(Version 2) Non-Avian Reptile Learning 40 Years On
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1 RUNNING HEAD: Review learning in Reptiles 1 PREPRINT (Version 2) 2 Non-avian reptile learning 40 years on: advances and promising 3 new directions 4 5 Birgit Szaboa*, Daniel W. A. Nobleb, Martin J. Whitinga 6 7 a Department of Biological Sciences, Macquarie University, Sydney, Australia 8 b Division of Ecology and Evolution, Research School of Biology, The Australian National 9 University, Canberra, Australia 10 11 12 13 14 15 *Corresponding author: Birgit Szabo, Department of Biological Sciences, Macquarie 16 University, Marsfield, NSW 2109, Australia; mobile: +61 411 78 60 61; email: 17 [email protected], ORCID: 0000000232268621 18 19 M.J. Whiting ORCID: 0000-0002-4662-0227 20 D.W.A. Noble ORDID: 0000-0001-9460-8743 21 22 Word count: 27,623 2 RUNNING HEAD: Review learning in Reptiles 23Abstract 24Recently, there has been a surge in cognition research using non-avian reptile systems. As 25a diverse group of animals, non-avian reptiles (turtles, the tuatara, crocodilians, and 26squamates - lizards, snakes and amphisbaenids) are good model systems for answering 27questions related to cognitive ecology; from the role of the environment in impacting brain, 28behaviour and learning, to how social and life-history factors correlate with learning ability. 29Furthermore, given their variable social structure and degree of sociality, studies on reptiles 30have demonstrated that group living is not a pre-condition for social learning. Past research 31has undoubtedly demonstrated that non-avian reptiles are capable of more than just 32instinctive reactions and basic cognition. Despite their ability to provide answers to 33fundamental questions in cognitive ecology, and a growing literature base, there have been 34no systematic syntheses of research in this group. Here, we systematically, and 35comprehensively review studies on reptile learning. We identify 92 new studies investigating 36learning in reptiles not included in previous reviews on the same topic – affording a unique 37opportunity to provide a more in-depth synthesis of existing work, its taxonomic distribution, 38the types of cognitive domains tested and methodology that has been used. Our review 39therefore provides a major update on our current state of knowledge and ties the collective 40evidence together under nine umbrella research areas: (1) habituation, (2) conditioning, (3) 41aversion learning, (4) spatial learning, (5) learning during foraging, (6) numerical 42competency, (7) learning flexibility, (8) problem solving, and (9) social learning. Importantly, 43we identify knowledge gaps and propose themes which offer important future research 44opportunities including how cognitive ability might influence fitness and survival, testing 45cognition in ecologically relevant situations, comparing cognition in invasive and non- 46invasive populations of species, and social learning. To move the field forward, it will be 47immensely important to build upon the descriptive approach of testing if a species can learn 48a task with experimental studies elucidating causal reasons for cognitive variation within and 49between species. With the appropriate methodology, this young but rapidly growing field of 3 RUNNING HEAD: Review learning in Reptiles 50research should advance greatly in the coming years providing significant opportunities for 51addressing general questions in cognitive ecology and beyond. 52 53Keywords: Amphisbaenia, Chelonia, Crocodilia, Rhynchocephalia, Squamata, Serpentes, 54Sauria, cognition, integrative review 4 RUNNING HEAD: Review learning in Reptiles 55 Conten 56 PREPRINT (Version 2)...............................................................................................1 57 Non-avian reptile learning 40 years on: advances and promising new directions........1 58 1. Habituation of behaviour.......................................................................................10 59 2. Animal training through operant conditioning........................................................13 60 3. Avoiding aversive stimuli.......................................................................................17 61 4. Spatial learning and memory.................................................................................25 62 5. Learning during foraging.......................................................................................31 63 6. Quality and quantity discrimination........................................................................35 64 7. Responding to change..........................................................................................37 65 8. Solving novel problems.........................................................................................41 66 9. Social learning......................................................................................................42 67 1. The fitness consequences of individual differences in cognition............................47 68 2. Cognition in ecologically relevant contexts............................................................48 69 10. Cognition and behaviour in invasive species.......................................................49 70 11. Social learning in social reptiles..........................................................................50 71 12. Avoidance of harmful invasive prey species........................................................51 72 13. Executive function...............................................................................................52 73 14. Spatial cognition in the context of sexual selection.............................................52 74I. Introduction.................................................................................................................5 75II. Systematic Review and Literature Compilation........................................................8 76III. What have we learnt from the last 40 years of studying learning in reptiles?.......9 77 1. Habituation of behaviour........................................................................................9 78 2. Animal training through operant conditioning.......................................................12 5 RUNNING HEAD: Review learning in Reptiles 79 3. Avoiding aversive stimuli......................................................................................16 80 4. Spatial learning and memory................................................................................24 81 5. Learning during foraging......................................................................................30 82 6. Quality and quantity discrimination.......................................................................34 83 7. Responding to change.........................................................................................36 84 8. Solving novel problems........................................................................................40 85 9. Social learning......................................................................................................41 86IV. Future directions.......................................................................................................45 87 1. The fitness consequences of individual differences in cognition...........................46 88 2. Cognition in ecologically relevant contexts...........................................................47 89 3. Cognition and behaviour in invasive species........................................................48 90 4. Social learning in social reptiles...........................................................................49 91 5. Avoidance of harmful invasive prey species.........................................................50 92 6. Executive function................................................................................................51 93 7. Spatial cognition in the context of sexual selection...............................................51 94V. Conclusions..............................................................................................................52 95VI. Acknowledgements..................................................................................................54 96VII. Supporting information............................................................................................54 97VIII. References.................................................................................................................55 98 6 RUNNING HEAD: Review learning in Reptiles 99I. Introduction 100Cognition, the process by which animals collect, store, and use information, is integral to 101fitness. It is essential for finding food and shelter, avoiding predators, finding and 102distinguishing between conspecifics and potential mates and adapting when environmental 103conditions suddenly change (Shettleworth, 2010). It is therefore not surprising that there has 104been immense interest in understanding what drives variation in cognition (e.g. Boogert et 105al., 2018; Dougherty & Guillette, 2018; Volter et al., 2018), how learning and cognitive 106processes impact fitness (e.g. Huebner et al., 2018; Madden et al., 2018; Thornton et al., 1072014) and the underlying mechanistic basis for species differences in decision making and 108problem solving (e.g. Lefebvre et al., 2004; Mustafar et al., 2018; Volter et al., 2018). While 109we have seen a surge in cognitive studies, particularly a move towards those done in the 110wild, there has been a clear focus on particular taxonomic groups, such as birds and 111mammals.