Repeated exposure to social stress alters the development of agonistic behavior in male golden hamsters

In male golden hamsters, exposure to social stress during puberty alters aggressive behavior. Interestingly, agonistic behavior undergoes two major transitions during puberty: a decline in attack frequency and a shift from play fighting to adult-like aggression. Based on previous observations, we developed an approach for characterizing offensive responses as play fighting or adult-like. The present studies had two aims. First, we validated our approach by looking at the development of attack types during puberty. Second, we looked at the effects of repeated social stress on the development of agonistic behavior by repeatedly exposing individuals to aggressive adults during puberty. In the first phase of the study, our results point to three different developmental periods. Initially, animals engage in agonistic behavior though attacks targeted at the face and cheeks. This period lasts from Postnatal Day 20 (P-20) to P-40 (early puberty). This phase corresponding to play fighting is followed by a transitional period characterized by attacks focused on the flanks (from P-40 to P-50, mid-puberty). Afterward, animals perform adult-like aggression characterized by attacks focused on the belly and rear. Our data also show that repeated exposure to aggressive adults has two separate effects on the development of agonistic behavior. Repeated social stress accelerated the onset of adult-like agonistic responses. Furthermore, attack frequency, while decreasing during puberty, remained at a higher level in early adulthood in stressed animals. These results show that repeated exposure to social stress during puberty alters the development of agonistic behavior both qualitatively and quantitatively.     

Agonistic behavior in naïve juvenile lobsters depleted of serotonin by 5,7-dihydroxytryptamine

We have been exploring the role of serotonin in fighting behavior in lobsters using a specific model of agonistic behavior, the establishment of hierarchical relationships between pairs of socially naive juvenile lobsters. We selected this model because the behavior is easily evoked, readily quantifiable, and the effects of experience are eleminated by using socially naive animals. In these studies we injected a specific neurotoxin, 5,7-dihydroxytryptamine, into juvenile lobsters over a 4-week period and then measured the effects on fighting behavior. This treatment reduces the levels of serotonin in the nervous system and immunocytochemical studies show a dramatic reduction in neuropil staining for the amine. Control animals received vehicle injection alone. All injected animals were paired against larger or smaller non-injected opponents, and three successive 30-min fights were carried out and statistically analyzed. The results were surprising: As with elevations of serotonin, reduced levels of serotonin increased the amount of time animals engaged in fighting behavior. No significant effects were seen on who initiated encounters, who retreated first, or who the eventual winner would be. Thus, in this model, elevation or reduction of serotonergic function increases the tendency of animals to engage in agonistic encounters.     

The Effects of Arginine Vasotocin on the Calling Behavior of Male Cricket Frogs in Changing Social Contexts

We investigated the effects of the neurohypophysial peptide, arginine vasotocin (AVT), on the calling behavior of maleAcris crepitansduring and immediately following a simulated acoustic agonistic encounter. AVT did not block the aggressive response to agonistic calls, as the changes in temporal call characteristics in response to the encounter were similar to those of saline-treated males. However, AVT caused males to begin calling sooner during the agonistic encounter and to call significantly more than saline males during and after the agonistic encounter. In addition, AVT-treated males maintained a higher dominant frequency compared to saline animals during and following the agonistic encounter. Changes in temporal characteristics in the period following the agonistic encounter indicated that control males were more likely to exhibit a rebound effect which resulted in larger changes in calling parameters compared to AVT-treated animals. The results indicate that AVT causes changes in calling behavior in maleA. crepitansduring and following an agonistic encounter that are consistent with animals highly motivated to maintain vigorous active calling throughout changing social conditions.     

Sickness and Aggressive Behavior in Dominant and Subordinate Mice*

Sick animals show a set of organized behavioral changes (sickness behavior), which is the result of a motivational re‐organization of the behavior as a whole. Sickness behavior display can be influenced by the social context. In this work, we sought to investigate the regulation of sickness behavior within a pair of mice in the presence of an intruder mouse. Dominant and subordinate mice were treated with the bacterial endotoxin lipopolysaccharide (LPS) and were challenged with the presence of an intruder mouse. LPS effects depended on ranking and social context. Even though dominant mice displayed more agonistic interaction towards the intruder, subordinate mice displayed agonistic behavior towards the intruder when their dominant companion was treated with LPS. The results show that, not only sickness behavior is differentially expressed among different social ranks, but also that sickness behavior is related to different reactions among surrounding animals. These data are relevant for a biological approach to the relation between sickness behavior and social behavior.     

Postweaning environmental and social factors influencing the onset and expression of agonistic behavior in Norway rats

Two studies were conducted to determine the importance of the postweaning environment and social milieu in regulating the expression of intraspecific aggression in Norway rats. In Experiment 1, male rats were housed either individually or in pairs at 21 days of age. In addition, one-half of the singly housed and paired animals were given experiences with intruders during maturation. At 85 days of age, all animals were given a brief intruder test and then removed from their postweaning environment and provided individually with homecages for a two week period until tested for aggression toward intruders. Results of intruder tests given during maturation indicated agonistic exchanges appeared earlier and more frequently in cages housing a single resident than cages with cohabiting males. However, agonistic exchanges between singly reared residents and intruders had detrimental consequences in adulthood especially under long-term combat situations. That is, although individually reared animals, with early fighting experiences, were capable of initiating intraspecific aggression, such individuals were unable to defend their homecage over a long period of time as evidenced by the high number of wounds and tendency to lose body weight during adult fighting.In Experiment 2, male Norway rats were reared in pairs from 21 days of age and identified as dominant or subordinate on the basis of intracolony social interactions shown during maturation. At 80 days of age, animals were paired with individually reared males in an unfamiliar cage for a 20 day period and examined for agonistic behavior toward intruders at 100 days of age. Group-reared subordinate males exhibited defensive behavior during confrontations with individually reared animals and incurred more wounds and lost more body weight than their cohabiting partner. In addition, subordinate males showed significantly fewer offensive postures toward intruders than individually reared cohabitants. In contrast, group-reared dominant animals did not differ from individually reared males in display of agonistic patterns, in number of wounds, and body weight changes during the period of cohabitation. These findings demonstrate that early rearing factors have pronounced effects on agonistic behavior. Animals experiencing defeat during development are more likely to lose agonistic confrontations in unfamiliar territory than either animals dominant in their early social interactions or animals without the experience of winning or losing agonistic encounters. These results have implications for the understanding of agonistic behavior and predicting outcomes of animal contests, and reveal important differences in agonistic experiences among animals reared in groups.     

Klassische Konditionierung agonistischen Verhaltens beim Syrischen Goldhamster (Mesocricetus auratus Waterhouse)

Nine different reactions of unconditioned agonistic behavior of golden hamsters (Mesocricetus auratus Waterhouse) which could be elicited by an air blow (UCS) were classically conditioned at a sound of a xylophone (tone g), a previously neutral stimulus. Tone g (CS) was paired with UCS for a different number of trials/day. In all animals exposed to over 20 pairings/day components of the agonistic behavior were brought under the control of Cs, but it was not possible to predict which one of the agonistic reactions would appear. Most of the animals generalized and also showed conditioned reactions (CR) when presenting tone c' instead of tone g. When utilizing a differential conditioning procedure the animals learned to discriminate between the different tones. Extinction of CR at tone g was reached after an individually different number of trials.     

Field observations of intraspecific agonistic behavior of two crayfish species,Orconectes rusticus and Orconectes virilis,in different habitats

Agonistic behavior is a fundamental aspect of ecological theories on resource acquisition and sexual selection. Crustaceans are exemplary models for agonistic behavior within the laboratory, but agonistic behavior in natural habitats is often neglected. Laboratory studies do not achieve the same ecological realism as field studies. In an attempt to connect laboratory results to field data and investigate how habitat structure affects agonistic interactions, the nocturnal behavior of two crayfish species was observed by scuba diving and snorkeling in two northern Michigan lakes. Intraspecific agonistic interactions were analyzed in three habitats: two food resources-macrophytes and detritus-and one sheltered habitat. The overall observations reinforce the concept that resources influence agonistic bouts. Fights in the presence of shelters were longer and more intense, suggesting that shelters have a higher perceived value than food resources. Fights in the presence of detritus patches had higher average intensities and ended with more tailflips away from an opponent, suggesting that detritus was a more valuable food resource than macrophytes. In addition, observations of aggressive behavior within a natural setting can add validity to laboratory studies. When fights in nature are compared with laboratory fights, those in nature are shorter, less intense, and less likely to end with a tailflip, but do show the fundamental fight dynamics associated with laboratory studies. Extrinsic and intrinsic factors affect intraspecific aggression in many ways, and both should always be recognized as having the potential to alter agonistic behavior.     

Serotonin and octopamine elicit stereotypical agonistic behaviors in the squat lobster Munida quadrispina (Anomura, Galatheidae)

Serotonin and octopamine have been implicated as modulators of posture and behavior in several crustaceans. Here we characterize the agonistic behaviors of normally interacting squat lobsters Munida quadrispina (Anomura, Galatheidae) and their responses to serotonin and octopamine injected into the ventral hemolymph sinus, in order to evaluate the potential roles of these amines in modulating agonistic behaviors. Normally interacting M. quadrispina do not develop lasting dominance hierarchies, although transient aggressive and submissive displays do occur. Injected serotonin elicits postures and behaviors in isolated individuals similar to those typical of aggressive, normally interacting animals. Injected octopamine can produce postures and behaviors typical of submissive animals, and elicits behaviors which imply a modulatory role for octopamine in tailflipping. The effects of both amines are reversible and dose dependent, and the dose-response curves parallel the normal progression of agonistic interactions. The social behaviors and reactions to injected serotonin and octopamine of M. quadrispina differ from those of lobsters and crayfish, indicating that interspecific differences in neuromodulation of behavior and motor output exist. Such differences have implications for the understanding of aminergic modulation of aggression and the evolution of aminergic modulation in crustaceans. Accepted: 22 June 1997     

The escape reactions in cats during electrical stimulation of the hypothalamus leading to the occurrence of aggressive behavior]

The influence of brain electrical stimulation, which induced some elements of agonistic behavior, on the preference of an animal of one of two compartments of the experimental chamber was studied in 7 male cats with implanted hypothalamic electrodes. The animals avoided the compartment in which they were stimulated. Self-stimulation reaction could not be formed on the basis of the electrical brain stimulation inducing certain elements of agonistic behavior. Passage latencies were shorter when an animal left the less preferential compartment that in the case when in started from the more preferential one. The obtained evidence suggests that hypothalamic stimulation producing certain elements of agonistic behavior evokes in an animal a negative internal state.     

Serotonin, social status and aggression

Serotonin, social status and aggression appear to be linked in many animal species, including humans. The linkages are complex,and, for the most part, details relating the amine to the behavior remain obscure. During the past year, important advances have been made in a crustacean model system relating serotonin and aggression. The findings include the demonstration that serotonin injections will cause transient reversals in the unwillingness of subordinate animals to engage in agonistic encounters, and that at specific synaptic sites involved in activation of escape behavior, the direction of the modulation by serotonin depends on the social status of the animal.     

Threat calls in alliance formation by members of a captive group of Japanese monkeys

The vocal behavior of threat calls was investigated in a captive group of Japanese monkeys (Macaca fuscata fuscata). The vocalizations were heard most often when they undertook winner-support during triadic agonistic interactions. The likelihood of call emission in support of the winner was affected by the attributes of the participants, and not by the types of agonistic behavior. The calls were emitted by intermediate ranking animals frequently in support of high ranking animals and in support of females. The calling behavior of winner-supporters appears to advertise the partner and distant group members of their support for reciprocation in the near future.     

Cortisol controls the pubertal development of agonistic behavior in male golden hamsters via type II corticosteroid receptors

In male golden hamsters, agonistic behavior undergoes a pubertal transition from play fighting to adult aggression. Previous studies have shown that this aspect of behavioral development is associated with pubertal increases in glucocorticoids and that daily social stress or injections of a synthetic glucocorticoid accelerate the transition. The goals of this study were to confirm the effects of cortisol on the development of agonistic behavior and to investigate the role of type II corticosteroid receptors in this process. First, animals treated with cortisol during early puberty [from postnatal days 31 (P-31) to P-36] showed an accelerated transition from play fighting to adult aggression. In a second experiment, the behavioral effects of cortisol were blocked by a co-treatment with a type II corticosteroid receptor antagonist. These findings are the first to show a facilitating role for type II corticosteroid receptors in the pubertal development of a social behavior. As such, these findings provide new insights into the neuroendocrine mechanisms controlling behavioral development during puberty.     

Reciprocation and interchange of grooming,agonistic support,feeding tolerance,and aggression in semi‐free‐ranging Barbary macaques

Evidence from a range of primate species indicates that grooming can be exchanged either for itself or for other rank‐related “commodities,” such as agonistic support, feeding tolerance, or reduced aggression. Patterns of exchange behavior have been found to vary considerably between species, and understanding the causes of this variation is central to the study of the evolution of primate social systems. It is, therefore, essential that exchange behavior is examined in a wide range of species and settings. This article is the first to explore the reciprocation and interchange of grooming in the Barbary macaque (Macaca sylvanus). We collected focal data on semi‐free‐ranging adult female Barbary macaques at Trentham Monkey Forest, England, and analyzed dyadic data using Generalized Linear Mixed Models. We found evidence for the reciprocal exchange of grooming and for the interchange of grooming for agonistic support and tolerance while feeding. There was no evidence that grooming was traded for a reduction in aggression; indeed, we found a positive relationship between aggression given and grooming received. This may reflect the “extortion” of grooming from subordinates by dominant animals. These results will facilitate comparative analyses of exchange behavior by adding to the current database a new species, characterized by a different social style from those macaque species previously investigated. Am. J. Primatol. 73:1127–1133, 2011. © 2011 Wiley Periodicals, Inc.     

Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra

Patterns of agonistic and nonagonistic behaviors were studied in a troop of wild pig-tailed macaques in West Sumatra, Indonesia. The animals were provisioned and the identities of all adult and adolescent individuals were known. The females could be divided into high-, mid-, and low-ranking subsets of individuals. Most grooming occurred within, instead of between members of these subsets. The members of each subset also tended to feed together at the baiting sites, and they probably represented groups of close kin. Among females, grooming appeared to be a conciliatory behavior and was generally performed by the subordinate partner, while mounting was performed by the dominant partner and appeared to be a reassertion of dominance. High-ranking males tended to form agonistic alliances with females and to exchange grooming with estrous females. Low-ranking males did not have such associations with females and were frequently the targets of agonistic alliances of females and juveniles. Mounting between males appeared to be a conciliatory behavior. It seemed effective since severe aggression between males was not observed. The subordinate partner mounted more frequently than the dominant one, but the direction of mounting was apparently controlled by the latter. This suggests that, among pig-tailed macaques, the dominant male plays an important role in the coexistence of males in the troop.     

Behavioral characteristics of freemartins administered estradiol, estrone, testosterone, and dihydrotestosterone

Eighteen genetic females born co-twin with males and diagnosed as being sterile intersexes (freemartins) were studied from birth to 79 weeks of age. Testosterone (T) and estrone (EI) were administered in Silastic capsules of two groups from birth to 50 weeks of age and other animals were left untreated. At 50 weeks the two treated groups had larger implants installed and the untreated animals were assigned to a new estrone (EII) and estradiol (E2) treatment. Later a dihydrotestosterone (DHT) group was formed in comparison with new E2 and testosterone propionate-enanthate (TP-TE) groups, plus untreated controls. Vulvar interest, Flehmen lip curl, mounting, and agonistic behavior were recorded daily for 30 min while animals were allowed social interaction. Agonistic behavior, interest in the genital area, and mounting were induced or stimulated by T, TP-TE, and E2, but not by DHT or estrone (EI or EII). Also, only animals in the T, TP-TE, and E2 groups induced to mount displayed the standing type of behavioral estrus. Flehmen lip curl was stimulated only by T or TP-TE. The evidence is interpreted to indicate that T, per se, evokes the lip curl, but it probably stimulates other responses at the neural level by conversion to E2. Also, the freemartin response, the response of castrates to steroid hormones, and current knowledge of circulating steroid hormones in male and female cattle could be interpreted to indicate that the neural tissue responsible for sexual behavior in both sexes of this species may respond similarly in several respects.     

Exposure to the steroid hormone 20-hydroxyecdysone modulates agonistic interactions in male Homarus americanus

In this study we present evidence that 20-hydroxyecdysone (20E) affects agonistic behavior in male American lobsters and that male and female animals differ in their response to the hormone. Thirty-minute staged fights were conducted between large males exposed either to artificial seawater (ASW) or 20E and small, anosmic opponents. The nephropores of both combatants were blocked. Fights were videotaped and quantitatively analyzed for aggressive, defensive and avoidance behaviors using an ethogram in which behaviors are ranked according to aggressiveness. Unlike female lobsters, exposing male lobsters to 20E did not increase their aggressive behavior; however, there was a marginally significant trend toward an increase in defensive behaviors with a lower aggressive content than in their ASW-exposed counterparts. The opponents of 20E-exposed animals performed significantly more aggressive behaviors than their counterparts. In fights with 20E-exposed animals, the overall aggressive intensity of the fight was increased and the animals performed a greater number of avoidance behaviors. Unlike the effects of 20E on females, where exposure to 20E caused an increase in overall agonistic arousal, males only exhibited a change in frequency of their behaviors. These findings suggest that while 20E affects both males and females in agonistic encounters, the nature of the effect is different for the two sexes.     

The smell of success and failure: the role of intrinsic and extrinsic chemical signals on the social behavior of crayfish

Animals commonly modify their behavior in the presence of aconspecific or in response to signals. This is particularlytrue in the context of aggressive exchanges, which animals useto form networks of social relationships and to communicatesocial status associated with those relationships. Althoughhierarchical structures are a widespread phenomenon that hasbeen studied extensively, the dynamic communication processes,specifically chemical communication in this review, is relativelyoverlooked. In particular, it is the exchange of informationduring agonistic interactions that mediates hierarchies and/oralters the outcomes of agonistic interactions. Given the theoreticalappeal of these interactions, and the evolutionary importanceand taxonomic diversity associated with social hierarchies,it is not surprising that the sensory mechanisms involved inthe formation and maintenance of hierarchical structures havereceived recent attention. In crayfish, dominance is thoughtto be largely determined by physical superiority, where encountersare largely dyadic and fighting behavior is highly stereotyped.However, recent evidence has shown that the outcome of dyadicencounters are dependent upon a number of factors other thanphysical size, that include the exchange of chemical informationduring encounters, previous social history, and the intrinsicneurochemical state of opponents. We have attempted to providea comprehensive analysis of the extrinsic chemical processes(previous history, sensory communication, etc.) and intrinsicchemical processes (neurochemical state) that produce and maintaindominance relations and social hierarchies in crayfish. We hopethat this review will bring together a global picture of theprocesses that determine a crayfish's social standing and howintrinsic and extrinsic chemicals have substantial effects onaggressive states and agonistic bouts.     

Visual Sensation of an Ethological Stimulus, the Agonistic Display of Betta splendens, Revealed using Multi-Unit Recordings from Optic Tectum

We made multi-unit recordings from the optic tectum of Betta splendens while they viewed the agonistic display of conspecifics. Movement of displaying animals evoked brisk, arrhythmic bursting in tectal units. Particularly high frequency spike bursts coincided with the onset of full display, a behavioral element known to be of ethological significance. These results show that it is possible to obtain informative electrophysiological recordings from optic tectum using behaving conspecifics as stimuli. More frequent use of natural stimuli can be expected to contribute to a greater understanding of the link between the neural substrates of vision and visually guided behavior.     

Population size,social behaviour,and dispersal in house mice: A quantitative investigation

An experimental study was conduced to examine some relationships between population size, social behaviour, and dispersal utilizing wild genotype Mus musculus in seminatural enclosures. Groups of male and female mice were used to simulate natural populations. The results indicate that male territoriality occurred significantly more often in populations of greater size but equal density, and these groups demonstrated a significantly greater rate of agonistic interactions per animal when compared to smaller populations. No significant differences were observed for other categories of social interaction. The percentage of animals emigrating and the population density following emigration were the same in small and large groups.     

Agonistic aiding: Kinship,rank, age,and sex influences

An analysis of 3,774 episodes of agonistic aiding collected during a two-year study of a rhesus monkey group (Macaca, mulatta) indicated the differential influence of kinship and rank relationships on the participation of different age-sex classes in both aid to victims and aid to aggressors. Most aiding favored victims rather than aggressors and was much more likely to occur when matrilineal kin were involved. Females were more likely to aid than were males, and the frequency of their participation increased with age. Females were much more influenced by kinship than were males and defended or aggressively supported kin against any third party regardless of dominance relationships. Adult males seldom aided against animals that were dominant to themselves; the rare exceptions occurred when adult males defended kin. Aiding was far more likely to occur if the victim was squealing, and noisy agonistic episodes often involved multiple aiders on both sides. Aiding patterns had some potential to insure dominance rank inheritance within families, in accordance with the Kawamura hypothesis. In aiding animals outside of their own matrilines, however, group members aided randomly with respect to this model. There was little evidence that aiding functioned to support individuals when they targeted animals to which they should be dominant as adults based on matrilineal dominance relationships. Most defensive aiding seemed to function primarily to defend victims (primarily kin) of aggression. Aggressive support of the attacker, on the other hand, seemed to function primarily to reinforce coalitions with the attacker. The identity of the victim was unimportant as long as it was neither kin to nor dominant to the aider. Aggressive support of attackers did not overturn existing dominance relationships.