Hormonal Correlates of Dominance and Starvation-induced Aggression in Chicks of the Blue-footed Booby

In the blue-footed booby (Sula nebouxii), the first-hatched chick aggressively dominates its sibling and sometimes kills it when food is in short supply. To investigate the endocrine correlates of dominance-subordinance and hunger-induced agonism, we deprived 15–20-d-old single-chick and two-chick broods of food during 48 h by taping chicks' necks to prevent ingestion of parentally provided food (a protocol used previously and known to elicit escalated sibling fighting). We monitored weight and levels of circulating testosterone, oestradiol and corticosterone in deprived and normally fed broods comprising singletons, seniors (= dominants) and juniors (= subordinates), and observed behaviour to verify that aggression increased in deprived two-chick broods. During the 2 d of fasting, experimental chicks lost on average 6% of their baseline weight. After normal feeding was reinstated, seniors and singletons recovered normal (control) weight, but juniors remained significantly lighter than controls. No testosterone was detected in any nestling, but baseline corticosterone level was 109% higher in juniors than in seniors or singletons, implying that elevated corticosterone in juniors is a consequence of social subordination and may facilitate submissive behaviour. Although there was evidence that aggression of seniors increased under food deprivation, the increase was not accompanied by the rise in levels of testosterone expected under the ‘Challenge hypothesis’ (Wingfield et al. 1990). This result implies that this hypothesis probably does not apply to booby nestlings in the context of starvation-induced aggression. During the 2 d deprivation period, corticosterone levels of experimental chicks increased significantly, then declined to baseline levels a day after tapes were removed. The increase was probably due to the combined effects of starvation and frustration. We suggest that corticosterone could alter responsiveness of nestling blue-footed boobies to external stimuli, resulting in more aggression by dominants and greater readiness of subordinates to submit.     

Size dominance affecting the social interactions and growth of juvenile Japanese flounder,Paralichthys olivaceus

Juvenile flounder Paralichthys olivaceus were size‐graded into three groups (small, large and mixing of small and large) and social interactions (feeding, aggressive attacking and activity) and growth of the fish were investigated. Growth of the subordinates (small flounder) was markedly suppressed by the presence of the dominants (large flounder). Dominants did not significantly suppress the overall food intake of the subordinates, but exhibited high aggressive attacking on the subordinates and consequently inhibited their activity. Size dominant interactions had little influence on the aggressive behaviour, feeding, activity and growth of the dominants. Results substantiated the hypothesis that the retardation in the growth of the subordinate flounder was attributed to the physiological costs of ‘stress’ by the aggression of the dominants. Individual differences in aggressive behaviour, feeding and activity were at least partly responsible for the growth depensation of the juvenile flounder. The dominants could not effectively defend the food in excess and disproportional food acquisition of the subordinates and dominants was not the primary mechanism responsible for the size hierarchy effect. In culture, size grading of the early juvenile flounder could markedly improve the growth and survival and thus possibly increase the overall biomass production of the flounder.     

Mating Resets Male Cricket Aggression

An animal’s motivational state can significantly impact its behavior. We examined the effects of mating on the aggression of male Acheta domesticus crickets. Pairs of males were allowed to establish dominance and subordinance and were then physically separated. Subordinate males were then allowed to either copulate with a female or to have chemo-tactile contact with, but to not copulate with, a female. Less than 15 min after separation, all male pairs engaged in a second agonistic encounter. Subordinate males that copulated with females were significantly more aggressive toward their dominant partners than un-mated subordinate males. Many mated subordinates became dominant. Allowing a subordinate male to contact, but not copulate with, a female had a similar effect, suggesting that chemo-tactile cues from the female are sufficient to elicit this change in aggression.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

Formal biting in stumptailed macaques (Macaca arctoides)

Form and function of a specific kind of biting were studied in a captive group of stumptailed macaques (Macaca arctoides) composed of 1 adult male and 10 females. Behavior patterns were recorded with all occurrence and scan sampling techniques. Formal biting consisted of slowly gripping with teeth a part of the body of an apparently willing partner, most often the forearms, lips, or eyebrows. It may occur either following an agonistic interaction or outside the context of aggression. Such biting was directed from dominants towards subordinates, and appeared especially frequently between individuals having frequent agonistic interactions. It is concluded that this behavior represents a ritualized interaction expressing formal dominance between partners.     

Benefits and Costs of Dominance in the Angelfish Centropyge bicolor

Social groups are often structured by dominance hierarchies in which subordinates consistently defer to dominants. High‐ranking individuals benefit by gaining inequitable access to resources, and often achieve higher reproductive success; but may also suffer costs associated with maintaining dominance. We used a large‐scale field study to investigate the benefits and costs of dominance in the angelfish Centropyge bicolor, a sequential hermaphrodite. Each haremic group contains a single linear body size‐based hierarchy with the male being most dominant, followed by several females in descending size order. Compared to their subordinate females, dominant males clearly benefited from disproportionately high spawning frequencies, but bore costs in lower foraging rates and greater aggressive defence of their large territories. Within the female hierarchy, more dominant individuals benefited from higher spawning frequencies and larger home ranges, but displayed neither higher foraging rates nor spawn order priority. However, dominance in females was also linked to aggressiveness, particularly towards immediate subordinates, suggesting that females were using energetically costly aggression to maintain their high rank. We further showed by experimentally removing dominant females that the linear hierarchy was also a social queue, with subordinates growing to inherit higher rank with its attendant benefits and costs when dominants disappeared. We suggest that in C. bicolor, the primary benefit of high rank is increased reproductive success in terms of current spawning frequency and the prospect of inheriting the male position in the near future, which may be traded off against the cost of aggressively defending rank and territory.     

How Food Controls Aggression in Drosophila

How animals use sensory information to weigh the risks vs. benefits of behavioral decisions remains poorly understood. Inter-male aggression is triggered when animals perceive both the presence of an appetitive resource, such as food or females, and of competing conspecific males. How such signals are detected and integrated to control the decision to fight is not clear. For instance, it is unclear whether food increases aggression directly, or as a secondary consequence of increased social interactions caused by attraction to food. Here we use the vinegar fly, Drosophila melanogaster, to investigate the manner by which food influences aggression. We show that food promotes aggression in flies, and that it does so independently of any effect on frequency of contact between males, increase in locomotor activity or general enhancement of social interactions. Importantly, the level of aggression depends on the absolute amount of food, rather than on its surface area or concentration. When food resources exceed a certain level, aggression is diminished, suggestive of reduced competition. Finally, we show that detection of sugar via Gr5a⁺ gustatory receptor neurons (GRNs) is necessary for food-promoted aggression. These data demonstrate that food exerts a specific effect to promote aggression in male flies, and that this effect is mediated, at least in part, by sweet-sensing GRNs.     

Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the ‘pay-to-stay’ hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced ‘idle’ period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers.     

Repeated agonistic encounters in hamsters modulate AVP V1a receptor binding

Arginine vasopressin (AVP) regulates aggression in male Syrian hamsters. In this study, we used radioligand receptor autoradiography to examine whether changes in agonistic behavior following acute and repeated social defeat are accompanied by changes in AVP V1a receptor binding. Social defeat produced high levels of submissive behavior and a loss of territorial aggression when hamsters were subsequently tested with a novel intruder, and repeated agonistic encounters produced similar behavioral changes in subordinates. AVP V1a receptor binding was not reduced by acute social defeat but was affected by repeated agonistic encounters. Dominants had significantly more AVP V1a receptor binding in lateral portions of the ventromedial hypothalamus (VMHL) than did their subordinate opponents, but subordinates were no different from controls. In contrast, receptor binding did not differ in most other brain regions examined. The changes in receptor binding appear to be independent of testosterone levels, as testosterone levels did not differ among dominants, subordinates, and controls. Our results suggest that changes in AVP V1a receptors do not account for the changes in agonistic behavior produced by acute social defeat but AVP V1a binding in the VMHL correlates with, and may modulate, the behavioral changes that occur following repeated experiences of victory.     

Reproductive Consequences of Aggression in a Territorial Songbird

Territorial aggression can influence males’ ability to obtain high‐quality resources and access to mates; however, in many species, the reproductive consequences of variation in aggression are unknown. In this study, we investigated how individual variation in aggressive behavior relates to reproductive success in socially monogamous, genetically polygynous song sparrows (Melospiza melodia). Prior research in this species shows that male song sparrows differ in their willingness to engage in agonistic interactions with territorial intruders and that individual variation in aggression appears to have functional significance. Aggressive males have been shown to obtain territories where females produce larger clutch sizes, suggesting that individuals who display high levels of territorial aggression are defending high‐quality territories or females. Further, aggressive males are considered a greater threat to territory‐holding males than less aggressive males. In this study, we ask whether individual differences in aggression are linked to differences in extra‐pair reproductive success, annual reproductive success, and offspring quality. We did not uncover a relationship between aggression and annual reproductive success or patterns of extra‐pair paternity. However, we found that the nestlings of aggressive males grew at a faster rate than the nestlings of less aggressive males. Future studies should attempt to identify mechanisms to explain the relationship between offspring growth rate and male aggression and investigate whether faster offspring growth rates translate to greater survival and recruitment of offspring.     

Cellular and molecular basis of decision‐making

People think they are in control of their own decisions: what to eat or drink, whom to marry or pick a fight with, where to live, what to buy. Behavioural economists and neurophysiologists have long studied decision‐making behaviours. However, these behaviours have only recently been studied through the light of molecular genetics. Here, we review recent research in mice, Drosophila melanogaster and Caenorhabditis elegans, that analyses the molecular and cellular mechanisms underlying decision‐making. These studies interrogate decision‐making about food, sexual behaviour, aggression or foraging strategies, and add molecular and cell biology understanding onto the consilience of brain and decision.     

Dominance Interactions Regulate Worker Mating in the Polygynous Ponerine Ant Gnamptogenys menadensis

In queenless ants, workers compete aggressively to be reproductives instead of sterile helpers. To limit the number of reproductives, either mating or egg-laying by mated workers can be regulated. In Gnamptogenys menadensis , all mated workers reproduce, and field data presented here indicate that mating is not random. We removed gamergates experimentally (n=16 groups) to induce mating and gamergate replacement. Virgin workers engaged in agonistic interactions, allowing us to classify them into two groups: dominants performed antennal boxing and biting, while subordinates did not. However, a few subordinates cooperated to immobilize individual dominant workers. This effectively reduced the number of dominants because immobilized dominants became subordinates. Six to 12 wks after the removal of reproductives, between one and eight dominants per colony started to perform 'sexual calling' outside the nest entrance. Sixteen (out of 33) dominants mated with foreign males introduced in five experimental groups. None of the subordinate workers mated. The probability of mating is thus regulated by dominance interactions among workers and immobilizations initiated by infertile workers in this polygynous queenless ant.     

Better safe than sorry--socio-spatial group structure emerges from individual variation in fleeing, avoidance or velocity in an agent-based model

In group-living animals, such as primates, the average spatial group structure often reflects the dominance hierarchy, with central dominants and peripheral subordinates. This central-peripheral group structure can arise by self-organization as a result of subordinates fleeing from dominants after losing a fight. However, in real primates, subordinates often avoid interactions with potentially aggressive group members, thereby preventing aggression and subsequent fleeing. Using agent-based modeling, we investigated which spatial and encounter structures emerge when subordinates also avoid known potential aggressors at a distance as compared with the model which only included fleeing after losing a fight (fleeing model). A central-peripheral group structure emerged in most conditions. When avoidance was employed at small or intermediate distances, centrality of dominants emerged similar to the fleeing model, but in a more pronounced way. This result was also found when fleeing after a fight was made independent of dominance rank, i.e. occurred randomly. Employing avoidance at larger distances yielded more spread out groups. This provides a possible explanation of larger group spread in more aggressive species. With avoidance at very large distances, spatially and socially distinct subgroups emerged. We also investigated how encounters were distributed amongst group members. In the fleeing model all individuals encountered all group members equally often, whereas in the avoidance model encounters occurred mostly among similar-ranking individuals. Finally, we also identified a very general and simple mechanism causing a central-peripheral group structure: when individuals merely differed in velocity, faster individuals automatically ended up at the periphery. In summary, a central-peripheral group pattern can easily emerge from individual variation in different movement properties in general, such as fleeing, avoidance or velocity. Moreover, avoidance behavior also affects the encounter structure and can lead to subgroup formation.     

Etho-biochemical mechanisms of early differentiation in juveniles of the Atlantic salmon <Emphasis Type="Italic">Salmo salar</Emphasis>

The social status of hatchery-reared juveniles of Atlantic salmon Salmo salar at the age of 11–19 months in conditions of lack of shelters was investigated experimentally. It was demonstrated that biochemical differentiation in such juveniles begins at the age of 13 months—one month before the first differences in the social status of fish and four months prior to the beginning of smoltification. The dominants occupy bottom areas with shelters and extrude the subordinates to the water column. The subordinates undergo smoltification or die from aggression of the dominants. Concentrations of dopamine, noradrenalin, and of their metabolites in the brain of fish in the beginning of smoltification were higher in the dominants and, by the end of smoltification, were higher in smolts. The social behavior of fish is considered to be one of the ethological mechanisms of differentiation of salmon juveniles into smolts and parr.     

Social rank‐dependent expression of arginine vasotocin in distinct preoptic regions in male Oryzias latipes

This study examined arginine vasotocin (AVT) expression in the brains of dominant and subordinate male medaka Oryzias latipes after short‐ and long‐term competition. High AVT expression in distinct preoptic regions was found in dominants and subordinates within minutes of encountering each other. During long‐term competition, AVT expression remained high in dominants but not in subordinates.     

Pheromone, juvenile hormone, and social status in the male lobster cockroach Nauphoeta cinerea

In this study, the major pheromone component, 3‐hydroxy‐2‐butanone (3H‐2B), released by dominants was measured during early scotophase. Both the JH III titer in the hemolymph and the 3H‐2B content of the sternal glands of the dominants and subordinates were then measured during late scotophase and late photophase. These investigations were performed on encounter days 1, 2, 3, 5, 7, 9, 12, and 20. The results showed that, for non‐aggressive posture (AP)‐adopting socially naïve males (SNMs), both the 3H‐2B release and the hemolymph JH III titer were maintained at a low level. Once a fight occurred, 3H‐2B release was raised significantly in the AP‐adopting dominants, but not in non‐AP‐adopting subordinates, and remained raised throughout the entire experimental period. At 30 min after the first encounter, the hemolymph JH III titer was significantly increased in dominants, but not in subordinates. A significantly higher hemolymph JH III titer was observed in dominants during late scotophase on days 3, 5, 12, and 20 and during late photophase on days 3, 5, and 20. After fighting, the sternal gland 3H‐2B content of the dominants or subordinates was significantly lower than in SNMs. In dominants, the sternal gland 3H‐2B content during late scotophase was significantly lower than that during late photophase in the first 9 domination days, while, in the subordinates, the 3H‐2B content during late scotophase was either similar to, or significantly higher than, that in late photophase. In the dominants, 3H‐2B release and JH III titer were positively correlated. In rank switchers, the switched social status was positively correlated with both 3H‐2B release and JH III titer. Comparison of 3H‐2B release and JH III titer in 1‐time, 3‐time, or 5‐time dominants showed that, although winning significantly increased both 3H‐2B release and JH III titer, there is no significant difference in 3H‐2B release between 3‐ and 5‐time winners, while the JH III titer was most significantly increased in the 3‐time winners. The possible relationship between pheromone release, JH III titer, and social status is discussed. Arch. Insect Biochem. Physiol. 2008. © 2008 Wiley‐Liss, Inc.     

Non‐sex‐biased Dominance in a Sexually Monomorphic Electric Fish: Fight Structure and Submissive Electric Signalling

Males and females commonly compete for limited resources. When interaction costs are similar for both sexes and there are no sexual differences in resource value estimation, a non‐sex‐biased dominance is expected. Moreover, only non‐sex‐biased assessment of contenders fighting ability (Resource Holding Potential, RHP) should influence contest decisions. To test these predictions, we evaluated non‐breeding agonistic intra‐ and intersexual dyadic interactions in the weakly electric fish, Gymnotus omarorum. During the non‐breeding season, resource value is not expected to depend on individuals’ reproductive status and should thus be equal for males and females. In addition, as G. omarorum presents no sexual differences in body size, interaction costs can be considered symmetric between sexes. We confirmed that body size differences, but not individuals’ gender, is the best predictor of dominance. We correlated RHP asymmetries with contest duration and evidenced that body size but not sex influences assessment in intrasexual and intersexual encounters. All dyads tested engaged in agonistic interactions (N = 33) in which a clear dominant emerged. The analysis of conflict phases evidenced the submissive role of electric displays. Electric organ discharge (EOD) interruptions appear early in the contest as an electric hiding attempt, whereas chirps are post‐resolution signals of subordinate status. Interestingly, the decision of interrupting the EOD was also influenced by RHP asymmetries, whereas chirping activity was influenced by the intensity of the attacks received. Our results confirm that body size is the best RHP proxy in non‐breeding intra‐ and intersexual contests of this monomorphic species and demonstrated a sequential pattern of submissive signalling by means of two different electric displays.     

Social relationships in a herd of Sorraia horses Part I. Correlates of social dominance and contexts of aggression

Factors related to dominance rank and the functions of aggression were studied in a herd of Sorraia horses, Equus caballus, under extensive management. Subjects were 10 adult mares 5-18 years old and a stallion introduced into the group for breeding. Dominance relationships among mares were clear, irrespective of rank difference, and remained stable after introduction of the stallion. The dominance hierarchy was significantly linear and rank was positively correlated with age and total aggressiveness. Higher-ranking mares received lower frequency and intensity of agonistic interactions. Nevertheless, higher-ranking dominants were not more likely to elicit submission from their subordinates than lower-ranking dominants. Neither close-ranking mares nor mares with less clear dominance relationships were more aggressive towards each other. Agonistic interactions seemed to be used more importantly in regulation of space than to obtain access to food or to reassert dominance relationships. Contexts of aggression were related to mare rank. The results suggest that dominance relationships based on age as a conventional criterion were established to reduce aggressiveness in a herd where the costs of aggression are likely to outweigh the benefits.     

Function and variability of male sex traits in a blenniid fish, Parablennius tentacularis

Juvenile flounder Paralichthys olivaceus were size‐graded into three groups (small, large and mixing of small and large) and social interactions (feeding, aggressive attacking and activity) and growth of the fish were investigated. Growth of the subordinates (small flounder) was markedly suppressed by the presence of the dominants (large flounder). Dominants did not significantly suppress the overall food intake of the subordinates, but exhibited high aggressive attacking on the subordinates and consequently inhibited their activity. Size dominant interactions had little influence on the aggressive behaviour, feeding, activity and growth of the dominants. Results substantiated the hypothesis that the retardation in the growth of the subordinate flounder was attributed to the physiological costs of 'stress' by the aggression of the dominants. Individual differences in aggressive behaviour, feeding and activity were at least partly responsible for the growth depensation of the juvenile flounder. The dominants could not effectively defend the food in excess and disproportional food acquisition of the subordinates and dominants was not the primary mechanism responsible for the size hierarchy effect. In culture, size grading of the early juvenile flounder could markedly improve the growth and survival and thus possibly increase the overall biomass production of the flounder.     

Vocal Coordination of Group Movement by Green Woodhoopoes (Phoeniculus purpureus)

Communication signals are used by many species to maintain group cohesion when moving over larger areas. Groups of green woodhoopoes (Phoeniculus purpureus) generally move around their territory as a close‐knit unit. Dominant individuals were more likely than subordinates to initiate movement to a new foraging site, but there was no intersexual difference. Dominants were also more likely than subordinates to be followed immediately. Vocalizations were shown to play an important role in mobilization: in the thick forests inhabited by woodhoopoes, visual cues to coordinate movement are likely to be less successful. When responding to the rallying call of a neighboring group, dominants and subordinates were equally likely to lead, as were males and females. As other group members followed immediately on most of these occasions, vocalizations were less important in this context than when moving to a new foraging site.