Does serotonin influence aggression? comparing regional activity before and during social interaction

Serotonin is widely believed to exert inhibitory control over aggressive behavior and intent. In addition, a number of studies of fish, reptiles, and mammals, including the lizard Anolis carolinensis, have demonstrated that serotonergic activity is stimulated by aggressive social interaction in both dominant and subordinate males. As serotonergic activity does not appear to inhibit agonistic behavior during combative social interaction, we investigated the possibility that the negative correlation between serotonergic activity and aggression exists before aggressive behavior begins. To do this, putatively dominant and more aggressive males were determined by their speed overcoming stress (latency to feeding after capture) and their celerity to court females. Serotonergic activities before aggression are differentiated by social rank in a region-specific manner. Among aggressive males baseline serotonergic activity is lower in the septum, nucleus accumbens, striatum, medial amygdala, anterior hypothalamus, raphe, and locus ceruleus but not in the hippocampus, lateral amygdala, preoptic area, substantia nigra, or ventral tegmental area. However, in regions such as the nucleus accumbens, where low serotonergic activity may help promote aggression, agonistic behavior also stimulates the greatest rise in serotonergic activity among the most aggressive males, most likely as a result of the stress associated with social interaction.     

Interannual Variation in Nut Abundance Is Related to Agonistic Interactions of Foraging Female Japanese Macaques (Macaca fuscata)

The importance of dominance status to foraging and ultimately survival or reproductive success in wild primates is known; however, few studies have addressed these variables simultaneously. We investigated foraging and social behavior among 17 adult female Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan, from September to November in 2 consecutive years (2004 and 2005) to determine whether interannual variation in food availability was related to variation in agonistic interactions over food resources and the feeding behavior of individuals of different dominance rank. We compared energy obtained with daily energy requirements and also examined the effect of variation in feeding behavior on female survival and reproductive success. Fruiting conditions differed considerably between the 2 yr: of four nut-producing species, the nuts of only Torreya nucifera fruited in 2004, whereas all four species, particularly Fagus crenata, produced nuts in abundance in 2005. The abundance and average crown size of trees of Torreya nucifera were smaller than those of Fagus crenata, and there was a higher frequency of agonistic interactions during 2004, when dominant, but not subordinate, individuals were able to satisfy daily energy requirements from nut feeding alone through longer nut feeding bouts. In contrast, all macaques, regardless of their dominance rank, were able to satisfy their energy requirements by feeding on nuts in 2005. Subordinate macaques appeared to counter their disadvantage in 2004 by moving and searching for food more and maintaining larger interindividual distances. Several lower-ranking females died during the food-scarce season of 2004, and only one dominant female gave birth the following birth season. In contrast, none of the adult females died during the food-scarce season of 2005, and 12 females gave birth the following birth season. These findings suggest that an interaction between dominance rank and interannual variation in food availability are related to macaque behavior, survival, and reproduction.     

Social interaction over time, implications for stress responsiveness

Behavioral interaction during social situations is a continuumof action, response, and reaction. The temporal nature of socialinteraction creates a series of stressful situations, such asaggression, displacement from resources, and the variable psychologicalchallenge of adapting to dynamic social hierarchies. The ebband flow of neurochemical and endocrine secretions during socialstress provide a unique tool for understanding individualizedresponses to stress. Each social station is an adaptive responseto a stressful social condition, resulting in unique neuroendocrineand behavioral responses. By examining the temporal changesof limbic monoamines and plasma glucocorticoids, aspects ofmechanisms for adaptation emerge. The similarity of temporalpatterns induced by social stress among fish, reptiles and primatesare remarkable. Even different specific coping mechanisms pointout the similarity of vertebrate stress responses. The lizardAnolis carolinensis exhibits a unique sign stimulus generatedduring social stress by the sympathetic nervous system thatserves as a temporal landmark to distinguish neuroendocrinepatterns. During social interaction dominant males have a shorterlatency to eyespot darkening than opponents, inhibiting aggressivedisplay. Eyespot coloration can be delayed using a serotoninreuptake inhibitor, causing dominant social status in many animalsto be lost. Reversal of social status via serotonergic activationappears to mimic chronic serotonergic activity. The patternof eyespot darkening, faster in dominant males, is coincidentwith that for serotonergic activity. The fundamental temporalrelationship between dominant and subordinate limbic monoaminergicactivity over a continuous course of social interaction appearsto be a two-phase response, temporally specific to brain region,and always faster in dominant individuals.     

The Burden of Motherhood: The Effect of Reproductive Load on Female Lizard Locomotor,Foraging, and Social Behavior

The costs of reproduction, involving demands associated with both current and future reproductive efforts, may place a substantial burden on females. However, animals may minimize these costs by modifying their behavior across the reproductive cycle. We examined the effects of reproductive load on three types of behavior (locomotion, foraging, and social displays) in green anole lizards (Anolis carolinensis) by comparing egg, follicle, and oviduct mass and volume with field observational data. We found that female locomotor and social display behaviors decreased as reproductive load increased, suggesting behavioral modification in these traits, but we detected no relationship between foraging and reproductive load. We also examined these relationships across eight Anolis species using a phylogenetically informed analysis and found no associations between the evolution of reproductive load and any of the three behaviors. These results suggest that the evolution of increased reproductive load is not associated with the interspecific variation in behavior across the anoles and may result from varying life history traits or selective ecological pressures across species.     

Social dominance does not increase oxidative stress in a female dominance hierarchy of an African cichlid fish

In many group living animal species, individuals use aggression to gain and maintain social dominance to secure access to ecological resources and potential mates. While social dominance has many fitness benefits, there are also potential costs associated with frequent agonistic interactions and status display. One potential cost of social dominance is oxidative stress, the imbalance of reactive oxygen species and antioxidant capacity. In the cichlid species Astatotilapia burtoni, dominant males are aggressive, hold a breeding territory, and have an activated reproductive system resulting in larger gonads. Subordinate males are submissive, school with females, and are nonreproductive. Females are submissive under natural conditions, but in a female-only group, a dominance hierarchy will form with dominant females taking on male-typical behaviours including aggression, territory defence, and increased androgen levels. However, in contrast to males, social dominance is not linked to increased activation of the reproductive system in females, allowing us to test whether social dominance alone exposes individuals to increased oxidative stress. We compared dominant and subordinate females in female-only groups in five markers of oxidative stress. Dominant females did not have higher levels of oxidative damage compared to same-sex subordinates. This result contrasted to the trend in males in which dominant males had higher oxidative damage than their subordinate counterparts. Our findings suggest that the oxidative cost of social dominance is limited and support the notion that previously reported associations between high rank and increased oxidative stress is most likely driven by increased investment in reproduction.     

The role of the basal hypothalamus in the regulation of reproductive behavior in the lizard, Anolis carolinensis: lesion studies

Bilateral radiofrequency lesions in the anterior and posterior basal hypothalamus decreased courtship and agonistic behaviors in both intact, sexually active, and castrated, androgen treated male Anolis carolinensis. Intact males receiving lesions in the anterior basal hypothalamus had atrophied testes, aspermia, and decreased epithelial cell height of the renal sex segment. Lesions of the posterior basal hypothalamus had no effect on testicular activity or the development of accessory organs. All animals demonstrating behavioral changes had lesion destruction in the ventromedial nucleus and the accompanying periventricular system. It is concluded that the basal hypothalamus in male A. carolinensis is involved both in the regulation of reproductive behavior and pituitary function.     

Social context influences aggressive and courtship behavior in a cichlid fish

Social interactions require knowledge of the environment and status of others, which can be acquired indirectly by observing the behavior of others. When being observed, animals can also alter their signals based on who is watching. Here we observed how male cichlid fish (Astatotilapia burtoni) behave when being watched in two different contexts. In the first, we show that aggressive and courtship behaviors displayed by subordinate males depends critically on whether dominant males can see them, and in the second, we manipulated who was watching aggressive interactions and showed that dominant males will change their behavior depending on audience composition. In both cases, when a more dominant individual is out of view and the audience consists of more subordinate individuals, those males signal key social information to females by displaying courtship and dominant behaviors. In contrast, when a dominant male is present, males cease both aggression and courtship. These data suggest that males are keenly aware of their social environment and modulate their aggressive and courtship behaviors strategically for reproductive and social advantage.     

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.     

The Haremic Mating System and Mate Choice in the Wide-Eyed Flounder, Bothus podas

The social structure and reproductive behaviour of the wide-eyed flounder, Bothus podas, was studied in the coastal waters around the Azorean Islands. Both sexes are territorial throughout the year. Adult males defend large territories, which include several smaller female territories. Intraspecific agonistic behaviour was frequent and differed between sexes: males were more aggressive towards other males, while females were only aggressive towards each other and juveniles. During the reproductive season and only at dawn, territorial males court and mate successively with females in their territories, and females seem to show mating fidelity to their dominant male. Such territoriality and mating patterns indicate a haremic social system in the wide-eyed flounder. In order to identify potential factors influencing female mate choice acting on this haremic system, we examined male mating success and some of its potential correlates. We found no evidence for female preference for any of the males' physical or territory characteristics. However, courtship effort was strongly correlated with the total number of attempted and successful spawnings, indicating that females seem to mate preferentially with males that court them more vigorously. Thus, our data suggest that courtship plays an important role in determining male mating success in the wide-eyed flounder and, that it may possibly serve as an honest indicator of male `quality' for female choice.     

Mating behaviors,courtship rank and mating success of male feral cat (Felis catus)

The mating behavior of the male feral cat (Felis catus) living on a small island was investigated. The cats in the study area (6.0 ha) formed the “feeding groups” at the garbage sites (Yamane et al. 1994; Izawa et al. 1982). We examined the factors influencing fighting ability, rank during courtship, and mating success of the male cat. Males with heavier body weight mostly won over lighter males in the agonistic encounters during the estrous season. Heavier males occupied the more advantageous positions to copulate with the estrous females and had higher mating success. These results suggest that body weight was one of the important factors affecting the courtship rank and the mating success of the male cat. When males visited and courted the females of feeding groups other than their own, they were sometimes defeated by the lighter males in that particular group, which lowered their courtship rank and success in copulations. These results indicate that the location of the courting male (inside or outside of its own group) and the kind of females they courted (member of the same group or not) were also important factors.     

Environmental Effects on Agonistic Interactions between Males of the Cockroach Nauphoeta cinerea

The effects of different environments on the agonistic behavior of males of the cockroach, Nauphoeta cinerea were investigated. We compared the social interactions between pairs of males that had been reared during the period of sexual maturation, when social behavior develops, under one of four environmental treatments: (1) control (28°C with ad libitum food and water) (2) heat stress (35°C, ad libitum food and water) (3) water deprivation (28°C), or (4) food and water deprivation (28°C). Different environments affected the structure of the interactions between males and the behavior of both dominant and subordinate individuals. The mean number of agonistic acts per minute was similar for all treatment groups except the water-deprived group, which was significantly lower. Water-deprived, food- and water-deprived, and heat-stress rearing conditions reduced the stability of agonistic interactions relative to the control group. When reared under stressful conditions, dominant-scored males decreased the number of aggressive acts and increased the number of submissive acts, and subordinate-scored males decreased the number of submissive acts and increased the number of aggressive acts. Thus, stressful environmental conditions can disrupt agonistic interactions and cause both dominant and subordinate male N. cinerea to adopt different behavioral strategies during male-male competition.     

Behavioral correlates to gonadal state in the lizard, Anolis carolinensis

Female Anolis carolinensis of unknown reproductive condition were introduced into cages containing a sexually active male and the resulting sexual behavior was noted. Female sexual receptivity was found to be correlated with the stages of follicular maturation. These results suggest that sexual receptivity in female A. carolinensis is restricted to a time immediately preceding the ovulation of each follicle and is dependent upon hormonal conditions normally arising during follicular development. Evidence is offered to suggest that during the breeding season, female sexual receptivity is rhythmical and contingent upon the cyclic ovarian changes peculiar to lizards of this genus.     

Parallel changes in agonistic and non-agonistic behaviors during dominance hierarchy formation in crayfish

Agonistic and non-agonistic behaviors were studied before, during, and after the formation of social status in crayfish. Differences in the expression of a non-agonistic behavior by dominant and subordinate crayfish developed in parallel with the differences in agonistic behaviors that indicate the animals' social status. An increase in burrowing behavior marked the ascendancy of the dominant animal, while an immediate suppression of burrowing paralleled the inhibition of aggressive behavior in the new subordinate. The strikingly similar changes in both agonistic and non-agonistic behaviors following the decision on status suggest related underlying neural mechanisms.     

Male Reproductive Success in a Social Group of Urban Feral Cats (Felis catus L.)

Dominance rank, morphological characteristics and reproductive success of adult males were measured in a multi‐male multi‐female group of urban feral cats (Felis catus L.). Paternity of nine litters (34 kittens) of the domestic cat from six females was determined through microsatellites analyses at nine loci. The percentage of multiple paternities in this social group was as high as 78%. A positive correlation was found between male size/body weight and dominance. The males who sired the highest number of kittens were the dominant ones. Additionally, dominant males were more likely to be infected by the feline immunodeficiency virus, a virus transmitted by bites through aggressive interactions. Thus this study demonstrates that rank and body weight were both important in predicting the annual reproductive success. However, it shows that the reproductive benefit associated to rank may be balanced by cost due to at‐risk aggressive behaviour of dominant males.     

Acoustic signaling in fish

The paper lists basic data on the role of sounds in fish behavior. The involvement of acoustic signaling in the control of reproductive, territorial, agonistic, aggressive, social, and feeding behavior in fish that differ in the systematics and mode of life is considered. Species and population specifics and individual sound variation in fish, diurnal and seasonal cyclicity of sound activity, and behavior that accompany acoustic signaling and the effects upon it of different environmental factors are considered. Evidence on the formation of acoustic signaling in ontogenesis of fish is provided; the range of sound signaling and correspondence between sound spectra and auditory sensitivity are discussed. Possible applied aspects of results of study of fish bioacoustics are analyzed.     

The physiology of rainbow trout in social hierarchies: two ways of looking at the same data

Salmonids form dominance hierarchies in environments, where space or food are limiting. Our first objective was to investigate the physiology of individual rainbow trout in 4-fish hierarchies. Our second was to compare conclusions drawn from grouping physiological data on the basis of social rank with those based on relating individual physiology to individual aggressive behavior. To create a social hierarchy, groups of 4 juvenile trout were fed (1 % ration) using a darkened feeding container, twice daily (morning and evening). Each morning feeding was videotaped to record aggressive behavior, thereby facilitating the assignment of a social status rank to each fish. On days 5 and 10–11, physiological parameters were measured in fish fasted for 24 h. Social hierarchies formed in all tested groups. One fish would become dominant, whereas the three subordinate individuals would each assume a stable social rank. When classified according to this social rank, the three subordinate individuals all displayed similar physiology, different from the physiology of the dominant fish. The latter included higher ammonia excretion rate, greater protein utilization in aerobic metabolism, greater feeding, higher specific growth rate, greater increase in condition factor, and lower routine oxygen consumption rate. However, when individual aggression was taken into account, a continuous gradient was observed between aggression and physiology for most parameters, regardless of social status. These relationships could be improved by normalizing the aggression score to the overall level of aggression in each hierarchy. We argue that individual behavior should be considered instead of just social rank when studying the physiology of trout in social hierarchies.     

Low-ranking individuals present high and unstable fecal cortisol levels in provisioned free-ranging adult male rhesus macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) during the birth season in a mountain area of northern China

Social hierarchy commonly exists in animal societies, affecting both the endocrine functioning and the behavior of animals. In nonhuman primates, the relationship between social rank and cortisol levels varies across species and even within species. Here, we assessed the relationships between social rank and fecal cortisol levels in adult male Taihangshan macaques (rhesus macaques, Macaca mulatta tcheliensis) from the provisioned, free-ranging Wulongkou-2 (WLK-2) group inhabiting Wulongkou Scenic Area, Jiyuan, China. From March to May 2014, we recorded 195 agonistic behaviors and collected 54 fresh fecal samples from eight adult male Taihangshan macaques. Males were assigned a social rank according to an agonistic behavior matrix, and enzyme-linked immunosorbent assay was then used to measure the cortisol concentration in the fecal samples. We found that social rank among the eight male Taihangshan macaques in WLK-2 group followed a strict linear hierarchy, and that fecal cortisol levels were significantly higher and more variable in low-ranking males than in more dominant individuals. Age was not significantly associated with social rank or fecal cortisol levels. Our results suggest that social rank and maintenance of the social hierarchy within the WLK-2 group is a chronic stressor, with low-ranking males maintaining heightened stress levels and enlarged reactive scope relative to dominant males. This provides new support for the theory that social environment can influence endocrine functioning.     

Visible sympathetic activity as a social signal in Anolis carolinensis: changes in aggression and plasma catecholamines

Darkening of postorbital skin in Anolis carolinensis occurs during stressful situations and is stimulated by sympathetic activation of beta(2)-adrenergic receptors via adrenal catecholamines. This eyespot forms more rapidly in dominant males during social interaction. Eyespot darkening (green to black) appears to function as a social signal communicating sympathetic activation and limiting aggressive interaction. To assess the value of the eyespot as a social signal, males were painted postorbitally with green, black, or red paint. Each male was exposed to a mirror following acclimation to the cage. The total number of aggressive displays toward the mirror image was greatest when eyespots were masked by green paint. In contrast, black or red artificial eyespots, regardless of size, inhibited biting behavior toward the mirror image. The most aggressive males, those who saw a reflected opponent with no eyespot (hidden with green paint), had significantly higher levels of all plasma catecholamines. These results suggest that A. carolinensis use information from the eyespot to assess their opponent's readiness to fight and thereby determine whether to be aggressive. Darkened eyespots are capable of inhibiting aggression, whereas aggressive displays from an opponent in the mirror without darkened eyespots do not. Darkened eyespots reflect rapid changes in plasma NE, DA, and Epi that may signal dominant social status.     

Dynamics and mechanics of social rank reversal

Stable social relationships are rearranged over time as resources such as favored territorial positions change. We test the hypotheses that social rank relationships are relatively stable, and although social signals influence aggression and rank, they are not as important as memory of an opponent. In addition, we hypothesize that eyespots, aggression and corticosterone influence serotonin and N-methyl-D-aspartate (NMDA) systems in limbic structures involved in learning and memory. In stable adult dominant-subordinate relationships in the lizard Anolis carolinensis, social rank can be reversed by pharmacological elevation of limbic serotonergic activity. Any pair of specific experiences: behaving aggressively, viewing aggression or perceiving sign stimuli indicative of dominant rank also elevate serotonergic activity. Differences in the extent of serotonergic activation may be a discriminating and consolidating factor in attaining superior rank. For instance, socially aggressive encounters lead to increases in plasma corticosterone that stimulate both serotonergic activity and expression of the NMDA receptor subunit 2B (NR_2B) within the CA₃ region of the lizard hippocampus. Integration of these systems will regulate opponent recognition and memory, motivation to attack or retreat, and behavioral and physiological reactions to stressful social interactions. Contextually appropriate social responses provide a modifiable basis for coping with the flexibility of social relationships.     

Temporal Pattern of Agonistic Interaction in Two Gerbil Species (Rhombomys opimus and Gerbillus perpallidus) Differing in Resistance to Social Pressure

This study compares temporal patterns of intraspecific agonistic interactions in two gerbil species in order to indicate interspecific differences in levels of social resistance. Both cross-sex and same-sex pairs of great gerbils (Rhombomys opimus Licht., 1823), and only same-sex male pairs of pallid gerbils (Gerbillus perpallidus Setzer 1958) were observed during staged encounters on a neutral arena. Analysis of three latency measures—latency to first agonistic interaction; latency to overt aggression (attack and/or ‘arrested’ fight); and latency to establishment of a stable winner-loser asymmetry among opponents—revealed both similarities and differences among the species. Latencies to first agonistic interaction were similar (did not differ significantly) among species and sexes. However, great gerbil males showed significantly more long latencies to establishment of a stable asymmetry among opponents, than great gerbil females or pallid gerbil males. So, the periods of symmetrical struggle in agonistic conflict last longer in great gerbil males, than in great gerbil females or pallid gerbil males. These differences in temporal pattern of agonistic interaction may reflect sex and species differences in resistance to social stress.