Fourteenth Australian Weeds Conference

Analysis of the non-target attack by the sap-sucking bug, Aconophora compressa, and its implications for biological control in Australia

William A. Palmer, Michael D. Day, Kunjithapatham Dhileepan, Elizabeth L. Snow and A. Peter Mackey Alan Fletcher Research Station, Queensland Department of Natural Resources, Mines and Energy, PO Box 36, Sherwood, Queensland 4075, Australia

Summary The lantana sap–sucking bug, Acono- INTRODUCTION phora compressa was released in Australia in 1995 The woody shrub L. () for the biological control of Lantana camara. In is one of the worst weeds in Australia and the world 1999, the was also found on fi ddlewood trees, (Thorp and Lynch 2000, Day et al. 2003). It has been , before heatwaves extirpated a target for biological control in various countries for the localised populations. In spring 2002, the insect over a century, during which time 30 agents have been reappeared on fi ddlewoods and by autumn 2003 fi d- released in Australia and 41 agents have been released dlewoods throughout Brisbane were being severely world wide (Day et al. 2003). affected. Massive populations built up on these trees Aconophora compressa Walker (Homoptera: and ‘overfl ow’ populations then produced a range of Membracidae) was released in Australia in 1995. host-insect relationships on other garden plants. Heat- The insect was sourced from Mexico, where Lantana waves in early 2004 again reduced populations from spp. are the only identifi ed hosts (Dietrich and Deitz most areas of Brisbane, south-eastern Queensland and 1991). It was tested against 62 plant species (Palmer northern NSW. et al. 1996) before being approved for release by the Investigative research indicated that 10 species appropriate authorities. The insect was mass reared in including Duranta erecta and Jacaranda mimosifolia Brisbane and over 130,000 were released in Queens- were marginal hosts on which the insect can complete land and NSW during the next eight years. The insect its life cycle but not build up to damaging populations. established on lantana at various sites and considerable The insect was able to feed but not complete a life damage to lantana was recorded. cycle on 10 other species. Although the host testing required for release in This first substantial non-target attack by an Australia was conducted using the centrifugal design approved weed biological control agent recorded in proposed by Wapshere (1975), the West Indian ver- Australia has already led to a more conservative ap- benaceous tree, fi ddlewood, was not included in the proach to introductions by both approving agencies and approved host test list (Palmer et al. 1996) and the rea- sponsoring organisations that do not want community sons for its omission have been discussed (McFadyen and political opprobrium associated with a signifi cant et al. 2003, Palmer 2004). It was also not included in non-target effect. For example, the leaf beetle Chari- the host testing in South Africa, where lantana is also dotis auroguttata was not approved for biocontrol of a serious weed and where fi ddlewoods are also grown cat’s claw creeper Macfadyena unguis-cati, principally as ornamental trees. because adults fed on other plant species to the extent After fi eld establishment, it became evident that that overfl ow populations from cat’s claw creeper might fi ddlewood is also a good host for A. compressa. This cause observable damage in gardens. paper describes the non-target attack by A. compressa Non-target effects of biocontrol agents are of obvi- on fi ddlewood and other plants and comments on the ous concern but should be kept in perspective. For that importance of this attack in relation to the future ap- reason, agents have been released in the past despite proval and release of other biocontrol agents. their developing on non-target species during testing (with very low levels of survival) or feeding but not DESCRIPTION OF INFESTATION reproducing on non-target plants. In 1999, and again in 2001, the insect was found on Biological control offers great prospects for the fi ddlewood trees, but on each occasion the popula- control of many of Australia’s worst invasive exotic tions were extirpated by heatwaves before they could weeds. Any scientifi c or regulatory over-reaction to be studied. In spring 2002 a further population was a case of non-target attack will adversely affect the found in the Brisbane bay side suburb of Capalaba. A overall prospects of controlling these serious weeds. trickle of new infestations occurred over the next six Keywords Aconophora, non-target effects, biological months before they became of widespread concern by control, fi ddlewood, observed host range. May 2003. Over 1000 infestations of fi ddlewood with

341 Fourteenth Australian Weeds Conference

A. compressa were reported by concerned house- Table 1. Assessment of various plants as hosts for holders between May and December 2003. In early A. compressa. 2004 two heatwaves occurred across south-eastern Class 1. Hosts capable of sustaining populations over Queensland, such that almost all populations were extended periods and supporting population increase. again extirpated and the problem abated. Lantana camara (Verbenaceae) During May and December 2003, fi ddlewood trees Citharexylum spinosum (Verbenaceae) became very heavily infested with A. compressa. No attempt was made to estimate populations but some Class 2. Hosts capable of supporting oviposition and trees may have had millions of individuals as they complete immature development, but not supporting encrusted all available branches and stems. Symptoms population increase. of damage became evident as populations built up and Aegiceras corniculatum (L.) Blanco (Myrsinaceae) eventually some trees were completely defoliated. Baccharis halimifolia L. (Asteraceae) While feeding on the trees, the exuded copi- Clerodendrum ugandense Prain. (Lamiaceae) ous quantities of honeydew. In some circumstances Duranta erecta L. (Verbenaceae) the honeydew became a signifi cant problem as plants, Eremophila bignoniifolia (Benth.) F.Muell. (Myoporaceae) paths and vehicles became sticky and then blackened Eremophila nivea Chinnock (Myoporaceae) by resulting sooty moulds. The high sugar content Jacaranda mimosifolia D.Don (Bignoniaceae) of the honeydew also caused lawns to yellow. After alba (Mill.) Br. ex Britton & Wilson (Verbenaceae) trees were defoliated, they no longer supported large Tecoma stans (L.) Juss. ex Kunth (Bignoniaceae) populations and the trees received some respite. The Vitex trifolia L. (Verbenaceae) trees then re-foliated, with much of the new growth coming from epicormic buds. Very few, if any, trees Class 3. Hosts capable of supporting limited feeding died, although mortalities were anticipated had the suffi cient for survival of adults and partial development of attack been sustained. nymphs. When populations became high on the fid- Avicennia marina (Forssk.) Vierh. (Avicenniaceae) dlewoods and particularly in the defoliation phase, Clerodendrum costatum R.Br. (Lamiaceae) numbers of the insect overfl owed onto other plants Eremophila glabra (R.Br.) Ostenf. (Myoporaceae) in proximity to the fi ddlewoods. The bug exhibited a Eremophila maculata (Ker Gawl.) F.Muell. (Myoporaceae) range of responses to these various plants from simply Myoporum acuminatum R.Br. (Myoporaceae) ‘resting’ on them through to feeding, oviposition and Myoporum montanum R.Br. (Myoporaceae) nymphal development. Pandorea jasminoides (Lindl.) K.Schum. (Bignoniaceae) OBSERVED HOST RANGE Pandorea pandorana (Andrews) Steenis Public reports indicated that A. compressa was being Petrea volubilis L. (Bignoniaceae) found on a range of plants in the vicinity of heavily Prostanthera striatifl ora F.Muell. (Lamiaceae) infested fi ddlewood. It was quickly recognised that an ‘overfl ow’ was occurring and that the insect was only Class 4. Plants not suitable for feeding or oviposition by resting on many of these plants. Further, these plants the insect. were being continually reinfested from populations Camellia japonica L. (Theaceae) on the fi ddlewoods making it very diffi cult to assess Gardenia spp. (Rubiaceae) the actual host status. The host range of the insect Grevillea sp. (Proteaceae) was determined using two techniques. Staff visited Leea indica Merr. (Leeaceae) householders reporting non-target attack and placed Myoporum ellipticum R.Br. (Myoporaceae) mosquito-netting bags around populations on a pos- Myoporum parvifolium R.Br. (Myoporaceae) sible host. The bags, which prevented new insects ar- Pentas sp. (Rubiaceae) riving and old insects from leaving, were kept on the Prostanthera ovalifolia R.Br. (Lamiaceae) plant until all insects had died and periodic examina- Stachytarpheta cayennensis (Rich.) J.Vahl (Verbenaceae) tions allowed any oviposition, feeding and nymphal Stachytarpheta mutabilis (Jacq.) J.Vahl (Verbenaceae) development to be noted. The second technique was to conduct no-choice, caged tests in glasshouses at the Alan Fletcher Research Station. These assessments indicated that fi ddlewood and From these tests, supported by appropriate ad- lantana were the only ‘good’ hosts capable of sustain- ditional fi eld observations, the suitability of 34 plant ing populations of A. compressa. Other marginal hosts species was assessed (Table 1). (Table 1, Class 2) were able to support a low level

342 Fourteenth Australian Weeds Conference of immature development that was insuffi cient to time thought to be hosts were not capable of sustain- sustain the population over time. Plants in this group ing populations through several generations. Even so, were mainly members of the Verbenaceae or closely the insect could have a temporary impact on various related families such as Bignoniaceae, Lamiaceae or plant species. Myoporaceae. The eventual outcome was ultimately not greatly at variance with the original host testing which suggested AN EARLY CONSEQUENCE that D. erecta and other verbenaceous plants might be In spring 2003 the leaf beetle Charidotis auroguttata marginal hosts. Research on issues to improve the host (Boheman), which had previously been released in testing of phloem feeding insects, in particular whether South Africa, was proposed for release in Australia potted small plants can refl ect a bug’s response on a for the biocontrol of cat’s claw creeper Macfadyena large tree and whether actual feeding can and should unguis-cati (L.) Gentry. Laboratory experiments in be measured, is to be undertaken. quarantine indicated that the insect had a very narrow There have been very few cases of non-target at- host range. In addition to normal attack on cat’s claw tack by biocontrol agents of weeds (Louda et al. 2003). creeper the insect was able to complete its life cycle on Perhaps the most serious is the attack of Rhinocyllus Myoporum boninense ssp. australe Chinnock, albeit conicus Froehlich on native Cirsium spp. in North with very high mortality and much longer development America (Louda et al. 1997, Louda 1998). However, times. The survival and development of the larvae on while this may prove to be the most serious attack in M. boninense ssp. australe was such that the insect terms of long term ecological signifi cance, these ef- could not sustain a population on this plant, let alone fects were still subtle and the general public was largely build up in damaging numbers. The adults were also unaware and therefore unconcerned. The attack by A. able to feed on Myoporum spp. and several other re- compressa was almost the reverse, with no ecological lated species such that some feeding by adults could damage, but signifi cant concern by the urban public. be anticipated on these plants if they were growing The fact that the urban public was involved is also near heavily infested cat’s claw creeper. of particular interest because risk assessments for The ability of a prospective insect to maintain a prospective agents tend to focus on native fl ora and population on a non-target host has been an interna- agricultural crops and pastures. tionally accepted criterion when determining whether Because the urban public became concerned an insect should be approved for release. Examples about the non-target attack, it was inevitable that of cases when beetles have been approved for release those charged with deciding whether agents are safe even though the adults fed on non-targets include to release in Australia would be sensitive to the issue. Zygogramma bicolorata Pallister and Listronotus se- It is therefore important that this instance be properly tosipennis (Hustache) which could feed on sunfl ower investigated and explained so that host testing proce- (Wild et al. 1992, McFadyen 1998), Microlarinus spp. dures and guidelines can be improved for the future and which could feed on various crops including alfalfa that decision makers have confi dence in the system. (lucerne) (Andres and Angalet 1963, Andres 1978) and It is also important that there is not a ‘knee jerk’ more recently Galerucella spp. which feed on crepe reaction to instances of non-target attack because bio- myrtle (Schooler et al. 2003). logical control offers great prospects for the control of In this case the application to release C. aurogut- many of Australia’s worst invasive exotic weeds. Any tata was rejected largely because of the concerns about scientifi c or regulatory over-reaction to a case of non- adult feeding and comments received from reviewers target attack will adversely affect the overall prospects indicated that the unfolding situation with A. com- of controlling these serious weeds. pressa had made their judgements more conservative. Further, even if approval had been obtained there may ACKNOWLEDGMENTS have been considerable, but understandable, reluctance Many people have contributed to this study particularly to release the insect because of possible community Mariano Trevińo, Rose Broe, Wilmot Senaratne, Allan and political opprobrium associated with a signifi cant Tomley, Tanya Grimshaw, Peter Jones and Anne-Rose non-target effect following so quickly after those of Chamberlain. Aconophora. REFERENCES DISCUSSION Andres, L.A. (1978). Biological control of puncture- After the A. compressa event had run its course, it vine, Tribulus terrestris (Zygophyllaceae): Post became evident that only one good host other than introduction collection records of Microlarinus lantana was involved and that the other plants at one spp. (Coleoptera: Curculionidae). Proceedings

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of the IV International Symposium on Biological McFadyen, R.E., Day, M.D. and Palmer, W.A. (2003). Control of Weeds, ed. T.E. Freeman, pp. 132-6. Putting a price on ornamentals. Biocontrol news (University of Florida, Gainsville, Florida). and information 24, 48-9. Andres, L.A. and Angalet, G.W. (1963). Notes on Palmer, W.A. (2004). Risk analyses of recent cases of the ecology and host specifi city of Microlarinus non-target attack by potential biocontrol agents in lareynii and M. lypriformis (Coleoptera: Curcu- Queensland. Proceedings of the XI international lionidae) and the biological control of puncture symposium on biological control of weeds, ed. vine, Tribulus terrestris. Journal of Economic J.M. Cullen. (CSIRO, Canberra). (In press). Entomology 56, 333-40. Palmer, W.A., Willson, B.W. and Pullen, K.R. (1996). Day, M.D., Wiley, C.J., Playford, J. and Zalucki, M.P. The host range of Aconophora compressa Walker (2003). ‘Lantana: Current management status and (Homoptera: Membracidae): a potential biologi- future prospects’. (ACIAR, Canberra). cal control agent for Lantana camara L. (Verben- Dietrich, C.H. and Deitz, L.L. 1991. Revision of aceae). Proceedings of the Entomological Society the neotropical tribe Aconophorini of Washington 98, 617-24. (Homoptera: Membracidae). North Carolina Schooler, S.S., Coombs, E.M. and McEvoy, P.B. Agricultural Research Service, Raleigh, North (2003). Nontarget effects on crepe myrtle by Carolina. Galerucella pusilla and G. calmariensis (Chry- Louda, S.M. (1998). Population growth of Rhinocyl- somelidae), used for biological control of purple lus conicus (Coleoptera: Curculionidae) on two loosestrife (Lythrum salicaria). Weed Science 51, species of native thistles in prairie. Environmental 449-55. Entomology 27, 834-41. Thorp, J.R. and Lynch, R. (2000). The Determination Louda, S.M., Kendall, D., Connor, J. and Simberloff, of Weeds of National Signifi cance. National Weeds D. (1997). Ecological effects of an insect intro- Strategy Executive Committee, Launceston. duced for the biological control of weeds. Science Wapshere, A.J. (1975). A protocol for programmes for 277, 1088-90. biological control of weeds. PANS 21, 295-303. Louda, S.M., Pemberton, R.W., Johnson, M.T. and Fol- Wild, C.H., McFadyen, R.E.C., Tomley, A.J. and Wil- lett, P.A. (2003). Nontarget effects – The Achilles’ son, B.W. (1992). The biology and host specifi city heel of biological control? Retrospective analyses of the stem-boring weevil Listronotus setosipennis to reduce risk associated with biocontrol introduc- (Coleoptera: Curculionidae) a potential biocontrol tions. Annual Review of Entomology 48, 365-96. agent for Parthenium hysterophorus (Asteraceae). McFadyen, R.E.C. (1998). Biological control of weeds. Entomophaga 37, 591-8. Annual Review of Entomology 43, 369-93.

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