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Social learning in juvenile lemon sharks, Negaprion brevirostris

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Abstract

Social learning is taxonomically widespread and can provide distinct behavioural advantages, such as in finding food or avoiding predators more efficiently. Although extensively studied in bony fishes, no such empirical evidence exists for cartilaginous fishes. Our aim in this study was to experimentally investigate the social learning capabilities of juvenile lemon sharks, Negaprion brevirostris. We designed a novel food task, where sharks were required to enter a start zone and subsequently make physical contact with a target in order to receive a food reward. Naive sharks were then able to interact with and observe (a) pre-trained sharks, that is, ‘demonstrators’, or (b) sharks with no previous experience, that is, ‘sham demonstrators’. On completion, observer sharks were then isolated and tested individually in a similar task. During the exposure phase observers paired with ‘demonstrator’ sharks performed a greater number of task-related behaviours and made significantly more transitions from the start zone to the target, than observers paired with ‘sham demonstrators’. When tested in isolation, observers previously paired with ‘demonstrator’ sharks completed a greater number of trials and made contact with the target significantly more often than observers previously paired with ‘sham demonstrators’. Such experience also tended to result in faster overall task performance. These results indicate that juvenile lemon sharks, like numerous other animals, are capable of using socially derived information to learn about novel features in their environment. The results likely have important implications for behavioural processes, ecotourism and fisheries.

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References

  • Bonfil R, Meyer M, Scholl MC et al (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Sci 310:100–103

    Article  CAS  Google Scholar 

  • Bres M (1993) The behavior of sharks. Rev Fish Biol Fish 3:133–159

    Article  Google Scholar 

  • Brown C, Day R (2002) The future of stock enhancements: lessons for hatchery practice from conservation biology. Fish Fish 3:79–94

    Article  Google Scholar 

  • Brown C, Laland KN (2001) Social learning and life skills training for hatchery reared fish. J Fish Biol 59:471–493

    Article  Google Scholar 

  • Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288

    Article  Google Scholar 

  • Brown C, Laland KN (2011) Social learning in fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Fish and aquatic resources series. Blackwell Publishers, Cambridge. doi:10.1002/9781444342536.ch11

  • Bushnell P, Lutz P, Gruber SH (1989) Metabolic rate of an active tropical elasmobranch, the lemon shark Negaprion brevirostris. Exptl Biol 48(5):279–284

    CAS  Google Scholar 

  • Clark E (1959) Instrumental conditioning of lemon sharks. Science 130:217–218

    Article  PubMed  CAS  Google Scholar 

  • Compagno LJV (1984) FAO species catalogue. Sharks of the world: an annotated and illustrated catalogue of shark species known to date. II. Carcharhiniformes. FAO Fisheries Synopsis, Rome, Italy

  • DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008) Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795

    Article  PubMed  Google Scholar 

  • Economakis AE, Lobel PS (1998) Aggregation behaviour of the grey reef shark, Carcharhinus amblyrhychos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fish 51:129–139

    Article  Google Scholar 

  • Fernö A, Huse G, Jakobsen PJ, Kristiansen TS, Nilsson J (2011) Fish behaviour, learning, aquaculture and fisheries. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Fish and aquatic resources series. Blackwell Publishers, Cambridge. doi:10.1002/9781444342536.ch16

  • Gruber SH (1982) Role of the lemon shark, Negaprion brevirostris (Poey), as a predator in the tropical marine environment: a multidisciplinary study. Fl Sci 45:46–75

    Google Scholar 

  • Gruber SH, Schneiderman N (1975) Classical conditioning of nictitating membrane response of lemon sharks (Negaprion brevirostris). Behav Res Meth Instru 7:430–434

    Article  Google Scholar 

  • Guttridge TL, Gruber SH, Gledhill KS, Croft DP, Sims DW, Krause J (2009a) Social preferences of juvenile lemon sharks, Negaprion brevirostris. Anim Behav 78:543–548

    Article  Google Scholar 

  • Guttridge TL, Myrberg AA, Porcher IF, Sims DW, Krause J (2009b) The role of learning in shark behaviour. Fish Fish 10:450–469

    Article  Google Scholar 

  • Guttridge TL, Gruber SH, DiBattista JD, Feldheim KA et al (2011) Assortative interactions and leadership in a wild population of juvenile lemon sharks. Mar Eco-Prog Ser 423:235–245

    Article  Google Scholar 

  • Helfman GS, Schultz ET (1984) Social tradition of behavioural traditions in a coral reef fish. Anim Behav 32:379–384

    Article  Google Scholar 

  • Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231

    Article  PubMed  CAS  Google Scholar 

  • Hoppitt W, Laland KN (2008) Social processes influencing learning in animals: a review of the evidence. Adv Study Behav 38:105–165

    Article  Google Scholar 

  • Jacoby DMP, Busawon DS, Sims DW (2010) Sex and social networking: the influence of male presence on social structure of female shark groups. Behav Ecol 21:808–818

    Article  Google Scholar 

  • Jacoby DMP, Croft DP, Sims DW (2011) Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish Fish. doi:10.1111/j.14672979.2011.00436.x

  • Kessel ST (2010) An investigation into the behaviour and population dynamics of the lemon shark (Negaprion brevirostris). PhD thesis, Cardiff University, UK

  • Klimley AP, Nelson DR (1981) Schooling of the Scalloped Hammerhead Shark, Sphyrna-lewini, in the Gulf of California. Fish Bull 79:356–360

    Google Scholar 

  • Klimley AP, Le Boeuf BJ, Cantara KM, Richert JE, Davis SF, Sommeran SV, Kelly JT (2001) The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Mar Biol 138:617–636

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford series in ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Laland KN, Atton N, Webster MM (2011) From fish to fashion: experimental and theoretical insights into the evolution of culture. Phil Trans R Soc B 366:958–968. doi:10.1098/rstb.2010.0328

    Article  PubMed  CAS  Google Scholar 

  • Leadbeater E, Chittka L (2007) The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris). Behav Ecol Sociobiol 61:1789–1796

    Article  Google Scholar 

  • Mineka S, Cook M (1988) Social learning and the acquisition of snake fear in monkeys. In: Zentall TR, Galef BF (eds) Social learning: psychological and biological perspectives. Lawrence Erlbaum Associates, New Jersey, pp 51–74

    Google Scholar 

  • Myrberg AA, Gruber SH (1974) The behavior of the bonnethead shark, Sphyrna tiburo. Copeia 1974:358–374

    Article  Google Scholar 

  • Myrberg AA, Banner A, Richard JD (1969) Shark attraction using a video-acoustic system. Mar Biol 2:264–276

    Google Scholar 

  • Nelson DR, Johnson RH (1980) Behavior of reef sharks of Rangiroa, French Polynesia. Nat Geo Soc Res Rep 12:479–499

    Google Scholar 

  • Nixon A, Gruber SH (1988) Diel metabolic and activity patterns of the lemon shark (Negaprion brevirostris). J Exptl Zool 248(1):1–6

    Article  Google Scholar 

  • Noldus IT (2007) The Observer XT. Information Technology

  • O’Connell CP, Abel DC, Stroud EM, Rice PH (2011) Analysis of permanent magnets as elasmobranch by catch reduction devices in hook-and-line and longline trials. Fish Bull 109:394–401

    Google Scholar 

  • Powter DM, Gladstone W (2009) Habitat-mediated use of space by juvenile and mating adult port jackson sharks, Heterodontus portusjacksoni, in Eastern Australia. Pac Sci 63:1–14

    Article  Google Scholar 

  • Robbins WD, Peddemors VM, Kennelly SJ (2011) Assessment of permanent magnets and electropositive metals to reduce the line-based capture of Galapagos sharks, Carcharhinus galapagensis. Fish Res 109:100–106

    Article  Google Scholar 

  • Ryer CH, Olla BL (1992) Social mechanisms facilitating exploitation of spatially variable ephemeral food patches in a pelagic marine fish. Anim Behav 44:69–74

    Article  Google Scholar 

  • Speed CW, Field IC, Meekan MG, Bradshaw CJA (2010) Complexities of coastal shark movements and their implications for management. Mar Ecol Prog Ser 408:275–293

    Google Scholar 

  • Springer S (1967) Social organization of shark populations. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. John Hopkins Press, Baltimore, pp 149–174

    Google Scholar 

  • Vilhunen S (2006) Repeated anti-predator conditioning: a pathway to habituation or to better avoidance? J Fish Biol 68:25–43

    Article  Google Scholar 

  • Wetherbee BM, Gruber SH, Rosa RS (2007) Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes. Mar Ecol Prog Ser 343:283–293

    Article  Google Scholar 

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Acknowledgments

T.L.G. was supported by a Leverhulme Study Abroad Studentship. S.VD was supported by grants from the Marco Polo Fund and the Groningen University Fund. We thank the volunteers and staff at the Bimini Biological Field Station for their contribution. We also thank the Department of Animal Behaviour of the University of Groningen for use of their ‘Observer XT’ behavioural analysis software. The study was financially supported by the Bimini Biological Field Station, Lacy Hoover, Earthwatch Institute, National Science Foundation (NSF-OCE 97-12793), NERC (NE/D011035/1) and Department of Education, State of Florida (FLORIDA 8749703000001). This research was carried out under a permit from Michael Braynen, Department of Fisheries of the Commonwealth of the Bahamas. We also thank anonymous reviewers for their helpful comments that improved our MS.

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Correspondence to Tristan L. Guttridge.

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Guttridge, T.L., van Dijk, S., Stamhuis, E.J. et al. Social learning in juvenile lemon sharks, Negaprion brevirostris . Anim Cogn 16, 55–64 (2013). https://doi.org/10.1007/s10071-012-0550-6

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  • DOI: https://doi.org/10.1007/s10071-012-0550-6

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