Behavioral Ecology and Sociobiology

, Volume 60, Issue 1, pp 77–86 | Cite as

Subhabitat selection by foraging threespine stickleback (Gasterosteus aculeatus): previous experience and social conformity

Original Article


Any mechanism that allows animals to increase their foraging efficiency is likely to be selected for, including the ability to learn to recognise and subsequently discriminate between habitat types based on their profitability. In a series of laboratory studies, we manipulated prey densities across two different experimental subhabitats and demonstrated that threespine stickleback (Gasterosteus aculeatus) can develop foraging preferences for subhabitats that have previously yielded prey. Fish were not recalling the spatial location of prey patches; rather, they were discriminating between subhabitats based on foraging experience there and allocating foraging effort accordingly. Foraging preferences took around 14 days to develop, and once established, they persisted independently of experimental prey density, suggesting that fish were using experience rather than real-time sampling to select foraging grounds. When we presented focal fish with social information cues, we found that they preferentially used local enhancement and current public information cues when they conflicted with previous experience, but that they did not use prior public information. This suggests that in the presence of conspecifics, individuals prioritise social conformity over the use of private information. We discuss our results in the context of optimal foraging and the trade-offs associated with balancing conflicting private and social information.


Optimal foraging Social conformity Public information Memory Threespine stickleback 



Work was carried out at the Department of Biology, University of Leicester, LE1 7RH, UK. We gratefully thank I. Coolen, T.J. Pitcher, A.J.W. Ward and two anonymous referees for helpful criticism of this manuscript. M.M. Webster was supported by a NERC studentship. P.J.B. Hart was supported by NERC grant NER/A/S/2001/01208. The experimental procedures detailed here comply with the current laws of the United Kingdom.


  1. Auster PJ, Malatesta RJ, Donaldson CLS (1997) Distributional responses to small-scale habitat variability by early juvenile silver hake, Merluccius bilinearis. Environ Biol Fisches 50(2):195–200CrossRefGoogle Scholar
  2. Auster PJ, Lindholm J, Schaub S, Funnell G, Kaufman LS, Valentine PC (2003) Use of sand wave habitats by silver hake. J Fish Biol 62(1):143–152CrossRefGoogle Scholar
  3. Boyero L, Bosch J (2004) The effect of riffle-scale environmental variability on macroinvertebrate assemblages in a tropical stream. Hydrobiologia 524(1):125–132CrossRefGoogle Scholar
  4. Brown C, Laland KN (2002) Social learning of a novel avoidance task in the guppy: conformity and social release. Anim Behav 64(2):41–47CrossRefGoogle Scholar
  5. Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136PubMedCrossRefGoogle Scholar
  6. Coolen I, van Bergen Y, Day RL, Laland KN (2003) Heterospecific use of public information by fish in a foraging context. Proc R Soc Lond B Biol Sci 270(1531):2413–2419CrossRefGoogle Scholar
  7. Coolen I, Ward AJW, Hart PJB, Laland KN (2005) Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues. Behav Ecol 16(5):865–870CrossRefGoogle Scholar
  8. Dall SRX, Giraldeau LA, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20(4):187–193PubMedCrossRefGoogle Scholar
  9. Danchin E, Giraldeau LA, Valone TJ, Wagner RH (2004) Public information: from nosy neighbours to cultural evolution. Science 305:487–491PubMedCrossRefGoogle Scholar
  10. Day RL, MacDonald T, Brown C, Laland KN, Reader SM (2001) Interactions between shoal size and conformity in guppy social foraging. Anim Behav 62:917–925CrossRefGoogle Scholar
  11. Ellis T, Hughes RN, Howell BR (2002) Artificial dietary regime may impair subsequent foraging behaviour of hatchery-reared turbot released into the natural environment. J Fish Biol 61(1):252–264CrossRefGoogle Scholar
  12. Frank AH, Flood NB, Overmier JB (1972) Reversal-learning in forebrain ablated and olfactory tract sectioned teleost, Carassius auratus. Psychon Sci 26(3):149–155Google Scholar
  13. Fretwell S, Lucas HL (1970) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36CrossRefGoogle Scholar
  14. Giraldeau L-A, Valone TJ, Templeton JJ (2002) Potential disadvantages of using socially acquired information. Philos Trans R Soc Lond B Biol Sci 357:1559–1566PubMedCrossRefGoogle Scholar
  15. Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Lond B Biol Sci 265(1399):913–918CrossRefGoogle Scholar
  16. Gotceitas V, Colgan P (1991) Assessment of patch profitability and ideal free distribution: the significance of sampling. Behaviour 119:65–76Google Scholar
  17. Hart PJB (2003) Habitat use and feeding behaviour in two closely related fish species, the three-spined and nine-spined stickleback: an experimental analysis. J Anim Ecol 72:777–783CrossRefGoogle Scholar
  18. Hoare DJ, Ruxton GD, Godin JJ, Krause J (2000) The social organisation of free-ranging fish shoals. Oikos 89:546–554CrossRefGoogle Scholar
  19. Hughes RN, Blight CM (1999) Algorithmic behaviour and spatial memory are used by two intertidal fish species to solve the radial maze. Anim Behav 58:601–613PubMedCrossRefGoogle Scholar
  20. Kendal RL, Coolen I, Laland KN (2004) The role of conformity in foraging when personal and social information conflict. Behav Ecol 15(2):269–277CrossRefGoogle Scholar
  21. Kendal RL, Coolen I, van Bergen Y, Laland KN (2006) Trade offs in the adaptive use of social and asocial learning. Adv Stud Behav (in press)Google Scholar
  22. Krause J (1993) The influence of hunger on shoal size choice by three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 43:775–780CrossRefGoogle Scholar
  23. Lachlan RF, Crooks L, Laland KN (1998) Who follows whom? Shoaling preferences and social learning of foraging information in guppies. Anim Behav 56:181–190PubMedCrossRefGoogle Scholar
  24. Laland KN (2004) Social learning strategies. Learn Behav 32(1):4–14PubMedGoogle Scholar
  25. Laland KN, Williams K (1997) Shoaling generates social learning of foraging information in guppies. Anim Behav 53:1161–1169PubMedCrossRefGoogle Scholar
  26. Langley R (1979) Practical statistics simply explained. Pan Books, New YorkGoogle Scholar
  27. Levin LE, Vergara E (1987) Reversal learning in groups of the schooling fish Aphyocharax erithrurus on an avoidance paddle. J Comp Psychol 101(4):317–321CrossRefGoogle Scholar
  28. Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253Google Scholar
  29. Magurran AE, Seghers BH (1990) Population differences in the schooling behaviour of newborn guppies, Poecilia reticulata. Ethology 84(4):334–342CrossRefGoogle Scholar
  30. Magurran AE, Seghers BH (1994) Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour 128:121–134Google Scholar
  31. Milinski M (1994) Long-term memory for food patches and implications for ideal free distributions in sticklebacks. Ecology 75(4):1150–1156CrossRefGoogle Scholar
  32. Milinski M, Parker GA (1991) Competition for resources. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Cambridge, pp 137–168Google Scholar
  33. Odling-Smee L, Braithwaite VA (2003) The role of learning in fish orientation. Fish Fish 4(3):235–246Google Scholar
  34. Pitcher TJ, Magurran AE (1983) Shoal size, patch profitability and information exchange in foraging goldfish. Anim Behav 31:546–555CrossRefGoogle Scholar
  35. Pitcher TJ, Magurran AE, Winfield IJ (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10(2):149–151CrossRefGoogle Scholar
  36. Ryer CH, Olla BL (1995) Influences of food distribution on fish foraging behaviour. Anim Behav 49(2):411–418CrossRefGoogle Scholar
  37. Seghers BH, Magurran AE (1995) Population differences in the schooling behaviour of the Trinidadian guppy, Poecilia reticulata—adaptation or constraint. Can J Zool 73(6):1100–1105CrossRefGoogle Scholar
  38. Steingrund P, Fernö A (1997) Feeding behaviour of reared and wild cod and the effect of learning: two strategies of feeding on the two-spotted goby. J Fish Biol 51(2):334–348CrossRefGoogle Scholar
  39. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton, NJGoogle Scholar
  40. Taniguchi H, Tokeshi M (2004) Effects of habitat complexity on benthic assemblages in a variable environment. Freshw Biol 49(9):1164–1178CrossRefGoogle Scholar
  41. Taniguchi H, Nakano S, Tokeshi M (2003) Influences of habitat complexity on the diversity and abundance of epiphytic invertebrates on plants. Freshw Biol 48(4):718–728CrossRefGoogle Scholar
  42. Valone TJ, Templeton JJ (2002) Public information for the assessment of quality: a widespread social phenomenon. Philos Trans R Soc Lond B Biol Sci 357:1549–1557PubMedCrossRefGoogle Scholar
  43. van Bergen Y, Coolen I, Laland KN (2004) Nine-spined sticklebacks exploit the most reliable source when public and private information conflict. Proc R Soc Lond B Biol Sci 271(1542):957–962CrossRefGoogle Scholar
  44. Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4(3):203–215Google Scholar
  45. 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(6):925–929CrossRefGoogle Scholar
  46. 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(6):575–583CrossRefGoogle Scholar
  47. Webster MM, Hart PJB (2004) Substrate discrimination and preference in foraging fish. Anim Behav 68:1071–1077CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of BiologyUniversity of LeicesterLeicesterUK

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