Sex-specific discrimination of familiar and unfamiliar mates in the Tokay gecko.

Social animals need to keep track of other individuals in their group to be able to adjust their behaviour accordingly and facilitate group cohesion. This recognition ability varies across species and is influenced by cognitive capacities such as learning and memory. In reptiles, particularly Squamates (lizards, snakes, and worm lizards), chemical communication is pivotal for territoriality, reproduction, and other social interactions. However, the cognitive processes underlying these social interactions remain understudied. In our study, we examined the ability of male and female Tokay geckos (Gekko gecko) to chemically differentiate familiar and unfamiliar mating partners. Our findings suggest that both sexes can make this distinction, with males responding more to the odour of a familiar mate, and females responding more to unfamiliar mates. The lizards maintained their discriminatory abilities for two to three weeks but not up to six weeks after separation. This research highlights the efficacy of using odours as social stimuli for investigating social cognition in lizards, a promising avenue to better understand social cognition in these animals.

Smarter in the city? Lizards from urban and semi-natural habitats do not differ in a cognitive task in two syntopic species.

Urbanization occurs at a global scale, imposing dramatic and abrupt environmental changes that lead to biodiversity loss. Yet, some animal species can handle these changes, and thrive in such artificial environments. One possible explanation is that urban individuals are equipped with better cognitive abilities, but most studies have focused on birds and mammals and yielded varied results. Reptiles have received much less attention, despite some lizard species being common city dwellers. The Italian wall lizard, Podarcis siculus, and the common wall lizard, Podarcis muralis, are two successful lizards in anthropogenic habitats that thrive in urban locations. To test for differences in a cognitive skill between urban and semi-natural environments, we investigated inhibitory control through a detour task in syntopic populations of the two species, across 249 lizards that were tested in partially artificial field settings. Sophisticated inhibitory control is considered essential for higher degrees of cognitive flexibility and other higher-level cognitive abilities. In this task, we confronted lizards with a transparent barrier, separating them from a desired shelter area that they could only reach by controlling their impulse to go straight and instead detour the barrier. We found no differences between lizards in urban and semi-natural environments, nor between species, but females overall performed better than males. Moreover, 48% of the lizards in our study did not perform a correct trial in any of the 5 trials, hinting at the difficulty of the task for these species. This study is among the first to address lizard cognition, through their inhibitory control, as a potential explanation for success in cities and highlights one should be careful with assuming that urban animals generally have enhanced cognitive performance, as it might be taxa, task, or condition dependent.

Regardless of personality, males show similar levels of plasticity in territory defense in a Neotropical poison frog.

Animal personality traits are sometimes linked to an individual's degree of plasticity, with certain personality types being more plastic than others. In territorial species, consistently high levels of aggression might increase the risk of harmful fights, while consistently low aggression might lead to the loss of a territory. Consequently, reacting plastically with an appropriate territorial response should be beneficial to avoid these risks. An integrative investigation of both personality traits and plasticity can help us better understand the dynamics of aggressive interactions during male-male competition. Here, we used a free-ranging Neotropical poison frog population to investigate the role of plasticity in male territorial aggression towards intruders. We conducted repeated standardized territorial intrusion experiments mimicking frogs of different body sizes via playback calls with different peak frequencies. We found individual repeatability for the latency to reach and approach a simulated intruder and observed that both aggressive and less aggressive males decreased their level of aggression towards big intruders. However, our results do not support a correlation between personality and plasticity in the context of male territory defense during the breeding season. We discuss how such a correlation between personality and plasticity might be conditional on the costs and benefits across contexts.

Geckos differentiate self from other using both skin and faecal chemicals: evidence towards self-recognition?

Self-recognition is the ability to recognise stimuli originating from oneself. Humans and some non-human animals show evidence of true visual self-recognition in the mirror test. They use their reflection to inspect themselves and to remove a mark that is only visible in the mirror. Not all animals, however, rely primarily on vision. In lizards, chemical cues are crucial in social interactions, and therefore, lizards would benefit from a chemical self-other distinction. Here, we test the tokay gecko (Gekko gecko), a social species, on their ability to discriminate their own skin and faecal chemicals from those of same-sex, unfamiliar conspecifics. We predicted that individuals would show more self-directed behaviour when confronted with the chemicals from unfamiliar individuals within their home enclosure as a sign of the need for increased comparison. Geckos showed higher self-directed responses towards chemicals from unfamiliar individuals compared to self-produced chemicals and a water control. Furthermore, scat and skin chemicals (regardless of origin) elicited similar but stronger responses than peppermint oil pointing towards a possible social function of scat piles. Although further tests and controls are needed, our study provides evidence towards chemical self-recognition and for a social function of scat piling in tokay geckos.

Fear of the new? Geckos hesitate to attack novel prey, feed near objects and enter a novel space.

Neophobia, the fear of novelty, is an ecologically important response which enables animals to avoid potentially harmful situations. Neophobia is a cognitive process by which individuals distinguish novelty from familiarity. In this study, we aimed to quantify this cognitive process in captive tokay geckos (Gekko gecko) across three contexts: when encountering novel prey, foraging near novel objects and entering a novel space. We also investigated individual consistency across trials using different novel stimuli, and correlation of individual responses across the three contexts. We found that geckos hesitate to attack novel prey and prey close to objects (familiar and novel). Geckos hesitated the most when entering novel space. Repeatability of behaviour within and across contexts was low (R = 0.101-0.190) indicating that neophobia might not be expressed similarly across contexts. The strength of a neophobic response can indicate how anxious or curious an individual is. This test has great potential to help answer questions about how captivity, enrichment, rearing environment and cognition affect fear responses in different contexts in lizards. By studying reptiles, we can better understand the universality of what is known about the causes leading to difference in neophobia across individuals and species.

Prey size preference in the tokay gecko (Gekko gecko).

The optimal foraging theory posits that animals aim to maximize energy intake while minimizing predation and handling costs during foraging. Most observed animal behaviour supports this theory, but occasional deviations provide insights into the ecological factors that shape foraging decisions. We tested prey-size preference using a two-choice test between different prey sizes in tokay geckos. We expected geckos to prefer larger prey and decision latencies to be longer when discrimination was more difficult and when small prey was offered. Geckos preferred larger prey when the size difference was large, although decision latency remained consistent. This aligns with prior research on sit-and-wait predators. Together with previous findings showing freezing behaviour after prey capture in tokay geckos, our findings suggest a strong influence of predator avoidance on foraging decisions opening up a new avenue for future research investigating the link between decision making and predator avoidance in tokay geckos.

Behavioural consistency across metamorphosis in a neotropical poison frog.

Animals often show consistency in their behavioural repertoire across time and/or contexts that differs from other individuals of the same population, i.e. animal personality. We currently have quite an incomplete understanding of the factors that lead to behavioural traits remaining stable - or becoming decoupled - over an animal's lifetime. In this study, we investigated the role of metamorphosis in the development of animal personality in a Neotropical poison frog, a species that undergoes drastic morphological and ecological changes during its development. We used lab-reared individuals of the brilliant-thighed poison frog Allobates femoralis to assess if consistent individual differences are already present at the tadpole stage, and if these differences are maintained throughout metamorphosis. We found evidence for two personality traits, exploration and boldness, already present in A. femoralis tadpoles. Despite the drastic changes in morphology, physiology, and habitat in the transition from tadpoles to metamorphs, personality traits persisted throughout metamorphosis, suggesting a physiological and/or genetic basis for the measured behavioural traits. We also found that exploration and boldness related behaviours were correlated with growth speed. Very bold and explorative individuals took fewer days until metamorphosis compared to very shy and non-explorative ones, which is in line with the concept of a Pace-of-Life Syndrome. These findings provide important insights into the proximate mechanisms that generate personality in species with complex life cycles.

Lizards lack speed-accuracy trade-offs in a quantitative foraging task when unable to sample the reward.

To make decisions, animals gather information from the environment in order to avoid costs (e.g., reduced survival) and increase benefits (e.g., foraging success). When time is limited or information is insufficient, most animals face a speed-accuracy trade-off (SAT) - they have to balance the benefits of making quick decisions against the costs of inaccurate decisions. Here, we investigated the relationship between decision accuracy and decision speed in gidgee skinks (Egernia stokesii) performing a food-based spontaneous quantity discrimination task. Rather than a SAT we found a speed-accuracy alignment; lizards made decisions that were fast and accurate, rather than inaccurate. Furthermore, we found only within-, but no between-individual differences in decision making indicating behavioural plasticity in the absence of individual decision styles. Finally, latency to choice was highly repeatable, more so than choice accuracy. Previous work has shown that learning, the costs of a bad decision and task difficulty frequently result in SATs. The lack of a SAT in our lizards might be a direct consequence of our simple testing methodology which prevented learning by not allowing lizards to consume the chosen quantity. To fully understand how SATs develop, different methodologies that control the costs and benefits of decisions should be compared.

A new protocol for investigating visual two-choice discrimination learning in lizards.

One of the most widely studied abilities in lizards is discrimination learning. The protocols used to test lizards are often novel or adapted from other taxa without proper validation. We need to ensure that tests of discrimination learning are appropriate and properly applied in lizards so that robust inferences can be made about cognitive ability. Here, we present a new protocol for testing lizard discrimination learning that incorporates a target training procedure, uses many daily trials for efficiency and reinforcement, and has a robust, validated, learning criterion. We trained lizards to touch a cue card using operant conditioning and tested lizards separately on a colour, and pattern discrimination test. Lizards successfully learnt to touch a cue card and to discriminate between light and dark blue but had issues discriminating the patterns. After modifying the test procedure, some lizards reached criterion, revealing possible issues with stimulus processing and interference of generalisation. Here, we describe a protocol for operant conditioning and two-choice discrimination learning in lizards with a robust learning criterion that can help researcher better design future studies on discrimination learning in lizards.

Wild cognition - linking form and function of cognitive abilities within a natural context.

Interest in studying cognitive ecology has moved the field of animal cognition into the wild. Animals face many challenges such as finding food and other resources, avoiding and deterring predators and choosing the best mate to increase their reproductive success. To solve these dilemmas, animals need to rely on a range of cognitive abilities. Studying cognition in natural settings is a powerful approach revealing the link between adaptive form and biological function. Recent technological and analytical advances opened up completely new opportunities and research directions for studying animal cognition. Such innovative studies were able to disclose the variety in cognitive processes that animals use to survive and reproduce. Cognition indeed plays a major role in the daily lives of wild animals, in which the integration of many different types of information using a diverse range of cognitive processes enhances fitness.

Naive poison frog tadpoles use bi-modal cues to avoid insect predators but not heterospecific predatory tadpoles.

For animals to survive until reproduction, it is crucial that juveniles successfully detect potential predators and respond with appropriate behavior. The recognition of cues originating from predators can be innate or learned. Cues of various modalities might be used alone or in multi-modal combinations to detect and distinguish predators but studies investigating multi-modal integration in predator avoidance are scarce. Here, we used wild, naive tadpoles of the Neotropical poison frog Allobates femoralis ( Boulenger, 1884) to test their reaction to cues with two modalities from two different sympatrically occurring potential predators: heterospecific predatory Dendrobates tinctorius tadpoles and dragonfly larvae. We presented A. femoralis tadpoles with olfactory or visual cues, or a combination of the two, and compared their reaction to a water control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multi-modal stimuli (a combination of visual and chemical information) originating from dragonfly larvae with avoidance but showed no reaction to uni-modal cues or cues from heterospecific tadpoles. In addition, visual cues from conspecifics increased swimming activity while cues from predators had no effect on tadpole activity. Our results show that A. femoralis tadpoles can innately recognize some predators and probably need both visual and chemical information to effectively avoid them. This is the first study looking at anti-predator behavior in poison frog tadpoles. We discuss how parental care might influence the expression of predator avoidance responses in tadpoles.

Learning simple and compound stimuli in a social lizard (Egernia stokesii).

We tested learning and behavioral flexibility in family-living gidgee skinks (Egernia stokesii) using a multistage visual discrimination task that included acquisition and reversal stages using simple and compound stimuli composed of black shapes superimposed on a colored background. We evaluated how lizards learn compound cues through a probe test. Lizards showed behavioral flexibility through reversal learning using simple stimuli (only color or shape). Our lizards used compound stimuli to learn a discrimination but had problems reversing and generalizing across novel compound stimuli. In the probe test, lizards chose the correct stimulus in a novel pairing with a distractor feature even without previous experience with compound stimuli. Our results suggest that some lizards are likely able to attend selectively to the relevant features of our compound stimuli while ignoring irrelevant features instead of using the configuration of a cue card as a whole to learn to discriminate between compound stimuli. We hope that our work will spark interest in further studies looking at how lizards (and reptiles in general) learn to solve visual discrimination problems. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

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

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.

Do lizards have enhanced inhibition? A test in two species differing in ecology and sociobiology.

Waiting for the right moment to strike, avoiding the ingestion of harmful foods, or ignoring stimuli associated with ephemeral or depleted resources requires the inhibition of prepotent responses. Good response inhibition facilities flexibility in behaviour which is associated with survival in unpredictable environments. To investigate differences in behavioural flexibility in lizards, we tested reversal learning in the sleepy lizard (Tiliqua rugosa asper) and compared its performance to the relatively closely related eastern blue-tongue skink (Tiliqua scincoides scincoides). We presented both species with a choice between either a light and dark blue stimulus or a triangle and X shape. Both species were able to learn to discriminate between these stimuli and showed similar learning ability during the acquisition of the discrimination. Sleepy lizards, however, demonstrated a higher probability of making a correct choice at the start of the reversal, hinting towards enhanced stimulus response inhibition. Sleepy lizards and blue-tongue skinks inhabit different environments and show differences in ecology and sociobiology, all of which could possibly lead to adaptive specialisation in cognitive ability. Although further research is required, we propose that selection might have led to a change in stimulus response inhibition in the arid-adapted sleepy lizard, because better response inhibition may help them avoid the costs of repeated choices towards stimuli which no longer predict a beneficial outcome.

Sex-dependent discrimination learning in lizards: A meta-analysis.

We have a poor understanding of differences in learning performance between male and female non-avian reptiles compared to other vertebrates. Learning studies in non-avian reptiles have greatly increased in the last 10 years providing an opportunity to test for sex-based learning using a meta-analysis. Although, we initially considered all reptiles, only lizard studies (N = 11) provided sufficient data to calculate effect sizes. We found weak evidence for sex-dependent learning and moderate heterogeneity in effect sizes across studies. Although, our hypothesized moderator variables (stimulus or task type, species, genus and family) explained little variation. Indeed, our results show that only one species (Egernia striolata) exhibited a sex-dependent learning difference, with males learning faster than females. Together, our meta-analysis indicated a general lack of effective reporting on attributes of study methodology (i.e., animal sex, sample sizes). We propose that future research improve reporting by openly sharing their data for the use in similar analyses. The limited sample currently constrains our ability to effectively disentangle whether sex differences vary across different tasks and stimuli. We urge authors to incorporate both sexes in experimental designs and test them on ecologically relevant cognitive assays to improve our understanding of the degree of sex differences in non-avian reptile learning.

Context-specific response inhibition and differential impact of a learning bias in a lizard.

Response inhibition (inhibiting prepotent responses) is needed for reaching a more favourable goal in situations where reacting automatically would be detrimental. Inhibiting prepotent responses to resist the temptation of a stimulus in certain situations, such as a novel food item, can directly affect an animal's survival. In humans and dogs, response inhibition varies between contexts and between individuals. We used two contextually different experiments to investigate response inhibition in the eastern water skink (Eulamprus quoyii): reversal of a visual two-choice discrimination and a cylinder detour task. During the two-choice task, half of our lizards were able to reach an initial learning criterion, but, thereafter, did not show consistent performance. Only two individuals reached a more stringent criterion, but subsequently failed during reversals. Furthermore, half of our animals were not able to inhibit a pre-existing side preference which affected their ability to learn during the two-choice task. Skinks were, however, able to achieve a detour around a cylinder performing at levels comparable to brown lemurs, marmosets, and some parrot species. A comparison between the tasks showed that reaching the initial criterion was associated with low success during the detour task, indicating that response inhibition could be context-specific in the water skink. To the best of our knowledge, this is the first study to examine inhibitory control and motor self-regulation in a lizard species.

Object permanence in the Goffin cockatoo (Cacatua goffini).

The ability to represent hidden objects plays an important role in the survival of many species. In order to provide an inclusive synopsis of the current benchmark tasks used to test object permanence in animals for a psittacine representative, we tested eight Goffin cockatoos (Cacatua goffini) on Stages 3-6 of Piagetian object permanence as well as derivations of spatial transposition, rotation, and translocation tasks. Subjects instantly solved visible displacement 3b and 4a but showed an extended plateau for solving Stage 5a at a very late age (10 months). Subjects readily solved most invisible displacement tasks including double hidings and four angles (90°, 180°, 270°, and 360°) of rotation and translocations at high performance levels, although Piagetian Stage 6 invisible displacement tasks caused more difficulties for the animals than transposition, rotations, and translocation tasks.