Classical Biological Control of Arthropods in Australia (ACIAR Monographs)

Classical Biological Control of Arthropods in Australia

Contents

Arthropod index General index List of targets

D.F. Waterhouse D.P.A. Sands

CSIRo Entomology Australian Centre for International Agricultural Research Canberra 2001

Back Forward

Contents

Arthropod index General index The Australian Centre for International Agricultural Research (ACIAR) was established in June 1982 by an Act of the Australian Parliament. Its primary mandate is to help identify agricultural problems in developing countries and to commission collaborative research between Australian and developing country researchers in fields where Australia has special competence. Where trade names are used this constitutes neither endorsement of nor discrimination against any product by the Centre.

ACIAR MONOGRAPH SERIES This peer-reviewed series contains the results of original research supported by ACIAR, or material deemed relevant to ACIAR’s research objectives. The series is distributed internationally, with an emphasis on the Third World.

© Australian Centre for International Agricultural Research, GPO Box 1571, Canberra ACT 2601, Australia

Waterhouse, D.F. and Sands, D.P.A. 2001. Classical biological control of arthropods in Australia. ACIAR Monograph No. 77, 560 pages.

ISBN 0 642 45709 3 (print) ISBN 0 642 45710 7 (electronic) Published in association with CSIRO Entomology (Canberra) and CSIRO Publishing (Melbourne) Scientific editing by Dr Mary Webb, Arawang Editorial, Canberra Design and typesetting by ClarusDesign, Canberra Printed by Brown Prior Anderson, Melbourne Cover: An ichneumonid parasitoid Megarhyssa nortoni ovipositing on a larva of sirex wood wasp, Sirex noctilio.

List of targets

Back Forward

Contents

Arthropod index General index

Foreword

List of targets

WHEN THE CSIR Division of Economic Entomology, now Commonwealth Scientific and Industrial Research Organisation (CSIRO) Entomology, was established in 1928, classical biological control was given as one of its core activities. This was indicative of the emphasis to be placed on biological control in Australia for the foreseeable future and was logical when one considers the potential targets for this approach amongst the many exotic pests of the introduced plants on which Australia still depends almost entirely for its agricultural productivity. Biological control has continued as a mainstay of pest management to the present time, with an impressive number of successes over the years. The first comprehensive review of biological control projects in Australia (which also included those in Papua New Guinea) was that of Wilson (1960). This covered attempts against 53 arthropod pests or groups of pests and 12 weeds. There followed coverage of the world scene by Clausen (1978a), which added brief accounts on Australian projects. Worldwide projects on weeds have been regularly summarised in an abbreviated form by M.H. Julien (Julien and Griffiths 1999) but a comprehensive account of the entire range of arthropod projects in Australia up to the present time, now totalling 98 arthropod pests or groups of pests, has been sorely needed for some time. The authors are to be congratulated on their dedication and persistence in amassing the extensive and scattered information required for the task. Congratulations are also due to the Australian Centre for International Agricultural Research (ACIAR), the publisher of this book. This project further extends our close collaboration on biological control activities in the oceanic Pacific and Southeast Asia. ACIAR has already published an impressive number of volumes relevant to the development of significant programs (Li Li-ying et al. 1997; Waterhouse 1993a,b, 1994, 1997, 1998; Waterhouse and Norris 1987, 1989; Waterhouse et al. 1999; Klein Koch and Waterhouse 2001; Morris and Waterhouse 2001). One spectacular success has been the effective control of a serious defoliator, the

3

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index banana skipper in Papua New Guinea. This has, so far, halted its spread to Australia, with an extraordinarily high estimated benefit–cost ratio of 607:1. This is an excellent example of ACIAR’s policy of taking preemptive action to help an overseas country and, at the same time, Australia, by dealing with a threat to Australian agriculture before it reaches our shores. Classical biological control has the capacity to yield extensive and enduring returns in pest management, though success is not always guaranteed. In their brief overview, the authors estimate an overall success rate of about two-thirds for all projects. This in itself represents a remarkable return on the scientific investment made. I warmly commend this volume not only for the wealth of information it contains, but also as an invaluable record of what can and has been achieved by this approach and as an indication of the opportunities that still exist to extend and improve the approach further for Australia’s benefit.

Jim Cullen Chief, Division of Entomology CSIRO, Canberra

4

General index

List of targets

Back Forward

Arthropod index General index

List of targets

Contents

Foreword A Tribute Abstract Acknowledgments

3 7 8 9

Introduction List of targets List of tables Arthropod pests and natural enemies released Details of biological control projects Overview References Arthropod index General index

5

11 17 20 25 99 437 441 503 546

Back Forward

Contents

Arthropod index General index

List of targets

6

Back Forward

Contents

Arthropod index General index

A Tribute

List of targets

IN HIS retirement from 1981 to 2000, the late Dr Doug Waterhouse authored or co-authored 12 books on the biological control, distribution and importance of pests and weeds. These publications are of immense importance and relevance to the objectives of both CSIRO Entomology and ACIAR as they promote the economic, social and environmental benefits to be had with appropriate management of insects. His texts have drawn together relevant information available from as many sources as possible, enabling students and research workers to locate easily, most or all of the information on pests and weeds of Pacific and Southeast Asian countries. The books are essential for planning future biological control projects in the region. This most recent book by Dr Waterhouse, Classical Biological Control of Arthropods in Australia co-authored with Dr Sands, is the last in the series on regional biological control programs. It covers the history until 1999, of arthropod biological control introductions into Australia, and updates information on biological control projects carried out since the publication by Wilson (1960). Entomologists, including the scientists affiliated with CSIRO Entomology, are deeply indebted to Dr Waterhouse for the contributions he has made in all the books published after his retirement. They will be referred to for years to come, guiding new initiatives and recording part of the history of safely and successfully controlling pests and weeds, by classical biological control in Australia and the neighbouring developing nations.

R.J. Clements Director, ACIAR

7

Back Forward

Contents

Arthropod index General index

Abstract

List of targets

AN ACCOUNT is provided of attempts at biological control of arthropod pests in Australia. Ninety-eight pests or groups of pests have been involved, totalling some 150 species, most of which are exotic. Some 70 were targetted in specific projects. The pests are listed alphabetically under Collembola (1), Hemiptera (56), Thysanoptera (1), Orthoptera (2), Coleoptera (9), Diptera (7), Lepidoptera (13), Hymenoptera (4), Acari (4) and Diplopoda (1). In addition to a summary table of results, a short dossier on each pest species or group provides (a) a precis of the outcomes, together with basic data on biology and pest status, (b) information on native natural enemies and (c) an account of the attempt(s) at biological control and the biology of the most important natural enemies. Without recent evaluations it is often not possible to assess accurately the level of successful control, but a general overview indicates that about 30 of the target pests are very well controlled and a further 20 are no longer important pests, indicating an overall success rate for target pests of about two-thirds. With the exception of the dung-breeding bush fly, native pests have not proved susceptible to classical biological control.

8

Back Forward

Contents

Arthropod index General index

Acknowledgments MANY COLLEAGUES within CSIRO Entomology, State Departments of Agriculture and universities have provided valuable information and comment, often providing more accurate and up-to-date accounts of the various projects than is available from publications. Although it is not possible to acknowledge all of the many individuals involved, very special thanks are due to Dr M. Carver for much unpublished information on the aphid pests listed. Mr D. Smith of the Queensland Department of Primary Industries (QDPI), Nambour, Queensland provided most valuable information on scales and mealybugs. Mr J. Feehan supplied unpublished information on the distribution and impact of dung beetles and this was supplemented by Drs M. Tyndale-Biscoe, T.J. Ridsdill-Smith and J.N. Mathiessen. Others in CSIRO Entomology include Drs G.H. Baker, J. Daly, P. Greenslade, B.H. Halliday, G.A. Macqueen, W. Milne, R.J. Milner, L.A. Mound, K.R. Norris, J.L. Readshaw, J.P. Spradbery, R.W. Sutherst and K.G. Wardhaugh. Valuable inputs were also provided by Queensland

New South Wales

G.K. Waite, QDPI Nambour; B.C.G. Scholtz and D.A.H. Murray, QDPI Toowoomba; Prof. R.A.I. Drew, Griffith University; J.F. Grimshaw and B.M. Waterhouse, Northern Australia Quarantine Strategy (NAQS) Mareeba; K.H. Halfpapp, QDPI, Mareeba; K.J. Chandler and Dr P.G. Allsopp, Bureau of Sugar Expermiment Stations Dr B.J. Fletcher (retired CSIRO); Major S.P. Francis, Army Malaria Research Unit; J. McIntosh, Australian Museum

9

List of targets

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index Australian Capital Territory

Victoria South Australia Western Australia Northern Territory The Natural History Museum, London

Dr P. Ferrar, ACIAR; Dr G.V. Maynard, Australian Quarantine and Inspection Service (AQIS) Dr R.P. Field, National Museum; Dr T.R. New, La Trobe University Dr F.D. Morgan, formerly Waite Institute A.C. Postle, NAQS, Broome; G.R. Strickland, Department of Agriculture T.L. Fenner, NT Quarantine; D. Chin, Department of Agriculture Dr D.J. Williams

We are most grateful for the valuable data processing inputs provided by Mrs Leanne Slarke and Mrs Bev Johnstone. To Dr Mary Webb, Mrs Kerry Highley and Mr Peter Lynch (ACIAR), we extend our thanks for invaluable editorial advice and help during the later stages of preparation of the text, tables and maps for the book. It would not have been possible to undertake a major task such as this, when in retirement, without the encouragement, support and patience of Dawn and Susan, our wives, to whom very special appreciation and thanks are due.

10

General index

List of targets

Back Forward

Contents

Arthropod index General index

Introduction

List of targets

MANY INSECTS that are of little or no economic importance in their country of origin become important pests when they are introduced to another country without their own natural enemies. Classical biological control is the term used when some or all of these natural enemies are introduced and established in the new country. Areas of the world where much of today’s agriculture is based on introduced crops (e.g. Australia, New Zealand, Hawaii and California) are notable for two facts. One is that a high proportion of their important arthropod pests are exotic; the other is that classical biological control has resulted in many important successes. Worldwide, biological control—either standing alone or as a component of integrated pest management—is attracting increasing interest, partly in order to reduce dependence upon pesticides. Much can be learnt from successes (and failures) with classical biological control projects around the world. A major aim of this publication is to provide ready access, in a single table, to a summary of information on the natural enemies that have been liberated for classical biological control of arthropods in Australia up to 2000, including (when available) their origin, year(s) of liberation, whether they have been established and with what effect. We have adopted, in the ‘Effect’ column of Table 1 page 29, a simple rating system where an introduced natural enemy has become established. The number of ‘+’ symbols in this column is an indication either of (a) when known, the impact of the presence of the natural enemy on the pest population or (b) the resulting abundance of the natural enemy, when the relationship between its abundance and the pest population has not been established. In many cases the indication of effect is a very subjective one, since there has often been no adequate evaluation in recent years, if at all. It is, perhaps, also not surprising that some species have been introduced into quarantine but not liberated. Sometimes this has been due to the very low numbers of living natural enemies imported, to difficulties in breeding them on the target host, or a decision not to liberate because of real or apparent lack of specificity or effectiveness.

11

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index A further problem when considering the effectiveness of introductions is the very wide range of situations (agroecosystems) in which a pest may occur in a country as large and diverse as Australia. Introduced natural enemies are sometimes very highly effective in one of a set of microclimates or one group of crops, but far less effective in another set. An example of this is provided by the parasitoid Trissolcus basalis and the once very widespread green vegetable bug, Nezara viridula. The bug is now suppressed by the parasitoid in much of south-eastern New South Wales and Victoria to the extent that it has become an uncommon pest. However, in southern Queensland (particularly where soybeans are grown) and also in a strip of inland New South Wales, extending even into Victoria, it is still regarded as a serious pest. Thus biological control has undoubtedly been highly successful over a vast area, although the pest continues to be a problem elsewhere. It should be pointed out that, whatever the level of suppression brought about by natural enemies, it is highly likely that any contribution they can give to the suppression of pest numbers will be a useful contribution to the integrated management of the pest. In addition to records in the main table (Table 1 page 29), a brief dossier is provided on each pest and Australian locations mentioned in the text are shown in Map 1 page 22. Only about one-third of the target pests were subjected to major, as contrasted with minor, biological control projects. Since a great deal more information is available on the major attempts than on the remaining targets, these pests are dealt with in considerably greater detail in the individual dossiers. The dossiers outline relevant aspects of biology and pest status and provide details of the attempt(s) at biological control and native natural enemies. It would not be feasible in a book of this size to deal exhaustively with all these aspects. However, key references are provided to facilitate access to the sometimes very extensive literature. Eleven of the pests have already been dealt with, often in far greater depth, in dossiers published elsewhere (Waterhouse 1993a, 1998; Waterhouse and Norris 1987, 1989) and these have been drawn on extensively in the present accounts of these pests.

12

General index

List of targets

Back Forward

Contents T ARGET P EST N O . I NTRODUCTION

Arthropod index Australia’s first involvement with classical biological control was when it served as a source of parasitoids and predators of insect pests (including the Australian cottony cushion scale, Icerya purchasi) that had become established in California and Hawaii. This occurred when A. Koebele visited Australia in 1888 and 1891. The natural enemies sent to California included the predaceous coccinellid beetles Rodolia cardinalis, Rhyzobius ventralis and Cryptolaemus montrouzieri and the parasitic flies Cryptochetum iceryae and C. monophlebi. Information on early attempts at classical biological control of insects in Australia was assembled in a valuable review by Wilson (1960), but the names of many of the insects involved have since undergone taxonomic changes. The first record of an attempt at establishment of a biological control agent in Australia was of the coccinellid Harmonia conformis sent from New South Wales to Western Australia in 1896. However, it only later became established from Tasmanian adults in 1902, following fruitless liberations in intervening years from New South Wales and Tasmania. Although both South Australia and Tasmania, as well as Western Australia, introduced various coccinellids from other parts of Australia on several occasions before 1900, it was Western Australia that took the lead in relation to the introduction of exotic species when, in 1901, it appointed G. Compere as entomologist to its Department of Agriculture. His task was to introduce natural enemies of the main pests. He travelled widely around the world until 1910, sending back many parasitoids and predators. Wilson (1960) commented that many of these species were not identified and much of this early work was very poorly documented. Modern classical biological control should certainly not be carried out in this way. The precise identity of a pest is of minor significance for chemical control, since very few insecticides are sufficiently selective for the exact identity to influence the situation. However, it is quite different for classical biological control. It is then highly desirable (a) that it is the target pest species that suffers by far the greatest adverse effect from the introduction of a natural enemy, (b) that even close relatives, and especially species less closely related to the pest, are not attacked and (c) if they are attacked, that the impact on their abundance is relatively minor.

13

General index

List of targets

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index There have been many changes over the years in the nomenclature of the natural enemies referred to in this publication. Although these have usually not been indicated in the text, where the generally-accepted modern name is used, the older, sometimes more familiar name may be found in the arthropod index, referring to its modern counterpart. It is to be expected that further name changes will be made in the future. The name of the author of each valid species is given in the arthropod index. It is necessary here to issue a word of caution in relation to the validity of the name changes that have been made because, in the majority of cases, it is only the published name of the natural enemy that has been changed. It has not been feasible to check the identity of the natural enemies against voucher specimens and it is possible that the published name has, on occasion, been wrongly applied to the species concerned. Valuable advice on taxonomic problems has been given by colleagues associated with the Australian National Insect Collection, Canberra: Hemiptera, Dr M. Carver; Hymenoptera, J.C. Cardale; Lepidoptera, E.D. Edwards; Diptera, Dr K.R. Norris; Coleoptera, T.A. Weir and Dr E.C. Zimmerman; and Acari, Dr B.H. Halliday. Taxonomic treatment has generally followed that in Insects of Australia (1991). The present nomenclature has been based, inter alia, on the Australian Standard List of Common Names (Naumann 1993), the Catalogue of the Chalcidoidea of the World on CD-ROM (Noyes 1998) and the CABI Arthropod Name Database on CD-ROM (CABI 1995). The nomenclature of mites is based on Halliday (1998) and that of economic plants follows of Lazarides and Hince (1993). The number of aphid pest species considered to be targets in Table 1 ( page 29) cannot be defined easily. This is due to an early adopted practice of introducing polyphagous parasitoids for a particular target species (e.g. Aphis craccivora), but with the hope that they might also assist in the control of one or more non-target pest species (Carver 1989), by developing ‘reservoirs’ of parasitoids in non-target species nearby.

14

General index

List of targets

Back Forward

Contents T ARGET P EST N O . I NTRODUCTION

Arthropod index

1.

2.

3.

With regard to aphid parasitoids (Table 2 page 107): many of the effective parasitoids are polyphagous, although some are restricted to an aphid genus or to a particular habitat (e.g. to aphids on cereals); polyphagous parasitoids have been intentionally introduced that will (or might) attack a range of pest species (Stary 1967b; Carver 1989). Any important pest species attacked by the parasitoid can, therefore, be regarded as a legitimate target of the introduction, and several have been included for this reason; and in earlier years, aphid parasitoids introduced intentionally were often not adequately identified. Whether from this cause, or because they have arrived unaided, the origin and year of arrival of a number of exotic aphid parasitoids that have become established is undocumented. An incomplete picture would be presented if these species were excluded from being listed, so they appear with the symbol (U) for unknown time and method of arrival. At times, additional (often more host-specific) strains of these same species have been introduced to increase the range of pest aphids attacked.

In addition, a deliberate attempt was made to establish, on several non-target aphid pest species already present in Australia, parasitoid species that would be established and waiting should the highly damaging Russian wheat aphid, Diuraphis noxia, arrive in Australia (Hughes et al. 1994). Thus, it was decided to record in Table 1 page 29 a number of pest species which were not primarily or intentionally targetted. These species are annotated throughout the book by the symbol †. Although it would not be reasonable to include such species in calculations of the success of biological control, the information presented is relevant to a consideration of the impact of parasitoids on non-target species. It was also decided to include attempts to control several native pest species by the introduction of exotic natural enemies, although this procedure does not fit the strict definition of classical biological control. The native species involved are: the Queensland fruit fly, Bactrocera tryoni; the native budworm, Helicoverpa punctigera; several native mosquitoes; the pink sugarcane mealybug, Saccharicoccus sacchari; the wingless grasshopper, Phaulacridium vittatum; and the black field cricket, Teleogryllus commodus. Another species, the citrophilus mealybug, Pseudococcus calceolariae, is believed to be native to the Sydney region, where it is rare.

15

General index

List of targets

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index When it appeared in inland areas of South Australia, Victoria and New South Wales, two parasitoids from the Sydney region were introduced to extend biological control of this mealybug to these regions. Not all host records of exotic agents and natural enemies of exotic arthropods have been included in this book, particularly when the information was incomplete. For example, studies on exotic and native natural enemies of Bemisia tabaci biotype B are current (De Barro et al. 2000), but all are not yet completed or documented (P.J. De Barro, pers. comm.). Other records may have been overlooked. However, we hope that an opportunity will be found to add this additional information to a revised edition of this book.

16

General index

List of targets

Back Forward

Contents

Arthropod index General index

List of Targets COLLEMBOLA 1

Sminthurus viridis

100

HEMIPTERA 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33

Acyrthosiphon kondoi Acyrthosiphon pisum Aleurodicus dispersus Aonidiella aurantii Aonidiella citrina Aonidiella orientalis Aphis craccivora Aphis gossypii † Asterodiaspis variolosa Brevicoryne brassicae Cavariella aegopodii Ceroplastes ceriferus † Ceroplastes destructor Ceroplastes floridensis † Ceroplastes rubens Ceroplastes sinensis † Chrysomphalus aonidum Coccus hesperidum Coccus longulus † Coccus pseudomagnoliarum † Coccus viridis Comstockaspis perniciosus Diaspis bromeliae † Edwardsiana froggatti Eriococcus araucariae Eriosoma lanigerum Hyperomyzus lactucae Lepidosaphes beckii † Lepidosaphes gloverii † Macrosiphum rosae Metopolophium dirhodum mirid bugs

105 114 117 120 120 126 129 132 134 137 139 141 144 151 154 159 163 166 170 172 174 177 180 182 184 186 189 192 195 197 199 201

17

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57

Myzus persicae † Nezara viridula Parasaissetia nigra † Parthenolecanium persicae Pentalonia nigronervosa † Pineus boerneri Pineus pini Planococcus citri Pseudococcus calceolariae † Pseudococcus longispinus Pseudococcus viburni Pulvinaria polygonata † Rhopalosiphum maidis † Rhopalosiphum padi † Saccharicoccus sacchari Saissetia coffeae † Saissetia oleae Therioaphis trifolii forma clover † Therioaphis trifolii forma maculata Toxoptera aurantii Toxoptera citricidus Trialeurodes vaporariorum Tuberculatus annulatus Unaspis citri

203 205 210 212 214 216 216 219 226 231 234 236 238 240 243 247 249 254 256 260 260 263 265 267

THYSANOPTERA 58

Heliothrips haemorrhoidalis

272

ORTHOPTERA 59 60

Phaulacridium vittatum Teleogryllus commodus

274 277

COLEOPTERA 61 62 63 64 65 66 67 68 69

Brontispa longissima Bruchus pisorum canegrubs Cosmopolites sordidus Ips grandicollis Listroderes difficilis Pyrrhalta luteola Rhabdoscelus obscurus Sitona discoideus

279 282 284 287 290 294 296 298 300

18

General index

List of targets

Back Forward

Contents T ARGET P EST N O . L IST OF T ARGETS

Arthropod index DIPTERA 70 71 72 73 74 75 76

General index

Bactrocera tryoni Ceratitis capitata Haematobia exigua Lucilia cuprina mosquitoes Musca vetustissima Stomoxys calcitrans

305 316 322 328 333 337 348

LEPIDOPTERA 77 78 79 80 81 82 83 84 85 86 87 88 89

armyworms, cutworms and semi-loopers Cryptophlebia ombrodelta Cydia pomonella Grapholita molesta Helicoverpa armigera Helicoverpa punctigera Hellula undalis Oncopera spp. Phthorimaea operculella Phyllocnistis citrella Pieris rapae Plutella xylostella Sitotroga cerealella

351 357 360 364 369 369 377 379 382 388 392 399 405

HYMENOPTERA 90 91 92 93

Caliroa cerasi Sirex noctilio Vespula germanica Vespula vulgaris

407 409 417 417

ACARI 94 95 96 97

Boophilus microplus Halotydeus destructor Panonychus ulmi Tetranychus urticae

420 422 427 429

JULIDA 98

Ommatoiulus moreleti

433

19

List of targets

Back Forward

Contents

Arthropod index General index

List of Tables Table 1. Table 2. Table 3. Table 4. Table 5. Table 6. Table 7. Table 8. Table 9. Table 10. Table 11. Table 12. Table 13. Table 14. Table 15. Table 16. Table 17. Table 18. Table 19. Table 20. Table 21. Table 22. Table 23. Table 24. Table 25. Table 26. Table 27. Table 28. Table 29. Table 30. Table 31. Table 32.

List of targets

Target, including incidental target (†), pests and natural enemies released Parasitoids of pest aphids in Australia Hyperparasitoids of aphid parasitoids Aphid predators recorded in the aphid data base Fungi attacking pest aphids in Australia Indigenous natural enemies of Aonidiella aurantii and A. citrina Indigenous natural enemies of Aonidiella orientalis Indigenous natural enemies of Ceroplastes ceriferus Indigenous natural enemies of Ceroplastes destructor Indigenous natural enemies of Ceroplastes floridensis Indigenous natural enemies of Ceroplastes rubens Indigenous natural enemies of Ceroplastes sinensis Indigenous natural enemies of Chrysomphalus aonidum Indigenous natural enemies of Coccus hesperidum Indigenous natural enemies of Coccus pseudomagnoliarum Indigenous natural enemies of Coccus viridis Indigenous natural enemies of Comstockaspis perniciosus Indigenous natural enemies of Diaspis bromeliae Indigenous natural enemies of Lepidosaphes beckii Indigenous natural enemies of Nezara viridula Indigenous natural enemies of Parasaissetia nigra Indigenous natural enemies of Parthenolecanium persicae Hymenopterous parasitoids of Planococcus citri on citrus at Mundubbera, Queensland Hymenopterous parasitoids of Pseudococcus calceolariae Hymenopterous parasitoids of Diuraphis noxia in Ukraine, southern Russia and Georgia Natural enemies of Saccharicoccus sacchari Indigenous natural enemies of Saissetia coffeae Indigenous natural enemies of Saissetia oleae Indigenous natural enemies of Unaspis citri Indigenous natural enemies of Haematobia exigua Natural enemies of Lucilia cuprina and other sheep and carrion-feeding Calliphoridae Some Australian mosquito-eating fish

20

29 107 108 109 113 124 128 143 150 153 157 161 165 168 173 176 179 181 194 209 211 213 225 230 242 246 248 252 271 327 332 336

Back Forward

Contents T ARGET P EST N O . L IST OF T ABLES

Arthropod index Table 33. Month of first release in each State and the establishment, where known (*), of exotic dung beetles Table 34. Parasitoids of Stomoxys calcitrans in eastern Australia Table 35. Common Australian cutworms, armyworms and semi-loopers Table 36. Indigenous arthropod natural enemies of armyworms, cutworms and semi-loopers Table 37. Natural enemies of Cryptophlebia ombrodelta in Australia Table 38. Parasitoids attacking Cydia pomonella in Australia Table 39. Parasitoids attacking Grapholita molesta in Australia Table 40. Indigenous arthropod natural enemies of Helicoverpa armigera and H. punctigera Table 41. Natural enemies of Pieris rapae Table 42. Natural enemies of Plutella xylostella Table 43. Natural enemies of Halotydeus destructor in southern New South Wales, 1987–1993 Table 44. Some predators of Tetranychus urticae Table 45. Exotic species that have been (or still are) major pests in Australia Table 46. Exotic species that have been (or are still) minor pests in Australia Table 47. Species that are (or may be) native to the Australian region

21

346 350 355 355 358 363 368 373 396 404 426 432 439 440 440

General index

List of targets

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index Map 1.

Locations of places mentioned in the text

1

Adelaide Hills

45

Mackay

2

Adelaide River

46

Magnetic Island

3

Albany

47

Main Divide

4

Alice Springs

48

Mareeba

5

Alstonville

49

Maryborough

6

Applethorpe

50

Mornington Peninsula

7

Armidale

51

Moe

8

Atherton

52

Moree

9

Bamaga

53

Moruya

10

Batlow

54

Mossman

11

Benalla

55

Mount Isa

12

Bilpin

56

Mundubbera

13

Boigu Island

57

Murray Island

14

Bridgewater

58

Murray River

15

Broome

59

Murray Valley

16

Bundaberg

60

Murrumbidgee Irrigation Area

17

Byfield

61

Murrumbidgee River

18

Cairns

62

Nangiloc

19

Cape York Peninsula

63

Narromine

20

Casino

64

Newcastle

21

Clarence River

65

Norfolk Island

22

Coconut Island

66

Ord

23

Cooktown

67

Palm Island

24

Darnley Island

68

Port Lincoln

25

Dauan Island

69

Prince of Wales Island

26

East Gippsland

70

Queanbeyan

27

Elizabeth Beach

71

Richmond

28

Fremantle

72

Riverina

29

Gippsland

73

Riverland

30

Gosford

74

Rockhampton

31

Goulburn Valley

75

Sabai Island

32

Griffith

76

Sale

33

Grafton

77

Sarina

34

Gympie

78

Seisia

35

Hammond Island

79

Stanthorpe

36

Horn Island

80

Thursday Island

37

Hunter River

81

Torres Strait

38

Innisfail

82

Townsville

39

Kimberley

83

Tully

40

Kuranda

84

Yam Island

41

Lachlan River

85

Yarwun

42

Launceston

86

Yorke Island

43

Lord Howe Island

87

Weipa

44

Loxton

88

Wollongong

22

General index

List of targets

28 3

15 66

Kimberley (39)

4

68

1 44

55

32

82

23 54

42

77

18 38 83 67 46

12

53

52

63

70 72 10 59 14 31 11 29 26 50 76 51

62

58 61 41

Cape York Peninsula (19) 48 8

87

Gre at

2

35, 36, 69, 80

25, 76 84,24 57,86 9,78 22

(47) ge

an

gR

74

45

88

17

30 71

37

7

33 27 64

6,79

56

85

D i di n v i din ivi gR a nge (4 7) Gr e at D

Torres Strait (81) 13

5 20 21

16 49 34

43

Norfolk Island (65) 29°02'S 167°57'E

Back Forward

Contents

Arthropod index General index

List of targets

Back Forward

Contents

Arthropod index General index

List of targets

24

Back Forward

Contents

Arthropod index General index

Target arthropod pests and natural enemies released

List of targets

Back Forward

Contents C LASSICAL B IOLOGICAL C ONTROL OF A RTHROPODS IN A USTRALIA

Arthropod index General index

List of targets TABLE 1 provides a condensed record of the published attempts at biological control of 98 species or groups of species of Australian arthropod pests. Eight of these species or species groups are native to Australia and 18 have only been incidental targets, leaving 72 species that have been direct targets of classical biological control attempts. Further details are provided in the next section for each target pest. The pests are arranged alphabetically under each order and the insect orders arranged from the most primitive to the most advanced. More detailed explanations and clarification of table inclusions are given in the Introduction.

Explanation of abbreviations and symbols used: † ?

pest not primarily targetted not certain A blank space indicates that information was either not available or not relevant.

Biological control agent (U) (#)

unknown time and method of arrival; an exotic natural enemy which apparently arrived unaided introduced primarily against another target pest species (specified at the end of each pest entry)

Host stage

(H.S.)

E L

egg larva (or nymph) (with 1, 2 etc. representing larval instar stages—in later tables) pre-pupa pupa adult

PP P A

26

Back Forward

Contents T ARGET P EST N O . T ARGET ARTHROPOD PESTS AND NATURAL ENEMIES RELEASED

Arthropod index Origin of agent/Liberation location N S E W ACT NSW NT NZ Qld SA Tas UK USA Vic WA

north or northern south or southern east or eastern west or western Australian Capital Territory New South Wales Northern Territory New Zealand Queensland South Australia Tasmania United Kingdom United States of America Victoria Western Australia

Liberation date Where liberations of a natural enemy have been made at various times spanning a sequence of years (e.g. 1963–72), this does not necessarily indicate that all the intervening years were involved. Established (Est.) + (+) –

successfully established established, but only briefly did not establish

Effect (on pest status in the absence of disruption by pesticides) (Eff.) +++ ++ + –

effective biological control, sometimes only regionally partially effective little effect no known effect

27

General index

List of targets

Back Forward

Contents

Arthropod index General index

List of targets

28

Origin of agent

29 L,A

L,A

Aphidius pisivorus (#)

L,A

Aphidius ervi

BRACONIDAE

Aphelinus abdominalis (U)

APHELINIDAE

HYMENOPTERA

1976 1991 1993 1993

WA WA WA WA

1980

1980–81

Japan via USA via NZ, Europe USA

1977–79

Tas, Japan via USA

1979

1965

France

Tas

Liberated

1985–90

1969

France, Morocco France

1965