RUNNING HEAD: Review learning in Reptiles 1 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 RUNNING HEAD: Review learning in Reptiles 2 23 Abstract 24 Recently, there has been a surge in cognition research using non-avian reptile systems. As 25 a diverse group of animals, non-avian reptiles (turtles, the tuatara, crocodilians, and 26 squamates - lizards, snakes and amphisbaenids) are good model systems for answering 27 questions related to cognitive ecology; from the role of the environment in impacting brain, 28 behaviour and learning, to how social and life-history factors correlate with learning ability. 29 Furthermore, given their variable social structure and degree of sociality, studies on reptiles 30 have demonstrated that group living is not a pre-condition for social learning. Past research 31 has undoubtedly demonstrated that non-avian reptiles are capable of more than just 32 instinctive reactions and basic cognition. Despite their ability to provide answers to 33 fundamental questions in cognitive ecology, and a growing literature base, there have been 34 no systematic syntheses of research in this group. Here, we systematically, and 35 comprehensively review studies on reptile learning. We identify 92 new studies investigating 36 learning in reptiles not included in previous reviews on the same topic – affording a unique 37 opportunity to provide a more in-depth synthesis of existing work, its taxonomic distribution, 38 the types of cognitive domains tested and methodology that has been used. Our review 39 therefore provides a major update on our current state of knowledge and ties the collective 40 evidence together under nine umbrella research areas: (1) habituation, (2) conditioning, (3) 41 aversion learning, (4) spatial learning, (5) learning during foraging, (6) numerical 42 competency, (7) learning flexibility, (8) problem solving, and (9) social learning. Importantly, 43 we identify knowledge gaps and propose themes which offer important future research 44 opportunities including how cognitive ability might influence fitness and survival, testing 45 cognition in ecologically relevant situations, comparing cognition in invasive and non- 46 invasive populations of species, and social learning. To move the field forward, it will be 47 immensely important to build upon the descriptive approach of testing if a species can learn 48 a task with experimental studies elucidating causal reasons for cognitive variation within and 49 between species. With the appropriate methodology, this young but rapidly growing field of 50 research should advance greatly in the coming years providing significant opportunities for RUNNING HEAD: Review learning in Reptiles 3 51 addressing general questions in cognitive ecology and beyond. 52 53 Keywords: Amphisbaenia, Chelonia, Crocodilia, Rhynchocephalia, Squamata, Serpentes, 54 Sauria, cognition, integrative review 55 RUNNING HEAD: Review learning in Reptiles 4 56 Content 57 I. Introduction ................................................................................................................ 5 58 II. Systematic Review and Literature Compilation ....................................................... 8 59 III. What have we learnt from the last 40 years of studying learning in reptiles? ....... 9 60 1. Habituation of behaviour ....................................................................................... 9 61 2. Animal training through operant conditioning....................................................... 12 62 3. Avoiding aversive stimuli ..................................................................................... 16 63 4. Spatial learning and memory ............................................................................... 24 64 5. Learning during foraging ..................................................................................... 30 65 6. Quality and quantity discrimination ...................................................................... 34 66 7. Responding to change ........................................................................................ 36 67 8. Solving novel problems ....................................................................................... 40 68 9. Social learning .................................................................................................... 41 69 IV. Future directions ...................................................................................................... 45 70 1. The fitness consequences of individual differences in cognition .......................... 46 71 2. Cognition in ecologically relevant contexts .......................................................... 47 72 3. Cognition and behaviour in invasive species ....................................................... 48 73 4. Social learning in social reptiles .......................................................................... 49 74 5. Avoidance of harmful invasive prey species ........................................................ 50 75 6. Executive function ............................................................................................... 51 76 7. Spatial cognition in the context of sexual selection .............................................. 51 77 V. Conclusions ............................................................................................................. 52 78 VI. Acknowledgements ................................................................................................. 54 79 VII. Supporting information ........................................................................................... 54 80 VIII. References ............................................................................................................... 55 81 RUNNING HEAD: Review learning in Reptiles 5 82 I. Introduction 83 Cognition, the process by which animals collect, store, and use information, is integral to 84 fitness. It is essential for finding food and shelter, avoiding predators, finding and 85 distinguishing between conspecifics and potential mates and adapting when environmental 86 conditions suddenly change (Shettleworth, 2010). It is therefore not surprising that there has 87 been immense interest in understanding what drives variation in cognition (e.g. Boogert et 88 al., 2018; Dougherty & Guillette, 2018; Volter et al., 2018), how learning and cognitive 89 processes impact fitness (e.g. Huebner et al., 2018; Madden et al., 2018; Thornton et al., 90 2014) and the underlying mechanistic basis for species differences in decision making and 91 problem solving (e.g. Lefebvre et al., 2004; Mustafar et al., 2018; Volter et al., 2018). While 92 we have seen a surge in cognitive studies, particularly a move towards those done in the 93 wild, there has been a clear focus on particular taxonomic groups, such as birds and 94 mammals. Only recently, has research begun to appreciate the diversity of cognitive 95 variation across a broader range of animal groups and moved to take a more 96 comprehensive comparative approach. 97 Non-avian reptiles, from here on called reptiles (including turtles, crocodilians, tuatara 98 and squamates - lizards, snakes and amphisbaenids), are starting to become model 99 systems for addressing a host of questions in cognitive ecology. For example, because 100 many squamates are egg layers it is possible to explore how early developmental 101 environments (independent of maternal environment) impact learning. Incubation 102 temperature affects sexual development (temperature dependent sex determination, 103 Warner, 2010), brain morphology (e.g. Amiel et al., 2016), behaviour (e.g. Booth, 2006; 104 Matsubara et al., 2017) and learning (e.g. Amiel et al., 2014; Dayananda & Webb, 2017; 105 Munch et al., 2018a). Moreover, many reptiles are precocial and the juvenile brain is much 106 more developmentally advanced at birth compared to altricial species (Charvet & Striedter, 107 2011; Grand, 1992) which impact learning ability at an early age (Szabo et al., 2019a). 108 Reptiles also show individual variation in learning ability which has been linked to 109 behavioural type, age, dominance status and sex (e.g. Carazo et al., 2014; Chung et al., RUNNING HEAD: Review learning in Reptiles 6 110 2017; Kar et al., 2017; Noble et al., 2014). Because some reptiles have evolved early forms 111 of sociality (While et al., 2015; Whiting & While, 2017) they have also been foundational in 112 understanding how familiarity affects social learning ability (e.g. Munch et al., 2018b; Whiting 113 et al., 2018). 114 Phylogenetically, reptiles (including birds) split from mammals about 320 million 115 years ago and about 280 million years ago, the reptiles diverged into two clades: archosaurs 116 (birds and crocodiles) and lepidosaurs (tuatara and squamates [lizards, amphisbaenids, 117 snakes])(Alföldi et al., 2011).