Advertisement

Evidence for non-random co-occurrences in a white shark aggregation

  • Adam Schilds
  • Johann Mourier
  • Charlie HuveneersEmail author
  • Leila Nazimi
  • Andrew Fox
  • Stephan T. Leu
Original Article

Abstract

Groups or aggregations of animals can result from individuals being attracted to a common resource or because of synchronised patterns of daily or seasonal activity. Although mostly solitary throughout its distribution, white sharks (Carcharodon carcharias) seasonally aggregate at a number of sites worldwide to feed on calorie-rich pinnipeds. At the Neptune Islands, South Australia, large numbers of white sharks can be sighted throughout the year, including during periods of low seal abundance. We use a combination of photo-identification and network analysis based on co-occurrence of individuals visiting the site on the same day to elucidate the population structure and aggregatory behaviour of Australia’s largest aggregation of sub-adult and adult white sharks. We photo-identified 282 sharks (183 males, 97 females, 2 unknown) over a 4.5-year period (June 2010–November 2014) and found that white sharks did not randomly co-occur with their conspecifics, but formed four distinct communities. Tendency to co-occur varied across months with males co-occurring with more individuals than females. Sex-dependent patterns of visitation at the Neptune Islands and resulting intraspecific competition likely drive the observed community structure and temporal variability in co-occurrences. This study provides new insights into the aggregatory behaviour of white sharks at a seal colony and shows for the first time that white shark co-occurrence can be non-random.

Significance statement

White sharks are top marine predators that are typically solitary but can also form aggregations around seal colonies to feed. Using a combination of photo-identification and network analysis, we investigated the co-occurrence patterns of white sharks. We showed, for the first time, that white sharks form non-random associations with conspecifics. We hypothesise that the observed sex-dependant variations in co-occurrence are linked to intraspecific competition for resources, providing new insights into the aggregatory behaviour of white sharks at a seal colony. Our study adds to the growing literature of animals showing non-random interaction or co-occurrence patterns, providing important comparative knowledge for other researchers as it broadens our knowledge to marine top predators.

Keywords

Social network analysis Gregariousness Social behaviour Aggregation Photo-ID Carcharodon carcharias 

Notes

Acknowledgements

We thank Rachel Robbins who initiated the use of photo-identification at the Neptune Islands to assess the white shark population dynamics. We also thank Tullio Rossi from Animate Your Science (https://www.animateyour.science/) for designing the white shark photo-identification catalogue. A large number of volunteers are thanked for their assistance with photo and video sorting and processing. We thank the anonymous reviewers who helped improving this manuscript.

Funding information

The Norman Wettenhall Foundation contributed funds towards a white shark photo-identification catalogue.

Compliance with ethical standards

Ethical approval

AF owns a cage-diving licence and business at the study sites which enabled the photographs to be collected. The study conformed with the Australian code for the care and use of animals for scientific purposes.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2019_2745_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 25 kb)

References

  1. Anderson SD, Chapple TK, Jorgensen SJ, Klimley AP, Block BA (2011) Long-term individual identification and site fidelity of white sharks, Carcharodon carcharias, off California using dorsal fins. Mar Biol 158:1233–1237PubMedPubMedCentralGoogle Scholar
  2. Aplin LM, Farine DR, Morand-Ferron J, Cockburn A, Thornton A, Sheldon BC (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538–541PubMedGoogle Scholar
  3. Armansin N, Lee K, Huveneers C, Harcourt R (2016) Integrating social network analysis and fine-scale positioning to characterize the associations of a benthic shark. Anim Behav 115:245–258Google Scholar
  4. Atton N, Galef B, Hoppitt W, Webster M, Laland K (2014) Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals. Proc R Soc B 281:20140579PubMedGoogle Scholar
  5. Baylis AM, Page B, Peters K, McIntosh R, McKenzie J, Goldsworthy S (2005) The ontogeny of diving behaviour in New Zealand fur seal pups (Arctocephalus forsteri). Can J Zool 83:1149–1161Google Scholar
  6. Bejder L, Fletcher D, Bräger S (1998) A method for testing association patterns of social animals. Anim Behav 56:719–725PubMedGoogle Scholar
  7. Bezanson M, Garber PA, Murphy JT, Premo LS (2008) Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata). Am J Primatol 70:282–293PubMedGoogle Scholar
  8. Brena PF, Mourier J, Planes S, Clua EE (2018) Concede or clash? Solitary sharks competing for food assess rivals to decide. Proc R Soc B 285:20180006PubMedGoogle Scholar
  9. Bruce BD, Bradford RW (2013) The effects of shark cage-diving operations on the behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia. Mar Biol 160:889–907Google Scholar
  10. Bruce B, Bradford R (2015) Segregation or aggregation? Sex-specific patterns in the seasonal occurrence of white sharks Carcharodon carcharias at the Neptune Islands, South Australia. J Fish Biol 87:1355–1370PubMedGoogle Scholar
  11. Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469Google Scholar
  12. Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date, vol. 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, ItalyGoogle Scholar
  13. Couzin ID, Krause J, Franks NR, Levin SA (2005) Effective leadership and decision-making in animal groups on the move. Nature 433:513–516Google Scholar
  14. Croft D, Arrowsmith B, Webster M, Krause J (2004) Intra-sexual preferences for familiar fish in male guppies. J Fish Biol 64:279–283Google Scholar
  15. Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, PrincetonGoogle Scholar
  16. Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507PubMedGoogle Scholar
  17. Cross PC, Lloyd-Smith JO, Bowers JA, Hay CT, Hofmeyr M, Getz WM (2004) Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffalo in the Kruger National Park. Ann Zool Fenn 41:879–892Google Scholar
  18. Csárdi G, Nepusz T (2006) The igraph software package for complex network. Int J Complex Syst 1695:1–9Google Scholar
  19. Domeier ML (2012) Global perspectives on the biology and life history of the white shark. CRC Press, Boca RatonGoogle Scholar
  20. Domeier M, Nasby-Lucas N (2007) Annual re-sightings of photographically identitifed white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Mar Biol 150:977–984Google Scholar
  21. Duffy C, Francis MP, Manning MJ, Bonfil R (2012) Regional population connectivity, oceanic habitat, and return migration revealed by satellite tagging of white sharks, Carcharodon carcharias, at New Zealand aggregation sites. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca RatonGoogle Scholar
  22. Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol Evol 4:1187–1194Google Scholar
  23. Farine DR (2014) Measuring phenotypic assortment in animal social networks: weighted associations are more robust than binary edges. Anim Behav 89:141–153Google Scholar
  24. Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320PubMedPubMedCentralGoogle Scholar
  25. Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163PubMedPubMedCentralGoogle Scholar
  26. Fewell JH (2003) Social insect networks. Science 301:1867–1870PubMedGoogle Scholar
  27. Findlay R, Gennari E, Cantor M, Tittensor D (2016) How solitary are white sharks: social interactions or just spatial proximity? Behav Ecol Sociobiol 70:1735–1744Google Scholar
  28. Finger J, Dhellemmes F, Guttridge T (2017) Personality in elasmobranchs with a focus on sharks: early evidence, challenges, and future directions. In: Vonk J, Weiss A, Kuczaj SA (eds) Personality in nonhuman animals. Springer, Berlin, pp 129–152Google Scholar
  29. Franks DW, Ruxton GD, James R (2010) Sampling animal association networks with the gambit of the group. Behav Ecol Sociobiol 64:493–503Google Scholar
  30. Godfrey SS, Bull CM, James R, Murray K (2009) Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav Ecol Sociobiol 63:1045–1056Google Scholar
  31. Goldman KJ, Anderson SD (1999) Space utilization and swimming depth of white sharks, Carcharodon carcharias, at the South Farallon Islands, central California. Environ Biol Fish 56:351–364Google Scholar
  32. Goldsworthy SD (2006) Maternal strategies of the New Zealand fur seal: evidence for interannual variability in provisioning and pup growth strategies. Aust J Zool 54:31–44Google Scholar
  33. Gubili C, Johnson R, Gennari E, Oosthuizen WH, Kotze D, Meyer M, Sims DW, Jones CS, Noble LR (2009) Concordance of genetic and fin photo-identification in the great white shark, Carcharodon carcharias, off Mossel Bay, South Africa. Mar Biol 156:2199–2207Google Scholar
  34. Guttal V, Couzin ID (2010) Social interactions, information use, and the evolution of collective migration. Proc Natl Acad Sci U S A 107:16172–16177PubMedPubMedCentralGoogle Scholar
  35. Guttridge TL, Gruber SH, Krause J, Sims DW (2010) Novel acoustic technology for studying free-ranging shark social behaviour by recording individuals’ interactions. PLoS One 5:e9324PubMedPubMedCentralGoogle Scholar
  36. Guttridge TL, Gruber SH, DiBattista JD, Feldheim KA, Croft DP, Krause S, Krause J (2011) Assortative interactions and leadership in a free-ranging population of juvenile lemon shark Negaprion brevirostris. Mar Ecol Prog Ser 423:235–245Google Scholar
  37. Hay D, McKinnell S (2002) Tagging along: association among individual Pacific herring (Clupea pallasi) revealed by tagging. Can J Fish Aquat Sci 59:1960–1968Google Scholar
  38. Hewitt AM, Kock AA, Booth AJ, Griffiths CL (2018) Trends in sightings and population structure of white sharks, Carcharodon carcharias, at Seal Island, False Bay, South Africa, and the emigration of subadult female sharks approaching maturity. Environ Biol Fish 101:39–54Google Scholar
  39. Höjesjö J, Johnsson JI, Petersson E, Järvi T (1998) The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta). Behav Ecol 9:445–451Google Scholar
  40. Huveneers C, Lloyd M (2017) Residency of white sharks, Carcharodon carcharias, at the Neptune Islands Group Marine Park (2016–17). Flinders University, AdelaideGoogle Scholar
  41. Huveneers C, Rogers PJ, Beckmann C, Semmens J, Bruce B, Seuront L (2013) The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks. Mar Biol 160:2863–2875Google Scholar
  42. Huveneers C, Holman D, Robbins R, Fox A, Endler JA, Taylor AH (2015) White sharks exploit the sun during predatory approaches. Am Nat 185:562–570PubMedGoogle Scholar
  43. Huveneers C, Meekan MG, Apps K, Ferreira LC, Pannell D, Vianna GM (2017) The economic value of shark-diving tourism in Australia. Rev Fish Biol Fish 27:665–680Google Scholar
  44. Jacoby DM, Freeman R (2016) Emerging network-based tools in movement ecology. Trends Ecol Evol 31:301–314PubMedGoogle Scholar
  45. Jacoby DM, Brooks EJ, Croft DP, Sims DW (2012) Developing a deeper understanding of animal movements and spatial dynamics through novel application of network analyses. Methods Ecol Evol 3:574–583Google Scholar
  46. Jacoby DM, Fear LN, Sims DW, Croft DP (2014) Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behav Ecol Sociobiol 68:1995–2003Google Scholar
  47. Jacoby DM, Papastamatiou YP, Freeman R (2016) Inferring animal social networks and leadership: applications for passive monitoring arrays. J R Soc Interface 13:20160676PubMedPubMedCentralGoogle Scholar
  48. Johnson DD, Kays R, Blackwell PG, Macdonald DW (2002) Does the resource dispersion hypothesis explain group living? Trends Ecol Evol 17:563–570Google Scholar
  49. Keller BA, Finger J-S, Gruber SH, Abel DC, Guttridge TL (2017) The effects of familiarity on the social interactions of juvenile lemon sharks, Negaprion brevirostris. J Exp Mar Biol Ecol 489:24–31Google Scholar
  50. Klimley AP, Ainley DG (1996) Great white sharks: the biology of Carcharodon carcharias. Academic Press, LondonGoogle Scholar
  51. Klimley A, Le Boeuf B, Cantara K, Richert J, Davis S, Van Sommerman S (2001) Radio acoustic positioning as a tool for studying site-specific behavior of the white shark and other large marine species. Mar Biol 138:429–446Google Scholar
  52. Kock A, O’Riain MJ, Mauff KM, Kotze D, Griffiths C (2013) Residency, habitat use and sexual segregation of white sharks, Carcharodon carcharias in False Bay, South Africa. PLoS One 8:e55048PubMedPubMedCentralGoogle Scholar
  53. Komdeur J (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358:493–495Google Scholar
  54. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  55. Krause J, Croft D, James R (2007) Social network theory in the behavioural sciences: potential applications. Behav Ecol Sociobiol 62:15–27Google Scholar
  56. Laroche KR, Kock AA, Dill LM, Oosthuizen H (2007) Effects of provisioning ecotourism activity on the behaviour of white sharks Carcharodon carcharias. Mar Ecol Prog Ser 338:199–209Google Scholar
  57. Lavoie D, Simard Y, Saucier FJ (2000) Aggregation and dispersion of krill at channel heads and shelf edges: the dynamics in the Saguenay-St. Lawrence Marine Park. Can J Fish Aquat Sci 57:1853–1869Google Scholar
  58. Leu ST, Godfrey SS (2018) Advances from the nexus of animal behaviour and pathogen transmission: new directions and opportunities using contact networks. Behaviour 155:567–583Google Scholar
  59. Leu ST, Farine DR, Wey TW, Sih A, Bull CM (2016) Environment modulates population social structure: experimental evidence from replicated social networks of wild lizards. Anim Behav 111:23–31Google Scholar
  60. Lusseau D, Wilson B, Hammond PS, Grellier K, Durban JW, Parsons KM, Barton TR, Thompson PM (2006) Quantifying the influence of sociality on population structure in bottlenose dolphins. J Anim Ecol 75:14–24PubMedGoogle Scholar
  61. Mackas DL, Louttit GC (1988) Aggregation of the copepod Neocalanus plumchrus at the margin of the Fraser River plume in the Strait of Georgia. Bull Mar Sci 43:810–824Google Scholar
  62. Marshall AD, Pierce SJ (2012) The use and abuse of photographic identification in sharks and rays. J Fish Biol 80:1361–1379PubMedGoogle Scholar
  63. Marshall AD, Dudgeon CL, Bennett M (2011) Size and structure of a photographically identified population of manta rays Manta alfredi in southern Mozambique. Mar Biol 158:1111–1124Google Scholar
  64. Martin RA (2007) A review of shark agonistic displays: comparison of display features and implications for shark-human interactions. Mar Freshw Behav Physiol 40:3–34Google Scholar
  65. Martin RA, Hammerschlag N, Collier RS, Fallows C (2005) Predatory behaviour of white sharks (Carcharodon carcharias) at Seal Island, South Africa. J Mar Biol Assoc UK 85:1121–1135Google Scholar
  66. Milinski M (1987) Tit for tat in sticklebacks and the evolution of cooperation. Nature 325:433–435PubMedGoogle Scholar
  67. Möller LM, Beheregaray L, Allen SJ, Harcourt R (2006) Association patterns and kinship in female indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Behav Ecol Sociobiol 61:109–117Google Scholar
  68. Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Anim Behav 83:389–401Google Scholar
  69. Nasby-Lucas N, Domeier ML (2012) Use of photo identification to describe a white shark aggregation at Guadalupe Island, Mexico. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 381–392Google Scholar
  70. Nazimi L, Robbins WD, Schilds A, Huveneers C (2018) Comparison of industry-based data to monitor white shark cage-dive tourism. Tour Manag 66:263–273Google Scholar
  71. Newman ME (2004) Analysis of weighted networks. Phys Rev E70:056131Google Scholar
  72. Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577–8582PubMedPubMedCentralGoogle Scholar
  73. Papastamatiou YP, Bodey T, Friedlander A, Lowe C, Bradley D, Weng K, Priestley V, Caselle J (2018) Spatial separation without territoriality in shark communities. Oikos 127:767–779Google Scholar
  74. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
  75. Robbins RL (2007) Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia. J Fish Biol 70:1350–1364Google Scholar
  76. Robbins R, Fox A (2013) Further evidence of pigmentation change in white sharks, Carcharodon carcharias. Mar Freshw Res 63:1215–1217Google Scholar
  77. Rogers P, Huveneers C (2016) Residency and photographic identification of white sharks Carcharodon carcharias in the Neptune Islands Group Marine Park between 2013 and 2015. SARDI publication no. F2015/000825-1. SARDI research report series no. 893. South Australian Research and Development Institute (aquatic sciences), Adelaide, South AustraliaGoogle Scholar
  78. Ryklief R, Pistorius P, Johnson R (2014) Spatial and seasonal patterns in sighting rate and life-history composition of the white shark Carcharodon carcharias at Mossel Bay, South Africa. Afr J Mar Sci 36:449–453Google Scholar
  79. Sah P, Leu ST, Cross PC, Hudson PJ, Bansal S (2017) Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proc Natl Acad Sci U S A 201613616Google Scholar
  80. Semmens J, Payne N, Huveneers C, Sims DW, Bruce B (2013) Feeding requirements of white sharks may be higher than originally thought. Sci Rep 3:1471PubMedPubMedCentralGoogle Scholar
  81. Sperone E, Micarelli P, Andreotti S, Spinetti S, Andreani A, Serena F, Brunelli E, Tripepi S (2010) Social interactions among bait-attracted white sharks at Dyer Island (South Africa). Mar Biol Res 6:408–414Google Scholar
  82. Skomal, GB, Chisholm J, Correia SJ (2012) Implications of increasing pinniped populations on the diet and abundance of white sharks off the coast of Massachusetts. In: DomeierML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 405–418Google Scholar
  83. Sperone E, Micarelli P, Andreotti S, Brandmayr P, Bernabò I, Brunelli E, Tripepi S (2012) Surface behaviour of bait-attracted white sharks at Dyer Island (South Africa). Mar Biol Res 8:982–991Google Scholar
  84. Towner AV, Wcisel MA, Reisinger RR, Edwards D, Jewell OJ (2013) Gauging the threat: the first population estimate for white sharks in South Africa using photo identification and automated software. PLoS One 8:e66035PubMedPubMedCentralGoogle Scholar
  85. Weng KC, Boustany AM, Pyle P, Anderson SD, Brown A, Block BA (2007) Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Mar Biol 152:877–894Google Scholar
  86. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, ChicagoGoogle Scholar
  87. Wilson AD, Brownscombe JW, Krause J, Krause S, Gutowsky LF, Brooks EJ, Cooke SJ (2015) Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior. Behav Ecol 26:1577–1586Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Science and EngineeringFlinders UniversityBedford ParkAustralia
  2. 2.UMR MARBEC (IRD, Ifremer Univ. Montpellier, CNRS)SèteFrance
  3. 3.Fox Shark Research FoundationAdelaideAustralia
  4. 4.Department of Biological SciencesMacquarie UniversityNorth RydeAustralia

Personalised recommendations