Abstract
Protection from predators is a recognized benefit of group living for animals. The selfish herd effect implies that individuals in a central position within the group suffer lower predation than individuals at the edges of the group. The midge, Aphidoletes aphidimyza, is a furtive predator that lives within aphid colonies where it benefits from a dilution effect that reduces the incidence of intraguild predation. We hypothesized that the selfish herd effect also contributes to midge survival. In laboratory experiments, we examined the distribution of midge larvae within aphid (Macrosiphum euphorbiae) colonies and determined the susceptibility of central and peripheral individuals to lacewing, Chrysoperla rufilabris, and coccinellid, Coleomegilla maculata larvae, two common intraguild predators. The probability of observing a midge in the central zone of an aphid colony was higher than predicted after a 24-h period. During predation tests, midges and aphids in the peripheral zone were attacked first significantly more often than prey in the central zone of the colony. However, because foraging coccinellid and lacewing larvae rapidly disrupt the cohesion among aphids in the colony, midge mortality was subsequently similar in both zones. We conclude that A. aphidimyza preferentially choose the central position of their aphid prey colonies. Such a preference reduces the probability of becoming the first prey attacked by intraguild predators. The effectiveness of the selfish herd for slow-moving midge larvae would depend on the nature and foraging behavior of the predator, as well as on cohesion of the aphid colony.
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References
Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108
Brodsgaard HF, Enkegaard A (1997) Interactions among polyphagous anthocorid bugs used for thrips control and other beneficials in multi-species biological pest management systems. Recent Res Dev Entomol 1:153–160
De Vos A, O’Riain MJ (2010) Sharks shape the geometry of a selfish seal herd: experimental evidence from seal decoys. Biol Lett 6:48–50
Edmunds M (1974) Defence in animals. Longman Inc., New-York
Fauchald P, Rodven R, Bardsen B-J, Langeland K, Tveraa T, Yoccoz et al (2007) Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer. Oikos 116:491–499
Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 296:466–467
Fréchette B, Lucas F, Larouche É (2008) Leucopis annulipes larvae (Diptera: Chamaemyiidae) use a furtive predation strategy within aphid colonies. Eur J Entomol 105:399–403
Gagnon A-È, Heimpel GE, Brodeur J (2011) The ubiquity of intraguild predation among predatory arthropods. PLos ONE (on-line) 6:e28061
Gardiner MM, Landis DA (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311
Harris KM (1973) Aphidophagous Cecidomyiidae (Diptera): taxonomy ecology and assessments of field populations. Bull Entomol Res 63:305–325
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
Inman AJ, Krebs J (1987) Predation and group living. Trends Ecol Evol 2:31–32
Klingauf F (1967) Abwehr- und Meidereaktionen von Blattläusen (Aphididae) bein Bedrohung durch Räuber und parasiten. J Appl Entomol 60:269–317
Lingle S (2000) Anti-predator strategies and grouping patterns in white-tailed deer and mule deer. Ethology 107:295–314
Losey JE, Denno RF (1998a) Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators. Oecologia 115:245–252
Losey JE, Denno RF (1998b) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecol Entomol 23:53–61
Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364
Lucas E (2012) Intraguild interactions. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behavior of the ladybird beetles (Coccinellidae). Wiley, pp 343–374
Lucas E, Brodeur J (1999) Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environ Entomol 28:622–627
Lucas E, Brodeur J (2001) A fox in sheep’s clothing: furtive predators benefit from the communal defense of their prey. Ecology 82:3246–3250
Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092
Maisonhaute J-E, Lucas E (2011) Influence of landscape structure on the functional groups of an aphidophagous guild: active-searching predators, furtive predators and parasitoids. Eur J Environ Sci 1:41–50
Mooring MS, Hart BL (1992) Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123:173–193
Orpwood JE, Magurran AE, Armstrong JD, Griffiths SW (2008) Minnows and the selfish herd: effects of predation risk on shoaling behaviour are dependent on habitat complexity. Anim Behav 76:143–152
Polis GA, Myers C, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 2nd edn. Sinauer Associates Inc. Publishers, Sunderland Massachusetts, pp 122–147
Quinn JL, Cresswell W (2006) Testing domains of danger in the selfish herd: sparrow hawks target widely spaced redshanks in flocks. P Roy Soc B 273:2521–2526
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rayor LS, Uetz GW (1990) Trade-offs in foraging success and predation risk with spatial position in colonial spiders. Behav Ecol Sociobiol 27:77–85
Rayor LS, Uetz GW (1993) Ontogenic shifts within the selfish herd: predation risk and foraging trade-offs change with age in colonial web-building spiders. Oecologia 95:1–8
Romey WL (1995) Position preferences within groups: do whirligigs select positions which balance feeding opportunities with predator avoidance? Behav Ecol Sociobiol 37:195–200
Rosenheim JA, Limburg DD, Colfer RG (1999) Impact of generalist predators on a biological control agent, Chrysoperla carnea: direct observations. Ecol Appl 9:409–417
Sadedin SR, Elgar MA (1998) The influence of flock size and geometry on the scanning behaviour of spotted turtle doves, Streptopelia chinensis. Aust J Ecol 23:177–180
Sentis A, Lucas É, Vickery WL (2012) Prey abundance, intraguild predators, ants and the optimal egg-laying strategy of a furtive predator. J Insect Behav 25:529–542
Sluss TP, Foote BA (1973) Biology and immature stages of Leucopis verticalis (Diptera: Chamaemyiidae). Can Entomol 103:1427–1434
Vulinec K (1990) Collective security: aggregation by insects as a defense. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New-York Press, Albany, pp 251–288
Watt DJ, Mock DW (1987) A selfish herd of martins. Auk 104:342–343
Wcislo WT (1984) Gregarious nesting of a digger wasp as a selfish herd response to a parasitic fly (Hymenoptera: Sphecidae; Diptera: Sarcophagidae). Behav Ecol Sociobiol 15:157–160
Wrona FJ, Dixon RWJ (1991) Group size and predation risk: a field analysis of encounter and dilution effects. Am Nat 137:186–201
Acknowledgments
This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) to J. Brodeur, and by a graduate scholarship from NSERC to É. Lucas. We thank W. Vickery, L.-A. Giraldeau, S. Tessier, Y. Francoeur-Pin, and two anonymous reviewers for the helpful comments on a previous version of the manuscript, and L. Sénéchal, M. Fournier, and A. Bouchard for the technical assistance.
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Communicated by W. T. Wcislo
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Dumont, F., Lucas, E. & Brodeur, J. Do furtive predators benefit from a selfish herd effect by living within their prey colony?. Behav Ecol Sociobiol 69, 971–976 (2015). https://doi.org/10.1007/s00265-015-1909-x
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DOI: https://doi.org/10.1007/s00265-015-1909-x