Hemiptera: Coreidae) with a summary of Armstrong, J.W., Hu, B.K. and Brown, S.A. (1995) food plants of species of this genus. Bulletin of Single-temperature forced hot-air quarantine Entomological Research 49, 543–554. treatment to control fruit flies (Diptera: Brunner, B.R., Davis, M.J., Ferwerda, F.H., Ramirez, Tephritidae) in papaya. Journal of Economic L.M. and Pantoja, A. (1996) Recent advances in Entomology 88, 678–682. papaya bunchy top research. Annual Meeting of Baker, R.E.D. (1936) Papaya mosaic disease. Tropical the Puerto Rican Society for Agricultural Sciences, Agriculture 16, 159–163. 22 November 1996. Hato Rey, Puerto Rico. Bautista, R.C., Harris, E.J. and Lawrence, P.O. (1998) CABI and EPPO (1997) Quarantine Pests for Europe. Biology and rearing of the fruit fly parasitoid CAB International, Wallingford, Oxon, UK, Biosteres arisanus: clues to insectary propaga- 1425 pp. tion. Entomologia Experimentalis Applicata 89, Campbell, C.W. (1984) Papaya –tropical fruits and 79–85. nuts. In: Martin, F.W. (ed.) Handbook of Tropical Becerra L., E.N. (1987) Dinámica poblacional y Food Crops. CRC Press, Boca Raton, Florida, hospederas de áfidos vectores de virus de pp. 246–247. la mancha anular del papayo en Veracruz Campbell, R.J. (1996) South American fruits deserv- XIV. Congreso Nacional Fitopatología. Morelia ing further attention. In: Janick, J. (ed.) Progress Michoacán, Mexico, p. 11. in New Crops. ASHS Press, Arlington, Virginia, Becerra L., E.N. (1989) Preferencia del color de pp. 431–439. papaya (Carica papaya) y barreras de jamaica Castrejón, F. (1987) Aspectos de la biologia y (Hibiscus sabdariffa L.) Como medio para habitos de Toxotrypana curvicauda Geas- reducir la transmisión por áfidos de virosis taecker (Diptera: Tephritidae) en condiciones en papaya. Revista Mexicana Fitopatologia 7, de laboratorio y su distribucion en una 218–222. plantacion de Carica papaya L. en Yutepec, Ben-Dov, Y. (1993) A Systematic Catalogue of the Morelos. BS thesis, Instituto Politecnico Mealybugs of the World (Insecta: Homoptera: Nacional, Mexico, D.F.

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Wood, M. and Hardin, B. (2000) Spinosad battles O.V., Ishida, J.T., Keeler, J.T. and Nakasone, crop pests. Agricultural Research 48, 10–12. H.Y. (1970) Papayas in Hawaii. University of Woolcott, G.N. (1933) An Economic Entomology of the Hawaii Cooperative Extension Service Circular West Indies. Clay and Sons, Bungay, Suffolk. 436, 57 pp. Woolcott, G.N. (1948) The insects of Puerto Rico. Young, D.A. (1953) Empoascan leafhoppers of Journal of Agriculture of the University of Puerto the solana group with description of two new Rico 32, 101–145. species. Journal of Agriculture of the University of Yadava, U.L., Burris, J.A. and McCrary, D. (1990) Puerto Rico 37, 151–160. Papaya a potential annual crop under middle Zapata, R. (1994) A review of papaya research in Georgia conditions. In: Janick, J. and Simon, Hawaii, Florida, Guam, Virgin Islands, and J.E. (eds) Advances in New Crops. Timber Press, Puerto Rico. Cultivo, produccion y manejo de Portland, Oregon, pp. 364–366. la Papaya. Proceedings of a Workshop on Papaya. Yee, W., Akamine, E.K., Aoki, G.M., Hamilton, Colegio Regional de Aguadilla, Agricultural R.A., Haramoto, F.H., Hine, R.B., Holtzmann, Experiment Station Puerto Rico, 20 May 1994.

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6 Pests of Pineapple

Graham J. Petty,1 Graham R. Stirling2 and Duane P. Bartholomew3 1Institute for Tropical and Subtropical Crops, Agricultural Research Council, Private Bag X1, Bathurst 6166, Republic of South Africa; 2Biological Crop Protection (Pty) Ltd, 3601 Moggill Road, Moggill, Queensland 4070, Australia; 3Department of Agronomy and Soil Science, University of Hawaii at Manoa, 1910 East-West Road, Honolulu, Hawaii 96822, USA

The pineapple, Ananas comosus (L.) Merr., tropics and subtropics. Just over 13 million t a member of the Bromeliaceae family, is a of pineapple were produced by 76 countries self-sterile herbaceous, perennial, mono- on 704,912 ha of land in 1997 (Food and Agri- cotyledonous plant. The commercial cultivars culture Organization, 1998). Few data are are placed in five distinct groups, i.e. available on the fraction of fruit sent to local ‘Cayenne’, ‘Spanish’, ‘Queen’, ‘Pernambuco’ markets, processed, or exported (Loeillet, and ‘Perolera’. Christopher Columbus and 1997; Barbeau and Marie, 1997; Pinon, 1997; his crew were the first Europeans to discover Rougé and N’Goan, 1997). However, Loeillet this fruit when, in 1493, they landed on a (1997) reported that 70% of pineapple fruits West Indian island which they later named are consumed within the country of produc- Guadeloupe. Since that time the pineapple tion. Twenty-three countries produce more has been taken to and grown in other coun- than 100,000 t (Table 6.1), and production in tries with tropical and subtropical climates, all countries has increased by 14% in the past and a number of pests have gone along 10 years. Pineapple is an important crop in a with it. Most pests are endemic to the new large number of countries and provides vari- countries and have adapted to utilize the ety in the fruit market and a source of foreign pineapple to support their life cycles. exchange. The low yield for Indonesia and This chapter outlines the importance the very high yield for Colombia suggests and phenology of pineapple as a commercial that some data may not be reliable. However, crop. It goes on to discuss key pineapple pest much of the variation can be explained biologies and economic thresholds, and the by differences in climate in the different principles and practices of sampling, monitor- growing regions, intensity of management, ing and controlling these species. Tables list level of inputs, and of relevance to this the pests, worldwide, giving their importance chapter, the technology available and applied and distribution. to control pests.

Importance of the Crop Phenology

Pineapple ranks after bananas and mangoes The phenology of the pineapple plant begins as the third largest fruit crop harvested in the with the initiation of propagules, all of which

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 157

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Table 6.1. Statistics on pineapple production for countries producing more than 100,000 t in 1997 and the increase in production between 1990 and 1997 (FAO, 1998).

Area Production Yield Increase or decrease Country (1000 ha) (1000 t) (t ha−1) (%, 1990–1997)

Australia 2.67 13,124.9 46.7 −0.0 Bangladesh 13.77 13,148.5 10.8 −9.4 Brazil 55.21 1,936.5 35.1 −43.9 China 26.30 13,899.1 34.2 −22.4 Colombia 5.34 13,329.3 61.6 −3.8 Costa Rica 8.19 13,260.0 31.7 −38.5 Cote d’Ivoire 5.50 13,260.6 47.4 −10.8 Congo 3.30 13,145.0 25.4 −2.1 Dominican Republic 4.40 13,109.9 24.7 −35.6 Guatemala 3.85 13,109.8 28.5 −38.8 Hawaii 8.05 13,294.0 36.5 −77.4 India 82.00 1,100.0 13.4 −19.9 Indonesia 80.00 13,537.9 6.7 −27.4 Kenya 8.50 13,290.0 34.1 −22.4 Malaysia 7.05 13,163.0 23.1 −30.7 Mexico 7.69 13,301.4 39.2 −50.8 Nigeria 100.00 13,800.0 8.0 −4.6 Peru 7.37 13,125.1 17.0 −45.3 Philippines 52.00 1,700.0 32.7 −32.0 South Africa 6.10 13,151.6 24.9 −12.0 Thailand 85.00 2,000.0 23.5 −6.7 Venezuela 10.00 13,189.4 18.9 −57.5 Vietnam 24.50 13,185.0 7.6 −152.9 World 704.90 13,060.2 18.5 −14.0

are shoots formed on the stem or fruit of temperature, with little growth occurring if the mother plant. Propagules include ground the temperature is below about 15°C. New and stem suckers, hapas, slips, and crown. root development and extension continues at Ground and stem suckers arise from the stem least until the time of flower induction. The at its base or along its length. Hapas arise presence of white root tips has been used in in the transition zone between the stem and Hawaii as a diagnostic of root health (Sanford, fruit peduncle. Slips are borne on vestigal 1962). Leaf growth resumes at or soon after fruits near the top of the peduncle, and the root initiation begins. New growth of older crown develops at the top of the fruit. These leaves is readily discerned by an abrupt propagules consist of a stem and leaves, increase in leaf width at the point where though large suckers may also have adventi- growth resumed. Once root and leaf growth tious roots. After planting, development begin, growth is continuous at a rate of the pineapple plant is continuous once determined by the prevailing temperature, initiated unless arrested by environmental irradiance, and water and nutrient supply stress, pests or disease. Some pests attack the until canopy closure occurs. After the leaf can- propagule while it is still on the plant or in opy closes in, the degree of mutual shading, storage, but most problems are encountered which is in part a function of plant population after planting. density, reduces the light available to plants The first phenological stage after planting and growth is then determined to some extent is root initiation. The rate of initiation of new by the intensity of this shading. In any case, roots is determined by water supply and leaf number per plant, and thus plant weight,

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Pests of Pineapple 159

increases until inflorescence development Pests is environmentally induced or forced with a plant growth regulator (Zhang et al., 1997). Nematodes Inflorescence development in commercial practice is initiated by a growth regulator Plant-parasitic nematodes are present wher- (ethylene gas or ethephon (2-chloroethyl- ever pineapple is grown and are one of the phosphonic acid)). Sucker development, the most important constraints to pineapple pro- source of the ratoon crop, commences at duction worldwide. Nematodes may reduce or soon after the floral initiation process the length of primary roots to such an extent breaks apical dominance in cooler environ- that plants have poor anchorage, or they may ments such as Australia and South Africa, but destroy secondary roots and leave infested in more tropical environments (Cote d’Ivoire, plants with a poorly developed root system. Thailand) may be delayed until after fruit mat- Such plants are susceptible to moisture and uration. Circumstantial evidence indicates nutrient stress and, because pineapple roots that stem starch levels at the time of floral do not regenerate once they are killed back to initiation determine whether sucker initiation the stem, nematode-infested plants have little begins at flower induction or much later. chance of reaching their full yield potential. Fruitlet initiation and development is temper- Although nematodes can cause significant ature dependent (Fleisch and Bartholomew, reductions in plant crop yield, they are 1987). In summer in Hawaii fruitlet initiation primarily a problem of ratoon crops. The is completed in 34 days (Bartholomew, 1977) number, size and vigour of the suckers that and an average-sized fruit of ‘Smooth Cay- produce the ratoon crop is heavily dependent enne’ contains 100 or more fruitlets. Crown on the health of the initial root system development begins once fruitlet develop- produced by the mother plant. When these ment is completed (Bartholomew, 1977). The roots are damaged by nematodes, ratoon young inflorescence is protected by a whorl crop yields may be drastically reduced or the ± of leaves for the first 40 days of its develop- crop may fail (Caswell et al., 1990). ment. Anthesis begins 3 to 4 weeks after inflo- More than 100 species of plant-parasitic rescence appearance and occurs acropetally nematodes have been recorded in association over a period of about 2 weeks. Once anthesis with pineapple roots, and between three and is completed and the petals dry, fruit and five species are usually found in most pine- crown development are essentially continu- apple fields. Since this complex of parasitic ous until the fruit is mature. Sucker number nematodes must be kept under control if a per plant is highly correlated with plant popu- pineapple plantation is to achieve maximum lation density, declining as density increases. productivity, this chapter takes a holistic view Development of suckers may continue after of nematode management. It concentrates on initiation or may be arrested, presumably due the general principles which are applicable to a lack of resources. Those that do develop to all plant-parasitic nematodes and provides become the source of the ratoon crop and only a limited amount of information on will grow until the flower initiation process particular nematode species. is forced. Pest injury due to feeding or transmission of disease is to some extent dependent on phenological development. Root pests can Key nematode pests attack as soon as root development begins, and pests that feed on leaves can attack at The key nematode pests of pineapple are almost any time. Mites can feed on developing all endoparasites. They either establish a fruitlets and propagules as soon as they permanent feeding site within the root and are accessible and probably before they are then become sedentary, e.g. root-knot and visible, and pests can enter fruitlets and feed reniform nematodes, or they live inside roots or transmit diseases at the time of anthesis. but remain migratory, e.g. lesion nematodes.

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160 G.J. Petty et al.

Root-knot nematode (Meloidogyne javanica favour its development. The life cycle is and M. incognita) generally completed in about 4 weeks. Root-knot nematode is a particularly impor- Lesion nematode (Pratylenchus brachyurus) tant pest of pineapple because nematodes invade the tips of primary roots and stop Lesion nematodes are migratory endopara- them from elongating (Plate 33). Thus plant sites. Adult females lay eggs in root tissue anchorage is markedly reduced. A terminal, and in soil, but all stages can migrate into and club-shaped gall is usually produced in out of roots. Damage is difficult to diagnose response to the developing nematode in the field, but dark-coloured lesions (Godfrey and Oliveira, 1932), but small, develop in response to nematodes feeding non-terminal galls may also form, causing in cortical tissue. These lesions can be brooming of the root system (Godfrey, 1936). microscopic in size, but they may extend The disease cycle begins when second-stage progressively to cover the whole surface juveniles hatch from eggs and establish a of the root. Secondary roots and root hairs feeding site behind the root tip. They then are destroyed by the nematode, resulting in become sedentary and develop through a root system composed mainly of poorly subsequent moults into saccate females. At developed primary roots. The length of the maturity, each female produces about 1000 life cycle is 4 weeks at temperatures of about eggs which are contained in a gelatinous egg 30°C (Olowe and Corbett, 1976). mass. Worm-like adult males are sometimes produced, but they are unimportant because females reproduce by mitotic partheno- genesis. Temperatures of 25–30°C are ideal Secondary nematode pests for nematode multiplication and at these temperatures, the life cycle is completed Spiral nematodes (Helicotylenchus spp., Roty- in 4–5 weeks. lenchus spp. and Scutellonema spp.), ring nematodes (Criconemella spp.), and stubby root Reniform nematode nematodes (Paratrichodorus spp.) commonly (Rotylenchulus reniformis) occur in pineapple fields. The most widely distributed species is H. dihystera, which is In contrast to root-knot nematode, reniform often found at population densities greater nematode does not prevent primary roots than 2000 nematodes per 100 ml soil. Although from elongating. Roots infected by reniform their pathogenicity has not been studied in nematode will provide the plant with good detail, it is generally assumed that these ecto- anchorage, but because secondary root parasitic species are not of major economic formation is inhibited, root systems tend to importance on pineapple. They live in soil, be poorly developed. Second-stage juveniles feeding externally on cortical tissues, root hatch from eggs and develop into males and hairs and root tips, and the symptoms they immature females without feeding. Males produce tend to be relatively non-specific. do not feed, but immature females enter the They can be disregarded as pests unless their root and establish a feeding site. They then population densities are very high. become sedentary, developing into kidney- shaped, egg producing adults (Linford and DISTRIBUTION AND IMPORTANCE Although Oliveira, 1940). When soil is moist, root the key nematode pests of pineapple are exudates of certain hosts will stimulate eggs widely distributed, management systems, e.g. to hatch. In dry soil, the nematode survives in crop rotation practices, and environmental the egg stage or as anhydrobiotic juveniles factors, e.g. soil moisture, soil pH and temper- (Apt, 1976; Tsai and Apt, 1979). Reniform ature, can influence distribution at a local level. nematode is widely distributed in tropical Thus the distribution and relative importance and subtropical regions and soil tempera- of various species varies between and within tures in most pineapple-growing regions pineapple-growing regions (Table 6.2).

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Pests of Pineapple 161 Asia in southern sandy pest situations (Dole loams areas by tropics. in e.g. cooler and moisture clay in elevations Clink economic soils nematode greatest pest regions, Favoured J.W. equatorial subtropical pH major higher are Dr in occasional of the low is in from regions. and important well-structured nematode Losses Australia, there important and key most tropical The soils The in where stress Prevalent pineapple-growing Africa, Hawaii. monoculture, importance Less Importance comments additional Thailand in of Philippines some the areas with of distribution densities some areas low (1990), areas . limited and at

al some

areas et limited Africa Queensland . Africa, hectarage a and occurs in areas Philippines north Caswell only limited western the subtropical southern a present most Thailand pineapple generally in in in in on in in of tropical not (1986), Africa to important Apt populations pests and southern Widespread Uncommon, High Widespread Limited Widespread Locally Widespread Widespread Generally Significant Significant Widespread Distribution Significant Widespread nematode Rohrbach America America America main the (1982), South South South of and and and Keetch Region Africa Asia Australia Hawaii Central Africa Asia Australia Hawaii Central Africa Asia Australia Hawaii Central importance (1975), ) ) and , Guérout

reniformis

brachyurus javanica Distribution from ) nematode nematode nematode 6.2. e l incognita b a

Meloidogyne Rotylenchulus Pratylenchus Summaries T Ltd). Root-knot ( Reniform ( Nematode a ( M. Lesion

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162 G.J. Petty et al.

STRATEGIC DECISION MAKING For the last 50 densities. Thus the only way to obtain reliable years, nematode pests of pineapple have information on nematodes and their distri- largely been controlled by pre-plant fumiga- bution within a field is to take a number of tion. Fumigants were relatively inexpensive samples from the field. Since each sample and so effective that they were applied must be representative of the area sampled, it routinely as an insurance against crop losses must be a composite of a large number of soil from nematodes. In situations where non- cores. The monitoring service in Australia, for volatile nematicides are needed to suppress example, is based on a composite sample of resurging nematode populations, they usu- 50 cores from a sampling area of 0.5–1 ha. ally have been applied at regular intervals This sampling scheme provides an estimate of using a calendar-based approach (Rohrbach nematode density that is within about 25% of and Apt, 1986). the true mean (Stirling and Kopittke, 2000). With the development of modern concepts of integrated pest management, there MONITORING PROCEDURES Populations of has been a move within most sectors of the all plant-parasitic nematodes follow the same pineapple industry towards a more strategic basic pattern during the pineapple cropping approach to nematode management. Nema- cycle: they are highest during the ratoon tode infestation levels are determined by crop, they decline during the fallow intercycle sampling fields and decisions on whether period and then re-establish during the plant action should be taken against the pest are crop (Fig. 6.1). made on the basis of this information. Many Any sampling scheme for nematodes pineapple companies regularly sample their must take these fluctuations into account. In fields for nematodes, while a commercial Australia, for example, root-knot nematode is nematode monitoring service is provided for the main pest and samples are collected at four the numerous small growers who comprise key times during the cropping cycle: the Australian industry. 1. Samples collected near the end of the SAMPLING METHODS Nematodes are never ratoon crop indicate the likely importance of uniformly distributed in pineapple fields. nematodes in the next crop. Subtle changes in soil texture, for example, 2. Samples taken just prior to planting will markedly affect nematode population show the impact of the intercycle period on

New cropFallowPrevious crops

1 4

2 3 Number of nematodes

−12 −6 0 6 12 24 Time (months before and after planting) Fig. 6.1. Diagrammatic representation of the dynamics of nematode populations during the pinapple cropping cycle. (The four key times to sample for nematodes are designated by numerals.)

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Pests of Pineapple 163

nematode populations. Data from this and the this situation, yields in the ratoon crop can be previous sample can be used to determine the increased by as much as 25% (Sipes and need for a pre-plant nematicide. Schmitt 1994a). For lesion nematode, pre- 3. Samples taken about 12 months after plant populations of less than one nematode planting indicate whether nematode popula- per 100 ml soil can substantially reduce fruit tions have started to increase on the present weight (Sarah, 1986). Under the environ- crop. mental conditions of West Africa, population 4. Samples at plant crop harvest indicate densities of this magnitude can reduce plant whether the nematode population is high crop yields by 30%, and ratoon crops may be enough to warrant application of a nematicide uneconomic. to the ratoon crop. CHEMICAL CONTROL Regardless of where Populations of reniform nematode do pineapples are grown and which nematode not decline as rapidly as root-knot nematode species is the key pest, chemical nematicides during the intercycle period, and they are the primary means of control. Ethylene increase more rapidly on the newly planted dibromide (EDB), dibromochloropropane crop. It may therefore be necessary to modify (DBCP) and 1,3-dichloropropene (1,3D) were the above sampling scheme if this nematode is widely used in the pineapple industry the key pest. Sampling would probably start until the late 1970s, when the health and earlier, and it would continue on a regular environmental problems associated with basis (perhaps every 3 months) until early in the fumigant nematicides became apparent the ratoon crop. (Thomason, 1987). In most countries, 1,3D is now the only registered pre-plant fumigant, ECONOMIC THRESHOLDS Because of the and it is generally injected under plastic at length of the pineapple cropping cycle, the a rate of 224–336 l ha−1. Non-volatile organo- relatively short generation times of all impor- phosphate and carbamate nematicides are tant plant-parasitic nematodes, and the wide also registered as pre-plant treatments in range of factors that can influence the rate some countries. Commonly used chemicals of nematode multiplication, it has proved include fenamiphos, which is formulated as a difficult to determine relationships between granule, and oxamyl, which is applied via pre-plant nematode densities and yield. trickle irrigation. Although they provide an Root-knot nematodes have such a capacity alternative to the soil fumigants, they do not to increase that populations as low as one provide the same length of control. nematode per 100 ml soil have the potential to Regardless of which nematicide is used cause problems (Keetch, 1982). In Australia, prior to planting, there are many situations the population density 12 months after plant- where nematodes will increase later in the ing is considered a more useful indicator of the crop to levels that will cause economic dam- potential for damage. Populations as high as age. If good ratoon crops are to be produced, 200 root-knot nematodes per 100 ml soil have the root system must be protected from nema- no measurable effect on plant crop yield, but tode attack for at least the first 12–15 months, can result in ratoon crop failure. As few as 1–5 and to achieve this a post-plant nematicide nematodes per 100 ml soil at 12 months will may be needed. When trickle irrigation reduce ratoon crop yields by 10% (Stirling and is available, emulsifiable formulations of Kopittke, 2000). fenamiphos and oxamyl may be applied in Damage thresholds for reniform and the irrigation water (Apt and Caswell, 1988; lesion nematodes on pineapple have not been Schneider et al., 1992). Since pineapple is quantified (Caswell et al., 1991), but in both unique in enabling non-volatile nematicides cases they are likely to be very low. Pre-plant to be translocated systemically from the leaves densities of about two reniform nematodes to the roots (Zeck, 1971), control may also be per 100 ml soil can increase to more than 600 obtained by spraying these materials on the nematodes per 100 ml soil within 12 months of foliage. The effectiveness of post-plant appli- planting. When nematicides are applied in cations of non-volatile nematicides means that

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it is possible to monitor nematode populations crops that are poor hosts of all the important in pineapple fields and apply control nematode pests of pineapple. There are a measures before populations increase to number of crops that are potentially useful damaging levels. against Meloidogyne spp., e.g. grasses such as Rhodes grass (Chloris gayana), green panic NON-CHEMICAL CONTROL (Panicum maximum), pangola grass (Digitaria Fallow. Since plant-parasitic nematodes decumbens) and forage sorghum (Sorghum are obligate parasites of plants, they will die of bicolor × S. sudanense) and legumes such as starvation when fields are kept free of weeds velvet bean (Mucuna pruriens) and forage and volunteer pineapple plants. Bare fallows peanut (Arachis pintoi), but all of them are can be achieved by regularly applying herbi- not necessarily poor hosts of R. reniformis and cides or by cultivation, with the latter having P. brachyurus. Rhodes grass may also be useful the added benefit of bringing some nematodes against R. reniformis because it is not a host to the soil surface where they are killed by the (Caswell et al., 1991), and it was one of a heating and drying effects of the sun. The number of crops that increased the rate of amount of nematode control achieved with a decline of reniform nematode in comparison bare fallow depends on the nematode species to bare fallow (Ko and Schmitt, 1996). involved, the environmental conditions dur- One plant family which contains crops ing the fallow and the length of time that the that have been assessed in recent years fallow is maintained. The rate of decline in for their capacity to suppress nematodes is nematode populations is greatest in warm, the Cruciferae. When residues of cruciferous moist soils because eggs continue to hatch plants decompose in soil, glucosinolates pres- under such conditions and vermiform stages ent in plant tissue are converted by enzymatic remain metabolically active and will soon decomposition into isothiocyanates, the active exhaust their food reserves. Dryness during ingredient of the soil fumigant metham the fallow period can reduce its effectiveness sodium. There has therefore been interest in as some species, particularly R. reniformis, sur- using these crops as green manures to obtain a vive well in dry soils (Apt, 1976; Tsai and Apt, ‘biofumigation’ effect. However, results with 1979). In current systems of pineapple culture, Brassica crops have been equivocal (Mojtahedi a bare fallow is often maintained for 4–12 et al., 1991, 1993; Johnson et al., 1992), possibly months between crop cycles, and this is long because many Brassica spp. are good nema- enough to reduce nematode populations to tode hosts (Bernard and Montgomery-Dee, non-detectable levels (Guérout, 1975; Stirling 1993; McSorley and Frederick, 1995) or because and Nikulin, 1993). Bare fallow therefore of low glucosinolate concentrations in culti- provides a significant level of control, but vars that are currently available. If high gluco- has the disadvantage of subjecting soil to the sinolate cultivars suitable for subtropical and risk of erosion and of reducing populations of tropical climates are eventually released, it beneficial soil microorganisms. may be worthwhile evaluating them as rotation crops in pineapple cropping systems. Crop rotation. One method of obtaining the benefits of bare fallow while overcoming Resistance and tolerance. Because ‘Cayenne’ its disadvantages is to grow a non-host is widely accepted in both canning and fresh crop during the intercycle period. A variety of fruit markets, pineapple plantings through- crops has been suggested (Caswell et al., 1990), out the world are dominated by a clone which but some of these are likely to be of limited is both nematode susceptible and intolerant value because they do not grow vigorously (Py et al., 1984). There have been claims that enough to compete with weeds, they do not varieties with nematode tolerance have tolerate the residual herbicides used in many been identified in the Hawaiian pineapple pineapple cropping systems, or they are likely breeding programme (Caswell and Apt, 1989; to become weeds in the next pineapple crop. Williams et al., 1993) and there are reports Another problem is that it is difficult to find of nematode resistance in species other than

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Pests of Pineapple 165

Ananus comosus (Caswell et al., 1990). How- increased. Some of that evidence comes from ever, this material has never been developed experiments with Hawaiian pineapple soils as a commercial cultivar and Sipes and in the era before soil fumigation became wide- Schmitt (1994b) showed that some of it was spread. Damage caused by root-knot nema- not resistant to either Meloidogyne javanica or tode was reduced when chopped pineapple Rotylenchulus reniformis. material was incorporated into soil, probably From a research perspective, one of because there was an increase in the activity of the challenges of the future is to determine naturally occurring parasites and predators of whether modern genetic engineering technol- nematodes (Linford, 1937; Linford et al., 1938). ogies can improve the nematode resistance The challenge of those interested in develop- of pineapple when conventional selection ing more sustainable methods of pineapple and breeding programmes have failed. Recent culture is to develop cropping systems which progress with pineapple transformation sys- can harness these natural suppressive forces. tems (Graham et al., 1998) suggests that it will Conservation of organic matter will be a eventually be possible to introduce foreign key element in such systems and could be genes into pineapple. The Mi gene, which achieved with practices such as intercrop- confers resistance to several species of Meloid- ping, green manuring, minimum tillage, trash ogyne, has been cloned (Kaloshian et al., 1998; retention, mulching and addition of organic Williamson, 1998), while several synthetic amendments. resistance systems, e.g. proteinase inhibitors and systems which interfere with giant cell Integrated pest and disease management. function, are being actively studied in other Although the major pests of pineapple are crops. Less is known about mechanisms of discussed individually in this chapter, it is resistance to reniform and lesion nematodes, important to recognize that interactions occur which means that resistance to these nema- between pests. Nowhere is this more apparent todes will be more difficult to achieve. than in soil, where nematodes, white grubs, symphylids and the root rotting fungus, Phy- Alternative cropping systems. In the pine- tophthora cinnamomi, may all act on the apple cropping system used in most parts same root system. Since damage caused by of the world, reliance on a monoculture with one pest can influence other components of limited breaks between cycles means that this root disease complex, it is vital to correctly nematode population densities are rarely diagnose such problems and direct control limited by the absence of a host plant, and measures at all the causal factors. There is little some nematodes are always carried over from to be gained, for example, in treating a crop one crop to the next. Nematode problems are for a chronic Phytophthora root rot problem compounded by soil management practices if plant-parasitic nematodes increase on the that reduce populations of antagonistic micro- newly available food source and destroy the organisms to negligible levels (Rohrbach and new root system. Apt, 1986). Excessive cultivation, for example, hastens the breakdown of organic matter and indirectly effects the soil biota, while soil Arthropods fumigation reduces the number and diversity of beneficial soil microorganisms. Thus the Arthropods may be defined as invertebrates, typical pineapple-cropping system provides with jointed legs and an outer body layer plant-parasitic nematodes with an ample food which functions as a rigid protective exo- source and a soil environment in which they skeleton. The arthropod pests of pineapples can multiply with little competition. include mite, symphylid and insect species. There is a large body of experimental and These are listed in Table 6.3, including 102 empirical evidence (Stirling, 1991) to show species from which it may be concluded that that soils become more suppressive to nema- the percentage composition for these three todes when levels of organic matter are taxa is: mites, 4%; symphylids, 3%; insects

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Table 6.3. Pineapple pests of the world. Referenced listing of reported locations, on plants and geographically, of arthropod pests (mites, symphylids and insects) of the pineapple, Ananas comosus (L.) Merr., with economic importance indicators.

Plant part affected and Pests and location Reference economic importancea

Acari: Eriophyidae Phyllocoptruta sakimurae Keifer Fruit Hawaii Sakimura, 1966 2 Acari: Tarsonemidae Steneotarsonemus ananas (Tryon) Floral cavities (pineapple fruit mite/leathery pocket mite) Young leaf bases Probably universal Rohrbach, 1983 Australia Tryon, 1898 3 Waite, 1993 Hawaii Carter, 1967 3 Indonesia Fauzan, Lampung, 1999, 2 personal communication Ivory Coast A. Adiko and M. Kèhè, Abidjan, 1 1999, personal communication Réunion Vuillaume, 1982 2 South Africa Petty, 1975 3 Swaziland Dodson, 1969 3 Tarsonemus sp. Fruit Hawaii Sakimura, 1966 2 Acari: Tenuipalpidae Dolichotetranychus floridanus (Banks) Base of leaves (pineapple red mite/flat mite) Australia Waite, 1993 1 Brazil Sanches, 1980 1 Hawaii Carter, 1967 1 Indonesia Fauzan, Lampung, 1999, 2 personal communication Mexico Linford, 1952 1 Réunion S. Quilici, Réunion, 1999, 2 personal communication South Africa Petty, 1978b 1 Most other pineapple growing Waite, 1993 countries, including Malaysia Acari: Cryptostigmata Root apex (oribatid mites) Lamellobates palustris Hammer 5 Paralamellobates bengalensis 5 Bhaduri & Raychaudhuri Paroppis sp. 5 West Bengal Sanyal and Das, 1989 Rostrozetes foveolatus Sellnick 5 Scheloribates curvialatus Hammer 5 Myriapoda: Symphyla (garden centipedes/symphylids) Hanseniella unguiculata (Hansen) Root apex, root hairs Hawaii Sakimura, 1966 1 Carter, 1967

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Pests of Pineapple 167

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Hanseniella spp. Australia Waite, 1993 1 Brazil N.F. Sanches, Bahia, 1999, 2 personal communication Many other pineapple growing countries Waite, 1993 Hanseniella ivorensis Juberthie-Jupeau Root apex, root hairs & Kèhè Ivory Coast Kèhè et al., 1997 1 Scutigerella sakimurai Scheller Root apex, root hairs Hawaii Sakimura, 1966 2 Insects Orthoptera: Blaberidae Diploptera punctata (Eschscholtz) Fruit Hawaii Sakimura, 1966 2 Orthoptera: Acrididae Atractomorpha sinensis Bolivar Leaves Hawaii Sakimura, 1966 2 Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Locusta migratoria Linnaeus Leaves Indonesia Fauzan, Lampung, 1999, 3 personal communication Oxya chinensis (Thunberg) Leaves Hawaii Sakimura, 1966 2 Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Orthoptera: Tettigoniidae Conocephalus saltator (de Saussure) Fruit Hawaii Sakimura, 1966 2 Elimae punctifera (Walker) Fruit Hawaii Sakimura, 1966 2 Nastonotus reductus (Brunner von Fruit Wattenwyl) Venezuela F. Leal, Maracay, 1999, 3 personal communication Tarbinskiellus portentosus (Lichtenstein) Leaves China Li Liying, Guangzhou, 1999, 1 personal communication Orthoptera: Gryllidae Gryllus bimaculata De Geer Fruit (black cricket) Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Teleogryllus mitratus (Burmeister) Fruit (oriental garden cricket) Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Teleogryllus oceanicus (Le Guillou) Fruit Hawaii Sakimura, 1966 2 continued

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168 G.J. Petty et al.

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Isoptera: Termitidae Macrotermes subhyalinus Rambur Roots French Guinea J.-F. Vayssieres, Ligne 3 Paradis/St Pierre, 1999, personal communication Procornitermes striatus (Hagen) Leaves, roots Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Syntermes obtusus Holmgren Leaves, roots Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Trinervitermes oeconomus (Trägårdh) Roots French Guinea J.-F. Vayssieres, Ligne 3 Paradis/St Pierre, 1999, personal communication Isoptera: Rhinotermitidae Coptotermes formosanus Shiraki Leaves, roots China Li Liying, Guangzhou, 1999, 3 personal communication Taiwan Hung-Chieh Wen,Taiwan, 2 1999, personal communication Thysanoptera: Thripidae Frankliniella fusca (Hinds) Floral cavities Hawaii Sakimura, 1966 3 Frankliniella occidentalis (Pergande) Floral cavities Hawaii Sakimura, 1966 3 Réunion S. Quilici, Réunion, 1999, 2 personal communication Frankliniella schultzei (Trybom) Floral cavities Réunion S. Quilici, Réunion, 1999, 2 personal communication South Africa Petty, 1978c 3 Holopothrips ananasi Lima Leaves Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Thrips tabaci Lindeman Floral cavities, leaves Hawaii Sakimura, 1966 1 Philippines Sérrano, 1935 1 Réunion Plenet, 1965 2 South Africa Petty, 1978c 3 Homoptera: Pseudococcidae Dysmicoccus brevipes (Cockerell) Fruit base and (pink pineapple mealybug) peduncle, fruit floral cavities, leaf axils, roots Worldwide Carter, 1954 1 Py and Tisseau, 1965 Dysmicoccus neobrevipes Beardsley Fruit, leaves (grey pineapple mealybug) Brazil Sanches, 1981 1 Fiji Rohrbach, 1983 1 Hawaii Beardsley, 1959 1 Philippines Rohrbach, 1983 1 Taiwan Rohrbach, 1983 1

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Pests of Pineapple 169

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Very widely distributed, including Rohrbach, et al., 1988 Micronesia, Malaysia, Mexico, Jamaica Ferrisia virgata (Cockerell) Fruit, leaves (striped mealybug) Hawaii Sakimura, 1966 4 Taiwan Hung-Chieh Wen, Taiwan, 2 1999, personal communication Geococcus coffeae Green Roots Hawaii Sakimura, 1966 4 Phenacoccus solani Ferris Floral cavities, heart leaves Hawaii Carter, 1963 4 South Africa Willers, 1992 4 Planococcus citri (Risso) Leaves Brazil Sanches, 1980 3 Hawaii Sakimura, 1966 3 Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Pseudococcus longispinus Fruit crown (Targioni-Tozzetti) Hawaii Rohrbach et al., 1988 3 South Africa Petty, 1976a 2 Taiwan Hung Chieh Wen, Taiwan, 3 1999, personal communication Homoptera: Diaspididae Aspidiotus nerii Bouché Fruit, leaves Brazil Sanches, 1980 3 Aulacaspis maculata Cockerell Fruit, leaves Unspecified location Borchsenius, 1966 5 Recorded on pineapple by Ferald (1903) Diaspis boisduvalii Signoret Fruit, leaves Brazil Sanches, 1980 3 Hawaii Py et al., 1987 1 Ivory Coast A. Adiko and M. Kèhè, Abidjan, 2 1999, personal communication Latin America Py et al., 1987 1 Sri Lanka Py et al., 1987 1 Taiwan Py et al., 1987 1 Diaspis bromeliae (Kerner) Fruit, leaves Asia Petty, 1978a 3 Australia Petty, 1978a 3 Brazil Sanches, 1981 3 Hawaii Sakimura, 1966 1 Ivory Coast A. Adiko and M. Kehe, Abidjan, 2 1999, personal communication Pacific Islands Petty, 1978a 3 Réunion S. Quilici, Réunion, 1999, 2 personal communication South Africa Petty, 1978a 3 Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication continued

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170 G.J. Petty et al.

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Gymnaspis aechmeae Newstead Fruit, leaves Unspecified location Borchsenius, 1966 5 Recorded on pineapple by Ferris (1937) Melanaspis smilacis (Comstock) Fruit, leaves (M. bromeliae (Leonardi)) Brazil Sanches, 1980 3 Hawaii Sakimura, 1966 2 Pseudaonidia trilobitiformis (Green) Fruit, leaves Unspecified location Borchsenius, 1966 5 Recorded on pineapple by Balachowsky (1958) Pseudischnaspis anassarum Lindiger Fruit, leaves (purple scale) This species is a synonym of Melanaspis smilacis (Comstock) Taiwan Hung-Chieh Wen, Taiwan, 2 1999, personal communication Homoptera: Ortheziidae Orthezia praelonga Douglas Fruit, leaves Brazil N.F. Sanches, Bahia, 1999, personal communication Heteroptera: Lygaeidae Nysius clevelandensis Evans Fruit, leaves (grey cluster bug) Australia Waite, 1993 2 Nysius vinitor Bergroth Fruit, leaves (Rutherglen bug) Australia Waite, 1993 2 Heteroptera: Coreidae Lybindus dichrous (Stal.) Fruit inflorescence Argentina Menezes Mariconi, 1953 3 Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Lepidoptera: Lycaenidae Thecla basilides (Geyer) Fruit, slips (Tmolus echion (Linnaeus)) Brazil Sanches, 1980 1 Guatemala Collins, 1960 1 Mexico Linford, 1952 1 South America Sakimura, 1966 1 Trinidad Harris, 1927 1 Anon., 1995 Venezuela Martinez, 1976 1 Lepidoptera: Castniidae Castniomera licus (Drury) Stem (giant/white stem borer) Brazil Sanches, 1980 3 Castnia penelope Schaufuss Stem Brazil Sanches, 1980 2 Venezuela F. Leal, Maracay, 1999, 1 personal communication

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Pests of Pineapple 171

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Lepidoptera: Nymphalidae Dynastor darius (Stichel) Leaves Brazil Sanches, 1980 3 Venezuela F. Leal, Maracay, 1999, 3 personal communication Lepidoptera: Noctuidae Agrotis ipsilon Hufnagel Leaf (black cutworm) Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Autographa biloba (Stephens) Fruit Hawaii Sakimura, 1966 2 Elaphria agrotina Guenée Leaf Brazil Sanches, 1981 3 Mythimna convecta Walker Flowers, developing (common army worm) fruit, leaves Australia Waite, 1993 3 Spodoptera exigua (Hübner) Leaf bases (lesser army worm/lesser cotton leaf worm/beet army worm) South Africa Petty, 1990a 3 Spodoptera litura Fabricius Leaf (tobacco cutworm) Taiwan Hung-Chieh Wen, Taiwan, 3 1999, personal communication Lepidoptera: Coleophoridae Batrachedra methesoni Busck Fruit Caribbean Sakimura, 1966 3 Puerto Rico Perez, 1957, 1959 3 Lepidoptera: Cosmopterygidae Pyroderces hemizopha (Meyrick) Floral cavity (scavenging) Ivory Coast Py et al., 1987 4 Pyroderces rileyi (Walsingham) Floral cavity (formerly in the genus Anatrachyntis) (scavenging) (pink bud moth) Hawaii Sakimura, 1966 4 South Africa Petty, 1991 4 Lepidoptera: Tineidae Neodecadarchis flavistriata Floral cavity (Walsingham) (scavenging) Hawaii Sakimura, 1966 4 Opogona sacchari (Bojer) Stem (formerly in the genus Alucita) Réunion S. Quilici, Réunion, 1999, 2 personal communication Lepidoptera: Tortricidae Amorbia emigratella Busck Fruit Hawaii Sakimura, 1966 4 continued

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172 G.J. Petty et al.

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Lepidoptera: Limacodidae Darna trima (Moore) Leaves China Li Liying, Guangzhou, 1999, 1/2 personal communication Setothosea asigna (van Eecke) Leaves China Li Liying, Guangzhou, 1999, 3 personal communication Coleoptera: Scarabaeidae (white grubs) Melolonthinae Antitrogus mussoni (Blackburn) Roots (possible misidentification of A. consanguineus (Blackburn) and A. rugulosus (Blackburn)) Allsopp, 1993 Australia Waite, 1993 3 Asthenopholis subfasciata (Blanchard) Roots South Africa Petty, 1977a 1 Congella valida Péringuey Roots (previously misidentified as Adoretus tessulatus Burmeister) South Africa Smith et al., 1995 2 Hoplochelus marginalis (Fairmaire) Roots Réunion Quilici et al., 1992 3 Lepidiota gibbifrons Britton Roots Australia Waite, 1993 3 Lepidiota grata Blackburn Roots Australia Waite, 1993 3 Lepidiota noxia Britton Roots Australia Waite, 1993 3 Lepidiota squamulata Waterhouse Roots Australia Waite, 1993 3 Lepidiota stigma (Fabricius) Roots Indonesia Fauzan, Lampung, 1999, 2 personal communication Macrophylla ciliata (Herbst) Roots South Africa Petty, 1976b 3 Phyllophaga portoricensis Smyth Roots Puerto Rico and other Caribbean Islands Py and Tisseau, 1965 3 Rhopaea magnicornis Blackburn Roots Australia Waite, 1993 3 Trochalus politus Moser Roots South Africa Petty, 1976b 2 Rutelinae Adoretus (Adoretus) ictericus Burmeister Roots South Africa Petty, 1976b 2 Adoretus (Lepadoretus) sinicus Burmeister Leaves, roots Hawaii Sakimura, 1966 2 Anomala expansa Bates Roots (green beetle) 1 Taiwan Hung-Chieh Wen, Taiwan, 1999, personal communication Anoplognathus porosus (Dalman) Roots Australia Waite, 1993 3

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Pests of Pineapple 173

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Blitopertha (Exomala) orientalis Roots (Waterhouse) (formerly in the genus Anomala) Hawaii Sakimura, 1966 1 Popillia bipunctata (Fabricius). Roots South Africa G.J. Petty, Bathurst, 1997, 4 personal observation Popillia mutans Newman Roots China Li Liying, Guangzhou, 1999, 3 personal communication Dynastinae Augosoma centaurus (Fabricius) Fruits, inflorescence French Guinea J.F. Vayssieres, Ligne Paradis 3 St Pierre, 1999, personal communication Ivory Coast Guérout, 1974 2 Heteronychus arator (Fabricius) Subterranean stump (black maize beetle) South Africa Petty, 1977b 1 Strategus jugurtha Burmeister Roots (pineapple rhinoceros beetle) Bolivia Munro, 1954 2 Venezuela F. Leal, Maracay, 1999, 2 personal communication Strategus validus (Fabricius) Roots (rhinoceros beetle) Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Coleoptera: Curculionidae (Weevils) Rhynchophorinae Metamasius dimidiatipennis (Jekel) Fruit, stem (pineapple black spot beetle) Venezuela F. Leal, Maracay, 1999, 1 personal communication Metamasius fasciatus (Olivier) Fruit, stem (pineapple black beetle) Venezuela F. Leal, Maracay, 1999, 1 personal communication Metamasius ritchiei Marshall Fruit, stem Caribbean Sakimura, 1966 2 Jamaica Marshall, 1961 2 Paradiaphorus crenatus (Gyllenhal) Lower stem Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Rhabdoscelus obscurus Boisduval Fruit (New Guinea sugar cane weevil) Australia Waite, 1993 2 Brachycerinae Pantomorus cervinus (Boheman) Roots (synonym of P. godmanni (Crotch)) Hawaii Sakimura, 1966 2 continued

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174 G.J. Petty et al.

Table 6.3. Continued.

Plant part affected and Pests and location Reference economic importancea

Curculioninae Baris sp. Leaves (pineapple weevil) Venezuela F. Leal, Maracay, 1999, 2 personal communication Cholus seabrai Vaurie Peduncle, slips Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Diastethus sp. (formerly Kuschel, 1983 Leaves Gladosius Casey, 1922) Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Parisoschoenus ananasi Moure Leaves Brazil N.F. Sanches, Bahia, 1999, 3 personal communication Coleoptera: Colydiidae Bitoma sp. Fruit Brazil N.F. Sanches, Bahia, 1999, 3 personal communication

a1 = major pest; 2 = minor pest; 3 = occasional pest; 4 = minor pest of limited distribution; 5 = economic importance unknown.

93%. A breakdown of the insect species (ii) pineapple souring beetles (Coleoptera: reveals the following composition: Orthop- Nitidulidae) do not harm sound fruits, and tera, 12% (grasshoppers, 4%; katydids, 4%; only become a nuisance when subgrade fruits crickets, 3%; cockroaches, 1%); Isoptera are left to over-ripen in the fields; (iii) fruit (termites), 6%; Thysanoptera (thrips), 5%; flies (Diptera: Tephritidae), e.g. oriental fruit Homoptera, 15% (mealybugs, 7.5%; scale fly, Bactrocera dorsalis, melon fly, Bactrocera insects, 7.5%); Heteroptera (bugs), 3%; cucurbitae and Mediterranean fruit fly, Lepidoptera, 18% (moths, 16%; butterflies, Ceratitis capitata, have been suspected at times, 2%); Coleoptera (beetles), 35% (white grubs, but studies have shown that, if oviposition in 24.5%; weevils 9.8%). fruits does occur, most eggs do not hatch and It is thus apparent that a tremendous larvae do not survive (Carter, 1967). range of ecological niches of the pineapple plant are occupied by species with widely differing biologies – and economic impor- Key arthropod pests tance (Table 6.3). Due to space constraints it is only possible to deal with a very few species. Apart from one insect species, the pink pine- An attempt has been made to present accounts apple mealybug, key status does not apply of the most important (‘key’) representatives universally to these species, their occurrence of some of the taxa. Although Table 6.3 lists and importance in different pineapple pro- Isoptera species, it should be noted that they ducing regions varying considerably. The are not obligately pests of pineapples and occurrence of some species may be extremely probably only attack dead or ailing plants. The limiting to crop production in one or more table does not list species of the following geographical regions but of little or no con- groups, for the reasons given: (i) true ants sequence elsewhere. Classification as ‘key’ of (Hymenoptera: Formicidae), as these are not some of the following arthropod species, pests per se but important only by virtue of should therefore be understood as such, their association with pineapple mealybugs; with these species attaining either key or

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Pests of Pineapple 175

secondary pest status depending on geo- numbers increase with plant growth, peaking graphical location. Other species given key from 6 weeks after forcing (artificially induced status may generally be considered as minor flowering) in the warmer months of the year, pests in specific locations but, because of their to 12 or more weeks in the cooler months universal distribution, their total impact on (G.J. Petty, 1976, unpublished). pineapple production justifies key status. FRUIT–DISEASE ASSOCIATION Fruit mites feed Pineapple leathery pocket mite/pineapple fruit on trichome cells on the base of young mite, Steneotarsonemus ananas (Tryon) heart leaves, and on the bracts and sepals of developing fruits (Rohrbach and Apt, 1986). Steneotarsonemus ananas (Tryon), pineapple Damage to the latter gives a glossy ‘waxy leathery pocket mite/pineapple fruit mite, is mutant’-like appearance to fruits. These host-specific to pineapples, occurring world- damaged trichomes provide a favourable wide. It is important primarily because of substrate for development of the fungus, its association with the fruit diseases – inter- Penicillium funiculosum Thom., causal fruitlet corking, leathery pocket, and fruitlet organism of leathery pocket, fruitlet core rot/ core rot/black spot (Plate 34). black spot, and inter-fruitlet corking. Leathery pocket can be particularly severe if fruit matu- BIOLOGY ration occurs under low moisture conditions Description of stages. (M.K.P. Meyer, Pre- followed by rainfall during later fruit enlarge- toria, 1999, personal communication). Egg: ment, due to cracking of fruit tissues followed oval, opaque white, and large relative to the by fungus infection (Rohrbach and Apt, adult; they are laid singly. Larva: the oval, 1986). Its incidence is extremely variable white active larva has three pairs of legs in the and normally low. However, it peaks between position of the adult’s first three pairs of legs. January and April (South Africa), and cannery Pupa: mature larvae enter a quiescent pupal slice recovery has been reduced from a poten- stage, which is shiny white and elongate tial 16% to as low as 3% (Petty, 1990b). It oval. Adult female: elongate oval (150–240 µm was generally found that plants with a high wide), light amber to creamy brown; the mite infestation after forcing bore fruits with fourth pair of legs is very thin terminating in high levels of leathery pocket (G.J. Petty, 1976, long setae (Plate 35). Adult male: the fourth unpublished). Mourichon et al. (1987) found pair of legs of the smaller male is robust and that fruit mite infestation in pineapple flowers claw-like. 9 to 10 weeks after forcing could be correlated with the subsequent incidence of leathery Life cycle. Due to culturing difficulties, pocket. Further evidence for the importance very little biological information is available. of these mites was provided by research The cycle may be completed in 7–14 days showing that both mites and leathery pocket (Py et al., 1987). Male and female larvae pass are very effectively controlled with foliar through the sessile pupal stage in which trans- sprays of endosulfan, which does not control formation to the adult takes place within the P. funiculosum (Petty, 1990c). In the southern bloated larval integument. A fourth pair of hemisphere, relatively moister south-facing legs and genitalia develop distally, append- plantation slopes are more affected by these ages are withdrawn from the old integument, fruit diseases than are north-facing slopes. and the adult emerges through the dorsally split pupal skin. By parthenogenetic repro- SAMPLING AND MONITORING Sampling for duction, males may be produced from haploid the monitoring of infestations should take eggs. Warm temperatures with very high cognizance of the distribution of these mites. relative humidity and low light intensity Petty (1992) found most mites in the light are optimal for the mites’ development. Their green zone of leaf bases, i.e. between the soft preferred locations on pineapples are on leaf white basal section and the dark green distal bases and the inflorescence and developing section. On the plant as a whole, total number fruit, especially in blossom cups. Their of mites per leaf increased from the youngest,

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176 G.J. Petty et al.

A-whorl, leaf to a maximum on 300–400 mm average, and up to 90% control. Timing of long C-whorl leaves (third spiral from apical sprays is critical. Mite infestation should be as meristem), progressively decreasing there- low as possible during the 5-week post-force after to very low numbers lower on the plant period (Rohrbach and Apt, 1986), and minimal where leaf angle to the stem is more obtuse. mite infestation following endosulfan treat- The lower dirt and trichome contamination ment requires 5 weeks. In studies on the of C leaves facilitates mite counting. Because control of blackspot disease (G.J. Petty, 1999, of their small size, a stereomicroscope is unpublished), good control resulted from required for fruit mite counting – which foliar sprays of benomyl (from 1 week before may be directly on leaves; but the procedure to 11 weeks after forcing) combined with endo- recommended for the pineapple flat mite is sulfan (at 5 weeks and 1 week before forcing). advantageous, i.e. removal of mites into liquid suspension, filtration, and total or subsample Cultural control. For plant crops on south- counting. facing aspects (southern hemisphere) or north-facing aspects (northern hemisphere) ECONOMIC THRESHOLD An economic thresh- avoid, as far as possible, forcing the plants old must be based on fruit mite infestation for crop maturity at a time of year when immediately preceding time of forcing, with P. funiculosum diseases are known historically the objective of attaining minimal infestation to attain maximum severity. during the following 5 or more weeks. This goal is usually impractical and, therefore, the Pineapple flat mite/pineapple red mite, threshold should be the following situations Dolichotetranychus floridanus (Banks) which are conducive to high leathery pocket incidence: (i) plant (as opposed to ratoon) crop Dolichotetranychus floridanus (Banks), the plantations; (ii) plantations on cool, moist pineapple flat mite/pineapple red mite, aspects; and (iii) forcing dates which ensure although probably universal (Annecke and harvesting at a time of year historically known Moran, 1982), has been reported in locations for high leathery pocket incidence. including the pineapple growing countries and regions of Central America, the Philip- CONTROL pine Islands, Brazil, Hawaii, Cuba, Taiwan, Natural enemies. No effective natural India, South Africa and Australia. enemies are known, but the thrips, Podothrips lucasseni (Krüger), is a predator of fruit mites BIOLOGY in Hawaii (Meyer, 1981). However, the host Host plants. Their greatest importance is mite may have been incorrectly identified as on pineapple, but in Egypt they occur on grass S. ananas (Beer, 1954). and bamboo species (Wafa et al., 1968–1969), and in India on cardamom spice crops, Chemical control. Only when the fruit dis- Elettaria cardamomum Maton (Siddappaji et al., eases are potentially of economic importance 1989). may it be justifiable to apply control measures for leathery pocket mite and, in fact, measures Description of stages. Egg: light orange and are seldom applied as these diseases are diffi- oval; large, relative to mite size. Larva: amber, cult to predict, depending on weather condi- with distinct red eyes and six legs. Proto- tions, and are usually sporadic. Endosulfan is nymph and deutonymph: orange-yellow, registered for leathery pocket control in South with eight legs. Adult female: orange-red Africa (Krause et al., 1996). Petty (1990c) found and elongate oval, measuring 450 by 170 µm. that good control may be obtained with foliar Adult male: slightly smaller than females, i.e. sprays of 140 ml endosulfan 350 EC per 100 l 300 by 140 µm, with a more pointed abdomen. water. Five sprays at 4-week intervals starting 4–5 weeks pre-forcing and ending 11–12 Life cycle. Published information is lack- weeks post-forcing gave 69.1% control, on ing, but under the hot conditions of late

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Pests of Pineapple 177

summer and autumn, the cycle may be infestations may result in economic damage. completed in less than 10 days. Under conditions for optimal plant growth, even heavy infestations may not result in SAMPLING AND MONITORING After digging significant damage as colonies diminish or out a plant sample as large as is practicable, disappear. However, if a warm, dry period peel back the leaves to determine feeding is anticipated, planting material should be damage on the bases of older leaves. Older disinfested. damage appears as dents above leaf bases (Waite, 1993). Feeding sites occur in the CONTROL narrow space between leaf bases and plant Natural enemies. The phytoseiid mite, stem, on the whitish adaxial leaf surface Amblyseius benjamini Schicha, is commonly (Petty, 1990e). For monitoring of infestation, found with flat mites in South Africa, their remove the oldest ten living basal leaves to body contents coloured orange by their prey obtain a mite count. The basal section of each (Meyer, 1981). It also occurs in Australia leaf is then excised and immersed in a solution (Waite, 1993) but cannot suppress severe flat such as ethanol or formaldehyde + acetic acid mite infestations. Other South African preda- + ethanol, for some hours. Thereafter, mites tory mites include Lasioseius spp. and Procto- may be filtered out of suspension for counting laelaps spp. (Ascidae), Anystis baccarum (L.) under a stereoscopic microscope. Alterna- (Anystidae), Cunaxoides spp. (Cunaxidae) and tively, record the mean number of infested Triophtydeus spp. (Tydeidae) (Petty, 1990e). leaves per ten leaves for a suitably large plant Mohamed et al. (1982) found that the female sample (Petty, 1988). Egyptian predatory cheyletid mite, Cheyletus cacahuamilpensis Baker, consumed 224 flat ECONOMIC THRESHOLDS Plants of all ages are mites, and the male, 104, during their life attacked, but the mites are most damaging on spans. new plantings where growth can be severely curtailed, with progressive wilt (Giacomelli Chemical control. Planting material dips and Py, 1981; Waite, 1993). In Australia flat with systemic organophosphate pesticides mites are a serious pest, and in Bahia, Brazil, were effective despite the mites’ location in they are widely distributed and important concealed niches (Meyer et al., 1987). Dipping in commercial plantations (Sanches and Zem, of ‘Perola’ pineapple slips in 0.11% ethion, 1978). Heavy infestations may kill plants, or 0.03% omethoate or 0.09% vamidithion for reduce their vigour and fruit yield (Meyer, 6 min gave better control of flat mites than a 1981; Meyer et al., 1987; Petty, 1990e). number of other pesticides evaluated Damage is primarily to the whitish leaf (Sanches and Zem, 1978). Foliar sprays with bases, which develop brown/black necrotic systemic organophosphate pesticides gave lesions and appear progressively dehydrated, better control of flat mites than other pesticide with feeding mites around lesion peripheries, groups (Petty, 1990e). For mite control on or as orange patches on leaf bases. Infestations large ‘Queen’ pineapple plants, 6 l dimethoate may increase on planting material during 400 g l−1 EC in 2000 l water ha−1 gave good storage, resulting in damage and rejection, control (Petty and Webster, 1981b). or irregular establishment in the field. Occa- sionally, crowns are destroyed and fruits Symphylids damaged before harvesting (Waite, 1993). The economic threshold of infestation These pineapple associated myriapods are is related to prevailing weather conditions – species of Hanseniella (Symphyla: Scutigerel- warmer and drier weather generally lowers lidae), e.g. H. unguiculata, H. ivorensis, and the threshold (Petty, 1990e; Waite, 1993) when Scutigerella sakimurai (Symphyla: Scolopend- plant growth and hence leaf elongation is rellidae). Unidentified species of Hanseniella slower, allowing mites to feed for longer are of economic importance in Martinique, periods in specific concealed areas; their num- Brazil and Australia, as is H. ivorensis in Ivory bers increase more rapidly, and initially low Coast.

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BIOLOGY Symphylids preferentially feed on young, Description of stages. Eggs hatch to give the meristematic root tissues, leaving a small cav- 2 mm long, white, centipede-like symphylids, ity in the tip. Resultant symptoms depend on with six (Scutigerella spp.) or seven (Hansen- stage of plant development and the intensity iella spp.) pairs of legs. They grow and moult, and duration of attack. Newly established progressively developing more antennal and plants may be unable to develop roots more body segments and legs so that the 6–10 mm than a few centimetres in length and the root long adults (depending on species) have 12 system becomes a bush of short, branching pairs of legs. They have prominent antennae witches’ brooms. A later, less sustained attack and well developed cerci. will allow the development of longer roots with terminal swellings and secondary roots Life cycle. Ten or 11 eggs are laid in the which, if also damaged, will form witches’ soil and hatch in about 10 days to give the brooms (M. Kéhé, 1980, unpublished). Infesta- immature stage, developing into adults which tions result in plants appearing unthrifty, wilted may live for several years. The life cycle may and near death, with poor ground anchorage be completed in less than 50 days, under and fruit yield (Sinclair and Scott, 1997). optimum conditions. Drought conditions exacerbate the problem, and new plantings may be slow to establish Habits and behaviour. They live in soil, under symphylid attack (Waite, 1993). The especially well structured clay loams, and uniformity of plant damage in plantations, gravelly sandy and clay loams (Sinclair and due to symphylids, is positively correlated to Scott, 1997). Stony, coarse grained soil struc- the uniformity of soil moisture (Py et al., 1987). tures are favourable (Waite, 1993). They feed Economically important infestations may on organic matter and on rootlets and root develop if soil conditions and food supply are hairs and, by their pruning action, multiple optimal, especially with degeneration of resi- branching occurs giving roots the typical dues of soil applied pesticides (Waite, 1993). ‘witches’ broom’ effect (Waite, 1993). Infesta- In Martinique, experimental symphylid tions are normally sporadic. Symphylids sur- control increased mean fruit mass by 77%, and vive drought conditions by moving deeper suckers per plant by 530% (J.J. Lacoeuilhe, into the soil, through naturally formed 1977, unpublished). In Ivory Coast, similar apertures, but they do not reproduce at these results were obtained (Py et al., 1987). In greater than normal depths (Masses, 1979). Australia, when potted pineapple plants were infested with 12, 24 or 48 symphylids per plant, roots were reduced, in 9 weeks, by MONITORING The presence of these white symphyla may be determined by scattering 47.7%, 61.7% and 92.8%. The latter failed to soil samples on a sheet of black plastic, as establish; the others were severely retarded they are easily visible on this background. (Murray and Smith, 1983). Likewise, shake pineapple root systems over Regarding an economic threshold, Waite black plastic; the roots should be checked for (1993) stated that when symphylid numbers witches’ brooms. in the preceding crop exceed 20 per plant, chemical control is likely to be beneficial.

ECONOMIC IMPORTANCE AND THRESHOLD Symphylids have been a problem to the CONTROL Hawaiian pineapple industry since about Natural control. Predation, in Australia, is 1925 (Sinclair and Scott, 1997). Known in Aus- ineffective (Waite, 1993). In Hawaii, predators tralia since 1968, they occur throughout include a centipede and a beetle larva (Py et al., Queensland and south of Mackay are the most 1987). important soil arthropod pests; they affect about 35% of the Australian pineapple indus- Cultural control. Thorough intercycle soil try. Only Hanseniella spp. is of economic preparation will ensure minimal symphylid importance. infestation at time of planting.

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Chemical control. Presently, synthetic pes- Initial symptoms are small yellow spots on ticide application is the only method that can adaxial leaf surfaces, increasing in size up be recommended for symphylid control (Py to 15 mm and fusing to form yellow streaks et al., 1987); pesticides should be applied which become brown and necrotic (Collins, as pre-plant soil treatments to protect the 1960). The infection spreads downwards, critical early plant development (Masses, eventually affecting the apical meristem; 1979). Good, long lasting control is achieved with unequal growth the plant assumes a with lindane at 23 l ha−1 of the 20% formula- bent growth form, eventually succumbing to tion. Slow release granules of ethoprophos, the infection. Fruits become infected through chlorpyrifos and carbofuran applied as pre- the crowns while these are still attached to plant, soil incorporated treatments reduced fruits on the plants. Infected crowns die and symphylid root damage and significantly dry out, and the internal fruit tissues become increased ‘Smooth Cayenne’ pineapple yield necrotic (Pegg, 1993). Infections initiated (Waite, 1996). Post-plant treatments are also in floral cavities at flowering destroy the usually essential, and must be applied as foliar affected fruitlet, and some of those adjoining sprays, or granules at the plant bases (Py et al., it, resulting in a dry, blackened cavity – 1987). commonly known as ‘dead-eye’. There is a tendency for surrounding fruitlets to Integrated pest management. Thoroughly develop into the cavity and for the whole prepare soil during the intercycle period. fruit to assume a curvature towards the Prior to planting, determine symphylid dead-eye side (Petty, 1990f) (Plate 37). For infestation on a black plastic sheet (as onion thrips to become infective they must described above). If numbers exceed the eco- feed on infected plants as nymphs (not nomic threshold, or where soils have a history adults), and they remain infective thereafter. of high symphylid infestation, ensure that approved pesticides for symphylid control are BIOLOGY Both monocotyledons and dicot- applied. yledons are included in a wide range of host plants. Cultivated species include cucurbits, crucifers, legumes, garlic, onion, cotton and Onion thrips or yellow spot thrips, the tomato family (Annecke and Moran, 1982). Thrips tabaci Lindeman Weed hosts, found in pineapple fields, include As a vector of the tomato spotted wilt virus Emilia sonchifolia, Emilia sagittata, Bidens pilosa (TSWV) (Sakimura, 1960) from weed host and Datura stramonium (Py et al., 1987). species to pineapples, this thrips is occasionally responsible for severe occurrences of Description and life cycle. Few males occur yellow spot (YS) disease of pineapples – in warm climates (Macgill, 1927; Sakimura, first observed in Hawaii in 1926, and sub- 1932) and reproduction, as in glasshouses sequently in the Philippines and Australia (Morison, 1957), is mainly parthenogenetic. (Lewcock, 1937), and in 1937 in South Africa White, bean-shaped eggs are laid singly, on (Carter, 1939). More than 80% of fruits in various parts of the plant, either scattered or one plantation block in South Africa were in short rows along leaf veins. The eggs are discarded due to YS (G. Petty, Eastern Cape, embedded deeply by the ovipositor blades South Africa, 1981, personal observation) and the incision closes almost completely (Plate 36). Fortunately, this degree of severity (Lewis, 1973). At 18°C an average of 80 eggs is unusual. Most susceptible to YS are young per female were laid; at higher temperatures, plantations from crowns; slips are less more were laid and they hatched more susceptible. These, especially crowns, are the quickly and more successfully (Lewis, 1973). predominant planting materials for ‘Smooth The amount and quality of food available Cayenne’ pineapple. Suckers/shoots are least play an important role in determining egg susceptible – perhaps providing less attrac- production. The first of the four nymphal tive feeding sites for thrips (Collins, 1960). stages emerge after 5–10 days’ incubation.

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These are pale yellow or brownish, and CONTROL mature within 30 days. The 1–1.5 mm long Natural enemies: predators. According to adult is slightly darker than nymphs, with Lewis (1973), there are many general preda- yellowish fringed wings. They may be dis- tors, including anthocorid and mirid bugs, tinguished from Frankliniella thrips species lacewings, dipterous larvae, ladybird beetles occurring in pineapples by ascertaining the and other thrips. Macgill (1939) reported that following morphological characters (Petty, five or six thrips per day may be killed by 1978c). Antennae: seven segments; terminal mesostigmatid and trombidiid mites, which segment not divided and very short. Pro- attach themselves to thrips’ intersegmental notum: no prominent setae on front angles. membranes. Forevein: distal portion has four setae. At 21°C (Sakimura, 1937) the adult female Natural enemies: parasites and pathogens. life span of 59 days includes 3 days pre- Species of minute parasitic wasps (Eulo- oviposition, 50 days oviposition and 6 days phidae) attack the larvae, and Trichogram- post-oviposition. matidae and Mymaridae parasitize the The method of feeding, which is unique eggs. Pathogenic fungi, e.g. Entomophthora to thrips, has been variously described as: sphaerosperma, also inflict mortality (Charles, (i) puncturing of tissues and draining cell 1941; Stradling, 1968). contents causing their walls to collapse; (ii) piercing the epidermis and rasping the tissues Integrated pest control. Onion thrips, and within; or (iii) rasping leaf tissues and sucking the YS virus disease that they transmit, can the sap. There is a progressive histological be very well controlled with a combination degeneration of the leaf as a result of feeding. of chemical and cultural practices which A glandular secretion from the thrips’ mouth- maintain plantations free of weeds, especially parts area is thought to partially predigest those species which are virus and thrips hosts. their food (Lewis, 1973). Appropriate herbicides are required. Linford Mixed populations of onion thrips and (1943) found that the virus can be carried by Frankliniella spp. were monitored in a pine- thrips from weed hosts for many hundreds of apple plantation in the Eastern Cape (South metres. Care should therefore be taken not Africa) in 1976 (Petty, 1978c) to determine sea- to disturb such weeds when pineapples are sonality, and the effect of a weed infestation most susceptible to thrips, i.e. in early growth (mainly B. pilosa). They predominated in the stages and at fruiting. summer and autumn months, and in weed infested areas. Pink pineapple mealybug, Dysmicoccus brevipes (Cockerell) SAMPLING AND MONITORING These actions are not normally taken, as the control mea- Worldwide, pineapple industries regard this sures described below are usually adequate to mealybug as a major threat to the crop obviate any thrips-associated problems. How- because of its association with the devastat- ever, if monitoring is required, thrips can ing disease, pineapple mealybug wilt (PMW) be satisfactorily trapped (Petty, 1978c) by (Plate 38). applying an adhesive coating of polybutene (suitably thinned with paraffin/kerosene) BIOLOGY This species originated in tropical to a sheet of polythene which may then be America, where the pineapple itself origi- wrapped around a 5 l cylindrical drum. By nated. The mealybug was spread on planting affixing the drum to a pipe it can be placed at material to plantations around the world plant-canopy height and will capture flying (Rohrbach et al., 1988). Its more than 50 host adult thrips. The polythene sheet may be species include sugarcane, perennial grasses, removed for the identification and counting, e.g. Panicum barbinode and Tricholaena rosea, with a stereoscopic dissecting microscope, of and sisal Agave sisalana (Petty, 1976a). The thrips adhering thereto. mobile immature crawler stage, with flattened

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bodies and long hairs, may be wind-dispersed long crawlers are produced per reproductive for hundreds of metres within plantations mealybug, with a maximum of 692 recorded. (Rohrbach et al., 1988). The big-headed ant, The 3–4 mm long adult female is Pheidole megacephala (Fabricius), also plays an elongate-oval, distinctly segmented and important role in its dispersal (Carter, 1932). coated with a white waxy secretion. Around Pineapple roots and lower leaf axils are the lower periphery of their bodies are predominantly infested (Carter, 1949). On the 34 waxy filaments – lateral filaments are ‘Queen’ pineapple cultivar, numbers declined 0.25 × body width; caudal filaments, 0.5 × from 3.35 on the oldest living leaf to 0.19 on the body width. Mature mealybugs are fairly tenth leaf, continuing to decline thereafter; immobile as body development exceeds leg 88% of aerial infestation was on the oldest ten development. basal leaves (Petty and Webster, 1981a). In mature plants, heavy infestations may occur MEALYBUG–ANT SYMBIOTIC RELATIONSHIP Ant on slip bases, lower fruit surfaces around importance in pineapple plantations is solely peduncles, and within fruitlet floral cavities. due to their positive promotion, through Planting material infestation, originating from symbiosis, of mealybugs and PMW (Reimer mother plants, may increase during its storage et al., 1990). Symbiotically related ant species but typically declines if planted in the absence include P. megacephala; fire ant, Solenopsis of ants (Carter, 1932). geminata (Fabricius); Argentine ant, Irido- Reproduction is parthenogenetic and myrmex humilis (Mayr); Technomyrmex albipes ovoviviparous. However, a bisexual race (Smith); Camponotus friedae Forel; Anoplolepis occurs in Ivory Coast, Madagascar, Domini- gracilepes (S. Smith) (formerly known as can Republic and Martinique; apart from this A. longipes Jerdon); and Araucomyrmex spp. race, pink mealybugs only produce females Caretaking by these species includes the (Beardsley, 1964). Until about 1959, D. brevipes building with debris, and maintenance, of was confused with Dysmicoccus neobrevipes shelters, protecting mealybugs from natural Beardsley, the grey pineapple mealybug. enemies and inclement weather (Rai and Ito (1938) noted biological and behavioural Sinha, 1980). differences, and Beardsley (1959) noted Ants remove mealybug excreted honey- morphological differences as summarized dew, preventing an unhygienic build-up of in Table 6.4. Capnodium sp. sooty mould (Beardsley et al., At 23.5°C, developmental stages of the 1982; Duodu and Thompson, 1992). Mealybug pink mealybug have the following durations leaf infestation of ‘Queen’ cultivar pineapples (Ito, 1938): three larval (crawler) instars, decreased by 90% within 20 weeks of P. 34.03 days; adult pre-larva position, 26.58 megacephala control with hydramethylnon days; adult larva position, 24.84 days; adult bait-toxin, and root infestation by almost post-larva position, 4.70 days; total adult life 100% within 12 weeks (Petty and Tustin, span, 56.23 days; total life span, 90 days. 1993). Under these conditions, a high positive On average, 234 yellowish, less than 1 mm linear correlation prevailed between ant

Table 6.4. Biological and morphological differences between pink and grey mealybugs.

Variable Pink mealybug Grey mealybug

Ventral sclerotization of anal lobes Quadrate Elongate Long dorsal abdominal setae Present Absent Reproduction Parthenogenetic Bisexual Mature female colour Pinkish orange Greyish Preferred location on plant Roots and lower plant Fruits, crowns, upper plant Graminaceous plant hosts Yes No Green spotting of leaves No Yes

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infestation and mealybug leaf infestation SAMPLING AND MONITORING Mealybug (r = 0.978, P < 0.01), and root infestation infestation of the roots and basal ten leaves (r = 0.769, P < 0.01). The relationship between should be assessed (Petty and Webster, 1981a), ant distribution and mealybug infestation was just prior to environmental conditions favour- similar. When uncontrolled, ant numbers did ing their development – plant phenology and not correlate, i.e. were no longer a limiting seasonal climate being major factors. In South factor, and pineapple growth in 52 weeks was Africa, infestations increase during the drier reduced by 17%. autumn and winter months. By assessing symbiotic ant infestations, PINEAPPLE MEALYBUG WILT PMW commences mealybugs may be indirectly monitored. A with cessation of root growth (Carter, 1935), peanut butter–soybean oil mixture is highly root systems becoming reduced and necrotic. attractive to big-headed ants, which may be Leaves turn a deep pink, yellowing and counted on wooden laths with the mixture, wilting; tips die back as edges curl down- placed at suitable intervals around plantation wards. Fruits may fail to develop, or remain blocks. Even a small number of these ants is small, fibrous and sour. Symptom expression sufficient to warrant further investigation and may take a number of months to develop, and possibly control measures. plants may appear to recover (Carter, 1945). PMW is of worldwide distribution, limited ECONOMIC THRESHOLD Occasionally, single only by the climate suitable for the host plant mealybugs result in PMW (Carter, 1937). (Carter, 1954). When grown commercially Because of the close big-headed ant– and continuously on the same land, PMW mealybug relationship (Petty and Tustin, becomes a limiting factor. In Cuba (and many 1993), tolerance for both species appears mini- other countries) it is one of the most important mal. The relationship between wilt in virus pineapple diseases, causing up to 40% crop infected plants and mealybug induced stress losses (Borroto et al., 1998). First reported by is presently unknown, and for virus-free Hawaiians in 1910 (Rohrbach et al., 1988), it plants the effect of mealybug infestation devastated their industry in the 1920s and densities. Such information is essential to the 1930s. Carter (1933) hypothesized a toxic formulation of economic thresholds. mealybug secretion aetiology for PMW, later (1963) modifying this hypothesis as subse- CONTROL Once established, wilt is difficult quent findings indicated a viral aetiology. The to control because of vegetative propagation existence of a virus in both mealybugs and and latent symptoms in planting material pineapples with PMW symptoms was proven (Rohrbach and Apt, 1986). Management of by Gunasinghe and German (1989), with the PMW problem requires the integration of their finding of double stranded RNA and monitoring of the species involved and the long, flexuous rod-shaped virus particles. application of chemical measures designed to With dimensions of 1200 by 12 nm, and coat maximize the impact of natural and biological protein molecular weight of 23 by 103 Da, the controlling factors for mealybugs. Cultural subgroup II closterovirus was indicated. This control measures should also be applied if virus was detected with a monoclonal anti- possible. body test in mealybugs from PMW plants. It could not be detected in seedling pineapples Mealybug and ant management. From the (Hu et al., 1996). Sether et al. (1998) proposed late 1920s, mealybugs were controlled with the name ‘Pineapple mealybug wilt- the following succession of pesticides: oil associated virus’ (PMWaV). PMWaV from emulsions, parathion, malathion, diazinon diseased Australian pineapples was sero- and dimethoate. The latter are still used as logically related to the Hawaiian isolate foliar sprays or planting material dips (Krause (Wakman et al., 1995). It appears to comprise et al., 1996). Dips materially suppress infesta- a group of closely related closteroviruses tions and their spread in new plantations. (Thomas et al., 1999), and in Australian pine- However, fumigation with methyl bromide apples a bacilliform virus (PBV) also occurs. gas is highly effective (Petty, 1984; Willers,

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1990; Petty et al., 1991), without phytotoxicity immunoassay which detects the virus in if applied correctly (Petty, 1987). The practice symptomless plants. does unfortunately have practical problems and environmental hazards. Pineapple scale, Diaspis bromeliae (Kerner) From the mid-1940s, ant control pesticides included DD, benzene hexachloride, Pineapple plantations worldwide are subject heptachlor, chlordane, HHDN/dieldrin, to pineapple scale insect (PSI) infestation Mirex bait toxin, hydramethylnon bait toxin/ (Annecke and Moran, 1982; Bedford et al., Amdro® (American Cyanamid Company, 1987; Waite, 1993). Carter (1967) stated that Wayne, New Jersey). Amdro 1500 p.p.m. it is the only scale insect of economic − formulation at 2.24 kg ha 1 was shown in 1980 importance on pineapples. (Su et al.) to give big-headed ant control comparable to the then standard treatment, Mirex. BIOLOGY Reimer and Beardsley (1990), Petty (1993) Hosts, location and damage. Alternative and Petty and Manicom (1995) subsequently hosts include agave and bromeliads (Waite, confirmed its exceptional efficacy. It has full 1993) and Billbergia spp. (Brimblecombe, 1955). − registration in South Africa, at 2 kg ha 1, and is PSI typically infests the lower pineapple accepted (Samways, 1985) by myrmicine ants leaves, which are more shaded, but where (Pheidole, Myrmicaria and Monomorium spp.) plants are growing in shaded positions PSI are and dolichoderine ants (Technomyrmex spp.) inclined to occur higher on plants. Suckers but not by formicine species of Anoplolepis, in densely grown ratoon crops are most sub- Acantholepis and Camponotus. ject to damage. Fruits may be very heavily infested, especially ratoon fruits lodged Biological control. A number of potentially between ridges (walking spaces). PSI infesta- effective coccinellid beetles and encyrtid para- tion of mature fruits in spring is typically of sitoids have been identified. Anagyrus ananatis the lower parts (Waite, 1993). Where a PSI has Gahan (Hymenoptera: Encyrtidae) effectively inserted its long, hair-like mouthparts into a controls mealybugs in the absence of ants leaf for feeding, a yellow spot develops due (Gonzalez-Hernandez, 1995). It originates in to its toxic saliva (Py et al., 1987). This may be Brazil, is very host specific, and has a 20-day the full extent of their damage but heavily generation period. Exochomus concavus Fursch infested plants assume a greyish scaly appear- (Coleoptera: Coccinellidae), under laboratory ance, are weakened and stunted, have foliar conditions, consumed 61 and 94 (155 total) dieback and small, unsightly, unmarketable mealybugs per larva and adult, respectively fruits. Fruit cracking may result from heavy (Petty, 1985). PSI feeding (Carter, 1967).

Cultural control. Hot water immersed, Description and life cycle. The adult female PMWaV-infected, ‘Smooth Cayenne’ crowns PSI secretes and is covered by a hard, circular, lost their infection, and if maintained mealy- waxy, beige coloured shell which at maturity bug-free, PMW did not develop after planting is about 1.3 mm wide (Petty, 1990d). The soft- (Ullman et al., 1991). This could not be verified bodied, yellow insect is roughly triangular in in Australia (Thomas et al., 1999). outline; legs and antennae are not apparent Selection of apparently healthy plants in and it has long hair-like stylets for mouth- Mexican commercial plantations has resulted parts. A number of oval, translucent-yellow in PMW-resistant selections which also have eggs are laid under the scale cover. These other commercially favourable characteristics hatch in about 7 days. Newly hatched imma- (Torres Navarro et al., 1989). The selection ture ‘crawlers’ are minute, yellowish and very process could be speeded up and made more active. On establishing a feeding site, crawlers reliable with a technique developed by Hu shed their legs at the first moult and remain at et al. (1997), using specific monoclonal anti- that site thereafter. The three larval stages, and bodies to the PMWaV in a tissue blotting a pupal stage, are completed in about 60 days

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in summer (Carter, 1967). Immature male scale of the species in the Afrotropical region insects develop under an elongate, whitish (Prinsloo, 1985). The female is black with scale cover less than 1 mm long, emerging at a partially yellow abdomen (lacking in the maturity as small, winged, orange-coloured male), and 0.671 mm in length. They are insects which mate and die after a short life highly numerous, at times causing heavy scale span. mortality. At a mean temperature of 24°C, mean development time – egg to adult – was Population fluctuations. There are up to 27 days (G.J. Petty, 1998, unpublished). four, overlapping, generations per year. Eggs In Australia, two small parasitoid wasp are laid throughout the year, in Australia, species, Aphytis sp. and Aspidiotiphagus sp., with peaks in summer and early winter are important, as is the ladybird Rhyzobius (Waite, 1993). PSI is spread into new planta- iophanthae (Coleoptera: Coccinellidae) (Waite, tions mainly on infested planting material 1993). when this is not insecticidally treated (Bedford et al., 1987). Crawlers are spread by Integrated pest management. Pesticides for wind, and on the clothing of farm workers. pineapple mealybug control will also control PSI (Waite, 1993). However, the injudicious use SAMPLING AND MONITORING Plants, espe- of persistent insecticides may result in a PSI cially shaded ratoons and where growth is infestation explosion by destroying their natu- dense, should be visually inspected on a ral enemies (Sakimura, 1966). Before reaching regular basis, especially during dry periods a decision to spray insecticides, examine the (Petty, 1990d). Where a zinc deficiency in scale insects to determine if natural enemies plants occurs, extra vigilance is required as are present in significant numbers. this appears to favour multiplication (Py et al., The spread of PSI from heavily infested 1987). Cognizance is required, in monitoring ratoon crops to new plantations may be con- of PSI, of the potential effect of natural ene- trolled either by burning the plants at the end mies, especially hymenopterous parasitoids, of the ratoon crop cycle, or by sanitizing the on these insects. Less than 50% of female planting material (‘Queen’ suckers or ‘Smooth scales were found to be living in most Cayenne’ tops and slips). As far as possible, months in Australia (Brimblecombe, 1955) the use of planting material from PSI infested and Murray (1984) ascribed a 40% mortality blocks should be avoided. If it must be used it level to the combined actions of predators may be effectively sanitized by fumigation and parasitoids. Internal parasitoids, on com- with methyl bromide as described by Petty pleting immature development, chew small (1984) and Willers (1990). Fumigation of plant- emergence holes in the scale cover – these are ing material with 40 g m−3 methyl bromide readily detected with the naked eye, or a hand gas for 2 h, with a temperature range of 20 to lens. 25°C, gave almost 100% PSI control without plant phytotoxicity (Petty, 1987). Similar CONTROL results were obtained in Australia (Murray Natural enemies. The need for chemical et al., 1979). control is largely obviated by the existence of a number of effective internal hymenopterous Pineapple caterpillar, Thecla basilides (Geyer) parasitoids. In South Africa these include Ablerus elegantulus (Silvestri) and Encarsia spp. The pineapple caterpillar’s distribution is (Aphelinidae); Tetrastichus sp. (Eulophidae) limited to the Americas from Mexico to (this species may now have been transferred Argentina (Py and Tisseau, 1965), and to a new genus); Coccidencyrtus ochraceipes Trinidad (Harris, 1927). Gahan (Encyrtidae). C. ochraceipes was first collected at Hluhluwe, South Africa, by the BIOLOGY senior author and identified by Dr G.L. Host plants. In Brazil, on wild pineapple Prinsloo, who noted that it was the first record species, e.g. Ananas ananassoides (Smith), and

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other indigenous Bromeliaceae; in Honduras, 16 days larvae attach themselves with a fine on maize and cacao (Rohrbach, 1983); in silk thread to the plant’s leaf axils and pupate. Trinidad, on Heliconia sp. (Harris, 1927). Within 11 days the butterfly emerges. Devel- opment time, from egg laying to adult, varies Description of stages. The following is from 23 to 32 days, with an adult life span of 22 according to Harris (1927) and Sanches (1993). days, and total life span of about 51 days. Egg: a whitish, reticulated 0.8 mm sphere, flattened basally; a small dorsal spot demarcates Damage. The larval galleries in fruits fill the micropyle. Larva: on hatching, the first (of with a clear gum-like fluid which exudes out four) instars measures about 1.5 mm, is pale of fruits, hardening and darkening to amber yellow, darkening with age, with head and and dark brown. These fruits develop an thoracic region somewhat darker. It is finely unpleasant smell and taste and are unsaleable. pubescent with four rows of long abdominal Fusariosis disease may be greatly increased hairs and four rows of shorter hairs. The sec- due to creation of ports of entry for Fusarium ond, and subsequent, instars are woodlouse- subglutinans fungus infection. Infection is also like and at maturity are about 20 mm long and increased through dissemination of fungus 6 mm wide. Five pairs of pink longitudinal spores by visiting butterflies. Decomposition stripes gives the yellowish body a pink of the fruit occurs on the plant, with dehydra- appearance. The head is concealed by the pro- tion, shrivelling and blackening. Surveys thorax, the body compressed dorsoventrally, conducted in Brazilian states have estimated and the terminal abdominal segments are damage at between 30 and 80%. It follows that flattened, wedge-like. Pupa: about 13 mm this species is one of the main pests of pineap- long; pink coloured with dark spots and a ple in Brazil, causing great losses to growers characteristic dorsal hump. The imago adult (Sanches, 1981). Winter forcings (November– female: a butterfly with a 28–35 mm wing- March) in Brazil are most at risk; in Mexico the span, dorsally slate-grey with a darker border high risk period commences in April (Py et al., and white fringe; posterior wings have two 1987). orange spots near a pair of filiform appendages. Ventrally, wings are silvery grey with MONITORING Slips and developing fruits a number of orange spots. The imago adult should be examined for the presence of eggs at male: a somewhat smaller butterfly than the the time inflorescences appear. Eggs are easily female with a large black spot centrally on the seen, provided carbide has not been applied anterior wings. for forcing the plants. In areas of low incidence, effective control is easily achieved Habits and life cycle. Female butterflies (Sanches, 1993). Particular vigilance is required deposit their eggs singly and widely sepa- at those times of the year when the pest is most rated mainly on upper and middle fruitlet active. bract bases, from prior to anthesis until anthesis is well advanced (Harris, 1927), but ECONOMIC THRESHOLD Plantation densities − also on peduncles and slip bases. The potential of 60,000–72,000 plants ha 1 suffer more dam- egg laying capability is 150 per female. Mature age than greater or lesser densities (Choairy fruits are avoided, as the epidermis is too and Fernandes, 1983). However, the presence tough for larvae to penetrate. Already infested of one larva in a fruit is sufficient to render the fruits are also avoided (Rhainds et al., 1996). fruit useless (Sanches, 1981). Larvae hatch within 5 days and burrow into the bracts, or slips, or directly enter buds and CONTROL open flowers. After a short feeding period Natural enemies. Three hymenopteran they exit the fruits and again burrow in to natural enemies are known: Heptasmicra spp., form a feeding chamber, up to one-third fruit a chalcid parasite, and Polistes rubiginosus, diameter in depth. Initial symptoms pre- a vespid predator, both in Trinidad (Harris, dominate on the fruit’s lower half. Within 1927). The latter was said to be potentially

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effective. Metadontia curvidentata is a hymen- problem species occur in Australia and South opteran predator (Py et al., 1987). Africa, and are melolonthids and rutelids (Table 6.3). Chemical control. Chemical control is effective if applied from time of flower induction to BIOLOGY protect the young developing fruit to beyond Host plants. White grubs feed on the roots anthesis (Py et al., 1987). Organochlorines are and subterranean parts of pineapple plants advantageous in being less toxic than the (Smith et al., 1995). Pasture grasses and sugar- organophosphorus pesticides, and give lon- cane are also hosts and if they precede a ger residual control. However, their greater pineapple plantation, white grub infestation persistency is a potential environmental of the latter crop may result (Waite, 1993). hazard, which encourages greater use of the organohalides and carbamates (Martinez, Description of stages. The beetle sub- 1976). Pesticides which have been used to families infesting pineapples are very similar good effect include endrin, heptachlor, in many respects. The eggs are white, oval chlordane, toxaphene, carbaryl (Py et al., and 1–2 mm long producing larvae which, to 1987), trichlorfon, malathion, diazinon and the untrained eye, are indistinguishable one parathion (Sanches, 1993). Insecticide sprays species from the other. The white or cream applied at 12-day intervals from bud differen- coloured larval body is cylindrical and tiation to the early fruiting stage reduced fruit assumes a C-shaped posture, and is soft and damage from 35.8 to 0.8% (Suplicy et al., 1966) wrinkly. It has a reddish brown head capsule No reference was found to the use of IGRs with short antennae and prominent, sharply (insect growth regulators), which are effec- pointed mandibles. Mandibular characteris- tively applied for the control of Lepidoptera in tics, such as the number of notches and a other crops. stridulatory area, are diagnostic of the species. Other mouthparts – labrum, maxilla, labium Cultural control. and epipharynx, and the head capsule – pro- 1. The pineapple caterpillar’s spread to vide useful and reliable diagnostic structures, other geographic regions should be controlled e.g. sutures and setae, for laboratory identifi- by preventing free movement of its host plants cation of species. Field identification of larval from infested areas. species is possible by examining, with a hand 2. Less/least susceptible pineapple culti- lens, the setae on the ventral surface of the vars, e.g. ‘Perola’ cv. should be grown where terminal abdominal segment. The arrange- possible. ment, number, and structure of these setae 3. Through artificial flower induction, (the raster) is diagnostic of different species. breeding is restricted to the limited time of The raster area is grey-brown in colour due to fruit sensitivity. the larva’s translucent body wall and the soil 4. Flowering may be induced when the content of its hindgut. pest’s numbers are normally minimal. An individual larva passes through a number of growth stages (instars) and, Pineapple white grubs, Coleoptera: whereas the body posterior to the head con- Scarabaeidae tinues to grow in size, in some species up to 35 mm in length, the head capsule – which Pineapple white grubs are the larvae of a is a more rigid structure – maintains its size number of beetle species in the Scarabaeidae. throughout each larval instar and is character- Of a total of 23 species of greater or lesser istic and diagnostic of each instar (Plate 39). economic importance in pineapples in Mature larvae pupate in the soil, the various parts of the world, 14 species belong pupae gradually darkening to a light to the Melolonthinae, seven to the Rutelinae brown colour. The pupa of each species has and two to the Dynastinae. Most of the characteristics which, with experience, makes

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identification possible. Adult beetles develop- SAMPLING AND MONITORING Sampling size ing from the pupae are all of a medium to must compromise between time available and large size and various shades of brown; some acceptable destruction of plants, on the one bear white scales or fine hairs. Adult beetles hand, and a large enough sample to counter- are generally not recognized by pineapple act the uneven distribution of grubs in planta- growers as the source of their white grub tions to give an acceptable variance between problem. samples. Sinclair and Scott (1997) assessed pineapple root volumes for five-plant sample Habits and life cycle. Pineapple white grub sizes, concluding that this is a practical sample species have a 1-or 2-yearlife cycle. A few, e.g. size but insufficient to give a good population Lepidiota grata and Rhopaea magnicornis, have estimate. The senior author has found a ten- 2 either, as unfavourable environmental condi- plant sample per 1500 m plantation block to tions result in the longer period of develop- be adequate; soil in a 300 mm square around ment (Allsopp et al., 1997). Beetles lay their each plant to a 150 mm depth is excavated and eggs in the soil in plant root zones in spring– sifted through to locate and remove grubs. summer. For the rutelid, Adoretus ictericus, Pre-plant assessments for grub infestation of the average incubation period at 17–22°C soil may utilize a large diameter soil auger was 19 days (Prins, 1965). The melolonthid, mounted behind a tractor and operated via the Macrophylla ciliata, lays up to 70 eggs and these tractor’s power-take-off (PTO). hatch after about 42 days. Eggs hatch at different times of the year, depending on the ECONOMIC THRESHOLDS The feeding activi- species, giving larvae which normally have ties of white grubs – predominantly third three instars (commonly designated L.1, L.2 instar larvae – result in the progressive and L.3). For the Australian species (Allsopp destruction of the root system, followed et al., 1997) larvae (L.2 or L.3) descend in May/ by plants becoming stunted, wilted and June to greater depths, i.e. 350–600 mm, in soil chlorotic, a condition aggravated by drought and hibernate in earthen cells until August/ (Petty, 1990 g) (Plate 40). For Australian spe- September when they pupate (1-year cycle) or cies with a 1-year cycle, damage occurs from change from L.2 to L.3 (2-year cycle). Pupae February to May, and from October (year 1) to mature to adult beetles, emerge from the soil April (year 2) for 2-year cycle grubs (Allsopp after the first soaking rains between Septem- et al., 1997). Heavy infestations result in the ber and November (depending on species) subterranean plant stump having a shaved and fly to feeding trees (some do not feed) appearance, with feeding cavities. Plants lose prior to mating, and egg-laying in the soil. their anchorage in the soil and are easily Larvae becoming L.3 in August/September pulled out. come up again in the soil to feed on roots until In a lysimeter trial, A. subfasciata, L.1 stage April/May of the following year when they larvae were seeded at various infestation again descend to hibernate until September. levels with growing ‘Smooth Cayenne’ cv. Development thereafter is as for a 1-year life plants. At the end of a 12-month period, plant cycle. growth had been reduced by 5.5% with an In South Africa, Asthenopholis subfasciata infestation density of 0.5 grubs per plant is an important melolonthid species. Adult (Petty, 1996). beetles occur from November to January; the The probability of infestation by white males fly actively in December but the females grubs is greatly determined by the nature and do not appear to fly, and the adults do not physical structure of soils. Species specific appear to feed. Larval peaks in soil occur preferences are clearly apparent, e.g. A. sub- in April/May (L.1) May/June (L.2) and fasciata occurs exclusively on red clay–loam October/November (L.3). Pupae occur in soils (Petty, 1996); Antitrogus consanguineus October/December. Most individuals have a on sandy alluvial or yellow podsol soils 1-year life cycle; a minority have a 2-year cycle (Allsopp et al., 1997); and Lepidiota spp. only (G.J. Petty, 1990, unpublished). on red volcanic soil (Sinclair and Scott, 1997).

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CONTROL isazophos was applied in mid-October and Natural control. In South Africa these again in mid-November (Petty, 1996). include a number of bird species, e.g. Hage- dashia hagedash and Numida meleagris, various mammals, e.g. pigs, rodents, mongooses, Conclusions and the toad, Bufo regularis, on beetles (Petty, 1990h). They are also preyed on by species of Pineapple is a perennial crop which requires wasp, robber fly and wireworm; infected by protection from a complex of pests for a pathogenic fungi, e.g. the green soil fungus, period of up to 6 years in cooler subtropical Metarhizium anisopliae and Paraisaria sp., and climates. This creates difficulties which do the milky disease bacterium, Bacillus popilliae not arise in shorter term crops, in the manage- (Allsopp et al., 1997). ment of soil dwelling pests, e.g. nematodes, symphylids and white grubs. It is of crucial Abiotic control. If, after beetle emergence importance that pineapple root systems be and egg-laying, hot dry weather persists for a effectively protected during at least the initial lengthy period, mortality of eggs and young 15 months of their development; damage hatchlings will result (Allsopp et al., 1997). during this time commonly has repercussions mainly in the ratoon crop, on which growers Cultural control. Deep pre-plant ploughing may rely for their profit. in March/April will kill 2-year life cycle L.2 Worldwide, the pineapple industry larvae; between January and May, larvae of depends primarily on the use of chemical 1-year cycle grubs will be killed (Allsopp et al., nematicides for nematode control. These can 1997). be very effective but are also costly and hold potential dangers to both user and environ- Chemical control. Pre-plant chemical soil ment. In order to obtain maximum benefit treatments can be applied only once in more and minimize the dangers, the need to apply than 4 years. Most presently available pesti- pre-plant and/or post-plant foliar nematicide cides are totally broken down to inactive com- treatments should be determined by nema- ponents in the soil in a far shorter period than tode counts for soil, sampled at key times in 4 years. Fortunately, the most critical period the natural development cycle of pineapple for subterranean plant protection is during nematodes. the early development of the plant and The efficacy of volatile pre-plant nema- that can be accomplished with available pesti- ticides, e.g. ethylene dibromide, if required, cides. In Australia, the 50% active formulation should be ensured by only applying these of chlorpyrifos is applied, pre-plant, at the rate at soil temperatures and moisture levels of 5 l ha−1. Annual post-plant booster treat- which exceed the thresholds for satisfactory ments of 3 l ha−1 are applied as high volume soil fumigation; winter temperatures in some foliar sprays (Sinclair and Scott, 1997). southern hemisphere producer countries are Slow/controlled release granular formula- frequently sub-optimum. A too rapid loss tions of, inter alia, chlorpyrifos gave very of fumigant from the soil may be prevented promising experimental results for extend- with a plastic mulch. A suitably fine tilth, ing this chemical’s residual activity in soil, without large soil clods, promotes fumigation but practical application problems have effectiveness. obstructed its marketing (Sinclair and Scott, It is important that forces which are 1997). naturally suppressive to nematodes should A promising new strategy to obtain be encouraged through the development of extended control of white grub infestations is appropriate cropping systems. In this regard, the use of carefully timed insecticide sprays to the organic matter component of soil should coincide with beetle emergence from the soil be conserved and increased by, for example, and egg laying. By this means, A. subfasciata green manuring and reincorporation of plants larval infestation was reduced by 78.5% when on completion of the ratoon crop cycle. Other

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strategies in nematode management, which 1. Spray volume should be adjusted accord- will limit the use of chemical nematicides, are: ing to the location of the pest on the plant. For maintenance of a bare fallow for a number of protection of fruits and slips, lower volumes months; the use of certain nematode-resistant are required than for pests on the basal leaves grass and legume species in a system of crop of the plant. rotation; the use of modern genetic engineer- 2. Water pH could adversely affect pesti- ing technologies to introduce foreign genes cide efficacy, due to alkaline hydrolysis of the which will impart a degree of resistance or tol- active ingredient. erance to the crop. 3. Some pesticide mixtures are incompati- A knowledge of the previous history of ble – either physically or chemically. Mixtures plantation blocks, as regards incidence of soil may also result in phytotoxicity, for example infestation by pest species, is of great value in if bromacil weedkiller and dimethoate are developing a strategic management pro- applied together, severe plant damage will gramme. Pest species often have clear prefer- result. ences for specific soil types and textures, for 4. Pineapple pests usually exist in a com- example, root-knot nematodes on sandy soils plex with other pest species. In the selection of and well-structured clay loams; symphylids a pesticide programme, cognizance should be on, inter alia, the latter and on gravelly sandy taken of this – a subject dealt with by Petty and and clay loams; some white grub species on van der Westhuizen (1992). The loss of effec- red clay loams. Pre-plant soil insecticide tive natural control of pests, for example by application for symphylid and white grub hymenopterous parasitoids of scale insects, control should be made on the basis of pre- due to injudicious insecticide spray applica- vious infestation history and soil type. Pre- tion should be avoided at all costs. ventive control of these pests is required as 5. To obtain the greatest possible benefit attempts at post-plant corrective control are from insecticide sprays, the timing of these generally ineffective. However, certain melo- should take pest life cycles and behaviour into lonthid grub species may be effectively con- account. trolled by carefully timed adulticide sprays. 6. The use of a specific bait toxin to disrupt The control of fruit and foliar insect and the symbiotic relationship between ant and mite pests also tends to be heavily dependent mealybug species is more ecologically sound, on chemical insecticides/acaricides. To some and effective, than the use of broad spectrum extent chemical usage can be reduced by the insecticides. careful selection of planting material from In an integrated pest management pro- pineries which are essentially infestation gramme there should be no weak links which free. It is important to start a plantation could, for example, promote root growth with propagules (tops or slips) which are through disease control only to have the roots minimally infested. If, due to a shortage, destroyed by the nematode component of the infested propagules must be used, they total complex. should be disinfested by dipping in a suitable insecticide, or by fumigating the material with an approved fumigant. Subsequent to the planting of a crop, pest Acknowledgements management should be based on sampling and monitoring of plantations for the presence Sincere appreciation is expressed to the fol- of pests, their natural enemies and symbio- lowing taxonomists of the Plant Protection tically associated arthropods. The methods, Research Institute of the Agricultural Research techniques and use of these strategies are dis- Council of South Africa for their efforts cussed in the text above for the different key to ensure the correctness of the arthropod arthropod species. nomenclature and classification given in When foliar pesticide sprays are deemed Table 6.3: I. Miller, G.L. Prinsloo, R. Stals, necessary, the following should be borne in M. Stiller, E.A. Ueckermann and V.M. Uys. mind: Thanks are also due to those who supplied

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information for the same table, as indicated in Bulletin 411, Department of Agriculture and the table by ‘personal communication’. Water Supply, Republic of South Africa, pp. 27–32. Beer, R.E. (1954) A revision of the Tarsonemidae of the western hemisphere (Order: Acarina). References The University of Kansas Science Bulletin 36(16), 1276–1369. Allsopp, P.G. (1993) Identity of canegrubs Bernard, E.C. and Montgomery-Dee, M.E. (1993) attributed to Antitrogus mussoni (Blackburn) Reproduction of plant-parasitic nematodes on (Coleoptera: Scarabaeidae: Melolonthinae). winter rapeseed (Brassica napus ssp. oleifera). The Coleopterist’s Bulletin 47(2), 195–201. Journal of Nematology 25, 863–868. Allsopp, P.G., Chandler, K.J., Sampson, P.R., Story, Borchsenius, N.S. (1966) A Catalogue of the Armoured P.G., Brodie, A. and Whittle, P. (1997) Root Scale Insects (Diaspidoidea) of the World. ‘Nauka’, feeders. In: Agnew, J.R. (ed.) Australian Moskow, Leningrad, 449 pp. (in Russian). Sugarcane Pests. Bureau of Sugar Experiment Borroto, E.G., Cintra, M., González, J. and Borroto, Stations, Brisbane, pp. 1–21. C. (1998) First report of a Closterovirus-like Annecke, D.P. and Moran, V.C. (1982) Subtropical particle associated with pineapple plants fruits, pineapples. In: Insects and Mites of (Ananas comosus cv. Smooth Cayenne) affected Cultivated Plants in South Africa. Butterworths, with pineapple mealybug wilt in Cuba. Plant Durban/Pretoria, p. 91. Disease 82, 263. Anonymous (1995) Survey on pineapple pests Brimblecombe, A.R. (1955) Pineapple scale investi- and diseases in the Caribbean. Tropical Fruits gations. Queensland Journal of Agricultural Newsletter 14, 3–4. Science 12(3), 81–94. Apt, W.J. (1976) Survival of reniform nematodes in Carter, W. (1932) Studies of populations of Pseudo- desiccated soils. Journal of Nematology 8, 278. coccus brevipes (Ckl.) occurring on pineapple Apt, W.J. and Caswell, E.P. (1988) Application plants. Ecology 13(3), 296–304. of nematicides via drip irrigation. Journal of Carter, W. (1933) The pineapple mealybug, Nematology (Suppl.)2, 1–13. Pseudococcus brevipes, and wilt of pineapples. Barbeau, G. and Marie F. (1997) La production de Phytopathology 23(3), 207–241. l’ananas dans la Caraibe Hispanophone et Carter, W. (1935) Studies on the biological control Anglophone (Pineapple production in the of Pseudococcus brevipes (Ckll.) in Jamaica Spanish and English speaking Caribbean). and Central America. Journal of Economic Acta Horticulturae 425, 53–62. Entomology 28, 1037–1041. Bartholomew, D.P. (1977) Inflorescence develop- Carter, W. (1937) The toxic dose of mealybug wilt ment of pineapple (Ananas comosus (L.) Merr.) of pineapple. Phytopathology 27, 971–981. induced to flower with ethephon. Botanical Carter, W. (1939) Geographical distribution of Gazette 138(3), 312–320. yellow spot of pineapples. Phytopathology Beardsley, J.W. (1959) On the taxonomy of pine- 29(3), 285–286. apple mealybugs in Hawaii, with a description Carter, W. (1945) Some etiological aspects of mealy- of a previously unnamed species (Homoptera : bug wilt. Phytopathology 35(5), 305–315. Pseudococcidae). Proceedings, Hawaiian Ento- Carter, W. (1949) Insect notes from South America mological Society 17(1), 29–37. with special reference to Pseudococcus brevipes Beardsley, J.W. (1964) Notes on the pineapple and mealybug wilt. Journal of Economic mealybug complex, with description of two Entomology 42, 761–766. new species (Homoptera : Pseudococcidae). Carter, W. (1954) The insect and the plant diseases. Proceedings, Hawaiian Entomological Society Journal of Economic Entomology 47, 210- 215. 19(1), 55–68. Carter, W. (1963) Mealybug wilt of pineapple: Beardsley, J.W., Su, T.H., McEwen, F.L. and Gerling, a reappraisal. Annals of the New York Academy D. (1982) Field investigations on the inter- of Sciences 105, 741–764. relationships of the big-headed ant, the Carter, W. (1967) The scale insects. In: Insects and gray pineapple mealybug, and the pineapple Related Pests of Pineapple in Hawaii. Manual of the mealybug wilt disease in Hawaii. Proceedings of Pineapple Research Institute of Hawaii, pp. 53–56. the Hawaiian Entomological Society 24, 51–67. Caswell, E.P. and Apt, W.J. (1989) Pineapple Bedford, E.C.G., Bruwer, I.J., de Villiers, E.A. and nematode research in Hawaii: past, present Petty, G.J. (1987) Hard (armoured) scales. and future. Journal of Nematology 21, 147–157. In: Myburgh, A.C. (ed.) Crop Pests in Southern Caswell, E.P., Sarah, J.-L. and Apt, W.J. (1990) Africa, Vol. 2, Citrus and Other Subtropicals . Nematode parasites of pineapple. In: Luc, M.,

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7 Pollinators and Pests of Annona Species

J.E. Peña,1 H. Nadel,2 M. Barbosa-Pereira3 and D. Smith4 1Tropical Research and Education Center, University of Florida, University of Florida 18905 SW 280 Street, Homestead, FL 33031, USA; 2International Centre for Insect Physiology and Ecology (ICIPE), PO Box 30772, Nairobi, Kenya; 3Department of Entomology, ESALQ-USP, Piracicaba, São Paulo, Brazil; 4Department of Primary Industries, Maroochy Horticultural Research Station, Nambour, Queensland 4560, Australia

Importance of the Crop, Classification easily distinguished from the other groups by and Ecology its elongated flowers and triquetrous buds. The inner petals of Attae may be absent or The most primitive angiosperm order Mag- minute. The most well-known species within noliales consists of ten families and almost this section are A. cherimola P. Miller, A. 3000 species. The highly diversified family squamosa L., A. reticulata, L., and A. longiflora Annonaceae includes about 2300 species, and Watts. Fruits of Annona are fleshy aggregates therefore makes up roughly three-quarters that arise from coalesced carpels and contain of this order. The genus Annona embraces large seeds with reticulate endosperm. several valuable fruit trees and is centred in Most species of Annona have specific the Neotropics, with about 110 species there climatic requirements for growth, flowering, and only three representatives in the Old and fruit maturation. The origins of the World: Annona senegalensis Persoon and A. tropical species such as the sugar apple stenophylla Engler et Diels are widespread in (A. squamosa) are the warm lowland regions of Africa, but do not occur in America, whereas Brazil, Guiana, Venezuela, Mexico, and the A. glabra L. occurs in both (Safford, 1914; West Indies. A distinctly subtropical species is Kessler, 1987). The genus is divided into sec- the cherimoya (A. cherimola), which originates tions, including the [Eu-Annona] Guanabani from the cool Andean valleys of Peru and (soursops), Pilaeflorae (silky annonas), Acuti- Ecuador at elevations of around 2000 m. The florae (custard apples), [Atta] Attae (custard hybrid atemoya (A. cherimola × A. squamosa) apples), and Annonellae (dwarf annonas). that appeared spontaneously when parent Among these sections two are horticulturally trees were cultivated side by side, and can be important, the Guanabani and Attae. The produced through manual cross-pollination, Guanabani is characterized by a subglobose, exhibits intermediate climatic requirements pyramidal flower and broadly imbricate for growth and fruiting. inner petals. The most well-known species Within the family Annonaceae, fruits within this section are A. muricata L., A. of the cherimoya, sugar apple, atemoya, and montana McFadden, A. glabra L., A. salzmannii soursop (A. muricata) have the greatest poten- A. DC, A. purpurea Sesse et Mocino, and tial for utilization and export in the American, A. senegalensis Persoon. The Attae section is Caribbean, Asian and Australian countries.

©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 197

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Much of the production of commercially pollinators and only two to three are key grown species has spread from their pests that cause significant crop damage in indigenous areas to tropical and subtropical various production systems. parts of Australia, New Zealand, Asia and around the Mediterranean. Thus, production methods vary from more sophisticated Pollinators and Pollination systems to less intensive, small farm or backyard type production. For instance, soursop Until the mid-1980s natural pollination was yields in Hawaii can reach 83 kg per tree. investigated in no more than 20 to 30 species At Paramaribo, Surinam, soursop yields of of Annonaceae (Gottsberger, 1985), but the 54 kg per tree are achieved at 278 trees ha−1 number of new studies keeps rising (e.g. (Nakasone and Paull, 1998). Andrade, 1996; Nagamitsu and Inoue, 1997; Most research on control of Annona Webber and Gottsberger, 1997; Momose et al., pest arthropods stemmed from generalized 1998). Inadequate pollination is implicated practices already in use on other tropical fruit as a major factor limiting production of crops, i.e. intensive application of chemical commercial Annona fruits in many locations control measures without knowledge of pest (Gazit et al., 1982). This is attributed, in biology or susceptibility, or alternative control part, to the temporal separation of female methods. The major constraints to high pro- and male function within the flower, which ductivity of these crops are not only attack by limits its potential to self-pollinate without key pests, but often the lack of pollinating external factors. The commonest problem is agents. Crop losses due to key pests range lack of pollinators. This is a direct result of the from 40 to 90% in heavily infested areas. expansion of plantations into regions outside Natural fruit set in the absence of pollinating the native range of the plants and their agents is lower than 5% of flowers. Survey and pollinators, and may be due even to the manipulation of pollinating agents as well unnatural conditions imposed by cultivation, as basic studies on the biology and methods regardless of locality. of controlling the pests are prerequisites The majority of Annonaceae are pollinated for successful management of these crops. by beetles, although some are pollinated by The purpose of this chapter is to elucidate thrips (e.g. Momose et al., 1998), true bugs current knowledge of pollinators and their (Farre et al., 1997), and even cockroaches relationship to fruit set, and to assess studies (Nagamitsu and Inoue, 1997). Pollination by on key pests of Annona crops, including their flies may also occur, though evidence for dynamics, behaviour, and management this is scanty (Gottsberger, 1970). The flowers systems. range from showy to drab, often attracting their pollinators through strong odours. Some species have thermogenic flowers that attain a Arthropod Fauna temperature higher than that of surrounding air, presumably to intensify volatilization Annonas throughout the world host a broad of the odoriferous chemicals in the petals variety of arthropods. Surveys of arthropods (Gottsberger, 1970). Annonaceous flowers associated with these plants reveal that the produce no nectar, but rewards for pollinators number of species found in the Neotropics include fleshy edible petals (Gottsberger, ranges from a dozen to a few hundred 1988), fleshy sterile tissue at the tips of the (Ebeling, 1959; Venturi, 1966; D’Araujo et al., stamens (Nadel and Peña, 1994), pollen 1968; Alata, 1973; Marin, 1973; Gutierrez and (Gottsberger, 1988; Deroin, 1989), and stigmal Trochez, 1977; Peña et al., 1984; Bennett and exudates (Vithanage, 1984; Gottsberger, 1988). Alam, 1985; Anonymous, 1989; Medina-Gaud The flowers are used as mating sites by some et al., 1989; Peña et al., 1990; Coto et al., 1995; pollinators (Webber, 1981; Gottsberger, 1988; Peña and Bennett, 1995). The vast majority Deroin, 1989). The activities of beetles in the of these insects are also pests of other well flowers, including feeding, mating, and quies- established crops, while some are beneficial cence, result in prolonged visits of several

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hours to a few days while the flowers advance in Mexico, from March to July (Castaneda from the female to the male phase. et al., 1997). Annonaceous flowers are protogynously dichogamous, opening as females with receptive stigmas and closed anthers, and later losing stigmal receptivity as the flowers Pollination of Commercial Annonas turn into pollen-shedding males (Gottsberger, 1970). This evolutionary adaptation prevents Natural pollination of commercial Annona deposition of pollen on to the stigmas in the species was shrouded in mystery for decades. same flower, and is one of many techniques Through a lack of easily observed alterna- that plants employ to avoid self-fertilization. tives, it was assumed to occur through the Prevention of the transfer of pollen between action of wind, honeybees, or pollen falling different flowers on the same plant is another on to the stigmas. In the early 1900s, Wester technique used by many Annonaceae, and is (1910) suggested that the small beetles he achieved through synchronization of flower- occasionally found in sugar apple flowers ing, where, at any time, open flowers on one might be the pollinating agents, but his sug- plant are functionally of only one sex. These gestion went unheeded for the next 60 years. temporal floral traits, commonly enhanced Ahmed (1936a,b) recognized the entomophil- with inherent incompatibility between pollen ous nature of sugar apple flowers, but did not and ovule from the same plant, render most elaborate. Gottsberger’s (1970) interest in annonaceous species unable to self-pollinate. the evolution of floral traits led him to the The flowering season of commercial Neotropics where he clinched the role of bee- annonas appears to be highly variable but tles in the pollination of wild Annona species. is usually concentrated around the warmer Reiss (1971) was the first to document polli- months of the year. The season for sugar nation by nitidulid beetles, to the exclusion apples and atemoyas lasts for 3–5 months. In of other factors, in cultivated atemoyas and Florida, USA, flowering of atemoyas begins in cherimoyas, and Villalta (1988) documented April, and sugar apples in May, and continues scarab beetle pollination of soursop. Today, until early August (Nadel and Peña, 1991b). natural pollination of Annona is believed to Likewise, in northeastern India and New be largely restricted to the action of beetles, Delhi, sugar apples flower approximately though some ‘self-fertility’ is mentioned in from March through August, with a peak in much of the literature and awaits elucidation. May (Kumar et al., 1977). In Israel, atemoyas Pollination of the larger-flowered Guana- and sugar apples flower from June to bani [Eu- Annona] section is effected mainly by September (Oppenheimer, 1947; Podoler et al., scarab beetles (Scarabaeidae), and the smaller- 1985), whereas in Egypt they flower from flowered Attae section by a variety of smaller May to July (Ahmed 1936a; Rokba et al., 1977). beetles, mainly sap beetles (Nitidulidae), Atemoyas flower from November to the end weevils (Curculionidae), cucujids (Cucujidae), of January in Queensland, Australia (George rove beetles (Staphylinidae), and anthicids et al., 1992). (Anthicidae). The role of beetles as pollinators Cherimoya flowering periods are often was determined through field observations of shorter. In New Zealand, cherimoyas flower insects that contact the floral sexual organs for only 2–9 weeks, during late December and carry pollen, and through examination of through February, with one cultivar reported fruit set following exclusion or confinement to produce a second small flush at the end of of potential pollinators with the flowers. The March (Hopping, 1983). In Chile, peak bloom story that emerged from areas as widely occurs in January and February (Lopez and divergent as South America, Australia, Israel, Rojas Dent, 1992; Saavedra, 1977). In India, and the USA revealed that the small- they are reported to flower in August (Thakur chambered Atta flowers share a similar floral and Singh, 1965). However, in California, and pollination biology, and that it is some- USA, bloom lasts usually from May to what different from the large-chambered October (Thomson, 1974), and nearly as long soursop flowers.

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Cherimoya, sugar apple, and atemoya Cohorts of flowers open synchronously on a tree (Gazit et al., 1982; Kahn and Arpaia, The pendulous flowers bear three elongate, 1990; Nadel and Peña, 1994), resulting in open firm, fleshy petals that are closely appressed flowers that are functionally of the same sex at the start of anthesis and gradually spread on any tree. A new cohort opens when the apart as the flower matures. The flowers are petals and stamens of the old cohort drop off, protogynously dichogamous (Ahmed, 1936a; or soon after. Noonan, 1954; Schroeder, 1956; Thakur and These annonas are most often pollinated Singh, 1965; Reiss, 1971), spending about by nitidulid beetles (Table 7.1), which breed 18–25 h in the female phase followed by about and feed in decaying fruits or sap flows. The 12 h in the male phase (Podoler et al., 1984, beetles are attracted to the fruity, fermenting 1985; Nadel and Peña, 1994) (Plate 41). The odour of Annona flowers, especially when flowers of sugar apple are generally reported hungry (Podoler et al., 1985). Some species to open in early morning, but the shedding of occasionally feed in flowers, gnawing tissue at pollen is variously reported to begin either at the tip of stamens or the bases of petals (Nadel any time of day (Ahmed 1936a; Kumar et al., and Peña, 1994), or feed on pollen grains 1977), or usually in the afternoon (Wester, (Podoler et al., 1985), and possibly on stigmal 1910), or around midnight (Nadel and Peña, exudates (Vithanage, 1984). Mating is not 1994). Atemoyas open in mid-to late after - known to occur inside the flowers. The beetles noon, begin shedding pollen around noon of generally enter female phase flowers in the the next day, and drop the stamens and petals morning and remain almost inactive at the around midnight (Nadel and Peña, 1994). The base of the petals against the stamens and time of day that they begin to open may differ stigmas, dispersing several hours later after with climatic conditions (Kumar et al., 1977), the flowers become male and cover them with species, cultivar, or individual. pollen (Nadel and Peña, 1994). Annona pollen

Table 7.1. Pollinators of commercial annonas.

Commodity Region Pollinators Source

Atemoya, Israel Nitidulidae: Carpophilus humeralis, C. hemipterus, Gazit et al., 1982 cherimoya C. mutilatus, Haptoncus luteolus Atemoya Queensland, Nitidulidae: Carpophilus hemipterus George et al., Australia 1989 Atemoya Florida, USA Nitidulidae: Carpophilus fumatus, C. dimidiatus spp. Nagel et al., 1989 cmplx., Haptoncus luteolus, Colopterus posticus Atemoya, Florida, USA Nitidulidae: Carpophilus fumatus, C. hemipterus, Nadel and Peña, sugar apple C. humeralis, C. marginellus, C. mutilatus, 1994 Colopterus posticus, C. truncatus spp. complex, Haptoncus luteolus Cherimoya Quillota, Chile Nitidulidae: Carpophilus hemipterus, Colopterus sp. Lopez and Rojas, 1992 Nitidulidae: C. hemipterus Lopez and Uquillas, 1997 Cherimoya Mexico and Cucujidae: Cryptolestes ferrugineus, Silvanus Castañeda et al., Michoacan planatus. 1997 States, Mexico Nitidulidae: Conotelus sp. Staphylinidae: Phloenomus sp. Cherimoya California, USA Staphylinidae: Eusphalerum sp. Kahn, 1997 Cherimoya Spain Anthocoridaea: Orius sp. Farre et al., 1997 Soursop Costa Rica Scarabaeidae: Cyclocephala amazona, C. brittoni, Villalta, 1988 C. stictica

aOrder Hemiptera; all other pollinators are in the order Coleoptera.

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is sticky and remains viable for at least 24 h nine species of native and exotic nitidulids (Reiss, 1971), sufficiently long for movement visit the flowers (Plate 42), but C. mutilatus between old and new cohorts of flowers. is the most important pollinator in terms of The number of beetles per flower affects efficacy and abundance in flowers, followed the likelihood of fruit set (Fig. 7.1), and also the by C. fumatus and H. luteolus. Although quality of the fruit in some cases. All studies C. humeralis is very abundant in the annona provide evidence for increased fruit set as grove environment, it rarely visits the flowers. numbers of visiting beetles increase (Gazit When it does visit, it induces a very low rate of et al., 1982; George et al., 1989, 1992; Nadel and fruit set, in contrast with its behaviour in Israel Peña, 1994; Lopez and Uquillas, 1997). Fruit (Nadel and Peña, 1994). The number of species symmetry is poor when only 1–3 beetles visit a visiting flowers in Ecuador, Colombia and flower, but is good when at least four beetles the Caribbean region is similar to that found visit (Gazit et al., 1982). However, fruit sym- in Florida (Peña and Bennett, 1995). In other metry is sometimes unaffected by the number regions the guilds are smaller, and in some of pollinators per flower (George et al., 1989; cases inadequate for commercial fruit produc- Lopez and Uquillas, 1997). It must be noted, tion without the aid of manual pollination. though, that in these studies the number per Because of the dichogamous nature of flower was generally lower (two) than the the flower, the stigmas cannot receive pollen threshold for good symmetry found by Gazit from the same flower under most conditions. et al. (1982). Most workers report that the stigmas glisten The guilds of pollinating beetles in com- with moisture when receptive, but turn dry mercial Annona species vary geographically, before the stamens split open. However, if and species may even perform differently humidity is high or temperature moderate, in each area. The four major pollinators in the stigmas are thought to remain moist and Israel, Carpophilus humeralis, C. hemipterus, C. receptive until the pollen is released, allowing mutilatus, and Haptoncus luteolus, are equally a small proportion of self-pollination to effective as pollinators. In Florida, USA, about occur without the aid of insects (George et al.,

Fig. 7.1. Percentage fruit set as a function of the number of nitidulid beetles per flower. Number of inspected flowers are written above each bar. (Source: Nadel and Peña, 1994.)

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1989). Previous workers have noted that occurs in synchrony among flowers on a tree Annona trees growing near bodies of water or and also with other trees. in especially humid climates set higher levels The petals are stiff and leathery and of fruit than those in drier climates (Schroeder, the inner ones form a large space around 1943; Sarasola, 1960; Thakur and Singh, 1965; the sexual organs that is referred to as the Thomson, 1970). Cultivations in relatively dry pollination chamber. In the soursop this is areas have low natural fruit set (Thakur very different from the tight space provided and Singh, 1965; Gazit et al., 1982); and in for small beetle pollinators in the section the dry areas of southern California annonas Atta of Annona. Dynastine scarab beetles must be manually pollinated to obtain such as Cyclocephala are the most important commercial yields (Schroeder, 1943, 1956). pollinators of annonas with large pollination However, many of these observations were chambers, and are generally attracted by made before convincing evidence was pre- nocturnal scents (Gottsberger, 1985, 1988). sented for insect pollination in annonas, and In addition to the Cyclocephala species that the studies were made outside the native pollinate soursop, Cyclocephala quatuordecim- range of the plants and their pollinators. It is punctata and other scarab beetles are consid- likely that climatic factors such as humidity ered likely pollinators for the Guanabani group benefit pollinator populations and that natu- (Gottsberger, 1991). Vidal (1997) reports that ral fruit set in these areas is at least partly due the main insects found in A. muricata flowers to their activities. in Mexico are Nitidulidae and Chrysomeli- dae, while species of Apidae and Formicidae (Hymenoptera) are abundant on the external Soursop surfaces of the flowers where contact cannot occur with the flowers’ sexual structures. Villalta (1988) reported between 18% and Villalta (1988) described the floral morphol- 24% natural fruit set of soursop in Costa Rica. ogy, phenology and pollination of A. muricata Some authors believe that entomophilous pol- in Costa Rica (Plate 43). The flowers spend lination of A. muricata has lower potential than about 3 days in the female phase when manual pollination in commercial production the outer petals spread apart slightly and (Cogez and Lyannaz, 1996). a copious viscous exudate appears on the surface of the stigmas. It ends when the tips of the stigmas are shed in the form of a cap-like structure. The ensuing male phase Pollinator Management begins at about 0830 h and lasts about 12 h until the stamens and petals fall off. During Trials to increase fruit set in atemoya anthesis the three outer petals spread apart orchards by augmenting nitidulid popula- slightly, but the inner three petals remain tions have yielded mixed results. In Israel, closed. The flowers attract the beetles one one-time additions of decaying apples as day before the male phase at about 1800 to an attractant failed to increase the number 2200 h, when they emit a strong odour. Pollen of beetles in the flowers or fruit set (Galon is transported by Cyclocephala beetles (Scara- et al., 1982). Release of 10,000 nitidulids (70% baeidae) on the hairs of the legs and body C. hemipterus and 30% C. mutilatus) in a grove (Plate 44). The beetles remain in the flowers also failed to show any increase in these for 24 h and leave after the pollen is shed. parameters. Galon et al. (1982) suggested that They feed on pollen and on the bases of the decaying fruit baits compete with the flowers. petals, and engage in mating. They do not They found that flowering branches enclosed feed on the stigmal exudate, which may in mesh bags supplied with nitidulids and contain toxins that protect the stigmas from decaying apples had only half the percentage chewing beetles. Anthesis begins at any time of fruit set compared with bags supplied with of the day or night, but most often between beetles but no fruit (15% and 29%, respec- 1100 and 1500 h; anther dehiscence, however, tively). In Australia, success was achieved by

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adding pineapples in an atemoya orchard Other species are considered secondary throughout the flowering season. This and localized. In Asia, the western Pacific resulted in more beetles in the flowers and and Australasia, the main pests in Annona are 62% higher fruit set compared with an orchard 2–3 species each of mealybugs, coreid fruit- not provided with fruit (George et al., 1992). spotting bugs, Bactrocera fruit flies, pyralid Nitidulid pollination in Annonaceae can fruit-boring moths, and soft scales (De also be improved by using chemical lures Leon and German, 1917; Estalilla, 1921; (Bartelt et al., 1992; 1994). The effect of Paguirigan, 1951; Galang, 1955; Vinas, 1972; nitidulid-pheromone bait stations on sugar Gabriel, 1975; Cantillang, 1976; Brun and apple and atemoya fruit set was determined in Chazeau, 1980; Coronel, 1983; George and southern Florida. Maximum percentage fruit Nissen, 1991; Koesriharti 1991; Smith 1991a,b; set fluctuated between 10% and 38% during Khoo et al., 1991; Waterhouse, 1993). the first 4 weeks after treatment in plots with bait stations, and was significantly higher than in the control plots (Peña et al., 1999). Key Pests To the best of our knowledge, no management techniques have been reported The Annona seed borers, for soursop pollinators. Bephratelloides species

Chalcidoid wasps are best known as parasites Pests of other insects. However, many species in the families Torymidae, Eurytomidae, and In the Neotropics 296 species of arthropods all Agaonidae and Tanaostigmatidae have are recorded as associated with Annona spe- evolved the ability to induce galls or feed on cies. The families most frequently observed plant seeds. Phytophagous eurytomids are on Annona species are Coccidae (Homoptera), considered by some to be the most primitive Noctuidae, Oecophoridae (Lepidoptera), and in the superfamily Chalcidoidea. The Eurytomidae (Hymenoptera). The most com- Neotropical genus Bephratelloides has species mon species in various Neotropical countries known to develop strictly in Annona seeds: are Bephratelloides cubensis (Ashmead), B. B. pomorum, B. cubensis, B. paraguayensis pomorum (F.) (Hymenoptera: Eurytomidae), (Crawford), and B. petiolatus Grissell and Cerconota anonella Sepp. (Lepidoptera: Oeco- Schauff (Grissell and Schauff, 1990); B. ablusus phoridae), Parasaissetia nigra (Neitner), Grissel and Foster develops in seeds of the Saisssetia coeffeae (Walter), S. oleae (Olivier) wild Cymbopetalum, a close relative of Annona (Homoptera: Pseudococcidae), and Cocytius in southern Mexico (Grissell and Foster, 1996). antaeus (Cramer) (Lepidoptera: Sphingidae). Bephratelloides species that attack Annona The first three species are considered key species commonly occur in damaging pests of Annona. They are multivoltine, numbers in South and Central America, stenophagous feeders of Annona seeds and the Caribbean and southern Florida (Dozier, fruits. B. cubensis has been reported from the 1932; Brunner and Acuña, 1967; Brussel USA, Caribbean, Central America and South and Weidijik, 1975; Peña et al., 1984; Mendes America, whereas B. pomorum is listed from and Pereira, 1997). Hosts recorded for Annona Central and South America. Their biology, seed borers include A. muricata, A. squamosa, behaviour and habits are quite similar, except A. squamosa × A. cherimola, A. cherimola, A. that B. cubensis is uniparental. The seasonality reticulata, A. montana and A. glabra (Nadel and of B. cubensis on various hosts in a given Peña, 1991a). Economic damage occurs when area can be attributed to the relative fruiting the adults chew their way out of the fruit, cre- phenologies of the available Annona species ating a 2 mm diameter tunnel that provides (Nadel and Peña, 1991b). Cerconota anonella entry for other insects and decay organisms. has been reported from tropical America The biology of B. cubensis was studied on and the Caribbean (Peña and Bennett, 1995). A. reticulata in Cuba by Brunner and Acuña

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(1967). They concluded that B. cubensis is In the atemoya host, B. cubensis prefers to thelytokous, reproducing without males. It oviposit in fruits ranging from 1.5 to 5.5 cm in has approximately 4–5 generations year−1. The diameter, which corresponds to fruit ages of egg stage lasts 12–14 days, the larval stage 6–8 3–7 weeks after bloom (Fig. 7.2). This size weeks, the pupal stage 12–18 days, and the range was confirmed by Evangelista-Lozano adult rarely lives beyond 15 days (Plate 45). et al. (1997). Although fruits larger than 5.5 cm One egg is laid per young seed and the larva are probed, usually when B. cubensis popula- feeds and pupates within it. Evangelista- tions are high, most of these attacks do not Lozano et al. (1997) determined that B. cubensis result in infestation. Preferred fruit sizes pre- has five instars and the average generation sumably correspond with seeds that have not time is 62 days. Anjos and Pereira (1997) yet hardened and are easy to penetrate with reported the same number of instars for B. the ovipositor, while the seeds of older fruits pomorum on A. muricata. Pereira et al. (1997a) are probably too hard to penetrate. Larger determined that the generation time of B. fruits may be less preferred also because the pomorum lasts from 43 to 113 days. Sex of distance from the fruit surface to the seed B. pomorum can be distinguished in the pupal may exceed the length of the ovipositor. The stage by the length of the antennae, which in probes in young sugar apple and atemoya males extend posteriorly beyond the tips of fruits look like dark pinpricks surrounded by the wings, and by the elongated segments of a round whitish patch, and are visible for the prothoracic tarsi. In the female the anten- about 2 weeks; in older fruits the whitish patch nae do not extend to the tips of the wings and does not appear, and the probe marks are the prothoracic tarsi have rounded segments. permanent and often ooze sap. Pereira et al. (1998) observed that adult females Oviposition activity by B. cubensis in of B. pomorum live up to 10 days, while males Florida begins at about 0900 h and continues live for only 2 days. Pereira et al. (1998) and throughout the daylight hours with peaks in Leal et al. (1997) have observed an attraction activity around 1200–1300 h (H. Nadel and by B. pomorum males to caged virgin females J.E. Peña, unpublished). The wasps appear to and have suggested the possible presence of a spend the night on the underside of leaves on female pheromone. their host trees, and move to the upper surface

Fig. 7.2. Growth curve for atemoya var. ‘Gefner’ and fruit size preferred for oviposition by Bephratelloides cubensis. Vertical bars represent standard error of the mean. (Source: H. Nadel and J.E. Peña, unpublished.)

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at sunrise. Flying individuals can be observed (A. reticulata). In Florida, A. reticulata sets fruit soon afterwards and throughout the day. The in September–November, and fruits remain females probe fruits repeatedly with the on the trees as late as May. Atemoyas set fruit ovipositor, each probe lasting up to about from April to August, and sugar apples from 300 s, but not all result in oviposition. Probes May to August (Nadel and Peña, 1991a). Nadel lasting between 100 and 200 s are most likely and Peña (1991b) concluded that B. cubensis to result in oviposition (corroborated by seed populations in Florida overwinter mainly in dissection) (J. Fortier, H. Nadel and J.E. Peña, A. reticulata and then move to atemoyas that unpublished). begin to set fruit during April. After a develop- Pereira et al. (1997b,c) reported that the mental time of 9 weeks, the adults emerge female of B. pomorum initially walks on the from the early atemoyas and proceed to infest fruit, using the antennae to locate an oviposit- younger atemoya and available sugar apple ion site. However, the purpose of antennation fruits. A second and third peak of adult emer- of oviposition sites by chalcidoids is often to gence and infestation occur in atemoya and detect odours of conspecific competitors, and sugar apples until young fruits are no longer is also likely to play such a role in this pest available and the wasps switch to A. reticulata genus. fruits in September. Wasp populations Leal et al. (1997) reported that males of increase throughout the warm months in B. pomorum are strongly attracted to female- Florida because of the availability of large baited traps, showing a peak of activity at concentrations of atemoya trees, and are noon. Lima et al. (1997) determined that males bottlenecked in winter because A. reticulata is are attracted to fruit odours while they search grown only sporadically as a garden tree. Low for emerging females. Males are able to locate infestations in sugar apples may be due to the region of the fruit where adults will a lack of incentive for the pests to disperse emerge and regularly try to copulate with from plentiful atemoya orchards to other newly emerged adults of either sex. Females areas. No evidence of diapause was found in can copulate more than once. mummified stemoya and sugar apple fruits The response of Bephratelloides to various overwintering on trees or on the ground. Annona fruit volatiles has not been investi- Peña et al. (1984) observed that peaks of gated extensively. McLeod and Pieris (1981) activity of adult B. cubensis are observed at and Idstein et al. (1984) discovered several 1500 h when the average temperature fluctu- volatiles characteristic of ripe Annona fruits. ates around 31–33°C. While testing the possib- Among these, methyl hexanoate is signifi- ility of visual monitoring to assess population cantly attractive to B. cubensis but other levels of this pest, H. Nadel and J.E. Peña mixtures of Annona compounds such as 3 : 1 (unpublished) observed that 50% of adult seed hexanoic acid: octanoid acid, or a 2 : 1 : 1 borers were concentrated in the middle third mixture of isoamyl alcohol : butanol : linalool of the tree’s height, on both leaves and fruits. are not attractive. The positive response to Of these, 67% were concentrated in the outer the first compound was obtained in an olfacto- half of the tree canopy. Peaks in wasp numbers meter but could not be replicated under field on the trees occurred between 1100 and 1700 h, conditions (Peña, 1988). and numbers were highest during the warmer part of the summer. Flight was observed MONITORING AND SAMPLING Nadel and Peña mostly before 1000 h and after 1600 h. (1991b) monitored the weekly infestation rates of B. cubensis in commercially grown YIELD LOSSES Injury is caused by the emerg- sugar apples and atemoyas in Florida. They ing adult as it bores through the seed and fruit reported that infestation increased through- pulp (Plate 46). A circular hole is created on out the summer in atemoyas but remained the surface that facilitates entry of micro- very low in sugar apples. The observed pat- organisms and other insects, and causes a sig- terns were attributable to the relative fruiting nificant necrosis (Korytowski and Peña, 1966; phenologies of the commercial species and Nadel and Peña, 1991; Pereira, 1996). Yield of the overwintering host, the bullock’s heart loss due to attack of B. pomorum in soursop

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ranges from 41% to 80% (Reyes, 1967; In some countries, burying infested fruits Escandon et al., 1982; Zarate 1987). is advised as the best method to keep the infestation at low levels. Zarate (1987) recommends CONTROL TACTICS Chemical control is collecting all infested fruit in the orchard, widely used, but is seemingly inefficient in placing them in a 60 cm deep hole and cover- some areas (Zarate, 1987). Zarate (1987) rec- ing the fruit with CaCO3 and aldrin (!) 2.5%. ommends the use of organophosphates and At present, the decision to take action for the carbamates but does not report the results seed borer depends on a combination of: (i) of their application. He also recommends the presence of significant numbers of vulnerable use of organophosphates mixed with sugar or fruits that are 1.5–5 cm in diameter; and (ii) molasses as attractant. Peña and Nagel (1988) visual monitoring to determine the presence found that the use of malathion plus molasses, of the adult seed borer in the orchard. fenvalerate, or permethrin provided signifi- It is also prudent to remove (or avoid cant adult mortality of the seed borer; how- planting) unpreferred Annona species from ever, counts of infested fruits remained high areas of commercial production if those spe- after treatment. The authors suggested that cies allow the wasps to overwinter. Removal the poor performance of the insecticides was of the winter-fruiting A. reticulata from south- due to insufficient knowledge of pest dynam- ern Florida would probably reduce damage ics, emergence peaks and pesticide timing. by B. cubensis to below economic levels (Nadel Ramnanan (1996) reported that malathion and Peña, 1991b). provided significant damage reduction by B. pomorum on soursop. Chemical interven- BIOLOGICAL CONTROL No significant native tions are made in some countries using full- parasitization or predation of Bephratelloides coverage airblast sprayers, generally at rates species has been reported. When wasp exit of 1000 and 2000 l ha−1, or they are done by holes are observed in the fruit, ants will invade backpack sprayers, where coverage is erratic. the tunnels, but their effect on the insects Fruit bagging is considered by several remaining in the seeds is unknown. In Florida, researchers (Villalobos, 1987; Zarate, 1987) the fungus Beauveria bassiana was collected to be one of the best methods to prevent from a B. cubensis adult still inside the seed B. cubensis infestation. Ramnanan (1996) (J.E. Peña, unpublished). To our knowledge recommends sleeving or bagging fruits when this is the only biological control agent the fruit is 5–10 cm in diameter. H. Nadel and identified from B. cubensis. The fungus was J.E. Peña (unpublished) found no infestation applied to B. cubensis adults under laboratory in fruits bagged before they reached 2 cm conditions and provided 90% adult mortality in diameter, compared with unbagged fruits up to 8 days after treatment. under the following conditions: 39% infested in an unsprayed atemoya orchard, 16% in PLANT RESISTANCE Martinez and Cabrera a chemically treated atemoya orchard, and (1997) reported a higher incidence of B. 11% in an unsprayed sugar apple orchard. cubensis in some soursop cultivars IV-10, In another study (H. Nadel and J.E. Peña, VII-14 and 1V-16 compared with infestation unpublished), atemoya fruits bagged with registered in the cultivar IV-16 in Puerto Rico. chlorpyrifos-treated and plain polyethylene Selection for trees with good quality seedless bags also remained free of infestation, com- fruits would provide completely effective pared with 8% of infested controls. Bagged control against Bephratelloides. Parthenocarpy fruits were also cleaner and aesthetically can be artificially induced on normal trees by better than unbagged fruit. However, bagging plant hormones (Campbell, 1979). Campbell encourages the growth of mealybugs on some (1979) treated female-phase flowers and then fruits, probably because natural enemies are the fruits repeatedly with a spray of gibberel- excluded. Although the method is effective, lins (1000 p.p.m.), and found good fruit set a cost comparison must be made between and production of parthenocarpic, seedless bagging and other potential control methods fruits that were, however, smaller than seeded to determine its economic feasibility. fruits and of poorer flavour.

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Lepidopterous annona fruit borers larger with larval maturation, and webbing forms across it like a screen, which becomes The annona fruit borers, Cerconota anonella covered with faecal pellets and particles of (Oecophoridae), Talponia batesi Heinrich fruit. The characteristic symptom of the attack (Tortricidae) and Thecla ortyginus (Lycanei- of C. anonella is the excrement eliminated by dae), are second in importance as key pests the larvae, and the necrosis caused by oppor- of Annona. Cerconota anonella is recorded in tunistic fungi that enter the fruit through South America, Central America and the the injury (Fennah, 1937a) (Plate 48). Damage Caribbean. (Fennah, 1937a; Zenner and to flowers is observed during spring. Yield Saldarriaga, 1969; Lawrence, 1974; Gutierrez losses caused by this pest fluctuate between and Trochez, 1977; Martinez and Godoy, 70% and 100% (Martinez and Godoy, 1983; 1983). The larvae damage the fruit epidermis, Calzavara and Muller, 1987; Ruiz, 1991). pulp and seeds of soursop and cherimoya Preliminary observations show that C. during feeding (Fennah, 1937a). In Brazil, anonella males are attracted to virgin females yield losses can be as high as 70%. Talponia placed in cardboard traps; male capture was batesi is distributed in the Caribbean, observed in 45% of the traps tested (Bustillo Venezuela, Colombia, Brazil and Mexico and Peña, 1992). The same authors observed (Castañeda and Pineda, 1997). Thecla spp. are that adults were attracted to black-light traps, reported from Mexico, the Caribbean region, which could be useful in monitoring popula- Central and South America (Fennah, 1937a). tions of C. anonella.

Annona fruit borer, Cerconota anonella MONITORING Junqueira et al. (1996) recommend placing black light traps (1 trap ha−1) The life cycle of C. anonella, as investigated by and starting treatment as soon as one moth is Bustillo and Peña (1992), averages 36.4 days. captured per trap. Bustillo and Peña (1992) The adult moth is uniformly of a pale straw suggest using virgin females placed in small colour, with one spot on the upper surface of cages as bait in Delta traps, approximately the forewing, halfway between the fore- and 1.5 m above the ground. Duarte (1947) hindwing margins at approximately the dis- suggests inspecting the orchard at the onset tal two-thirds of the wing (Fennah, 1937a) of blooming and collecting infested fruits in (Plate 47). The female is approximately 1 cm screen cages that restrain the moths but allow long with a 2.5 cm wingspan, while males are the exit of the parasitoids, Brachymeria and 0.8 cm long with a wingspan of 1.8 cm (Nuñez Apanteles. and De la Cruz, 1982). They have nocturnal habits, and deposit eggs not only on unripe BIOLOGICAL CONTROL Biological control of fruits, but also on the inflorescence (Costa C. anonella was studied in Colombia and Ecua- Lima, 1945; Pireira et al., 1991b). Eggs are elon- dor. Sampling for parasites of C. anonella con- gated or ovoid, 0.6 mm in length and 0.25 mm sisted of rearing collections of Annona fruits. in diameter. They are pale green to translu- Two braconid species, an Apanteles sp., and a cent in colour, and bear parallel and trans- species in an unknown genus of the subfamily verse ridges (Fennah, 1937a; Nuñez and de la Rogadinae, were identified as natural enemies Cruz, 1982). After hatching, the neonate larva of C. anonella in Colombia and Ecuador. Para- is off- white in colour, which changes to red- sitism by Apanteles sp., however, was very dish purple during later instars. The insect low, ranging around 2–5% in Colombia and undergoes five instars, and the larval stage 2% in Ecuador (J.E. Peña, unpublished). The lasts 18.6 days at room temperature (21°C). observations were in contrast to high para- Newly hatched C. anonella larvae make small sitism levels from other braconids (Apanteles traces all over the fruit surface, and penetrate spp.) and an ichneumonid, Xiphosomella sp., the fruit on the fourth day after eclosion (Ruiz, reported from Venezuela by Martinez and 1991). While feeding, the larvae periodically Godoy (1983). The pupae are parasitized clear their tunnel by pushing excreta towards by the chalcid, Brachymeria pseudovata (Costa the entrance. The orifice of the tunnel grows Lima, 1948; Ruiz, 1991; Pireira et al., 1991a).

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CHEMICAL AND CULTURAL CONTROL The effect of malathion when the fruit is small is of various types of protective bags and insecti- recommended in Colombia (Saldarriaga et al., cides was tested in 3–5-year-old A. muricata 1987). trees. Bagging and use of bags treated with chlorpyrifos resulted in less damaged fruit Talponia batesi compared with the control (Bustillo and Peña, 1992). Pesticide-treated bags also reduce infes- Castañeda and Pineda (1997) determined that tation by B. cubensis in Costa Rica (Villalobos, T. batesi prefers fruit of 1.3 to 8.1 cm diameter, 1987) and may therefore give an adequate con- but it can also cause flower injury. The larval trol of both insect species. Ramnanan (1996) stage of T. batesi lasts 91 days, while the pupal suggests that permethrins and cipermethrins and adult stages last 15 and 10 days, respec- provide good control of the damage due to tively. In Mexico, infestations of T. batesi peak C. anonella. In Brazil, Junqueira et al. (1996) during the summer, but injury to fruit from recommend spraying the small fruits with larval feeding is more noticeable during fenthion, monocrotophos or endosulfan every autumn. 15 days. Yellow peach moth Conogethes punctiferalis Thecla ortygnus Yellow peach moth, Conogethes punctiferalis This borer is established in Guatemala, (Gueneé) (Pyralidae), occurs throughout Mexico, Costa Rica, Panama, Trinidad and South-East Asia and in Japan, Indonesia and southern Brazil as a pest of soursop (Fennah, Australia (Smith, 1991a; Smith et al., 1997). It 1937b). The adult butterfly is 12 mm long is an attractive yellow moth with a wingspan with a 36 mm wingspan. The sexes are differ- of 25 mm. In eastern Australia, larvae dam- entiated by the colour of the wings, males age the pulp of mature fruit from February having blue iridescent wings with well- to May, usually with losses of less than 5%, defined dark marginal areas. The wings in but occasionally 50% or higher. The Annona females are smoky blue with black margins. variety Pinks Mammoth is much more Eggs are deposited in the perianth close susceptible than African Pride. to the floral peduncle. Generally, eggs are The scale-like eggs are deposited singly laid singly, but during high infestations, it is on the fruit surface and the young larvae possible to find two eggs per flower. Eggs are burrow through the epidermis into the pulp. hemispherical, 0.9 mm long and 0.5 mm wide Activity is betrayed by brown frass extruded (Fennah, 1937b). The newly eclosed larva is to the fruit surface. After about 3 weeks, the 1.3–1.9 mm long, with a characteristic light last stage larvae pupate in shelters of frass green colour. When eggs are deposited on on the fruit surface. The life cycle takes about flowers, the larva bores through the petals 6 weeks and there are 5–6 generations each and feeds on stamens and stigmas. When an year. This moth infests a wide range of other egg is deposited on a young fruit, the larva fruit hosts such as papaya, citrus and stone- penetrates into the pulp. Fully developed fruit. Field crops like maize and sorghum larvae reach 17 mm in length. The larval stage are also favoured hosts and can be a source has four instars and lasts 12 days; the pupal of infestation to fruit crops. stage lasts 12–14 days (Fennah, 1937b). In Australia, tachinid parasitoids such as Fruit infested by Thecla sp. exhibit irregu- Argyrophylax proclinata Crosskey are impor- lar holes surrounded by a mass of excrement tant, providing up to 40% parasitism. The that the larvae push out from their tunnels adult parasitoid (which is about 8 mm long (Saldarriaga et al., 1987). and similar to a housefly in appearance) attaches its eggs to the host larvae. The fly CONTROL Chemical control should be larva develops within the host, killing the host applied at the begining of flowering. Removal larva at or near the time of pupation. of infested flowers is suggested in Trinidad The assassin bug, Pristhesancus plagipennis (Fennah, 1937b), while removal or application Walker, is a significant predator of the larvae

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in eastern Australia (Smith, 1991a; Smith et al., Irapuá bee 1997). In northern Brazil, the Irapuá bee, Trigona Atis moth borer, Anonaepestis bengalella spinipes F. (Hymenoptera: Apidae), damages leaves, shoots, flowers and young fruits The atis moth borer, Anonaepestis (Hetero- (Bastos, 1985; Gallo et al., 1988). Damage to graphis) bengalella Raq. (Pyralidae), is the most soursop fruits and flowers is characterized by important fruit boring pest in the Philippines rasping on the epidermis. This insect is and is found also in India and Indonesia brown, 5.0–7.5 mm long, and colonies build (De Leon and German, 1917; Estatilla, 1921; nests in trees. Galang, 1955; Gabriel, 1975; Coronel, 1983; Braga et al. (1998) recommend destruction Koesriharti, 1991). Larvae tunnel in the pulp of nests close to soursop groves and weekly of small fruit and extrude frass to the surface. monitoring of flowers and fruits. If damage is Damaged fruit fail to develop and often extreme, chemical control should be applied fall. The mature larva pupates close to the (Braga et al., 1998). Control, however, must surface. be carefully considered, due to the important pollination service the bees perform on Other uncommon Lepidoptera various other flowers in the area.

Phycita semilutea Walker (Pyralidae) has been observed on annonas in Thailand Coreid spotting bugs (Morokote, 1999, personal communication). The orange fruit borer Isotenes miserana The banana spotting bug, Amblypelta lutescens (Walker) (Tortricidae) is an uncommon pest lutescens (Distant), in north Queensland, and in eastern Australia. both A. lutescens and the fruitspotting bug, A. nitida Stal, in southern Queensland and northern New South Wales, are serious pests Fruit flies of custard apple. Adults and nymphs pierce the fruit from In eastern Australia, the Queensland fruit near fruit set until harvest, causing round fly, Bactrocera tyoni (Froggatt), is a significant black spots (up to 1 mm in diameter) and pest of custard apples and soursops, infesting damage about 1 cm deep (Smith, 1991a). maturing fruit from March to May. Eggs are Adult bugs are yellow-green and 15 mm long. laid in batches of about a dozen particularly The eggs are pale green, oval and about 2 mm where the stem joins the fruit (Smith, 1991a). long. The five nymphal instars are ant-like and The thinner-skinned African Pride variety is pinkish with prominent antennae and but- more susceptible than the Pinks Mammoth. ton-like abdominal scent glands. The life cycle Infested fruit can be difficult to detect and lasts about 6 weeks in summer and there are at Cuelure male attractant traps are used to help least three overlapping generations each year. monitor fly populations, while protein baits Infestations are worst in trees adjacent to are applied for control (Smith, 1991a). The eucalypt forests where the bugs breed. There lesser Queensland fruit fly, B. neohumeralis are no significant natural enemies and control Hardy, also occurs in custard apples in is with selective pesticides applied when 2% eastern Australia. In South-East Asia, the or more of fruit show fresh damage (Smith, fruit flies B. dorsalis (Hendel) and B. papayae 1991a). Drew and Howard can infest custard apple and soursop. In Ecuador and Colombia, infestation of cherimoya by Anastrepha spp. Thrips and Ceratitis capitata is characterized by early ripening and drop of fruit (J.E. Peña, personal In eastern Australia, the red-banded thrips, observation; Saldarriaga et al., 1987). Selenothrips rubrocinctus (Giard), and in

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Thailand (Morokote personal communica- Many of these scale species occur on tion, 1999) and India, the orchard thrips, custard apples in New Caledonia (Brun Chaetonaphothrips orchidii (Bagnall), occasion- and Chazeau, 1980). Two lac scales also occur ally cause grey scarring on the fruits. on custard apples in India – Kerria communis (Mahdibassan) and Tachardia labata (Green). Icerya aegyptiaca (Douglas), H. biclavis and Minor Pests Ceroplastes floridensis Comstock are also recorded from India. Several other species of insects and mites may cause minor losses as foliage, trunk, and branch feeders. In the Neotropics, the foliage Armoured scales feeders most frequently reported in Annona are scales, mealybugs, leafhoppers and Armoured scales are also uncommon and whiteflies (Homoptera), lace bugs (Hemip- include Aspidiotus destructor Signoret, Hemi- tera), and some Lepidoptera and mites. berlesia palmae (Cockerell), Pseudaulacaspis Trunk and branch feeders consist mainly of pentagona (Targioni-Tozetti), Chrysomphalum coleopteran stem borers. aonidum (L.), C. dictyospermi (Morgan), Isch- naspis longirostris (Signoret), Howardia biclavis (Comstock), Lindingaspis sp., Aonidiella orien- Foliage Pests talis (Newstead) and Abgrallaspis cyanophyllis (Signoret). Soft scales

About 20 species of soft scales are reported Mealybugs from Annona in the Neotropics (Peña and Bennett, 1995). The scales Parasaissetia nigra, Some species of mealybugs can cause sig- Saissetia coffeae, S. oleae and Philephedra tuber- nificant crop losses, although they seldom culosa Nakahara and Gill, cause damage by approach major pest status. Phillips et al. feeding on sap. Sudden increases in popula- (1987) regard Pseudococcus aonidum (Cockerell) tions of these insects usually coincide with as a minor sporadic pest that, in areas of plant stress and absence of effective natural heavy infestation, may affect the fruit, flow- enemies. ers and leaf growth. Peña and Bennett (1995), In eastern Australia the most common in a review of pests of annonas in the Neo- scale pest of custard apples is P. nigra. It infests tropics, list Dysmicoccus brevipes (Cockerell), the twigs, leaves and fruit, producing copious Ferrisia virgata (Cockerell), Nipaecoccus nipae honeydew and encouraging heavy sooty (Maskell), Planococcus citri (Risso), Pseudo- mould. Infestations are well attended by ants coccus longispinus (Targioni), P. maritimus (Pheidole spp. and Iridomyrmex spp.) and tend (Ehrhorn) and Pseudotectococcus anonae to occur more on young trees up to 2 m high. Hempel. Factors that may contribute to In Australia, the pteromalid parasitoid increases in mealybug populations include Scutellista caerulea (Fonscolombe) normally certain ants that reduce effectiveness of controls P. nigra but is easily disrupted by pes- natural enemies and transport mealybugs ticides or by ants. Larvae of the pyralid moth, from one place to another. Phillips et al. (1987) Catoblemma dubbia (Buttler), are predators. reported that the Argentine ant, Iridomyrmex Other much less common soft scales in humilis displaces other ant species in cheri- eastern Australia are long soft scale, Coccus moya orchards in California and interferes longulus (Douglas), soft brown scale, C. with biological control agents associated hesperidum L., and pink wax scale, Ceroplastes with the long-tailed mealybug Pseudococcus rubens Maskell. In Brazil, the scales S. coffeae aonidum. Most parasites of these mealybugs and Ceroplastes sp., are considered occasional are hymenopterans of the family Encyrtidae pests of Annona (Junqueira et al., 1996). and the most effective predators are

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coccinellid beetles. The judicious use of known to have toxic saliva that stunts and kills several insecticides can result in reduction young shoots. of P. aonidum (Phillips et al. 1987). However, Several factors affect M. hirsutus infesta- the use of some pesticides (e.g. organophos- tions: weather, host, and perennial versus phates) is limited because they are not annual host growth. It prefers weak or young currently registered for use in Annona crops. growth, and the apical portions of plants. The In the Caribbean, a recent introduction of rate of development increases with increasing the pink mealybug, also known as the hibiscus temperatures, but slows with rising relative or grape mealybug, Maconellicoccus hirsutus humidity (Babu and Azam, 1987; Mani and (Green) (previously reported as Pseudococcus Thontadarya, 1988). hibisci Hall or Phenacoccus hirsutus Green), Several insecticides have been tested produced severe damage to soursop during against this mealybug. Beevi et al. (1992) the late 1990s. Its original distribution is in reported that the use of neem oil resulted in the Oriental, Australian, Palaearctic and Ethi- reduction of egg hatching. However, most opian regions (Mani, 1989). It has also been researchers agree that chemical and cultural reported from Pakistan and some islands in control provide relief for only a short period of the Pacific, including Hawaii and Guam time or are ineffective (McComie, 1996). (Beardsley, 1985; Peña, 1998). Maconellicoccus An integrated pest management pro- hirsutus is an extremely polyphagous species, gramme has been proposed for the Caribbean utilizing at least 144 genera in 74 plant region, with classical biological control as families. Some major hosts include mango, the main component. One of the candidate hibiscus, palms, coffee, grape, citrus and natural enemies, the lady beetle Cryptolaemus Annona species. Williams (1985) reported that montrouzieri Mulsant (Coleoptera: Coccinel- it causes bunchy leaves on limes in Australia. lidae), was introduced to Trinidad from India Tropical fruit crops in the Caribbean that are in 1996 (Gautam et al., 1996). Results of this affected include Annona species, carambola, predator introduction are given by McComie litchi, mango, avocado, Citrus sp., bananas (1997). At the time of lady beetle release, the and papaya (Etienne et al., 1998). pink mealybug density averaged 19 ovisacs The development of this species occurs and 14 adults per shoot but declined sig- in 3–4 weeks and the females can produce nificantly within 12 weeks (McComie, 1996). approximately 500 eggs each (Ghose, 1972). Another important natural enemy of M. Ghose (1972) demonstrated that reproduction hirsutus is the parasitoid Anagyrus kamali in this species is strictly sexual. During late Moursi (Hymenoptera: Encyrtidae), while autumn and winter, the female seeks a shel- Mani (1989) lists at least 30 species of preda- tered position to lay her eggs, usually forming tors and 16 hymenopterous parasitoids that an aggregation of conspecific females. In the can be considered candidates for biological summer, females may not seek shelter to lay control of this mealybug. eggs. Eggs hatch in 3–8 days (Misra, 1920; The citrus mealybug, Planococcus citri,is Ghose, 1972) and the nymphal stage lasts a serious pest in eastern Australia, infesting 10–22 days (Mani, 1989). the fruits when they are half-to full-grown Infestation symptoms appear first on the in December to January. Less common growing tips. Shoots become twisted, with species in this area are Ferrisia virgata, Plano- shortened internodes, forming bunchy heads coccus pacificus Cox, Pseudococcus longispinus of small bushy leaves at the tips, assuming a (Targioni-Tozzetti), Maconellicoccus hirsutus, multiheaded appearance with multiple dam- and Pseudococcus lilacinus (Cockerell). age. In heavy infestations, leaves and shoots The citrus mealybug is a cosmopolitan become compact and crisp. Symptoms in species infesting a wide range of hosts. Eggs mulberry are known as Tukra disease (Misra, (600) are laid in a loose cottony egg sac. There 1920). On mango, infested flowers dry and are three moults for female mealybugs and drop, resulting in fewer, smaller, abnormally four for males, the whole life cycle taking shaped fruit that may drop early. Maconelli- about 6 weeks in summer. There are 4–6 coccus hirsutus is one of the mealybug species generations year−1. P. citri produces copious

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honeydew resulting in heavy sooty mould the immature stages that suck sap from the that disfigures the fruit. Low hanging fruit underside of the leaves, favouring the attract heavy ant activity (Pheidole spp. and development of sooty mould and hindering Iridomyrmex spp.) that disrupts predators and photosynthetic activity (Vazquez et al., 1996). parasitoids, exacerbating the problem. Tree The whitefly, Diauropora decempunctata skirting is practised in winter after each crop (Quaintance and Baker), occurs on custard to lift branches off the ground and to improve apples in India; Aleurodicus destructor Mackie the efficacy of ant sprays applied to the trunk occurs throughout South-East Asia (Water- in spring and summer. house, 1993). The main natural enemies of P. citri in eastern Australia are the parasitoid, Leptomastix dactylopii Howard, the mealybug Lace bugs ladybird, C. montrouzieri, and the lacewing, Oligochrysa lutea (Walker) (Smith 1991b). Soursops are not generally troubled with L. dactylopii can achieve 50–80% parasitism tingids, but local outbreaks of the species while up to 40% of mealybug-infested fruit Antiteuchus tripterus (F.) and Corythucha attract activity from C. montrouzieri and/or gossypii (F.) may occur. These insects are O. lutea. L. dactylopii is augmentatively rel- found on the undersides of leaves and on eased at about 10,000 ha−1 in early summer. fruits. Destruction of leaf cells due to the In the Philippines, mealybugs, mainly sucking habit of these insects causes yellow- F. virgata and P. lilacinus, are common pests ish and silver or brownish necrotic areas of custard apples (De Leon and German, 1917; (Gutierrez and Trochez, 1977). Gutierrez Paguirigan, 1951; Galang, 1955; Vinas, 1972; and Trochez (1977) noted that feeding by Cantillang, 1976; Coronel, 1983). P. lilacinus A. tripterus on fruits causes stunting and (and P. citri) occur on a wide range of hosts desiccation, with extensive fruit drop later. throughout South-East Asia, and are recorded from custard apple in India, Malaysia, Thailand, Vietnam, Indonesia and Brunei (Khoo et al., 1991; Waterhouse, 1993). They are Aphids commonly attended by ants such as Oecophylla smaragdina (F.) and Dolichoderus thoracicus The cotton aphid, Aphis gossypii Glover, and (Smith). Coccinellids such as Scymnus spp., the black citrus aphid, Toxoptera aurantii slugs, and parasitoids, such as Anagyrus spp, (Boyer de Fosncolombe), infest young leaf help keep populations in check. shoots.

Whiteflies Lepidopterous leafminers

In Cuba, several species of whiteflies have Lepidopterous leafminers and other cater- been observed in soursop, sugar apple and pillars ocurr in annonas, but only as minor or bullock’s heart. They include Aleurocanthus localized pests in some areas, and are com- trachoides (Back), Bemisia tabaci (Grenadius), monly held in check by parasites. Arevalo Aleurodicus dispersus Russell, and Aleuro- (1982) studied damage caused by Phyllocnistis thrixus floccosus (Maskell) (Vazquez et al., sp. (Gracillariidae), a pest of A. cherimola 1996). Whitefly populations tend to increase in Colombia and Ecuador. Arevalo (1982) in poorly tended orchards as well as in trees reported that 85% of the leaves are attacked planted too densely. The damage they cause by this insect, and described its various is of two main types. One is caused by the life stages. Two common biological control adults while sucking sap from shoots, thus agents of this pest are Apanteles sp. and weakening them. The other is caused by Horismenus sp. (Arevalo, 1982).

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Coleopteran leafminers chilensis attacking cherimoya in Chile seldom causes significant injury to the foliage. Ochoa In Brazil, Prinomerus anonicola Bondar et al. (1994) also reported that leaves infested (Coleoptera: Curculionidae) deposits eggs on by Eriophyes annonae Keifer (= Aceria annonae leaves of soursop, and the emerging larvae [Keifer]) show initial protuberances on the make irregular blotch mines on the upper upper surface corresponding to a fine lint of side of the leaf. This pest is more common in trichomes on the lower surface. As the leaves plant nurseries, but can attack field-grown develop and the colony increases in size the plants (Braga et al., 1998). lint grows to surround the main leaf vein, a symptom called erineum. Young leaves attacked early can shrivel or fold inwards together and galls may be observed on the Lepidopterous leaf feeders upper surface. In eastern Australia, mites are minor In eastern Australia, the main leaf feeder is pests of custard apple. The tetranychids the larva of the pale-green triangle butterfly, Tetranychus urticae Koch, T. ludeni Zacher, Graphium ecrypylus lycaon (C. and R. Felder). and T. neocaledonicus (André) occur. In The smooth, velvety, green, yellowand tan Thailand, Oligonychus biharensis (Hirst) and caterpillars eat large holes in the young Brevipalpus sp. are minor pests (Morokote, leaves and occasionally feed on the skin of the 1999, personal communication). fruit. They are heavily parasitized by tachinid flies and are rarely a problem except on young trees less than 2 m high. In South-East Asia (India, Thailand, Pests of the Trunk and Branches Indonesia) the caterpillars of Meganotron rufescens (Butler) (Sphingidae), Papilio aga- Coleopteran stem borers memnon L. (Papilionidae), Archips micaceanus Attacus atlas (Tortricidae), and L. (Satumiidae) In eastern Australia, the elephant weevil, are minor pests (Koesriharti, 1991; Water- Orthorhinus cylindrirostris (F.), is a sporadic house, 1993). Larvae of two woodboring pest on custard apples. The adults cause fruit Zuezera coffeae species, Nietner (Cossidae) drop by chewing pieces of bark from the fruit Squamurae disciplaga and (Swinhoe) (Metar- stalk (Smith, 1991a). A number of beetles belidae), damage twigs (Vinas, 1972; Gabriel, occasionally bore into the trunk and main et al 1975; Khoo ., 1991). limbs, e.g. Xyleborus perforans (Wollaston), Leptopius setosus Lea, and Euthyrrhinus meditabundus (F.). In the Philippines, the Mites white grub, Anomala sp., attacks the roots, sometimes causing wilting (Vinas, 1972; Polyphagotarsonemus latus Banks infestations Gabriel, 1975; Coronel, 1983). are mostly observed in greenhouses, induc- In Brazil, the curculionid Cratosomus ing smaller leaves to roll towards the lower bombinus bombinus is a 22-mm-long weevil surface. In the field, damage to small fruits that is black to dark grey with transverse has been observed as bronzing that covers the yellowstripes on its thorax and elytra fruit and prevents their development (Ochoa (Junqueira et al., 1996) (Plate 49). The female et al., 1994). Brevipalpus phoenicis affects up to inserts its eggs in branches and the larvae 85% of the epidermal surface of unripe sour- bore through the vascular system, reducing sop fruit. The fruit becomes bronze coloured plant growth and vigour (Caloba and Silva, with darker epidermal cracking and lighter 1995; Junqueira et al. 1996). The characteristic striations, resembling rust. On cherimoya, symptom of infested branches is the discharge damage is similar to that of Brevipalpus of a dark exudate mainly where the branches pseudostriatus Ochoa and Salas (Ochoa et al., fork. This injury serves as a port of entry for 1994). Astudillo (1989) reported that B. the fungi Lasiodiplodia theobromae and Phomosis

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sp. (Caloba and Silva, 1995; Junqueira et al., as well as on basic biological information on 1996). the key pests, Bephratelloides spp. and Cerco- Egg incubation lasts approximately 16 to nota. In general, chemical interventions and 21 days; the larval stage lasts approximately very timid cultural approaches are the status 100 days. The larva pupates inside the stem of arthropod management so far achieved for and the adult emerges after a 50-day period Annona species in the Neotropics. (Junqueira et al., 1996). Bagging of fruit to prevent infestation, sanitation of borer-infested fruit in groves, CONTROL In Brazil, it is recommended to and general spray schedules against the two cut and burn infested branches, followed by major key pests is the norm. Monitoring tech- painting the cut with a salve made with lime, niques based on insect behaviour and biology copper sulphate, sulphur, Diazinon, sodium have not been developed. However, surveys chloride, soybean oil and water. Another of insects attacking these crops provide at method is injection of insecticides into the least some information on the type of tree or plugging exit holes with beeswax or damage and frequency of pests (Gutierrez soap (Junqueira et al., 1996). Planting Cordia and Trochez, 1977; Astudillo, 1989). Thus, verbenacea as an adult trap crop is also from the information available at present, recommended (Nascimento et al., 1986). An sanitation and/or chemical treatment does unidentified tachinid has been collected from not suffice for the two key pests. Their basic pupae (Dominguez, 1980). biology and behaviour, and those of their In Brazil, another curculionid, Heilipus natural enemies, must also be incorporated velamen, is also considered a serious pest into a holistic pest management strategy. of trunks and branches (Costa Lima, 1956; Pereira et al., 1996). The symptoms of attack from this weevil are similar to those observed Pest Management in Custard Apples when Cratosomus bombinus bombinus attacks in Eastern Australia annona trees; however, the galleries made by Heilipus affect only the tree cortex and bark The key pests in Australia are P. citri, A. l. (Plate 50). Junqueira et al. (1996) reported that lutescens, A. nitida, B. tryoni, P. nigra and C. adults and larvae may be infected by the punctiferalis. Minor pests include G. ecrypylus fungus Metarhizium sp. while Goncalves lycoen, O. cylindrirostris, tetranychid mites, (1973) has observed Agonocryptus sp. (Ichneu- thrips, bark-boring weevils and other scales. monidae) parasitizing the larvae. Because of the size of trees and the difficulty of effectively spraying for mealybugs and scales, an integrated approach to pest control Present Status of Insect Pest is vital. Management in the Neotropics Biological control is an important component of management. All pests except the Annona culture in the Neotropics has been Amblypelta spp. and B. tryoni have significant experiencing significant changes over the natural enemies. P. citri is parasitized by the past 20 years, which also bears on insect encyrtid wasp, L. dactylopii, and is attacked by management. There have been large the mealybug ladybird, C. montrouzieri, and increases in Annona hectarage in the the lacewing, O. lutea (Walker). L. dactylopii Caribbean region, Central America, South provides 50–80% parasitism, and up to 40% of America, and California. In consequence, mealybug-infested fruit attract activity from some advancement has occurred in under- the two predators. P. nigra is normally heavily standing the pollinator and pest communities parasitized by the pteromalid wasp, S. caerulea. in these crops. However, before satisfactory Dusty conditions arising, for example, from pollinator and pest management program- roads should be avoided, as dust will disrupt mes are established, more information must parasitoids. Infestations often develop in be gathered on insect pollination mechanisms, young trees especially when there are many

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Pollinators and Pests of Annona Species 215

ants of the genera Pheidole and Iridiomyrmex. hosts like guava and loquat should not be The fungus V. lecanii causes heavy mortality planted in or near the orchard. in P. nigra and other soft scales during wet Although biocontrol options are avail- weather. able for mealybugs and scales, selective spray- The tachinid fly, A. proclinata, is an impor- ing is usually necessary for Amblypelta spp. tant parasitoid of C. punctiferalis, parasitizing and B. tryoni. When fruitspotting bug damage up to 40% of the late instar larvae (Smith, is detected (usually during mid-summer 1991b). The assassin bug P. plagiopennis is to mid-autumn), selective spraying with a a common predator of C. punctiferalis, G. ‘soft’ insecticide is necessary. Some growers ecrypylus and other caterpillars. Tachinid flies attempt to control the bugs during December– also heavily attack larvae of G. ecrypylus. January, before releasing L. dactylopii, but The larvae of the fruit flies B. tryoni, sometimes spraying is also necessary later in B. neohumeralis, B. dorsalis and B. papayae are the season. Selective pesticides disrupt natu- parasitized by the braconids Opius perkinsi ral enemies of P. citri but still allow significant Fullaway, Fopius deeralensis (Fullaway), F. survival of the beneficial species. The fruit fly arisanus (Sonan) and Diachasmimorpha tryoni B. tryoni is controlled with weekly applica- (Cameron), but these have limited impact. tions of protein bait (from the time that the The introduced parasitoid L. dactylopii is fruit are three-quarters grown to harvest). A commercially mass reared and augment- patch of foliage about 1 m2 is sprayed on each atively released by growers during early tree. Selective insect growth regulators are summer at about 10,000 ha−1. Adults of C. available for fruit borer control if necessary. montrouzieri are also released by growers if the Monitoring is important to minimize species is absent. Spraying for fruitspotting the number of sprays. P. citri is considered a bugs must be coordinated with parasitoid serious problem if 20% or more of the fruit are releases. Sprays should be avoided for at least infested with one or more large adult females. 7 days after a release, and the follow-up spray Ten randomly selected fruit are examined in should not be applied after 3–4 weeks when situ on 20 random trees ha−1 at fortnightly the next generation of parasitoids are emerg- intervals from January to April. Mealybugs ing. Alternatively, if a spray has just been are checked for parasitism and predation. applied, 7 days at least should elapse before To determine the level of infestations of parasitoid release. To avoid redundancy, P. nigra, five 1-year-old lateral branches 1 cm L. dactylopii should not be released sooner thick are assessed on 20 random trees ha−1 than 1 week before or after a major emergence once or twice per season. Scales are checked of conspecifics in the target area. for parasitism. Ant control is important for pest manage- Fruitspotting bugs are monitored at ment. At the end of the growing season, i.e. fortnightly intervals from late December to during winter, the tree skirts are pruned up late March by sampling ten random fruit in about 1 m off the ground to minimize contact situ on each of 20 random trees ha−1. Action is with the soil the following season. Fruits near necessary if 2% or more have fresh damage. the soil are more likely to develop diseases like Damaged fruit are removed during sampling. diplopia rot and cylindrocladium spot and to Yellow peach moth is monitored as for develop heavy mealybug and ant infestations. fruitspotting bug, from February to April at The ants disrupt natural enemies of mealy- fortnightly intervals, and fruits are checked bugs and scales. Ant sprays are applied two or for signs of frass. Action is necessary if 5% or three times (in early and mid-season) to the more of fruit are attacked. lower trunk. Attention must be given to orchard hygiene and alternative host plants that can increase pest pressure in the custard apple References orchard. Mature fruit infested with yellow peach moth or with fruit fly should be Ahmed, M.S. (1936a) Pollination and selection in collected and destroyed. Preferred fruit fly Anona squamosa and Anona Cherimolia. Ministry

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of Agriculture of Egypt, Technical Science Service mulberry Morus alba. Journal of Insect Science 5, Horticultural Section Bulletin No. 57. 114. Ahmed, M.S. (1936b) The Anonas in Egypt. Ministry Bennett, F.D. and Alam, M. (1985) An Annotated of Agriculture of Egypt, Horticultural Section Check List of the Insects and Allied Terrestrial Booklet No. 14. Arthropods of Barbados. Caribbean Agricultural Alata, J. (1973) Lista de insectos y otros animales Research Development Institute, 81 pp. dañinos a la agricultura del Perú. Ministerio de Braga, R., Oliveira, M.A., Warumby, J. and Moura, J. Agricultura, Estacion Experimental Agricola de la (1998) Pragas da gravioleira. In: Braga, E., Molina, Manual No. 38, 47–48. Cardoso, J. and Chagas, F. (eds) Pragas de Andrade, B.M. (1996) Pollination and breeding fruteiras tropicais de importancia agroindustrial. system of Xylopia brasiliensis Sprengel Empresa Brasileira de Pesquisa Agropecuaria, (Annonaceae) in south-eastern Brazil. Journal pp. 131–141. of Tropical Ecology 12, 313–320. Brun, L.O. and Chazeau, J. (1980) Catalogue des Anjos, N. and Pereira, M.J.B. (1997) Quantidade Ravageurs d’Interest Agricole de Nouvelle – de instares larvais em Bephratelloides pomorum Caledonie. Office de la Recherche Scientifique (Fab.) (Hymenoptera: Eurytomidae). Resumos et Technique Outre Mer, Centre de Noumee, 16 Congresso Brasileiro de Entomologia, Salvador, Nouvelle – Caledonie, 120 pp. BA, Marco de 1997, p. 63. Brunner, S.C. and Acuña, J. (1967) Sobre la biologia de Anonymous (1989) Prospeccion de Insectos y Acaros Bephrata cubensis Ashm., el insecto perforador de Fitofagos Asociados al Chirimoyo. Universidad las frutas Annonaceas. Academia Ciencias de Catolica de Valparaiso, Facultad de Cuba. Instituto Agronomico Serie Agricultura Agronomia, Chile, 107 pp. 1, 14 pp. Arevalo de, I.S. (1982) Anotaciones sobre Phyllo- Brussel, E.W. and Wiedijk, F. (1975) Prospects for cnistis spp., minador del follaje del chirimoyo. cultivation of soursop in Surinam with special Revista Colombiana de Entomologia 8, 15–22. references to the soursop wasp Bephrata Astudillo, P. (1989) Determinacion de Insectos y Acaros maculicollis Cam. Suriname Landbouw 21, 48–61. Asociados a Frutos de Chiromoyo Annona Bustillo, A.E. and Peña, J.E. (1992) Biology and con- cherimola Mill. Determinacion y evaluacion de la trol of the Annona fruit borer Cerconota anonella naturaleza de desecho. Universidad Catolica de (Lepidoptera: Oecophoridae). Fruits 47, 81–84. Valparaiso, Facultad de Agronomia, Quillota, Caloba, J.S. and Silva, N.M. da (1995) Insects Chile, 107 pp. asociados a graviola, Annona muricata L., e Babu, T.R. and Azam, K.M. (1987) Studies on biol- Rollinia mucosa (Jacq.) Bail no estado do ogy, host spectrum and seasonal fluctuation of Amazonas. Anais Sociedade Entomologia the mealybug Maconellicoccus hirsutus (Green) Brasileira 24, 179–182. on grapevine. Indian Journal of Horticulture 44, Calzavara, B. and Muller, C. (1987) Fruticultura 284–288. tropical: a gravioleira Annona muricata L. Bartelt, R., Dowd, P.F., Vetter, R.S., Shorey, H.H. and Belem. Empresa Brazileira de Pesquisa Agro- Baker, R.C. (1992) Responses of Carpophilus pecuaria, CNTU, Documento 47, 36 pp. hemipterus (Coleoptera: Nitidulidae) and other Campbell, C.W. (1979) Effect of gibberellin sap beetles to the pheromone of C. hemipterus treatment and hand pollination on fruit-set of and other related coattractants in California atemoya (Annona hybrid). Proceedings of the field tests. Environmental Entomology 21, Tropical Region, American Society of Horticultural 1143–1153. Sciences 23, 122–124. Bartelt, R., Vetter, R.S., Carlson, D.G. and Baker, T.C. Cantillang, P.L. (1976) Philippine atis – the sweetest (1994) Responses to aggregation pheromones fruit. Greenfields 6, 26–27. for five Carpophilus species (Coleoptera: Carneiro, J. da and Bezerril, E. (1993) Controle Nitidulidae) in a California date garden. das brocas dos frutos (Cerconota anonella)e Environmental Entomology 23, 1534–1543. da semente (Bephratelloides maculicollis)da Bastos, J.M. (1985) Principais plagas das culturas e seus graviola no Planlato da Ibiapaba. Annais controles, 3rd edn. São Paulo, Nobel, Brazil, Sociedade Entomologia Brasil 22, 155–160. 329 pp. Castañeda V., A. and Pineda, S.G. (1997) Identifica- Beardsley, J.W. (1985) Maconellicoccus hirsutus tion, description and behavior of cherimola’s (Green). Proceedings of the Hawaii Entomological fruit borer in Coatepec Harina, Mexico. Society 25, 27. Memorias Congreso Internacional de Annonaceaes, Beevi, N., Janarthanan, R. And Natarajan, K. (1992) Chapingo, Mexico, 39 pp. Efficacy of some insecticides against eggs Castañeda V., A., Pineda, S.G. and Rebollar, A. of Maconellicoccus hirsutus Green on (1997) Searching for cherimola pollinator

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insects in the states of Mexico and Michoacan. Estatilla, H. (1921) The atis moth borer. Philippine I. Identification. Memorias Fundacion Salvador Agriculture 10, 169. Sanchez Colin. Coatepec Harinas, pp. 197–204. Etienne, J., Matile-Ferrero, D. and Lablanc, F. (1998) Cogez, X. and Lyannaz, J.P. (1996) Manual of First record of the mealybug Maconellicoccus pollination of sugar apple. Tropical Fruit hirsutus (Green) from Guadeloupe: present Newsletter 19, 5–6. state of this pest of crops in the French Carib- Coronel, R.E. (1983) Promising Fruits of the bean (Hem.: Pseudococcidae). Bulletin de la Philippines. University of the Philippines, Societé Entomologique de France 103, 173–174. Laguna, Philippines, 508 pp. Evangelista-Lozano, S., Aldana, L. and Valdes, M. Costa Lima, A. (1945) Insetos do Brasil, Tomo (1997) Estudio del barrenador de la semilla 5. Lepidopteros 1a parte. Escola Nacional de de la guanabana Bephratelloides cubensis Agronomia, Serie Didactica No. 7. 5, 259–270. Ashmead (Hymenoptera: Eurytomidae). Costa Lima, A. (1948) Entomofagos sul Americanos Memorias Congreso Internacional de Annonaceaes, (Parasitos e predadores) de insetos nocivos Chapingo, Mexico, 264 pp. a agricultura. Boletin Sociedade Brasileira da Farre, M., Perez, J.M., Hermoso, M. de los A. Agronomia 11, 1–32. and Orgata R., J.M. (1997) Estudio sobre Costa Lima, A. (1956) Insetos do Brasil, Tomo polinizacion de chirimoyo (Annona cherimola 10: Coleopteros 4a parte. Escola Nacional de Mill) en Espana. Memorias Congreso Inter- Agronomia, Serie Didactica No. 12. 10, 94–106. national de Annonaceas. Chapingo, Mexico, Coto, D., Saunders, J.L., Vargas, C. and King, A. pp. 43–55. (1995) Plagas invertebradas de cultivos tropi- Fennah, R.G. (1937a) Lepidopterous pests of cales con enfasis en America Central. Centro soursop in Trinidad. Tropical Agriculture 14, Agricola Investigacion y Enseñanza, Serie Tecnica 175–178. 12, 7–9. Fennah, R.G. (1937b) Lepidopterous pests of D’Araujo e Silva, A.G., Goncalves, C.R., Galvao, soursop in Trinidad. Thecla ortygnus. Tropical D.M., Goncalves, A.J., Jones, J., Silva, M.D. and Agriculture 14, 244–247. DeSimoni, L. (1968) Quarto catalogo dos Gabriel, B.P. (1975) Insects and Mites Injurious to insectos que vivem nas plantas do Brasil, seus Philippine Crop Plants. Department of Ento- Parasitos e predadores, Parte II, Tomo I, 622 p., mology, College of Agriculture, University Tomo II 253 pp. of Philippines, Los Baños, Laguna. De Leon, B. and German, J. (1917). Forms of some Galang, F.G. (1955) Fruit and Nut Growing in the Philippine fruits. Philippine Agriculturist and Philippines. AIA Printing Press, Malabon, Forester 5, 251–283. Rizal, Philippines. Deroin, T. (1989) Evolution des modalites de la Gallo, D., Nakano, O., Silvera-Neto, S., Carvalho, R., pollinisation au cours du developpement des Batista, G., Berti, E., Parra, J., Zucchi, R., axes aeriens chez une Annonacee savanicole Alves, S. and Vendramin, J. (1988) Manual soumise aux feux annuels: Annona senegalensis de entomologia agricola. Agronomica Ceres, Pers. Comptes Rendus de l’Académie des Sciences São Paulo, 649 pp. Paris serie III, 308, 307–311. Galon, I., Gazit, S. and Podoler, H. (1982) Improve- Dominguez, G. (1980) Insectos perjudiciales de la ment of natural fruit set of Annona by guanabana (Annona muricata L.) en el estado increasing the population of pollinating Zulia, Venezuela. Revista Lationoamericana de insects. Alon Halontea 9, 611–614. Ciencias Agrarias 15, 43–55. Gautam, R.D., De Chi, W. and Maraj, C. (1996) Dozier, H.L. (1932) Two important West Indian A successful journey of ladybirds from India seed-infesting chalcid wasps. Journal of Agri- to Trinidad. Interamerican Institute Ciencias culture of Puerto Rico 16, 103–112. Agricolas, Caraphin News 14, 1–2. Duarte, F.E. (1947) Insetos holometabolicos. Gazit, S., Galon, I. and Podoler, H. (1982). The role Agronomia 6, 178–211. of nitidulid beetles in natural pollination Ebeling, W. (1959) Subtropical Fruit Pests. University of Annona in Israel. Journal of the American of California Press, 389 pp. Society Horticultural Science 107, 840–852. Escandon, Q., Lamus, E. and Calderon, J. (1982) George, A.P. and Nissen, R.J. (1991) Annona Incidencia de Bephrata maculicollis Cameron cherimola Miller, Annona squamosa L., A. perforador del fruto del guanabano Annona cherimola × A. squamosa. In: Verheij, E.W.M. muricata L., metodos preliminares de control y and Coronel, R.E. (eds) Plant Resources of South rentabilidad de la practica en dos zonas del East Asia. 2. Edible Fruits and Nuts. Pudoc-DLO Valle, Colombia. Facultad de Ciencias Agro- Wageningen, the Netherlands and Prozea pecuarias, Palmira, Colombia. 80 pp. (Thesis). Foundation, Bogor, Indonesia, 447 pp.

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George, A.P., Nissen, R.J., Ironside, D.A. and Kessler, P.A. (1987) Some interesting distribution Anderson, P. (1989) Effects of nitidulid beetles patterns in the Annonaceae. Annonaceae News- on pollination and fruit set of Annona spp. letter (Utrecht, The Netherlands) 6, 7 pp. hybrids. Scientia Horticulturae 39, 289–299. Khoo, K.C., Ooi, P.A.C. and Ho, C.T. (1991) George, A.P., Nissen, R.J. and Campbell, J. A. (1992) Crop Pests and their Management in Malaysia. Pollination and selection in Annona species Tropical Press, Kuala Lumpur, Malaysia. (cherimoya, atemoya, and sugar apple). Acta Koesriharti (1991) Annona muricata L. In: Verheij, Horticulturae 321, 178–185. E.W.M. and Coronel, R.E. (eds) Plant Resources Ghose, S.K. (1972) Biology of the mealybug, of South East Asia. 2. Edible Fruits and Nuts. Maconellicoccus hirsutus (Green) (Pseudo- Pudoc-DLO Wageningen, Holland and Prozea coccidae: Hemiptera). Indian Agriculturist 16, Foundation, Bogor, Indonesia, 447pp. 323–332. Korytowski, G.C. and Peña, D. (1966) Bephrata Goncalves, C.R. (1973) Observacoes sobre cubensis Ashm. (Hymenoptera: Eurytomidae): hospedeiros de Himenopteros da Familia Una nueva especie dañnina a las anonaceas en Ichneumonidae no Brasil. Annais Sociedade el Perú. Revista Peruana de Entomologia 9, 56–60. Entomologica do Brasil 2, 31–36. Kumar, R., Hoda, M.N. and Singh, D.K. (1977) Gottsberger, G. (1970) Beitrage zur Biologie von Studies on the floral biology of custard Annonaceen-Bluten. Osterreichische Botanische apple (Annona squamosa Linn.). Indian Journal Zeitschrift 118, 237–279. of Horticulture 34, 252–256. Gottsberger, G. (1985) Pollination and dispersal in Lawrence, G. (1974) A preliminary list of fruit the Annonaceae. Annonaceae Newsletter 1, 6–7. pests in Trinidad. Journal of the Agricultural Gottsberger, G. (1988) The reproductive biology of Society of Trinidad and Tobago 24, 258–265. primitive angiosperms. Taxon 37, 630–643. Leal, W.S., Moura, J., Bento, J., Vilela, E. and Pereira, Gottsberger, G. (1991) As annonaceas do cerrado e P. (1997) Electrophysiological and behavioral sua polinizacao. Revista Brasileira Biologia 54, evidence for a sex pheromone in the wasp 391–402. Bephratelloides pomorum. Journal of Chemical Grissell, E.E. and Foster, M.S. (1996) A new Ecology 23, 1281–1290. Bephratelloides (Hymenoptera: Eurytomidae) Lima, I., Do Nascimento, R., Mendoca, C., Duarte, A. from seeds of Cymbopetalum (Annonaceae) in and Silva, L. (1997) Mating behavior of the Mexico. Proceedings of the Entomological Society Annona seed borer Bephratelloides pomorum of Washington 98, 256–263. (Hymenoptera: Eurytomidae) in semi-field Grissell, E.E. and Schauff, M.E. (1990). A synopsis conditions. Memorias Congreso Internacional de of the seed-feeding genus Bephratelloides Annonaceaes, Chapingo, Mexico, 272 pp. (Chalcidoidea: Eurytomidae). Procedings of the Lopez, E. and Rojas Dent, R. (1992) Arthropods asso- Entomological Society of Washington 92, 177–187. ciated with cherimoya (Annona cherimola Mill.) Gutierrez, B.A. and Trochez, A. (1977) Estudio sobre flowering in Quillota, Chile. Acta Entomologica las plagas de las anonaceas en el Valle del Chilena 17, 101–106. Cauca. Revista Colombiana de Entomologia 3, Lopez, E. and Uquillas, C. (1997) Carpophilus hemip- 39–47. terus (Coleoptera: Nitidulidae) as cherimoya Hopping, M.E. (1983) Pollination and fruit set of (Annona cherimola Mill.) pollination agent cherimoya. Australian Horticulture 82, 11–14. under controlled conditions. Acta Entomologica Idstein, H., Heeres, W. and Schneier, P. (1984) High Chilena 21, 89–99. resolution gas chromatography, mass spectro- Mani, M. (1989) A review of the pink mealybug metry and gas chromatography Fourier trans- Maconellicoccus hirsutus (Green). Insect Science form analysis of A. cherimola volatiles. Journal of and its Application 10, 157–167. Agricultural and Food Chemistry 32, 383–389. Mani, M. and Thontadarya, T.S. (1988) Population Junqueira, N., Cunha, N. and Oliveira, M. (1996) dynamics of the mealybug Maconellicoccus Graviola para a exportacao: aspectos fitosanitarios. hirsutus (Green) and its natural enemies in Empresa Brasileira da Pesquisa Agropecuaria, grapevine ecosystem. Journal of Biological Brasilia, 67 pp. Control 2, 93–97. Kahn, T.L. (1997) Pollination Theory and Practice. Marin, J.C. (1973) Preliminary list of pests of Cherimoya Handbook. The California Cheri- Annonaceae, sapodilla (Achras zapota L.) moya Association, pp. 2–220. and guava (Psidium guajava L.) in Venezuela. Kahn, T.L. and Arpaia, M.L. (1990) Methods of Agronomia Tropical 23, 205–216. cherimoya hand pollination. California Martinez, N.B. de and Godoy, F.J. (1983) Cherimoya Association Newsletter 3, 1–3. Natural enemies of the soursop fruit borer,

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Cerconota anonella Sepp. Agronomia Tropical 33, Nakasone, H.Y. and Paull, R.E. (1998) Tropical Fruits. 155–161. CAB International, Wallingford, UK, 445 pp. Martinez, S. and Cabrera, I. (1997) Incidencia de Nascimento, A., Mesquita, A. and Caldas, R. (1986) Bephratelloides cubensis Ashmead y Apate mona- Flutuacao populacional e manejo da broca cha (Fabricius) en seis selecciones de guana- da laranjeira, Cratosomus flavofasciatus Guerin, bana en Puerto Rico. Memorias Congreso Inter- 1844 (Coleoptera: Curculionidae) com Maria nacional de Annonaceaes, Chapingo, Mexico,p.37. Preta Cordia verbenaceae (Borraginaceae). Annals McComie, L.D. (1996) Incidence and treatment of Soceidade Entomologia Brasileira 15, 45–51. the hibiscus mealybug Maconellicoccus hirsutus Noonan, J.C. (1954) Review of investigations of the (Green) one year after its discovery in Trini- Annona species. Natural Horticultural Magazine dad. First Regional Symposium on the hibiscus 33, 219–225. mealybug June 1996, St Georges, Grenada, Nuñez, R. and de la Cruz, J. (1982) Reconocimiento pp. 4–6 y descripcion de las principales insectos Mcleod, A. and Pieris, N.M. (1981) Volatile flavor observados en cultivares de guanabana components of soursop Annona muricata. (Annona muricata L.) en el departamento del Journal of Agricultural and Food Chemistry 29, Valle. Acta Agronomica 32, 45–51. 488–490. Ochoa, R., Aguilar, H. and Vargas, C. (1994) Phyto- Medina-Gaud, S., Bennett, F., Segarra, A.E. and phagous mites of Central America: an illus- Pantoja, A. (1989) Notes on insect pests of trated guide. Centro Agronomico Investigacion y soursop (guanabana), Annona muricata L., and Ensenanza. Serie Technica 6, 234 pp. their natural enemies in Puerto Rico. Journal of Oppenheimer, C. (1947) The acclimatisation of new Agriculture of the University of Puerto Rico 73, tropical and subtropical fruit trees in Palestine. 383–390. Bullettin Agricultural Research Station, Rehovot Mendes, J. and Pereira, M.J.B. (1997) Danos de 44, 94–103. Bephratelloides pomorum (FAB) (Hymenoptera: Paguirigan, D.B. (1951) Outline of Philippine Eurytomidae) em pomares de graviola crops: soursop and sugar-apple. Agricultural (Annona muricata L.). Resumos 16 Congresso Industrial Life 13, 34–35. Brasileiro Entomologico. Salvador-Bahia, Marco Peña, J.E. (1988) Toxotrypana y Bephratelloides spp. 1997, p. 296. ejemplos de adaptacion de monofagos a Misra, C.S. (1920) Tukra disease of mulberry. plantas hospederas. Memorias XV Congreso Proceedings Third Entomological Meeting, Pusa, Socolen, Julio 1987, Bogota, Colombia, pp. 42–46. pp. 610–618. Peña, J.E. (1998) Current and potential arthropod Momose, J., Nagamitsu, T. and Inoue, T. (1998) pests threatening tropical fruit crops in Florida. Thrips cross-pollination of Popowia pisocarpa Proceedings of the Florida State Horticultural (Annonaceae) in a lowland dipterocarp forest Society 111, 327–329. in Sarawak. Biotropica 30, 444–448. Peña, J.E. and Bennett, F.D. (1995) Arthropods Nadel, H. and Peña. J.E. (1991a) Hosts of Bephratel- associated with Annona spp. in the neotropics. loides cubensis (Hymenoptera: Eurytomidae) in Florida Entomologist 78, 329–349. Florida. Florida Entomologist 72, 207–211. Peña, J.E and Nagel, J. (1988) Effectiveness of Nadel, H. and Peña, J.E. (1991b) Seasonal ovipos- pesticides against two tropical fruit pests. ition and emergence activity of Bephratelloides Procedings of the Florida State Horticultural cubensis (Hymenoptera: Eurytomidae), a pest Society 101, 249–251. of Annona species in Florida. Enviromental Peña, J.E., Glenn, H. and Baranowski, R.M. (1984) Entomology 72, 208–211. Important insect pests of Annona sp. in Florida. Nadel, H. and Peña, J.E. (1994) Identity, behavior, Proceedings of the Florida State Horticultural and efficacy of nitidulid beetles (Coleoptera: Society 97, 337–340. Nitidulidae) pollinating commercial Annona Peña, J.E., Nadel, H. and Torres, V. (1990) Pests of species in Florida. Environmental Entomology Annona species. Tropical Fruit World 1, 121–122. 23, 878–886. Peña, J.E., Castiñeiras, A., Bartelt, R. and Duncan, R. Nagamitsu, T. and Inoue, T. (1997) Cockroach polli- (1999) Effect of pheromone bait stations for sap nation and breeding system of Uvaria elmeri beetles (Coleoptera: Nitidulidae) on Annona (Annonaceae) in a lowland mixed-dipterocarp fruit set. Florida Entomologist 82, 475–480. forest in Sarawak. American Journal of Botany 84, Pereira, M.J.B. (1996) Biologia de Bephratelloides 208–213. pomorum (Fab.) (Hymenoptera: Eurytomidae), Nagel, J., Peña, J.E. and Habbeck, D. (1989) Insect broca da semente de graviola. Tese de pollination of atemoya in Florida. Florida Mestrado em Entomologia, Universidade Entomologist 7, 207–211. federal de Vicosa, Minas Gerais, 71 pp.

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Pereira, M.J.B., Bastos-Neto, E. and Cavalcanti, M. Reyes, A.J. (1967) Algunas recomendaciones para el (1991a) Parasitoides de larvas de Cerconota control del perforador de las semillas de Anno- Anonella (Sepp. 1830) (Lep: Stenomatidae). naceaes (Bephrata sp. Orden Hymenoptera). Congresso Brasileiro de Iniciacao Cientifica em Revista Agricultura Tropical, Bogota, Colombia 25, Ciencias Agrarias, 10: Lavras. Resumos. Minas 325–326. Gerais:FEAB, ESAL, p. 40. Rokba, A.M., El-Waked, A.T. and Ali, N.H. (1977) Pereira, M.J.B., Bastos-Neto, E.M., Cavalcanti, Lima, Studies and evaluation of some annona I. and Santana, A. (1991b) Ciclo biologico de varieties. Agricultural Research Review 55, Cerconota anonella (Sepp. 1830) (Lep: Steno- 13–21. matidae) em dieta artificial. Congresso Brasileiro Ruiz, R.V. (1991) Manejo de problemas entomol- de Iniciacao Cientifica em Ciencias Agrarias, ogicos en huertos de guanabana. XXII Foro 10, 1991, Lavras. Resumos. Mians Gerais: FEAB, entomologico plagas de frutales en Colombia y ESAL, p. 44. alternatives de manejo. Casos: Guanabana, curuba, Pereira, M.J.B., Anjos, N. and Picanco, M. (1996) citricos. Universidad Nacional de Colombia, Ocorrencia de Heilipus velamen (Coleoptera: Palmira, pp. 59–92. Curculionidae) em Minas Gerais. Congresso Saavedra, E. (1977) Influence of pollen grain stage at Brasileiro de Zoologia, 21, Porto Alegre. Resumos, the time of hand pollination as a factor on fruit Rio Grande do Sul: SBZ,UFRGS, p. 82. set of cherimoya. HortScience 12, 117–118. Pereira, M.J.B., Anjos, N. and Picanco, M. (1997a) Safford, W.E. (1914) Classification of the genus Ciclo biologico de Bephratelloides pomorum Annona with descriptions of new and imper- (Fab.) (Hymenoptera: Eurytomidae) da fectly known species. United States National broca da semente. 16 Congresso Brasileiro de Herbarium, Smithsonian Institution 18, 68 pp. Entomologia, Salvador, BA, Marco de 1997,p.50. Saldarriaga, A., Polania, I., Cardenas, R., Posada, L. Pereira, M.J.B., Sant’ana, A. and Anjos, N. (1997b). and Garcia, F. (1987) Guia para el Control Comportamento de oviposicao de Bephratel- de Plagas. Instituto Colombiano Agropecuario. loides pomorum (Fab) (Hymenoptera: Eury- Manual de Asistencia Tecnica No. 1, 4th edn., tomidae), broca da semente de graviola. 401 pp. 16 Congresso Brasileiro de Entomologia. Salvador, Sarasola, L. (1960) Cherimoya culture in Spain. BA, Marco de 1997, p. 50. California Avocado Society Yearbook 44, 47–53. Pereira, M.J.B., Anjos, N. and Picanco, M. (1997c) Schroeder, C.A. (1943) Hand pollination studies Ciclo biologico del barrenador de semillas on the cherimoya. Proceedings of the American de guanabana Bephratelloides pomorum (Fab.) Society Horticultural Science 43, 39–41. (Hymenoptera: Eurytomidae). Agronomia Schroeder, C.A. (1956) Cherimoyas, sapotes and Tropical 47, 4. guavas in California. California Avocado Society Pereira, M.J.B., Eiras, A. and Anjos, N. (1998) Yearbook 40, 49–56. Comportamiento de cortejo y copula de la Schroeder, C.A. (1971) Pollination of cherimoya. broca de semilla de guanabana Bephratelloides California Avocado Society Yearbook 54, 119–122. pomorum (Fab.) (Hymenoptera: Eurytomidae). Smith, D. (1991a) Insect pests. In: Sanewski, G. (ed.) Revista Biologia Tropical 46, 105–108. Custard Apple Cultivation and Crop Protection. Philips, P., Bekey, R. and Goodall, G. (1987) Queensland Department of Primary Indus- Argentine ant management in cherimoyas. tries, Information Series Q190031, 103 pp. California Agriculture (March–April 1987) 41, Smith, D. (1991b) The use of Leptomastix dactylopii 8–9. Howard (Hymenoptera: Encyrtidae) to control Podoler, H., Galon, I. and Gazit, S. (1984) The role Planococcus citri (Risso) (Hemiptera: Pseudo- of nitidulid beetles in natural pollination coccidae) in custard apples in Queensland. of Annonas in Israel: attraction of nitudulid General and Applied Entomology 23, 3–8. beetles to Annona (atemoya) flowers in Israel. Smith, D., Beattie, G.A.C and Broadley, R. (eds) Oecologia Applicata 5, 369–381. (1997) Citrus pests and their natural enemies: Podoler, H., Galon, I. and Gazit, S. (1985) The effect integrated pest management in Australia. of atemoya flowers on their pollinators: Queensland Department of Primary Indus- nitidulid beetles. Acta Oecologica 6, 251–258. tries, Horticultural Research and Development Ramnanan, N. (1996) Recommendations for the Corporation Publication, Information Series sustainable cultivation of soursop (Part II). Ql 97030, 272 pp. Tropical Fruit Newsletter 18, 12–14. Thakur, D.R. and Singh, R.N. (1965) Studies on Reiss, A. (1971) Pollination and fruit set of Annona pollen morphology, pollination and fruit set cherimola and Annona squamosa. MSc thesis, in some annonas. Indian Journal of Horticulture The Hebrew University of Jerusalem, Israel. 22, 10–18.

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Thomson, P. (1970) The cherimoya in Cali- Affairs Office Press, Bureau of Plant Industries, fornia. California Rare Fruit Growers Yearbook Manila, pp. 31–36. 2, 20–34. Vithanage, H.I.M.V. (1984) Pollen–stigma inter- Thomson, P. (1974) Cherimoya and pawpaw actions: development and cytochemistry of pollination. Pomona 7, 3–6, 24. stigma papillae and their secretions in Annona Vazquez, L., Jimenez, R. and Iglesia, M. (1996) squamosa L. (Annonaceae). Annals of Botany 54, Whiteflies (Homoptera: Aleyrodidae) inhabit- 153–167. ing the principal fruit trees grown in Cuba. Waterhouse, D.F. (1993) The Major Arthropod Pests Tropical Fruits Newsletter 20, 3–4. and Weeds of Agriculture in Southmost Asia: Venturi, F. (1966) Insetti e arachnidi delle pieante Distribution, Importance and Origin. ACIAR comuni del Venezuela signalati nel periodo Monograph Series, Canberra, ACT, 141 pp. 1938-1963. Relazione e monografie agrarie Webber, A. (1981) Algunos aspectos da biologia subtropicali e tropicali. Firenze Instuti floral de Annona sericea Dun. (Annonaceae). Agronomico per l’Otremare 86, 13–16. Acta Amazonica 11, 61–65. Vidal, H.L. (1997) Identificacion y frequencia de Webber, A.C. and Gottsberger, G. (1997) Floral insectos polinizadores en guanabana Annona biology and pollination of Bocageopsis multi- muricata. Memorias Congreso Internacional de flora and Oxandra euneura in Central Amazonia. Annonaceaes, Chapingo, Mexico, p. 36. Annonaceae Newsletter 11, 61–66. Villalobos, E. (1987) Use of endosulfan and poly- Wester, P.J. (1910) Pollination experiments with ethylene bags to control Bephrata sp. Ashmead, anonas. Bulletin of the Torrey Botanical Club 37, the Annona seed borer in (Annona cherimola 529–539. Mill). MSc thesis, National University, Costa Williams, D.J. (1985) Australian mealybugs. London Rica. British Museum Natural History 13, 194–196. Villalta, R. (1988) Estudio de la biologia floral Zarate, R.D. (1987) Principales problemas fitosanitarios e identificacion de agentes polinizadores del guanabano Annona muricata y medidas de la guanabana (Annona muricata L.) en la preliminares de control. Universidad Nacional zona atlantica de Costa Rica. Thesis, National de Colombia, FCA-Palmira, Colombia. 28 pp. University, Costa Rica, 61 pp. Zenner, I. and Saldarriaga, A. (1969) Fruit borer Vinas, R.C. (1972) Atis (Annona squamosa L., of annona and soursop Cerconota (Stenoma) Annonaceae). In: Cultural Directions for Philip- anonella Sepp. (Lepidoptera: Stenomiidae). pine Agricultural Crops, Vol. I, Fruits. Public Agricultura Tropical Bogota 25, 325–326.

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8 Pests and Pollinators of Avocado

Manes Wysoki,1 Michael A. van den Berg,2 Gad Ish-Am,3 Shmuel Gazit,3 Jorge E. Peña4 and Geoff K. Waite5 1Department of Entomology, ARO, Institute of Plant Protection, The Volcani Center, PO Box 6, Bet Dagan 50250, Israel; 2Institute for Tropical and Subtropical Crops, Private Bag X11208, Nelspruit 1200, South Africa; 3Department of Horticulture, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel; 4Queensland Horticulture Institute, Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, FL 33031, USA; 5Maroochy Research Station, PO Box 5083, SCMC, Nambour, Queensland 4560, Australia

The avocado, Persea americana Mill. (Laura- islands of the Caribbean, but also in Poly- ceae), is of Central American origin and well nesia, the Philippines, Australia, New known to the native inhabitants of Mexico, Zealand, Madagascar, Mauritius, Madeira, Central America and northern South America the Canary Islands, Algeria, tropical Africa, (Schieber and Zentmyer, 1987; Zentmyer South Africa, southern Spain, southern et al., 1987). It was brought to the West Indies France, Sicily, Crete, Israel and Egypt. and first reported in Jamaica in 1696. It was According to the FAO, the five top taken to the Philippines at the end of the 16th avocado-producing countries are: Mexico, century; to the Dutch East Indies by 1750 and Indonesia, the USA, the Dominican Republic to Mauritius in 1780; it was first brought to and Brazil. World avocado production reached Singapore between 1830 and 1840; it reached 2 million t in 1999 (FAO, 1999). According India in 1892 but never became very popular; to Swirski et al. (1997), the main producing it was planted in Hawaii in 1825, and intro- countries in Africa and its surrounding duced from Mexico into Florida in 1833 and islands are South Africa, Zaire, Cameroon, California in 1871 (Morton, 1987). It is grown Kenya, Egypt and the Canary Islands. in many tropical and subtropical countries in The objective of this chapter is to areas suitable for cultivation, e.g. Australia, review information on pests and pollinators South Africa, Israel and the USA (Florida of avocado in its growing areas throughout and California). Today, avocado is grown the world. Insect pests and mites of avocado commercially not only in North America and have also recently been reviewed by Waite throughout tropical America and the larger and Martinez (2002).

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PHYTOPHAGOUS ARTHROPODS: Many natural enemies, mostly predacious PHYLUM ARTHROPODA mites, are associated with O. coffeae. In South Africa, according to Meyer (2001), the Class Arachnida following predacious mites were found: Anystis baccarum (L.) (Anystidae), Agistemus ORDER ACARI africanus (Meyer and Ryke), A. tranatalensis Meyer (Stigmaeidae), Eupalopsellus brevipilus Tetranychidae (Meyer and Ryke) (Eupalopsellidae), Tydeus grabouwi Meyer and Ryke (Tydeidae), The most important tetranychids affecting Amblyseius munsteriensis Van der Merwe, avocado are Oligonychus punicae (Hirst), O. A. herbicolus (Chant), A. multidentatus (Swirski perseae (Tuttle, Baker and Abbatiello), O. and Shechter), A. transvaalensis (Van der coffeae (Nietner), O. yothersi (McGregor), Para- Merwe and Ryke), A. tutsi Pritchard and Baker, tetranychus sp., Panonychus citri (McGregor) and Typholdromus buccalis Van der Merwe and Eotetranychus sexmaculatus (Riley). (Phytoseiidae). In Australia, the main predators of the mite in coastal areas are Stethorus Tea red mite, Oligonychus coffeae (Nietner) spp., whereas in drier inland areas, phytoseiid mites prey on them (Waite and Pinese, 1991). In South Africa, the tea red mite was Coccinellids, especially Stethorus madecassus described by Nietner (1861, unpublished) Chazeau in the Malagasy Republic, were found from Sri Lanka (De Villiers, 1998). It is known feeding on eggs and other stages of O. coffeae. to attack avocado, cashew nuts, citrus, coffee, The larvae of Chrysopa spp. also attack the guava, mango, tea, cotton, grape, mulberry, active stages of this mite (Blommers and protea, rubber, strawberry, and about 30 other Gutierrez, 1975). plant species (Meyer, 1987). O. coffeae prefers In South Africa, chemical control of the the dorsal surface of avocado leaves but will tea red mite is for the most part unnecessary inhabit both sides during severe infestations. since its natural enemies keep its numbers In general, these mites favour the older, low. In Australia, when necessary, chemical firmer leaves (Meyer, 1987). Injury to plants is control is practised with sprays of fenbutatin first seen as a yellowish spotting along the oxide. Avocados can withstand approx. 20% midrib and veins of leaves and occasionally leaf bronzing before action needs to be taken on the petioles. As the mites continue to (Waite and Pinese, 1991). feed, these patches darken, until the entire leaf becomes deeply bronzed and necrotic, Avocado brown mite, often falling from the plant; thus growth is Oligonychus punicae (Hirst) retarded (Meyer, 1987; De Villiers, 1998). A heavy infestation of tea red mite occur- In Mexico, Oligonychus punicae (Hirst) and red on young avocado trees in the Nelspruit Oligonychus perseae (Tuttle, Baker and area after 120 ha of Pinkerton avocados had Abbatiello) appear to be the most important been sprayed with wettable sulphur (De mite species. O. punicae are found on the Villiers, 1998). In Australia, the tea red spider leaf’s upper side, causing leaf bronzing and mite is a common pest of avocados in Queens- a reduction in photosynthetic activity. In Cal- land and northern NSW, usually appearing ifornia, the avocado brown mite, O. punicae, during the autumn. This may be a result of the and the six-spotted mite, Eotetranychus sex- numerous sprayings of endosulfan, applied maculatus (Riley), are pests of avocados for the control of fruitspotting bugs. (McMurtry, 1985a; Bailey and Olsen, 1990a; Das (1955) reported that the mite’s life Aponte and McMurtry, 1997a,b). cycle on tea in India lasts 9–12 days in summer In Mexico, different cultivars show differ- and about 30 days in winter. Under these con- ent responses to O. punicae. One generation ditions, 22 generations can occur annually. can be obtained in 15.4 days when the average These mites are spread by wind, animals, temperature is 22°C (Hernandez et al., 2000). implements and labourers (Meyer, 1987). O. punicae densities are reduced under low

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temperature and high humidity. The same The reproductive period ranged from 5 to 14 authors believe that O. punicae originated in days at all temperatures tested. The estimated the south of Mexico and north of Guatemala. rm values showed that this species can only O. punicae infests 71% of the avocado orchards grow at 25°C (Ramirez et al., 1993). Martinez in the area of Uruapan, Michoacan. Coria- (1989) reported that O. perseae had developed Avalos (1993) recommends applying sulphur resistance to organophosphates in the states and propargite three or four times during of Morelos, Mexico and Michoacan. the dry season, between December and May. According to Hernandez et al. (2000), no Reyes and Salgado (1994) demonstrated that known specific predators of O. perseae have avocado cultivars 175PLS, 54PLS, 131PLS, been reported to date. Hernandez et al. (2000) 120PLS, 18PLS, 137PLS and 30PLS show suggested the removal of fallen foliage as a some tolerance to O. punicae, while Colin and cultural control method. However, this tactic Rubi (1992) indicated that cultivars Colinmex does not appear to be very practical. Use of and 148PLS are moderately susceptible. The hot-pepper extracts did not afford any type cultivars Rincon and Fuerte have been consid- of mite control in Mexico (Reyes et al., ered tolerant to the mite species by Ortega and 1995). Andrade (1988) found the best chemical Ewart (1972; cited in Gallegos, 1983). control with organophosphates and the worst The phytoseiid mites, Amblyseius limo- with sulphur. nicus Garman and McGregor and Typhlo- The following predacious mites were dromus floridanus Muma are considered released and established in southern Califor- to have good predatory potential against nia against the persea mite: Galendromus anne- O. punicae (McMurtry and Johnson, 1966; ctens (DeLeon), G. helveolus (Chant), G. pilosus McMurtry, 1985a,b). (Chant), G. porresi (McMurtry), Iphiseius degen- erans (Berlese), Iphiseiodes zuluagai Denmark Persea mite, Oligonychus perseae Tuttle, and Muma, Metaseiulus occidentalis (Nesbitt), Baker and Abbatiello Neoseiulus californicus (McGregor) and Typhlo- dromus rickeri Chant. Additionally, the native The persea mite, Oligonychus perseae Tuttle, Euseius hibisci Chant was released. Stethorus Baker and Abbatiello (previously misidenti- picipes Casey (Coleoptera: Coccinellidae) is fied as Oligonychus peruvianus (McGregor)), is important in controlling the avocado brown found in Mexico and Costa Rica. It was found mite but does not suppress outbreaks of in California in 1990 damaging the avocado persea mite. In addition, the six-spotted thrips variety Hass, and to a lesser extent the variet- (Thysanoptera: Thripidae), a specialized pre- ies Gwen and Reed, whereas no damage dator of the spider mite, is commonly found was inflicted on varieties Fuerte, Zutano feeding in persea mite nests (Hoddle, 1998). and Bacon. O. perseae feed in colonies under protective webbing along veins and midribs Avocado red mite, Oligonychus on the undersides of leaves, producing yothersi (McGregor) necrotic, purplish, irregular spots (Hoddle, 1998). Recently O. perseae was found in In Florida, the avocado red mite is a common avocado orchards of western Galilee, Israel pest of avocados. Feeding is initially confined (E. Swirski, personal observation) The mites to the upper surface of avocado leaves; it are covered by a whitish cobweb, where they is found first along the midrib, then along spend most of their lives. Their damage is secondary leaf veins. The areas along the characterized by almost geometrical necrosis veins become reddish brown. During heavy of areas close to the secondary and mid-veins. infestations, leaves can be covered with Salinas (1992) determined the life cycle of this mites’ cast skins. Damage to the leaf area species to be 20.95 days under laboratory is regularly observed from October through conditions. Ramirez et al. (1993) calculated February, causing up to a 30% reduction in life and fecundity tables for O. perseae at leaf photosynthetic activity. Leaves affected 10 and 14°C. Development from the egg to by this mite regularly drop earlier (45–60 adult emergence required 227 degree-days. days after infestation) than their uninfested

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counterparts. This mite is an occasional pest variety Pinkerton, especially in drier areas in some orchards and is seldom observed in (Swirski et al., 1998). others. Periodic inspections are recommended during December, January and Feb- ruary. Control measures may be started when Eriophyidae the population reaches six or more mites per leaf (Peña and Johnson, 1999). The duration In Brazil, the mite Tegolophus perseaeflorae of the life stages varies from 14 to 15 days. (Keifer, 1969) injures flowers and contributes Females are capable of laying 40–50 eggs to flower drop. In Florida, T. perseaflorae is during their life span (Peña and Johnson, observed in developing buds. Peña and Den- 1999). In Florida, few miticides are registered mark (1996) related the presence of this mite for use on avocados when fruit is present. to excessive flower drop and fruit defor- Sulphur or oil emulsion sprays are recom- mation. The mites cause necrotic spots, and mended (Peña and Johnson, 1999). subcircular and irregular openings on apical leaves. Feeding by this mite may cause fruit Six-spotted mite, Eotetranychus deformation and discoloration. The adult sexmaculatus (Riley) avocado bud mite has a yellowish appear- The six-spotted mite was introduced into ance. Its life cycle has not been determined. Queensland in 1986, apparently on budwood Avocado bud mite populations begin to that had been illegally imported from Cali- increase from March to May (Peña and John- fornia. When its presence became known, an son, 1999). Medina et al. (1978) recommend eradication campaign was mounted and all chemical applications to reduce their density. known infested plantings were treated with The eriophyid Calepitrimerus muesebecki miticide. The infestation did not spread and it Keifer causes bronzing and virus-like chlorotic has not been a problem since. The phytoseiid damage to avocado foliage in Guatemala; the Phytoseiulus persimilis Athias-Henriot was mite may cause damage while remaining found among mite colonies on mature avo- hidden inside the vegetative buds (Velasquez cado trees. It is suspected that this predator, and Santizo, 1992). along with Stethorus spp. and other phytoseiids, has suppressed the populations to undetectable levels (Waite and Pinese, 1991). Tarsonemidae E. sexmaculatus infests avocados in New Zea- land, but chemical control is rarely necessary The broad mite, Polyphagotarsonemus latus (D. Steven, 1997, personal communication). (Banks) (Tarsonemidae), sometimes attacks avocado seedlings in glasshouses, causing Paratetranychus spp., Panonychus citri rolling and browning of the young leaves, (McGregor), Tetranychus cinnabarinus severe harm to the foliage of apical buds, Boisduval, Tetranychus urticae Koch development of shoots by lateral buds, as well as dwarfing of the seedlings (Waite and In Peru, Paratetranychus spp. and Panonychus Pinese, 1991; Swirski et al., 1998). citri (McGregor) mites affect avocado when it is grown together with citrus trees (Wolfe et al., 1969). In Israel, red spider mites are rarely found in avocado orchards; however, Class Insecta in the early 1980s, the carmine mite T. cinnabarinus and the two-spotted mite T. urticae ORDER ISOPTERA were found in some avocado plots adjacent to cotton fields, which were treated aerially Termitidae with synthetic pyrethroids. Occasionally, the oriental spider mite Anychus orientalis Klein Africa has a large number of termite causes considerable damage to leaves of species, many of which are present in

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avocado-growing areas. They live in nests plays a large role in limiting the establishment and feed on the cellulose in wood, grass, of new nests (Gouse et al., 1998). In South humus and other plant matter. In avocado Africa, the following control measures are orchards, termites destroy mainly the roots recommended. and lower stems of young trees, but they may also cause ringbark and kill large trees. PRETREATMENT OF NEW ORCHARDS It is advis- Termites are therefore more destructive able to find and destroy termite nests in and during the first year after planting, as the around the area in which a new orchard is to trees become less susceptible once they are be established. This should be done before soil well established (Webb, 1974). preparations commence. Since termites can In Africa, termite mounds are often work up to or even more than 100 m from large and occupy considerable surface area. their nests, it is important that the nests be Macrotermes spp. mounds often exceed 4 m in destroyed in adjacent areas as well. height. In some areas, Microhodotermes spp. According to Gouse et al. (1998), it is often build mounds which cover up to 25% of the difficult to find the nests of Odontotermes ground surface. badius (Havil), especially after the soil has been The largest contribution to our know- prepared. The nests can occur from 300 mm ledge of the taxonomy, biology, distribution to more than 3 m deep in the soil (Hartwig, and ecology of termites in Africa was made by 1966). The termite mounds are usually only Coaton and Sheasby (e.g. Coaton, 1971, 1974; slightly raised, 100–300 mm in height and Coaton and Sheasby, 1972, 1978) and Skaife approximately 1.5 m in diameter above (1956). Ruelle (1985) provided a synopsis of ground. The nest of O. badius can be detected our knowledge of the termites of southern because when the termites enlarge it, the Africa. discarded soil is cemented together to form Aspects of termite control have been small compact heaps, close to the nest. During studied by a large number of researchers humid weather, numerous small white mush- (Skaife, 1956; Nel, 1961; Sands, 1962; Hartwig, rooms can be seen on these sites for a few days. 1966; Coaton and Sheasby, 1972). There are A product containing carbon bisulphide, three groups of termites that are of economic cresylic acid and para-dichlorobenzene may importance in avocado orchards, all in the be used for nest fumigation. family Termitidae. Some nests of Odontotermes spp. are characterized by air pipes, or ‘chimneys’ of 1. Large fungus growers in the genera clay. Mactrotermes spp. make heaps above the Macrotermes and Odontotermes. ground with a thick wall. Ancis-trotermes and 2. Small fungus growers in the genera Microtermes make small underground nests Microtermes, Allodontotermes and Ancistro- that are spread over a wide area. There are no termes. signs above the ground to betray their nests. 3. Carton nest builders of the genus Micro- The nests of Microcerotermes spp. are also com- cerotermes. Members of this group are of less pletely underground (Gouse et al., 1998). importance than those of the other two The nests of small fungus-grower ter- groups. mites are small and spread over a wide under- Natural enemies of termites include ants, ground area. These termites are very common especially of the genera Dorylus and Anoplo- and can probably be found in many of the lepis. Fungi and parasitic nematodes seem to tropical and subtropical orchards in Africa. play an important role in causing termite nests The small fungus-grower termites prefer dead to die out. Anteaters dig the nests open and plant material. Therefore, their presence is not can totally destroy them; various birds scratch always a problem, especially where mulching open the protective clay passageways and eat is practised. However, precautions should be the exposed termites. An exceptionally large taken to ensure that the trees are not exposed variety of animals, including insects, birds to serious stress (Gouse et al., 1998). and mammals, feed on winged termites that The winged adults or alates that fly out of fly out after the rains. This natural mortality the nests during the late afternoon after spring

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rains usually come out of passages that open females, which are dark blue to black (Clausen directly into the central nest cavity, making and Berry, 1932; Quayle, 1938; Ebeling, 1959). these most suitable for fumigation (Gouse The general colour of the wings is broken by et al., 1998). lightish spots on the edges. Ebeling (1959) In some countries in Africa, carbosulfan is states that a female lays more than 100 eggs registered to protect newly planted trees. If no and that there can be 35–50 eggs per spiral. treatments have been applied to the soil and The minimum life cycle from egg to egg is the plants are attacked by termites, 200 g l−1 6–9 weeks (Clausen and Berry, 1932). In imidacloprid SL (Confidor) can be applied South Africa, during the early summer, the by soil drench or trunk application to protect egg stage lasts 18 days and the total life the trees against termite attacks (Gouse et al., cycle about 80 days (Bedford, 1998b). Adult 1998). numbers peak in October, with smaller peaks It has been shown that once the leaves in early December and February/March and and flush of a young tree have started to wilt considerable overlapping of stages. as a result of termite damage, subsequent The parasitoid, Eretmocerus serius Sil- control of this pest will not be able to save that vestri, has been introduced and successfully specific tree. However, if chemical control established in many countries for the bio- is then applied to the adjacent trees, many logical control of A. woglumi.Upto72%of of those that have not yet shown wilting the pupae of A. woglumi were parasitized in symptoms can still be saved. citrus orchards in South Africa (Bedford and Thomas, 1965). In Mexico. the species Trialeurodes vaporariorum (Westwood), Tetraleurodes spp. and ORDER HEMIPTERA – SUBORDER Paraleyrodes perseae Quantaince have little HOMOPTERA importance in avocado. Tetraleurodes is more abundant during the months of June through Aleyrodidae November. During heavy attacks, leaves from the lower tree canopy become weak and The citrus blackfly, Aleurocanthus woglumi the injury may cause defoliation. P. perseae is Ashby, is a minor pest of avocado. According found close to the mid-vein of the leaves and to Bedford (1998b), the original home of the its feeding causes chlorotic circular spots on citrus blackfly is India, Ceylon and the Philip- them. Heavy damage may be associated with pines. It also occurs in the West Indies, Costa low flower production and defoliation. Peaks Rica, Canal Zone, Mexico and Kenya. The are observed between June and November citrus blackfly breeds on 75 different plants, (Coria-Avalos, 1993). In Cuba, Aleurodicus including avocado, banana, citrus, coffee, cardini (Back.) is recorded as a pest of grape, mango and persimmon (Bosman, avocados; its biocontrol agents include Baccha 1959). The citrus blackfly is an important clavata (F.), B. parvicornis Loew (Syrphidae), pest of citrus in many countries. It produces Chrysopa sp. (Chrysopidae), Isodromus iceryae honeydew, on which sooty mould grows and (How.) and Carthasis distinctus (Harris) stains the fruit, leaves and branches. Severe (Nabidae) (Brunner et al., 1975). infestations stunt tree growth and inhibit In Israel, the Japanese bayberry whitefly, blossom formation (Van den Berg and De Parabemisia myricae (Kuwana), was discovered Villiers, 1987a; Bedford, 1998c). in 1978, causing heavy damage to avocado The egg of the citrus blackfly is creamy and citrus trees (Sternlicht, 1979). Local pre- white when freshly laid, turning brown with dacious mites of the family Phytoseiidae, age. It has a short pedicel which attaches it to lacewings (Neuroptera), lady beetles (Coc- the leaf. Eggs are laid on the underside of the cinellidae), predacious bugs of the family leaves in characteristic spirals. The nymphs Anthocoridae and parasitic wasps were not and the pupae are sedentary, dark brown effective. Thus, the parasitoid Eretmocerus to black. Adults are just over 1 mm in length. debachi Rose and Rosen (Aphelinidae) The males are light blue and smaller than the was imported from California, successfuly

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Pests and Pollinators of Avocado 229

established and eventually controlled P. and apterous females are found, whereas myricae (Rose and DeBach, 1992). Other exotic males are absent. Females are yellow-green to natural enemies, Eretmocerus sp., Encarsia sp. green, or almost black depending on their host (Aphelinidae) (from Japan), the lady beetles plant, with a body length between 1.2 and Nephaspis amnicola Wingo and Delphastus 2.0 mm (Avidov and Harpaz, 1969). Live pusillus (Le Conte) (from Hawaii), the beetle young aphids are produced by both winged Cybocephalus binotatus Grouvelle (Cybocep- and apterous females. The females may live halidae) and the fungus Aschersonia aleyrodis for 2 to 3 weeks and produce two or more Webber were released in numerous avocado offspring each day (Hill, 1975). Ebeling (1959) and citrus groves but probably did not refers to a nymphal period of 3–20 days. become established (Swirski et al., 1987). In The aphelinid, Aphelinus sp., attacks Israel, outbreaks of the Japanese bayberry A. gossypii in South Africa (Prinsloo and whitefly were recorded in 1992 in some Neser, 1994). avocado orchards of western Galilee. These outbreaks were probably caused by drift Green peach aphid, Myzus persicae (Sulzer) of baits containing insecticides (malathion), which were applied aerially against the The green peach aphid was described by Mediterranean fruit fly, Ceratitis capitata Sulzer in 1776 (Müller and Schöll, 1958). It Wiedemann (Trypetidae), in adjacent groves is cosmopolitan and was recorded in Africa of citrus, deciduous or subtropical fruit trees. as early as 1801 (Theobald, 1914). In South E. debachi was re-established and controlled Africa it has been recorded on many plant the pest population (Swirski et al., 1998). species representing 55 plant families (Millar, Five species of Aleurodidae attack avo- 1994). These include its primary host, peach, cado in California: Aleurodicus dugessii Cocke- as well as avocado, granadilla and papaya. rell, Trialeurodes vaporariorum (Westwood), M. persicae feeds on the flowers and young Tetraleurodes morii (Quaintance), Paraleyrodes leaves of avocado. The damage caused by mineii Iaccarino and Tetraleurodes perseae sucking sap and by fouling the plants with Nakahara (Soliman and Hoddle, 1998; Faber cast skins, honeydew and black sooty mould and Philips, 2001). The last species was recently is for the most part insignificant (Daiber, found in avocado plantations in Israel. 1992). It also transmits viral diseases in many other plants (Van den Berg and De Villiers, 1987a). Aphididae The aphids are soft-bodied, slow-moving insects, 1.5–2.5 mm in length, with long, Cotton aphid, Aphis gossypii Glover spindly legs. Winged and apterous, sexual and asexual forms occur. The wingless, asex- A. gossypii has worldwide distribution ual females are light green with fairly long, (Schwarz, 1998; Millar, 1994). In Israel, it is green cornicles. The winged asexual females found on young foliage and occasionally on have a dark head and thorax, a dark patch inflorescences of two avocado varieties, Nabal on the upper side of the abdomen and dark and Horshim (Swirski et al., 1991b). Accord- cornicles. The sexual males are winged and ing to Avidov and Harpaz (1969), damage superficially similar to the winged asexual caused by the cotton aphid is characterized females. The sexual females are apterous. by foliar and floral discoloration and defor- In tropical and subtropical areas, the mities caused by the aphid’s toxic saliva, green peach aphid lives asexually throughout resulting in stunted development of infested the year but sexual forms develop in areas plants, and growth of extensive layers of with cold winters. In the colder areas, some sooty mould on the excreted honeydew. of the winged asexual females leave various The nymphs are greenish to brownish vegetable and other hosts and fly to the with a very distinctive appearance, being primary host, which is peach (Daiber, 1992). spotted with an exudation of powdery wax Two parasitoid species, Aphelinus (Van den Berg and De Villiers, 1987a). Winged abdominalis (Dalman) and Aphelinus asychis

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Walker (Aphelinidae), have been bred from In Israel, during the 1960s and 1970s, avo- M. persicae (Prinsloo and Neser, 1994). Accord- cado orchards adjacent to cotton fields were ing to Daiber (1992), the green peach aphid is heavily damaged by the long-tailed mealy- attacked by ladybird beetles and by a fungal bug, P. longispinus. Drift of broad-spectrum disease. Control of the green peach aphid on insecticides from aerially sprayed fields killed avocado is seldom necessary. In some coun- its natural enemies, thereby interfering with tries in Africa, mercaptothion is registered for the biological equilibrium and resulting in the control of aphids on avocado, granadilla severe outbreaks of mealybug. Additionally, and papaya. females of the honeydew moth, Cryptoblabes gnidiella Milliere, were attracted to the honeydew of the mealybug and their caterpillars Pseudococcidae nibbled at the fruit (Ben Yehuda, 1990; Wysoki et al., 1992). The problem was solved by Long-tailed mealybug – Pseudococcus drastically limiting aerial applications of longispinus (Targioni-Tozzetti), broad-spectrum insecticides within 200 m of Pseudococcus nipae (Maskell), avocado orchards, and by releasing the para- Planococcus lilacinti Cockerell sitic wasps Arhopoideus peregrinus Compere (= Hungariella peregrina) in 1954 and Anagyrus The long-tailed mealybug, P. longispinus, has fusciventris (Girault) introduced from Austra- a cosmopolitan distribution (Ebeling, 1959; lia in 1971 (Swirski et al., 1980, 1998). Hattingh et al., 1998). In temperate regions it In Cuba, several biological control agents is mostly unable to pass the winter outdoors are used to control the mealybug Pseudococcus but may still be a pest in protected environ- nipae (Maskell): Scymnus bahamicus Csy ments and glasshouses. In many parts of (Coccinellidae), Lobodiplosis pseudococci (Felt), Africa, the long-tailed mealybug is a poten- Pseudoaphycus utilis (Timberlake), Verticillium tially serious pest in all areas where avocados lecanii (Zimmerman) and Empusa fresenii are cultivated. Nowak (Zygomycota). The long-tailed mealybug has a soft, oval, In the Philippines, Planococcus lilacinti segmented body. The distinctions between Cockerell infests young shoots and fruit the head, thorax and abdomen are not clear. peduncles. Heavy infestations may cause fruit The life cycle of P. longispinus lasts about to drop but the pest is generally of minor 4 weeks in summer and several months in concern (Cendana et al., 1984). winter, with three overlapping generations per year (De Villiers et al., 1987d). Both sexes of the mealybug pass through Coccidae three nymphal instars. After the third instar, the female transforms into an adult while the White wax scale, Ceroplastes male forms a flimsy, cottony cocoon in which destructor Newstead the pupa forms and the adult develops. The adult male has one pair of wings and two C. destructor has been collected in South long waxy anal filaments (Ebeling, 1959). The Africa from avocado (Munro and Fouché, long-tailed mealybug is viviparous. 1936). It has also been recorded on coffee and All stages of the mealybug, except for the persimmon from Kenya and Uganda (Hill, male pupa, are motile and often move slowly 1975). However, the most important host in from one area to another. Mealybugs are usu- Africa is citrus. In Australia, the white wax ally held at low numbers by natural enemies. scale Gascardia destructor (Newstead), Indian Most outbreaks are associated with chemical white wax scale Ceroplastes ceriferus disruption of these enemies. Furthermore, (Fabricius) and pink wax scale Ceroplastes ants are attracted to the honeydew that rubens Maskell are minor pests that rarely mealybugs excrete. By protecting them warrant spraying (Waite and Pinese, 1991). against natural enemies, ants may also help According to Cilliers (1998), the wax of cause a mealybug outbreak. the adult female C. destructor is shiny white

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with two external bands of pulverized wax producing thin-walled eggs that hatch within leading upwards from the stigmal grooves. a few minutes (Annecke, 1966). Crawlers The stigmal groove has about 45 spines, settle on leaves and twigs. Feeding sites are of which the middle subconical spine is the often selected on the main or subsidiary veins largest. The eggs are brick red and smooth on both the ventral and dorsal surfaces when laid. According to Zeck (1932), C. of leaves. The first instar lasts from 15 to destructor lays about 3000 eggs. The crawlers 46 days, body length increasing from 0.37 to are brick red, and settle along the midribs or 0.41 mm (mean 0.39 mm). The second instar main veins of the dorsal surface of the leaves. lasts from 10 to 57 days and increases from Very soon after the first moult, C. destructor 0.80 to 1.01 mm (0.92 mm). This instar is migrates from the leaves to the twigs (Cilliers, characterized by the formation of a longitudi- 1967). The third moult occurs about 3 months nal dorsal row of minute ventral columns after the crawler has settled. There is a pre- of glassy wax. The duration of the pre- oviposition period of about 8 months. oviposition period is 27–74 days, the body Observations of C. destructor in South length increasing from 1.26 to 1.82 mm Africa are largely restricted to Melia azedarach, (1.52 mm) before eggs are produced and on which it goes through one generation a from 1.52 to 2.70 mm (2.07 mm) afterwards. year, the eggs being produced from October to No further moult ensues; a pre-oviposition December. This unisexual species has three period of 1–2 months intervenes (Annecke, moults on M. azedarach (Cilliers, 1967). A total 1966). The sexually mature female may reach of 24 primary parasitoids attack this wax scale a body length of 5 mm (Bodenheimer, 1951; in South Africa (Cilliers, 1967; Snowball, 1969; Avidov and Harpaz, 1969). A mean 73 eggs, Annecke and Insley, 1971; Prinsloo, 1984). but up to 200, are produced in the pest’s life- Two secondary parasitoids have also been time (Bodenheimer, 1951). Although males recorded. Three important predators of have been described by Newstead (1903) the white wax scale are Coccothera spissana from the date palm, Phoenix dactylifera,in Zell. (Olethreutidae), Eublemma costimacula England, the occurrence of males is unknown Saalm. and E. scitula Rambur (Noctuidae) in South Africa (Annecke and Georgala, (Cilliers, 1998). In Australia, Paraceraptrocerus 1978). nyasicus (Compere) provides good control of In spring, crawlers of soft brown scale C. destructor. tend to move outwards in the tree (Annecke and Georgala, 1978). According to Smith et al. Soft brown scale, Coccus hesperidum L. (1997), only the egg-producing adults are sedentary, since the nymphs and non-producing The soft brown scale is a cosmopolitan pest of adults of the soft brown scale may move from many tropical and subtropical plants. Infesta- one feeding position to another, especially if tions on citrus are usually the consequence feeding conditions deteriorate. of non-judicious insecticidal usage and/or Ants of various species are invariably of uncontrolled ant activity (Annecke and associated with infestations of this pest. The Georgala, 1978). These latter authors indi- brown house ant, Pheidole megacephala (F.), cated that infestations on other plants could the pugnacious ant, Anoplolepis custodiens have been caused by the same factors. Munro (Smith), and related species are commonly and Fouché (1936) list guava, mango, papaya encountered. In late summer, the growth of and many others, including citrus, as host sooty mould, which may cause extensive plants. Avocado (Ebeling, 1950) and grana- blackening of the foliage fruit, often pin- dilla (De Villiers and Van den Berg, 1987b) points small populations in a tree (Annecke are also attacked. In avocado, the direct loss and Georgala, 1978). of fruit due to soft brown scale appears to There is evidence of three overlapping be small. However, fruit may be stained by generations per year on citrus in South Africa. sooty mould deposits and consequently Surges of crawlers seem to appear in mid- downgraded. On English ivy, Hedera helix,at November and early February, and a third one 22°C, the parent females are ovoviviparous, probably in May (Annecke, 1959, 1966).

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Annecke (1959, 1964) recorded 22 pri- the scale was rather poor on ‘Fuerte’, ‘Hor- mary and six secondary hymenopterous shim’ and ‘Wurz’, but higher on ‘Ettinger’, parasitoids from soft brown scale. A number ‘Pinkerton’ and ‘Reed’ (De Meijer et al., 1989). of predators of soft brown scale have been P. pyriformis feeds on avocado, guava, recorded (Searle, 1964). Predators seem to be Aphanamixis polystachya (= A. moora rohituka) of greater importance at times of soft brown (De Villiers, 1981) and citrus (Bedford, 1978a). scale outbreaks and may be of lesser value in According to De Villiers (1989), a steady maintaining the scale at low levels for long increase in the occurrence of the heart- periods. shaped scale was reported from 1986 to 1989 Although ant control is usually not a on avocado in parts of South Africa. standard recommendation in orchards of The scale secretes excessive quantities tropical non-citrus and subtropical crops of honeydew on which sooty mould grows, (Annecke and Georgala, 1978; Bedford, staining the fruit leaves (Du Toit and De 1998b), it is regarded as essential for suppress- Villiers, 1988, 1990; Steyn et al., 1994; De ing soft brown scale in orchards where it Villiers, 2001d). Furthermore, photosynthesis occurs. Soft brown scale can be chemically is affected, leading to crop yield reductions controlled on avocado by using 500 g l−1 (Ray and Williams, 1982). Leaf drop can occur mercaptothion EC at 250 g 100 l−1 water or with heavy infestations. 250 g kg−1 mercaptothion WP at 500 g 100 l−1 Du Toit et al. (1991) defined the following water (Krause et al., 1996). These latter authors morphological stages: egg, crawler stage (first recommend spot-spraying individual trees instar), second instar, third instar, A− female with large populations of C. hesperidum, and (unsclerotized females without eggs, ring following up with ant control. stage), A+ female (sclerotized females with eggs) (Plate 51). The female lays about 200 or Pyriform scale, Protopulvinaria pyriformis 300 eggs which are kept in a white, woolly (Cockerell) secretion beneath her body. According to Du Toit et al. (1991), the eggs are oval-shaped and Protopulvinaria pyriformis has a cosmopolitan light yellow. The first-to third-instarscales are distribution (Wysoki, 1987; Du Toit and De flat, oval-shaped and light green, with mean Villiers, 1988) In Israel, P. pyriformis was first lengths of 0.35, 0.73 and 1.12 mm, respectively recorded in 1980 (Ben-Dov and Amitai, 1980), (Ray and Williams, 1982). The adult egg-lay- and is now found in almost all areas of the ing female (A+) is about 3 mm in length and country. In Africa, the pyriform scale (also reddish brown with prominent radial stripes called the heart-shaped scale), was first recor- dorsally. A white woolly ovisac is visible ded on avocado in 1916 at Pietermaritzburg, around the hind margin of the A+ females. No KwaZulu-Natal (Brain, 1920). P. pyriformis is males have yet been observed in South Africa. the most damaging insect affecting avocado In Florida, males have been recorded (Ebeling, in Peru (Wolfe et al., 1969) and sometimes 1959). In the laboratory, at 27°C and 70% RH, causes serious damage to avocado trees in the life cycle of the heart-shaped scale on Florida (Ebeling, 1959) and to citrus and avocado seedlings (W.J. Du Toit, 1994, unpub- avocado trees in Spain (Del Rivero, 1966). A lished) was as follows: the mean duration of preference for certain avocado cultivars was the first instar (which includes the crawler observed (De Villiers and Van den Berg, stage) was 10.5 days, the second instar lasted 1987b; Wysoki, 1987). ‘Nabal’ is the most 17.5 days, the third instar 24.5 days, the A− susceptible cultivar to this scale, followed female stage 28.0 days, and the A+ female by cultivars. ‘Ein Vered’, ‘Reed’, ‘Hass’ and stage (including the ring stage) 45.5 days. Two ‘Fuerte’, whereas ‘Ettinger’ is attacked when generations are completed per year on avo- located close to infested trees of the suscepti- cado in Nelspruit, South Africa (De Villiers, ble cultivars. In laboratory trials, the pyriform 1989), whereas in Israel, two generations scale completed development and reproduced appear annually – a winter generation with a on ‘Nabal’ and ‘Ein Vered’ seedlings, and to a peak in November/December and a summer lesser extent on those of ‘Hass’. Survival of generation with a high level in June/July

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(Hadar, 1993). In South Africa, peaks of the (Zimmerman) (Hadar, 1993) were unable to first instar were reached in November and curb populations of pyriform scale to below March, and peaks of adults in October and economic thresholds. Thus, efforts were March. The winter generation lasted about exerted to import various natural enemies. 7 months from egg to adult; the summer Metaphycus swirskii (imported from Kenya), generation lasted 5 months. P. pyriformis feeds initially the most abundant parasite, was soon on the ventral side of the leaves. Fruits are replaced by Metaphycus stanleyi (imported normally not attacked (De Villiers, 2001d). from the USA, South Africa and Spain), which Avocado cultivars favoured by the scale in is today the dominant natural enemy of the South Africa in descending order are Hass, pyriform scale in Israel. Metaphycus helvolus Collinson, Ryan, Fuerte and Edranol (De (imported from the USA) is rare in avocado Villiers and Robertson, 1988). orchards and M. galbus (from South Africa) The following natural enemies of the probably failed to become established. Two heart-shaped scale have been identified in lady beetles were imported from Spain: Crypto- South Africa (Robertson and De Villiers, laemus montrouzieri Mulsant is sporadically 1986): Metaphycus galbus Annecke, Metaphycus found in avocado orchards, whereas Nephus helvolus (Compere), Metaphycus stanleyi peyerimhoffi Sicard is very rare. The two sec- (Compere) (Encyrtidae), Coccophagus basalis ondary parasites Marietta javensis (Howard) Compere, Coccophagus pulvinariae Compere and Pachyneuron concolor (Forster) have an (Aphelididae) and Tetrastichus sp. (Eulo- adverse effect on the efficiency of Metaphycus phidae). Two hyperparasitoids, Cheiloneurus spp. In some avocado plots, 70% of the total cyononotus Waterston (Encyrtidae) and parasite fauna may consist of these two Marietta javensis (Howard) (Aphelinidae), secondary parasites. Population studies of the were also found. Predators included active parasitization of the scale by M. stanleyi Chilocorus angolensis Crotch and Hyperaspis showed an increase in September, with high senegalensis hottentota Mulsant. levels during the winter, a peak in May and Du Toit et al. (1991) found that, on aver- a decline in summer. The high rates of encap- age, 70% parasitism occurs in the adult female sulation of Metaphycus eggs by the pyriform stage, 4% in the second instar, 14% in the third scale during the summer may interfere with instar. Metaphycus spp. were dominant on efficient biocontrol of the pest (Blumberg and P. pyriformis during the late summer and Blumberg, 1991; Hadar, 1993). In Peru, bio- autumn, but were replaced in winter by logical control of this pest can be achieved by Coccophagus spp. and Tetrastichus sp. Accord- releasing the wasp Microterys flavius. The site, ing to Du Toit et al. (1991), Marietta javensis duration and rate of oviposition, as well as (Howard) has a negative influence on the host marking and preference of host stages parasitoid complex and, in Israel, attacks the in the various species of Metaphycus, were two Metaphycus species, M. stanleyi Compere studied by Hadar (1993). Since local and exotic and M. swirskii Annecke and Mynhardt. Since natural enemies are not sufficiently effective local and introduced parasitoids are not at suppressing the pyriform scale populations, sufficiently effective at controlling the scale mineral oil – the selective scalicide – is recom- population, selective scalicides such as oil are mended. It kills the three nymphal instars of used, killing the nymphal stages of the pest the pest, but does not affect the ovipositing but not the ovipositing females (Swirski et al., females. Oil sprays are likely to produce 1988). In Israel, the parasitic wasps Microterys satisfactory results if applied in December/ flavus (Howard), Metaphycus flavus Howard January (or January/February) and in July/ (Encyrtidae), Coccophagus lycimnia Walker August, when the pest populations consist (Aphelinidae), predators Chilocorus bipustu- mainly of young nymphal instars (Hadar, latus L., Oenopia (Synharmonia) conglobata L., 1993). Only heavily infested trees are treated Scymnus flavicollis Redtenbacher (lady beetles, with broad-spectrum scalicides (Wolfe et al., Coccinellidae), Anisochrysa (Chrysoperla) carnea 1969; Swirski et al., 1998). Stephens (green lacewings, Chrysopidae), A survey carried out in a heart- spiders and the fungus Verticillium lecanii shaped scale-infested avocado orchard near

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Nelspruit, South Africa, demonstrated that 370 host plants in Florida. Davidson and trees nearest to a dust road had the highest Miller (1990) state that H. lataniae feeds on scale infestation (Robertson and De Villiers, ornamentals from 78 families of 278 genera. 1986; E.C.G. Bedford, 1945, unpublished). In According to Ebeling (1959), the rostralis South Africa, buprofezin WP at 30 g 100 l−1 of H. lataniae irritates the flesh of ‘Fuerte’ water is registered as a full-cover application avocado and possibly other thin-skinned when first-generation crawlers become avocado cultivars. This is indicated by active. The addition of an adjuvant, e.g. nodules adhering to the inside of the peel with Agral, is advised (Krause et al., 1996). A corresponding depressions in the flesh of ripe thorough wetting of the inside of the tree fruit. The scale attacks the branches or twigs, canopy, especially the ventral sides of leaves and fruit of avocado. Infested fruit is leaves, is essential for effective control (Du degraded or culled. In South Africa, heavy Toit and De Villiers, 1988). infestations were observed on fruit of cv. Hass, but smooth-skinned cultivars are also susceptible to this scale insect (De Villiers, Diaspididae 2001c). A heavier scale infestation on ‘Hass’ fruit hanging near the ground than higher up in the tree was reported (Steyn, 2001a). Avocado scale, Fiorinia fioriniae The adults are variable: on leaves they are (Targioni-Tozzetti) grey to white, circular and convex; on stems The avocado scale F. fioriniae has been found they are brown and slightly convex. The exuvia on avocados in Florida, Hawaii, the continen- is subcentral and yellow-brown (Davidson tal USA and the West Indies (Ebeling, 1959). and Miller, 1990). Males are not always In South Africa, it is regarded as a minor present (Davidson and Miller, 1990). pest of avocado and other crops (Munro H. lataniae is unisexual in southern Cali- and Fouché, 1936; De Villiers and Van den fornia (McKenzie, 1935) and Israel (Gerson Berg, 1987b; Erichsen and Schoeman, 1992; and Zor, 1973), and bisexual in Maryland Claassens, 1994). On avocado, the avocado (Stoetzel and Davidson, 1974). Annually, scale attacks the leaves and fruit. Small latania scale completes two generations in brown spots develop where nymphs feed, Maryland (Stoetzel and Davidson, 1974), which on ‘Hass’ fruit, fade as the fruit colour three generations in Egypt (El-Minshawy develops (Claassens, 1994). et al., 1971) and four generations in Israel The female scales are oval, shield-shaped, (Gerson and Zor, 1973). From egg to egg- with a thin, translucent covering. They are laying female takes 56–65 days in southern brownish yellow to orange-brown, 1.0–1.3 mm California (McKenzie, 1935). In Australia, long (De Villiers and Van den Berg, 1987b). A H. lataniae infests leaves, twigs, branches and morphological description and illustrations fruit. Heavy infestations on terminal growth of the first instar of F. fioriniae have been can cause dieback of the growing points. provided by Howell and Tippens (1977). The presence of scale on the fruit presents an aesthetic problem. Rough-skinned cultivars, Latania scale, Hemiberlesia lataniae (Signoret) especially ‘Hass’, are the worst affected because the scales cannot be brushed off The latania scale, or palm scale, was easily in the packing house. Scale infestations originally described from a palm, Latania are worse where the natural enemy complex borbonica, in 1869 (Quayle, 1938). H. lataniae is upset by disruptive insecticides such has been recorded on avocado in countries as methidathion, dimethoate and synthetic including Australia, Israel, South Africa and pyrethroids. Natural enemies include para- the USA (California and Florida) (Quayle, sitic wasps of the Aphytis sp. proclia Walker 1938; Ebeling, 1959; Avidov and Harpaz, group, Signiphora perpauca Girault, Encarsia 1969; Howard and Oliver, 1985; Swaine et al., citrina (Craw.), Signiphora flavella Girault, the 1985; De Villiers and Van den Berg, 1987b). green lacewing Chrysopa oblatis Banks, and According to Dekle (1976), it has more than the coccinellid Rhizobius satellus Blackburn.

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Pests and Pollinators of Avocado 235

Chemical control is via methidathion or low Ebeling, 1959). In South Africa, C. dictyospermi viscosity oil (Waite, 1988). has been recorded on avocado, guava and Natural enemies in South Africa include mango, among others (De Villiers, 2001c). the aphelinid parasitoids Aphytis lingnanensis Quayle (1938) provided a list of 67 host plants, Compere, Aphytis africanus Quednau, the including avocado, banana, citrus, guava, encyrtids Habrolepis obscura Compere and mango, pecan, rose, apple and tea plant. Annecke and Comperiella lemniscata Compere The female scale is circular, slightly and Annecke. Predators are the coccinellids convex, 1.5–2.0 mm in diameter and light Rhyzobius lophanthae Blaisdell, Chilocorus sp., brown or red-brown. The scale covering may as well as a cybocephalid Cybocephalus sp. be readily separated from the insect, even (De Villiers and Van den Berg, 1987b; Daneel, during the moulting period, distinguishing it 1998). from the red scale, Aonidiella aurantii (Maskell) The predatory mites, Cheletomimus (Quayle, 1938). berlesei Oudemans (Cheyletidae) and the Scales from Ventura County, California, Hemisarcoptes spp. (Hemisarcoptidae) feed on reproduce parthenogenetically, whereas in diaspidid crawlers such as those of H. lataniae those from the New Orleans district, fertiliza- (Gerson and Zor, 1973). Coccinellids such as tion is necessary for reproduction (Ebeling, R. lophanthae and Chilocorus sp. are high 1959). According to Quayle (1938), there can density feeders of scale insects, Dentifibula be from three to four generations per year in obtusilobae Felt is a cecidomyid predator of southern California and from five to six in the latania scale. Evans and Prior (1990) state southern Florida. that armoured scale insects, particularly in Parasitoids recorded from C. dictyospermi the humid tropics, are subject to periodic and in the USA include Aphytis chrysomphali often devastating attacks by highly adapted (Mercet), Prospaltella aurantii (Howard), Thy- fungal pathogens, such as Nectria flammea sanus merceti (Malenotti) and Thysanus flavo- (Tull.) Dingley (Ascomycota). palliata (Ashmead). The coccinellids Rhizobius In most areas where the scale is present, debilis (Blackburn) and Lindorus lophantae their natural enemies keep them under bio- (Blaisdell) seem to be of greater importance logical control under field conditions. Where than the parasitoids (Ebeling, 1959). natural enemies have been suppressed by the misuse of insecticides, scale-infested avocado Other scales fruit need to be cleaned before marketing (Ebeling, 1959; Swaine et al., 1985). In Peru, Selenaspidus articulatus Morg. and Unaspis citri Comstock are common pests Spanish red scale, Chrysomphalus of citrus, regularly found attacking avocado dictyospermi (Morgan) when the orchards are located close to citrus orchards. In Mexico, 14 species of diaspidid The Spanish red scale attacks a large number scales, Abgrallaspis howardi (Cockerell), Acu- of host plants and is also common in green- taspis albopicta Cockerell, Aspidiotus spinosus houses (Ebeling, 1959). It feeds on the twigs, Comstock, Chrysomphalum aonidum (L.), C. branches, leaves and fruits of the plants dyctiospermi (Morgan), Diaspis cacoccois Linch- (Van den Berg et al., 1999). Avocado twigs tenstein, Hemiberlesia diffinis (Newstead), H. and branches that have been severely infested lataniae (Signoret), H. rapax (Comstock), Mela- with C. dictyospermi become roughened and naspis aliena (Newstead), Myxetaspis personata crack. Leaf drop may also occur. The Spanish (Comstock), Pinnaspis strachani (Cooley), red scale has an almost cosmopolitan distri- Quadraspidiotus sperniciosus (Comstock), Vela- bution which includes Africa, the Bahamas, taspis dentate (Hoke), three Coccidae, Saissetia the Canary Islands, Corsica, the Philippines, oleae (Oliver) (McGregor and Gutierrez, 1983), Seychelles and the USA. Coccus hesperidum L., Pulvinaria simulans Spanish red scale is a pest of avocado and Cockerell, the mealybugs, Planococcus citri has occasionally been found on avocado and (Risso), Dysmicoccus brevipes (Cockerell), citrus in California and Florida (Quayle, 1938; Ferrisia virgata (Cockerell) and Nipaecoccus

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nipae (Maskell), are considered the most probably a phloem feeder. It is more abun- frequent Coccoidea attacking avocado. dant on avocado (3.1%) than on macadamia (0.5%). The adult is 15 mm long and 7 mm wide, with a mottled appearance varying from orange-green through green to a brown- Flatidae ish colour; ventrally its abdomen is bright red. The nymphs are dark brown with long Avocado planthopper, Decipha anal filaments. viridis (Synave)

D. viridis is a minor pest of both avocado and macadamia. Nymphs and adults suck plant Cicadellidae sap from the leaves and fruit stalks. Large amounts of honeydew are produced which The leafhopper, Idona minuenda Ball (Cica- support the growth of sooty mould. This may dellidae) in Mexico, is a common pest of spoil the appearance of avocado fruit. avocados grown in more temperate areas The adult D. viridis is light green with a with frequent rainfall. Its peaks are observed blackish spot on the distal edge. When at rest, during the months of July to October. The the wings are kept folded over the abdomen in nymphs feed on the leaves, causing a grey- tent-like fashion. Eggs are laid in oval-shaped coloured injury on the leaf’s upper side. masses which are about 5 mm in diameter. When the attack occurs on young leaves these The tops of the eggs are white and the sides of turn yellow and remain underdeveloped. the egg masses light brown. Nymphs are light This species is suspected of transmitting a green with white and yellow stripes on their virus. backs. Long white waxy filaments protrude Penthimiola bella (Stol), the citrus leaf- from the tips of their abdomens. hopper, is a well-known pest of citrus in South The life cycle of the avocado planthopper Africa. It has been shown (Du Toit et al., 1993; lasts about 6 weeks in summer. There may be Bruwer, 1996) that this species is probably up to six generations per year. In South Africa, one of the causative agents of protrusions, as the populations of D. viridis seem to be sta- especially on ‘Hass’ avocado fruit from old ble, there are probably sufficient natural ene- trees. Eggs are laid singly through a minute mies to keep them below the economic level. slit and placed in a superficial envelope formed by the tissue of either leaves or fruit. There are five nymphal instars. The adult Acanalonidae is largely brownish, mottled with paler markings measuring 3.0–3.9 mm in length. ° Parathiscia sp. near truncata Walker Incubation lasts 9–20 days at 20–27 C and nymphal development takes 25–63 days In South Africa, both adults and nymphs (N.H.S. Pretorius, 1971, unpublished). The feed on avocado and macadamia. The 8 mm eggs of P. bella are attacked by seven adults are mustard green. At rest, the wings Chalcidoidea species (Annecke, 1965) result- are folded over the abdomen, giving them a ing in 50% parasitism (Annecke, 1964b). flattened appearance. The nymphs are green.

Psyllidae Eurybrachidae Trioza anceps Tuthill Mottled avocado bug, Parapioxys jucundus Distant T. anceps is 2–5 mm long and is considered to be widely distributed in Mexico, where Both adults and nymphs of P. jucundus feed it attacks regional non-commercial cultivars. on avocado and macadamia. This species is T. anceps causes large, finger-like galls on the

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Pests and Pollinators of Avocado 237

dorsal surfaces of leaves of avocado trees in considers the most important injury to be Central America (Hollis and Martin, 1997). caused by the feeding of nymphs and adults. However, T. anceps is very seldom observed on commercial cultivars, such as ‘Hass’ and ‘Fuerte’. A heavy infestation of this stenophagous species may cause defoliation ORDER HEMIPTERA – SUBORDER (Hernandez et al., 2000). HETEROPTERA

Trioza perseae Tuthill Coreidae

T. perseae is reported from Peru (Chavez et al., Many of the coreids that, among others, 1985) and Venezuela. This insect is approxi- also damage tropical and subtropical crops mately 2.5 mm long, yellowish with dark are known as tip wilters, as their feeding bands on the abdomen and thoracic regions, often causes wilting of new shoots (Brain, wings which are almost transparent, with 1929; Smit, 1964a; Van den Berg, 1998). A reduced venation. Taxonomic characteristics comprehensive study of three members of are reported by Chavez et al. (1985). The this family was also performed by Hartwig female deposits its eggs on the tender flush, and De Lange (1978). preferring the leaf underside, close to the The adults and nymphs of tip wilters suck mid-vein. The eggs have a pedicel; they are the sap of succulent new growth. In many whitish and difficult to see with the naked plant species, the saliva injected by tip wilters eye. The emerging nymph is yellowish with into plant tissue causes wilting and dieback inconspicuous body segmentation. Most of the new shoots, beyond the point of feeding occurs on the leaf underside, but feeding. Because of dieback of the growth tip, some nymphs and adults can be found on secondary axillary buds start to grow, which the upper side of the leaf. Hollis and Martin may cause dense sprouting. Their attacks are (1997) provide the identification key to differ- most serious during periods of growth flush, ent psyllids associated with P. americana. especially on young trees. T. perseae galls are formed on the leaf In South Africa, the most important underside, while the adaxial surface shows species attacking some tropical and sub- depressions which are surrounded by yellow- tropical crops, including avocado, are: Ano- ish circles. The psyllid is regularly found in plocnemis curvipes F., Leptoglossus australis (F.) those places that are located more than 900 m and Pseudotheraptus wayi Brown. above sea level. Other psyllid species reported by Hollis and Martin (1997) are T. aguacatae Large blacktip witer, Hollis and Martin deforming shoots and Anoplocnemis curvipes F. leaves, and T. godoyae Hollis and Martin causing leaf roll. Chavez et al. (1985) reported A. curvipes is the most common tip wilter several unidentified Eulophidae and Ptero- found on tropical and subtropical crops. The malidae as parasitoids of T. perseae. adult is a dull grey-brown, about 25 mm in length. The femora of the males are thickened and noticeably bent, with a thorn-like spine. The eggs are grey-brown, barrel- shaped, Membracidae and deposited in single rows, each consisting of about 6–12 eggs, on the branches and leaves Metcalfiella monogramma Germar of their host plants (Smit, 1964b). At an average temperature of 28°C, eggs hatch after 4 to 6 Brom (1970) provides a description and life days on mango and nymphal development history of M. monogramma, a common pest takes about 4 to 6 weeks. Depending on the in Mexico. Its injury is characterized by the availability of new growth, there are from deposition of eggs into young branches, caus- three to six overlapping generations annually ing death of the infested tissue. Brom (1970) in the Nelspruit area (Van den Berg, 1998).

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According to Hartwig and De Lange (1978), lifetime. The egg stage lasts 5–9 days, the five the females exhibit maternal care of the eggs nymphal stages 27–31 days. The life cycle and young. takes 63–74 days. Adults live up to 41 days. Of the parasitoids, the egg parasitoid Gryon sp. (Hymenoptera: Scelionidae) is the Coconut bug, Pseudotheraptus wayi Brown most important in Nelspruit. The total percentage of parasitism of egg masses tied to The coconut bug is endemic to Africa and mango trees in an orchard at Nelspruit was was first recorded as a serious pest on coco- just below 15% (Van den Berg, 1998). Hermya nuts in East Africa (Way, 1953). It has also sp., a tachinid, parasitizes 2% of the adults been recorded on the islands of Zanzibar, (Van den Berg, 1998). Pemba and Mafia along the east coast of Hartwig and De Lange (1978) found Africa (Way, 1953; Vanderplank, 1958). In Pheidole megacephala (F.) preying on A. curvipes South Africa, P. wayi was recorded for the nymphs. Predation by this and other species first time in 1977 on mangoes (De Villiers was recorded in Pretoria North. Predation and Wolmarans, 1980). Since then the bug of the first spring generation caused 96% has been found on avocado and various other mortality of older nymphs, but summer adult subtropical crops (De Villiers, 1992). Accord- mortality was below 16%. ing to Joubert (2001), the pest status of this insect is on the rise. Leaf-footed plant bug, Leptoglossus The coconut bug can also cause extensive australis (F.) damage to avocado (Viljoen, 1986; De Villiers and Van den Berg, 1987a), macadamia The leaf-footed plant bug L. australis was pre- (Bruwer, 1987), guava, mango, loquat (De viously known as Leptoglossus membranaceus Villiers, 1990b, 1992) and pecan nuts (Joubert (F.). L. australis adults are dark brown to black and Neethling, 1994). with orange spots on the ventral parts of the According to De Villiers (1990b), the abdomen and thorax. An orange spot is also nymphs and adults of P. wayi suck sap from present on each of the hind flattened tibiae. the avocado fruit. About 2 days after feeding This species is not as robust as most of the on a mature avocado, the lesion can be recog- other tip wilters. According to Bedford nized as a patch that is slightly darker than the (1978b), L. australis is present in most areas rest of the skin and resembles a bruise. As the of South Africa where citrus is grown, which lesion becomes older, it enlarges to approxi- would therefore also include the areas in mately 8 mm in diameter, becomes indented which tropical and subtropical crops are like a hail mark and turns brown to black. The cultivated. It also occurs in Zimbabwe lesion may sometimes also become tumescent (Hall and Ford, 1933), Kenya (Ondieki, 1975), and wart-like. If the insect has fed on a young Australia (Murray, 1976), India (Jadhav et al., fruitlet, the avocado can have a malformed 1980) and Japan (Yasuda and Kinjou, 1983). L. and asymmetrical appearance at maturity. australis has been reported to feed on legumes Internally, the lesions display a brown stain and many other plant species, including that can penetrate the avocado fruit to a depth granadilla, cacao and coffee (Hill, 1975), of 10 mm. It forms a typical hard clot that is macadamia (Ironside, 1995), avocado and easily removed together with the skin when mango shoots. According to Hill (1975), the latter is pulled off. Coconut bugs do not young fruits show dark spots where feed- cause rotting of the fruit flesh (De Villiers, ing has taken place, while mature fruits fall 1990b). In South Africa, Dennill and Erasmus prematurely. Furthermore, terminal shoots (1991) and Erichsen and Schoeman (1992) that are attacked may wither and die beyond indicated that damage by P. wayi during the the point of feeding. 1990–1991 seasons amounted to 4.7% and Jadhav et al. (1980) reared L. australis 2.8%, respectively. on pomegranate and reported on its biology. The eggs are laid singly, scattered over Eggs are laid in strips along the twigs, an the fruit, small twigs and blossom stems. individual female laying up to 60 eggs in her They are creamy white to light brown, oval,

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approximately 1.5 mm in length. Prior to an excessive number of dropped fruit from hatching, they change to a darker red-brown, October to December. The inside of the green the egg stage lasting approximately 7 days husk and shell can be examined for brown to (Bruwer, 1992; De Villiers, 1992). black feeding marks. Nuts can also be picked Newly hatched nymphs are 5 mm in from trees and examined for stink bug dam- length, 1.5 mm in width and light brown. Five age (Froneman and De Villiers, 1993). instars occur, during which the nymphs are To maximize the benefit of natural ene- morphologically very similar, with their char- mies in orchards, chemicals should only be acteristically long antennae. The adult coco- applied when absolutely necessary (Joubert, nut bugs are strong fliers with well-developed 2001). Pyrethroids should not be used more wings. The dorsal side of the bug is red- than once per season and then only to reduce brown while the ventral side is lighter in the original population early in the season. colour. Adults are approximately 15 mm in Endosulfan is much more compatible with the length and 4 mm in width, with males slightly concept of integrated pest management (IPM), smaller than females (De Villiers, 1992). The but should also be used judiciously to prevent female lays on average 80 eggs and the life the build-up of resistance in pest organisms. cycle from egg to adult lasts 31–48 days, depending on temperature (Bruwer, 1992). Green coconut bug, Homoeocerus sp. The adult life span of P. wayi ranges from near elongatus Dallas 73 to 84 days (Lever, 1969). Nine or more generations per year can occur on coconuts H. elongatus is up to 15 mm long and 5 mm in eastern Africa and Zanzibar (Way, 1953). wide. It has almost the same size and general In East Africa and its coastal islands, form as the coconut bug, P. wayi, but is pale where P. wayi is a serious pest on coconuts, the green. It is an indigenous species to South bug is controlled by a tree-nesting ant Oeco- Africa and probably does the same damage phylla longinoda (Latr.) (Way, 1951). In South as P. wayi to tropical and subtropical crops. It Africa, two egg parasitoids of P. wayi were has been found in small numbers on avocado. collected on macadamia and were identified In Taiwan, the coreid fruitspotting bug as Anastatus sp. (Eupelmidae) and Trissolcus Paradasynus spinosus Hsiao, which breeds sp. (Scelionidae), responsible, respectively, for on Magnolia spp., damages avocado fruit 58% and 26% of parasitism (Bruwer, 1992). in a manner similar to the Australian and Stink bugs, which include the coconut South African coreids (Hung and Jong, 1997). bug as well as pentatomids, should be moni- Sprayings of carbaryl are recommended, as tored to determine the approximate size of the well as bagging fruit to prevent bug access. pest complex (Joubert, 2001). Two methods Parasitism levels of 40–90% by an unidenti- are currently being used in South Africa fied egg parasitoid have been recorded (S.C. (Froneman and De Villiers, 1993): in the first, Hung, 1998, personal communication). ten trees are chosen weekly at random per unit/block (not larger than 5 ha) and sprayed Amblypelta spp. with dichlorvos (150 ml 100 l−1 water). Later, if more than 1.2 stink bugs are found per tree, a Amblypelta nitida Stal and A. lutescens lutescens full-coverage spray should be considered. In (Distant) (Coreidae) are the major pests of the second method, ten trees can be selected avocado in Queensland, northern New South weekly at random per unit, shaking the Wales. They attack the fruit from the time it lower branches on each tree. Branches must sets in September/October until the end of be shaken early in the morning before the April. Damage can be caused by bugs of all temperature exceeds 18°C, otherwise the stink stages feeding on the fruit but it is mostly bugs escape when the branches are shaken. If adult bugs migrating into orchards from more than 0.7 stink bugs are found per tree, a nearby breeding areas that cause most of the full-coverage spray should be considered. damage. The most severe damage occurs in There are also other signs that may orchards which are situated close to the indicate the presence of stink bugs, e.g. rain-forest. The egg parasitoids Gryon sp.

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(Scelionidae), Ooencyrtus caurus (Encyrtidae) Powdery stink bug, Atelocera raptoria Germar and Anastatus sp. (Eupelmidae) may account for up to 90% of eggs but the immigrant The powdery stink bug is indigenous to adults which result from non-parasitized southern Africa. It is brown, sprinkled with eggs cause severe damage. Because immi- red-brown and has a whitish wax. The gration is constant throughout the season, ventral side of the thorax and abdomen is individual crops may require sprays of mostly covered with a whitish growth of a endosulfan every 2 weeks. Orchards in more waxy substance. The powdery stink bug open situations may require only occasional occurs on many tropical and subtropical sprayings. Thin-skinned cultivars, especially crops. It has been reported to be the most Fuerte, appear to suffer most, but the thick- abundant stink bug on avocado, and the skinned Hass can be just as badly affected second most adundant on macadamia. without showing the severe lesions and cracks that develop on Fuerte (Fay and Grey-brown stink bug, Coenomorpha Huwer, 1993; Waite and Huwer, 1998). nervosa Dallas In South Africa, the dorsal side of the adult grey-brown stink bug is brown with grey- Pentatomidae black dots forming patterns all over the head, thorax, abdomen and wings. It is up to 14 mm The pentatomids dealt with in this chapter long, the ventral side of the abdomen and are, except for the cosmopolitan Nezara viri- thorax is off-white to a whitish brown. One of dula L., indigenous to southern Africa. Many the characteristics of this species is the width of them probably also occur further north in of the abdomen. It sticks out beneath the Africa. In Israel, the variegated caper bug, wings and is also broader than the thorax. Stenozygum coloratum Klug (Pentatomidae), The parts of the abdomen that can be seen develops generally on wild caper bush, Cap- from the dorsal side have grey-black lines paris spinosa, sometimes migrating to various that accentuate each segment. cultivated plants, including avocado (mainly C. nervosa was recorded as occurring in cv. Hass, but also Fuerte and Ettinger). The fairly large numbers on avocado (Joubert and damage to fruit is accompanied by heavy Claassens, 1994). In later surveys, however, secretion of persein and by the appearance of this species was found in small numbers on black spots (Izhar et al., 1990b). both avocado and macadamia, where feeding Feeding of pentatomids on small devel- probably takes place on fruits, nuts or on the oping fruits and nuts and their pedicels causes bark (Van de Berg and Greenl, unpublished many of them to drop, while larger fruits and data). nuts are blemished. Growth points at which feeding takes place may wither and die. Spotted stink bug, Farnya sp. The biology, life history and control of the pentatomids dealt with here are quite similar The spotted stink bug is green-brown to grey- for the different species. Furthermore, their ish brown with yellow-brown spots. It is up natural enemies consist of egg parasitoids to 14 mm in length and feeds on avocado and (Hymenoptera), adult parasitoids (Diptera: macadamia. Eggs are whitish, turning light Tachinidae) and predators such as ants. The brown as development progresses. They are tachinids may occasionally also parasitize laid in masses averaging 26 eggs per mass. At nymphs but complete their development in a constant 25°C and 75% RH, the egg stage the adult stink bug. In general, the parasitoids lasts on average 6.8 days, and the first to fifth of the different pentatomids are, except for (final) instar nymphs take, respectively, 5.0, species differences, comparable. Their effec- 10.4, 7.7, 6.8 and 10.8 days. From egg to adult tiveness at controlling the different species, takes 48 days (Bruwer, 1992). however, varies greatly from species to Egg parasitism by two Trissolcus spp. (Sce- species with seasons of the year. lionidae) and a Pachyneuron sp. (Pteromalidae)

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at Nelspruit accounted, respectively, for 72.6% macadamia, pecan, tobacco and various and 4.5% of the parasitism (Bruwer, 1992). vegetables. In South Africa, Dennill and Dupont (1992) reported that feeding by N. Yellow-edged stink bug, Nezara viridula causes protrusions on avocado fruit. pallidoconspersa Stål. N. viridula was reported on avocado, macadamia and pecan (Joubert and Claassens, 1994; Small numbers of the yellow-edged stink bug Joubert and Neethling, 1994). N. pallidoconspersa were collected on avocado The eggs are yellowish white, barrel- and macadamia. Feeding has been recorded shaped and laid in clusters of 60 to over 100, on macadamia by De Villiers (1986). The eggs usually on the underside of leaves, but also on of N. pallidoconspersa are yellowish white and the stems (Van Heerden, 1933). A female may laid in clusters averaging about 70 eggs. These lay up to 320 eggs (Van Heerden, 1933). The are mostly laid on the leaves of their host developing eggs change to orange with darker plants. The final instar nymph has a black orange showing through a whitish lid prior background colour with pale orange dots on to nymphal emergence. The newly emerged the thorax. Two brighter orange dots and white nymphs usually remain closely clustered, but markings are also present on the abdomen. do not feed until the second moult (Van den Adult females of N. pallidoconspersa are Berg, 1998). There are five nymphal instars; up to 18 mm long, males from 11 to 14 mm. the final instar is green with reddish colouring They are green, with abdomen edges that are in the centre of the abdomen and a row of four yellowish with brown lines that accentuate whitish dots on each side of the red. The adult each segment. They also have yellowish hind- is a typical shield stink bug, about 15 mm wings which are striking when they fly. long. When N. viridula hibernates, it changes N. pallidoconspersa can be found in the hot- to an orange-brown to bronze colour. In South ter areas, such as Nelspruit and Mpumalanga, Africa, the life cycle from egg to adult lasts where they breed throughout the year on the about 6 weeks (Van Heerden, 1933). There are wild-growing castor oil plants, Ricinus communis. three full generations per year and stages Natural enemies of N. pallidoconspersa overlap in summer. In the Cape Province, the include the egg parasitoid Trissolcus sp. adult hibernates in sheltered sites. In the hot- (probably not Trissolcus basalis Wollaston) ter areas like the Mpumalanga Lowveld, some and two unidentified tachinid parasitoids of the adults become more orange-brown to that attack adult stink bugs. bronze in colour, but at least some individuals do not hibernate since adults and nymphs Small green stink bug, Nezara prunasis Dallas may be found on wild-growing castor oil plants throughout the winter months (Van The small green stink bug is often encoun- den Berg, 1998). tered on subtropical crops. N. prunasis was Two tachinid parasitoids of the adult found in relatively large numbers on avocado green vegetable bugs, Bogosia bequaerti Ville- (Joubert and Claassens, 1994), and pecan neuve and Cylindromyia sp. (Van den Berg, (Joubert and Neethling, 1994). Since no 1998) and the egg parasitoid Trissolcus basalis nymphs were found, it is not certain whether (Wollaston) (Scelionidae) are present in South feeding and breeding take place on these Africa but are unable to keep the numbers plants. Adults of N. prunasis are green and of N. viridula acceptably low. A tachinid 9–11 mm in length. At the beginning of the parasitoid of the adult green vegetable bug, winter they congregate in sheltered areas, Trichopoda pennipes (F.), was first introduced such as barns or even in the roofs of houses. from Hawaii in 1978, and from Florida in 1983 through 1995, but it failed to become Green vegetable bug, Nezara viridula L. established (De Villiers et al., 1980; Van den Berg, 1995). A second parasitoid, Trichopoda The green vegetable bug is a cosmopolitan giacomellii (Blanchard), was introduced from species which attacks more than 200 cultivated Australia. Establishment of the two Trichopoda plants, including avocado, citrus, granadilla, spp. has not been confirmed.

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Two viruses, NVV-1 and NVV-2, were attack the shoots and fruit of avocados, caus- identified from a green vegetable bug (Von ing significant damage (Cendana et al., 1984). Wechmar et al., 1991). When fed to second instar nymphs, 75% reduced longevity, Dagbertus fasciatus (Reuter), D. olivaceous 67% reduced life span and 95% reduced egg (Reuter), Rhinacloa sp. production were achieved (Williamson and Von Wechmar, 1995). In Florida, a number of mirids (Dagbertus The following method is recommended fasciatus (Reuter), D. olivaceous (Reuter) and to monitor stink bug populations in avocado Rhinacloa sp.) feed and insert their eggs on and other trees: choose ten trees at random per opening buds, leaves, flowers and small fruit. unit or block (smaller than 5 ha); spread light- Attacks seem to especially affect flowers coloured cloth beneath the drip areas of the and recently set fruit, causing them to drop. trees; spray the ten trees with dichlorvos Wounds on fruit may serve as a point of entry (150 ml 100 l−1); count all stink bugs that fall for decay organisms. These insects are green- from the trees during the next hour. As a brown, comparatively small at 1 cm in length. general recommendation, control should be Mirids usually appear during the bloom and considered if 1.2 or more stink bugs are early fruit-setting stages. It is suggested that counted per tree. weeds and grass in the grove be mowed as closely as practicable to reduce places that could harbour mirids. Mirid populations are most common from January through April, Miridae when avocado flowers are fully open. The parasitoid, Leiophron, probably fumi- Avocado bug, Taylorilygus sp. pennis Loan, has been registered in Florida. In Africa, the adult avocado bug, Taylorilygus Sprays during flowering should be applied sp., is brown to black and up to 3 mm in late in the afternoon to reduce loss of honey- length. Two dirty white spots are present on bees (Peña and Johnson, 1999). the base of the wings. The first two nymphal instars are green. Adults and nymphs feed on avocado flowers, young avocado fruit Tingidae and presumably also young leaves. Avocado flowers seem to be preferred to fruit. Because Avocado lace bug, Pseudacysta perseae of the large numbers of flowers produced, (Heidemann) feeding on them is of minor importance. Damage to avocado fruit is caused within the The avocado lace bug was described in 1908 first few weeks after fruit set. This leads to the as Acysta perseae from Florida specimens and development of protrusions on larger fruit considered a minor pest of avocado for sev- which are only visible about a month after eral years. However, persistent population feeding. The lesions that occur on avocado outbreaks of P. perseae observed since the fruit are in the form of pimply elevations mid-1990s in Florida and in the Caribbean on the fruit surface (Du Toit et al., 1993) region, reveal that P. perseae has become one and are known as ‘Vosknoppe’. This can be of the most important pests of avocado very severe, especially on ‘Hass’ fruit. Upon (Abud-Antum, 1991; Medina-Gaud et al., dissection, brown corky scar tissue can be 1991). P. perseae is found in Florida and found in the centres of the lesions: 30–40 Georgia in the USA, Bermuda, the Dominican protrusions per fruit make them unsuitable Republic, Puerto Rico and Mexico (Mead for export. If surveys indicate that large and Peña, 1991). Common hosts for this pest, populations of the avocado bug are present besides avocado, are red bay, Persea borbonia shortly after fruit set, chemical control should (L.) and camphor, Cinnamomum camphora be applied immediately (Van den Berg et al., (L.). The life cycle of P. perseae was reported 1999). In the Philippines, the mirid bugs by Abud-Antum (1991). It requires 22 days Helopeltis bakeri Pop. and H. collaris Donovan from egg stage to adult. The most complete

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description of adults and late instar nymphs develops on plants of the family Malvaceae, it was given by Heidemann (1908). sometimes feeds on the leaves and stem of P. perseae confines its attack to the lower avocado seedlings and may even cause some surface of the foliage, causing chlorosis, damage (Swirski et al., 1998). necrosis and severe defoliation of avocado, reducing yields (Peña et al., 1998) (Plate 52). This bug usually lives in colonies, depositing ORDER HYMENOPTERA eggs upright in irregular rows in clusters on the lower leaf surface. This insect opens an Formicidae avenue of penetration for the leaf anthracnose fungus, Colletotrichum gloeosporioides (Mead In Peru, Atta sexdens L. causes very severe and Peña, 1991). Since the avocado lace bug damage by cutting new leaf flushes and by was not considered an important pest, it consuming leaves. In Mexico, Atta mexicana is suggested that in recent times, suitable (Smith) is a variably sized ant, 3 to 14 mm natural enemies were decimated by applica- long, with polymorphic markings. It is red- tion of pesticides or by some other type of dish to dark brown in colour. The workers are environmental disequilibria. polymorphic with spines on the pronotum, In Florida, avocado lace bug population mesonotum and propodeum. The ant cuts the densities increase during the dry season leaves into irregular pieces, frequently start- (November–February), and decline during ing the damage at the leaf apex. The central spring and summer (Peña et al., 1998). The vein of the leaf remains. The severity of the cultivars ‘Waldin’, ‘Booth 8’ and ‘Loretta’ damage depends on the time of year when have the highest natural infestation levels. The the infestation occurs. most susceptible cultivar appears to be ‘Booth In South Africa, the driver or red ant, 8’, with average damage levels of 20–28% to Dorylus helvolus L., causes damage to avocado the leaf area. Leaf photosynthesis is reduced when the fruit hang or lie on the ground under by 50% when the leaves sustain 40% damage. the trees. Parts of the fruit peel are damaged Cultivars (e.g. ‘Simmonds’) with 100% of their and fruits with such feeding marks are leaves infested exhibited early leaf drop and unsuitable for export. Confusion surrounds an overall reduction in fruit set. By contrast, a the identity of the organism causing this × West Indies Guatemala hybrid was scarcely damage. It has been ascribed by Dennill and affected by the pest. Erasmus (1991) to an unidentified ant species. The major biological control agents in However, Erichsen and Schoeman (1992) state Florida are two egg parasitoids, Oligosita sp. that it may be due to feeding by a species of (Hymenoptera: Trichogrammatidae), and an slug or snail. unidentified mymarid wasp; if undisturbed by chemical applications, the green lace wing Chrysoperla rufilabris Burmeister and a mirid, ORDER THYSANOPTERA Hyaliodes vitripennis Say keep avocado lace bug densities from reaching economic levels. Thripidae Several pesticides – M-Pede (soap), citrus oil and Mycotrol (Beauveria bassiana (Balsamo) Vuillemin) – significantly reduced lace bug Considerable numbers of thrips species infest densities compared with the untreated control avocado orchards in different geographical (Peña et al., 1998). regions of the world. New species have appeared recently (e.g. the avocado thrips, Scirtothrips perseae Nakahara in southern California; the orchid thrips, Chaetanapho- Lygaeidae thrips orchidii (Moulton) in Israel), demanding prompt management. These new arrivals In Israel, although the cottonseed bug, Oxy- may be the result of increased international caraenus hyalinipennis (Costa) (Lygaeidae), commerce, but the severity of their damage

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may have been intensified by changes in when 7% of fruits, leaves and flowers are horticultural practices, or by the introduction infested with thrips. Cultural control is of new cultivars. For instance, in Israel the recommended by removing weeds and introduction of new varieties, highly sus- fallowing around the tree. Reyes and Salgado ceptible to thrips, combined with irrigation (1994) demonstrated that leaves of the supplied at shorter intervals, favoured orchid avocado cultivars ‘30PLS’, ‘54PLS’, ‘Rincoatl’ thrips infestation. The Ardit variety of ‘18PLS’ and ‘158PLS’ and blossoms of avocado is susceptible to the greenhouse cultivars ‘18PLS’, ‘44PLC’, ‘ColinV-101’, thrips, Heliothrips haemorrhoidalis (Bouché) ‘175PLS’, ‘158PLS’ and ‘PV2’ are tolerant to (Thripidae) and varieties ‘TX 531’ and Scirtothrips. Ebeling et al. (1959) reported that ‘Horshim’ to the black vine thrips, Retithrips the cultivars ‘Fuerte’ and ‘Dickinson’ are syriacus (Mayet) (Thripidae). moderately resistant to Scirtothrips spp.

Citrus thrips, Scirtothrips aurantii Faure Scirtothrips perseae Nakahara

In Africa, the citrus thrips, Scirtothrips aurantii An unknown species of Scirtothrips was Faure, has been reported from avocado, discovered damaging fruits and foliage of citrus, guava and litchi (Faure, 1929), and avocado in California in 1997. The species in Egypt (Mound and Palmer, 1981); its pres- was described later as S. perseae (Nakahara, ence has been confirmed in the Cape Verde, 1997). S. perseae feeding damage to foliage is Yemen, Mauritius and Réunion (Vuillaume observed on upper and lower leaf surfaces as et al., 1981; Gilbert and Bedford, 1998). well as on developing fruit. Fruit is suscepti- Both the adults and larvae of S. aurantii cause ble to damage until it reaches approximately lesions when feeding on fruit of avocado, 2.5 cm in diameter. Feeding scars develop citrus, guava, macadamia and mango (Grové, from the calyx and fruit scarring results 2001a,b). S. aurantii is a very important pest in ‘alligator skin’ (Hoddle, 1997). Avocado on citrus (Bedford, 1943; Wentzel et al., 1978) thrips larvae and adults can build to high and mango (Grové, 2001b) but it seldom does densities from autumn through spring on any economically significant damage on avo- young leaves, causing excessive leaf drop. cado. Some natural enemies were reported The main source of economic loss attributable by Grouth, 1994; Grouth and Richard, 1992; to avocado thrips is scarring of immature and Grouth and Stephen, 1995. For more fruit in the spring (Hoddle and Morse, 1998). information, see Chapter 3. Female S. perseae lay eggs singly into soft plant tissue. Eggs are kidney-shaped and Scirtothrips aguacatae Johansen and Mojica whitish yellow in colour. Between 20 and 31 and Scirtothrips kupae Johansen and Mojica eggs are laid per female, egg to adult development time lasts 16 to 27 days, and eggs hatch Larvae and adults of S. aguacatae and S. kupae within 9 to 14 days depending on the tempera- are found on young leaf flushes, flowers and ture (Hoddle and Morse, 1998). Following egg fruit. Damage to the fruit epidermis results in hatching, developing thrips pass through two fruit deformation. To reduce thrips densities, actively immature stages. Larvae pupate in Hernandez et al. (2000) recommended treat- leaf litter under trees, in crevices in the bark, or ment during blooming followed by another within persea mite nests on leaves. Surveys of two chemical treatments when the thrips leaf litter indicate that 89% of pupating thrips populations are increasing. Coria-Avalos are found in the upper non-decomposed leaf (1993) suggested applying pesticides three to layers. Hoddle and Morse (1998) recommend four times. The first spray should be applied the use of sabadilla, because of its short resid- when the trees show 10% bloom, followed ual activity and low toxicity to most natural by a second spray at full bloom, a third enemies. In California, Franklinothrips vespi- one immediately after bloom and a fourth formis is considered to have good potential as a application when newly formed fruits are predator during high infestations of S. perseae observed. Economic thresholds are observed (M.S. Hoddle, 2000, personal communication).

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Red-banded thrips, Selenothrips S. rubrocinctus and Heliothrips haemorrhoidales rubrocinctus (Giard) (Bouché); Leptothrips macro-ocellatus (Watson) is considered a predator of S. rubrocinctus The red-banded thrips has been a serious pest (Johansen and Mojica-Guzman, 1996). No of cacao in the French West Indies since 1901 parasitoids or predators of S. rubrocinctus (Russell, 1912). According to Hill (1975), S. have yet been recorded from South Africa. rubrocinctus has an almost pantropical distri- Observations should be made on leaves and bution. In Taiwan, symptoms similar to those fruit for red-banded thrips during summer caused by Heliothrips haemorrhoidalis result and autumn for any developing infestation. In from the feeding of S. rubrocinctus (Giard). Florida, the following materials are labelled This species can be a problem in California, for use against thrips: malathion (various Florida, South Africa, Australia, Reunion and labels), permethrin (Pounce, Ambush), Taiwan. pyrethrins + rotenone (Pyrellin) (Peña and In Florida and Australia, infested leaves Johnson, 1999). In Australia, the pest is are spotted on the upper surface with generally suppressed by the frequent sprays dark reddish brown faecal pellets, or on the of endosulfan applied to control fruitspotting lower side of the leaf (Hill, 1975; Waite and bugs (Waite and Pinese, 1991). Pinese, 1991), damaged areas turn rusty with numerous small, shiny black spots of excreta. The edges of affected leaves curl up. Heavy Frankliniella chamulae Johansen and feeding on fruit causes a russet appearance, Frankliniella bruneri Watson with cracking and decay. Greenhouse thrips In Mexico, F. chamulae and F. bruneri are damage fruit and tend to feed on the larger found on avocado flowers in the region of and more mature ones. They are found most Uruapan. There are unconfirmed reports that frequently where two fruits are in contact or both species damage the fruit. Coria-Avalos where a leaf contacts the fruit. Fruits damaged (1993) reports that Frankliniella spp., Scirtho- by slight russetting show leathery scarring trips aceri (Moulton) and Liothrips perseae are and cracks on the skin. becoming the most important avocado pests Eggs are inserted into the leaf tissue. in the Michoacan area. However, this author They are white, kidney-shaped and about does not specify which of these species injure 0.25 mm long (Hill, 1975). The first and second the fruit, reducing fruit quality. nymphal stages are yellow with a bright red band around the base of the abdomen. When Western flower thrips, Frankliniella fully grown, the second instar is about 1 mm occidentalis (Pergande) long. The tip of the nymph’s abdomen is turned up and carries a drop of excreta on the In the past, the Western flower thrips anal setae (Hill, 1975). The pre-pseudo pupa appeared infesting avocado inflorescences is yellowish with red eyes, with a red band near infested mango orchards in the south of across the first three abdominal segments. The Israel. Many different thrips species were also appearance of the pseudo pupa is similar to found on avocado inflorescences. Among that of the pre-pseudo pupa (Hill, 1975; Steyn, them, high numbers of Thrips tabaci Linde- 2001b). The adult female is dark brown and man and T. major Uzel (M. Wysoki, R. zur just over 1 mm long. Males are smaller and Strassen and W. Kuzlicky, unpublished). rare (Hill, 1975). Reproduction by the red- banded thrips is parthenogenetic (Avidov and Black vine thrips, Retithrips syriacus Mayet Harpaz, 1969). Females live about 7 weeks and lay an average of 25 eggs, which hatch in 12 In Israel, the black vine thrips has recently to 18 days (Hill, 1975). The nymphal stage lasts caused damage to avocado fruits and leaves, 6 to 10 days and the pre-pseudo pupal and cultivars ‘Horshim’, ‘TX-531’, ‘4102’, ‘4203’ pseudo pupal stages last 3 to 6 days. and ‘T-142’ being the most heavily infested The predator Franklinothrips vespiformis (Plate 53). The black vine thrips can be readily (D.L. Crawford) is considered a predator of controlled with sabadilla (Izhar et al., 1992).

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Greenhouse thrips, Heliothrips backwards while that of the pre-pseudo pupa haemorrhoidalis (Bouché) is not. There are four generations per year in The greenhouse thrips was first described in most countries but as many as six to seven 1833 (Russell, 1909) (Plate 54). It is widely generations per year have been recorded in spread throughout the world, attacking a California. The life cycle, from egg to adult, wide range of economically important crops lasts about 8 weeks (Hill, 1975). Mortality rate (Rivnay, 1934; Avidov and Harpaz, 1969; of the thrips is high at relative humidities Hill, 1975; Skaife, 1979; De Villiers and Van below 60% and temperatures above 27°C den Berg, 1987a; De Villiers, 1990c; Steyn, (Rivnay, 1935). 2001a). The greenhouse thrips is an economi- Various parasitoids and predators have cally important pest of avocados in California been recorded attacking the greenhouse (Ebeling, 1959; McMurtry et al., 1991) and thrips. In South Africa, the pirate bug, Orius Cuba (Cañizares, 1975), and of citrus in Israel tripoborus (Hesse) (Hemiptera: Anthocoridae), (Rivnay, 1934; Bodenheimer, 1951). In Israel, feeds on nymphs of H. haemorrhoidalis on large populations of H. haemorrhoidalis usu- avocado fruits, reducing thrips outbreaks ally start on pest-susceptible trees, such as (Dennill and Erasmus, 1992a,b) and Thripobius seedlings of the Mexican cultivars, or trees semiluteus Boucek (Hymenoptera: Eulophidae) of cultivars ‘Ardit’, ‘Benik’, ‘Hass’, ‘Stuart’, parasitizes greenhouse thrips nymphs (Steyn, ‘Nahlat’ and ‘Horshim’ (Plate 55). From these 1996). This parasitoid has been established foci, the thrips disperse to commercial culti- in some avocado orchards in California, vars ‘Fuerte’, ‘Nabal’ and ‘Ettinger Heavy’ reducing greenhouse thrips densities within (Izhar et al., 1990a). 2 years (McMurtry et al., 1991). In California The 1.25-mm-long adult greenhouse and Israel, the egg parasitoid Megaphragma thrips is black, with the exception of the mymaripenne Timberlake and the imported legs, wings and antennae which are white larval parasitoid, Thripobious semiluteus, are (De Villiers, 1990c). The sex ratio is female- important natural enemies of H. haemor- biased, with parthenogenetic reproduction. rhoidalis (Wysoki et al., 1997; Faber and The female lives for about 7 weeks and lays an Phillips, 2001). The wasp Thripobius semiluteus average of 25 eggs (Avidov and Harpaz, 1969). was introduced into California in 1986 and The eggs are white, kidney-shaped and about into Israel in 1991. The female endoparasitoid 0.3 mm long. They are inserted singly into the inserts its egg in first or second stage nymphs. leaf tissue just beneath the epidermis. They In the laboratory, development of the parasite increase in size and become considerably is completed at 23°C within 22–25 days swollen shortly before hatching. The opti- (McMurtry et al., 1991). The following pre- mum temperature range for oviposition is ° dators of the greenhouse thrips have been between 20 and 28 C (Ebeling, 1959). recorded in Israel: Typhlodromus athiasae The first and second nymphal stages are Porath and Swirski, Amblyseius swirskii whitish to slightly yellowish, the eyes are red. Athias-Henriot (Phytoseiidae), Franklinothrips Temperature and humidity are critical factors megalops Trybon (Thysanoptera) spiders, and during the development of the nymphs. The anthocorids (Wysoki et al., 1997). optimum level of humidity for development is As the greenhouse thrips occurs sporadi- 85%. If humidity falls below 60%, many of the cally for the most part in many African nymphs desiccate. The two nymphal stages countries, control measures are seldom neces- last for about 9 to 30 days (Hill, 1975). sary. Chemicals registered against thrips on The mature second instar nymph moults avocado include mercaptothion 25% WP at to form the pre-pseudo pupa, which is yellow- 500 g 100 l−1 water or 50% EC at 250 ml 100 l−1 ish with red eyes. After a day or two, it moults water. Mercaptothion has a 7-day safety to form the pseudo pupa. The pseudo pupa period. Sulphur 80% WP is also registered at has longer wings than the pre-pseudo pupa. 300 g 100 l−1 water or 98% DP at 10–40 kg ha−1 The pseudo pupa stage lasts for 3–14 days. (Steyn, 2001a). In the past, in the USA, oil The antenna of the pseudo pupa is tilted was combined with pyrethrum against eggs

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Pests and Pollinators of Avocado 247

(Ebeling, 1959). In Israel, the initial killing of the base followed by reddish brown ones. post-embryonic stages of the thrips by pyre- The forewing is cream coloured with rows of thrum was very high but the eggs hidden black rings encircling reddish brown spots. under the plant cuticle were not affected and a The forewing is 15–23 mm in length. Moths population build-up was observed after 15 are active at night and a female can lay about and 22 days. Oil gave similar results, but was 270 eggs (De Villiers, 1973). not as effective as pyrethrum. In Israel, two Two parasitic wasps of the genus treatments of pyrethrum at an interval of 21 Genaemirum sp. (Ichneumonidae) have been days gave good results (Ben-Yehuda et al., recorded. In South Africa, bark borer larvae 1994). However, in trials carried out in avo- can be controlled chemically by spraying the cado orchards in California in 1985 and 1986, lesions with carbaryl 850 g kg−1 WP at 250 g pyrethrum gave inconsistent results against 100 l−1 water (De Villiers, 2001b). the greenhouse thrips (Goodall et al., 1987). Avocado leafroller, Homona spargotis Meyrick; Ivy leafroller, Cryptoptila ORDER LEPIDOPTERA immersana (Walker) In Australia, the major caterpillar pests are Metarbelidae the avocado leafroller and the ivy leafroller. These pests web leaves together and feed on Bark borers, Salagena obsolescens Hampson them, but the more serious damage is caused and Salagena transversa Walker when they chew into fruit from the shelters that they construct between touching fruit In South Africa, the bark borers, S. obsolescens or by webbing leaves to fruit (Waite and and S. transversa feed on avocado, guava, Pinese, 1991). Natural enemies recorded for litchi, macadamia, pecan, wild fig (Ficus sp.), C. immersana include the predatory larva of bush willows (Combretum zeyheri and C. the syrphid fly Melanostoma agrolas Walker, as collinum), jacketplum (Pappea capensis), water well as the parasitoids Goniozus sp. (Bethy- berry (Syzygium cordatum) and Eugenia sp. lidae), Sympiesis sp. (Eulophidae) and Phyto- (De Villiers, 1973; Pinhey, 1975; De Villiers dietus celsissimae Turner (Ichneumonidae). A et al., 1987c). S. obsolescens has been recorded trichogrammatid also parasitizes the eggs from East Africa, Mozambique, South Africa, (Waite and Pinese, 1991). Chemical control West Africa and Zimbabwe (Pinhey, 1975). has been achieved with chlorpyrifos/ddvp, The eggs are cream-coloured and laid in but the IGR tebufenocide (Mimic) is currently clusters on the bark (De Villiers, 2001b). The pending registration (Waite and Pinese, young, light-brown larva feeds on the bark of 1991). trees and later makes a tunnel in the wood for shelter. The final instar can be up to 30 mm in length. The larva feeds on the bark of trees under a frass-covered silken web. The older Oecophoridae larva tunnels into the wood, usually where branches fork. The larva may kill a branch. The avocado seed moth, Stenoma catenifer The tunnel which serves as a shelter for the Walsingham, is considered one of the most larva is up to 70 mm long with a diameter of important pests of avocado in the Neotropics about 5 mm when the larva is fully grown (De and has been reported from Mexico to Argen- Villiers, 1973). tina. However, in Mexico it is not commonly The pupa is dark brown and develops found in the state of Michoacan (Gallegos, in the tunnel, its head facing the opening 1983). In Peru, S. catenifer affects avocado (De Villiers, 2001b). The adult of S. obsolescens orchards located close to the jungle or near (Pinhey, 1975) has a variegated pale and dark the coast. In Guyana, it also attacks Chloro- brown thorax. The abdomen is grey with cardium rodiei (Lauracea) (Cervantes et al., prominent black or brown dorsal tufts near 1999). The avocado seed moth can perforate

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95% of the fruits, depending on the type of by Meyrick (1913). This species was trans- cultivar attacked (Arellano, 1975, 2000). ferred to the genus Cryptophlebia by Clarke The adult is 1 cm long, a yellow-ochre (1958). Gunn (1921) reported the biology, moth showing sexual dimorphism. Moths will ecology and control of the false codling regularly mate 2–3 days after emergence and moth on citrus, guava and avocado. can live up to 10 days. One day after mating, According to De Villiers et al. (1987b) the female deposits as many as 240 eggs on the and Joubert and Du Toit (1993), a tiny hole is crevices of the fruit. Boscan and Godoy (1984) visible where the larva penetrates the skin of determined the life cycle of this insect. The egg the avocado fruit. This is usually surrounded is 0.6 mm long, oval and light green. The egg by a white powdery substance. A small feed- ecloses in 5–6 days, the larva penetrates the ing tunnel is made just beneath the skin but fruit and consumes the seed in 20 days. There large larvae are seldom found. Kok (in Milne, are five instars. Early instars are whitish, 1973a,b; Gunn, 1918) mentions that an adult while late instars are pink or reddish. The false codling moth has been reared only once, larval stage lasts 16–21 days and the pupal in that case from an avocado seed. ‘Pinkerton’ stage lasts 11–19 days. The life cycle lasts avocados which had been interplanted with between 44 and 49 days with three complete maize were extensively damaged by false cod- generations per year. The highest damage is ling moth after the maize was sprayed with observed from May through August. cypermethrin (Joubert and Du Toit, 1993). In Brazil, Apanteles spp. are reported The false codling moth has a wide range as parasites and in Panama, Xiphosomella of indigenous host plants from which culti- stenomae Cushanan (Gallegos, 1983). Boscan vated crops have been invaded (Catling and and Godoy (1982) reported that Apanteles spp. Aschenborn, 1978). A. Schwartz (1981, unpub- were responsible for 30% of the parasitism lished) listed some 14 indigenous and 21 when a high percentage of trees (80%) were cultivated host plants in South Africa, includ- infested with S. catenifer. Chelonus spp. (Braco- ing citrus, guava, litchi, macadamia, pecan, nidae) and Eudeleboea sp. (Ichneumonidae) mango and, occasionally, avocado. Further- parasitize S. catenifer in Guyana (Cervantes more, it is also a pest of peaches (Daiber, 1976), et al., 1999). In Mexico, insecticides should acorns, almonds, olives, tea seeds and walnuts be applied at least 12 times in order to be (Catling and Aschenborn, 1978). In Israel, it is effective. In Peru, the best control is afforded a pest of macadamia (Wysoki et al., 1986). by removal of infested fruit. Freshly laid eggs are pearl-white and translucent, turning slightly reddish with a black spot shortly before hatching. The × Tortricidae 0.77 0.60 mm egg is oval and flattened, with a reticulate sculpture. Eggs are laid singly on False codling moth, Cryptophlebia fruits and nuts and, according to Gunn (1921), leucotreta (Meyrick) also on guava leaves. The first instar larva is cream-white with The false codling moth was first reported as a dark brown head and is about 1.5 mm in a pest of citrus in KwaZulu, Natal (Fuller, length. The full-grown larva is pinkish red 1901). It was also reported to attack citrus in with a brown head and it is 12–15 mm in other parts of South Africa (Howard, 1909). length. The pupa, which is dark brown, is According to Hill (1975), the false codling formed in a silken cocoon in the soil. The adult moth is distributed in both tropical and is inconspicuous, with mottled dark grey southern temperate regions in Ethiopia, coloration (Gunn, 1921; Daiber, 1979; A. Senegal, the Ivory Coast, Togo, Upper Volta, Schwartz, 1981, unpublished). down to South Africa and also in Mauritius According to Newton (1998), the sex ratio and Madagascar (Angelini and Labonne, of field populations is close to unity. Females 1970; Reed, 1974). The false codling moth, mate shortly after emergence and pre- previously known as Carpocapsa sp. (Fuller, oviposition lasts 5–6 days in the field and 1–2 1901), was described as Argyroploce leucotreta days in laboratory cultures. Multiple mating

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takes place in both sexes (A. Schwartz, 1981, Ullyett, 1939; Thompson, 1946; G.J. Begemann, unpublished). Daiber (1980) found an average 1994, personal communication). fecundity of 456 eggs at a constant 25°C and 87 Rhynochorus albopunctatus (Stol) and Orius eggs per female at 15°C. Five days after moth sp. and Pheidole megacephala F. have been emergence, a peak of 29 eggs per female was recorded as predators of the false codling observed at 20°C. Peak egg laying occurs dur- moth (Omer-Cooper, 1939; Steyn, 1954; ing the first night of the oviposition period, Newton, 1998). Beauveria bassiana (Balsamo) which is normally 2 days after emergence. Vuillemin has often been recorded in pupae It was estimated that five generations can found on leaf litter (G.J. Begemann, 1994, develop per year in the Pretoria area (Daiber, personal communication). It has also been 1980). Adults live between 2 and 3 weeks in reported that infection by an unidentified the field (Ripley et al., 1939). In an unsprayed granulosus virus may destroy complete citrus orchard, the peak flight activity batches of larvae in laboratory cultures was found to take place in November and (A. Schwartz, 1981, unpublished). February/March (A. Schwartz, 1981, unpub- Catling and Aschenborn (1974) recom- lished). Adults are not attracted to light traps mended augmentative or inundative releases (Gunn, 1921; Catling and Aschenborn, 1978). of the egg parasitoid T. cryptophlebiae. This A female pheromone was isolated by method, practised with strict orchard sanita- Read et al. (1968, 1974) but it was later con- tion, brought a very high infestation of false cluded (Newton and Mastro, 1989; Newton codling moth down to a lower equilibrium et al., 1993) that true sex pheromones are com- (Schwartz et al., 1982). However, other results prised of several structural optical isomers. have been unpredictable and often unsatisfac- However, bioassays of various combinations tory (Newton et al., 1986). of pheromones from Malawi and the Ivory Although T. cryptophlebiae were seen Coast have not excluded the possibility of to disperse up to 1.3 km in a habitat devoid geographical variation (Attygalle et al., 1986; of host plants (Van den Berg et al., 1987), Newton, 1998). movement within a citrus orchard is limited According to Gunn (1921), the life cycle (Newton, 1988b) to the extent that hetero- on guavas in the Pretoria area (commencing in geneous population densities have a critical January/February) takes an average of 152 impact on the performance of the parasitoid days. Incubation takes from 11 to 14 days, from orchard to orchard. larval development from 59 to 71 days, the According to current information on prepupal stage from 21 to 30 days and the the distribution of natural enemies of the pupal stage from 43 to 66 days. A. Schwartz false codling moth, the prospects for classical (1981, unpublished) found that when fed on biological control are poor (CIBC, 1984). New- artificial medium at 25°C, the false codling ton (1998) is of the opinion that parasitoids moth completes its development in 28 days. of other Cryptophlebia spp. from places like Catling and Aschenborn (1974) report Australia, Fiji, Hawai, India and Taiwan may that parasitism by Trichogrammatoidea crypto- be sources for the introduction of parasitoids phlebiae Nagaraja may increase from January into southern Africa. Orchard sanitation, onwards, resulting in between 59% and 89% recommended by Fuller (1901) and Gunn parasitism for the rest of the season. The (1921), is still one of the most important egg-larval parasitoid, Chelonus curvimaculatus methods of reducing damage by the false Cameron (Braconidae), has been reported by codling moth. Nothing has been registered for Searle (1964) and Broodryk (1969). A number chemical control of the false codling moth on of larval parasitoids have been recorded avocado. in southern Africa, namely the ichneumonid Apophua leucotretae (Wilkinson), the braco- Western avocado leafroller, Amorbia nids Agathis bishopi Nixon, Agathis leucotreta cuneana Walsingham (Nixon), Bassus sp., Phanerotoma curvicarinata Cam., the chalcid Oxycoryphe edax Waterston The western avocado leafroller is a sporadic and an unidentified tachinid (Ford, 1934; pest of avocados in California and Mexico.

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The A. cuneana larva rolls and feeds on the spring by looking for leaf roll in young foliage folded edge of the leaves. The injury can be and feeding damage in mature fruit. There extended to superficial feeding on fruits, are no established thresholds for chemical frequently when two fruits are close together, control. Bailey and Olson (1990b) reported causing economic losses (Bailey and Olsen, Lannate and Orthene to be the most effective 1990b; Coria-Avalos, 1993). pesticides if applied by ground equipment. Adult female moths lay light green, oval- The egg, larval and pupal stages of shaped, overlapping flat masses of 5 to 100 Amorbia are parasitized by a variety of eggs. Eggs are generally laid on upper leaf beneficial insects. The most important egg surfaces close to the midrib, hatching within parasitoid is Trichogramma platneri Nagarkatti. 13 to 15 days. Newly hatched larvae are Results of a preliminary study by Oatman yellowish green and gradually turn darker and Platner (1985) showed at least 87% para- green as they reach maturity. Amorbia larvae sitization of Amorbia eggs. Fleschner et al. roll and tie leaves together with a silken web. (1957) reported Elachertus proteoteraris This forms a shelter or nest in which the larva Howard, and an ichneumonid parasitizing feeds on leaves and fruit and is protected from the larvae of Amorbia, and the tachinid, pesticide applications. Larvae go through five Phorocera erecta Coq., parasitizing the pupae. instars, and pupate in leaf rolls. The pupal stage lasts about 17 days. Adult moths are Apple leafroller, Tortrix capensana (Walker) bell-shaped, with a wingspan of about 2.5 cm. Adults are active at night. Female moths In South Africa, the apple leafroller was deposit 400–500 eggs over the course of 2 or recorded on citrus as early as 1947 (Taylor, 3 weeks (Faber and Phillips, 2001). 1957). T. capensana is a species indigenous Young Amorbia larvae typically feed only to the Ethiopian region (Pinhey, 1975) that on the surface of avocado leaves, leaving occurs throughout Africa (Begemann et al., a thin brown membrane or skeleton of leaf 1998). T. capensana is polyphagous and feeds veins. Mature larvae consume the whole leaf. on trees indigenous to southern Africa, However, mature avocado trees can tolerate weeds, and fruit trees such as apple, apricot, considerable leaf damage by the Amorbia citrus, peach, pear and plum (Matthew, 1975; larvae without severely affecting tree growth Barrow and Bedford, 1998; Begemann et al., or fruit yield. Nevertheless, fruit damage may 1998) as well as on avocado (Van den Berg occur where the larval web leans against fruit, et al., 1999). The larva spins leaves or fruit or where webs are made between touching together to form a protective niche where it fruit. Larvae may feed on fruit skin and cause feeds on those leaves or fruit. In most cases, scarring, resulting in severe downgrading or only the peel of the fruit is fed on, resulting in culling (Faber and Phillips, 2001). In Califor- its downgrading. In a survey carried out nia, Hoffman et al. (1983) tested two compo- in the Nelspruit-Hazyview region (South nents of the sex pheromone of A. cuneana, Africa), Erichsen and Shoeman (1992) found (E,Z)-10,12 and (E,E)-10,12 tetradecadien-1-ol that the apple and citrus leafrollers together acetate (McDonough et al., 1982) and obtained had damaged 0.34% of avocado fruit during optimum trap catches with an isomer content the previous season. This represented a of 29 to 82% EZ (as a percentage of EE + EZ) calculated loss of US$14,000. and dosages of 0.06 to 1.7 mg per rubber Overlapping eggs are laid in oval egg septum. Later, Bailey et al. (1988) tested a masses on the dorsal leaf surface (Begemann combination of the two components – et al., 1998). Freshly laid eggs are a dull yellow- (E,Z)-10,12 and (E,E)-10,12 tetradecadien-1-ol cream which changes to a yellow-orange acetate – at a 1 : 1 ratio and at a 9 : 1 ratio to before hatching. The newly hatched larva is trap populations of A. cuneana. The difference pale yellow with a black head. As the larva in moth response led them to believe that ages, the body darkens to a yellow-green. Five populations represented different species or instars occur in males and six in females, different races of A. cuneana. Faber and Phil- reaching 20–25 mm in length (Begemann et al., lips (2001) suggest monitoring larvae in late 1998). Pupation takes place in the tree in leaves

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Pests and Pollinators of Avocado 251

that have been webbed together. Female 0.34% of avocado fruit, representing a calcu- pupae are, on average, 11 mm long, males lated loss of 78,700 rand (US$14,000) for the 9 mm (Begemann et al., 1998). season (Erichsen and Schoeman, 1992). Both male and female adults are brown, The eggs of the citrus leafroller are laid on with varying patterns of a darker or lighter the leaves in compact, oval-shaped masses colour on the forewing. At rest, the female of between 20 and 176 eggs (Newton and is on average 13 × 7 mm, the larger male Catling, 1998). Early larvae are pale orange form 10 × 5 mm, the small form 6 × 4 mm with a darkly pigmented brown head capsule (Begemann et al., 1998). (Newton and Catling, 1998), turning pale Development averages 10 days in green later (Van den Berg et al., 1999). Accord- summer and 21 days in winter. At 26°C, male ing to Newton and Catling (1998), the insect larvae complete their development in 18–29 usually pupates in the rolled leaves; the pupa days, female larvae in 18–29 days, and the is dark brown. The adult’s anterior wings are pupal stage lasts 8–12 days. The duration from overall brown with two oblique bands and a egg to egg is 41–73 days (Begemann et al., darker area at the apex (Newton and Catling, 1998). Six generations of T. capensana occur 1998). The anterior margin is curved (bell- annually in citrus orchards in South Africa, shaped), more strongly in the female than the first and second being the most important in the male. The posterior wings are bright (Begemann et al., 1998). orange. The female of A. occidentalis has a A considerable number of natural wingspan of 24 mm, whereas the male is enemies of the apple leafroller have been considerably smaller. recorded. Trichogrammatoidea lutea Girault Working on citrus, Newton and Catling was found to parasitize T. capensana eggs on (1998) found that climatic conditions during citrus (Begemann et al., 1998). Barrow (1977) the summer months, and particularly the reared the following parasitoids from T. abundance of young leaves and fruitlets at the capensana larvae: Apanteles sp. (Braconidae), beginning of the season, led to high popula- Goniozus sp. (Bethylidae) and Pediobius tions later on. The insect has no dormant stage, amaurocoelus (Westwood) (Eulophidae). Pupal but survives through winter at low popu- parasitoids include Nemorilla afra Curran lation levels on citrus and alternative host (Tachinidae), Theronia sp. (Ichneumonidae) plants. Avocado fruit is damaged mostly from and Brachymeria boranensis Masi (Chalcididae) January to April (Van den Berg et al., 1999). (Barrow, 1977). Nothing is registered to con- Parasitoids reported from this pest trol leafrollers on avocado in South Africa. (Newton and Catling, 1998) include Brachy- However, Bacillus thuringiensis var. kurstaki meria microlinea (Walker), B. boranensis Masi Berliner is registered for leafrollers on citrus (Chalcididae), Apanteles spp. (Braconidae) and (Krause et al., 1996). Pristomerus sp. (Ichneumonidae) (Prinsloo, 1984; Newton and Catling, 1998). Because the Citrus leafroller, Archips occidentalis parasitoids of the citrus leafroller keep the (Walsingham) pest in check, chemical intervention is usually not necessary. The citrus leafroller has been recorded as a significant pest of citrus in Swaziland and Other leafrollers as an occasional pest on citrus in some parts of South Africa (Newton and Catling, 1998). The brown-headed leafrollers, Ctenopseustis On avocado, the larva of the citrus leafroller obliquana (Walker) and C. herana (Felder and spins leaves or fruit together to form a protec- Rogenhofer), are the major pests of avocados tive niche, where it feeds. Damage to the fruit in New Zealand. A complex of six leafroller (Van den Berg et al., 1999) is characterized by species, which feed on both foliage and fruit, large epidermal lesions which lead to fruit can cause up to 30% rejection of fruit for degradation. A survey in the Nelspruit– export from unsprayed orchards. An average Hazyview region of South Africa indicated of seven insecticide applications per year are that the citrus and apple leafrollers damaged used in most commercial orchards to combat

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the pests (Stevens et al., 1996, 1998). Frequent molle), Acacia sp., Pappea sp., Rhus sp., wattle, applications of Bacillus thuringiensis have willow and Ziziphus sp. (Pinhey, 1975). It been shown to provide acceptable control is considered to be of minor importance of these pests despite the increased cost on avocado, coffee and macadamia in certain associated with the additional sprays: the parts of Africa (De Villiers, 2001a). advantage of being able to pick fruit immedi- On avocado, the larvae feed on the skin of ately after spraying outweighs the extra cost young and mature fruit. Young larvae gnaw (Stevens, 1997, 1999). on the skin of the fruit superficially while on mature fruit the lesions on the skin caused by full-grown larvae are deeper, slightly pene- Gracillariidae trating the fruit flesh (De Villiers and Van den Berg, 1987a). In South Africa, Erichsen and Schoeman (1994) found the greatest damage In Mexico, Gracillaria perseae Busk is con- by the citrus looper on cultivar ‘Edranol’, sidered a pest in the states of Oaxaca and followed by cultivars ‘Pinkerton’, ‘Hass’, Veracruz (Gallegos, 1983). The adult is 2–3 ‘Fuerte’ and ‘Ryan’ (De Villiers, 2001a). mm in length with whitish cream-coloured Braconid larval parasitoids include Rogas wings; the larvae mine the tender leaves, spp., Cardiochiles sp. and the ichneumonid causing deformations; however, very seldom Charops sp. (Schoeman, 1998). Dipterous do they cause defoliation. In general, G. perseae parasitoids include Peribaea cervina (Mesnil), is not considered an important pest. There is Exorista sorbillans (Wiedemann), Sturmia no knowledge of its life cycle or natural ene- imberbis (Falten), Pales coerulea (Jaennike), and mies (Gallegos, 1983). In Peru, Phyllocnistis Muscina stabulans (Falten). An entomopatho- spp. (Lepidoptera: Gracillariidae) can reduce genic fungus, Beauveria bassiana (Balsamo) tree vigour by mining on the leaves, whereas Vuillemin, also attacks the larvae (Schoeman, in Florida, Phyllocnistis spp. are considered a 1998). minor pest problem. Apanteles n.sp. (Braconidae) and Sympiesis dolichogaster (Ashm.) (Eulophidae) have been Avocado loopers – Anacamptodes defectaria reported to parasitize G. perseae in Cuba. (Guenée), Epimeces detexta (Walker), Epimeces matronaria (Guenée), Oxydia vesulia transponens (Walker), and Sabulodes aegrotata Guenée Geometridae Several loopers, namely E. detexta, E. matro- Citrus looper, Ascotis reciprocaria naria, A. defectaria (Guenée) and O. vesulia reciprocaria (Walker) transponens, feed on avocado leaves in Florida, while S. aegrotata is reported The citrus looper was recorded in South in California (Bailey and Hoffman, 1979). Africa in the early 1940s by Bedford (1943). In Florida, the most common of these is It was also recorded on avocado in 1974 E. detexta, a medium-sized grey or greyish (De Villiers, 2001a). A. reciprocaria reciprocaria white moth. Young larvae are 0.6 cm or less has been recorded in equatorial Africa, in size, usually grey or greyish black. They Cameroon, Malawi, Uga, South Africa, Zaire, grow rapidly to 3–4 cm in length. Older Zambia and Zimbabwe. Besides citrus, larvae are generally tan or greenish yellow in avocado, coffee (Robusta and Arabica) and colour. E. detexta and S. aegrotata larvae also macadamia, the citrus looper has a wide feed on flower panicles, even fruit, but prefer range of host plants (Le Pelley, 1968; the tender growth in the upper part of the Hill, 1975; De Villiers, 2001a). According to tree (Bailey et al., 1986). In Florida, looper Schoeman (1998), 78 plant species, including infestations appear to be somewhat seasonal 62 indigenous and 16 exotic species, are hosts and are more severe in spring and summer, of the citrus looper larva. Examples of these generally becoming less of a problem in are boxwood, kei apple, pepper tree (Schinus autumn and winter. The adult E. detexta is

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short-lived, and mates and oviposits soon populations and prevents outbreaks (Waite after emergence from the pupa. Eggs are laid and Pinese, 1991). in narrow elongated masses, preferentially on needles of Australian pine (Casuarina sp.), Cleora inflexaria Snellen, Lophodes sinistraria and they hatch in about 5 days. The larvae (Guenée), and Eucyclodes pieroides (Walker) grow rapidly and pupate 17–22 days after egg hatch. The pupal stage can last 10 days. Thus In Australia, the grey looper, Cleora inflexaria a full generation is expected to last between Snellen, the brown looper, Lophodes sinistraria 34 and 37 days. Pupae drop to the ground (Guenée), and the bizarre looper, Eucyclodes and the adult emerges in 12 days to start pieroides (Walker), as well as the orange fruit the cycle again. Some avocados are culled borer, Isotenes miserana (Walker) (Tortricidae), because of damage from feeding on the fruit are all minor pests which occasionally attack by two or three kinds of small caterpillars the fruit. (Peña and Johnson, 1999). Bailey et al. (1986) determined that the The giant looper, Boarmia (Ascotis) selenaria compound 6,9-nonadecadiene provides maxi- Denis and Schiffermuller mum trap catch of S. aegrotata males. Lannate 90 WP, lannate 1.8 L, permethrin (Pounce 3.2 In Israel, the giant looper is the most impor- EC, Ambush 2 EC) and Bacillus thuringiensis tant pest of avocado in regions where cotton Berliner preparations are recommended in is grown. It produces five generations a year, Florida for control of the avocado looper of which the most destructive are the first (Peña and Johnson, 1999). (spring) and second (early summer) (Wysoki Native natural enemies of E. detexta and lzhar, 1986). Its reproductive behaviour include the predators Calleida decora was studied by Hadar (1983). (Fabricius) and Podisus maculiventris (Say). A long list of natural enemies of the giant Alcaerrhynchus grandis (Dallas), Parapanteles looper in Israel was compiled in earlier sp. and Trichospilus diatreae Cherian are publications (Wysoki and lzhar, 1980; Swirski natural enemies of E. matronaria, A. defectaria et al., 1988). Spiders contribute to some extent and O. vesulia transponens, respectively (Peña to biocontrol of the pest (Mansour et al., 1985), et al., 1996). Several attempts to introduce whereas Apanteles cerialis Nixon (Braconidae) exotic biological control agents, e.g. Telenomus parasitizes young caterpillars, providing the sp. and Trichogramma platneri Nagarkatti, highest parasitization (70%) in October and failed (H. Glenn, personal communication). November (Wysoki and lzhar, 1981). Tachinid In Peru, Sabulodes caberata Guenée is flies (Tachinidae), Compsilura concinnata common on orchards located near the jungle. Meigen and Exorista nr. sorbillans Wiedemann Even though it may cause some defoliation, attack late instars of the giant looper and para- its attack is not frequent enough to demand sitization reaches its peak in late summer the application of chemicals. or autumn. Local egg parasites of the giant looper have not been recorded in Israel. Thus, two exotic wasps, Ooencyrtus ennomophagus Ectropis sabulosa Warren Yoshimoto (Encyrtidae) and Telenomus also- E. sabulosa can be a serious pest in north philae Viereck (Scelionidae), were introduced, Queensland, Australia, where it feeds on unsuccessfully (Wysoki and lzhar, 1980). leaves. It can completely defoliate trees, Approximately 16 million Trichogramma exposing fruit and resulting in sunburn. It platneri Nagarkatti (Trichogrammatidae) can also cause severe damage to fruit when were released from 1988 to 1990 in the avo- it feeds on the skin. Infestations are more cado groves but have not yet been recovered severe near windbreaks and good control in (Wysoki et al., 1988). In Israel, natural enemies an orchard can be obtained by spraying suppress giant looper populations in the avo- just a few rows near the windbreak, thus cado groves effectively, but in regions where sparing the parasitoid Apanteles sp. nr. cotton is widely grown, pesticide-induced vitripennis Curtis which normally suppresses outbreaks of the looper may occur owing to

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the disrupted balance with its natural enemies Psychidae by the drift of pesticides from aerially sprayed nearby cotton fields. Oiketicus kirbyi (Guild.) Infestations are controlled, when necessary, by preparations containing Bacillus thur- This insect is common in South American ingiensis var. kurstaki. Timing of the control avocado orchards. Eggs are deposited within measures is based on traps baited with virgin cases, eclosing in 30 days. Female larvae are females and on scouting the groves for young 60–70 mm long, while male larvae are 45–50 caterpillars. Since mass production of giant mm. The larva remains within the case and looper virgin females for monitoring pur- moves around, selecting new feeding places. poses is laborious and expensive, efforts The pupa develops within the case; when the were made to replace the virgin females adults emerge, the apterous female remains with synthetic pheromone. (Z,Z)-6,9-cis-3S, 4R within the case where it is fertilized by the epoxynonadecadiene and (Z,Z,Z)-3,6,9-non- male. Alate males are attracted by female sex- adecatriene were identified as sex pheromone ual pheromones. Later, the female deposits components (Becker et al., 1990). Bioassays the eggs in the case in which she spent her life performed by electroantennograph (EAG) in a and once the egg depositing is finished, she wind tunnel gave positive results, but in field dies (Sanchez, 1983). tests males were not sufficiently attracted Larval feeding on leaves causes almost to these two compounds (Becker et al., 1990). uniform 1 cm diameter holes. Likewise, Following experiments involving decapita- Oiketicus elongatus Saunders (Psychidae) tion of the giant looper and subsequent PBAN occasionally defoliates parts of individual injections, a third compound was revealed. trees. The ichneumonid Chirotica spp. (Ichneu- monidae) is its natural enemy.

Noctuidae Other lepidopteran defoliators American (cotton) bollworm, Helicoverpa armigera (Hübner) In Mexico, Copaxa multifenestrata (Heinrich- Shaffer) (Saturnidae) is considered a specific H. armigera is known in South Africa as the but minor pest of avocado. It feeds on older American bollworm. The true American leaves, whereas Papilio garanas garanas Hubner bollworm is the closely related Helicoverpa zea (Papilionidae) feeds on tender leaves and may (Boddie), which is not found in southern cause some economic damage (Hernandez Africa. H. armigera has been recorded et al., 2000). throughout Africa, Asia, Australia and Pyrrhopyge chalybea Scudder (Hesperi- Europe (CIE, 1967). idae), or the confetti worm, eventually defoli- Chelonus curvimaculatus Cameron (Braco- ates avocado trees by making holes in the nidae), a Pales sp. and a Drino sp. (Tachinidae) leaves. The adult deposits its eggs on the were found as parasitoids of H. armigera on cit- foliage, eclosing within 20 days; the neonate rus in Rustenburg, South Africa (Vermeulen larva chews a circular hole in the leaf, folding and Bedford, 1998). Other parasitoids, and hiding in the damaged area; the larva is Telenomus ullyetti Nixon (Ichneumonidae), active during the night. Two generations are Trichogrammatoidae lutea Girault (Trichogram- observed per year, the first occurring in March matidae) (Parry-Jones, 1937) and Paradino halli and the second in August. (Curran) (Tachinidae) (Parry-Jones, 1938) were The pine emperor, Imbrasia cytherea (F.) also found from this host feeding on citrus at (Saturnidae), is an important defoliator of Mazoe. According to Vermeulen and Bedford Pinus spp. It also attacks a few other exotic and (1998), the indigenous natural enemies are a large number of indigenous plants (PPRI, not able to control the periodic outbreaks of 1970). The subspecies Imbrasia cytherea clarki H. armigera. Geertsema feeds on avocado leaves in Africa

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(Van den Berg, 1973). In Africa, I. cytherea clarki ORDER DIPTERA has been found from Zimbabwe to KwaZulu- Natal in the south. The other subspecies, Tephritidae I. cytherea cytherea (F.), occurs further south in the Eastern and Western Cape Provinces Fruit flies – the Mediterranean fruit fly Ceratitis (Geertsema, 1971). I. cytherea clarki larvae are capitata (Wiedemann), the Natal fruit fly present from March to October, with damage Ceratitis rosa Karsch, and the Marula taking place during the driest and coldest fruit fly Ceratitis cosyra (Walker) months of the year. The egg stage lasts from 26 days at 20°C to up to 84 days at 14°C. In the The Mediterranean fruit fly enjoys a cosmo- field, at approximately 15°C, the five larval politan distribution (Kok and Georgala, 1978; instars are completed in about 100 days. Pupa- Barnes, 1983; White and Elson-Harris, 1992). tion takes place in the soil beneath the trees. According to White and Elson-Harris (1992), The pupal stage lasts about 8 months, mainly the Marula fruit fly and the Natal fruit during the summer (Van den Berg, 1975). fly are widespread throughout Africa. The In Brazil, Papilio scamer scamer (Boius- Mediterranean fruit fly has been recognized duval) and Saurita cassra (L.) can cause serious as a problem for avocado in Central America injury to avocado leaves. P. scamer scamer is a (Mitchell et al., 1977) and appears in Australia brown moth, approximately 80 mm in length. and Israel as well (Ebeling, 1959). It has been S. cassra is a 30-mm-long brown moth. The cat- shown that fruit fly maggots do not develop erpillars of the first species are whitish brown in the avocado fruit of commercial cultivars and during their later instars change to a green under normal orchard practices (De Villiers colour. Larval instars of S. cassra are predomi- and Van den Berg, 1987a; Du Toit and nantly dark in colour (Medina et al., 1978). De Villiers, 1990). Furthermore, the avocado Fornazier et al. (1997) suggested that is not considered an ideal host for fruit fly the cultivars ‘Ouro Verde’, ‘Primavera’ and development (Brink et al., 1997). There are, ‘Briosqui’ are the least attacked by an however, isolated instances in which larvae unidentified Geometridae. were found in over-ripe avocado fruit rotting on the ground underneath the trees. In Hawaii, Armstrong et al. (1983) showed that Sharwil avocados could only be infested Natural enemies of lepidopteran defoliators with C. capitata if fruit flies were confined to artificially damaged avocado fruit in cages on Gallegos (1983) reported that in Mexico, the tree. These authors concluded that avoca- Trichogramma fasciatus Perkins spp. have been dos harvested with the stem attached and pro- collected parasitizing eggs of Pyrrhopyge tected from postharvest fruit fly infestations chalybea Scudder, and the Eupelmidae present no danger of fruit flies entering Anastatus spp. have been found parasitizing another country. However, avocado fruit can its larva. The most important natural enemies be damaged by the ovipositor of the fruit fly of I. cytherea clarki include the eupelmid egg when it lays its eggs. These holes develop parasitoid Mesocomys pulchriceps Cameron, into typical cracks or star-shaped lesions three other egg parasitoids, and larval and (Du Toit et al., 1979). Such damage has also larval-pupal parasitoids. The most effective been observed on some commercial varieties predator of I. cytherea clarki was found to be in Israel. the Cape chacma (CK SP) baboon, Papio The first report on C. capitata on avocado ursinus (Kerr). Other important predators fruit in Israel was from Rivnay in 1936, with include the vervet monkey, Cercopithecus almost all the fruit being infested (Ebeling, aethiops (L.), and birds such as the Cape 1959). Later, it came to be considered a major raven, Corvultur albicollis (Latham). Further- pest of cultivated fruits (Avidov and Harpaz, more, viruses and three species of fungi were 1969) and avocado was listed as a host found to attack the larvae and pupae (Van among other subtropical fruits by Swirski and den Berg, 1974). Arenstein (1970) and mentioned as a host of

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C. capitata by Freidberg and Kugler (1989). (Du Toit, 1998). Du Toit (1998) suggested that Recently, infestations have been reported on plants that serve as alternative host plants cv. TX-531 and on newly introduced summer for fruit flies be eradicated. These include varieties (S. Ben Yehuda, personal communi- bug weed, bramble and wild-growing guavas. cation). Adults of these fruit flies have clear Secondly, routine orchard sanitation should wings with light and dark brown dots and be carried out. Thirdly, monitoring adult fruit brownish veins. The wings are mostly held in flies using traps baited with sex pheromones a drooping position (Du Toit, 1998). would determine when a population build-up The Natal fruit fly is the largest of the occurs. In most countries, baiting is carried three species (6.0 mm in length), followed by out with either mercaptothion or trichlorofon, the Mediterranean fruit fly (4.5 mm) and the applied with sugar or a solution of protein Marula fruit fly (4.0 mm). The thorax of the hydrolysate. Natal fruit fly is dorsally greyish brown, with small black and white patches posteriorly and Bactrocera spp. a white patch on either side. Natal fruit fly males have black feathery bristles on their In Australia, the Queensland fruit fly, middle pair of legs. The thorax of the Mediter- Bactrocera tryoni (Froggatt), attacks avocado ranean fruit fly is black with ivory white fruit from the time it is about half-size. The markings while the thorax of the Marula fruit damage from oviposition causes small star- fly is brown with three relatively large shiny shaped cracks in the skin. This damage is black spots on each side and two smaller ones only aesthetic, as the eggs do not hatch in further back (Van den Berg et al., 1999). the hard, green fruit. Although they will According to Du Toit (1998), the eggs sting rough-skinned cultivars (e.g. Hass), the of fruit flies are white, about 1 mm long damage is usually not visible and is of no and banana-shaped. They are usually laid consequence. However, in cultivars ‘Fuerte’, in clumps in the fruit. Larvae are broad and ‘Wurtz’ and ‘Rincon’, the scars are quite truncate in the rear, tapering anteriorly to a noticeable and sprays may be required to point. The larvae are creamy white and up to prevent excessive damage. Cover sprays 9 mm long. The mature larva has the ability to of dimethoate have been used, but in an flex itself and make short jumps. Pupation integrated system protein autolysate bait takes place in the soil. The puparium is brown, sprays are effective and the preferred option cylindrical and up to 6 mm long. (Waite and Pinese, 1991). Depending on the presence of hosts and Fruit flies of the Bactrocera dorsalis com- on climatic conditions, up to 15 generations plex, probably B. philippinensis and B. papayae, can be completed per year (Du Toit, 1998). attack avocado fruit produced in the Philip- Adults overwinter in evergreen shrubs and pines (Drew and Hancock, 1994). A variety of trees (Ripley and Hepburn, 1930). Adult thin-skinned types are grown throughout the populations reach peak numbers in the late islands and have been found to be infested summer and autumn (Du Toit, 1998). Most of with fruit fly larvae (G.K. Waite, 1999, the damage to avocado fruit is done during personal communication). these periods. The larval parasitoids Opius concolor Anastrepha spp. Szepligeti, O. humilis Silvestri (Braconidae) and a pupal parasitoid Trichopria capensis In Mexico, Enkerlin et al. (1993) found that Kieffer (Diapriidae) attack C. capitata and C. under artificial laboratory conditions, the rosa (Searle, 1964; Annecke and Moran, 1982). fruit fly species Anastrepha serpentina Wied., Futhermore, Tetrastichus sp. (Eulophidae) was A. ludens Loew and A. striata Schiner infest reared from the pupae of both C. cosyra and cv. ‘Hass’. However, under field conditions, C. rosa (Grové, 2001b). Pheidole megacephala F. ‘Hass’ avocados were not infested by fruit is a predator of C. capitata (Searle, 1964). flies. Therefore, it is doubtful that these fruit Fruit flies can only be controlled success- flies would use ‘Hass’ avocado as a normal fully if a combination of actions is taken host.

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ORDER COLEOPTERA about 5 mm long when fully grown. They pupate in the soil. Their life cycle takes about Chrysomelidae 2 months, with three to four generations occurring annually. Adults emerge after rain Avocado beetles – Monolepta apicalis (Fay and De Faveri, 1990). M. apicalis is active (Sahlberg), Monolepta australis (Jacoby) in avocado orchards in the early mornings. and Monolepta bifasciata Hornst During the warmer parts of the day, the insect seeks shade underneath the leaves and Since early 1990, the avocado beetle M. on shady stems. When disturbed, M. apicalis apicalis has been a pest of avocado orchards, will hide behind the leaves or drop and fly mostly in the higher lying areas, in the away. Kiepersol region of South Africa. The infesta- In Kiepersol, South Africa, M. apicalis was tions were more severe in orchards situated noticed in avocado orchards in 1992 and 1993. next to blue gum plantations and natural In a heavily infested orchard, 50–100 insects vegetation. M. apicalis was also reported in per young tree were counted. During 1998, two other areas in the Mpumalanga Province the insect was still present, but in very small of South Africa (Claassens, 2001). M. apicalis numbers. The crop loss due to M. apicalis also occurred as a sporadic pest in South Africa varied on individual trees from about 5% up for two seasons. It fed on avocado twigs, to 100% (Du Toit and Claassens, 1993; Erich- leaves, leaf stalks and fruit. In certain sen et al., 1993). Monolepta spp. are especially instances, the epidermis of the fruit was threatening because they produce an aggre- completely removed, causing a brown blem- gating pheromone and form swarms that can ish covering the entire fruit. Lighter damage invade an orchard and cause extensive dam- appeared as darkish holes of about 2 mm in age in a short period (Fay and De Faveri, 1990). diameter. Very young leaves were often eaten Insecticides such as carbaryl, dimethoate, completely, while older leaves were mainly endosulfan and trichlorfon have been used eaten from the ventral side, resulting in a effectively in Australia for the related Mono- skeletonized appearance (Claassens, 2001). lepta spp. (G. Waite, 1992, personal communi- M. apicalis was also recorded from Namibia in cation). Spot sprays may be adequate once Central Africa (G.L. Prinsloo, Plant Protection swarms are detected. In South Africa, scouting Research Institute, Pretoria, 1993, personal for beetles should begin in November, in the communication). M. bifasciata (Coleoptera: early morning or late afternoon, under cool Chrysomelidae) occasionally damages conditions when the beetles are more likely to foliage in the Philippines (Cendana et al., be on the upper side rather than on the under- 1984). The red-shouldered leaf beetle, M. side of the leaf (Erichsen, 1993). The beetles australis (Chrysomelidae) can defoliate trees aggregate on windbreaks of Eucalyptus when swarms descend on an orchard. In torreliana. Growers regularly control swarms Australia, the black swarming leaf beetle and on the windbreaks before they invade the avo- the brown swarming leaf beetle, Rhyparida cado orchard. Fay and Defaveri (1990) found spp., cause similar damage to avocado (Waite that numerous individual beetles present at and Pinese, 1991). Bridelia macrantha, litchi flowering (i.e. not in a swarming phase) were and macadamia leaves have been reported as actually beneficial for pollination. However, hosts of M. apicalis (Erichsen and Schoeman, when swarms invade, there is no alternative 1993). Other recorded hosts are Hibiscus but to spray, and action must be quick to trionum, Triumfetta rhomboidae, Sida rhom- prevent damage. Carbaryl and endosulfan are boidea and Protea spp. (Claassens, 2001). The most commonly used. adult M. apicalis is bright red with shiny black elytra. The insects vary from 3 to 5 mm. The Blue-green citrus nibbler, Colasposoma life history of M. apicalis has not been studied fulgidum Lefèvre in South Africa. In Australia, the closely related M. australis (Jacoby) lays eggs in the The blue-green citrus nibbler is indigenous soil. The larvae feed on grass roots and are to South Africa and has been collected on a

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variety of wild trees and shrubs (Webb, 1974). Bostrichidae It also feeds on avocado (Bedford, 1998a), guava (Joubert, 1936) and pecan (De Villiers Black giant bostrychid, Apate monachus et al., 1987a). Heavy infestations of C. fulgidum F. (Bostrichidae) occur on rare occasions and damage to the young leaves and avocado fruit is seldom The black giant bostrychid is found attacking serious. However, young fruit can be scarred, avocados in different South American and reducing the mature fruit’s marketability. Caribbean countries. The female of A. Eggs are about 0.9–1.0 mm long, cylindri- monachus oviposits on dry branches and cal and pale yellow. They are laid in egg trunks. The eggs are laid on areas lacking tree clusters which are mostly deposited on the cortex, at random, and they eclose in between extreme tips of leaves (Bedford, 1998a). The 7 and 8 days. The number of eggs per female egg stage lasts 2–4 weeks. Soon after the larva ranges between 64 and 106. Larval develop- has hatched, it falls to the ground, and enters ment lasts 67 days, the pupa 8 to 9 days, and the soil (Joubert, 1936). The newly hatched adults live for up to 40 days. They are active larva is about 1 mm in length (Bedford, 1998a) during the night and the two sexes are and 8 mm when mature. The larva has a whit- found copulating within the galleries during ish colour and an irregular translucent mark daylight hours. The complete cycle lasts 87 to on the posterior abdominal segments (Joubert, 190 days. In Brazil, Apate terebrans (Pallas) 1936). The larvae live in the soil at a depth of and Acanthoderes jaspidea (Germar) affect about 75 mm and the larval stage lasts an esti- branches, by ovipositing or sometimes by mated 9 months (Joubert, 1936). The pupa is larval boring and adult feeding (Medina et al., formed in a cell constructed of soil particles, 1978). Descriptions of adults are provided by and this stage lasts about 1 month (Joubert, Medina et al. (1978). The adults attack healthy 1936). The adults are mostly bright blue-green plants, they use their mandibles to construct or metalic green. They are 4.5 to 6.9 mm long their galleries within branches and the and 2.6 to 4.2 mm wide (Joubert, 1936). Soon trunk. Injured branches are recognized by after the adults emerge from the soil, they con- the yellowing of their leaves; these branches gregate on the foliage of indigenous trees such commonly break down easily. as the bush willow, Combretum erythrophyllum. A Bethylidae (Hymenoptera) and Clypto- Some of the females lay more than 400 doryctes (Braconidae) are registered as natural eggs and they live from about 2 to 4 enemies of A. monachus. months (Joubert, 1936). Two (or possibly three) unidentified species of parasitoids have frequently been bred out of C. fulgidum eggs Curculionidae (Bedford, 1998a). It is normally not necessary to control this minor pest on avocado trees. Conotrachelus perseae Barber, Conotrachelus aguacatae Barber, and Conotrachelus Other chrysomelids serpentinus (Klug)

In Brazil, Sternocolaspis quatuordecimcostata These three species of Conotrachelus are known Lefevre is a common pest of other fruit and or suspected pests of commercially grown forest trees. The greenish blue, 8-mm-long avocado fruits in Mexico and Central Amer- adult has longitudinal stripes on the elytra. ica, but are poorly understood. Taxonomic The female deposits its egg masses near the keys and diagnoses are given by Whitehead soil surface. The adults feed on new foliage (1979), expanding the information provided and green fruits; injury to fruits is character- by Barber (1919). Muñiz and Barrera (1958) ized by shallow grooves on the fruit epider- provide a taxonomic key that includes mis. The major peaks of this pest are observed species of Conotrachelus collected from during the rainy season in the state of tropical and subtropical America. São Paulo, between October and February C. perseae is a small, shiny, almost black (Medina et al., 1978). weevil not usually observed in orchards in

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which Heilipus lauri is prevalent. However, Muñiz (1960) and Diaz (1971). Major activity is it can cause up to 85% fruit loss. It is observed observed during the months of June and July. in the areas of Queretaro, Michoacan, Jalisco, However, Garcia et al. (1986) demonstrated Puebla, Morelos and Guanajuato. The adults that in the warm regions of Yautepec, the are 7 mm long, and they can copulate immedi- presence of adults is observed from May to ately after emergence. Adults are nocturnal, November; eggs could be collected between and remain hidden on folded leaves or in any July and January and pupae between June and crevices in the trunk (Plate 56). The adults February, while in the more temperate area of can attack newly formed fruits, and the Tetela del Volcan, adults are found between females deposit one to four eggs per fruit, but June and February, eggs are observed in sometimes the number can be as high as 70. September, larvae are found throughout the Eggs are whitish, and eclose in 7–10 days. The year and pupae from May to December. These larva develops in the seed and lasts 20–35 authors suspect that some of the weevils could days. The number of larvae per fruit can be as be diapausing as larvae from January to high as three or four. The larvae leave the fruit April. Canseco (1971) reports that C. aguacatae to pupate in the soil at a depth of 5 cm. The life spends the winter as an adult, hiding in the cycle from egg to adult lasts 42–75 days. The fallen leaves. During the spring, it moves to first generation starts in January and February the foliage in the tree and starts feeding on the and lasts approximately 10 weeks. The second leaves. Later on, the copula starts and as soon generation starts in April and ends in June or as the fruits are formed, they start feeding on July (Anonymous, 1991). The female prefers to them. Emergence of the adults coincides with oviposit in the stylar area of the fruit; more the first rains. Eggs are inserted in the fruit damage can be found in the lower tree canopy pulp by the females. After each egg deposi- than in the upper part (Hernandez et al., 2000). tion, the female seals the site with a gelatinous The latter authors recommend collection of substance. Each female will deposit 70 indi- fallen fruits, weed removal and fallowing vidual eggs. The eggs eclose within 7–10 days the soil to expose pupae. The only biocontrol and the larva bores through the pulp and agent observed to date is Beauveria bassiana seed. When it reaches the seed, the galleries affecting larvae and pupae. within the seed are sinuous. Close to the end of C. aguacatae causes economic losses in the the larval stage, it bores through the pulp area of Queretaro, Mexico, ranging from 20 to again and falls to the soil surface. It pupates 80%, depending on the control tactics used. inside the soil at 2.5–5 cm from the surface. Canseco (1971) explains that there is some The pupal stage can last 15–30 days. The num- confusion surrounding the distribution of the ber of overlapping generations is estimated at species C. perseae and C. aguacatae. The species two (Canseco, 1971). Gallegos (1983) reports C. aguacatae can be confused not only with that most of the infestations are found in C. perseae, but also with C. sapotae. However, small orchards where the regional cultivars the major difference is in the shape of the are grown without any type of pest manage- aedeagus. Canseco (1971) provides a detailed ment, while Coria-Avalos (1993) indicates that description of the different stages of C. agua- this pest can be found in orchards located catae. It is a stout reddish brown univoltine in warm climates. Damage is concentrated in weevil 4 mm in length that exhibits diurnal the upper half of the tree top (Salazar-Garcia activity. The female deposits its eggs on tender and Bolio-Garcia, 1992). Sticky green or blue branches, but it has been observed damaging traps are more attractive than white, yellow or older branches. The egg stage lasts 10–12 days, red traps. Hernandez et al. (2000) recommend while larvae can live up to 117 days. Pupae cutting and removing infested branches, then will develop in approximately 17–19 days applying organophosphates. Insecticides can andthe adults live for approximately 34–44 be applied to the soil to control the larva when days. Overall, one generation lasts 169–192 it falls to the ground or to control adults after days (Hernandez et al., 2000). An extensive their emergence. Aldrin is recommended, as taxonomic description of different stages of well as parathion (Canseco, 1971). Some chal- the weevil is provided by Kissinger (1957), cidoid wasps have been observed as active

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biocontrol agents of these weevils. However, information on development is provided the species have not yet been identified. Huerta by Salgado and Bautista (1993). In Mexico, et al. (1990) collected Camponotus sp. within the two generations are observed. The first occurs galleries made by C. aguacatae and speculated from January to August and the second from that Camponotus sp. could be preying on C. July to February (Anonymous, 1991). aguacatae. The same authors suggested that the species Oncophanes (Braconidae), Euderus (Eulophidae), Erythmelus (Mymaridae) and Heilipus catagraphus (Germar) Eurydinoteloides (Pteromalidae) could be associated with C. aguacatae. Steinernema feltiae In Brazil, H. catagraphus attacks branches of (= bibiones) Poinar provided 10% larval avocado. According to Lourencao et al. (1984), mortality, whereas Heterorhabditis heliothidis H. catagraphus also feeds on the epicarp and Khan, Brooks and Hirschmann provided avocado pulp without injuring the seed. The 45–75% mortality under laboratory conditions larva of this species attacks different plant (Huerta et al., 1990). species within the families Lauraceae and Annonaceae. An anonymous (1984a) report Large borer weevil, Heilipus lauri Bohemann recommends the use of CaCo3 to prevent H. catagraphus egg deposition. The large borer weevil damages up to 80% of avocado fruits, causing extensive fruit drop (Plate 57). It is distributed in Mexico in the states of Hidalgo, Morelos, Puebla, Veracruz Copturomimus perseae Hustache and Guerrero. The dark brown (with two In Venezuela and Colombia, C. perseae,a incomplete yellow bands on the elytra) adult small greyish weevil, 3.7–5 mm long with is 14–17 mm long, and emerges from the a black transversal band on the elytra, fallen fruits (Ebeling, 1950; Salgado and causes damage to branches and stems. Both Bautista, 1993). It can fly and regularly mates the larva and the adult bore through them. 2.5 months after emergence. The female The legless, curculionid larva is 10–12 mm deposits her eggs under the epidermis of the long and whitish. The damage is normally developing fruit, making a ‘half-moon’ punc- concentrated on the branches; infested ture. The small oval eggs are 1 mm long and branches show white dust exuding from the change from pale green to cream-coloured. galleries made by this insect; affected parts The female deposits one to two eggs per fruit exhibit slow dieback and eventually the tree −1 and a total of 36 eggs month . Twelve to 15 dies (Saldarriaga, 1977; Avilan et al., 1997). days after oviposition, the legless larva bores Cultural control, collecting and burning through the pulp into the seed, where it feeds infested branches, is the method suggested and spends its larval and pupal stages by Avilan et al. (1997). (Ebeling, 1950). The larva has five instars that last approximately 54–63 days. The late instar larva measures approximately 2.5 cm (Anon- ymous, 1984b). Arellano (1975) provides a Scarabaeidae key for the identification of H. lauri. The pupal stage lasts 15 days. Emerging adults In Peru, Oncideres poecila Bates (Coleoptera: feed on the foliage and live up to 4 months. Scarabaeidae) causes girdling of branches. In the case of fallen fruits, the larvae O. poecila deposits its eggs on fallen branches; sometimes leave the fruit and enter the soil to collection of these branches is recommended pupate. Because of larval feeding, rotting of to reduce the pest problem. Macrodactylus the pulp, mainly near its tunnels, and partial mexicanus Burmeister, a univoltine, highly or total rotting of the seed occur, eventually polyphagous insect is associated with resulting in premature fruit drop. The adult avocado and vegetation found in the hot feeds on leaves, buds and sprouts, as well and temperate areas of central and western as on the fruit (Ebeling, 1950). Further Mexico.

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Scolytidae in tree tissues. As a result, the portion of the tree terminal to the burrow entrance usually Corthylus, Aegeria and Xylosandrus species dies. White crystals of sap around the burrow entrances are evidence of infestation. Beetles In Mexico, Corthylus spp. are considered are brownish to almost black and small, about avocado pests. The adults are 1.2–4.3 mm 0.05 × 0.13 cm. Eggs and beetle larvae are long, with a stout body and colour that varies white and found in the galleries. Larvae feed from light brown or dark brown to black. on the mycelia of ‘ambrosia’ fungi growing in It displays sexual dimorphism; the females the galleries (Peña and Johnson, 1999). have a concave front with obvious setae, the antennal club is very large, its anterior margin decorated with a long tuft of setae. Eggs are white, translucent and elliptical. The Conclusions white larvae are legless and C-shaped. Pupae are exarate. Avocado pest management practices are Different species have two or more gener- affected not only by the domestic and export ations per year, depending on the altitude and fruit market, but also by consumer attitudes latitude conditions where they are found. The towards health concerns and the cosmetic males initiate attack by selecting trunks or appearance of the fruit. In general, avocado branches of live or recently cut trees. The male pest management is largely dependent on the makes an entry gallery and the initial part of use of pesticides. Costs of pest control, and one or both transverse oviposition galleries. the current lack of information and lack of The female mates with the male and enters the registration for a new generation of pesticides gallery. Here she digs two oviposition galler- (Wysoki et al., 1999), is complicating the con- ies that extend perpendicular to the axis of the tinuation or development of pest manage- trunk or branch, extending approximately 5 or ment programmes in avocado. From the 10 mm deep. The female makes a chamber information compiled herein, we can deduce where ambrosia fungi are inoculated. One egg that countries such as South Africa, Mexico, is deposited in each chamber. Upon emerging, Israel, Australia, and the USA are making an the larvae feed on the fungi that develop in the effort to maintain and develop avocado pest surrounding debris. management programmes. In Israel, the IPM Trunks or branches of weakened or felled system in avocado orchards (until the intro- trees are attacked. The greatest damage is duction of the orchid thrips) was based caused by the introduction of staining fungi on large-scale use of insect pathogens, in the wood. In Taiwan, ambrosia beetles augmentation of local natural enemies, and are reported to attack avocado trees in poor importation and acclimatization of exotic health. Maintaining the health of the tree natural enemies – parasitoids and predators. through good agronomic practice helps Other countries, such as New Zealand and reduce attack by these pests (Hung and Jong, Brazil, are either beginning to work towards 1995). this goal, or are accumulating basic informa- The avocado bark borer, Aegeria sp., feeds tion on the biology and life histories of the beneath the bark of avocado trees in the pests and describing damage inflicted to the Philippines. Sap may ooze from the wound crop, while no research is being conducted and branches may be weakened so that they on other aspects of pest management, i.e. eco- snap in strong winds. The pest is of minor nomic injury levels, monitoring, sampling, importance (Cendana et al., 1984). biological and autocidal control. In Florida, ambrosia beetles, Xylosandrus Some of the large differences in informa- sp., burrow into three trunks, stems and tion provided by different countries could branches. Infested trees are regularly stressed be based on economics. For instance, those before the attack, but frequently the trees countries, where avocado is a major source of appear to be healthy and vigorous. Fungi income for growers, i.e. the USA, Australia, accompany the beetles and develop mycelia Israel and Mexico, place more emphasis

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on pest knowledge and responses to grower and improving spray techniques to prevent needs. Those countries in which avocado is any detrimental effect on natural enemies; still grown on small farms or in backyards and (vii) plant pest-resistant cultivars and avoid produced for domestic consumption exhibit planting susceptible varieties; (viii) conduct very little involvement or research aimed at surveys for new pests and pest problems in rational pest management. Sometimes, within order to find an appropriate solution as soon the same country contradictory attitudes as possible, before full establishment of the are observed. For instance, Gallegos (1983) pest or acceleration of the pest problem by reports that in the Michoacan region, there are augmentation of local natural enemies. big differences in avocado pest management. Some orchards may receive at least 12 insecticide applications per year, while others Pollinators will not receive any pesticides. According to Colin (1990), to avoid important infestations Avocado flowers and flowering of either mites or thrips, it is necessary to evaluate different pesticides. The information Flower morphology on pesticides, however, is concentrated on the use of organophosphates and sulphur (Colin, The avocado flower is circular, about 1 cm in 1991). diameter. It is bisexual, having both female The usual recommended control tactics and male reproductive organs. The flower against avocado pests in Colombia concen- consists of one pistil and six trimerous alter- trate on cultural control (removing and burn- nate whorls: two whorls of greenish yellow ing infested parts) or application of chemical tepals, three of stamens and one of short products. arrow-shaped staminodes (Fig. 8.1). Each of In Florida, where the most important the nine stamens bears an anther with four cultivars grown are Guatemalan or West pollen sacs. The valves of the pollen sacs turn Indian in origin, avocado pests are entirely up while opening, and draw out a pack of controlled through the use of chemical pollen grains attached to them. The avocado products, applied on a calendar schedule. pollen grain is spherical and is covered with This practice continues despite the presence numerous conical spinules. A pair of oval, of several native biological control agents for yellow-orange nectaries is located at the base some insect pests and several attempts to of each of the three inner stamen filaments. introduce exotic biological control agents and The three yellow-orange staminodes also the development of IPM techniques for others, function as nectaries. The pistil is located cen- such as mirids (Peña et al., 1996). trally, and consists of a greenish, ball-shaped, The generally followed rules for the superior ovary, a hairy, slender, cylindrical improvement of IPM in avocado and in other style and a cone-shaped stigma, 0.3–0.6 mm subtropical fruit crops are: (i) search for and in diameter. The stigmatic surface is com- import suitable and effective natural enemies, posed of elongated papilla cells. Usually, propagate them, and distribute them among it is somewhat depressed in its centre. All the infested plants; (ii) import plant material cultivars have a similar flower structure, and natural enemies with strict enforcement though they may differ slightly with respect of quarantine instructions to avoid introduc- to flower size and some other features tion of other pests or hyperparasitoids; (iii) (Nirody, 1922; Stout, 1933; Bergh, 1969; conserve and augment local natural enemies; McGregor, 1976; Davenport, 1986; Ish-Am (iv) carefully monitor the pests, study their and Eisikowitch, 1991b). biology and behaviour; (v) do not interfere The flowers are carried on terminal pani- with the biological equilibrium, use insecti- cles. A typical panicle carries a few hundred to cides only if absolutely necessary, avoid the more than a thousand flowers. New flowers use of non-selective insecticides and use only open daily during the long flowering period. highly selective ones; (vi) avoid drift of insec- Each flower opens twice (dianthesis), usually ticides from adjacent plots by limiting sprays on two successive days, in a dichogamous–

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Fig. 8.1. The floral parts of the avocado flower (Ish-Am and Eisikowitch, 1991b).

protogynous rhythm (Fig. 8.2). During the flower stay fresh during the first dehiscence first female (pistillate) opening, the stigma stages (D1,D2, Fig. 8.2) and the tepals spread is exposed and white. The stamens with upright to the style, or even remain only the closed valves are parallel and close to partially open. Under cool conditions, some the tepals and nectar is secreted by the three cultivars open their female flower only staminodes. At the beginning of the second partially or not at all (Nirody, 1922; Stout, male (staminate) opening the tepals are 1933; Bergh, 1969; Ish-Am and Eisikowitch, 10–20% longer. The three inner stamens move 1991b). towards the style, and their filaments lengthen until their anthers more or less cover the Flowering behaviour stigma. The six outer stamens also lengthen, move up and hold a position of about 45° to All avocados display unique flowering the pistil. Anther dehiscence takes place about behaviour, which may be termed ‘diurnally 1 to 2 h later, first by the two lower valves of synchronous dichogamous protogyny, with each anther, and about 1 h later by the two intermediate closing’. The flower opens twice, upper valves. Nectar is secreted by the six first as a female and then as a male. Each nectaries, while the three staminodes move flower stage opening and closing occurs closer to the ovary and turn brown. The nearly synchronously within the tree (and the stigma gradually shrinks, and also turns cultivar). Based on flowering rhythm, all avo- brown (Nirody, 1922; Stout, 1933; Bergh, 1969; cado cultivars are divided into two comple- McGregor, 1976; Davenport, 1986; Ish-Am mentary flowering groups. In warm weather, and Eisikowitch, 1991b). ‘Group A’ cultivars open female stage During anthesis, flower shape changes flowers from the morning till noon, and male gradually in a regular sequence, which stage flowers during the afternoon. ‘Group was divided by Ish-Am and Eisikowitch B’ cultivars, on the other hand, open female (1991b) into ten distinct morphological stages stage flowers in the afternoon and male stage (Fig. 8.2). These flower stages are similar in flowers during the morning hours (Fig. 8.3). all cultivars, and are somewhat influenced This flowering rhythm may be termed by the weather. On hot and dry days, the ‘temporal dioecy’ (Clark, 1923; Stout, 1923, male flower stigma and staminodes dry 1933; Robinson and Savage, 1926; Bergh, upon anthesis, and the tepals bend towards 1969; McGregor, 1976; Papademetriou, 1976b; the pedicel. In cool weather, however, both Davenport, 1986; Ish-Am and Eisikowitch, stigma and staminodes of the male stage 1991b).

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Fig. 8.2. Morphological stages of the avocado flower, at its female (pistillate) and male (staminate) openings and closings (Ish-Am and Eisikowitch, 1991a).

Many avocado cultivars also present a several consecutive flower stages occur con- daily phase of overlap, within the tree, of coin- currently within the panicle (Ish-Am and ciding dehisced male stage and open female Eisikowitch, 1991b). stage flowers (Fig. 8.3), which usually takes place for a period of 1–3 h. In some cultivars, this overlap period is almost constant, regard- Pollination less of temperature, but in others, it gets shorter during warmer weather and may dis- Pollination modes appear on hot days. In cool weather, there is a significant delay in the whole daily flowering Cross-pollination sequence, which may result in complete rever- sal of the times of day when female and male Cross-pollination occurs between group B stage flowers are open (Clark, 1923; Stout, male stage (Plate 58) and group A female 1923, 1933; Robinson and Savage, 1926; Lesley stage flowers (Plate 59) in the morning (in and Bringhurst, 1951; Gustafson and Bergh, warm weather), and vice versa in the after- 1966; Bergh, 1969; McGregor, 1976; Papade- noon. It may also occur among different metriou, 1976b; Sedgley, 1977; Sedgley and cultivars of the same flowering group, when Annells, 1981; Sedgley and Grant, 1983; Dav- there is a period of overlap between female enport, 1986; Ish-Am and Eisikowitch, 1991b). and dehiscing male openings (Stout, 1923, Although the beginning (and the end) of 1933; Robinson and Savage, 1926; Bergh, each flower stage manifestation is synchro- 1969; Davenport, 1986; Ish-Am and Eisiko- nized within the tree and among trees of a witch, 1991a,b). Cross-pollination effective- cultivar, the individual flowers do not open ness depends on: the distance between the and close simultaneously. Rather, they pro- ‘pollenizer’ (pollen donor) and the pollinated ceed through each stage individually, over trees; the effective overlap period between a period of 2–3 h. Flowers that open earlier female and male openings; and pollinator also proceed earlier to the following stages. mobility, density and effectiveness. In many Therefore, during most of the flowering day, cases, cross-pollination of a group A cultivar

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Fig. 8.3. Daily flowering course of A and B type avocados in warm weather.

by a group B is more efficient than the female flowers overlap with old male flow- other way around, due to the greater overlap ers, which have finished pollen release and period between group A female and group are closing (Ish-Am and Eisikowitch, 1991b; B male flowering (Stout, 1933; Ish-Am, Ish-Am, 1994). 1994; Papademetriou, 1976b; Ish-Am and Eisikowitch, 1991b). Self-pollination

Close pollination Self-pollination occurs when pollen released at the male stage, reaches the stigma within Close pollination occurs during the phase the same flower. This process does not neces- of female and dehisced male stage flower sarily demand pollinator involvement, and overlap within the tree (Stout, 1923, 1933; may be facilitated by wind or gravity. Self- Robinson and Savage, 1926; Lesley and pollination of the male flower is a common Bringhurst, 1951; Bergh, 1969; Snir, 1971; phenomenon, but in most cases does not lead Papademetriou, 1976b; Davenport, 1986; to fertilization (Stout, 1923, 1933; Robinson and Ish-Am and Eisikowitch, 1991a,b). Since close Savage, 1926; Bergh, 1969; Snir, 1971; Daven- pollination takes place when male and female port, 1986; Ish-Am and Eisikowitch, 1991a,b). stage flowers are in close proximity, its However, Davenport (Davenport, 1985, 1989; efficiency may be very high. It depends on Davenport et al., 1994) concluded that in both length and effectiveness of the overlap south Florida, spontaneous self-pollination is period within the tree, and on pollinator the predominant means for fruit set. density and effectiveness. Most Mexican- and Guatemalan-type cultivars, and their hybrids, present a daily effective period of Pollination requirements overlap within the tree. Generally, close pollination is more efficient in group A cultivars, The need for pollination and pollinators since their open female flowers overlap with young pollen-releasing male flowers, and less Effective pollination is essential for normal so in group B types, where newly opened fruit set. Furthermore, in most growing areas

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self-pollination within the male flower does outcrossed fruits over the selfed ones (Degani not result in fruit set. Hence, pollen has to be and Gazit, 1984; Degani et al., 1986, 1989, transferred from dehisced anthers of a male 1990, 1997). stage flower to a female flower’s receptive In many cases, avocado cultivars have stigma (Stout, 1923; Peterson, 1955, 1956; been found to differ significantly in their need Snir, 1971; Sedgley, 1977; Sedgley and Grant, for cross-pollination, and in their effectiveness 1983; Shoval, 1987; Robbertse et al., 1997, as pollenizers (Gazit, 1976; Degani et al., 1997; 1998a). Fruit set is minimal or absent when Gazit and Gafni, 1986; Eisenstein and Gazit, insect pollinators such as bees and flies 1989; Robbertse et al., 1996, 1997). Moreover, are excluded by caging. Therefore, flying the cross-pollination advantage during the pollinators are needed and wind pollination initial fruit set and young fruit drop period is not effective (Clark, 1923; Lesley and appears to increase under conditions of stress, Bringhurst, 1951; Peterson, 1955; Bergh, 1967, such as hot and dry weather. The perceived 1969, 1975; Gazit, 1976; Du Toit, 1994; situation, therefore, is that all avocado Robbertse et al., 1996, 1997). As mentioned cultivars are self-fertile, but, due to cross- earlier, an exception to this rule was found in pollination advantages during fertilization south Florida by Davenport (Davenport, and throughout young fruit drop, mainly 1985; Davenport et al., 1994), who reported under stress conditions, most of them need that spontaneous self-pollination within the cross-pollination to realize their full yield male stage flower is the main fruit set potential. mechanism for commercial cultivars.

The need for cross-pollination Pollination as a yield limiting factor As a rule, all avocado types are self-fertile, and may yield good fruit set upon pollination One may assume that pollination rate should with self-pollen (Stout, 1923; Clark, 1924; not be a yield-limiting factor of avocado, McGregor, 1976; Davenport, 1986). Neverthe- because of the following facts: a medium- less, numerous cases of significant decline sized mature avocado tree produces during in yield with increasing distance from the blooming season about 1 million flowers pollenizers have been reported (Stout, 1923; (Lahav and Zamet, 1999); thus, 10,000 to Robinson and Savage, 1926; Bergh and 40,000 female flowers open each day. For all Gustafson, 1958; Bergh and Garber, 1964; that, a final set of only 400 to 600 flowers per Bergh et al., 1966; Bergh, 1969, 1975; Goldring tree is enough to produce a good crop, and et al., 1987; Degani et al., 1989, 1990 1997; Guil only two to three honeybees per tree, during and Gazit, 1992; Ish-Am, 1994; Kobayashi 1 h of overlap between male and female stage et al., 1996; Johannsmeier et al., 1997; Clegg flowers, can pollinate this number of flowers. et al., 1998). Pollination experiments under However, most pollinated flowers do not enclosure also demonstrated a clear advan- produce a fruit, and when the percentage tage for cross-vs. self-pollination(Clark and of pollinated flowers is below 10–20%, yield Clark, 1926; Stout, 1933; Peterson, 1955; Gazit, is usually low (Papademetriou, 1976a; Tzafti, 1976). Using hand pollination, a clear advan- 1981; Eisikowitch and Melamud, 1982; Shoval, tage in pollen germination and pollen tube 1987). Noticeable initial fruit set occurs only growth was shown for foreign over self- when five to ten bees are observed on a pollen (Robbertse et al., 1996), and most medium-sized tree during the daily female avocado cultivars were found to achieve blooming period. At least 1 week at this a higher initial set when cross-pollinated visitation level is needed for a fair crop, and (Papademetriou, 1976b; Gazit and Gafni, much more for a good one (Ish-Am, 1994; 1986; Eisenstein and Gazit, 1989). In addition, Ish-Am and Eisikowitch, 1998a). isozyme analysis studies revealed selective The honeybee, which serves as the major young fruit drop, with a clear advantage for pollinator for avocado in most countries, tends

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to abandon avocado orchards when a more Flower visitation behaviour attractive bloom is available. In addition, it does not perform efficient cross-pollination, Honeybees visiting avocado flowers usually due to its location-constancy behaviour walk among neighbouring flowers, and fly (Stout, 1923, 1933; Lesley and Bringhurst, between inflorescences. While visiting the 1951; Bringhurst, 1952; Schroeder, 1954; Peter- relatively small flower the bee often slips, son, 1955; Gustafson and Bergh, 1966; Bergh, and grasps other parts of the inflorescence 1967, 1975; Gazit, 1976; McGregor, 1976; (Davenport, 1986; Vithanage, 1990; Ish-Am Eisikowitch and Melamud, 1982; Davenport, and Eisikowitch, 1991a, 1993). Honeybees 1986; Visscher and Sherman, 1998; Bekey, usually collect avocado nectar, or nectar with 1989; Vithanage, 1990; Eardley and Mansell, pollen and, rarely, only pollen. The nectar- 1993, 1994, 1996; Du Toit, 1994; Hofshi, 1995; collecting bees (Plate 60), as well as the Ish-Am and Eisikowitch, 1998a,b,c; Robbertse nectar-with-pollen collectors, visit both et al., 1998a,b). Consequently, inadequate female and male stage flowers, and as such pollination is a major yield-limiting factor may serve as effective pollinators. In contrast, of avocado in Israel, California and probably the pollen-only-collecting bees visit almost also in other countries, mainly under Mediter- exclusively male flowers, and do not contrib- ranean climate conditions. ute to pollination (Stout, 1933; McGregor, 1976; Davenport, 1986; Free, 1993; Ish-Am and Eisikowitch, 1993). While visiting a Avocado pollination ecology dehisced male flower, the bee’s body Avocado flowering behaviour exhibits a becomes dusted with pollen, which the bee sophisticated mechanism, which encourages cleans off after every two to four visits, while cross-pollination, usually prevents self- hovering or hanging on a leaf. The nectar- pollination (within a flower) and usually and-pollen collectors pack the pollen into enables the existence of close-pollination their curbiculae, forming pellets, whereas the (between neighbouring flowers within a tree, nectar-only collectors ‘deliberately’ unload and cultivar). The flower carries only one the pollen and throw it down (Ish-Am and ovule, and its P/O (Pollen grains per Ovule) Eisikowitch, 1993). The pollen-only collec- ratio is 5000–10,000, which lies within the tors’ visits are very short: in about 1 s they range of obligate cross-pollinated species touch the anthers while hovering, or while (Cruden, 1977). Moreover, its long blooming landing for an instant. These bees may also period and mass flowering, with only several perform one to two refuelling nectar collec- hundreds of fruits produced, are typical tions per ten pollen collections, during which adaptations for cross-pollination. Even they may visit female flowers, if present in though the flowering rhythm (of most the vicinity (Ish-Am and Eisikowitch, 1993). cultivars) enables both cross-and close- The positions of bees visiting female and pollination, selection, which appears during male stage flowers of equivalent form are very the fertilization and young-fruit drop peri- similar (Fig. 8.4). Only limited and defined ods, favours the cross-pollinated flowers. zones of the bee’s body, the ‘collection zones’ These features may be interpreted as an (Fig. 8.5), contact the flower’s reproductive adaptation to tropical forest conditions, organs. While visiting the male flower, the where tree-species specimens are sparse, and bee touches the exposed pollen on the open cross-pollination probability is very low. valves with its vertex, proboscidal fossa, legs and some ventral regions (Plate 61) (Figs 8.4 and 8.5), collecting large amounts Pollinators and visitors of pollen there. The same ‘collection zones’ also touch the stigma of the female flower, The honeybee (Apis mellifera L.) is apparently due to the similarity of the female and the major pollinator of avocado in all male stage flowers, and to the similar location countries. of the stigma and inner stamens’ anthers

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268 M. Wysoki et al.

(Figs 8.2 and 8.4) (Ish-Am and Eisikowitch, Mobility among the trees and 1993). cross-pollination efficiency

For cross-pollination implementation, honey- Constancy for flower stage and bees need to move between pollen-releasing close-pollination efficiency male flower trees and female flower trees of a different cultivar. In mature avocado Most honeybees that visit avocado during the orchards, an average 40% of the bees were period of overlap between female and male found to move between adjacent trees in openings within a tree, move between the 10 min (Ish-Am and Eisikowitch, 1998b). male and female flowers, collect nectar and However, this constitutes short-range move- pollen, or nectar only, and efficiently carry ment, since during foraging most honeybees out close pollination (Clark, 1923; Gustafson visit only one to three adjacent trees (Clark, and Bergh, 1966; Gazit, 1976; Davenport, 1923; Stout, 1923, 1933; Free and Spencer- 1986; Ish-Am and Eisikowitch, 1993). Booth, 1964; Bergh et al., 1966; Gustafson

Fig. 8.4. The position of the honeybee while visiting avocado flowers at various stages (Ish-Am and Eisikowitch, 1993).

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Pests and Pollinators of Avocado 269

and Bergh, 1966; Bergh, 1967; McGregor, this phenomenon presents a major yield- 1976; Davenport, 1986; Visscher and limiting factor for the early-and medium- Sherman, 1998; Vithanage, 1990; Free, 1993; blooming cultivars, which flower in March/ Hofshi, 1995, 2000). Indeed, scout bees April, during the blooming season of citrus move, while foraging, further throughout and many wildflower species (Clark, 1923; the orchard; but, under avocado orchard Stout, 1923, 1933; Gustafson and Bergh, conditions they were found to comprise 1966; Bergh, 1967; Gazit, 1976; McGregor, only 2–4% of the field bees (Stout, 1933; 1976; Papademetriou, 1976b; Tzfati, 1981; Ish-Am and Eisikowitch, 1998b). Therefore, Eisikowitch and Melamud, 1982; Davenport, honeybees serve as efficient cross-pollinators 1986; Shoval, 1987; Visscher and Sherman, only in the case of neighbouring trees 1998; Vithanage, 1990; Ish-Am and Eisiko- with complementary flower types, and their witch, 1998a; Hofshi, 2000). efficiency decreases sharply with increasing This low attractiveness to honeybees distance between the pollen source and the has been attributed to the avocado flower female bloom (Ish-Am, 1994; Ish-Am and and flowering properties, which are not well Eisikowitch, 1998b). suited to this pollinator (Faegri and Van der Pijl, 1979; Kevan and Baker, 1983; Vithanage, Attractiveness of avocado bloom 1990; Ish-Am and Eisikowitch, 1993; Visscher to honeybees and Sherman, 1998; Ish-Am et al., 1999). The avocado flower is greenish yellow, has a The attractiveness of the avocado bloom slightly bitter smell and its nectar is fully to honeybees under Mediterranean climatic exposed. It has radial symmetry, lacks a conditions appears to be low compared to landing platform and nectar trails, and is numerous other species that are in bloom at somewhat small for the honeybee, while the the same time, such as citrus, litchi and wild- inflorescence is too sparse to be visited as flower species. Therefore, honeybee foragers a unit (Davenport, 1986; Vithanage, 1990; from hives placed in the avocado orchard Ish-Am and Eisikowitch, 1993). Moreover, often abandon the avocado and collect pollen neither avocado pollen nor its nectar suits and nectar from competing blooms. In Israel, fully the honeybee’s needs (Ish-Am, 1994).

Fig. 8.5. The ‘pollinating zones’ of avocado pollen on the honeybee body (Ish-Am and Eisikowitch, 1993).

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270 M. Wysoki et al.

Pollinators and visitors in Central the honeybees (Apis mellifera L.), and three America and Mexico fly species: Eristalis tenax L. (Syrphidae), Phaenicia mexicana Macquart (Calliphoridae) Visitors and Palpada mexicana Macquart (Syrphidae). However, in unsprayed orchards, as well Until recently, little information had been as on backyard trees, much larger insect reported on avocado pollination and pol- populations of a greater variety of species linators in Central America and Mexico. were found (Table 8.1). Sometimes, at such Potential pollinators that have been reported locations, hundreds of specimens per tree of to visit avocado flowers are honeybees, tens of species of bees, wasps, flies and others stingless bees, wasps, flies and beetles, and were observed. even bats (Nieto, 1984; Crane, 1992; Roubik, 1995). In only a few cases has the effective- Pollinators ness of these visitor insects as avocado pollinators been studied. In south Puebla, Mexico, For successful pollination, an insect visitor Nieto (1984) collected insects visiting avocado has to exhibit the following behavioural traits flowers. In addition to honeybees, he also (Faegri and van der Pijl, 1979; Ish-Am, 1994): found flies of the Syrphidae, Sarcophagidae, (i) visit both female and male stage flowers; Muscidae, Calliphoridae and Tachinidae, (ii) touch both anthers and stigmas with the wasps of the Vespidae and Ichneumonidae, same body parts (the ‘pollinating zones’); and beetles of the Scarabaeidae and Lam- (iii) carry avocado pollen on the ‘pollinating pyridae. He counted visits per 5 min to the zones’; (iv) for cross-pollination – the polli- avocado flowers, and found: 61 visits for the nator visits male and female stage flowers honeybees, 11 and 8 visits for Calliphoridae on trees of different cultivars. Indeed, beetle and Muscidae flies, respectively, and less species, which collect pollen and visit only than that for the other visitor insects. A recent male flowers, hover-flies, which collect nectar 5-year study of avocado pollinators has been while fluttering, without touching anthers or conducted in Mexico (Castañeda-Vildózola stigmas, and wasps that touch the flower et al., 1999; Ish-Am et al., 1999). In well- reproductive organs but carry no pollen maintained orchards, where insecticides on their smooth bodies cannot accomplish are sprayed regularly, the avocado visitor pollination (Castañeda-Vildózola et al., 1999; populations were usually small. The species Ish-Am et al., 1999). Nevertheless, most of observed included about 45 Diptera species the species visiting avocado flowers do effect (five families), 20 Hymenoptera species (six its pollination, although sometimes not families) and five Coleoptera species (five efficiently. The main effective pollinators families). The predominant species were observed and collected (Castañeda-Vildózola

Table 8.1. Insects collected on avocado bloom in Mexico. (From Ish-Am et al., 1999.)

Order Suborder level Specimens collected (No.) Speciesa (estimated No.)b

Hymenoptera Meliponinae 444 10 Other bees 84 16 Wasps 245 25 Diptera 153 40 Coleoptera 33 10 Heteroptera 44 8 Others 18 6 Total 1021 115

aSpecies identification performed by the SEL (Systematic Entomology Laboratory) of the USDA. Identification of the bee species was carried out by Dr David Roubik of the Smithsonian Tropical Research Institute in Panama. bThe number of species is an estimate, since identification had not yet been completed.

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Pests and Pollinators of Avocado 271

et al., 1999; Ish-Am et al., 1999) were: the et al., 1999). The only wasp species found to honeybee, seven to nine species of stingless efficiently pollinate avocados is the ‘Mexican bees (Apidae: Meliponinae), a few Bombus sp. honey wasp’ (Brachygastra mellifica Say) (Table (Apidae: Bombinae), a nectar-collecting social 8.2) (Plate 64). This social wasp collects nectar wasp Brachygastra mellifica Say (Vespidae) and stores it as honey for the larvae; it carries and a blowfly Chrysomya megacephala F. large amounts of avocado pollen on its hairy (Calliphoridae) (Table 8.2). All of these carry head, thorax and legs, as well as inside unique large amounts of avocado pollen on their thoracic cavities. It appears on avocado bloom ‘collection zones’, which effectively come in in high density and visits its flowers at a contact with the stamens and the stigma, visit high rate. This species is found on avocado many avocado flowers per minute and are blooms throughout Mexico. Other wasp attracted to avocado bloom in high numbers. species that visit avocado flowers, of the genera Polistes, Mischocyttarus and others, HONEYBEE (APIS MELLIFERA L., APINAE, APIDAE) cannot be considered efficient pollinators, At present, the feral honeybee population because of low flower visitation rate, small in Central America and Mexico consists of amounts of avocado pollen on the body or the African race (A. mellifera scutellata) and small populations on the trees. its hybrids with the Italian race. The African race reached Mexico about 15 years ago, and FLIES (DIPTERA) Many fly species were col- today exists there as a domesticated, as well as lected visiting avocado flowers (Table 8.1). a feral honeybee (Roubik, 1998). In most cases, Sometimes they are observed at high densities honeybees are the main visitor to the avocado of tens, or even hundreds per tree (Nieto, 1984; flowers and behave as efficient pollinators. Castañeda-Vildózola et al., 1999; Ish-Am et al., However, sometimes they prefer other 1999). Some species of the Calliphoridae (Plate blooms, while the local stingless bees and 65), Muscidae, Sarcophagidae and Syrphidae wasp species prefer the avocado (Papa- also carry large amounts of avocado pollen demetriou, 1976b; Castañeda-Vildózola et al., and make effective contact with stamens and 1999; Ish-Am et al., 1999). stigmas. However, their pollination efficiency is not high because of a low rate of flower visitation. STINGLESS BEES (MELIPONINAE, APIDAE) Nine species of this subfamily have been found visiting avocado flowers (Castañeda-Vildózola Pollination rates et al., 1999; Ish-Am et al., 1999) (Table 8.2). Pollination rates of avocado flowers, at their These bee species seem to be well adapted for female stage opening, were determined in avocado pollination: they are smaller than the a few locations in Mexico. Rates fluctuated honeybee (Plate 62); while visiting avocado widely, from 0 to 52%, in relation to flowers they achieve effective contact with pollinator density (G. Ish-Am et al., 1999, both stamens and stigma on the ventral and unpublished). In most cases, honeybees, lateral zones of both the thorax and abdomen. stingless bees, wasps and other pollinators On these zones, they collect large amounts of were simultaneously visiting the bloom. avocado pollen, which is later transferred to However, in one location all honeybees left the hind legs and used to build up a pollen the avocados for senecio (Senecio salignus) load (Plate 63). Six of these species were bloom, while up to 100 specimens per tree observed visiting avocado bloom in high of Meliponinae and Brachygastra species density, and moving frequently among male remained on the avocado flowers. When only and female stage flowers. native pollinators were active, pollination rates reached 52% of cross-pollination and WASPS (HYMENOPTERA) Many wasp species daily total pollination. These values are visit avocado flowers (Table 8.1) (Free higher than those determined in Israel and Williams, 1976; Papademetriou, 1976b; for a typical honeybee pollination (Ish-Am, Castañeda-Vildózola et al., 1999; Ish-Am 1994).

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272 M. Wysoki et al. high high high high high high high high high high Medium Very Very Very Very Very Very Very High Very Very Avocado pollination effectiveness Very Medium Medium Medium on high high high high Very High Very High Very High High Medium High High Low Density avocado bloom Very Medium Low Medium Avocado pollen amount Large Large Large Large Large Large Large Large Large Medium Large Medium Large Medium Medium − − ? + + + + + + + + + + + + Pollen Collecting + + + + + + + + + + + + + + + Nectar 20 20 .5 .5 .5 .5 .5 .5 .5 .5 .5 .5 .5 – – 6 8 6.5 4 6 5 6 7 8.5 4 8 10 14 Body (mm) length 10 10 stingless stingless stingless stingless stingless stingless stingless stingless stingless bees bee bee, wasps bee, bee, bee, bee, bee, bee, bee, bee, wasp bees Mexico. in Description Social Social Solitary Social Social Social Social Social Social Social Social Social Social Blowfly Social avocado of Torre Provancher Cresson F.

Dalla nigra Schwarz Strand rin ) Say é pollinators Say Gu Cresson Friese

pectoralis mexicana

L. perilampoides mellifica spp. Effective

megacephala acapulconis bilineata

Frieseomelitta spp. spp.

nigerrima ( fulviventris frontalis 8.2.

mellifera e l b a

T Name Apis Geotrigona Trigona Partamona Nannotrigona Scaptotrigona Trigona Scaptotrigona Trigona Plebeia Bombus Exomalopsis Brachygastra Polistes Chrysomya

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Pests and Pollinators of Avocado 273

The original avocado pollinators Pollinators and visitors in other tropical climates The avocado flower’s sugar amounts are within the typical bee flower range (Cruden Only few reports on avocado pollination et al., 1983; Harder and Barrett, 1992). How- and pollinators in the tropics are available. ever, its flower has an open ‘general form’, In Jamaica, Free and Williams (1976) found with exposed nectar and easily collected mainly honeybees and Polistes wasps visiting pollen. Therefore, it does not fit a specific the avocado flowers. They found an average pollinator species (Faegri and van der Pijl, of 2710 and 1575 avocado pollen grains 1979; Visscher and Sherman, 1998). Since it per honeybee, and only 580 and 225 pollen exhibits mixed features of the typical bee, grains per Polistes wasp, which were collected wasp and fly flowers (Faegri and van der Pijl, on dehisced male and female stage flowers, 1979; Vithanage, 1990; Roubik, 1995; Visscher respectively. They also found large numbers and Sherman, 1998; Ish-Am et al., 1999), it is of other flower species’ pollen grains carried not surprising to find that numerous species by these insects. Papademetriou (1976b) of these groups visit the avocado bloom reported that in Trinidad ‘the most abundant (Table 8.1). Which are the avocado original species visiting the avocado flowers’ are main pollinators? Evidently not the honey- two wasp species of the Vespidae: Polistes bee, which was only brought to the ‘New canadensis and Metabolybia singulata.He World’ at the beginning of the 16th century observed honeybees visiting the avocado for by the Europeans (Roubik, 1998). The survey only 2 weeks during one blooming season of avocado pollinators that was conducted in and almost none during the next one, Mexico indicates that the original pollinators and assumed that more attractive nectar were stingless bee species and the ‘Mexican and pollen plants had drawn the honeybees honey wasp’ (Table 8.2). All of these are social away. He found more avocado pollen hymenopterans, which are adapted to visit- grains on the honeybees than on the wasps. ing a wide range of flower types year-round, He also saw small numbers of Musca sp. and and the avocado bloom was found to be some other fly species visiting the avocado highly attractive to them (Castañeda- flowers. Vildózola et al., 1999; Ish-Am et al., 1999). In south Florida, Robinson and Savage However, since the social hymenopterans (1926), Stout (1932), Davenport (1985, 1986, may be attracted by competing blooms, the 1989, 1992), and Davenport et al. (1994) avocado flowers are also available for num- observed only small numbers of insects erous species of wasps, flies and beetles, visiting the avocado bloom. Most of the time, which serve as second-order pollinators honeybee visitation to the avocados was very (Bergh, 1967, 1975; Visscher and Sherman, low. Some avocado cultivars, e.g. ‘Booth 7’ 1998; Vithanage, 1990; Castañeda-Vildózola and ‘Hardee’, were more attractive to honey- et al., 1999; Ish-Am et al., 1999). bees than others. The main visitors to avocado All of this aside, the avocado flower may blooms were Polistes wasps, flies (Caliphor- represent a Meliponinae flower type, which is idae, Muscidae, Tabanidae and Syrphidae), mainly adapted for tropical bees, with body bugs (Miridae, Reduviidae, Phymatidae) sizes of 4–8 mm, and also available for wasp (Stout, 1923, 1932; Stout and Savage, 1925; and fly pollinators (Bawa, 1980; Givnish, 1980; Davenport, 1986, 1989) and many flower Visscher and Sherman, 1998). The synchro- thrips (Frankliniella spp.). Sometimes half a nized bloom of the mass-flower trees is dozen or more Frankliniella per flower were well suited to the needs and behaviour of noticed (Davenport, 1986). Although their the highly social bees (Kubitzki and Kurz, pollination ability had been considered (Peter- 1984). These insects are well adapted for son, 1955), they were proven ineffective by fast reactions to the trees’ blooming changes, comparing enclosed branches where thrips exploiting the large amounts of nectar and were present to similar enclosed branches pollen that are released, thus carrying pollen treated with insecticides (Davenport, 1992). from male blooming trees to the female ones. Pollination rates of the female stage flowers

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274 M. Wysoki et al.

were usually very low, around 1.5% Many other insect visitors to avocado (sometimes up to 4%), with one to two pollen flowers have been observed in Israel. Most grains per stigma (Davenport, 1986, 1989; of them are flies (Calliphoridae, Syrphidae, Davenport et al., 1994). However, self- Muscidae, Bibionidae, Sarcophagidae, Tach- pollination within the male stage flower was inidae and others), bee and wasp species, found to reach 10–80%, according to cultivar and more rarely, butterflies, beetles and bugs. and weather. This self-pollination was found Thrips and ant are also observed (Bergh, to lead to fertilization, and fruit set. Accord- 1975; Gazit, 1976; Tzfati, 1981; G. Ish-Am, ingly, it has been concluded that in avocado 1994, unpublished). B. Gefen (in Bergh, 1975) orchards there is no need for honeybee hives reported that the housefly seems to be an effi- and pollenizer trees, in order to obtain good cient transporter of avocado pollen. Ish-Am yields in that region. (1985, 1994) found an average of 200 avocado pollen grains per fly on the body of Muscidae Pollinators and visitors in a flies, which were collected on dehisced male Mediterranean climate stage ‘Fuerte’ flowers. During days of very low honeybee activity (zero to one bee per CALIFORNIA In California, the honeybee is tree) he found 0% pollinated flowers on days the main avocado pollinator, and other visit- with no fly activity and 10–20% on days with ing insects are rare (Clark, 1923; Bergh, 1967). high fly activity. Pollination rates were some- Early work revealed the need for honeybee times even higher, reaching 72%, in a ‘Hass’ pollination for fruit set, and the need for plot that had been covered with fluid manure adjacent foreign pollen donor (pollenizer) 2 weeks earlier and had a huge housefly popu- trees to maximize yield (Clark, 1923; Stout, lation. However, since fly-pollinated flowers 1923 Robinson and Savage, 1926). However, usually carried only one or two pollen grains since in some years solid ‘Hass’ blocks proper stigma, and since after consecutive ‘fly duced well without placing honeybee hives days’ with no honeybee activity almost no there, growers and researchers concluded that fruit set could be observed, he concluded that pollination is not a limiting factor. Neverthe- the fly’s contribution to avocado set is very less, new pollination studies, and innovative limited. A beetle pollination experiment was practices involving high densities of both performed by Tzfati (1981). She introduced honeybee hives and pollenizer trees, have ‘flower beetles’ (Scarabaeidae), which had confirmed the earlier conclusions (Hofshi, been collected earlier on avocado bloom, into 1995, 2000; Kobayashi et al., 1996; Clegg et al., enclosed ‘Reed’ inflorescences, and after 3 h 1998; Visscher and Sherman, 1998). found 30% pollinated flowers. Numerous other insect visitors to Wild bumblebees (Bombus terrestris L.), avocado flowers were observed in California, have been observed visiting and pollinating mainly flies and wild bees. Some of these avocado flowers (Ish-Am et al., 2000). Subse- visitors were assumed to contribute to avo- quently, a 5-year experiment was conducted cado pollination (Bergh, 1967; Schroeder and by Ish-Am et al. (2000) to improve avocado Hofshi, 1998; Visscher and Sherman, 1998). pollination, using hives of domesticated bum- Ants are common visitors to avocado flowers blebees of the same species. They compared there, but do not effect pollination (Lesley and 3 ha plots in which honeybee hives were Bringhurst, 1951). placed at different densities (3–10 hives ha−1), to similar plots where 25 bumblebee hives ISRAEL In Israel, the honeybee is also the (containing a few hundred bees per hive) main avocado pollinator and its hives are per plot had been placed in addition to the routinely placed in avocado orchards during honeybees. The best results were obtained in the blooming season. However, its effective- plots of combined honeybee and bumblebee ness as an avocado pollinator is often inade- hives. The bumblebees were more effective on quate, constituting a crucial yield-limiting cool days and under competitive pollination factor (see pages 269 and 270). conditions, and at a distance of more than

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two rows (10 m) performed cross-pollination pollinators from the native fauna to increase more effectively. However, under hot weather avocado productivity. conditions and when not attracted by competing blooms honeybees were more efficient. AUSTRALIA In New South Wales, Vithanage (1990) identified as regular visitors to avocado SOUTH AFRICA In the northern Transvaal, flowers (‘Hass’ and ‘Fuerte’): honeybees, one DeMeillon (1979) observed seven Forcipomyia wasp and one ant species (Hymenoptera), 11 and a few Atrichopogon species (Ceratopo- fly species (Diptera) and one species of each of gonidae: Diptera) visiting avocado flowers, the orders Coleoptera and Neuroptera. Other whereas honeybees were rarely seen. How- species were identified as occasional visitors, ever, in the eastern Transvaal lowlands, and were not recorded. For each of the visitor Du Toit and Swart (1993) and Du Toit (1994) species, he measured the number of speci- found honeybees to be responsible for 81% mens and the number of visited flowers per of the visits. Since other visitor species were specimen on ten inflorescences (about 1.0 m2 very sparse, they concluded that honeybee is of canopy) for each hour of the blooming day. the only effective avocado pollinator. Three Pooling the data, which were gathered during years later, Johannsmeier et al. (1997) studied 3 days week−1 from two cultivars at three sites, the role of honeybee pollination in a combined he calculated the average flower-to-insect ‘Hass’ and ‘Ettinger’ avocado orchard. They ratio for each visitor species. He also deter- found pollination to present a crucial yield- mined the average pollen-carrying capacity limiting factor, due to both low honeybee of each species by washing a sample of six visitation rate and low honeybee efficiency specimens and counting the pollen grains for in cross-pollination performance at long each. For each visitor species, he calculated the distances. ‘pollinator index’ as a measure of pollination In Westfalia, Eardley and Mansell (1993, efficiency. ‘Pollinator index’ was defined as 1994, 1996) recorded 48 visitor species on the product of the average flower-to-insect avocado bloom. Honeybees alone constituted ratio per visitor species in an hour by the 85% of the visitors, while six wild bee species average number of pollen grains per insect. and six wasp species made up only 2.8% and The average number of pollen grains per 0.4%, respectively. Flies were the second most insect was above 4000 for the honeybees and important visitors: 26 species (Calliphoridae, the wasp species, around 1500 for the beetle Muscidae, Syrphidae and others) constituted and one fly species (Aphyssura sp.), 950–150 8.7% of the visitors. Also recorded were for another nine fly species, and less than 100 ants, butterflies, bugs and beetles (two, two, for one fly and the Neuroptera species. The two and three species, respectively). Avocado average number of insects per 100 flowers in pollen was carried mainly by honeybees and an hour was above 20 for two fly species other bee species, as well as by some of the (Simosyrphus gricornis and Calliphora sp.), 16 Calliphoridae fly species, whereas the other for the honeybees, 14 and 8 for two other fly visitors carried almost no avocado pollen. The species (Calliphora sp. and Chrysomya varipes, authors concluded that in the research area respectively), and two or fewer for the other honeybee is the main avocado pollinator, species. Therefore, the pollination index was and that a small native carpenter bee more than 25,000 for the honeybees, about species (Allodape microsticta Cockerell) is a 1600 for one calliphorid fly, from 830 to 130 very efficient avocado pollinator; however, for another four fly species, and less for its population is too small to also serve as the other species. Vithanage (1990) concluded an effective one. They noted that honeybees that the honeybee was by far the major were mostly attracted by other flower species, avocado pollinator in the research area, and such as litchi, and deduced that the honeybee that the flies as a group contributed about 14% is not an optimal pollinator for avocado to the seasonal pollination. He also found that (see also Westerkamp, 1991). Therefore, they adding honeybee hives to avocado orchards called for research aimed at using alternative could increase the yield.

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Conclusion stingless bee and wasp species which are evolutionally related to avocado’s original The avocado originated and has evolved pollinators and may pollinate it effectively, for millions of years in Central America. Its in subtropical countries there are almost no flowers were pollinated by native pollinators, suitable local candidate pollinator species, which co-evolved with the avocado. The except for the honeybee. Therefore, in those avocado flower presents typical generalist countries, mostly under a Mediterranean features, including large amounts of exposed climate, the honeybee serves as the only effec- nectar and pollen. Thus, its rewards are tive avocado pollinator, whereas many local readily available to almost all visitors, from fly, wasp and bee species visit its flowers, but bees, wasps, ants and flies to beetles, bugs make only a limited contribution to its pollina- and butterflies. However, effective avocado tion. Although honeybee hives are regularly pollinators have to visit both female and male placed in avocado orchards throughout the stage flowers and come into contact with season, honeybees are frequently attracted the dehisced anthers and the receptive stigma to competing local flowers and abandon the at the same hairy ‘pollen collection zones’. avocado bloom. Therefore, inadequate polli- Flying insects of small to medium size (3 to nation constitutes in those regions an impor- 8 mm in length) are especially fit to efficiently tant limiting factor for avocado productivity. collect avocado nectar. While visiting male In contrast with the other avocado grow- stage flowers they get pollen at the ‘collection ing regions, in south Florida insect pollinators zones’, which will touch the stigma of female were found not to be needed for commercial stage flowers. avocado pollination, since spontaneous self- The main original avocado pollinators pollination occurs within the male stage apparently are social Hymenoptera species: flower. This odd feature may be a product of several small to medium size stingless bees the local humid and warm climate, combined (Meliponinae) and the ‘Mexican honey wasp’ with human selection for fruitfulness of (Brachygastra mellifica Say). Second-order the local West Indian-related cultivars. In this pollinators are numerous species of wasps region there is almost no effective overlap and flies, and probably also beetles. between female and male stage flowers The arrival of the honeybee in Central and pollinator activity is very low. In this America and the modern agricultural tech- situation, close-and cross-pollinationare niques, especially spraying with potent inadequate. Hence, apparently the productive insecticides, changed the ecological condi- cultivars selected there were those that have tions there. The honeybee became the major the rare ability for effective self-pollination at pollinator of many species, including the the flower’s male stage. avocado, and the original pollinators were excluded into the reduced uncultivated areas. In locations where the original pollinator References species have survived they are still observed together with the honeybee on avocado bloom, Abud-Antum, A. (1991) Presence of avocado sometimes in large numbers. However, lacebug, Pseudacysta perseae (Heidemann) throughout the huge area of sprayed orchards (Hemiptera: Tingidae) in Dominican in Michoacán, the honeybee constitutes the Republic. Primera Jornada de Proteccion Vegetal, only effective pollinator. Over the last two Universidad de Santo Domingo, Dominican centuries, the avocado has been exported from Republic, abstract, p.4. Andrade, G.S. (1988) Control quimico de la araña its region of origin to most tropical and sub- cristalina Oligonychus perseae, Tutle, Baker and tropical regions of the world. Since its original Abatiello en el cultivo del aguacatero. Thesis, pollinator species were never transferred Universidad Michoacana de San Nicolas to the new growing regions, it is pollinated Hidalgo, Uruapan, Michoacan, Mexico. there by local species (Valentine, 1987). While Angelini, A. and Labonne, V. (1970) Mise au point in most New World tropics there are local sur l’etude de Cryptophlebia (Argyroploce)

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Steyn, W.P., Du Toit, W.J. and De Villiers, E.A. (1994) Swirski, E., Wysoki, M. and Izhar, Y. (1998) Avocado Effect of insect growth regulator, CGA 211446, pests in Israel. Proceedings of the World Avocado on the third instar of the heart-shaped scale on Congress III. Tel-Aviv, Israel, 22–27 October avocados. Subtropica 15(4), 15–18. 1995, pp. 419–428. Stoetzel, M.B. and Davidson, J.A. (1974) Biology, Taylor, J.S. (1957) Notes on Lepidoptera in the morphology and taxonomy of immature Eastern Cape Province. Part IV. Journal of stages of 9 species in the Aspidioti. Annals of the the Entomological Society of Southern Africa 20, Entomological Society of America 67, 475–509. 312–332. Stout, A.B. (1923) A study in cross-pollination Theobald, F.V. (1914) African Aphididae. Bulletin of of avocado in southern California. California Entomological Research 4, 313–337. Avocado Association Annual Report 7, 29–45. Thompson, W.R. (1946) A catalogue of the parasites Stout, A.B. (1932) Sex in avocados and pollination. and predators of insect pests. Sec. 1. Parasite California Avocado Association Yearbook 17, host catalogue. Part 8. In: Parasites of the 172–173. Lepidoptera (N-P). Imperial Agricultural Stout, A.B. (1933) The pollination of avocados. Bureaux, Belleville, Canada, pp. 386–523. Florida Agricultural Experimental Station Bulletin Tzfati, N. (1981) Some aspects of the relation 257, 1–44. between honeybee activity and pollination rate Stout, A.B. and Savage, E.M. (1925) The flower of avocado in the Jordan Valley. High school behavior of avocados with special reference final thesis, Beit-Yerach (in Hebrew). to interplanting. Proceedings of the Florida State Ullyett, G.C. (1939) Parasites of the false codling Horticultural Society 38, 80–91. moth (Argyroploce leucotreta Meyr.) in South Swaine, G., Ironside, A. and Yarrow, W.H.T. (1985) Africa. Mimeograph. Proceedings of the Entomo- Insect Pests of Fruit and Vegetables. Queensland logical Conference, Union Buildings, Pretoria, Department of Primary Industries, Informa- pp. 54–55. tion Series Q 183021, Brisbane, 176 pp. Valentine, D.H. (1987) The pollination of introduced Swirski, E. and Arenstein, Z. (1970) List of common species, with special reference to the British insects found in subtropical orchards. In: Isles and the genus Impatiens. In: Richards, A.J. Diseases and Pests of Fruit Trees (Except Citrus) (ed.) The Pollination of Flowers by Insects. in Israel. The Volcani Institute of Agriculture Academic Press, London, pp.117–123. Research, Bet Dagan, Israel. Published on the Van den Berg, M.A. (1973) Host plants of three occasion of the 18th International Horticultural saturniids and the degree of defoliation they Congress, pp. 12–15. cause to Pinus patula Schlechtd. & Cham. Swirski, E., lzhar, Y., Wysoki, M., Gurevitz, E. and Phytophylactica 5, 65–70. Greenberg, S. (1980) Integrated control of the Van den Berg, M.A. (1974) Natural enemies and long-tailed mealybug, Pseudococcus longispinus diseases of the forest insect Nudaurelia cytherea [Hom.: Pseudococcidae], in avocado planta- clarki Geertsema (Lepidoptera: Saturniidae). tions in Israel. Entomophaga 25, 415–426. Phytophylactica 6, 39–44. Swirski, E., Blumberg, D., Wysoki, M. and lzhar, Y. Van den Berg, M.A. (1975) Bio-ecological studies (1987) Biological control of the Japanese bay- on forest pests 3. Nudaurelia cytherea clarki berry whitefly, Parabemisia myricae (Kuwana) Geertsema (Lepidoptera: Saturniidae). Forestry (Homoptera: Aleyrodidae), in Israel. Israel in South Africa 17, 1–16. Journal of Entomology 21, 11–18. Van den Berg, M.A. (1995) Is suksesvolle vestiging Swirski, E., Wysoki, M. and lzhar, Y. (1988) van Trichopoda pennipes (F.) (Dipt.: Tachinidae), Integrated pest management in the avocado parasitoïde van stinkbesies bereik? Macadamia orchards of Israel. Applied Agricultural Research Yearbook 3, 76–78. 3, 1–7. Van den Berg, M.A. (1998) Tip wilters and stink bugs Swirski, E., lzhar, Y. and Wysoki, M. (1991) Appear- on citrus. In: Bedford, E.C.G., Van den Berg, ance of Aphis gossypii Glover and Aphis M.A. and De Villiers, E.A. (eds) Citrus Pests spiraecola Patch (Rhynchota: Aphidoidea) on in the Republic of South Africa. Dynamic Ad. avocado, persimmon and macadamia. Alon Nelspruit. pp. 161–163. HaNotea 45, 413–416 (in Hebrew, English Van den Berg, M.A. and De Villiers, E.A. (1987a) summary). Psyllids, aphids and whiteflies. In: Myburgh, Swirski, E., Wysoki, M. and Ben-Dov, Y. (1997) A.C. (ed.) Crop Pests in Southern Africa, Vol. 2, Avocado. In: Ben-Dov, Y. and Hodgson, C.J. Citrus and Other Subtropicals. Perskor, Pretoria, (eds) Soft Scale Insects – Their Biology, Natural pp. 43–48. Enemies and Control. Elsevier Science Pub- Van den Berg, M.A. and De Villiers, E.A. (1987b) lishers, Amsterdam, pp. 231–240. Leafhoppers and stinkbugs. In: Myburg, A.C.

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(ed.) Crop Pests in Southern Africa, Vol. 2, bugs Amblypelta nitida Stal and Amblypelta Citrus and Other Subtropicals. Plant Protection lutescens lutescens (Distant) (Hemiptera: Research Institute Bulletin 411, pp. 49–53. Coreidae). Journal of the Australian Entomo- Van den Berg, M.A., Newton, P.J., Deacon, V.E. and logical Society 37, 340–349. Crause, C. (1987) Dispersal of Trichogram- Waite, G.K. and Martinez, B.R. (2002) Insect and matoidea cryptophlebiae (Hymenoptera: Tricho- mite pests. In: Whiley, A.W., Schaffer, B. and grammatidae), an egg parasitoid of the Wolstenholme, B.N. (eds) Avocado: Botany, false codling moth, Cryptophlebia leucotreta Production and Uses. CAB International, (Lepidoptera: Tortricidae), in an empty Wallingford, UK. habitat. Phytophylactica 19, 515–516. Waite, G.K. and Pinese, B. (1991) Pests. In: Broadley, Van den Berg, M.A., De Villiers, E.A. and R.H. (ed.) Avocado Pests and Disorders. Joubert, P.H. (1999) Identification Manual Queensland Department of Primary Industries for Avocado Pests. Dynamic Ad, Nelspruit, Information Series, Q190013, 74 pp. 53 pp. Way, M.J. (1951) An insect pest of coconuts and Vanderplank, F.L. (1958) Studies on the coconut its relationship to certain ant species. Nature, pest, Pseudotheraptus wayi Brown (Coreidae), in London 168, 302. Zanzibar. 1. A method of assessing the damage Way, M.J. (1953) Studies on Theraptus sp. (Coreidae); caused by the insect. Bulletin of Entomological the cause of the gumming diseases of coconuts Research 49, 559–584. in East Africa. Bulletin of Entomological Research Van Heerden, P.W. (1933) The green stink bug 44, 657–667. (Nezara viridula Linn.). Annals of the University Webb, D.V.V. (1974) Forest and Timber Entomology in of Stellenbosch 11A(7), 1–26. the Republic of South Africa. Entomological Mem- Velasquez, M. and Santizo, L. (1992) El acaro oir No. 34. Republic of South Africa, Depart- Calepitrimerus muesebecki, plaga del follaje ment of Agricultural Technical Services, 21 pp. del aguacate. Nota Tecnico Cientifica 14. Wentzel, P.C., Georgala, M.B. and Bedford, E.C.G. Instituto de ciencia and tecnologia agricola (1978) Citrus thrips, Scirtothrips aurantii Faure. (Guatemala), Disciplina de proteccion vegetal, In: Bedford, E.C.G. (ed.) Citrus Pests in the 2 pp. Republic of South Africa. Department of Agricul- Vermeulen, J.B. and Bedford, E.C.G. (1998) Ameri- tural Technical Services, Pretoria, Republic of can bollworm Helicoverpa (= Heliothis) armigera South Africa, Science Bulletin 391, pp. 137–141. (Hübner). In: Bedford, E.C.G., Van den Berg, Westerkamp, C. (1991) Honeybees are poor pol- M.A. and De Villiers, E.A. (eds) Citrus Pests linators – why? Plant Systematics and Evolution in the Republic of South Africa. Dynamic Ad, 177, 71–75. Nelspruit, pp. 217–221. White, I. and Elson-Harris, M. (1992) Fruit Flies of Viljoen, H.M. (1986) Kokosneutstinkbesie-‘n Economic Significance: Their Identification and potensiële plaag op avokado’s. South African Bionomics. CAB International, Wallingford, Avocado Growers’ Association Yearbook 9, 72–74. UK, 601 pp. Visscher, P.K. and Sherman, G. (1998) Insect visitors Whitehead, D. (1979) Recognition characters and to avocado flowers. Subtropical Fruit News 6, distribution records for species of Conotrach- 7–10. elus (Coleoptera: Curculionidae) that damage Vithanage, H.I.N.V. (1990) The role of the European avocado fruits in Mexico and Central America. honeybee (Apis mellifera L.) in avocado pollina- Proceedings Entomological Society Washington 8, tion. Journal of Horticultural Science 65, 81–86. 105–107. Von Wechmar, M.B., Williamson, C. and Collett, H. Williamson, C. and Von Wechmar, M.B. (1995) The (1991) Nezara viridula virus: preliminary char- effects of two viruses on the metamorphosis, acterization of a naturally occurring biocontrol fecundity and longevity of the green stinkbug, agent. Journal of the Southern African Society for Nezara viridula. Journal of Invertebrate Pathology Horticultural Sciences 1, 29. 65, 1–5. Vuillaume, C., Aubert, B., Viladerbo, B. and Laville, Wolfe, H., Franciosi, R., Van Oordt, E. and E. (1981) The principal pests of avocado in Figueroa, R. (1969) El culivo del palto en el Réunion. Fruits 36, 347–350. Peru. Ministerio de Agricultura y Pesqueria, Waite, G.K. (1988) Biological control of latania Estacion experimental Agricola de La Molina, scale on avocados in south-east Queensland. Lima, Peru. Boletin Tecnico 73. Queensland Journal of Agricultural and Animal Wysoki, M. (1987) A bibliography of the pyriform Sciences 45, 165–167. scale, Protopulvinaria pyriformis (Cockerell), Waite, G.K. and Huwer, R.K. (1998) Host plants and 1894 (Homoptera: Coccidae), up to 1986. their role in the ecology of the fruitspotting Phytoparasitica 15(1), 73–77.

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Wysoki, M. and lzhar, Y. (1980) The natural enemies moth, Cryptoblabes gnidiella (Lep., Pyralidae). of Boarmia (Ascotis) selenaria Schiff. (Lepidop- Alon HaNotea 47, 2–10 (in Hebrew). tera: Geometridae) in Israel. Acta Oecologica, Wysoki, M., Kuzlitzky, W., Izhar, Y., Swirski, E., Oecologia Applicata 1, 283–290. Ben-Yehuda, S., Hadar, D. and Rene, S. (1997) Wysoki, M. and lzhar, Y. (1981) Biological data Successful acclimatization of Thripobius semilu- on Apanteles cerialis Nixon (Hymenoptera: teus, a parasitoid of Heliothrips haemorrhoidalis Braconidae), a parasite of Boarmia (Ascotis) (Bouche) in Israel. Phytoparasitica 25, 155. selenaria Schiff. (Lepidoptera: Geometridae). Wysoki, M., Rene, S., Eliahu, M. and Blumberg, D. Phytoparasitica 9, 19–25. (1999) Influence of spinosad on natural Wysoki, M. and lzhar, Y. (1986) Fluctuation of the enemies of avocado and other pests. In: Arpaia, male population of Boarmia (Ascotis) selenaria M. and Hofshi, R. (eds) Proceedings of Avocado (Lepidoptera: Geometridae) estimated by Brainstorming ’99, Calfornia Avocado Com- virgin female baited traps. Acta Oecologica, mission, University of California, Riverside, Oecologia Applicata 7, 251–259. 124 pp. Wysoki, M., Chen, C., Klein, Z. and Bar-Zakay, I. Yasuda, K. and Kinjou, T. (1983) Seasonal preva- (1986) The false codling moth, Cryptophlebia lence of the leaf-footed bug, Leptoglossus leucotreta (Meyrick), a new potential pest in australis Fabricius (Heteroptera: Coreidae) on Israel. Alon HaNotea 40, 572–576 (in Hebrew). fruit of the wild host, Diplocyclos palmatus C. Wysoki, M., de Jong, M. and Rene, S. (1988) Tricho- Jeffrey, and development of immature stages gramma platneri Nagarkatti (Hymenoptera: at various constant temperatures. Proceedings Trichogrammatidae), its biology and ability to of the Association for Plant Protection of Kyushu search for eggs of two lepidopterous avocado 29, 89–91. pests, Boarmia (Ascotis) selenaria Schiff. (Geo- Zeck, E.H. (1932) Investigations on two white metridae) and Cryptoblabes gnidiella (Milliere) wax scales (Ceroplastes) as pests in Australia. (Phycitidae) in Israel. Trichogramma and Other Agricultural Gazette of New South Wales 43, Egg Parasites. Second lnternational Symposium, 611–616. Guanghzou, China, 10–15 Nov. 1986. INRA, Zentmyer, G., Schieber, E. and Popenoe, W. (1987) Paris (Les Colloques de l’INRAS, No. 43). Early history of the avocado during the time Wysoki, M., Ben-Yehuda, S. and Rosen, D. (1992) of the conquistadores. South African Growers’ Reproductive behavior of the honeydew Association Yearbook 10, 11–12.

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9 Pests of Guava

W.P. Gould1 and A. Raga2 1USDA-ARS, Subtropical Horticulture Research Station, 13601 Old Cutler Road, Miami, FL 33158, USA; 2Instituto Biologico, Caixa Postal 70, 13.001-970, Campinas, SP, Brazil

Guava, Psidium guajava L., belongs to the manipulation of water, fertilizer, pruning Myrtaceae. This plant family has between 110 and defoliation, guavas can be forced to and 130 species of trees and shrubs. Myrtaceae produce a larger crop outside of the normal contains a number of fruit trees of economic fruit phenology. In south Brazil, guavas are importance including rose apple (Syzygium available in the fresh market all year long. jambos (L.)), Surinam cherry (Eugenia uniflora Fruits are mature 90–150 days after flower- L.), and Java plum (Syzygium cumini (L.)). ing, depending on the variety or clone of Most of the species occur naturally from the fruit and cultural and weather conditions southern Mexico to South America and (Nakasone and Paull, 1998). The large white the Caribbean. Guava is a small tree that is flowers attract a large variety of pollinating grown worldwide in the tropics and warm insects including many species of bees. In subtropics for its edible fruit. many tropical regions the honeybee, Apis mellifera L., is the most important pollinator species. Tree Phenology, Origin, World Production, Importance Origin Tree phenology The guava is native to the American tropics, Guavas can flower and bear fruit con- and probably originally grew from Peru tinuously in the tropics; however, there are north to Mexico and the Caribbean (Kwee normally two crops a year. In Florida and and Chong, 1990). Early Spanish explorers in Puerto Rico (USA) there is a large crop the Caribbean observed that guavas were in early to mid-summer (June and July), cultivated by the Caribbean Indians. The and a smaller crop in late winter (February) Spanish brought the guava with them to the (Morton, 1987). A smaller crop is harvested Philippines, and from there it spread to most in Hawaii (USA) in April to May and a Asian countries. The guava was deliberately heavier crop in September and November spread but it is also dispersed by animals (Nakasone and Paull, 1998). In India and eating the fruits. In some parts of the world Malaysia the main crop is harvested in it is considered a weed because it invades mid-winter and the lesser crop during habitats and displaces native plant species. the rainy season (July–September) (Morton, Today guavas are found in all subtropical 1987; Kwee and Chong, 1990). Through and tropical parts of the world. ©CAB International 2002. Tropical Fruit Pests and Pollinators (eds J.E. Peña, J.L. Sharp and M. Wysoki) 295

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World production, importance countries such as Brazil, Venezuela and Ecua- dor. According to European importers, pink Guavas are either eaten fresh, or used in juice, guava juice has a higher usage rate because of ice cream, jellies, pastes or preserves. Accord- its colour and flavour (Galinsky, 2000). ing to Chitarra (1996) guava is considered an important fruit nutritionally because of the high level of ascorbic acid which can be five Key Pests times greater than in oranges and ten times greater than in tomatoes. Fruit flies In south Florida, guavas are grown as backyard fruits and 32.4 ha are grown BIOLOGY Wherever guavas are grown commercially (Murray and Campbell, 1989). commercially, fruit flies are the key pests Hurricane Andrew, in 1992, did a large (Table 9.1). Guava is almost a universal host amount of damage to south Florida’s tropical for fruit-infesting Tephritidae. The female fruit industry. About 84% of the guava trees fruit fly seeks the host fruit using odour and survived the hurricane (Crane et al., 1993) but visual stimuli; using a piercing ovipositor she some groves were abandoned by owners put deposits eggs under the surface of the fruit out of business by the storm. (Plate 66). Some fruit fly species deposit single In many parts of the tropics guavas are eggs, and leave oviposition-deterring phero- a major crop. In recent years production for mones to ensure that the larvae will have juice processing has increased. The countries enough resources, while other species deposit which produce the largest crops of guavas are several hundred eggs in one oviposition punc- India, Brazil and Mexico (Kwee and Chong, ture. Even if eggs are not laid in the fruit or do 1990). Brazil is the largest producer of guavas, not hatch, the oviposition punctures or stings in 1996 production volume was estimated at can render a fruit unmarketable. After several 251,264 t, grown on 11,035 ha. About 80% of days the eggs hatch into larvae. The larvae Brazilian production is in the states of São burrow and feed under the surface of the fruit Paulo (southeast) and Pernambuco (north- for 7–10 days depending on temperature. The east), including fresh market and industry larvae pass through three instars inside the processing (Agrianual, 2000). In 1987, guavas fruit. As the larvae grow, and especially if high were estimated to be grown on more than populations are present, they may leave the 50,000 ha in India, producing 27,319 t annu- surface region of the fruit and burrow through ally (Morton, 1987). Kwee and Chong (1990) the central pulp area. During cool periods lit- reported that in 1969 India produced over tle or no development occurs, which extends 200,000 t. Most of this fruit is locally con- the amount of time the insect spends inside sumed, so production figures are difficult to the fruit. Under favourable conditions the determine. Other countries with significant larvae emerge from the fruit 1–2 weeks after production are Colombia, Cuba, Dominican oviposition. The larvae cut an exit hole from Republic, Egypt, Guyana, Haiti, Jamaica, the fruit and drop or ‘jump’ from the fruit. Kenya, Malaysia, Philippines, South Africa, If the fruit has fallen to the ground, the larvae Taiwan, and USA (primarily Florida, Hawaii may pupariate immediately underneath the and Puerto Rico) (Kwee and Chong, 1990). fruit. They usually burrow several centimetres Exact production figures are often not into the soil before pupariation (Hennessey, reported, or multiple fruit crops are reported 1994). The duration of the puparial stage again together. In the USA, Hawaii produces and depends on temperature. Under favourable consumes the bulk of guava juice and papaya conditions adults emerge 7–10 days after juice. Mexico produces guavas commercially pupariation. The adult flies must feed for in the central states of Aguascalientes and several days to a week on carbohydrate and Zacatecas (Aluja and Liedo, 1986). White protein sources before they can mate and guava juice is exported from India, and lay eggs. Mating takes place in groups or pink juice is exported from South American leks on or near the host tree. Dispersal after

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emergence from pupariation is common and males. Some of the pheromones are very host- allows flies to colonize new areas and find specific, others less so. This host specificity is new hosts as the original host fruits age. good if only one type of fly is desired, but pheromone or parapheromone baits do not SAMPLING, MONITORING Trapping is used exist for many species. to detect and identify fruit fly populations. Less widely used is a fruit mimic trap, a Traps are baited with pheromones used by coloured ball coated with sticky substance. the flies to attract mates, parapheromones These traps often catch non-target organisms derived originally from plants, and also with and are messy to work with. They are most protein, cane sugar or food-based odours. The commonly used for temperate fruit flies, in pheromone and parapheromone lures attract the genus Rhagoletis, in temperate fruit crops. primarily males. The protein, cane sugar or They are also used for the papaya fruit fly, food-based odours attract both sexes. Lures Toxotrypana curvicauda Gerstaecker (Landolt are not available for all species. The phero- et al., 1991, 1992). A variety of these traps mones and parapheromones are specific for are commercially available from integrated closely related species of fruit flies. Methyl pest management (IPM) supply companies. eugenol and cuelure attract many species of Trapping is the basic tactic for fruit fly IPM Bactrocera. Tri-medlure only attracts species because the monitoring can prevent damage, closely related to the Mediterranean fruit fly and avoid the establishment of exotic species (Medfly), Ceratitis capitata (Wiedemann). Dev- in new regions. eloping pheromone lures can be a difficult and Another way to sample populations of an expensive process, so lures exist mainly for fruit flies is to collect the host fruits and rear the most economically important species. The the larvae that emerge. This can be a labour- protein lures are useful in general surveys, but intensive process, but it gives accurate infesta- they are not as powerful an attractant as some tion rates, and also gives information on of the parapheromone lures. parasitism. The fruit are simply collected, and There are a number of widely used trap held in containers over a pupariation sub- types. The McPhail trap (McPhail, 1937) is a strate such as sand or vermiculite. The larvae glass or plastic trap often used with a liquid emerging from the fruits can be sifted from the protein bait (Plate 67). The bait odour travels pupariation medium and held for emergence. out through a central hole. Flies attracted to Souza Filho (2000) obtained an average of 36.9 the odour fly upwards into the trap and fall larvae kg−1 of unsprayed guava in the state of into the liquid. This type of trap has been used São Paulo from eight tephritid species. to trap nuisance flies for many years in Asia and Europe even before McPhail rediscovered ECONOMIC THRESHOLDS Fruit fly population it (Steyskal, 1977). The advantage of this trap management can be placed in one of two cate- is that it can be used to detect many fruit fly gories; management by individual growers to species including Bactrocera, Anastrepha and produce a marketable crop, and management Ceratitis. The disadvantages are that it is heavy, on a large scale by some regulatory pro- expensive, glass versions are fragile, and the gramme. In large-scale eradication program- liquid refilling can be a logistical problem. mes, the capture of a single fruit fly will trigger Another commonly used trap is the cylin- increased trapping and mass suppression drical trap which can be plastic (Steiner trap) efforts. The economic threshold for the or cardboard (Jackson trap). In the Steiner trap individual grower will depend upon whether an insecticide is placed along with the bait in a the crop is intended to be used for juice or pulp cotton wick. In the Jackson trap a pheromone or for the fresh market. The threshold for the or parapheromone bait is placed inside along fresh market is very low because a single larva with a panel coated with a sticky substance. in the pulp is generally not tolerated by the The attracted flies become stuck on the sticky consumer. As a result of this, economic thresh- panel. The Jackson trap is inexpensive and olds have not been determined. Unsprayed attracts great numbers of flies. If the traps guavas are almost always infested with fruit are baited with pheromones they catch only fly larvae.

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298 W.P. Gould and A. Raga minor minor minor minor key key key minor key minor minor minor minor minor key key key key minor minor minor minor minor minor minor minor key Pest status Parts attacked fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit Iran Guam, Thailand Tobago Papua Guam, China, and America Myanmar, Thailand Malaysia, Guinea Taiwan, Myanmar, Hawaii, Guinea, South Trinidad Trinidad New Asia, Cambodia, Lanka, New Malaysia, America Japan, Sri Papua Philippines, Malaysia, America, America, America America Vietnam Caribbean, South China, South-East Tanzania, Indonesia, Bangladesh, Pakistan, South South South South Florida Pakistan, Indonesia, Myanmar, India, Australia Australia Thailand, Taiwan, America America, and and and America, and India, Kenya, America America America America Nepal, Guinea, Distribution Brazil Central South Central Brunei, Central Brazil South South Central Caribbean Central Brazil South Argentina Central Brazil Central Caribbean, Brazil Brazil Northern Northern Australia, Taiwan, India, New Indonesia, Thailand, Southern Hawaii, Egypt, fly fly fruit fly fly fly fly fruit fly fly fruit fruit name fruit fruit fruit fruit fly American Indian Common Guava Melon Oriental West Serpentine Guava Caribbean South Mexican (Loew) (Hardy) (Wiedemann) (Wiedemann) Bezzi (Hendel) (Coquillett) (Loew) Lima Bezzi Lima Hendel Stone Lima Zucchi Zucchi (May) (Tryon) Blanchard (Bezzi) (Fabricius) (Macquart) (Walker) (Hendel) (Loew) Stone Schiner

antunesi bahiensis bistrigata daciformis fraterculus leptozona ludens minensis obliqua ocresia parishi pseudoparallela punctata schultzi serpentina sorocula striata suspensa turpiniae zenildae aquilonis breviaculeus bryoniae caudata correcta cucurbitae dorsalis a complex) guava. of (species Species Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera pests fly Fruit Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Family 9.1. e l b a T Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Order

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Pests of Guava 299 minor minor minor key minor minor key minor minor minor minor minor key minor key key minor minor minor minor key minor Malavasi 1993; fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit Kapoor, Laos, Africa, Thailand Africa South Vietnam, Mali, 1993; Central Africa, ., Zambia,

al Western South Asia, South Laos,

et Yemen Malawi, South Indonesia, Fiji, Pakistan, Zaire, Tonga Europe, Thailand, Pacific Mauritius Foote East, Namibia, China, Kenya, Burma, Island, South-East South Indonesia, Islands, Zimbabwe, Samoa Guinea Rwanda, Guinea Taiwan, Uganda, America, 1992; Vietnam, Islands Seychelles Caledonia Middle Pakistan Niue New Malawi, Asia, Cook New Lanka, Vanuatu Ethiopia, Guinea, Guinea, South Zambia, Western Cook Fiji, New Nigeria, Cambodia, Sri union, é Tanzania, Lanka, Papua Thailand, R Philippines, New Papua New Pacific, Tonga, Africa, Sri Zimbabwe, Elson-Harris, India, Botswana, Angola, Kenya, Pacific, Pacific, Pacific, Pacific, Nepal, South-East Lanka, and Zimbabwe Brazil Swaziland, Mozambique, Madagascar Africa, Sudan, Africa, Africa, Tonga Australia, Pacific Australia South South Australia, South Malaysia South Burma, Indonesia, Australia, Southern Samoa, India, India, Malaysia, Sri Hawaii, America Mauritius, China, White fly fly fly fly 1989; fly fruit fruit fruit fruit fly fruit fly fly fly Hooper, fly fruit fruit fruit fruit and Mediterranean Mascarene Marula Madagascan Five-spotted Natal Queensland Peach Mango Fijian Robinson neville 1988; (Hardy) é (Froggatt) (Schiner) (Broun) (Coquillett) (Bezzi) Kim, rin-M (Coquillett) Munroe (Coquillett) é (Drew) (Saunders) (Tryon) (Froggatt) (Bezzi) (Wiedemann) (Froggatt) and (Froggatt) (Walker) Gu (Walker) Karsch

diversa facialis frauenfeldi jarvisi kirki melanota neohumeralis passiflorae pedestris psidii tau trivialis tryoni xanthodes zonata spp. capitata catoirii cosyra malgassa quinaria rosa Norrbom 1978; Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Bactrocera Ceratitis Ceratitis Ceratitis Ceratitis Ceratitis Ceratitis Neosilba .,

et Drew 2000. Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Tephritidae Lonchaeidae Zucchi, References: and Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera Diptera a

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300 W.P. Gould and A. Raga

CONTROL TACTICS Control tactics for large- A. Raga (unpublished) have shown that there scale eradication programmes are outside of is potential in this area. In general, fruits the scope of this work, so this discussion will which develop more rapidly (are available centre on control tactics for the individual on the tree for a shorter time), have thicker grower. The primary methods of control have rind, or have unfavourable chemical environ- been chemical control and physical barriers. ments in the peel, may effectively reduce Biological control has been attempted fly populations (Greany and Shapiro, 1993). on an area-wide basis by release of parasites Jalaluddin et al. (1998a) reported that pre- against fruit flies (Plate 68). Due to chemical colour break treatment of guava fruits with spraying and consumers’ low tolerance for 50 p.p.m. gibberellic acid (GA3) reduced fruit fruit damage, these projects have had limited susceptibility to infestation by Bactrocera cor- success. A long-term augmentative release recta (Bezzi). Jalaluddin et al. (1998b) demon- project might be the most successful tech- strated that cultivar ‘Lucknow 46’ was highly nique, but high costs of parasite mass-rearing resistant to B. correcta, whereas cultivars have prevented this from being adopted on a ‘AC 10’, ‘Lucknow 49’ and ‘Chittidar’ were wide scale. moderately resistant, susceptible and highly Chemical control is used almost every- susceptible to B. correcta attack, respectively. where that guavas are grown commercially. Autocidal techniques have been used in Cover sprays of carbamates, synthetic pyre- eradication programmes with great success. throids, and organophosphates are applied This technique is very expensive and requires on a calendar basis to prevent fruit fly mass rearing of millions of insects which are populations from building up in the orchard. then sterilized and released. Many outbreaks These sprays are not effective unless the area of exotic fruit flies have been eradicated sprayed is very large because of the flight using this tool in combination with bait ability of the fruit fly. One of the potential sprays. Bait sprays have not generally been negative results of calendar spraying on a used by growers but have remained primarily large scale is outbreaks of secondary pests. a tool of large-scale eradication projects. When a large guava orchard in Florida (USA) Eradication projects are extremely expensive was sprayed on a regular basis to prevent and are undertaken by government and inter- fruit fly infestation, outbreaks of scale insects national agencies when the potential cost from became a problem. The mass spraying of crops damage by new invasive species is extreme. destroys natural and introduced biological Costs for these programmes are high, so they controls (predators and parasites). In south are not attempted against well established Florida (USA), parasites of the Caribbean fruit or native species. The widespread spraying fly, Anastrepha suspensa (Loew), both naturally of pesticide over urban areas has also occurring and augmentative releases, have raised concerns among the public about the been reduced to very low levels by regular desirability of these programmes. The effect pesticide spraying. Only in unsprayed reser- of these spray programmes on non-target voirs such as parks, back yards and natural organisms in the environment is another areas, can any parasites be found (W.P. Gould, serious concern. unpublished; Souza Filho et al., 2000). In the The second major method of preventing state of São Paulo, four braconid species infestation is the use of barriers. Plastic net- reached 3.1% of parasitism of Anastrepha ting, plastic bags and paper bags have been spp. where 94.9% were Doryctobracon areolatus used successfully to prevent fruit flies from (Szépligeti) (Souza Filho, 2000). Four species ovipositing in guavas (Howard, 1986; Kwee of Figitidae were detected in guavas in Brazil and Chong, 1990) (Plate 69). Fruits must be (Guimarães et al., 1999). The importance of wrapped early in their development before Figitidae is probably underestimated in the they are suitable for oviposition by fruit flies. biological control agent complex. The bags must be adequately ventilated to Few plant resistance studies have been prevent humidity from allowing establish- attempted against Anastrepha sp. in guavas, ment of fungi. The bags may also allow but works by Hennessey et al. (1995, 1996) and build-up of scale insects and mealybugs. The

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Pests of Guava 301

main disadvantage to bagging of fruit is the last resort, and that the minimum treatment labour cost (Kwee and Chong, 1990). necessary be used to effect control. Some alternative methods of control are either not practised, or are only practised as parts of large-scale regulatory efforts. Qureshi Hemiptera: Heteroptera (bugs) and Hussain (1993) found that mass trapping reduced fly populations of Bactrocera dorsalis In Malaysia, Heliopeltis theobromae Miller (Hendel) and B. zonata (Saunders) in guava (Miridae), a serious pest of cacao, also attacks and mango orchards to subeconomic levels guavas (Kwee and Chong, 1990). These bugs (5.5%) which were considerably lower than feed on many parts of the plant including the those produced by pesticide spraying fruit. Damage to the fruit results in necrotic (20.25%). lesions which render it unmarketable. The It is often recommended that growers symptoms of damage are clear, but the causal remove and destroy all unused fruits in the insect is often missed by the grower. There field, to reduce reservoirs of fruit fly larvae. are no biological controls known, and control This practice has been an effective part of is usually by pesticide applications. In south large-scale eradication programmes; on a Florida (USA), South America, and parts of small scale its effectiveness may not be as the South Pacific, several species of Lepto- great (Burton, 1930; Hansen and Armstrong, glossus (Coreidae) attack the fruits, also caus- 1990; Liquido, 1993). Soil drench pesticide ing necrotic scab-like lesions when the fruits sprays have also been used against fruit mature (Nafus and Schreiner, 1999; Peña fly puparia and larvae in large eradication et al., 1999). These types of pests are usually programmes. This method is expensive and only a problem to the grower during fruit for- has limited effectiveness. mation, and treatment is seldom necessary. Fruit flies present a considerable phyto- These bugs often form aggregations on only a sanitary or quarantine problem for shippers few trees so spot treatment may be an option. of fresh market fruits. Unless the guavas are Cultural control of alternative nymphal hosts grown in areas certified to be free of fruit such as thistle species or other nearby weeds flies, a postharvest commodity treatment will may lower populations of this pest. need to be applied prior to shipment to areas which do not have that fruit fly species. Few quarantine treatments have specifically been developed for guavas. Currently, hot water, Hemiptera: Homoptera (mealybugs, hot air, and irradiation have been developed scale insects) as treatments for the Caribbean fruit fly (Gould and Sharp, 1992; Arthur et al., 1993; There are two families of mealybugs found Gould, 1994). Hot water and irradiation treat- on guavas: Pseudococcidae, which contains ments have been used to ship Florida guavas most of the species; and Margarodidae, the to Texas and California within the USA. giant mealybugs (Table 9.2). Many species are found worldwide. Some commonly reported species on guava are Ferrisia virgata (Cock- erell), Planococcus citri (Risso), Planococcus Secondary Pests pacificus Cox, and Pseudococcus citriculus Cox (Kwee and Chong, 1990), Pseudococcus nipae, There are many secondary or minor pests of Planococcus minor (Maskell) and Pseudococcus guava. Most of these species are of minor lilacinus Cock. importance, but population outbreaks can Mealybugs are soft-bodied insects that occur locally, making these pests important. secrete a waxy protective layer that looks like Very little is known about many of these cotton or snow. The first instars or crawlers pests, and management strategies are also not are the only dispersal stage. They are spread available for most of them. Common sense by the wind or they may walk to new hosts. dictates that controls be applied only as a Once established on a host, large populations

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302 W.P. Gould and A. Raga Pest status minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor fruit fruit fruit fruit fruit stems, fruits shoots, stems, stems, fruit fruit fruit fruit fruit fruit fruit fruit fruit stems stems leaves, leaves, leaves, and buds attacked leaves, Parts fruit, flower fruit fruit fruit fruit fruit fruit fruit fruit leaves, terminal leaves leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, stems, stems, stems, leaves, leaves, America, subtropics subtropics Islands Islands, Caribbean and and Central Pacific Ocean tropics tropics tropics tropics, tropics Pacific America Pacific Florida Florida Florida Japan, America, Indian Africa Africa World World Distribution South Worldwide Malaysia India Brazil South South South South Brazil North Worldwide Old Worldwide Old India Mexico Worldwide Asia, Caribbean India, Malaysia Malaysia Worldwide Asia, Asia, Asia Southern citron scale mealybug mealybug bug bug bug bug, mealybug mealybug mealybug bug name mealybug mealybug mealybug mealybug mealybug mealybug mealybug bug footed footed footed footed hibiscus Common Mosquito Leaf Leaf Leaf Leaf plant Pineapple Striped Pink Spiked Spherical Citrus Cacao Passionvine Long-tailed Mango Mango Giant Steatococcus (Green) Morrison (Green) Cox Cockerell Williams (L.) Newstead Miller (Walker) (Cockerell) (Fabricius) (Fabricius) Cox (Dallas) (Herbst) Cockerell (Herbst) (Westwood) (Newstead) (Maskell) (Maskell) (Risso)

Signoret ferox hirsutus

(Cockerell) citriculus longispinus

psidiarum iceryoides invadens samaraius australis balteatus concolor gonagra stigma zonatus brevipes nipae viridis citru lilacinus minor pacificus clavigera

theobromae antonii Tozetti)

virgata

seychellarum a

Species Helopeltis Helopeltis Holhymenia Leptoglossus Leptoglossus Leptoglossus Leptoglossus Leptoglossus Leptoglossus Dysmicoccus Ferrisia Maconellicoccus Nipaecoccus Nipaecoccus Perissopneumon Phenacoccus Planococcus Planococcus Planococcus Planococcus Pseudococcus Pseudococcus (Targioni Rastrococcus Rastrococcus Icerya Steatococcus guava. of pests insect Miridae Miridae Coreidae Coreidae Coreidae Coreidae Coreidae Coreidae Coreidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Pseudococcidae Margarodidae Margarodidae Family Other 9.2. e l b a Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera T Order

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Pests of Guava 303 minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor

continued fruit fruit fruit fruits fruits fruits fruits fruits fruit fruit fruit fruit fruit fruit fruit fruit fruit stems, fruit fruit stems, stems, stems, stems, stems stems, stems stems stems, stems stems, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, flowers, leaves, leaves, and Asia subtropics Central America, and Caribbean Asia Africa Mediterranean, greenhouses, Europe, South tropics tropics in tropics Florida and Asia, Australia America, America, Malaysia Australia, Worldwide Worldwide Mexico Central Barbados Mexico Mexico, Worldwide Caribbean Africa, Malaysia Malaysia Asia, Malaysia Mediterranean, Africa, Asia, South Worldwide Worldwide North Asia Worldwide Worldwide Worldwide Brazil aphid green aphid, aphid whitefly aphid aphid melon whitefly whitefly whitefly whitefly aphid, aphid, whitefly or peach blackfly aphid citrus legume aphid scale citrus Violet Green Black Soft Greenhouse Black cowpea Groundnut Cotton Spiraea Citrus Spiralling Coconut Woolly Bayberry Avocado de (Singh) Sampson Gray Ashby (Maskell) (Maskell) Hempel Russell Maki (Kuwana) Quaintance

canangae cherasensis psidii (Boyer Takahashi Corbett Patch Koch Sulzer Laing

woglumi Glover truncatus floccosus urichii myricae floridensis vaporariorum psidii janeirensis dispersus maritimus pulvinatus

ficicola formosana aurantii

ornatus persicae craccivora gossypii spiraecola Drews Baker Fonscolombe) Corbett Corbett Quaintance Westwood and Aleurocanthus Aleurodicus Aleurodicus Aleurodicus Aleurothrixus Aleurotuberculatus Aleurotuberculatus Aleurotuberculatus Dialeurodes Parabemisia Paraleyrodes and Tetraleurodes Trialeurodes Trialeurodes Aphis Aphis Aphis Greenidea Greenidea Myzus Myzus Toxoptera Ceroplastes Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aleyrodidae Aphididae Aphididae Aphididae Aphididae Aphididae Aphididae Aphididae Aphididae Coccidae Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera

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304 W.P. Gould and A. Raga Pest status minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, stems, attacked Parts leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, Pacific Tonga Trinidad Asia, subtropics subtropics Guinea Pacific South and and America New Africa, Pacific, Bermuda, Caribbean, South distribution distribution distribution distribution distribution distribution distribution tropics tropics Southern Caribbean Papua Pacific Pacific Pacific Caribbean, India, Asia, Pacific Southern Tobago Distribution Malaysia, Worldwide Caribbean Malaysia Malaysia, Worldwide Florida South Worldwide Florida, Worldwide Worldwide Worldwide Worldwide and Southern Worldwide Mediterranean, Asia, Africa, Southern Caribbean, Worldwide Worldwide Florida, Southern Malaysia Malaysia, scale scale scale, oriental scale scale scale scale scale olive scale scale black red name scale scale scale red scale, scale scale mealy soft shield scale scale scale, scale wax scale wax Common Green Brown Green Acuminate Nigra Pyriform Guava Hemispherical Caribbean Black Soft Red Fig Stellate California Oriental yellow Coconut Dictyospermum Spanish Comstock Signoret Maskell L. Signoret Maskell (Newstead) (Nietner) Lotto Cockerell (DeLotto) (Cockerell (Maskell) (Westwood) L. (Walker) (Signoret)

(Maskell) dictyospermi (Olivier) De Hempel

psidii DeLotto pyriformis Green tessellatus nigra

floridensis rubens rusci

destructor ficus psidii urbicola aurantii orientalis coffeae miranda neglecta oleae stellifera

acuminatus celatus hesperidum viridus

acuminata deltoides Parrott) and Species Ceroplastes Ceroplastes Ceroplastes Cloropulvinaria Coccus Coccus Coccus Coccus Eucalymnatus (Signoret) Kilifia Kilifia Parasaissetia Protopulvinaria (Cockerell) Pulvinaria Pulvinaria Pulvinaria Saissetia Saissetia Saissetia Saissetia Vinsonia Aonidiella Aonidiella Aspidiotus Chrysomphalus (Morgan) . Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Coccidae Diaspididae Diaspididae Diaspididae Diaspididae Family

Continued 9.2. e l b a Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera T Order

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Pests of Guava 305 minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor

continued fruits fruits fruits fruits fruits fruits fruits fruits fruits fruits buds, buds, stems, stems, stems, stems, stems, stems stems stems stems, stems, stems, stems, stems, fruit flower flower tips leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, leaves, bark leaves, leaves, leaves, leaves leaves, leaves leaves, leaves, fruit leaves, fruit leaves leaves shoot leaves leaves leaves leaves fruit Pacific Rico America Lanka Pacific Puerto Southern Korea South Sri Asia distribution distribution tropics distribution distribution Pacific China, China, Mexico Antilles, India, Central, Southern Malaysia China, Florida, Worldwide Florida Florida, Florida Florida Brazil Worldwide Brazil Brazil Worldwide South-East Brazil Lesser Brazil North, Brazil Florida Florida Florida Florida, Worldwide India, Worldwide Southern scale scale gusano scale thrips scale worm scale scale scale mining scale scale scale red fruit skipper, n snow parlatoria scale ó scale Guava Florida Cynophyllum Latania Palm Greedy Armoured Chaff Camellia Camphor Bowrey False Citrus Red-banded Guava cabez e) é (Giard) (Cockerell) (Morgan) (Sepp) (Cockerell) Busck Westwood (Signoret) (Cockerell) (Cockerell) Hood Ashmead Beardsley (Guen (Newstead) Comstock (Comstock) (Stoll) Cramer Reakirt

bowreyi parlatorioides Moulton

ficus involuta

similis laterochitinosa clavigera duplex articulatus cyanophylli diffinis lataniae palmae rapax icasia rubrocinctus dorsalis (Comstock)

charybdis eugeniella arnobia

pergandii sp.

sp. polybius bondari citri

suppressaria Hewitson (Signoret) Green (Comstock) Chrysomphalus Hemiberlesia Hemiberlesia Hemiberlesia Hemiberlesia Hemiberlesia Lepidosaphes Lepidosaphes Parlatoria Pseudaonidia Pseudaonidia Pseudischnaspis Pseudoparlatoria Selenaspidus Unaspis Triozoida Liothrips Selenothrips Selenothrips Eupseudosoma Hypercompe Brachmia Buzura Thyrinteina Phocides Pyrrhopyge & Argyresthia Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Diaspididae Psyllidae Phlaeothripidae Thripidae Thripidae Arctiidae Arctiidae Gelechiidae Geometridae Geometridae Hesperiidae Hesperiidae Hyponomeutidae Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Hemiptera Thysanoptera Thysanoptera Thysanoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera

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306 W.P. Gould and A. Raga Pest status minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor fruits leaves attacked Parts leaves leaves leaves leaves leaves leaves bark leaves leaves fruits fruits leaves leaves, leaves leaves leaves leaves fruits leaves leaves branches leaves buds, fruits India, Minor Myanmar, Pacific Trinidad, Asia Rica Lanka India, South Australia Asia Asia Bangaledesh, Myanmar Sri Costa Asia Africa, Taiwan Asia, Asia, Colombia, Pacific Bangladesh Distribution Malaysia, Thailand, Europe, China, Mexico Bangladesh, Pakistan, Brazil South Africa, Mexico Malaysia India, Malaysia Venezuela Europe, Africa, South-East South-East Brazil Brazil India Malaysia Brazil Malaysia Malaysia Brazil, Tobago, borer moth caterpillar caterpillar name mexicana cotton hairy capsule leafroller bearer moth seda caterpiller eating piercing butterfly moth la Common Anar Coffee Nun Borreguillo Bark Sack Fruit Egyptian leafworm Rice Bagworm Bagworm Castor Atlas Citrus Palomilla de Joannis (Walker)

trujillo Cramer Busck (Boisduval) (Zeller) L. (Stainton) (Salle) (Stoll) Cramer (Fabricius) Butler Hubner (Moore) (Clerck)

pendula Hampson Swinhoe Guilding Moore (Stoll-Cramer) ismene psidii L. defoliata punctiferalis littoralis palpalis zizyphi clotilda

vita laocoon monacha xylina fullonia fraterna quadrinotata kirbyi isocrates leda armigera

emigratella spp. amilia minuscula atlas e)

tongaensis é

Species Eutachyptera Odonestis Deudorix Euproctis Lymantria Lymantria Megalopyge Schaus Indarbela Mimallo Anua Eudocima Heliothis Gonodonta Spodoptera Melanitis Cremastopsyche Eumeta Oiketicus Conogethes (Guen Attacus Citheronia Timocratica Psorosticha Amorbia Amorbia . Lasiocampidae Lasiocampidae Lycaenidae Lymantriidae Lymantriidae Lymantriidae Megalopygidae Metarbelidae Mimallonidae Noctuidae Noctuidae Noctuidae Noctuidae Noctuidae Nymphalidae Psychidae Psychidae Psychidae Pyralidae Saturniidae Saturniidae Stenomidae Tineidae Tortricidae Tortricidae Family

Continued 9.2. e l b a Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera T Order

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Pests of Guava 307 minor minor minor minor minor minor minor minor minor minor key key minor minor minor minor minor minor minor minor minor minor

continued stems, stems, roots roots in in leaves leaves fruits leaves buds, buds, leaves boring twigs boring twigs leaves fruit fruit fruit leaves, leaves, leaves leaves leaves leaves leaves leaves leaves fruits Indian Bolivia Asia, Tobago and Panama Caribbean Caribbean Venezuela Venezuela, Pacific Pacific Pacific, Africa South South Malaysia Malaysia Trinidad Africa, Brazil Brazil, Florida Mexico Brazil, Florida, Caribbean Malaysia Mexico Mexico Mexico South Ocean Mexico, Malaysia Mexico citrus moth weevil moth weevil, leaf bud beetle weevil borer codling borer beetle False Guava Black Trunk Yellow Apopka weevil Golden Green Rose Temolillo Meyrick

indetana L. (Walker) (Busck) Burmeister Champion Dietz (Boheman) L. Marshall Walker Harold Fabricius (Meyrick)

thoracicus dimidiatus psidii leucotreta lunulata ejectana rothia smithiana tetropsis vitticollis irroratus ferruginea albosignatus cervinus squamosus

abbreviatus splengleri sp.

versutus sp.

aprobola monachus

Cryptophlebia Dudua Strepsicrates Strepsicrates Strepsicrates (Dyar) Strepsicrates Apate Retrachyderes (Oliver) Costalimaita (Fabricius) Anthonomus Conotrachelus Champion Conotrachelus Diaprepes Diaprepes Hypomeces (Fabricius) Pandeleteius Pantomorus Boheman Pantomorus Adoretus Cyclocephala Maladera Euphoria Tortricidae Tortricidae Tortricidae Tortricidae Tortricidae Tortricidae Bostrichidae Cerambycidae Chrysomelidae Curculionidae Curculionidae Curculionidae Curculionidae Curculionidae Curculionidae Curculionidae Curculionidae Curculionidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Lepidoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera Coleoptera

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308 W.P. Gould and A. Raga Pest status minor minor minor minor minor minor minor minor minor minor minor minor minor minor minor 1992; twigs, twigs, wood Filho, fruit fruit fruit fruit, fruit fruit fruit fruit fruit fruit in in in attacked Batista Parts leaves boring stems boring stems leaves boring leaves, leaves, leaves, leaves, branches leaves, leaves, leaves, leaves, leaves, leaves, and Kubo of 1990; States Republic Seychelles Australia Chong, distribution distribution India, Mexico United Brazil and Asia, Pacific Korea, Kwee Distribution Islands, Philippines Malaysia South Florida Florida Worldwide Worldwide Malaysia Malaysia, India India, Georgia, Africa, Malaysia, Mexico Florida 1988; mite mite mite 1999. Medina, termite scorch ., mite name

al mite leaf tree flat brown

spider et 1988; mite a ., ñ al Pe Common Grasshopper Forest Guava Citrus False Pecan Citrus Red et 1999; Gallo banes Klein é (Banks) 1987; (Hirst) (Geijskes) Snyder Hopkins Est Brenske (Boczek) Schreiner, Sjost

eruditus psidii Morton, and hicoriae orientalis sp.

sp. biharensis psidium guavae californicus phoenicis connexus rufoflava 1981;

nigricornis Nafus sp. Baker 1999; Species (Westwood) (McGregor) Holotrichia Hypothenemus Hypothenemus Valanga Neotermes Tegolophus Tarsonemus Brevipalpus Brevipalpus Panonychus Eotetranychus Eutetranychus Oligonychus Oligonychus and Tydeus Anonymous, Gaona, 1968; ., .

et Gonzalez Scarabaeidae Scolytidae Scolytidae Acrididae Kalotermitidae Eriophyidae Tarsonemidae Tenuipalpidae Tenuipalpidae Tetranychidae Tetranychidae Tetranychidae Tetranychidae Tetranychidae Tydeidae Family Silva

Continued 1999; 9.2. e l b a References: Anonymous, Coleoptera Coleoptera Coleoptera Orthoptera Isoptera Acarina Acarina Acarina Acarina Acarina Acarina Acarina Acarina Acarina Acarina T Order a

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Pests of Guava 309

are produced around the original colonizer. Aphididae (plant lice, aphids) Mealybugs can be found on twigs, stems, leaves and fruits. Normally these insects do There are only two important pest species of not damage the host severely, but large popu- aphids attacking guava, and these species lations cause the fruit to become misshapen are both generalists that attack many crops. and deformed. Honeydew produced by Populations seldom build to the level where mealybugs often results in sooty mould which damage is done or control is necessary. lowers the fruit’s market value. Presence of Biological controls of many kinds, parasites mealybugs on the fruit may also be of phyto- and predators, normally keep these aphid sanitary importance. Normally parasites and populations in check. Their life cycle is simi- predators control mealybug populations, but lar to other Homoptera, except that they have misuse or overuse of pesticides may disturb parthenogenetic forms. This allows for very this balance. Oil or soap sprays are often used rapid population increase after colonization. more effectively since they are safer for biolog- In the sequence of several generations on a ical control agents. Ants are often associated new host, reproductive winged forms are with mealybugs, aphids and other homop- produced which then can disperse to new terans that produce honeydew. Ants protect hosts. mealybugs from predators and parasites. Bagging fruits to protect them from fruit flies Coccidae and Diaspididae (scale insects) actually benefits the mealybugs, protecting There are two families of scale insects them from predators and parasites and form- found on guava: Coccidae (soft scales) and ing a favourable microclimate inside the bag. Diaspididae (armoured scales). Scales may be In Venezuela, the cottony scale Capulinia found on stems, leaves and fruits. The life sp. near jaboticabae von Ihering (Eriococcidae) cycle of scales is similar to that of mealybugs. has become one of the most destructive guava Biological control keeps scale populations pests since 1993 (Chirinos, 2000). The adult in check most of the time. Unusual weather female measures c. 1.36 × 0.86 mm (length × conditions like drought, or use of pesticide width); the female undergoes two nymphal may cause population outbreaks. Oil or soap instars whereas the male undergoes four sprays are normally effective in controlling nymphal instars (Chirinos, 2000). Chirinos scale outbreaks and minimizing damage to (2000) reported that survival of Capulinia was biological controls. Some pheromone traps lower on cv. 12 (Psidium friedichsthalianum are used to time sprays to coincide with scale × P. guineense) and higher in P. guajava cv. outbreaks. With all Homoptera, their extreme ‘criolla roja’. reproductive capabilities must be respected. Only apply controls when necessary. Follow- Aleyrodidae (whiteflies) up treatments are needed to control the Whiteflies have a life cycle similar to mealy- crawlers which hatched from eggs sub- bugs. Most of the information given for sequent to the first treatment. Use the mealybugs applies to whiteflies as well. One minimum treatment necessary to control major difference is that adult whiteflies the problem. Scale insects may also be a are much more mobile than mealybugs. phytosanitary issue, and the coating of scales A number of species have been identified on the fruits makes them less marketable. attacking guava (Table 9.2). In Cuba, Vazquez et al. (1996) reported that among fruit trees, guava has the highest Thysanoptera (thrips) frequency of Aleyrodicus floccosus Maskell and it also supports the largest number of whitefly Thrips are tiny, but important, pests of many species (e.g. Aleurocanthus woglumi Ashby, crops. The red-banded thrips, Selenothrips Aleyrodicus dispersus Russell, Aleyroglandulus rubrocinctus (Giard) is a widely distributed malangae Russell, Bemisia tabaci (Gennadius) pest of tropical crops. It attacks cacao, cashew, among others). mango (Palmer et al., 1989), coffee, rubber,

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passion fruit, coconuts, avocados as well as fruits. This feeding leaves the growing fruit guavas. In Brazil it is also recorded in Euca- misshapen, and damage is similar to that lyptus and Eugenia (Monteiro, 1994). The caused by bugs. Fruit piercing moths are economic impact of the damage is hard very difficult to control because they can fly to assess. The thrips feed on the leaves and great distances in large numbers and cause fruit and cause a russetting or bronzing of the severe damage. Chemical sprays have little or plant surface. Bronzing on the fruit decreases no effect on the transient adults. The only the marketability and value of the crop. Some method to prevent damage is the bagging of predators and parasites are known to attack the guavas while they are still very small. S. rubrocinctus (Bennett and Baranowski, 1982; Dennill, 1992). Chemical control is used in cacao, but is seldom necessary on guava. Coleoptera (beetles) In South-East Asia, Scirtothrips dorsalis Hood also attacks guava (Kwee and Chong, 1990). The most serious pests of guava outside Thrips are most likely to cause problems of the fruit flies are several species of fruit when the plant is grown under stress boring weevils. Conotrachelus psidii Marshall conditions such as drought (Kwee and and C. dimidiatus Champion, though limited Chong, 1990) or with nutritional deficiency in distribution, can be a serious problem for (Fennah, 1963). growers (Boscán de Martínez and Casares, 1980, 1981). Infestation rates are reported to vary widely among cultivars, and the best Lepidoptera (butterflies and moths) control was obtained by timing insecticide application to the emergence of adults from the soil directly beneath the trees. These There are a number of families of Lepidop- weevils would be more serious pests if they tera that have members which can be found were widely distributed; but because of their on guava. Most Lepidoptera larvae are narrow host range, they have not become as foliage feeders, but some species bore into widespread and as damaging as the many the fruits as well. The surface feeding species species of fruit flies. normally do not cause great damage to the A number of species of Curculionidae tree. The trees can survive defoliation with and Scarabaeidae feed as adults on the leaves little harm to the crop. Frequent severe defoli- and cause minor defoliation. Some of the ation can kill small trees. A number of species Curculionidae feed on the roots as larvae and of Lepidoptera fold the leaves about them- may damage nursery trees. Nematodes can be selves (leafrollers), so they are difficult to an effective control method for weevils with find. Some species feed only at night. The burrowing larvae. There are several scolytid best IPM control method is to use some form beetles and a bostrichid beetle that tunnel of Bacillus thuringiensis Berliner, a bacterial in the wood of the guava tree (Table 9.2). A pesticide, since it is specific for Lepidoptera heavy infestation of these pests can kill small and does not harm parasites and predators. trees. Larvae that are protected from direct contact with this natural pesticide, such as those which bore into the fruit, are leafrollers, or bagworms, and are harder to kill. Internal- Arachnida: Acarina, mites feeding larvae may also be a phytosanitary problem. Very large larvae like those of the Mites are ubiquitous on plants, but they are Atlas moth, Attacus atlas (Linnaeus), can be so small they often go unrecognized. Their hand picked from the trees. The fruit piercing feeding drains the cell contents, leaving the moth, Eudocima fullonia (Clerck), is unique in tissue with a bleached or scalded look. If the that it is the adult stage that causes damage to feeding extends to the fruits, the fruits may the fruit. These moths have a piercing probos- be less marketable. In Costa Rica, colonies of cis which they use to feed on the juices of the Oligonychus yothersi (see Chapter 8) are found

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on the leaf upperside (Ochoa et al., 1994). In losses. An outbreak of scale insects or mealy- Malaysia, sporadic attacks of Panonychus sp., bugs is better tolerated to allow biological Eotetranychus sp. and Oligonychus biharensis controls adequate time to respond. (Hirst) are observed (Kwee and Chong, 1990). The fruit flies are a difficult problem. These species are reported feeding on the Eradication of exotic species has become a underside of the leaves, causing leaves to major industry, but it is very expensive and is become dull green, and then bronzed. Popu- only undertaken by large governmental orga- lations are higher during dry spells and in nizations. For the control of an established situations when the plants tend to suffer from species on guava, bagging the fruits remains water stress, such as when guava is grown in the only effective method of control, and the sandy soils (Kwee and Chong, 1990). economics of hand labour make it difficult to In Florida, USA, the mites, Tegolophus accomplish on a large scale. Heavy chemical guavae (Boczek) and Brevipalpus spp., cause spraying may lead to subsequent outbreaks of damage to fruits and tender leaves (Peña secondary pests and should be avoided. The et al., 1999). Highest numbers of T. guavae are flies are only vulnerable as adults, and the observed in early autumn, through winter and effect of foliar spray is limited. Bait sprays during spring months. The mites are most show promise, and as new formulations and often observed on the fruit, causing ‘pimples’ baits are invented, these may become key or deformations. methods of control. In Florida, USA, Brevipalpus sp. densities only increased on the leaves between the summer months and autumn. However, in Central References America, Brevipalpus phoenicis (Geijskes) have been observed causing fruit to turn brown, Agrianual (2000) Anuário da Agricultura Brasileira. smooth and shiny, with epidermal cracking. Argos Comunicação, São Paulo, 546 pp. Symptoms on leaves are characterized by Aluja, M.R. and Liedo, P.F. (1986) Perspectives on epidermal cracking on the leaves (Ochoa future integrated management of fruit flies in et al., 1994). Mexico. In: Mangel, M., Carey, J.R. and Plant, In Costa Rica, Ochoa et al. (1994) reported R.E. (eds) Pest Control Operations and Systems that injuries to fruit, i.e. deep striations Analysis in Fruit Fly Management, NATO ASI resembling craters, caused by Selenothrips Series G: Ecological Sciences, Vol. 11. Springer Verlag, New York, pp. 9–42. rubrocintus (Thysanoptera: Thripidae), can be Anonymous (1981) Plagas de los principales used by B. phoenicis to form colonies. cultivos de Mexico. Fitofilo 86, 98–99. Mite populations develop resistance to Anonymous (1999) Crop Protection Compen- pesticides very rapidly because they have dium Global Module. CAB International, such a short generation time. Soap or oil Wallingford, UK, CD-ROM. sprays may be an alternative control method. Arthur, V., Leme, M.H.A., Wiendl, F.M., Silva, A.C., Faria, J.T. and Wiendl, J.A. (1993) Desin- festacao de fruto de goiaba infestados pela mosca-da-fruta Anastrepha obliqua (Mac., 1835) Conclusions (Diptera: Tephritidae) através da radiação gama do cobalto-60. Revista de Agricultura Guava pest management is divided into two (Brazil) 68, 207–217. parts: (i) dealing with the key pests, usually Bennett, F.D. and Baranowski, R.M. (1982) First species of tephritid fruit flies; and (ii) manag- record of the thrips parasite Goetheana ing the minor pests which are varied. The parvipennis (Gahan) (Eulophidae: Hymenop- tera) from the Bahamas. Florida Entomologist minor pests seldom need treatment. If a treat- 65, 185. ment is necessary, the minimum treatment Boscán de Martínez, N. and Casares, M.R. (1980) to obtain control should be used. Biological El gorgojo de la guayaba Conotrachelus controls and cultural methods should be the psidii Marshall (Coleoptera: Curculionidae). first line of defence. Damage to the trees does Evaluacion de daños. Agronomic Tropical not usually translate directly into heavy crop (Venezuela) 30, 77–83.

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Boscán de Martínez, N. and Casares, M.R. (1981) Gould, W.P. (1994) Heat quarantine treatments Distribucion en el tiempo de las fases del for guavas infested with the Caribbean fruit gorgojo de la guayaba Conotrachelus psidii fly. Proceedings of the Florida State Horticultural Marshall (Coleoptera: Curculionidae) en el Society 107, 240–242. campo. Agronomic Tropical (Venezuela) 31, Gould, W.P. and Sharp, J.L. (1992) Hot-water 123–130. immersion quarantine treatment for guavas Burton, R.P. (1930) Citrus grove sanitation. Proceed- infested with Caribbean fruit fly (Diptera: ings of the Florida State Horticultural Society 43, Tephritidae). Journal of Economic Entomology 140–142. 85, 1235–1239. Chirinos, D.T. (2000) Biología de la mota blanca del Greany, P.D. and Shapiro, J.P. (1993) Manipulation guayabo, Capulinia sp., cercana a jaboticabae and enhancing citrus fruit resistance to the von Ihering (Hemiptera: Eriococcidae) y Caribbean fruit fly (Diptera: Tephritidae). su potencial de desarrollo de poblaciones Florida Entomologist 76, 258–263. sobre varias especies de Psidium. Universidad Guimarães, J.A., Zucchi, R.A., Diaz, N.B., Souza Central de Venezuela, Facultad de Agronomía, Filho, M.F. and Uchôa, F., M.A. (1999) Espécies Maracay, Venezuela (Thesis). de Eucoilinae (Hymenoptera: Cynipoides: Chitarra, M.I.F. (1996) Características das frutas de Figitidae) parasitóides de larvas frugívoras exportação. In: Goiaba Para Exportação: Procedi- (Diptera: Tephritidae e Lonchaeidae) no Brasil. mentos de Colheita e Pós-colheita. Ministério Anais da Sociedade Entomológica do Brasil 28, da Agricultura, do Abastecimento e Reforma 263–273. Agrária, Brasília, DF, pp. 9–11. Hansen, J.D. and Armstrong, J.W. (1990) The failure Crane, J.H., Campbell, R.J. and Balerdi, C.F. (1993) of field sanitation to reduce infestation by Effect of hurricane Andrew on tropical fruit the mango weevil Cryptorhynchus mangiferae trees. Proceedings of the Florida State Horti- Fabricius (Coleoptera: Curculionidae). Tropical cultural Society 106, 139–144. Pest Management 36, 359–361. Dennill, G.B. (1992) Orius thripoborus (Antho- Hennessey, M.K. (1994) Depth of pupation of coridae), a potential biocontrol agent of Caribbean fruit fly (Diptera: Tephritidae) Heliothrips haemorrhoidalis and Selenothrips in soils in the laboratory. Environmental rubrocinctus (Thripidae) on avocado fruits in Entomology 23, 1119–1123. the eastern Transvaal. Journal of the Entomo- Hennessey, M.K., Knight, R.J. Jr and Schnell, R.J. logical Society of Southern Africa 55, 255–258. (1995) Antibiosis to Caribbean fruit fly Drew, R.A.I., Hooper, G.H.S. and Bateman, M.A. (Diptera: Tephritidae) immature stages in (1978) Economic Fruit Flies of the Pacific Region. carambola germplasm. Florida Entomologist 78, Brisbane, Australia, 137 pp. 354–357. Fennah, R.G. (1963) Nutritional factors associated Hennessey, M.K., Knight, R.J. Jr and Schnell, R.J. with seasonal population increase of cacao (1996) Relative resistance of avocado germ- thrips, Selenothrips rubrocinctus (Giard) plasm to Caribbean fruit fly. In: McPheron, (Thysanoptera), on cashew, Anacardium B.A. and Steck, G.J. (eds) Fruit Fly Pests: occidentale. Bulletin of Entomological Research 53, a World Assessment of Their Biology and 681–713. Management. St Lucie Press, Delray Beach, Foote, R.H., Blanc, F.L. and Norrbom, A.L. (1993) Florida, pp. 339–342. Handbook of the Fruit Flies (Diptera: Tephritidae) Howard, F.W. (1986) Protection de goyaves contre la of America North of Mexico. Cornell University mouch Caraïbe des fruits au moyen de filets. Press, Ithaca, New York, 571 pp. Fruits 41, 621–624. Galinsky, B. (2000) India, Latin America compete Jalaluddin, S., Katarajan, K. and Sadakathula, S. for Europe’s tropical juice market. http:// (1998a) Enhancement of guava resistance to www.marketag.com/ma/news/archive/ fruit fly. Fifth International Symposium of Fruit v.35/juice.stm Flies of Economic Importance. Penang, Malaysia, Gallo, D., Nakano, O., Silveira Neto, S., Carvalho, p. 31. R.P.L., Batista, G.C., Berti Filho, E.B., Jalaluddin, S., Katarajan, K. and Sadakathula, S. Parra, J.R.P., Zucchi, R.A., Alves, S.B. and (1998b) Relative resistance of guava germ- Vendramim, J.D. (1988) Manual de Entomologia plasm to guava fruit fly Bactrocera correcta Agrícola. Ceres, Piracicaba, São Paulo, 649 pp. (Bezzi). Fifth International Symposium of Fruit González Gaona, E. (1999) Manejo de plagas en el Flies of Economic Importance. Penang, Malaysia, cultivo del guayabo en Calvillo, Agua- p. 32. scalientes. Memorias del XXXIV Congreso Kapoor, V.C. (1993) Indian Fruit Flies. International Nacional de Entomologia, p. 708. Science Publisher, New York, 228 pp.

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Kubo, R.K. and Batista Filho, A. (1992) Ocorrência Department of Agriculture (Animal Plant de Amorbia spp. (Lepidoptera: Tortricidae) em Health Inspection Service 81–52), Washington, frutos de goiabeira (Psidium guajava L.) na DC, 114 pp. região de Campinas. Anais da Sociedade Ochoa, R., Aguilar, H. and Vargas, C. (1994) Entomológica do Brasil 21, 257–260. Phitophagous mites in Central America: Kwee, L.T. and Chong, K.K. (1990) Guava in an illustrated guide. Serie Tecnica, CATIE, Malaysia: Production, Pests and Diseases. Turrialba, CR 6, 51–52. Tropical Press Sdn. Bhd., Kuala Lumpur, Palmer, J.M., Mound, L.A. and Heaume, G.J. (1989) Malaysia, 260 pp. Guides to insects of importance to man. Landolt, P.J., Gonzalez, M., Chambers, D.L. In: Betts, C.R. (ed.) Thysanoptera. CAB Inter- and Heath, R.R. (1991) Comparison of field national, Wallingford, and British Museum of observations and trapping of papaya fruit fly Natural History, London, 74 pp. in papaya plantings in Central America and Peña, J.E., Hennessey, M., Duncan, R. and Vasquez, Florida. Florida Entomologist 74, 408–414. T. (1999) Arthropod seasonality and control of Landolt, P.J., Reed, H.C. and Heath, R.R. fruit flies on guava in south Florida. Proceedings (1992) Attraction of female papaya fruit fly of the Florida State Horticultural Society 112, Toxotrypana curvicauda (Diptera: Tephritidae) 206–209. to male pheromone and host fruit. Environ- Qureshi, Z.A. and Hussain, T. (1993) Monitoring mental Entomology 21, 1154–1159. and control of fruit flies by pheromone traps Liquido, N.J. (1993) Reduction of oriental fruit fly in guava and mango orchards. In: Aluja, M. (Diptera: Tephritidae) populations in papaya and Liedo, P. (eds) Fruit Flies: Biology and orchards by field sanitation. Journal of Agri- Management. Springer Verlag, New York, cultural Entomology 10, 163–170. pp. 375–380. Malavasi, A. and Zucchi, R.A. (2000) Moscas- Robinson, A.S. and Hooper, G. (eds) (1989) Fruit das-frutas de Importância Econômica no Brasil – Flies, Their Biology, Natural Enemies and Control, Conheciomento Básico e Aplicado. Holos Editora, Vol. 3a. Elsevier, Amsterdam, 372 pp. Ribeirão Preto, pp. 277–283. Silva, A.G., Gonçalves, C.R., Galvão, D.M., McPhail, M. (1937) Relation of time of day, Gonçalves, A.J.L., Gomes, J., Silva, M.N. and temperature and evaporation to attractiveness Simoni, L. (1968) Quarto Catálogo dos Insetos que of fermenting sugar solution to Mexican fruit Vivem nas Plantas do Brasil, seus Parasitos e fly. Journal of Economic Entomology 30, 793–799. Predadores. Ministério da Agricultura, Rio de Medina, J.C. (1988) Cultura. In: Goiaba: Cultura, Janeiro. Tome 1, Part II, 662 pp. Matéria-prima, Processamento e Aspectos Souza Filho, M.F. (2000) Biodiversidade de Econômicos. Instituto de Tecnologia de moscas-das-frutas (Diptera: Tephritidae) e Alimentos, Campinas, pp. 1–121. seus parasitóides (Hymenoptera) em plantas Monteiro, R.C. (1994) Espécies de tripes (Thysanop- hospeeiras no Estado de São Paulo. MSc thesis. terea: Thripidae) associadas a algumas The University of São Paulo, Piracicaba, Brazil. culturas no Brasil. MSc thesis. The University Souza Filho, M.F., Raga, A. and Zucchi, R.A. (2000) of São Paulo, Piracicaba, Brazil. Moscas-das-frutas nos Estados Brasileiros. Morton, J.F. (1987) Fruits of Warm Climates. J.F. In: Malavasi, A. and Zucchi, R.A. (eds) Moscas- Morton, Miami, Florida, 505 pp. das-frutas de Importância Econômica no Brasil – Murray, M.J. and Campbell, C.A. (1989) Guava and Conheciomento Básico e Aplicado. Holos Editora, passionfruit as commercial crops in Florida. Ribeirão Preto, pp. 277–283. Proceedings of the Florida State Horticultural Steyskal, G.C. (1977) History and use of the McPhail Society 102, 212–213. trap. Florida Entomologist 60, 11–16. Nafus, D. and Schreiner, I. (1999) Insect pests Vazquez, L., Jiménez, R. and de la Iglesia, M. of Micronesia. http://www.nmcnet.edu/Lg/ (1996) Whiteflies (Homoptera: Aleyrodidae) aubweb/bugweb/bugroot.htm inhabiting the principal fruit trees grown in Nakasone, H.Y. and Paull, R.E. (1998) Tropical Fruits. Cuba. Tropical Fruits Newsletter 20, 3–4. CAB International, Wallingford, UK, 445 pp. White, I.M. and Elson-Harris, M.M. (1992) Fruit Norrbom, A.L. and Kim, K.C. (1988) A List of Flies of Economic Significance: Their Identification the Reported Host Plants of the Species and Bionomics. CAB International, Wallingford, Anastrepha (Diptera: Tephritidae). United States UK, 601 pp.

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10 Pests of Minor Tropical Fruits

Peter A.C. Ooi,1 Amporn Winotai2 and J.E. Peña3 1FAO Regional Office for Asia and the Pacific, 39 Phra Atit Road, Bangkok 10200, Thailand; 2Biological Control Group, Division of Entomology and Zoology, Department of Agriculture, Chatuchak, Bangkok 10900, Thailand; 3Tropical Research and Education Center, University of Florida, 18905 SW 280 Street, Homestead, FL 33031, USA

Among the tropical fruits, durian, Durio Durian (Durio zibethinus Murray) zibethinus Murray (Bombaceae), mangosteen Garcinia mangostana L. (Clusiaceae), rambutan, Durian, a common fruit in South-East Asia, Nephelium lappaceum L. (Sapindaceae), caram- originated in Borneo and Sumatra, and is bola Averrhoa carambola L. (Oxalidaceae) and held in high esteem from Sri Lanka and acerola Malpighia glabra L. (Malpighiaceae) are south India to New Guinea. The ripe fruits, or considered minor crops. Their distribution rather the arils which form the edible part, are and cultivation have been restricted to the generally eaten fresh. Its strong and unmis- areas where they originated, perhaps because takable smell is present in every market and some of these fruits have a unique eating street stall during the fruiting season. The quality and often require an acquired taste fruit can be also preserved, deep frozen or to appreciate them. That is particularly true consumed in ice creams, cakes and cookies. of durian, the ‘king of tropical fruits’, whose Thailand is the largest producer with strong and unmistakable smell makes it the 444,500 t in 1987, followed by Indonesia. most controversial (Chin and Yong, 1980) Large fruits of superior cultivars fetch about among this group (Lim, 1990). Currently, US$5–10 each in Thailand and Malaysia. there is much interest in expanding the range The export of fruit from Thailand in 1987 was where these fruits can be cultivated, par- worth US$9.5 million, with exports to Hong ticularly in those areas with similar climate. Kong, USA and France. Therefore, it would be worthwhile to recognize the pests recorded on these fruits in their native range so as to minimize their spread to new sites. Moreover, an understanding of Crop phenology the pests will give an idea of their damage potential for other parts of the world. This The fruit is a globose, ovoid or ellipsoid cap- chapter will attempt to review the literature sule, up to 25 cm long and 20 cm diameter, on pests of durian, mangosteen, rambutan, green to brownish, covered with numerous acerola and carambola in their centre of broadly pyramidal, sharp, up to 1 cm long origin and in some of their adopted growing spines; valves usually five, thick, fibrous. regions. Seeds are up to 4 cm long and completely

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covered by a white or yellowish, soft, very pupal stage lasts 10–15 days. Adults are sweet aril. about 15 mm in length. The durian phenology and harvest seasons differ in those countries where it CONTROL Little is known of the natural is grown. In Thailand, durian trees flower biological control of this weevil although over a period of 2–3 weeks in March and unidentified tachinid flies were observed to bear fruit once a year. Fruit development parasitize it (Choonhawong et al., 1982). When requires 95–105 days after pollination for it occurs in large numbers, spot spraying early cultivars and more than 130 days for with 0.1% methamidophos or 0.15% acephate late cultivars. In the wet lowland tropics in solution has been effective. Malaysia and Indonesia, durian may flower twice a year. In Peninsular Malaysia, the main Allocaridara malayensis (Crawford) durian season is between June and August. (Hemiptera: Psyllidae)

The durian psyllid is considered to be the most destructive insect pest of durian. Eggs Key pests are inserted into young leaves. A cluster of 8–14 eggs forms a yellow or brown circle on Yunus and Ho (1980) provided the most the leaf. Full grown nymphs measure about comprehensive record of pests of plants 8 mm long with white, cotton-like, feather in Peninsular Malaysia. These records were shaped particles along its body, especially in based on reports made to the Department of the caudal area. Adult longevity lasts about Agriculture since 1920, and 40 insect pests 6 months. Both nymphs and adults live were recorded from durian (Yunus and Ho, and feed on the underside of the leaf. Injured 1980). A survey by Waterhouse (1993) listed leaves show yellow spots, followed by leaf 20 major pests of durian in South-East Asia. curling and leaf fall. The nymphs excrete In Malaysia, Khoo et al. (1991) described ten copious amounts of white honeydew which insects attacking durian. In eastern Thailand, encourages the development of sooty mould. Sirisingh et al. (1994) considered only five or six species as serious pests of durian CONTROL The natural enemies, Menochilus that required bimonthly insecticide usage. sexmaculatus Fabricius, Micraspis discolor However, Yunus and Balasubramaniam (Fabricius), Coccinella transversalis (Fabricius), (1981) considered only Mudaria luteileprosa Chrysopa sp., spiders, and undetermined Holloway (= magniplaga) as the key pest of encyrtids are associated with durian psyllid durian in Malaysia. The more conspicuous (Disthaporn et al., 1996). insect pests are described in this chapter: Conogethes punctiferalis (Guenée) (Lepidoptera: Pyralidae) Hypomeces squamosus F. (Coleoptera: Curculionidae) The highly polyphagous durian fruit borer, previously known in older references as This is a polyphagous weevil in which the Dichocrocis punctiferalis (Guenée), damages adult stage feeds on leaves, causing extensive both young and mature fruits by boring defoliation of young plants (Plate 70). Eggs of through the pulp (Plate 71). Infested fruits the weevil are laid singly in the soil. A female can be distinguished by the presence of frass could lay 40–131 eggs (Choonhawong et al., covering the infested surface area. Adults 1982). The egg stage lasts about a week. can be found on undersides of leaves during Larvae, which are yellow with a brown the day. Wing width measures 2.0–2.3 cm; the head and black mandibles, feed on roots. The forewing is yellow with scattered black spots. larval stage requires 22–37 days. Full-grown Newly hatched larvae feed on the fruit sur- larvae measure 15–20 mm in length and face. Larvae are greenish brown with several pupation occurs in the same habitat. The spots. Full-grown larvae measure 1.5–1.8 cm

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in length with black spots scattered along the attack by the pest. Light trapping reduces the body. Pupation occurs in soil and sometimes moth population and thereby reduces fruit on fallen leaves. When reared on castor infestation. Ripe bananas mixed with some beans, the larval stage is 12–13 days, and the insecticides are used as bait. Although bag- pupal stage requires 7–9 days. Adult male ging young fruit provides physical protection longevity is 14 days, while female longevity against this borer, it is not generally utilized. is about 16 days. Highest insect densities occur between April and August in Malaysia Planococcus minor (Maskell), and between February and June in Thailand. Planococcus lilacinus (Cockerell) Conogethes punctiferalis uses longan, rambu- (Hemiptera: Pseudococcidae) tan and pomegranate as alternative hosts. Adults of Planococcus minor and P. lilacinus CONTROL Fallen fruits should be collec- are flat and oval, approximately 3 mm in ted and burnt or buried. Spraying with length, pale yellow and covered with wax. cyhalothrin-L plus a surfactant at 20-day One female can lay an average of 100–200 intervals has been recommended. Little is eggs per cluster. Capacity for egg laying known regarding biological control of this ranges from 600 to 800 eggs in a period of insect. 14 days, and eggs hatch within 6–10 days. Crawlers move around until they find Mudaria luteileprosa Holloway suitable feeding sites or until they complete (Lepidoptera: Noctuidae) their nymphal development. The female mealybugs have three nymphal stages. Regu- The durian seed borer has been misidentified larly, two or three generations are produced as Mudaria magniphaga (Walker) (Kuroko per year. Planococcus spp. feed on branches, and Lewvanich, 1993) (Plate 72). The females inflorescences and fruits. Infestations increase oviposit on the durian fruit spines. Newly though ant tending and damaged plants hatched larvae feed initially on the skin of the become stunted and covered with sooty fruit and later bore into the husk and then mould. Although mealybugs attack only into the seeds. The full-grown purple-red the fruit epidermis and their proboscis rarely, larvae are ca. 4 cm in length. The larvae if ever, penetrates the flesh, infested fruits emerge from the fruit to pupate in damp are considered to have low quality and soil. An exit hole measuring about 5–8 mm are non-marketable. Planococcus feeds on in diameter surrounded by white-orange roots of grasses when no suitable host plants excreta can be observed on the surface of the are available. In eastern Thailand, Planococcus fruit. All stages of durian fruit are susceptible can be found attacking durian after fruit to Mudaria attack. Sirisingh et al. (1994) con- set during the beginning of the hot and sidered that this insect is the most important dry season starting in March. This infestation postharvest pest in Thailand. Losses vary continues until the fruits mature in mid July. according to locality but generally 50% of the fruits are unmarketable if it is not controlled. CONTROL Water or oil sprays are con- Usually only one larva can be found per fruit. sidered effective control methods. Indirect control by banding the trunk or branches with CONTROL Chemical treatment, light traps pesticides or petroleum oil to keep out ants and baits have been recommended. Spraying is also reported to be effective. Cryptolaemus should be stopped 2 weeks before harvesting. montrouzieri Mulsant, Scymnus sp. and Nephus Fenthion, dimethoate, deltamethrin, metha- sp. (Coleoptera: Coccinellidae), Ankylopteryx midophos, and methidathion have been octopunctata (Fabricius) (Neuroptera: Chry- recommended in Malaysia, while carbaryl, sopidae), and Sphenolepis sp. (Hymenoptera: methamidophos, endosulphan, and phosa- Eulophidae) have been reported to be natural lone are recommended in Thailand. Fruit enemies of Pseudococcus sp. (Disthaporn et al., thinning at an early stage can also reduce 1996).

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Eutetranychus africanus (Tucker) CONTROL Charanasri and Kongchuensin (Acarina: Tetranychidae) (1991) report the phytoseiids Amblyseius syzygii Gupta, Amblyseius cinctus Corpuz Charanasri and Kongchuensin (1991) and et Rimando, Amblyseius deleoni Muma et Anonymous (2000) reported the African red Denmark, and Amblyseius largoensis (Muma) mite Eutetranychus africanus (Tucker) as one as predators of African red mites, while of the most important mite pests of durian. Anonymous (2000) suggests that the domi- Severe infestation often causes yield reduc- nant predatory species of the African red tion and increases the amount of pesticides mite in Thailand is Amblyseius largoensis used, with resulting market problems. Afri- (Muma). Other unidentified species of can red mites feed on the upper side of the Stigmaeidae, Canaxidae and Bdellidae have leaf especially along the mid-vein, causing also been reported. A. largoensis develops and withering spots that later spread over the multiplies quickly, and the female lays 2–3 whole leaf. In the eastern part of Thailand eggs day−1. The life cycle from egg stage where severe damage has been reported, to adult is 4 days. During its life span, a single growers sprayed large amounts of acaricides, A. largoensis feeds on 27 African red mite eggs. causing the development of acaricide-resistant mite strains. Lawana conspersa (Walker) (Hemiptera: Flatidae) BIOLOGY Female African red mite is flat and oval, about 0.42 mm in length and The white moth cicada has been reported on 0.35 mm wide. It is dark brown in colour cocoa and Bauhinia spp. Damage is caused without an empodium at the end of the legs. A by oviposition in the leaf and fruit stalks pair of red dots is located at the anterior end. (Ibrahim and Ibrahim, 1989). Both the adult The short setae on the dorsal part of the body and nymphs feed on plant sap, causing are spatulate, whereas the ventral setae are dehydration of plant parts, and loss in photo- slender. The male African red mite reportedly synthesis due to the presence of sooty moulds completes its life cycle within 9.2 days. caused by excretions of the insect. Generally, the egg stage has been observed to Eggs are laid into young twigs or into last 4.8 days, but eggs of female mites were midribs of leaves. Nymphs feed on young reported to eclose within 4.5 days. The mites shoot tips, young leaves and flowers. The pass through three nymphal stages of 1.6, 1.3 nymphs are usually covered with white, and 1.6 days, respectively. The unmated male waxy material. Adults are 2 cm long with adult has a longevity of 4.7 days. The male is two orange stripes on the basal portion of slightly smaller and more elongated than the the forewings (Dammerman, 1929). female. Female longevity lasts 9.3 days. The pre-oviposition period has been 4.8 days. The CONTROL No chemical control of L. average number of eggs laid per female is 14. conspersa is recommended. Natural biological Longevity for unmated females is 8 days while control by the entomogenous fungus, Metarr- for mated females it is 6.5 days. In Thailand, hizium anisopliae (Metschnickoff) Sorokin var. populations of red mites have been reported anisopliae Tulloch, has been reported as to be high from September until October, effective. depending on rainfall and relative humidity. Population peaks in December and January, Cataenococcus hispidus (Morrison) then declines, increasing again in March and (Hemiptera: Pseudococcidae) April. In general, the population is usually high during long dry periods. Several species This mealybug can be found in large numbers of host plants are damaged by this mite. They on durian fruits and peduncles, reducing the include fruit trees, vegetables, legumes and cosmetic value of the fruits. Its host plants ornamental plants. include durian, rambutan, guava and cocoa

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(Plate 73). The insect has both sexual and Daphnusa ocellaris Walker parthenogenetic reproduction. Females are (Lepidoptera: Sphingidae) ovoviviparous. Females pass through three nymphal instars which last 8, 6 and 7 days Daphnusa ocellaris is considered to be an before becoming adults. The males undergo endemic pest, with low importance. For two nymphal stages, one prepupal and example, this sphingid is not recorded as a one pupal stage, lasting 7, 8, 2 and 4 days, serious pest of durian (Yunus and Ho, 1980; respectively. Adult longevity is 23 days Waterhouse, 1993). However, Ramasamy under laboratory conditions. (1980) reported a large outbreak of D. ocellaris in the Malaysian state of Perak. These oppo- site reports suggest that not much is known CONTROL No chemical control is necessary against this insect. Ho and Khoo (1997) and of the potential of this endemic pest, and Na (1988) provide an extensive study on the much less about its natural enemies. close mutualistic relationship between the ant The life cycle of D. ocellaris is completed Dolichoderus thoracicus (Smith) (Hymenoptera: in 32–44 days (Ramasamy, 1980). The cream Formicidae) and C. hispidus and reiterate the and pink eggs are laid in groups of 6–20, each necessity to manipulate both organisms for measuring 1.5–2 mm and hatch in 4–6 days. control of the mealybug. Control of the The larval stages are completed in 17–21 days. ants associated with the mealybugs may be Larvae are voracious defoliators. They are recommended if any intervention is required. usually green with a distinct dorsal red stripe. Spraying the basal part of tree trunk with Full-grown larvae measure 6–6.5 cm in length gamma-HCH (0.1% a.i.) or chlorpyrifos (0.1% (male caterpillars) while female larvae mea- a.i.) will reduce the ant populations. sure 7.5–8 cm long. Pupation occurs in the soil and pupae of male moths are smaller (3.5 cm long) than pupae of female moths Chalcocelis albiguttatus (Snellen) (4 cm long). Pupation period varies between (Lepidoptera: Limacodidae) 12 and 17 days. Chalcocelis albiguttatus or gelatine grub is a polyphagous insect recorded on tea, oil palm, CONTROL Ramasamy (1980) recorded two durian, rambutan, Malay apple (Eugenia tachinids from pupae of D. ocellaris, namely malaccensis L.) and candle nut (Aleurites triloba Blepharipa sugens (Wiedmann) and Exorista Forst.); it is collected regularly in forests sp. (Diptera: Tachinidae). Ramasamy (1980) in Sabah, Malaysia (Chey et al., 1997). This determined that light trapping could reduce gelatine grub is recorded as an important moth density. pest of coconut in Malaysia and Indonesia. Damage caused by larvae scraping off the leaf tissue serves as a portal of entry for plant Mangosteen (Garcinia mangostana L.) pathogens. Eggs are generally flat, scale-like, and laid Mangosteen is known only as a cultivated on the leaf underside. Egg stage is 2–3 days. species, although there have been occasional Total larval stages range from 59 to 70 days. wild specimens in Malaysia. The mangosteen The larva is about 17 mm long; it is characteris probably the most highly praised tropical ized by its spines and appears to be enclosed fruit (Verheij, 1992). The scarcity of mango- in a gelatinous cover. Full-grown larvae form steen orchards, limited fruit supply and the cocoons attached to leaves or stems. The pupal fruit’s short shelf life are major marketing stage lasts 21–31 days. problems. Much of the limited fruit supply is due to the long juvenile period of 10–15 CONTROL This insect is usually kept under years that discourages commercial produc- control by natural biological agents including tion. Thailand is the largest producer of man- microbial diseases. However, if chemical con- gosteen in South-East Asia. The mangosteen trol is needed, 0.01% cypermethrin solution fruit is a globose and smooth berry, turning can be used for spot spraying. dark purple at ripening. It is a crop of the

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humid tropics, often found in association Phyllocnistis citrella Stainton (Lepidoptera: with durian. The fruit has a diameter of Phyllocnistidae) 4–7 cm. The edible part is the sweet white aril that envelops the seeds within the pericarp This insect is better known as a citrus (Verheij, 1992). leafminer. Mining of young leaves cause Generally, the mangosteen season coin- deformation and often leads to early leaf fall cides with that of the durian. Floral initiation (Plate 74). Its damage is serious on young to anthesis takes about 25 days and the fruit plants. ripens 100–120 days later. The main harvest Studies of this moth, particularly those on season in Thailand is May/June and July. citrus, showed that eggs are laid singly on In Peninsular Malaysia, fruits are available young leaves. Larvae mined the leaf epider- from June to August, while in Sarawak, mis, resulting in characteristic serpentine fruits are available from November through mines lined with excrement. Full-grown January. larvae would grow up to 3 mm in length. Pupation takes place on the leaf. The complete life cycle in Indonesia was found to be 16 days (Kalshoven, 1981). (For more information, see Key pests Chapter 3.)

A total of 25 insects were recorded from CONTROL Many natural enemies keep mangosteen over a period of c. 60 years this insect in check in Indonesia. The most (Yunus and Ho, 1980). A survey by Water- important parasitoid is Ageniaspis sp. house (1993) listed only three major pests of (Hymenoptera: Encyrtidae) (see Chapter 3). mangosteen in South-East Asia. Khoo et al. (1991) described two insects that attack Stictoptera cucullioides Guenée mangosteen. (Lepidoptera: Noctuidae)

Hyposidra talaca (Walker) Stictoptera cucullioides is reported to feed (Lepidoptera: Geometridae) voraciously on young flushes of mangosteen. Two other species have also been recorded, Little is known of the biology of this highly namely, S. columba (Walker) and S. signifera polyphagous insect. Hyposidra talaca is found (Walker). As with many insects that have in tropical lowlands and highlands. Besides occasional outbreaks, little is known of the mangosteen, H. talaca has been recorded on egg and early larval stages. The full-grown, cacao, cinchona, coffee, tea and other fruit 30 mm long larvae have a distinct orange trees (Entwistle, 1972). The larvae are typical coloured head capsule. Pupation takes place loopers, brown with dorsal transverse rows in the soil. As the insect occurs infrequently, of white spots. Full-grown larvae drop to no prophylactic control measures are neces- the ground by silken threads and pupate sary. Further ecological studies will probably about 2–4 cm deep in the soil. Eggs of H. explain the role of biological control in keep- talaca are iridescent and laid in clusters. ing the insect in check. In cases of occasional H. talaca develops within 2.5–3.5 months in outbreaks, carbaryl was found to be effective. the highlands of Indonesia when recorded on cinchona (Kalshoven, 1981).

CONTROL To our knowledge there is no Rambutan (Nephelium lappaceum Blume) information on chemical control for this insect. Entwistle (1972) reports that in cocoa Rambutan is a tropical relative of litchi, with undetermined parasitoids reduce H. talaca a distribution that ranges from southern densities. China through the Indo-Chinese region,

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Malaysia, Indonesia to the Philippines (Stone, management and biological control of this 1992). As the name suggests (the Malay word pest. Lim et al. (1987) provide an extensive ‘rambut’ meaning hair) the fruit is glabrose, literature review of this insect. resembling a ‘burr’ (Chin and Yong, 1980). Much of the information on the biology of Rambutan, while highly prized in its region this insect is from studies made with cocoa. of origin, remains a minor fruit inter- Eggs of C. cramerella are laid singly on the nationally. The fruits are consumed fresh, surface of the fruit. Each egg is less than or canned. The canning industry has boosted 0.5 mm, flat and rather oval in shape; they the cultivation of rambutan in its native range hatch within a week. The newly hatched with Thailand as the largest producer. The larvae bore straight through the base of the rambutan fruit is an ellipsoid to subglobular egg into the fruit. The larvae tunnel in the fruit schizocarp, up to 7 cm × 5 cm, usually con- until they reach the fruit stalk. In the case sisting of one nutlet. The skin colour varies of cocoa fruits, the larvae tunnel between from yellow to purplish red and is usually the beans causing them to stick together, glabrous. The seed is usually covered by a undersized and poor in quality. In the case thick, sweet, juicy, white to yellow, translu- of rambutan fruits, the damage is often less cent sarcotesta which is the edible part (Stone, obvious and would not usually damage the 1992). The main flowering period occurs sarcotesta. In cocoa, the larval stage is com- during the dry season. Fruits ripen about 110 pleted in 14–18 days. Four to six larval instars days after bloom. In Thailand, insect pests of have been recorded and a full-grown larva rambutan are not serious and not much is measures 12 mm long; the larva leaves the known of their ecology. The situation may fruit and pupates on the leaf surface or among change if some of these pests are transported leaf debris on the ground. Pupation occurs to other tropical countries where these fruits inside an oval-shaped cocoon. The pupal are being planted (e.g. Costa Rica). stage lasts between 6 and 8 days. As noted above, this insect would tend to damage only the part of the fruit next to Key pests the fruit stalk (Plate 76). Hence, its damage to rambutan is often ignored. The current low A total of 127 insects were recorded from population densities may suggest that some rambutan over a period of c. 60 years (Yunus mortality factors and an early fruiting season and Ho, 1980). A survey by Waterhouse may keep C. cramerella from reaching higher (1993) listed 28 major pests of rambutan in density peaks. South-East Asia. Khoo et al. (1991) described 15 insects that attack rambutan. Some of the CONTROL Walker and Huddleston (1987) key pests are described in detail below. reported Chelonus chailini Walker and Huddleston (Hymenoptera: Braconidae) as Conopomorpha (= Acrocercops) cramerella an egg–larval parasitoid of C. cramerella. (Snellen) (Lepidoptera: Gracillariidae) Goryphus sp. (Hymenoptera: Ichneumonidae), Ceraphron aguinaldoi Dessart (Hymenoptera: Conopomorpha (= Acrocercops) cramerella Ceraphronidae), Xanthopimpla sp. (Hymen- (Snellen) attained notoriety as the most optera: Ichneumonidae), Brachymeria sp. serious pest of cocoa beans in South-East (Hymenoptera: Chalcididae), Ooencyrtus ooii Asia in the last two decades. The insect is Noyes (Hymenoptera: Encyrtidae), Tricho- native to the region, as is rambutan (Plate 75). spilus pupivorous Ferriere (Hymenoptera: However, for it to switch to a fruit from the Eulophidae) and Paraphylax sp. (Hymeno- New World some 200 years ago (Ooi et al., ptera: Ichneumonidae) have been reported 1990) is unique. Because of its new found from C. cramarella attacking rambutan status, much is known of its biology in Peninsular Malaysia (Ooi, 1987; Noyes, and advances have been made in the 1991).

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Adoretus (= Lepadoretus) compressus leaf damage is observed, spraying with (Weber) (Coleoptera: Scarabaeidae) synthetic pyrethroids such as cypermethrin (0.01% a.i.) has been recommended. Adoretus (= Lepadoretus) compressus is a highly polyphagous cockchafer beetle that is active at night. This species is the most common of Chalcocelis albiguttatus (Snellen) about seven species within the genus. While (Lepidoptera: Limacodidae) damage to older rambutan plants may be See pests of durian. tolerated, damage to developing seedlings may lead to a significant setback in growth. Characteristically, adults feed on the Parasa lepida (Cramer) interveinal areas close to the centre of the leaf. (Lepidoptera: Limacodidae) Eggs of this scarabaeid beetle are laid in the soil usually under grasses or weeds. Grubs This blue-striped nettle caterpillar is poly- feed on decaying plant materials and roots. phagous and causes severe defoliation of Five larval instars have been recorded and rambutan trees. It is known throughout the full-grown larva would grow to 14 mm in South and South-East Asia. Desmier de length. Pupation takes place in the soil. When Chenon (1982) provided an extensive study large numbers of chafer beetles are observed of the insect as a pest of coconut. The egg feeding on rambutan plants, especially stage of P. lepida lasts 5–7 days. Eggs are laid young ones, the use of stomach poisons in groups of 15–40. Upon hatching, cater- such as trichlorfon at 0.1% a.i. is advised pillars are gregarious until fully grown. The (Rao and Suppiah, 1971). Little is known of male larva has seven instars and often eight the biological control of this insect. are recorded for females. The larva has many protuberances on the body. Young larvae Apogonia cribricollis Burmeister are yellow and in the third instar a blue (Coleoptera: Scarabaeidae) band is observed on the dorsum. Larval development requires an average of 40 days Apogonia cribicollis feeds on more than 30 (32–46 days). Pupation is also gregarious and plant species and is known from Singapore the pupal stage lasts about 22 days (21–24 and Malaysia. Its damage to young plants is days). more significant than to mature plants (Entwistle, 1972). Like other cockchafers, CONTROL Cock et al. (1987) provided a eggs of A. cribricollis are laid in the soil at comprehensive list of natural enemies of the base of plants. The elongated eggs are P. lepida. The study by Desmier de Chenon white in colour, measuring 1.0 × 1.3 mm. (1982) listed Apanteles parasae Rohwer These are laid some 2.5–5 cm deep in the soil (Hymenoptera: Braconidae), Chaetexorista in groups of 5–35 eggs. The mean incubation javana Brauer and Bergenstamm (Diptera: period has been recorded to be around 9 days Tachinidae), Sarcorohdendorfia (Sarcophaga) (Lever, 1953). Larvae grew from 3 to 15 mm antilope (Bottcher) (Diptera: Calliphoridae), in 10 to 11 weeks, feeding on the roots of and Buysmania oxymora (Tosquinet) (Hymeno- plants. A pupal period of 7–10 days is ptera: Ichneumonidae) as the most frequently preceded by a prepupal period of 2–3 days. recorded parasitoids. Beetles are chestnut brown in the first 2 Often populations of P. lepida are deci- weeks, turning black later. Adults are active mated during the rainy season which sets at night, feeding on foliage from the leaf off epizootics of a viral disease. In general, margin inwards, leaving an untidy look on this insect is kept in check by its numerous the leaves (Entwistle, 1972). natural enemies. However, in the rare event of outbreaks, spraying with synthetic pyre- − CONTROL Little is known of the biological throids or Bacillus thuringiensis at 1 kg ha 1 has control of this cockchafer. Often when severe been recommended.

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Hyperaeschrella insulicola (Kiriakoff) flushes of cocoa. Larvae are usually found (Lepidoptera: Notodontidae) feeding inside a flush of young leaves held together by the silk produced. Occasionally, outbreaks of green caterpillars Eggs of this insect are laid on the young have been reported from isolated rambutan leaves or shoots. Upon hatching, the cater- orchards (Ooi, 1978) (Plate 77). The large pillar feeds on the leaves and soon pulls numbers of caterpillars quickly defoliate leaves together with silk. The larval period whole trees leaving a ‘withering’ effect. As lasts about 6 days. Pupation occurs within the quickly as it developed, the outbreaks sub- folded leaves. side during the dry season. Little is known of Usually damage is not serious, although the biology and ecology of this insect. Egg the plant may look untidy. It is suspected and larval stages are found on the tree while that natural biological control often takes care pupation occurs among the leaf litter at the of the population. A chalcid, Brachymeria sp. base of the tree. Besides rambutan, the insect nr. apicicornis (Cameron), has been recorded is also reported to feed on cashew. (Khoo et al., 1991).

Conogetes punctiferalis (Guenée) (Lepidoptera: Pyralidae) Carambola (Averrhoa carambola L.) See pests of durian. Known as carambola, star apple, or five corner, this fruit tree is a 5–12 m high ever- Attacus atlas L. (Lepidoptera: Saturniidae) green tree native to southern Asia. Leaves Attacus atlas L. is one of the largest moths are imparipinnate, with flowers in axillary known. Larvae of this moth are polyphagous or cauliflorous panicles, pentamerous. The and it has 37 different host plants (Yunus and fruit is a large berry, ovoid to ellipsoid in Ho, 1980). A. atlas causes occasional to severe outline, with five pronounced ribs, stellate in defoliation on rambutan. cross-section (Samson, 1992). The tree grows One or several eggs are laid on the leaf well in tropical or subtropical lowland lower surface. The eggs develop better under conditions (Sedgley, 1984) and flowers high humidity conditions. The egg stage lasts abundantly. 10–13 days. Larvae are white with characteris- Flowers need to be pollinated. Carambola tic soft tubercles on the body. Fully grown has been introduced since the 19th century larvae measure about 150 mm. The larval into different areas in the western hemisphere stage lasts 28–38 days. Pupation occurs within and is now one of the most popular crops a cocoon constructed from leaves. The pupal in Guyana, and Surinam (Ramsammy, 1989). stage lasts from 23 to 28 days. In Malaysia carambola is produced in mixed The rather rare outbreaks suggest that family holdings with an average size of less the insect is often under natural biological than 2 ha. Estimated production in Malaysia control. It has been reported that insectivo- fluctuates around 24,000 t and in the Philip- rous birds use the caterpillars as prey. Besides pines trees yield approximately 2150 t (Abdul predators, seven species of parasitoids have et al., 1989; Samson, 1992). Florida is the only been recorded (Yunus and Ho, 1980). place in continental USA where carambola is grown commercially, with 179 ha of com- Adoxophyes privatana Walker mercial orchards, 89% of which are 4 years (Lepidoptera: Tortricidae) old or younger (Campbell, 1989). Most of the information on pests of carambola comes from Like many insects feeding on rambutan, South-East Asia and Australia. In Florida, this webworm is a polyphagous herbivore the insects that have been recorded from recorded on 13 species of agricultural and carambola include: Morganella longispina ornamental plants (Yunus and Ho, 1980). It (Morgan) (Homoptera: Diaspididae), Dia- is recorded as an important pest of young prepes abbreviatus L., Nezara viridula (L.),

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Ecpantheria scribonia (Stoll) (Lepidoptera: and females are strong fliers and will fly long Arctiidae) feeding on leaves and Platynota distances if they cannot find a good source of rostrana (Walker) feeding on fruit (Peña and food or a site to lay eggs. Data from B. dorsalis Duncan, 1999). have shown that the adults can fly over 50 km from the emergence site (Midgarden and Fleurkens, 1998). Adults may live 30–60 Key pests days in nature. Females can lay more than 1000 eggs over their lifetime. Eggs are white, Bactrocera carambolae (Diptera: Tephritidae) banana-shaped and 1 mm long, shining white to milky when ready to hatch. Larvae have The carambola fruit fly, Bactrocera carambolae three instars inside the fruit where they feed (Drew and Hancock) was reported for the on the pulp and make tunnels in the fruit. first time in the western hemisphere in Larvae are elongate and pointed at the head. Surinam in 1975, although it was properly Length of larvae is 1 mm just after hatching to identified in 1986 (Plate 78). This species is 7–8 mm just before pupation. The colour is endemic to Indonesia, Malaysia and southern white or the same colour as the fruit pulp Thailand (Van Sauers-Mueller, 1991). In Suri- (Midgarden and Fleurkens, 1998). At the end nam, the major hosts are carambola and the of the third instar, the larvae leave the fruit Curaçao apple, Syzygium samarangese. Minor and burrow 2–7 cm into the soil to pupate. hosts include: West Indian cherry, Malpighia Pupae are dark reddish brown, barrel-shaped punificolia, mango Mangifera indica, sapodilla, and about 4–5 mm long. Since its detection, Manilkara achras, guava Psidium guajava, the fruit fly has spread throughout the coastal Indian jujube Ziziphus jujuba, Citrus spp. areas of Surinam and French Guiana (Van and cashew Anacardium occidentale L., as Sauers-Mueller and Vokaty, 1996). occasional hosts. Export losses of infested countries are estimated to be US$25.3 million CONTROL An effective control method (Midgarden and Fleurkens, 1998). called the male annihilation technique has been developed for members of the Bactrocera BIOLOGY The life cycle of B. carambolae is dorsalis complex. Baits are impregnated with a typical of other fruit flies. From egg to mature combination of lure and insecticide. Methyl adult takes about 22 days under good condi- eugenol, a parapheromone lure, is also used tions (26°C and 70% RH) (Midgarden and to attract male fruit flies before they become Fleurkens, 1998). Eggs take 1–2 days to hatch. sexually mature. Surveillance methods are The larval stage lasts 6–9 days, and pupation accomplished using delta-shaped Jackson 8–9 days. Adults are 3.5–5 mm, yellowish traps impreganated with methyl eugenol and black with a brown tinge, especially on the an insecticide. Another surveillance method abdomen, head and legs, ovipositor of female performed in the infested areas consists of is knife-shaped (Midgarden and Fleurkens, collecting fruit and rearing the larvae in 1998). Adults become sexually mature 8–10 screened cages with sand or sawdust. days after emergence. The minimum period of time for one generation is approximately 30 Morganella longispina (Morgan) days (Midgarden and Fleurkens, 1998). Before (Homoptera: Diaspididae) laying eggs, the adult female fly feeds for a week on protein, e.g. on bacteria growing on Plumose scale, Morganella longispina, has been fruit and plant surfaces, on bird faeces and on found in Florida since 1980 (Hamon, 1981). sugars, e.g. honeydew and nectar, and spoiled The female armour of the scale is circular to fruit. Mature adults copulate after groups of oval (1–1.5 mm × 1.0 mm) convex, dull black, males gather and perform a courtship dance in with a thick and opaque texture. The male the early evening, just before sunset. Females armour is similar in colour, smaller, slightly puncture the skin of green or mature fruit convex and elongate. The scale is known and lay eggs in groups of 3–5 just under the from Algeria, South Africa, China, India, Sri skin (Midgarden and Fleurkens, 1998). Males Lanka, Sandwich Islands, Tahiti, Hawaiian

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Islands, Mauritius and most of the Caribbean cultivar with the highest number of punc- Islands, including Barbados, Dominican tures was ‘Pasi’, followed by ‘Sri kembagen’ Republic, Trinidad, Haiti, Jamaica, Puerto and ‘Cheng Chui’ (Peña and Duncan, 1999). Rico, and from Guyana and Brazil in South America (Hamon, 1981). Its polyphagous Toxoptera aurantii (Boyer de Fonscolombe) habits include the following host plants: (Homoptera: Aphidae) Citrus sp., Ligustrum sp., Nerium sp., Severinia sp., Averrhoa carambola, Eucalyptus, Carica In Florida, the black citrus aphid, Toxoptera papaya, Coffea sp., Ficus, Persea americana, aurantii (Boyer de Fonscolombe) is found in Mangifera indica, and macadamia among large colonies on flowering terminals feeding others (Hamon, 1981). on flower peduncles of carambola (Plate 79). In Florida, the number of M. longispina- The black citrus aphid is dark reddish to infested branches peaked during November brown. Wingless forms (apterous) are about 1997 and was reduced between the months 2 mm long and by production of honeydew, of June and July. The cultivar with highest sooty mould fungi develop around the plumose scale infestation was ‘B-10’, followed infested areas. Aphids are a problem in by ‘Kajang’, ‘Wai Wei’, ‘Cheng Chui’, ‘Meis’ carambola during the flowering season. The and ‘Kary’ (Peña and Duncan, 1999). major problem could be excessive flower drop, followed by sooty mould on leaves and CONTROL The products pymetrozine, pyri- fruits. Black citrus aphids were most common proxifen and imidacloprid were effective for during the month of November 1997 at the reducing plumose scale density compared to peak of carambola flowering. Other insects the control (Peña and Duncan, 1999). Zim- such as Planococcus citri (Risso) (Homoptera: merman (1948) reported Archenomus perkinsi Pseudococcidae) and Daghbertus spp. (Fullaway) and Prospatella koebelei Howard as (Hemiptera: Miridae) were observed on the parasitoids of M. longispina in Hawaii. inflorescences. In Florida, the highest aphid infestation peaks were observed on ‘B-10’, Nezara viridula (L.) (Homoptera: followed by ‘Pasi’, ‘Wai Wei’, ‘Cheng Chui’, Pentatomidae) and Leptoglossus spp. ‘Kary’ and ‘Erlin’ (Peña and Duncan, 1999). (Homoptera: Coreidae) Gonodonta spp. (Lepidoptera: Noctuidae) In Florida, the plant bugs, southern stink and Eudocima spp. bug Nezara viridula (L.) and the leaf-footed bug Leptoglossus spp., move from vegetables Fruit piercing moths, Gonodonta spp. planted during the autumm and winter to Eudocima spp. (Lepidoptera: Noctuidae), feed carambola orchards that have mature and at night by piercing the skin of the ripe or ripe fruit. Adults and nymphs insert their ripening fruit with their strong proboscis, the piercing–sucking mouthparts into the fruit, damage results in crop loss or unmarketable extracting fruit fluids leaving a small punc- fruit. The internal injury to the fruit resembles ture. With time, the area around this punc- a honeycomb. Secondary rots develop at the ture or scar becomes soft and shows decay. puncture site and the fermented fruits are Leptoglossus spp. were only observed in Feb- frequently visited by other insects, such as ruary and October 1998; however, the highest sap beetles (Nitidulidae). The fruit piercing number of punctures per fruit were detected moths are dark brown, with orange or dark between January and February. Lesions on yellow coloured hindwings. In Florida, the fruit were also observed during July, August larvae do not feed on carambola, but have and November (Peña and Duncan, 1999). In been collected from leaves of atemoya (Peña Florida, this plant bug is also considered a and Duncan, 1999). In Queensland, Australia, pest of citrus, where its feeding on ripening fruit piercing moth larvae feed on native fruit causes premature colour break and fruit vines isolated from the orchard environment drop (Mead, 1971). In Florida, the carambola (Fay, 2000).

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CONTROL Control for fruit piercing moths fruits mature in approximately 30 days (Stahl with insecticides is problematic, and alterna- et al., 1955; Ledin, 1958). tive methods have been sought in Australia to combat these pests. Netting trees and bagging fruits can be effective, but are not options Key pests for most crops unless other significant pests (e.g. birds, flying foxes) are also controlled. Trapping using black light traps can reduce Acerola weevil, Anthonomus macromalus damage by 60–70%, while a new baiting Gyllenhal (Coleoptera: Curculionidae) system has provided 75–85% security in citrus The most important insect pest of Barbados trials (Fay, 2000) For information on fruit cherry in Florida is the acerola weevil, Antho- piercing moths, see Chapter 11 on the litchi. nomus macromalus Gyllenhal (= A. flavus, = A. bidentatus,=A. malpighia) (Coleoptera: Brevipalpus phoenicis (Geijskes) Curculionidae). This weevil is small (Acarina: Tenuipalpidae) (2.1–3.4 mm long) and dark brown (Plate 80). There is a distinct chevron pattern of light Tenuipalpids, possibly Brevipalpus phoenicis and dark scales on the elytra (Clark and (Geijskes), is also an important pest of citrus, Burke, 1985). Members of this species are papaya, guava and more than 50 other plant oligophagous within the botanical family species (Jeppson et al., 1975). This mite Malpighiaceae. This weevil appears to be appears to be responsible for bronzing of native to the Neotropics, with reports from carambola fruit. It prefers crevices and fruit Florida (USA) and from many of the islands angles. In Florida, B. phoenicis peak densities of the Caribbean region (Clark and Burke, were observed between August and October 1985). The first report in Florida was in 1972 1998 (Peña and Duncan, 1999). (Stegmaier and Burke, 1974). Stegmaier and Burke (1974) and Balloff (1993) reviewed the biology of A. macromalus. Barbados cherry or acerola Adults deposit eggs on the anthers of flowers, (Malpighia glabra L.) stem terminals and in immature fruits. The larvae develop in the flowers and fruit, Barbados cherry or acerola, Malpighia glabra causing extensive damage to floral reproduc- (L.) (= punicifolia L.), is a tropical fruit native tive structures and to the flesh of the fruit, to the West Indies, Central America and which reduces yield. Adult weevils feed on South America (Stahl et al., 1955; Phillips, immature, expanding leaves which causes a 1991). The genus Malpighia is present from ‘shot-gun hole’ appearance to the leaves as south Texas to Peru (Asenjo, 1980). Recently, they expand (Hunsberger et al., 1998). the Barbados cherry has received attention because its fruits are an exceptionally high SEASONALITY In Florida, the adult popula- natural source of ascorbic acid (vitamin C). Its tion peaks in late June through July. Infested cultivation has extended throughout the sub- trees typically showed leaf damage. Adult tropics and tropics (Ledin, 1958) and some weevil densities sampled from the upper and of the largest plantings are in Brazil (Anony- middle strata of branches and lower branches mous, 1996). Estimated commercial hectarage were statistically equal. in the Caribbean region is > 160 ha with a The peak months for adult emergence potential crop value of several million US from fruit were from late June through dollars (Gonzalez-Ibañez, 1983). In Florida, September. In June, the percentage fruit infes- Barbados cherry is grown in the southern tation was estimated at 45–75%. By August, part of the state in homeowners’ yards and the respective estimates were 65–75%. A as a small commercial crop. Flowering and 1-month delay in peak adult emergence from fruit set occur almost continuously from fruit followed the peak number of adults in the April through November in Florida, and field (Hunsberger et al., 1998).

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Both eggs and larvae were found in flow- Aphis tavaresi argentiniensis Blanchard, Toxo- ers. Eggs were laid before flower opening. The ptera aurantii, Aphis spiraecola) are mentioned female eats a hole into the flower bud and as pests of acerola (Couceiro, 1985; Araujo deposits the eggs on to the anthers. Larvae and Minami, 1994), of which the most were observed eating the floral ovary when important is considered to be T. citricidus, the flower was fully open. Larvae were found appearing often in very large numbers on the tunnelling inside the new growth of branches apical buds and fruit peduncles. Batista et al. (Plate 81). External evidence of larval feeding (1994) reported that T. citricidus can produce was sudden wilt and premature death of an average of 49.7 nymphs when the female infested shoots (Hunsberger et al., 1998). is feeding in acerola. During dry weather infested plants show leaf curling, stunting, BIOLOGICAL CONTROL Surveys for parasit- and damage to trees and fruit by the dis- oids of A. macromalus have yielded a single charge of honeydew. In Brazil, Braga et al. parasitoid, Catolaccus hunteri Crawford (Hym- (1998) recommend careful applications of enoptera: Pteromalidae) (Hunsberger and organophosphates. Peña, 1997). No other parasitoids were found Other common pests of acerola in Brazil in Florida. are: Orthezia praelonga Douglas, Coccus viridis and C. hesperidium L. The recommended PHEROMONES There is some evidence that control is the use of emulsifiable oils. A. macromalus can produce aggregation pheromones. Adult weevils have been found Fruit flies (Diptera: Tephritidae) in aggregations in orchards (A.G.B. Hunsber- ger and J.E.Peña, personal observations) In Brazil, fruit flies of the genus Anastrepha and individuals were attracted to crushed A. and the Mediterranean fruit fly, Ceratitis macromalus in Petri dish arenas (Hunsberger capitata Wiedemann, are pests of acerola et al., 1998). Furthermore, aggregation phero- (Malavasi et al., 1980). These flies cause mones have been identified from two Antho- premature fruit maturity, and reduce fruit nomus spp. Tumlinson et al. (1968) identified quality. the aggregation pheromone (grandisol) from the cotton boll weevil (Anthonomus grandis Leptoglossus spp. (Homoptera: Coreidae); grandis Boh.) and Eller et al. (1994) identified Crinocerus spp. (Homoptera: Coreidae); the aggregation pheromone from the pepper and Nezara viridula L. weevil, A. eugenii Cano. (Homoptera: Pentatomidae) The coreid Leptoglossus phyllopus Herbst and CHEMICAL CONTROL The appropriate time to apply adulticides appears to be in the spring, the pentatomid Nezara viridula L have been before weevil densities start to increase. Also, observed attacking acerola fruits in Florida, because of the uneven and overlapping fruit- USA (Ledin, 1958). In Brazil, the coreids ing phenology, fruits bear different weevil Crinocerus sanctus Fabr. and Leptoglossus generations, allowing a rapid reinfestation of stigma Herbst. cause fruit deformation by the orchard. inserting their proboscis into the fruit, and are probably responsible for early fruit rotting (Braga et al., 1998).

Other pests Minor pests In Brazil, losses caused by pests are not quantified, and the information on pest In Brazil, Trigona spinips Fabr. (Hymenoptera: biology and integrated pest management is Apidae), a pest of citrus and banana, opens very limited (Boaretto and Brandao 1995). In galleries on acerola fruits, reducing fruit Brazil, several species of aphids (Toxoptera quality (Braga et al., 1998). (See pests of citricidus Kirkaldy, Aphis tavaresi DelGuercio; banana, in Chapter 2.)

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Conclusions Agropecuaria, Servicio de Producao de Informacao, Brasilia, pp. 33–40. We selected these fruit species as examples of Campbell, C.W. (1989) Carambola production in the United States. Proceedings of the Inter-American minor fruits grown in the world. Very little Society of Tropical Horticulture 33, 47–54. information can be acquired for management Charanasri, V. and Kongchuensin, M. (1991) African of their pests. Moreover, production of other red mite, Eutetranychus africanus (Tucker), an tropical fruit is becoming more extensive and important pest of durian in Thailand. Entomol- propagation of several of them, e.g. borojo, ogy and Zoology Bulletin 13, 62–68 (in Thai). Borojoa patinoi, bread fruit Artocarpus spp., Chey, V.K., Holloway, J.D. and Speight, M.R. (1997) sapodilla, Manilkara sapota L., cirvela, Spon- Diversity of moths in forest plantations and dias cytherea Sonnerat, is becoming more natural forests in Sabah. Bulletin of Entomo- frequent in tropical areas. On the other logical Research 87, 371–385. hand, emigration of ethnic groups from Asia, Chin, H.F. and Yong, H.S. (1980) Malaysian Fruits in Colour. Tropical Press Sendirian Berhad, Kuala Africa and the Americas and their settlement Lumpur, 129 pp. in Europe, Australia, USA and Canada, has Choonhawong, W., Kongkanjana, A., Wongkobrat, produced a demand for fruits that have been A., Chawanapong, M., Jumroenma, K. and ignored in the major world markets. Thus, Meksongsee, B. (1982) Study on biology and if rules for sanitation and food security are host plants of leaf eating weevil (Hypomeces followed in the importing countries, there squamosus Fabricius). In: Annual Report 1982, will be a need to develop IPM programmes Corn and other Field Crops Entomology Research, for these fruit species. Entomology and Zoology Division, Department of Agriculture, Bangkok, pp. 34–38 (in Thai). Clark, W.E. and Burke, H.R. (1985). Revision of the venustus species group of the weevil genus References Anthonomus Germar (Coleoptera: Curculion- idae). Transactions of the American Entomological Abdul, W., Ahmad, I. and Hassan, A. (1989) Caram- Society 111, 103–170. bola production, processing and marketing Cock, M.J.W., Godfray, H.C.J. and Holloway, J.D. in Malaysia. Proceedings of the Inter-American (eds) (1987) Slug and nettle caterpillars. In: The Society of Tropical Horticulture 33, 30–43. Biology, Taxonomy and Control of the Limacodidae Anonymous (1996) Acerola. California Rare Fruit of Economic Importance on Palms in South-East Growers. www.crfg.org/pubs/ff/acerola.html Asia. CAB International, Wallingford, UK, Anonymous (2000) Durian pests. http://www.oae. 270 pp. gi.th./projects /durian/thai/news Couceiro, E.M. (1985) Curso de extensao sobre a Araujo, P. and Minami, K. (1994) Acerola. Campinas: cultura da acerola: UFRP, Recife, 45 pp. Fundacao Cargil, 81 pp. Dammerman, K.W. (1929) The Agricultural Zoology Asenjo, C.F. (1980) Acerola. In: Nagy, S. and of the Malay Archipielago. J.H. de Bussy, Shaw, P.E. (eds) Tropical and Subtropical Fruit: Amsterdam, 473 pp. Composition, Properties, and Uses. AVI Pub- Desmier de Chenon, R. (1982) Latoia (Parasa) lepida lishing Company, Connecticut, pp. 341–374. (Cramer) (Lepidoptera: Limacodidae), a coco- Balloff, S. (1993) Anthonomus malpighiae Clark and nut pest in Indonesia. Oleagineux 37, 177–183. Burke (Coleoptera: Curculionidae) a pest of the Disthaporn, S., Kraturuek, C. and Sutthiarrom, S. Barbados cherry in Guadeloupe. MSc thesis, (1996) Manual for Integrated Pest Management Ecole Nationale Superieure Agronomique de in Durian. Thai–German Project IPM in Montpellier, Guadeloupe, 37 pp. selected fruit crops, Department of Agri- Boaretto, M. and Brandao, A. (1995) Pragas da culture and Department of Agricultural cultura da acerola. In: Sao Jose, A. and Alves, Extension, Thailand, 97pp. R. (eds) Acerola do Brasil: Producao e Mercado. Eller, F.J., Bartelt, R.J., Shasha, B.S., Schuster, D.J., Vittoria da Conquista: Universidad de Estad- Riley, D.G., Stansly, P.A., Mueller, T.F., Shuler, ual do Sudoeste da Bahia, Brazil, pp. 58–61. K.D., Johnson, B., Davis, J.H. and Sutherland, Braga, R., Luna-Batista, J., Campos, L. and C.A. (1994) Aggregation pheromone for the Warumby, J. (1998) Pragas da aceroleira. In: pepper weevil, Anthonomus eugenii Cano Braga, R., Cardoso, J. and das Chagas (eds) (Coleoptera: Curculionidae): identification Pragas de Fruteriras Tropicais de Importancia and field activity. Journal of Chemical Ecology 20, Agroindustrial. Empresa Brasileira de Pesquisa 1537–1555.

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Entwistle, P.F. (1972) Pests of Cocoa. Longmans, Lever, R.J.A.W. (1953) Cockchafer pests of cocoa and London, 779 pp. other crops. Malaysian Agricultural Journal 36, Fay, H.A. (2000) Fruitpiercing moths and fruit- 89–113. spotting bugs: intractable pests of tree Lim, G.S., Ho, C.T., Md. Jusoh Mamat, Teoh, C.H., fruits in an insecticide-reduction environment. Khoo, K.C., Chan, L.G. and Ooi, P.A.C. (1987) International Symposium on Tropical and Subtrop- The Cocoa Pod Borer (an introduction and ical Fruits. Cairns Australia, 26 November–1 abstracts). Malaysian Plant Protection Society, December 2000, Symposium Booklet, p. 27. Kuala Lumpur, Malaysia, 103 pp. Gonzalez-Ibañez, J. (1983) Evaluation of herbicides Lim, T.K. (1990) Durian Diseases and Disorders. for container-grown acerola (Malpighia punici- Tropical Press Sendirian Berhad, Kuala folia L.) under greenhouse conditions. Puerto Lumpur, 95 pp. Rico University Journal of Agriculture 67, Malavasi, A., Morgante, J.S. and Zucchi, R.A. (1980) 112–116. Biologia das moscas das frutas (Diptera: Tep- Hamon, A.B. (1981) Plumose scale, Morganella hritidae) I. Lista de hospedeiros e-ocorrencia. longispina (Morgan). Florida Department of Revista Brazileira de Biologia 40, 9–16. Agriculture and Consumer Services. Division Mead, F. (1971) Leaffooted bug, Leptoglossus of Plant Industry, Entomology Circular 226, phyllopus (Linnaeus) (Hemiptera: Coreidae). 2 pp. Florida Department of Agriculture, Entomology Ho, C.T. and Khoo, K.C. (1997) Partners in biological Circular 107, 2 pp. control of cocoa pests: mutualism between Midgarden, D. and M. Fleurkens. (1998) Dolichoderus thoracicus (Hymenoptera: Formi- Carambola Fruit Fly Programme. http://www. cidae) and Cataenococcus hispidus (Hemiptera: carambolafly.com/English/english.htm Pseudococcidae). Bulletin of Entomological Na, A.B. (1989) The cocoa black ant–mealybug Research 87, 461–470. relationship: artificial establishment of Hunsberger, A.G.B. and Peña, J.E. (1997) Catolaccus Cataenococcus hispidus (Homoptera: Pseudo- hunteri (Hymenoptera: Pteromalidae), a para- coccidae) on cocoa. PhD thesis, Universiti site of Anthonomus macromalus (Coleoptera: Putra Malaysia, Malaysia. Curculionidae) in south Florida. Florida Noyes, J.S. (1991) A new species of Ooencyrtus Entomologist 80, 301–304. (Hymenoptera: Encyrtidae) from Malaysia, a Hunsberger, A.G.B., Peña, J.E., Giblin-Davis, R., prepupal parasitoid of the cocoa pod borer, Gries, G. and Gries, R. (1998) Biodynamics Conopomorpha cramerella (Snellen) (Lepidop- of Anthonomus macromalus (Coleoptera: tera: Gracillariidae). Journal of Natural History Curculionidae) a weevil pest of Barbados 25, 1617–1622. cherry in Florida. Proceedings of the Florida Ooi, P.A.C. (1978) An important new pest of State Horticultural Society 111, 334–338. rambutan. MAPPS Newsletter 2, 5 Ibrahim, A.G. and Ibrahim, D.K. (1989) Biology Ooi, P.A.C. (1987) Advances in the biological control of Lawana conspersa Walker (Homoptera: of cocoa pod borer. In: Ooi, P.A.C. et al. (eds) Flatidae) a minor pest of cocoa in Malaysia. Management of the Cocoa Pod Borer. Malaysian Malaysian Applied Biology 18, 93–98. Plant Protection Society, Kuala Lumpur, Jeppson, L.R., Keifer, H. and Baker, E. (1975) pp. 103–117. Mites Injurious to Economic Plants. University Ooi, P.A.C., Day, R.K. and Mumford, J.D. (1990). of California Press, Berkeley, 614 pp. Evolution of the cocoa pod borer. MAPPS Kalshoven, L.G.E. (1981) Pests of Crops in Indonesia. Newsletter 14, 37–38. (Revised and translated by P.A. van der Laan Peña, J.E. and Duncan, R. (1999) Seasonality and and G.H.L. Rothschild.) P.T. Ichtiar Baru-Van control of arthropods on carambola cultivars Hoeve, Jakarta, 701 pp. in southern Florida. Proceedings of the Florida Khoo, K.C., Ooi, P.A.C. and Ho, C.T. (1991) Crop State Horticultural Society 112, 210–212. Pests and their Management in Malaysia. Tropical Phillips, R.L. (1991) Barbados cherry. University of Press Sendirian Berhad, Kuala Lumpur, Florida, Institute Food Agricultural Sciences, 242 pp. Fact Sheet FC-28, Gainesville, 2 pp. Kuroko, H. and Lewvanich, A. (1993) Lepidopterous Ramasamy, S. (1980) An outbreak and some aspects Pests of Tropical Fruit Trees in Thailand (in Thai). of the biology of the hawk moth, Daphnusa Japan International Cooperation Agency, ocellaris Walk. on durian in Perak. Malaysian Tokyo, Japan, 132 pp. Agricultural Journal 52, 213–218. Ledin, R.B. (1958) The Barbados or West Indian Ramsammy, P. (1989) The carambola in Guyana. cherry. Florida Agricultural Experiment Station, Proceedings of the Inter-Amercian Society of Bulletin 594, 15–17. Tropical Horticulture 33, 12–25.

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Rao, B.S. and Suppiah, K. (1971) Cockchafers as (1968) Boll weevil attractant: isolation studies. plantation pests in Malaysia and their control. Journal of Economic Entomology 61, 470–474. In: Wastie, R.L. and Wood, B.J. (eds) Crop Van Sauers-Mueller, A. (1991) An overview of Protection in Malaysia. Incorporated Society the carambola fruit fly Bactrocera species of Planters. Kuala Lumpur, pp. 173–186. (Diptera: Tephritidae), found recently in Samsom, J.A. (1992) Averrhoa L. In: Verheij, E.W.M. Surinam. Florida Entomologist 74, 432–440. and Coronel, R.E. (eds) Plant Resources of Van Sauers-Mueller, A. and Vokaty, S. (1996) South-East Asia No. 2 Edible Fruits and Nuts. Carambola fruit fly projects in Surinam and PROSEA, Bogor, Indonesia, 443 pp. Guyana. Tropical Fruits Newsletter 18, 6–8. Sedgley, M. (1984) Oxalidacea. In: Page, P.E. (ed.) Verheij, E.W.M. (1992) Garcinia mangostana L. In: Tropical Tree Fruits for Australia. Queensland Verheij, E.W.M. and Coronel, R.E. (eds) Plant Department of Primary Industries, Brisbane, Resources of South-East Asia: No. 2 Edible Fruits series QI83018, pp. 125–128. and Nuts. PROSEA, Bogor, Indonesia, 443 pp. Sirisingh, S., Ithnin, B. and Unahawutti, C. (1994) Walker, A.K. and Huddleston, T. (1987) Chelonus Entomology and pests. In: Nanthachai, S (ed.) chailini sp. n. (Hymenoptera: Braconidae) Durian: Fruit Development, Postharvest Physiol- from Malaysia, parasitizing gracillariid ogy, Handling and Marketing in ASEAN. ASEAN moths (Lepidoptera). Bulletin of Entomological Food Handling Bureau, Kuala Lumpur, Research 77, 437–440. Malaysia, 156 pp. Waterhouse, D.F. (1993) The Major Arthropod Stahl, A.L., Kaplow, M. and Nelson, R. (1955) The Pests and Weeds of Agriculture in Southeast present and future possibilities of Barbados Asia: Distribution, Importance and Origin. The cherry. Proceedings of the Florida State Horti- Australian Centre for International Agri- cultural Society 68, 138–143. cultural Research (ACIAR), Canberra, ACT. Stegmaier, C.E. Jr and Burke, H.R. (1974) Monograph 21, 141 pp. Anthonomus flavus (Coleoptera: Curculion- Yunus, A. and Balasubramaniam, A. (1981) Major idae) a fruit-infesting weevil of the Barbados Crop Pests in Peninsular Malaysia, 2nd edn. cherry, Malpighia glabra (Malpighiaceae), new Bulletin No. 138. Ministry of Agriculture, to North America. Florida Entomologist 57, Peninsular Malaysia. 81–90. Yunus, A. and Ho, T.H. (1980) List of Economic Stone, B.C. (1992) Nephelium lappaceum L. In: Verheij, Pests, Host Plants, Parasites and Predators in E.W.M. and Coronel, R.E. (eds) Plant Resources West Malaysia (1920–1978). Bulletin No. 153. of South-East Asia: No. 2 Edible Fruits and Nuts. Ministry of Agriculture, Malaysia, 538 pp. PROSEA, Bogor, Indonesia, 443 pp. Zimmerman, E. (1948) Insects of Hawaii, Vol. 5, Tumlinson, J.H., Hardee, D.D., Minyard, J.P., Homoptera: Sternorhyncha. University of Thompson, A.C., Gast, R.T. and Hedin, P.A. Hawaii Press, Honolulu, 464 pp.

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11 Pests of Litchi and Longan

G.K. Waite1 and J.S. Hwang2 1Queensland Horticulture Institute, Maroochy Research Station, PO Box 5083, SCMC, Nambour, Queensland 4560, Australia; 2Taiwan Agricultural Chemicals and Toxic Substances Research Institute, 189 Chung-Cheng Road, Wufeng, Taichung Hsien, Taiwan 413, Republic of China

The litchi (Litchi chinensis Sonn.) and longan panicles in order to maintain freshness, and (Dimocarpus longan Lour.) are closely related are sold in street markets or at roadside stalls species belonging to the family Sapindaceae. within a few days of harvest. Frequent sprin- Of South-East Asian origin, they thrive in klings with water help to maintain the colour subtropical areas with cool dry winters and of the skin and overall freshness. If allowed to warm wet summers (Menzel, 1983), but may dry out, the skin turns brown and becomes be grown in tropical areas at high elevation. brittle, lowering consumer appeal. Although Around the world, litchis have been success- South African and Israeli litchis sent to fully grown commercially in latitudes from European markets are treated with sulphur 15° to 35° (Menzel and Simpson, 1990). Some dioxide to retain attractive fruit colour, inter- cultivars are grown in warmer areas in Thai- nal quality is not preserved. This marketing land and Indonesia but the fruit is generally issue needs to be overcome before world trade of poor quality. Longans are often cultured in can expand. the same geographical areas as litchis but, except in China and Thailand, are usually less popular. Importance of the Crop The litchi is a traditional fruit in China, and it occupies a special place in Chinese Litchi culture. The first official record dates back to the 2nd century BC, while unofficial records World production of litchis is about 1 million date to 1766 BC. Indo-China is the centre of ori- t with the bulk of the crop grown in China gin for this species and many old specimen and India (Partridge, 1997). Though much of trees have been identified. Several trees in this production is consumed as fresh fruit, Guangdong and Hainan Island are believed to a large proportion is processed in the form be at least 2000 years old. Similarly, longan of canned fruit and juice. Over 700,000 t of occupies a special place in the culture of fresh litchis are estimated to be consumed in Thailand, but in contrast it is a relatively South-East Asia and India annually. Because recent arrival there. of the special significance of litchis to the Litchi and longan fruits are best when Chinese people, demand outstrips produc- eaten fresh, but they can also be processed tion, and fruit is imported from Vietnam by canning, juicing or drying to litchi nuts. and Thailand during the northern season. In Asia they are usually harvested as whole Countries such as South Africa, Mauritius,

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Madagascar, Réunion and Australia have winter. If conditions are cool during the early relatively low populations and must export part of the flush, development of the new part of their crop to maintain profitability. In growth will be floral. However, if warm addition, their crop matures when South-East weather is encountered, the new growth will Asian litchis are unavailable, especially produce leaves (Menzel and Simpson, 1995). around Chinese New Year. Exports to Litchi and longan are often cultivated in the Singapore, Hong Kong and mainland China same geographical areas and many pests are can be quite lucrative, especially for suppliers common to both crops. Tan et al. (1998) found of high quality fruit from Australia. Fruit that in Guanxi Province, China, more than from African countries, treated with sulphur, 90% of the insect species recorded for each is less popular. were common and suggested that this might Apart from China and India, large litchi be used to advantage in area-wide manage- industries have been developed in Taiwan, ment of pests. Thailand, Vietnam, Madagascar, South Africa and Réunion. Smaller but expanding industries exist in Australia, Bangladesh, Mauritius, Pests Mexico, the Seychelles, Spain and the USA (California, Florida and Hawaii). Fruit borers (Lepidoptera: Gracillariidae)

Conopomorpha sinensis Bradley Longan DISTRIBUTION AND BIOLOGY The major pest of lychees and longans in China, Taiwan and In general, longans can be successfully grown Thailand is Conopomorpha sinensis Bradley, wherever litchis are cultivated. Although known as the litchi stem-end borer in China both species flower at about the same time, and the litchi fruit borer in Thailand (Plate 82). longans take longer than litchis to mature. Bradley (1986) described three previously China (400,000 t), Thailand (150,000 t) and unrecognized species congeneric with the Vietnam (20,000 t) are the major world cocoa pod borer, Conopomorpha cramerella producers. Snellen, previously known as Acrocercops cramerella, which was thought to be the damaging species. Two of the new species, Litchi and Longan Phenology C. sinensis and Conopomorpha litchiella Bradley attack litchis, while the host range of Litchi and longan are adapted to the warm C. cramerella is restricted to rambutan and subtropics and produce the best crops when cocoa (Bradley, 1986). The confusion regard- winters are short, dry and cool, but frost-free. ing these true identities and hence the actual Such climatic conditions initiate the develop- species causing certain damage, is demon- ment of flower panicles. The inflorescences strated in papers from India (Singh, 1975; emerge during late winter and the flowers Butani, 1977; Lall and Sharma, 1978), China, open in early spring. Most cultivars set fruit (Anonymous, 1978) and Taiwan (Hwang and far in excess of what an individual tree can Hsieh, 1989). Since Bradley’s taxonomic carry through to maturity and will shed the study, Yao and Liu (1990), Huang et al. (1994, excess at various times during fruit develop- 1997) and Zhang, Z. (1997) have recognized ment. Longan flowers about 2 to 3 weeks later the differences and have described the pest than litchi, and matures 4 to 8 weeks later. status of each accordingly. Harvesting fruit as whole panicles has the C. sinensis lays yellow, scale-like eggs, effect of pruning and stimulates new leaf 0.4 × 0.2 mm long, on the fruit any time after growth after harvest. It also reduces tree size. fruit set, as well as on new leaves and shoots of Ideally, trees should produce one or two litchi and longan. The eggs hatch in 3–5 days vegetative flushes after harvest. The aim is to and the larva immediately penetrates the fruit, have the second or third flush commence in leaf or shoot. One or more eggs may be laid on

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a fruit but only one larva per fruit survives. (1994) recorded five hymenopterous para- Mature larvae are 6–10 mm in length and sitoids, of which Phanerotoma sp. was the most brownish in colour, or green if they have fed important, causing up to 22% mortality of on leaves. After 8 –12 days they leave the feed- larvae in fallen fruit. ing site to pupate on or under mature leaves in cream-coloured oval cocoons. The light DAMAGE C. sinensis shows a preference green pupae change to dark brown just before for litchis over longans but in both crops, eclosion, and the moth emerges after 5–7 days. damaged fruit may fall from the tree. Huang The moth is very small with long filiform et al. (1994) found that the pest had damaged antennae and narrow, fringed forewings mea- 87.9–99.0% of fallen fruit and 16.0–86.5% suring 8–11 mm when expanded. The moths of fruit remaining on the tree in sprayed live for about 5–8 days. In Taiwan, the pest orchards. Corresponding damage rates in may complete 4–5 generations during the unsprayed orchards were 96.1–100% and litchi and longan fruiting seasons. It appears 41.5–96.7%, respectively. to continue to develop over the winter period, either in alternative hosts or in the terminals of MONITORING AND CONTROL In Thailand, the main hosts, litchi and longan. During the fruit are inspected weekly immediately after off-season, when fruit is not available to the fruit set to detect eggs of Conopomorpha, which pest, it can survive by feeding on young leaves are very small and almost invisible to the and shoots, similar to C. litchiella. naked eye. The use of a ×20 hand lens facilitates monitoring. Infested fruit should be BIOLOGICAL CONTROL Most of the natural picked as it is found and destroyed, at infesta- enemies of C. sinensis in Thailand are micro- tion levels of 1–2%. When the pest becomes hymenopterous parasitoids. Most of them more active, permethrin is applied at weekly also parasitize the litchi leafminer, C. litchiella intervals, ceasing at least 2 weeks before har- (Dolsopon et al., 1997a). Phanerotoma sp., vest. Assessment of natural enemy activity Colastes sp. and Pholestesor sp. (Braconidae) can be done by inspecting fruit that has fallen and Goryphus sp. (Ichneumonidae) all attack from the tree. If parasitism is significant, the larva, while the latter may also attack the allowance for this must be made in deciding pupal stage. The ichneumonid, Paraphylax when to spray. Recently, assessment of moth sp., has been reared from pupae, but it is populations based on the catch of males apparently a hyperparasitoid. The braconids at sticky traps using pheromones as the bait, are recognized as being the most effective of has been used. Fruit may also be bagged the complex. Pests present in fallen fruit may to exclude the pest. This does not provide have been parasitized either before the fruit complete protection, but fruit colour and qual- has fallen from the tree, or after it has fallen. ity are improved in both litchi and longan. For this reason, it is recommended that Because litchis mature earlier than longans, all fallen fruit should be left under trees in the trees are pruned after harvest to remove order to permit parasitoid populations in the any remaining fruit that might harbour pupae orchard to increase. of the pest and so present a threat to the longan Two species of hymenopterous pupal crop (S. Dolsopon, Bangkok, 1999, personal parasitoids, Phanerotoma sp. and Apanteles sp., communication). have been recorded from C. sinensis in Taiwan. The actual sex pheromone of C. sinensis Tetrastichus sp. and Elasmus sp. have been has not been determined, but that of C. cramer- found attacking the larvae, and the egg ella has been used as a lure in male traps for parasitoid, Trichogrammatoidea bactrae fumata C. sinensis in Taiwan. More moths are caught Nagaraja, has been introduced to Taiwan from in traps that are placed inside the canopy than Thailand, with unknown results. in traps outside, and trapping can be used In Bihar, India, Mesochorus sp., Chelonus to monitor the abundance of the pest. The sp., Bracon sp. and Apanteles sp. were found to application of cypermethrin, deltamethrin, parasitize C. cramerella (most likely C. sinensis) carbofuran or fenthion during the early (Sharma and Agrawal, 1988). Huang et al. fruit set period is recommended to prevent

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excessive damage during fruit maturation. do not need to be sprayed. This allows the Moths can be excluded by enclosing the parasitoids to multiply. Sticky traps that are fruit panicles in nylon mesh bags, but the used for fruit borer can be used to help moni- economics of this procedure may preclude its tor for the presence of adult moths, particu- widespread use. If parasitoids are not active, larly during major flushes in June–October. orchard sanitation through the removal and destruction of fallen, infested fruit helps to reduce the build-up of moths. Fruit borers (Lepidoptera: Tortricidae) Conopomorpha litchiella Bradley DISTRIBUTION AND BIOLOGY The tortricid DISTRIBUTION AND BIOLOGY All stages of genus, Cryptophlebia, contains several species the litchi leafminer, Conopomorpha litchiella that attack litchis and longans throughout the Bradley, are similar to those of the fruit borer. world. In South Africa and the Indian Ocean The female moth lays the eggs on a new shoot. islands of Madagascar, Mauritius, Seychelles The small, light-yellow egg hatches 3–5 days and Réunion, Cryptophlebia peltastica Meyr. later. The newly hatched larva is creamy white is a major pest of litchis (Quilici et al., 1988; and it bores into the shoot. Larvae also mine in De Villiers and Stander, 1989; Quilici, 1996). the leaf blade. Mature larvae prefer to feed Cryptophlebia leucotreta Meyr. also attacks on the midrib and veins of young leaves. The litchis in South Africa but the frequency larval stage occupies 10–14 days after which of attack is insignificant compared to that the larva pupates on mature leaves. The pupal of C. peltastica (Newton and Crause, 1990). stage lasts 7–10 days and moths live for about Cryptophlebia bactrachopa Meyr. is recorded a week. attacking litchis in Malawi (La Croix and Thindwa, 1986). NATURAL ENEMIES The same species of para- The insect originally referred to as sitoids that attack the fruit borer effectively Argyroploce illepida Butler (= Cryptophlebia suppress C. litchiella in Thailand (Dolsopon carpophaga Walsingham) as a pest of litchis in et al., 1997a). India (Butani, 1977), is actually Cryptophlebia ombrodelta Lower (Bradley, 1953). This species DAMAGE The leafminer is attracted to leaf also occurs in Thailand, China, Japan, Taiwan, flushes of litchi and longan, especially during Hawaii and Australia (CIE, 1976), but only the rainy season from June to October in in the latter two areas is it regarded as a signifi- Thailand. Litchi is more heavily infested than cant pest of litchis and longans. Cryptophlebia longan. Damage caused to the shoots causes illepida is found only in Hawaii where it is a them to wilt. Dolsopon et al. (1997b) found pest of litchi and macadamia (Jones, 1994). All that 75% of litchi shoots were destroyed com- of these species utilize similar alternative host pared to 50% in longan. In addition, the num- plants such as Bauhinia galpinii and other ber of infested shoots was highly correlated Bauhinia spp., Delonix regia (flamboyant), with the number of pupae found on leaves. Caesalpinia pulcherima, Cassia spp., Macadamia integrifolia and Acacia spp. (Ironside, 1974; MONITORING AND CONTROL Bearing trees Newton and Crause, 1990). should be inspected for the presence of Namba (1957) detailed the biology of leafminer during major flushes in both litchi C. illepida, and that of C. ombrodelta was and longan. Eggs laid on the shoots can be described by Ironside (1974). The creamy detected by using a ×20 hand lens. Damaged white eggs are oval and flat, have a reticulate leaves should also be randomly checked. surface and are about 1.0 × 0.8 mm in size. Sprays, if they are necessary, must be applied They may be laid singly or in groups of up to to the very young leaves of any important 15, on the fruit. As incubation progresses, the flushes, especially the second flush. If 30–40% eggs turn pink and then red, before finally of larvae are parasitized, spraying is not appearing black as the head capsule of the recommended. Young, non-bearing trees fully developed larva becomes visible. Under

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normal summer temperatures in Queensland, recorded in the same study were Goniozus eggs hatch in 4–5 days. On hatching, the larva sp. nr. triangulus Keiff. (Bethylidae), Agathis commences to feed on the skin of the fruit, and sp. (Braconidae), Apanteles sp. (ater group) it then tunnels towards the seed. The mature (Braconidae) and Phanerotoma dentata Panz. larva is pinkish in colour with a brown (Braconidae). None of these attained high head capsule, and is about 20 mm long. levels of parasitism. T. fulva was introduced The prepupal period occupies 4 days during into Mauritius from India in 1973 to control which the larva chews an exit hole for its C. leucotreta on litchi, but its establishment emergence as a moth. When the moth is ready has never been confirmed (Quilici et al., 1988). to emerge, the pupa wriggles through the pre- C. ombrodelta in Queensland is parasitized pared opening to expose about two-thirds of by Apanteles briareus Nixon, Apanteles sp. its length and facilitate the moth’s emergence. (ater group), Apanteles sp. (myoecenta group), Female moths live for 7–10 days and may lay Bracon sp. (Braconidae), Brachymeria pomonae up to 250 eggs. (Cameron) (Chalcididae), Euderus sp. (Eulo- phidae), Echthromorpha insidiator Smith. F., DAMAGE All Cryptophlebia species that are Gotra bimaculata Cheeseman (Ichneumonidae) pests of litchis and longans are fruit borers. and Thelariosoma sp. (Tachinidae). The redu- The eggs are laid on the surface of the fruit. viid, Pristhesancus maculipennis Stål, also If the fruit are immature, the young larva occasionally preys on larvae (Ironside, 1974; will bore directly into the seed, which is Sinclair, 1979). The egg parasitoid, Trichogram- completely eaten. One larva may damage matoidea bactrae Nagaraja, has been recorded two or even three fruit, if very small fruit from eggs of C. ombrodelta collected from are attacked. However, there is a preference litchis, longans, macadamias and Bauhina for more mature fruit with larger seeds, espe- galpinii in southeast Queensland and in cially as the fruit begins to colour (Rogers and 1998/99, T. cryptophlebiae Nagaraja was found Blair, 1981; Newton and Crause, 1990). At this for the first time parasitizing a significant stage, newly emerged larvae generally tunnel proportion of C. ombrodelta eggs laid on these in the skin before attempting to get to the seed. same hosts (G.K. Waite, 1999, unpublished) If the route taken to the seed commences adja- (Plate 83). cent to the peduncle, then the larva usually The eulophid ectoparasitoid, Elachertus survives, but if it attempts to bore through the sp. nr. lateralis, parasitizes C. ombrodelta larvae mature flesh, it usually drowns in the juice, tunnelling in the seed pods of Bauhinia which seeps into the wound caused by its purpurea in Guangzhou, China, where parasit- feeding. In either case, the fruit will not be ism levels of up to 67% have been recorded marketable. In addition, the juice that oozes (G.K. Waite, 1988, unpublished). C. ombrodelta from borer wounds may stain neighbouring has been considered an important pest of fruit on a panicle and cause further losses litchis in Guangdong Province (Anonymous, (Waite, 1992a). This is particularly so in 1978) but, in reality, its impact seems to be cultivars such as Bengal, which produces minor. This is in contrast to Queensland large panicles bearing many fruit in a tight where, although the insect is known as the cluster. macadamia nut borer, it is a more serious problem in litchis and longans. This consider- BIOLOGICAL CONTROL The various species ation led to the importation of Elachertus sp. of Cryptophlebia are known to be attacked by into Queensland and its release in 1993. The complexes of egg, larval and pupal parasit- parasitoid has been recovered from the field oids that are not always capable of preventing but no measure of its effect is available. economic damage in orchard crops. In India In South Africa, the egg parasitoid T. the egg parasitoid, Trichogrammatoidea fulva cryptophlebiae has been found to be particu- Nagaraja, was considered to be the most larly effective and it has been used extensively important of a number of natural enemies for inundative release into citrus for the con- of C. ombrodelta, parasitizing up to 68% of trol of C. leucotreta (Newton and Odendaal, eggs (Anonymous, 1976). Larval parasitoids 1990). It has been recorded parasitizing 63% of

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the eggs of C. peltastica in litchis, comparable fruit colouring have generally been applied, to the result achieved against C. leucotreta in usually on a calendar basis rather than as a citrus under normal conditions (Newton and result of monitoring for the presence of eggs Crause, 1990). (Waite, 1992b). Newer insecticides including In Hawaii, numerous parasitoids attack- the insect growth regulator tebufenozide ing C. illepida were identified by Namba (1957). (Mimic®) promise to provide better control These were Cremastus hymeniae Vierick, with less disruption of natural enemies. Horogenes chilonus (Cushman), Coccygomimus sanguipes (Cresson), C. punicipes (Cresson), Pristomerus hawaiiensis Perkins (Ichneumo- Fruit piercing moths nidae), Brachymeria obscurata (Walker) (Chal- (Lepidoptera: Noctuidae) cididae), Bracon mellitor Say (Braconidae), Omphale metallicus Ashmead (Eulophidae), DISTRIBUTION AND BIOLOGY Fruit piercing Perisierola emigrata Rohwer (Bethylidae) and moths attack a range of fruit throughout Sierola cryptophlebiae Fullaway (Dryinidae). South-East Asia, the South Pacific and Australia (Banziger, 1982; Fay and Halfpapp, MONITORING AND CONTROL Newton and 1993). Fruits such as mango, carambola, citrus, Crause (1990) found that there was no differ- mangosteen and stonefruits, as well as litchi ence in the distribution of eggs laid on litchi and longan, are damaged by a complex of fruit by C. peltastica and C. leucotreta with moth species. respect to height on the tree, or aspect. Rela- The larvae of fruit piercing moths tively low oviposition rates were recorded on develop on a variety of host plants. In the immature fruit, but the number of eggs laid Pacific Islands, Eudocima (Othreis) fullonia increased rapidly as fruit approached matu- (Clerck) breeds on Erythrina spp., commonly rity. Monitoring for infestations should con- known as coral trees. However, in Australia centrate on maturing fruit, with samples taken and Thailand, this species breeds only on from any part of the tree. Similar recommen- vines of the family Menispermaceae (Legne- dations apply for C. ombrodelta in Queensland phora, Stephania, Fawcettia, Tinospora, Carronia, litchis (Waite, 1992a). Jones (1995) found that Sarcopetalum, Pleogyne and Hypserpa spp.), the presence of eggs, either hatched or even though Erythrina spp. are common unhatched, was not a good predictor of larval throughout its range in these countries infestation of litchi fruit in Hawaii. Only 12% (Sands and Schotz, 1991). Eudocima salaminia of fruit with Cryptophlebia spp. eggs, exhibited (Cramer) larvae utilize Stephania japonica larval damage. A sequential sampling proce- Miers and its subspecies as host plants. Fay dure was developed, which indicated that and Halfpapp (1999) recorded E. fullonia, a maximum 220 fruit sample was required Eudocima salaminia (Cramer) and Eudocima to make a decision with respect to chemical jordani (Holland) as primary feeders on litchi control, but if damage was greater than 10%, fruit on the wet tropical coast of Queensland. the sample could be reduced to fewer than 50 Populations of fruit piercing moths that fruit. appear in the subtropical southeast of the De Villiers (1992a) recommended the state in late summer and autumn, originate application of the insect growth regulator in breeding areas of the tropical north, triflumuron as a single, full cover spray with seasonal migration bringing them south 40 days before harvest, or two sprays of (Sands and Brancatini, 1995). teflubenzuron a fortnight apart, commencing when the fruit is 10 mm in diameter. An alter- DAMAGE Unlike most lepidopterous pests, native recommendation is to cover the fruit of which the larva is the damaging stage, in panicles with paper bags to exclude the this case it is the adult that causes the damage pest. This also improves fruit colour and through its feeding on the fruit. The moths overall quality. In Queensland, carbaryl and possess a proboscis that is able to drill a neat azinphos-methyl have been used with vary- hole in the skin of a range of fruit, including ing success. Several sprays commencing at litchi and longan. Considering the thickness of

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the skin of some cultivars, this is no easy task. Thailand, ripe fruit of banana and pineapple The moths suck juice from the fruit, leaving are dipped in insecticide and hung in the trees an opaque area of flesh that is drier than the to poison the feeding moths. In some coun- surrounding tissue. A day or so after feeding tries, panicles of fruit are covered with paper by a moth the flesh of the fruit commences bags to protect them from a range of pests. to ferment. The fermentation is initiated by These are effective against fruit piercing yeasts and bacteria that are introduced to the moths and are recommended in Thailand. wound on the proboscis of the moth (Sands In recent times, parrots and fruit bats and Schotz, 1989). Drosophila spp., which are have become a severe problem for litchi and attracted to the fermenting fruit, hasten the longan growers in eastern Australia. To pre- process of fruit deterioration. Within a few vent total loss of crops from these pests, many days a frothy exudate begins to seep from the growers have erected protective nets. These hole and this may stain undamaged fruit on have ranged from nets draped over individual the panicle, causing further losses. trees, to tunnel nets covering entire rows, or complete enclosures that surround the entire BIOLOGICAL CONTROL Several egg parasit- orchard. Although these have a high capital oids of E. fullonia have been identified in cost, they last for years and the entire cost is Papua New Guinea and the western Pacific usually saved through the prevention of dam- region. Those originating in Papua New age in one season. These same nets exclude Guinea were thought to provide a good fruit piercing moths and, if the mesh is fine opportunity to achieve biological control of enough, may also keep out some other pests. the pest in the Pacific Islands. However, only Nets that are merely draped over trees offer one of the introduced species, Telenomus sp., poor protection, since the fruit upon which established well and contributed significantly they rest is still accessible to the various pests. to egg mortality. Two parasitoids from Papua New Guinea, Ooencytus papilionis Ashmead (Encyrtidae) and Telenomus lucullus Nixon Loopers (Lepidoptera: Noctuidae) (Scelionidae), have been identified as potentially useful biological control agents for fruit DISTRIBUTION AND BIOLOGY Oxyodes scrobic- piercing moths in Australia. They have not yet ulata F. and Oxyodes tricolor Guen. occupy been introduced because of fears that they will similar niches in Thailand and Australia, attack non-target species (Sands, 1996). respectively. In Australia, O. tricolor attacks litchis in southeast Queensland but is not PEST MONITORING AND CONTROL In Australia a pest in north Queensland. The castor oil and Thailand, farmers go to their orchards at looper, Achaea janata (L.), is a voracious leaf night with spotlights and attempt to manually feeder in Queensland and often infests trees in remove as many moths as possible. This may large numbers at the same time as O. tricolor. be achieved by catching the moths as they feed The white eggs of O. scrobiculata are laid on the fruit, or by catching them in a net or on the leaves of litchi, longan and rambutan, swatting them with a tennis racquet as they fly with litchi being preferred. The larvae grow to from tree to tree. When moths are numerous, 40–50 mm in length and may be greenish yel- this becomes a futile exercise. low to brown when mature. The larval stage Australian farmers also make traps by takes 14–17 days to complete and the small, draping shade cloth loosely over a frame of light-brown moths emerge about 10 days wire and baiting it with fermenting fruit such after pupation. The main period of activity as citrus and bananas. The moths are attracted is during the postharvest vegetative flush. to and feed on the fermenting fruit, and become entangled in the folds of shade cloth DAMAGE The caterpillars feed on the when they fly off. They are then killed manu- foliage of litchi trees and can cause severe ally each morning. Large numbers of these defoliation. Although they will eat leaves traps are required to protect an orchard and, of any age, they prefer the younger leaves. even then, substantial damage is sustained. In The whole leaf is consumed, leaving only

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the midrib intact and imparting a ragged eggs. These take an average of 6 days to hatch, appearance to infested trees. with the larvae adopting the typical tortricid habit of rapid backwards movement and BIOLOGICAL CONTROL The final larval instar dropping by silken threads when disturbed. is often attacked by unidentified hymenop- The larvae web and roll leaves together to terous parasitoids which in Thailand, may form a shelter in which they feed (Anony- account for 30–40% of the larvae. mous, 1978).

MONITORING AND CONTROL In Thailand it is DAMAGE Although it is primarily a leaf- recommended that carbaryl be applied when roller, O. praecedens may also feed on flowers infestations reach two or three young larvae and fruit. However, it is not regarded as a per leaflet. Shaking the tree to dislodge larvae serious pest, since it is often suppressed by a on to the ground improves the effect of complex of three microhymenopterous para- the insecticide. If 40% or more of larvae are sitoids: Goniozus sp. (Bethylidae), Apanteles sp. parasitized, sprays should not be applied. (Braconidae) and Pristomerus sp. (Ichneumo- In Queensland, Bacillus thuringiensis Berliner nidae). In addition, it attacks young fruit (Bt), endosulfan or methomyl may be used during the period of natural fruit shedding, against O. tricolor when significant damage is when much of the damaged fruit would caused to the new flush and natural enemies have fallen regardless of being damaged have not controlled the infestation. (Vayssieres, 1997). O. perdulata attacks flowers and foliage in Queensland, but rarely feeds on fruit. Foliage damage is generally ignored, but Leafrollers (Lepidoptera: Tortricidae) sprays may be applied at flowering to control this species along with several others, which DISTRIBUTION AND BIOLOGY Olethreutes may infest the flower panicles at the same praecedens Wals. is a minor pest of litchis in time. Réunion (Vayssieres, 1997) while Olethreutes In China and India, where it is regarded perdulata Meyr. is an occasional pest in as a minor pest, P. aprobola rolls leaves and Queensland (Waite, 1992a). Platypeplus attacks flowers but in Australia, as part of aprobola (Meyrick) has been recorded on litchis a complex of species attacking flowers, it is in Australia (Waite, 1992a), China (Anony- considered to contribute to production losses. mous, 1978) and India (Butani, 1977) while In China, A. cyrtosema and H. coffearia feed on Epiphyas postvittana (Walker) is recorded leaves, flowers and fruit (Anonymous, 1978). from Australia (Storey and Rogers, 1980) and Hawaii (Higgins, 1917). Adoxophyes cyrtosema BIOLOGICAL CONTROL All of these species Meyr. and Homona coffearia Nietner, attack are subject to attack by numerous parasitoids litchi and longan in Guangzhou and Fujian that generally have been poorly studied. Provinces of China (Anonymous, 1978). The In China, A. cyrtosema is parasitized by latter species, as well as Homona difficilis,is Trichogramma sp., Apanteles sp., Brachymeria recorded from litchi, longan and rambutan obscurata (Wlkr.), Phaeogenes sp. and Nemorilla in Thailand. The orange fruit borer, Isotenes floralis maculosa Meig., as well as being pre- miserana (Walker), is another omnivorus dated on by the beetle, Calleida sp., and the fly, leafrolling species that also attacks flowers Xanthandrus comtus Harris. and fruit in Queensland. In Guangzhou, A. cyrtosema has a host MONITORING AND CONTROL In Australia, the range of about 27 plant species and undergoes damage caused by leafrollers is generally tol- nine generations a year. The larvae overwinter erated so long as it is restricted to the foliage. in citrus nurseries or on grasses, and pupate in If necessary, sprays of methomyl or carbaryl March. The emerging moths then fly into litchi may be applied when 50% of leaf flushes and citrus orchards where they mate and lay are infested, to minimize damage to critical eggs on the leaves. Female moths lay up to flushes, especially in young trees (Waite and three egg masses, each containing about 140 Elder, 1996). In India, the manual removal of

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rolled leaves which contain larvae was recom- experimental conditions provided 73.3–100% mended when infestations were light, with control (Xu et al., 1995). sprays of phosphamidon, fenitrothion or endosulfan applied under severe attack MONITORING AND CONTROL Regular inspec- (Butani, 1977; Sahoo and Maiti, 1992). tions of orchards during the period of adult activity, enables orchard workers to remove the beetles manually when they ‘play dead’. Longicorn beetles (Coleoptera: Also at this time, eggs and young larvae can Cerambycidae) be removed from accessible branches. Estab- lished larvae can be located through the pres- DISTRIBUTION AND BIOLOGY The litchi longi- ence of frass packed into the ends of tunnels, corn beetle, Aristobia testudo (Voet), is a serious and ‘fished out’ with wire hooks or a knife. pest of both litchi and longan in Guangdong A skilled worker can kill 112 larvae in 2 h Province in China (Zhang, Z., 1997). The beetle (Ho et al., 1990). Alternatively, dichlorvos may has one generation per year, with adults be injected into the tunnels, which are then emerging from June to August. They girdle sealed with clay (Zhang, Z., 1997). branches by chewing off 10 mm strips of bark. The eggs are laid on the wound and are covered with an exudate. The larvae hatch Weevils (Coleoptera: Curculionidae) from late August and live under the bark until January when they then bore into the xylem DISTRIBUTION AND BIOLOGY Cratopus angust- and create tunnels up 60 cm long in the wood atus Boh. and Cratopus humeralis Boh. are (Ho et al., 1990). These tunnels have openings both found attacking litchis on the Island of packed with frass, situated at regular intervals Réunion. The weevils mate mostly at night and opening to the exterior, for aeration. In and the eggs are laid in irregular groups June, the tunnels are blocked with wood fibre between leaves that are glued together with and frass, just before the larva pupates. a mucilaginous secretion produced by the In Taiwan, the white spotted longicorn female. On hatching, the larvae migrate to the beetle, Anoplophora maculata (Thomson), has a soil, where they feed on the roots of the tree. 1-year life cycle. Adults emerge in the spring Sometimes the adults aggregate on certain and a female beetle lays about 20 eggs that are trees but the reason for this has not been inserted individually into T-shaped incisions ascertained (Vayssieres, 1997). In Queensland, in the bark, usually less than 0.5 m above the Australia, the weevils, Euthyrrhinus medita- soil surface. The larval period lasts about 10 bundus Fab. and Orthorrhinus klugii Boh., chew months. small patches of bark from twigs in which they Platyomopsis humeralis (White) and lay their eggs, but damage to the tree is minor. Ceresium sp. have been recorded attacking litchis in Australia (Waite, 1992a) and DAMAGE Cratopus spp. feed on leaves, Réunion (Vayssieres, 1997), respectively, flower panicles and fruit less than 10 mm though neither is regarded as a pest. long, although the primary target is probably the fruit peduncle (Vayssieres, 1997). O. klugii DAMAGE Tunnelling by the larvae in and E. meditabundus occasionally ring-bark branches may kill branches, and in severe terminals and cause them to die, but the infestations trees may die. Ring-barking damage is insignificant. of twigs by ovipositing adults causes the extremities to die and snap off. PEST MONITORING AND CONTROL Chemical controls can be applied when infestations BIOLOGICAL CONTROL There are no known are noted on the trees. However, care needs natural enemies of A. testudo but injection of to be taken since the pyrethroid, cyhalothrin the nematode Steinernema carpocapse (Weiser) (Karate®), applied to control Cratopus spp. in (Agriotes strain) into the larval tunnels under Réunion, eliminated the natural enemies of

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Icerya sp., resulting in an outbreak of that pest The most serious problem is caused by Rhypa- (Vayssieres, 1997). Systemic insecticides that rida discopunctulata Blackburn, which emerges will control the larvae in the soil without in swarms after spring rains and proceeds to harming the beneficial species are being strip the leaves from host trees in their flight tested. path. The red-shouldered leaf beetle, Mono- lepta australis (Jacoby), may do the same, especially in southern Queensland. The beetles lay Scarab beetles (Coleoptera: Scarabaeidae) their eggs in the soil and the larvae feed on the roots of a range of weeds and grasses. Swarms DISTRIBUTION AND BIOLOGY The elephant may emerge at any time of the year, but most beetle, Xylotrupes gideon (Linnaeus), damages swarms emerge after spring storms. litchi fruit in all production areas of Australia. The larvae develop in the soil or in composting DAMAGE Individual beetles are commonly organic matter where they feed on plant roots seen on litchi and longan trees, usually and the humus material in the compost. They attracted to split fruit. Even when they grow to a length of about 50–70 mm and are numerous but not swarming, no damage pupate in the soil or compost. The large, results. However, once swarms form and a heavily sclerotized and sexually dimorphic feeding frenzy develops, extensive damage adults emerge in spring. may occur, with whole trees being stripped of their leaves. DAMAGE The beetles breed in litchi orchards or close by, and are attracted to the PEST MONITORING AND CONTROL Most grow- trees just prior to harvest by ripe fruit that has ers are aware of the potential for leaf-feeding split or has been damaged by other pests, beetle swarms to cause severe and rapid especially by parrots or fruit bats. Once they damage and they monitor orchards regularly have infested a tree and start feeding on the for the incidence of the pest. Neighbours damaged fruit, they inevitably start to feed on will also assist one another in this, and if sound fruit and may inflict severe damage. swarms are detected on windbreak trees, they are sprayed with carbaryl or endosulfan BIOLOGICAL CONTROL Natural enemies of before they can move on to the orchard trees the beetles are not known. (Waite and Pinese, 1989).

MONITORING AND CONTROL Regular inspection of orchards when the fruit is ripening is Soft scales (Homoptera: Coccidae) necessary to detect the presence of the beetles. They are tolerant of many of the routine DISTRIBUTION AND BIOLOGY Pulvinaria sprays applied for other pests and high dosage (Chlorpulvinaria) psidii (Maskell), the green rates of carbaryl or chlorpyrifos are required shield scale, infests litchi trees in China, Tai- to kill them. Alternatively, they can be manu- wan, Australia, Florida and India (Plate 84). It ally removed by knocking them into buckets reproduces parthenogenetically (Swirski et al., with a stick, but in Australia at least, this is 1997) and has three to four generations a costly because of the labour involved. year in Taiwan. In Queensland, crawlers are produced in early spring by adult scales that infest the leaves and twigs. Some of these Leaf feeding beetles (Coleoptera: crawlers move onto developing flower pani- Chrysomelidae) cles and later onto the young fruit. The life cycle takes about 5–6 weeks (El-Minshawy DISTRIBUTION AND BIOLOGY The small black and Moursi, 1976) and the progeny of these or brown leaf-eating beetles belonging to the early colonists often cover the surface of genus Rhyparida often attack the new leaf flush the fruit. The female scales are sometimes of litchis and longans in north Queensland. mistaken for mealybugs by farmers because

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the egg masses, which are covered in waxy Heavy infestations of K. lacca may cause filaments, cover the end of the scale. twigs to wilt and die, affecting flowering Soft brown scale, Coccus hesperidum and fruiting. The heavy deposits of honeydew Linnaeus, is an occasional pest of litchis in which are produced encourage the growth of Queensland where its parasitoids have been sooty mould (Hsieh and Hwang, 1981). disrupted by chemical sprays or where it is protected by ants (Waite, 1986). Parasaissetia BIOLOGICAL CONTROL The mealybug lady- nigra (Nietner) and Saissetia coffeae (Walker) bird, Cryptolaemus montrouzieri Mulsant, infest litchis in India, but along with C. psidii and the green lacewing, Mallada signata they are not important (Butani, 1977). (Shneider), are the most effective predators Pink wax scale, Ceroplates rubens Maskell, of P. psidii in Queensland, the egg masses occurs in most litchi and longan producing being particularly attractive to them. Numer- countries but is a pest only on longans in ous parasitoids have been introduced to Queensland, Australia. Ceroplastes ceriferus certain areas over the years to control the (Fabricius), Indian white wax scale, and pest on ornamentals. Microterys kotinskyi Nipaecoccus vastator (Maskell) are common on (Fullaway) (Encyrtidae) is regarded as an litchis in Taiwan, but are only minor pests. In important parasitoid of the scale on Réunion, only Icerya seychellarum West. and a ornamentals in Burma (Swirski et al., 1997). Pulvinaria sp. have been recorded on litchis, No significant parasitism has been noted the former often attended by the ant Solenopsis in the scale on litchis in Queensland, but sp. (Vayssieres, 1997). in China, Anicetus ceroplastis Ishii parasitizes The lac insect, Kerria lacca Kerr, was intro- nymphs and female scales. An unidentified duced into Taiwan from Thailand in 1940 for coccinellid and several predatory mites are the production of shellac. Modern synthetic also reported to feed on the scales there, substances have made the insect obsolete for and during the wet season, an unspecified that purpose, but it lives on as a pest of many entomophagous fungus may cause significant fruit and flower species, among them litchi mortality (Anonymous, 1978). and longan. Female scales may be ovo- Pink wax scale is often well controlled viviparous or produce eggs. Two generations in coastal Queensland by the parasitoid occur each year, in December–February and Anicetus beneficus Ishii and Yasumatsu, but May–June (Hwang and Hsieh, 1981). such control may be patchy. The parasitoid is known to have poor dispersal abilities DAMAGE P. psidii is not considered to be and infestations of pink wax scale may important in India (Butani, 1977). The scales develop unchecked in longan orchards cause no damage as they feed, but when sig- because infested trees have been isolated nificant populations develop on the fruit, as from sources of the parasitoid. In addition, they often do in Florida (Butcher, 1954), China, sprays applied to control the macadamia nut Taiwan and Australia (Waite and Elder, 1996), borer may suppress developing parasitoid these become unmarketable because of the populations. presence of the scales. The scales also produce Several parasitoids and predators are honeydew, which supports the growth of mentioned as attacking I. seychellarum in sooty mould not only on infested fruit and Réunion. These include Rodolia chermesina panicles, but on those below. This discolor- Mulsant (Coccinelidae), Borniochrysa squamosa ation reduces their appeal to consumers and (Tjeda) (Chrysopidae), Aprostocetus sp. (Eulo- results in downgrading or rejection of the fruit phidae) and Cryptochaetum sp. (Cryptochae- in the market place. C. hesperidum causes simi- tidae) (Vayssieres, 1997). Parasitoids of K. lar problems. lacca in Taiwan include Eupelmus tachardiae, C. rubens infests the leaves of longan trees, Tachardiaephagus tachardiae, Tachardiaephagus giving rise to heavy films of sooty mould sp., Tetrastichus purpureus and Phycus sp. which probably affect photosynthesis. In Several predators have also been recorded, addition, on heavily infested trees, every fruit but even so, natural control is ineffective is spoiled by sooty mould deposits. (Hwang and Hsieh, 1981).

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PEST MONITORING AND CONTROL In Queens- Blackburn were also found to feed on the land, it is recommended that green shield scales (Waite, 1988). scale populations be monitored just before and during the emergence of flower panicles to determine infestation levels on the twigs. Bugs (Hemiptera: Tessaritomidae) If a significant proportion of twigs is infested with scales, an oil spray should be applied to DISTRIBUTION AND BIOLOGY Several bugs prevent infestation of the flowers and subse- belonging to the family Tessaritomidae quently, the fruit (Waite and Elder, 1996). Pink attack litchis and longans throughout China, wax scales and the sooty mould they produce South-East Asia and Australia. Tessaritoma are easily seen on the leaves of longans, papillosa Drury occurs in southern China, and corrective sprays of low viscosity oil or Vietnam, Thailand, Burma, the Philippines methidathion should be applied to limit fruit and India (Anonymous, 1978), although contamination. Proper timing of sprays with Butani (1977) notes that Tessaritoma javanica insecticides, such as dimethoate and fenthion, Thunberg and Tessaritoma quadrata Distant at the time when nymphs are being produced, are the species found on litchi in India. In provides good control of K. lacca (Hsieh and Australia, Lyramorpha rosea Westw. is known Hwang, 1983). as the litchi stink bug, but it is a rare visitor to litchi orchards and is never a problem. In China, apart from utilizing litchi Armoured scales (Homoptera: Diaspididae) and longan as hosts, T. papillosa attacks citrus, pomelo, castor oil, pomegranate, eucalyptus, DISTRIBUTION AND BIOLOGY The diaspidid canna, loquat and rose flowers (Anonymous, scales, Hemiberlesia lataniae (Signoret) and 1978). The bug has one generation per year Fiorinia sp. nr. nephelii Maskell, occasionally and both the adults and nymphs feed on the infest litchis in Queeensland but they seldom terminals, flowers and fruit. Adults tend to cause problems (Waite, 1992a). Similarly, aggregate and overwinter mostly on litchis Fiorinia nephelii, Parlatoria pseudopyri Kuwana, and longans, but may also be found on other P. cinerea Danne and Hadden and Aulacaspis hosts, in areas out of the wind but with ade- spp. are recorded from the crop in India, but quate sunshine. In spring the female bugs are are of no consequence (Butani, 1977). especially attracted to trees with many flowers and new terminals, where they mate and lay DAMAGE The hard scales generally infest up to 14 egg masses, each containing about 14 twigs and if allowed to multiply unchecked eggs. These are usually attached to the back of they can kill the terminal growth, and in leaves. Peak egg laying occurs in late March the case of young trees may threaten their in Guangdong, but continues throughout the vitality. summer until September (Anonymous, 1978). The eggs, which are round and creamy white BIOLOGICAL CONTROL Microhymenoptera in colour, turn red just before hatching takes undoubtedly suppress hard scale populations place after about 13 days at 25°C (Anonymous, in the absence of disruptive chemical sprays, 1978; Unahawutti, 1990). Newly hatched but the identity of those operating on the nymphs are reddish in colour and the individ- above species has not been determined, except uals from each egg mass remain aggregated for H. lataniae in Queensland. There, latania for several hours after hatching, before they scale attacking avocados has been shown to be disperse. They develop through five instars to controlled by a complex of natural enemies the light-brown coloured adult stage in about which include Aphytis sp. proclia group and 80 days. When disturbed, or during the heat of Encarsia citrina (Craw.) (Aphelinidae), as well the day, first and second instar nymphs may as Signiphora flavella Girault and S. perpauca drop to the ground, returning to the tree later Girault (Signiphoridae). Chrysopa oblatis when temperatures have cooled. Nymphs are Banks (Chrysopidae) and Rhizobius satellus able to withstand periods of up to 12 days

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without feeding. Both adults and nymphs are silkworm, Samia cynthia ricini (Drury), but able to expel smelly defensive odours when Liu et al. (1988) reported that Anastatus sp. disturbed. had been successfully reared on artificial host The first nymphs mature in June while eggs. Xin and Li (1989) found that the average there are still old adults in the trees. These old rate of parasitism of the artificial eggs was adults may have lived for up to 370 days, and 40–44% while emergence was 94–96%. After they die during July/August. The new adults continuous rearing for three generations in the do not mate immediately, since their repro- artificial eggs, the viability of A. japonicus was ductive organs are not mature. They over- better than when they were reared in the eggs winter and recommence the cycle in spring. of Antheraea pernyi (Guénerin-Méneville). In Guangxi Province, Zhou and Xian DAMAGE In litchis and longans, adults (1994) report that the main parasitoids of T. and nymphs feed on terminals, which may be papillosa eggs are Ooencyrtus sp. and Anastatus killed, and also on flowers and fruit, causing sp. and that these species parasitized an these to fall. Zhang, D.P. (1997) studied the average of 66.8% of eggs. Mass releases physiology of stink bug stings in detail, and of Ooencyrtus sp. into litchis and longans found that the type of damage caused resulted in Guangxi have given significant levels of in more immature fruit than mature fruit fall- control. ing from the tree. Liu and Lai (1998) claimed In Thailand, native species of egg that 20–30% of fruit is damaged by litchi stink parasitoids, Anastatus sp. nr. japonicus and bug and that chemical control has not given Ooencyrtus phongi, operate in a similar manner satisfactory results. to their counterparts in China, i.e. low levels of control during the critical fruit production BIOLOGICAL CONTROL In Guangdong, the period early in the season, building up to good main natural enemies of T. papillosa are the egg levels later. Mass rearing of the local para- parasitoids Encyrtus (Ooencyrtus) sp., Anastatus sitoids in the wild silk worm Philosamia ricini sp. and Blastophaga sp. These may parasitize Hutt. and releasing them early in the season, 70–90% of eggs late in the season, with produced results similar to those achieved in Encyrtus sp. being the most effective (Anony- China, with Anastatus sp. and O. phongi para- mous, 1978). Similar parasitism levels were sitizing 79% and 21% of eggs, respectively recorded by Liu and Lai (1998) when para- (Nanta, 1992). sitized egg cards were hung in trees during March. Liu and Gu (1998) found that in an MONITORING AND CONTROL orchard under integrated pest management, Manual control. When cheap communal combined parasitism rates by Anastatus sp. labour was available in China in the 1970s, and Ooencyrtus sp. were 41.9–47.1% in June, manual control was combined with mass but only 0–2.8% in an orchard that relied on releases of the egg parasitoid to minimize chemical control. During the 1970s, biological damage caused by the litchi stink bug. It was control of the litchi stink bug in Guangdong recommended that adults be destroyed dur- was initiated using the egg parasitoid, ing the winter period by shaking or beating Anastatus japonicus Ashmead, the flat venter trees to dislodge the adult bugs, which wasp, after field trials in the late 1960s had could then be collected and destroyed. Alter- demonstrated its value (Huang et al., 1974). natively, they could be caught using nets Since early season parasitism rates were of the wetted with human or bovine urine, presum- order of only 10% in April when most of the ably to induce them to release their grasp on eggs are laid, natural control did not prevent the tree. The burnt remains of dead bugs could severe damage to the crop. Boosting para- be used in the same way. Egg rafts, which are sitoid numbers in the orchard at this time of easily detected, could also be removed manu- the year through mass releases of wasps was ally and destroyed, with any parasitized eggs found to increase parasitism levels to 90% and determined by their black colour placed in give good control. The wasps have tradition- receptacles for rearing of the parasitoids for ally been reared in the eggs of the castor later release. Nymphs were swept from the

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trees using straw dipped in human or bovine 2 days. Female parasitoids are partheno- urine attached to bamboo poles. A glue made genetically arrhenotokous. To prevent the from resin and castor oil and painted on to production of excess males, fresh host eggs the tree trunks prevented the nymphs from are used, the temperature is maintained at climbing back up (Anonymous, 1978). 25–30°C, and humidity at 70–80%, and adequate light is provided. Adult parasitoids Chemical control. Mass releases of egg emerge after about 20 days at 26–28°C. If parasitoids are effective in controlling litchi necessary, in order to accumulate sufficient stink bug and, at least during the time that numbers of parasitoids that emerge at the people’s communes were in place in China, same time, the host eggs can be stored at were a cheaper form of control than the use 10–12°C for up to 6 months when the para- of chemicals (Huang et al., 1974). After the sitoid larvae are in the first or second instar break-up of the communes, chemical insecti- (Huang et al., 1974). For field release, the para- cides seemed to be the favoured method sitized eggs are glued on to cards and attached of control for this pest, although biological to the trunks and branches of the trees. control using egg parasitoids is once again being considered. Timing of sprays is especially critical for success with the litchi stink Fruitspotting bugs (Hemiptera: Coreidae) bug because it has been found to vary in its susceptibility at different times of the year DISTRIBUTION AND BIOLOGY Amblypelta nitida to trichlorfon, the commonly used chemical, Stål, the fruitspotting bug, and Amblypelta depending on the body fat content and its lutescens lutescens (Distant), the banana spot- nature. Maximum resistance was recorded ting bug, are major pests of most of the tropical during the winter when fat levels reached and subtropical tree crops grown in Queens- 20–25%, and the proportion of unsaturated fat land (Waite, 1990). A. nitida is more common was high. Maximum susceptibility occurred in southern Queensland, while A. l. lutescens from February until June/July when fat levels dominates in north Queensland. were 4–12% and the proportion of unsatu- The adult bugs overwinter on citrus or rated fat was low. On this basis, one spray was non-crop hosts, which may be native plants or applied in early March, when resistance was exotic ornamentals. In spring, when the litchi low and before the first eggs had been laid. and longan trees start to flower, the bugs In late April and early May, adult resistance commence to move into the orchards. How- is still low and most of the new generation ever, they prefer to feed on green fruit, and nymphs are in instars one and two, which are most fruitspotting bugs migrate into the trees also susceptible. This is a good time to apply a just after fruit set. Orchards located adjacent second spray if necessary, before the nymphs to the natural rainforest breeding areas of develop to the third instar, which is difficult the bugs are particularly susceptible to attack to kill (Anonymous, 1978). Good coverage, (Waite and Huwer, 1998). Female bugs lay especially of old, very large trees, is essential. individual eggs, mostly on leaves. These take about 7 days to hatch and the nymphs pass Biological control. The annual life cycle through five instars before maturing after of T. papillosa is tied to seasonal conditions, approximately 42 days. and activity commences in spring, coinciding In South Africa, the coconut bug, Pseudo- with the production of litchi and longan theraptus wayi Brown, has become a problem flower panicles. Therefore, releases of the in a variety of crops over the last 20 years (De egg parasitoid A. japonicus are timed for Villiers, 1990b). It is not currently recognized this period in both China and Thailand. The as a pest of litchis in that country, but its parasitoids are reared in the eggs of silkworm history of adopting new hosts there suggests moths which are in turn reared on castor oil that it may eventually become a problem in leaves. About 1500–2000 silkworm eggs are the crop. Paradasynus longirostris Hsiao has exposed to 600 mated female parasitoids for recently been described as an important pest

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of longans in Fujian, China. The adults and ground, dissection of this fruit is the best way nymphs attack the fruit (Huang et al., 2000). to sample for the presence of bugs. Litchis and longans usually set more fruit than the tree DAMAGE Amblypelta spp. feed on the devel- can mature, and a period of natural fruit drop oping seed within the fruit and this initiates occurs every season. Inspection of the seed of abscission with the fruit falling a couple of the fruit which has fallen is the only way to days later (Plate 85). The puncture mark is determine if that fruit is part of the natural invisible on the surface of the fruit and the drop or has been damaged by fruitspotting only way to distinguish bug-damaged from bugs. If 10% or more of the fallen fruit has been naturally shed fruit is to dissect them to detect damaged by bugs then a spray of endosulfan the typical tan lesion that is produced on the should be applied. Usually, a maximum of dark brown seed testa. In south Queensland, two sprays of endosulfan applied 2 weeks A. nitida was shown to have damaged an aver- apart during the first 6 weeks after fruit set age of 95% of fallen fruit on unsprayed litchis is sufficient to protect the crop from the over three seasons, and in north Queensland, bugs. In longans, which are subject to attack A. l. lutescens had damaged 98% of fallen fruit over a longer period, further sprays may be (Waite, 1990). Comparable data are not avail- necessary but those applied for the control of able for longans but observations indicate that C. ombrodelta also control fruitspotting bugs. a similar situation exists, with the susceptible period extending up to harvest (G.K. Waite, 1990, unpublished). In litchis, adults may occasionally feed on mature fruit, but usually Mites (Acari: Eriophyidae) only nymphs, which are trapped on the trees because they are flightless, can be found feed- DISTRIBUTION AND BIOLOGY The litchi ing on the fruit after it has commenced to erinose mite, Aceria litchii (Keiffer), also colour. known in China as litchi hairy mite, hairy spider, or dog ear mite (Anonymous, 1978), BIOLOGICA L CONTROL Fruitspotting bugs occurs throughout China and Taiwan (Huang have few natural predators apart from spiders, et al., 1990), India (Puttarudriah and Channa particularly those belonging to the family Basavanna, 1959; Prasad and Singh, 1981), Thomisidae. However, egg parasitoids often Pakistan (Alam and Wadud, 1963), Hawaii have a significant effect. In north Queensland, (Nishida and Holdaway, 1945) and Australia the egg parasitoids, Ooencyrtus sp., Anastatus (Pinese, 1981; Waite, 1986). It does not occur in sp. and Gryon sp. account for 30–60% of the litchis in South Africa, Israel, Canary Islands, eggs of A. l. lutescens (Fay and Huwer, 1993). In Mauritius, Madagascar and Réunion. south Queensland, Anastatus sp. and Gryon Female mites lay eggs singly on the leaf meridianum have been found to parasitize eggs surface among the erineum induced by their of A. nitida and A. l. lutescens to a similar extent feeding. The eggs are small (0.032 mm in (Waite and Petzl, 1997). diameter), spherical and translucent. They hatch in 3–4 days, producing a slow-moving MONITORING AND CONTROL In most crops protonymph. This stage is followed by two attacked by fruitspotting bugs, the insects further nymphal stages or deutonymphs themselves are extremely difficult to detect, (Plate 86). The adult stage is reached about being well camouflaged because of their colour 13 days after oviposition (Alam and Wadud, and having good sensory perception, which 1963) and 13–15 overlapping generations enables them to quickly escape predation. In are produced each year in India and China litchis and longans, where the fruit is borne on (Prasad and Singh, 1981; Zhang, Z., 1997). The the outside of the tree, the bugs can be easily mites are minute, being 0.13 mm in length and seen. However, reliance on finding the bugs to pinkish white in colour. All stages possess determine when to spray is often misleading, only four legs. However, they are quite mobile particularly if monitoring is carried out irreg- and are able to move easily from old infested ularly. Because damaged fruit fall to the leaves to the new leaves of fresh growth

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flushes, where their feeding stimulates the on leaves as a result of feeding by eriophyiids production of the erineum among which they is discussed by Westphal and Manson (1996). shelter and feed. Population abundance follows the flushing activity of the trees, with DAMAGE The mites attack the new growth, numbers booming during the summer flush, causing a felt-like erineum to be produced on and moderating during winter when lower the leaflets. This may form as small blisters, temperatures slow both tree growth and mite but if the infestation is severe, it may reproduction. Alam (1959) claimed a reduc- eventually cover the entire leaflet, causing it to tion in activity during the rainy season in Paki- curl. Whole terminals may be deformed. The stan, while Thakur and Sharma (1990) found erineum is at first silver-white, changing as it that maximum mite numbers were correlated ages to light brown and then dark reddish with maximum temperatures, wind velocity brown (Nishida and Holdaway, 1945). Very and sunshine during May, in Bihar, India. old erinose is almost black. Maximum popu- Trees may be infested with erinose mites lations are present in light brown, verging from the time they are planted out if they have on dark brown, erinose, and Nishida and been produced as marcots from infested par- Holdaway (1945), quoting Misra (1912), state ent trees. Otherwise, for infestation to occur, that mites are not present after the erinose has the mites must move directly between touch- turned dark brown. This is only partly true, ing trees (Prasad and Singh, 1981) or be either and some mites do remain there until a new physically transported from tree to tree by vegetative flush is produced, unless seasonal human activity or other agents, or carried conditions or tree health prevent that. In such on the wind (Wen et al., 1991). While wind cases the infestation may die out before new transport may be the most common method of leaves become available for colonization (G.K. movement, they may be transported between Waite, 1990, unpublished; Wen et al., 1991). trees via honeybees at flowering (Waite and Many leaves may fall if infestations McAlpine, 1992; Waite, 1999). become very severe. While established trees The cause of the development of erineum can tolerate substantial infestations without as a result of feeding by A. litchii has been detriment to their growth, that of young trees questioned by Somchoudhury et al. (1989) may be restricted. At flowering, if leaves and Sharma (1991), who proposed that the immediately below a flower panicle are erineum does not arise from stimulated leaf infested, that panicle will also be affected, cells, but is in fact formed by the thalli of the with attack on the florets preventing fruit alga, Cephaleuros viriscens Kunze, with the alga set or producing malformed fruit (Plate 87). and mite sharing a symbiotic relationship. Even after fruit has set and has developed to On the basis of this, Somchoudhury et al. half the final size, the mites can colonize it, (1989) proposed a name change for A. litchii to producing erinose on the skin that detracts ‘litchi algal mite’. Saha et al. (1996) studied from its appearance, and which may make it the symptoms associated with the presence of unmarketable as a quality product. C. virescens and A. litchii at a fundamental leaf level and agreed that the alga was involved BIOLOGICAL CONTROL Numerous species of in the production of erinose. While C. virescens mite have been recorded in association with commonly grows on litchi trunks, branches A. litchii. Not all have been proven to be and leaves, where it may be a problem in its predators. In India, Lall and Rahman (1975) own right, it is doubtful whether it is responsi- reported that Phytoseius intermedius Evans ble for the erinose associated with A. litchii, and Macfarlane, Phytoseius sp., Typhlodromus since chemical applications that kill the mites fleschneri Chant and Cunaxa setirostris were allow new foliage to develop without erinose found in association with A. litchii. Som- symptoms (Waite and Elder, 1996; Gupta et al., choudhury et al. (1987) added a further six 1997). In addition, erinose symptoms are not species, namely Amblyseius largoensis Muma, present on litchis grown in countries that have Amblyseius syzygii, Amblyseius herbicolus never recorded the mite, but where the alga is (Chant), Typhlodromus sonprayagenis, Typhlo- present. The development of erinea and galls dromus homalii, and Agistemus sp. Thakur and

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Sharma (1989) added Amblyseius coccineae Agistemus exsertus Gonzalez (Stigmaei- Gupta, Amblyseius finlandicus Oudemans, dae), has been used to control A. litchii in Amblyseius purni Gupta, and Amblyseius Guangdong, Guangxi and Fujian Provinces paraaerialis Muma. in China (Ren and Tian, 2000). In east Pakistan (Bangladesh), Alam and Wadud (1963) claimed that along with MONITORING AND CONTROL Trees should be an unidentified species of predatory mite, monitored specifically for erinose mite inci- two different spider mites of the genus dence on a monthly schedule. Additionally, Tetranychus preyed on A. litchii. This constant vigilance during the conduct of rou- observation was surely erroneous! tine orchard operations will assist in the early Wu et al. (1991) recorded the phytoseiid detection of mite infestations. mites found on litchis in China and the predator guilds associated with A. litchii Mechanical. During the non-fruiting in Australia and China were compared by period, particularly during postharvest prun- Waite and Gerson (1994). They found that ing, infested branches should be cut off and nine phytoseiid mites, Amblyseius herbicolus burned (Anonymous, 1978; Wen et al., 1991; (Chant), Amblyseius largoensis (Muma), Zhang, Z., 1997). Amblyseius barkeri (Hughes), Amblyseius nambourensis Schicha, Amblyseius neomarkwelli Chemical. The critical time for treatment Schicha, Phytoseius hawaiiensis Prasad, with chemical sprays is when the trees are Phytoseius rubiginosae Schicha, Okisieus about to flush (Pinese, 1981; Waite, 1992a; morenoi Schicha and Typhlodromus haramotoi Waite and Elder, 1996). Monitoring for the Prasad, and six other mite species belonging presence of erinose mite on litchi trees is to five families (Anystidae, Ascidae, simply a matter of carrying out regular inspec- Cheyletidae, Cunaxidae and Stigmaeidae), tions of the foliage to detect erinose symptoms were associated with litchi erinose mite around the time the trees are expected to flush, in Queensland. A cecidomyiid fly larva, although not all the trees in an orchard will do Arthrocnodax sp., was also a common preda- so at the same time. The mites themselves are tor. The limited census carried out in China virtually invisible to the naked eye. However, over a shorter period recorded nine to determine whether leaves carrying erinose phytoseiid species – Amblyseius eharai Amitai are active, they should be picked and left to and Swirski, A. herbicolus, A. largoensis, desiccate overnight. As the leaves dry, the Amblyseius ovalis (Evans), Amblyseius mites move to the surface of the erinose where cantonensis Schicha, Amblyseius okinawanus they are easily visible the next morning with Ehara, P. hawaiiensis, Phytoseius fujianensis the aid of a hand lens or microscope. Popula- Wu and Okisieus subtropicus Ehara. On advice tions in excess of 100,000 per leaflet have been provided by entomologists at the Guangdong assessed using this method in association Entomological Institute that A. eharai was with a washing and centrifuge technique the most effective predator of A. litchii,it (Waite, 1992a). In Queensland, three sprays was imported into Australia in 1993 for of dimethoate or wettable sulphur, applied host specificity testing. The mite was never at 2–3 week intervals during terminal released following a general natural reduction emergence and leaf expansion, protect the in the severity of erinose mite infestations in new flush from infestation by mites migrating commercial orchards around that time. This upwards from infested leaves below. If this coincided with the promotion of an integrated operation is carried out during the post- approach to controlling the complex of litchi harvest flush, the mite population on the tree pests, and an increased awareness by farmers will be minimal when the flower panicles of the need to reduce toxic pesticide applica- emerge. If infested leaves remain below the tions for pests such as fruitspotting bugs and emerging flower panicle, a similar series of the macadamia nut borer (G.K. Waite, 2001, chemical applications should be made to unpublished). prevent mites moving up and damaging the

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flowers and fruit. Sprays applied at times which often prevails during the February– other than flushing often give poor control April period in Thailand. Similar symptoms because of the protection provided to the occur on longans in China where a dif- mites by the erineum in which they shelter. ferent mite and a phytoplasma have been In India, Prasad and Bagle (1981) found implicated. that dicofol gave the best control of litchi erinose mite, but that monocrotophos, carba- BIOLOGICAL CONTROL No natural enemies ryl, cyhexatin and chlordimeform also per- are recorded for the mite, but it is assumed formed satisfactorily. Sharma and Rahman that there is a suite of predatory mites associ- (1982) confirmed that dicofol gave good con- ated with it, similar to that found in associa- trol, but dimethoate also provided acceptable tion with the litchi erinose mite in Queensland results. Sprays of wettable sulphur have been and China (Waite and Gerson, 1994). recommended for the control of erinose mite in Australia (Waite, 1992b), China (Anony- MONITORING AND CONTROL A monitoring mous, 1978), Hawaii (Nishida and Holdaway, procedure similar to that recommended for 1945), and Taiwan (Wen et al., 1991). Other litchi erinose mite should be undertaken chemicals recommended for use in China and severely infested branches removed include dichlorvos, dimethoate (Anonymous, and destroyed. Wettable sulphur should be 1978), dicofol, chlorpyrifos, omethoate and applied according to the flushing activity of isocarbophos (Zhang, Z., 1997). the trees.

Longan erinose mite (Acari: Eriophyidae) Longan gall mite (Acari: Eriophyidae)

DISTRIBUTION AND BIOLOGY The longan DISTRIBUTION AND BIOLOGY The longan gall erinose mite, Aceria longana Boczek and mite, Aceria dimocarpi (Kuang), is associated Knihinicki, is recorded as a sporadic but with longans in China where it is recorded major pest of longans in Thailand (Chai-ai as causing erineum on leaves (Kuang, 1997) and Visitpanich, 1997). A. longana is specific and also witches’ broom symptoms (He et al., to longan, severely affecting the terminals 2000). and flowers. The mite is microscopic, creamy white, and lives among the erineum produced DAMAGE Witches’ broom symptoms have on the leaves, similar to A. litchii,orinthe been reported from the provinces of Fujian, terminal buds. Boczek and Knihinicki (1998) Guangxi, Guangdong and Hainan as well describe this species as being very similar to as from Taiwan, though the cause of these A. dimocarpi. symptoms has only recently been attributed to A. dimocarpi by He et al. (2000). As well DAMAGE Mites feeding on the growing as relating mite presence to witches’ broom points and flowers cause malformation and symptoms they were able to reduce the stunting of these plant parts and severely incidence of those symptoms in affected infested trees may stop growing. Leaves may orchards through a combination of pruning exhibit curling due to erinose development, and the application of miticides. Others claim and damage to buds produces a witches’ that the symptoms are caused by a phyto- broom effect. There appears to be some plasma infection that can be transmitted by uncertainty as to whether the witches’ broom litchi stink bug and longan psylla and via is always caused by the mite, or whether a dodder weed (Cuscuta tempestris) and in bud phytoplasma is also involved, in which case it wood (Chen et al., 2000). Typically, infested is suggested that the mites may be vectors young leaves fail to expand, and roll up, and of the disease (S. Dolsopon, Thailand, 1999, shoots form compact clusters. Inflorescences personal communication). Increased activity are malformed and flowers fail to produce of the mite is noticed during hot, dry weather fruit.

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BIOLOGICAL CONTROL Natural enemies of parathion can be distributed on the ground the mite have not been recorded but it under the tree, or isofenphos (0.001%) can would be expected that predatory mites be sprayed on the ground just prior to the would be associated with infestations in expected emergence of the adult flies. In unsprayed situations. autumn, isocarbophos (0.001%) should be sprayed twice over a period of 14 days during MONITORING AND CONTROL Longan trees the leaf flush (Zhang, Z., 1997). should be inspected regularly and when witches’ broom symptoms are found, an appropriate miticide should be applied. In Fruit flies (Diptera: Tephritidae) Guangdong, the application of a mixture of omethoate, dicofol and colloidal sulphur DISTRIBUTION AND BIOLOGY Ceratitis capitata reduced the incidence of affected shoots by up (Weidemann) and Ceratitis (Pterandrus) rosa to 92% (He et al., 2000). Karsch are recorded from litchi orchards in South Africa and Réunion and C. capitata, Bactrocera dorsalis Hendel and Bactrocera Gall flies (Diptera: Cecidomyidae) cucurbitae (Coquillett) from Hawaii. In Queensland, Bactrocera tryoni (Froggatt) is DISTRIBUTION AND BIOLOGY The litchi leaf occasionally found attacking litchis. midge, Dasyneura sp., is regarded as one of Female fruit flies lay their eggs through the major pests of litchi in China (Zhang, Z., the skin of the litchi fruit, often utilizing cracks 1997). Litchiomyia chinensis Yang and Luo was and wounds made by other pests (Vayssieres, described from specimens reared from galls 1997). Although the eggs may hatch, the collected on litchi leaves in Guangdong (Yang larvae rarely survive (De Villiers, 1990a, and Luo, 1999). The larvae of the midges over- 1992b; Vayssieres, 1997) probably because of winter in the galls that form on the leaves as a the amount of juice present in mature litchis, result of their feeding. They pupate in the soil which drowns the larvae. and the adult flies emerging in March/April, initiate the first of seven to eight overlapping DAMAGE All of the above-mentioned spe- generations for the year. The midge prefer cies are capable of ovipositing through the trees that have dense foliage and where the skin of litchis, although in some cultivars the environment is damp. thickness of the skin may prevent successful oviposition. Only in South Africa do fruit flies DAMAGE The adult midge lays its eggs, appear to be regarded as a problem in litchis, often in lines, on young leaves. When the despite the relatively low damage levels larvae hatch they mine in the leaf, causing recorded. C. rosa is thought to be responsible ‘watery dots’ which, as they grow, become for most of this damage (Grové et al., 1999a,b). galls. The galls turn brown and eventually The physical damage thus caused, as well as drop out, giving the leaf a ‘shot-hole’ appear- some damage inflicted on the flesh by early ance and reducing the area of photosynthetic larval instars, allows the development of tissue. microorganisms that ferment and rot the fruit (De Villiers, 1992b). Most often, the presence BIOLOGICAL CONTROL No natural enemies of fruit fly eggs and the occasional larva in are mentioned in the literature. litchi fruit can be attributed to oviposition through prior damage. MONITORING AND CONTROL In susceptible orchards, monitoring is not an option and BIOLOGICAL CONTROL Numerous parasit- preventive procedures are adopted. As with oids, especially Opius spp. and Biosteres spp., the litchi erinose mite, infested leaves can have been recorded attacking the fruit fly be removed after harvest, and destroyed. species that damage litchis. Despite the activ- Later in the spring, 75 kg ha−1 of 2.5% methyl ity of such parasitoids, fruit flies continue to

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flourish and they often require chemical mango, mulberry and pomegranate as well as control in susceptible crops. litchi. Eggs are laid in April/May and the caterpillars are fully grown by December. MONITORING AND CONTROL In South Africa, Pupation is delayed until March/April and the use of pheromone-baited traps is recom- the insect has one generation per year (Butani, mended for monitoring fruit fly populations 1977). Lepidarbela dea Swinhoe attacks litchi around litchi orchards. Control is achieved trees in Guangdong. Trials over large areas of with bait sprays of protein hydrolysate mixed orchard showed that the application of the with trichlorfon or mercaptothion. Alterna- entomopathogenic nematode, S. carpocapse, tively, fruit panicles may be protected with gave an average of 94.3% control of the pest paper bags applied just after the November (Xu and Xie, 1997). fruit drop (De Villiers, 1988). Grové et al. (1999c) found that quarantine cold treatment DAMAGE The larvae of all species feed on was effective in preventing survival of C. rosa the bark and bore in the wood. If bark damage in litchi fruit. In other countries, no specific extends right around branches, they are ring- action is recommended because the problem barked and die. The wounds may also allow is not serious and is not recognized as a quar- infection by fungi, which can cause dieback. antine risk. In Queensland, insecticide sprays applied for the control of the macadamia nut BIOLOGICAL CONTROL Two unidentified borer help to suppress fruit fly populations in parasitoids have been recorded from the the orchard. pupae of Salagena sp. and they are considered to assist in the suppression of the pest.

MONITORING AND CONTROL During routine Bark borers (Lepidoptera: Metarbelidae) orchard operations, the frass-covered webbing associated with the workings of the bor- DISTRIBUTION AND BIOLOGY The dark-brown, ers can be seen on the branches. Unspecified slightly hairy larvae of Salagena sp. feed on insecticide applications applied to areas of the bark and wood of litchi trees in the north- activity, denoted by a covering of fresh frass, eastern Transvaal and Natal south coast areas are effective against Salagena sp. (De Villiers, in South Africa. The cream-coloured eggs, 1983a). In India, it was recommended that the which are laid on the bark of the tree, take a frass and webbing be cleared away and the few weeks to hatch. On hatching, the larvae holes plugged with cotton wool soaked in bore into the wood, forming tunnels up to petrol, chloroform, formalin, etc. These chem- 70 mm long and 5 mm in diameter, usually icals were considered to be too expensive, and in the crotches of branches. They cover the Shah (1946) proposed the use of hot water feeding site with a mass of frass which is injected by syringe. Later, Khurana and Gupta held together by webbing. Pupation occurs in (1972) suggested using dichlorvos, trichlorfon the tunnel and moths emerge from November and endosulfan in the same way. to January. The pest also attacks pecan, macadamia, guava, avocado, lavender tree (Heteropyxis natalensis), marula (Sclerocarya birrae), wild fig (Ficus spp.), bush willow Fruit borers (Lepidoptera: Lycaenidae) (Conbretum zeyheri and C. collinum), wild plum (Pappea capensis) and water berry (Syzygium Deudorix spp. are recorded as minor pests of cordatum) (De Villiers, 1983a). litchis and longans in India (Deudorix epijarbas In India, Indarbela quadrinotata Walker Moore), China, Thailand (Deudorix epijarbas and Indarbela tetraonis Moore are also amatius) and Australia (Deudorix epijarbas polyphagous, attacking trees such as aonla diovis Hewitson). The adults are pretty, (Emblica officinalis), ber (Zizyphus spp.), citrus, grey-blue moths with black, orange and falsa (Grewia asiatica), guava, jack fruit, loquat, white markings and filamentous tails on the

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hindwings. Single eggs are laid on the fruit damages the bark of litchi trees. The larvae and the larva bores inside, completely are protected by a double layer of webbing destroying the flesh and seed. Unlike that incorporates the larval faeces, making Cryptophlebia spp., whose larvae usually chemical control very difficult. Entomopatho- attack only one fruit, Deudorix larvae move genic nematodes provided variable levels from fruit to fruit, damaging three or four of control. Application during rainy spring in the process. A neat round hole is chewed weather was most effective (Xu et al., in the skin of the fruit and the larva plugs 2000). this with its flattened rear end, as it feeds inside. The larvae also apparently produce a substance attractive to ants, since these Mealybugs (Homoptera: Pseudococcidae) insects can often be seen in attendance. In Queensland, longans are more severely The citrus mealybug, Planococcus citri (Risso), attacked than litchis. is widely distributed throughout the world on numerous hosts. It sporadically attacks litchis in Taiwan where it may contribute to Leaf feeders (Lepidoptera: Saturniidae) the production of sooty mould.

The larvae of Gonimbrasia belina Westwood, commonly known as mopane worms, were Thrips (Thysanoptera) recorded defoliating litchis in South Africa by van den Berg (1995). It completed two generations in a year and was attacked by In India, Dolichothrips indicus Hood and four egg parasitoids and one tachinid larval Megalurothrips distalis Karny, were reported parasitoid. Rather than applying an insecti- by Ananthakrishnan (1971) to have attacked cidal spray to control the pest, it was recom- the flowers and leaves of litchi respectively. mended that larvae be removed by hand and The damage caused by these species was destroyed, or used as a food source. not quantified, but phosphamidon and dimethoate were recommended for their control (Butani, 1977). The tea yellow thrips, Scirtothrips dorsalis Branch borers (Lepidoptera: Cossidae) Hood, infests litchis and longans in China. All life stages feed on the shoots, causing The coffee leopard moth, Zeuzera coffeae malformation of the leaves in the new flush. Nietner, has two generations a year in main- The crimped, yellowish leaves have a mosaic land China and Taiwan. Eggs are laid in appearance, and eventually lose their sheen groups of 20–30 in crevices in the bark of and may fall. The thrips are most numerous litchis and longans. On hatching, the larvae from August to October, especially when bore into the branches, which may be killed. seasonal conditions are dry. Sprays of They pupate just below the surface of the isocarbophos, omethoate or dimethoate are bark, and the empty pupal case remains recommended to control the pest, along extruding from the exit hole when the moth with orchard management procedures that emerges. The pest is of minor importance, encourage uniform flushing (Zhang, Z., 1997). mainly in abandoned orchards. The plague thrips, Thrips imaginis Bagnall, often infests litchi flowers in Queensland. As its name implies, it may be present in extra- Bark borers (Lepidoptera: Yponomeutidae) ordinary numbers and it appears to feed on the litchi florets. However, experimental data Comoritis albicapilla Moriuti is a new pest have indicated that the insect has little, if any, in Guangdong Province, China, where it effect on fruit set (Waite, 1992a).

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Mites (Acari: Tetranychidae fruitspotting bugs, Amblypelta spp., in this and Tarsonemidae) respect (Waite, 1992a). The damage symptoms are characteristic and easily distin- The tea red spider mite, Oligonychus coffeae guished from those of Amblypelta spp. in that (Nietner) (Tetranychidae), occasionally infests Leptocoris spp. leave only a ‘pin-prick’ on the litchi leaves in Queensland, but is never a seed compared to the extensive lesion pro- problem. duced by the former. These bugs are generally In Queensland, Polyphagotarsonemus latus controlled by sprays applied for the control of (Banks) (Tarsonemidae), may occasionally fruitspotting bugs, but if necessary, specific damage individual terminals on orchard sprays of endosulfan may be applied, based trees. However, it is most often seen on on monitoring and damage assessment nursery trees where it can be easily controlled carried out by dissecting fallen green fruit. with sprays of dicofol, sulphur or endosulfan.

Pollination Beetles (Coleoptera: Bostrychidae and Scolytidae) Du Toit and Swart (1995) concluded that litchi has a limited ability for self-pollination Vayssieres (1997) discussed the occurrence of and that insect pollination of litchi flowers several species of boring beetles in litchis in seems to be necessary to ensure optimum Réunion. The species involved were not iden- fruit set in the crop. In India, 16 species tified. The bostrychids were all secondary of bees, flies, wasps and other insects were invaders of dead branches, but the scolytids recorded visiting litchi flowers by Singh were suspected of being able to attack live and Chopra (1998). Most common were the wood. honeybees, Apis cerana Fabricius, Apis dorsata Fabricius, Apis mellifera Linnaeus and Apis florea Fabricius, and the syrphid flies Bugs (Hemiptera: Miridae, Melanostoma univittatum Wiedemann and Lygaeidae, Rhopalidae) Episyrphus balteatus (De Geer). Pollination by these insects resulted in a 387% increase in Five species of mirid bugs were found infest- fruit set and a 505% increase in fruit retention. ing litchi in Réunion, but no damage could Of the bees, A. dorsata has been considered be attributed to their presence (Vayssieres, the most important, although A. mellifera is 1997). also a regular visitor to litchi flowers and In Queensland, the Rutherglen bug, most likely has a significant impact on polli- Nysius vinitor Bergroth, invades many crops nation (Abrol, 1999; Kitroo and Abrol, 1996; during spring in some years. The bugs migrate Kumar et al., 1996). In Thailand, A. mellifera is from the weed hosts on which they breed preferred as a large-scale producer of honey as these dry off. Litchis are often infested at and for the pollination of longans, while flowering or early fruit set, but the true pest A. cerana is preferred for small-scale honey status of the bugs is uncertain, despite 74% production and the pollination of litchis, of fallen fruit up to 15 mm long having been rambutans and mangoes (Wongsiri and fed upon by N. vinitor in an outbreak year. Chen, 1995). Trigona iridipennis Smith may Much of this fruit may have fallen regardless also contribute to pollination in both longans of being damaged, since it coincided with the and litchis in Thailand and India (Boonithee annual natural fruit thinning (Waite, 1992a). et al., 1991; Kumar et al., 1996). Eardley and The rhopalids, Leptocoris rufomarginata Mansell (1996) concluded that of 38 insect (Fabricius) and Leptocoris tagalica Burm., infest species visiting litchi flowers near Ofcolaco litchi trees in Queensland on a sporadic basis. in South Africa, most were ineffectual as They have been shown to cause green fruit to pollinators and that honeybees and several fall, and may sometimes be as important as the species of indigenous bees such as Plebeina

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denoiti (Vachal), Meliponula erythra junodi strong belief in the concept of biological (Friese), Ctenoceratina moerenhouti (Vachal), control combined with sound orchard man- Ctenoceratina rufigaster (Cockerell) and agement practices, especially the pruning Braunsapis facialis (Gerstaecker) contribute out of infested branches or leaves, as the significantly to litchi pollination. In contrast, basis for the IPM system. In addition, many litchis at Tzaneen were visited mostly by studies have been conducted on the effect of honeybees and very few other insects. orchard floor management on pest incidence. When litchi flowers are bagged to deny As well as providing a suitable habitat access to pollinating insects, fruit set is for natural enemies of some pests, suitable reduced. In India, Kumar et al. (1996) recorded ground cover may also provide beneficial an average of 1.4 fruits on panicles when effects through modification of the orchard insects were excluded, 8.9 on panicles caged environment (Liang and Huang, 1994; Liu with A. mellifera and 14.9 on panicles with free and Tan, 1999). During the years when access to pollinators. An average of six fruits farm communes existed, such management per panicle were set in South Africa when systems were widely used. However, since honeybees were allowed free access to flowers the demise of the communes and the wider compared with two per panicle when panicles availability of more effective insecticides and were bagged (Du Toit, 1994). spray application equipment, adherence to the more environmentally friendly approach has waned. Integrated Pest Management (IPM) Zhang, Z. (1997) has divided the year in Litchis and Longans into phenological stages so that the currently recommended management strategies can be implemented as the various growth character- As with all crops, the ultimate aim in the istics, which favour particular pest activity, protection of the litchi and longan crops develop. A disease management system is from insect pests is to implement a viable also included. Although various biological integrated pest management (IPM) system. controls are detailed in the preamble, the This system will have been developed for commercial recommendations, listed below, each country’s growing regions, accounting do not include them: for the variation in geography and latitude that determines the timing of different phen- 1. Winter flushing period – suppression of ological processes in the trees, and the local leaf flushes at this time of the year not only insect and mite fauna. promotes flowering, but also suppresses some The tactics adopted against each pest of the insect and mite pests which overwinter depend on how well they fit in with the overall there. management strategy for an orchard. Some 2. Spring flush/flower panicle production pests may be effectively controlled by natural period – a spray of trichlorfon for the control enemies, and the options considered for the of litchi stink bug and suppression of erinose control of other pests must always take into mite and leaf gall midge, in combination account the possible side effects on these, with chlorbenside for downy blight disease, is and the possible induction of pest problems applied at this time. Two sprays of the latter caused by the injudicious use of insecticides. chemical may be required during prolonged It should be noted, however, that when a rainy periods at flowering. damaging pest infests the crop, it should 3. Fruitlet period – the pest targets are be controlled, but with consideration of the stem-end borer and litchi stink bug, which are impact of the chosen method on the rest of the controlled with a mixture of cypermethrin or orchard ecosystem. chlorpyrifos plus trichlorfon. Ridomil-MZ® or In China, where litchis have been culti- Sandofan® may be applied for downy blight vated for thousands of years, the need to control. control pests to produce quality fruit has been 4. Maturing fruit period (varies according well recognized over the years. There is a to the cultivar) – targets are stem-end borer

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and downy blight. Further sprays of the above introduction of tebufenozide promises the pesticides are applied at the relevant times. opportunity for better control of this pest, with 5. Autumn flush period – to protect this fewer sprays and less disuption to the natural flush from stem-end borer, erinose mite, leaf enemy complex. midge and various lepidopterous caterpillars, The complex of pests attacking litchis two sprays, 10–15 days apart, of isocarbophos and longans throughout the world invariably or acephate are recommended. includes at least one species of fruit borer. In the absence of completely effective natural Presumably, releases of Anastatus sp. enemies of these pests, some chemical applica- could be substituted for the stink bug sprays, tions will remain a necessary part of the IPM provided they are correctly timed and inte- systems implemented for each region. These grated with the stem-end borer sprays. will generally be the key determinants not The use of A. japonicus in combination only of the eventual fruit yield and its quality, with O. phongi has been adopted in Thailand, but also of the viability of the whole IPM where the bug is very well controlled on litchis system. and longans by mass releases of these egg parasitoids at flowering. If neceassary, carbaryl can be applied at fruit set to control excessive numbers of nymphs if egg parasitism Acknowledgements has been poor. The subsequent control of C. sinensis using permethrin has no effect on Dr J.F. Vayssieres, Département des produc- the biological control, since the oviposition tions fruitières et horticoles, CIRAD-FLHOR, period for the bugs, and hence the critical pro- Réunion; Dr M. Van den Berg, Citrus and tection period for the parasitoids, has passed Subtropical Fruits Research Institute, Nel- by the time the small fruit become susceptible spruit, South Africa; and Supatra Dolsopon, to the borer. In Thailand also, pruning to Chiang Rai Research Centre, Chiang Rai, remove infested leaves and fruit, and to Thailand. restrict tree size so that necessary sprays can be applied effectively, is recommended. Fruit bagging, while it may not always give perfect References pest control, provides the bonus of enhanced fruit colour in both litchi and longan. Abrol, D.P. (1999) Pollination importance value of Waite (1992a) detailed the procedure that bees. Insect Environment 5, 140–141. should be adopted for implementing IPM Alam, M.Z. and Wadud, M.A. (1963) On the biology in Queensland litchis. Basically, this system of litchi mite, Aceria litchii Keifer (Eriophyidae: follows the phenological cycle of the trees and Acarina) in east Pakistan. Pakistan Journal of by monitoring at least once monthly during Science 18, 232–240. Alam, Z. (1959) On the biology and control of litchi autumn/winter and weekly during the mite, Aceria sp. (Eriophyidae: Acarina) in east flower/fruit production period in spring Pakistan. Scientist Pakistan 3, 13–18. and summer, the more important pests can Ananthakrishnan, T.N. (1971) Thrips (Thysanop- be detected and timely controls applied. In tera) in agriculture, horticulture and forestry this way, conservation biological control is – diagnosis, bionomics and control. Journal of employed for pests such as the soft scales Scientific and Industrial Research 30, 113–146. and erinose mite, although the latter may still Anonymous (1976) Report of investigations on require occasional chemical control. Leaf- natural enemies of Cryptophlebia ombrodelta eating loopers are tolerated until excessive (Lower) (Lep.: Tortricidae) in India. Common- foliage is consumed and Bacillus thuringiensis wealth Institute of Entomology Special Report, Indian Station, Bangalore, 16 pp. (Bt) applied if necessary. In the past, carbaryl Anonymous (1978) Lychee pest and disease control. has been applied up to five times or In: Academy of Guangdong Agricultural azinphos-methyl up to three times during Science (eds) Monograph of Guangdong Lychee. the fruit maturation phase, to control the Guangdong Science and Technology Press, macadamia nut borer. The imminent pp. 119–146 (in Chinese).

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arthropod communities in china. Agriculture, Prasad, V.G. and Singh, R.K. (1981) Prevalence and Ecosystems and Environment 50, 29–37. control of litchi mite, Aceria litchii Keifer in Liu, D.G. and Tan, B.L. (1999) Studies on the Bihar. Indian Journal of Entomology 43, 67–75. parasitoid community in a complex litchi Puttaruddriah, M. and Channa Basavanna, G.P. orchard. Natural Enemies of Insects 21, 134–139 (1959) A preliminary account of polyphagous (in Chinese). mites of Mysore. In: Proceedings of the First Liu, X.D. and Lai, C.Q. (1998) Experiment of control All India Congress on Zoology, Bangalore, Vol. 2, of litchi stink bug by using Anastatus japonicus 530–539. Ashmead. South China Fruits 27, 31. Quilici, S. (1996) Enquête sur les ravageurs et Liu, Y.F. and Gu, D.X. (1998) Control of litchi auxiliaires sur litchi à la Réunion. Réport stink bug by egg parasitoids. Chinese Journal au Département des Productions Fruitières et of Biological Control 14, 145–147 (in Chinese). Horticoles, CIRAD-FLHOR, Ile de la Réunion, Liu, Z.C., Wang, Z.Y., Sun, Y.R., Liu, J.F. and Yang, 13 pp. W.H. (1988) Studies on culturing Anastatus sp. Quilici, S., Verbizier, B., Trahais, B. and Manikom, R. a parasitoid of litchi stink bug, with artificial (1988) Note sur les ravageurs du litchi à la host eggs. Colloques de l’INRA No. 43, 353–360. Réunion. Fruits 43, 459–464. Menzel, C.M. (1983) The control of floral initiation Ren, S. and Tian, M. (2000) Litchi pests and their in lychee: a review. Scientia Horticulturae 21, natural enemies. 1st International Symposium on 201–215. Litchi and Longan. Guangzhou China. Abstract Menzel, C.M. and Simpson, D.R. (1990) Perfor- No. E-02. mance and improvement of lychee cultivars: Rogers, D.J. and Blair, A.D. (1981) Assessment a review. Plant Varieties Journal 44, 197–215. of insect damage to litchi fruit in northern Menzel, C.M. and Simpson, D.R. (1995) Tempera- Queensland. Queensland Journal of Agricultural tures above 20°C reduce flowering in lychee and Animal Sciences 38, 191–194. (Litchi chinensis Sonn.). Journal of Horticultural Saha, K., Somchoudhury, A.K. and Sarkar, P.K. Science 70, 981–987. (1996) Structure and ecology of Cephaleuros Misra, C.S. (1912) Litchi leaf curl. Agricultural Journal virescens Kunze and its relationship with Aceria of India 7, 286–293. litchii Keifer (Prostigmata: Acari) in forming Namba, R. (1957) Cryptophlebia illepida (Butler) litchi erineum. Journal of Mycopathological (Lepidoptera: Eucosmidae) and other insect Research 34, 159–171. pests of the macadamia nut in Hawaii. Proceed- Sahoo, A.K. and Maiti, B. (1992) Control of ings of the Hawaiian Entomological Society XVI, litchi leaf roller. Environment and Ecology 10, 285–297. 553–554. Nanta, P. (1992) In: Biological Control of Insect Pests. Sands, D. (1996) Natural enemies and prospects Biological Control Branch, Entomology and for biological control of fruit piercing moth. Zoology Division, Department of Agriculture, In: Welch, T. and Ferguson, J. (eds) Proceedings Bangkok, Thailand, 206 pp. (in Thai). of the Fourth National Lychee Seminar Including Newton, P.J. and Crause, C. (1990) Oviposition Longans, Yeppoon, Queensland. Australian on Litchi chinensis by Cryptophlebia species Lychee Growers’ Association, pp. 110–117. (Lepidoptera: Tortricidae). Phytophylactica 22, Sands, D.P.A and Brancatini, V.A. (1995) Country 365–367. Report – Australia. Proceedings of the Workshop Newton, P.J. and Odendaal, W.J. (1990) Commercial on Fruit Piercing Moths. CSIRO Division of inundative releases of Trichogrammatoidea cryp- Entomology, Long Pocket Laboratories, tophlebiae (Hym.: Trichogrammatidae) against Brisbane, Australia, pp. 47–48. Cryptophlebia leucotreta (Lep.: Tortricidae) in Sands, D.P.A. and Schotz, M. (1989) Advances in citrus. Entomophaga 35, 545–556. research on fruit piercing moths of subtropical Nishida, T. and Holdaway, F.G. (1945) The erinose Australia. In: Batten, D. (ed.) Proceedings of the mite of lychee. Hawaii Agriculture Experiment Fourth Australasian Conference on Tree and Nut Station Circular No. 48. Crops. Lismore, New South Wales, Australia, Partridge, I. (1997) Tropical fruit becomes major pp. 378–383. industry. Rural Research 174, 9–12. Sands, D.P.A. and Schotz, M. (1991) Ecology of Pinese, B. (1981) Erinose mite – a serious litchi pest. fruit piercing moths in subtropical Australia. Queensland Agricultural Journal 107, 79–81. In: Magallona, E.D. (ed.) Proceedings of the Prasad, V.G. and Bagle, B.G. (1981) Evaluation of 11th International Congress of Plant Protection. acaricides for the control of litchi mite, Aceria Manila, Philippines, pp. 229–232. litchii Keifer (Acarina: Eriophyidae). Pesticides Shah, R. (1946) An effective and inexpensive method 1, 22–23. for the control of stem borers in fruit trees with

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special reference to santra trees in C.P. and Thakur, A.P. and Sharma, D.D. (1989) New records Berar. Current Science, Bangalore 15, 135. of predatory mites on mite pests of economic Sharma, D.D. (1983) New record of predatory mites crops in Bihar. Biojournal 1, 155–156. on litchi mite (Aceria litchii Keifer) in Bihar. Thakur, A.P. and Sharma, D.D. (1990) Influence FAO Plant Protection Bulletin 31, 36. of weather factors and predators on the popu- Sharma, D.D. (1991) Occurrence of Cephaleuros lations of Aceria litchii Keifer. Indian Journal of virescens, a new record of leaf-curl in litchi Plant Protection 18, 109–112. (Litchi chinensis). Indian Journal of Agricultural Unahawutti, C. (1990) Insect pests of fruit trees. Sciences 61, 446–448. In: Proceedings of the Fifth Workshop on Insect Sharma, D.D. and Agrawal, M.L. (1988) Studies on Pests and Their Control. Entomology and the biology and immature stages of litchi Zoology Division, Department of Agriculture, fruit borer Conopomorpha cramerella (Snellen) Bangkok, Thailand, 121 pp. (in Thai). (Lepidoptera: Gracillariidae). Journal of van den Berg, M.A. (1995) Life history of the Research, Rajendra Agricultural University 6, mopane emperor moth Gonimbrasia belina 84–87. (Lepidoptera: Saturniidae). Inligtingsbulletin Sharma, D.D. and Rahman, M.F. (1982) Control of Instituut Tropiese en Subtropiese Gewasse litchi mite Aceria litchii (Keifer) with particular No. 270, pp. 10–12 (in Afrikaans). reference to evaluation of pre-bloom and post- Vayssieres, J.F. (1997) Enquête sur les arthropodes bloom application of insecticides. Entomon 7, ravageurs et auxiliaires du litchi à la Réunion. 55–56. Réport au Département des Productions Fruitières Sinclair, E.R. (1979) Parasites of Cryptophlebia et Horticoles. CIRAD-FLHOR, Ile de la Réunion, ombrodelta (Lower) (Lepidoptera: Tortricidae) 40 pp. in Southeast Queensland. Journal of the Waite, G.K. (1986) Pests of lychees in Australia. Australian Entomological Society 18, 329–335. In: Menzel, C.M. and Greer, G.N. (eds) The Singh, H. (1975) Acrocercops cramerella Snell Potential of Lychee in Australia. Proceedings of (Gracillariidae: Lepidoptera) as a pest of litchi the First National Seminar. Sunshine Plantation, in Uttar Pradesh and its control. Indian Journal Nambour, Queensland, Australia, pp. 41–50. of Horticulture 32, 152–153. Waite, G.K. (1988) Biological control of latania scale Singh, R. and Chopra, S.K. (1998) Flower visitors on avocados. Queensland Journal of Agricultural of litchi (Litchi chinensis Sonn.) and their role and Animal Sciences 45, 165–167. in pollination and fruit production. Pest Waite, G.K. (1990) Amblypelta spp. and green fruit Management and Economic Zoology 6, 1–5. drop in lychees. Tropical Pest Management 36, Somchoudhury, A.K., Sarkar, P.K., Singh, P. and 353–355. Mukherjee, A.B. (1987) Bioefficacy of some Waite, G.K. (1992a) Pest Management in Lychees. Final pesticides against Aceria litchii (Keifer) (Acari: Report, DAQ 81A, Australian Rural Industries Eriophyidae). First National Seminar on Agri- Research and Development Corporation, cultural Acarology, Kalyani, 48 pp. Canberra, Australia, 42 pp. Somchoudhury, A.K., Singh, P. and Mukherjee, A.B. Waite, G.K. (1992b) Integrated pest management in (1989) Interrelationship between Aceria litchii lychee. In: Fullelove, G.D. (ed.) Proceedings of (Acari: Eriophyidae) and Cephaleuros virescens, the Third National Lychee Seminar, Bundaberg, a parasitic alga in the formation of erineum- Queensland, Australia, pp. 39–43. like structure on litchi leaf. In: Basavanna, Waite, G.K. (1999) New evidence further incrimi- G.P. and Viraktamath, C.A. (eds) Progress in nates honey-bees as vectors of lychee erinose Acarology 2, 147–152. mite Aceria litchii (Acari: Eriophyidae). Experi- Storey, R.I. and Rogers, D.J. (1980) Lepidopterous mental and Applied Acarology 23, 145–147. pests of the litchi in north Queensland. Queens- Waite, G.K. and Elder, R.J. (1996) Lychee/longan land Journal of Agricultural and Animal Sciences insect pests and their control. In: Welch, T. 37, 207–212. and Ferguson, J. (eds) Proceedings of the Fourth Swirski, E., Ben-Dov, Y. and Wysoki, M. (1997) 3.3.5 National Lychee Seminar Including Longans. Guava. In: Ben-Dov, Y. and Hodgson, C.J. (eds) Yeppoon, Queensland. Australian Lychee Soft Scale Insects – Their Biology, Natural Enemies Growers’ Association, pp. 102–109. and Control (7B), pp. 255–263. Waite, G.K. and Gerson, U. (1994) The predator Tan, S., Wei, J. and Lan, R. (1998) Analysis of the guild associated with Aceria litchii (Acari: similarity of the structure of the litchi and Eriophyidae) in Australia and China. longan pest communities. Guanxi Science Entomophaga 39, 275–280. and Technology of Tropical Crops 69, 4–10 Waite, G.K. and Huwer, R.K. (1998) Host plants and (in Chinese). their role in the ecology of the fruitspotting

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bugs Amblypelta nitida Stål and Amblypelta (Ashmead) and the results of its continuous lutescens lutescens (Distant) (Hemiptera: rearing in vitro. Natural Enemies of Insects 11, Coreidae). Australian Journal of Entomology 37, 61–64 (in Chinese). 340–349. Xu, J.L. and Xie, R.C. (1997) Mass application of Waite, G.K. and McAlpine, J.D. (1992) Honey bees as entomogenous nematode against litchi stem carriers of lychee erinose mite Eriophyes litchii borer. Acta Phytophylactica Sinica 24, 150–154 (Acari: Eriophyidae). Experimental and Applied (in Chinese). Acarology 15, 299–302. Xu, J.L., Han, R.H., Liy, X.L., Cao, L. and Yang, P. Waite, G.K. and Petzl, N. (1997) A search for egg (1995) The application of codling moth nema- parasites of Amblypelta spp. (Hemiptera: tode against the larvae of the litchi longicorn Coreidae) in south-east Queensland. In: beetle. Acta Phytophylactica Sinica 22, 12–16 (in Menzel, C. and Crosswell, A. (eds) Maroochy Chinese). Research Station Report No. 7, pp. 13–14. Xu, J.L., Yang, P. and Xie, R.C. (2000) Studies on the Waite, G.K. and Pinese, B. (1989) Pests. In: Broadley, applications of some entomopathogenic nema- R.H. (ed.) Avocado Pests and Disorders. Queens- todes against litchi yponomeutid Comoritis land Department of Primary Industries, albicapilla Moriuti. Acta Phytophylactica Sinica Brisbane, Australia, pp. 8–24. 27, 27–31 (in Chinese). Wen, H.C., Lee, H.S. and Lin, C.C. (1991) Field Yang, C.K. and Luo, Q.H. (1999) A new genus and studies on litchi erineum mite (Eriophyes litchii species of gall midge (Diptera: Cecidomyiidae) Keifer) in southern Taiwan. Journal of Agri- infesting litchi from China. Entomotaxonomia cultural Research China 40, 298–304 (in Chinese). 21, 129–132 (in Chinese). Westphal, E. and Manson, D.C.M. (1996) Feeding Yao, Zheng-Wei and Liu, Siu-King (1990) Two effects on host plants: gall formation and other gracillariid insect pests attacking litchi and distortions. In: Lindquist, E.E., Sabelis, M.W. longan. Acta Entomologica Sinica 33, 207–211 and Bruin, J. (eds) Eriophyoid mites – Their (in Chinese). Biology, Natural Enemies and Control. Elsevier Zhang, D.P. (1997) A study of the pericarp of litchi Science, Amsterdam, pp. 231–242. fruit and the injury caused by litchi stinkbug, Wongsiri, S. and Chen, P. (1995) The effects of Tessaritoma papillosa (Hem.: Pentatomidae). agricultural development on honey bees in Wuyu Science Journal 13, 198–303. Thailand. Bee World 76, 3–5. Zhang, Z. (ed.) (1997) Litchi Pictorial Narration Wu, W.N., Lan, W.M. and Liu, Y.H. (1991) of Cultivation. Pomology Research Institute, Phytoseiid mites on litchis in China and their Guangdong Academy of Agricultural application. Natural Enemies of Insects 13, 82–91 Sciences, 189 pp. (in Chinese). Zhou, Z.H. and Xian, X.Y. (1994) Investigation on Xin, J.C. and Li, L.Y. (1989) Observation on the the morphology and parasitism of Ooencyrtus oviposition behaviour of Anastatus japonicus sp. Plant Protection 20, 41–42 (in Chinese).

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12 Passion Fruit

Elen L. Aguiar-Menezes,1 Euripedes B. Menezes,2 Paulo Cesar R. Cassino2 and Marco A. Soares2 1Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa de Agrobiologia, BR 465, Km 7, Caixa Postal 74505, Seropedica, RJ 23890-000 Brazil; 2Universidade Federal Rural do Rio de Janeiro, Centro Integrado de Manejo de Pragas ‘Cincinnato Rory Gonçalves’, BR 465, Km 7, Seropedica, RJ 23890-000 Brazil

Introduction important Passifloraceae, such as Passiflora ligularis Juss. (granadilla) and P. quadrangularis Passion fruits belong to Passiflora L. (family L. (badea, parcha granadina, tumbo) are culti- Passifloraceae) which has a wide genetic base. vated in Central America and in the Andean While some species are undomesticated, oth- regions of South America (Kluge, 1998). ers are cultivated as ornamental plants, for Commercial production of passion fruits nourishment and for medical purposes. The is currently increasing due to industrialization majority of Passiflora species are indigenous of the processed passion fruit products to the tropical and subtropical regions of (Akamine et al., 1954; Pires and São José, 1994). South America; Brazil is the centre of diver- Although the passion fruit crop has great eco- sity of the Passifloraceae (Cunha, 1996; Manica, nomic potential, its establishment and expan- 1997). Of the 400 known species of Passiflora, sion have been hindered by various problems. about 50 or 60 bear edible fruits. The majority For example, a wide host range of diseases, of these species are unknown outside their insects and mites attack passion fruit. Some centre of origin (Martin and Nakasone, 1994). pest species cause significant crop losses, A few species are economically important reaching the status of key pests or secondary e.g. Passiflora edulis botanical form flavicarpa, pests. Another limiting factor is the low sexual the yellow passion fruit, whose juice and self-compatibility. Increased fruit set depends pulp are used extensively as ingredients of on effective cross-pollination. Therefore, hand beverages, salads, fruit cocktails and desserts cross-pollination is the second most expensive (Donadio, 1983). Passiflora edulis f. flavicarpa production cost of passion fruit culture. Deneger, P. edulis Sims. (purple passion fruit) Knowledge of effective pollinating agents and P. alata Dryand (sweet passion fruit) are might be useful to secure maximum fruit the main species cultivated in the world. The production at lower cost. major producers of passion fruit are found in South America, mainly Brazil, Colombia, Peru and Ecuador (Ruggiero et al., 1996). Flowering and Fruit Setting Commercial plantations of passion fruit are also found in Australia, Hawaii, USA, The period of flowering of passion fruit India, New Guinea, Kenya, South Africa, Sri varies among species and among regions. For Lanka and Costa Rica (Kluge, 1998). Other example, in Hawaii, USA, the passion fruit

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flowers for 8–9 months a year with two but is unlikely to deposit it on the stigma. distinct periods of flowering and fruit setting. When the flower begins to close, the styles The first period of flowering occurs in late return to an upright position. The process of winter or early spring (April and May), and recurvature requires about 1 h. However, the the fruit matures in midsummer. The second styles of some flowers do not curve down- period of flowering occurs in late summer ward as much as others, and because there is (July and August), and the fruit matures in a greater distance between anther and stigma midwinter (Free, 1993). for a pollinator to bridge, they are less likely According to Akamine et al. (1954), there to be pollinated. This applies particularly is little or no overlapping of the functional to those flowers whose styles always remain periods of the flowers so that not much cross- upright, many of which are infertile as female ing takes place between the purple and yellow flowers (Akamine et al., 1954; Free, 1993). In types. In Hawaii, USA, and Brazil, the flowers Brazil, no fruit set is obtained on flowers of the purple passion fruit open early in of yellow passion fruit pollinated when their the morning, usually around dawn, and close styles are upright. On flowers with styles par- before noon. The flowers of the yellow passion tially curved and totally curved, 13% and 45% fruit open about noon and close about 2100 fruit set is obtained, respectively (Ruggiero or 2200 h (Akamine et al., 1954; Free, 1993; et al., 1976). Studies of Vasconcellos (1991) Teixeira, 1994). showed that the percentage of fruit set for In New South Wales, Australia, passion sweet passion fruit was 0, 44.19 and 73.47% fruit flowers start to open in the night or early on flowers with styles upright, partially morning and start to close at about midday curved and totally curved, respectively. the following day, but the stigmas are fully Under natural conditions, the stigma remains receptive on the morning of the first day only. receptive only on the day of flower opening, Anthers of the most flowers do not dehisce and the pollen loses its viability after 24 h until the afternoon (Cox, 1957). (Akamine and Girolami, 1959; Ruggiero et al., In Jaboticabal and Botucatu, SP (Brazil), 1976; Vasconcellos, 1991). the sweet passion fruit flowers for 12 months a The flowers of passion fruit are fragrant year with two flowering peaks, one in January when open. Nectar is secreted in a groove and February and the other in September at the base of the gynophore, and the pollen and October. Its flowers open at about is heavy and sticky. These features, in conjunc- 0400 to 0500 h and close at 1800 to 2000 h tion with the position of the anthers when the (Vasconcellos, 1991; Ruggiero et al., 1996). pollen is exposed and the functional position of the stigmas, indicate that flowers of passion fruit are adapted to pollination by insects rather than by wind. Wind is not important Characteristics of Passion Fruit Flowers in cross-pollination (Akamine et al., 1954; and Their Pollination Akamine and Girolami, 1959; Nishida, 1963; Semir and Brown, 1975; Free, 1993), and this Recent interest in commercial production of was confirmed in studies of caged plants passion fruit has prompted several studies that prevented access to insects; no fruit set on the pollination ecology. When the flowers occurred although plants flowered profusely first open, the stamens hang down, and the (Akamine and Girolami, 1957). anthers dehisce on the undersides, exposing Corbet and Willmer (1980) reported the pollen, the style remains erect, and there nectar sugar concentration of P. edulis f. flavi- is no stickiness on the stigmatic surfaces. carpa to be about 45–50%, which varies little Eventually, the erect styles curve downwards throughout the day. They calculated that the and outwards, and when the process is com- mean volume of the nectar chambers of yellow pleted, they are more likely to be touched passion fruit is 180 µl and that nectar secretion by insects collecting nectar and pollen. How- continues throughout the afternoon. The ever, for the first hour of flowering, a visiting hypothesis in this study is that in order to insect is likely to receive pollen on its body support large bee pollinators, nectar sugar

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concentrations will be low, and nectar pro- In the West Indies, the successful duction rates will be high. pollinators of passion flowers included three In Hawaii, the principal insects visiting species of hummingbird, and in higher passion fruit flowers include honeybee, numbers, Xylocopa mordax Smith (Corbet Apis mellifera L. (Apidae) and carpenter bee, and Willmer, 1980). While collecting nectar, X. Xylocopa varipuncta Patton (Anthophoridae) mordax moves around the flower while facing (Akamine et al., 1954). It is doubtful whether inward, often making at least one complete the honeybee is effective for pollinating the circuit. Only the tip of the galeae can be flowers because of its small size. However, inserted past the operculum at the mouth according to Hammer (1987), the foraging of the nectary and into the nectar groove. habits of honeybees, not their size, may cause Because of the depth of the nectar groove, at less than expected fruit set. The carpenter bee, least 13 µl of nectar remained inaccessible to on the other hand, is large enough so that, in the bees. The collected nectar load has about moving around the flower to obtain nectar, its 50–70 µl volume, and 45–49% sugar concen- body brushes along the anthers and stigmas, tration. Xylocopa mordax spends about 8.5 s transferring pollen from one organ to the per flower visit. On sunny days each flower other (Plate 88). received a mean of four visits in the morning Approximately, 700 species of bees and two in the afternoon; overcast conditions belong to Xylocopa Latreille (Anthophoridae). reduced the visits. Besides nectar, X. mordax They are found throughout the tropical regions collected pollen on the dorsum when in con- of the world (Hurd and Moure, 1963; Hurd, tact with the fully recurved stigmas in differ- 1978) with two generations and activity peaks ent passion fruit species (Free, 1993). Accord- during the periods of December to March and ing to Corbet and Willmer (1980), most yellow July to September (Camillo, 1978a; Camillo passion flower pollination by X. mordax occurs and Garófalo, 1982), coinciding with the flow- between 1330 and 1500 h (Fig. 12.1) when the ering peaks of the passion fruit. Pope (1935) stigmas have curved downward. The daily stated that carpenter bee, X. varipuncta, certain percentage of flowers pollinated ranged from moths and hummingbirds were large enough 25% on overcast days to 94% on bright sunny to transfer pollen from the stamens to the days. Flowers on lower branches were less stigmas of the passion flowers. Nishida (1958, likely to receive a visit by X. mordax and are 1963) reported insect species within Diptera, less likely to set fruit than flowers on higher Hymenoptera, Coleoptera, Thysanoptera and branches. Orthoptera visiting flowers of passion fruit In Brazil, Ruggiero et al. (1975, 1976) in Hawaii, with X. varipuncta and hover fly, observed that three species of Xylocopa and Eristalis arvorum (Syrphidae), being the most Africanized honeybees were the most abun- abundant species. Nishida (1958, 1963) stated dant pollinators of passion fruit, but the pol- that thrips and midges were too small to trans- linating efficiency of the honeybee was low fer the relatively large pollen grains of flowers compared with Xylocopa spp. (3% and 75% of passion fruit. set, respectively). Xylocopa bees were more The insects most commonly visiting efficient pollinating flowers whose styles were passion flowers in El Salvador are Bombus totally and partially curved and less efficient spp., Trigona spp., and Xylocopa spp. (Free, on rainy days. Camillo (1978b, 1980) also found 1993). In São Paulo (Brazil), the most common that Xylocopa suspecta Moure & Camargo is a species visiting passion fruit flowers are more effective pollinator of yellow passion Xylocopa spp., Epicharis spp. and Apis mellifera flowers than X. frontalis (Olivier) in Brazil. scutellata (Nishida, 1963; Ruggiero et al., 1976). The author cited other insects, i.e. Epicharis Akamine and Girolami (1959) noticed that rustica (Friese) (Anthophoridae), Bombus hover fly E. arvorum and long-horned grass- morio, B. atratus, Apis mellifera, Scaptotrigona hopper Conocephalus saltator (Tettigoniidae) postica, Geotrigona sp. (Apidae), and Oxaea feed on pollen of passion flowers, but consid- flavescens Klug (Oxaeidae) visiting flowers ered that their value as potential pollinators of yellow passion fruit. However, S. postica outweighed their potential pest status. and A. mellifera usually collect pollen while

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Fig. 12.1. Pollination of Passiflora edulis flavicarpa, yellow passion fruit. Changes throughout a day in the number of bee visits, number of flowers with at least one stigma curved downward to another level, and the number of pollinated flowers (those with pollen on at least one stigma) (after Corbet and Willmer, 1980).

E. rustica, B. morio, and O. flavescens collect Three carpenter bees, Xylocopa mordax nectar. Smith, X. scutellata Moure, and X. (Megaxy- Sazima and Sazima (1989) also reported locopa) fimbriata Fabricius, were the most that X. suspecta and X. frontalis were effective important pollinators of passion fruit in east pollinators of passion fruit in Ribeirão Preto, and southeast of Lake Maracaibo (Venezuela). SP (Brazil), but Trigona spinipes (Fabricius) Xylocopa nests were observed in wooden (Apidae) collected nectar and pollen without trellis supporting passion fruit plants. Most pollinating the flowers. When T. spinipes was flower visits occurred between 1500 and numerous, their visits depleted the flowers 1800 h (Dominguez-Gil and McPheron, 1992). of nectar, thereby diminishing foraging by Ways of facilitating pollination by Xylocopa. Moreover, Trigona attacked and Xylocopa have been advocated. Nishida (1958) repelled Xylocopa when the latter attempted to advised that either the area of passion fruit visit passion fruit flowers, resulting in 6–25% should not exceed the pollinating capacity fruit set reduction. The deleterious effect of of the insects present, or the number of Trigona colonies is likely to be more serious in pollinators on the crop should be increased. small plantations. Different ways to increase the population Hoffmann and Pereira (1996) found the of pollinators have been suggested (Nishida, following species of bees visiting flowers 1954; Akamine and Girolami, 1959; Cobert of yellow passion fruit in Campos dos and Willmer, 1980). The carpenter bee builds Goytacazes, RJ (Brazil): A. mellifera, Xylocopa its nest in wood or plant stems, and thus ordinaria, X. frontalis, Eulaema nigrita, and its presence as a pollinating agent can be E. cingulata (Apidae). Most flower pollination encouraged by placing wooden posts by Xylocopa bees occurred between 1400 and throughout the passion fruit plantation. The 1700 h. Species of Eulaema were observed only post may be redwood, kukui, or some other during the morning. suitable soft wood. Abundance of nesting In Malaysia, Mardan et al. (1991) observed sites might reduce time spent searching for that carpenter bee, Platynopoda latipes, was nests and diminish competition between the most important pollinator of passion fruit. adult females (Akamine et al., 1954; Free, They suggested that honeybees (Apis cerana 1993). Studies of Camillo and Garófalo (1982) and A. dorsata) were detrimental to fruit set by showed that eucalyptus was the wood removing pollen before effective pollination preferred by Xylocopa bees given a choice by P. latipes could occur. between nine types of wood. Hoffmann (1997)

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recommended the use of posts about 20 cm honeybees are plentiful, it has been observed diameter have been 60–70 cm length in which that they visit the flowers as soon as flowers two holes of 1.5 cm diameter have been made. have opened. The bees remove the pollen The first hole is longitudinal, 20 cm deep, and from the anthers and carry it back to the hive. the second one is perpendicular to the first at By the time the styles have moved into 15 cm high, allowing them to meet. The first position where their stigmas can be pollinated hole is closed by a woody piece or a cork, and by carpenter bees, the pollen may be entirely the second is used as the nest entrance. gone. Unless the carpenter bees have some Camillo (1996) increased the pollination pollen remaining on their bodies from early of passion fruit by introducing into planta- visits to the flowers, pollination is entirely tions Xylocopa spp. in Holambra, São Paulo precluded and fruit setting fails to occur. (Brazil). Before the placement of Xylocopa In Hawaii, Nishida (1958) found that in nests, the natural pollination resulted in 3.2% two localities, flowers bagged and pollinated fruit set. With the introduction of 49 nests by hand had about the same percentage set of X. frontalis and X. grisescens into 1.5 ha as unbagged flowers. However, in two other of passion fruit, the percentage of fruit set localities, bagged and hand pollinated flowers increased to 25%. had a greater fruit set, indicating that the local Carpenter bee populations can be insect pollinators were too few in these sites increased by providing seasonal spreads of (Fig. 12.2). His results also showed that the nectar and pollen sources, thereby reducing fruit set from cross-pollinating, bagged flow- competition with other nectar sources while ers varied from 50 to 100%, depending on the passion fruit is flowering (Akamine et al., locality. So the maximum fruit set in some 1954). In Brazil, Hibiscus spp., Cassia spp., localities was limited by factors other than Ipomoea purpurea, and Crotalaria juncea have pollinators. The percentage of fruit set from flowers that are very attractive to carpenter hand pollination and the difference in set bees (Ruggiero et al., 1996). between hand and natural pollination also Evaluation of the need to either increase varied within a season. Akamine and numbers of carpenter bees or perform hand Girolami (1959) reported that natural fruit set pollination is by counting the number of was less than that achieved by hand pollina- flowers dropped, because this may be caused tion. Corbet and Willmer (1980) confirmed by lack of fertilization, indicating low popula- that bagged flowers only set fruit following tion density of insect pollinators. To evaluate cross-pollination (mean of 77% fruit set). Fur- whether the pollinators occur in the crop at a thermore, manually cross-pollinating flowers suitable level, Ruggiero et al. (1996) recom- exposed to insect pollinators increased fruit mended that three opening flowers per plant set from 27 to 73%, indicating that natural should be labelled on a sunny day. For 2–3 ha, pollination was inadequate. this operation must be repeated with > 34 Nishida (1963) found that the abundance plants, labelling 100 flowers in total. If the area of honeybees on the crop and the proportion is greater, the quantity of labelled flowers of pollen gathered varied greatly from one should be increased proportionally. Four days month to the next and was probably associ- later, the fruit set on the labelled flowers is ated with the presence of competing sources counted. Of the 100 labelled flowers, Ruggiero of forage. He observed that sometimes honey- et al. (1996) observed that 40–50% developed bees were so abundant that nearly all pollen into fruit, meaning that the population density was removed soon after the flowers opened. of carpenter bees was adequate. However, A few honeybees were present on the crop values < 30% indicated there was a lack of when it was not flowering and in the morn- pollinators and, in this case, flowers must be ings before the flowers opened; these bees hand pollinated. were collecting from the extrafloral nectaries According to Akamine et al. (1954), on the leaf petioles. He found that when the Akamine and Girolami (1957, 1959), and density of honeybees present increased to a Nishida (1958), honeybees may actually cause certain level there was a tendency for the fruit unfruitfulness of passion fruit. In areas where set to decrease. However, there was a positive

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correlation between the increase in fruit set (1963) suggested that X. varipuncta is a and the increase in the population of X. more efficient pollinator than the honeybee, varipuncta that was present (Fig. 12.3). Nishida because it is larger, works faster and carries

Fig. 12.2. An experiment to determine the efficiency of natural pollination of Passiflora edulis, passion fruit, in three sites in each of four localities: A, flowers bagged; B, flowers bagged and hand pollinated; C, flowers not bagged nor hand pollinated (after Nishida, 1958).

Fig. 12.3. Relationship between the number of Xylocopa varipuncta, carpenter bees, in Passiflora edulis, passion fruit, fields and percentage of flowers pollinated (after Nishida, 1963).

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larger loads. Ruggiero et al. (1976) confirmed Table 12.1. Reciprocal crosses between this by experiments in which caged plants varieties of passion fruit, and the percentage of resulted in better fruit set when confined with fruit set following cross-pollination. (From Akamine Xylocopa spp. than with honeybees (75% and and Girolami, 1959.) 45% fruit set, respectively). Reciprocal No. flowers Percentage of On the other hand, Free (1993) suggested crosses pollinated fruit set that honeybees as pollinators are important because they forage in the lowlands and in the C 39 and C 37 258 92 humid uplands, and may be easily manipu- C 39 and C 77 250 97 C 39 and C 80 167 97 lated. Cox (1957) reported that honeybees are C 37 and C 77 83 2 abundant and effective pollinators of passion C 37 and C 80 106 2 fruit in Australia. In Florida, USA, where hon- C 77 and C 80 80 4 eybees are the sole pollinators of P. edulis,up to 25% of its flowers produce fruit (Hardin, 1986). pollinators. However, other hymenopterans As pointed out by Gilmartin (1958), it has (e.g. Apis, Bombus, Epicharis, Oxaea) and orth- not been determined that cross-pollination opterans, dipterans, etc., visit the flowers of between flowers of different clones or variet- passion fruit, and may pollinate, even though ies is necessary for maximum fruit setting. It is they may be less effective than Xylocopa. advisable to plant several selected varieties in Thus, as stated by Price (1997) studies of an orchard to enhance the possibility of cross- pollination ecology, co-evolution between pollination and to minimize crop losses which plant and pollinator, energetic relationships, might occur from planting with a variety demographics of plant and pollinator, repro- strain that proved to be highly self-incompati- ductive strategies, population dynamics and ble. Akamine and Girolami (1959) found that community ecology, are still warranted and any cross that involved variety ‘C 39’ (Table needed for Passifloraceae. 12.1) was compatible, but crosses between other varieties were nearly completely incom- patible. They suggested that plants of compat- Pests ible clones, which flower at the same time, should be distributed in the field to ensure the Although passion fruit is attacked by several maximum possibility of cross-pollination. pest species of insects and mites that feed upon all parts of the plant, a limited number of species are clearly of major economic Conclusions importance. Few have key pest status, while some species are secondary pests because Plants of the Passifloraceae depend on cross- they are sporadic or occur at low population pollination to set fruit because their flowers levels, and therefore do not require control present characteristics that make it difficult strategies. Insect and mite pests that are for self-pollination, such as presence of stig- frequently associated with passion fruit are mas above the level of the anthers and stigma described below, including their description, receptivity and low self-fertility. Thus, the life history, behaviour, hosts, damage and passion fruit depends largely on mutualistic control (Santo, 1931; Lordello, 1952b; Correa relationships, with insects as pollinators. In et al., 1977; ICA, 1987; Dominguez-Gil et al., fact, the flowers of passion fruit are large, 1989; Figueiro, 1995; Lima and Veiga, 1995). attractive, colourful, fragrant, and produce plentiful nectar and pollen that facilitate insect cross-pollination. Most of the studies Lepidopterous defoliators dealing with pollination of the Passifloraceae support the theory that carpenter bees, Three heliconiine species, Dione juno juno mainly Xylocopa spp., are the most effective Cramer, Agraulis vanillae vanillae Linnaeus,

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and Eueides isabella huebneri Ménétries full-grown larva is about 35–40 mm in length, (Nymphalidae), are the most common the dorsum has orange, blue and white stripes lepidopterans feeding upon foliage of and six longitudinal lines of branched black passion fruit (Dominguez-Gil and McPheron, spines (Plate 90). The larvae has five instars, 1992). Dione juno juno is the key pest of and lasts about 17 days (Lordello, 1952a). passion fruit in Brazil and causes severe The chrysalis is suspended by the cremaster, damage to the plants (De Bortoli and Busoli, which is usually attached to a branch of the 1987; Gravena, 1987). D. juno is distributed host plant. The chrysalis is about 25 mm in in the southern USA, the Antilles, Guyana, length, sharply angled, and creamy white and Surinam, French Guiana, Trinidad, and from lasts about 7 days. Colombia to Argentina (Toledo, 1991), while Two-thirds of the forewing of Eueides A. vanillae occurs in South America and isabella huebneri is dark brown, almost black, over a large part of the southeastern USA with irregular yellow spots, and one-third is (Carter, 1992). Eueides isabella is found in orange with black stripes. The hindwings are Venezuela and south of Brazil (Silva et al., orange with black borders and a central stripe. 1968; Brown Júnior and Mielke, 1972; The wingspan is 70–80 mm. Females oviposit Dominguez-Gil and McPheron, 1992; Boiça single eggs on leaves or stems. The eggs Júnior et al., 1993). are whitish yellow when recently laid, and are darker close to hatching, which occurs DESCRIPTION AND LIFE HISTORY Adults of D. 4–7 days after oviposition. The newly hatched juno have orange wings with black borders larva is 1–3 mm long, white with black head and venation. The wingspan is about 60 mm. and body hairs. The full-grown larva is 30 mm Eggs are laid in groups of 40–70 on the leaf long. The dorsal surface of its body is black underside, near the border. The 0.9 × 0.6 mm with transversal narrow white stripes, and egg is light yellow when first laid, and darkens the dorsal surface of the eighth and ninth just before hatching. Eggs hatch in 6–7 days. abdominal segments is orange. The larvae The larvae pass through four or five instars, require five instars. The chrysalis has spines requiring 19–27 days to reach full growth. on the thorax and abdomen, differing from the When fully grown, the larva is about other heliconiines. 29–35 mm in length, 3–5 mm in width, dark brown, with small yellow spots, and covered HOST PLANTS Caterpillars of D. juno feed with black setae arranged in rows. The larvae on all Passiflora species, except P. foetida are gregarious and, when disturbed, raise (Echeverri et al., 1991; Carter, 1992). According their head and thorax, and stand on their to Boiça Júnior et al. (1993), P. alata, P. setacea pseudolegs. The chrysalis is suspended by and the hybrid P. alata × P. macrocarpa are the cremaster, is obtect, cream in colour, more resistant to attack by D. juno than and about 16–25 mm in length. The pupal P. edulis, P. cincinnata, P. caerulea and the stage requires 7–9 days (D´Almeida, 1944; hybrid P. edulis × P. alata. Lordello, 1954; Silva, 1979; Chacón and Rojas, 1984; De Bortoli and Busoli, 1987; Toledo, INJURY The three species of heliconiine 1991; Dominguez-Gil and McPheron, 1992; defoliators reduce leaf area, thereby indirectly Dominguez-Gil, 1998). reducing yield. Dione juno usually causes The A. vanillae butterfly has red-orange damage that is more serious because of its wings, with black markings and venation, gregarious behaviour (Fancelli and Mesquita, and silver spots on the underside (Plate 89). 1998). During the first instar, the caterpillars Wingspan varies from 60 to 75 mm (Carter, scrape the leaf epidermis of young leaves, 1992). The female lays eggs singly on leaves or leaving small holes in the leaves, while older stems. The eggs are light yellow when recently larvae devour both young and older leaves oviposited, spindle shaped, and about 1 mm (Lordello, 1954; Chacón and Rojas, 1984). in length. The eggs hatch in 3 days (Lordello, Besides defoliation, the caterpillars may 1952a). The newly hatched larva, approxi- feed on the apical buds, flowers or stems mately 3 mm long, is creamy white. The (De Bortoli and Busoli, 1987).

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NATURAL ENEMIES Several predators and regular intervals until the crop is harvested. In parasitoids have been reported from these passion fruit it is very important to protect heliconiids. However, these natural enemies pollinating insects by timing insecticidal treat- are not considered to be effective. For instance, ments when pollinators are not present in the Silva et al. (1968) reported Alcaeorrynchus field. Choosing an insecticide that is selective grandis (Dallas) and Apateticus mellipes for the pest and less toxic to pollinators, preda- Bergroth (Pentatomidae) as predators of tors and parasitoids is important in these D. juno. In Argentina, A. vanillae was recorded agroecosystems. Bacillus thuringiensis (Bt) to be parasitized by Pteromalus caridei Berliner, which effectively controls a variety Brèthes (Pteromalidae). Silva (1979) reported of caterpillars and has little or no effect on Spilochalcis spp. (Chalcididae) parasitizing natural enemies, is commonly recommended. D. juno. In the state of Pernambuco (Brazil), Menezes et al. (1989) performed a laboratory Lima and Veiga (1995) found Spilochalcis experiment with different strains of Bt to con- spp., Polistes sp. (Vespidae), Paratrechina trol D. juno. Figueiro (1995) demonstrated that longicornis, Crematogaster sp., Pseudomyrmex suspensions of Baculovirus dione at concentra- gracilis (Formicidae), and Forcipomuia sp. tions of 10, 20, 40 and 80 g of larvae per 500 l of (Ceratopogonidae) as natural enemies of water, were highly pathogenic and efficient D. juno. Ruggiero et al. (1996) recorded the at controlling larvae of D. juno under labora- hymenopteran wasps, Polistes spp. and Polybia tory conditions. Studies of Moura et al. (2000) spp. (Vespidae), as predators of passion on selectivity of insecticides to vespid preda- fruit heliconiids in Brazil. In Lake Maracaibo tors of D. juno, showed that the deltamethrin (Venezuela), Dominguez-Gil and McPheron was highly selective to Polybia scutellaris (1992) reared two specimens of Spilochalcis sp. and Polybia fastidiosuscula, and showed inter- from field-collected larvae and chrysalis of mediate selectivity to Protonectarina sylveirae. A. vanillae and E. isabella. Cartap was moderately selective to all Lima and Veiga (1993) verified the occur- three species of predatory wasps. Malathion rence of nuclear polyhedrosis virus (NPV) was selective to P. sylveirae and showed inter- infesting D. juno caterpillars in Pernambuco. mediate selectivity to P. fastidiosuscula. In Lake Maracaibo, larvae of D. juno were also infected by NPV. Once infected, larvae became sluggish, and their cuticles become discoloured and fragile. Chacón and Rojas Coreid bugs (1984) estimated that NPV kills 100% of the D. juno population in Colombia. A NPV Many species of bugs attack passion fruit and epizootic occasionally reduced populations of the majority belongs to the Coreidae (leaf- A. vanillae in plantations located east of Lake footed bugs). In passion fruit producing Maracaibo where NPV was very abundant areas, three main species of coreids are repor- during January and February for 3 consecu- ted: Diactor bilineatus Fabricius, Leptoglossus tive years (Dominguez-Gil et al., 1989). spp. and Holhymenia spp. D. bilineatus is the most common species, and is known as the CONTROL In small areas, cultural control passion fruit bug because it feeds only on during periodic crop inspection includes hand fruit of Passiflora spp. Among the Holhymenia, picking and destruction of eggs and cater- H. clavigera (Herbst.) and H. histrio (Fabricius) pillars (Rossetto et al., 1974). However, these are the most common species attacking methods require considerable time and labour passion fruit. The bugs Leptoglossus, L. and are often impractical for a large-scale cul- gonagra Fabricius and L. australis Fabricius, tivation. In this case, injurious populations of usually cause damage to passion fruit. defoliating caterpillars infesting passion fruit D. bilineatus is considered the most must be controlled with insecticidal sprays. important pest of passion fruit in Brazil Action thresholds have not been defined. by Mariconi (1952) and Fancelli and Growers spray the foliage, often starting Mesquita (1998). However, Dominguez-Gil with appearance of the pest, and continue at and McPheron (1992) consider that Diactor

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bilineatus Fabricius, Leptoglossus spp. and with black legs and antennae. The bugs pass Holhymenia spp. are the second most signifi- through five nymphal instars in about 55 cant phytophagous group of pests in passion days (Chiavegato, 1963, De Bortoli and Busoli, fruit plantations in the Lake Maracaibo region 1987). The adult passion vine bug, L. australis, (Venezuela). is elongate, approx. 20 mm in length, and dull black in colour with orange spots on the DESCRIPTION AND LIFE HISTORY Adults of D. underside of the body. In Hawaii, passion bilineatus are orange on the ventral face of the vine bugs migrate from surrounding scrub head, and the dorsal face is dark metallic green to infest passion fruit plantations. Neglect of with two orange longitudinal lines that vines may allow populations of the bug to continue on the prothoracic tergum and the build up. Feeding usually occurs on flowers or scutellum, both of which are dark metallic green-mature fruit. Nymphs often cluster on green. The hind legs have the tibia expanded fruit when feeding. Damage to mature fruit and leaf-like, dark green in colour with some is not pronounced; however, young fruit orange markings. Males are about 20 mm develops dimple-like surface blemishes at in length, and females, 21.5 mm. When the feeding sites (Murray, 1976). disturbed, they walk or make short flights, mainly in cold periods. A female lays a batch HOST PLANTS Silva et al. (1968) listed several of six to nine eggs on the underside of the species of Passiflora as being hosts of D. leaves. They are about 3 mm long, light yel- bilineatus. Mariconi (1952) verified that P. low, bright, elipsoid and flattened in the base. quadrangularis is seriously damaged by this The incubation period for eggs is 13–16 days. pest. Besides passion fruit, H. clavigera feed The nymphs, which pass through five instars, on guava (Fancelli and Mesquita, 1998). Silva require about 43–46 days to reach the adult et al. (1968) mentioned P. edulis as host of this stage (Mariconi, 1952). The first instar nymph species. L. gonagra feeds on a large number of has an orange head that turns dark blue in host plants, including passion fruit, chayote, the following instars. The thorax is orange, citrus, tobacco, guava, sunflower, cucumber, and a white stripe surrounds the femurs and grape, pomegranate, São Caetano melon tibiae. The hind legs are characterized by the (Cayaponia espelina), bixa (Bixa orellana), expanded leaf-shaped tibia. The abdomen araçazeiro (Psidium araca), and Anisosperma is orange with six pairs of lateral, dark passiflora (Chiavegato, 1963). blue expansions from the third to the eighth abdominal segments (Dominguez-Gil, 1998). NATURAL ENEMIES Silva et al. (1968) reported The adult body of Holhymenia spp. is that D. bilineatus eggs were parasitized by black with orange spots. The legs are reddish Hadronotus barbiellinii Lima (Scelionidae). orange. The head, the prothoracic tergum and Eggs of H. clavigera were reported to be the scutellum are black with white spots parasitized by Hexacladia smithii Ashmead (De Bortoli and Busoli, 1987; Brandão et al., (Encyrtidae) (Silva et al., 1968). 1991; Dominguez-Gil, 1998). The adult L. gonagra (Plate 91) is about INJURY Both immature and adult bugs 15–19 mm in length and dark brown in colour. injure the crop, piercing stems, leaves, fruits The head colour ranges from dark brown to and flowering buds, and sucking plant juices. almost black, with two yellow longitudinal However, the nymphs prefer to feed on flow- lines. The prothoracic tergum is brown with ering buds and young fruits, usually resulting a yellow transverse line. The antennae are in excessive dropping. The adults may also brown with the second, third and distal attack leaves, stems and fruits at any stage of two-thirds of the forth segments light yellow ripening. If larger fruits are fed upon, they wilt in colour. The hind tibiae are expanded and and show a wrinkled surface. Fruits may also leaf-like. The longevity of adults is about 37 develop dimple-like blemishes at the feeding days. Eggs are 1.4 mm in length, dark brown sites on the fruit surface (Murray, 1976). Lepto- with triangular cross-section. The eggs hatch glossus gonagra often causes misshaping or in 8 days. Newly hatched nymphs are reddish dropping of young fruits (Chiavegato, 1963).

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CONTROL In small passion fruit producing HOST PLANTS In Brazil, yellow passion fruit areas, hand picking and destruction of is susceptible to attack by Philonis spp. while eggs, nymphs and adults is recommended Passiflora alata, P. maliformis, P. serrato digitada (Mariconi, 1952). Chiavegato (1963) suggests and P. caerulea are not infested by this pest the removal of the alternative cucurbit host, (Oliveira and Busoli, 1983). Cruz et al. (1993) ‘São Caetano melon’, a preferred host of L. observed that yellow passion fruit is very sus- gonagra, or to avoid the cultivation of chayote ceptible to Philonis obesus attack, but P. alata and Anisosperma passiflora in adjacent areas as and P. giberti show some plant resistance. tactics to reduce pest densities. In southeast Queensland, Australia, regular inspections INJURY Larvae of Philonis spp. feed within are recommended during the summer months the stems, opening longitudinal galleries to detect any build-up of L. australis (Murray, inside stems that prevent plant development. 1976). The attacked stems are easily identified by the presence of excrement and sawdust (Santos and Costa, 1983). As the larva develops, infested stems become weak and frail, and Stem weevil die (Fancelli, 1992a). According to De Bortoli and Busoli (1987), the simultaneous attack of In Brazil, the stem weevil Philonis spp. (Cur- several larvae is characteristic of weevil infes- culionidae) was first reported in Alagoas in tations, which causes hypertrophy in stems 1972. Currently, the infestation has expanded where the pupal cell will be constructed to several states in Brazil (Warumbi and (Rossetto et al., 1978; Oliveira and Busoli, Veiga, 1978; Leão, 1980; Torres Filho and 1983; Racca Filho et al., 1993). Attack by Araújo, 1981; Oliveira and Busoli, 1983; Cruz the stem weevil also causes fruit drop before et al., 1993; Racca Filho et al., 1993; Boaretto maturation (Costa et al., 1979). et al., 1994). It is commonly found on borders of young plantations (Fancelli, 1992a). Severe CONTROL Periodic inspections of the crop outbreaks of this pest have caused the are essential for an early detection of weevil- eradication of 250 ha in Brazil (Rossetto et al., infested stems (Fancelli, 1992a). When infesta- 1978). Racca Filho et al. (1993) reported the tion symptoms are detected on the crop, occurrence of P. passiflorae O´Brien and P. affected stems should be pruned and burned obesus Champion in Rio de Janeiro. The spe- (De Bortoli and Busoli, 1987). According to cies that occurs in São Paulo was identified Leão (1980) and Costa et al. (1979), a contact as P. crucifer (Piza Júnior and Kavati, 1995). insecticide (e.g. decamethrin at 25% (5–10 g a.i. ha−1)) should be applied during early DESCRIPTION AND LIFE HISTORY Adults of P. afternoon hours for stem weevil control, at passiflorae are about 7 mm in length, brown the time of adult emergence. After 4–5 days, with whitish elytra with two brown stripes. systemic insecticides for control of future stem Adults of P. crucifer are 4 mm in length, brown infestations should be used. with black markings. They are nocturnal (Piza Júnior and Kavati, 1995). According to Santos and Costa (1983) and Boaretto et al. (1994), females lay eggs on young or old stems. The Flies eggs hatch in 8–9 days. The larvae are white and legless. The full-grown larva is about Some fly species feed upon the fruits of 8 mm long. The larval stage is 53–64 days, and Passiflora spp., and others attack flowering the pupal period is 14–35 days (Costa et al., buds. In Brazil, Lordello (1954), Santos and 1979). All stages of development of this Costa (1983) and Teixeira (1994) reported the species occur inside the stem. Pupae and following genera of flies damaging passion recently emerged adults are frequently found fruits: Anastrepha Schiner (Tephritidae) and in cocoons spun by the full-grown larva Lonchaea Fallén (Lonchaeidae). A. consobrina (De Bortoli and Busoli, 1987). (Loew), A. curitis Stone, A. dissimilis Stone,

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A. fraterculus (Wiedmann), A. kuhlmanni from puparia buried up to 2–5 cm deep in the Lima, A. lutzi Lima, A. pseudoparallela (Loew), soil, and crawl to the surface. They feed A. striata Schiner, and A. xanthochaeta Hendel on juice of ripening fruits (Plate 92) and are reported as being the most common on honeydew excreted by aphids, mealybugs, species associated with passion fruit in Brazil and soft scale insects. Females deposit their (Santos and Costa, 1983; Teixeira, 1994; eggs mainly in ripening fruit, depositing two Zucchi, 1988, 2000). Anastrepha pallidipennis to six eggs in the cavity beneath the skin. After Guerne was reported on yellow passion fruit 2 or 3 days, the whitish eggs hatch. The cream in Colombia (Chacón and Rojas, 1984). The coloured larvae bore into the fruit pulp and oriental fruit fly, Bactrocera dorsalis (Hendel), contaminate it with bacteria and fungi, melon fly, Bactrocera cucurbitae Coquillett, which cause the fruit to decay. Large fruits and the Mediterranean fruit fly, Ceratitis may contain as many as 100 larvae. Under capitata Wiedmann, are known to attack the favourable conditions, larvae complete devel- passion fruit vines in Hawaii, USA (Back and opment in about 9–13 days. They exit the Pemberton, 1918); however, the relative fruit while it is hanging on the tree or after importance of each species appears to vary it has fallen to the ground. In the tropical with respect to location of the vineyard areas, the pupae complete development in (Akamine et al., 1954). The Queensland fruit 10–14 days. In temperate areas, the pupae fly, Bactrocera tryoni (Froggatt), is the most complete development in 7–11 days during important insect pest of passion fruit in the summer, but in winter may remain Australia (Murray, 1976). dormant for several months. Flies of the Neosilba pendula (Bezzi) and Dasiops sp. genus Anastrepha produce a variable (Lonchaeidae) are the most common species number of generations depending on the attacking flowering buds of passion fruit inhabited region (Orlando and Sampaio, 1973; (Rossetto et al., 1974; Silva, 1982; Fancelli and Morgante, 1991). Mesquita, 1998). Dasiops sp. attacking flower- The adult of Bactrocera tryoni is wasp-like ing buds was reported in Rio de Janeiro, Brazil in appearance, about the size of a house fly, (Silva et al., 1968; Vasconcellos et al., 1995). The with transparent wings bearing a dark band species of Dasiops known to attack flowering on the front margin. Bright yellow patches buds or fruits of Passiflora spp. in the Americas interrupt the general reddish brown body are D. curubae Steykal, D. inedulis Steykal, and colour. The female lays several pale cream, D. passifloris McAlpine (Steyskal, 1980). elongate eggs beneath the skin surface of the Other flies may also feed upon flowering fruit. Creamy coloured maggots may emerge buds, such as Lonchaea cristula McAlpine from the eggs in 2 or 3 days and tunnel within (Lonchaeidae) and Zapriothrica salebrosa the fruit while feeding. During the warmer Wheeler (Drosophilidae) (Chacón and Rojas, weather the larval stage is completed in about 1984). Hernández et al. (1985) observed that L. 2 weeks. The mature larvae then leave the cristula is more common in curuba (Passiflora fruit to burrow into soil to pupariate for an molissima) when this crop is cultivated near additional 2 weeks, after which adults emerge areas where other host fruits grow. The larvae from puparia. Very few eggs laid in immature of these fly species destroy pollen by boring passion fruit produce adult flies. The develop- into anthers, and may cause intensive drop- ment of woody tissue around eggs in the rind ping of infested buds (Chacón and Rojas, of the fruit prevents some eggs from hatching, 1984). or when hatching occurs, causes high mortality of young larvae. Egg hatching in ripe fruit DESCRIPTION AND LIFE HISTORY Anastrepha is mostly unaffected since the fruit has ceased adults are 6.5–8.0 mm in length, predomina- growing and does not form the woody tissue tely yellow in colour, with brown and yellow around the eggs (Murray, 1976). In Queens- markings on the wings. The adult Medfly is a land (Australia), B. tryoni invades passion smaller colourful insect with yellow and black fruit vines from alternative host plants and is markings on the body and black and orange most active from September to April (Swaine markings on the wings. Adult flies emerge et al., 1985).

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The adult Dasiops curubae is blackish blue. secondary pest of several fruits, especially tan- The wings are hyaline and slightly smoky gerine (Rossetto et al., 1974). Dasiops curubae yellowish, while the calypters and wing damages flowers of curuba (P. mollissima) fringes are pale yellowish (Steyskal, 1980). (Steyskal, 1980; Causton, 1993). Dasiops The adult Dasiops inedulis is bright inedulis is reported in Panama to be a serious metallic dark blue with hyaline wings; the pest of purple granadilla, P. edulis (Steyskal, calypters and wing fringes are yellowish to 1980). This species has been implicated in nearly white (Steyskal, 1980). Peñaranda et al. 21–65% loss of flowering buds of passion fruit (1986) reported that the length of the life cycle in the Cauca Valley (Colombia) (Peñaranda of this species takes 22.8 days under labora- et al., 1986). Dasiops passifloris attacks fruits of tory conditions. The period of incubation P. suberosa (syn., P. pallida) (Steykal, 1980). requires 2–3 days; the larval stage, 4–9 days; and the pupal stage, 10–17 days (Peñaranda INJURY Fruit fly adult damage is caused by et al., 1986). oviposition in green fruits, causing disfigurat- Dasiops passifloris was described by ions of the fruit surface. The larvae damage McAlpine (1964), who recorded its distribu- the fruit by feeding on its pulp, contaminating tion in Florida. Adults are metallic blue- it with bacteria and fungi (Plate 93), and black, and females have a long ovipositor causing premature fruit drop (Medina et al., resembling those species in the Otitidae and 1980; Santos and Costa, 1983; Morgante, 1991). Tephritidae. They oviposit one to four eggs According to Akamine et al. (1954), the in the pulp of immature fruit. After hatching, oriental, melon, and Mediterranean fruit flies larvae bore through the immature fruit and puncture the fruit while the rind is still tender. feed on developing seeds. The maturing As the fruit enlarges, a woody area (callus) larvae then begin feeding on the fruit pulp develops around the puncture. If the fruit is immediately beneath the skin. In about small and undeveloped, the damage may be 12 days the larvae mature and drop to the sufficient to cause it to shrivel and fall from the ground, where they pupariate within the soil plant. If the fruit is well developed, it may or possibly beneath some refuse. The pupal continue to maturity. At the time of ripening, stage lasts 14 days (Stegmaier, 1973). the area around the puncture has the appear- The adult Neosilba pendula is about 4 mm ance of a small, woody crater, which disfig- long, bright metallic dark blue, with hyaline ures the outer appearance of the fruit but does wings (Rossetto et al., 1974). not impair pulp quality. Although oviposition scars are present on ripening fruits, they HOST PLANTS The highly polyphagous Ana- generally do not contain living larvae. Larvae strepha spp. infest approximately 270 plant appear to be able to develop better in imma- species in 41 families, and are considered to be ture than in mature fruit. the major fruit pests of tropical and subtropi- Oviposition by B. tryoni in immature cal America. Passiflora has been reported as a green fruit also results in the formation of host of the larvae of two groups of Anastrepha calluses in the skin of the fruit at the puncture (chiclayae and pseudoparallela) (Norrbom and site. Punctured fruits may persist on the plant Kim, 1988; Stefani and Morgante, 1996). to maturity but are not acceptable for fresh Anastrepha chiclayae Greene has been found market sale because of the damage (May, 1953; associated with Passiflora spp. in Mexico Hargreaves, 1979). (Hernández-Ortiz, 1992). Larvae of A. limae According to Murray (1976), passion fruit Stone feed upon fruits of P. quadrangularis increase rapidly in size during the first 10–15 (Stone, 1942; Caraballo, 1981). Lordello (1954) days after fruit set. During this period the skin observed infestations by Anastrepha and of the fruit is turgid and easily punctured by Lonchaea species on Passiflora quadrangularis the ovipositor. Infested immature fruit shows and P. macrocarpa. The Medfly attacks 253 characteristic skin blemishes. The woody kinds of fruits, nuts, and vegetables; many of tissue, which forms around the eggs, develops which are tropical plants. Neosilba pendula is a hard raised area around the puncture mark. known as the key pest of cassava, and is a Egg laying or puncture often cause young

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fruit to shrivel and drop. Puncture marks are papaya, tomato, and other fruits in which difficult to detect on ripe fruit. A few days the flies breed and on which the adults feed. after larval infestation, mature fruit will show Santos and Costa (1983) recommended that wrinkling and breakdown. passion fruit must be planted far away from Anastrepha pseudoparallela lays eggs in coffee plantations and wild host plants that unripe fruits of P. alata, and the larvae develop grow adjacent to the passion fruit crop should by feeding on the seeds. Cyanogenic com- be removed. Fruit flies may be controlled pounds are present in all parts of Passiflora using bait sprays composed of molasses (7%) plants, including seeds of unripe fruits. These or protein hydrolysate (1%), and an insecti- glycosides protect the plant by preventing cide. The bait is sprayed over 1 m2 of the plant feeding by herbivore species. Thus, the use of canopy, using 100–200 ml of bait per plant these resources by A. pseudoparallela for larval (Santos and Costa, 1983). The bait should be breeding is probably associated with its ability applied during the night (Rossetto et al., 1974). to tolerate these chemical defences and sug- Boaretto et al. (1994) reported that bud flies gests a high degree of specialization (Stefani may be controlled by insecticide baits com- and Morgante, 1996). posed of fenthion, molasses and water. The The larvae of flies that attack the flower- bait is applied at the beginning of the flowering buds and immature fruits cause prema- ing peak, and usually three applications ture fruit drop (Brandão et al., 1991). Immature spaced at 8–10 days are necessary. The authors fruits infested by D. passifloris become dirty, also suggested burying the attacked buds and whitish green in colour, while infested ripe planting trap crops, such as sweet pepper. fruits become bluish white (Stegmaier, 1973). Dasiops inedulis larvae bore into the anthers, and the ovary, causing flowering bud drop (Peñaranda et al., 1986). Mites

NATURAL ENEMIES Most species of tephritid Several species of mites have been reported fruit flies are attacked by a complex of larval from passion fruit (Sanches, 1996). Brevipalpus parasitoids while egg and pupal parasitoids phoenicis (Geijskes) (Tenuipalpidae), the red are much less common (Bateman, 1972). spider mites Tetranychus mexicanus (McGregor) Doryctobracon Enderlein, Diachasmimorpha and T. desertorum Banks (Tetranychidae) are Viereck, Opius Wesmael, Psyttalia Walker and known to infest passion fruit plants. Warm Utetes Foerster (Braconidae) are the most com- temperature and low precipitation favour mon larval parasitoids of tephritid fruit flies development of these species (Haddad and (Wharton, 1996). Pachycrepoideus vindemiae Millán, 1975; Oliveira, 1987; Brandão et al., (Rondani) and Spalangia endius Walker (Ptero- 1991). On the other hand, Polyphagotarsonemus malidae) are pupal parasitoids of Medfly latus (Banks) (Tarsonemidae) prefers high (Back and Pemberton, 1918). In Colombia, temperatures and > 80% relative humidity Opius sp., Zelus rubidus (Reduviidae), and (Oliveira, 1987; Brandão et al., 1991). spiders of Thomisidae were reported as natural enemies of D. inedulis (Peñaranda DESCRIPTION AND LIFE HISTORY Brevipalpus et al., 1986). phoenicis mites are quite small, e.g. 0.3 mm in According to Silva et al. (1968), larvae of length, and pass through five stages in their N. pendula are parasitized by Alysia lonchaeae life cycle: egg, larva, protonymph, deutony- Lima, Ganaspis carvalhoi Dettmer, Tropideucoila mph, and adult. Adults are bright red, depos- weldi Lima (Cynipidae), and Opius sp. iting bright red, oval eggs of about 0.1 mm and preyed upon by Belonuchus rufipennis long, on the underside of leaves or in crevices (Fabricius) (Staphylinidae). on the stems (Swaine et al., 1985). The length of the cycle from egg to adult varies from as little CONTROL Akamine et al. (1954) argued that as 18 days (30°C) to as long as 49 days (20°C) one of the most important steps in controlling (Oliveira, 1987). In Queensland (Australia), fruit flies is the elimination of over-ripe the life cycle takes about 6 weeks. According

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to Flechtmann (1989), this mite develops on necrosis, culminating in leaf drop. Attacked both upper and lower leaf surface, but prefers young stems dry from the extremity to the lower leaf surface. Large numbers congre- the base and eventually die (Flechtmann, gate in leaf axils, along grooves in the terminal 1989). In Queensland, Australia, B. phoenicis shoots and leaf stalks, and along the main infestations are usually most damaging dur- veins of leaves (Swaine et al., 1985). Severely ing the summer and autumn. Heavy infesta- infested leaves are completely webbed by tion may result in defoliation (Swaine et al., spider mites (Oliveira, 1987). 1985). In Hawaii, B. papayensis, known as red Female spider mites are < 0.5 mm long, mite, is one of the most troublesome pests of and red. Males are slightly smaller than passion fruit, but it is usually most damaging females, and greenish yellow. The life cycle in areas of low rainfall and during prolonged of spider mites comprises five stages: egg, dry weather. Its effects are yellowing, shrivel- larva, protonymph, deutonymph, and adult. ling, and falling of the leaves. With heavy and The length of female and male life cycles is prolonged infestation, leaf fall increases and about 18 and 20 days, respectively (Oliveira, the vine has the appearance of dying back. At 1987). The period of incubation is 5–6 days. the same time, developing fruit may begin to The larva of T. mexicanus is light yellow with shrivel and fall prematurely from the plant. three pair of legs, and the larval stage requires Close examination reveals the presence of 4–7 days. Its protonymph is reddish yellow mites as scattered reddish patches on the with four legs and develops in 4–5 days. The surface of the fruit, particularly around the deutonymph completes its development in stem end, along the midrib and veins of the 2–4 days (Dominguez-Gil, 1998). leaf, especially on the under-surface. If red Polyphagotarsonemus latus females are spider mites are left uncontrolled, the plant about 0.2 mm in length. The body varies may eventually die (Akamine et al., 1954). in colour from white to yellowish. Males are Red spider mites cause a general weaken- smaller than females, and hyaline (Brandão ing of the plants. Initial damage to foliage et al., 1991). The entire cycle from egg to adult appears as fine silver speckling on the lower takes about 3–5 days. The species develops surface of the leaves, which turn brownish rapidly through four stages: egg, larva, pupa, on the upper side as mites continue to feed. If and adult. This mite attacks young leaves, and a large number of mites are present, entire its colonies are localized on the lower leaf leaves or plants turn yellow and necrotic surface (Oliveira, 1987). (Oliveira, 1987). Photosynthesis and trans- piration of the plants are suppressed. Dense HOST PLANTS A wide variety of host plants populations of spider mites produce silken are attacked by the mites. Brevipalpus phoenicis webs that cover the leaves. Heavy infestations feeds on citrus, coffee, cashew, papaya, cause leaves to drop and plants to lose vigour banana, guava, pomegranate, apple, loquat, (Oliveira, 1987). peach, pear, grape, grevillea, and various P. latus induces malformations in devel- weeds (Oliveira, 1987). Tetranychus desertorum oping leaves, which later dry and drop. It occurs on cotton, sweet potato, bean, papaya, may attack flowering buds, causing a reduc- passion fruit, strawberry, peach, tomato, tion in the number of flowers, and in turn, grape, and certain ornamentals. Tetranychus of fruits produced per plant (Oliveira, 1987; mexicanus feeds upon cotton, citrus, apple, Flechtmann, 1989). papaya, passion fruit, pear, peach, cacao, walnut, and ornamentals (Flechtmann, 1989). NATURAL ENEMIES Important natural ene- Hosts of P. latus are bean, potato, cotton, mies of spider mites are predacious mites coffee, citrus, apple, pumpkin, walnut, grape, belonging to Phytoseiidae. The life history of peach, pepper, rubber plantation, and various these predators is closely related to that of weeds (Oliveira, 1987). their host. Larvae and adults of Stethorus sp. (Coccinellidae) were also observed as preda- INJURY Brevipalpus phoenicis is responsible tors of T. mexicanus in passion fruit plantations for general discoloration of the leaves, and in Lake Maracaibo (Venezuela) when spider

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mites reached high population densities DESCRIPTION AND LIFE HISTORY The charac- (Dominguez-Gil and McPheron, 1992). teristic of Myzus is the presence on the head of tubercles at the base of the inner side of anten- CONTROL Periodic inspections of the nae. Because of this, the frons shows an outline orchard and other adjacent hosts, including that is scooped out in the middle. The apterous weeds, are essential to verify the occurrence form of M. persicae is 1.2–2.3 mm long, and fre- and first symptoms of mite attacks (Oliveira, quently pale green in colour, but populations 1987; Brandão et al., 1991). Mites have also also occur that are yellowish or tending to red- become resistant to many of the organophos- dish. The cornicles are long and cylindrical, phate miticides. Selective miticides, dosages, sometimes with a slight swelling of the distal timing, and refining application techniques part, which is often blackish. The cauda is may be useful in an integrated mite manage- subtriangular, shorter than the cornicles. The ment system. The four principal requirements length of the antennae is a little less than for a practical operation are: (i) presence of that of the body. The alate form is about predacious mites in the orchard; (ii) know- 1.2–2.2 mm in length and green in colour; ledge of the appearance and habits of plant- head, antennae and thorax are brown or feeding and predacious mites; (iii) careful blackish (Barbagallo et al., 1997). examination of relative numbers of predators The apterous form of the cotton aphid, and plant-feeding mites, particularly during a A. gossypii, has an ovoid body shape, and period when rapid population changes are is medium to small in size (1.0–1.8 mm in occurring; and (iv) knowledge of pesticides to length). Colour is variable, from ochreous use, how to use them, and what pesticides to brown to mottled, more or less dark green or avoid, in order to conserve predators. even bluish tinged. Antennae are brown with Flechtmann (1989) recommended the use the middle part cream coloured; cornicles and of sulphur that is not toxic to pollinating cauda are blackish brown. The alate form has insects. According to Piza Júnior (1992), head and thorax blackish, as are the antennae, fenthion, propargite, chlorfentezine, and cornicles and cauda; the abdomen has the avermectin are effective miticides. same variation in colour as does the apterous form. Length of body is 1.2–2.0 mm. The cotton aphid has a nearly cosmopolitan world Secondary Pests distribution. This species is of greater seriousness in warm-temperate regions and in the intertropical zone. It is typically anholocyclic, Secondary pests include various species remaining active during the whole year with of insects that may become abundant, and uninterrupted generations of parthenogenetic occasionally damage the passion fruit crop. females. However, there are recorded cases The insects in this group are either associated of the appearance of sexual forms, with the frequently with a particular environmental subsequent deposition of resistant eggs on condition, or else occur within limited various plants (Barbagallo et al., 1997). geographical areas. M. solanifolii is about 2.6–4.0 mm in length, green, with wax secretions on the body of immature forms (Barbagallo et al., 1997). Aphids HOST PLANTS Peach is the preferred primary Aphids (Aphidae) are known to attack host of M. persicae. It may infest other Prunus passion fruit vines, although they seldom species, in particular almond and plum. Its cause serious damage. Nevertheless, at least secondary host plants include numerous wild three species of aphids, Myzus persicae and cultivated plants, such as passion fruit (Sulzer), Aphis gossypii (Glover), and Macro- (Barbagallo et al., 1997). Aphis gossypii infests siphum solanifolii Ashmead (= M. euphorbiae numerous species of dicotyledonous plants, (Thomas)), must be regarded as potentially including passion fruit. Favoured hosts are important pests of passion fruit. in the Malvaceae (cotton, hibiscus, etc.) and

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Cucurbitaceae (pumpkin, cucumber, water- Fancelli, 1993). Peridroma saucia (Hübner) melon, melon) (Barbagallo et al., 1997). M. (Noctuidae) attacks the floral structure, and solanifolii is a very polyphagous species, show- may reduce fruit production (Chacón and ing preference for the Solanaceae, i.e. potato, Rojas, 1981). Pyrausta perelegans (Hampson) tomato, etc. (Barbagallo et al., 1997). (Pyralidae) is also associated with passion fruit flowers. In Colombia, this species is INJURY Although these aphids cause mal- one of the most important pests of curuba, formation in foliage, they are more important and may infest 70% of the crop. Caterpillars as disease vectors. Myzus persicae and A. of Aepytus (Pseudodalaca) serta (Schaus) gossypii transmit a virus disease that causes a (Hepialidae) and Odonna passiflorae Clarke disease associated with hardening of fruits (Oecophoridae) are passion fruit stem borers (Brandão et al., 1991; Piza Júnior and Resende, (Chacón and Rojas, 1984). 1993). Myzus persicae and M. solanifolii are vectors of the passion fruit woodiness virus in DESCRIPTION AND LIFE HISTORY Caterpillars Australia. In Hawaii, however, where these of A. penicillana lodge in flowering buds or in a two species are present, this virus does not nest made from leaves, which are joined by occur (Akamine et al., 1954). silk webs produced by the insect. The caterpillar is whitish, and when fully grown, NATURAL ENEMIES Naturally occurring pre- 25 mm long. The adult is a small pale greyish dators and parasites are effective against moth (Santos and Costa, 1983; Fancelli, 1992b; aphids. The Coccinellidae are effective against Fancelli, 1993). P. saucia is a moth with a cotton aphids, and in particular the larval 39 mm wingspan. Forewings are crimson red, stage of Scymnus. Other predators include the hindwings are whitish. Females lay their eggs Chrysopidae (Chrysoperla), Cecidomyiidae on the underside of leaves, usually in clusters (Aphidoletes) and Syrphidae (Syrphus). Para- of 60–244. Eggs are about 0.7 mm in diameter. sitism by Lysiphlebus sp. (Aphidiidae) has Eggs are creamy white when first laid, but been reported (Barbagallo et al., 1997). Accord- turn reddish blue when close to hatching, after ing to Grasswitz and Paine (1993), Lysiphlebus 8–10 days, depending on temperature. The testaceipes (Cresson) parasitizes Myzus, Aphis, newly hatched larva, approximately 0.97 mm and Macrosiphum. Silva et al. (1968) reported long, is reddish brown; full-grown larvae are parasitism of M. solanifolii by Aphidius platensis about 40 mm, and brownish grey. The larva Brèthes, A. brasiliensis Brèthes, Diaeretiella has six instars and becomes fully grown in rapae (McIntosh) (Aphidiidae), and predation 31–38 days. The pupa is about 18.1 mm in by Bacha clavata (F.) (Syrphidae), Coccinella length and dark brown. The pupal stage lasts ancoralis Germar, Cycloneda sanguinea (L.), and from 18 to 22 days (Chacón and Rojas, 1981). Eriopis connexa (Germar) (Coccinellidae). They Moths of A. serta are pale brown and have also reported parasitism of M. persicae by a wingspan of about 45 mm. Eggs, each about Aphelinus mali (Hald.) (Aphelinidae), A. 0.65 mm in diameter, are light yellow and laid platensis, and D. rapae in Argentina and on the bark of stems near the ground. The Uruguay. Cabbage aphid is the primary host larva is cream in colour with a dark brown of D. rapae which is commercially available head. The full-grown larva is about 38 mm. for release against a wide range of aphids, Pupae are light brown and about 39 mm long, especially Myzus and Brachycaudus spp. and 34 mm in length for females and males, (Hsieh and Allen, 1986). respectively (Chacón and Rojas, 1984). The adult moth of O. passiflorae has a wingspan of 24–30 mm. The head and thorax are greyish, and the dorsal of the abdomen is Caterpillars olive-green anteriorly, and greyish posteriorly. The full-grown larva is 18–21 mm long Caterpillars of Azamora penicillana (Walker) with a light brown head and cream coloured (Pyralidae) are defoliators of passion fruit body, with several setae. The pupa is dark yel- (Santos and Costa, 1983; Fancelli, 1992b; low and about 9.5–13.0 mm long. The pupal

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stage occurs inside galleries constructed by outside the principal and lateral stems. Sev- the larvae (Chacón and Rojas, 1984). eral larvae in different stages of development The adult P. perelegans is a pale coloured attack simultaneously at the same point of the microlepidopteran with a wingspan of about stem, and cause cellular hypertrophy. They 35 mm. The wings are yellow semi-hyaline. form galleries in different directions, resulting The borders of the forewings are dark rose. in total destruction of the stem. The young larva is about 1.95 mm long and The caterpillars of P. perelegans infest green. The full-grown larva is about 23.8 mm 6-month-old plants, and remain during the long, and the pupa is dark brown and about whole vegetative period. They attack the buds 13.24 mm long (Chacón and Rojas, 1984). and developing flowers, feeding on nectaries, gynophores, and young fruits (Chacón and HOST PLANTS A. penicillana was reported Rojas, 1984). damaging a wild species of passion fruit (Passiflora cincinnata) in Brazil (Fancelli, 1993). NATURAL ENEMIES Naturally occurring pre- P. saucia damages and causes reduction in dators and parasites are particularly effective fruit production of curuba (Passiflora mollis- against P. saucia in Colombia. A tachinid fly, sima). It is a polyphagous insect, feeding on Incamyia sp., is an important factor for reduc- potato (Solanum tuberosum), oak (Quercus ing the population of P. saucia caterpillars. suber), Calendula officinallis, cotton, tobacco, Another dipterous parasitoid is Megaselia bean, tomato, lucerne, soybean, and beet scalaris (Phoridae). Adults of the predator (Chacón and Rojas, 1981). Anisotarus sp. (Carabidae) feed on caterpillars and prepupae. Some caterpillars may also INJURY Although the caterpillars of A. be infected by bacteria (Bacillus cereus, Pseudo- penicillana cause defoliation, the most serious monas aeruginosa and Streptococcus spp.) damage is caused by the phytotoxic effects of and nematodes (Pseudodiplogasteridae). The the fluid secreted by the caterpillar on the larval stage of O. passiflorae is infected with the leaves and young stems. Heavy infestations fungus Beauveria bassiana and is parasitized cause leaves to dry and drop, and passion fruit by the hymenopteran Neotheronia sp. (Ichneu- plants lose vigour and bear fewer flowers. monidae). Sathon sp. (Braconidae) and Enytus In Bahia, Brazil, the population peak of this sp. (Ichneumonidae) parasitize larvae of P. pest occurs during the rainy season (April to perelegans. The former has gregarious behav- June) (Santos and Costa, 1983; Fancelli, 1992b, iour, and on average 11 adult wasps may 1996). emerge from one larva (Chacón and Rojas, P. saucia larvae feed upon floral struc- 1984). tures of P. mollissima. Young larvae migrate from leaves to the flowers where they feed CONTROL According to Chacón and Rojas on the floral tube, nectary and gynophore, (1984), the infestation of A. serta depends causing flower dropping. The sixth instar on the wood used to made the trellises. The larvae may occasionally continue feeding authors suggest the use of resistant wood on the young fruit, or drop onto the soil to such as mangrove (Rhizophora mangle). Wood pupate. In Colombia, P. saucia infested 64% of Barbados cherry (Malpighia glabra) and of the flowers during the summer (July to Cassia tomentosa are susceptible to attack by September) (Chacón and Rojas, 1981). A. serta, and are not recommend for trellises. Larvae of A. serta bore into roots located near the surface, and occasionally bore into stems. Stem injury is characterized by the presence of sawdust. A single larva is Mealybugs regularly found in 1-year-old plants, while in 6–8-year-old plants, up to five larvae may Citrus mealybug, Planococcus citri Risso, and develop (Chacón and Rojas, 1984). the passion vine mealybug, Planococcus The damage of O. passiflorae caterpillars is pacificus Cox (Pseudococcidae), are pests of characterized by the presence of sawdust lesser importance on passion fruit.

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Passion Fruit 379

DESCRIPTION AND LIFE HISTORY Citrus mealy- death of the plant (Murray, 1976; Swaine et al., bug, P. citri, is a small, oval-shaped sucking 1985). insect commonly found on passion fruit in Hawaii, USA. A white, mealy powder covers NATURAL ENEMIES Lady beetles (Coccinel- the upper surface of the insect body. Wax lidae), especially mealybug lady beetle, strands radiate from the body with slightly Cryptolaemus montrouzieri Mulsant, and longer strands posteriorly. Females are wing- maculate lady beetle, Harmonia octomaculata less and vary in length from 3 to 4 mm. The (Fabricius), substantially reduce mealybug males are fragile, with two wings, and 2 mm numbers. Of secondary importance are in length with two long white filaments small wasp parasitoids such as Leptomastidea extending from the end of the abdomen. The abnormis (Girault) (Encyrtidae) and Ophelosia female is active and feeds throughout its sp., and lacewing larvae (Oligochrysa lutea life. The male feeds only during the first (Walker)) (Murray, 1978; Swaine et al., 1985). stage (Murray, 1976). After mating, the female Silva et al. (1968) reported several species deposits up to 500 yellowish eggs in a of parasitoids and predators of P. citri in loose cottony mass or ovisac and then dies. Argentina. It is parasitized by Apanteles para- Crawlers emerge from the eggs in 3–9 days guayensis Brèthes (Braconidae), Coccophagus and moult several times until the adult stage is caridei (Brèthes) (Aphelinidae), Anagyrus reached. There are three moults in the female coccidivorus Dozier, A. pseudococci (Girault), and four in the male. Approximately 4 weeks Leptomastidea abnormis (Girault), Leptomatrix are required for completion of the cycle dactylopii Howard (Encyrtidae), and Pachyneu- during warm weather (Murray, 1976). ron sp. (Pteromalidae). Leptomastix dactylopii is The females of passion vine mealybug, P. commercially available. It is a yellowish brown pacificus, are white, oval and about 3–4 mm wasp that lays its eggs in late instar nymphs long. Eggs are laid in a loose, cottony mass and and adult mealybugs. Leptomastix prefers hatch to produce crawlers 3–9 days later. hosts in warm, sunny, humid environments. It Development from egg to adult takes about may complete one generation in 2 weeks at 4 weeks during summer. In Queensland (Aus- 30°C or in 1 month at 21°C (Fisher, 1963). tralia), these species are most common in late summer and autumn (Swaine et al., 1985). CONTROL Clusters of mealybugs under dead leaves are well protected from the insec- HOST PLANTS Citrus mealybug infests citrus ticide sprays, and little control can be achieved and many greenhouse and indoor plants. unless vines are cleaned thoroughly to allow Other plants recorded as its hosts include spray penetration. Pruning may enhance the avocado, pineapple, pumpkin, cotton, rice, effectiveness of the spray; however, this is sweet potato, potato, cacao, coffee, sugarcane, often impractical, as laterals to be pruned are chayote, tobacco, guava, mango, rose, pome- generally bearing fruits (Murray, 1976). granate, etc. (Silva et al., 1968). According to Murray (1976), occasional outbreaks of this pest are best controlled by INJURY Mealybugs characteristically aggre- two sprays of 1 : 60 oil or methidathion 0.05% gate on the plant, especially at leaf nodes combined with 1 : 100 oil, 2 weeks to 1 month and under dead leaves and trash. Aggregation apart. The 1 : 60 oil is preferred, as methidath- may also occur under dried flower bracts. ion is highly toxic to the mealybug’s natural Secretion of a sugary solution from the mealy- enemies. For good control, thorough coverage bugs promotes growth of a black fungal is essential. mould on the fruits and leaves. Ants are often found tending mealybugs for this secretion and interfere with the natural control of the mealybugs by parasites and predators. Scales If a severe infestation occurs, loss of vigour, leaf drop, and fruit malformation may Soft brown scale (Coccus hesperidum Lin- occur. Unchecked, an infestation may cause naeus) (Coccidae) may occasionally infest

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380 E.L. Aguiar-Menezes et al.

leaves and stems of passion fruit. California Azya luteipes Mulsant, Coccidophilus red scale, Aonidiella aurantii (Maskell) (Dia- citricola Brèthes, and Pentilia egena Mulsant spididae), is most common on older passion have been recorded as predators of California fruit vines (Swaine et al., 1985). red scale. Two species recorded as pathogenic fungi of this scale are Nectria coccophila and DESCRIPTION AND LIFE HISTORY Adults of soft Myriangium duriaei (Silva et al., 1968). brown scale are approximately 3 mm long, According to Forster et al. (1995), Aphytis and covered by a brown, oval, dome shaped melinus is the most important parasitoid scale. A sweet, sticky secretion produced by attacking California red scale. The adult is a this insect promotes growth of sooty mould on tiny yellow wasp. The female A. melinus feeds the fruit and leaves. Ants also tend the scale on and oviposits in immature scales, prefer- for this secretion (Murray, 1976). ring the virgin adult female scale. The solitary, California red scale is a small, flattened, ectoparasitic larva leaves a flat and dehydrated reddish orange scale. The dull-red female pro- scale body beneath the scale cover, where duces living young or crawlers that shelter the parasitoid’s cast skin and faecal pellets under the parent scale for some time. After (meconia) may be observed. The parasitoid’s leaving the protection of the parent scale, the short life cycle (10–20 days) results in two crawlers quickly settle on the vine or fruit and or three parasitoid generations for each scale then moult – twice if a female, three times if a generation. Comperiella bifasciata is an impor- male – before reaching the adult stage. The life tant encyrtid that parasitizes California red cycle from egg to adult takes about 6 weeks in scale. Adult parasitoids are black, with two summer (Swaine et al., 1985). white stripes on the female’s head. One parasitoid generation requires about 3–6 HOST PLANTS California red scale infests weeks to develop, with faster development citrus and many ornamental plants (Forster occurring on larger (later instar) hosts and at et al., 1995). Silva et al. (1968) cited several warmer temperatures. other host plants of this species such as pump- Parasitoids of C. hesperidum in Argentina kin, coconut, papaya, rose, mulberry, etc. are Aneristus coccidis Blanchard, Coccophagus Soft brown scale uses various plants caridei (Brèthes), Ablerus ciliatus De Santis (sec- as host, such as avocado, sapodilla, plum, ondary parasitoid) (Aphenilidae), Aphycus mulberry, coconut, gladiolus, papaya, laurel, flavus Howard, A. luteolus (Timberlake), and salvia, maté, pear, rose, grape, etc. (Silva et al., Cheiloneurus longisetaceus De Santis (Encyr- 1968). tidae). Among the predators is Azya luteipes Mulsant (Coccinellidae) (Silva et al., 1968). INJURY Soft scales and diaspidids injure plants by sucking sap, and when numerous CONTROL Chemical control is often not can kill the plant. They sometimes heavily required since parasitization by small wasps encrust the leaves, fruits, twigs or branches. substantially reduces populations. Should Mealybugs may be found on almost any part chemical control be necessary, a 1 : 60 oil of the host plant from which they suck the sap spray is satisfactory (Murray, 1976). (Murray, 1976; Swaine et al., 1985).

NATURAL ENEMIES Parasitic wasps are Termites important to control A. aurantii, mainly Comperiella bifasciata (Howard), and Aphytis Termites are increasingly common in passion chrysomphali (Mercet) (Aphelinidae) (Murray, fruit plantations, but losses attributable to 1976; Swaine et al., 1985). In Argentina, this them have not been quantified. Three termite species was reported to be parasitized by species, Heterotermes convexinotatus (Snyder), the aphelinids, A. chrysomphali, A. maculicornis Amitermes foreli Wasmann, and Microceroter- Masi, and Aspidiotiphagus citrinus (Crawford) mes arboreus Emerson, were observed to feed (Silva et al., 1968). on roots and stems of 2–4-year-old passion

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Passion Fruit 381

fruit plants in Venezuela (Dominguez-Gil Bees and McPheron, 1992). In some passion fruit growing areas, the DESCRIPTION AND LIFE HISTORY Heterotermes honeybee Apis mellifera L. (Apidae) is consid- (Rhinotermitidae) is a widespread genus. It is ered a pest since it robs the pollen from the characterized by the soldier which has a long carpenter bees, thereby causing a reduction and rectangular head. It does not have teeth of fruit set (Akamine et al., 1954). Adults of on the interior curvature of the mandibles. The Trigona spinipes Fabricius (Apidae), known as pronotum is wide and flat (Hadlington, 1987). irapuá or arapuá in Brazil, attack leaves, It has subterranean habits, and does not con- stems, trunk, developing buds, developing struct an exposed nest. The colony always fruits, and fruit peduncles of several plant remains in contact with the soil through the species (Puzzi, 1966; Bastos, 1985; Teixeira galleries (Dominguez-Gil, 1998). et al., 1996). It may be found from northern to Amitermes (Termitidae) is cosmopolitan southern Brazil (Silva et al., 1968; Bleicher and in distribution and especially conspicuous in Melo, 1993). Carvalho et al. (1994) reported the tropics and in the warmer areas of the serious damage caused by T. amazonensis to temperate zones (Krishna and Weesner, 1970). yellow passion fruit in Acre (Brazil). The members of this genus are essentially subterranean in habit. The nest is usually situated DESCRIPTION AND LIFE HISTORY Trigona in the soil (Krishna and Weesner, 1970). Its spinipes is about 5–6.5 mm in length, black soldiers have the mandibles curvated, thin, with transparent wings and without an ovi- not too long, and with a prominent tooth and positor (Santos and Costa, 1983). It constructs not clearly rectangular (Hadlington, 1987). its nests on trees, usually between their Subterranean soldiers of Microcerotermes branches, or in abandoned termite nests. It (Termitidae) have long, rectangular mandi- uses fibrous filaments of plant material and bles, which are serrated on the interior face agglutinative elements, mainly resin. Like (Hadlington, 1987). A queen of M. arboreus, honeybees, they exist in large colonies with measuring 21 mm in length, may deposit 1680 a queen, without corbiculae, and with thou- eggs in 24 hours (Krishna and Weesner, 1970). sands of workers (Riek, 1979).

INJURY Termites penetrate and excavate the INJURY Trigona spinipes causes malfor- roots and continue upwards within the stems. mation of foliage and dropping of flowers, The plant often dies, and death may be associ- resulting in a reduction in the number of fruits ated with the presence of soil pathogens, which produced per plant. It also attacks developing usually cause rotting, including Fusarium spp. flowering buds (Fancelli and Mesquita, 1998). and Phytophthora spp. (Dominguez-Gil and McPheron, 1992; Piza Júnior, 1992). HOST PLANTS Trigona spinipes damages various plant species, especially flowering CONTROL The use of tillage operations to buds and leaves, of sapodilla, mulberry, reduce populations of soil-inhabiting insects banana, citrus, coconut, mango, rose, pine, may work in several ways. In the case of and fig (Silva et al., 1968). termites, it may change the physical condition of soil and expose the colony to the sun. Piza NATURAL ENEMIES Silva et al. (1968) reported Júnior (1992) recommended that after tillage, the parasitism of larvae of T. spinipes by the soil should be treated with Thiodan 350 CE Pseudohypocera nigrofascipes Borgn. & Schn. (endosulfan) at 100–500 cm3 per 100 l of water. (Phoridae). The soil must be treated when it is wet to allow the penetration of the insecticidal solution. CONTROL Recommendations to prevent When the crop is already established, the insec- honeybees from robbing passion fruit flowers ticidal solution must be applied to the soil of their pollen have been made. One of them is around the plants in large quantities to reach a to plant more attractive plant species such depth of 35 cm. as eucalyptus and basil in adjacent areas to

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382 E.L. Aguiar-Menezes et al. n ó .,

al 1993; 1995 ., et Chac al Bortoli 1977; McPheron, McPheron, McPheron, McPheron, 1984; 1984; 1984 1984 1984

et ., De Silva al Kavati, 1974; 1994 1994 1994 and and and and 1991;

et ., ., Filho Rojas, Rojas, Rojas, Rojas, Rojas, al a 1987 al and 1984; ê

et 1952b; 1994 1994 et 1994 and and and and and nior o n n n n n Teixeira, Racca Teixeira, Corr Teixeira, ú ã ó ó ó ó ó J Busoli, Rojas, Chac Teixeira, Teixeira, Rossetto Dominguez-Gil 1992; Dominguez-Gil 1992; Chac Dominguez-Gil 1992; Teixeira, 1968; Chac References Dominguez-Gil 1992; Brand Piza Chac Lordello, and Chac and adult adult adult adult adult adult and and and and and and stage adult adult nymph nymph nymph nymph nymph nymph and and Adult Larva, Larva, Larva, Larva, Larva, Larva, Damaging Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Larva Larva Larva Larva Larva Larva Larva Adult Adult Adult Larva world. the chewer chewer chewer chewer chewer leaf leaf fruit around flower chewer pollen habits and and and borer borer borer borer borer borer borer on sucker sucker sucker sucker sucker sucker chewer chewer chewer chewer chewer chewer chewer and chewer chewer chewer spp.) Feed Fruit Leaf Leaf Leaf Leaf Leaf Feeding Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Flower-bud Seedling Leaf Stem Stem Stem Stem Stem Stem Stem Leaf Flower Flower Calyx

Passiflora ( M. fruit (F.) é (Banks) é (Banks) (Germar) (McGregor) Degeer

Schaarschmidt latus (Geijsks) Bechyn Brien passion (F.) ’ Wood Harold Latreille Hood (F.) (F.) (Koch) Bechyn O (F.) Germ. with undecinpunctata Champion

melanocephala sp.

stammeri mexicanus desertorum urticae sp. auripes phoenicis sp. bispinus marginata famelica melanoptera orphelia walteriana cingulata bogotana sp. fasciculatus poss. sp.

diadema sp.

name conspicua atomaria passiflorae obesus crucifer associated

Scientific Tarsonemus Polyphagotarsonemus Tetranychus Tetranychus Tetranychus Brevipalpus Frankliniella Trichaltica Euryscopa Cacoscelis Cacoscelis Cacoscelis Cacoscelis Cacoscelis Diabrotica Maecolaspis Monomarca Acalymma Litostylus Philonis Philonis Philonis Chramesus Stenygra Lepturges Stizocera Epicauta Cyclocephala Leucothyreus Araecerus arthropods Thripidae Tarsonemidae Tetranychidae Tenuipalpidae Chrysomelidae Family Curculionidae Scolytidae Cerambycidae Meloidae Scarabaeidae Anthribidae Phytophagous 12.2. e l b a INSECTA Thysanoptera ARACHNIDA Acari T Class/Order Coleoptera

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Passion Fruit 383 and De n Brown ó and 1952a, Sazima continued n McPheron, McPheron, 1984 1984 1984; 1984 1984 1984; 1984 ó 1983; 1972; 1987; Chac 1968; 1998 1998 ., 1992 1994; and and

al Chac ., Dominguez-Gil Lordello, 1989; Rojas, Rojas, Rojas, Rojas, Rojas, Rojas, Rojas, al et Costa, 1968; Busoli, Mielke,

et ., 1992b and and and and and and and al 1976; and 1992; 1931; and 1984 1984 and n n n n n n n Silva et ó ó ó ó ó ó ó McPheron, Sazima, nior ú Silva Fancelli, Chac Chac Santos Chac Chac and Bortoli Carter, Rojas, Chac and Dominguez-Gil, Dominguez-Gil 1992 J Chac Carvalho 1954; Santo, Murray, Rojas, Chac Dominguez-Gil, Dominguez-Gil 1992 adult adult adult and and and (workers) (workers) (workers) Adult Adult Adult Adult Adult Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Nymph Nymph Nymph Adult Adult Adult stem stem stem borer chewer and and and fruit sucker fruit stem stem root root root chewer chewer chewer chewer chewer chewer and borer borer borer sucker sucker on on on on on stem flower, chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer Feed Flower Flower Flower Feed Stem Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Stem Flower Flower Flower Stem Bud, Leaf Calyx Stem Stem Leaf, Feed Feed Feed tries (R) é e) bner) n é bner) Druce (Snyder) ü é ü S. Emerson (Weymer) M (H (Godart) (Godart) (H (L.) (F.) (Guen Felder) . bner)

wernickei (Hampson) L.

matrica (Walker) (Walker) ü Clarke R (L.)

robigus (Schaus) (Olivier) (H & arboreus aliphera narcaea F. huebneri dianosa vanillae maculosa Wasmann phyllis (L.) (L.) apseudes sp. sp. poss.

conexinotatus (C.

serta sp.

ornihogalli sp.

sp. foreli juno dido wernickei sp. silvana sara ethilla erato saucia consueta sp. phaetusa perelegans penicillana

isabella isabella aliphera vanillae vanillae (P.) passiflorae amalthea spinipes amazonensis hesperidium

juno glycera

Trigona Trigona Trigona Crematogaster Solenopsis Heterotermes Microcerotermes Amitermes Eueides Eueides Eueides Dione Dione Agraulis Agraulis Dryadula Philaethria Philaethria Heliconius Heliconius Heliconius Heliconius Sabulodes Aepytus Peridroma Copitarsia Spodoptera Odonna Pyrausta Azamora Pococera Langsdorfia Coccus Ceroplastes Hexaleurodicus Coccidae Aleyrodidae Nymphalidae Rhinotermitidae Termitidae Geometridae Hepialidae Noctuidae Oecophoridae Pyralidae Cossidae Apidae Formicidae Homoptera Isoptera Lepidoptera Hymenoptera

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384 E.L. Aguiar-Menezes et al. o ã ., ., and

al al and n and ó

et et n Brand Lordello, ó Busoli, 1988; Santos nior 1984 1992 Rojas, ú 1968; Chac Dominguez- J and Chac ., Chiavegato, 1974; 1954; 1954; and Swaine 1976; Dominguez-Gil, Swaine al ., ., ., Zucchi, Rojas, n Piza al al et al 1983; ó 1987; 1987 1993 Bortoli 1980; et 1952; et et 1994 and 1976; 1976; 1976; McPheron, 1984; 1984 n Murray, ICA, De Chac ICA, Silva 1991; ó Costa, ., and

al Rossetto Resende, Murray, Teixeira, Chac Rojas, 1954; and 1987; Gil 1984; Murray, 1998; References 1985; Akamine 1985 Mariconi, 1963; Steyskal, Rojas, Akamine Murray, et adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult stage and and and and and and and and and and and and and and and Damaging Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Nymph Nymph Nymph Nymph Nymph Nymph Nymph suckers bud bud bud bud chewer stem sucker sucker sucker sucker sucker sucker sucker sucker fruit flower flower flower flower fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit habits on on on on on on on on on on on on on on on on fruit fruit fruit fruit fruit fruit fruit fruit fruit, sucker sucker sucker sucker sucker Feeding Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Feed Feed Feed Feed Flower-bud Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Leaf, Leaf Leaf Leaf Leaf Leaf (Loew) (Stal) Guerne (Morgan) marginella Ashmead (F.) (Loew) Lima Wheeler (F.) Cox (Herbest.) (F.) (Walker) (Macquart) (Hendel) McAlpine (F.) McAlpine Coquillett (Maskell) (F.) Steykal Risso Steykal (Dallas) Lima (Sulzer) (Wiedemann) (Glover)

articulatus solanifolii Bezzi gonagra conspersus citri pacificus (Froggatt) histro clavigera salebrosa pallidipennis consobrina ethalea grandis kuhlmanni lutzi pseudoparallela foliacea flavolineata dorsalis

auranti cristula name

capita curubae inedulis passifloris zonatus bilineatus persicae curcubitae tryoni gossypii pendula

Scientific Selenaspidus Aonidiella Myzus Aphis Macrosiphum Planococcus Planococcus Holhymenia Holhymenia Veneza Leptoglossus Leptoglossus Anisoscelis Anisoscelis Diactor Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Ceratitis Dacus Bactrocera Dacus Zapriothrica Lonchaea Silba Dasiops Dasiops Dasiops . Tephritidae Drosophilidae Lonchaeidae Coreidae Diaspididae Aphididae Pseudococcidae Family

Continued 12.2. e l b a Diptera Hemiptera T Class/Order

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passion fruit. Collection of wild swarms is also Back, E.A. and Pemberton, C.E. (1918) The Medi- recommended (Boaretto et al., 1994). The con- terranean fruit fly in Hawaii. United States trol strategies recommended for T. spinipes Department of Agricultural Bulletin 536, 1–118. include the destruction of nests near the crop, Barbagallo, S., Cravedi, P., Pasqualini, E. and Patti, I. (1997) Aphids of the Principal Fruit-Bearing and weekly inspections to verify the occur- Crops. Bayer, Milan, 123 pp. rence of this pest on flowers. In exceptional Bastos, J.A.M. (1985) Principais Pragas das Culturas cases, chemical control is recommended. e Seus Controles, 3rd edn. Nobel, São Paulo, 329 pp. Bateman, M.A. (1972) The ecology of fruit flies. Conclusions Annual Review of Entomology 17, 493–518. Bleicher, E. and Melo, Q.M.S. (1993) Artrópodes Associados ao Cajueiro no Brasil. EMBRAPA/ Several different species of arthropods have CNPAT, Fortaleza, Documentos 9, 33 pp. been reported in passion fruit. Other pests Boaretto, M.A.C., Brandão, A.L.S. and São José, A.R. doubtless occur, and new ones will appear in (1994) Pragas do maracujazeiro. In: São José, the future. Fortunately the majority of these A.R. (ed.) Maracujá, Produção e Mercado. DFZ/ species are not injurious. The species listed UESB; Vitória da Conquista, pp. 99–107. in Table 12.2 are generally accepted as being Boiça Júnior, A.L., Lara, F.M. and Oliveira, J.C. responsible for most of the insect and mite (1993) Resistência de genótipos de maracu- damage wherever passion fruit grows. jazeiro ao ataque de Dione juno juno Cramer, For control of insect and mite pests which 1779 (Lepidoptera: Nymphalidae). In: Resumos attack passion fruit, we must consider two do 14 Congresso Brasileiro de Entomologia. SEB, Piracicaba, p. 143. basic problems: (i) creation and preservation Brandão, A.L.S., São José, A.R. and Boaretto, M.A.C. of conditions favourable to carpenter bees, (1991) Pragas do maracujazeiro. In: São José, whose function in pollination is of vital A.R., Ferreira, F.R. and Vaz, R.L. (eds) A importance for fruit set; (ii) suitable control Cultura do Maracujá no Brasil. FUNEP, of insects and mites that damage the plant. Jaboticabal, pp. 136–168. Additionally, a latent problem is the conserva- Brown Júnior, K.S. and Mielke, O.H.H. (1972) The tion of natural enemies, which is complicated heliconians of Brazil (Lepidoptera: Nympha- because beneficial and noxious insects and lidae). Part II. Introduction and general mites are closely associated with the plant. comments, with a supplementary revision The timing of spraying is critical, so that of the tribe. Zoologia 57, 1–40. Camillo, E. (1978a) Aspectos reprodutivos de applications are not made when passion algunas espécies de Xylocopa (Hymenoptera: fruit flowers are open and the carpenter bees Anthophoridae). Ciência e Cultura 30, 594–595. are active. The choice of a selective pesticide, Camillo, E. (1978b) Polinização do maracujazeiro. with low toxicity to predators and parasites, is In: Anais do 2 Simpósio Sobre a Cultura do important to maintain not only natural control Maracujazeiro, Jaboticabal, pp. 32–39. but also pollinators. Camillo, E. (1980) Polinização do maracujazeiro. In: Ruggiero, C. (ed.) Cultura do Maracujazeiro. FCAN, Jaboticabal, pp. 47–53. Camillo, E. (1996) Utilização de espécies de References Xylocopa (Hymenoptera: Anthophoridae) na polinização do maracujá amarelo. In: Anais Akamine, E.K. and Girolami, D.G. (1957) Problems do 2 Encontro Sobre Abelhas. Ribeirão Preto, in fruit set in yellow passion fruit. Hawaii Farm pp. 141–146. Science 5, 3–5. Camillo, E. and Garófalo, C.A. (1982) On the Akamine, E.K. and Girolami, D.G. (1959) Pollination bionomics of Xylocopa frontalis (Olivier) and and Fruit Set in Yellow Passion Fruit. Hawaii Xylocopa grisescens (Lepeletier) in southern Agricultural Experiment Station, Honolulu, Brazil. I. Nest construction and biological cycle. Technical Bulletin 39, 32 pp. Revista Brasileira de Entomologia 42, 571–582. Akamine, E.K., Hamilton, R.A., Nishida, T., Caraballo, J. (1981) Las moscas de las frutas del Sherman, G.D. and Storey, W.B. (1954) Passion género Anastrepha Schiner, 1868 (Diptera: Fruit Culture. University of Hawaii, Extension Tephritidae) de Venezuela. MSc thesis, Circular 345, 23 pp. University Central de Venezuela, 210 pp.

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Carter, D. (1992) Butterflies and Moths. Dorling cuenca del Lago de Maracaibo, Venezuela: Kindersley, London, 304 pp. características morfológicas. Boletín del Centro Carvalho, E.F., Calixto, A.R.Y., Silva Filho, J.R. de Investigaciones Biológicas 32, 1–66. and Morato, E.F. (1994) Avaliação da Dominguez-Gil, O.E. and McPheron, B.A. (1992) polinização artificial na redução dos danos Arthropods associated with passion fruit in causados por Trigona amazonensis na cultura western Venezuela. Florida Entomologist 75, do maracujá amarelo. In: Anais do 13 607–612. Congresso Brasileiro de Fruticultura. SBF, Dominguez-Gil, O.E., Vera, H., Socarras, G. and Salvador, pp. 798–799. Carvajal, R. (1989) Posible epizootia de tipo Causton, C.E. (1993) Una mosca del genero Dasiops viral en larvas de Eueides isabella Ménétries y (Diptera: Lonchaeidae) atacando la curuba Dione juno juno (Cramer) defoliando planta- (Passiflora mollissima) en el Edo. Merida, Vene- ciones de parchita maracuyá en el Estado zuela. Boletín de Entomología Venezolana 8, 146. Zulia. In: Resúmenes del 11 Congreso Venezolano Chacón, P. and Rojas, M. (1981) Biologia y control de Entomologia. Sociedad Venezolana de Ento- natural de Peridroma saucia, plaga de la flor de mología, Maracaibo, p. 33. la curuba. Revista Colombiana de Entomologia 7, Donadio, L.C. (1983) Frutíferas tropicais de 47–53. valor potencial. In: Donadio, L.C. (ed.) Fruti- Chacón, P. and Rojas, M. (1984) Entomofauna cultura Tropical. FCAV/UNESP, Jaboticabal, asociada a Passiflora mollissima, P. edulis f. flavi- pp. 20–30. carpa y P. quadrangularis en el Departamento Echeverri, F., Cardona, G., Torres, F., Pelaez, C., del Valle del Cauca. Turrialba 34, 297–311. Quiñones, W. and Renteria, E. (1991) Ermanin: Chiavegato, L.G. (1963) Leptoglossus gonagra – praga an insect deterrent flavonoid from Passiflora do maracujá. O Agronômico, 15, 31–36. foetida resin. Phytochemistry 30, 153–155. Corbet, S.A. and Willmer, P.G. (1980) Pollination Fancelli, M. (1992a) A Broca da Haste do Maracujazeiro. of the yellow passionfruit: nectar, pollen and EMBRAPA/CNPMF, Bahia, Maracujá em carpenter bees. Journal of Agricultural Science Foco 53, 2 pp. 95, 655–666. Fancelli, M. (1992b) A Lagarta de Teia do Maracu- Corrêa, L.S., Ruggiero, C. and Oliveira, J.C. (1977) jazeiro. EMBRAPA/CNPMF, Bahia, Maracujá Ocorrência de Acalymma sp. (Coleoptera: em Foco 54, 2 pp. Chrysomelidae) sobre mudas de maracujá- Fancelli, M. (1993) Ocorrência de Azamora penicillana amarelo (Passiflora edulis f. flavicarpa Deg.). (Walk.) (Pyralidae: Chrysauginae) em mara- Científica 5, 229–230. cujá silvestre. Anais da Sociedade Entomológica do Costa, J.M., Correa, J.S., Santos, Z.F.A. F. and Ferraz, Brasil 22, 121–124. M.C.V.D. (1979) Estudos da Broca do Maracu- Fancelli, M. (1996) Insetos-pragas do maracujazeiro jazeiro na Bahia e Meios de Controle. EPABA, e controle. In: Lima, A.A., Borges, A.L., Santos Salvador, Comunicado Técnico 37, 10 pp. Filho, H.P., Fancelli, M. and Sanches, N.F. (eds) Cox, I.E. (1957) Flowering and pollination of passion Instruções Práticas Para o Cultivo do Maracu- fruit. Agricultural Gazette of New South Wales 68, jazeiro. EMBRAPA/CNPMF, Bahia, Circular 573–576. Técnica, 20, 44 pp. Cruz, C.A., Graça, D. and Lima, A.F. (1993) Fancelli, M. and Mesquita, A.L.M. (1998) Pragas Ocorrência de Philonis obesus em maracujazeiro do maracujazeiro. In: Braga Sobrinho, R., no Estado do Rio de Janeiro. In: Resumos do Cardoso, J.E. and Freire, F.C.O. (eds) Pragas de 14 Congresso Brasileiro de Entomologia. SEB, Fruteiras Tropicais de Importância Agroindustrial. Piracicaba, p. 16. EMBRAPA/SPI, Brasília, pp. 169–180. Cunha, M.A.P. (1996) Recursos genéticos e Figueiro, C.L.M. (1995) Aspectos biológicos e modificações em métodos de seleção para controle da lagarta Dione juno juno (Lepidop- produtividade em maracujá. Revista Brasileira tera: Heliconiinae) do maracujazeiro (Passiflora de Fruticultura 18, 413–423. edulis) por Baculovirus dione. MSc thesis, UFPa, D´Almeida, R.F. (1944) Estudos biológicos sobre Brazil, 73 pp. alguns lepidópteros do Brasil. Archivos de Fisher, T.W. (1963) Mass Culture of Cryptolaemus Zoologia do Estado de São Paulo 4, 44. and Leptomastix – Natural Enemies of Citrus De Bortoli, S.A. and Busoli, A.C. (1987) Pragas. Mealybug. University of California Agricul- In: Ruggiero, C. (ed.) Cultura do Maracujazeiro. tural Experiment Station Bulletin, No. 797. Legis Summa, Ribeirão Preto, pp. 111–123. Flechtmann, C.H.W. (1989) Ácaros de Importância Dominguez-Gil, O.E. (1998) Fauna fitófaga de Agrícola. Nobel, São Paulo, 189 pp. parchita maracuyá (Passiflora edulis f. flavicarpa) Forster, L.D., Luck, R.F. and Grafton-Cardwell, E.E. en las regiones oriental y suroriental de la (1995) Life Stages of California Red Scale and its

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In: Resumos do 14th Congresso Brasileiro de Heliconiidae). MSc. thesis, UFPR, Curitiba, Entomologia. SEB, Piracicaba, p. 166. Brazil, 99 pp. Riek, E.F. (1979) Hymenoptera (wasps, bees, Silva, L.M.S. (1982) O controle das pragas do ants). In: The Insects of Australia. Melbourne maracujazeiro e a preservação dos seus University Press, Carlton, pp. 867–959. inimigos naturais. In: Anais do 2nd Encontro Rossetto, C.J., Cavalcante, R.D., Grisi Júnior, C. and Estadual Sobre a Cultura do Maracujá, pp. 54–58. Carvalho, A.M. (1974) Insetos do Maracujazeiro. Stefani, R.N. and Morgante, J.S. (1996) Genetic vari- Instituto Agronômico, Campinas, Circular ability in Anastrepha pseudoparallela: a specialist Técnica 39, 12 pp. species. In: McPheron, B.M. and Steck, G.J. Rossetto, C.J., Longo, R.S., Rezende, J.A.M. and (eds) Fruit Fly Pests, a World Assessment of Their Branco, E.M.C. (1978) Ocorrência de Philonis Biology and Management. St Lucie Press, Delray sp. (Coleoptera: Curculionidae) como praga de Beach, pp. 277–280. maracujazeiro. Ciência e Cultura 30, 9. Stegmaier, C.E. (1973) Dasiops passifloris (Diptera: Ruggiero, C., Lam-Sanchez, A. and Miguel, S. (1975) Lonchaeidae), a pest of wild passion fruit in Estudos da incompatibilidade em flores do south Florida. Florida Entomologist 56, 8–10. maracujá amarelo (Passiflora edulis f. flavicarpa Steyskal, G.C. (1980) Two-winged flies of the genus Deg.). In: Anais do 3rd Congresso Brasileiro de Dasiops (Diptera: Lonchaeidae) attacking Fruticultura. SBF, Rio de Janeiro, pp. 491–495. flowers or fruit of species of Passiflora (passion Ruggiero, C., Banzatto, D.A. and Lam-Sanchez, A. fruit, granadilla, curuba, etc.). In: Proceedings (1976) Studies on natural and controlled of Entomological Society of Washington 82, pollination in yellow passion fruit (Passiflora 166–170. edulis f. flavicarpa Deg.). Acta Horticulturae 57, Stone, A. (1942) The Fruit Flies of the Genus 121–124. Anastrepha. United States Department of Ruggiero, C., São José, A.R., Volpe, C.A., Oliveira, Agriculture, Washington, Miscellaneous J.C., Duringan, J.F., Baumgartner, J.G., Silva, Publications 439, 112 pp. J.R., Nakamura, K., Ferreira, M.E., Kavati, R. Swaine, G., Ironside, D.A. and Yarrow, W.H.T. and Pereira, V.P. (1996) Maracujá Para (1985) Insect Pests of Fruit and Vegetables. Expotação: Aspectos Técnicos da Produção. Queensland Department of Primary Indus- EMBRAPA/SPI, Brasília, Publicações Técnicas tries, Brisbane. FRUPEX 19, 64 pp. Teixeira, C.A.D., Aviles, D.P. and Fernandes, L.M. Sanches, N.F. (1996) Ácaros do maracujazeiro. In: (1996) Danos de Trigona sp. (Hymenoptera: Lima, A.A., Borges, A.L., Santos Filho, H.P., Apidae) em flores de maracujazeiro (Passiflora Fancelli, M. and Sanches, N.F. (eds) Instruções edulis) em Porto Velho. In: Resumos do 8th Práticas Para o Cultivo do Maracujazeiro. Encontro de Pesquisadores da Amazonia. UNIR/ EMBRAPA/CNPMF, Bahia, Circular Técnica PIUAL, Porto Velho, p.13. 20, 44 pp. Teixeira, C.G. (1994) Maracujá. I – cultura. In: Santo, E. (1931) Inimigos e Doenças das Fruteiras. Teixeira, C.G., Castro, J.V., Tocchini, R.P., Biblioteca Agric. D’O Campo, Rio de Janeiro, Nishida, A.L.A.C., Turatii, J.M., Leite, 80 pp. R.S.S., Bliska, F.M.M. and Garcia, E.B. (eds) Santos, Z.F.A.F. and Costa, J.M. (1983) Pragas da Maracujá, Cultura, Matéria-Prima, Processa- Cultura do Maracujá no Estado da Bahia. EPABA, mento e Aspectos Econômicos, 2nd edn. ITAL, Salvador, Circular Técnica 4, 10 pp. Campinas, pp. 3–131. Sazima, I. and Sazima, M. (1989) Mamangavas Toledo, Z.D.A. (1991) Fauna del noroeste argentino. e irapuás (Hymenoptera: Apoidea): visitas, Contribucion al conocimiento de los lepidop- interações e consequências para polinização do teros argentinos. IX. Dione juno (Cramer) maracujá (Passifloraceae). Revista Brasileira de (Lepidoptera: Rhopalocera: Heliconiidae). Entomologia 33, 109–118. Acta Zoológica Lilloana 40, 109–117. Semir, J. and Brown, K.S. (1975) Maracujá: flor da Torres Filho, J. and Araújo, G.C. (1981) Broca do paixão. Revista Geografica Universal 2, 41–47. caule Philonis sp., nova praga do maracu- Silva, A.G.A., Gonçalves, C.R., Galvão, D.M., jazeiro, Passiflora edulis Sims. no Estado do Gonçalves, A.J.L., Gomes, J., Silva, M.N. and Ceará. Fitossanidade 5, 50–51. Simoni, L. (1968) Quarto Catálogo dos Insetos que Vasconcellos, M.A.S. (1991) Biologia floral do Vivem nas Plantas do Brasil, Seus Parasitos e maracujá doce (Passiflora alata Dryand) nas Predadores, Part II, Vol. 1. Ministério da condições de Botucatu – SP. MSc thesis, Agricultura/DDIA, Rio de Janeiro, 622 pp. UNESP, Jaboticabal, SP, Brazil, 98 pp. Silva, C.C.A. (1979) Morfologia e biologia de Vasconcellos, M.A.S., Aguiar, E.L., Bicalho, A.C., Dione juno juno (Cramer, 1779) (Lepidoptera: Menezes, E.B. and Prado, A.P. (1995)

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Ocorrência de Dasiops n. sp. (Diptera: Lonch- Zucchi, R.A. (1988) Moscas-das-frutas (Dip., aeidae) em maracujazeiro, no município de Tephritidae) no Brasil; taxonomia, Itaguaí, RJ. In: Resumos do 15 Congresso distribuição geográfica e hospedeiros. Brasileiro de Entomologia. SEB, Caxambu, p. 335. In: Anais do 1 Encontro Nacional Warumbi, T.T. and Veiga, A.F.S.L. (1978) Uma nova Sobre Moscas-das-Frutas. Fundação Cargill, praga no maracujá no nordeste do Brasil. Campinas, pp. 1–10. In: Resumos do 3 Congresso Latinoamericano de Zucchi, R.A. (2000) Espécies de Anastrepha, Entomologia. CEPLAC, Ilhéus, p. 20. sinonímias, plantas hospedeiras e para- Wharton, R.A. (1996) Parasitoids of fruit-infesting sitóides. In: Malavasi, A. and Zucchi, R. A. Tephritidae – how to attack a concealed host. (eds) Moscas-das-frutas de importância econômica In: Abstracts of XX International Congress of no Brasil, conhecimento básico e aplicado. Holos, Entomology. Firense, Italia, p. 665. Ribeirão Preto, pp. 41–48.

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13 Quarantine Treatments for Pests of Tropical Fruits

Jennifer L. Sharp1 and Neil W. Heather2 1USDA-ARS, 13601 Old Cutler Road, Miami, FL 33158, USA; 2School of Land and Food, The University of Queensland, Gatton College, Queensland 4345, Australia

Multitudes of new pests regularly threaten eradicate quarantine pests once they become agricultural commodities and significantly established. For example, officials dealing with impact agricultural businesses that market various exporters and importers handling the commodities on a global scale, especially commodities originating from countries with with expanding trade and tourism. Primary quarantine pests must satisfy the importing pests of major concern include members of countries’ rules, regulations, and requirements the phyla Arthropoda and Mollusca. These before the commodities are permitted entry insect, mite, slug and snail pests attack many into that country. Numerous strategies com- commodities, including the tropical fruits mencing with a Pest Risk Analysis (AQIS, discussed in this volume. The risk of pest 1991; Shannon, 1994; Anonymous, 1996) have introduction and means to stop the establish- been developed to ensure quarantine security ment of these pests in new areas continues before any pest host is permitted entry. to be a major concern of regulatory officials. Quarantine security, a degree of statistical Without the use of quarantine intervention probability and confidence (Chew, 1994; by these authorities, pests could be trans- Robertson et al., 1994), may require quarantine ported over the globe, rapidly become estab- treatments including operational systems to lished in new areas, devastate tropical fruits, ensure that tropical fruits do not contain any and cause economic havoc to members of the unwanted target pests capable of establish- agricultural communities and to consumers, ment on arrival. who demand high quality tropical fruits When the use of plant quarantine to pre- grown and marketed without the use of vent the movement of exotic pests first became chemicals. Means to protect tropical fruits important for fresh horticultural produce include the use of quarantine, which is early in this century, disinfestation treat- intended to prevent the establishment of ments, such as fumigation, heat or cold, were exotic pest species in places where they are virtually the sole means by which effective not already found. control could be exercised over the risk of Prevention of pest entry by inspection, infested produce. For almost all pests, and with or without pretreatment, and early detec- especially for fruit flies, the earliest treatments tion of incursions through active monitoring were the application of heat or cold. These are the first lines of defence employed by reg- were supplanted for a time by fumigants ulatory officials who must use these methods (e.g. ethylene dibromide, methyl bromide) to avoid expensive programmes required to and sometimes by residual chemicals (e.g.

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dimethoate). Consumer preference is now evidence. Their origins probably lie more identified clearly as being for the use of in the efficacies achievable from treatments non-chemical and residue-free physical treat- available at the time than what was required ments with heat/cold, modified atmospheres by the risk. Disinfestation treatments are and, in an increasing number of countries, likely to remain the most important means irradiation (Heather, 1994). Modern develop- of obtaining market access where there are ments in electronic temperature control and pest quarantine impediments. greater physiological understanding of fruit The US Department of Agriculture, tolerance are enabling the increasing use of Animal and Plant Health Inspection Service, heat disinfestation, which takes only a few Treatment Manual provides compilations of hours and is much faster than cold, which treatments presented as schedules for all com- often requires many days or weeks. Heat is modities requiring quarantine action before particularly useful for many tropical fruits the commodities are imported into the USA which, not unexpectedly, tend to be intolerant (APHIS, 1998). The schedules are arranged in of cold. When commodities cannot tolerate sections and cover a wide variety of applica- heat or cold because the treatments may cause tions including fumigation, heat, cold, combi- damage, other treatments are available and nation treatments, and hot water treatments. will be discussed in this chapter. An increas- The manual is available by writing to: Printing ing number of countries are using radiation as and Distribution, US Department of Agri- an alternative treatment to fumigation and culture, Animal and Plant Health Inspection other treatment methods to control tropical Service, Methods and Development, 4700 fruit pests. River Road, Room 1A01, Riverdale, MD Successful disinfestation treatments must 20737. Several states within the USA, such achieve the quarantine security needed to con- as Florida, Texas, Arizona, California, and trol the pest specified by authorities without Hawaii, have separate quarantine treatment causing damage to the product, which would manuals and directives, with procedures and render it unacceptable to consumers. The treatment schedules that must be followed to required efficacy needed to reach the security satisfy each state’s regulatory requirements. goal varies from country to country. For the Other countries have similar internal and United States of America (USA) the required international schedules which list proclaimed efficacy has usually been 99.9968% (probit pests and conditions of entry for commodities, 9) demonstrated at the 95% confidence level including treatments before or after entry. In with no survivors from 100,000 treated insects Chapter 1 of this volume, J. Peña discusses (Baker, 1939; Couey and Chew, 1986). For the pests associated with tropical fruits. Many Japan, efficacy is determined as no survivors of these pests require quarantine regulatory from a minimum of 30,000 treated pests, and action. Quarantine pests of tropical fruits New Zealand has a concept of Maximum Pest include numerous species of tephritid fruit Limit, currently of allowing five surviving flies, leaf and fruit miners, other moths and flies in 1,000,000 pieces of fruit for critical fruit flies, weevils and other beetles, thrips, scales fly species such as Mediterranean fruit fly, and mealybugs, mites, snails and slugs. Ceratitis capitata (Wiedemann) and Queens- Quarantine pests can be restricted to the land fruit fly, Bactrocera tryoni (Froggatt) surface of fruits, under a calyx, in residual (Baker et al., 1990). It is not unusual for a pro- structures such as in the navel of some citrus spective market (e.g. Japan and New Zealand) cultivars, or they can be present internally in to require a treatment to be demonstrated the pulp, inside seeds, or simply present as repetitively on each cultivar to be imported. hitch-hikers on fruits and in packaging. Each efficacy requirement forms part of a This chapter discusses various quaran- disinfestation research procedure or protocol, tine treatment measures that may be applied aspects of which may be unique to each mar- to keep tropical fruits free from exotic pests. ket. Increasingly, these traditional standards The quarantine measures have been divided are being questioned, as most would have arbitrarily into three broad categories which been set arbitrarily or based on anecdotal are: measures to eliminate need for treatment;

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single treatments; and combination treat- lends itself to this type of strategy (e.g. fruit ments. Emphasis is given to studies published fly). Many examples exist that make use of since the mid-1990s. Comprehensive book the pest-free area concept: honeydew melons reviews for quarantine treatments have been from an area in Brazil declared to be free of presented by Sharp and Hallman (1994), Paul Anastrepha grandis (Macquart) can be impor- and Armstrong (1994), and Champ et al. ted into the USA (Federal Register, 1993a); (1993). municipalities within the State of Sonora, Mexico, are proclaimed free of Mediterra- nean fruit fly and Anastrepha species (Federal Measures that Eliminate the Need Register, 1994a); and some geographical for Treatments subdivisions of the Riverina and Sumaysia districts of Australia are proclaimed free of Pest risk analysis (PRA) Mediterranean fruit fly, Queensland fruit fly, and other exotic members of the Tephritidae (Federal Register, 1995b). There is an international standard for pest risk analysis (PRA) endorsed by the 1995 Food and Agriculture Organization Conference (Anonymous, 1996). PRA is typically done Production-based pest management in the recipient country but relies largely assurance systems on information provided by the producer country. For the discussion herein, it divides Ideally, an export quarantine security conveniently into probability of arrival and programme should be based on a holistic probability of establishment. The probability pest management system such as the model of pest arrival is more complex, if not of Jang and Moffitt (1994). Alone, a quality more difficult, to assess than the second, and control system structured in this way may includes the host status of the commodity, be adequate to meet the quarantine security seasonal pest incidence, field pest manage- required by an importing country; but this ment and handling procedures after harvest, can be difficult to demonstrate conclusively. all of which influence pest survival. It is Quarantine security assurance of this kind essential that any PRA be done with absolute works best when groups such as producers, objectivity. packers, exporters, and importers are all dedicated to a market. If the contribution of pest management systems to quarantine Pest-free area security is recognized, for the groups which have the potential to enable less severe treatment schedules, it can lead to a longer time Regulatory officials may declare areas within that these tropical fruits may remain in the a state, municipality, or district to be free of marketplace available for consumers. certain injurious pests. The area must meet certain criteria according to lawful codes and regulations. In most countries, a pest-free area or zone status needs to rely on the long-term Non-host status climatic unsuitability of production areas to the pest, islands separated by sea distance, Tropical fruits that are never attacked by mountainous areas, and major desert zones pests or are resistant to infestation by them with climatic extremes. Production areas are termed non-hosts of those pests. However, granted pest-free status need to be protected the condition can be difficult to determine, by quarantine prohibitions and monitored by and even more often difficult to understand. trapping or sampling to enable early detec- Reviews that discuss the term and its tion and eradication of incursions by the pest. concepts have been provided by Armstrong Ongoing protection can also be supported by (1994) and Greany (1994). The non-host status mass sterile release programmes if the pest of a commercially produced tropical fruit to a

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pest needs to be assessed in terms of the prob- and, often, one or more times when tropical abilities, both that it might become infested fruits are packed for shipment to markets. and that viable adults capable of initiating Inspection is done to find and remove pests a further generation could emerge from the not normally found with the tropical fruits. exported product. The susceptibility of tropi- Although not strictly tropical, stone fruits cal fruits to attack by a quarantine pest can from Chile present the risk of introducing differ because of several factors including various pests which do not normally feed the type of fruit, its physical characteristics, on stone fruits but which may be present in and its stage of physiological maturity and shipments of the fruit as hitch-hiking pests ripeness at the time of harvest. Perhaps the (Federal Register, 1989). Given that all widest use of non-host status is for trade of assumptions underlying a sampling plan bananas harvested at the stage of maturity can be met, inspection is a very powerful and ripeness commonly known as hard green. tool. Although normally labour-intensive Bananas at the preclimacteric hard-green and hence costly, it can provide a means by stage are recognized internationally as non- which trade can proceed when no treatment hosts of fruit flies of concern, although ripen- is available. Sampling and inspection need to ing bananas may be susceptible (Armstrong, be recognized more widely both as a bona 1994). Another example is ‘Solo’ papaya from fide treatment and as a component of an inte- the Costa Rica provinces of Guanacaste, San grated or holistic quarantine security system. Jose, and Puntarenas, which can be imported The USA often uses sampling and inspection into continental USA, Puerto Rico, and the US and, for example, permits the importation Virgin Islands (Federal Register, 1992a). of avocado fruits from New Zealand subject Rigid quality control in the packing house to inspection at the port of first arrival by ensures that the exact fruit physiological US plant quarantine inspectors. If pests are conditions required are met in order to found, then the avocados would be treated ensure non-susceptibility. If tropical fruit can to kill the pests (Federal Register, 1991). If be harvested at an early stage of ripeness that the avocados are never infested by a pest or is not subject to infestation by a pest, no treat- never used as a source of transportation (e.g. ment is required. If physical characteristics of hitch-hiker), then no need exists for a treat- tropical fruit, such as having a thick and hard ment, and the avocados may be imported. peel, preclude attack by a pest, then the fruit Use of a preclearance programme, involving may be able to be exported without treat- inspection by US or Japanese inspectors in ment. Gould et al. (1996) showed that Florida the country of origin, is another example of grown litchi, Litchi chinensis Sonn., cultivars eliminating a need for treatment. Other ways ‘Brewster’ and ‘Mauritius’, and longan, Dimo- to eliminate the requirement for a treatment carpus longan (Lour.), cultivar ‘Kohala‘, were include the establishment of pest-free areas non-hosts of Caribbean fruit fly, Anastrepha (Riherd et al., 1994), elimination of the pest suspensa (Loew), as long as the peel was intact from an area by eliminating host materials, and without any cut or opening. and use of sterile insect releases. ‘Hass’ avocado fruits from Mexico may enter the USA without treatment if the avocados are shipped to and consumed in Alaska (Federal Sampling and inspection Register, 1993b). Also, avocados from Hawaii may be imported into Alaska without treat- Statistical sampling theory has a long history ment. The US Department of Agriculture has of usage in industry as well as quarantine. concluded that climatic conditions in Alaska Guidelines are available to determine sample ensure that pests of avocados in Mexico and size for combinations of tolerance and statisti- Hawaii will not pose a risk to agriculture in cal confidence limits (Couey and Chew, that state and that the possibility that some 1986). Inspection of a sample of a consign- of the avocados might move from Alaska to ment of produce is part of most quarantine other states is almost nil (Federal Register, security systems. It is done at export, import, 1993b, 1994b). When quarantine measures

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such as pest risk analysis, the establishment Fumigation and maintenance of pest-free areas, proving non-host status, sampling and inspection are A fumigant is a toxic chemical released in the not successful, other means may be required, gaseous phase and dispersed in toxic concen- such as the use of a statistically proven trations so that it reaches pest species that successful single treatment, combinations of could be found either on the surface of the single treatments, and systems approaches. tropical fruit, under the calyx, in the naval areas of the tropical fruit, in the pulp tissues, and inside the seed(s). Concentration of the Single Treatments fumigant, time of exposure (C × T product), temperature and relative humidity, and load Individual treatments that provide quaran- factor (percentage of the chamber occupied tine security when they are used alone are by the commodity versus the size of the termed single treatments. Residue data as chamber) are critical to the efficacy of the appropriate should be included when a treat- treatment. Fumigants that control pests of ment uses a chemical. Data must show that tropical fruits include methyl bromide, the treatment residues do not exceed a Maxi- methyl iodide, ethylene dibromide, phos- mum Residue Level (MRL), an amount based phine, and hydrogen cyanide. Fumigation on good agricultural practice and usually practices and fumigants used for disinfesta- much lower than any health safety level. tion purposes have been reviewed by Stark Commodity tolerance to the treatment should (1994) and Yokoyama (1994). form part of the data required to establish the treatment. Selected examples of single Methyl bromide treatments used to control pests of tropical fruits are presented by Heather (1993a). Methyl bromide is a colourless, odourless gas, non-flammable in air, stable, and not corrosive. It has been used since the 1930s to disinfest agricultural warehouses, museums Insecticide application after harvest and homes, freight containers, processed commodities, fresh fruits and vegetables, Dimethoate and fenthion applied as dips ornamental foliage and cut flowers, and bulk or in-line flood sprays have proven to be grain. It is the principal fumigant used for highly effective disinfestation treatments to the postharvest treatment of a wide range of control Queensland fruit fly in tomatoes and food and non-food commodities by countries mangoes and Bactrocera cucumis (French), around the globe (APHIS, 1998). However, in members of the Cucurbitaceae (Heather, methyl bromide has been identified as a 1993a, 1994). Each insecticide is used at a significant ozone-depleting chemical and its −1 concentration of 400 mg l , and fruit is production and use by the USA are being dipped or flood sprayed for 1 min. Despite its restricted (Federal Clean Air Act, 1990; Anon- effectiveness to control pests, insecticide ymous, 1992). The US Congress recently applications after harvest pose problems with amended the Federal Clean Air Act of 1990 to residue, operator exposure, consumer accep- completely phase out the use of methyl bro- tance, and are not approved treatments in mide by 1 January 2005 (Anonymous, 1998). countries such as the USA and Japan, which differentiate between before and after harvest Methyl iodide application in their proclamation of MRLs. However, they are economical, logistically Also known as iodomethane, methyl iodide simple, and have fewer problems of product is a colourless, transparent liquid having a injury due to phytotoxicity than physical boiling point at 42.5°C. It is a stronger methy- treatments or fumigants, and they confer lating agent than methyl bromide, rapidly residual protection against any perceived risk destroyed by ultraviolet light, and probably of reinfestation subsequent to treatment. not likely to deplete the stratospheric ozone

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as does methyl bromide. It has been tested 15°C. Magnesium phosphide as plates was successfully as a soil fumigant to control developed to generate phosphine under con- fungi, nematodes, and weeds (Ohr et al., 1996; ditions of high relative humidity. It is also Zhang et al., 1997). In preliminary studies, available as phosphine in cylinders for direct Sharp and King (1997) showed that it con- application to a fumigation space. Phosphine trolled eggs and larvae of Caribbean fruit fly acts slowly and requires 5–12 days to control in vitro and in grapefruit and guavas. Guavas most pests. It is corrosive to metals, especially infested with eggs and larvae of the fly were copper electrical wiring. It is not currently fumigated for 2 h with doses of 16, 32, and approved for controlling pests of fresh tropi- 48 g m−3. Treated eggs and larvae did not sur- cal fruits because of the severe injury caused vive treatment at any of these doses. Treat- at dosages required to kill quarantine pests. ment of guavas infested in a similar manner It may also cause chromosome rearrange- and exposed to 16 g m−3 of methyl iodide for ment among operators (Garry et al., 1989). 20, 30, and 40 min resulted in 54%, 62%, and 64% mortality, respectively. Caribbean fruit Hydrogen cyanide fly eggs, 24 h old, obtained from a laboratory colony and exposed to 2, 4, and 8 g m−3 Hydrogen cyanide was one of the earliest for 30 min resulted in 24%, 49%, and 90% quarantine fumigants used in the 20th mortality, respectively. This study was the century. It is a colourless gas or liquid form- first to demonstrate that methyl iodide could ulated for fumigation as sodium cyanide, cal- be used to control a fruit fly quarantine pest. cium cyanide, or potassium cyanide. It is very The fumigant, however, is not registered for soluble in water and unsafe to use on moist use to control quarantine pests that attack materials. A solution of hydrogen cyanide in tropical fruits. water is a dilute acid, which renders tropical fruits unpalatable, perhaps hazardous for human consumption, and unmarketable due Ethylene dibromide to burn, wilt, and discoloration. Under very Ethylene dibromide is a colourless, non- controlled conditions, hydrogen cyanide is flammable liquid. Unti1 1983, the chemical used in California to kill surface pests such as was used extensively to control pests in many scales that attack fruits (Fiskaali, 1989). commodities. Beginning 28 September 1983, actions were taken by the US Environmental Protection Agency to remove ethylene Hot water immersion dibromide from the marketplace because it was found to be carcinogenic to mammals Some tropical fruits can be immersed in (Federal Register, 1983). It cannot be used to water heated to about 46°C for a time, usually treat fruit for consumption in the USA. It 1–2 h, to control pests without unacceptable is currently approved in some countries, loss of market quality. Fruit injury can be including Australia, but under conditions minimized by preconditioning some fruits of greatly reduced MRLs, which restrict such as mangoes to 37°C for 12 h before its usage. Because of the impending loss of immersion (Joyce and Shorter, 1994). Hot methyl bromide, questions have been raised water immersion is the preferred method to about the possibility of reinstatement of control tephritid fruit flies in mangoes in ethylene dibromide for some uses. continental USA. Fruit size is limited to 700 g for each mango imported into the USA Phosphine because data on the temperature and time mortality relationship required to control Phosphine (hydrogen phosphide) is a colour- fruit fly eggs and larvae have not been devel- less, flammable gas usually generated from oped for larger mangoes (APHIS, 1998). This an aluminium phosphide tablet or pellet is not a major problem since most retail preparations activated when exposed to marketed mangoes are in the vicinity moisture in the air at temperatures above of 450–500 g. Nevertheless, some mango

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producers in Caribbean countries and Mexico are approved for mango from South-East Asia have requested that the US Department of and Australia for the markets in Japan and for Agriculture develop a hot water immersion citrus, papaya, and pineapple for markets in quarantine treatment that controls fruit fly the USA (APHIS, 1998). Vapour heat, depend- pests in mangoes weighing more than 700 g. ing on temperature and air flow rate, is not Studies are underway to determine the time as efficient a heat conductor as hot water. of exposure in water at 46.7°C required to Application of vapour heat as a quarantine control fruit flies such as West Indian fruit fly, treatment was first used to control Mediterra- Anastrepha obliqua (Macquart), eggs and lar- nean fruit fly in grapefruit in Florida in 1929 vae present in ‘Keitt’ mangoes weighing up (Hallman and Armstrong, 1994). The appli- to 950 g. McGuire and Sharp (1997) reported cation was crude but effective. As with hot that ‘Keitt’ mangoes weighing 701–950 g water, time of exposure and target tempera- immersed in water at 48°C without pre- ture needed to control pests are critical fac- conditioning were damaged at the exposure tors that influence market quality of treated times of 180 min, a time of exposure believed fruits. Vapour heat treatment temperatures necessary to control fruit fly eggs and larvae usually range between 40 and 47°C and that might be present in the larger mangoes. require several hours of exposure. Time of Due to the success of the hot water exposure needed to reach a target tempera- immersion treatment to control fruit fly eggs ture can be controlled depending on the tem- and larvae that attack mangoes, the number perature and the flow rate of the saturated air of commercial hot water treatment facilities as it passes over the fruit as well as the type of in Mexico, Caribbean countries, Central fruit treated, size, and density of the load. and South America could soon exceed 100 (P. Whiterell, USDA-APHIS, North Carolina, 1998, personal communication). The major Forced air heating supplier of hot water treatment equipment has been the USA. Mangoes treated with hot A system of heating tropical fruits using water benefit from the treatment because post- forced air that is heated, humidified, and cir- harvest decay-forming organisms are reduced culated around fruit was developed in Japan or killed, thus extending the shelf life of the and termed a differential pressure–vapour fruit, and the fruit are also cleaned by the treat- heat process (Sugimoto et al., 1983). Unfortu- ment. Australia uses locally manufactured nately this was abbreviated to vapour heat hot water–benlate dips set at around 52°C for and has become confused with the original 5–10 min to control diseases of mango fruit vapour heat treatment developed in the USA. after harvest (Johnson et al., 1997). The longer The Japanese vapour heat treatment system times necessary for fruit fly control have is used for exports of mango and papaya resulted in fruit damage when attempted from the Philippines, Hawaii, Thailand, and commercially on the predominant ‘Kensing- Australia to Japan and is accepted primarily ton’ variety (Johnson and Heather, 1994). Hot by world markets located in South-East water is a preferred method used to control Asia, Malaysia, and Australia. New Zealand fruit fly pests in a variety of tropical fruits that is another country currently developing tolerate the treatment (Smith, 1992; Corcoran forced air heating–disinfestation treatment et al., 1993; Sharp, 1994; Waddell et al., 1997). equipment. Typical fruit fly disinfestation schedules for mangoes treated with forced air heating are based on fruit temperatures at the Vapour heat seed surface 46–47°C held for up to 15 min (Heather et al., 1997). Heated air that is saturated with water vapour Air that is heated but humidified below has been used successfully to control fruit the level at which condensation occurs on the flies in mango, papaya, and citrus in the USA treated fruit has been termed heated air (Sharp since around 1930. Vapour heat treatments et al., 1991) or high temperature forced air

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(Armstrong et al., 1989). Recently developed the storage time. Citrus, litchi, guava, and treatments first use low then high humidity carambola can be treated with cold tem- air within the same treatment cycle to reduce perature, but mangoes are damaged at tem- fruit injury without loss of efficiency (Una- perature and time combinations required to hawutti et al., 1992). Thermal heating with control pests. Hill et al. (1988), Jessup et al. air becomes less efficient as the humidity (1993), and Heather et al. (1996) reported dis- is decreased, but some fruits tolerate treat- infestation treatments of Australian-grown ment better with this system compared with oranges, lemons, and mandarins that control- immersion in heated water. Fruits such as led Mediterranean fruit fly and Queensland citrus do not tolerate hot water immersion fruit fly with storage times of 16 or 14 days at treatment, but the market quality of citrus is 1°C. Armstrong et al. (1995b) demonstrated not adversely affected by forced heated air. that the cold temperature and exposure time Sharp (1993a), Mangan and Ingle (1994) and combinations needed to control Mediterra- Sharp and McGuire (1996) demonstrated that nean fruit fly, oriental fruit fly, and melon fly tephritid fruit flies are controlled in citrus in Hawaiian-grown carambolas were about with hot air without damaging the fruit. the same as those shown by Gould and Sharp Also, Armstrong et al. (1995a) reported that (1990). Mediterranean fruit fly, oriental fruit fly, Bactrocera dorsalis (Hendel), and melon fly, Bactrocera cucurbitae Coquillett in Hawaii were Controlled (modified) atmospheres controlled in papaya with forced hot air without fruit injury. The US Department A modified atmosphere maintained with of Agriculture approved the use of forced air almost no variation in gas compositions is heating to control pests of mango and grape- called a controlled atmosphere. Examples of fruit from Mexico imported into the USA controlled or modified atmospheres used to (Federal Register, 1995a), and for tangerines, control pests of tropical fruits are elevated oranges (except for navel oranges), and grape- concentrations of carbon dioxide, reduced fruit from Mexico and areas of the USA oxygen levels, combinations of the two, or in Texas and California (Federal Register, the incorporation of nitrogen gas at different 1997b). Also, Gould (1996) reported that concentrations. The gaseous mixtures are papaya fruit fly, Toxotrypana curvicauda contained in a confined space where the Gerstaecker, eggs and larvae were controlled tropical fruits are exposed to different in papaya exposed to forced air heat at 48°C temperatures and time periods. Each fruit for 167 min. cultivar varies in its response to a particular modified atmosphere with respect to fruit quality. Usually, however, modified atmo- Cold temperature spheres extend the market life of the fruits and control pests. Exposure of the tropical Cold storage at temperatures above 0°C fruits usually requires several days of treat- is used to disinfest different fruits (Gould, ment to particular mixes of gasses at elevated 1994). Treatments can require up to 3 weeks temperatures to control pests. of cold storage after the commodity has Carpenter and Potter (1994) reviewed reached the temperature to achieve total the literature on controlled atmosphere dis- disinfestation of quarantine pests. For fruit infestation. Whiting et al. (1995) showed that flies the time required for cold storage varies disinfestation of fruit to control Tortricidae greatly from species to species, but this is in a modified atmosphere was accelerated at probably related more to the disjunct origins a temperature of 40°C. Whiting and van den of the underlying research. For example, Heuvel (1995) controlled diapausing adult applicability of the method depends on the two-spotted spider mites, Tetranychus urticae cold tolerance of the pest relative to that of Koch, with various controlled atmosphere the host commodity, the temperature, and treatments applied at 20 and 40°C.

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Coatings and wraps molecules and convert them to ions. Gamma rays and X-rays form part of the electro- Atmospheres also may be altered by use of magnetic spectrum. Gamma rays are pro- film wraps and fruit coatings (Hallman et al., duced by the spontaneous disintegration of 1994). Coatings trap gases inside the fruits radionuclides. Cobalt-60 and caesium-137 are and restrict gaseous exchange. Methyl cellu- the radionuclides used exclusively to sterilize lose and shellac, when applied to the surface food and medical products which form the of fruits, can cover eggs and trap surface basis of a commercial industry. Cobalt-60 is pests and seal them, resulting in the death of produced by neutron bombardment of the the pest presumably by suffocation. Internal metal cobalt-59 inside a nuclear reactor, then feeding pests are believed to be controlled by double encapsulated in stainless steel pencils atmospheres that are modified inside coated to prevent any leakage during its use in a fruits. Usually, carbon dioxide levels are radiation plant. Cobalt-60 has a half-life of 5.3 increased and oxygen levels are decreased in years. Caesium-137 is produced by reprocess- the pulp tissue. ing used nuclear fuel elements and is not Coatings such as Prima Fresh 31 (S.C. in widespread commercial use. Caesium-137 Johnson and Son, Racine, WI) contain amine has a half-life of 30 years. Neither of these fatty acid soap, waxes, and food-grade shellac. sources gives rise to radiation levels in the When applied as a coating, Prima Fresh 31 treated commodity which could cause radio- reduced the number of immature Caribbean activity, due to the inherently low energy fruit fly in grapefruit and guava but was not levels. adequate as a single treatment (Hallman et al., Machines capable of producing high 1994, 1995). Prima Fresh 31, however, killed all energy electron beams by accelerating elec- exposed eggs, nymphs and adults of Chilean trons are machine sources of radiation. A false spider mite on cherimoya from Chile that beam of accelerated electrons from a linear were immersed in the wax material (Thomp- accelerator is used to directly irradiate the son, 1990; Undurraga and Lopez, 1992). commodity to be disinfested or to bombard Incorporation of insect growth regulators a metal target and produce X-rays to which such as 20% methoprene with wax when the commodity is exposed. Electron machines applied to papaya was reported by Saul and capable of accelerating electrons produce high Seifert (1990) to control Mediterranean fruit energy electron beams, but electron beams fly, oriental fruit fly, and melon fly eggs and cannot penetrate deeply into fruits and are larvae at the 99.9968% efficacy level. limited to a maximum of about 4 cm or fruit 8 cm in diameter. Cobalt-60 and caesium-137 gamma rays will penetrate more than a metre through bulk commodities, although their Irradiation strength is attenuated requiring rotation to achieve a uniform dosage at the outside and Irradiation is a proven method of disinfesting reduced dosage at the centre. The difference tropical fruits and many other agricultural is known as the minimum–maximum ratio commodities of quarantine pests (Komson (expressed as Dmin and Dmax) and varies et al., 1987; Heather, 1993b; Burditt, 1994). The with the commodity and geometry of the American Society for Testing and Materials irradiator. Machine sources may be preferred published a standard (guide) that explains by some users because no radioactive materi- dosimetry in radiation research on food and als are used, and when the radiation process is agricultural products (ASTM, 1997). Irradia- completed, the power to the machine is turned tion treatment of the fruit is done by exposure off. Their disadvantage lies in their very high to an ionizing energy source which can be capital cost and mechanical complexity com- gamma rays, X-rays, or accelerated electrons. pared with cobalt source irradiators, which is Such radiations are referred to as ionizing the type most widely used by the industry. radiations because their energy is great The process cannot increase the normal radio- enough to dislodge electrons from atoms and activity level of the fruit, regardless of the

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exposure time or the dose used to treat the ethylene dibromide and methyl bromide used fruit. Radiation affects rapidly dividing cells as fumigants, irradiation is becoming a more in arthropods and living plant products and accepted type of quarantine treatment. The slows the development of colour and ripening US Food and Drug Administration regulates of fruits and vegetables. Some types of living the use of irradiation in the USA and permits plant structures, such as fruits, tolerate radia- consumption there of fresh fruits treated with tion treatment better than others, thus allow- irradiation doses up to 1 kGy. For spices and ing them to be treated to control pests. herbs, 30 kGy is allowed (Federal Register, Radiation dose is the amount of radiation 1986). Many publications present literature energy absorbed by the fruit as it passes reviews for irradiation as a quarantine treat- through the radiation field (Federal Register, ment (Moy, 1985; IAEA, 1992; Anonymous, 1996a). The Gray (Gy) is currently the accep- 1993). The International Atomic Energy ted Système International (SI) unit. One Gy is Agency, Vienna, Austria, published a booklet equal to 0.001 kilogray (kGy), 100 rad, or 0.1 in 1991 that discussed facts about food irradia- kilorad, terms that were often used in the past. tion (Anonymous, 1991). The booklet contains A working group of the International Consul- 14 fact sheets that explain the food irradiation tative Group on Food Irradiation (ICGFI) con- process and is available by writing to: The cluded that a minimum absorbed dose of 150 ICGFI Secretariat, Joint FAO/IAEA Division Gy would provide quarantine security against of Nuclear Techniques in Food and Agri- all species of Tephritidae and 300 Gy would culture, Wagramerstrasse 5, PO Box 100 provide quarantine security against most A-1400, Vienna, Austria. other arthropod pests (ICGFI, 1994). The US Department of Agriculture has accepted irradiation as a quarantine treatment and developed schedules of irradiation doses Microwave energy against fruit flies of from 150 to 250 Gy to treat commodities for movement from Hawaii to Microwaves are radio frequency waves (not the mainland USA and to allow carambola heat energy). However, microwave energy is and litchi to be moved from Hawaii with converted to heat by interaction with charged a minimum irradiation treatment dose of particles and polar molecules. The agitation 250 Gy (Federal Register, 1996a,b, 1997a). The is evidenced as heat. Microwaves in the elec- same agency has reviewed the literature con- tromagnetic spectrum ranging from 10 kHz cerning irradiation for pests of tropical fruits to 100 GHz have been used to heat objects and recommended a minimum dose to control by converting electromagnetic energy to heat seven major economically important species energy and are a potential quarantine treat- of tephritid fruit flies with doses ranging from ment method to control some insect pests and 150 to 250 Gy depending on the species. These also to study the biology of treated pests due required doses far exceed research results to various heating rates (Hallman and Sharp, on some species. For example, Heather et al. 1994; Sharp et al., 1999). Microwave energy (1991) demonstrated a maximum requirement impinging on spherical and cylindrical prod- for > 99.9968% efficacy of < 100 Gy for both ucts is focused toward their centres (Buffler, Queensland fruit fly and Jarvis fruit fly, 1993). Sharp (1993b, 1996) studied heating Bactrocera jarvisi (Tryon). Use of the lowest profiles in different fruits by exposing them dose that will meet the minimum efficacy to various heating rates with a research- required by an importing country will reduce quality microwave oven and developed time the possibility of product injury. and temperature data at various powers, The USA recently assumed leadership which could be used to control pests. Subse- in using irradiation as a quarantine pest dis- quently, Sharp et al. (1999) studied the effects infestation treatment, largely because of the of rapid heating on the mortality of mature objections raised by activist consumer groups. larvae of Caribbean fruit fly and found that However, with a better informed public and rapid heating failed to control the larvae at the loss of highly effective chemicals such as temperatures normally lethal to the larvae.

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The studies also showed that at controlled requirements for growing, treating, packing, power levels larvae can be killed, perhaps and shipping, field sanitation, fruit fly trap- without significant damage to the treated ping, and issuance of a phytosanitary certifi- fruit. Until cost efficient ways can be found cate (Federal Register, 1998). Also, treatments to obtain precise consistent temperatures, the must be consumer safe, environmentally microwave method is unlikely to be adopted friendly, and easy to regulate and enforce. commercially. ‘Magic bullet’ treatments such as ethylene dibromide and methyl bromide fumigations are no longer available for use in many parts of Combination Treatments the world. The difficult challenge is to develop successful new strategies following the loss of Two or more single treatments used simulta- these chemicals. neously or sequentially to provide quarantine security are combination treatments (Mangan and Sharp, 1994). Examples of such treat- Conclusion ments are modified atmosphere followed by fumigation, modified atmosphere plus Until tropical fruits are produced in pest-free temperature, and refrigeration followed by enclosures and remain free of exposure to fumigation. Grapes grown in Australia may pests or until fruits are genetically altered to be imported into the USA after refrigeration be resistant to pests, quarantine treatments in transit and then fumigation at the port and methodologies will be required to con- of arrival (Federal Register, 1990). Another trol pests that attack tropical fruits. The risk example of a combination treatment is soapy that new pest introductions will be encoun- water immersion followed by immersion tered increases, for example, as world popu- in wax to control Chilean false spider mite, lations increase, fruit production and inter- Brevipalpus chilensis (Baker), on cherimoya national trade increase, and as new markets and limes from Chile (Federal Register, are created to provide fresh fruits to a grow- 1992b; APHIS, 1998), and use of warm soapy ing population of consumers over the globe. water and brushing to control external pests The expansion of air travel allows rapid such as scales and mealybugs on durian shipment of fruits within hours from one (APHIS, 1998). side of the globe to the another. Contraband commodities carried by travellers who fail to heed quarantine requirements are arguably Systems approach the greatest risk of introduction of new pests to an area. Access for commercial produce Jang (1996) discussed a systems approach to under conditions of low quarantine security quarantine security to control Mediterranean risk removes much of the temptation for fruit fly, oriental fruit fly, and melon fly in travellers to carry it as high risk contraband. ‘Sharwil’ avocado fruits grown in Hawaii. To keep the cost of tropical fruits low Components of systems approaches for consumers, quarantine treatments must include seasonal pest incidence determined be affordable. New treatments must be easily by surveys, trapping for basic levels of adapted by industry and be economical to incidence in the production area, sampling, use. Average costs to build facilities that use pest management in the field, inundative hot water, forced hot air, vapour heat, and sterile insect releases, cultural practices, host irradiation currently range from US$200,000 resistance, safeguards after harvest, inspec- to US$3,000,000 (Anonymous, 1991; US Envi- tion, and quality control (Jang and Moffitt, ronmental Protection Agency, 1996). Estima- 1994; Jang, 1996). An example of the systems ted costs for using controlled atmospheres approach is the importation into the USA are US$5000 per container per shipment (US of papayas from Brazil and Costa Rica. Environmental Protection Agency, 1995). All Conditions of entry into the USA include costs are expected to increase.

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References Research on Food and Agricultural Products. Designation: E1900–97, 9 pp. Anonymous (1991) Facts About Food Irradiation.A Baker, A.C. (1939) The basis for treatment of prod- Series of Fact Sheets from the International ucts where fruitflies are involved as a condition Consultative Group on Food Irradiation, for entry into the United States. US Department IAEA/PI/A33E, 91–05549. International of Agriculture Circular 551. Atomic Energy Agency. Vienna, Austria, Baker, R.T., Cowley, J.M., Harte, D.S. and Frampton, 38 pp. E.R. (1990) Development of a maximum pest Anonymous (1992) United Nations Environmental limit for fruit flies (Diptera: Tephritidae) in Programme. Methyl bromide: atmospheric sci- produce imported into New Zealand. Journal of ence, technology and economics. UN Head- Economic Entomology 83, 13–17. quarters, Ozone Secretariat, Nairobi, Kenya. Buffler, C.R. (1993) Microwave Cooking and Pro- Anonymous (1993) Cost–benefit aspects of food cessing: Engineering Fundamentals for the Food irradiation processing. In: Proceedings of Sym- Scientist. Van Nostrand Reinhold, New York, posium. Aix-En-Provence, 1–5 March. Interna- 166 pp. tional Atomic Energy Agency, Vienna, 505 pp. Burditt, Jr, A.K. (1994) Irradiation. In: Sharp, J.L. and Anonymous (1996) International Standards for Phyto- Hallman, G.J. (eds) Quarantine Treatments for sanitary Measures. Part 1 – Import Regulations. Pests of Food Plants. Westview Press, Boulder, Guidelines for Pest Risk Analysis. Secretariat of Colorado, pp. 101–117. IPPC, FAO of UN, Rome, 21 pp. Carpenter, A. and Potter, M. (1994) Controlled Anonymous (1998) Changes to Methyl Bromide Atmospheres. In: Sharp, J.L. and Hallman, G.J. Phaseout in the United States. http//:www.epa. (eds) Quarantine Treatments for Pests of Food gov/ozone/mbr/harmoniz/html Plants. Westview Press, Boulder, Colorado, APHIS (Animal and Plant Health Inspection pp. 171–198. Service) (1998) Plant Protection and Quarantine Champ, B.R., Highley, E. and Johnson, G.I. (eds) Treatment Manual. US Department of Agri- (1993) Postharvest Handling of Tropical Fruits. culture. US Government Printing Office, Proceedings of an International Conference. Washington, DC. Chiang Mai, Thailand, 19–23 July 1993. Austra- AQIS (Australian Quarantine and Inspection Ser- lian Centre for International Agricultural vice) (1991) The Application of Risk Management Research Proceedings No.50, 500 pp. in Agricultural Quarantine Import Assessment. Chew, V. (1994) Statistical methods for quarantine AGPS, Canberra, 33 pp. treatment data analysis. In: Sharp, J.L. and Armstrong, J.W. (1994) Commodity resistance to Hallman, G.J. (eds) Quarantine Treatments for infestation by quarantine pests. In: Sharp, J.L. Pests of Food Plants. Westview Press, Boulder, and Hallman, G.J. (eds) Quarantine Treatments Colorado, pp. 33–46. for Pests of Food Plants. Westview Press, Corcoran, R.J., Heather, N.W. and Nimmo, A.L. Boulder, Colorado, pp. 199–211. (1993) Comparative heat response of eggs of Armstrong, J.W., Hansen, J.D., Hu, B.K.S. and the Queensland fruit fly, Bactrocera tryoni Brown, S.A. (1989) High-temperature forced- and Mediterranean fruit fly, Ceratitis capitata. air quarantine treatment for papaya In: Proceedings, Australasian Postharvest Confer- infested with tephritid fruit flies (Diptera: ence. 20–24 September 1993. The University Tephritidae). Journal of Economic Entomology of Queensland, Gatton College, Lawes, 82, 1667–1674. Queensland 4343, Australia, pp. 303–307. Armstrong, J.W., Hu, B.K.S. and Brown, S.A. (1995a) Couey, H.M. and Chew, V. (1986) Confidence limits Single-temperature forced hot-air quarantine and sample size in quarantine research. Journal treatment to control fruit flies (Diptera: of Economic Entomology 79, 887–890. Tephritidae) in papaya. Journal of Economic Federal Clean Air Act (1990) Public Law 101–549, Entomology 88, 678–682. enacted 15 November 1990. Washington, DC. Armstrong, J.W., Silva, S.T. and Shishido, V.M. Federal Register (1983) Environmental Protection (1995b) Quarantine cold treatment for Agency. Notices. Tuesday, 11 October 1983. Hawaiian carambola fruit infested with OPP-30000/25D; PH-FRL 2450-1. Ethylene Mediterranean fruit fly (Diptera: Tephritidae) dibromide; intent to cancel registrations of eggs and larvae. Journal of Economic Entomology pesticide products containing ethylene 88, 683–687. dibromide; determination concluding the ASTM (American Society for Testing and Materials) rebuttable presumption against registration; (1997) Standard Guide for Dosimetry in Radiation availability of position document. Federal Register 48 (197), 46234–46248.

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Federal Register (1986) Department of Health and Rules and Regulations. Wednesday, 28 Human Services. Food and Drug Administra- December 1994.7 CFR Part 318. Docket tion, Part I11. Friday 18 April 1986.21 CFR Part No. 93-088-2. Avocados from Hawaii. Federal 179. Irradiation in the production, processing, Register 59(248), 66638–66642. and handling of food; final rule. Federal Register Federal Register (1995a) Department of Agriculture. 51 (75), 13376–13399. Animal and Plant Health Inspection Service. Federal Register (1989) Department of Agriculture. Rules and Regulations. Monday, 6 February Animal and Plant Health Inspection Service. 1995.7 CFR Parts 300 and 319. Docket No. Proposed Rules. Thursday, 13 July 1989.7 CFR 93-028-5. Grapefruit and mangoes from Part 319. Docket No. 88-176. Apricots, nectar- Mexico; addition of treatment. Federal Register ines, peaches, and plums from Chile. Federal 60(24), 6957–6958. Register 54(133), 29566–29569. Federal Register (1995b) Department of Agriculture. Federal Register (1990) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Proposed Rules. Monday, 11 September 1995.7 Rules and Regulations. Tuesday, 26 June 1990. CFR 319. Docket No. 93-119-1. Importation of 7 CFR Parts 300 and 319. Docket No.90-039. citrus fruits from Australia. Federal Register Importation of grapes from Australia. Federal 60(175), 47101–47103. Register 55(123), 25950–25954. Federal Register (1996a) Department of Agriculture. Federal Register (1991) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Rules and Regulations. Wednesday, 15 Rules and Regulations. Wednesday, 15 May May 1996.7 CFR Part 319. Docket No. 1991.7 CFR Part 319. Docket No.91-039. Impor- 95-088-1. The application of irradiation to tation of avocados from New Zealand. Federal phytosanitary problems. Federal Register Register 56(94), 22295–22297. 61(95), 24433–24439. Federal Register (1992a) Department of Agriculture. Federal Register (1996b) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Proposed Rules. Friday, 3 January 1992. 7 CFR Proposed Rules. Tuesday, 23 July 1996.7 CFR Part 319. Docket No.91-068. Importation of Part 318. Docket No. 95-069-1. Papaya, caram- papayas from Costa Rica. Federal Register 57(2), bola, and litchi from Hawaii. Federal Register 217–219. 61(142), 38108–38114. Federal Register (1992b) Department of Agriculture. Federal Register (1997a) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Rules and Regulations. Monday, 30 November Rules and Regulations. Thursday, 10 July 1997. 1992.7 CFR Part 319. Docket No.91-160-2. 7 CFR Parts 300 and 318. Docket No.95-069-2. Importation of cherimoyas from Chile. Federal Papaya, carambola, and litchi from Hawaii. Register 57(230), 56434–56437. Federal Register 62(132), 36967–36976. Federal Register (1993a) Department of Agriculture. Federal Register (1997b) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Rules and Regulations. Tuesday, 25 February Proposed Rules. Tuesday, 30 December 1997. 7 1994.7 CFR Part 319. Docket No.92-126-2. CFR Parts 300 and 301. Docket No.96-069-1. Honeydew melons from Brazil. Federal Register High-temperature forced-air treatments for 58 (36), 11363–11364. citrus. Federal Register 62(249), 67761–67764. Federal Register (1993b) Department of Agriculture. Federal Register (1998) Department of Agriculture. Animal and Plant Health Inspection Service. Animal and Plant Health Inspection Service. Rules and Regulations. Tuesday, 27 July 1993. Rules and Regulations. Friday, 13 March 1998. 7 CFR Part 319. Docket No. 92-111-3. Hass 7 CFR Part 319. Docket No.96–046–5. Importa- avocados from Mexico. Federal Register 58(142), tion of fruits and vegetables; papayas from 40033–40037. Brazil and Costa Rica. Federal Register 63(49), Federal Register (1994a) Department of Agriculture. 12383–12396. Animal and Plant Health Inspection Service. Fiskaali, D.A. (ed.) (1989) California Commodity Rules and Regulations. Monday, 28 February Treatment Manual, Vol 1. Treatments. State of 1994.7 CFR Part 319. Docket No.93-095-2. California Department of Food and Agri- Importation of apples, apricots, peaches, culture, 342 pp. persimmons, pomegranates, and citrus for Garry, V.F., Griffith, J., Danzl, T.J., Nelson, R.L., Sonora. Federal Register 59(39), 9381–9382. Whorton, E.B., Krueger, L.A. and Cervenka, J. Federal Register (1994b) Department of Agriculture. (1989) Human genotoxicity: pesticide applica- Animal and Plant Health Inspection Service. tors and phosphine. Science 246, 251–255.

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Gould, W.P. (1994) Cold storage. In: Sharp, J.L. and Heather, N.W. (1994) Pesticide quarantine treat- Hallman, G.J. (eds) Quarantine Treatments for ments. In: Sharp, J.L. and Hallman, G.J. Pests of Food Plants, Westview Press, Boulder, (eds) Quarantine Treatments for Pests of Food Colorado, pp. 119–132. Plants. Westview Press, Boulder, Colorado, Gould, W.P. (1996) Mortality of Toxotrypana pp. 89–100. curvicauda (Diptera: Tephritidae) in papayas Heather, N.W., Corcoran, R.J. and Baños, C. exposed to forced hot air. Florida Entomologist (1991) Disinfestation of mangoes against two 79, 407–413. Australian fruit flies (Diptera: Tephritidae). Gould, W.P. and Sharp, J.L. (1990) Cold-stor- Journal of Economic Entomology 84, 1304–1307. age quarantine treatment for carambolas Heather, N.W., Whitfort, L., McLaughlan, R.L. infested with the Caribbean fruit fly (Diptera: and Kopittke, R.A. (1996) Cold disinfestation Tephritidae). Journal of Economic Entomology 83, of Australian mandarins against Queensland 458–460. fruit fly (Diptera: Trypetidae). Postharvest Gould, P., Nguyen, R., Hennessey, M.K., Sharp, J.L. Biology and Technology 8, 307–315. and Crane, J. (1996) Infestation studies on Heather, N.W., Corcoran, R.J. and Kopittke R.A. lychees and longans to determine their host (1997) Hot air disinfestation of Australian status in relation to the Caribbean fruit fly. Pro- ‘Kensington’ mangoes against two fruit flies ceedings of the Florida State Horticultural Society (Diptera: Tephritidae). Postharvest Biology and 109, 276–277. Technology 10, 99–105. Greany, P.D. (1994) Plant host status and natural Hill, A.R., Rigney, C.J. and Sproul, A.N. (1988) Cold resistance. In: Paull, R.E. and Armstrong, J.W. storage of oranges as a disinfestation treatment (eds) Insect Pests and Fresh Horticultural against the fruit flies Dacus tryoni (Froggatt) Products. Treatments and Responses. CAB and Ceratitis capitata (Wiedemann) (Diptera: International, Wallingford, UK, 360 pp. Tephritidae). Journal of Economic Entomology 81, Hallman, G.J. and Armstrong, J.W. (1994) Heated air 257–260. treatments. In: Sharp, J.L. and Hallman, G.J. ICGFI (1994) Irradiation as a Quarantine Treatment of (eds) Quarantine Treatments for Pests of Food Fresh Fruits and Vegetables. A Report of the Plants. Westview Press, Boulder, Colorado, Working Group Convened by ICGFI (1994). 149–163. ICGFI Document No. 17, 40 pp. Hallman, G.J. and Sharp, J.L. (1994) Radio frequency International Atomic Energy Agency (1992) Use of heat treatments. In: Sharp, J.L. and Hallman, Radiation as a Quarantine Treatment of Food and G.J. (eds) Quarantine Treatments for Pests of Food Agricultural Commodities. Proceedings of the Final Plants. Westview Press, Boulder, Colorado, Research Coordination Meeting. Kuala Lumpur, pp. 165–170. Malaysia, 27–31 August 1990. IAEA, Vienna, Hallman, G.J., Nisperos-Carriedo, M.O., Baldwin, Austria, 220 pp. E.A. and Campbell, C.A. (1994) Mortality Jang, E.B. (1996) Systems approach to quarantine of Caribbean fruit fly (Diptera: Tephritidae) security: postharvest application of sequential immatures in coated fruits. Journal of Economic mortality in the Hawaiian grown ‘Sharwil’ Entomology 87, 752–757. avocado system. Journal of Economic Ento- Hallman, G.J., McGuire, R.G., Baldwin, E.A. and mology 89, 950–956. Campbell, C.A. (1995) Mortality of feral Carib- Jang, E.B. and Moffitt, H.R. (1994) Systems bean fruit fly (Diptera: Tephritidae) immatures approaches to achieving quarantine secu- in coated guavas. Journal of Economic Entomol- rity. In: Sharp, J.L. and Hallman, G.J. ogy 88, 1353–1355. (eds) Quarantine Treatments for Pests of Food Heather, N.W. (1993a) Quarantine disinfestation Plants. Westview Press, Boulder, Colorado, of tropical fruits: non-chemical options. In: pp. 225–237. Champ, B.R., Highley, E. and Johnson, G.I. Jessup, A.J., de Lima, C.P.F., Hood, C.W., Sloggett, (eds) Postharvest Handling of Tropical Fruits. R.F., Harris, A.M. and Beckingham, M. (1993) The Australian Centre for International Quarantine disinfestation of lemons against Agricultural Research (ACIAR) Proceedings Bactrocera tryoni and Ceratitis capitata (Diptera: No.50, ACIAR, Canberra, pp. 272–279. Tephritidae) using cold storage. Journal of Heather, N.W. (1993b) Irradiation as a quarantine Economic Entomology 86, 795–802. treatment of agricultural commodities against Johnson, G.I. and Heather, N.W. (1994) Disease and arthropod pests. Management of Insect Pests: pest control in tropical fruits. In: Champ, B.R. Nuclear and Related Molecular and Genetic Tech- and Highley, E. Postharvest Technology for Agri- niques. International Atomic Energy Agency, cultural Products in Vietnam. ACIAR Proceed- Vienna, Austria, pp. 627–640. ings No.60, ACIAR, Canberra, pp. 100–126.

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Johnson, G.I., Sharp, J.L., Milne, D.L. and Quarantine Treatments for Pests of Food Plants. Oosthuyse, S.A. (1997) Postharvest technology Westview Press, Boulder, Colorado, pp. 47–65. and quarantine treatments. In: Litz, R.L. (ed.) Saul, S. and Seifert, J. (1990) Methoprene on The Mango: Botany, Production and Uses. CAB papayas: persistence and toxicity to different International, Wallingford, UK, pp. 447–507. developmental stages of fruit flies (Diptera: Joyce, D.C. and Shorter, A.J. (1994) High- Tephritidae). Journal of Economic Entomology 83, temperature conditioning reduces hot water 901–904. treatment injury of ‘Kensington Pride’ mango Shannon, M.J. (1994) APHIS. In: Sharp, J.L. and fruit. HortScience 29, 1047–1051. Hallman, G.J. (eds) Quarantine Treatments for Komson, P., Sutantawong, M., Smitasiri, E., Pests of Food Plants. Westview Press, Boulder, Lapasatukul, C. and Unahawutti, U. (1987) Colorado, pp. 1–10. Irradiation as a quarantine treatment for the Sharp, J.L. (1993a) Hot-air quarantine treatment for oriental fruit fly Dacus dorsalis Hendel in man- ‘Marsh’ white grapefruit infested with Carib- goes. Modern Insect Control: Nuclear Techniques bean fruit fly (Diptera: Tephritidae). Journal of and Biotechnology. IAEA Vienna, pp. 319–324. Economic Entomology 86, 462–464. Mangan, R.L. and Ingle, S.J. (1994) Forced hot-air Sharp, J.L. (1993b) Microwaves as a quarantine quarantine treatment for grapefruit infested treatment to disinfest commodities of pests. In: with Mexican fruit fly (Diptera: Tephritidae). Champ, B.R., Highley, E. and Johnson, G.I. Journal of Economic Entomology 87, 1574–1579. (eds) Postharvest Handling of Tropical Fruits. Pro- Mangan, R.L. and Sharp, J.L. (1994) Combination ceedings of an International Conference. Chiang and multiple treatments. In: Sharp, J.L. and Mai, Thailand, 19–23 July 1993, No.50. Austra- Hallman, G.J. (eds) Quarantine Treatments for lian Centre for International Agricultural Pests of Food Plants. Westview Press, Boulder, Research, Canberra, Australia, 500 pp. Colorado, pp. 239–247. Sharp, J.L. (1994) Hot water immersion. In: Sharp, McGuire, R.G. and Sharp, J.L. (1997) Quality of J.L. and Hallman, G.J. (eds) Quarantine Treat- colossal Puerto Rican ‘Keitt’ mangoes after ments for Pests of Food Plants. Westview Press, quarantine treatment in water at 48°C. Tropical Boulder, Colorado, pp. 133–147. Science 37, 154–159. Sharp, J.L. (1996) Microwave heating of agricultural Moy, J.H. (1985) Radiation Disinfestation of Food and products. In: Vijaysegaran, S., Pauziah, M., Agricultural Products. Proceedings of an Inter- Mohamed, M.S. and Ahmad Tarmizi, S. (eds) national Conference. Honolulu, Hawaii, 14–18 Proceedings of the International Conference on November 1983. Hawaii Institute of Tropical Tropical Fruits, Vol. II, Kuala Lumpur, Agriculture and Human Resources. University Malaysia, 23–26 July 1996. Malaysian Agri- of Hawaii at Manoa, Honolulu, Hawaii, 424 pp. cultural Research and Development Institute, Ohr, H.D., Sims, J.J., Grech, N.M., Becker, J.O. Malaysia, pp. 329–343. and McGiffen, M.E. Jr (1996) Methyl iodide, Sharp, J.L. and Hallman, G.J. (1994) Quarantine an ozone-safe alternative to methyl bromide Treatments for Pests of Food Plants. Westview as a soil fumigant. Plant Disease 80, 731–735. Press, Boulder, Colorado, 290 pp. Paul, R. and Armstrong, J.W. (1994) Insect Pests Sharp, J.L. and King, J.R. (1997) Methyl iodide as a and Fresh Horticultural Products: Treatments quarantine treatment for Caribbean fruit fly. and Responses. CAB International, Wallingford, In: Stanley, D. (ed.) Methyl Bromide Alternatives UK, 360 pp. Newsletter. US Department of Agriculture 3, Rigney, C.J. and Wills, P.A. (1986) Efficacy of p. 11. gamma irradiation as a quarantine treatment Sharp, J.L. and McGuire, R.G. (1996) Control of against Queensland fruit fly. In: Moy, J. H. (ed.) Caribbean fruit fly (Diptera: Tephritidae) in Radiation Disinfestation of Food and Agricultural navel orange by forced hot air. Journal of Products. University of Hawaii at Manoa, Economic Entomology 89, 1181–1185. Honolulu, Hawaii, pp. 116–120. Sharp, J.L., Gaffney, J.J., Moss, J.I. and Gould, W.P. Riherd, C., Nguyen, R. and Brazzel, J.R. (1994) Pest (1991) Hot-air treatment device for quarantine free areas. In: Sharp, J.L. and Hallman, G.J. research. Journal of Economic Entomology 84, (eds) Quarantine Treatments for Pests of Food 520–527. Plants. Westview Press, Boulder, Colorado, Sharp, J.L., Robertson, J.L. and Preisler, H.K. (1999) pp. 213–223. Mortality of mature third instar Caribbean fruit Robertson, J.L., Preisler, H.K., Frampton, E.R. fly (Diptera: Tephritidae) exposed to micro- and Armstrong, J.W. (1994) Statistical analyses wave energy. Canadian Entomologist 131, 1–7. to estimate efficacy of disinfestation treat- Smith, E.S.C. (1992) Fruit fly disinfestation in ments. In: Sharp, J.L. and Hallman, G.J. (eds) mangoes by hot water dipping. In: Ooi, P.A.C.,

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Lim, G.S. and Teng, P.S (eds) Proceedings of the United States Environmental Protection Agency Third International Conference on Plant Protection (1995) Office of Air and Radiation (6205-1). in the Tropics. Kuala Lumpur, Malaysia. Malay- EPA430-R-95-009. July 1995. Stratospheric sian Plant Protection Society. No. 6, 188–195. Ozone Protection. Alternatives to Methyl Stark, J.D. (1994) Chemical fumigants. In: Paull, R.E. Bromide. Ten Case Studies – Soil, Commodity, and Armstrong, J.W. (eds) Insect Pests and and Structural Use. Fresh Horticultural Products: Treatment and United States Environmental Protection Agency Responses. CAB International, Wallingford, (1996) Office of Air and Radiation (6205-1). UK, pp. 69–84. EPA430-R-96-021. December 1996. Strato- Sugimoto, T., Furusawa, K. and Mizobuchi, M. spheric Ozone Protection. Alternatives to (1983) Effectiveness of vapor heat treatment Methyl Bromide. Vol. 2 – Ten Case Studies. against the oriental fruit fly, Dacus dorsalis Soil, Commodity, and Structural Use. Hendel, in green pepper and fruit tolerance to Waddell, B.C., Clarke, G.K. and Maindonald, J.H. the treatment. Research Bulletin Plant Protection (1997) Comparative mortality responses of Service 19, 81–88 (in Japanese). two Cook Island fruit fly (Diptera: Tephritidae) Thompson, A. (1990) Efecto de la aplicatión de cera y species to hot water immersion. Journal of aceie en frutos de chirimoya (Annona cherimola Economic Entomology 90, 1351–1356. Mill.) cv. Concha Lisa, sobre el control de Whiting, D.C. and van den Heuvel, J. (1995) Oxygen, Brevipalpus chilensis Baker y evaluación del carbon dioxide, and temperature effects on comportamiento de la fruta en post-cosecha. mortality responses of diapausing Tetranychus Thesis in agronomy, Universidad Cató1ica de urticae (Acari: Tetranychidae). Journal of Valparaiso, Chile, 92 pp. Economic Entomology 88, 331–339. Unahawutti, U., Chettananachitara, C., Poomthong, Whiting, D.C., O’Connor, G.M., van den Heuvel, J. M., Komson, P., Smitasiri, E., Lapasathukool, and Maindonald, J.H. (1995) Comparative C., Worawissithumrong, W. and Intarakum- mortalities of six tortricid (Lepidoptera) heng, R. (1992) Evaluation of vapor heat species to two high-temperature controlled treatment for control of the oriental fruit fly atmospheres and air. Journal of Economic and the melon fly in ‘Nan Klarngwan’ mango. Entomology 88, 1365–1370. Technical Report, Department of Agriculture, Yokoyama, V. (1994) Fumigation. In: Sharp, J.L. and Bangkok, Thailand, 106 pp. Hallman, G.J. (eds) Quarantine Treatments for Undurraga, M.P. and Lopez, L.E. (1992) Use of wax Pests of Food Plants. Westview Press, Boulder, and soapy water, alone or combined as a quar- Colorado, pp. 67–87. antine method of control of Brevipalpus chilensis Zhang, W.M., McGiffen, M.E. Jr, Becker, J.O., Baker on cherimoyas (Annona cherimola Mill.) Ohr, H.D., Sims, J.J. and Kallenbach, R.L. (1997) (Report) Universidad Cató1ica de Valparaiso, Dose response of weeds to methyl iodide and Valparaiso, Chile, 22 pp. methyl bromide. Weed Research 37, 181–189.

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Index

Abgrallaspis howardi 235 Adoxophyes 61 Ablerus ciliatus 380 cyrtosema 338 Acalymma 382 fasciculana 136 Acanalonidae 236 privatana 323 Acanthoderes jaspideae 258 Aegeria 261 Acari, Acarina 114, 137, 166, 308, 382 Aegerita webbneri 73 Aceria 114 Aepytus serta 377 annonae 213 Aepytus (P.) serta 383 biological control 349 Aethalion reticulatum 120 dimocarpi 348, 349 African red mite 318 litchi 345, 346, 347, 348 biology 318 longana 348 control 318 monitoring 349 Ageniaspis citricola 79 acerola 326 Agiommatus 41 minor pests 327 Agonocryptus 214 Acerola weevil 326 Agraulis biological control 327 occipitalis 62 biology 326 vanillae 367 chemical control 327 vanillae maculosa 383 pheromones 327 vanillae vanillae 383 seasonality 326 Agrotis ipsilon 136, 171 Achaea 62, 80 Alcaeorrynchus grandis 369 janata 337 Aleurocanthus 71, 212 Achalcerinys 75 spiniferus 59, 71, 73 Acicnemis crassiusculus 135 woglumi 61, 73, 134, 303 Acletoxenus 73 Aleurodicus Acremonium 26 cardini 228 Acrididae 167, 308 destructor 134 Acroclisoides tectacorisi 87 dispersus 118, 134, 303 Aculus pelekassi 58, 60 maritimus 303 Acuminate scale 304 pulvinatus 303 Acutaspis albopicta 235 Aleurothrixus floccosus 73, 60, 71, 303 Adoretus Aleurotuberculatus (Adoretus) ictericus 172 canangae 303 compresus 322 cherasensis 303 (Lepadoretus) sinicus 172 psidii 303 tessulatus 172 Aleyrodidae 118, 134, 228, 303, 383 versutus 307 Allocaridara malayensis 316

407

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408 Index

Allotropa 72 curitis 371 Alucita 171 daciformis 298 Amblypelta 148, 239 dissimilis 371 cocophaga 132, 148 ethalea 384 costalis szentivanyi 132 fraterculus 84, 298, 371 gallegonis 132 grandis 384 lutescens 87, 112 kuhlmanni 371, 384 lutescens lutescens 239, 344 leptozona 298 lutescens papuensis 132 life cycle 84 nitida 87, 112, 239, 344 ludens 84, 108, 135, 298 parasitoids 240 lutzi 371, 384, 384 theobromae 132, 148 minensis 298 Amblyseius 63, 65, 107, 346 obliqua 108, 298 benjamini 177 ocresia 298 cinctus 66 pallidipennis 372, 384 citri 66 parishi 298 coccineae 347 physical control 85 deleoni 66 pseudoparalella 298, 371, 384 largoensis 346 punctata 298 limonicus 225 schultzi 298 longispinus 66 serpentina 108, 298 swirskii 115, 246 sorocula 298 ambrosia beetles 119 striata 108, 298, 371 avocado 261 suspensa 84, 108, 135, 298 American (cotton) bollworm 254 trapping 84 Amitermes foreli 380 turpiniae 298 Amitus xanthochaeta 371 hesperidum 72, 73, 118 zenildae 298 spiniferus 72, 73 Anatrachyntis 171 woglumi 72 Ancistotermes 227 Amorbia 306 Anicetus cuneana 250 beneficus 67, 116, 341 biology 250 ceroplastis 341 parasitoids 250 communis 67 pheromone 250 nyasicus 67 emigratella 136, 171, 306 Anisoscelis Amradiplosis echinogalliperada 114 flavolineata 384 Amritodius atkinsoni 104 foliacea 384 Anacamptodes defectaria 252 Anisotarus 378 Anagrus 75 Annona 197 Anagyrus 71 arthropods 198 agraensis 71, 72 cherimola 197 fusciventris 71, 72 coleopteran leafminers 213 mangicola 117 commercial pollination 199 pseudococci 71, 72 flowering 199, 200 Ananas comosus 157 foliage pests 210 anar caterpillar 306 fruit borers 208 Anastatus 41, 87, 113, 343 fruit flies 209 japonicus 343 fruit pests 209 Anastrepha 60, 84, 140, 256, 297, 371 IPM 214 antunesi 298 key pests 203 bahiensis 298 leaf feeders 213 biological control 84 leafminers 212 bistrigata 298 muricata 197 chiclayae 108 muricata pollinators 202 consobrina 371, 384 pollination 198, 200 cultural control 84 pollinator management 202

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Index 409

pollinators 201 Aphidius 76 seed borers 203 brasiliensis 377 seed borers damage 204 matricariae 75 squamosa 197 platensis 377 trunk pests 213 aphids 74 Anomala 173, 213 Aphidus colemani 75 expansa 172 Aphis Anonaepestis bengalella 209 coeropsidis 134, 146 Anoplocnemis curvipes 87, 113, 237 craccivora 74, 134, 303 Anoplognathus porosus 172 gossypii 74, 75, 134, 146, 212, 229, 303, 376, Anoplolepis 227 384 custodiens 231 damage avocado 229 Anoplophora 80 middletonii 134 chinensis 61 nerii 134, 146 maculata 339 spireacola 60, 75, 134, 146, 303 Anthonomus Aphyssura 275 irroratus 307 Aphytis 68, 235 macromalus 326 africanas 68 Anthophoridae 363 chrysomphali 68, 235 anthracnose 61 columbi 68 Anthribidae 135, 382 debachi 69 antibiosis 30 hispanicus 68 Antichloris 42 holoxanthus 68, 69 Antiteuchus tripterus 212 lepidosaphes 68, 69 Antitrogus lignanensis 68, 69, 235 consanguineus 172 melinus 380 mussoni 172 proclia 68 rugulosus 172 roseni 68, 70 antixenosis 29 yanonensis 68, 70 ants 25, 87–88, 210 Apidae 271, 383 Anua 80 Apis tongaensis 306 cerana 121, 352, 364 Anychus orientalis 226 dorsata 352 Anystis florea 352 agilis 107 mellifera 4, 120, 267, 270, 271, 272, 363, baccarum 177 381 Aonidiella Apoderus tranquebaricus 118 aurantii 59, 68, 133, 304, 384 Apogonia cribicollis 322 citrina 68 control 322 comperei 133 life cycle 322 inornata 133 Apopka weevil 307 orientalis 133, 304 see also Diaprepes Apanteles 77, 147, 207 apple leafroller 250 briareus 335 parasitoids 251 erionotae 41 Aprostocetus 341 paraguayensis 379 ceroplastae 67 Apate 258 Arachnida 382 monachus 258, 307 Araecerus Apateticus mellipes 369 fasciculatus 382 Aphanomerus 75 vieillardi 135 Aphelinidae 67, 68, 72, 73, 75, 87 Archips Aphelinus 76 micaceanus 213 abdominalis 230 occidentalis 251 asychis 230 Arctiidae 305 gossypii 75 Argentine ant 60, 87, 181 mali 377 Argyresthia eugeniella 305 Aphididae 134, 229, 303, 384 Argyrophylax proclinata 208

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410 Index

Argyroploce illepida 334 IPM 261, 262 Aristobia testudo 339 lace bug 242 armoured scales 210, 305 leafminer 252 life cycle 69 leafroller 247, 252 litchi 342 lepidopteran defoliators 255 parasitoids 68 natural enemies 255 Artipus 80 loopers 252, 253 Aschersonia 73 biology 253 Ascidae 177 control 253 Ascotis 253 damage 253 reciprocaria reciprocaria 252 natural enemies 253 Asecodes delucchi 79 mirids 242 Asian greening 61 phytophagous arthropods 224 Asononychus cervinus 80 planthopper 236 Aspidiotus pollen 269 destructor 133, 148, 304 pollination 264–265, 268, 269, 276 excisus 133 ecology 267 hederae 62 rates 271 macfarlanei 133 requirements 266 nerii 169 yield 266 assassin bug 208 pollinators 267, 270, 273, 274 Asterolecaniidae 133 red mite 225 Asterolecanium pustulans 133 damage 225 Asthenopholis subfasciata 172 scale 234 Asynonychus cervinus 61 biology 234 Atelocera raptoria 240 natural enemies 235 atemoya 197 seed moth247 see also Annona self-pollination 265 atis moth borer 209 thrips 244 atlas moth306 weevils 259, 260 Atractomorpha sinensis 167 biology 259 Atrichopogon 275 damage 259 Atta 60, 88 natural enemies 260 sexdens 243 seasonality 259 see also ants whiteflies 229, 303 Attacus atlas 213, 306, 310, 323 biological control 229 biology 323 Azadirachta indica 31 Augosoma centaurus 173 Azamora penicillana 377, 383 Aulacaspis maculata 169 tubercularis 115 Baccha clavata 228 biology 116 Bacillus thuringiensis 42 parasitoids 116 Bactrocera 41, 82, 139, 140, 256, 297 Australian citrus whitefly 71 aquilonis 82, 298 Autographa biloba 171 biological control 83 Averrhoa carambola 323 breviaculeus 298 avocado 223–293 bryoniae 298, 135 bark borer 261 carambolae 108, 324 beetles 257, 258 caryeae 82 control 257 caudata 82, 298 bud mite 226 correcta 298 close pollination 265 cucumis 135 cross-pollination 264 cucurbitae 135, 298, 372, 398 flower morphology 262–263 damage 82–83 flower visitors 270 avocado 256 flowering behaviour 263–264 diversa 135, 299

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Index 411

dorsalis 61, 82, 135, 139, 298, 301, 384, semiochemicals 16 398 yield losses 18 trapping 110 Barbados cherry 326 facialis 135, 299 Baris 174 frauenfeldi 108, 135, 299 bark borers avocado 247 jarvisi 135, 299 biology 247 kirki 135, 299 Bark borers litchi 350 melanota 135, 299 bark eating caterpillar 306 monitoring 83 Batocera 119 musae 40, 135 numetor 119 neohumeralis 82, 108, 135, 299 royilei 119 papayae 82, 108, 141 rubus 119 passiflorae 135, 299 rufomaculata 119 pedestris 299 Batrachedra methesoni 171 phillippinensis 62 bayberry whitefly 303 psidii 299 Beauveria 42 tau 299 bassiana 25, 65 trilineola 136 beet armyworm 171 trivialis 299 Belonuchius ferrugatus 24 tryoni 40, 108, 136, 299 Bephratelloides 5, 203 xanthodes 136, 299 behaviour 205 zonata 136, 299 biological control 206 Baculovirus dione 369 control tactics 206 bagworm 41, 306 cubensis 203 control 42 life cycle 204 life history 42 monitoring 205 banana 13, 21, 30, 41 paraguayensis 203 aphid 42 petiolatus 203 biology 43 plant resistance 206 distribution 42 pomorum 5, 203 caterpillars 42 yield losses 205 fruit fly 40, 41 Binodoxiys 75 fruit scarring beetles 37 biological control 7, 23–25, 72, 81, 109 mites 43 biological control tenuipalpids 65 moths 38 Biosteres 83 pests 14 longicaudatus 109 pseudostem borer 32, 33 Biprorulus bibax 59, 87 rust mite 43 Bitoma 174 scab moth39 Blaberidae 167 skipper 41 black borer 307 spider mite 43 black citrus aphid 59, 60, 61, 62, 75, 303 weevil 14, 19, 27, 28, 30 black cricket 167 biological control 23–24 black cutworm 171 biology 15 black giant bostrychid 258 chemical control 31 black legume aphid 303 damage 18 black maize beetle 173 development 17 black parlatoria 61, 68 dispersal 16 black scale 60, 62, 304 distribution 15 black spiny whitefly 61 host range 15 black spot 61 management 20 black spot pineapple 175 microbial control 25–26 black vine thrips 246 natural enemies 24–25 blackflies 71 oviposition 16 Blitopertha (Exomala) orientalis 173 pest status 18 blowfly 272 sampling methods 17 blue-green citrus nibbler 257–258

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412 Index

blue-striped nettle caterpillar 322 Calacarus biology 322 brionese 137, 144 control 322 citrifolii 58, 137 Boarmia selenaria 253 Cales noaki 73 natural enemies 253 California red scale 304 Bombinae 271 Caligo 42 Bombus 271, 272, 363 control 42 morio 363 Caliothrips bicinctus 36 terrestris 274 Calleida 338 Boring beetles litchi 352 decora 253 Borniochrysa squamosa 341 Calliphora 275 Borreguillo 306 Calliphoridae 275 Bostrichidae 258, 307 Calpe 80 bowrey scale 305 camellia mining scale 305 Brachmia 305 camphor scale 305 Brachycerinae 173 Canthartus 24 Brachygastra 271, 272 Capnodium 181 Brachylybas variegatus 132 carambola 323 Brachymeria 41, 77 fruit fly 324 obscurata 336, 338 key pests 324 pomonae 335 pests 325, 326 pseudovata 207 Caribbean black scale 60, 304 Bracon 75 Caribbean fruit fly 298 Braconidae 75, 77 see also Anastrepha suspensa Braunsapis facialis 353 carmine spider mite 144 Brevipalpus 60, 65, 213 carpenter bee 364, 365 californicus 66, 308 Carpophilus lewisi 66 hemipterus 201 ovatus 66 maculatus 135 phoenicis 60, 65, 137, 308, 311, 326, 374, mutilatus 201 382 carrot weevil 24 pseudostriatus 213 Carthasis distinctus 228 broad mite 59, 60, 61, 62, 64, 115, 145 Casinaria 42 biological control 64 Castnia penelope 170 chemical control 64 Castniidae 170 control 145 Castniomera licus 170 damage papaya 145 castor capsule borer 306 entomopathogens 65 castor oil looper 337 injury 64 Catolaccus hunteri 327 brown citrus aphid 60, 61, 62, 75, 76 Cecidomyiidae 106, 114, 349 rust mite 58, 59 Centrodora brown garden snail 88 darwini 87 brown house ant 231 penthimiae 75, 76 brown soft scale 70, 304 scolypapae 75 Bruchophagus felli 59, 87 viriscens 346 bud mite 59, 60, 61, 62 cerambycid borers 61 bud moth62 Cerambycidae 80, 119, 307, 339, 382 Buzura suppressaria 305 Ceranissus menes 107 Ceratitis 59, 83, 108, 140 biological control 83 cacao mealybug 302 capitata 59, 109, 136, 255, 299, 384 Cacoscelis catoirii 109, 136, 299 famelica 382 cosyra 255, 299 marginata 382 malgassa 299 melanoptera 382 parasitoids 84 walteriana 382 quinaria 299

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Index 413

rosa 59, 109, 136, 255, 299 cicadas 87 Ceratogramma etiennei 82 Cicadellidae 104, 134, 236 Cerconota anonella 207 Cirrospilus 79 biological control 207 quadristriatis 79 control 208 Citheronia laocoon 306 life cycle 207 Citripestis sagittiferella 62 monitoring 207 citron plant bug 302 Ceresium 339 Citrostichus phyllocnistoides 79 Ceroplastes 210, 383 citrus 57–102 brevicauda 67 aphids 74 ceriferus 231, 341 parasitoids 76 destructor 230 armoured scales 69 floridensis 59, 67 bark borer 62 janeirensis 303 blackfly 61, 228, 303 pseudoceriferus 116 life cycle 228 rubens 59, 67, 70, 116, 231, 304, 341 blossom midge 85 rusci 62, 304 brown mite 308 Chaetanaphothrips 85 canker 61 orchidii 36 coleopteran pests 80 signipennis 36, 59 coreid bugs 86 Chaetomymar flat mite 308 gracile 75 fly 61 lepidius 75 fruit flies 82 chaff scale 60, 61, 68, 305 gall wasp 59, 87 Chalcididae 77 grey mite 58 Chalcocelis 322 insect pests 59 albiguttatus 319 key pests 58, 62 biology 319 citrus leafhopper 59 control 319 leafhopper 59, 76, 236 Chavesia 36 biology 236 Cheiloneurus longisetaceous 380 leafminer 59, 60, 61, 76 cherimoya 197 biological control 78 chilli thrips 61 chemical control 78 Chilocorus 233 classical biological control 79–80 circumdatus 69 economic threshold 78 lignanensis 69 injury 77 negritus 69, 117 parasitoids 79 Chilomenes lunata 76 pheromone 78 Chiracanthium inclusum 80 predators 80 Chlumetia transversa 106, 119 seasonality 78 Cholus seabrai 174 leafminer biology 77 Chramesus bispinus 382 leafroller 251, 306 Chrysocharis pentheus 79 avocado damage 251 Chrysomelidae 257, 307, 340, 382 biology 251 damage 340 looper 252 monitoring 340 mealybug 59, 61, 62, 71, 302 Chrysomphalum midge 85 aonidum 59, 68, 69 mite pests 59 dictyospermi 62, 68, 133, 235, 304 nematode 88 ficus 305 Orthezia 60 Chrysomya 272 orthopteran pests 87 megacephala 271 pest management 88–90 varipes 275 pests 57, 60, 61, 62, 66, 76 Chrysonotomyia pulcherrima 114 planthopper 76 Chrysopa oblatis 235 Psylla 59 Chrysophila ferruginosa 24 psyllids 73

421 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:33 PM Color profile: Disabled Composite 150 lpi at 45 degrees

414 Index

citrus continued damage 239 red mite 59, 60, 61, 62, 66 scale 304 biological control 66 whitefly 303 root weevils 80–81 Coelophora 76 biological control 81 Coenomorpha nervosa 240 parasitoids 81–82 coffee hairy caterpillar 306 rust mite 58, 59, 60, 61, 62, 63 Colaspis 37, 38 biological control 63 Colasposoma fulgidum 258 monitoring 63 cold temperature 398 rust thrips 59 Coleophoridae 171 scab 61 Coleoptera 111, 135, 172, 173, 174, 186, 257, 261, snout weevil 81 307, 308, 316, 326, 339, 340, 382 snow scale 59, 60, 68, 305 stem borers 213 soft scales 66, 70 control 214 parasitoids 67 pests 80 spiny whitefly 61 Colgar peracutum 75–76 stink bug 62 Colgaroides acuminata 75, 76, 120 thrips 59, 85, 244 Colletotrichum gloeosporiodes 85, 114 weevil 118, 307 Colydiidae 174 whitefly 61, 71, 72 common army worm 171 woolly 60, 62 Comoritis albicapilla 351 Cixiidae 134 Comperiella classical biological control 23 bifasciata 68, 380 Cleora inflexaria 253 lemniscata 68 Cloropulvinaria psidii 304 Compsus 81 Closterocerus trifasciatus 79 Conchaspididae 132 Clubiona 80 Conchaspis angraeci 132 coating and wraps 399 Congella valida 172 Coccidae 132, 230, 303, 304, 383 Conocephalus saltator 167, 363 Coccidoxenoides peregrinus 71, 72 Conogetes 323 Coccinella Conogethes punctiferalis 208, 306, 316 ancoralis 377 Conopomorpha transversalis 76 biology 321 Coccophagus 70, 233 control 321 caridei 379, 380 cramerella 321 catherinae 67 litchiella 334 ceroplastae 67 sinensis 332 cowperi 67 Conotrachelus 310 eritreansis 116 aguacatae 259 gurneyi 71–72 dimidiatus 307 lycimnia 67 perseae 259 pulvinariae 67 psidii 307, 310 semicircularis 67 serpentina 259 Coccus 70 controlled atmospheres 398 acuminatus 304 Copaxa multifenestrata 254 celatus 304 Copitarsia consueta 383 discrepans 132 Coptorumimus perseae 260 elongatus 67 Coptotermes hesperidum 60, 67, 70, 231, 304, 341, acinaformis 120 383 formosanus 168 hesperidum hesperidum 132 Coreidae 87, 112, 113, 132, 170, 237, 302, 344, longulus 59, 132 384 pseudomagnoliarum 67 parasitoids 87 viridis 59, 61, 67, 304 spotting bugs 209 Coccygominus sanguipes 336 corn earworm 59, 62 coconut bug 113, 238 Corthylus 261 biology 239 Corythucha gossypii 132, 212

422 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:33 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 415

Cosmolure 22 Dactylosternum hydrophiloides 23 Cosmopolites sordidus 14 Dacus taxonomy 15 bivittatus 136 Cosmopterygidae 171 curcubitae 384 Cossidae 351, 383 tryoni 384 Costalimaita ferruginea 307 Dagbertus cotton aphid 74, 229, 303 fasciatus 242 cottonseed bug 243 olivaceous 242 cottony cushion scale 59, 60, 70 Daphnusa ocellaris 319 cowpea aphid 74, 303 control 319 Cratopus life cycle 319 angustatus 339 Darna trima 172 damage 339 Dasiops 372 humeralis 339 curubae 372, 384 Cratosomus bombinus bombinus 213 nedulis 372, 384 Cremastopsyche pendula 306 passifloris 372, 384 Cremastus hymeniae 336 Dasyneura 349 Crematogaster 383 mangiferae 106 crickets 87 Davara carica 136 Criconemella 160 Deanolis sublimbalis 112 crop sanitation 22 Decadarchis minuscula 136 Cryptoblabes ganidiella 62 Decipha viridis 236 Cryptochetidae 67 Deporus marginatus 118 Cryptochetum iceryae 67 Derbidae 134 Cryptolaemus montrouzieri 71, 341, 379 Deudorix 350 Cryptophlebia 334 damage 351 bactrachopa 334 epijarbas 350 biological control 335 isocrates 306 biology 334, 335 Diabrotica 382 carpophaga 334 Diachamismorpha 109 control 336 longicaudata 84, 141 damage 335 Diactor bilineatus 369, 384 distribution 334 Dialeurodes 71 leucotreta 77, 248, 307, 334 citri 61, 71, 73 monitoring 336 citrifolii 61, 71 ombrodelta 334 psidii 303 peltastica 334 Diaphorencyrtus aligarhensis 75 Cryptoptila immersana 247 Diaphorina citri 61, 73, 75 Cryptostigmata 166 Diaprepes 60 Cryptotympana atrata 87 abbreviatus 4, 81, 135, 148, 307 Ctenoceratina flamelicus 81 moerenhouti 353 splengleri 307 rufigaster 353 Diaspididae 115, 133, 169, 304, 305, 324, cultural practices 8 387 Cunaxidae 177 Diaspis boisduvalii 169 Cunaxoides 177 bromeliae 169, 183 Curculionidae 80, 111, 118, 135, 173, 174, 259, 307, Diastethus 174 316, 326, 339, 382 dictyospermum scale 62, 304 cyanophyllum scale 305 Diglyphus begini 79 Cybocephalus binotatus 116 Dimocarpus longan 331 Cyclocephala 202 Dione lunulata 307 glycera 383 melanocephala 382 juno juno 367, 368, 383 Cycloneda sanguinea 377 Diploptera punctata 167 cydnid bugs 36 Diptera 82, 108, 114, 135, 255, 298, 299, 324, 349, Cytosoma 87 384

423 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:33 PM Color profile: Disabled Composite 150 lpi at 45 degrees

416 Index

Diversinervus merceti 73 elegans 67 opulenta 72, 73, 118 stramineus 67 perniciosi 68 Dolichogenidea arisanus 77 smithi 73 Dolichotetranychus floridanus 166, 176 Encyrtidae 67, 68, 72, 75, 77, 79 Doryctobracon 84, 109 Encyrtus 343 toxotrypanae 141 aurantii 67 Dorylus 227 infelix 67 Drepanococcus chiton 132 Ensete 15 Drosicha 118 entomopathogenic fungi 26 stebbingii 118 nematodes 27–28 Drosophilidae 384 Entomophthora sphaerosperma 180 Dryadula phaetusa 383 Eotetranychus hicoriae 308 Dudua aprobola 307 Epicauta atomaria 382 dune snail 88 Epicharis rustica 363 durian 315 Epimeces fruit borer 316 detexta 252 key pests 316, 317 matronaria 252 mealybugs 317 Epiphyas postvittana 77, 338 phenology 315 Episyrphus balteatus 352 psyllid 316 Epitomiptera orneodalis 136 seed borer 317 Eretmocerus 72 Durio zibethinus 315 haldemani 73 Dynastinae 173 portoricensis 73 Dynastor darius 171 series 73 Dysmicoccus erineum 346, 348 brevipes 168, 180, 302 Erinnys ello 147 neobrevipes 168 control 147 nesophilus 133 Erionota thrax 41 Eriophyes 59 annonae 213 Echthromorpha insidiatur 335 sheldoni 58, 59 Ectropis sabulosa 253 Eriophyidae 58, 114, 166, 308, 345, 348 egg parasitoids 76, 81–82 Eriophyies mangifereae 114 Egyptian cotton leafworm 306 Eristalis Elachertus 335 arvorum 363 Elaphria agrotina 171 tenax 270 Elasmidae 75 Erosomyia 114 Elasmus zehntneri 75 mangiferae 106 elephant beetle 340 Erybrachidae 236 elephant weevil 213 Erynnis 136 Elimae punctifera 167 alope 136 Empoasca 145 ello 136 canavalia 134, 145 Erynnis lassauxi merianae 136 dilataria 134, 145 ethylene dibromide 396 fabalis 134 Eucalymnatus tessellatus 132, 304 insularis 134 Eucyclodes pieroides 253 papayae 134, 145, 146 Euderus 335 smithi 59, 75 Eudocima 113, 325, 336 solana 134 biological control 337 stevensi 134, 146 control 337 Encarsia 69, 72, 73 damage 336 citrina 68, 116 fullonia 136, 306, 310, 336 clypealis 73 jordani 336 inquerenda 69 materna 113 lahorensis 72, 73 monitoring 337

424 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:33 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 417

salaminia 113, 336 forced air heating 397 Eueides aliphera aliphera 383 Forcipomya 275 dianosa 383 forest tree termite 308 huebneri 383 Formicidae 383 isabella 368 Frankliniella 107 Eugnamptus marginatus 118 auripes 382 Eulaema 364 bispinosa 107 Eulophidae 67, 75, 77, 79 bruneri 245 Eumeta minuscula 306 chamulae 245 Eupelmidae 87 kelliae 107 Eupelmus tachardiae 341 occidentalis 107, 135, 168, 245 Euphoria 307 parvula 36 Euphranta lemniscata 136 schultzei 168 Euplectrus 106 usca 135, 168 kurandaensis 77 Franklinothrips megalops 246 Euproctis fraterna 306 fruit borer 61, 62 Eupseudosoma involuta 305 fruit flies 40, 108, 209, 296, 327 Euryischomyia 67 autocidal techniques 300 Euryscopa cingulata 382 avocado 255, 256 Euseius 63, 145 biological control 109 addoensis 86 biology 139 citrifolius 65 chemical control 300 victorensis 66 control 109 Eutachyptera psidii 306 damage mango 109 Eutetranychus distribution 108 africanus 318 economic thresholds 297 banksi 60, 63, 66, 137 litchi 349 cendani 61, 66 damage 349 orientalis 59, 66, 308 management mango 110 sexmaculatus 60, 226 monitoring 109 Euthyrrhinus meditabundus 213, 339 parasitoids 256 Exocortis 61 plant resistance 300 Exomalopsis 272 sampling 141, 297 Exopthalmus 81 fruit piercing moth59, 61, 80, 306, 325, 336 fruit scarring bee 38 false codling moth248, 307 fruitlet core rot 175 biology 248, 249 fruitspotting bugs 112, 113, 344 host plants 248 damage 113 parasitoids 249 litchi 344, 345 pheromone 249 biological control 345 false parlatoria scale 305 monitoring 345 false spider mite 308 Fuller’s rose weevil (beetle) 61, 80 Farnya 240 Fulvius angustatus 132 Ferrisia virgata 118, 133, 169, 301, Fusarium 26 302 fig wax scale 62, 304 Fijian fruit fly 299 gall flies litchi 349 Fiorinia fioriniae 234 gall midges 114 fire ant 60, 181 biological control 114 five-spotted fruit fly 299 mango 114 flat mite 60, 166 Garcinia mangostana 319 see also Brevipalpus Gascardia destructor 231 Flatidae 76, 120, 236, 318 gelatine grub 319 Flavithorax 67 Gelechiidae 305 Florida red scale 59, 60, 61, 69, 305 Geococcus coffeae 169 Florida wax scale 59, 61, 62 Geometridae 252, 305, 320, 383

425 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:34 PM Color profile: Disabled Composite 150 lpi at 45 degrees

418 Index

Geotrichium 27 fruit worm 305 Geotrigona 363 IPM 311 acapulconis 272 key pests 296 giant looper 253 mealy scale 304 giant mealybug 302 mite 308 giant northern termite 87 origin 295 giant/white stem borer 170 pests 295 Gladosius casey 174 phenology 295 Glovers scale 68, 70 production 296 Goethana secondary pests 301, 310 parvipennis 114 skipper 305 shakespeari 87 gummosis 61 gold dust weevil 118 gusano cabezón 305 golden leaf weevil 307 Gymnadrosoma aurantium 80 Gonatocentrus 105 Gymnaspis aechmeae 170 Gonimbrasia belina 351 Gonodonta 325 clotilda 306 Habrolepis rouxi 68 Gracillaria perseae 252 Hadronotus barbiellinii 370 Gracillariidae 252 Hanseniella 166, 177 Graphium ecrypylus lycaon 213 ivorensis 167, 177 grasshoppers 87, 308 unguiculata 166, 177 greedy scale 305 Haplothrips bedfordi 86 green beetle 172 Haptoncus luteolus 201 green citrus aphid 303 Harmonia green coconut bug 239 conformis 76 green coffee scale 59, 61, 70 octomaculata 379 green peach aphid 229, 303 testudinaria 76 biology 229 Heilipus 214 damage avocado 229 catagraphus 260 green scale 304 lauri 260 green shield scale 304 biology 260 green vegetable bug 241 damage 260 natural enemies 242 Heliconius green weevil 307 erato phyllis 383 greenhouse thrips 246 ethilla narcaea 383 biology 246 sara apseudes 383 control 247 silvana robigus 383 damage avocado 246 Helicotylenchus 160 parasitoids 246 Helicoverpa predators 246 armigera 59, 77, 254 greenhouse whitefly 303 punctigera 77 Greenidea Heliopeltis theobromae 301 ficicola 303 Heliothis armigera 306 formosana 303 Heliothrips 85 greening 59 haemorrhoidalis 36, 87, 246 greening disease 73 Helix 88 grey cluster bug 170 Helopeltis 113 grey pineapple mealybug 168 antonii 302 grey-brown stink bug 240 theobromae 302 groundnut aphid 303 Hemiberlesia cyanophylli 305 Gryllidae 167 diffinis 305 Gryllus bimaculata 167 lataniae 234, 305, 342 Gryon 87 palmae 305 guava 295–313 rapax 305 bud moth307 Hemiptera 112, 113, 132, 228, 301, 302, 303, 304, fruit flies 296, 298 305, 316, 318, 344, 384

426 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:34 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 419

hemispherical scale 60, 70, 304 Icerya Hepialidae 383 aegyptiaca 133 Hesperiidae 305 purchasi 59, 67, 70, 133 Heterographis 209 seychellarum 133, 302, 341 Heteronychus arator 173 Ichneumonidae 77 Heteroptera 170, 301 Idioscopus 104 Heterorhabditis 25, 27 clypealis 104 Heterotermes convexinotatus 380, 383 biological control 105 Hexacladia smithii 370 biology 104 Hexaleurodicus 383 control 105 hibiscus mealybug 211 damage 104 damage 211 monitoring 105 natural enemies 211 parasitoids 105 Hirsutella 65 magpurensis 104 thompsoni 63 Idona minuenda 236 Hivana 80 Imbrasia cytherea 255 Holhymenia 369 Incamyia 378 clavigera 302, 369, 384 Indarbela histro 384 control 350 Holopothrips ananasi 168 damage 350 Holotrichia rufoflava 308 monitoring 350 Homalodisca 60 quadrinotata 306, 350 Homoeocerus 239 tetraonis 350 Homona Insecta 382 coffearia 338 integrated pest management 20 difficilis 338 Iphiaulax 42 spragotis 247 Irapua bee 38, 209, 381 Homoptera 104, 118, 120, 132, 168, 169, 170, 228, Iridomyrmex 59, 88 301, 324, 383 irradiation 399, 400 honeybee 270, 274 Isoptera 120, 168, 226, 308, 383 see also Apis mellifera Isotenes miserana 77, 209, 338 Hoplochelus marginalis 172 ivy leafroller 247 Horismenus 212 hornworms 147 Horogenes chilonus 336 Kalotermitidae 308 host plant resistance 8, 28 katydids 87 hot water immersion 396 Kerria lacca 341 Howardia biclavis 133 Kilifia Hyaliodes 243 acuminata 304 hydrogen cyanide 396 deltoides 304 Hymenoptera 383 Kratosyma citri 79 Hyperaeschrella insulicola 323 Hyperaspis 233 Hypercompe icasia 305 lace bugs 212 Hypoaspis aculifer 107 ladybirds 70 Hypocryphalus mangiferae 119 Lamellobates palustris 166 Hypomeces 81 Langsdorfia 383 squamosus 62, 118, 307, 316 large blacktip wilter 237 biology 316 biology 238 control 316 parasitoids 238 Hyponomeutidae 305 large borer weevil avocado see Heilipus Hyposidra talaca 320 Lasiocampidae 306 biology 320 Lasiodiplodia theobromae 213 control 320 Lasioseius 177 Hypothenemus latania scale 234, 305 eruditus 308 Lawana conspersa 318 psidii 308 leaf eating weevil 62

427 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:34 PM Color profile: Disabled Composite 150 lpi at 45 degrees

420 Index

leafcutting ants 88 biology 332, 333 leaf-footed bugs 238, 302, 369 control 333 leafhoppers 76 damage 333 leathery pocket mite 166 monitoring 333 Lecaniorum 67 IPM 353–354 Lepadoretus 322 leaf feeders 351 Lepidiota leaf feeding beetles 340 gibbifrons 172 control 340 grata 172 leaf midge 349 noxia 172 control 349 squamulata 172 damage 349 stigma 172 monitoring 349 lepidoptera 76, 112, 113, 119, 136, 170, 171, 172, leafminer 334 247, 305, 306, 307, 310, 317, 319, 320, 323, biology 334 336, 350, 351, 383 control 334 lepidopterous Annona fruit borers see Cerconota damage 334 lepidopterous defoliators passion fruit see Dione, distribution 334 Agraulis monitoring 334 Lepidosaphes natural enemies 334 becki 59, 68, 69 loopers 337 gloveri 68, 70 biological control 338 laterochitinosa 305 control 338 similis 305 damage 337 Lepolexis scutellaris 75 monitoring 338 Leptochirus unicolor 24 mealybugs 351 Leptocoris mites 352 rufomarginata 352 phenology 332 tagalica 352 pollinators 352 Leptoglossus 301, 325, 327, 369 soft scales 340 australis 238, 302, 369 licthi/longan 339–340 balteatus 302 biological control 339 concolor 302 biology 339 conspersus 384 control 339 gonagra 302, 384 damage 339 stigma 302 distribution 339 zonatus 302 longicorn beetles 339 Leptomastidea abnormis 72, 379 leafrollers 338 Leptomastix 379 monitoring 339 dactilopii 71, 72 scarabs 340 Leptopius setosus 213 distribution 340 Lepturges 382 weevils 339 lesion nematode 160 biology 339 lesser army worm 171 control 339 lesser cotton leaf worm 171 damage 339 Leucothyreus 382 distribution 339 Limacodidae 172, 319, 322 monitoring 339 Linepithema humilis 60, 87 Litchiomyia chinensis 349 Liothrips bondari 305 Litostylus diadema 382 Lisiphlebus testaceipes 377 Lixophaga sphenophori 35 Listronotus oregonensis 25 Locusta migratoria 167 Litchi 331 Lonchaea 371 bark borers 350, 351 cristula 372, 384 branch borers 351 Lonchaeidae 299, 384 crop importance 331 long soft scale 59 erinose mite 345 longan 331 fruit borer 332, 334, 350 longan crop importance 332 biological control 333 longan erinose mite 348

428 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:34 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 421

biological control 348 monitoring 107 erinose mite damage 348 malformation 115 monitoring 348 mealybug 117, 302 gall mite 348 midges 106 IPM 353–354 midges biological control 106 leaf feeding beetles 340 mite 115 phenology 332 pest management 121 longicorn beetles 119, 339 pests 118 long-tailed mealybug 230, 302 pests of flowers 104 life cycle 230 planthopper 76, 120 parasitoids 230 pollinators 120, 121 Lophodes sinistraria 253 production 103 Lucilia 121 resistant cultivars 110 Lybindus dichrous 170 scale 115 Lycaenidae 170, 207, 306, 350 seed borer 112 Lygaeidae 170, 243 biological control 112 Lymantria control 112 monacha 306 damage 112 xylina 306 seed borer monitoring 112 Lymantriidae 306 shield scale 116 Lysiphlebus shoot borer 119 japonica 75 biological control 119 fabarus 75 monitoring 119 testaceipes 75 thrips 107 biological control 107 control 107 Maconellicoccus hirsutus 5, 211, 302 damage 107 Macrocentrus delicatus 106 witches’ broom 115 Macrodactylus mexicanus 261 mangosteen 319 Macrophylla ciliata 172 key pests 320 Macrosiphum Mapighia glabra 326 euphorbiae 134, 148 Margarodidae 118, 133, 302 solanifolii 376, 384 Marpissa tigrina 74 Macrotermes 227 Marula fruit fly 255, 299 subhyalinus 168 Mascarene fruit fly 299 Madagascan fruit fly 299 Mastotermes darwinensis 87, 120 Maecolaspis 382 Mcphail traps 110 Maladera 307 mealybugs 210, 301 Mallada signata 71, 341 biological control 117 mango 103–129 damage 117 boring pests 118, 119 Mediterranean fruit fly 59, 60, 62, 108, 255, 299, bud mite 114 372, 398 control 115 Mediterranean mango thrips 114 crop 103 Megalopyge defoliata trujillo 306 flower lepidoptera biological control 106 Megalopygidae 306 flower pests 106 Meganotron rufescens 213 fly 299 Megaphragma mymaripenne 87 fruit flies 108 Megaselia scalaris 378 fruit pests 108 Melanaspis bromeliae 170 fruitspotting bugs 113 Melanaspis smilacis 170 hoppers 104 Melanitis leda ismene 306 leaf pests 114 melanose 61 leaf-cutting weevil 118 Melanostoma univittatum 352 lepidoptera 106 Melipona 38 control 107 Meliponula erythra 353 damage 106 Meloidae 382

429 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:34 PM Color profile: Disabled Composite 150 lpi at 45 degrees

422 Index

Meloidogyne Monolepta incongita 160 apicalis 257 javanica 160 australis 80, 257, 340 Melolonthinae 172 bifasciata 257 melon aphid 61, 74, 303 Monomarca 382 melon fly 298, 372 Moranila california 67 Membracidae 237 Morganella longispina 133, 324, 325 Menochiles sexmaculatus 316 control 325 Metabolybia singulata 273 mosquito bug 302 Metamasius mottled avocado bug 236 callizona 33 Mudaria luteileprosa 317 dimidiatipennis 173 Musa fasciatus 173 acuminata 13, 28 hemipterus 135 balbisiana 28 hemipterus sericeus 33, 135 Muscidae 270, 271, 275 chemical control 35 Musgraveia sulciventris 87 damage 34 mussel scale 61 life history 33 Mymaridae 75 natural enemies 35 Myoleja nigroscutellata 136 sampling 34 Myriangium duriaei 380 seasonality 34 Myriapoda 166 trapping 34 myriapods see Myriapoda ritchiei 173 Mythimna convecta 171 Metaphycus 67, 70, 71, 233 Myzus bartletti 67 ornatus 303 galbus 67 persicae 134, 229, 303, 376, 384 helvolus 67 lounsburyi 67 luteolus 67 Nacoleia octasema 39 stanleyi 67 biology 39 Metarbelidae 247, 306, 350 control 40 Metarhizium anisopliae 25 damage 39, 40 Metcalfiella monogramma 237 Nannotrigona 272 methyl bromide 395 Nastonotus reductus 167 methyl iodide 395 Nasutitermes 120 Mexican fruit fly 298 natal fruit fly 59, 255, 299 Mexican honey wasp 273 natural enemies soft scale 70 Micraspis discolor 316 Nectria coccophila 380 Microbracon phyllocnistoides 75 neem 31 Microcerotermes 227 nematicides 163 arboreus 380, 383 nematodes Microplitis 77 distribution 160 Microtermes 120 economic thresholds 163 Microterys 233 pineapple 160 flavus 70, 116 Nemorilla floralis maculosa 338 kotinskyi 341 Neochetina eichorniae 25 nietneri 67 Neodecadarchis flavistriata 171 microwave energy 400 Neosilba 299 midges 85, 106 Neotermes connexus 308 Milviscultulus mangiferae 116, 132 Neotheronia 378 Mimallo amilia 306 Nephelium lappaceum 320 Mimallonidae 306 New Guinea sugar cane weevil 173 minor fruit pests 315, 328 Nezara mirid bugs litchi 352 pallidoconspersa 241 Miridae 132, 242, 302 prunasis 241 mite damage banana 43 viridula 87, 132, 240, 241, 265 mites litchi 352 nigra scale 304

430 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:35 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 423

Nipaecoccus Opius 83, 109 nipae 302 Opogona 38 vastator 341 sacchari 171 viridis 59, 72, 133, 302 control 39 Niphonoclea damage 38 capito 119 life history 38 albata 119 Opsiphanes 42 Nitidulidae 135 orange fruit borer 338 Noctuidae 113, 136, 171, 254, 306, 317, 320, 336, Orchamoplatus citri 73 383 Oribatid mites 166 Noesilba pendula 372 oriental fruit fly 61, 62, 298, 372 non-host status 393 oriental garden cricket 167 Noorda albizonalis 112 oriental spider mite 59, 226 Notodontidae 323 oriental yellow scale 304 nuclear polyhedrosis virus 369 Orius thripoborous 86 nun moth306 Orthezia praelonga 60, 71, 170, 327 Nymphalidae 171, 306, 383 Ortheziidae 170 Nysius Orthoptera 167, 308 clevelandensis 170 Orthorhinus vinitor 170, 352 cylindrirostris 213 klugi 339 Othreis 59, 61, 77, 80, 113, 336 Ocideres poecilla 261 Oxaea flavescens 363 Odoipurus longicollis 24, 32, 33 Oxya chinensis 167 Odonestis vita 306 Oxycaraenus hyalinipennis 243 Odonna passiflorae 377, 383 Oxydia Odontotermes 120, 227 vesulia 106 badius 227 transponens 252 Oecophoridae 247, 383 Oxyodes Oecophylla smaragdina 118 scrobiculata 337 Oencyrtus 113 tricolor 337 erionotae 41 Oiketichus kirbyi 41, 254, 306 oleander scale 62 Pachnaeus 118 Olethreutes Paecelomyces 65 perdulata 338 pale-triangle butterfly 213 praecedens 338 palm scale 305 Oliarus complectus 134 palomilla mexicana de la seda 306 Oligochrysa lutea 71, 379 Palpada mexicana 270 Oligonychus Pandeleteius vitticollis 307 biharensis 213, 308 Panonychus 308 coffeae 224 citri 59, 66, 226 mangiferae 115 Pantomorus perseae 225 albosignatus 307 psidium 308 cervinus 173, 307 punicae 224 godmanni 173 yothersi 225, 310 papaya 131 Oligosita 243 aphid 146 olive scale 304 arthropods 139, 142 Omolicna puertana 134 bunchy top 145, 146 Omphale metalicus 336 defoliators 147, 148 onion thrips 179 fruit flies 139 Ooencyrtus 75, 77 fruit fly 62, 140 caurus 240 control 141 phongi 343 monitoring 141 Ophelosia 72, 379 fruit pests 139 Ophideres 80 fruitspotting bugs 148

431 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:35 PM Color profile: Disabled Composite 150 lpi at 45 degrees

424 Index

papaya continued natural enemies 370 hopper burn 146 defoliators 368 IPM 147, 148, 149 control 369 leaf edge roller mite 144 host plants 368 leafhoppers 145 injury 368 mealybug 143 life history 368 biological control 144 natural enemies 369 control 144 flowering 361 minor pests 148 fruit flies 371 mites 144 biology 372 pests 131 host plants 373 production 138 injury 373 ringspot virus 146 natural enemies 374 resistant varieties 146 IPM 385 varietal resistance 142 mealybugs 378 paper wasps 88 control 379 Papilio 77 injury 379 agamemnon 213 life cycle 379 garanas garanas 254 mites 374 scamer scamer 255 biology 374 Parabemisia myricae 228, 303 host plants 375 Paraceraptrocerus 67 natural enemies 375 Paracoccus marginatus 133, 143 pests 367 Paradiaphorus crenatus 173 pollination 361, 362 Paralamellobates bengalensis 166 scales 379 Paraleyrodes 60, 73 biology 379 perseae 228 host plants 380 urichii 303 injury 380 Parapioxys jucundus 236 natural enemies 380 Parasa lepida 322 stem weevil 371 Parasaissetia nigra 132, 210, 304 biology 371 parasitoids 67 control 371 Paratetranychus 226 weevil injury 371 Parathiscia 236 termites 380 Paratrichodorus 160 biology 380 Parisoschoenus ananasi 174 control 381 Parlatoria injury 381 cincrea 60 peach fruit fly 299 pergandii 68, 305 pecan leaf scorch mite 308 zizyphus 61, 68 Pediobius 41 Paroppis 166 Penicillaria jocosatrix 106 Partamona 272 Penicillium funiculosum 175 Passiflora edulis 361 Pentalonia nigronervosa 42 passion fruit 361–390 Pentatomidae 132, 240 aphids 376 Penthimeola bella 59, 75, 76, 236 injury 77 Pentilia egena 380 natural enemies 377 Peridroma saucia 377, 383 caterpillars 377 Perisierola emigrata 336 biology 378 Perissopneumon ferox 302 control 378 Persea americana 223 injury 378 Persea mite 225 natural enemies 378 life cycle 225 coreid bugs 369 predators 225 control 371 pest free area 393 host plants 370 pest management 3 injury 370 pest risk analysis 393 life history 370 pests of banana 36

432 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:35 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 425

flowers 36 monitoring 185 fruits 36 natural enemies 185 foliage 41 flat mite 176 Phaenicia mexicana 270 biology 176 Phaeogenes 338 chemical control 177 Phanerotoma dentata 335 economic thresholds 177 Pheidole 210 natural enemies 177 see also ants sampling 177 Pheidole megacephala 25, 181, 231 fruit mite 166, 175 Phenacaspis dilitata 116 IPM 188, 189 Phenacoccus key nematode pests 159 psidiarum 302 key pests 174 solani 169 mealybug 302 pheromones 7 biological control 183 Philaethria 383 control 182 dido 383 cultural control 183 wernickei wernickei 383 economic thresholds 182 Philephedra 210 IPM 182 tuberculosa 132, 143 sampling 182 Philonis 371 wilt 182 crucifer 382 nematodes 160 obesus 382 control 163 passiflorae 382 economic thresholds 163 Phlaeothripidae 305 IPM 165 Phocides polybius 305 monitoring 162 Phoenix canariensis 34 non-chemical control 164 Phosphine 396 sampling 162 Phycita semilutea 209 phenology 157, 158, 159 Phycitidae 136 pocket mite 175 Phyllocnistis 212 biology 175 citrella 59, 79, 320 cultural control 176 Phyllocoptruta economic threshold 176 musae 43 fruit disease 175 oleivora 58, 59 life cycle 175 sakimurae 166 natural enemies 176 Phyllophaga portoricensis 172 sampling 175 Phytodietus 77 red mite 166, 176 Phytophthora 61 resistance nematodes 164 cinnamomi 165 rhinoceros beetle 173 Phytoseiidae 63, 65 scale 183 Phytoseiulus biology 183 hawaiiensis 145 IPM 184 macropilis 145 natural enemies 184 persimilis 226 sampling 184 Phytoseius symphilids 177 hongkongensis 66 thrips 179 intermedius 346 weevil 174 pineapple 157–195 white grubs 186 arthropods 165 biology 186 black beetle 173 economic thresholds 187 black spot beetle 173 life cycle 187 caterpillar 184 natural control 188 biology 185 sampling 187 chemical control 186 control 188 cultural control 186 pink bud moth171 damage 185 pink citrus rust mite 58, 60 economic threshold 185 pink hibiscus mealybug 302

433 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:35 PM Color profile: Disabled Composite 150 lpi at 45 degrees

426 Index

pink pineapple mealybug 180 Protopulvinaria 70 ant symbiosis 181 pyriformis 132, 232, 304 biology 181 Pseudacysta perseae 242 pink wax scale 59, 61, 116, 231, 341 damage 243 Plaeseius havanus 23 parasitoids 243 Planococcus 59 see also avocado lace bug citri 59, 71, 133, 169, 302, 384 Pseudaonidia 133 lilacinti 230 clavigera 305 lilacinus 118, 302, 317 duplex 305 minor 302, 317 trilobitiformis 133, 170 pacificus 302, 384 Pseudaphycus plant resistance 29, 43, 74 flavidulus 71, 72 planthoppers 76 maculipennis 72 Platygasteridae 72, 73, 75 Pseudaulacaspis Platynopoda latipes 364 cockerelli 133 Platynota 106 pentagona 133, 142 Platyomopsis humeralis 339 Pseudischnaspis Platypeplus aprobola 338 anassarum 170 Plebeia 272 bowreyi 305 Plocaederus ruficornis 119 Pseudococcidae 133, 168, 230, 302, 384 Pnigalio Pseudococcus flavipes 79 calceolariae 71–72 minio 79 citri 72 Pococera 383 citriculus 302 atramentalis 106 cryptus 62 Poeciloscarta 145 jackbeardsleyi 133 laticeps 134, 146 longispinus 71, 72, 133, 169, 230, 302 Polistes 87, 272 nipae 230 canadensis 273 viburni 72, 133 pollinating beetles 201 Pseudoparlatoria pollination 8 ostreata 133 passion fruit 363–367 parlatorioides 305 pollinators, mango 120 Pseudotectococcus anonae 210 Polyphagotarsonemus latus 59, 64, 115, 137, 145, 213, Pseudotheraptus wayi 113, 238 226, 374, 382 Psorosticha zizyphi 306 Popillia Psychidae 254, 306 bipunctata 173 Psyllaephagus pulvinatus 75 mutans 173 Psyllidae 73, 237, 305, 316 post harvest 394 Pteromalidae 67, 72, 77, 87 fumigation 395 insecticide treatment 395 sampling 394 Quadrastichus 79, 82 powdery stink bug 240 quarantine combination treatments 401 Pratylenchus 88 quarantine systems approach401 brachyurus 160 quarantine treatments 391, 392 Prays citri 62 Queensland fruit fly 59, 299, 372 predators broad mite 65 fruitspotting bugs 113 rambutan 320 Pristhesancus plagipennis 208 key pests 321 Pristomerus hawaiiensis 336 Rastrococcus 117 Procontarinia matteiana 114 biological control 117 Procornitermes striatus 168 control 117 Proctolaelaps 177 iceryoides 302 Prodiplosis longifila 85 invadens 117, 302 see also citrus blossom midge monitoring 117 Protaetia orientalis 135 spinosus 117

434 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:35 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 427

red ant 118 Samia cynthia ricini 343 red mite 60, 308 sampling 5, 17 red scale 59, 60, 61, 62, 68 Sanctanus 145 red wax scale 304 fasciatus 134 red-banded thrips 114, 209, 245, 305 Sarcophaga 121 biology 245 lambens 42 damage 245 Sarcophagidae 270 natural enemies 245 satsuma sudden wilt 61 red-shouldered leaf beetle 340 Saturniidae 306, 351 reniform nematode 160 Saurita cassra 255 Retithrips syriacus 246 scale insects 301 Retrachyderes thoracicus 307 papaya 142, 143 Rhabdoscelus obscurus 135, 173 Scaptotrigona 272 Rhinacloa 242 postica 363 rhinoceros beetle 173 Scarabaeidae 135, 172, 186, 261, 307, 308, 322, 340, Rhinotermitidae 168, 383 382 Rhizobius scarring beetles 37 lophanthae 116 Scelionidae 77, 87 satellus 235 Scenocharops 41 Rhopaea magnicornis 172 Scheloribates curvialatus 166 Rhopalosiphum maidis 134 Scirtothrips 59, 85 Rhynchaenus mangiferae 118 aguacatae 244 Rhynchocoris humeralis 62 aurantii 59, 113, 244 Rhynchophorinae 173 biology 111 Rhyparida 340 damage 85 discopunctulata 340 dorsalis 61, 107, 351 Rhyzobius 70 kupae 244 rice butterfly 306 life cycle 86 ring nematodes 160 mangiferae 114 Rodolia chermesina 341 dispersal 111 root weevils 80–81 control 111 biology 81 natural enemies 86 injury 81 perseae 244 root-knot nematode 160 biology 244 rose beetle 307 damage 244 Rostrozetes foveolatus 166 seasonality 86 rotten sugarcane stalk borer 33 Scolopopa australis 75 Rotylenchus 160 Scolytidae 261, 308, 382 reniformis 160 Scutellista caerulea 67, 210 Rutelinae 172 Scutellonema 160 Rutherglen bug 170, 352 Scutigerella sakimurai 167, 177 Scutigerellidae 177 Scymnodes 76 Sabulodes 383 Scymnus 233, 377 aegrotata 252 seed weevil 111 caberata 253 Selenaspidus articulatus 60, 68, 235, 305, 384 sack bearer 306 Selenothrips Saissetia 70 dorsalis 305 coffeae 60, 67, 132, 210, 304 rubrocinctus 114, 135, 209, 245, 305 miranda 304 Semielacher petiolatus 79 neglecta 60, 304 serpentine fruit fly 298 nigra 67 Setothosea asigna 172 oleae 60, 67, 304 sex attractant 78 oleae oleae 132 Sharp shooters 60 Salagena 350 Sierola cryptophlebiae 336 obsolescens 247 Signiphora perpauca 235 transversa 247 Silba pendula 384

435 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:36 PM Color profile: Disabled Composite 150 lpi at 45 degrees

428 Index

Simosyrphus 76 mangiferae 111 gricornis 275 quatuordecimcostata 258 Siphanta 59, 75, 76 Stethorus 107, 115, 145, 226, 375 six-spotted mite 60, 61, 226 Stictoptera cuculliodes 320 small green stink bug 241 stingless bee 272 social bee 272 stingless wasps 270 soft brown scale 60, 61, 231, 341 Stizocera 382 biology 231 Strategus control 232 jugurtha 173 life cycle 70 validus 173 soft scales 303, 304, 340 Strepsicrates mango 116 ejectana 307 Solenopsis 60, 383 rothia 307 soursop lace bug 212 smithiana 307 soursop pollination 202 tetropsis 307 South African citrus thrips 113 striped mealybug 169, 302 South American fruit fly 298 stubby root nematodes 160 Spalangia grotiusi 109 subterranean termite 87 Spanish red scale 235, 304 sugarcane rootstalk borer 60 biology 235 Symphyla 166, 177 parasitoids 235 symphylids 177 Sphaceloma fawcettii 65 biology 178 spherical mealybug 59, 302 chemical control 179 Sphingidae 136, 147, 319 control 178 spider mites 115 economic thresholds 178 spiked mealybug 302 IPM 179 Spilochalcis 42, 369 Sympiesis striatipes 79 spined citrus bug 59 Synopeas 85 spiny blackfly 59 Syntermes obtusus 168 spirea aphid 60, 61, 62, 75, 303 Syrphidae 270, 363 see also Aphis spiral nematodes 160 spiralling whitefly 303 Thrips hawaiiensis life history 37 Spodoptera Tachardiaephagus tachardiae 341 exigua 171 Tachinidae 270 littoralis 306 Tallula 106 litura 171 Talponia batesi 207, 208 ornithogalli 383 Tamarixia spotted stink bug 240 dryi 75 Squamurae disciplaga 213 radiata 75 Steatococcus 302 Tarbinskiellus portentosus 167 samaraius 133, 302 Tarsonemidae 64, 137, 166, 308, 382 Steinernema 27 Tarsonemus 166, 308 Stellate scale 304 stammeri 382 Steneotarsonemus ananas 166, 175 Taylorilygus 242 Stenoma catenifer 247 tea yellow thrips 351 hosts 248 Tegolophus life cycle 248 australis 58 parasitoids 248 guavae 308, 311 Stenomesius japonicus 79 perseaflorae 226 Stenomidae 306 Teleogryllus Stenozygum coloratum 240 mitratus 167 Stenygra conspicua 382 oceanicus 167 Stephania japonica 336 Telsemia 69 Sternochetus temolillo 307 frigidus 111 Tenuipalpidae 65, 137, 166, 308, 382 gravis 111 Tephritidae 108, 135, 255, 298, 299, 324, 384

436 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:36 PM Color profile: Disabled Composite 150 lpi at 45 degrees

Index 429

termites see Termitidae Thysanoptera 107, 135, 168, 305, 382 Termitidae 87, 120, 168, 226, 380, 383 Thysanus merceti 235 Tessaritoma 343 Timocratica palpalis 306 biological control 343, 344 Timolius echion 170 biology 342 Tinea 38 control 343, 344 Tineidae 171, 306 damage litchi 343 Tingidae 132, 242 distribution 342 tip wilters 113 javanica 342 Tiracola 77 papillosa 342 plagiata 136 quadrata 342 Tirathaba 38 Tessaritomidae 342 tobacco cutworm 171 Tetracnemoidea Tortricidae 106, 136, 207, 306, 307, 323 brevicornis 71, 72 Tortrix 77 peregrina 72 capensana 250 sydneyensis 72 Toxoptera 60 Tetraleurodes aurantii 5, 134, 146, 212, 303, 325 acaciae 134 citricidus 59, 60, 75 truncatus 303 Toxotrypana 139 Tetramorium guineense 24 biology 140 Tetranychidae 66, 137, 308, 318, 382 curvicauda 136, 140, 398 Tetranychus 43 Trachelas 80 cinnabarinus 137, 144, 226 Trialeurodes desertorum 374, 382 floridensis 303 lambi 43 vaporariorum 228, 303 mexicanus 374, 382 variabilis 134 neocaledonicus 213 Trichaltica bogotana 382 truncatus 137 Trichogramma 77 tumidus 137 bactrae 335 urticae 60, 66, 137, 213, 226, 382, fulva 335 398 Trichogrammatidae 77, 87 Texas citrus mite 60, 66 Trigona 38, 120, 272, 363 Theba 88 amalthea 383 Thecla 208 amazonensis 383 basilides 170, 184 iridipennis 352 biology 208 spinipes 209, 327, 364, 381, 383 control 208 control 381 ortyginus 207 injury 381 Thripidae 113, 135, 168, 243, 305, 382 life cycle 381 Thrips 85, 107, 113, 209 natural enemies 381 damage mango 113 Trinervitermes oeconomus 168 hawaiiensis 36 Triophtydeus 177 imaginis 107, 351 Trioza litchi 351 anceps 237 monitoring 107 eritreae 59, 73, 74, 75 palmi 107 biology 73 parasitoids 87 damage 73 tabaci 135, 168, 179 IPM 74 biology 179 monitoring 74 IPM 180 parasitoids 74 monitoring 180 perseae 237 parasites 180 damage 237 pathogens 180 Triozoida 305 predators 180 Thripobius semiluteus 87 sampling 180 Trissolcus 87 Thyphlodromus athiasae 246 basalis 87 Thyrinteina arnobia 305 mitsukurii 87

437 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:36 PM Color profile: Disabled Composite 150 lpi at 45 degrees

430 Index

Trissolcus continued weevils 339 nakagawai 87 trapping 22 oenone 87 West Indian fruit fly 298 tristeza 61 West Indian red scale 60, 68 Trochalus politus 172 western avocado leafroller 250 tropical citrus 57, 58 western flower thrips 245 tropical fruit 1, 2, 3 white grubs 186 economic importance 166 white moth cicada 318 economic injury levels 64 biology 318 economic thresholds 6 control 319 pesticides 31 white peach scale 142 phenology 1 white wax scale 230 quarantine treatments 398 parasitoids 231 world production 2 predators 231 true bugs 86–87 whiteflies 118 trunk borer 307 cloudy-winged 61 Tryphactothrips 36 damage 72 Tuckerella parasitoids 72 ornata 137, 148 soursop 212 pavoniformis 137 woolly whitefly 61, 303 Tuckerellidae 137 world distribution citrus pests 59, 60 two-spotted mite 60, 62 see also Tetranychus urticae Tydeidae 137, 177, 308 Xanthopimpla 77 Tydeus 137, 308 Xiphosomella 207 Tylenchus 88 Xyleborus perforans 213 Typhlodromalus peregrinus 65 Xylocopa 364 Typhlodromus 346 frontalis 365 fleschneri 346 mordax 363 floridanus 225 suspecta 363 varipuncta 363, 366 Xylosandrus 261 Unaspis compactus 119 citri 59, 68, 69, 305 Xylotrupes gideon 340 yanonensis 61, 68, 69

yanone scale 61, 62, 68, 69 Valanga nigricornis 308 yellow beetle 307 vapour heat 397 yellow peach moth 208 variegated caper bug 240 yellow spot thrips 179 Veneza zonatus 384 yellow-edged stink bug 241 Vespidae 270 yield loss 19 Vinsonia stellifera 304 Yponomeutidae 351 violet aphid 303

Zaommomentedon brevipetiolatus 79 wasps 87 Zapriothrica salebrosa 372, 384 water hyacinth weevil 24 Zeuzera coffeae 213, 351

438 Z:\Customer\CABI\A4285 - Pena\A4351 - Pena #D.vp Monday, July 08, 2002 1:39:36 PM