Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Individual- and population-level drivers of consistent foraging success across environments

Abstract

Individual foraging is under strong natural selection. Yet, whether individuals differ consistently in their foraging success across environments, and which individual- and population-level traits might drive such differences, is largely unknown. We addressed this question in a field experiment, conducting over 1,100 foraging trials with subpopulations of guppies, Poecilia reticulata, translocated across environments in the wild. We show that individuals consistently differed in reaching and acquiring food resources, but not control ‘resources’, across environments. Social individuals reached and acquired more food resources than less-social ones and males reached more food resources than females. Yet, overall, individuals were more likely to join females at resources than males, which might explain why individuals in subpopulations with relatively more females reached and acquired, on average, more food resources. Our results provide rare evidence for individual differences in foraging success across environments, driven by individual- and population-level (sex ratio) traits.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Relationship between the proportion of food and control resources reached by an individual fish in its initial pool (first pool) and after translocation (second pool).
Fig. 2: Markov chain model of the guppy fission–fusion social system.
Fig. 3: Proportion of food and control resources reached per pool in relation to individual social time.
Fig. 4: Proportion of food and control resources reached per pool for individual males and females.
Fig. 5: Joining of first arriving fish by subpopulation members in relation to its sex.
Fig. 6: Proportion of detected resources reached by an individual per pool in relation to the sex ratio of its subpopulation.

Similar content being viewed by others

References

  1. Humphries, N. E., Weimerskirch, H., Queiroz, N., Southall, E. J. & Sims, D. W. Foraging success of biological Lévy flights recorded in situ. Proc. Natl Acad. Sci. USA 109, 7169–7174 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Merkle, J. A., Sigaud, M. & Fortin, D. To follow or not? How animals in fusion–fission societies handle conflicting information during group decision-making. Ecol. Lett. 18, 799–806 (2015).

    Article  PubMed  Google Scholar 

  3. Day, L. B., Crews, D. & Wilczynski, W. Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim. Behav. 57, 393–407 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Sheenaja, K. K. & Thomas, K. J. Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792). Mar. Freshw. Behav. Physiol. 44, 349–358 (2011).

    Article  Google Scholar 

  5. Bartumeus, F. et al. Foraging success under uncertainty: search tradeoffs and optimal space use. Ecol. Lett. 19, 1299–1313 (2016).

    Article  PubMed  Google Scholar 

  6. Aplin, L. M., Farine, D. R., Morand-Ferron, J. & Sheldon, B. C. Social networks predict patch discovery in a wild population of songbirds. Proc. R. Soc. Lond. B 279, 4199–4205 (2012).

    Article  CAS  Google Scholar 

  7. Mattern, T., Ellenberg, U., Houston, D. M. & Davis, L. S. Consistent foraging routes and benthic foraging behaviour in yellow-eyed penguins. Mar. Ecol. Prog. Ser. 343, 295–306 (2007).

    Article  Google Scholar 

  8. Patrick, S. C. et al. Individual differences in searching behaviour and spatial foraging consistency in a central place marine predator. Oikos 123, 33–40 (2014).

    Article  Google Scholar 

  9. Niemelä, P. T. & Dingemanse, N. J. Individual versus pseudo-repeatability in behaviour: lessons from translocation experiments in a wild insect. J. Anim. Ecol. 86, 1033–1043 (2017).

    Article  PubMed  Google Scholar 

  10. Krause, J. & Ruxton, G. D. Living in Groups (Oxford Univ. Press, Oxford, 2002).

  11. Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32, 4–14 (2004).

    Article  Google Scholar 

  12. Danchin, É., Giraldeau, L. A., Valone, T. J. & Wagner, R. H. Public information: from nosy neighbors to cultural evolution. Science 305, 487–491 (2004).

    Article  CAS  PubMed  Google Scholar 

  13. Webster, M. M., Whalen, A. & Laland, K. N. Fish pool their experience to solve problems collectively. Nat. Ecol. Evol. 1, 0135 (2017).

    Article  Google Scholar 

  14. Clark, C. W. & Mangel, M. The evolutionary advantages of group foraging. Theor. Popul. Biol. 30, 45–75 (1986).

    Article  Google Scholar 

  15. Tanner, C. J. & Jackson, A. L. Social structure emerges via the interaction between local ecology and individual behaviour. J. Anim. Ecol. 81, 260–267 (2012).

    Article  PubMed  Google Scholar 

  16. Dall, S., Giraldeau, L., Olsson, O., Mcnamara, J. & Stephens, D. Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187–193 (2005).

    Article  PubMed  Google Scholar 

  17. Galef, B. G. Jr & Giraldeau, L.-A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim. Behav. 61, 3–15 (2001).

    Article  PubMed  Google Scholar 

  18. Valone, T. J. & Templeton, J. J. Public information for the assessment of quality: a widespread social phenomenon. Philos. Trans. R. Soc. Lond. B 357, 1549–1557 (2002).

    Article  Google Scholar 

  19. Giraldeau, L. A. & Caraco, T. Social Foraging Theory (Princeton Univ. Press, Princeton, 2000).

  20. Zajonc, R. B. Social facilitation. Science 149, 269–274 (1965).

    Article  CAS  PubMed  Google Scholar 

  21. Reader, S. M., Kendal, J. R. & Laland, K. N. Social learning of foraging sites and escape routes in wild Trinidadian guppies. Anim. Behav. 66, 729–739 (2003).

    Article  Google Scholar 

  22. Morand-Ferron, J., Wu, G.-M. & Giraldeau, L.-A. Persistent individual differences in tactic use in a producer–scrounger game are group dependent. Anim. Behav. 82, 811–816 (2011).

    Article  Google Scholar 

  23. Kurvers, R. H. J. M. et al. Personality predicts the use of social information. Ecol. Lett. 13, 829–837 (2010).

    Article  PubMed  Google Scholar 

  24. Wilson, A. D. M. et al. Dynamic social networks in guppies (Poecilia reticulata). Behav. Ecol. Sociobiol. 68, 915–925 (2014).

    Article  Google Scholar 

  25. Wilson, A. D. M. et al. Social networks in changing environments. Behav. Ecol. Sociobiol. 69, 1617–1629 (2015).

    Article  Google Scholar 

  26. Krause, S. et al. Guppies occupy consistent positions in social networks: mechanisms and consequences. Behav. Ecol. 28, 429–438 (2017).

    Google Scholar 

  27. Laland, K. N. & Williams, K. Shoaling generates social learning of foraging information in guppies. Anim. Behav. 53, 1161–1169 (1997).

    Article  CAS  PubMed  Google Scholar 

  28. Swaney, W., Kendal, J., Capon, H., Brown, C. & Laland, K. N. Familiarity facilitates social learning of foraging behaviour in the guppy. Anim. Behav. 62, 591–598 (2001).

    Article  Google Scholar 

  29. Day, R. L., MacDonald, T., Brown, C., Laland, K. N. & Reader, S. M. Interactions between shoal size and conformity in guppy social foraging. Anim. Behav. 62, 917–925 (2001).

    Article  Google Scholar 

  30. Kendal, R. L., Coolen, I. & Laland, K. N. The role of conformity in foraging when personal and social information conflict. Behav. Ecol. 15, 269–277 (2004).

    Article  Google Scholar 

  31. Reader, S. M. & Laland, K. N. Diffusion of foraging innovations in the guppy. Anim. Behav. 60, 175–180 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Lindström, K. & Ranta, E. Social preferences by male guppies, Poecilia reticulata, based on shoal size and sex. Anim. Behav. 46, 1029–1031 (1993).

    Article  Google Scholar 

  33. Webster, M. M. & Laland, K. N. Local enhancement via eavesdropping on courtship displays in male guppies, Poecilia reticulata. Anim. Behav. 86, 75–83 (2013).

    Article  Google Scholar 

  34. Croft, D. P. et al. Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata. Oikos 100, 429–438 (2003).

    Article  Google Scholar 

  35. Darden, S. K. & Croft, D. P. Male harassment drives females to alter habitat use and leads to segregation of the sexes. Biol. Lett. 4, 449–451 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Darden, S. K., James, R., Ramnarine, I. W. & Croft, D. P. Social implications of the battle of the sexes: sexual harassment disrupts female sociality and social recognition. Proc. R. Soc. Lond. B 276, 2651–2656 (2009).

    Article  Google Scholar 

  37. Trivers, R. in Sexual Selection and the Descent of Man 1871–1971 (ed. Campbell, B.) 136–179 (Aldine, Chicago, 1972).

  38. Reznick, D. & Yang, A. P. The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies. Ecology 74, 2011–2019 (1993).

    Article  Google Scholar 

  39. Abrahams, M. V. The trade-off between foraging and courting in male guppies. Anim. Behav. 45, 673–681 (1993).

    Article  Google Scholar 

  40. Laland, K. N. & Reader, S. M. Foraging innovation in the guppy. Anim. Behav. 57, 331–340 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Griffiths, S. W. Sex differences in the trade-off between feeding and mating in the guppy. J. Fish Biol. 48, 891–898 (1996).

    Article  Google Scholar 

  42. van de Waal, E., Renevey, N., Favre, C. M. & Bshary, R. Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc. R. Soc. Lond. B 277, 2105–2111 (2010).

    Article  Google Scholar 

  43. Silk, J. B., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance infant survival. Science 302, 1231–1234 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. Cameron, E. Z., Setsaas, T. H. & Linklater, W. L. Social bonds between unrelated females increase reproductive success in feral horses. Proc. Natl Acad. Sci. USA 106, 13850–13853 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Griffiths, S. W. & Magurran, A. E. Sex and schooling behaviour in the Trinidadian guppy. Anim. Behav. 56, 689–693 (1998).

    Article  CAS  PubMed  Google Scholar 

  46. Webster, M. M. & Laland, K. N. Reproductive state affects reliance on public information in sticklebacks. Proc. R. Soc. Lond. B 278, 619–627 (2011).

    Article  CAS  Google Scholar 

  47. Magurran, A. E. & Seghers, B. H. Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118, 214–234 (1991).

    Article  Google Scholar 

  48. Rodd, F. H. & Reznick, D. N. Variation in the demography of guppy populations: the importance of predation and life histories. Ecology 78, 405–418 (1997).

    Google Scholar 

  49. Pettersson, L. B., Ramnarine, I. W., Becher, S. A., Mahabir, R., & Magurran, A. E. Sex ratio dynamics and fluctuating selection pressures in natural populations of the Trinidadian guppy Poecilia reticulata. Behav. Ecol. Sociobiol. 55, 461–468 (2004).

    Article  Google Scholar 

  50. White, D. J., Watts, E., Pitchforth, K., Agyapong, S. & Miller, N. ‘Sociability’ affects the intensity of mate-choice copying in female guppies, Poecilia reticulata. Behav. Processes 141, 251–257 (2017).

    Article  PubMed  Google Scholar 

  51. Aureli, F. et al. Fission–fusion dynamics: new research frameworks. Curr. Anthropol. 49, 627–654 (2008).

    Article  Google Scholar 

  52. Couzin, I. D. & Laidre, M. E. Fission–fusion populations. Curr. Biol. 19, R633–R635 (2009).

    Article  CAS  PubMed  Google Scholar 

  53. Hasenjager, M. J. & Dugatkin, L. A. Familiarity affects network structure and information flow in guppy (Poecilia reticulata) shoals. Behav. Ecol. 28, 233–242 (2017).

    Article  Google Scholar 

  54. Laland, K. N. & Williams, K. Social transmission of maladaptive information in the guppy. Behav. Ecol. 9, 493–499 (1998).

    Article  Google Scholar 

  55. Pelé, M. & Sueur, C. Decision-making theories: linking the disparate research areas of individual and collective cognition. Anim. Cogn. 16, 543–556 (2013).

    Article  PubMed  Google Scholar 

  56. Clément, R. J. G., Wolf, M., Snijders, L., Krause, J. & Kurvers, R. H. J. M. Information transmission via movement behaviour improves decision accuracy in human groups. Anim. Behav. 105, 85–93 (2015).

    Article  Google Scholar 

  57. Rieucau, G. & Giraldeau, L.-A. Persuasive companions can be wrong: the use of misleading social information in nutmeg mannikins. Behav. Ecol. 20, 1217–1222 (2009).

    Article  Google Scholar 

  58. Burns, J. G. & Rodd, F. H. Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim. Behav. 76, 911–922 (2008).

    Article  Google Scholar 

  59. Borner, K. K. et al. Turbidity affects social dynamics in Trinidadian guppies. Behav. Ecol. Sociobiol. 69, 645–651 (2015).

    Article  Google Scholar 

  60. Croft, D. P. et al. Predation risk as a driving force for sexual segregation: a coss‐population comparison. Am. Nat. 167, 867–878 (2006).

    Article  PubMed  Google Scholar 

  61. Reznick, D. & Endler, J. A. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160 (1982).

    PubMed  Google Scholar 

  62. Heathcote, R. J. P., Darden, S. K., Franks, D. W., Ramnarine, I. W. & Croft, D. P. Fear of predation drives stable and differentiated social relationships in guppies. Sci. Rep. 7, 41679 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hasenjager, M. J. & Dugatkin, L. A. Fear of predation shapes social network structure and the acquisition of foraging information in guppy shoals. Proc. R. Soc. Lond. B 284, 20172020 (2017).

    Article  Google Scholar 

  64. Beauchamp, G., Belisle, M. & Giraldeau, L.-A. Influence of conspecific attraction on the spatial distribution of learning foragers in a patchy habitat. J. Anim. Ecol. 66, 671–682 (1997).

    Article  Google Scholar 

  65. Lucon-Xiccato, T. & Bisazza, A. Sex differences in spatial abilities and cognitive flexibility in the guppy. Anim. Behav. 123, 53–60 (2017).

    Article  Google Scholar 

  66. Monk, C. T. et al. How ecology shapes exploitation: a framework to predict the behavioural response of human and animal foragers along exploration-exploitation trade-offs. Ecol. Lett. 21, 779–793 (2018).

    Article  PubMed  Google Scholar 

  67. Bell, A. M., Hankison, S. J. & Laskowski, K. L. The repeatability of behaviour: a meta-analysis. Anim. Behav. 77, 771–783 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Snijders, L. et al. Social networking in territorial great tits: slow explorers have the least central social network positions. Anim. Behav. 98, 95–102 (2014).

    Article  Google Scholar 

  69. Cote, J., Fogarty, S. & Sih, A. Individual sociability and choosiness between shoal types. Anim. Behav. 83, 1469–1476 (2012).

    Article  Google Scholar 

  70. Jolles, J. W., Boogert, N. J., Sridhar, V. H., Couzin, I. D. & Manica, A. Consistent individual differences drive collective behavior and group functioning of schooling fish. Curr. Biol. 27, 2862–2868.e7 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Clément, R. J. G. et al. Collective decision making in guppies: a cross-population comparison study in the wild. Behav. Ecol. 28, 919–924 (2017).

    Article  Google Scholar 

  72. Magurran, A. E. Evolutionary Ecology: The Trinidadian Guppy (Oxford Univ. Press, Oxford, 2005).

  73. Grether, G. F., Millie, D. F., Bryant, M. J., Reznick, D. N. & Mayea, W. Rain forest canopy cover, resource availability, and life history evolution in guppies. Ecology 82, 1546–1559 (2001).

    Article  Google Scholar 

  74. Croft, D. P., Krause, J. & James, R. Social networks in the guppy (Poecilia reticulata). Proc. R. Soc. Lond. B 271, S516–S519 (2004).

    Article  Google Scholar 

  75. Croft, D. P. et al. Sex-biased movement in the guppy (Poecilia reticulata). Oecologia 137, 62–68 (2003).

    Article  PubMed  Google Scholar 

  76. Kodric-Brown, A. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol. 25, 393–401 (1989).

    Article  Google Scholar 

  77. Friard, O. & Gamba, M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).

    Article  Google Scholar 

  78. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  79. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  80. Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644 (2017).

    Article  Google Scholar 

  81. Boccaletti, S., Latora, V., Moreno, Y., Chavez, M. & Hwang, D.-U. Complex networks: structure and dynamics. Phys. Rep. 424, 175–308 (2006).

    Article  Google Scholar 

  82. Farine, D. R. & Whitehead, H. Constructing, conducting and interpreting animal social network analysis. J. Anim. Ecol. 84, 1144–1163 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to S. Bouet and S. García Martín for assistance with the video analysis and to F. Dhellemmes, H. te Brake and R. Seifert for assistance with the data collection. L.S. was funded by an IGB Postdoc Fellowship 2017.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed considerably to the design of the study and the collection of the primary data. L.S. and S.K. analysed the data and L.S. wrote the main manuscript. All authors commented on the manuscript and accepted its last version.

Corresponding author

Correspondence to Lysanne Snijders.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods and Results, Supplementary References, Supplementary Tables 1–13, Supplementary Figures 1–7

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Snijders, L., Kurvers, R.H.J.M., Krause, S. et al. Individual- and population-level drivers of consistent foraging success across environments. Nat Ecol Evol 2, 1610–1618 (2018). https://doi.org/10.1038/s41559-018-0658-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0658-4

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing