Abstract
Animals that form groups are typically assorted by phenotype. For example, fish shoals are notably composed of closely size-matched individuals, yet the sensory mechanisms that promote this behaviour have not been fully determined. Here, we show that two freshwater shoaling fish species, three-spined stickleback and banded killifish, have a greater preference for the chemical cues of conspecifics that are the same size as themselves than for those of larger or smaller conspecifics. We suggest that this ability to determine their own size relative to conspecifics may be based on chemical self-referencing. This provides a novel insight to the mechanisms underlying a widespread phenomenon in social behaviour, and provides further evidence of the crucial role played by chemical cues in structuring the interactions of fishes.
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References
Aeschlimann PB, Haberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54:119–126
Bryant BP, Atema J (1987) Diet manipulation affects social-behavior of catfish—importance of body odor. J Chem Ecol 13:1645–1661
Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission–fusion model. Proc R Soc Lond B 267:2213–2218
Ferrari MCO, Messier F, Chivers DP (2006) The nose knows: minnows determine predator proximity and density through detection of predator odours. Anim Behav 72:927–932
Freon P (1984) Body length variability in fish schools and cohorts. 1. Observations and interpretation. Oceanol Acta 7:457–468
Giaquinto PC, Volpato GL (2005) Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans. Acta Ethol 8:65–69
Griffiths SW, Magurran AE (1997) Schooling preferences for familiar fish vary with group size in a wild guppy population. Proc R Soc Lond B 264:547–551
Hara TJ (1992) Fish chemoreception. In: Fish and fisheries. Chapman & Hall, London
Herbert-Read JE, Logendran D, Ward AJW (2010) Sensory ecology in a changing world: salinity alters conspecific recognition in an amphidromous fish, Pseudomugil signifer. Behav Ecol Sociobiol 64:1107–1115
Hoare DJ, Krause J, Peuhkuri N, Godin JGJ (2000a) Body size and shoaling in fish. J Fish Biol 57:1351–1366
Hoare DJ, Ruxton G, Godin JGJ, Krause J (2000b) The social organization of free-ranging fish shoals. Oikos 89:546–554
Krakauer DC (1995) Groups confuse predators by exploiting perceptual bottlenecks—a connectionist model of the confusion effect. Behav Ecol Sociobiol 36:421–429
Krause J, Godin JGJ (1994) Shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae)—effects of predation risk, fish size, species composition and size of shoals. Ethology 98:128–136
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford, UK
Krause J, Godin JGJ, Brown B (1998) Body length variation within multi-species fish shoals: the effects of shoal size and number of species. Oecologia 114:67–72
Krause J, Hoare DJ, Croft D, Lawrence J, Ward A, Ruxton GD, Godin JGJ, James R (2000) Fish shoal composition: mechanisms and constraints. Proc R Soc Lond B 267:2011–2017
Krause J, Ward AJW, Jackson AL, Ruxton GD, James R, Currie S (2005) The influence of differential swimming speeds on composition of multi-species fish shoals. J Fish Biol 67:866–872
Kusch RC, Mirza RS, Chivers DP (2004) Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551–555
Landeau L, Terborgh J (1986) Oddity and the confusion effect in predation. Anim Behav 34:1372–1380
Neff BD, Sherman PW (2005) In vitro fertilization reveals offspring recognition via self-referencing in a fish with paternal care and cuckoldry. Ethology 111:425–438
Neill SRS, Cullen JM (1974) Experiments on whether schooling by their prey affects hunting behavior of cephalopods and fish predators. J Zool 172:549–569
Olsen KH (1989) Sibling recognition in juvenile arctic charr, Salvelinus alpinus (L). J Fish Biol 34:571–581
Olsen KH, Grahn M, Lohm J (2003) The influence of dominance and diet on individual odours in MHC identical juvenile Arctic charr siblings. J Fish Biol 63:855–862
Pitcher TJ, Magurran AE, Allan JR (1986) Size-segregative behavior in minnow shoals. J Fish Biol 29:83–95
Ranta E, Lindstrom K, Peuhkuri N (1992) Size matters when 3-spined sticklebacks go to school. Anim Behav 43:160–162
Sorensen PW, Stacey NE (1999) Evolution and specialization of fish hormonal pheromones. In: Advances in chemical signals in vertebrates edited by Johnston et al. Kluwer Academic, New York
Svensson PA, Barber I, Forsgren E (2000) Shoaling behaviour of the two-spotted goby. J Fish Biol 56:1477–1487
Ward AJW, Hart PJB (2003) The effects of kin and familiarity on interactions between fish. Fish Fish 4:348–358
Ward AJW, Krause J (2001) Body length assortative shoaling in the European minnow, Phoxinus phoxinus. Anim Behav 62:617–621
Ward AJW, Hart PJB, Krause J (2004) The effects of habitat- and diet-based cues on association preferences in three-spined sticklebacks. Behav Ecol 15:925–929
Ward AJW, Holbrook RI, Krause J, Hart PJB (2005) Social recognition in sticklebacks: the role of direct experience and habitat cues. Behav Ecol Sociobiol 57:575–583
Ward AJW, Webster MM, Hart PJB (2007) Social recognition in wild fish populations. Proc R Soc Lond B 274:1071–1077
Ward AJW, Duff AJ, Horsfall JS, Currie S (2008) Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish. Proc R Soc Lond B 275:101–105
Ward AJW, Webster MM, Magurran AE, Currie S, Krause J (2009) Species and population differences in social recognition between fishes: a role for ecology? Behav Ecol 20:511–516
Webster MM, Goldsmith J, Ward AJW, Hart PJB (2007) Habitat-specific chemical cues influence association preferences and shoal cohesion in fish. Behav Ecol Sociobiol 62:273–280
Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Phil Trans R Soc Lond B 355:1205–1208
Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074
Acknowledgments
The authors would like to thank Professor Theo Bakker, the associate editor, Dr Jo Frommen, and two anonymous reviews for comments which greatly improved this manuscript.
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All experiments reported here comply with the current laws of the country in which they were performed.
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Ward, A.J.W., Currie, S. Shoaling fish can size-assort by chemical cues alone. Behav Ecol Sociobiol 67, 667–673 (2013). https://doi.org/10.1007/s00265-013-1486-9
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DOI: https://doi.org/10.1007/s00265-013-1486-9