Ongoing Projects
Amphibian cognition - can ecology inform performance differences (Review)
The cognitive abilities of amphibians are quite well known. Especially their spatial orientation abilities, individual and kin discrimination abilities and communication in natural environments. Less is known about learning, memory, inhibition or numerical abilities. In other taxa such abilities are more often tested in controlled lab settings. Ecology might explain difference in cognitive ability across species and we are working on linking results from published studies to measures of ecology.
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Cognitive styles in discrimination learning (Meta-analysis)
Studying individual variation in cognition is receiving increasingly more attention. Individual behaviour falls along a fast-slow scale trading speed at the cost of accuracy and so does cognition. Using a meta-analytic approach we analyse the relationship between learning rate in a discrimination acquisition and reversal task across taxa to reveal cognitive styles.
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Behavioural lateralisation across three contexts in Tokay geckos (MSc project)
Bettina, a master student, is currently collecting data on lateralised behaviour in a foraging, social and predatory context across 22 Tokay geckos (Gekko gecko). Laterality has been hypothesised to contribute to faster processing of information across contexts with, for example, predator related stimuli being processed with one hemisphere while foraging related cues are processed with the other hemisphere. This allows animals to stay vigilant and avoid predation while foraging. To investigate parallel processing data from the same individuals across contexts is required.
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How does pair housing affect neophobia in the Tokay gecko
It is recommended to house Tokay geckos in pairs. We have, however, no knowledge if pair housing in captivity is beneficial to the animals wellbeing compared to single housing. We were interested in finding out if single versus pair housing affects neophobia across three contexts (food, object and space neophobia) by comparing neophobic responses between single and pair housing in the same individuals.
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Discrimination of prey number and size in the Tokay gecko (MSc project)
Tokay geckos are sit-and-wait/ ambush predators and prefer larger prey if given the choice between different prey sizes. In this Master project we want to investigate their choice behaviour in more detail by presentinhg a wide range of prey sizes as well as number of similar sized prey adding controls for prey movement and volume of choices. We exect that discrimination ability based on size will depend on the size difference between option and that choices regarding prey number will depend on how many prey can be captured showing an optimal number that is preferred. Finally, we expect geckos to be attracted to faster moving prey in the controls as movement is the main cue that elicits hunting behaviour.
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Spatial learning in the radial arm maze (ASAB Research Grant funded project)
In this study I am investigating spatial learning in the 8-arm radial arm maze in adult as well as subadult Tokay geckos. Geckos have to learn 4 locations in which they can find food and 4 location that do not provide food. We are looking at differences in learning based on maze orientation (horizontal with gravity cues controlled and vertical), differences across the sexes and between adults and subadults.
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Early social-life effects on cognition in the facultative social Tokay gecko
This study was designed as a pilot to investigate if early social-life experiences (being raised socially versus in isolation) influences the development of object neophobia, space neophobia, habituation and associative learning.
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Context dependent discrimination of familiar and unfamiliar handlers in the Tokay gecko
In this study, we explore the effects of handler identity on measures of fearfulness and feeding behaviour. Such investigations are important as handler effects can additional variation to behavioural measurements which might hamper the detection of small effects in studies in which multiple experimenters are involved.
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Is physical closeness a good measure to capture variation in Pair association in captive Tokay geckos ?(BSc project)
Using scan sampling, we measured the physical closeness of individuals in a pair and related this measures to other spatial behaviours such as movement to understand if physical closeness can capture variation in pair association and therefore pair quality or if it is another measure of spatial behaviour.​
Published Projects
Effects of the early social environment on behavioural flexibility in a cooperatively breeding cichlid fish
The ability to adapt behaviour flexibly to the current situation, also referred to as ‘behavioural flexibility’, is crucial for survival and reproductive success. The early social environment is an important driver of variation in cognitive abilities including behavioural flexibility. However, few studies have investigated this relationship across contexts. Likewise, few studies have investigated the development of modular versus general cognition (i.e. inconsistent versus consistent performance across social and nonsocial contexts) in social species. Here, (1) we investigated the influence of the early social environment (rearing group size) on behavioural flexibility in adult helpers of a cooperatively breeding cichlid fish (Neolamprologus pulcher) and (2) we assessed the presence of general or modular cognition irrespective of early experience by using three nonsocial flexibility tests (innovation test, reversal learning, set shifting) and two social flexibility tests (hierarchy test, integration test). Overall, early social experience only influenced social but not nonsocial flexibility. Helpers raised in large social groups were less flexible in the hierarchy test but tended to be accepted more often when integrated with an unfamiliar breeding pair, compared to fish raised in small groups. The early social environment did not affect nonsocial flexibility, although fish were able to adjust behaviour flexibly in both social and nonsocial contexts. For all fish, performances were not correlated across tests, implying the existence of domain-specific cognition. Nevertheless, results of a principal component analysis suggest an association between performances in social and nonsocial contexts, which may hint at domain-general cognition, albeit with the caveat that not all tests were associated with the same principal component. Future research should develop approaches that can clearly distinguish between general and modular cognition, and thatcompare species with different environmental predictability.
Sex-specific discrimination of familiar and unfamiliar mates in the Tokay gecko (MSc project)
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.
Changes in enclosure use and basking behaviour associated with pair housing in Tokay geckos (Gekko gecko)
Due to often insufficient information, reptiles suffer welfare issues and increased mortality in captivity. In particular, the impact of the social environment remains poorly understood, despite evidence suggesting its’ importance for welfare in a wide range of social animals. The current study investigated how pair housing changes enclosure use, basking and hiding behaviour in tokay geckos (Gekko gecko). While the captive conditions and husbandry procedures employed in this study align with existing literature recommendations, they have not been previously evaluated for their suitability for this particular species. The results show that, when socially deprived, lizards were more likely to move and hide before feeding. Furthermore, males were more likely to be found at the front than females during pair housing but not during single housing. Finally, contrary to single housing, enclosure temperature had no effect on the probability to move and hide behind a shelter during pair housing. Consistently, lizards were more likely to bask after feeding across housing conditions, and females were more likely to bask before their first clutch. Together, pair housing decreases movement and hiding in relation to human presence (feeding), which might indicate that pair housing improves tokay gecko welfare and suggest that the presence of a conspecific should be considered to improve welfare policies in social reptiles. This study serves as a baseline for future research into how enclosure furnishings, husbandry techniques, and enrichment practices impact the welfare of tokay geckos which will be crucial for refining our understanding of and improving on the welfare of reptiles in captivity.
Prey size preference in the tokay gecko (Gekko gecko) (BSc project)
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.
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.
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.
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 need, our study provides evidence towards chemical self-recognition and for a social function of scat piling in tokay geckos.
Spontaneous quantity discrimination in the Australian sleepy lizard (Tiliqua rugosa)
Animals employ quantitative abilities to gauge crucial aspects of their environment, such as food or predator density in a given area or the number of eggs in a nest. These quantitative skills hold ecological implications and can impact an animal’s fitness. However, our comprehension of how these abilities intersect with environmental challenges remains limited. We tested for spontaneous quantity discrimination in the sleepy lizard (Tiliqua rugosa), a long-lived species known for forming life-long pair bonds in which pairs come together for the breeding season. We subjected lizards to a Y-maze experiment presenting both discrete (comparisons involving two vs. four, two vs. six, two vs. eight, four vs. six, four vs. eight, and six vs. eight pieces) and equivalent continuous combinations (single pieces differing in size) of pumpkin pieces. Our findings revealed that sleepy lizards exhibited spontaneous quantity discrimination, favoring the larger quantity in three discrete comparisons (eight vs. two, two vs. six, four vs. six) and two continuous comparisons (eight vs. two, eight vs. four). However, low accuracy may be attributable to difficulty in visual acuity exacerbated by difficulty discriminating quantities at small ratios. Furthermore, we found no evidence for a speed-accuracy trade-off in their decision-making process. Our results suggest that sleepy lizards likely employ multiple cues to estimate quantity accurately. Considering these results in the context of previous studies on various lizard species, it becomes apparent that lizards, as a group, offer a valuable model for unraveling the evolution of cognition, given their diverse ecology and sociobiology.
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.
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.
Lizards lack speed-accuracy trade-offs in a quantitative foraging task when unable to sample the reward (MSc project)
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.
Naïve 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 both and compared their reaction to a water-control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multimodal 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 likely 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.
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.
Sub-problem learning and reversal of a multidimensional visual cue in a lizard: Evidence for behavioural flexibility?
Behavioural flexibility, the ability to adjust behaviour to environmental change by adapting existing skills to novel situations, is key to coping with, for example, complex social interactions, seasonal changes in food availability or detecting predators. We tested the tree skink, Egernia striolata, a family-living skink from eastern Australia, in a set-shifting paradigm of eight colour/shape discriminations including reversals, an intradimensional acquisition of a new colour/shape and extradimensional shift from colour to shape (and vice versa). Skinks could learn to discriminate between colour/shape pairs and reverse this initial stimulus-reward association; however, they showed no significant decrease in the probability of making a correct choice in the extradimensional shift suggesting that they did not form an attentional set. Subjects appear to have learnt each stage as a new problem instead of generalizing stimuli into specific dimensions (set formation). In conclusion, tree skinks solved a discrimination reversal by focusing their attention towards visual stimuli and flexibly adjusting their choice behaviour accordingly. These lizards learned to use multidimensional visual stimuli to find a food reward but did not generalize stimuli into dimensions. Furthermore, this study is the first to test for set shifting in a lizard species and thereby allows us to extend set-shifting theory to a new taxon for comparison with primates, rodents, a bird and a turtle.
Spontaneous quantity discrimination in a family-living lizard
While foraging or during social interactions, animals may benefit from judging relative quantity. Individuals may select larger prey or a patch with more food and, likewise, it may pay to track the number and type of individuals and social interactions. We tested for spontaneous quantity discrimination in the gidgee skink (Egernia stokesii), a family-living lizard. Lizards were presented with food quantities differing in number or size and were able to select the larger quantity of food items when they differed in number but not when items differed in size. We show, for the first time, superior spontaneous discrimination of items differing in number over size in a lizard species, which contrasts with previous findings. Our simple method, however, did not include controls for the use of continuous quantities, and further tests are required to determine the role of such information during quantity discrimination. Our results provide support for the use of the parallel individuation system for the discrimination of small quantities (four or fewer items). Lizards might, however, still use the approximate number system if items in larger quantities (more than four) are presented. Overall, we uncovered evidence that species might possess specific cognitive abilities potentially adapted to their niche with respect to quantity information (discrete and/ or continuous) and the processing system used when judging quantities. Importantly, our results highlight the need for testing multiple species using similar testing procedures to gain a better understanding of the underlying causes leading to differences across species.
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.
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. Recently, learning studies in non-avian reptiles greatly increased enabling us 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. We found moderate heterogeneity in effect sizes across studies, yet our hypothesized moderator variables (type of stimuli, 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.
Precocial juvenile lizards show adult-level learning and behavioural flexibility
In altricial species, young rely on parental care and brain maturation mainly occurs after birth. In precocial species, young are born in a more advanced developmental stage in need of less or no parental care and brain development is mostly completed at the time of birth. We therefore predicted early maturation of learning ability in precocial species. We used a series of visual discrimination and reversal stages to investigate the ability of the precocial eastern blue-tongue lizard, Tiliqua scincoides scincoides, a long-lived Australian lizard species with slow-developing young, to respond to changes in stimulus relevance and test for behavioural flexibility. To test whether age affects learning in this species, we compared juveniles (23–56 days) with adults (sexually mature, at least 2 years). In accordance with our expectations, adults and juveniles performed similarly well in all stages, suggesting that juveniles of this precocial species learn at adult levels from an early age. Both age classes performed well during reversals showing good behavioural flexibility. This is the first study in lizards to directly compare juvenile and adult behavioural flexibility. Importantly, we demonstrate that precocial lizards can begin life with an advanced cognitive ability already in place.
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 bluetongue 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 might help them avoid the costs of repeated choices towards stimuli which no longer predict a beneficial outcome.
Are lizards capable of inhibitory control? Performance on a semi-transparent version of the cylinder task in five species of Australian skinks
Inhibitory control, the inhibition of prepotent actions, is essential for higher-order cognitive processes such as planning, reasoning, and self-regulation. Individuals and species differ in inhibitory control. Identifying what influences inhibitory control ability within and between species is key to understanding how it evolved. We compared performance in the cylinder task across five lizard species: tree skinks (Egernia striolata), gidgee skinks (Egernia stokesii), eastern blue-tongue skinks (Tiliqua s. scincoides), sleepy lizards (Tiliqua r. asper), and eastern water skinks (Eulamprus quoyii). In our task, animals had to inhibit the prepotent motor response of directly approaching a reward placed within a semi-transparent mesh cylinder and instead reach in through the side openings. Additionally, in three lizard species, we compared performance in the cylinder task to reversal learning to determine the task specificity of inhibitory ability.Within species, neither sex, origin, body condition, neophobia, nor pre-experience with other cognitive tests affected individual performance. Species differed in motor response inhibition: Blue-tongue skinks made fewer contacts with the semi-transparent cylinder wall than all other species. Blue-tongue skinks also had lower body condition than the other species which suggest motivation as the underlying cause for species differences in task performance. Moreover, we found no correlation between inhibitory ability across different experiments. This is the first study comparing cylinder task performance among lizard species. Given that inhibitory control is probably widespread in lizards, motor response inhibition as exercised in the cylinder task appears to have a long evolutionary history and is likely fundamental to survival and fitness.
Non-avian reptile learning 40 years on: advances, promises and potential
Recently, there has been a surge in cognition research in non-avian reptiles. As a diverse group of animals, non-avian reptiles (turtles, the tuatara, crocodilians, and squamates - lizards, snakes and amphisbaenids) have shown to be good model systems for answering questions related to cognitive ecology; from the role of the environment in 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, reptiles have been pivotal in demonstrating that group living is unnecessary for animals to learn effectively from conspecifics. Past research has undoubtedly 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 base, there have been no systematic syntheses of research in this group. Here, we systematically, and comprehensively review studies on reptile learning. We identify 83 new studies investigating learning in reptiles not included in previous reviews on the same 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 methodology that has been used. Our review therefore provides an up-to-date knowledge overview by tying the collected evidence together under eight cognitive umbrella terms: (1) aversion learning, (2) spatial cognition, (3) learning during foraging, (4) numerical competency, (5) learning flexibility, (6) social learning and (7) memory. 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 an ecologically relevant setup, testing invasive compared to non-invasive species, and social learning in social reptiles. Overall, we believe that, for the field to move forward, it will be immensely important to build upon the descriptive approach (testing if a species can learn a task) with experimental studies elucidating causal reasons for cognitive variation between and within species. With the appropriate methodology, this still young field of research should advance greatly in the coming years and represents a significant opportunity for testing general questions in cognitive ecology and beyond.
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.
Can Cognitive Ability Give Invasive Species the Means to Succeed? A Review of the Evidence
Invasive species are a global conservation problem that have an enormous economic cost. Understanding the attributes of invasive species and what makes them successful at colonizing and flourishing in novel environments is therefore essential for preventing and ameliorating their negative impact. Learning ability and behavioral flexibility—the ability to adjust behavior flexibly when conditions change including to learn to solve novel problems or existing problems in a novel way, are thought to play a key role during invasions although cognitive ability is rarely considered in studies of invasive species. We begin by reviewing the evidence that flexible learning and problem solving can influence invasion success in both invertebrates and vertebrates. We also review brain size as an index of cognitive ability with respect to invasion success. We then focus on the specific attributes of cognition that are likely to be important for species entering novel environments as they learn the location of resources (e.g., food, shelter), and as they encounter and interact with conspecifics, heterospecifics, and potential predators. We suggest that enhanced spatial learning ability in conjunction with behavioral flexibility are likely to be adaptive. Furthermore, good memory retention and the ability to learn from others (both conspecifics and heterospecifics) are beneficial. Finally, we suggest future directions for studying the link between cognition, fitness, and invasion success. Studies of closely related “invasive” and “non-invasive” species, as well as invasive populations and their source, should provide important baseline information about the potential role of cognitive ability in determining invasion success. We also advocate an experimental approach. In particular, we borrow methods from experimental evolutionary ecology. We suggest that experimental studies in which potential invasive species can be assayed for behavior and their cognitive ability measured prior to population-level release on small islands will help inform us about the potential role of cognitive ability in determining the fitness of invasive species. The idea that cognitive ability may determine invasion success is only now starting to gain traction. This is a rich field worthy of further study that will help us better understand what makes a successful invasive species.
Why preen others? Predictors of allopreening in parrots and corvids and comparisons to grooming in great apes
Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.
Within-group relationships and lack of social enhancement during object manipulation in captive Goffin’s cockatoos (Cacatua goffiniana)
Different types of social relationships can influence individual learning strategies in structured groups of animals. Studies on a number of avian species have suggested that local and/or stimulus enhancement are important ingredients of the respective species’ exploration modes. Our aim was to identify the role of enhancement during object manipulation in different social contexts. We used focal observations to identify a linear dominance hierarchy as well as affiliative relationships between individuals in a group of 14 Goffin’s cockatoos (Cacatua goffiniana, formerly goffini). Thereafter, in an unrewarded object choice task, several pairs of subjects were tested for a possible influence of social enhancement (local vs. stimulus) in three conditions: dominance, affiliation, and kinship. Our results suggest strong individual biases. Whereas previous studies on ravens and kea had indicated that enhancement in a non-food-related task was influenced by the social relationship between a demonstrator and an observer (affiliated – nonaffiliated), we found no such effects in our study group. In this context, Goffin’s cockatoos’ object learning seems to take place more on an individual level, despite their generally high motivation to manipulate nonfood items.
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.
Spontaneous innovation in tool manufacture and use in a Goffin’s cockatoo
Accounts of complex tool innovations in animals, particularly in species not adaptively specialized for doing so, are exceedingly rare and often linked to advanced cognitive abilities in the physical domain. Among birds, there are several reports of tool innovations in corvids, but very few documented records in other families. During routine behavioural observations, a captive male named Figaro successfully, reliably and repeatedly made and used stick-type tools. Later during a test, he used these tools to rake in food, manufacturing them from two different materials and displaying different steps and techniques. Our observations prove that innovative tool-related problem-solving is within this species’ cognitive resources. As it is unknown for tools to play a major role in this species’ ecology, this strengthens the view that tool competences can originate on general physical intelligence, rather than just as problem-specific ecological solutions.