Unfamiliar Opponents Research Articles

Territorial behaviour and conflict management in a semi-social cichlid fish, Neolamprologus caudopunctatus

Abstract Conflict solving strategies can prevent fights from escalating and reduce the costs of aggressive encounters. Having the capacity to efficiently assess an opponent’s fighting abilities before fully committing to a fight is a useful social skill. Here, we conducted two experiments to investigate how a colony living, cichlid species, Neolamprologus caudopunctatus, changes its aggressive behaviour when faced with familiar vs unfamiliar opponents. First, we staged size matched, same-sex, dyadic resource contests and found that fights were always of low-intensity with neither familiarity nor sex influencing how quickly the conflict ended. Second, we explored the dual defence of mated territorial pairs together defending their territory boundaries against other pairs, either familiar or unfamiliar ones, and discovered that fights between two pairs were more vigorous, and that unfamiliar neighbouring pairs were attacked significantly more often than familiar pairs. We also observed that dark bars sometimes appeared on the sides of contestant’s bodies, and that these bars were far more common in winners than in losers, suggesting that these might be visual signals of dominance. However, conflicts where contestants displayed bars were of longer duration than those without. Taken together, our results further advance our understanding of territoriality and conflict resolution strategies and set the stage for future studies focusing on how animals manage to co-exist in closely aggregated breeding territories and to form colonies.

Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system.

Losing a fight against a conspecific male (social defeat) induces a period of suppressed aggressiveness and general behaviour, often with symptoms common to human psychiatric disorders. Agonistic experience is also discussed as a potential cause of consistent, behavioral differences between individuals (animal “personality”). In non-mammals, however, the impact of single agonistic encounters typically last only hours, but then again studies of repeated intermittent defeat (chronic social defeat) are seldom. We report the effect of chronic social defeat in adult male crickets (Gryllus bimaculatus), for which all known behavioral effects of defeat last only 3 h. Firstly, after 48 h social isolation, crickets that experienced 5 defeats at 24 h intervals against the same, weight-matched opponent exhibited suppressed aggressiveness lasting >24 h, which was still evident when the animals were matched against an unfamiliar opponent at the last trial. Secondly, this longer-term depression of aggression also occurred in 48 h isolated crickets that lost 6 fights at 1 h intervals against unfamiliar opponents at each trial. Thirdly, crickets isolated as larvae until adult maturity (>16 days) were significantly more aggressive, and less variable in their aggressiveness at their very first fight than 48 h isolates, and also significantly more resilient to the effects of chronic social defeat. We conclude that losing an aggressive encounter in crickets has a residual effect, lasting at least 24 h, that accumulates when repeated defeats are experienced, and leads to a prolonged depression of aggressive motivation in subordinates. Furthermore, our data indicate that social interactions between young adults and possibly larvae can have even longer, possibly lifelong influences on subsequent behavior. Social subjugation is thus likely to be a prime determinant of inter-individual behavioral differences in crickets. Our work also opens new avenues for investigating proximate mechanisms underlying depression-like phenomena.

The role of ultraviolet coloration in intrasexual interactions in a colonial fish

Ultraviolet (UV) coloration varies drastically across species and likely plays fundamentally different roles in facilitating social communication depending on the ecological or social context. While it is well known that UV coloration serves important social functions in species that school and flock, far less is known about the role of UV coloration in group-territorial and colonial species, where individuals have long-lasting and potentially cooperative relationships with many neighbours. We measured spectral reflectance in Neolamprologus pulcher, a group-living, colonial Tanganyikan cichlid fish, and found prominent UV coloration on both sexes. We manipulated the visibility of this UV coloration using a clear UV-blocking filter or a UV-transparent filter during behavioural contests across a barrier. We found that trials between similarly sized same-sex opponents involved significantly lower frequencies of aggression when opponents' UV coloration was obscured compared to when opponents' UV coloration was visible. As aggression is typically high between similarly sized same-sex individuals in N. pulcher, this reduction in aggression suggests that UV coloration aids in motivating individuals to engage in conspecific intrasexual interactions. We found no difference in aggression in trials between familiar and unfamiliar opponents in female–female and male–female trials, regardless of the presence of UV coloration. In male–male trials, we found significantly higher frequencies of aggression in contests between familiar male opponents than in contests between unfamiliar male opponents, but only when UV coloration was visible. Collectively, these results suggest that UV coloration is important for intrasexual interactions and prompts further investigation as to the benefits of having visual signals of communication extend into the ultraviolet spectrum.

Opponent familiarity and contest experience jointly influence contest decisions in Kryptolebias marmoratus.

IntroductionIndividual recognition and winner/loser effects both play important roles in animal contests, but how their influences are integrated to affect an individual’s contest decisions in combination remains unclear. Individual recognition provides an animal with relatively precise information about its ability to defeat conspecifics that it has fought previously. Winner/loser effects, conversely, rely on sampling information about how an animal’s ability to win compares with those of others in the population. The less precise information causing winner/loser effects should therefore be more useful to an individual facing an unfamiliar opponent. In this study, we used Kryptolebias marmoratus, a hermaphroditic mangrove killifish, to test whether winner/loser effects do depend on opponent familiarity. In addition, as previous studies have shown that subordinates that behave aggressively sometimes suffer post-retreat retaliation from contest winners, we also explored this aspect of contest interaction in K. marmoratus.ResultsIn the early stages of a contest, subordinates facing an unfamiliar dominant were more likely to signal their aggressiveness with either gill displays or attacks rather than retreating immediately. A winning experience then increased the likelihood that the most aggressive behavioral pattern the subordinates exhibited would be attacks rather than gill displays, irrespective of their opponents’ familiarity. Dominants that received a losing experience and faced an unfamiliar opponent were less likely than others to launch attacks directly. And subordinates that challenged dominants with more aggressive tactics but still lost received more post-retreat attacks from their dominant opponents.ConclusionsSubordinates’ contest decisions were influenced by both their contest experience and the familiarity of their opponents, but these influences appeared at different stages of a contest and did not interact significantly with each other. The influence of a losing experience on dominants’ contest decisions, however, did depend on their subordinate opponents’ familiarity. Subordinates and dominants thus appeared to integrate information from the familiarity of their opponents and the outcome of previous contests differently, which warrants further investigation. The higher costs that dominants imposed on subordinates that behaved more aggressively toward them may have been to deter them from either fighting back or challenging them in the future.

Hermit crab, Pagurus middendorffii, males avoid the escalation of contests with familiar winners

Prior contest outcomes often affect subsequent contest behaviour (winner/loser effects). If contestants discriminate between familiar and unfamiliar opponents, individual recognition may alter the strength and/or manner of winner/loser effects. We examined whether hermit crabs, Pagurus middendorffii, changed their contest behaviour based on winner/loser effects, whether they distinguished a familiar opponent from an unfamiliar opponent, and how the familiarity with the opponent related to the winner/loser effects in male–male contests. Males of this species show precopulatory guarding behaviour, and male–male contests often occur between a guarding male and an intruder. In contests between unfamiliar males, intruders use self-assessment during the initial contact phase and mutual assessment during the physical combat phase to determine their behaviours. Precopulatory guarding males and females collected in the field were used in two consecutive trials of male–male contests. Losers in the first trial were used as focal intruders in the second trial with (1) a familiar opponent that had won the first trial, (2) an unfamiliar opponent that had won the first trial with another intruder, or (3) a naive opponent with no trial experience. Focal intruders did not alter their aggressiveness against either unfamiliar or naive opponents in the second trial. However, they rarely initiated physical combat against familiar opponents in the second trial. When they initiated combat, they gave up sooner against familiar opponents than against unfamiliar opponents. These results suggest that intruders are able to distinguish familiar opponents from others and decrease their aggressiveness only when they encounter familiar opponents. Our study therefore shows loser effects in P. middendorffii related to the familiarity with the opponent and suggests intruders can obtain information about their opponents during the initial encounter.

Behavioural determinants of agonistic success in invasive crayfish

Ecosystems today increasingly suffer invasions by multiple invasive species, some of which may share similar advantageous life history traits and ecological niche. In such cases, direct competition can influence invasion success of both species, and provide insights into competition without co-evolution in species equally novel to the environment. We used two widespread crayfish invaders of freshwater ecosystems of Europe, signal crayfish (Pacifastacus leniusculus) and spiny cheek crayfish (Orconectes limosus), to investigate how behavioural decisions in agonistic encounters contribute to competitive advantages in the absence of adaptation to either opponents or an environment. In direct competition against novel but comparable opponents, the key factor for establishing clear dominance of P. leniusculus in interspecific bouts was its greater tendency towards continued engagement in high-intensity fights. With O. limosus individuals consistently retreating from staged bouts as fights became more intense, P. leniusculus individuals did not need to adapt their strategy to be successful, suggesting that their agonistic behaviour intrinsically predisposed them to win. While both species are detrimental to invaded ecosystems, our results indicate that aggressive behaviour of P. leniusculus against unfamiliar opponents could allow it to more easily outcompete other comparable species and consequently present a potentially greater threat for native ecosystems.

Opponent familiarity influences the audience effect in male–male interactions in Siamese fighting fish

It is well established that communication in social organisms often occurs within a network of individuals rather than within signaller–receiver dyads. Most of these investigations, however, have not assessed how other social factors might influence communication. In the present study, we investigated whether previous exposure to an opponent influences audience effects on male–male interactions in Siamese fighting fish, Betta splendens. Males interacted with an unfamiliar opponent or a familiar opponent in the presence of a male, a female or no audience. Opponent-directed gill flaring was greatest when opponents were unfamiliar with one another and a male audience was present. In contrast, opponent-directed tail beats were most frequent when a female audience was present, especially when opponents were unfamiliar. Opponent familiarity appears to have a greater effect on opponent-directed gill flaring than on tail beats. This may reflect the difference in the function of these behaviours as tail beats are commonly used in courtship as well as during aggressive encounters. Our findings suggest that audience type and the social history of the opponents work together to influence aggressive interactions in this species.

Opponent recognition and social status differentiate rapid neuroendocrine responses to social challenge

Individual social status discriminates rapid neuroendocrine responses to non-social stress in male Anolis carolinensis, but whether such status-influenced reactions are retained in response to subsequent social stress is unknown. Dominant and subordinate males modify their behavioral responses to social challenge according to familiarity of the opponent, suggesting that accompanying neuroendocrine responses may differ according to opponent recognition despite social rank. We examined endocrine and neurochemical correlates of prior social status and opponent recognition during the opening stages of social challenge. Male pairs interacted and established dominant/subordinate status, followed by 3 days separation. Subsequently, subjects were paired with either the same opponent or an unfamiliar male according to rank (dominant with subordinate). After 90 s of social exposure, subjects were caught and brains and plasma collected for measurement of circulating corticosterone and limbic monoamines. Controls included pairs experiencing just one 90 s encounter plus a group of non-interacting subjects. Opponent recognition differentiated status-influenced responses, such that dominant lizards paired with familiar subordinate opponents had increased hippocampal dopamine and epinephrine, but showed increased plasma corticosterone and ventral tegmental area (VTA) norepinephrine when challenged with an unfamiliar opponent. Subordinate lizards encountering familiar opponents also had increased corticosterone, along with decreased hippocampal dopamine and increased VTA epinephrine, but showed no changes in response to an unfamiliar opponent. Such plasticity in status-influenced rapid neuroendocrine responses according to opponent recognition may be necessary for facilitating production of behavioral responses adaptive for particular social contexts, such as encountering a novel versus familiar opponent.

Intersexual differences in European lobster (Homarus gammarus): recognition mechanisms and agonistic behaviours

Dominance can be maintained through status recognition or recognition of individual (familiar) opponents. In crustaceans, both types of recognition exist, often based on chemical signals. Fight behaviours involved in establishment and maintenance of dominance relationships in male and female European lobster (Homarus gammarus) were examined. Same-sex pairs of size-matched animals interacted on two consecutive days, encountering either the same (familiar) or another (unfamiliar) opponent of the opposite dominance status in the second fight. Results show that both female and male H. gammarus establish dominance in a first encounter, and maintain dominance in a second interaction against a familiar animal, resulting in decreased fight duration and lower aggression levels. Female losers that met an unfamiliar dominant also had short second days with low aggression, while male losers responded to unfamiliar animals with high aggression and long fights. Thus, males distinguish between familiar and unfamiliar opponents, indicating individual recognition whereas females do not, indicating that they use dominance status recognition rather than individual recognition. Female-female fights involved more high-level aggression (claw lock) than male-male fights, contrary to the belief that male lobsters are more aggressive than females. H. gammarus fights also escalated to unrestrained violence fast, indicating low levels of ritualisation. (Less)

Individual recognition in crayfish (Cherax dispar): the roles of strength and experience in deciding aggressive encounters

The outcomes of agonistic interactions modulate access to resources and thereby affect fitness. Success in agonistic encounters may depend on intrinsic physical and physiological performance, and on social experience. Here we test the hypothesis that previous experience will override physical strength in determining the outcome of fights in the freshwater crayfish Cherax dispar. Between unfamiliar opponents, greater chelae closing force significantly increases the chances of winning. However, even when the chelae of the original winners were disabled, the winners kept on winning against the same opponents after 30min and 24h. This winner effect disappeared when previous winners encountered unfamiliar individuals. Similarly, a previous loss did not affect the outcomes of subsequent encounters with unknown crayfish. We suggest that this prolonged recognition of individuals and their relative fighting ability is a mechanism that can reduce the number of agonistic encounters experienced by individuals.

Learning and memory associated with aggression in Drosophila melanogaster

Male Drosophila melanogaster (Canton-S strain) exhibit aggression in competition for resources, to defend territory, and for access to mates. In the study reported here, we asked: (i) how long flies fight; (ii) whether flies adopt distinct winning and losing strategies as hierarchical relationships are established; (iii) whether flies exhibit experience-dependent changes in fighting strategies in later fights; and (iv) whether flies fight differently in second fights against familiar or unfamiliar opponents. The results showed that flies fought for up to 5 h. As hierarchical relationships were established, behavioral strategies changed: winners progressively lunged more and retreated less, whereas losers progressively lunged less and retreated more. Encounters between flies were frequent during the first 10 min of pairing and then dropped significantly. To ask whether flies remembered previous fights, they were re-paired with familiar or unfamiliar opponents after 30 min of separation. In familiar pairings, there were fewer encounters during the first 10 min of fighting than in unfamiliar pairings, and former losers fought differently against familiar winners than unfamiliar winners. Former losers lost or no decision was reached in all second fights in pairings with familiar or unfamiliar winners or with naive flies. Winner/winner, loser/loser, and naive/naive pairings revealed that losers used low-intensity strategies in later fights and were unlikely to form new hierarchical relationships, compared with winners or socially naive flies. These results strongly support the idea that learning and memory accompany the changes in social status that result from fruit fly fights.

Effects of Previous Experience on the Agonistic Behaviour of Male Crickets, Gryllus bimaculatus

Male solitary animals frequently enter aggressive interactions with conspecific individuals to protect their territory or to gain access to females. After an agonistic encounter, the loser (subordinate individual) changes its behaviour from aggression to avoidance. We investigated agonistic interactions between pairs of male crickets to understand how dominance is established and maintained. Two naïve males readily entered into agonistic interactions. Fights escalated in a stereotyped manner and were concluded with the establishment of dominance. If individuals were isolated after the first encounter and placed together 15 minutes later, subordinate crickets tended to avoid any further contact with the former dominant opponent. Moreover, subordinate males also avoided unfamiliar dominant and naïve opponents. They displayed aggressive behaviour only towards unfamiliar subordinate opponents. This suggests that the subordinate male change their behaviour depending on the dominance status of the opponent. Dominant crickets, in contrast, displayed aggressive behaviour towards familiar as well as unfamiliar opponents. If the interval between the first and second encounter was longer than 30 minutes, the former subordinate male showed aggressive behaviour again. However, if the subordinate cricket was paired with the same opponent three consecutive times within 45 minutes, it avoided the former dominant opponent for up to 6 hours following the third encounter. Our results suggest that the maintenance of dominance in male crickets depends largely on the behavioural change of subordinate individuals. Possible mechanisms to maintain dominance are discussed.

Opponent recognition in male green anoles, Anolis carolinensis

Male green anoles convey territorial ownership to rivals through use of stereotyped aggressive displays, with intrasexual interactions often escalating to physical combat. In the laboratory, losers of such interactions significantly reduce their aggressive behaviour when interacting with the same opponent 7 days later. In the current study, we examined whether this behavioural modification is a function of opponent recognition. Pairs of size-matched male A. carolinensis were allowed to interact for 2 h. Following this, subjects were separated for varying intervals, and then participated in a second interaction with either the same or an unfamiliar opponent. Losers of the first interaction significantly reduced their total aggressive behaviour when re-paired with the same opponent after a 3-day interval but not after a 10-day interval between the first and second interaction. However, losers of the first interaction failed to show reduced aggression during their second interaction when paired 3 or 10 days later with an unfamiliar opponent. Therefore, A. carolinensis appear to learn information specific to their opponent during an initial agonistic interaction, with the salience of this information declining when the interval between interactions increases. Males also showed low levels of chemosensory taste behaviour during agonistic interactions, suggesting that opponent recognition does not rely on chemoreception. Similarities between our results and findings from other vertebrate species suggest that the motivation to behave aggressively during social interactions can be influenced by opponent recognition rather than by previous experience of social defeat alone.

DOMINANCE HIERARCHIES AND STATUS RECOGNITION IN THE THREATENED CRAYFISH AUSTROPOTAMOBIUS ITALICUS

This study aims at investigating the formation and maintenance of dominance hierarchies in the white-clawed crayfish, Austropotamobius italicus, a threatened species in Italy. To this end, we investigated the behaviour of size-matched pairs of intact males and followed an experimental design composed of three phases: (1) isolation for a week, (2) combat for five days, and (3) experimental phase in Day 6. This latter phase consisted in switching individuals of the same or of a different status between 15 pairs and in leaving the remaining 5 pairs as before. Therefore, we formed pairs composed of unfamiliar (and familiar) opponents having different (and the same) status. The results show that (a) A. italicus establishes stable dominance hierarchies; (b) A. italicus is able to recognise the status, but not the identity, of its rival; and (c) status recognition is associated with “winner and loser” effects.

Multimodal individual recognition in the crayfish cherax destructor

There is some evidence that macrurans recognize each other as individuals. In freshwater crayfish there are conflicting reports and there is limited information about the sensory mechanisms involved. To determine the extent to which the crayfish Cherax destructor is capable of individual recognition, we performed experiments that familiarized animals with each other and then manipulated their recent success in dominance contests. Crayfish were more likely to win an encounter when paired against a familiar opponent than an unfamiliar one after the manipulation stage. In other experiments, animals were attracted to familiar conspecifics when only visual or chemical cues were present. This demonstrates that C. destructor is able to discriminate between a familiar and an unfamiliar opponent. The results highlight the complex nature of intraspecific communication in crayfish and suggest elements likely to be of importance in the social interactions of groups in the wild state.

Dominance hierarchies and status recognition in the crayfishProcambarus acutus acutus

In the eastern white river crayfish, Procambarus acutus acutus, the processes that act during hierarchy formation were explored by analyzing the behavior of 23 symmetric pairs of form I males. The experimental design comprised three subsequent phases: isolation, familiarization, and experimental phases. In the latter, pairs were formed of (i) unfamiliar opponents having different status, (ii, iii) unfamiliar opponents having the same status, either two alphas or two betas, and (iv) familiar opponents. The first result was that P. a. acutus is capable of establishing stable dominance hierarchies. Secondly, behavioral differences between the winners and the losers, a fast assessment of status, and self-reinforcing effects of recent experience were demonstrated. Thirdly, P. a. acutus was found to recognize the status of its rival but not its individual identity. In fact, even if paired with unfamiliar opponents, previous winners and losers behaved as in the preceding days. Conversely, both frequency and intensity of fighting increased when individuals of the same rank were opposed. These phenomena might be a consequence of "winning and losing effects". However, the increased readiness of former betas to attack contradicts the loser effect and validates the hypothesis of status recognition.

Urine makes the difference: chemical communication in fighting crayfish made visible.

Chemical communication is a widespread phenomenon in aquatic animals but is difficult to investigate because the signals are not visible. Here, we present the results of a study into chemical communication in blindfolded fighting crayfish (Astacus leptodactylus) in which we employed a new method: visualisation of urine using the dye Fluorescein. The probability of urine release is greater during fights than during non-social activities or inactivity. The eventual winners are more likely to release urine during fights than the eventual losers. In both winners and losers, urine release is coupled to offensive behaviours, and the probability of urine release increases with increasing levels of aggression. In A. leptodactylus, urine is carried to the opponent by the forward-projecting gill currents. During spontaneous release, urine is fanned laterally with the aid of the exopodites of the maxillipeds. Aggressive behaviour is effective in intimidating blindfolded opponents only in conjunction with urine release: receivers decrease offensive behaviour and increase defensive behaviour. Aggressive behaviour alone does not intimidate opponents. The loser of a recent fight is deterred equally well by a familiar and an unfamiliar opponent. Hence, in crayfish, individual recognition of the urine scent of a dominant individual does not appear to be significant for the maintenance of dominance hierarchies. Our results suggest that urine contains information about the fighting ability and/or aggressiveness of the signaller. The chemical signals thus far unidentified appear to be important in determining the outcome of a fight.

Fighting Strategies of Silvereyes, Zosterops lateralis.

We examined the cost-benefit patterns of strategies used by Silvereyes initiating aggressive encounters against unfamiliar opponents at a localized food source. We recorded initiator behaviour of individually colour-banded birds at a feeding station on Heron Island, Great Barrier Reef, and found that, in crowded conditions where most fighting occurred indiscriminately, initiators used more threat elements than attack elements and that dominant and lower-ranking birds did not differ in their strategies when initiating encounters. This is in contrast to more attack-oriented initiator behaviour of captive birds fighting against familiar opponents. Between familiar members the initiator would use different strategies according to the rank of the opponent relative to the initiator. Our results indicated that birds fighting unfamiliar opponents would adopt strategies similar to those used against higher ranks by captive silvereyes, supporting the prediction of the cost-benefit hypothesis in agonistic encounters.

Familiarity influences body darkening in territorial disputes between juvenile salmon

Escalated contests between animals are potentially costly because of increased energy expenditure and risk of predation or injury. Hence we would expect selection to favour any mechanism that avoids unnecessary prolonged fighting. One such means of avoiding escalated fights could be the use of information gained through individual recognition. Previous work has shown that a darkening of the body colour is closely associated with submission in contests between juvenile Atlantic salmon,Salmo salar , and it has been hypothesized that this may act as a visual signal to the opponent. We tested the hypothesis that body darkening is used to reduce the cost of contests between familiar fish such that losers darken more quickly when faced with familiar than unfamiliar opponents. In contests between unfamiliar fish, submissive darkening occurred after more escalated contests in which the loser incurred more aggression, whereas the opposite occurred when familiar fish were in conflict. In addition familiar fish either submitted quickly or engaged in protracted conflicts in which neither fish signalled submission, whereas in unfamiliar fish contests were of intermediate duration regardless of whether either fish darkened. We suggest that body darkening is used by familiar fish to signal submission to familiar dominants in order to avert a costly escalated fight, but familiarity can lead to escalation without submission if perceived competitive asymmetries are finely balanced.

Social inertia in white-throated sparrows results from recognition of opponents

Social inertia is a term for the stability of dominance relationships despite changes in the intrinsic dominating abilities of opponents. In a standard test for social inertia, low-ranking birds in an established hierarchy receive implants with testosterone (treated) and high-ranking birds receive empty implants (untreated). Social inertia occurs when the treated birds remain subordinate to untreated opponents in these groups, despite evidence that similarly treated birds dominate untreated strangers. In previous demonstrations of social inertia, however, treated and untreated birds were returned to their original aviaries and tested with familiar opponents, and thus the effects of familiarity with the location and those of familiarity with opponents were not separated. To address this issue, we investigated social inertia in 16 groups of white-throated sparrowsZonotrichia albicollis. When low-ranking treated birds were placed in new aviaries with familiar high-ranking, untreated opponents (treatment S, same opponents), dominance relationships showed social inertia. When such birds were placed in new aviaries with unfamiliar opponents (treatment N, new opponents), testosterone influenced dominance. When groups of high-ranking, untreated birds acquainted with each other were placed with unfamiliar treated opponents (treatment G, grouped dominants), ‘coat-tail’ effects (dominance by association with high-ranking individuals) sometimes outweighed the effects of testosterone. Social inertia in this species is thus a result of familiarity with opponents, rather than familiarity with locations of encounters. Measurements of aggressive tendencies confirmed a previous report that social inertia suppresses activation of aggression by testosterone. White-throated sparrows can thus recognize their opponents, and this ability affects the expression of both dominance and aggression.