Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom‐up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top‐down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) ‘kinetic null modelling’ of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature‐insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.     

Behavioural syndrome in a solitary predator is independent of body size and growth rate

Models explaining behavioural syndromes often focus on state-dependency, linking behavioural variation to individual differences in other phenotypic features. Empirical studies are, however, rare. Here, we tested for a size and growth-dependent stable behavioural syndrome in the juvenile-stages of a solitary apex predator (pike, Esox lucius), shown as repeatable foraging behaviour across risk. Pike swimming activity, latency to prey attack, number of successful and unsuccessful prey attacks was measured during the presence/absence of visual contact with a competitor or predator. Foraging behaviour across risks was considered an appropriate indicator of boldness in this solitary predator where a trade-off between foraging behaviour and threat avoidance has been reported. Support was found for a behavioural syndrome, where the rank order differences in the foraging behaviour between individuals were maintained across time and risk situation. However, individual behaviour was independent of body size and growth in conditions of high food availability, showing no evidence to support the state-dependent personality hypothesis. The importance of a combination of spatial and temporal environmental variation for generating growth differences is highlighted.     

Colonization of novel White Sands habitat is associated with changes in lizard anti‐predator behaviour

Colonization of novel habitats is often associated with differences in ecological community composition. For small diurnal animals, differences in predator diversity and abundance can lead to behavioural shifts in the novel habitat. The eastern fence lizard Sceloporus undulatus (Bosc and Daudin, 1801) recently colonized the gypsum dunes of White Sands, a predator‐poor community relative to the predator‐rich community of the surrounding Chihuahuan dark‐soil habitat. We used field experiments to assess S. undulatus anti‐predator behaviour in white‐sand versus dark‐soil habitats, and used laboratory assays to determine whether behavioural differences could be mediated by hormonal regulation. Overall, we found that white‐sand lizards were less vigilant but more wary than their dark‐soil counterparts; it took them longer to detect a simulated predator, but once detected they were more likely to retreat from their perches than dark‐soil lizards. At the proximate level, differences in anti‐predator behaviour could not be explained by differences in plasma hormone levels (corticosterone and testosterone); we detected elevated corticosterone for lizards in our stress treatment relative to control treatment, but found no differences between habitats in baseline or acute corticosterone levels. At the evolutionary level, we suggest that differences in anti‐predator behaviour may be explained by differences across habitats in predation environment, habituation, and/or the cost of retreating. Our study implicates changes in predator community composition in mediating ecological divergence in behaviour. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 657–667.     

The Moral Economy of Water: Equity and Antiquity in the Andean Commons

This article focuses on irrigation and water use in a community in the Peruvian Andes, one of numerous villages in the region where these activities are carried out in an unusual way. The practices and principles that make up this tradition, defining the rights and duties of community members in making use of the resource most vital for life, are identified and evaluated based on comparative ethnographic research. It is argued that they provide a highly effective way of managing a scarce and fluctuating resource that is held in common, an older Andean tradition that may have been adopted by the Incas and endorsed as an official policy—all of which might help to account for its wide distribution in the region today. In this particular case, the principles help to create an extraordinary kind of community, a transparent and equitable one in which a basic material symmetry or proportionality is expressed at many levels. This symmetry is closely related to other basic commonalities among community members, but of particular interest are its effects on social solidarity and cooperation and its association with a strong sense of ethnic identity. The implications of this tradition for solving contemporary problems in water management are also briefly discussed, [sociocultural anthropology, irrigation, Andes, common-property]     

Behavioural ecology in traditional societies

Can models from behavioural ecology explain cultural diversity in human populations? Studies of variation in reproductive and productive behaviour, both within and between traditional societies, are beginning to show that specific predictions from sexual selection and optimal foraging theory can be developed and tested with human data. Greatest success has been in the study of foraging; whereas attempts to understand patterns of marriage and parental investment have been most convincing in those cases where behaviour is related to specific ecological and social conditions. The aim of human behavioural ecologists in the future will be to determine the constraints that the dual goals of reproduction and production place on individuals.     

Diabetes and hypertension in Britain's ethnic minorities: implications for the future of renal services.

Diabetes and hypertension are much more prevalent among Britain''s 2.5 million Asian and African-Caribbean population than among the white population and are major contributors to end stage renal failure. Asians and African-Caribbeans have threefold to fourfold higher acceptance rates on to renal replacement therapy than white people, and in some districts they comprise up to half of all patients receiving such treatment. Their greater need for renal replacement treatment is accompanied by difficulties of tissue matching in cross racial transplants and a shortage of donor organs. The aging of ethnic minority populations will increase local need for renal services significantly. Measures to control diabetes, hypertension, and secondary complications in Asian and African-Caribbean communities will contribute both to safeguarding health and to economies in spending on renal services. Education about diabetes and hypertension, modification of behavioural risk factors, early diagnosis, effective glycaemic and blood pressure control, and early referral for signs of renal impairment are essential preventive measures. Primary and community health care professionals have a critical role to play here.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk

The hypothesis that the parasite Toxoplasma gondii manipulates the behaviour of its intermediate rat host in order to increase its chance of being predated specifically by its feline definitive host, rather than a non-definitive host predator species, was tested. The impact of a range of therapeutic drugs, previously demonstrated to be effective in preventing the development of T. gondii-associated behavioural and cognitive alterations in rats, on definitive-host predator specificity was also tested. Using a Y-shaped maze design, we demonstrated that T. gondii-associated behavioural changes, apparently aimed to increase predation rate, do appear to be specific to that of the feline definitive host--there were significant and consistent differences between the (untreated) infected and uninfected rats groups where T. gondii-infected rats tended to choose the definitive host feline-predator-associated maze arm and nest-box significantly more often than a maze arm or nest-box treated with non-definitive host predator (mink) odour. Drug treatment of infected rats prevented any such host-specificity from being displayed. We discuss our results in terms of their potential implications both for T. gondii epidemiology and the evolution of parasite-altered behaviour.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities

The feeding behaviour and diets of fishes in two tropical habitats, a marine reef and a freshwater pond, were studied comparatively in Brazil. Similarities were found in the tactics employed to obtain food, the social patterns during foraging, and the general diet, notwithstanding lower-level taxonomic differences between the food items. The feeding behaviours of about one-third of the fish fauna from each community were approximately equivalent. The feeding categories of these fishes are briefly described. The similarities in the feeding modes probably reflect structural and functional properties shared by the two communities. Additional behavioural similarities of fishes in both habitats are presented and the lack of some particular foraging modes in each community is noted. The picture emerged that different, unrelated fish assemblages have the ability to evolve towards a similar behavioural and structural organization in response to comparable situations and constraints. The value of underwater observations and naturalistic studies on tropical freshwater fish assemblages is indicated.     

Using mathematical models to understand the AIDS epidemic

The most urgent public-health problem today is to devise effective strategies to minimize the destruction caused by the AIDS epidemic. This complex problem will involve medical advances and new public-health and education initiatives. Mathematical models based on the underlying transmission mechanisms of the AIDS virus can help the medical/scientific community understand and anticipate its spread in different populations and evaluate the potential effectiveness of different approaches for bringing the epidemic under control. Before we can use models to predict the future, we must carefully test them against the past spread of the infection and for sensitivity to parameter changes. The long and extremely variable incubation period and the low probability of transmitting the AIDS virus in a single contact imply that population structure and variations in infectivity both play an important role in its spread. The population structure is caused by differences between people in numbers of sexual partners and the use of intravenous drugs and because of the way in which people mix among age, ethnic, and social groups. We use a simplified approach to investigate the effects of variation in incubation periods and infectivity specific to the AIDS virus, and we compare a model of random partner choices with a model in which partners both come from similar behavior groups.     

Wanting,liking and welfare: The role of affective states in proximate control of behaviour in vertebrates

Animals choose a course of action countless times each day. To do so, they need to prioritise their behaviour within a set of alternative actions and decide which of these actions to perform at any one time and for how long, that is, determine when the behaviour has reached its desired effect. This process has classically been called the proximate behavioural control mechanism. Several aspects contribute to this process: internal and external stimuli, the emotions that they elicit, motivation (wants), behavioural goals, valuation, decision‐making and its modulation by mood, and the assessment of behavioural outcomes (liking). I will address all these aspects in the form of an integrated conceptual model. In the process of behavioural control, options need to be valued, and I will refer to evidence showing that an affective hedonic process in respect to (future) reward and punishment heavily affects this value. Moreover, I view motivation, the force that finally drives a specific behavioural output, as being primarily influenced by affective states or even corresponding fully to them. Given the feedback in behavioural control by (dis‐)liking outcomes of behaviour, I reason that in respect to welfare it is more important for animals to reach proximate goals than to avoid negative stimuli. All behavioural choices are modulated, and I show how mood, a long‐term affective state, can cause such modulation. Proximate control of behaviour takes place in the brain, and I will briefly discuss how current and future brain research may elucidate how the brain computes these processes. Furthermore, the inclusion of affective states in the conceptual model raises the question of the subjective experience of animals, and I will address some of the important open questions in this area of research. I will conclude that neural studies cannot currently provide a detailed and general theory on the algorithms of proximate behavioural control. In parallel to further developing these approaches, I propose to strengthen a refined ethological approach with a focus on the states of “wanting” and “liking” in ecologically meaningful circumstances and with a strong ontogenetic (within species) and comparative (between species) component. I consider this ethological approach to be a highly promising step in understanding proximate behavioural control.     

Hepatitis C Transmission and Treatment in Contact Networks of People Who Inject Drugs

Hepatitis C virus (HCV) chronically infects over 180 million people worldwide, with over 350,000 estimated deaths attributed yearly to HCV-related liver diseases. It disproportionally affects people who inject drugs (PWID). Currently there is no preventative vaccine and interventions feature long treatment durations with severe side-effects. Upcoming treatments will improve this situation, making possible large-scale treatment interventions. How these strategies should target HCV-infected PWID remains an important unanswered question. Previous models of HCV have lacked empirically grounded contact models of PWID. Here we report results on HCV transmission and treatment using simulated contact networks generated from an empirically grounded network model using recently developed statistical approaches in social network analysis. Our HCV transmission model is a detailed, stochastic, individual-based model including spontaneously clearing nodes. On transmission we investigate the role of number of contacts and injecting frequency on time to primary infection and the role of spontaneously clearing nodes on incidence rates. On treatment we investigate the effect of nine network-based treatment strategies on chronic prevalence and incidence rates of primary infection and re-infection. Both numbers of contacts and injecting frequency play key roles in reducing time to primary infection. The change from “less-” to “more-frequent” injector is roughly similar to having one additional network contact. Nodes that spontaneously clear their HCV infection have a local effect on infection risk and the total number of such nodes (but not their locations) has a network wide effect on the incidence of both primary and re-infection with HCV. Re-infection plays a large role in the effectiveness of treatment interventions. Strategies that choose PWID and treat all their contacts (analogous to ring vaccination) are most effective in reducing the incidence rates of re-infection and combined infection. A strategy targeting infected PWID with the most contacts (analogous to targeted vaccination) is the least effective.     

Analysis of Complex Patterns of Human Exposure and Immunity to Schistosomiasis mansoni: The Influence of Age,Sex, Ethnicity and IgE

Background

Numerous factors may influence Schistosoma infection intensity and prevalence within endemic communities, including exposure-related factors such as local environment and behaviour, and factors relating to susceptibility to infection such as immunology and genetics. While animal studies performed in the laboratory can be tightly controlled, human populations are highly heterogeneous, varying according to demographic characteristics, genetic background and exposure to infection. The heterogeneous nature of human water contact behaviour in particular makes it difficult to distinguish between a lack of cercarial exposure and reduced susceptibility to infection as the cause for low levels of infection in the field.

Methods and Principal Findings

In this study we investigate risk factors for Schistosoma mansoni infection in a rural Ugandan fishing community receiving treatment as part of a multi-disciplinary longitudinal reinfection study. More specifically, we examine the influence that age, sex and ethnic background have on susceptibility to reinfection after anti-helminth drug treatment, but use individual estimates of cercarial exposure and multivariable methods in an attempt to remove noise created by environmental and behavioural heterogeneities. We then investigate whether schistosome-specific IgE immune responses could account for any remaining variations in susceptibility to reinfection. Our findings suggest that observed ethnic- and sex-related variations in S. mansoni reinfection were due to variations in cercarial exposure, as opposed to biological differences in susceptibility to infection. Age-related differences in reinfection were not explained by exposure, however, and appeared linked to the balance of IgE and IgG₄ to the tegumental antigen SmTAL1 (formerly Sm22.6), which itself was significantly related to resistance to reinfection.

Conclusions

This study highlights the benefit of taking a multidisciplinary approach in complex field settings; it allows the ecology of a population to be understood and thus more robust conclusions to be made.     

Pareto front analysis of flight time and energy use in long-distance bird migration

Optimality models are frequently used in studies of long distance bird migration to help understand and predict migration routes, stopover strategies and fuelling behaviour in a spatially varying environment. These models typically evaluate bird behaviour by focusing on a single optimization currency, such as total migration time or energy-use, without explicitly considering trade-offs between the involved objectives. In this paper, we demonstrate that this classic single-objective approach downplays the importance of variability in bird behaviour. In the light of these considerations, we therefore propose to use a full multi-criteria optimization method to isolate the set of non-dominated, efficient or Pareto optimal solutions. Unlike single-objective optimization where there is only one combination of bird behaviour maximizing fitness, the Pareto solution set represents a range of optimal solutions to conflicting objectives. Our results demonstrate that this multi-objective approach provides important new ways of analyzing how environmental factors and behavioural constraints have driven the evolution of migratory behaviour.     

Behavioural processes affecting development: Tinbergen's fourth question comes of age

Interest in relationships between behaviour and development has been spurred by research on related topics, including phenotypic plasticity, parental effects, extragenetic inheritance, individual differences and trait syndromes. Here, I consider several emerging areas of research in the interface between behaviour and development, with a focus on behavioural processes that are likely to affect the development and maintenance of interindividual variation in a wide array of morphological, physiological and behavioural traits. Using a norm of reaction approach, I introduce and illustrate the complexities of phenotypic development. Next, I consider the implications of environmental selection and niche construction for phenotypic development, and consider why these behavioural processes are likely to encourage the development and maintenance of repeatable, stable individual differences and trait syndromes. Parental effects involving behaviour also affect the development of a wide array of phenotypic traits; differential allocation is a currently underappreciated type of parental effect, by which males can affect the development of their offspring via nongenetic means, even if those males have no contact with their young. Behavioural parental effects also contribute to extragenetic inheritance, and recent studies suggest that this phenomenon may be more widespread than previously suspected. The effects of behavioural processes on phenotypic development have interesting implications for problems in related disciplines (e.g. ecology, evolution and conservation biology), providing additional impetus for future research on the effects of behavioural mechanisms on the development of behavioural and other traits. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Demographic and social constraints on male chimpanzee behaviour

Male chimpanzees, Pan troglodytes, are well known for affiliating and cooperating in a variety of behavioural contexts. Prior field research indicates that maternal kinship does not affect patterns of affiliation and cooperation by males in the same social group. Two questions remain unclear from this finding. First, why do male chimpanzees not bias their behaviour towards maternal kin? Second, what factors account for who affiliates and cooperates with whom? We conducted behavioural observations of an unusually large community of chimpanzees at Ngogo, Kibale National Park, Uganda, to test the hypothesis that demographic constraints limit the number of maternal kin with whom male chimpanzees can cooperate, and thereby lead them to form selective bonds with nonkin of similar age and status. Results indicated that male age and rank are significantly associated with four measures of social behaviour. Members of the same age class and individuals close in rank were more likely to affiliate and cooperate than males that belonged to different age and rank classes. Additional analyses replicate earlier findings and show that males who affiliated and cooperated were not closely related through the maternal line, as assayed by mtDNA haplotype sharing. These results add to our growing understanding of the important role demographic and social constraints play in animal behaviour.     

Lekking in birds: choice, competition and reproductive constraints

This paper discusses the importance of female choice and intrasexual competition in lek species. The importance of phenotypic differences between individuals is stressed. Reproductive constraints limit the possible behavioural strategies that can be used by males and females. I suggest that it is difficult to understand reproductive behaviour without a knowledge of these reproductive constraints.     

Taking a Comparative Approach: Analysing Personality as a Multivariate Behavioural Response across Species

Animal personality, repeatable behaviour through time and across contexts, is ecologically and evolutionarily important as it can account for the exhibition of sub-optimal behaviours. Interspecific comparisons have been suggested as important for understanding the evolution of animal personality; however, these are seldom accomplished due, in part, to the lack of statistical tools for quantifying differences and similarities in behaviour between groups of individuals. We used nine species of closely-related coral reef fishes to investigate the usefulness of ecological community analyses for the analysis of between-species behavioural differences and behavioural heterogeneity. We first documented behavioural carryover across species by observing the fishes' behaviour and measuring their response to a threatening stimulus to quantify boldness. Bold fish spent more time away from the reef and fed more than shy fish. We then used ecological community analysis tools (canonical variate analysis, multi-response permutation procedure, and permutational analysis of multivariate dispersion) and identified four 'clusters' of behaviourally similar fishes, and found that the species differ in the behavioural variation expressed; some species are more behaviourally heterogeneous than others. We found that ecological community analysis tools are easily and fruitfully applied to comparative studies of personality and encourage their use by future studies.     

Control of urinary schistosomiasis on Zanzibar (Unguja Island): a pilot evaluation of the educational impact of the Juma na Kichocho health booklet within primary schools

To improve health education within primary schools, the health education booklet "Juma na kichocho" was evaluated during a study within 5 schools using key-informant questionnaires that recorded children's knowledge and attitude (KA) towards schistosomiasis before and after daily structured-use of booklets. A total of 229 schoolchildren (114 boys : 115 girls) of between 11 and 15 years of age were interviewed and re-assessed after a working school week. Existing and putative booklet-induced changes in KA scores for schistosomiasis were compared directly against equivalent KA scores for malaria. In total 47.4% of children were already aware that schistosomiasis was a water-borne disease while only 10.5% knew of its exact aetiology; after booklet intervention these levels increased to 54.6 and 15.7%, respectively. The majority of children still failed, however, to realise that re-infection could take place soon after treatment. While a positive increase was observed for children's total KA questionnaire scores for both malaria and schistosomiasis after booklet intervention, these were not statistically significant. In the context of control, further educational efforts are needed to promote and guide behavioural change, especially in relation to reduction of environmental water contact.