Learning in non‐avian reptiles 40 years on: advances and promising new directions

Abstract

Recently, there has been a surge in cognition research using non‐avian reptile systems. As a diverse group of animals, non‐avian reptiles [turtles, the tuatara, crocodylians, and squamates (lizards, snakes and amphisbaenids)] are good model systems for answering questions related to cognitive ecology, from the role of the environment on the brain, behaviour and learning, to how social and life‐history factors correlate with learning ability. Furthermore, given their variable social structure and degree of sociality, studies on reptiles have shown that group living is not a pre‐condition for social learning. Past research has demonstrated that non‐avian reptiles are capable of more than just instinctive reactions and basic cognition. Despite their ability to provide answers to fundamental questions in cognitive ecology, and a growing literature, there have been no recent systematic syntheses of research in this group. Here, we systematically, and comprehensively review studies on reptile learning. We identify 92 new studies investigating learning in reptiles not included in previous reviews on this topic – affording a unique opportunity to provide a more in‐depth synthesis of existing work, its taxonomic distribution, the types of cognitive domains tested and methodologies that have been used. Our review therefore provides a major update on our current state of knowledge and ties the collective evidence together under nine umbrella research areas: (i) habituation of behaviour, (ii) animal training through conditioning, (iii) avoiding aversive stimuli, (iv) spatial learning and memory, (v) learning during foraging, (vi) quality and quantity discrimination, (vii) responding to change, (viii) solving novel problems, and (ix) social learning. Importantly, we identify knowledge gaps and propose themes which offer important future research opportunities including how cognitive ability might influence fitness and survival, testing cognition in ecologically relevant situations, comparing cognition in invasive and non‐invasive populations of species, and social learning. To move the field forward, it will be immensely important to build upon the descriptive approach of testing whether a species can learn a task with experimental studies elucidating causal reasons for cognitive variation within and among species. With the appropriate methodology, this young but rapidly growing field of research should advance greatly in the coming years providing significant opportunities for addressing general questions in cognitive ecology and beyond.

Mechanisms, development, and comparative perspectives on experience‐dependent plasticity in social behavior

“…However, the extent to which mating experiences affect these processes in nonmammalian vertebrates remains unknown. Given that cognitive processes underlying a number of evolutionarily important behaviors, it would be interesting to reveal the impact of mating experiences on cognitive processes like food caching in chickadees and corvids and various types of learning in reptiles (Emery & Clayton, 2004; Güntürkün & Bugnyar, 2016; reviewed in Szabo et al, 2021). Given the influence of incubation temperature on experience‐dependent plasticity in leopard geckos and the similarities in the effects of incubation temperature in leopard geckos and of intrauterine position in rodents on sexual differentiation (Ryan & Vandenbergh, 2002; Sakata & Crews, 2004; Sakata et al, 2005), it would be interesting to assess the degree to which males and females from different intrauterine positions demonstrate various types of experience‐dependent changes. Whereas nonapeptides such as oxytocin or vasopressin have been demonstrated to be critical for mating‐dependent changes in the processing of individual cues in mammals (i.e., preferences for mate's cues), little is known about the role of these peptide hormones in mating‐dependent sensory plasticity in birds, lizards, and amphibians (but see Tomaszycki & Atchley, 2017).…”

“…However, the extent to which mating experiences affect these processes in nonmammalian vertebrates remains unknown. Given that cognitive processes underlying a number of evolutionarily important behaviors, it would be interesting to reveal the impact of mating experiences on cognitive processes like food caching in chickadees and corvids and various types of learning in reptiles (Emery & Clayton, 2004; Güntürkün & Bugnyar, 2016; reviewed in Szabo et al, 2021).…”

Reinstating reptiles: from clueless creatures to esteemed models of cognitive biology

“…Despite that Burghardt (1977) provided useful recommendations to improve studies of reptilian cognition, the taxon was largely ignored in cognitive research for the next decades (Szabo et al, 2021b). Only very recently, the field of animal cognition experienced a true 'reptilian renaissance', in which the myth of the blunt, slow reptilian has finally been rebuked.…”

“…Reptiles exhibit fast and flexible learning, long-term memory, spontaneous problem-solving abilities, quantity discrimination, and even social learning. Font (2020) and Szabo et al (2021b) provide excellent overviews of the work that has been done on reptilian cognition in the past decades. Here, instead, we focus on the future, by pointing out the potential of reptiles as model species in cognitive research and suggesting an assortment of prospective avenues for future research.…”

“…Research in the 2000s and early 2010s already identified a diversity of spatial learning strategies in reptiles, such as response strategies based on egocentric cues (e.g., turn left) (in whiptail lizards: Day et al, 2003;in red-footed tortoises: Mueller-Paul et al, 2012), the use of a local cue (cooccurring with the goal) as guidance (in corn snakes: Holtzman, 1998;in red-eared sliders: López et al, 2000in red-eared sliders: López et al, , 2001, remembering multiple distal cues (e.g., features of the experimental room) to form a mental representation of the environment (in red-eared sliders: López et al, 2000López et al, , 2001in side-blotched lizards: Ladage et al, 2012, Figure 1E;in wall lizards: Font, 2019) or a mix of these (in spotted pythons: Stone et al, 2000, Figure 2E). Regardless, even closely-related reptile species can differ considerably in which of these strategies they employ (discussed in depth in Szabo et al, 2021b) and thus this variation (and its ecological relevance) remains poorly understood. In this special issue, Paulissen (2021) specifically tested whether little brown skinks (Scincella lateralis), a species capable of learning the location of a safe hiding spot based on distal (Paulissen, 2008) and local cues (Paulissen, 2014), are also capable of accomplishing the same task using a single positional cue.…”