Dietary experience alters predatory behavior of two ladybird species on tomato potato psyllid

Abstract

The tomato potato psyllid,Bactericera cockerelli, is an invasive pest in Australia, which can cause severe economic loss in the production of Solanaceous crops. As an invasive pest,B. cockerelli may also modify biotic interactions in Australian agricultural and native ecosystems. Resident generalist predators in an area may have the ability to utilize invasive pest species as prey but this will depend on their specific predatory behavior. The extent to which generalist predators learn from their previous dietary experience (i.e., whether they have used a particular species as prey before) and how this impacts subsequent prey choice will influence predator and prey population dynamics after invasion. In this study, one nonnative resident ladybird,Hippodamia variegata, and one native ladybird,Coccinella transversalis, were investigated. Dietary experience with B. cockerelli as a prey species significantly increased preference for the psyllid in a short term (6 h) Petri dish study where a choice of prey was given. Greater suppression of B. cockerelli populations by experienced ladybirds was also observed on glasshouse grown tomato plants. This was presumably due to altered prey recognition by experience. The result of this study suggest the potential to improve the impact of biological control agents on invasive pests by providing early life experience consuming the target species. It may prove valuable for developing improved augmentative release strategies for ladybirds to manage specific insect pest species.

Keywords

biological control / invasive pest / predator / predator experience / prey preference

References

[1] Ables, J.R.,Jones, S.L. and McCommas Jr, D.W. (1978) Response of selected predator species to different densities of Aphis gossypii and Heliothis virescens eggs. Environmental Entomology,7,402-404.

[2] Ardanuy, A.,Albajes, R. and Turlings, T.C. (2016) Innate and learned prey-searching behavior in a generalist predator. Journal of Chemical Ecology,42,497-507.

[3] Arinaitwe, W.,Guyon, A.,Tungadi, T.D.,Cunniffe, N.J.,Rhee, S.J.,Khalaf, A. et al. (2022) The effects of cucumber mosaic virus and its 2a and 2b proteins on interactions of tomato plants with the aphid vectors Myzus persicae and Macrosiphum euphorbiae. Viruses,14,1703.

[4] Cooper, W.R.,Horton, D.R.,Unruh, T.R. and Garczynski, S.F. (2016) Gut content analysis of a phloem-feeding insect,Bactericera cockerelli (Hemiptera: Triozidae). Environmental Entomology,45,938-944.

[5] Crawley, M.J. and Krebs, J.R. (1992) Foraging theory. In Natural Enemies: The Population Biology of Predators, Parasites and Diseases (ed. M.J. Crawley), pp. 90-114. Blackwell Scientific Publications.

[6] de Castro-Guedes, C.F.,de Almeida, L.M.,do Rocio Chiarello Penteado, S. and Moura, M.O. (2016) Effect of different diets on biology, reproductive variables and life and fertility tables of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae). Revista Brasileira de Entomologia,60,260-266.

[7] Dixon, A.F.G. (2000) Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, UK. pp. 257.

[8] DPIRD (Department for Primary Industries and Regional Development, Australia). (2021) Tomato potato psyllid. https://www.agric.wa.gov.au/tomato-potato-psyllid-tpp

[9] Enkegaard, A.,Brødsgaard, H.F. and Hansen, D.L. (2001) Macrolophus caliginosus: functional response to whiteflies and preference and switching capacity between whiteflies and spider mites. Entomologia Experimentalis et Applicata,101,81-88.

[10] Evans, E.W. (2000) Egg production in response to combined alternative foods by the predator Coccinella transversalis. Entomologia Experimentalis et Applicata,94,141-147.

[11] Ferrer, A.,Dixon, A.F. and Hemptinne, J. (2008) Prey preference of ladybird larvae and its impact on larval mortality, some life-history traits of adults and female fitness. Bulletin of Insectology,61,5.

[12] Franzmann, B.A. (2002) Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae), a predacious ladybird new in Australia. Australian Journal of Entomology,41,375-377.

[13] Hodek, I.,Honek, A. and Van Emden, H.F. (2012) Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). John Wiley & Sons, Blackwell, Chichester, pp. 600.

[14] Houck, M.A. (1991) Time and resource partitioning in Stethorus punctum (Coleoptera: Coccinellidae). Environmental Entomology,20,494-497.

[15] Jaworski, C.C.,Bompard, A.,Genies, L.,Amiens-Desneux, E. and Desneux, N. (2013) Preference and prey switching in a generalist predator attacking local and invasive alien pests. PLoS ONE,8,e82231.

[16] Li, Y.,Ke, Z.,Wang, S.,Smith, G.R. and Liu, X. (2011) An exotic species is the favorite prey of a native enemy. PLoS ONE,6,e24299.

[17] Liefting, L.W.,Sutherland, P.W.,Ward, L.I.,Paice, K.L.,Weir, B.S. and Clover, G.R. (2009) A new ‘Candidatus Liberibacter’ species associated with diseases of solanaceous crops. Plant Disease,93,208-214.

[18] Lima, S.L. and Steury, T.D. (2005) Perception of predation risk: the foundation of nonlethal predator-prey interactions. In Ecology of Predator-Prey Interactions (eds. P. Barbosa & I. Castellanos). Oxford University Press,Oxford, U.K. pp. 166-188.

[19] Lönnstedt, O.M.,McCormick, M.I.,Meekan, M.G.,Ferrari, M.C. and Chivers, D.P. (2012) Learn and live: predator experience and feeding history determines prey behaviour and survival. Proceedings of the Royal Society B: Biological Sciences,279,2091-2098.

[20] Lucas, E.,Coderre, D. and Vincent, C. (1997) Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae. Entomologia Experimentalis et Applicata,85,151-159.

[21] Mills, N.J. (1981) Some aspects of the rate of increase of a coccinellid. Ecological Entomology,6,293-299.

[22] Moir, M. L. (2021) Coextinction of Pseudococcus markharveyi (Hemiptera: Pseudococcidae): a case study in the modern insect extinction crisis. Austral Entomology,60,89-97.

[23] Munyaneza, J.E. (2012) Zebra chip disease of potato: biology, epidemiology, and management. American Journal of Potato Research,89,329-350.

[24] Munyaneza, J.E. (2015) Zebra chip disease,Candidatus Liberibacter, and potato psyllid: a global threat to the potato industry. American Journal of Potato Research,92,230-235.

[25] Niño, A.A. and Cave, R.D. (2023) Prey preference of Chrysoperla rufilabris (Neuroptera: Chrysopidae) between immature stages of Microtheca ochroloma (Coleoptera: Chrysomelidae) and Myzus persicae (Hemiptera: Aphididae). Florida Entomologist,105,275-279.

[26] Obata, S.,Johki, Y. and Hidaka, T. (1986) Location of hibernation sites in the ladybird beetle,Harmonia axyridis. In Ecology of Aphidophaga (ed. I. Hodek), pp. 193-198. Springer Netherlands,The Netherlands.

[27] Obermaier, E.,Heisswolf, A.,Poethke, H. J.,Randlkofer, B. and Meiners, T. (2008) Plant architecture and vegetation structure: two ways for insect herbivores to escape parasitism. European Journal of Entomology,105,233.

[28] Olaniyan, O.,Rodríguez-Gasol, N.,Cayla, N.,Michaud, E. and Wratten, S.D. (2020) Bactericera cockerelli (Šulc), a potential threat to China’s potato industry. Journal of Integrative Agriculture,19,338-349.

[29] Omkar and Pervez, A. (2016) Ladybird beetles. In Ecofriendly Pest Management for Food Security (ed. Omkar), pp. 281-310. Academic Press,San Diego, USA.

[30] Pervez, A.,Omkar and Harsur, M.M. (2020) Coccinellids on crops: nature’s gift for farmers. In Innovative Pest Management Approaches for the 21st Century: Harnessing Automated Unmanned Technologies (ed. A.K. Chakravarty), pp. 429-460. Springer International Publisher,Singapore.

[31] Pugh, A.R.,O’Connell, D.M. and Wratten, S.D. (2015) Further evaluation of the southern ladybird (Cleobora mellyi) as a biological control agent of the invasive tomato-potato psyllid (Bactericera cockerelli). Biological Control,90,157-163.

[32] Qureshi, S.A.,Midmore, D.J.,Syeda, S.S. and Reid, D.J. (2010) A comparison of alternative plant mixes for conservation bio-control by native beneficial arthropods in vegetable cropping systems in Queensland Australia. Bulletin of Entomological Research,100,67-73.

[33] Robertson, B.A. and Blumstein, D.T. (2019) How to disarm an evolutionary trap. Conservation Science and Practice,1,e116.

[34] Rutledge, C.E.,O’Neil, R.J.,Fox, T.B. and Landis, D.A. (2004) Soybean aphid predators and their use in integrated pest management. Annals of the Entomological Society of America,97,240-248.

[35] Sarkar, S.C.,Milroy, S.P. and Xu, W. (2022) Development and reproduction of a native generalist predator,Coccinella transversalis (Coleoptera: Coccinellidae), on the tomato potato psyllid,Bactericera cockerelli, with a greenhouse assay of biocontrol potential. Biological Control,176,105108.

[36] Sarkar, S.C.,Milroy, S.P. and Xu, W. (2023) Potential of variegated lady beetle Hippodamia variegata in management of invasive tomato potato psyllid Bactericera cockerelli. Pest Management Science,79,821-832.

[37] Schausberger, P.,Çekin, D. and Litin, A. (2021) Learned predators enhance biological control via organizational upward and trophic top-down cascades. Journal of Applied Ecology,58,158-166.

[38] Sih, A.,Bolnick, D.I.,Luttbeg, B.,Orrock, J.L.,Peacor, S.D.,Pintor, L.M. et al. (2010) Predator-prey naïveté antipredator behavior, and the ecology of predator invasions. Oikos,119,610-621.

[39] Soares, A.O.,Coderre, D. and Schanderl, H. (2004) Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Animal Ecology,73,478-486.

[40] Stephens, D.W. and Krebs, J.R. (1986) Foraging Theory. Princeton university press, Princeton.

[41] Tavoosi A.F.,Madadi, H. and Behnazar, T. (2014) Effect of wheat cultivars resistance on prey preference of Hippodamia variegata Goeze to Russian wheat aphid,Diuraphis noxia Mordvilko. Agricultural Pest Management,1,23-33.

[42] Tigreros, N.,Agrawal, A.A. and Thaler, J.S. (2021) Genetic variation in parental effects contributes to the evolutionary potential of prey responses to predation risk. The American Naturalist,197,164-175.

[43] Tigreros, N.,Norris, R.H.,Wang, E.H. and Thaler, J.S. (2017) Maternally induced intraclutch cannibalism: an adaptive response to predation risk? Ecology Letters,20,487-494.

[44] Waldbauer, G.P. and Friedman, S. (1991) Self-selection of optimal diets by insects. Annual Review of Entomology,36,43-63.

[45] Waldbauer, G.P.,Cohen, R.W. and Friedman, S. (1984) Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earworm,Heliothis zea (Boddie). Physiological Zoology,57,590-597.

[46] Wen, J. and Ueno, T. (2021) Predator cue-induced plasticity of morphology and behavior in planthoppers facilitate the survival from predation. Scientific Reports,11,16760.

[47] Yadav, T.,Omkar and Mishra, G. (2023) Maternal cannibalistic preferences affect offspring preferences and development in Menochilus sexmaculatus Fabricius (coleoptera: Coccinellidae): a transgenerational investigation. Ethology,129,107-115.

[48] Yang, X.B. and Liu, T.X. (2009) Life history and life tables of Bactericera cockerelli (Homoptera: Psyllidae) on eggplant and bell pepper. Environmental Entomology,38,1661-1667.

[49] Yang, X.B. Zhang, Y.M.,Henne, D.C. and Liu, T.X. (2013) Life tables of Bactericera cockerelli (Hemiptera: Triozidae) on tomato under laboratory and field conditions in southern Texas. Florida Entomologist,96,904-913.

RIGHTS & PERMISSIONS

2024 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.