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Exploring elasmobranch cognition using juvenile Port Jackson sharks

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posted on 28.03.2022, 13:02 authored by Catarina Vila Pouca
Learning plays a vital role in the behavioural development of all animals. Fish are not an exception, and teleosts have become a typical model in the study of animal cognition and behaviour. Among elasmobranchs, however, research in this field is very scarce. As one of the oldest extant jawed vertebrates, elasmobranchs hold a key phylogenetic position to understanding the evolutionary origins of the vertebrate cognitive toolbox. In addition, elasmobranchs have a wide range of life-history traits and occupy very diverse ecological niches, providing good models for an ecological or functional approach to cognition. This is especially relevant in an era where rapid climatic change is affecting the physiology, behaviour, and cognitive skills of many species. Despite an upsurge of cognitive research in elasmobranchs over the last decade, the number of species and cognitive abilities assessed are still hardly representative of the group, and the effects of near-future ocean warming on elasmobranch learning ability have not been assessed. In this thesis, I used juvenile Port Jackson sharks, Heterodontus portusjacksoni, as a model species to address some of these gaps in elasmobranch cognitive research, exploring three research areas that have been little investigated - sound discrimination learning, social cognition, and numerical competency. I also evaluated the effect of incubation under climate warming in behavioural lateralisation and numerical learning skills, and tested for a mechanistic link between individual personality and/or laterality traits and cognitive ability in each of the three areas. The marine environment is filled with biotic and abiotic sounds. Some of these sounds predict important events that influence fitness while others are unimportant. Animals can learn specific sound cues and use them for vital activities such as foraging, predator avoidance, and orientation. Chapter I investigated whether Port Jackson sharks could learn to associate a sound stimulus with a food reward, and discriminate between two distinct sound stimuli. I found that some sharks learned to associate a sound stimulus with a food reward. None were successful in discriminating between two sound cues and all developed strong side biases. Individual differences in activity and boldness were not linked to the learning performance assays we examined. Sociality is a widespread phenomenon across multiple taxa, including elasmobranchs. However, species and populations vary in their degree of sociality depending on the trade-off between fitness benefits and costs of living in a group. While adult Port Jackson sharks are known to form large social groups during the breeding season, very little is known about juveniles. Chapter II investigated sociality in captive-reared juvenile Port Jackson sharks, by testing their preference to associate with other sharks in a controlled laboratory binary choice experiment. I found that sharks did not actively choose to associate with one or three conspecifics, and that sex, size, swimming activity, or foraging motivation had no effect on the results. This suggests that sociality in Port Jackson sharks is not stable during ontogeny, and that predation pressure might not play an important role in shaping the social behaviour of juveniles, unlike other shark species. Animals often share similar needs and challenges with other individuals, such as finding food, the best habitat, or suitable mates. The ability to learn from another animal can, therefore, be beneficial as it can save them the costs of learning by trialand-error. This should apply equally to social and non-social individuals, as all animals are regularly exposed to other individuals, conspecifics or heterospecifics. Chapter III investigated social information use and social learning in juvenile Port Jackson sharks. Naïve 'observer' sharks observed and interacted with either 'demonstrator' sharks, trained to gain access to food through one of two arbitrary routes, or 'sham demonstrators', with no previous experience in the task. After 10 days of social exposure, observer sharks were tested in isolation. I found that a similar proportion of observer sharks from the demonstrator group and the sham demonstrator group learnt the task, and took approximately the same number of days to reach learning criterion, suggesting that social facilitation enhanced learning abilities in both group conditions. Only a small proportion of sharks in both groups performed well when tested without demonstration, suggesting release from conformity to the demonstrator's behaviour. The training intensity and quality of demonstration also influenced learning ability, while behavioural traits and laterality were not linked to any performance measurements. As many other elasmobranch species, Port Jackson sharks are oviparous and have a very long incubation period. Together with multiple other factors, these two life history traits render them vulnerable to the changing climatic conditions we currently face, such as rising sea water temperatures. With the known effects on development and physiology, is it anticipated that behavioural and cognitive abilities might also be hampered by climate warming. Chapter IV examined the effect of elevated incubation temperature in behavioural lateralisation. I found that hatchlings reared at forecasted end-of-century temperature showed stronger absolute laterality and a rightward bias compared to sharks reared in current conditions, suggesting elevated temperature altered brain development. The capacity to make relative quantity judgements is one among the many learning abilities animals evolved to deal with the ecological and social challenges they face. This ability has been extensively studied in all vertebrate groups except elasmobranchs. Chapter V investigated if Port Jackson sharks can discriminate between two quantities, and tested the effect of incubation temperature and laterality levels in learning ability. Here I show, for the first time, that sharks can discriminate between two quantities, and found that individuals incubated at elevated temperature performed better compared to sharks incubated at current conditions. I found some indication that individuals with stronger rightward bias reached learning criterion faster, yet further research is required in this topic. The findings of Chapters IV and V provide further evidence that elasmobranchs are susceptible to the effects of future ocean warming. Our results suggest that behavioural mechanisms might allow animals to adjust and/or counter some of the changes imposed by climate warming, potentially bringing beneficial effects to the individuals that are able to survive. In summary, this thesis extends the known cognitive abilities of elasmobranchs to research areas poorly, or never, addressed in the group and provides additional experimental support to the view that elasmobranchs share most of the cognitive toolbox of teleosts and other vertebrates.

History

Table of Contents

Introduction -- 1. Food approach conditioning and discrimination learning using sound cues in benthic sharks -- 2. Lack of social preference in juvenile sharks -- 3. Social facilitation of foraging behaviour in non-social juvenile sharks -- 4. Incubation under climate warming affects behavioural lateralisation in Port Jackson sharks -- 5. Quantity discrimination in sharks incubated under climate warming -- Appendices.

Notes

Theoretical thesis. Thesis by publication. Includes bibliographical references

Awarding Institution

Macquarie University

Degree Type

Thesis PhD

Degree

PhD, Macquarie University, Faculty of Science and Engineering, Department of Biology

Department, Centre or School

Department of Biology

Year of Award

2018

Principal Supervisor

Culum Brown

Rights

Copyright Catarina Vila Pouca 2018. Copyright disclaimer: http://mq.edu.au/library/copyright

Language

English

Extent

1 online resource (xv, 175 pages : illustrations)

Former Identifiers

mq:72004 http://hdl.handle.net/1959.14/1280444