Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera?

Biological Control

Volumn 59, Issue 1, 2011, Pages 53-60

  Kaplan, Ian ^a   Thaler, Jennifer S ^b  

^a PURDUE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Food web; Host plant resistance; Omnivory; Plant defense; Strict predators; Tri trophic interactions

Indexed keywords

HETEROPTERA;

EID: 80054683742     PISSN: 10499644     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocontrol.2010.12.005     Document Type: Article

References (73)

1. Agrawal A.A., Kobayashi C., Thaler J.S. Influence of prey availability and induced host-plant resistance on omnivory by western flower thrips. Ecology 1999, 80:518-523.
2. Agrawal A.A., Klein C.N. What omnivores eat: Direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. Journal of Animal Ecology 2000, 69:525-535.
3. Agrawal A.A., Karban R., Colfer R.G. How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 2000, 89:70-80.
4. Alomar O., Wiedenmann R.N. Zoophytopagous Heteroptera: Implications for Life History and Integrated Pest Management 1996, Entomological Society of America, Lanham, MD.
5. Álvarez-Alfageme F., Martinez M., Pascual-Ruiz S., Castanera P., Diaz I., Ortego F. Effects of potato plants expressing a barley cystatin on the predatory bug Podisus maculiventris via herbivorous prey feeding on the plant. Transgenic Research 2007, 16:1-13.
6. Armer C.A., Wiedenmann R.N., Bush D.R. Plant feeding site selection on soybean by the facultatively phytophagous predator Orius insidiosus. Entomologia Experimentalis et Applicata 1998, 86:109-118.
7. Barbour J.D., Farrar R.R., Kennedy G.G. Interaction of Manduca sexta resistance in tomato with insect predators of Helicoverpa zea. Entomologia Experimentalis et Applicata 1993, 68:143-155.
8. Barbour J.D., Farrar R.R., Kennedy G.G. Populations of predaceous natural enemies developing on insect-resistant and susceptible tomato in North Carolina. Biological Control 1997, 9:173-184.
9. Bartlett R. Negative interactions between chemical resistance and predators affect fitness in soybeans. Ecological Entomology 2008, 33:673-678.
10. Bell H.A., Down R.E., Fitches E.C., Edwards J.P., Gatehouse A.M.R. Impact of genetically modified potato expressing plant-derived insect resistance genes on the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae). Biocontrol Science and Technology 2003, 13:729-741.
11. Björkman C., Ahrné K. Influence of leaf trichome density on the efficiency of two polyphagous insect predators. Entomologia Experimentalis et Applicata 2005, 115:179-186.
12. Boethel D.J., Eikenbary R.D. Interactions of Host Plant Resistance and Parasitoids and Predators of Insects 1986, Halsted Press, New York.
13. Bottrell D.G., Barbosa P., Gould F. Manipulating natural enemies by plant variety selection and modification: A realistic strategy?. Annual Review of Entomology 1998, 43:347-367.
14. Bouchard E., Michaud D., Cloutier C. Molecular interactions between an insect predator and its herbivore prey on transgenic potato expressing a cysteine proteinase inhibitor from rice. Molecular Ecology 2003, 12:2429-2437.
15. Braman S.K., Duncan R.R., Hanna W.W., Engelke M.C. Arthropod predator occurrence and performance of Geocoris uliginosus (Say) on pest-resistant and susceptible turfgrasses. Environmental Entomology 2003, 32:907-914.
16. Coll M., Ridgway R.L. Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. Annals of the Entomological Society of America 1995, 88:732-738.
17. Coll M. Feeding and ovipositing on plants by an omnivorous insect predator. Oecologia 1996, 105:214-220.
18. Coll M. Living and feeding on plants in predatory Heteroptera. Predatory Heteroptera: Their Ecology and Use in Biological Control. Proceedings of the Thomas Say Publications in Entomology 1998, 89-130. Entomological Society of America, Lantham. M. Coll, J.R. Ruberson (Eds.).
19. Coll M., Ruberson J.R. Predatory Heteroptera: Their Ecology and Use in Biological Control. Proceedings of the Thomas Say Publications in Entomology 1998, Entomological Society of America, Lantham.
20. Coll M., Guershon M. Omnivory in terrestrial arthropods: Mixing plant and prey diets. Annual Review of Entomology 2002, 47:267-297.
21. Cortesero A.M., Stapel J.O., Lewis W.J. Understanding and manipulating plant attributes to enhance biological control. Biological control 2000, 17:35-49.
22. De Clercq P., Mohaghegh J., Tirry L. Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biological Control 2000, 18:65-70.
23. Desneux N., O'Neil R.J., Yoo H.J.S. Suppression of population growth of the soybean aphid, Aphis glycines matsumura, by predators: The identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environmental Entomology 2006, 35:1342-1349.
24. Eigenbrode S.D., Moodie S., Castagnola T. Predators mediate host plant resistance to a phytophagous pest in cabbage with glossy leaf wax. Entomologia Experimentalis et Applicata 1995, 77:335-342.
25. Eubanks M.D., Denno R.F. The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 1999, 80:1253-1266.
26. Eubanks M.D., Denno R.F. Host plants mediate omnivore-herbivore interactions and influence prey suppression. Ecology 2000, 81:936-947.
27. Eubanks M.D., Styrsky J.D., Denno R.F. The evolution of omnivory in heteropteran insects. Ecology 2003, 84:2549-2556.
28. Eubanks M.D. Predaceous herbivores and herbivorous predators: The biology of omnivores and the ecology of omnivore-prey interactions. Ecology of Predator-Prey Interactions 2005, 3-17. Oxford University Press, Oxford. P. Barbosa, I. Castellanos (Eds.).
29. Eubanks M.D., Styrsky J.D. Effects of plant feeding on the performance of omnivorous " predators" Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications 2005, 148-177. Cambridge University Press, Cambridge. F.L. Wäckers, P.C.J. van Rijn, J. Bruin (Eds.).
30. Gassmann A.J., Hare J.D. Indirect cost of a defensive trait: Variation in trichome type affects the natural enemies of herbivorous insects on Datura wrightii. Oecologia 2005, 144:62-71.
31. Gruenhagen N.M., Perring T.M. Velvetleaf: A plant with adverse impacts on insect natural enemies. Environmental Entomology 1999, 28:884-889.
32. Hare J.D. Effects of plant variation on herbivore-natural enemy interactions. Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics 1992, 278-300. University of Chicago Press, Chicago. R.S. Fritz, E.L. Simms (Eds.).
33. Hare J.D. Plant genetic variation in tritrophic interactions. Multitrophic Level Interactions 2002, 8-43. Cambridge University Press, Cambridge. T. Tscharntke, B.A. Hawkins (Eds.).
34. Härri S.A., Krauss J., Müller C.B. Natural enemies act faster than endophytic fungi in population control of cereal aphids. Journal of Animal Ecology 2008, 77:605-611.
35. Hedges L.V., Gurevitch J., Curtis P.S. The meta-analysis of response ratios in experimental ecology. Ecology 1999, 80:1150-1156.
36. Isenhour D.J., Wiseman B.R., Layton R.C. Enhanced predation by Orius insidiosus (Hemiptera: Anthocoridae) on larvae of Heliothis zea and Spodoptera frugiperda (Lepidoptera: Noctuidae) caused by prey feeding on resistant corn genotypes. Environmental Entomology 1989, 18:418-422.
37. Janssen A., Willemse E., van der Hammen T. Poor host plant quality causes omnivore to consume predator eggs. Journal of Animal Ecology 2003, 72:478-483.
38. Joseph S.V., Braman S.K. Predatory potential of Geocoris spp and Orius insidiosus on fall armyworm in resistant and susceptible turf. Journal of Economic Entomology 2009, 102:1151-1156.
39. Kaplan I., Lynch M.E., Dively G.P., Denno R.F. Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle. Oecologia 2007, 152:665-675.
40. Kaplan I., Thaler J.S. Plant resistance attenuates the consumptive and non-consumptive impacts of predators on prey. Oikos 2010, 119:1105-1113.
41. Kennedy G.G. Tomato, pests, parasitoids, and predators: Tritrophic interactions involving the genus Lycopersicon. Annual Review of Entomology 2003, 48:51-72.
42. Kessler A., Baldwin I.T. Herbivore-induced plant vaccination Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant Journal 2004, 38:639-649.
43. Lou Y.G., Cheng J.A. Role of rice volatiles in the foraging behaviour of the predator Cyrtorhinus lividipennis for the rice brown planthopper Nilaparvata lugens. Biocontrol 2003, 48:73-86.
44. Lovinger A., Liewehr D., Lamp W.O. Glandular trichomes on alfalfa impede searching behavior of the potato leafhopper parasitoid. Biological Control 2000, 18:187-192.
45. Lundgren J.G., Fergen J.K., Riedell W.E. The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Animal Behaviour 2008, 75:1495-1502.
46. Lundgren J.G., Hesler L.S., Tilmon K., Dashiell K., Scott R. Direct effects of soybean varietal selection and Aphis glycines-resistant soybeans on natural enemies. Arthropod-Plant Interactions 2009, 3:9-16.
47. Lundgren J.G. Relationships of Natural Enemies and Non-Prey Foods 2009, Springer Verlag, Dordrecht, The Netherlands.
48. Lykouressis D., Giatropoulos A., Perdikis D., Favas C. Assessing the suitability of noncultivated plants and associated insect prey as food sources for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae). Biological Control 2008, 44:142-148.
49. Magalhaes S., Janssen A., Montserrat M., Sabelis M.W. Host-plant species modifies the diet of an omnivore feeding on three trophic levels. Oikos 2005, 111:47-56.
50. Mahdian K., Tirry L., De Clercq P. Functional response of Picromerus bidens: Effects of host plant. Journal of Applied Entomology 2007, 131:160-164.
51. Mira A., Bernays E.A. Trade-offs in host use by Manduca sexta: Plant characters vs. natural enemies. Oikos 2002, 97:387-397.
52. Mooney, K.A., Singer, M., (in press). Plant mediation of herbivore-enemy interactions in natural systems. In: Ohgushi, T., Schmitz, O.J., Holt, R. (Eds.), Ecology and Evolution of Trait-Mediated Indirect Interactions: Linking Evolution, Community, and Ecosystem. Cambridge University Press.
53. Myint M.M., Rapusas H.R., Heinrichs E.A. Integration of varietal resistance and predation for the management of Nephotettix virescens (Homoptera: Cicadellidae) populations on rice. Crop Protection 1986, 5:259-265.
54. Neto F.D.M., Zanuncio J.C., Picanco M.C., Cruz I. Reproductive characteristics of the predator Podisus nigrispinus fed with an insect resistant soybean variety. Pesquisa Agropecuária Brasileira 2002, 37:917-924.
55. Orr D.B., Boethel D.J. Influence of plant antibiosis through 4 trophic levels. Oecologia 1986, 70:242-249.
56. Perdikis D.C., Lykouressis D.P. Macrolophus pygmaeus (Hemiptera: Miridae) population parameters and biological characteristics when feeding on eggplant and tomato without prey. Journal of Economic Entomology 2004, 97:1291-1298.
57. Perdikis D.C., Lykouressis D.P., Economou L.P. Influence of light-dark phase, host plant, temperature, and their interactions on the predation rate in an insect predator. Environmental Entomology 2004, 33:1137-1144.
58. Pfannenstiel R.S., Yeargan K.V. Partitioning two- and three-trophic-level effects of resistant plants on the predator, Nabis roseipennis. Entomologia Experimentalis et Applicata 1998, 88:203-209.
59. Pimentel D., Wheeler A.G. Influence of alfalfa resistance on a pea aphid population and its associated parasites, predators, and competitors. Environmental Entomology 1973, 2:1-11.
60. Powell J.E., Lambert L. Soybean genotype effects on big-eyed bug feeding on corn earworm in the laboratory. Crop Science 1993, 33:556-559.
61. Price P.W., Bouton C.E., Gross P., McPheron B.A., Thompson J.N., Weis A.E. Interactions among 3 trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 1980, 11:41-65.
62. Rogers D.J., Sullivan M.J. Nymphal performance of Geocoris punctipes (Hemiptera, Lygaeidae) on pest-resistant soybeans. Environmental Entomology 1986, 15:1032-1036.
63. Rogers D.J., Sullivan M.J. Growth of Geocoris punctipes (Hemiptera: Lygaeidae) on attached and detached leaves of pest-resistant soybeans. Journal of Entomological Science 1987, 22:282-285.
64. Romeis J., Meissle M., Bigler F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 2006, 24:63-71.
65. Rosenheim J.A., Wilhoit L.R., Armer C.A. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 1993, 96:439-449.
66. Rosenheim J.A., Goeriz R.E., Thacher E.F. Omnivore or herbivore? Field observations of foraging by Lygus hesperus (Hemiptera: Miridae). Environmental Entomology 2004, 33:1362-1370.
67. Salim M., Heinrichs E.A. Impact of varietal resistance in rice and predation on the mortality of Sogatella furcifera (Horvath) (Homoptera, Delphacidae). Crop Protection 1986, 5:395-399.
68. Sinia A., Roitberg B., McGregor R.R., Gillespie D.R. Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomologia Experimentalis et Applicata 2004, 110:243-248.
69. Styrsky J.D., Kaplan I., Eubanks M.D. Plant trichomes indirectly enhance tritrophic interactions involving a generalist predator, the red imported fire ant. Biological Control 2006, 36:375-384.
70. Verheggen F.J., Capella Q., Schwartzberg E.G., Voigt D., Haubruge E. Tomato-aphid-hoverfly: A tritrophic interaction incompatible for pest management. Arthropod-Plant Interactions 2009, 3:141-149.
71. Wäckers F.L., van Rijn P.C.J., Bruin J. Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications 2005, Cambridge University Press, Cambridge, UK.
72. Weathersbee A.A., Hardee D.D. Abundance of cotton aphids (Homoptera: Aphididae) and associated biological control agents on 6 cotton cultivars. Journal of Economic Entomology 1994, 87:258-265.
73. Zhi J.R., Margolies D.C., Nechols J.R., Boyer J.E. Host-plant-mediated interaction between populations of a true omnivore and its herbivorous prey. Entomologia Experimentalis et Applicata 2006, 121:59-66.