Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-26T14:16:21.865Z Has data issue: false hasContentIssue false

The functional response and prey preference of generalist Nabis (Hemiptera: Nabidae) predators to leafhopper prey (Hemiptera: Cicadellidae)

Published online by Cambridge University Press:  16 January 2018

David J. Stasek*
Affiliation:
Department of Biology, Miami University, Oxford, Ohio, 45056, United States of America
James N. Radl
Affiliation:
Department of Biology, Miami University, Oxford, Ohio, 45056, United States of America
Thomas O. Crist
Affiliation:
Department of Biology, Miami University, Oxford, Ohio, 45056, United States of America
*
3Corresponding author (e-mail: dstasek@ccga.edu)

Abstract

Insects of the family Nabidae (Hemiptera) are generalist predators commonly found in agroecosystems, but little is known about their predation rates on common pests of forage crops. We determined the functional response and prey preference of Nabis Latreille species to two common leafhopper pests of red clover (Trifolium pratense Linnaeus; Fabaceae): Agallia constricta Van Duzee (Hemiptera: Cicadellidae) and Ceratagallia agricola (Hamilton) (Hemiptera: Cicadellidae). We also determined the survivorship of A. constricta to predation by Nabis species over the course of five days. The Nabis species displayed a Type III functional response to both leafhopper species with a preference for A. constricta. The 10-A. constricta/cage treatments and 20-A. constricta/cage treatments had the highest survival probabilities after five days with survival probabilities of 0.19 and 0.23, respectively. These results indicate that Nabis species may help in controlling leafhopper populations in forage-crop systems.

Type
Behaviour & Ecology
Copyright
© Entomological Society of Canada 2018 

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

1

Present address: Department of Natural Sciences, College of Coastal Georgia, Brunswick, Georgia, 31520, United States of America

2

Present address: Department of Entomology, The Ohio State University, Columbus, Ohio, 43221, United States of America

Subject editor: Kevin Floate

References

Anderson, M. and Erlinge, S. 1977. Influence of predation on rodent populations. Oikos, 29: 591597.Google Scholar
Angioni, A., Dedola, F., Minelli, E.V., Barra, A., Cabras, P., and Caboni, P. 2005. Residues and half-life times of pyrethrins on peaches after field treatments. Journal of Agricultural and Food Chemistry, 53: 40594063.CrossRefGoogle ScholarPubMed
Antonious, G.F. 2004. Residues and half-lives of pyrethrins on field-grown pepper and tomato. Journal of Environmental Science and Health, B39, 4: 491503.CrossRefGoogle Scholar
Arthur, S.M., Manly, B.J.F., McDonald, L.L., and Garner, G.W. 1996. Assessing habitat selection when availability changes. Ecology, 77: 215227.CrossRefGoogle Scholar
Bilde, T. and Toft, S. 1994. Prey preference and egg production of the carabid beetle Agonum dorsale . Entomologia Experimentalis et Applicata, 15: 5156.Google Scholar
Black, L.M. 1936. Some insect and host relationships of the potato yellow dwarf virus. Phytopathology, 26: 87.Google Scholar
Black, L.M. 1944. Some viruses transmitted by agallian leafhoppers. Proceedings of the American Philosophical Society, 88: 132144.Google Scholar
Braman, S.K. and Yeargan, K.V. 1989. Intraplant distribution of three Nabis species (Hemiptera: Nabidae), and impact of N. roseipennis on green cloverworm populations in soybean. Environmental Entomology, 18: 240244.Google Scholar
Braman, S.K. and Yeargan, K.V. 1990. Phenology and abundance of Nabis americoferus, N. roseipennis, and N. rufusculus (Hemiptera: Nabidae) and their parasitoids in alfalfa and soybean. Journal of Economic Entomology, 83: 823830.CrossRefGoogle Scholar
Burnham, K.P. and Anderson, D.R. 2002. Model selection and multimodel inference: a practical information-theoretic approach, 2nd edition. Springer-Verlag, New York, New York, United States of America.Google Scholar
Butler, C.D. and O’Neil, R.J. 2008. Voracity and prey preference of insidious flower bug (Hemiptera: Anthocoridae) for immature stages of soybean aphid (Hemiptera: Aphididae) and soybean thrips (Thysanoptera: Thripidae). Environmental Entomology, 37: 964972.CrossRefGoogle ScholarPubMed
Cardinale, B.J., Harvey, C.T., Gross, K., and Ives, A.R. 2003. Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecology Letters, 6: 857865.Google Scholar
Chapman, R.F. 1971. The insects structure and function. American Elsevier, New York, New York, United States of America.Google Scholar
Chesson, J. 1983. The estimation and analysis of preference and its relationship to foraging models. Ecology, 64: 12971304.Google Scholar
Cohen, A.C. 2000. How carnivorous bugs feed. In Heteroptera of economic importance. Edited by C.W. Schaefer and A.R. Panizzi. CRC Press, New York, New York, United States of America. Pp. 563570.Google Scholar
Conover, R.J. 1966. Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous feeding. Limnology and Oceanography, 11: 346354.Google Scholar
Cook, R.M. and Cockrell, B.J. 1978. Predator ingestion rate and its bearing on feeding time and the theory of optimal diets. Journal of Animal Ecology, 47: 529547.CrossRefGoogle Scholar
Crist, T.O. and MacMahon, J.A. 1992. Harvester ant foraging and shrub-steppe seeds: interactions of seed resources and seed use. Ecology, 73: 17681779.CrossRefGoogle Scholar
Debach, P. and Rosen, D. 1991. Biological control by natural enemies. Cambridge University Press, New York, New York, United States of America.Google Scholar
Donahoe, M.C. and Pitre, H.N. 1977. Reduviolus roseipennis behavior and effectiveness in reducing numbers of Heliothis zea on cotton. Environmental Entomology, 6: 872876.Google Scholar
Finke, D.L. and Denno, R.F. 2003. Intra-guild predation relaxes natural enemy impacts on herbivore populations. Ecological Entomology, 28: 6773.Google Scholar
Finke, D.L. and Denno, R.F. 2004. Predator diversity dampens trophic cascades. Nature, 429: 407410.Google Scholar
Finke, D.L. and Denno, R.F. 2005. Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecology Letters, 8: 12991306.Google Scholar
Flinn, P.W., Hower, A.A., and Taylor, R.A.J. 1985. Preference of Reduviolus americoferus (Hemiptera: Nabidae) for potato leafhopper nymphs and pea aphids. The Canadian Entomologist, 117: 15031508.CrossRefGoogle Scholar
Formanowicz, D.R. 1984. Foraging tactics of an aquatic insect: partial consumption of prey. Animal Behaviour, 32: 774781.Google Scholar
Fox, G.A. 2001. Failure-time analysis: emergence, flowering, survivorship, and other waiting times. In Design and analysis of ecological experiments, 2nd edition. Edited by S.M. Scheiner and J. Gurevitch. Oxford University Press, New York, New York, United States of America. Pp. 235266.Google Scholar
Freund, R.L. and Olmstead, K.L. 2000. Role of vision and antennal olfaction in habitat and prey location by three predatory heteropterans. Environmental Entomology, 29: 721732.Google Scholar
Givens, R.P. 1978. Dimorphic foraging strategies of a salticid spider (Phiddipus audax). Ecology, 59: 309321.Google Scholar
Hamilton, K.G.A. 1998. The species of the North American leafhoppers Ceratagallia Kirkaldy and Aceratagallia Kirkaldy (Rhynchota: Homoptera: Cicadellidae). The Canadian Entomologist, 130: 427490.Google Scholar
Hansson, L. and Henttonen, H. 1985. Gradients in density variations of small rodents: the importance of latitude and snow cover. Oecologia, 67: 394402.Google Scholar
Haynes, K.J. and Crist, T.O. 2009. Insect herbivory in an experimental agroecosystem: the roles of habitat area, fragmentation, and the matrix. Oikos, 118: 14771486.CrossRefGoogle Scholar
Holling, C.S. 1959a. The components of predation as revealed by a study of small mammal predation of the European pine sawfly. The Canadian Entomologist, 91: 293320.Google Scholar
Holling, C.S. 1959b. Some characteristics of simple types of predation and parasitism. The Canadian Entomologist, 91: 385398.Google Scholar
Huffaker, C.B. and Messenger, P.S. 1976. Theory and practice of biological control. Academic Press, New York, New York, United States of America.Google Scholar
Irwin, M.E. and Shepard, M. 1980. Sampling predaceous Hemiptera on soybeans. In Sampling methods in soybean entomology. Edited by M. Kogan and D. Herzog. Springer-Verlag, New York, New York, United States of America. Pp. 505531.Google Scholar
Johnson, D.M., Akre, B.G., and Crowley, P.H. 1975. Modeling arthropod predation: wasteful killing by damselfly naiads. Ecology, 56: 10801093.CrossRefGoogle Scholar
Juliano, S.A. 2001. Nonlinear curve fitting: predation and functional response curves. In Design and analysis of ecological experiments, 2nd edition. Edited by S.M. Scheiner and J. Gurevitch. Oxford University Press, New York, New York, United States of America. Pp. 178196.Google Scholar
Kalbfleisch, J.D. and Prentice, R.L. 1980. The statistical analysis of failure time data. Wiley, New York, New York, United States of America.Google Scholar
LaHue, D.W. 1936. An annotated list of the Bythoscopinae of Indiana (Cicadellidae, Homoptera). Proceedings of the Indiana Academy of Science, 45: 310314.Google Scholar
Larsen, K.J., Heady, S.E., and Nault, L.R. 1992. Influence of ants (Hymenoptera: Formicidae) on honeydew excretion and escape behaviors in a Myrmecophile, Dalbulus quinquenotatus (Homoptera: Cicadellidae), and its congeners. Journal of Insect Science, 5: 109122.Google Scholar
Lattin, J.D. 1989. Bionomics of the Nabidae. Annual Review of Entomology, 34: 383400.Google Scholar
Lingren, P.D., Ridgway, R.L., and Jones, S.L. 1968. Consumption by several common arthropod predators of eggs and larvae of two Heliothis species that attack cotton. Annals of the Entomological Society of America, 61: 613618.Google Scholar
Ma, J., Li, Y.Z., Keller, M., and Ren, S.X. 2005. Functional response and predation of Nabis kinbergii (Hemiptera: Nabidae) to Plutella xylostella (Lepidoptera: Plutellidae). Insect Science, 12: 281286.CrossRefGoogle Scholar
Maupin, J.L. and Riechert, S.E. 2001. Superfluous killing in spiders: a consequence of adaptation to food-limited environments? Behavioral Ecology, 12: 569576.Google Scholar
Mayntz, D., Raubenheimer, D., Salomon, M., Toft, S., and Simpson, S.J. 2005. Nutrient-specific foraging in invertebrate predators. Science, 307: 111113.Google Scholar
Meyling, N.V., Enkegaard, A., and Brødsgaard, H. 2003. Two Anthocoris bugs as predators of glasshouse aphids-voracity and prey preference. Entomologia Experimentalis et Applicata, 108: 5970.Google Scholar
Mitchell, W.A. and Brown, J.S. 1990. Density-dependent harvest rates by optimal foragers. Oikos, 57: 180190.Google Scholar
Nadgauda, D. and Pitre, H.N. 1986. Effects of temperature on feeding, development, fecundity, and longevity of Nabis roseipennis (Hemiptera: Nabidae) fed tobacco budworm (Lepidoptera: Noctuidae) larvae and tarnished plant bug (Hemiptera: Miridae) nymphs. Environmental Entomology, 15: 536539.CrossRefGoogle Scholar
Nielson, M.W. 1968. The leafhopper vectors of phytopathogenic viruses (Homoptera, Cicadellidae) taxonomy, biology, and virus transmission. United States Department of Agriculture Technical Bulletin, 1382: 1386.Google Scholar
Östman, Ö and Ives, A.R. 2003. Scale-dependent indirect interactions between two prey species through a shared predator. Oikos, 102: 505514.CrossRefGoogle Scholar
Pollard, S.D. 1989. Constraints affecting partial prey consumption by a crab spider, Diea sp. indet. (Araneae, Thomisidae). Oecologia, 81: 392396.Google Scholar
Propp, G.D. 1982. Functional response of Nabis americoferus to two of its prey, Spodoptera exigua and Lygus hesperus . Environmental Entomology, 11: 670674.Google Scholar
R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from www.R-project.org [accessed 8 December 2017].Google Scholar
Rogers, D.J. 1972. Random search and insect population models. Journal of Animal Ecology, 41: 369383.Google Scholar
Rosenheim, J.A., Wilhoit, L.R., and Armer, C.A. 1993. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia, 96: 439449.CrossRefGoogle ScholarPubMed
SAS Institute. 2003. SAS for Windows, release 9.1. SAS Institute, Cary, North Carolina, United States of America.Google Scholar
Schoener, T.W. 1971. Theory of feeding strategies. Annual Review of Ecology and Systematics, 2: 369404.Google Scholar
Schotzko, D.J. and O’Keeffe, L.E. 1989. Comparison of sweep net, d-vac, and absolute sampling, and diel variation of sweep net sampling estimates in lentils for pea aphid (Homoptera: Aphididae), nabids (Hemiptera: Nabidae), lady beetles (Coleoptera: Coccinellidae), and lacewings (Neuroptera: Chrysopidae). Journal of Economic Entomology, 82: 491506.Google Scholar
Schroeder, B.J. 2007. Effects of landscape structure on generalist and specialist insect herbivores. M.Sc. thesis. Miami University, Oxford, Ohio, United States of America. Available from https://etd.ohiolink.edu/!etd.send_file?accession=miami1196180149&disposition=inline [accessed 8 December 2017].Google Scholar
Snyder, W.E. and Ives, A.R. 2001. Generalist predators disrupt biological control by a specialist parasitoid. Ecology, 82: 705716.Google Scholar
Snyder, W.E. and Ives, A.R. 2003. Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology, 84: 91107.Google Scholar
Snyder, W.E. and Wise, D.H. 2001. Contrasting trophic cascades generated by a community of generalist predators. Ecology, 82: 15711583.Google Scholar
Stasek, D.J. 2009. Population responses of a generalist insect predator and its prey to patch characteristics in forage crops. Ph.D. dissertation. Miami University, Oxford, Ohio, United States of America. Available from https://etd.ohiolink.edu/!etd.send_file?accession=miami1250189697&disposition=inline [accessed 8 December 2017].Google Scholar
Stephens, D.W. and Krebs, J.R. 1986. Foraging theory. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Symondson, W.O.C., Sunderland, K.D., and Greenstone, M.H. 2002. Can generalist predators be effective biocontrol agents? Annual Review of Entomology, 47: 561594.Google Scholar
Trexler, J.C., McCulloch, C.E., and Travis, J. 1988. How can the functional response best be determined? Oecologia, 76: 206214.Google Scholar
Venzon, M., Janssen, A., and Sabelis, M.W. 2002. Prey preference and reproductive success of the generalist predator Orius laevigatus . Oikos, 97: 116124.Google Scholar
Walker, S.E. and Rypstra, A.L. 2001. Sexual dimorphism in functional response and trophic morphology in Rabidosa rabida (Araneae: Lycosidae). American Midland Naturalist, 146: 161170.Google Scholar
Walker, S.E. and Rypstra, A.L. 2002. Sexual dimorphism in trophic morphology and feeding behavior of wolf spiders (Araneae: Lycosidae) as a result of differences in reproductive roles. Canadian Journal of Zoology, 80: 679688.Google Scholar
Watkins, T.C. 1941. Clover leafhopper (Aceratagallia sanguinolenta Prov.). New York Agricultural Experimental Station (Cornell) Bulletin, 758: 324.Google Scholar
Wiedenmann, R.N. and O’Neil, R.J. 1990. Response of Nabis roseipennis (Heteroptera: Nabidae) to larvae of Mexican bean beetle, Epilachna varivestis (Col.: Coccinellidae). Entomophaga, 35: 449458.Google Scholar