Generalist Predators Disrupt Biological Control by a Specialist Parasitoid
2001; Wiley; Volume: 82; Issue: 3 Linguagem: Inglês
10.2307/2680190
ISSN1939-9170
AutoresWilliam E. Snyder, Anthony R. Ives,
Tópico(s)Plant and animal studies
ResumoEcologyVolume 82, Issue 3 p. 705-716 Article GENERALIST PREDATORS DISRUPT BIOLOGICAL CONTROL BY A SPECIALIST PARASITOID William E. Snyder, William E. Snyder Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USA Present address: Department of Entomology, Washington State University, Pullman, Washington 99164-6382. E-mail: [email protected]Search for more papers by this authorAnthony R. Ives, Anthony R. Ives Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this author William E. Snyder, William E. Snyder Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USA Present address: Department of Entomology, Washington State University, Pullman, Washington 99164-6382. E-mail: [email protected]Search for more papers by this authorAnthony R. Ives, Anthony R. Ives Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this author First published: 01 March 2001 https://doi.org/10.1890/0012-9658(2001)082[0705:GPDBCB]2.0.CO;2Citations: 234 Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Two broad classes of arthropod natural enemies attack insect herbivores: specialists and generalists. The tight dynamical linkage of specialist natural enemies and their prey may make the specialists able to respond numerically to, and perhaps suppress, herbivore outbreaks. Because generalist predators may attack not only herbivores, but also the herbivores' specialist natural enemies, generalist predators may disrupt control of herbivore populations rather than contribute to it. We examined interactions between pea aphids (Acyrthosiphon pisum), a specialist parasitoid wasp (Aphidius ervi) that attacks the aphids, and a common generalist predator, carabid beetles (primarily Pterostichus melanarius). In two field experiments in alfalfa, we manipulated carabid densities to measure their direct (through predation) and indirect (through intraguild predation on A. ervi) impact on aphid population dynamics. The first experiment was initiated when plants were short (following cutting), and carabid predation of aphids led to an immediate reduction in aphid densities. This reduction was short-lived, however, because carabids reduced parasitism, leading to higher aphid population growth rates. Therefore, although the immediate direct effect of carabids was a reduction in aphid densities, this was offset in the longer term by the indirect effect of carabids disrupting the control of aphids by parasitoids. The second experiment was initiated after plants had regrown following cutting. When plants were tall, carabids had no direct impact on aphid densities. Nonetheless, the slow indirect effect of carabids on aphid densities through reduction in parasitism still occurred, leading to higher aphid population growth rates in the presence of carabids. Additional laboratory experiments demonstrated that carabids are able to climb into plants and prey upon the immobile parasitoid pupae ("mummies"), whereas antipredator behaviors of the aphids protect them from predation by carabids when plants are tall. Overall, carabid predation caused an immediate but ephemeral decrease in aphid density. In contrast, the indirect positive effect on aphid density caused by reducing parasitism developed later but persisted longer. Thus the generalist carabid primarily acted as an intraguild predator, interrupting aphid population control by the specialist parasitoid. Literature Cited Abrams, P. A. 1994. The fallacies of ratio-dependent predation. Ecology 75: 1842–55 1850. 10.2307/1939644 Web of Science®Google Scholar Abramson, W. G., J. F. Sattler, K. D. McCrea, and A. E. Weis . 1989. Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies. Oecologia 79: 15–22. 10.1007/BF00378234 Web of Science®Google Scholar Arditi, R., and H. Saiah . 1992. Empirical evidence of the role of heterogeneity in ratio-dependent consumption. Ecology 73: 1544–1551. 10.2307/1940007 Web of Science®Google Scholar Barney, R. J., and B. C. Pass . 1986. Foraging behavior and feeding preference of ground beetles (Coleoptera: Carabidae) populations in Kentucky alfalfa. Journal of Economic Entomology 79: 1334–1337. 10.1093/jee/79.5.1334 Web of Science®Google Scholar Bender, E. A., T. J. Case, and M. E. Gilpin . 1984. Perturbation experiments in community ecology: what are they and what can be detected? Ecology 65: 1–13. 10.2307/1939452 Web of Science®Google Scholar Berryman, A. A. 1992. The origins and evolution of predator-prey theory. Ecology 73: 1530–1535. 10.2307/1940005 Web of Science®Google Scholar Blackman, R. L., and V. G. Eastop . 1984. Aphids on the world's crops: an identification and information guide. John Wiley & Sons, New York, New York, USA. Google Scholar Brodeur, J., and J. N. McNeil . 1989. Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behavior. Science 244: 226–228. 10.1126/science.244.4901.226 CASPubMedWeb of Science®Google Scholar Brodeur, J., and J. N. McNeil . 1992. Host behavior modification by the endoparasitoid Aphidius nigripes: a strategy to reduce hyperparasitism. Ecological Entomology 17: 97–104. 10.1111/j.1365-2311.1992.tb01164.x Web of Science®Google Scholar Brodeur, J., and L. E. M. Vet . 1994. Usurpation of host behavior by a parasitic wasp. Animal Behavior 48: 187–192. 10.1006/anbe.1994.1225 Web of Science®Google Scholar Brown, J. H., D. W. Davidson, J. C. Munger, and R. S. Inouye . 1986. Experimental community ecology: the desert granivore system. Pages 41–61 in J. Diamond and T. J. Case, editors. Community Ecology. Harper and Row, New York, New York, USA. Google Scholar Chang, G. C. 1996. Comparison of single versus multiple species of generalist predators for biological control. Environmental Entomology 25: 207–212. 10.1093/ee/25.1.207 Web of Science®Google Scholar Chang, G. C., and P. Kareiva . 1999. The case for indigenous generalists in biological control. Pages 103–115 in B. A. Hawkins and H. V. Cornell, editors. Theoretical approaches to biological control. Cambridge University Press, New York, New York, USA. Google Scholar Debach, P., and D. Rosen . 1991. Biological control by natural enemies. Cambridge University Press, New York, New York, USA. Google Scholar Dungan, M. L. 1986. Three-way interactions: Barnacles, limpets and algae in a Sonoran desert rocky intertidal zone. American Naturalist 127: 292–316. 10.1086/284486 Web of Science®Google Scholar Edwards, C. A., K. D. Sunderland, and K. S. George . 1979. Studies on polyphagous predators of cereal aphids. Journal of Applied Ecology 16: 811–823. 10.2307/2402855 Web of Science®Google Scholar Ekbom, B. 1994. Arthropod predators of the pea aphid, Acyrthosiphon pisum Harr. (Hom., Aphididae) in peas (Pisum sativum L.), clover (Trifolium pratense L.) and alfalfa (Medicago sativa L.). Journal of Applied Entomology 117: 469–476. 10.1111/j.1439-0418.1994.tb00764.x Web of Science®Google Scholar Evans, E. W., and S. England . 1996. Indirect interactions in biological control of insects: pests and natural enemies in alfalfa. Ecological Applications 6: 920–930. 10.2307/2269495 Web of Science®Google Scholar Ferguson, K. I., and P. Stiling . 1996. Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108: 375–379. 10.1007/BF00334664 PubMedWeb of Science®Google Scholar Gonzalez, D., W. White, J. Hall, and R. C. Dickson . 1978. Geographical distribution of Aphiidae (Hym.) imported to California for biological control of Acyrthosiphon kondoi and Acyrthosiphon pisum (Hom.: Aphididae). Entomophaga 23: 239–248. 10.1007/BF02373098 Web of Science®Google Scholar Hagley, E. A. C., N. J. Holliday, and D. R. Barber . 1982. Laboratory studies of the food preferences of some orchard carabids (Coleoptera: Carabidae). Canadian Entomologist 114: 431–437. 10.4039/Ent114431-5 Web of Science®Google Scholar Hamon, N., R. Bardner, L. Allen-Williams, and J. B. Lee . 1990. Carabid populations in field beans and their effect on the population dynamics of Sitona lineatus (L.). Annals of Applied Biology 117: 51–62. 10.1111/j.1744-7348.1990.tb04194.x Web of Science®Google Scholar Harizanova, V., and B. Ekbom . 1997. An evaluation of the parasitoid, Aphidius colemani Viereck (Hymenoptera: Braconidae) and the predator Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae) for biological control of Aphis gossypii Glover (Homoptera: Aphididae) on cucumber. Journal of Entomological Science 32: 17–24. 10.18474/0749-8004-32.1.17 Web of Science®Google Scholar Harper, A. M., and M. S. Kaldy . 1982. Effect of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae), on yield and quality of forage alfalfa. Canadian Entomologist 114: 485–489. 10.4039/Ent114485-6 Web of Science®Google Scholar Harvey, T. L., H. L. Hackerott, and E. L. Sorensen . 1972. Pea aphid resistant alfalfa selected in the field. Journal of Economic Entomology 65: 1661–1663. 10.1093/jee/65.6.1661 Web of Science®Google Scholar Hassell, M. P. 1980. Foraging strategies, population models and biological control: a case study. Journal of Animal Ecology 49: 603–628. 10.2307/4267 Web of Science®Google Scholar Hassell, M. P., and R. M. May . 1986. Generalist and specialist natural enemies in insect predator–prey interactions. Journal of Animal Ecology 55: 923–940. 10.2307/4425 Web of Science®Google Scholar Helenius, J. 1990. Effect of epigeal predators on infestation by the aphid Rhopalosiphum padi and on grain yield of oats in monocrops and mixed intercrops. Entomologia Experimentalis et Applicata 54: 225–236. 10.1111/j.1570-7458.1990.tb01333.x Web of Science®Google Scholar Hoelmer, K. A., L. S. Osborne, and R. K. Yokomi . 1994. Interactions of the whitefly predator Delphastus pusillus (Coleoptera: Coccinellidae) with parasitized sweetpotato whitefly (Homoptera: Aleyrodidae). Environmental Entomology 23: 136–139. 10.1093/ee/23.1.136 Web of Science®Google Scholar Holland, J. M., and S. Smith . 1999. Sampling epigeal arthropods: an evaluation of fenced pitfall traps using mark–release–recapture and comparisons to unfenced pitfall traps in arable crops. Entomologia Experimentalis et Applicata 91: 347–357. 10.1046/j.1570-7458.1999.00501.x Web of Science®Google Scholar Hutchinson, W. D., and D. B. Hogg . 1984. Demographic statistics for the pea aphid (Homoptera: Aphididae) in Wisconsin and a comparison with other populations. Environmental Entomology 13: 1173–1181. 10.1093/ee/13.5.1173 Google Scholar Hutchinson, W. D., and D. B. Hogg . 1985. Time-specific life tables for the pea aphid, Acyrthosiphon pisum (Harris), on alfalfa. Researches on Population Ecology 27: 231–253. 10.1007/BF02515463 Web of Science®Google Scholar Ives, A. R., K. Gross, and V. A. A. Jansen . 2000. Periodic mortality events in predator-prey systems. Ecology 81: 3330–3340. 10.1890/0012-9658(2000)081[3330:PMEIPP]2.0.CO;2 Web of Science®Google Scholar Ives, A. R., S. S. Schooler, V. J. Jagar, S. E. Knuteson, M. Grbic, and W. H. Settle . 1999. Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. American Naturalist 154: 652–673. 10.1086/303269 PubMedWeb of Science®Google Scholar Jones, R. E. 1987. Ants, parasitoids, and the cabbage butterfly Pieris rapae. Journal of Animal Ecology 56: 739–749. 10.2307/4945 PubMedGoogle Scholar Kindlmann, P., and Z. Ruzicka . 1992. Possible consequences of a specific interaction between predators and parasites of aphids. Ecological Modelling 61: 253–265. 10.1016/0304-3800(92)90021-6 Web of Science®Google Scholar Losey, J. E., and R. F. Denno . 1998a.. The escape response of pea aphids to foliar-feeding predators: factors affecting dropping behavior. Ecological Entomology 23: 53–61. 10.1046/j.1365-2311.1998.00102.x Web of Science®Google Scholar Losey, J. E., and R. F. Denno . 1998b.. Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators. Oecologia 115: 245–252. 10.1007/s004420050513 PubMedWeb of Science®Google Scholar Losey, J. E., and R. F. Denno . 1998c.. Positive predator–predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79: 2143–2152. 10.1890/0012-9658(1998)079[2143:PPPIEP]2.0.CO;2 Web of Science®Google Scholar Lovei, G. L., and K. D. Sunderland . 1996. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41: 231–256. 10.1146/annurev.en.41.010196.001311 CASPubMedWeb of Science®Google Scholar Lucas, E., D. Coderre, and J. Brodeur . 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79: 1084–1092. 10.1890/0012-9658(1998)079[1084:IPAAPC]2.0.CO;2 Web of Science®Google Scholar Maiteki, G. A., and R. J. Lamb . 1985. Spray timing and economic threshold for the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae), on field peas in Manitoba. Journal of Economic Entomology 78: 1449–1454. 10.1093/jee/78.6.1449 Web of Science®Google Scholar McAllister, M. K., and B. D. Roitberg . 1987. Adaptive suicidal behavior in pea aphids. Nature 328: 797–799. 10.1038/328797b0 PubMedGoogle Scholar McAllister, M. K., B. D. Roitberg, and K. L. Weldon . 1990. Adaptive suicide in pea aphids: decisions are cost sensitive. Animal Behavior 40: 167–175. 10.1016/S0003-3472(05)80676-1 Web of Science®Google Scholar Menge, B. A. 1997. Detection of direct versus indirect effects: were experiments long enough? American Naturalist 149: 801–823. 10.1086/286025 CASPubMedWeb of Science®Google Scholar Müller, C. B., and H. C. J. Godfray . 1997. Apparent competition between two aphid species. Journal of Animal Ecology 66: 57–64. 10.2307/5964 Web of Science®Google Scholar Murdoch, W. W. 1994. Population regulation in theory and practice. Ecology 75: 271–287. 10.2307/1939533 Web of Science®Google Scholar Murdoch, W. W., J. Chesson, and P. L. Chesson . 1985. Biological control in theory and practice. American Naturalist 125: 344–366. 10.1086/284347 Web of Science®Google Scholar Niemela, J., J. R. Spence, and H. Carcamo . 1997. Establishment and interactions in carabid populations: an experiment with native and introduced species. Ecography 20: 643–652. 10.1111/j.1600-0587.1997.tb00433.x Web of Science®Google Scholar Ovaska, K., and M. A. Smith . 1987. Predatory behavior of two species of ground beetles (Coleoptera: Carabidae) towards juvenile salamanders (Plethodon vehiculum). Canadian Journal of Zoology 66: 599–604. 10.1139/z88-089 Web of Science®Google Scholar Polis, G. A. 1991. Complex trophic interactions in deserts: an empirical critique of food-web theory. American Naturalist 138: 123–136. 10.1086/285208 Web of Science®Google Scholar Polis, G. A., and R. D. Holt . 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends in Ecology and Evolution 7: 151–154. 10.1016/0169-5347(92)90208-S CASPubMedWeb of Science®Google Scholar Polis, G. A., C. A. Myers, and R. D. Holt . 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology and Systematics 20: 297–330. 10.1146/annurev.es.20.110189.001501 Google Scholar Polis, G. A., and D. R. Strong . 1996. Food web complexity and community dynamics. American Naturalist 147: 813–846. 10.1086/285880 Web of Science®Google Scholar Press, J. W., B. R. Flaherty, and R. T. Arbogast . 1974. Interactions among Plodia interpunctella, Bracon hebetor, and Xylocoris flavipes. Environmental Entomology 3: 183–184. 10.1093/ee/3.1.183 Web of Science®Google Scholar Rauwald, K. S., and A. R. Ives . 2001. Biological control in disturbed agricultural systems and the rapid re-establishment of parasitoids. Ecological Applications 11: in press. 10.1890/1051-0761(2001)011[1224:BCIDAS]2.0.CO;2 Web of Science®Google Scholar Rees, N. E., and J. A. Onsager . 1982. Influence of predators on the efficiency of the Blaesoxipha spp. Parasites of the migratory grasshopper. Environmental Entomology 11: 426–428. 10.1093/ee/11.2.426 Web of Science®Google Scholar Rees, N. E., and J. A. Onsager . 1985. Parasitism and survival among rangeland grasshoppers in response to suppression of robber fly (Diptera: Asilidae) predators. Environmental Entomology 14: 20–23. 10.1093/ee/14.1.20 Web of Science®Google Scholar Riechert, S. E., and L. Bishop . 1990. Prey control by an assemblage of generalist predators: spiders in garden test systems. Ecology 71: 1441–1450. 10.2307/1938281 Web of Science®Google Scholar Riechert, S. E., and T. Lockley . 1984. Spiders as biological control agents. Annual Review of Entomology 29: 299–320. 10.1146/annurev.en.29.010184.001503 Web of Science®Google Scholar Roland, J. 1988. Decline in winter moth populations in North America: direct versus indirect effect of introduced parasites. Journal of Animal Ecology 57: 523–531. 10.2307/4922 Web of Science®Google Scholar Roland, J. 1995. Biological control of the winter moth. Annual Review of Entomology 40: 475–492. 10.1146/annurev.en.40.010195.002355 CASWeb of Science®Google Scholar Rosenheim, J. A. 1998. Higher-order predators and the regulation of insect herbivore populations. Annual Review of Entomology 43: 421–447. 10.1146/annurev.ento.43.1.421 CASPubMedWeb of Science®Google Scholar Rosenheim, J. A., H. K. Kaya, L. E. Ehler, J. J. Marois, and B. A. Jaffee . 1995. Intraguild predation among biological-control agents: theory and practice. Biological Control 5: 303–335. 10.1006/bcon.1995.1038 Web of Science®Google Scholar Rosenheim, J. A., L. R. Wilhoit, and C. A. Armer . 1993. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96: 439–449. 10.1007/BF00317517 PubMedWeb of Science®Google Scholar Schoener, T. W. 1993. On the relative importance of direct versus indirect effects in ecological communities. Pages 365–411 in H. Kawanabe, J. E. Cohen, and K. Iwasaki, editors. Mutualism and community organization: behavioral, theoretical, and food-web approaches. Oxford University Press, New York, New York, USA. Google Scholar Sih, A., P. Crowley, M. McPeek, J. Petranka, and K. Strohmeier . 1985. Predation, competition and prey communities: a review of field experiments. Annual Review of Ecology and Systematics 16: 269–311. 10.1146/annurev.es.16.110185.001413 Web of Science®Google Scholar Sih, A., G. England, and D. Wooster . 1998. Emergent impacts of multiple predators on multiple prey. Trends in Ecology and Evolution 13: 350–355. 10.1016/S0169-5347(98)01437-2 CASPubMedWeb of Science®Google Scholar Snyder, W. E. 1999. Intraguild predation and the biocontrol effectiveness of generalist predators. Dissertation. University of Kentucky, Lexington, Kentucky, USA. Google Scholar Snyder, W. E., and A. R. Ives . 2001. Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82. 10.1890/0012-9658(2001)082[0705:GPDBCB]2.0.CO;2 PubMedWeb of Science®Google Scholar Snyder, W. E., and D. H. Wise . 1999. Predator interference and the establishment of generalist predator populations for biocontrol. Biological Control 15: 283–292. 10.1006/bcon.1999.0723 Web of Science®Google Scholar Snyder, W. E., and D. H. Wise . 2001 Contrasting trophic cascades generated by a community of generalist predators. Ecology, in press.. Google Scholar Soroka, J. J., and P. A. MacKay . 1990. Seasonal occurrence of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), on cultivars of field peas in Manitoba and its effects on pea growth and yield. Canadian Entomologist 122: 503–513. 10.4039/Ent122503-5 Web of Science®Google Scholar Stark, S. B., and K. R. Hopper . 1988. Chrysoperla carnea predation on Heliothis virescens larvae parasitized by Microplitis croceipes. Entomologia Experimentalis et Applicata 48: 69–72. 10.1111/j.1570-7458.1988.tb02300.x Web of Science®Google Scholar Strong, D. R. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73: 747–754. 10.2307/1940154 Web of Science®Google Scholar Symondson, W. O. C., D. M. Glen, C. W. Wiltshire, C. J. Langdon, and J. E. Liddell . 1996. Effects of cultivation techniques and methods of straw disposal on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda: Pulmonata) in an arable land. Journal of Applied Ecology 33: 741–753. 10.2307/2404945 Web of Science®Google Scholar Taylor, A. J., C. B. Muller, and H. C. J. Godfray . 1998. Effect of aphid predators on oviposition behavior of aphid parasitoids. Journal of Insect Behavior 11: 297–302. 10.1023/A:1021056226037 Web of Science®Google Scholar Thiboldeaux, R. 1986. The effect of temperature on population level interactions between the pea aphid, Acyrthosiphon pisum, and its primary parasitoid, Aphidius ervi. Thesis. University of Wisconsin, Madison, Wisconsin, USA. Google Scholar Thiele, H. U. 1977. Carabid beetles in their environments. Springer-Verlag, Berlin, Germany. Google Scholar Tostowaryk, W. 1971. Relationship between parasitism and predation of diprionid sawflies. Annals of the Entomological Society of America 64: 1424–1427. 10.1093/aesa/64.6.1424 Web of Science®Google Scholar Turchin, P., A. D. Taylor, and J. D. Reeve . 1999. Dynamical role of predators in population cycles of a forest insect: an experimental test. Science 285: 1068–1071. 10.1126/science.285.5430.1068 CASPubMedWeb of Science®Google Scholar Völkl, W. 1992. Aphids or their parasitoids: Who actually benefits from ant-attendance? Journal of Animal Ecology 61: 273–281. 10.2307/5320 Web of Science®Google Scholar Wooton, J. T. 1994. Putting the pieces together: testing the independence of interactions among organisms. Ecology 75: 1544–1551. 10.2307/1939615 Web of Science®Google Scholar Citing Literature Volume82, Issue3March 2001Pages 705-716 ReferencesRelatedInformation
Referência(s)