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Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark

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Abstract

Top predators inhabiting a dynamic environment, such as coastal waters, should theoretically possess sufficient cognitive ability to allow successful foraging despite unpredictable sensory stimuli. The cognition-related hunting abilities of marine mammals have been widely demonstrated. Having been historically underestimated, teleost cognitive abilities have also now been significantly demonstrated. Conversely, the abilities of elasmobranchs have received little attention, despite many species possessing relatively large brains comparable to some mammals. The need to determine what, if any, cognitive ability these globally distributed, apex predators are endowed with has been highlighted recently by questions arising from environmental assessments, specifically whether they are able to learn to distinguish between anthropogenic electric fields and prey bioelectric fields. We therefore used electroreceptive foraging behaviour in a model species, Scyliorhinus canicula (small-spotted catshark), to determine cognitive ability by analysing whether elasmobranchs are able to learn to improve foraging efficiency and remember learned behavioural adaptations. Positive reinforcement, operant conditioning was used to study catshark foraging behaviour towards artificial, prey-type electric fields (Efields). Catsharks rewarded with food for responding to Efields throughout experimental weeks were compared with catsharks that were not rewarded for responding in order to assess behavioural adaptation via learning ability. Experiments were repeated after a 3-week interval with previously rewarded catsharks this time receiving no reward and vice versa to assess memory ability. Positive reinforcement markedly and rapidly altered catshark foraging behaviour. Rewarded catsharks exhibited significantly more interest in the electrical stimulus than unrewarded catsharks. Furthermore, they improved their foraging efficiency over time by learning to locate and bite the electrodes to gain food more quickly. In contrast, unrewarded catsharks showed some habituation, whereby their responses to the electrodes abated and eventually entirely ceased, though they generally showed no changes in most foraging parameters. Behavioural adaptations were not retained after the interval suggesting learned behaviour was not memorised beyond the interval. Sequences of individual catshark search paths clearly illustrated learning and habituation behavioural adaptation. This study demonstrated learning and habituation occurring after few foraging events and a memory window of between 12 h and 3 weeks. These cognitive abilities are discussed in relation to diet, habitat, ecology and anthropogenic Efield sources.

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Acknowledgments

We thank J. Rundle for animal husbandry, K. Atkins for technical assistance, J. Mavin for help designing and constructing trap-door mechanism, I. Truckell for scanning assistance, B. Clutterbuck for assistance with ArcGIS, P. Rendle, P. Masterson, M. McHugh, J. Filer, V. Wearmouth, and the crew of R. V. Plymouth Quest for assistance with specimen collection. We also thank the anonymous reviewers for their comments. JAK was supported by a Fisheries Society of the British Isles funded studentship and by Cranfield University. DWS was supported by a Natural Environment Research Council (NERC) funded Marine Biological Association (MBA) Fellowship and by the NERC Oceans 2025 Strategic Research Programme (Theme 6 Science for Sustainable Marine Resources).

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Authors and Affiliations

  1. Department of Environmental Science and Technology, Cranfield University, Cranfield, Bedfordshire, MK43 0AL, UK

    Joel A. Kimber, Patricia H. Bellamy & Andrew B. Gill

  2. Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon, PL1 2PB, UK

    Joel A. Kimber & David W. Sims

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  1. Joel A. Kimber
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Correspondence to Joel A. Kimber.

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Kimber, J.A., Sims, D.W., Bellamy, P.H. et al. Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Anim Cogn 17, 55–65 (2014). https://doi.org/10.1007/s10071-013-0637-8

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