Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-20T05:41:29.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Risks associated with tandem release of large and small ladybirds (Coleoptera: Coccinellidae) in heterospecific aphidophagous guilds

Published online by Cambridge University Press:  23 December 2013

Omkar ,
Geetanjali Mishra ,
Bhupendra Kumar ,
Neha Singh  and
Garima Pandey
Omkar*
Affiliation:
Centre of Excellence in Biocontrol of Insect Pests, Department of Zoology, University of Lucknow, Lucknow 226 007, India
Geetanjali Mishra
Affiliation:
Centre of Excellence in Biocontrol of Insect Pests, Department of Zoology, University of Lucknow, Lucknow 226 007, India
Bhupendra Kumar
Affiliation:
Centre of Excellence in Biocontrol of Insect Pests, Department of Zoology, University of Lucknow, Lucknow 226 007, India
Neha Singh
Affiliation:
Centre of Excellence in Biocontrol of Insect Pests, Department of Zoology, University of Lucknow, Lucknow 226 007, India
Garima Pandey
Affiliation:
Centre of Excellence in Biocontrol of Insect Pests, Department of Zoology, University of Lucknow, Lucknow 226 007, India
*
1 Corresponding author (e-mail: [email protected]).
Get access Rights & Permissions [Opens in a new window]

Abstract

Multiple interactions occurring within aphidophagous guilds determine their final predation outcomes, i.e., antagonistic, additive, or synergistic. Based on these predatory outcomes, the suitability of guilds in suppressing aphid pests is determined. The present study assesses the efficacy of 11 guilds, formed from both larval and adult stages of four locally abundant aphidophagous coccinellids (Coleoptera: Coccinellidae), while exploiting the pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae). The observed antagonistic effects within these guilds are resultants of enhanced predator–predator interactions due to the size and diversity of guild predators. Smaller ladybird predators maintained their usual body mass, probably by increasing their conversion efficiencies to compensate for their reduced prey consumption. However, larger ladybirds reported loss in their body mass, owing to their higher energy needs. The overall guild conversion efficiencies and growth rates were reduced. Among the experimental guilds, the observed prey mortalities were relatively higher in two-predator guilds, and within these two-predator combinations, the higher prey mortalities were recorded in those guilds where Coccinella septempunctata was one of the predators.

Résumé

Les interactions multiples qui se produisent au sein des guildes d'aphidophages déterminent les résultats finaux de la prédation, par ex. antagonistes, additifs ou synergiques. Nous déterminons l'aptitude des guildes à éliminer les pucerons ravageurs d'après ces résultats de la prédation. Notre étude évalue l'efficacité de 11 guildes formées à la fois de stades larvaires et adultes de quatre coccinellidés (Coleoptera: Coccinellidae) aphidophages localement abondants qui exploitent le puceron du pois, Acyrthosiphon pisum Harris (Hemiptera: Aphididae). Les effets antagonistes observés au sein de ces guildes résultent d'interactions plus importantes entre prédateurs reliées à la taille et la diversité des guildes de prédateurs. Les coccinelles prédatrices de plus petite taille maintiennent leur masse corporelle habituelle, probablement en augmentant leurs rendements de conversion afin de compenser leur consommation réduite de proies. Cependant, les coccinelles plus grandes affichent une perte de masse corporelle à cause de leurs besoins énergétiques accrus. Les rendements de conversion globaux et les taux de croissance des guildes sont réduits. Parmi les guildes expérimentales, les mortalités observées chez les proies sont relativement plus élevées dans les guildes à deux prédateurs, et parmi ces guildes à deux prédateurs, les mortalités de proies plus élevées s'observent dans les guildes dont l'un des prédateurs est Coccinella septempunctata.

Type
Insect Management
Information
The Canadian Entomologist , Volume 146 , Issue 1 , February 2014 , pp. 52 - 66
Copyright
Copyright © Entomological Society of Canada 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Gilles Boiteau

References

Agarwala, B.K., Yasuda, H., Kajita, Y. 2003. Effect of conspecific and heterospecific feces on foraging and oviposition of two predatory ladybirds: role of fecal cues in predator avoidance. Journal of Chemical Ecology, 29: 357–376.Google Scholar
Amarasekare, P. 2000. Spatial dynamics in a host-multi parasitoid community. Journal of Animal Ecology, 69: 201–213.CrossRefGoogle Scholar
Armsby, M. Tisch, N. 2006. Intraguild predation and cannibalism in a size-structured community of marine amphipods. Journal of Experimental Marine Biology and Ecology, 333: 286–295.Google Scholar
Chang, G.C. 1996. Comparison of single versus multiple species of generalist predators for biological control. Environmental Entomology, 25: 207–622.CrossRefGoogle Scholar
Charnov, E.L., Orians, G.H., Hyatt, K. 1976. Ecological implications of resource depression. The American Naturalist, 110: 247–259.CrossRefGoogle Scholar
Denno, R.F. Finke, D.L. 2006. Multiple predator interactions and food-web connectance: implications for biological control. In Trophic and guild interactions in biological control. Edited by J. Brodeur and G. Boivin. Springer, Dordrecht, The Netherlands. Pp. 45–70.CrossRefGoogle Scholar
Dixon, A.F.G. 2000. Insect Predator-prey dynamics, ladybird beetles and biological control. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
Dixon, A.F.G. 2007. Body size and resource partitioning in ladybirds. Population Ecology, 49: 45–50.Google Scholar
Dixon, A.F.G. Hemptinne, J.L. 2001. Body size distribution in predatory ladybird beetles reflects that of their prey. Ecology, 82: 1847–1856.Google Scholar
Eubanks, M.D., Blackwell, S.A., Parish, C.J., Delamar, Z.D., HullSanders, H. 2002. Intraguild predation of beneficial arthropods by red imported fire ants in cotton. Environmental Entomology, 31: 1175–1183.Google Scholar
Evans, E.W. 1991. Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oecologia, 87: 401–408.Google Scholar
Evans, E.W. 2004. Habitat displacement of North American ladybirds by an introduced species. Ecology, 85: 637–665.Google Scholar
Eveleigh, E.S. Chant, D.A. 1982. Experimental studies on acarina predator – prey interactions: the effect of predator density on prey consumption, predator searching efficiency, and the functional response to prey density (Acarina: Phytoseiidae). Canadian Journal of Zoology, 60: 611–629.CrossRefGoogle Scholar
Felix, S. Soares, A.O. 2004. Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body mass. European Journal of Entomology, 101: 237–242.CrossRefGoogle Scholar
Ferguson, K.I. Stiling, P. 1996. Non-additive effects of multiple natural enemies on aphid populations. Oecologia, 108: 375–379.Google Scholar
Finlayson, C.J., Alyokhin, A.V., Gross, S., Porter, E.W. 2010. Differential consumption of four aphid species by four lady beetle species. Journal of Insect Science, 10: 1–10.Google Scholar
Gardiner, M.M., O'Neal, M.E., Landis, D.A. 2011. Intraguild predation and native lady beetle decline. PLoS One, 6: 1–9.Google Scholar
Godfray, H.C.J. Waage, J.K. 1991. Predictive modelling in biological control: the mango mealybug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology, 28: 434–453.CrossRefGoogle Scholar
Grez, A.A., Viera, B., Soares, A.O. 2012. Biotic interactions between Eriopis connexa and Hippodamia variegata, a native and an exotic coccinellid species associated with alfalfa fields in Chile. Entomologia Experimentalis et Applicata, 142: 36–44.Google Scholar
Hassell, M.P., Lawton, J.H., Beddington, J.R. 1976. The components of arthropod predation. I. The prey death rate. Journal of Animal Ecology, 45: 135–164.Google Scholar
Hautier, L., Gilles, S.M., Callier, P., de Biseau, J.C., Gregoire, J.C. 2011. Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biological Invasions, 13: 1805–1814.Google Scholar
Hodek, I. Michaud, J.P. 2008. Why is Coccinella septempunctata so successful? European Journal of Entomology, 105: 1–12.Google Scholar
Hodek, I., van Emden, H.F., Honek, A. 2012. Ecology and behavior of the ladybird beetles (Coccinellidae). Wiley-Blackwell Publishing Limited, Oxford, United Kingdom.Google Scholar
Janssen, A., Sabelis, M.W., Magalhaes, S., Montserrat, M., van der Hammen, T. 2007. Habitat structure affects intraguild predation. Ecology, 88: 2713–2719.Google Scholar
Kajita, Y., Takano, F., Yasuda, H., Evans, E.W. 2006. Interactions between introduced and native predatory ladybirds (Coleoptera, Coccinellidae): factors influencing the success of species introductions. Ecological Entomology, 31: 58–67.Google Scholar
Kaplan, I. Eubanks, M.D. 2002. Disruption of cotton aphid (Homoptera: Aphididae) – natural enemy dynamic by red imported fire ants (Hymenoptera: Formicidae). Environmental Entomology, 31: 1175–1183.Google Scholar
Labrie, G., Lucas, E., Coderre, D. 2006. Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biological Invasions, 8: 743–754.Google Scholar
Lawton, J.H. Hassell, M.P. 1981. Asymmetrical competition in insects. Nature, 289: 793–795.Google Scholar
Losey, J.E. Denno, R.F. 1998. Positive predator–predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology, 79: 2143–2152.Google Scholar
Losey, J.E. Denno, R.F. 1999. Factors facilitating synergistic predation: the central role of synchrony. Ecological Applications, 9: 378–386.Google Scholar
Lucas, E., Coderre, D., Brodeur, J. 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology, 79: 1084–1092.Google Scholar
Lucas, E., Labrecque, C., Coderre, D. 2004. Delphastuscatalinae and Coleomegilla maculata lengi (Coleoptera: Coccinellidae) as biological control agents of the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Pest Management Science, 60: 1073–1078.Google Scholar
Magalhães, S., Tudorache, C., Montseratt, M., van Maanen, R., Sabelis, M.W., Janssen, A. 2005. Diet of intraguild predators affects anti-predator behaviour in intraguild prey. Behavioural Ecology, 16: 364–370.Google Scholar
Majerus, M.E.N., Strawson, V., Roy, H. 2006. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecological Entomology, 31: 207–215.Google Scholar
Meszaros, A., Tixier, M.S., Cheval, B., Barbar, Z., Kreiter, S. 2007. Cannibalism and intraguild predation in Typhlodromus exhilaratus and T. phialatus (Acarina: Phytoseiidae) under laboratory conditions. Experimental and Applied Acarology, 41: 37–43.CrossRefGoogle Scholar
Michelakis, S. 1973. A study of the laboratory interaction between Coccinella septempunctata larvae and its prey Myzus persicae. M.Sc. Thesis. University of London, London, Ontario, Canada.Google Scholar
Mills, N. 2006. Interspecific competition among natural enemies and single versus multiple introductions in biological control. In Progress in biological control: trophic and guild interactions in biological control. Edited by J. Brodeur and G. Boivin. Springer, Dordrecht, The Netherlands. Pp. 191–220.CrossRefGoogle Scholar
Mishra, G., Kumar, B., Shahid, M., Singh, D. 2011. Evaluation of four co-occurring ladybirds for use as biocontrol agents of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Biocontrol Science and Technology, 21: 991–997.Google Scholar
Mishra, G., Omkar, Kumar, B., Pandey, G. 2012. Stage and age-specific predation in four aphidophagous ladybird beetles. Biocontrol Science and Technology, 22: 463–476.CrossRefGoogle Scholar
Mochizuki, A., Naka, H., Hamasaki, K., Mitsunaga, T. 2006. Larval cannibalism and intraguild predation between the introduced green lacewing, Chrysoperla carnea, and the indigenous trash carrying green lacewing, Mallada desjardinsi (Neuroptera: Chrysopidae), as a case study of potential non target effect assessment. Environmental Entomology, 35: 1298–1303.Google Scholar
Montserrat, M., Bas, C., Magalhães, S., Sabelis, M.W., de Roos, A.M., Janssen, A. 2007. Predators induce egg retention in prey. Oecologia, 150: 699–705.Google Scholar
Muller, H.C.B. Godfray, H.C.J. 1999. Predators and mutualists influence the exclusion of aphid species from natural communities. Oecologia, 119: 120–125.Google Scholar
Nakashima, Y., Birkett, M.A., Pye, B.J., Powell, W. 2006. Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. Journal of Chemical Ecology, 32: 1989–1998.Google Scholar
Noia, M., Borges, L., Soares, A.O. 2008. Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of intra and extraguild prey densities. Biological Control, 46: 140–146.CrossRefGoogle Scholar
Obrycki, J.J., Giles, K.L., Ormord, A.M. 1998. Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia, 117: 279–285.CrossRefGoogle ScholarPubMed
Omkar, 2004. Reproductive behaviour of two aphidophagous ladybeetles, Cheilomenes sexmaculata and Coccinella transversalis . Entomologia Sinica, 11: 113–124.Google Scholar
Omkar, Mishra, G. 2003. Ovipositional orientation of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Insect Science and its Application, 23: 211–219.Google Scholar
Omkar, Mishra, G., Pervez, A. 2002. Intraguild predation by ladybeetles: an ultimate survival strategy or an aid for advanced aphid biocontrol? In Commemoration. Edited by S.B. Singh. Zoological Society of India, Kolkata, India. Pp. 77–90.Google Scholar
Omkar, Pervez, A. 2002. Ecology of aphidophagous ladybird beetle, Coccinella septempunctata (Coleoptera: Coccinellidae): a review. Journal of Aphidology, 16: 175–201.Google Scholar
Omkar, Pervez, A. 2011. Functional response of two aphidophagous ladybirds searching in tandem. Biocontrol Science and Technology, 21: 101–111.Google Scholar
Omkar, Pervez, A., Mishra, G., Srivastava, S., Singh, S.K., Gupta, A.K. 2005. Intrinsic advantages of Cheilomenes sexmaculata over two coexisting Coccinella species (Coleoptera: Coccinellidae). Insect Science, 12: 179–184.Google Scholar
Pandey, K.P., Kumar, A., Singh, R., Shanker, S., Tripathi, C.P.M. 1984. Numerical response and area of discovery of a predator, Coccinella septempunctata L. Zeitschrift Fur Angewandte Entomologie, 97: 418–423.Google Scholar
Persson, L. 1985. Asymmetrical competition: are larger animals competitively superior? The American Naturalist, 126: 261–266.Google Scholar
Pervez, A. Omkar, A. 2006. Ecology and biological control application of multicolored Asian ladybird, Harmonia axyridis: a review. Biocontrol Science and Technology, 16: 111–128.CrossRefGoogle Scholar
Prasad, R.P. Snyder, W.E. 2004. Predator interference limits fly egg biological control by a guild of ground-active beetles. Biological Control, 31: 428–437.Google Scholar
Ramdev, Y.P. Rao, P.J. 1979. Consumption and utilization of castor by semilooper Achoea janata . Indian Journal of Entomology, 41: 260–266.Google Scholar
Roger, C., Coderre, D., Boivin, G. 2000. Differential prey utilization by the generalist predator Coleomegilla maculata lengi according to prey size and species. Entomologia Experimentalis et Applicata, 94: 3–13.Google Scholar
Rypstra, A.L., Schmidt, J.M., Reif, B.D., DeVito, J., Persons, M.H. 2007. Trade offs involved in site selection and foraging in wolf spider: effects of substrate structure and predation risk. Oikos, 116: 853–863.Google Scholar
Sato, S., Jimbo, R., Yasuda, H., Dixon, A.F.G. 2008. Cost of being an intraguild predator in predatory ladybirds. Applied Entomology and Zoology, 43: 143–147.Google Scholar
Sato, S., Shinya, K., Yasuda, H., Kindlmann, P., Dixon, A.F.G. 2009. Effects of intra and interspecific interactions on the survival of two predatory ladybirds (Coleoptera: Coccinellidae) in relation to prey abundance. Applied Entomology and Zoology, 44: 215–221.Google Scholar
Schuder, I., Hommes, M., Larnik, O. 2004. The influence of temperature and food supply on the development of Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 101: 379–384.Google Scholar
Sih, A., Englund, G., Wooster, D. 1998. Emergent impacts of multiple predators on prey. Trends in Ecology and Evolution, 13: 350–355.Google Scholar
Sloggett, J.J. 2008. Weighty matters: body size, diet and specialization in aphidophagous ladybird beetles (Coleoptera: Coccinellidae). European Journal of Entomology, 105: 381–389.CrossRefGoogle Scholar
Sloggett, J.J., Haynes, K.F., Obrycki, J.J. 2009. Hidden costs to an invasive intraguild predator from chemically defended native prey. Oikos, 118: 1396–1404.CrossRefGoogle Scholar
Snyder, W.E. Ives, A.R. 2001. Generalist predators disrupt biological control by a specialist parasitoid. Ecology, 82: 705–716.Google Scholar
Soluk, D.A. Collins, N.C. 1988. Synergistic interactions between fish and stoneflies: facilitation and interference among stream predators. Oikos, 52: 94–100.Google Scholar
Spiller, D.A. 1986. Interspecific competition between spiders and its relevance to biological control by general predators. Environmental Entomology, 15: 177–181.Google Scholar
Straub, C.S. Snyder, W.E. 2006. Experimental approaches to understanding the relationship between predator biodiversity and biological control. In Progress in biological control: trophic and guild interactions in biological control. Edited by J. Brodeur and G. Boivin. Springer, Dordrecht, The Netherlands. Pp. 221–240.Google Scholar
Waldbauer, G.P. 1968. The consumption and utilization of food by insect. Advances in Insect Physiology, 5: 229–288.CrossRefGoogle Scholar
Ware, R.L. Majerus, M.E.N. 2008. Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis . Biocontrol, 53: 169–188.Google Scholar
Wilder, S.M. Rypstra, A.L. 2004. Chemical cues from an introduced predator (Mantodea, Mantidae) reduce the movement and foraging of a native wolf spider (Araneae, Lycosidae) in the laboratory. Environmental Entomology, 33: 1032–1036.Google Scholar
Wissinger, S. McGrady, J. 1993. Intraguild predation and competition between larval dragonflies: direct and indirect effects on shared prey. Ecology, 74: 207–218.Google Scholar
Zannou, I.D., Hanna, R., Moraes, G.J.D., Kreiter, S. 2005. Cannibalism and interspecific predation in a phytoseiid predator guild from cassava fields in Africa: evidence from the laboratory. Experimental and Applied Acarology, 37: 27–42.Google Scholar