The correlation between subordinate fish eye colour and received attacks: a negative social feedback mechanism for the reduction of aggression during the formation of dominance hierarchies

Eye darkening has been linked to social status in fish. The subordinate's eyes darken, while the eyes of the dominant fish become pale. Although this phenomenon has been described in salmonid fishes and in the African cichlid Nile tilapia Oreochromis niloticus, it is unclear whether eye darkening correlates with a reduction in aggressive behaviour. Thus, we evaluated the link between social status and eye darkening. We evaluated whether the eye colours of subordinate fish correlate with the frequency of received attacks in a neotropical fish, the pearl cichlid Geophagus brasiliensis. We paired pearl cichlids and quantified both the aggressive behaviour and the eye darkening of each fish. As has been described for Nile tilapia and Atlantic salmon, a clear-cut hierarchical relationship formed, where dominance and subordination were associated with pale and dark eye colours, respectively. Initially, eye colour darkening was positively correlated with the frequency of received attacks; however, a negative association occurred following eye darkening, in which the intensity of aggressive interactions decreased. Thus, fish that initially received a high number of attacks signalled subordination more rapidly and intensely (rapid and dramatic eye darkening), thereby inducing a negative social feedback mechanism that led to reduced aggression.     

Physiology,endocrinology and chemical communication in aggressive behaviour of fishes

Fishes show remarkably diverse aggressive behaviour. Aggression is expressed to secure resources; adjusting aggression levels according to context is key to avoid negative consequences for fitness and survival. Nonetheless, despite its importance, the physiological basis of aggression in fishes is still poorly understood. Several reports suggest hormonal modulation of aggression, particularly by androgens, but contradictory studies have been published. Studies exploring the role of chemical communication in aggressive behaviour are also scant, and the pheromones involved remain to be unequivocally characterized. This is surprising as chemical communication is the most ancient form of information exchange and plays a variety of other roles in fishes. Furthermore, the study of chemical communication and aggression is relevant at the evolutionary, ecological and economic levels. A few pioneering studies support the hypothesis that aggressive behaviour, at least in some teleosts, is modulated by “dominance pheromones” that reflect the social status of the sender, but there is little information on the identity of the compounds involved. This review aims to provide a global view of aggressive behaviour in fishes and its underlying physiological mechanisms including the involvement of chemical communication, and discusses the potential use of dominance pheromones to improve fish welfare. Methodological considerations and future research directions are also outlined.     

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.     

Early behaviour in fishes

Synopsis The ethological approach to the study of early life histories of fishes is illustrated by examples of behavioural ontogeny in cichlid and salmonid fishes. In both species recognition and social organization, early experience is of crucial importance.Paper presented in the symposium \lsEmbryonic and larval periods of fishes: present status and significance\rs, Canadian Conference for Fisheries Research (CCFFR), Fredericton, New Brunswick, January 1977     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

Early hatch: a strategy for safe downstream larval transport in amphidromous gobies

The downstream migration to sea of newly-hatched larvae of amphidromous fishes exposes them to the risk of irreversible starvation if migration takes too long. Some fishes, especially sicydiine gobies, exhibit early hatch of eggs, often less than 48 h after fertilisation, and the newly-hatched larvae are at a very early stage of ontogeny, with no functional mouth or fins, no functional eye, and little pigmentation in the eye or elsewhere. This may facilitate survival as it means that downstream migration takes place when plenty of yolk remains, minimising the risk of starvation. Additional behaviours, such as positive phototaxis, continual swimming up into the water column, and hatching during elevated river flows, may also have contributed to rapid downstream transport and survival.     

Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain

Many studies suggest a role for biogenic amines in a variety of insect behaviors including intraspecific aggression. In ants, despite a rich behavioral repertoire and prominent aggressive interactions, little is known about the potential impact of biogenic amines. This may partly be due to the general lack of information about aminergic systems in the ant brain. The present study investigates serotonergic and dopaminergic neuronal systems in the brain of the ponerine ant Harpegnathos saltator. In H. saltator, intraspecific aggression is important for the regulation of reproduction. This species, therefore, is amenable to comparative studies of aminergic neuronal effects on long-term changes in aggression. Using immunocytochemistry and confocal microscopy, we found that in the brains of sterile workers, the distributions of serotonergic and dopaminergic neuronal processes differed substantially. In addition, branching patterns of serotonergic neurons showed marked differences between males and females. Brains of workers after 3 days and 3 weeks of aggressive interactions revealed no marked differences in serotonergic and dopaminergic neurons compared to those of reproductive and non-aggressive individuals. We conclude that different levels of intraspecific aggression do not involve profound anatomical changes in serotonergic and dopaminergic neurons. Subtle changes may be masked by inter-individual variances.     

The ontogeny of haematopoiesis in the marine teleost Leiostomus xanthurus and a comparison of the site of initial haematopoiesis with Opsanus tau

The ontogeny of haematopoiesis in the perciform fish, spot Leiostomus xanthurus , differed from that reported as the norm for fishes, as exemplified by the cypriniform zebrafish Danio rerio , and observed in the batrachoidiform oyster toadfish Opsanus tau . Erythropoiesis in spot was first evident in the head kidney of yolk‐sac larvae 3 days after hatching (DAH). No embryonic intermediate cell mass (ICM) of primitive stem cells or blood islands on the yolk were apparent within embryos. Erythrocytes were first evident in circulation near the completion of yolk absorption, c . 5 DAH, when larvae were c . 2·0 mm notochord length ( L _N). Erythrocyte abundance increased rapidly with larval development for c . 14 to 16 DAH, then became highly variable following changes in cardiac chamber morphology and volume. Erythrocytic haemoglobin (Hb) was not detected within whole larvae until they were 12 DAH or c . 3·1 mm L _N, well after yolk and oil‐globule absorption. The Hb was not quantified until larvae were >47 DAH or >7 mm standard length. The delayed appearance of erythrocytes and Hb in spot was similar to that reported for other marine fishes with small embryos and larvae. In oyster toadfish, a marine teleost that exhibits large embryos and larvae, the ICM and Hb were first evident in two bilateral slips of erythropoietic tissue in the embryos, c . 5 days after fertilization. Soon thereafter, erythrocytes were evident in the heart, and peripheral and vitelline circulation. Initial haematopoiesis in oyster toadfish conformed with that described for zebrafish. While the genes that code for the development of haematopoiesis are conserved among vertebrates, gene expression lacks phylogenetic pattern among fishes and appears to conform more closely with phenotypic expression related to physiological and ecological influences of overall body size and environmental oxygen availability.     

In your face: facial metrics predict aggressive behaviour in the laboratory and in varsity and professional hockey players

Facial characteristics are an important basis for judgements about gender, emotion, personality, motivational states and behavioural dispositions. Based on a recent finding of a sexual dimorphism in facial metrics that is independent of body size, we conducted three studies to examine the extent to which individual differences in the facial width-to-height ratio were associated with trait dominance (using a questionnaire) and aggression during a behavioural task and in a naturalistic setting (varsity and professional ice hockey). In study 1, men had a larger facial width-to-height ratio, higher scores of trait dominance, and were more reactively aggressive compared with women. Individual differences in the facial width-to-height ratio predicted reactive aggression in men, but not in women (predicted 15% of variance). In studies 2 (male varsity hockey players) and 3 (male professional hockey players), individual differences in the facial width-to-height ratio were positively related to aggressive behaviour as measured by the number of penalty minutes per game obtained over a season (predicted 29 and 9% of the variance, respectively). Together, these findings suggest that the sexually dimorphic facial width-to-height ratio may be an 'honest signal' of propensity for aggressive behaviour.     

Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes)

Studies investigating relationships between social parameters (such as dominance rank, rates of aggressive and sexual behaviors) and androgen (particularly, testosterone) levels in male primates have yielded inconsistent results. In the present study, we address the relationship between androgens, male dominance rank and rank-associated behaviors in two groups of captive chimpanzees, a species characterized by a pronounced dominance hierarchy between adult males. By combining behavioral observations with urinary testosterone (T) measurements, we found that the differences in T concentrations between males were small and not obviously related to their dominance rank. T levels were not related to the rates of initiated aggression and copulatory behavior, but a significant negative relationship between male T level and the rates of strong aggression received was apparent. Our findings, combined with those of others, suggest that any relationship between dominance rank and T depends upon the extent to which individual rank-associated behaviors (e.g. aggressive/sexual) are themselves related to T.     

Maintenance of female dominance in blue‐eyed black lemurs (Eulemur macaco flavifrons) and gray bamboo lemurs (Hapalemur griseus griseus) under semi‐free‐ranging and captive conditions

Several species of Malagasy prosimians are characterized by female dominance, an unusual trait among mammals. We compare the extent to which female dominance is displayed and the mechanisms that are used to maintain dominance in the frugivorous blue‐eyed black lemurs (Eulemur macaco flavifrons) and the folivorous gray bamboo lemurs (Hapalemur griseus griseus) housed at the Duke Lemur Center. All dominant–submissive interactions were recorded during 448 hr of focal animal observations. Both species of lemurs exhibited clear patterns of female dominance. However, the two species used aggressive dominance (defined as aggression+submission) and social dominance (defined as submission in the absence of aggression) to different extents in maintaining hierarchies within each group. The adult female blue‐eyed black lemurs used aggressive dominance (e.g., chase, cuff, bite) in more of their dominance interactions (66%) than did the adult female gray bamboo lemurs (40%). In both species, rates of aggressive dominance interactions were higher during feeding versus nonfeeding periods and while in smaller outdoor runs versus larger natural habitat enclosures, but the differences were not significant. Overall blue‐eyed black lemurs exhibit a more aggressive form of female dominance compared to the gray bamboo lemur. Zoo Biol 26:345–361, 2007. © 2007 Wiley‐Liss, Inc.     

Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

Alternative Ways to Become a Juvenile or a Definitive Phenotype (and on Some Persisting Linguistic Offenses)

Lack of knowledge of early and juvenile development often makes it difficult to decide when a fish becomes a juvenile or, for that matter, a definitive phenotype. According to the established life-history model, a fish develops naturally in a saltatory manner, its entire life consisting of a sequence of stabilized self-organizing steps, separated by distinct less stabilized thresholds. Changes are usually introduced during thresholds. In principle, there are two ways to reach the juvenile period: by indirect or by direct development. Indirectly developing fishes have a distinct larva period that ends in a cataclysmic or mild remodeling process, called metamorphosis, from which the fishes emerge as juveniles. During metamorphosis, most temporary organs and structures of the embryos and larvae are replaced by definitive organs and structures that are also possessed by the adults. In contrast, directly developing fishes have no larvae. Their embryos develop directly into juveniles and do not need major remodeling. Consequently, the beginning of their juvenile period is morphologically and functionally less distinct than in indirect development. The life-history model helps to find criteria that identify the natural boundaries between the different periods in the life of a fish, among them, the beginning of the juvenile period. Looking at it from a different angle, when ontogeny progresses from small eggs with little yolk, larvae are required as the necessary providers of additional nutrients (feeding entities similar to amphibian tadpoles or butterfly caterpillars) in order to accumulate materials for the metamorphosis into the definitive phenotypes. Directly developing fishes start with large demersal eggs provided with an adequate volume of high density yolk and so require no or little external nutrients to develop into the definitive phenotype. These large eggs are released and develop in concentrated clutches. It therefore becomes possible and highly effective to guard them in nests or bear them in external pouches, gill chambers or the buccal cavity. Viviparity is the next natural step. Now the maternal investment into large yolks can be supplemented or replaced by direct food supply to the developing embryos like, for example, the secretion of uterine histotrophe or nutrient transfer via placental analogues. When the young of guarders and bearers start exogenous feeding, they are much larger or better developed than larvae of nonguarders and the larva period in the former is reduced to a vestige or eliminated entirely. In the latter case, the juvenile period begins with the first exogenous feeding. Such precocial fishes are more specialized and able to survive better in competitive environments. In contrast, altricial forms retain or revert to a life-history style with indirect development and high fecundity when dispersal is advantageous or essential. Fishes become juveniles when the definitive phenotype is formed in most structures, either indirectly from a larva via metamorphosis or directly from the embryo.     

Extensive Reorganization of Behavior Accompanies Ontogeny of Aggression in Male Flesh Flies

Aggression, costly in both time and energy, is often expressed by male animals in defense of valuable resources such as food or potential mates. Here we present a new insect model system for the study of aggression, the male flesh fly Sarcophaga crassipalpis, and ask whether there is an ontogeny of aggression that coincides with reproductive maturity. After establishing that reproductive maturity occurs by day 3 of age (post-eclosion), we examined the behavior of socially isolated males from different age cohorts (days 1, 2, 3, 4, and 6) upon introduction, in a test arena, with another male of the same age. The results show a pronounced development of aggression with age. The change from relative indifference to heightened aggression involves a profound increase in the frequency of high-intensity aggressive behaviors between days 1 and 3. Also noteworthy is an abrupt increase in the number of statistically significant transitions involving these full-contact agonistic behaviors on day 2. This elevated activity is trimmed back somewhat by day 3 and appears to maintain a stable plateau thereafter. No convincing evidence was found for escalation of aggression nor the establishment of a dominance relationship over the duration of the encounters. Despite the fact that aggressive interactions are brief, lasting only a few seconds, a major reorganization in the relative proportions of four major non-aggressive behaviors (accounting for at least 96% of the total observation time for each age cohort) accompanies the switch from low to high aggression. A series of control experiments, with single flies in the test arenas, indicates that these changes occur in the absence of the performance of aggressive behaviors. This parallel ontogeny of aggressive and non-aggressive behaviors has implications for understanding how the entire behavioral repertoire may be organized and reorganized to accommodate the needs of the organism.     

Dominance,aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

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.     

Effects of maternal stress coping style on offspring characteristics in rainbow trout (Oncorhynchus mykiss)

Maternal size, age, and allostatic load influence offspring size, development, and survival. Some of these effects have been attributed to the release of glucocorticoids, and individual variation in these stress hormones is related to a number of traits. Correlated traits are often clustered and used to define the proactive and reactive stress coping styles. Although stress coping styles have been identified in a number of animal groups, little is known about the coupling between stress coping style and offspring characteristics. In the present study, plasma cortisol levels in ovulated mothers and cortisol levels in non-fertilized eggs from two rainbow trout (Oncorhynchus mykiss) strains selected for high (HR) and low (LR) post-stress plasma cortisol levels were compared. Offspring characteristics such as egg size, larval growth, and energy reserves also were compared between the two strains. Maternal plasma and egg cortisol levels were correlated, but no difference between the HR and LR strains was detected in either parameter. LR females produced larger eggs, and larvae with larger yolk sacs compared to HR females, however no differences in larval body size (excluding the yolk) was detected between strains. Considering that the HR and LR strains have a number of correlated behavioral and physiological traits that resemble the reactive and proactive stress coping styles, respectively, the results suggest that proactive mothers invest more energy into their offspring, producing larvae with larger energy reserves. It is possible that larger energy reserves in proactive larvae support the energy requirement for establishing and defending territory in salmonid fish. Furthermore, in the present study we found a positive relationship between mother plasma cortisol and egg cortisol; however neither mother plasma cortisol nor egg cortisol differed between strains. These results indicate that cortisol endowment from the mother to the offspring plays a minor role in the transfer of the behavioral and physiological traits which separates these strains.     

Counter aggression and reconciliation in Assamese macaques (Macaca assamensis)

Patterns of aggressive and affiliative behavior, such as counter aggression and reconciliation, are said to covary in the genus Macaca; this is referred to as the systematic variation hypothesis. These behavior patterns constitute a species dominance style. Van Schaik's [1989] socioecological model explains dominance style in macaques in terms of within- and between-group contest competition. Dominance style is also said to correlate with phylogeny in macaques. The present study was undertaken to examine phylogenetic and socioecological explanations of dominance style, as well as the systematic variation hypothesis. We collected data on counter aggression and reconciliation from a habituated group of Assamese macaques (Macaca assamensis) at the Tukeswari Temple in Assam, India. The proportion of agonistic episodes that involved counter aggression was relatively low. Counter aggression, however, occurred more often among males than among females, and it was most common when females initiated aggression against males. The conciliatory tendency for this group of Assamese macaques was 11.2%. The frequency of reconciliation was low for fights among males and for fights among females, but reconciliation was particularly rare for opposite-sexed opponents. Female social relationships were consistent with the systematic variation hypothesis, and suggest a despotic dominance style. A despotic dominance style in Assamese macaques weakens the correlation between dominance style and phylogeny in macaques, but it is not inconsistent with the socioecological model. Male-female relationships were not well explained by the despotic-egalitarian framework, and males may well have more tolerant social relationships than do females. Sex differences need to be considered when categorizing species according to dominance style.     

Sex differences in the behaviour of immature captive lowland gorillas

Studies of the behaviour of 26 (12 males and 14 females) captive infant and juvenile lowland gorillas showed clear sex differences. Females showed greater interest in young infants and were more active in nest building as well as in solitary and social grooming. Males were more active in locomotive, dominance, and aggressive behaviour and in social play. Hand-rearing further increased aggression. Males were more aggressive when they lived with only one partner, and they rose in rank even above older females, a pattern that has not been observed in naturally reared gorillas.     

The energetic cost of reproductive conflicts in the ant Pachycondyla obscuricornis

In a variety of social animals, individuals can secure reproductive rights through aggressive dominance. Direct individual benefits of aggression are widely recognized, but underlying costs affecting group productivity, and thus indirect benefits, are less clear. Costs of aggressive regulation of reproduction are especially important in small social insect colonies, where individual workers could potentially dominate male production. We estimated the energetic costs associated with the regulation of worker reproduction in the ponerine ant Pachycondyla obscuricornis, using the total CO2 emission of a colony as a measure. The level of CO2 emission of 12 experimental colonies varied significantly during five periods with varying levels of aggression and egg-laying. Overall, CO2 emission increased with the degree of fighting in a colony, but was not associated with differences in egg-laying. Aggressive regulation of reproduction and the formation of a dominance hierarchy thus pose an energetic cost to the colony. Furthermore, workers reduce their work-activities immediately after experimental orphaning, giving a further cost to the colony. These costs might influence the outcome of conflicts over male production in ants. This paper presents the first quantification of energetic costs of aggressive behavior regulating reproduction in ants.