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

Intraspecific Colour Variation among Lizards in Distinct Island Environments Enhances Local Camouflage.

This is the final version of the article. It first appeared from PLOS via http://dx.doi.org/ 10.1371/journal.pone.0135241Within-species colour variation is widespread among animals. Understanding how this arises can elucidate evolutionary mechanisms, such as those underlying reproductive isolation and speciation. Here, we investigated whether five island populations of Aegean wall lizards (Podarcis erhardii) have more effective camouflage against their own (local) island substrates than against other (non-local) island substrates to avian predators, and whether this was linked to island differences in substrate appearance. We also investigated whether degree of local substrate matching varied among island populations and between sexes. In most populations, both sexes were better matched against local backgrounds than against non-local backgrounds, particularly in terms of luminance (perceived lightness), which usually occurred when local and non-local backgrounds were different in appearance. This was found even between island populations that historically had a land connection and in populations that have been isolated relatively recently, suggesting that isolation in these distinct island environments has been sufficient to cause enhanced local background matching, sometimes on a rapid evolutionary time-scale. However, heightened local matching was poorer in populations inhabiting more variable and unstable environments with a prolonged history of volcanic activity. Overall, these results show that lizard coloration is tuned to provide camouflage in local environments, either due to genetic adaptation or changes during development. Yet, the occurrence and extent of selection for local matching may depend on specific conditions associated with local ecology and biogeographic history. These results emphasize how anti-predator adaptations to different environments can drive divergence within a species, which may contribute to reproductive isolation among populations and lead to ecological speciation.This work was supported by a Biotechnology and Biological Sciences Research Council studentship (www.BBSRC.com), the British Herpetological Society (www.thebhs.org), the Cambridge Philosophical Society (http://www.cambridgephilosophicalsociety.org) and Magdalene College, Cambridge (to KLAM), and a Biotechnology and Biological Sciences Research Council and David Philips Research Fellowship (grant number BB/G022887/1) to MS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Consequences of haemogregarine infection on the escape distance in the lacertid lizard, Podarcis vaucheri

Nowadays it is widely accepted that parasites play a significant role in the community structures in which they occur, and ultimately upon ecosystems. Furthermore, infection by parasites might be associated with considerable deterioration of individual host fitness. While the apicomplexan parasites belonging to the genus Hepatozoon can provoke severe deleterious effects in some mammals, impact on other hosts, such as reptiles, is still unclear. We assessed the effect of Hepatozoon parasites on Podarcis vaucheri flight-initiation distance from a simulated predator, a behaviour that is determinant for a successful escape and is therefore likely to have major implications on a lizard’s survival. We found that flight-initiation distance was not dependent on the time of the day or tail condition. Subadults exhibited worse body condition than adults and females had worse body condition than males. Regarding intensity of parasitism, subadults showed higher parasitemia levels. Escape distance was not associated with parasitic load or any of the other studied features, which is indicative of limited impact of the parasite. This negligible effect might explain the remarkably high prevalence (more than 96%) of this parasitic group within this P. vaucheri population

Playing dead: lizards show tonic immobility without human handling

Damas Moreira I. Playing dead: lizards show tonic immobility without human handling. Behaviour. 2021:1-9.**Abstract** Tonic immobility, or the ability to play dead, is widespread among vertebrates. It is a last line of defence against a threat, and usually follows physical restraint. Here, I report two lizards exhibiting tonic immobility in the presence of humans, but remarkably, without any handling or physical contact. These two lizards belonged to an invasive population of the Italian Wall Lizard (Podarcis siculus), and both events took place in different years and situations, suggesting this behaviour may be more common than previously thought. There are rare documented cases of animals exhibiting this behaviour without handling; however, to my knowledge, this is the first description of a lizard displaying tonic immobility to humans, in the absence of handling. This is also the first incident of tonic immobility in the Italian Wall Lizard. I discuss these anecdotal events in the light of this invasive population inhabiting a highly urbanized location

Understanding what makes a lizard invasive: the role of behaviour and cognition

Thesis by publication.Bibliography: pages 121-133.Introduction -- Aims of the study -- Chapter I. Is invasive potential linked to cognitive ability in a lizard? -- Chapter II. Learning from others : an invasive lizard uses social information from both conspecifics and heterospecifics -- Chapter III. Can behaviour explain invasion success? A comparison between sympatric invasive and native lizards -- Chapter IV. Getting ahead : exploitative competition by an invasive lizard -- General discussion -- Bibliography -- Appendices.The world has been changing at an unprecedented rate due to the 'progress' of human society. Globalization has changed our way of living, and it translates into severe negative effects on our ecosystems. Additionally, globalization also demands more connections and transport, creating frequent and dynamic networks worldwide, of both people and cargo. This can lead to the movement of thousands of species outside their native range, and biological invasions are now a contemporary global problem. While most invasions end in failure, some manage to successfully take hold and adapt to new locations. What determines a species' invasive success is of great interest and importance for conservation efforts. Behaviour is believed to play a key role in the success of invasive species, although the mechanisms are still unclear, especially for unintentional invasions. Members of the lizard genus Podarcis show high variability in their invasive potential and are thus a well-suited model for studying the role of behaviour during biological invasions. The Italian wall lizard, Podarcis sicula, is a globally invasive species that hitchhikes on transportation of people or cargo, and does well in novel environments. In addition to behaviour, there is mounting evidence that cognition may also be a determining factor for invasion success. The aim of my thesis is to understand the role of behaviour and cognition in determining what makes P. sicula such a good invader. I used animals from an introduced population in Lisbon (Portugal) to examine behavioural traits that might be linked to a species' invasive success.My original contribution to knowledge is uncovering the potential role of behavioural flexibility, social learning ability, behavioural traits, and competition in the invasion process. Although I focused on the invasive lizard P. sicula, my study highlights the potential role of behaviour and cognition in invasions more broadly. My thesis has thus 4 chapters written as stand-alone publications that deal with different behavioural components. I predicted that P. sicula would have greater levels of behavioural flexibility than congeneric non-invasive species - P. bocagei and P. carbonelli. The ability to reverse a previously learnt discrimination can be indicative of behavioural flexibility. I used a discrimination task and a reversal and quantified the number of errors and overall learning ability of all three species (chapter I). The invasive species had relatively less difficulty than the non-invasive species to reverse the task. Also, I found different cognitive ability between the invasive species and the two non-invasive species (P. bocagei and P. carbonelli had a more similar learning pattern between them). Chapter II dealt with the ability of P. sicula to obtain relevant social information to solve a task, from other P. sicula, or from a different species they had never encountered in nature (P. bocagei). The role of heterospecific learning in biological invasions has never been studied before. Remarkably, this invasive species learnt equally well from individuals of the same or different species. In chapter III, I used a sympatric congeneric species, P. virescens, native to the study site, to compare personality traits likely related to invasive success. I measured exploratory behaviour of lizards in a novel arena (activity and shelters visited); boldness (latency to emerge from a suboptimal shelter, after being scared into it); and neophobia (minimum distance between a lizard and a novel object placed in the arena). I found the invasive P. sicula to be more exploratory, neophilic, and bolder than the sympatric native species. Additionally, while the native species showed high repeatability in its behaviours and had all traits correlated, the invasive species was much less consistent and showed no correlation between traits. Finally, since the sympatric P. virescens has likely been displaced from gardens where P. sicula is found, interspecific competition could be an important factor governing their success as an invader. I thus assessed the mechanisms P. sicula might use to outcompete the sympatric P. virescens in this location (chapter IV). I established mixed groups of both species and scored several behaviours linked to competitive ability. Although I predicted competitive interference (e.g. the invasive species with more aggressive behaviours), I actually found evidence for competitive exploitation (e.g. the invasive species being more efficient at exploiting resources).Collectively, my thesis shows differences in cognitive skills between invasive and non-invasive Podarcis, and that the invasive P. sicula is able to socially learn from the same and different species. Also, P. sicula has behavioural traits (e.g. boldness and foraging efficiency) that can be linked to its invasive success. The results from these chapters highlight the potential importance of behaviour in biological invasions, and give insight into why this lizard species is such a successful invader, and into what impact it might have on native species. This work will hopefully contribute to a better understanding of the behavioural basis of invasions, and ultimately assist conservation efforts.Mode of access: World wide web1 online resource (ix, 139 pages) colour illustration

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

Consequences of haemogregarine infection on the escape distance in the lacertid lizard, Podarcis vaucheri

Nowadays it is widely accepted that parasites play a significant role in the community structures in which they occur, and ultimately upon ecosystems. Furthermore, infection by parasites might be associated with considerable deterioration of individual host fitness. While the apicomplexan parasites belonging to the genus Hepatozoon can provoke severe deleterious effects in some mammals, impact on other hosts, such as reptiles, is still unclear. We assessed the effect of Hepatozoon parasites on Podarcis vaucheri flight-initiation distance from a simulated predator, a behaviour that is determinant for a successful escape and is therefore likely to have major implications on a lizard's survival. We found that flight-initiation distance was not dependent on the time of the day or tail condition. Subadults exhibited worse body condition than adults and females had worse body condition than males. Regarding intensity of parasitism, subadults showed higher parasitemia levels. Escape distance was not associated with parasitic load or any of the other studied features, which is indicative of limited impact of the parasite. This negligible effect might explain the remarkably high prevalence (more than 96%) of this parasitic group within this P. vaucheri population. © Firenze University Press.Fieldwork was carried out under the permit of the Haut Commisariat aux Eaux and Forets of Morocco (HCEFLCD/DLCDPN/DPRN/DFF N°14/2010) and was supported by the Percy Sladen Memorial Fund (to DJH), by the British Herpetological Society (to IDM), and by the Chicago Herpetological Society (to JPM). JPM, DS, and AP are supported by grants and contract by Fundação para a Ciência e Tecnologia (FCT, Portugal) under the Programa Operacional Potencial Humano – Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência (JPM: PhD grant SFRH/BD/74305/2010; DS: post-doctoral grant SFRH/BPD/66592/2009; AP: contract IF/01257/2012). DJH is supported by FEDER through the compete program, the project “Genomics and Evolutionary Biology” co-financed by North Portugal Regional Operational Program (ON.2) under NSRF through the European Regional Development Fund.Peer Reviewe

Invasive lizard has fewer parasites than native congener

Tome B, Harris DJ, Perera A, Damas Moreira I. Invasive lizard has fewer parasites than native congener. Parasitology research. 2021.Invasive species can carry parasites to introduced locations, which may be key to understand the success or failure of species establishment and the invasive potential of introduced species. We compared the prevalence and infection levels of haemogregarine blood parasites between two sympatric congeneric species in Lisbon, Portugal: the invasive Italian wall lizard (Podarcis siculus) and the native green Iberian wall lizard (Podarcis virescens). The two species had significant differences in their infection levels: while P. virescens had high prevalence of infection (69.0%), only one individual of P. siculus was infected (3.7%), and while P. virescens exhibited an average intensity of 1.36%, the infected P. siculus individual had an infection rate of only 0.04%. Genetic analyses of 18S rRNA identified two different haemogregarine haplotypes in P. virescens. Due to the low levels of infection, we were not able to amplify parasite DNA from the infected P. siculus individual, although it was morphologically similar to those found in P. virescens. Since other studies also reported low levels of parasites in P. siculus, we hypothesize that this general lack of parasites could be one of the factors contributing to its competitive advantage over native lizard species and introduction success

Invasive lizard has fewer parasites than native congener

Tome B, Harris DJ, Perera A, Damas Moreira I. Invasive lizard has fewer parasites than native congener. Parasitology research. 2021;120:2953–2957.Invasive species can carry parasites to introduced locations, which may be key to understand the success or failure of species establishment and the invasive potential of introduced species. We compared the prevalence and infection levels of haemogregarine blood parasites between two sympatric congeneric species in Lisbon, Portugal: the invasive Italian wall lizard (Podarcis siculus) and the native green Iberian wall lizard (Podarcis virescens). The two species had significant differences in their infection levels: while P. virescens had high prevalence of infection (69.0%), only one individual of P. siculus was infected (3.7%), and while P. virescens exhibited an average intensity of 1.36%, the infected P. siculus individual had an infection rate of only 0.04%. Genetic analyses of 18S rRNA identified two different haemogregarine haplotypes in P. virescens. Due to the low levels of infection, we were not able to amplify parasite DNA from the infected P. siculus individual, although it was morphologically similar to those found in P. virescens. Since other studies also reported low levels of parasites in P. siculus, we hypothesize that this general lack of parasites could be one of the factors contributing to its competitive advantage over native lizard species and introduction success