Toward a Resolution of the Paradox of Aggressive Displays: II. Behavioral Efference and the Communication of Intentions

An inference from game-theory models of animal conflict is that adversaries should not inform one another about their level of aggressive motivation. This poses a paradox for the traditional ethological account of graded aggressive displays because it is usually assumed that the adaptive significance of these behavior patterns lies in their making such information available. To resolve the paradox, I propose that communication is only an incidental effect of displays, and that their primary adaptive function is regulation of the intensity of aggressive encounters through positive feedback on aggressive motivation, a process termed “behavioral efference.” Evidence in support of this hypothesis is drawn from studies of human facial expression, aggressive catharsis, and operant conditioning of aggressive behavior. Implications of the hypothesis and suggestions for further work are discussed.     

Calculating the ESS level of information transfer in aggressive communication

Summary We present a model of aggressive communication that demonstrates the use of evolutionarily stable ambiguous threat displays. We use stochastic dynamic programming to solve a game in which two contestants of differing fighting ability communicate using cost-free threats. These contestants use communication strategies that supply information of varying reliability to the opponent. The results demonstrate that communication does not need to be either costly or unambiguous to be evolutionarily stable.     

Multiple Cues in Status Signalling: The Role of Wingbars in Aggressive Interactions of Male House Sparrows

During aggressive interactions, animals may signal their competitive ability by various ornaments referred to as badges of status. The use of a single badge predicting dominance rank occurs in many vertebrate species. However, animals often display multiple ornaments that may convey information about either different or the same aspects of the signaller's quality, or alternatively, may serve as signal amplifiers. We observed the fighting behaviour of male house sparrows in two captive flocks to investigate whether they may use multiple cues in status signalling during aggressive interactions. Beside the status‐signalling bib, male sparrows possess a conspicuous white wingbar that they often display upon aggressive encounters. We tested whether bib size and the wingbar's conspicuousness (i.e. its achromatic contrast with the neighbouring dark feathers) or its area predicted success in various aspects of fighting. We found that bib size strongly predicted overall fighting success (i.e. proportion of fights won) and defence success (i.e. proportion of successful defences out of all attacks received). Wingbar conspicuousness was positively related to defence success after controlling for the effect of bib size in multivariate analyses. Furthermore, displaying the wings also tended to improve the birds’ success in defence but not in attack. Wingbar area was unrelated to any measured aspect of fighting ability. We suggest that bib size and wingbar conspicuousness may convey multiple messages on fighting abilities, specifically on overall aggressiveness and defending potential, respectively. Alternatively, wingbars may serve as amplifiers for the wing displays of aggressive motivation. Thus, male sparrows may use multiple cues in assessing the competitive ability of opponents during social interactions.     

Social Eavesdropping: A Game-Theoretic Analysis

Here we extend the classic Hawk-Dove model of animal conflict to allow for continuous variation in fighting strengths. Whereas the winner of a fight is chosen at random in the discrete game, in our continuous game, the winner of any fight is the stronger individual, and costs are higher for more evenly matched opponents. We identify the evolutionary stable strength threshold beyond which an animal should be prepared to engage in aggressive behaviour and show that this threshold increases with variance in fighting strength when the costs of aggression are insensitive to the level of strength asymmetry, but decreases with variance when the costs are sensitive to the level of asymmetry. In contrast to the classic discrete game, population-wide aggressive behaviour occurs only when the costs of fighting are zero. It is now known that animals can eavesdrop on the outcome of contests between neighbours and modify their behaviour towards observed winners and losers. We therefore further extend our model to allow for social eavesdropping within networks comprising three individuals. Whereas earlier work showed that eavesdropping increases the frequency of mutually aggressive contests in the discrete game by enhancing the value of victory, here we show that aggression thresholds in the continuous game are always higher with eavesdropping than without it: for sufficiently weak animals, avoiding the costs of challenging an observed winner over-rides the potential benefit of winning, so that eavesdropping reduces the frequency of aggressive encounters. Thus, even though strength is not directly observable, information is extracted from the variation in fighting ability that the classic Hawk-Dove game ignores.     

Chemoreception and the Assessment of Fighting Abilities in the Lizard Liolaemus monticola

When an individual faces the risk of a conflict, its ability to make ‘correct’ decisions is crucial to its fitness. Research on decision making has focused mainly on visual and acoustic signals, while chemical signals have received much less attention, despite their relevance for many species. Chemosignals can be detected in the absence of the signaller and, in the context of fighting risk, this property confers the advantage that the receiver can avoid agonistic interactions or, if they are unavoidable, that it can prepare itself for the conflict. I studied the behaviour of males of the lizard Liolaemus monticola in the laboratory when they were confronted with chemosignals of a potential opponent. During this ‘pre‐confrontation’ stage, I tested the following predictions: (1) lizards can derive precise information from chemosignals of conspecifics, and use this to respond with precision to the perceived risk and (2) the best predictor of the receiver behaviour, and therefore the best predictor of the risk involved in the fight, is the relative fighting ability of opponents. As a measure of fighting ability, I used body size. ‘Intruders’ were placed in the terrarium of unfamiliar ‘residents’ during the absence of the latter, and their behaviours were recorded. Simple regressions were performed between the different behavioural variables and with the body sizes of intruder and resident, and with the relative difference in body sizes of opponents. The latter was the best predictor of intruder behaviour: it was negatively correlated with behaviours associated with activity (i.e. motion time), chemoexploration (i.e. number of tongue flicks) and behaviours associated with social interactions (i.e. head bobs). These results suggest that males can process information from chemosignals and decisions made during the ‘pre‐confrontation’ stage are based on the assessment of the relative fighting abilities (i.e. relative body size) of opponents.     

Male Siamese fighting fish use gill flaring as the first display towards territorial intruders

The Siamese fighting fish (Betta splendens) is well known as an aggressive fish with unique spawning and parental care behavior. During reproduction, male fish construct a bubble nest, court females, protect the brood, and defend the territory through aggressive displays. Aggression in male Siamese fighting fish has long been the subject of investigation; however, the kinematics of aggression during contests have been largely overlooked. Here we investigated how nest-holding, male Siamese fighting fish use two different types of displays, gill flaring and fin spreading, towards intruders during various reproductive phases; before (BB) and after bubble nest building, and after spawning (AS), and hatching (AH). Males were more aggressive towards male than female intruders and the level of aggression changed significantly between reproductive phases. Gill flaring, the more energetically costly display, was the dominant initial display towards male and female intruders in BB, AS, AH phases. However, defending males switched to fin spreading after prolonged exposure to intruders. The results suggest that Siamese fighting fish use gill flaring as an acute response in order to defend their territory; this response may be replaced by fin spreading as a chronic response, probably to reduce the energetic costs during the contest.     

Fighting costs stabilize aggressive behavior in intersexual conflicts

We analyze the evolution of aggressive behavior in intersexual conflicts, with a special reference to mate guarding behavior in crustaceans. An analysis of a discrete-strategy game shows that an ESS with only one of the sexes being aggressive prevail if fighting costs or fitness values of winning are asymmetric. Non-aggressiveness of both sexes is stable if fighting behavior is very costly for females and if the cost is at least partly paid independent of the strategy of the opponent. Most interestingly, the solutions of both sexes being aggressive prevails only if both sexes have some probability of winning, and if fighting costs are small. Second, we solve for the expected levels of aggressiveness in a game with continuous strategies. The form of the fighting cost function largely determines the stability of the solution. When fighting cost increases linearly with aggressiveness, mutual aggressiveness fluctuates cyclically instead of stabilizing at an ESS. However, if there is an asymmetry in fitness payoffs, a solution with only the sex having most to lose being aggressive alone is possible. With quadratically increasing fighting costs an ES combination of mutual aggressiveness may exist. It is predicted that fights between the sexes should be hardest when payoffs are symmetric, and that an overt behavioral conflict will always take place as long as there is a fitness loss to each of the sexes if losing the conflict and both sexes have a chance to win. We discuss the models in the context of fights preceding precopulatory guarding, but the models offer a general frame for analyzing any intersexual conflict. This revised version was published online in July 2006 with corrections to the Cover Date.     

Pitch lowering enhances men's perceived aggressive intent,not fighting ability

Voice pitch is the primary perceptual correlate of fundamental frequency (f_o) and describes how low or high a voice is perceived by listeners. Prior research showed that men whose habitual voice pitch is lower are perceived to have stronger fighting ability. However, voice pitch is also flexible and can thus be used facultatively to signal states that change situationally, such as current aggressive intent (i.e., readiness to use aggression). Drawing on motivation-structural-rules theory, this research tests the hypothesis that male speakers will be perceived as more likely to attack when they lower (compared to raise) their pitch to address an adversary in a conflict situation. Three experiments using male speakers and listeners supported this hypothesis, both with and without controlling for the perception of the speakers' fighting ability. In contrast, the same experiments found no evidence that pitch lowering enhanced the speakers' perceived fighting ability after controlling for their perceived aggressive intent. Moreover, we found mixed evidence that the speakers' perceived physical strength interacted with pitch modulation to influence their perceived aggressive intent. On balance, these findings show that, at least for men, pitch modulation is primarily an aggressive-intent signal assessed independently of signalers' fighting ability. Future research should distinguish between perceptions of aggressive-intent and fighting-ability when examining the perceptual effects of male voice-pitch modulation in intrasexual competition.     

The role of asymmetries in animal contests

This paper contains a game theoretical analysis of animal contest situations which are asymmetric in more than one aspect: two opponents may for example be imagined which differ in ‘ownership status’ as well as in ‘relative fighting ability’. The following question is analysed: which aspect may or must be used for conventional settlement in a population ‘playing’ an evolutionarily stable strategy (ESS)? The contestants are assumed to be fully informed about the asymmetric features. In particular, the assessment of relative fighting ability is supposed to be unambiguous and without cost. This assumption of perfect information allows for a decomposition of the ‘evolutionary game’ into sub-games. Therefore an easy procedure for calculating the ESS's can be presented, and simple models are analysed. It is concluded that payoff-irrelevant aspects may be used for conventional settlement of a conflict even if payoff-relevant asymmetric aspects also exist. One of the aspects may, however, be of such strong relevance that, no matter which ESS is played, animals must base their decisions on that ‘dominant’ aspect. It may also occur that two different asymmetric features are each of strong payoff relevance for either of the opponents, such that they have no escalation-suppressing effect. The particular scenario of a conflict between an ‘owner of a resource’ and an ‘intruder’ is used to derive the more general conclusions.     

Absence of Mate Guarding in the Yellowhammer (Emberiza citrinella)?

The mate guarding behaviour of male yellowhammer (Emberiza citrinella) was studied with special reference to the effects of age, body size (tarsus length) and coloration of males. Measurements of intra-pair distance do at the most provide evidence for relatively lax mate guarding. On the other hand, patterns of male song activity and inter-male aggression were more in agreement with the predictions of the mate guarding hypothesis. The reasons for the comparatively low mate guarding intensity in the yellowhammer may be that males do not need to guard their mates intensely. Age differences were found in song and aggressive activity, older males singing and fighting the most. Size had no effect on guarding behaviour. Coloration was correlated with inter-male aggressiveness and conflict initiation propensity. Less colourful males fought the most in the pre-fertile period of their mates, whereas colourful and old males fought the most during the fertile period. This suggests that coloration may be an indicator of individual fighting and guarding ability.     

An empirical test of Lanchester's square law: mortality during battles of the fire ant Solenopsis invicta

Lanchester's models of attrition describe casualty rates during battles between groups as functions of the numbers of individuals and their fighting abilities. Originally developed to describe human warfare, Lanchester's square law has been hypothesized to apply broadly to social animals as well, with important consequences for their aggressive behaviour and social structure. According to the square law, the fighting ability of a group is proportional to the square of the number of individuals, but rises only linearly with fighting ability of individuals within the group. By analyzing mortality rates of fire ants (Solenopsis invicta) fighting in different numerical ratios, we provide the first quantitative test of Lanchester's model for a non-human animal. Casualty rates of fire ants were not consistent with the square law; instead, group fighting ability was an approximately linear function of group size. This implies that the relative numbers of casualties incurred by two fighting groups are not strongly affected by relative group sizes and that battles do not disproportionately favour group size over individual prowess.     

If animals know their own fighting ability, the evolutionarily stable level of fighting is reduced

We consider a version of the Hawk-Dove game in which an animal knows its own fighting ability but not the ability of its opponent. For this game at evolutionary stability there is a critical level of ability such that animals with ability greater than the critical level play Hawk and animals with ability below the critical level play Dove. We define the level of fighting to be the probability of a Hawk-Hawk fight when two opponents meet. We show that even if an animal does not know the ability of its opponent, knowing its own ability results in a lower level of fighting at evolutionary stability than is found in the standard Hawk-Dove game in which there are no differences in ability or abilities are not known.     

Know thine enemy: fighting fish gather information from observing conspecific interactions

Many of the signals that animals use to communicate transmit relatively large distances and therefore encompass several potential signallers and receivers. This observation challenges the common characterization of animal communication systems as consisting of one signaller and one receiver. Furthermore, it suggests that the evolution of communication behaviour must be considered as occurring in the context of communication networks rather than dyads. Although considerations of selection pressures acting upon signallers in the context of communication networks have rarely been expressed in such terms, it has been noted that many signals exchanged during aggressive interactions will transmit far further than required for information transfer between the individuals directly involved, suggesting that these signals have been designed to be received by other, more distant, individuals. Here we consider the potential for receivers in communication networks to gather information, one aspect of which has been termed eavesdropping. We show that male Betta splendens monitor aggressive interactions between neighbouring conspecifics and use the information on relative fighting ability in subsequent aggressive interactions with the males they have observed.     

Socially stable territories: the negotiation of space by interacting foragers

This article presents a theory of territoriality that integrates optimal foraging and conflict resolution through negotiation. Using a spatially explicit model of a sit-and-wait forager, we show that when resources are scarce, there is a conflict between foragers: there is not enough space for all individuals to have optimal home ranges. We propose that a division of space that solves this conflict over resources is the outcome of a negotiation between foragers. We name this outcome the socially stable territories (SST). Using game theory we show that in a homogenous patch occupied by two interacting foragers, both individuals receive identical energy yields at the socially stable territories; that is, there is economic equity. Economic inequity can arise in a heterogeneous patch or from asymmetries in fighting abilities between the foragers. Opportunity costs play a role in reducing economic inequity. When the asymmetry in fighting abilities is very large, a negotiated division of space is not possible and the forager with lowest fighting ability may be evicted from the habitat patch. A comparison between territories and overlapping home ranges shows that energy yields from territories are generally higher. We discuss why there are instances in which individuals nevertheless overlap home ranges.     

Sound Characteristics and Outcome of Contests in Male Croaking Gouramis (Teleostei)

A correlative study using similar-sized males of the croaking gourami Trichopsis vittata was carried out to investigate whether sound characteristics influenced winning and if relative fighting ability was assessed by acoustic signals. Pair-wise contests between males were decided using lateral displays (LD) and vocalization in 26 cases, whereas 66 fights escalated to the frontal display (FD) phase. Physical fighting (mouth wrestling) and injuries were rarely observed in this species. Winners were generally larger than their opponents, and this effect was more pronounced in non-escalated than in escalated contests. Sounds of fight winners had a higher sound pressure level and also a lower dominant frequency. Neither number of acoustic signals nor duration of lateral and frontal displays were predictors of contest outcome. Acoustic measures were highly correlated to body weight. These results indicate that traits correlated with RHP (such as sound pressure level and dominant frequency) were predictors of the outcome, while traits not correlated with size (such as number and duration of displays) did not influence winning. In accordance with the main prediction of assessment models, the contest duration (cost) increased with the decrease in asymmetry of body length as well as sound pressure level. No such relationships were found for weight and dominant frequencies in LD- and FD-contests. The present study indicates that morphological and sound characteristics influence winning in fish. Moreover, the results suggest that croaking gouramis settle conflicts without damaging combats by assessing asymmetries in different components of RHP such as body weight and length, which may reliably be signalled by acoustic and visual assessment signals.     

Is the parallel walk between competing male fallow deer, Dama dama, a lateral display of individual quality?

During competitive encounters protagonists are expected to use signals of individual quality particularly if there is a risk of injury or death. Lateral presentation of body profile, by which information regarding phenotypic characteristics associated with individual quality are displayed, may represent such a strategy. During aggressive interactions, male fallow deer frequently engage in parallel walking which is assumed to represent a mutual display of quality, as mediated by exposure of the maximal profile of the body or antlers. We examined the context and role of the parallel walk during competitive encounters to investigate whether there was evidence that dyads of competing males were assessing differences in phenotypic characteristics. There was no evidence to support the hypotheses that the parallel walk is a lateral display of body size or weaponry or that its use is associated with a reduced level of escalated or risky behaviours during fighting. Total time spent fighting was not shorter when a parallel walk was present than when there was no parallel walk. The parallel walk was highly associated with fighting and it was more likely to be initiated by the subsequent loser. Furthermore, parallel walking frequently followed bouts of fighting and as such may represent a strategy that permits an animal the opportunity to decide whether to continue fighting. Parallel walking was also associated with a failure to resolve contests in favour of one animal indicating that it may be a means of withdrawing from further fighting without incurring a loss in dominance status. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens

The evolution of signals has mainly been considered in the contextof an emitter-receiver dyadic interaction. However, communicationusually occurs in the presence of individuals (an audience)that are not directly involved in the communication interaction,and it is more realistic to assume that signal evolution occursin a network. Several types of information could be available to an audience, and, therefore, the presence of an audiencecould have effects on the behavior of the communicating animalsand on signal evolution. We investigated whether the presenceof an audience of conspecifics affected intrasexual aggressivecommunication in male fighting fish. We found that if the audiencewas a female, males increased the intensity of conspicuous displays that can be used in communication with both males andfemales and decreased highly aggressive displays that are solelydirected to males. If the audience was a male of similar size,there was no significant change in the way in which males displayed.These results suggest that the presence of an audience couldbe one reason that many long-range and conspicuous signals are often shaped to transmit information to both males and females     

Evolution of fighting behavior under asymmetric competition: an experimental test with juvenile salmonids

Large-dominant and small-subordinate species engaging in asymmetricinterference competition may optimize behavior under differenttrade-offs between the chance of winning and the cost of fighting.If fighting behavior is heritable and under selection, theorysuggests that large-dominant and small-subordinate species shouldevolve aggressive and passive fighting behaviors, respectively.To test this prediction, I manipulated the size and competitiveasymmetry of juveniles from sympatric populations of large-dominantcoho salmon (Oncorhynchus kisutch) and small-subordinate steelheadtrout (O. mykiss) and asked whether differences in fightingbehavior persisted independently of competitive ability. I observedfighting behavior during dyadic contests in two habitats, mutuallypreferred pools and energetically demanding riffles, under eachof three size treatments: natural size asymmetry, asymmetryremoved, and reversed size asymmetry. The results supportedthe prediction. Competitive ability depended primarily on size;large individuals of both species dominated smaller heterospecifics,and neither species dominated when size matched. Fighting behaviordepended primarily on species identity; coho salmon used a higherproportion of aggressive chases, whereas steelhead trout useda higher proportion of passive displays. Large individuals weremore likely to chase, and small individuals were more likelyto display. As evidence that asymmetric competition is associatedwith behavioral divergence, these results complement previouswork on morphological divergence under asymmetric competitionand provide a richer context for other features of the coho–steelheadsystem.     

Resource value and the context dependence of receiver behaviour

Many animals use signals of fighting ability to minimize the costs of competition. Theory predicts that signals must be costly to remain reliable indicators of their bearer's abilities, but many signals of fighting ability lack obvious developmental costs. Instead, receivers are thought to maintain signal accuracy by behaving aggressively towards individuals with inaccurate signals (i.e. social costs). Models predict that the evolutionary stability of social cost signals depends on receivers trusting signals in certain contexts and testing signal accuracy in other contexts. Here, I use the signals of agonistic ability in Polistes dominulus wasps to provide the first experimental evidence that receiver responses to social cost signals are context dependent. During contests over low-value resources, wasps trust signals; they avoid patches of food guarded by rivals with elaborate signals. As the value of the resource increases, wasps become more likely to test signal accuracy. In fact, receivers challenge guards regardless of their signal phenotype when the resource is sufficiently valuable. Context-dependent receiver responses are likely to be an important behavioural mechanism underlying the evolution of social costs, as context-dependent responses allow receivers to minimize the costs of conflict while also ensuring signal accuracy.     

The human anger face evolved to enhance cues of strength

Animals typically deploy their morphology during conflict to enhance competitors' assessments of their fighting ability (e.g. bared fangs, piloerection, dewlap inflation). Recent research has shown that humans assess others' fighting ability by monitoring cues of strength, and that the face itself contains such cues. We propose that the muscle movements that constitute the human facial expression of anger were selected because they increased others' assessments of the angry individual's strength, thereby increasing bargaining power. This runs contrary to the traditional theory that the anger face is an arbitrary set of features that evolved simply to signal aggressive intent. To test between these theories, the seven key muscle movements constituting the anger face were systematically manipulated one by one and in the absence of the others. Raters assessed faces containing any one of these muscle movements as physically stronger, supporting the hypothesis that the anger face evolved to enhance cues of strength.