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Nicola Atton Phd Thesis INVESTIGATIONS INTO STICKLEBACK SOCIAL LEARNING Nicola Atton A Thesis Submitted for the Degree of PhD at the University of St Andrews 2014 Full metadata for this item is available in Research@StAndrews:FullText at: http://research-repository.st-andrews.ac.uk/ Please use this identifier to cite or link to this item: http://hdl.handle.net/10023/6610 This item is protected by original copyright Investigations into Stickleback Social Learning Nicola Atton Thesis submitted to the School of Biology of the University of St. Andrews for the degree of Doctor of Philosophy October 2013 Acknowledgements I would like to acknowledge a number of people who have helped make this thesis possible. Mike Webster in particular has played an integral part. He helped me design and setup all experiments presented here. He spent many hours with me catching sticklebacks in the Kinnesburn, often in truly despicable weather. He has also provided very helpful advice with regards to data analysis and proof read every chapter. Will Hoppitt has also been of great assistance. He designed and implemented the version of NBDA used in chapters 6 and 7 and was a great help in writing the methods and results sections of those chapters with regards to the data analysis. My two supervisors, Kevin Laland and Jeff Galef, have provided valuable insight and advice for this thesis in its entirety. I would also like to thank my friends and colleagues in the Laland lab, in particular Laurel Fogarty, Alice Cowie, Tom Morgan, and Lewis Dean for providing the necessary commiseration and camaraderie when experiments inevitably ‘went wrong’. Finally I would like to thank my husband Drew for all his support over the years. Without his persistent nagging, I likely never would have gotten it finished. Abstract The objective of the experiments contained within this thesis was to provide further insight into the social learning capabilities of threespined sticklebacks and the factors affecting the transmission of information through populations. There are a number of previous studies which provide evidence that both threespined and ninespined sticklebacks possess the ability to learn socially under a range of contexts, such as foraging, anti-predator behaviour, mate choice, and cooperation. The studies presented in this thesis aim to extend this knowledge and shed light on the social learning processes used. Evidence was found to support previous opinion that threespined sticklebacks are capable of using a number of social learning processes, including local enhancement, stimulus enhancement, and the social enhancement of food preferences. However, there was no evidence to suggest that either threespined or ninespined sticklebacks are capable of using the social learning process of delayed local enhancement under a shelter choice context, a process which both species have previously been shown to use under a foraging context. This thesis also explores the effect of the social network within shoals of threespined sticklebacks upon the transmission of novel foraging information. It was discovered that both prior association preferences and prior diet have an effect on the order in which individuals discover a novel foraging task. Contents Chapter 1. An introduction to social learning 1 1.1 The importance of social learning 1 1.2 What is animal social learning? 2 1.2.1 Learning theory 2 1.2.1.1 Associative learning 3 1.2.1.2 Single stimulus learning 4 1.2.2 Social learning definitions and processes 4 1.1.2.1Imitation 4 1.1.2.2 Goal emulation 6 1.1.2.3. Observational conditioning 6 1.1.2.4 Local enhancement and stimulus enhancement 7 1.1.2.5 Social facilitation 8 1.1.2.6 Response facilitation 8 1.1.2.7Observational R-S learning 9 1.1.2.8 Social enhancement of food preferences 10 1.3 Social learning strategies 10 1.3.1 Empirical evidence for social learning strategies 11 1.3.1.1 “When” strategies 12 1.3.1.1.1 Copy-when-established-behaviour-is-unproductive 12 1.3.1.1.2 Copy-when-asocial-learning-is-costly 13 1.3.1.1.3 Copy-when-uncertain 14 1.3.1.2 “Who” strategies 15 1.3.1.2.1 Copy-the-majority 15 1.3.1.2.2 Copy-successful-individuals 16 1.4 Social learning in fish 17 1.4.1 Mate choice copying 19 1.4.2 Migration and orientation 21 1.4.3 Foraging 23 1.4.4 Anti-predator behaviour 23 1.4.5 Aggressive interactions 25 1.5 Broader Comparative perspective 27 1.6 Summary Chapter 2. The threespined stickleback 28 2.1 Phylogeny and natural history 28 2.2 Geographical distribution 29 2.3 Morphology 30 2.4 Ecology 31 2.4.1 Prey 31 2.4.2 Predators 31 2.4.3 Reproduction 31 2.5 Threespined sticklebacks as a model species 32 2.6 Social learning in threespined sticklebacks 33 2.6.1 Foraging 34 2.6.2 Anti-predator behaviour 36 2.6.3 Mate choice 36 2.6.4 Cooperation 38 2.7 Summary 38 Chapter 3. Threespined sticklebacks and ninespined sticklebacks don’t 39 use delayed local enhancement in a shelter choice assay 3.1 Introduction 39 3.2 Methods 45 3.2.1 Subjects and apparatus 45 3.2.2 Procedure 46 3.2.2.1 Demonstration phase 46 3.2.2.2 Test phase 47 3.2.2.3Video playback 47 3.3 Results 48 3.3.1 Demonstration phase 48 3.3.2 Test phase 49 3.2.2.1 Test phase binary choice 50 3.4 Discussion 52 3.5 Summary 56 Chapter 4. The social enhancement of food preferences 57 4.1 Introduction 57 4.2 Methods 63 4.2.1 Design 63 4.2.2 Subjects 64 4.2.3 Apparatus 65 4.2.4 Procedure 66 4.2.4.1 Stage 1 66 4.2.4.2 Stage 2 66 4.2.4.3 Stage 3 66 4.2.4.4 Stage 4 67 4.3 Results 67 4.3.1 Non-stressful to stressful (black to white) 67 4.3.2 Stressful to non-stressful (white to black) 69 4.3.3 Comparisons between treatments 69 4.4 Discussion 70 4.5 Summary 73 Chapter 5. An introduction to social networks 75 5.1 What is a social network? 75 5.2 Why study social networks? 77 5.2.1 Cooperation 78 5.2.2 Disease transmission 78 5.2.3 Social structure and identifying the role of individuals 80 5.3 Temporal networks 83 5.4 Network-based diffusion analysis 84 5.5 Summary 85 Chapter 6. Information flow through threespined stickleback networks 87 without social transmission 6.1 Introduction 87 6.2 Methods 89 6.2.1 Subjects and apparatus 89 6.2.2 Procedure 91 6.2.2.1 Determining the network structure 91 6.2.2.2 Testing for social learning 92 6.2.2.3 Network-based diffusion analysis 93 6.2.2.4 Comparison of network-specific and homogeneous effects 95 6.2.2.5 Social transmission vs an untransmitted social effect 96 6.3 Results 97 6.3.1 Two-task experiment 97 6.3.1.1 First discovery 97 6.3.1.2 First solve 99 6.3.1.3 Comparison of network-specific and homogeneous effects 100 6.3.2 One-task experiment 103 6.3.2.1 First discovery 103 6.3.2.2 First solve 104 6.3.2.3 Comparison of network-specific and homogeneous effects 104 6.4 Discussion 106 6.4.1 Discovery 106 6.4.2 Solution 107 6.4.3 Size effects 108 6.5 Summary 109 Chapter 7. Familiarity affects social network structure and discovery of 110 prey patch locations in foraging stickleback shoals 7.1 Introduction 110 7.2 Methods 113 7.2.1 Subjects and treatment groups 113 7.2.2 Test arena and procedure 114 7.2.3 Testing for effects of familiarity upon association preferences 116 7.2.4 Network-based diffusion analysis 116 7.3 Results 119 7.3.1 Effects of familiarity upon association preferences 119 7.3.2 Network-based diffusion analysis 119 7.3.2.1 First discovery 119 7.3.2.2 Support for effect of different social networks on discovery rate 120 7.3.2.3 Estimates of effects on discovery rate 121 7.3.2.4 Support for effect of different social networks on solving rate 124 7.3.3.5 Estimates of effects on solving rate 124 7.4 Discussion 126 7.5 Summary 129 Chapter 8. General discussion 130 8.1 Overall objective 130 8.2 Social learning processes 130 8.2.1 Social learning processes studied and identified 131 8.2.1.1 Delayed local enhancement 131 8.2.1.2 The social enhancement of food preferences 131 8.2.1.3. Local enhancement 133 8.2.1.4 Stimulus enhancement 134 8.3 Contexts under which social learning is used 134 8.3.1 Contexts studied 135 8.3.1.1 Shelter choice 135 8.3.1.2 Foraging 135 8.4 Impacts of the social network 136 8.5 Future studies 137 8.5.1 Avoidance of maladaptive information transmission 137 8.5.2 Self-referent matching or familiarity? 138 8.5.3 Additional phenotypic factors affecting the discovery of a food 139 source 8.6 Conclusions 140 Appendix 1 141 References 155 Chapter 1. An Introduction to Animal Social Learning In this chapter I shall introduce the reader to the concept and previous literature surrounding the topic of animal social learning. I shall start by discussing the different forms of learning and use these to help understand the process of social learning.
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