Repeated patterns in animal contest behaviour research

Among studies of contest behaviour that have been conducted within the framework of evolutionary theory, one can discern distinct phases of activity that have been associated with developments in an underpinning body of theory. As recounted in Geoff Parker's Foreword to this volume, the initial period of intense activity that occurred in the early to mid 1970s involved the laying down of a fundamental body of theory. During this time, contest behaviour provided the original context for the biological application of evolutionary game theory (as opposed to economic game theory, from which it derives). Game theory still acts as a cornerstone for behavioural ecology research and it is testament to its explanatory power that the Hawk–Dove game, wars of attrition and other examples of ‘Evolutionarily Stable Strategy, or ESS, thinking’ (Davies et al. 2012) still dominate undergraduate curricula in the subject. These early models stimulated empirical studies that provided evidence for ESSs in contests in diverse study systems including scorpionflies (Thornhill 1984), butterflies (Davies 1978) and red deer (Clutton-Brock et al. 1979). Studies such as these provided the early foundation for the cross-taxon approach to contests that we have continued in this book.

Summary

Since the seminal work of Davies in the late 1970s, territorial male butterfly contests have offered an excellent system for the empirical scrutiny of contest theories, particularly residency-related game-theoretic principles. Because butterflies lack the obvious morphological traits usually associated with animal aggression, their extended and often spectacular aerial duels both defy simple explanation and provide unique empirical opportunities. Residency win rates often approach 100% in this group, which, coupled with the apparently ‘weaponless’ nature of butterflies and the non-contact nature of their disputes, provided the early impetus for tests of the ‘bourgeois’ resident-wins model of contest resolution. Subsequent work has emphasised how potential residency-related RHP asymmetries, including those relating to temporally variable biophysical parameters, such as body temperature, may instead contribute to high rates of residents winning. The balance of empirical work in this group, however, suggests that morphological and/or biophysical factors bear little relevance to content settlement. Contest participation is not obviously mediated by energetics, which contrasts markedly and interestingly with the aerial wars of attrition of other insects, such as odonates. More recent approaches to understanding butterfly contest resolution have led to an appreciation of how life history-level factors, such as ageing and changes in residual reproductive value, may influence aggressive motivation and subsequent levels of contest participation. These principles apply generally, thereby placing butterfly contests as a potentially important system for the empirical investigation of the broader life-historical context of animal aggression.

Summary

Contests between beetles have attracted the attention of biologists and natural historians for a long time. Contests almost always involve males competing for females or for access to resources crucial to female reproduction. With only a few exceptions, beetle contests typically involve non-injurious trials of strength. In this chapter we begin by reviewing the literature on beetle contests with an emphasis on how ecological conditions and resource availability have shaped the nature of contests in diverse beetle families. We then focus on two inter-related aspects of the biology of beetle contests that have received particular and recent attention: the evolution of alternative reproductive tactics and the origin and diversification of weaponry. We describe the nature of alternative reproductive tactics in a range of beetle families, and explore the developmental and physiological mechanisms that have mediated contest diversification within and between species. We then explore the evolutionary developmental biology of weaponry in beetles, focusing on the elaborate horns of scarabs. Specifically, we describe how horns are built during development, and explore the relative contributions of conserved developmental mechanisms and novel developmental properties to the origin and diversification of horns. We then highlight several instances in which developmental studies have assisted our understanding of the evolution and ecology of contest behaviour, such as the ancestry of alternative phenotypes and sexual dimorphisms, the costs of weaponry and constraints and biases in the diversification of beetle weapons. Combining rich morphological and behavioural diversity with a diverse genetic and developmental toolbox, beetles emerge as a powerful model system in which to explore the causes, mechanisms and consequences of contest behaviour in nature.

Summary

Studies of contests among amphibians are heavily biased towards acoustic contests in frogs: in these, males compete to be attractive to females or to defend territories required for some aspect of reproduction. While the calls of frogs are species-specific and appear to be highly stereotyped, these studies have revealed a high degree of plasticity that enables males to vary their calls in response to their immediate circumstances. Because calling is energetically expensive, males must face trade-offs between increasing their immediate calling effort and conserving energy for future mating opportunities. In some species, they also trade-off between repelling rival males and attracting females; this is because females are averse to aggressive calls. There is a great deal less known about contests among salamanders and caecilians, primarily because these animals are much harder to observe and because their primary means of communication, olfaction, is harder to manipulate experimentally than the acoustic signals of frogs. Despite many unanswered questions, a great deal has been learned about aggressive behaviour in amphibians, and these studies have made important contributions towards a general understanding of animal contests. This chapter discusses the diversity of issues related to contest behaviour in amphibians and highlights how these organisms remain fruitful subjects for future studies of animal contests.

Introduction

Compared with birds and mammals, amphibians are still a poorly known group of animals with one or two new species still being described each week: 20 years ago, 5399 species were listed (Halliday & Adler 2002) with the number currently exceeding 7000 (AmphibiaWeb). In part, this reflects the fact that amphibians are typically small animals that lead secretive lives and engage in observable behaviour for limited periods of time. As a result, our knowledge of the social behaviour of amphibians is fragmentary, with only a few species studied intensively. An encyclopaedic overview of amphibian behaviour is provided by Wells (2007).

Summary

Animal contests were the focal topic that brought game theory to the attention of behavioural ecologists, giving rise to evolutionary game theory. Game theory has remained by far the most popular method of deriving theoretical predictions ever since, although it nowadays coexists with other methods of analysis. Here I review the developments to date and highlight similarities and differences between models. There is a clear progression from simple two-player models with fixed payoffs to explicit tracking of fitness consequences in a population context. In many cases this development has helped to discover that some of the early predictions may have been misleading. Despite the large number of current models, there are still gaps in the theoretical literature: sometimes simplifying assumptions have been relaxed in one context but not another. I hope that by highlighting these gaps theoreticians will be provided with new research ideas, and empiricists will be encouraged not only to distinguish between existing models but to be able to point out assumptions that are essential for deriving a result yet may be violated in existing systems, thus directing new modelling in the most useful direction.

Introduction

Until the mid 1960s, animal contests were viewed using group selectionist thinking. Julian Huxley (1966) thought that ritualised fights evolved to limit intraspecific damage, partly based on Konrad Lorenz's (1964, 1965) ideas that species need to evolve mechanisms that limit aggression in species that possess dangerous weapons for other reasons, e.g. as adaptations for capturing prey. Following George C. Williams’ (1966) book Adaptation and Natural Selection: A Critique of Some Current Thought, however, biologists became aware of the need to distinguish between explanations that are based on benefits to the individual versus those that rely on benefits accruing to a group (or a species).

Summary

Work on birds has prompted some key theoretical developments in the field of animal contests. Birds have an unusually conservative morphology, which constrains the ability of many species to fight physically, but many birds have evolved adaptations to aid in conflict resolution. These include the display of bright colours, elaborate vocalisations and physiological mechanisms. Birds also have a relatively conservative life history (parental care is ubiquitous), which influences the nature and extent of contests: for most birds, competition begins at birth for access to food provided by their carers. Intense resource competition continues into their adult lives, especially as many birds are territorial and/or reside in social flocks of related and/or unrelated conspecifics. At breeding, competition for access to mates is particularly severe, with birds competing both overtly and more cryptically to gain fertilisation precedence. Here I consider the diversity of avian contests.

Introduction

Bird contests can be highly conspicuous. An example is the ferocious fighting that occurs between two unfamiliar (or staged) jungle fowl (Gallus gallus domesticus) where males may fight to the death using sharp-pointed spurs as weapons (Mench 2009). Many avian contests are, however, less physical. Under more natural circumstances, for example within the jungle fowl's mixed-sex flock, disputes between flock members are unlikely to escalate to physical fighting (Ligon et al. 1990, Collias & Collias 1996). Agonistic encounters generally involve stereotyped behaviours, a range of complex vocalisations, and variation in conspicuously coloured morphological traits (e.g. Ligon et al. 1990, Cornwallis & Birkhead 2008). Nevertheless, the lack of physical contests does not necessarily indicate an absence of competition. Indeed, birds compete for the same things that cause and define competition in other taxa. However, there are a number of general avian morphological and life-history adaptations that are likely to have influenced the nature of competition in birds.

Summary

Animal conflict typically manifests itself as an aggressive interaction between two individuals, but the nature of this interaction can sometimes be influenced by third parties. For example, in some systems, individuals can observe fights between others and use the information they gain to help shape their own fighting strategies. Fighters themselves can modify their own behaviour dependent on whether an audience is present, and winners of fights sometimes display their victory to bystanders. In other systems, fights are genuinely polyadic and coalitions can form, with two or more individuals forming an alliance to protect or obtain a valuable resource. These coalitions often involve two individuals fighting one individual but sometimes contests more akin to warfare can take place between two large groups of individuals. Ecological interactions are shaped by natural selection and frequently involve cases in which the payoff from adopting any given behavioural strategy is dependent on the strategies adopted by other members of the population. So games, mathematical models of strategic interaction, are potentially a powerful tool to represent and analyse many of the multi-party contests described above. In this chapter we briefly review examples of multi-party contests in nature before going on to describe how and why such contests have been represented mathematically and the types of insight these models have delivered. Conflicts that take place within large networks are, almost by definition, complex affairs, but here we show that the representation of multi-party contests as triadic interactions can go some way to explaining a variety of phenomena ranging from victory displays to neighbour intervention and that these models can provide benchmarks for the exploration of more complex systems. Finally, we briefly review where this modelling work may lead, and identify some challenges that lie ahead.

Summary

Fishes have been central to our understanding of many of the major aspects of contest behaviour, extending from Tinbergen's early work on social releasers to some of the initial tests of assessment models and now to the neuroendocrine and genomic regulation of aggression and dominance. In this chapter, we focus on some exciting areas of research in fish contest behaviour that promise to shed light on the multidimensionality of resource holding potential (RHP), sex- and size-related differences in decision-making during contests, whole-organism performance and fight outcomes, selection and potential constraints on contest behaviour; and the role of developmental plasticity in driving RHP-related phenotypic variation. We have developed this chapter more as a prospectus than a review, using the concrete foundation laid down by numerous researchers to highlight areas that could be of great import in the years to come. This approach, of course, leaves us with many unanswered questions that we hope will serve as a springboard for rigorous hypothesis testing using an integrative framework for fish contest behaviour.

Introduction

The formal study of fish aggression has a long and prolific history dating back at least 70 years to a curious observation of three-spined sticklebacks, Gasterosteus aculeatus, responding intensely to a red postal truck that would occasionally pass the window of Niko Tinbergen's laboratory (Kruuk 2003, p. 87). What triggered aggression in the sticklebacks, of course, was not the truck but rather the colour red, a trait that males boast on their throat and ventral surface during the breeding season (ter Pelwijk & Tinbergen 1937), and that might indicate an imminent threat to a resident male's territory (Bolyard & Rowland 1996). Tinbergen and his contemporaries subsequently made significant efforts to identify behavioural, morphological and chromatic ‘releasers’ of aggression (e.g. Seitz 1940, Tinbergen 1948 and references in Earley et al. 2000).

Summary

Reptiles, especially sexually selected lizards, have proven to be good model systems for studying the evolution of contest competition. Aggression, especially by males, plays an important role in structuring reptilian social systems often characterised by territorial defence and both fixed and plastic alternative male tactics. Reptilian aggressive behaviour ranges from overt physical attacks that are likely to require significant energy expenditure and risk of injury to less costly signalling using visually conspicuous stereotypical motor patterns, striking colouration and chemical cues. Morphological traits that promote success in aggressive contests involve development of exaggerated and specialised physical armaments, colour conspicuousness, as well as whole animal performance traits and large overall size. Aggressive behaviour patterns may also be influenced by body temperature, prior social experience and other social variables that affect the context of social interactions. Lizards especially are important models for tests of both the proposed influence of hormones on aggression, as well as the possible effects of aggression on hormone levels. Lastly, lizards have also been used to test the extent to which game-theoretic models can be used to explain the evolutionary maintenance of alternative colour/behaviour morphs and the outcome of dyadic aggressive contests.

Introduction

Extant vertebrates commonly known as ‘reptiles’ actually include three lineages that are related only distantly (Zug et al. 2001, Vitt & Caldwell 2009). Although the fossil record suggests fascinating hypotheses pertaining to intraspecific aggression in some extinct reptiles (e.g. Hieronymus et al. 2009, Peterson et al. 2009), for obvious reasons, research on contest behaviour has focused on extant forms. For this chapter, ‘reptiles’ thus refers to the extant members of three clades: Crocodilians (alligators and crocodiles), Chelonians (turtles) and, especially, the Lepidosauria (tuataras, lizards and snakes).

Animal contests in nature

Next time you stand on a seashore and look carefully with your ‘zoologist's eyes’, you may be surprised at the high diversity of animal phyla that are present, even within a single intertidal rock pool. If you are patient and can stay still for a few minutes, another surprise in store is the preponderance of aggressive behaviour demonstrated by the intertidal fauna. Depending on which part of the world your rocky shore is in, you might observe some of the following: male Azorean blennies fighting over the nests that they need in order to attract females; pre-copula pairs of shore crabs with inter-male aggression over the ownership of recently moulted females, as these females are only receptive to sperm during a brief post-moult period; common European hermit crabs rapping in an attempt to evict an opponent from its gastropod shell; and, if you really have a lot of time on your hands, you might notice slow-moving sea anemones striking one another with special tentacles called acrorhagi, during disputes over space. Of course, aggressive behaviour is not restricted to intertidal marine animals. Take a walk in the woods and you could witness aggression over the ownership of territory; this is one of the reasons why male birds sing, why male butterflies perform many of their aerial displays and why armies of female worker wood ants try to kill individuals from a different colony. These examples illustrate two important points about aggression: first, animals will fight over a range of resources, when the ability to access those resources is a major constraint on fitness. In many cases this involves conflict over access to mates, as in the case of shore crabs. However, other resources such as territory, food and shelter are also contested, and influence the fitness of females as well as males. The second point is that aggressive behaviour is extremely widespread among animal taxa: these examples alone are drawn from three different phyla: chordates, arthropods and cnidarians.

Summary

Crustaceans have been used extensively to study aggression from a variety of perspectives. Traits that make them good models for studies of aggression include the possession of prominent weapons and a ready willingness to fight, the ease with which they may be obtained and their ease of maintenance in the laboratory. Furthermore, hard exoskeletons mean that equipment such as heartbeat sensors can be easily attached directly to the animals and they are very amenable to physiological investigation. Therefore a feature of studies into the contest behaviour of crustaceans is a strong link between ultimate ‘functions’ and proximate ‘mechanisms’. Given the very wide range of studies on crustacean aggression any review of this group could potentially be extremely broad in focus. Rather than attempt such a broad review, I focus on studies that have combined ethological data with data on underlying mechanisms in order to address questions that have arisen from the body of evolutionary contest theory described in Chapter 2. This has meant that some areas of research on aggression in the Crustacea, such as the neuroendocrine control of aggression and studies of social aspects of aggression such as dominance hierarchies, are outlined only briefly. I consider evidence for information-gathering and decision-making in respect of resource holding potential and resource value, and describe how studies of the underlying motivation to fight can provide useful insights into what information fighting animals might use when making strategic decisions. I also consider studies of agonistic signals, which in crustaceans include visual, tactile and chemical modalities, with a particular consideration of the extent to which ‘dishonesty’ might play a role in crustacean agonistic dealings. I then review physiological aspects of fighting in crustaceans, including studies based on post-fight assays of metabolites and by-products, studies based on ‘real-time’ non-invasive techniques and studies based on a functional morphology approach of investigating whole organism performance capacities. Finally, I suggest ways in which studies on crustacean contests could inform new theoretical models of contest behaviour and discuss the potential for applying approaches used to study crustaceans to the study of contests in other taxa.

Summary

The insect order Hymenoptera is speciose, diverse and common. Many wasps, bees and ants are well known for their ability, and propensity, to engage in agonistic interactions via biting and stinging (chemical injection), and may also interact using chemical deposition and volatile chemical release. Such behaviours are often exhibited during acquisition and defence of resources contested either by conspecifics or by allospecific hymenopterans. Here we examine the types of contests engaged in by social and non-social hymenopterans and highlight links between these and further aspects of evolutionary and applied biology. We first consider factors influencing the outcomes of contests between pairs of females over resources for reproduction. Studies of female–female contests in bethylids and several non-aculeate species of parasitoid wasps, especially scelionids, pteromalids and eupelmids, have addressed fundamental causes of the outcomes of contest interactions and have further linked contest behaviour to strategies of patch exploitation, clutch size and parental care. Further, we review links between the study of contest behaviour in parasitoids and their use as agents of biological pest control, particularly in terms of how contest behaviour may constitute intra-guild predation and influence strategic decisions to deploy single or multiple species of natural enemies. We then consider contests between males for access to mates, especially those engaged in by fig wasps and other wasps. Male–male contests are placed in the context of the evolution of alternative male morphs, mating systems, sex ratios and social behaviours. Finally, we return to female–female contests, this time examining them in the more complex context of the social Hymenoptera, in which both between-individuals (intra-colony) and between-group (inter-colony) contests occur.