Abstract
As many animals form aggregations, group-living is believed to be adaptive. It is not clear, though, if clonal aggregations should have spatial structure, as protecting clone-mates is the genetic equivalent of protecting self. ‘Fitness discounting’ theory states that immediate reproductive opportunities are of greater value than are delayed opportunities. Thus, we hypothesized that spatial structure should exist in colonies of unequal-aged, clonal organisms like aphids. We predicted that, compared to reproductive (5th instar) individuals, young (2nd and 3rd instar) juveniles (i.e., the youngest instars capable of emitting an alarm signal) should occupy the most dangerous feeding positions. As individuals approach reproductive maturity and alarm signals decline (4th instar), they should occupy increasingly safer feeding positions. We tested these predictions by documenting the spatial distribution of two (green and pink) pea aphid, Acyrthosiphon pisum, asexual lineages (“clones”) at 1, 3, 6, 24, 48, 72, 96, and 120 h after host plant colonization. Confirming our hypothesis, we found that early (2nd and 3rd) instar aphids occupied feeding positions with the highest predation risk. Upon reaching the penultimate (4th) instar, individuals dispersed from the colony to colonize other leaves. Thus, pea aphid colonies are not random aggregations; aphid colony structure can be explained by fitness discounting theory.
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References
Andersson M, Wiklund CG (1978) Clumping versus spacing out: experiments on nest predation in fieldfares (Turdus pilaris). Anim Behav 26:1207–1212
Barta Z, Flynn R, Giraldeau LA (1997) Geometry for a selfish foraging group: a genetic algorithm approach. Proc R Soc B Biol Sci 264:1233–1238
Benkmann CW (1988) Flock size, food dispersion and the feeding behaviors of crossbills. Behav Ecol Sociobiol 23:167–175
Biesinger Z, Haefner JW (2005) Proximate cues for predator searching: a quantitative analysis of hunger and encounter rate in the ladybird (Coccinella septempuctata). Anim Behav 69:235–244
Blackman RL (1979) Stability and variation in aphid clonal lineages. Biol J Linn Soc 11:259–277
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer, Sunderland
Braendle C, Weisser WW (2001) Variation in escape behavior of red and green clones in the pea aphid. J Insect Behav 14:497–509
Byers JA (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92:69–72
Caraco T, Pulliam HR (1984) Sociality and survivorship in animals exposed to predation. In: Price PW, Slobodchickoff CN, Gaud WS (eds) A new ecology: Novel approaches to interactive systems. Wiley Interscience, New York, pp 279–309
Caro TM (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago
Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75
Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer, Sunderland
Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379
Dawkins R (1982) The extended phenotype: The gene as the unit of selection. W.H. Freeman and Company, Oxford
Dehn MM (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342
Dixon AFG (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L). Trans R Soc London 110:319–334
Dixon AFG (1959) An experimental study of the searching behaviour of the predatory coccinellid beetle Adalia decempunctata (L.). J Anim Ecol 28:259–281
Dixon AFG (1977) Aphid ecology: life cycles, polymorphism and population regulation. Annu Rev Ecol Syst 8:329–353
Dixon AFG (1985) Aphid ecology. Blackie, Glascow
Dixon AFG, Wratten SD (1971) Laboratory studies on aggregation, size, and fecundity in the black bean aphid, Aphis fabae Scop. B Entomol Res 61:97–111
Gutierrez AP, Hagen KS, Ellis CK (1990) Evaluating the impact of natural enemies: a multitrophic perspective. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Intercept, Andover, pp 81–109
Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef- building corals. Ecology 77:950–963
Hamilton WD (1964) The genetical evolution of social behaviour II. J Theor Biol 7:17–52
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311
Harmon JP, Losey JE, Ives AR (1998) The role of vision and color in the close proximity foraging behavior of four coccinellid species. Oecologia 115:287–292
Harvell CD, Grosberg RK (1988) The timing of sexual maturity in clonal animals. Ecology 69:1855–1864
Houston AI, McNamara JM (1986) The influence of mortality on the behaviour that maximises reproductive success in a patchy environment. Oikos 47:267–274
Ide T, Suzuki N, Katayama N (2007) The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecol Entomol 32:455–460
Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76:1506–1515
Iwasa Y, Suzuki Y, Matsuda H (1984) Theory of oviposition strategy of parasitoids. I. Effect of mortality and limited egg number. Theor Popul Biol 26:205–227
Janzen DH (1977) What are dandelions and aphids? Am Nat 111:586–589
Johnson PCD, Whitfield JA, Foster WA, Amos W (2002) Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). Mol Ecol 11:1525–1531
Kidd NAC (1977) Factors influencing aggregation between nymphs of the lime aphid, Eucallipterus tiliae (L.). Ecol Entomol 2:273–277
Kidd NAC (1982) Predator avoidance as a result of aggregation in the grey pine aphid, Schizolachnus pineti. J Anim Ecol 51:397–412
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford
Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London
Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:15–21
Libbrecht R, Gwynn DM, Fellowes MDE (2007) Aphidius ervi preferentially attacks the green morph of the pea aphid, Acyrthosiphon pisum. J Insect Behav 20:25–32
Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20
Losey JE, Ives AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272
Loxdale HD (2008) The nature and reality of the aphid clone: genetic variation, adaptation, and evolution. Agric For Entomol 10:81–90
Maynard Smith J (1978) Optimization theory in evolution. Annu Rev Ecol Syst 9:31–56
McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126
Michaud JP, Jyoti JL, Qureshi JA (2006) Positive correlation of fitness with group size in two biotypes of Russian wheat aphid. J Econ Entomol 99:1214–1224
Mondor EB, Roitberg BD (2002) Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk. Can J Zool 80:2131–2136
Mondor EB, Roitberg BD (2003) Age-dependent fitness costs of alarm signaling in aphids. Can J Zool 81:757–762
Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. P Roy Soc B Biol Sci (Supp) 271:S341–S343
Mondor EB, Baird DS, Slessor KN, Roitberg BD (2000) Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum. J Chem Ecol 26:2875–2882
Nakamuta K (1985) Mechanism of the switchover from extensive to area-concentrated search behaviour of the ladybird beetle Coccinella septempunctata bruckii. J Insect Physiol 31:849–856
Nault LR, Edwards LJ, Styer WE (1973) Aphid alarm pheromones: secretion and reception. Environ Entomol 2:101–105
Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151:22–32
Obata S (1986) Mechanisms of prey finding in the aphidophagous ladybird beetle Harmonia axyridis (Col., Coccinellidae). Entomophaga 31:303–311
Obrycki JJ, Tauber MJ, Tingey WM (1983) Predator and parasitoid interaction with aphid-resistant potatoes to reduce aphid densities: a two-year field study. J Econ Entomol 76:456–462
Orpwood JE, Magurran AE, Armstrong JD, Griffiths SW (2008) Minnows and the selfish herd: effects of predation risk on shoaling behavior are dependent on habitat complexity. Anim Behav 76:143–152
Pickett JA, Wadham LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Annu Rev Entomol 37:67–90
Pike N, Manica A (2006) The optimal balance of defence investment strategies in clonal colonies of social aphids. Behav Ecol Sociobiol 60:803–814
Prasad RP, Kabaluk JT, Meberg HP, Bevon DA, Henderson DE (2009) Seasonal and spatial occurrence of aphid natural enemies in organic Brassica fields: diversity, phenology, and reproduction. J Sustain Agr 33:336–348
Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioral ecology: An evolutionary approach. Sinauer, Sunderland, pp 122–147
Ritz DA (1994) Social aggregation in pelagic invertebrates. Adv Mar Biol 30:155–216
Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086
Romey WL, Walston AR, Watt PJ (2008) Do 3-D predators attack the margins of 2-D selfish herds? Behav Ecol 19:74–78
SAS Institute Inc (2008) JMP 8.0—statistical discovery from SAS. SAS Institute, Cary
Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. P Roy Soc B Biol Sci 270:1905–1909
Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton
Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biological control. Ecology 84:91–107
Sozou PD, Seymour RM (2003) Augmented discounting: Interaction between ageing and time-preference behaviour. P Roy Soc B Biol Sci 270:1047–1053
Stadler B, Weisser WW, Houston AI (1994) Defence reactions in aphids: the influence of state and future reproductive success. J Anim Ecol 63:419–430
Sumpter DJT (2006) The principles of collective animal behaviour. Philos T Roy Soc B 361:5–22
Taylor LR, Woiwod IP, Perry JN (1978) The density-dependence of spatial behavior and the rarity of randomness. J Anim Ecol 47:383–406
Tomiuk J, Wohrmann K (1982) Comments on the stability of aphid clones. Experientia 38:320–321
Turchin P, Kareiva P (1989) Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology 70:1008–1016
van Veen FJF, Müller CB, Pell JK, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200
Villagra CA, Ramirez CC, Niemeyer HM (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state. Anim Behav 64:677–683
Viscido SV, Wethey DS (2002) Quantitative analysis of fiddler crab movement: evidence for ‘selfish herd’ behaviour. Anim Behav 63:735–741
Volkl W, Stadler B (1996) Colony orientation and successful defence behaviour in the conifer aphid, Schizolachnus pineti. Entomol Exp Appl 78:197–200
Watt DJ, Mock DW (1987) A selfish herd of martins. Auk 104:342–343
Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton
Wilson DS (1975) A theory of group selection. P Natl Acad Sci USA 72:143–146
Wynne-Edwards VC (1962) Animal dispersion in relation to social behaviour. Oliver & Boyd, Edinburgh
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs
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Laboratory assistance was provided by A. Shepard. Funding for this project was provided by the Department of Biology and Georgia Southern University.
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Duff, K.M., Mondor, E.B. All Clone-mates are not Created Equal: Fitness Discounting Theory Predicts Pea Aphid Colony Structure. J Insect Behav 25, 48–59 (2012). https://doi.org/10.1007/s10905-011-9275-7
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DOI: https://doi.org/10.1007/s10905-011-9275-7