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Latency in Problem Solving as Evidence for Learning in Varanid and Helodermatid Lizards, with Comments on Foraging Techniques
Abstract
Cognition and learning have been widely studied in vertebrates, but not across much phylogenetic breadth. Non-avian reptiles, for example, have been poorly studied. Anecdotal observations and a few previous studies suggest that lizards may have strong cognitive skills owing, in part, to behaviors such as optimal foraging and territoriality. We tested four lizard species, including three species of monitor lizard (Varanus spp.) and one species of beaded lizard (Heloderma), in a longitudinal, repeated-trials experimental design using a puzzle-feeder device to evaluate learning, in the form of latency trends over time. We used a Bayesian multilevel modeling statistical method and incorporated unsuccessful trials as censored data. Collectively, all lizards showed a pattern of decreasing latencies over time. We interpret this pattern as learning among our lizards. Notable individual and inter-specific differences were evident, however, suggesting that learning abilities differed among the lizards. In this case, the monitor lizards exhibited steeper declines in latencies and greatly reduced inter-individual variation in comparison to the beaded lizards. Finally, we found differential use of the claws versus the snout among the lizards, which is consistent with a previously posed hypothesis based on different species than we measured. T HE history of cognitive research in animals is long, but not particularly comparative between species, which has resulted in biases toward model organisms (e.g., rats, pigeons, and some primates; Huber and Wilkinson, 2012). Relatively few studies have considered the non-avian reptiles (see reviews by Wilkinson and Huber, 2012, and Miletto Petrazzini et al., 2017). With regard to non-avian reptiles, there is the often-repeated notion that monitor lizards (Varanidae) are intrinsically intelligent, being top predators in most of the ecosystems they occupy (King and Green, 1999; Burghardt et al., 2002; Bennett, 2004; Pianka and Sweet, 2016). Other reptiles have received scant attention. In this study, we compare cognitive performance in three species of Varanus, the phylogenetically proximal outgroup Heloderma (beaded lizards), and the more distantly related iguanid Cyclura, representing a broad phylogenetic diversity. Our results allow us to make preliminary comments on the generality of cognitive performance across Varanidae, as well as initial outgroup comparisons to allow a broader phylogenetic perspective of cognition in lizards. With only small sample sizes being available for each of our focal species, our aim was to document the relative levels of basic cognitive learning using a simple test. The key literature on varanid cognition includes only a single study (Firth et al., 2003) that compared multiple species using the same design, and no studies that compared both varanid and non-varanid species. Firth et al. (2003) reported that three individuals each of V. albigularis, V. exanthematicus, and V. niloticus showed reduced times to locate food placed, but not hidden, at the opposite end of their enclosure over repeated trials. Gaalema (2011) reported visual discrimination (black vs. white) and reversal learning in two individuals of V. rudicollis. Manrod et al. (2008) reported reduced latencies among eight individuals of V. albigularis over three trials in solving a transparent hinged-door puzzle-feeder device to access living mice within. Loop (1976) reported improved successes over time, but not strictly latencies, of conditioned responses to illumination cues associated with food rewards in four individuals of V. bengalensis. Mendyk and Horn (2011), using two individuals of V. beccarii, described consistent manual reaching, grasping, and retrieval of prey items located in crevices or holes too small to accommodate the head. Finally, an unpublished study on quantitative discrimination by J. Kaufman and A. Phillips and colleagues is often referenced in the varanid lizard literature. These previous studies support the contention that varanid lizards have substantial cognitive abilities. Building on this body of work, we also used varanid lizards as model organisms for our cognitive research and included outgroup comparisons with species of Heloderma (Helodermatidae) and Cyclura (Iguanidae). We used a puzzle-feeder device, somewhat similar to that of Manrod et al. (2008), to measure latencies of successful problem-solving events over repeated trials to compare cognitive performance across three species of Varanus and one each of Heloderma and Cyclura. We used species of Varanus widely distributed phylogenetically within the genus to test the level of generality of our data within the group. Similarly, our outgroup taxa were included in order to compare cognitive performance on a broader scale in squamates.
... Cognitive skills are the process that animals acquire, handle, and store information from the environment, and their cognitive abilities refer to the ways that they can act upon this information [73]. The varanid's higher intelligence has long been recognized [74][75][76], along with their curiosity, perceptiveness, apparent ability to recognize different keepers [56,61], and ability to be successfully target trained [32,77]. Experiments carried out on captive V. albigularis even suggest that they may have counting-like skills as they appeared to be able to count to six [78], which is theorized to be attributed to raiding the nests of other reptiles, birds, and mammals, given that the average clutch or litter size would be around six [61]. ...
... The cognitive abilities of monitor lizards have been studied a handful of times, concluding that this genus is capable of problem solving and rapid learning [75,[83][84][85], as well as reversal learning [86] and procedural learning [76]. Considering their biology and ecology, varanids, with excellent eyesight and active predatory foraging ability, would be expected to learn and respond to visual stimuli. ...
... albigularis) can become more efficient at solving food-based puzzles by reducing unnecessary behaviors that do not result in success [85]. Cooper et al. [75] found evidence of problem solving using puzzle feeders in three species of monitor lizards-V. rudicollis, V. prasinus, and V. mertensi. ...
Enrichment has become a key aspect of captive husbandry practices as a means of improving animal welfare by increasing environmental stimuli. However, the enrichment methods that are most effective varies both between and within species, and thus evaluation underpins successful enrichment programs. Enrichment methods are typically based upon previously reported successes and those primarily with mammals, with one of the main goals of enrichment research being to facilitate predictions about which methods may be most effective for a particular species. Yet, despite growing evidence that enrichment is beneficial for reptiles, there is limited research on enrichment for Varanidae, a group of lizards known as monitor lizards. As a result, it can be difficult for keepers to implement effective enrichment programs as time is a large limiting factor. In order for appropriate and novel enrichment methods to be created, it is necessary to understand a species’ natural ecology, abilities, and how they perceive the world around them. This is more difficult for non-mammalian species as the human-centered lens can be a hinderance, and thus reptile enrichment research is slow and lagging behind that of higher vertebrates. This review discusses the physiological, cognitive, and behavioral abilities of Varanidae to suggest enrichment methods that may be most effective.
... Some studies and reviews (e.g., Striedter, 2015) embrace the fact that birds are, in fact, reptiles, whereas others (e.g., Wilkinson and Huber, 2012;Roth et al., 2019) discuss results comparing birds to the nonmonophyletic assemblage of nonavian reptiles. In any case, there have been relatively few behavioral studies on cognition in squamate reptiles, relative to birds and mammals (e.g., Day et al., 1999;Manrod et al., 2008;LaDage et al., 2012LaDage et al., , 2017Cooper et al., 2019). The taxonomic imbalance in the number of studies of mammals and birds versus nonavian reptiles is problematic because, as brain anatomy underlies brain function (Rodriguez et al., 2002;Striedter, 2015;Tosches et al., 2018), the knowledge of homologous regions in the brain among organisms underlies our abilities to recognize homologous behaviors (Greene, 1994), or homologous abilities in cognition (e.g., Finn, 2017;Murray et al., 2018). ...
... Varanids are good candidates for longterm memory given that they live a relatively long time, approximately 10-20 yr (Mendyk, 2015), and maintain large territories in complex environments, with evidence that they learn about these landscapes (Auffenberg, 1981(Auffenberg, , 1988(Auffenberg, , 1994Sweet, 1999;Pianka et al., 2004;Sweet, 2007). Previous work has also demonstrated learning and problem-solving abilities in the clade (e.g., Burghardt et al., 2002;Manrod et al., 2008;Gaalema, 2011;Mendyk and Horn, 2011;Cooper et al., 2019). Considered together, these characteristics suggest that varanids may be capable of developing long-term memory (sensu Snell-Rood, 2013) related to a problem-solving task. ...
... Considered together, these characteristics suggest that varanids may be capable of developing long-term memory (sensu Snell-Rood, 2013) related to a problem-solving task. We had no precon-ceived notions regarding Heloderma, as the only cognitive work with those lizards of which we are aware was by Cooper et al. (2019). ...
Procedural memory allows animals to solve previously encountered tasks over weeks, months, or years efficiently. Although thoroughly documented in vertebrate clades such as mammals and birds, studies of procedural memory in squamate reptiles are lacking. Filling the gap in knowledge regarding procedural memory in squamates is important to understanding the degree to which procedural memory is unique to birds and mammals, as it is related to their unique cognitive abilities. We tested for memory of a problem-solving task in two species of monitor lizard (Varanus spp.) and a beaded lizard (Heloderma sp.) after a 20-mo hiatus in exposure, representing approximately 25% of their ages at the time of testing. All the monitor lizards had lower initial latencies to solve the task upon re-exposure posthiatus than they had as naïve individuals during the prehiatus trials and reached minimum latencies in fewer trials than when previously tested. Our results indicate procedural memory of puzzle-solving behaviors on the time scales of years. Our results add to an emerging literature suggesting that squamate and other nonavian reptiles share a number of cognitive traits with birds and mammals, suggesting that such traits are far more widespread across taxa than previously recognized. We also discuss a framework for studying cognition in squamates that would allow tests of cognition across a great diversity of body forms and ecologies.
... Krochmal et al. (2018) found that seven species of rattlesnakes all uniformly and consistently habituated to a thermal maze after a single trial, while none of the six non-rattlesnake pit viper species decreased their latency to make a decision in the maze across twelve trials. Another study showed that three species of monitor lizards all learnt a problem-solving task (Figure 1D) faster than the closely-related Guatemalan beaded lizard (Heloderma charlesbogerti) which the authors contributed to the active foraging style of monitor lizards (Cooper et al., 2019). In contrast to Krochmal et al. (2018), however, Cooper and colleagues reported considerable variation among and within species. ...
... Lizards as focal study animals in cognitive biological research: (a) testing flexibility on a shape discrimination task in tree skinks (Egernia striolata) (fromSzabo et al., 2018); (b) a leopard fringe-fingered lizard (Acanthodactylus pardalis) being tested on a colour discrimination task(from De Meester et al., unpublished); (c) a lid-removal task to assess problem-solving ability in Aegean wall lizards (Podarcis erhardii) (from De Meester et al., 2021); (d) a Guatemalan beaded lizard (Heloderma charlesbogerti) solving an extractive foraging task (fromCooper et al., 2019); (e) a Barnes maze to test spatial memory ability and cue use in side-blotched lizards (Uta transburiana) (fromLadage et al., 2012); (f) an anole lizard (Anolis evermanni) performing a colour-based discrimination trial (fromLeal & Powell, 2012). All pictures were reproduced with permission of the original authors. ...
Non-avian reptiles have long been neglect in cognitive science due to their reputation as slow and inflexible learners, but fortunately, this archaic view on reptile cognition is changing rapidly. The last two decades have witnessed a renewed interest in the cognitive capacities of reptiles, and more ecologically relevant protocols have been designed to measure such abilities. Now, we appreciate that reptiles possess an impressive set of cognitive skills, including problem-solving abilities, fast and flexible learning, quantity discrimination, and even social learning. This special issue highlights current research on reptiles in cognitive biology and showcases the diversity of research questions that can be answered by using reptiles as study model. Here, we briefly address (the key results of) the contributing articles and their role in the endeavour for total inclusion of reptiles in cognitive biological research, which is instrumental for our understanding of the evolution of animal cognition. We also discuss and illustrate the promising potential of reptiles as model organisms in various areas of cognitive research.
... Studies on reptile sentience (e.g. for reviews, see Lambert et al. 2019;Learmonth 2020), cognition (e.g. Cooper et al. 2019;Font 2019Font , 2020Burghardt 2020;LaDage et al. 2012;Szabo et al. 2021), play (e.g. Burghardt 2005Burghardt , 2013Burghardt , 2015Dinets 2015;Kane et al. 2019), and complex sociality (e.g. ...
Zoos and aquaria are paying increasing attention to environmental enrichment, which has proven an effective tool for the improvement of animal welfare. However, several ongoing issues have hampered progress in environmental enrichment research. Foremost among these is the taxonomic bias, which hinders our understanding of the value of enrichment for neglected groups, such as reptiles. In this study, we evaluated the status of environmental enrichment for reptiles in European zoos using a survey approach. A total of 121 zoos (32% response rate) completed our main survey, focusing on the use of different enrichment types for reptiles. We found significant differences in the use and/or type of enrichment between reptile groups. Tortoises (family Testudinidae) and monitor lizards (genus Varanus) were the most enriched taxa while venomous snakes were the least. The enrichment types most used across taxa were structural/habitat design and dietary. A second, more detailed, questionnaire followed, where participants were questioned about specific enrichment techniques. A total of 42 enrichment methods were reported, with two being represented across all taxa: increasing structural/thermal complexity and enrichment objects. Finally, we present information from participating zoos on enrichment goals, assessment methods, sources of information for enrichment ideas, and whether enrichment for reptiles is considered essential and/or implemented routinely. Results suggest that, although usage is widespread across European zoos, our understanding of enrichment for reptiles needs to be re-evaluated, since many of the techniques reported tread a fine line between basic husbandry and actual enrichment.
... One possible explanation is insufficient training session for the subjects to learn the association between the light stimulus and food reward. In learning studies of other lizards, large numbers of trainings (sometimes more than 20 times) were performed on each individual (e.g., Day et al., 2003;Leal and Powell, 2012;Clark et al., 2014;Qi et al., 2018;Batabyal and Maria, 2019;Cooper et al., 2019). Although we performed trainings for several consecutive days, Japanese geckos may need more experiences to establish a strong associative learning between a light cue and food reward. ...
Nocturnal predators of many taxa are known to come to artificial light at night for foraging on clumped food resources. Both innate and acquired light preferences seem to be possible mechanisms of light approaching behavior although empirical tests are lacking in most nocturnal predators. Here, using a Japanese gecko Gekko japonicus, we investigated whether geckos have a light preference and how foraging experiences under the light reinforce light approaching tendency. In a comparative experiment, there was no difference in light approaching behavior between urban and suburban geckos irrespective of their original light habitats. In an associative learning experiment, geckos did not significantly change light approaching behavior even after repeated opportunities to forage crickets near a lamp in the laboratory setting. These results imply that light approaching behavior of Japanese geckos may not be easily reinforced by foraging experiences under the light. Although we often witness geckos coming to artificial light at night, our findings may not suggest their light preference. Geckos may approach the light-up foraging spot based on other cues relating to the artificial light environment.
... The ability to acquire, process, remember, and act upon information from the environment, that is, cognition, is of vital importance to animals (Shettleworth 2010). Cognitive skills, such as learning and problem-solving, help animals finding food (e.g., Cooper et al. 2019), avoiding predators (e.g., Font 2019), locating and recognizing conspecifics and potential Lisa Van Linden and Gilles De Meester should be considered joint first author. ...
Cognition is an essential tool for animals to deal with environmental challenges. Nonetheless, the ecological forces driving the evolution of cognition throughout the animal kingdom remain enigmatic. Large‐scale comparative studies on multiple species and cognitive traits have been advanced as the best way to facilitate our understanding of cognitive evolution, but such studies are rare. Here, we tested 13 species of lacertid lizards (Reptilia: Lacertidae) using a battery of cognitive tests measuring inhibitory control, problem‐solving, and spatial and reversal learning. Next, we tested the relationship between species’ performance and a) resource availability (temperature and precipitation), habitat complexity (NDVI) and habitat variability (seasonality) in their natural habitat, and b) their life‐history (size at hatching and maturity, clutch size and frequency). Although species differed markedly in their cognitive abilities, such variation was mostly unrelated to their ecology and life‐history. Yet, species living in more variable environments exhibited lower behavioural flexibility, likely due to energetic constrains in such habitats. Our standardised protocols provide opportunities for collaborative research, allowing increased sample sizes and replication, essential for moving forward in the field of comparative cognition. Follow‐up studies could include more detailed measures of habitat structure and look at other potential selective drivers such as predation. This article is protected by copyright. All rights reserved
... Problem solving requires animals to express a new behaviour or apply an old behaviour in a novel context and is therefore considered an indicator of behavioural flexibility (Griffin & Guez, 2014;Tebbich & Teschke, 2014; but see Audet & Lefebvre, 2017). Lizards with better problem-solving skills may increase their foraging efficiency, e.g. by being better at extracting hidden or difficult prey (Cooper et al., 2019). We tested problem solving using an escape box task (Supplementary Figs. ...
Recently, biologists have become increasingly interested in cognitive variation among individuals and how it relates to differences in fitness. However, very few studies so far have studied the long-term repeatability and heritability of cognitive performance in wild animals. This is nevertheless crucial information to fully understand the potential ecological and evolutionary impact of individual variation in cognitive performance. In 2019, we assessed exploration, problem solving and spatial and reversal learning in 66 Aegean wall lizards, Podarcis erhardii, then released them in seminatural enclosures consisting of either simple or complex habitat. One year later, we recaptured and retested the surviving lizards and their offspring to estimate the long-term repeatability and heritability of these behavioural and cognitive characteristics. We found that exploration and spatial learning were moderately repeatable, but reversal learning only marginally and learning flexibility and problem solving not at all. Reversal learning ability declined over time in lizards kept in simple habitat, but not in those kept in complex habitats – suggesting habitat-dependent cognitive plasticity. To our knowledge, this is the first study demonstrating (long-term) consistency in cognitive traits within a nonavian reptile. The combination of modest repeatability and low heritability does suggest that, within our study species, personality and cognitive variation among individuals and populations is mostly moulded by environmental effects.
... Importantly, if latency is used as a measure of learning (e.g. Amiel and Shine 2012;Chung et al. 2017;Cooper et al. 2019) researchers need to be aware of how the testing procedure might affect latency measures. If individual lizards experience testing as more stressful and respond slowly, results might be negative, concluding that lizards did not learn when in fact the procedure was not suitable and confounded the results. ...
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.
... Indeed, navigating through a spatially complex habitat, keeping track of resources and hazards, is likely to be cognitively demanding, because it requires processing and storing large amounts of useful information (Safi and Dechmann 2005;Powell and Leal 2014;Calisi et al. 2017) while filtering out vast quantities of irrelevant background data (Shumway, 2008;Steck and Snell-Rood 2018). As a consequence, structured habitats are believed to select for superior spatial cognition (White and Brown 2014), learning flexibility (Clarin et al. 2013), and problem-solving abilities (Mettke-Hofman 2014; Cooper et al. 2019). ...
Animals exhibit considerable and consistent among-individual variation in cognitive abilities, even within a population. Recent studies have attempted to address this variation using insights from the field of animal personality. Generally, it is predicted that animals with “faster” personalities (bolder, explorative, and neophilic) should exhibit faster but less flexible learning. However, the empirical evidence for a link between cognitive style and personality is mixed. One possible reason for such conflicting results may be that personality–cognition covariance changes along ecological conditions, a hypothesis that has rarely been investigated so far. In this study, we tested the effect of habitat complexity on multiple aspects of animal personality and cognition, and how this influenced their relationship, in five populations of the Aegean wall lizard (Podarcis erhardii). Overall, lizards from both habitat types did not differ in average levels of personality or cognition, with the exception that lizards from more complex habitats performed better on a spatial learning task. Nevertheless, we found an intricate interplay between ecology, cognition, and personality, as behavioral associations were often habitat- but also year-dependent. In general, behavioral covariance was either independent of habitat, or found exclusively in the simple, open environments. Our results highlight that valuable insights may be gained by taking ecological variation into account while studying the link between personality and cognition.
... First, V. gouldii appears able to exploit prey odours (Garrett and Card 1993;Garrett et al. 1996), using its forked tongue to detect prey infochemicals before digging prey such as insects or small mammals from their burrows or under leaf litter (Pianka 1970(Pianka , 1994Thompson 1995). Prey is likely to be hunted once detected provided that it returns a net energetic gain (Losos and Greene 1988;Kaufman et al. 1996), with individuals rapidly learning new foraging techniques to reach detectable but not freely available foods (Cooper et al. 2019). In one study V. gouldii focussed its activity around the nests of a large (200-300 g) rodent, the greater stick-nest rat Leporillus conditor, apparently because the smell of the rats' urine signalled a potential food source (Bolton and Moseby 2004). ...
An important but understudied modality for eavesdropping between predators and prey is olfaction, especially between non-mammalian vertebrate predators and their prey. Here we test three olfactory eavesdropping predictions involving an apex reptilian predator, the sand goanna Varanus gouldii , and several species of its small mammalian prey in arid central Australia: 1) small mammals will recognise and avoid the odour of V. gouldii ; 2) V. gouldii will be attracted to the odour of small mammals, especially of species that maximise its energetic returns; and 3) small mammals will be less mobile and will show higher burrow fidelity where V. gouldii is absent compared with where it is present. As expected, we found that small mammals recognised and avoided faecal odour of this goanna, feeding less intensively at food patches where the odour of V. gouldii was present than at patches with no odour or a pungency control odour. Varanus gouldii also was attracted to the odour of small mammals in artificial burrows, and dug more frequently at burrows containing the odour of species that were energetically profitable than at those of species likely to yield diminished returns. Our third prediction received mixed support. Rates of movement of three species of small mammals were no different where V. gouldii was present or absent, but burrow fidelity in two of these species increased as expected where V. gouldii had been removed. We conclude that olfaction plays a key role in the dynamic interaction between V. gouldii and its mammalian prey, with the interactants using olfaction to balance their respective costs of foraging and reducing predation risk. We speculate that the risk of predation from this apex reptilian predator drives the highly unusual burrow-shifting behaviour that characterises many of Australia's small desert mammals.
... Prey is likely to be hunted once detected and provided that it returns a net energetic gain (Losos and Greene 1988). Varanids have even been observed to rapidly learn appropriate foraging techniques to reach detectable but not freely available food sources (Cooper et al. 2019). In one study, V. gouldii was found to be attracted to the nests of a large (200-300 g) Australian rodent, the greater stick-nest rat Leporillus conditor (Bolton and Moseby 2004). ...
An important but understudied modality for eavesdropping between predators and prey is olfaction, especially between non-mammalian vertebrate predators and their prey. Here we test three olfactory eavesdropping predictions involving an apex reptilian predator, the sand goanna Varanus gouldii , and several species of its small mammalian prey in arid central Australia. Firstly, as expected, we found that small mammals recognised and avoided the faecal odour of sand goannas, feeding less intensively at food patches where the odour of V. gouldii was present than at patches with no odour or a pungency control odour. Secondly, V. gouldii was attracted to the odour of small mammals in artificial burrows, and dug more frequently at burrows containing the odour of species that were energetically profitable than at those of species likely to yield diminished returns. Our third prediction received mixed support. Rates of movement of three species of small mammals were no different where V. gouldii was present or absent, but burrow fidelity in two of these species increased as expected in an area where V. gouldii had been removed. We conclude that olfaction plays a key role in the dynamic interaction between V. gouldii and its mammalian prey, with the interactants using olfaction to balance their respective costs of foraging and reducing predation risk. We speculate that the risk of predation from this apex reptilian predator drives the marked and highly unusual burrow-shifting behaviour that characterises many of Australia's small desert mammals.
... Problem-solving abilities are expected to help individuals to exploit new resources or familiar ones in a more efficient way (Greenberg, 2003;Griffin et al., 2016). In species with an active foraging style, such as Podarcis erhardii, problem-solving may help individuals to increase their foraging efficiency, e.g., by being able to extract otherwise inaccessible prey (Cooper et al., 2019;Henke-von der Malsburg et al., 2020). This may be particularly beneficial in periods of food scarcity. ...
Harsh and variable environments have been hypothesized to both drive and constrain the evolution towards higher cognitive abilities and behavioural flexibility. In this study, we compared the cognitive abilities of island and mainland Aegean wall lizards ( Podarcis erhardii ), which were expected to live in respectively a more variable and a more stable habitat. We used four proxies of behavioural flexibility: a neophobia assay, a problem-solving test and a spatial + reversal learning task. Surprisingly, the two populations did not differ in neophobia or problem-solving. Insular lizards, however, outperformed mainland conspecifics in an initial spatial learning task, but were less successful during the subsequent reversal learning. Our results thus seem to indicate that the effect of environmental variability on cognition is complex, as it may favour some, but not all aspects of behavioural flexibility.
... In the case of apex predators, does the arrival of a toxic invasive species alter attack strategies and/or cognitive skills? Lizards of the family Varanidae (monitor lizards, "goannas") are apex predators across much of Australia (Sutherland et al. 2011) and appear to have more advanced cognitive skills than do most other reptiles, with captive specimens rapidly learning complex tasks (e.g., Manrod et al. 2008;Cooper et al. 2019). Also, a single population of varanids may contain individuals with a wide variety of "personality" types that differ along continua such as boldness-shyness, activity levels and neophobia (Ward-Fear et al. 2018) that affect a variety of ecological traits including an individual's vulnerability to invasive toads (Ward-Fear et al. 2020). ...
Variation in morphological, genetic, or behavioural traits within and among native species can modify vulnerability to impacts from an invasive species. If an individual’s vulnerability depends upon its cognitive performance, we may see adaptive shifts in cognitive traits post-invasion. Commonly, animals with enhanced cognitive abilities perform better in novel tasks, often by prioritising decision accuracy over decision speed. In eastern Australia, giant monitor lizards (Varanus varius) are fatally poisoned if they ingest invasive cane toads (Rhinella marina), but vulnerability is lower for individuals that carefully evaluate the novel prey type before swallowing it. To test if toad-imposed selection for neophobia and caution affected cognitive performance, we tested free-ranging monitors with a device that required lizards to manipulate the apparatus in order to obtain food. Success at accomplishing that task, and the speed of that success, was lower and slower in lizards from long-colonised sites than from uninvaded sites. Our results suggest that toad invasion has modified cognitive phenotypes within populations of this apex predator, a change that might have substantial effects on other species.
Significance statement
Many studies of the impacts of biological invasions focus on the numerical effect of an invader on the abundances of native taxa, neglecting other types of impacts. Colonising taxa can also impose selection on behavioural traits of native species, generating shifts in behaviour as native taxa adapt to intruders. Such shifts in behaviour are interesting not only in their own right but also because such shifts (especially in apex predators) may influence other taxa within food webs. Importantly, the nature and magnitude of such shifts may change over time post-invasion.
Predation of nests and hatchlings can significantly reduce sea turtle reproductive output. On Cavalos island, Joo Vieira and Poilo Marine National Park, Bijagos archipelago, Guinea-Bissau, one of the primary threats to green turtle nests is predation by Nile monitors (Varanus niloticus). In this study, we tested 3 different nest protection techniquesdisguising scent cues, disguising visual cues, and placing a metal net over the nestto reduce predation on green turtle (Chelonia mydas) nests by Nile monitors. Nests were monitored for 10 d after they were laid, and we found that using metal nets and disguising scent cues led to a significant increase of the number of days it took for Nile monitors to find and predate the nests. Overall reduction in predation rates also approached significance when metal nets or disguising scent cues were used. We used the Risk Reduction metric to compare the effectiveness of our experiment with other nest protection techniques; our results corresponded to a > 50% decrease in the risk of predation, a value comparable to or better than other techniques used elsewhere. We suggest that camouflaging a nest's scent may be the most cost-efficient management option to reduce predation rates by Nile monitors in sensitive areas without damaging the local ecosystem.
An important but understudied modality for eavesdropping between predators and prey is olfaction, especially between non-mammalian vertebrate predators and their prey. Here we test three olfactory eavesdropping predictions involving an apex reptilian predator, the sand goanna Varanus gouldii, and several species of its small mammalian prey in arid central Australia: 1) small mammals will recognize and avoid the odour of V. gouldii; 2) V. gouldii will be attracted to the odour of small mammals, especially of species that maximize its energetic returns; and 3) small mammals will be less mobile and will show higher burrow fidelity where V. gouldii is absent compared with where it is present. As expected, we found that small mammals recognized and avoided faecal odour of this goanna, feeding less intensively at food patches where the odour of V. gouldii was present than at patches with no odour or a pungency control odour. Varanus gouldii also was attracted to the odour of small mammals in artificial burrows and dug more frequently at burrows containing the odour of species that were energetically profitable than at those of species likely to yield diminishing returns. Our third prediction received mixed support. Rates of movement of three species of small mammals were no different where V. gouldii was present or absent, but burrow fidelity in two of these species increased as expected where V. gouldii had been removed. We conclude that olfaction plays a key role in the dynamic interaction between V. gouldii and its mammalian prey, with the interactants using olfaction to balance their respective costs of foraging and reducing predation risk. We speculate that the risk of predation from this apex reptilian predator drives the highly unusual burrow-shifting behaviour that characterizes many of Australia's small desert mammals.
Young, Clark, Goffus, and Hoane (Learning and Motivation, 40(2), 160-177, 2009) documented significant advantages of linear and nonlinear mixed-effects modeling in the analysis of Morris water maze data. However, they also noted a caution regarding the impact of the common practice of ending a trial when the rat had not reached the platform by a preestablished deadline. The present study revisits their conclusions by considering a new approach that involves multilevel (i.e., mixed effects) censored generalized linear regression using Bayesian analysis. A censored regression explicitly models the censoring created by prematurely ending a trial, and the use of generalized linear regression incorporates the skewed distribution of latency data as well as the nonlinear relationships this can produce. This approach is contrasted with a standard multilevel linear and nonlinear regression using two case studies. The censored generalized linear regression better models the observed relationships, but the linear regression created mixed results and clearly resulted in model misspecification.
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 precondition for social learning. Past research has demonstrated that non-avian reptiles are capable of more than just instinctive reactions and basic cog-nition. 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.
The ability to identify the largest amount of prey available is fundamental for optimizing foraging behaviour in several species. To date, this cognitive skill has been observed in all vertebrate groups except reptiles. In this study we investigated the spontaneous ability of ruin lizards to select the larger amount of food items. In Experiment 1, lizards proved able to select the larger food item when presented with two alternatives differing in size (0.25, 0.50, 0.67 and 0.75 ratio). In Experiment 2 lizards presented with two groups of food items (1 versus 4, 2 versus 4, 2 versus 3 and 3 versus 4 items) were unable to select the larger group in any contrast. The lack of discrimination in the presence ofmultiple items represents an exception in numerical cognition studies, raising the question as to whether reptiles' quantitative abilities are different from those of other vertebrate groups. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
The genetic underpinnings associated with the earliest stages of plant and animal domestication have remained elusive. Because a genome-wide response to selection can take many generations, the earliest detectable changes associated with domestication may first manifest as heritable changes to global patterns of gene expression. Here, to test this hypothesis, we measured differential gene expression in the offspring of wild and first-generation hatchery steelhead trout (Oncorhynchus mykiss) reared in a common environment. Remarkably, we find that there were 723 genes differentially expressed between the two groups of offspring. Reciprocal crosses reveal that the differentially expressed genes could not be explained by maternal effects or by chance differences in the background levels of gene expression among unrelated families. Gene-enrichment analyses reveal that adaptation to the novel hatchery environment involved responses in wound healing, immunity and metabolism. These findings suggest that the earliest stages of domestication may involve adaptation to highly crowded conditions.
Food location times have been recorded in three captive monitor lizards (Varanus spp.). The results, in the form of regression equations, showed that in general the time taken to locate the food decreased with the number of times the food was offered. ITTLE work has been carried out on learning in varanid lizards (Phillips, 1994; Horn, 1999) which is perhaps surprising given their general impression of alertness even to the casual observer. We devised a simple experiment using food as a positive reinforcer to evaluate association learning in three adult monitor lizards from three species, Varanus niloticus ornatus, V. albigularis and V. exanthematicus. We used monitor lizards for two reasons. Firstly there was always a good response to food as a stimulus in our research animals. The second reason was that many types of monitor lizards are intense active foraging predators (Regal, 1978) travelling large distances in their search for food (Thompson & Withers, 1997; Thompson, 1999 and Bennett, 1998 for a review). We predicted that this behaviour, combined with the interest in food, increased the probability of the experiments giving meaningful results. The work was part of a second year HND research project on animal behaviour at Huddersfield Technical College carried out by IF, MT and MR under the supervision of RM. METHODS AND MATERIALS A variety of assumptions must be made when selecting methods of evaluating learning in animals. The method employed here was based on
The beaded lizard (Heloderma horridum) is a large diurnal predator that feeds predominantly on juveniles in vertebrate nests and eggs. Bird eggs constitute a special problem for predators as the energetic content is shielded by a hard calcareous shell. Still, eggs of ground nesting birds such as quail constitute a large part of the diet of Heloderma horridum. We investigated the mechanics of the egg eating behavior in H. horridum. We examined the morphology of the feeding system, measured egg toughness, and calculated bite forces of H. horridum. Additionally, we videotaped feeding sequences and simultaneously recorded the activity patterns of the jaw muscles. Egg eating behavior consists of a fixed behaviorial pattern including five distinct stages: approach, piercing, uptake, crushing, and swallowing. Two of these (piercing and crushing) can be directly related to the egg eating behavior in H. horridum. The piercing stage consists of several bites during which the anterior teeth are used to puncture (but not crush) the egg. Next, during the crushing stage the egg is crushed within the oral cavity (no longer any tooth contact). Based on our results, we conclude that behaviorial adaptations and subtle modifications of the motor patterns during feeding are present in H. horridum which allow the lizard to be an efficient ovophageous predator.
We describe two new species of morphologically cryptic monitor lizards (genus Varanus) from the Philippine Archipelago: Varanus dalubhasa sp. nov. and V. bangonorum sp. nov. These two distinct evolutionary lineages are members of the V. salvator species complex, and historically have been considered conspecific with the widespread, northern Philippine V. marmoratus. However, the new species each share closer phylogenetic affinities with V. nuchalis (and potentially V. palawanensis), than either does to one another or to V. marmoratus. Divergent from other recognized species within the V. salvator Complex of water monitors by as much as 3.5% pairwise genetic distance, these lineages are also distinguished by unique gular coloration, metrics of body size and scalation, their non-monophyly with "true" V. marmoratus, and insular allopatric distributions, suggesting biogeographically distinct and unique evolutionary histories. We compare the new species with the most geographically proximate and phenotypically relevant lineages. Although we show that these new taxa are nearly indistinguishable morphologically from V. marmoratus, both species can be readily distinguished from their closest relatives (each's respective sister taxon, V. palawanensis and V. nuchalis) by traditional morphological characters. Our findings underscore the high herpetological diversity and biogeographical complexity of vertebrates in the Philippines, and further emphasize the need for detailed study of species-level diversity, mechanisms of reproductive isolation, gene flow, and biologically relevant boundaries between taxa within the V. salvator Complex.
We compared six methods for regression on log-normal heteroscedastic data with respect to the estimated associations with explanatory factors (bias and standard error) and the estimated expected outcome (bias and confidence interval). Method comparisons were based on results from a simulation study, and also the estimation of the association between abdominal adiposity and two biomarkers; C-Reactive Protein (CRP) (inflammation marker,) and Insulin Resistance (HOMA-IR) (marker of insulin resistance). Five of the methods provide unbiased estimates of the associations and the expected outcome; two of them provide confidence intervals with correct coverage.
Many wildlife species are propagated in captivity as models for behavioral, physiological, and genetic research or to provide assurance populations to protect threatened species. However, very little is known about how animals evolve in the novel environment of captivity. The histories of most laboratory strains are poorly documented, and protected populations of wildlife species are usually too small and too short-term to allow robust statistical analysis. To document the evolutionary change in captive breeding programs, we monitored reproduction and behavior across 18 generations in six experimental populations of Peromyscusleucopus mice started from a common set of 20 wild-caught founders. The mice were propagated under three breeding protocols: a strategy to retain maximal genetic diversity, artificial selection against stereotypic behaviors that were hypothesized to reflect poor adaptation to captivity, and random bred controls. Two replicates were maintained with each protocol, and inter-replicate crosses at generations 19 and 20 were used to reverse accumulated inbreeding. We found that one of the stereotypic behaviors (repetitive flipping) was positively associated with reproductive fitness, while the other (gnawing) was relatively invariant. Selection to reduce these stereotypic behaviors caused marked reduction in reproduction, and populations not under artificial selection to reduce these behaviors responded with large increases in flipping. In non-selected populations, there was rapid evolution toward much higher proportion of pairs breeding and more rapid conception. Litter size, pup survival, and weaning mass all declined slowly, to the extent that would be predicted based on inbreeding depression. Inter-crossing between replicate populations reversed these declines in fitness components but did not reverse the changes in behavior or the accelerated breeding. These findings indicate that adaptation to captivity can be rapid, affecting reproductive patterns and behaviors, even under breeding protocols designed to minimize the rate of genetic change due to random drift and inadvertent selection.
Squamate reptiles (lizards and snakes) are one of the most diverse groups of terrestrial vertebrates. Recent molecular analyses have suggested a very different squamate phylogeny relative to morphological hypotheses, but many aspects remain uncertain from molecular data. Here, we analyse higher-level squamate phylogeny with a molecular dataset of unprecedented size, including 161 squamate species for up to 44 nuclear genes each (33 717 base pairs), using both concatenated and species-tree methods for the first time. Our results strongly resolve most squamate relationships and reveal some surprising results. In contrast to most other recent studies, we find that dibamids and gekkotans are together the sister group to all other squamates. Remarkably, we find that the distinctive scolecophidians (blind snakes) are paraphyletic with respect to other snakes, suggesting that snakes were primitively burrowers and subsequently re-invaded surface habitats. Finally, we find that some clades remain poorly supported, despite our extensive data. Our analyses show that weakly supported clades are associated with relatively short branches for which individual genes often show conflicting relationships. These latter results have important implications for all studies that attempt to resolve phylogenies with large-scale phylogenomic datasets.
Evolutionary biology has uncovered remarkable anatomical and physiological similarities among animal species (including humans). The most parsimonious assumption is that they may also share some cognitive and behavioural traits. This idea was put forward by Charles Darwin, who suggested that humans are not separated from the animal kingdom in terms of cognition, but rather, that there is mental continuity across species. This hypothesis has now transformed into the flourishing field of Cognitive Biology, which examines the cognitive abilities of nonhuman animals from a comparative perspective. In this chapter we describe the historical roots of the field and discuss why an evolutionary account alone is insufficient for a full understanding of cognition in animals. We emphasize the importance of studying a behaviour at four different levels: phylogeny (history), adaptation (ultimate function), proximate mechanisms (neurosciences) and development (ontogeny) before it can be entirely understood. Finally we review a selected subset of recent results and discuss their implications for our understanding of the evolution of cognition.
Reptile learning has been studied with a variety of methods and has included numerous species. However, research on learning in lizards has generally focused on spatial memory and has been studied in only a few species. This study explored visual discrimination in two rough-necked monitors (Varanus rudicollis). Subjects were trained to discriminate between black and white stimuli. Both subjects learned an initial discrimination task as well as two reversals, with the second reversal requiring fewer sessions than the first. This reduction in trials required for reversal acquisition provides evidence for behavioral flexibility in the monitor lizard genus.
It is widely accepted that providing stimulus enrichment is an important part of the development and maintenance of behavior and well-being in mammals. However, extending this idea to non-avian reptiles has barely been explored, certainly as an aid to cognitive development. Monitor lizards have a reputation for being highly curious and intelligent lizards, but quantitative experiments are necessary to evaluate such impressions as well as the value of providing enrichment to captive squamate reptiles. In this study eight juvenile black-throated monitors, Varanus albigularis, were tested in their home enclosures with three presentations, at weekly intervals, of a novel task apparatus: a transparent food tube containing several prey. The food tube allowed the monitors to obtain prey by using hinged doors at either end of the tube to access food. All eight lizards learned to open the tube, insert head, and capture the prey within 10 min in the first trial. By the second trial, both mean latencies to access the tube and capture the first prey item decreased significantly, as did the use of ineffective responses such as shaking the tube. A further slight decrease occurred in the third trial. Due to the results of this and similar studies, serious consideration should be given to further testing of cognitive abilities in squamate reptiles. Incorporating problem solving tasks may also be useful to increase the activity level and captive well-being of squamate reptiles, especially monitor lizards.
We report on the aquatic and terrestrial foraging behaviour and diet of the semi-aquatic Varanus mertensi. Foraging behaviour of V. mertensi is similar to that of other large terrestrial varanids: slow, methodical forwards movement with the head swaying from side to side with regular tongue flicks. Both olfactory and visual cues are used to detect prey. Foraging in the water is remarkably similar to that in the terrestrial environment, with this species using both visual and olfactory cues. Like other varanids, this species is able to use previous experiences to maximise its chance of locating prey. V. mertensi consume a large number of freshwater crabs (Holthuisana sp.) and a variety of small invertebrate and vertebrate prey across their distribution. Dietary differences across geographic regions are minor. Its diet is sufficiently catholic to enable it to adapt to seasonal and spatial differences in prey availability, one reason for its widespread distribution in the wet - dry tropics of Australia. Stomach contents differ from those of scats, with soft-bodied prey items being absent from scat samples.
Behavioral complexity, behavioral development, and play
- G M Burghardt
- D Chiszar
- J B Murphy
- J Romano
- T Walsh
- J Manrod
Burghardt, G. M., D. Chiszar, J. B. Murphy, J. Romano, T.
Walsh, and J. Manrod. 2002. Behavioral complexity,
behavioral development, and play, p. 78-117. In: Komodo
Dragons: Biology and Conservation. J. B. Murphy, C. Ciofi,
C. de La Panouse, and T. Walsh (eds.). Smithsonian
Institution Press, Washington, D.C.
Genetic adaptation to captivity can occur in a single generation
- M R Christie
- M L Marine
- R A French
- M S Blouin
Christie, M. R., M. L. Marine, R. A. French, and M. S.
Blouin. 2012. Genetic adaptation to captivity can occur in
a single generation. Proceedings of the National Academy
of Sciences of the United States of America 109:238-242.
Goannas: The Biology of Varanid Lizards
- D King
- B Green
King, D., and B. Green. 1999. Goannas: The Biology of
Varanid Lizards. University of New South Wales Press,
Adelaide, Australia.
The Oxford Handbook of Comparative Evolutionary Psychology
- A Wilkinson
- L Huber
Wilkinson, A., and L. Huber. 2012. Cold-blooded cognition:
reptilian cognitive abilities, p. 129-143. In: The Oxford
Handbook of Comparative Evolutionary Psychology. J.
Vonk and T. K. Shackelford (eds.). Oxford University Press,
Oxford, U.K.
Field observations by two American varanophiles
- E R Pianka
- S Sweet
Pianka, E. R., and S. Sweet. 2016. Field observations by two
American varanophiles, p. 1-68. In: Proceedings of the
2015 Interdisciplinary World Conference on Monitor
Lizards. M. Cota (ed.). Suan Sunandha Rajabhat University,
Bangkok, Thailand.