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Post-release evaluation of Eretmocerus hayati Zolnerowich and Rose in Australia

Published online by Cambridge University Press:  24 October 2008

P.J. De Barro  and
M.T. Coombs
P.J. De Barro*
Affiliation:
CSIRO Entomology, 120 Meiers Road, Indooroopilly, Queensland 4068, Australia
M.T. Coombs
Affiliation:
CSIRO Entomology, 120 Meiers Road, Indooroopilly, Queensland 4068, Australia
*
*Author for correspondence Fax: +61 7 3214 2885 E-mail: paul.debarro@csiro.au
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Abstract

Bemisia tabaci biotype B is a significant pest of agriculture world-wide. It was first detected in Australia in 1994. Assessments of the potential of parasitoids already present in Australia to control this pest indicated that two species of Eretmocerus and 11 species of Encarsia were present, but they did not exert sufficient control with a combined average of 5.0±0.3% apparent parasitism of 4th instars. Further, only 25% of samples containing biotype B had parasitised individuals present. The surveys also identified that fewer B biotype were being parasitised compared with the Australian indigenous biotype. Overall, Er. mundus was the most abundant parasitoid prior to the introduction. Previous research indicated that Er. hayati offered the best prospects for Australia and, in October 2004, the first releases were made. Since then, levels of apparent parasitism have averaged 29.3±0.1% of 4th instars with only 24% of collections having no parasitism present. Eretmocerus hayati contributed 85% of the overall apparent parasitism. In addition, host plants of the whitefly with low or no parasitism prior to the release have had an order of magnitude increase in levels of parasitism. This study covers the establishment of the case to introduce Er. hayati and the post-release establishment period November 2004–March 2008.

Keywords

biological controlEretmocerus mundusefficacy
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 2 , April 2009 , pp. 193 - 206
Copyright
Copyright © 2008 Cambridge University Press

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References

Abd-Rabou, S. (2002) Biological control of two species of whiteflies by Eretmocerus siphonini (Hymenoptera: Aphelinidae) in Egypt. Acta Phytopathologica et Entomologica Hungarica 37, 257–260.CrossRefGoogle Scholar
Abd-Rabou, S. & Ghahari, H. (2005) Biological studies of two strains of Eretmocerus mundus (Hymenoptera: Aphelinidae) on Bemisia argentifolii (Homoptera: Aleyrodidae) from Iran. Egyptian Journal of Agricultural Research 83, 513–523.CrossRefGoogle Scholar
Ardeh, M.J., de Jong, P.W. & van Lenteren, J.C. (2005a) Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretmocerus spp. Biological Control 33, 74–80.CrossRefGoogle Scholar
Ardeh, M.J., de Jong, P.W. & van Lenteren, J.C. (2005b) Selection of Bemisia nymphal stages for oviposition or feeding, and host-handling times of arrhenotokous and thelytokous Eretmocerus mundus and arrhenotokous E. eremicus. BioControl 50, 449–463.CrossRefGoogle Scholar
Borowiec, N., Issimaila, M.A., Chadhouliati, A.C., Youssoufa, M.A., Quilici, S., Delvare, G., Reynaud, B. & Ollivier, L. (2007) Programme de lutte biologique contre Aleurotrachelus atratus Hempel (Hemiptera: Aleyrodidae), principale espèce d'aleurode nuisible au cocotier aux Comores. Rapport technique en fin d'étape 3 et préconisations pour le contrôle durable d'A. atratus aux Comores, Déc. 2006–Sept. 2007. CIRAD-INRAPE-PRPV.Google Scholar
Boykin, L.M., Shatters, R.G., Rosell, R.C., McKenzie, C.L., Bagnall, R.A., De Barro, P.J. & Frohlich, D.R. (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial CO1 DNA sequence. Molecular Phylogenetics and Evolution 44, 1306–1319.CrossRefGoogle Scholar
Bukovinszky, T., Gols, R., Hemerik, L., van Lenteren, J.C. & Vet, L.E.M. (2007) Time allocation of a parasitoid foraging in heterogeneous vegetation: implications for host-parasitoid interactions. Journal of Animal Ecology 76, 845–853.CrossRefGoogle ScholarPubMed
Campbell, B.C., Steffen-Campbell, J.D. & Gill, R.J. (1994) Evolutionary origin of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) inferred from 18S rDNA sequences. Insect Molecular Biology 3, 73–88.CrossRefGoogle ScholarPubMed
Campbell, B.C., Steffen-Campbell, J.D. & Gill, R.J. (1996) Origin and radiation of whiteflies. pp. 29–51in Gerling, D. & Mayer, R.T. (Eds) Bemisia: 1995 Taxonomy, Biology, Damage, Control and Management. Andover, UK, Intercept.Google Scholar
Chermiti, B., Onillon, J.C., Dali, M. & Messelmani, H. (1993) Control of the woolly whitefly, Aleurothrixus floccosus (Hom., Aleurodidae) by the parasitoid, Cales noacki (Hymenopt., Aphelinidae). Bulletin OILB/SROP 16, 86–98.Google Scholar
De Barro, P.J. & Driver, F. (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Australian Journal of Entomology 36, 149–152.CrossRefGoogle Scholar
De Barro, P.J. & Hart, P. (2001) Antibiotic curing of parthenogenesis in Eretmocerus mundus Mercet (Australian parthenogenetic form) (Hymenoptera, Aphelinidae). Entomologia Experimentalis et Applicata 99, 225–230.CrossRefGoogle Scholar
De Barro, P.J., Driver, F., Naumann, I.D., Clarke, G.M., Schmidt, S. & Curran, J. (2000a). Descriptions of three species of Eretmocerus Haldeman (Hymenoptera: Aphelinidae) parasitising Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in Australia based on morphological and molecular data. Australian Journal of Entomology 39, 259–269.CrossRefGoogle Scholar
De Barro, P.J., Hart, P.J. & Morton, R. (2000b) The biology of two Eretmocerus spp. (Haldeman) and three Encarsia spp. Forster and their potential as biological control agents of Bemisia tabaci biotype B in Australia. Entomologia Experimentalis et Applicata 94, 93–102.CrossRefGoogle Scholar
Felsenstein, J. (1993) Phylogeny Inference Package (PHYLIP). Version 3.5. Seattle, WA, University of Washington.Google Scholar
Gerling, D., Rottenberg, O. & Bellows, T.S. (2004) Role of natural enemies and other factors in the dynamics of field populations of the whitefly Siphoninus phillyreae (haliday) in introduced and native environments. Biological Control 31, 199–209.CrossRefGoogle Scholar
Ghahari, H., Huang, J. & Wang, Z.H. (2005) Biology of a thelytokous biotype of Eretmocerus mundus (Hymenoptera: Aphelinidae) on Bemisia tabaci (Homoptera: Aleyrodidae). Insect Science 12, 461–465.CrossRefGoogle Scholar
Gingras, D., Dutilleul, P. & Boivin, G. (2002) Modeling the impact of plant structure on host-finding behaviour of parasitoids. Oecologia 130, 396–402.CrossRefGoogle Scholar
Goolsby, J.A., Legaspi, J.C. & Legaspi, B.C. (1996) Quarantine evaluation of exotic parasites of the sweetpotato whitefly, Bemisia tabaci (Gennadius). Southwestern Entomologist 21, 13–21.Google Scholar
Goolsby, J.A., Ciomperlik, M.A., Legaspi, B.C., Legaspi, J.C. & Wendel, L.E. (1998) Laboratory and field evaluation of exotic parasitoids of Bemisia tabaci (Biotype ‘B’) in the Lower Rio Grande Valley of Texas. Biological Control 12, 27–135.CrossRefGoogle Scholar
Goolsby, J.A., De Barro, P.J., Kirk, A.A., Sutherst, R., Canas, L., Ciomperlik, M., Ellsworth, P., Gould, J., Hartley, D., Hoelmer, K.A., Naranjo, S.J., Rose, M., Roltsch, B., Ruiz, R., Pickett, C. & Vacek, D. (2005) Post-release evaluation of the biological control of Bemisia tabaci biotype ‘B’ in the USA and the development of predictive tools to guide introductions for other countries. Biological Control 32, 70–77.CrossRefGoogle Scholar
Gould, J., Hoelmer, K. & Goolsby, J. (2008) Classical Biological Control of Bemisia tabaci in the United States. A Review of Interagency Research and Implementation. Progress in Biological Control 4, 343 pp.Google Scholar
Gunning, R.V., Byrne, F.J., Conde, B.D, Connelly, M.I., Hergstrom, K. & Devonshire, A.L. (1995) First report of B-biotype Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in Australia. Journal of the Australian Entomological Society 34, 116.CrossRefGoogle Scholar
Headrick, D.H., Bellows, T.S. & Perring, T.M. (1996a) Behaviors of female Eretmocerus sp. nr californicus (Hymenoptera: Aphelinidae) attacking Bemisia argentifolii (Homoptera: Aleyrodidae) on cotton, Gossypium hirsutum (Malvaceae) and melon Cucumis melo (Cucurbitaceae). Biological Control 6, 64–75.CrossRefGoogle Scholar
Headrick, D.H., Bellows, T.S. & Perring, T.M. (1996b) Host plant effects on the behaviors of Eretmocerus sp. nr. californicus raised from melon. Entomophaga 4, 15–26.CrossRefGoogle Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & de Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society London, Series B 270, 313–321.CrossRefGoogle ScholarPubMed
Hoddle, M.S., van Driesche, R.G. & Sanderson, J.P. (1998) Biology and use of the whitefly parasitoid. Annual Review of Entomology 43, 645–669.CrossRefGoogle ScholarPubMed
Horowitz, A.R., Podoler, H. & Gerling, D. (1984) Life table analysis of the tobacco whitefly Bemisia tabaci (Gennadius) in cotton fields in Israel. Acta Oecologica 5, 221–233.Google Scholar
Jetter, K.M. (2000) The economics of biological control. pp. 5–11in Hoddle, M. (Ed) California Conference on Biological Control II. University of California, Berkeley, CA, 11–12 July 2000, Riverside, CA.Google Scholar
Jones, W.A. & Greenberg, S.M. (1998) Suitability of Bemisia argentifolii (Homoptera: Aleyrodidae) instars for the parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Environmental Entomology 27, 1569–1573.CrossRefGoogle Scholar
Li, Z.H., Lammes, F., van Lenteren, J.C., Huisman, P.W.T., van Vianen, A. & de Ponti, O.M.B. (1987) The parasite-host relationship between Encarsia formosa Gahan (Hymenoptera, Aphelinidae) and Trialeurodes vaporariorum (Westwood) (Homoptera, Aleyrodidae). XXV. Influence of leaf structure on the searching activity of Encarsia formosa. Journal of Applied Entomology 104, 297–304.Google Scholar
Liotta, G., Agro, A. & Pinto, M. (2003) Biological control in citrus groves in the last 50 years: three successful cases in Western Sicily. ‘Integrated control in citrus fruit crops’. Proceedings of the IOBC/WPRS Working Group, 6–8 November 2002, Valencia, Spain, Bulletin OILB/SROP 26, 171–173.Google Scholar
Liu, S.S., De Barro, P.J., Xu, J., Luan, J.B., Zang, L.S., Ruan, Y.M. & Wan, F.H. 2007. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318, 1769–1772.CrossRefGoogle Scholar
Liu, T.X. (2007) Life history of Eretmocerus melanoscutus (Hymenoptera: Aphelinidae) parasitizing nymphs of Bemisia tabaci Biotype B (Homoptera: Aleyrodidae). Biological Control 42, 77–85.CrossRefGoogle Scholar
Martin, J.H. (1999) The whitefly fauna of Australia. A taxonomic account and identification guide. CSIRO Entomology Technical Paper No. 38.Google Scholar
McAuslane, H.J. & Nguyen, R. (1996) Reproductive biology and behavior of a thelytokous species of Eretmocerus (Hymenoptera; Aphelinidae) parasitizing Bemisia argentifolii (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 89, 686–693.CrossRefGoogle Scholar
McAuslane, H.J., Simmons, A.M. & Jackson, D.M. (2000) Parasitism of Bemisia argentifolii on collard with reduced or normal leaf wax. Florida Entomologist 83, 428–437.CrossRefGoogle Scholar
Miklasiewicz, T.J. & Walker, G.P. (1990) Population dynamics and biological control of the woolly whitefly (Homoptera: Aleyrodidae) on citrus. Environmental Entomology 19, 1485–1490.CrossRefGoogle Scholar
Naranjo, S.E. (2007) Intraguild predation on Eretmocerus sp. nr. emiratus, a parasitoid of Bemisia tabaci, by three generalist predators with implications for estimating the level and impact of parasitism. Biocontrol Science and Technology 17, 605–622.CrossRefGoogle Scholar
Naranjo, S.E. (2008) Establishment and impact of exotic Aphelinid parasitoids in Arizona: A life table approach. Journal of Insect Science 8, 36.Google Scholar
Naranjo, S.E. & Ellsworth, P.C. (2005) Mortality dynamics and population regulation in Bemisia tabaci. Entomologia Experimentalis et Applicata 116, 93–108.CrossRefGoogle Scholar
Nguyen, R. & Hamon, A.B. (2008) Biological control of giant whitefly, Aleurodicus dugesii Cockerell, in Florida. Florida Department of Agriculture & Consumer Services, http://www.doacs.state.fl.us/pi/methods/giant-whitefly-bc.html.Google Scholar
Pickett, C.H. & Wall, R. (2003) Biological control of ash whitefly Siphoninus phillyreae (Haliday) (Homoptera: Aleyrodidae) by Encarsia inaron (Walker) (Hymenoptera: Aphelinidae) in Northern California: 1990–2000. Pan-Pacific Entomologist 79, 156–158.Google Scholar
Powell, D.A. & Bellows, T.S. (1992) Development and reproduction of two populations of Eretmocerus species (Hymenoptera: Aphelinidae) on Bemisia tabaci (Homoptera: Aleyrodidae). Environmental Entomology 21, 651–658.CrossRefGoogle Scholar
Qiu, B.L., De Barro, P.J. & Ren, S.X. (2005) Development, survivorship and reproduction of Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on glabrous and non-glabrous host plants. Bulletin of Entomological Research 95, 313–319.CrossRefGoogle ScholarPubMed
Rose, M. & DeBach, P. (1992) Biological control of Parabemisia myricae (Kuwana) (Homoptera: Aleyrodidae) in California. Israel Journal of Entomology 25–26, 73–95.Google Scholar
Rose, M. & Rosen, D. (1992) Eretmocerus debachi n. sp. (Hymenoptera: Aphelinidae), an effective parasite of Parabemisia myricae (Homoptera: Aleyrodidae). Israel Journal of Entomology 25–26, 199–207.Google Scholar
Rose, M. & Woolley, J.B. (1984a). Previously imported parasite may control invading whitefly. California Agriculture 38, 24–25.Google Scholar
Rose, M. & Woolley, J.B. (1984b) Previously imported parasite may control invading whitefly. California Avocado Society Yearbook 68, 127–131.Google Scholar
Schmidt, S., Naumann, I.D. & De Barro, P.J. (2001) Encarsia (Hymenoptera: Aphelinidae) parasitoids of Bemisia tabaci and Trialeurodes vaporariorum in Australia and the Pacific. Bulletin of Entomological Research 91, 369–387.CrossRefGoogle ScholarPubMed
Sengonca, C. & Liu, B. (1998) Release of Eretmocerus longipes Compere (Hymenoptera: Aphelinidae) against Aleurotuberculatus takahashi David & Subramaniam (Homoptera: Aleyrodidae) on jasmine plantations in the Fuzhou region of southeastern China. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 105, 504–512.Google Scholar
Sengonca, C., Uygun, N., Kersting, U. & Ulusoy, M.R. (1993) Successful colonization of Eretmocerus debachi (Hym.: Aphelinidae) in the Eastern Mediterranean Citrus region of Turkey. Entomophaga 38, 383–390.CrossRefGoogle Scholar
Sengonca, C., Uygun, N., Kersting, U. & Ulusoy, M.R. (1995) Effectiveness of Eretmocerus debachi Rose and Rosen (Hym., Aphelinidae) in controlling the whitefly Parabemisia myricae (Kuwana) (Hom., Aleyrodidae). Anzeiger für Schadlingskunde, Pflanzenschutz, Umweltschutz 68, 123–127.CrossRefGoogle Scholar
Tentelier, C., Wajnberg, E. & Fauvergue, X. (2005) Parasitoids use herbivore-induced information to adapt patch exploitation behaviour. Ecological Entomology 30, 739–744.CrossRefGoogle Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Vail, P.V., Coulson, J.R., Kauffman, W.C. & Dix, M.E. (2001) History of biological control programs in the United States Department of Agriculture. American Entomologist 47, 24–50.CrossRefGoogle Scholar
Van den Berg, M.A., & Greenland, J. (2001) Pest status of two blackfly species on citrus in South Africa and Swaziland. African Plant Protection 7, 53–57.Google Scholar
Van den Berg, M.A., Hoppner, G. & Greenland, J. (2000) An economic study of the biological control of the spiny blackfly, Aleurocanthus spiniferus (Hemiptera: Aleyrodidae), in a citrus orchard in Swaziland. Biocontrol Science and Technology 10, 27–32.CrossRefGoogle Scholar
Vos, M. & Hemerik, L. (2003) Linking foraging behavior to lifetime reproductive success for an insect parasitoid: adaptation to host distributions. Behavioral Ecology 14, 236–245.CrossRefGoogle Scholar
Waage, J.K. (1979) Foraging for patchily distributed hosts by the parasitoid Nemeritis canescens. Journal of Animal Ecology 48, 353–371.CrossRefGoogle Scholar
Wang, X.G. & Keller, M.A. (2004) Patch time allocation by the parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). III. Effects of kairomone sources and previous parasitism. Journal of Insect Behavior 17, 761–776.CrossRefGoogle Scholar
Waterhouse, D. & Norris, K. (1989). Aleurodicus dispersus Russell. pp 12–22in Waterhouse, D. & Norris, K. (Eds) Biological Control Pacific Prospects, Supplement 1. Canberra, ACIAR.Google Scholar
White, G.L., Kairo, M.T.K. & Lopez, V. (2005) Classical Biological Control of the Citrus Blackfly Aleurocanthus woglumi by Amitus hesperidum in Trinidad. BioControl 50, 751–759.CrossRefGoogle Scholar
Zolnerowich, G. & Rose, M. (1998) Eretmocerus Haldeman (Hymenoptera: Aphelinidae) imported and released in the United States for control of Bemisia (tabaci complex) (Homoptera: Aleyrodidae). Proceedings of the Entomological Society of Washington 100, 310–323.Google Scholar