Eur. J. Entomol. 102 (3): 351-364, 2005 | DOI: 10.14411/eje.2005.052

Intraguild predation among aphidophagous predators

Éric LUCAS
Groupe de Recherche en Écologie Comportementale et Animale (GRECA), Département des Sciences Biologiques, Université du Québec L Montréal, C.P. 8888 Succ. Centre-ville, Montréal, Qc, Canada H3C 3P8; e-mail: lucas.eric@uqam.ca

Since the publication of papers by Polis et al. (1989, 1992), intraguild predation (IGP) has been considered in numerous systems and a growing number of papers have been published, demonstrating the ubiquity and the importance of this interaction. It appears that aphidophagous guilds constitute especially favourable systems for IGP. Temporal and spatial distributions of aphids promote interactions, such as IGP, among natural enemies. However, despite extensive laboratory and field studies, several questions remain to be answered: Which traits of the different protagonists of the system may promote or hamper the occurrence of IGP? How do ants tending aphids modulate the interaction? How should one consider the "sub-lethal" effects (and the defensive mechanisms) associated with the risk of IGP? May IGP disrupt or enhance aphid control? These different issues are discussed by focusing on the predatory species in the complex system of aphidophagous guilds. It appears that, first, IGP may constitute one of the main forces influencing the structure and dynamics of aphidophagous guilds, and therefore it has to be taken into account in research studies, and second, because of the ephemeral nature of aphid colonies and the great number of species belonging to aphidophagous guilds, understanding all the implications of the interaction, both direct and indirect, constitutes a very complex task.

Keywords: Intraguild predation, IGP, biological control, predation, aphidophaga, Coccinellidae, interaction

Received: January 6, 2005; Revised: February 28, 2005; Accepted: March 7, 2005; Published: August 15, 2005  Show citation

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LUCAS, É. (2005). Intraguild predation among aphidophagous predators. EJE102(3), 351-364. doi: 10.14411/eje.2005.052
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References

  1. AGARWALA B.K. & DIXON A.F.G. 1992: Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol. Entomol. 17: 303-309 Go to original source...
  2. AGARWALA B.K. & YASUDA H. 2001: Overlaping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids. J. Ethol. 19: 47-53 Go to original source...
  3. AGOIZ-BUSTAMANTE J.L. 2001: Un agresivo comportamiento alimentario de Aphodius (Ammoecius) lusitanicus Erichson, 1848 y nuevos datos sobre su corologia y tropismo (Coleoptera, Scarabaeoidea, Aphodiidae). Bol. Soc. Entomol. Aragon. 29: 79-80
  4. BABENDREIER D., ROSTAS M., HOFTE M.C.J., KUSKE S. & BIGLER F. 2003: Effects of mass releases of Trichogramma brassicae on predatory insects in maize. Entomol. Exp. Appl. 108: 115-124 Go to original source...
  5. BANKS C.J. 1962: Effects of the ant Lasius niger on insects preying on small populations of Aphis fabae on bean plants. Ann. Appl. Biol. 50: 669-679 Go to original source...
  6. BLACKITH R. & BLACKITH R. 1984: Larval aggression in Irish flesh-flies (Diptera: Sarcophagidae). Irish Nat. J. 21: 255-257
  7. BROWN M.W. 2004: Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia, USA. Biol. Control 29: 189-198 Go to original source...
  8. BRISTOW C.M. 1984: Differential benefits from ant attendance to two species of homoptera on New York ironweed. J. Anim. Ecol. 53: 715-726 Go to original source...
  9. BRODEUR J. & BOIVIN G. 2004: Functional ecology of immature parasitoids. Annu. Rev. Entomol. 49: 27-49 Go to original source...
  10. BRODEUR J. & ROSENHEIM J.A. 2000: Intraguild predation in aphid parasitoids. Entomol. Exp. Appl. 97: 93-108 Go to original source...
  11. BUCKLEY R.C. 1987: Interactions involving plants, Homoptera, and ants. Annu. Rev. Ecol. Syst. 8: 111-135 Go to original source...
  12. BURGIO G., SANTI F. & MAINI S. 2002: On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol. Control 24: 110-116 Go to original source...
  13. CHANG G.C. 1996: Comparison of single versus multiple species of generalist predators for biological control. Environ. Entomol. 25: 207-622 Go to original source...
  14. CLANCY K.M. & PRICE P.W. 1987: Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68: 736-738 Go to original source...
  15. CLOUTIER C. & JOHNSON S.G. 1993: Predation by Orius tristicolor (Hemiptera: Anthocoridae) on Phytoseiulus persimilis (Acarina: Phytoseiidae): Testing for compatibility between biocontrol agents. Environ. Entomol. 22: 477-482 Go to original source...
  16. COLFER R.G. & ROSENHEIM J.A. 2001: Predation on immature parasitoids and its influence of aphid population suppression. Oecologia 126: 292-304 Go to original source...
  17. CORBET P.S. & GRIFFITHS A. 1963: Observations on the aquatic stages of two species of Toxorhynchites (Diptera: Culicidae) in Uganda. Proc. R. Entomol. Soc. Lond. (A) 38: 125-135 Go to original source...
  18. COTTRELL T.E. & YEARGAN K.V. 1998: Intraguild predation between an introduced lady beetle Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J. Kans. Entomol. Soc. 71: 159-163
  19. DE CLERCQ P., PETERS I., VERGAUWE G. & THAS O. 2003: Interaction between Podisus maculiventris and Harmonia axyridis, two predators used in augmentative biological control in greenhouse crops. BioControl 48: 39-55 Go to original source...
  20. DIXON A.F.G. 1985: Aphid Ecology. Blackie, Chapman and Hall, New York, USA, 157 pp
  21. DIXON A.F.G. 1987: Parthenogenetic reproduction and the rate of increase in aphids. In Minks A.K. & Harrewijn P. (eds): World Crop Pests; Aphids, their Biology, Natural Enemies and Control. Vol. A. Elsevier, Amsterdam, The Netherlands, pp. 269-287
  22. DIXON A.F.G. 2000: Insect Predator-Prey Dynamic; Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, UK, 257 pp
  23. DOUMBIA M., HEMPTINNE J.-L. & DIXON A.F.G. 1998: Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 113: 197-202 Go to original source...
  24. EDMUNDS M. 1974: Defence in Animals. Longman, New York, USA, 357 pp
  25. EHLER L.E. 1996: Structure and impact of natural enemy guilds in biological control of insect pests. In Polis G.A. & Winemiller K.O. (eds): Food Webs; Integration of Patterns and Dynamics. Chapman & Hall, Toronto, Canada, pp. 337-342. Go to original source...
  26. ENDLER J.A. 1986: Defense against predators. In Feder M.E. & Lauder G.V. (eds): Predator-Prey Relationships: Perspectives and Approaches from the Study of Lower Vertebrates. University of Chicago Press, Chicago, USA, pp. 109-134 Go to original source...
  27. ENDLER J.A. 1991: Interactions between predators and prey. In Krebs J.R. & Davies N.B. (eds): Behavioural Ecology; An Evolutionary Approach. Blackwell Scientific Publications, Oxford, UK, pp. 169-202
  28. ENGLUND G. 1997: Importance of spatial scale and prey movements in predator caging experiments. Ecology 78: 2316-2325 Go to original source...
  29. EUBANKS M.D. 2001: Estimates of the direct and indirect effects of red imported fire ants on biological control in field crops. Biol. Control 21: 35-43 Go to original source...
  30. EUBANKS M.D., BLACKWELL S.A., PARRISH C.J., DELAMAR Z.D. & HULL-SANDERS H. 2002: Intraguild predation of beneficial arthropods by red imported fire ants in cotton. Environ. Entomol. 31: 1168-1174 Go to original source...
  31. EVANS E.W. 2004: Habitat displacement of North American ladybirds by an introduced species. Ecology 85: 637-665 Go to original source...
  32. FELIX S. & SOARES A.O. 2004: Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of bodyweight. Eur. J. Entomol. 101: 237-242 Go to original source...
  33. FERGUSON K.I. & STILING P. 1996: Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108: 375-379 Go to original source...
  34. FLANDERS S.E. 1951: The role of the ant in the biological control of Homopterous insects. Can. Entomol. 83: 93-98 Go to original source...
  35. FRECHETTE B., ALAUZET C. & HEMPTINNE J.-L. 2003: Oviposition behaviour of the two-spot ladybird beetle Adalia bipunctata (L.) (Coleoptera: Coccinellidae) on plants with conspecific larval tracks. Arquipelago, Life Mar. Sci. (Suppl.) 5: 73-77
  36. GODEAU J.-F., HEMPTINNE J.-L. & VERHAEGHE J.C. 2003: Ant trail: a highway for Coccinella magnifica Redtenbacher (Coleoptera: Coccinellidae). Arquipelago, Life Mar. Sci. (Suppl.) 5: 79-83
  37. HAMILTON W.D. 1971: Geometry for the selfish herd. J. Theor. Biol. 31: 295-311 Go to original source...
  38. HANSKI I. 1987: Nutritional ecology of dung- and carrionfeeding insects. In Slansky F. Jr. & J.G. Rodriguez (eds): Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. Wiley, New York, USA, pp. 837-884
  39. HEITHAUS M.R. 2001: Habitat selection by predators and prey in communities with asymmetrical intraguild predation. Oikos 92: 542-554 Go to original source...
  40. HEMPTINNE J.-L., DIXON A.F.G. & GAUTHIER C. 2000a: Nutritive cost of intraguild predation on eggs of Coccinella septempunctata and Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 97: 559-562 Go to original source...
  41. HEMPTINNE J.-L., LOGNAY G., GAUTHIER C. & DIXON A.F.G. 2000b: Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae). Chemoecology 10: 123-128 Go to original source...
  42. HINDAYANA D., MEYHOFER R., SCHOLZ D. & POEHLING H.-M. 2001: Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol. Control 20: 236-246 Go to original source...
  43. HIRONORI Y. & KATSUHIRO S. 1997: Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42: 153-163 Go to original source...
  44. HODEK I. 1996: Food relationships. In Hodek I. & Honek A. (eds): Ecology of Coccinellidae. Kluwer Academic Publishers, Boston, USA, pp. 143-238 Go to original source...
  45. HODGE M.A. 1999: The implications of intraguild predation for the role of spiders in biological control. J. Arachnol. 27: 351-362
  46. HOLT R.D. & POLIS G.A. 1997: A theoretical framework for intraguild predation. Am. Nat. 149: 745-764 Go to original source...
  47. INMAN A.J. & KREBS J. 1987: Predation and group living. Trends Ecol. Evol. 2: 31-32 Go to original source...
  48. JOHANSSON F. 1993: Intraguild predation and cannibalism in odonate larvae: effects of foraging behaviour and zooplankton availability. Oikos 66: 80-87 Go to original source...
  49. KAJITA Y., TAKANO F., YASUDA H. & AGARWALA B.K. 2000: Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl. Entomol. Zool. 35: 473-479 Go to original source...
  50. KANEKO S. 2002: Aphid-attending ants increase the number of emerging adults of the aphid's primary parasitoids and hyperparasitoids by repelling intraguild predators. Entomol. Sci. 5: 131-146
  51. KANEKO S. 2003: Different impacts of two species of aphid attending ants with different aggressiveness on the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids. Ecol. Res. 18: 199-713 Go to original source...
  52. KAPLAN I. & EUBANKS M.D. 2002: Disruption of cotton aphid (Homoptera: Aphididae) - natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ. Entomol. 31: 1175-1183 Go to original source...
  53. KRIVAN V. 2000: Optimal intraguild foraging and population stability. Theor. Popul. Biol. 58: 79-94 Go to original source...
  54. KULLENBERG B. 1944: Studien ueber die Biologie der Capsiden. Zool. Bidrag Fran Uppsala (Suppl.) 23: 1-522
  55. LANG A. 2003: Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia 134: 144-153 Go to original source...
  56. LAURENSEN M.K. 1994: High juvenile mortality in cheetahs (Acinonyx jubatus) and its consequences for mutual care. J. Zool. 234: 387-398 Go to original source...
  57. LIMA S.L. 1998: Nonlethal effects in the ecology of predatorprey interactions: What are the ecological effects of antipredator decision making? Bioscience 48: 25-34 Go to original source...
  58. LIMA S.L. & DILL L.M. 1990: Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 610-640 Go to original source...
  59. LOSEY J.E. & DENNO R.F. 1998: Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79: 2143-2152 Go to original source...
  60. LUCAS E. 1998: How do ladybirds (Coleomegilla maculata lengi, Coleoptera: Coccinellidae) feed on green lacewing eggs (Chrysoperla rufilabris, Neuroptera: Chrysopidae). Can. Entomol. 130: 547-548 Go to original source...
  61. LUCAS E. & ALOMAR O. 2000: Susceptibilite de Macrolophus caliginosus (Heteroptera: Miridae) L la predation intraguilde. IOBC/WPRS Bull. 23: 225-229
  62. LUCAS E. & ALOMAR O. 2001: Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biol. Control. 20: 147-152 Go to original source...
  63. LUCAS E. & ALOMAR O. 2002a: Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits. J. Econ. Entomol. 95: 1123-1126 Go to original source...
  64. LUCAS E. & ALOMAR O. 2002b: Impact of the presence of Dicyphus tamaninii Wagner (Heteroptera: Miridae) on whitefly (Homoptera: Aleyrodidae) predation by Macrolophus caliginosus (Wagner) (Heteroptera: Miridae). Biol. Control. 25: 123-128. Go to original source...
  65. LUCAS E. & BRODEUR J. 1999: Oviposition site selection by Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Environ. Entomol. 28: 622-627 Go to original source...
  66. LUCAS E. & BRODEUR J. 2001: A fox in a sheep-clothing: dilution effect for a furtive predator living inside prey aggregation. Ecology 82: 3246-3250 Go to original source...
  67. LUCAS E., CODERRE D. & BRODEUR J. 1997: Instar-specific defense of Coleomegilla maculata lengi (Coccinellidae): influence on attack success of the intraguild predator Chrysoperla rufilabris (Chrysopidae). Entomophaga 42: 3-12 Go to original source...
  68. LUCAS E., CODERRE D. & BRODEUR J. 1998: Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79: 1084-1092 Go to original source...
  69. LUCAS E., CODERRE D. & BRODEUR J. 2000: Selection of molting and pupating site by Coleomegilla maculata lengi Timberlake (Coleoptera: Coccinellidae): Avoidance of intraguild predation? Environ. Entomol. 29: 454-459 Go to original source...
  70. LUCAS E., GAGNE I. & CODERRE D. 2002: Impact of the arrival of Harmonia axyridis on adults Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur. J. Entomol. 99: 457-463 Go to original source...
  71. MALLAMPALLI N., CASTELLANOS I. & BARBOSA P. 2002: Evidence for intraguild predation by Podisus maculiventris on a ladybeetle, Coleomegilla maculata: Implications for biological control of Colorado potato beetle, Leptinotarsa decemlineata. BioControl 47: 387-398 Go to original source...
  72. MEYHOFER R. 2001: Intraguild predation by aphidophagous predators on parasitized aphids: the use of multiple video cameras. Entomol. Exp. Appl. 100: 77-87 Go to original source...
  73. MICHAUD J.P. 2002: Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ. Entomol. 31: 827-835 Go to original source...
  74. MICHAUD J.P. 2004: Natural mortality of Asian psyllid (Homoptera: Psyllidae) in central Florida. Biol. Control 29: 260-269 Go to original source...
  75. MICHAUD J.P. & GRANT A.K. 2003: Intraguild predation among ladybeetles and a green lacewing: do the larval spines of Curinus coeruleus (Coleoptera: Coccinellidae) serve as a defensive function? Bull. Entomol. Res. 93: 499-505 Go to original source...
  76. MINKS A.K. & HARREWIJN P. (eds) 1988: World Crop Pests; Aphids, their Biology, Natural Enemies and Control. Vol. B. Elsevier, Amsterdam, The Netherlands, 384 pp
  77. MULLER C.B. & BRODEUR J. 2002: Intraguild predation in biological control and conservation biology. Biol. Control 25: 216-223 Go to original source...
  78. MYLIUS S.D., KLUMPERS K., DE ROOS A.M. & PERSSON L. 2001: Impact of intraguild predation and stage structure on simple communities along a productivity gradient. Am. Nat. 158: 259-276 Go to original source...
  79. NIJVELDT W. 1988: Cecidomyiidae. In Minks A.K. & Harrewijn P. (eds): World Crop Pests; Aphids, their Biology, Natural Enemies and Control. Vol. A. Elsevier, Amsterdam, The Netherlands, pp. 271-277
  80. OBRYCKI J.J., GILES K.L. & ORMORD A.M. 1998a: Experimental assessment of interactions between larval Coleomegilla maculata and Coccinella septempunctata (Coleoptera: Coccinellidae) in field cages. Environ. Entomol. 27: 1280-1288 Go to original source...
  81. OBRYCKI J.J., GILES K.L. & ORMORD A.M. 1998b: Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117: 279-285 Go to original source...
  82. OKUYAMA T. 2002: The role of antipredator behavior in an experimental community of jumping spiders with intraguild predation. Popul. Ecol. 44: 121-125 Go to original source...
  83. OKUYAMA T. & RUYLE R.L. 2003: Analysis of adaptive foraging in an intraguild predation system. Web Ecol. 4: 1-6 Go to original source...
  84. OMKAR G.M. & PERVEZ A. 2002: Intraguild predation by ladybeetles: An ultimate survival strategy or an aid for advanced aphid biocontrol? In Prof. S.B. Singh Comm. Vol. Zool. Soc. India, pp. 77-90
  85. OMKAR G.M., PERVEZ A. & GUPTA A.K. 2004: Role of surface chemicals in egg cannibalism and intraguild predation by neonates of two aphidophagous ladybirds, Propylea dissecta and Coccinella transversalis. J. Appl. Entomol. 128: 691-695 Go to original source...
  86. PHOOFOLO M.W. & OBRYCKI J.J. 1998: Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol. Exp. Appl. 89: 47-55 Go to original source...
  87. POLIS G.A. & HOLT R.D. 1992: Intraguild predation: The dynamics of complex trophic interactions. Trends Ecol. Evol. 7: 151-154 Go to original source...
  88. POLIS G.A., MYERS C.A. & HOLT R.D. 1989: The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annu. Rev. Ecol. Syst. 20: 297-330 Go to original source...
  89. PRINCIPI M.M. & CANARD M. 1984: Feeding habits. In Canard M., Semeria Y. & New T.R. (eds): Biology of Chrysopidae. Dr. Junk, The Hague, The Netherlands, pp. 76-92
  90. PROVOST C., CODERRE D., LUCAS E. & BOSTANIAN N.J. 2003a: Impacts of Lambda-cyhalothrin on intraguild predation among three mite predators. Environ. Entomol. 32: 256-263 Go to original source...
  91. PROVOST C., CODERRE D., LUCAS E. & BOSTANIAN N.J. 2003b: Impact d'une dose subletale de lambda-cyhalothrine sur les predateurs intraguildes d'acariens phytophages en verger de pommiers. Phytoprotection 84: 105-113 Go to original source...
  92. ROOT R. 1967: The niche exploitation pattern of the blue-grey gnat catcher. Ecol. Monogr. 37: 317-350 Go to original source...
  93. ROSENHEIM J.A. 1998: Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43: 421-447 Go to original source...
  94. ROSENHEIM J.A., WILHOIT R. & ARMER C.A. 1993: Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96: 439-449 Go to original source...
  95. ROSENHEIM J.A., KAYA H.K., EHLER L.E., MAROIS J.J. & JAFFEE B.A. 1995: Intraguild predation among biological control agents: Theory and evidence. Biol. Control 5: 303-335 Go to original source...
  96. ROSENHEIM J.A., LIMBURG D.D. & COLFER R.G. 1999: Impact of generalist predators on a biological control agent, Chrysoperla carnea: Direct observations. Ecol. Appl. 9: 409-417 Go to original source...
  97. ROY H.E., ALDERSON P.G. & PELL J.K. 2003: Effect of spatial heterogeneity on the role of Coccinella septempunctata as an intra-guild predator of the aphid pathogen Pandora neoaphidis. J. Invertebr. Pathol. 82: 85-95 Go to original source...
  98. ROZAS L., AVILA J.M. & SANCHEZ-PINERO F. 1991: Observacion de habitos depredadores en Hybosorus illgeri Reiche, 1853 (Coleoptera, Scarabaeoidea, Hybosoridae). Bol. Assoc. Esp. Entomol. 15: 111-115
  99. RUzICKA Z. 1997: Recognition of oviposition-deterring allomones by aphidophagous predators (Neuroptera: Chrysopidae, Coleoptera: Coccinellidae). Eur. J. Entomol. 94: 431-434
  100. RUzICKA Z. & HAVELKA J. 1998: Effects of oviposition-deterring pheromone and allomones on Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Eur. J. Entomol. 95: 211-216
  101. RUzICKA Z. & ZEMEK R. 2003: Effects of conspecific and heterospecific larval tracks on mobility and searching patterns of Cycloneda limbifer Say (Coleoptera: Coccinellidae) females. Arquipelago, Life Mar. Sci. (Suppl.) 5: 85-93
  102. SATO S. & DIXON A.F.G. 2004: Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species. Agric. For. Entomol. 6: 21-24. Go to original source...
  103. SATO S., DIXON A.F.G. & YASUDA H. 2003: Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol. Entomol. 28: 628-633 Go to original source...
  104. SCHELLHORN N.A. & ANDOW D.A. 1999a: Cannibalism and interspecific predation: role of oviposition behavior. Ecol. Appl. 9: 418-428 Go to original source...
  105. SCHELLHORN N.A. & ANDOW D.A. 1999b: Mortality of coccinellid (Coleoptera: Coccinellidae) larvae and pupae when prey become scarce. Environ. Entomol. 28: 1092-1100 Go to original source...
  106. SENGONCA C. & FRINGS B. 1985: Interference and competitive behaviour of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga 30: 245-251 Go to original source...
  107. SHAPOSHNIKOV G.C. 1988: Organization (structure) of population and species, and speciation. In Minks A.K. & Harrewijn P. (eds): World Crop Pests; Aphids, their Biology, Natural Enemies and Control. Vol. A. Elsevier, Amsterdam, The Netherlands, pp. 415-430
  108. SIH A., ENGLUND G. & WOOSTER D. 1998: Emergent impacts of multiple predators on prey. Trends Ecol. Evol. 13: 350-355 Go to original source...
  109. SNYDER W.E. & IVES A.R. 2001: Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82: 705-716 Go to original source...
  110. SNYDER W.E. & IVES A.R. 2003: Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84: 91-107 Go to original source...
  111. SNYDER W.E. & WISE D.H. 2001: Contrasting trophic cascades generated by a community of generalist predators. Ecology 82: 1571-1583 Go to original source...
  112. SNYDER W.E., BALLARD S.N., YANG S., CLEVENGER G.M., MILLER T.D., AHN J.J., HATTEN T.D. & BERRYMAN A.A. 2004a: Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoids Aphelinus asychis on greenhouse roses. Biol. Control. 30: 229-235 Go to original source...
  113. SNYDER W.E., CLEVENGER G.M. & EIGENBRODE S.D. 2004b: Intraguild predation and successful invasion by introduced ladybird species. Oecologia 140: 559-565 Go to original source...
  114. SZEINFELD E.V. 1991: Cannibalism and intraguild predation in clupeoids. Mar. Ecol. Prog. Ser. 79: 17-26 Go to original source...
  115. WEISSER W.W. 2003: Additive effects of pea aphid natural enemies despite intraguild predation. Arquipelago, Life Mar. Sci. (Suppl.) 5: 11-15
  116. WHITE C. & EIGENBRODE S.D. 2000: Leaf surface waxbloom in Pisum sativum influences predation and intra-guild interactions between two predator species. Oecologia 124: 252-259 Go to original source...
  117. WISE D.H. 1993: Spiders in Ecological Webs. Cambridge University Press, Cambridge, UK, 328 pp Go to original source...
  118. YASUDA H. & KIMURA T. 2001: Interspecific interactions in a tritrophic arthropod system: effects of a spider on the survival of larvae of three predatory ladybirds in relation to aphids. Entomol. Exp. Appl. 98: 17-25 Go to original source...
  119. YASUDA H. & OHNUMA N. 1999: Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol. Exp. Appl. 93: 63-67 Go to original source...
  120. YASUDA H., KIKUCHI T., KINDLMANN P. & SATO S. 2001: Relationships between attack and escape rates, cannibalism, and predation in larvae of two predatory ladybirds. J. Insect Behav. 14: 373-384 Go to original source...
  121. YASUDA H., EVANS E.W., KAJITA Y., URAKAWA K. & TAKIZAWA T. 2004: Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141: 722-731 Go to original source...

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