Over the last century, humans have modified landscapes, generated pollution and provided opportunities for exotic species to invade areas where they did not evolve. In addition, humans now interact with animals in a growing number of ways (e.g. ecotourism). As a result, the quality (i.e. nutrient composition) and quantity (i.e. food abundance) of dietary items consumed by wildlife have, in many cases, changed. We present representative examples of the extent to which vertebrate foraging behaviour, food availability (quantity and quality) and digestive physiology have been modified due to human-induced environmental changes and human activities. We find that these effects can be quite extensive, especially as a result of pollution and human-provisioned food sources (despite good intentions). We also discuss the role of nutrition in conservation practices, from the perspective of both in situ and ex situ conservation. Though we find that the changes in the nutritional ecology and physiology of wildlife due to human alterations are typically negative and largely involve impacts on foraging behaviour and food availability, the extent to which these will affect the fitness of organisms and result in evolutionary changes is not clearly understood, and requires further investigation.

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Nutritional physiology and ecology of wildlife in a changing world.

Understanding the ways in which individuals cope with threats, respond to challenges, make use of opportunities and mediate the harmful effects of their surroundings is important for predicting their ability to function in a rapidly changing world. Perhaps one of the most essential drivers of coping behaviour of adults is the environment experienced during their early-life development. Although the study of coping, defined as behaviours displayed in response to environmental challenges, has a long and rich research history in biology, recent literature has repeatedly pointed out that the processes through which coping behaviours develop in individuals are still largely unknown. In this review, we make a move towards integrating ultimate and proximate lines of coping behaviour research. After broadly defining coping behaviours (1), we review why, from an evolutionary perspective, the development of coping has become tightly linked to the early-life environment (2), which relevant developmental processes are most important in creating coping behaviours adjusted to the early-life environment (3), which influences have been shown to impact those developmental processes (4) and what the adaptive significance of intergenerational transmission of coping behaviours is, in the context of behavioural adaptations to a fast changing world (5). Important concepts such as effects of parents, habitat, nutrition, social group and stress are discussed using examples from empirical studies on mammals, fish, birds and other animals. In the discussion, we address important problems that arise when studying the development of coping behaviours and suggest solutions.

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Why and how the early-life environment affects development of coping behaviours

Despite the taxonomic, behavioral, and lifestyle diversity among reptile species, behavioral consistency in reptiles has not been examined to the extent that it has been in fish, birds, and mammals. Careful use of terms such as individuality, temperament, personality, and behavioral syndromes is needed as they carry overlapping connotations and varying dangers of being applied in an anthropomorphic fashion. The majority of research on such phenomena in reptiles has utilized snakes and lizards. Studies on antipredator behavior in natricine snakes, primarily in the genus Thamnophis, has produced strong evidence of individual consistency of behavior over time, some evidence for consistency across situations, clear evidence for a heritable basis for individual differences in antipredator behavior, and limited evidence linking individual variation with fitness-related outcomes. Research in lizards has mirrored findings reported for other vertebrates, focusing on one or more of five traits: shyness–boldness, exploration-avoidance, activity, sociability, conspecific aggression, and possible relationships among them. We review the methodology and statistical analyses used to study these traits in lizards and the relationships of these traits to morphology, reproduction, hormones, fitness, life history, and other factors. The common lizard (Zootoca vivipara) has become a model species, for example, in studies assessing the pace-of-life hypothesis, with results differing from those found in other vertebrates. Studies on turtles and crocodilians are also presented that further illustrate the comparative and methodological value of reptilian studies.

Personality and Individuality in Reptile Behavior

Territory size and age explain movement patterns in the Eurasian beaver

Previous research has shown that competition, familiarity, diet, and relatedness can all influence aggregation patterns in garter snakes. We controlled for these factors and examined social aggregation patterns in juvenile Eastern garter snakes (Thamnophis sirtalis sirtalis). We assayed snakes individually for consistent individual differences in boldness and sociability. We then placed snakes in groups of 10 in an enclosure with four shelters and observed their social interactions over a period of 8 days. We demonstrate that the snakes actively seek social interaction, prefer to remain with larger aggregates, and associate nonrandomly with specific individuals or groups. We show that their social interaction patterns are influenced by individual boldness, sociability, and age. The snakes’ social networks were perturbed twice a day by “shuffling” their locations. Despite these disturbances, the snakes eventually re-formed their preferred social environment. Aggregation and exploration patterns also varied across time, with most activity occurring later in the day. These results highlight the complexity of snake sociality and may have important implications for conservation efforts. Snakes are often considered nonsocial animals, but this is inaccurate. We used social network analyses to compare juvenile Eastern garter snakes’ group behaviors to their individual personalities. Our research demonstrates that these snakes actively seek out social interaction and prefer to join and remain with larger groups and that their social interaction patterns are influenced by consistent individual differences in boldness and sociability. Our work contributes to a sparse but growing body of literature on sociability in reptiles. This work is important for changing perceptions among the scientific community and the public as a whole. As a consequence, it may aid efforts in developing appropriate conservation techniques that consider sociability patterns in relocated reptiles.

Aggregation and social interaction in garter snakes (Thamnophis sirtalis sirtalis)

An animal’s susceptibility to risk may be partly dependent on its body size. But are larger individuals bolder? We assessed this question by measuring time to emerge from a shelter in repeated trials on hatchling keelback snakes (Tropidonophis mairii). Estimates of repeatability of emergence times suggested they measure some underlying personality dimension related to boldness. Larger hatchlings emerged from shelter sooner than small ones. Hatchling mass of keelbacks is substantially influenced both by maternal phenotype and by incubation conditions. Given the environmental basis of much of the variation in offspring size, the size-boldness association may reflect a facultative ability to adjust behavioural tactics to body size, as well as innate differences in personality traits between large versus small hatchlings. The link between size and boldness suggests that the survival advantage of larger offspring size in this population may be driven by snake behaviour as well as morphology.

Bigger babies are bolder: effects of body size on personality of hatchling snakes

We investigated patterns of prevalence and intensity of gastrointestinal nematode infections in a tropical natricine snake, the keelback (Tropidonophis mairii). Ninety-eight per cent of keelbacks were infected with Tanqua anomala (Gnathostomidae), with infection intensities of up to 243 worms per snake. Infection with T. anomala caused severe inflammation of stomach mucosa and submucosa at the sites of parasite attachment and encystment. Nonetheless, we did not detect detrimental effects of nematode infection on measures of fitness among wild or captive snakes. Snakes with heavier nematode infections had higher body condition scores than less-infected individuals. Deworming captive snakes had no measurable effect on their growth rate, body condition or locomotor performance. In combination with an earlier study on blood-dwelling hepatozoons, our work suggests that keelbacks have a high tolerance to parasites. The ‘fast-pace’ life history and short lifespan of these snakes may make it beneficial for them to tolerate infection, rather than expend energy on resisting parasite attack.

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High infection intensities, but negligible fitness costs, suggest tolerance of gastrointestinal nematodes in a tropical snake

The ecological impacts of introduced species can reveal mechanisms underlying habitat selection and behaviour. We investigated the habitat use of native frog species and the invasive cane toads (Rhinella marina) in tropical northern Australia to measure overlap in habitat use, and to test if the presence of the cane toad influences frog behaviour. Native frog species and the cane toad both preferred habitats close to water and unvegetated holes. However, native frogs were found further from water (on average 19.4 m) than were toads (on average 12.6 m), and preferred areas with higher vegetation (8–50 cm) than did toads, which were more abundant in vegetation lower than 8 cm. For both types of anuran, the next neighbour was more often of the same type (89% in frogs, 52% in toads) than expected by chance (observed ratio: 75% frogs vs 25% toads), reflecting these differences in habitat use. Our counts of frog abundance increased on average 14.5% in areas from which we removed cane toads temporarily. This result suggests that cane toads inhibit the activity of native anurans either by inducing avoidance, or by reducing activity. By modifying the behaviour and spatial distribution of native taxa, invasive cane toads may curtail activities such as feeding and breeding.

Martin Mayer

Papers

Bigger babies are bolder: effects of body size on personality of hatchling snakes

High infection intensities, but negligible fitness costs, suggest tolerance of gastrointestinal nematodes in a tropical snake

Habitat use of the introduced cane toad (Rhinella marina) and native frog species in tropical Australia