Social information use and collective foraging in a pursuit diving seabird

Autoři: Julian C. Evans aff001;  Colin J. Torney aff002;  Stephen C. Votier aff003;  Sasha R. X. Dall aff001
Působiště autorů: Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, Cornwall, United Kingdom aff001;  School of Mathematics and Statistics, University of Glasgow, Glasgow, United Kingdom aff002;  Environment & Sustainability Institute, University of Exeter, Penryn Campus, Penryn, Cornwall, United Kingdom aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222600


Individuals of many species utilise social information whilst making decisions. While many studies have examined social information in making large scale decisions, there is increasing interest in the use of fine scale social cues in groups. By examining the use of these cues and how they alter behaviour, we can gain insights into the adaptive value of group behaviours. We investigated the role of social information in choosing when and where to dive in groups of socially foraging European shags. From this we aimed to determine the importance of social information in the formation of these groups. We extracted individuals’ surface trajectories and dive locations from video footage of collective foraging and used computational Bayesian methods to infer how social interactions influence diving. Examination of group spatial structure shows birds form structured aggregations with higher densities of conspecifics directly in front of and behind focal individuals. Analysis of diving behaviour reveals two distinct rates of diving, with birds over twice as likely to dive if a conspecific dived within their visual field in the immediate past. These results suggest that shag group foraging behaviour allows individuals to sense and respond to their environment more effectively by making use of social cues.

Klíčová slova:

Animal behavior – Birds – Cameras – Collective animal behavior – Foraging – Predation – Animal sociality – Bayesian method


1. Worden BD, Papaj DR. Flower choice copying in bumblebees. Biology Letters. 2005;1(4):504–7. doi: 10.1098/rsbl.2005.0368 17148244

2. Valone T. From eavesdropping on performance to copying the behavior of others: a review of public information use. Behavioral Ecology and Sociobiology. 2007;62(1):1–14. doi: 10.1007/s00265-007-0439-6

3. Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW. Information and its use by animals in evolutionary ecology. Trends in Ecology and Evolution. 2005;20(4):187–93. doi: 10.1016/j.tree.2005.01.010 16701367

4. Evans JC, Votier SC, Dall SRX. Information use in colonial living. Biological Reviews. 2015:1–16. doi: 10.1111/brv.12188 25882618

5. Godin J-GJ, Herdman EJ, Dugatkin LA. Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Animal Behaviour. 2005;69(4):999–1005.

6. Mery F, Varela SA, Danchin É, Blanchet S, Parejo D, Coolen I, et al. Public versus personal information for mate copying in an invertebrate. Current Biology. 2009;19(9):730–4. doi: 10.1016/j.cub.2009.02.064 19361993

7. Webster M, Laland K. Social learning strategies and predation risk: minnows copy only when using private information would be costly. Proceedings of the Royal Society of London B: Biological Sciences. 2008;275(1653):2869–76.

8. Boulinier T, McCoy KD, Yoccoz NG, Gasparini J, Tveraa T. Public information affects breeding dispersal in a colonial bird: kittiwakes cue on neighbours. Biology Letters. 2008;4(5):538–40. doi: 10.1098/rsbl.2008.0291 18647711

9. Jones TB, Patrick SC, Arnould JP, Rodríguez-Malagón MA, Wells MR, Green JA. Evidence of sociality in the timing and location of foraging in a colonial seabird. Biology letters. 2018;14(7):20180214. doi: 10.1098/rsbl.2018.0214 29997186

10. Beauchamp G. Function and structure of vigilance in a gregarious species exposed to threats from predators and conspecifics. Animal behaviour. 2016;116:195–201.

11. Dell AI, Bender JA, Branson K, Couzin ID, de Polavieja GG, Noldus LPJJ, et al. Automated image-based tracking and its application in ecology. Trends in ecology & evolution. 2014;29(7):417–28.

12. Lukeman R, Li Y-X, Edelstein-Keshet L, Simon AL. Inferring individual rules from collective behavior. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(28):12576–80. doi: 10.1073/pnas.1001763107 20616032

13. Buhl J, Sword GA, Clissold FJ, Simpson SJ. Group structure in locust migratory bands. Behavioral ecology and sociobiology. 2011;65(2):265–73.

14. Strandburg-Peshkin A, Farine DR, Couzin ID, Crofoot MC. Shared decision-making drives collective movement in wild baboons. Science. 2015;348(6241):1358–61. doi: 10.1126/science.aaa5099 26089514

15. Ramos A, Petit O, Longour P, Pasquaretta C, Sueur C. Collective decision making during group movements in European bison, Bison bonasus. Animal Behaviour. 2015;109:149–60.

16. Ballerini M, Cabibbo N, Candelier R, Cavagna A, Cisbani E, Giardina I, et al. Interaction ruling animal collective behavior depends on topological rather than metric distance: Evidence from a field study. Proceedings of the national academy of sciences. 2008;105(4):1232–7.

17. Mann RP, Perna A, Strömbom D, Garnett R, Herbert-Read JE, Sumpter DJ, et al. Multi-scale inference of interaction rules in animal groups using Bayesian model selection. 2013.

18. Herbert-Read JE, Perna A, Mann RP, Schaerf TM, Sumpter DJ, Ward AJ. Inferring the rules of interaction of shoaling fish. Proceedings of the National Academy of Sciences. 2011;108(46):18726–31.

19. Nelson B. Pelicans, Cormorants and Their Relatives: Pelecanidae, Sulidae, Phalacrocoracidae, Anhingidae, Fregatidae, Phaethontidae. Oxford: Oxford University Press; 2005.

20. Evans JC, Dall SRX, Bolton M, Owen E, Votier SC. Social foraging European shags: GPS tracking reveals birds from neighbouring colonies have shared foraging grounds. Journal of Ornithology. 2016;157(1):23–32. doi: 10.1007/s10336-015-1241-2

21. Schenkeveld LE, Ydenberg RC. Synchronous diving by surf scoter flocks. Canadian Journal of Zoology. 1985;63(11):2516–9. doi: 10.1139/z85-372

22. Beauchamp G. Diving behavior in surf scoters and Barrow's goldeneyes. The Auk. 1992:819–27.

23. Anderson JGT. Foraging Behavior of the American White Pelican (Pelecanus erythrorhyncos) in Western Nevada. Colonial Waterbirds. 1991;14(2):166–72. doi: 10.2307/1521506

24. Weimerskirch H, Bertrand S, Silva J, Marques JC, Goya E. Use of Social Information in Seabirds: Compass Rafts Indicate the Heading of Food Patches. PLoS ONE. 2010;5(3):e9928. doi: 10.1371/journal.pone.0009928 20360959

25. Wilson LJ, McSorley CA, Gray CM, Dean BJ, Dunn TE, Webb A, et al. Radio-telemetry as a tool to define protected areas for seabirds in the marine environment. Biological Conservation. 2009;142(8):1808–17.

26. Fox A, Green A, Hughes B, Hilton G. Rafting as an antipredator response of wintering White-headed duck Oxyura leucocephala. Wildfowl. 1994;45(45):232–41.

27. Fox A, Mitchell C. Rafting behaviour and predator disturbance to Steller's Eiders Polysticta stelleri in northern Norway. Journal für Ornithologie. 1997;138(1):103–9. doi: 10.1007/bf01651656

28. Barnard C, Thompson D, Stephens H. Time budgets, feeding efficiency and flock dynamics in mixed species flocks of lapwings, golden plovers and gulls. Behaviour. 1982:44–69.

29. Hoffman W, Heinemann D, Wiens JA. The ecology of seabird feeding flocks in Alaska. The Auk. 1981;98(3):437–56.

30. Battley PF, Poot M, Wiersma P, Gordon C, Ntiamoa-Baidu Y, Piersma T. Social foraging by waterbirds in shallow coastal lagoons in Ghana. Waterbirds. 2003;26(1):26–34.

31. Berlincourt M, Arnould JPY. At-Sea Associations in Foraging Little Penguins. PLoS ONE. 2014;9(8):e105065. doi: 10.1371/journal.pone.0105065 25119718

32. Takahashi A, Sato K, Nishikawa J, Watanuki Y, Naito Y. Synchronous diving behavior of Adélie penguins. Journal of Ethology. 2004;22(1):5–11. doi: 10.1007/s10164-003-0111-1

33. Ranta E, Rita H, Lindstrom K. Competition versus cooperation: success of individuals foraging alone and in groups. American Naturalist. 1993:42–58. doi: 10.1086/285528 19425970

34. Foster SA. Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Animal Behaviour. 1985;33(3):782–92.

35. Cresswell W. Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Animal Behaviour. 1994;47(2):433–42.

36. Ruxton G. Foraging in flocks: non-spatial models may neglect important costs. Ecological Modelling. 1995;82(3):277–85.

37. Roberts G. Why individual vigilance declines as group size increases. Animal Behaviour. 1996;51(5):1077–86.

38. Beauchamp G. Should vigilance always decrease with group size? Behavioral Ecology and Sociobiology. 2001;51(1):47–52.

39. Dall SR, Wright J. Rich pickings near large communal roosts favor ‘gang’foraging by juvenile common ravens, Corvus corax. PLoS ONE. 2009;4(2):e4530. doi: 10.1371/journal.pone.0004530 19240813

40. Götmark F, Winkler DW, Andersson M. Flock-feeding on fish schools increases individual success in gulls. Nature. 1986;319(6054):589–91. doi: 10.1038/319589a0 3945345

41. Noren SR, Biedenbach G, Edwards EF. Ontogeny of swim performance and mechanics in bottlenose dolphins (Tursiops truncatus). Journal of Experimental Biology. 2006;209(23):4724–31.

42. Thiebault A, Semeria M, Lett C, Tremblay Y. How to capture fish in a school? Effect of successive predator attacks on seabird feeding success. Journal of Animal Ecology. 2016;85(1):157–67. doi: 10.1111/1365-2656.12455 26768335

43. Benoit-Bird KJ, Au WW. Cooperative prey herding by the pelagic dolphin, Stenella longirostris. The Journal of the Acoustical Society of America. 2009;125(1):125–37. doi: 10.1121/1.2967480 19173400

44. Handegard Nils O, Boswell Kevin M, Ioannou Christos C, Leblanc Simon P, Tjøstheim Dag B, Couzin Iain D. The Dynamics of Coordinated Group Hunting and Collective Information Transfer among Schooling Prey. Current Biology. 2012;22(13):1213–7. doi: 10.1016/j.cub.2012.04.050 22683262

45. Templeton JJ, Giraldeau L-A. Patch assessment in foraging flocks of European starlings: evidence for the use of public information. Behavioral Ecology. 1995;6(1):65–72.

46. Dermody BJ, Tanner CJ, Jackson AL. The Evolutionary Pathway to Obligate Scavenging in Gyps Vultures. PLoS ONE. 2011;6(9):e24635. doi: 10.1371/journal.pone.0024635 21931786

47. Enstipp MR, Jones DR, Lorentsen S-H, Grémillet D. Energetic costs of diving and prey-capture capabilities in cormorants and shags (Phalacrocoracidae) underline their unique adaptation to the aquatic environment. Journal of Ornithology. 2007;148(2):593–600.

48. Wilson RP, Hustler K, Ryan PG, Burger AE, Noldeke EC. Diving Birds in Cold Water: Do Archimedes and Boyle Determine Energetic Costs? The American Naturalist. 1992;140(2):179–200. doi: 10.2307/2462606

49. Williams TM, Davis R, Fuiman L, Francis J, Le B, Horning M, et al. Sink or swim: strategies for cost-efficient diving by marine mammals. Science. 2000;288(5463):133–6. doi: 10.1126/science.288.5463.133 10753116

50. Williams TM, Fuiman LA, Horning M, Davis RW. The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. Journal of Experimental Biology. 2004;207(6):973–82. doi: 10.1242/jeb.00822 14766956

51. Stempniewicz L, Darecki M, Trudnowska E, Błachowiak-Samołyk K, Boehnke R, Jakubas D, et al. Visual prey availability and distribution of foraging little auks (Alle alle) in the shelf waters of West Spitsbergen. Polar Biology. 2013;36(7):949–55. doi: 10.1007/s00300-013-1318-4

52. White CR, Day N, Butler PJ, Martin GR. Vision and Foraging in Cormorants: More like Herons than Hawks? PLoS ONE. 2007;2(7):e639. doi: 10.1371/journal.pone.0000639 17653266

53. Brumm H, Teschke I. Juvenile Galápagos Pelicans Increase Their Foraging Success by Copying Adult Behaviour. PLoS ONE. 2012;7(12):e51881. doi: 10.1371/journal.pone.0051881 23251646

54. Strandburg-Peshkin A, Twomey CR, Bode NWF, Kao AB, Katz Y, Ioannou CC, et al. Visual sensory networks and effective information transfer in animal groups. Current Biology. 2013;23(17):R709–R11. doi: 10.1016/j.cub.2013.07.059 24028946

55. Bode NW, Wagoum AUK, Codling EA. Information use by humans during dynamic route choice in virtual crowd evacuations. Royal Society Open Science. 2015;2(1):140410. doi: 10.1098/rsos.140410 26064589

56. MATLAB. R2015a. Natick, Massachusetts: The MathWorks Inc.; 2015.

57. Bertsekas D. The Auction Algorithm for Assignment and Other Network Flow Problems. New Trends in Systems Theory. Progress in Systems and Control Theory. 7: Birkhäuser Boston; 1991. p. 105–12.

58. Patil A, Huard D, Fonnesbeck CJ. PyMC: Bayesian stochastic modelling in Python. Journal of statistical software. 2010;35(4):1. 21603108

59. Watanabe S. Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. Journal of Machine Learning Research. 2010;11(Dec):3571–94.

60. Ferguson EA, Matthiopoulos J, Insall RH, Husmeier D. Inference of the drivers of collective movement in two cell types: Dictyostelium and melanoma. Journal of The Royal Society Interface. 2016;13(123):20160695.

61. Galef BG Jr, Giraldeau L-A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Animal Behaviour. 2001;61(1):3–15. doi: 10.1006/anbe.2000.1557 11170692

62. White CR, Butler PJ, GrÉMillet D, Martin GR. Behavioural strategies of cormorants (Phalacrocoracidae) foraging under challenging light conditions. Ibis. 2008;150:231–9. doi: 10.1111/j.1474-919X.2008.00837.x

63. Krebs JR, Inman AJ. Learning and Foraging: Individuals, Groups, and Populations. The American Naturalist. 1992;140(ArticleType: research-article / Issue Title: Supplement: Behavioral Mechanisms in Evolutionary Ecology / Full publication date: Nov., 1992 / Copyright 1992 The University of Chicago):S63-S84. doi: 10.2307/2462354

64. Machovsky-Capuska GE, Howland HC, Raubenheimer D, Vaughn-Hirshorn R, Würsig B, Hauber ME, et al. Visual accommodation and active pursuit of prey underwater in a plunge-diving bird: the Australasian gannet. Proceedings of the Royal Society B: Biological Sciences. 2012;279(1745):4118–25. doi: 10.1098/rspb.2012.1519 22874749

65. Rands SA, Cowlishaw G, Pettifor RA, Rowcliffe JM, Johnstone RA. Spontaneous emergence of leaders and followers in foraging pairs. Nature. 2003;423(6938):432–4. doi: 10.1038/nature01630 12761547

66. Takahashi A, Sato K, Naito Y, Dunn M, Trathan P, Croxall J. Penguin–mounted cameras glimpse underwater group behaviour. Proceedings of the Royal Society of London Series B: Biological Sciences. 2004;271(Suppl 5):S281–S2.

67. Watanuki Y, Daunt F, Takahashi A, Newell M, Wanless S, Sato K, et al. Microhabitat use and prey capture of a bottom-feeding top predator, the European Shag, shown by camera loggers. Marine Ecology Progress Series. 2008;356:283–93.

68. Votier SC, Bicknell A, Cox SL, Scales KL, Patrick SC. A bird’s eye view of discard reforms: bird-borne cameras reveal seabird/fishery interactions. PLoS ONE. 2013;8(3):e57376. doi: 10.1371/journal.pone.0057376 23483906

69. Thiebault A, Mullers R, Pistorius P, Meza-Torres MA, Dubroca L, Green D, et al. From colony to first patch: Processes of prey searching and social information in Cape Gannets. The Auk. 2014;131(4):595–609. doi: 10.1642/auk-13-209.1

70. HydroSpatial One—Gridded Bathymetry. Seazone Solutions; 2015.

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