Optimal behaviour can violate the principle of regularity

Understanding decisions is a fundamental aim of behavioural ecology, psychology and economics. The regularity axiom of utility theory holds that a preference between options should be maintained when other options are made available. Empirical studies have shown that animals violate regularity but this has not been understood from a theoretical perspective, such decisions have therefore been labelled as irrational. Here, I use models of state-dependent behaviour to demonstrate that choices can violate regularity even when behavioural strategies are optimal. I also show that the range of conditions over which regularity should be violated can be larger when options do not always persist into the future. Consequently, utility theory—based on axioms, including transitivity, regularity and the independence of irrelevant alternatives—is undermined, because even alternatives that are never chosen by an animal (in its current state) can be relevant to a decision.     

Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free‐ranging sharks

Marine and terrestrial environments differ fundamentally in space‐time scales of both physical and ecological processes. These differences will have an impact on the animals inhabiting each domain, particularly with respect to their spatial ecology. The behavioural strategies that underpin observed distributions of marine species are therefore important to consider. Comparatively little is known, however, about how wild fishes actually respond to gradients in food supply and temperature, and to potential mates. This paper describes how behavioural theory is being used to elucidate the strategies and tactics of free‐ranging sharks in three specific areas of study, namely, foraging on zooplankton, behavioural energetics and sexual segregation. The studies discussed are novel because shark movements were tracked in the wild using electronic tags in relation to simultaneous measurements of prey densities and thermal resources. The results show that filter‐feeding (basking shark, Cetorhinus maximus ) and predatory (dogfish, Scyliorhinus canicula ) sharks have relatively complex behaviour patterns integrally linked to maximizing surplus power, often through making short and longer term 'trade‐off' decisions between optimal foraging and thermal habitats. Interestingly, female S. canicula exhibit alternative behavioural strategies compared to males, a difference resulting in spatial segregation by habitat. Sexual segregation in this species occurs primarily as a consequence of male avoidance by females. Studies on free‐ranging sharks provide a useful model system for examining how a predator's strategy is shaped by its environment. More theory‐based studies of the behavioural processes of sharks are required however, before critical comparisons with other vertebrate predators are possible. Suggestions for further research to address this knowledge gap are given.     

sOAR: a tool for modelling optimal animal life‐history strategies in cyclic environments

Periodic environments determine the life cycle of many animals across the globe and the timing of important life history events, such as reproduction and migration. These adaptive behavioural strategies are complex and can only be fully understood (and predicted) within the framework of natural selection in which species adopt evolutionary stable strategies. We present sOAR, a powerful and user‐friendly implementation of the well‐established framework of optimal annual routine modelling. It allows determining optimal animal life history strategies under cyclic environmental conditions using stochastic dynamic programming. It further includes the simulation of population dynamics under the optimal strategy. sOAR provides an important tool for theoretical studies on the behavioural and evolutionary ecology of animals. It is especially suited for studying bird migration. In particular, we integrated options to differentiate between costs of active and passive flight into the optimal annual routine modelling framework, as well as options to consider periodic wind conditions affecting flight energetics. We provide an illustrative example of sOAR where food supply in the wintering habitat of migratory birds significantly alters the optimal timing of migration. sOAR helps improving our understanding of how complex behaviours evolve and how behavioural decisions are constrained by internal and external factors experienced by the animal. Such knowledge is crucial for anticipating potential species’ response to global environmental change.     

Not-so-social learning strategies

Social learning strategies (SLSs) are rules specifying the conditions in which it would be adaptive for animals to copy the behaviour of others rather than to persist with a previously established behaviour or to acquire a new behaviour through asocial learning. In behavioural ecology, cultural evolutionary theory and economics, SLSs are studied using a ‘phenotypic gambit’—from a purely functional perspective, without reference to their underlying psychological mechanisms. However, SLSs are described in these fields as if they were implemented by complex, domain-specific, genetically inherited mechanisms of decision-making. In this article, we suggest that it is time to begin investigating the psychology of SLSs, and we initiate this process by examining recent experimental work relating to three groups of strategies: copy when alternative unsuccessful, copy when model successful and copy the majority. In each case, we argue that the reported behaviour could have been mediated by domain-general and taxonomically general psychological mechanisms; specifically, by mechanisms, identified through conditioning experiments, that make associative learning selective. We also suggest experimental manipulations that could be used in future research to resolve more fully the question whether, in non-human animals, SLSs are mediated by domain-general or domain-specific psychological mechanisms.     

Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.     

Climate change effects on animal ecology: butterflies and moths as a case study

Butterflies and moths (Lepidoptera) are one of the most studied, diverse, and widespread animal groups, making them an ideal model for climate change research. They are a particularly informative model for studying the effects of climate change on species ecology because they are ectotherms that thermoregulate with a suite of physiological, behavioural, and phenotypic traits. While some species have been negatively impacted by climatic disturbances, others have prospered, largely in accordance with their diversity in life-history traits. Here we take advantage of a large repertoire of studies on butterflies and moths to provide a review of the many ways in which climate change is impacting insects, animals, and ecosystems. By studying these climate-based impacts on ecological processes of Lepidoptera, we propose appropriate strategies for species conservation and habitat management broadly across animals.     

Reversed optimality and predictive ecology: burrowing depth forecasts population change in a bivalve

Optimality reasoning from behavioural ecology can be used as a tool to infer how animals perceive their environment. Using optimality principles in a 'reversed manner' may enable ecologists to predict changes in population size before such changes actually happen. Here we show that a behavioural anti-predation trait (burrowing depth) of the marine bivalve Macoma balthica can be used as an indicator of the change in population size over the year to come. The per capita population growth rate between years t and t+1 correlated strongly with the proportion of individuals living in the dangerous top 4 cm layer of the sediment in year t: the more individuals in the top layer, the steeper the population decline. This is consistent with the prediction based on optimal foraging theory that animals with poor prospects should accept greater risks of predation. This study is among the first to document fitness forecasting in animals.     

Negotiation may lead selfish individuals to cooperate: the example of the collective vigilance game

Game-theoretical models have been highly influential in behavioural ecology. However, these models generally assume that animals choose their action before observing the behaviour of their opponents while, in many natural situations, individuals in fact continuously react to the actions of others. A negotiation process then takes place and this may fundamentally influence the individual attitudes and the tendency to cooperate. Here, I use the classical model system of vigilance behaviour to demonstrate the consequences of such behavioural negotiation among selfish individuals, by predicting patterns of vigilance in a pair of animals foraging under threat of predation. I show that the game played by the animals and the resulting vigilance strategies take radically different forms, according to the way predation risk is shared in the pair. In particular, if predators choose their target at random, the prey respond by displaying moderate vigilance and taking turns scanning. By contrast, if the individual that takes flight later in an attack endures a higher risk of being targeted, vigilance increases and there is always at least one sentinel in the pair. Finally, when lagging behind its companion in fleeing from an attacker becomes extremely risky, vigilance decreases again and the animals scan simultaneously.     

The integration of behaviour into comparative physiology

Comparative physiology has traditionally focused on the physiological responses of animals to their physicochemical environment. In recent years, awareness has increased among physiologists of the potential for behavioural factors, such as the social environment of the animal, to affect physiological condition and responses. This recognition has led to an emerging trend within the field toward using multidisciplinary approaches that incorporate both behavioural and physiological techniques. Research areas in which the integrated study of behaviour and physiology has been particularly fruitful include the physiology of the social environment, sensory physiology and behaviour, and physiological constraints on behavioural ecology. The manner in which incorporating behavioural considerations has informed the physiological data collected is discussed for each of these areas using specific examples.     

Adaptive walks on behavioural landscapes and the evolution of optimal behaviour by natural selection

Summary One of the main challenges to the adaptationist programme in general and to the use of optimality models in behavioural and evolutionary ecology in particular is that natural selection need not optimise fitness. This challenge is addressed by considering the evolution of optimal patch choice by natural selection. The behavioural model is based on a state variable approach in which a strategy consists of a sequence denoting the patch to be visited as a function of the organism's state and time. The optimal strategy maximises expected terminal reproduction. The fitnesses of alternative strategies are computed by iteration of the associated equations for fitness; this characterises the adaptive behavioural landscape. There may be enormous numbers of strategies that have near optimal fitnesses. A population model is used to connect frequencies of behavioural types from one generation to the next. Theories on adaptive walks on fitness landscapes are considered in the context of behaviour. The main result is that within the context of optimality arguments at selective equilibrium, sub-optimal behaviours can persist. General implications for research in behavioural ecology, including tests of behavioural theories, are discussed.     

Colour spaces in ecology and evolutionary biology

The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best‐known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species‐specific, more complex models giving accurate but context‐dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log–linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.     

Mechanisms of sperm competition: Linking physiology and behavioural ecology

Sperm competition has received a great deal of attention from behavioural ecologists because it is the ultimate form of male-male competition, and may also be important for female choice. It is becoming clear that the adaptive value of the behavioural strategies of males and females will not be fully understood until we have a better understanding of the physiological mechanisms that come into play after copulation. We now have enough information to compare the underlying mechanisms in birds and mammals and to relate these to the way in which sperm competition operates in both groups. To integrate this knowledge, the boundaries between behavioural ecology and physiology will have to be crossed in what promises to be a most fruitful enterprise.     

Protean defence by prey animals

Summary Attention is drawn to the widespread occurrence ofprotean phenomena, in which the appearance and behaviour of prey animals are rendered variable and irregular, as a weapon in the biological arms race between predators and their prey. Protean behaviour is defined as that behaviour which is sufficiently unsystematic to prevent a reactor predicting in detail the position or actions of the actor.Single prey animals frequently flee from a predator in an irregular manner, zigzagging, spinning, looping, or bouncing. Thissingle erratic display occurs widely in the Animal Kingdom, and may also be utilised in everyday movements of potential prey as insurance against possible attack. Examples are given.In a group of prey animals the protean aspect of escape is enhanced by the effect of numbers. In scatter reactions the effect is of multiple choice and of the simultaneous operation of several single erratics. In mobbing displays there are also successive changes in the actors' behavioural role. In protean deterrence the shuffling of individuals within a tightly packed group prevents a predator from singling one out for attack.In many species the confusing effect of changes in movement and behavioural role is enhanced by rapid changes in appearance, particularly colour.It is suggested that those prey individuals which employ escape patterns unfamiliar to the predator will tend to be at a selective advantage. During phylogeny this is likely to lead to intra-specific and inter-specific increase in the number and diversity of escape behaviours. Apostatic polymorphism is seen as a special case of protean variation within populations.There is evidence that protean displays operate by arousing neurological conflict, thereby delaying the predator's reactions and reducing the effectiveness of predatory mechanisms. Also they insure against learned countermeasures by incorporating irregularities as a basic principle. It is stressed that the irregular variability of protean displays is not accidental but has been selected for in phylogeny. A number of poorly understood behavioural aspects of the ecology of predator-prey relationships are thus united in a single theory.     

Integrating sensory ecology and predator-prey theory to understand animal responses to fire

Fire regimes are changing dramatically worldwide due to climate change, habitat conversion, and the suppression of Indigenous landscape management. Although there has been extensive work on plant responses to fire, including their adaptations to withstand fire and long-term effects of fire on plant communities, less is known about animal responses to fire. Ecologists lack a conceptual framework for understanding behavioural responses to fire, which can hinder wildlife conservation and management. Here, we integrate cue-response sensory ecology and predator-prey theory to predict and explain variation in if, when and how animals react to approaching fire. Inspired by the literature on prey responses to predation risk, this framework considers both fire-naïve and fire-adapted animals and follows three key steps: vigilance, cue detection and response. We draw from theory on vigilance tradeoffs, signal detection, speed-accuracy tradeoffs, fear generalization, neophobia and adaptive dispersal. We discuss how evolutionary history with fire, but also other selective pressures, such as predation risk, should influence animal behavioural responses to fire. We conclude by providing guidance for empiricists and outlining potential conservation applications.     

Multi-objective behavioural mechanisms are adopted by foraging animals to achieve several optimality goals simultaneously

1. Animals foraging for resources are under a variety of selective pressures, and separate optimality models have been developed predicting the optimal reproductive strategies they should adopt. 2. In most cases, the proximate behavioural mechanisms adopted to achieve such optimality goals have been identified. This is the case, for example, for optimal patch time and sex allocation in insect parasitoids. However, behaviours modelled within this framework have mainly been studied separately, even though real animals have to optimize some behaviours simultaneously. 3. For this reason, it would be better if proximate behavioural rules were designed to attain several goals simultaneously. Despite their importance, such multi-objective proximate rules remain to be discovered. 4. Based on experiments on insect parasitoids that simultaneously examine their optimal patch time and sex allocation strategies, it is shown here that animals can adopt multi-objective behavioural mechanisms that appear consistent with the two optimal goals simultaneously. 5. Results of computer simulations demonstrate that these behavioural mechanisms are indeed consistent with optimal reproductive strategies and have thus been most likely selected over the course of the evolutionary time.     

Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent-offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent-offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent-offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent-offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.     

Evidence of social effects on mate choice in vertebrates

Study of determinants of mate selection by animals has a long history in evolutionary biology and behavioural ecology. However, only during the past decade have investigators begun to conduct experiments exploring the various ways in which observation of the behaviour of others might influence mate selection. Here, we review both field and laboratory studies of behavioural processes that underlie non-independence in mate choice, discussing both direct and indirect social influences on mate selection. We focus on laboratory studies in which guppies and Japanese quail, species that have received greatest attention from investigators, have served as subjects. Although much is now known about how public information can affect mate selection in controlled environments, there are still significant gaps in our knowledge of whether and how such information contributes to mate selections by members of free-living populations.     

Evolutionary accounts of human behavioural diversity

Human beings persist in an extraordinary range of ecological settings, in the process exhibiting enormous behavioural diversity, both within and between populations. People vary in their social, mating and parental behaviour and have diverse and elaborate beliefs, traditions, norms and institutions. The aim of this theme issue is to ask whether, and how, evolutionary theory can help us to understand this diversity. In this introductory article, we provide a background to the debate surrounding how best to understand behavioural diversity using evolutionary models of human behaviour. In particular, we examine how diversity has been viewed by the main subdisciplines within the human evolutionary behavioural sciences, focusing in particular on the human behavioural ecology, evolutionary psychology and cultural evolution approaches. In addition to differences in focus and methodology, these subdisciplines have traditionally varied in the emphasis placed on human universals, ecological factors and socially learned behaviour, and on how they have addressed the issue of genetic variation. We reaffirm that evolutionary theory provides an essential framework for understanding behavioural diversity within and between human populations, but argue that greater integration between the subfields is critical to developing a satisfactory understanding of diversity.     

Assessing models of optimal diving

Many birds and mammals forage under water and have to return to the surface to breathe. Models of optimal diving attempt to explain the behaviour of such animals in terms of selection for successful foraging given the constraints imposed by physiology. Several recent papers have questioned the accuracy of both the assumptions and the predictions of these models. Here, I provide a critical review of these papers, arguing that they misrepresent both the models and the data. As a result, they focus on inappropriate tests. I use the debate to suggest various new models and to explore the general relationship between theory and data in behavioural ecology. In particular, I consider the merits of qualitative and quantitative predictions.     

Integrating ecology,psychology and neurobiology within a food-hoarding paradigm

Many animals regularly hoard food for future use, which appears to be an important adaptation to a seasonally and/or unpredictably changing environment. This food-hoarding paradigm is an excellent example of a natural system that has broadly influenced both theoretical and empirical work in the field of biology. The food-hoarding paradigm has played a major role in the conceptual framework of numerous fields from ecology (e.g. plant–animal interactions) and evolution (e.g. the coevolution of caching, spatial memory and the hippocampus) to psychology (e.g. memory and cognition) and neurobiology (e.g. neurogenesis and the neurobiology of learning and memory). Many food-hoarding animals retrieve caches by using spatial memory. This memory-based behavioural system has the inherent advantage of being tractable for study in both the field and laboratory and has been shaped by natural selection, which produces variation with strong fitness consequences in a variety of taxa. Thus, food hoarding is an excellent model for a highly integrative approach to understanding numerous questions across a variety of disciplines. Recently, there has been a surge of interest in the complexity of animal cognition such as future planning and episodic-like-memory as well as in the relationship between memory, the environment and the brain. In addition, new breakthroughs in neurobiology have enhanced our ability to address the mechanisms underlying these behaviours. Consequently, the field is necessarily becoming more integrative by assessing behavioural questions in the context of natural ecological systems and by addressing mechanisms through neurobiology and psychology, but, importantly, within an evolutionary and ecological framework. In this issue, we aim to bring together a series of papers providing a modern synthesis of ecology, psychology, physiology and neurobiology and identifying new directions and developments in the use of food-hoarding animals as a model system.