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.     

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.     

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.     

Female-mediated causes and consequences of status change in a social fish

In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.     

Shoaling Decisions in Angelfish: The Roles of Social Status and Familiarity

Abstract Past research has shown that angelfish, Pterophyllum scalare , are capable of discriminating between shoals composed of familiar dominant and subordinate companions, whereas they show no preference for shoals of unfamiliar conspecifics. In this study, the relative importance of familiarity and social status (shoal factors) on the shoaling decision of juvenile angelfish, which also differed in social status (individual factor), was investigated as very little is known about such tradeoffs in fishes. Dominant and subordinate individuals were given the choice to shoal with a group of conspecifics composed of familiar dominants vs. unfamiliar dominants and composed of familiar subordinates vs. unfamiliar subordinates. The findings demonstrate that fish with different social status differed in their shoaling preference. Subordinate test fish showed a preferential association with familiar subordinates over unfamiliar subordinates, but preferred the unfamiliar shoal over the familiar one when both shoals were constituted by dominant individuals. The shoaling behaviour shown by dominant test fish, on the other hand, indicated no significant preference for any of the shoals regardless of their composition. A replicate preference test carried out 2 h 30 min after the first one indicated that the association pattern was relatively consistent. Results suggest that angelfish are able to differentiate between the stimulus shoals and demonstrate that the pervasive influence of familiarity on the shoaling decision may be restrained or overridden by the composition of the familiar shoals and the social status of the test fish.     

Intraspecific variation in competitive ability and food intake in salmonids: consequences for energy budgets and growth rates

The interactions between dominance status, feeding rate and growth in rainbow trout, Salmo gairdneri Richardson, were analyzed using published data on experimental populations. There was a positive correlation between metabolic expenditure and food intake in both dominant and subordinate fish, but dominants obtained a greater intake for a given expenditure than did subordinates. Subordinates that adopted a high–return/high–cost foraging strategy actually expended more energy than they acquired, whereas those that minimized energy expenditure obtained a net energy gain. This led to the surprising finding that the growth rate of subordinates was negatively correlated with food intake.     

Temperature affects insulin-like growth factor I and growth of juvenile southern flounder, Paralichthys lethostigma

Temperature profoundly influences growth of heterothermic vertebrates. However, few studies have investigated the effects of temperature on growth and insulin-like growth factor I (IGF-I) in fishes. The aim of this study was to examine effects of temperature on growth and establish whether IGF-I may mediate growth at different temperatures in southern flounder, Paralichthys lethostigma. In two experiments, juvenile flounder were reared at 23 and 28 degrees C and growth was monitored for either 117 or 197 days. Growth was similar across treatments in both experiments until fish reached approximately 100 mm total length. Body size then diverged with fish at 23 degrees C ultimately growing 65-83% larger than those at 28 degrees C. Muscle IGF-I mRNA, plasma IGF-I, and hepatosomatic index (HSI) were significantly higher in flounder at 23 degrees C, whereas hepatic IGF-I mRNA abundance did not differ with treatment. Muscle IGF-I mRNA was correlated with HSI, while plasma IGF-I was correlated with body size, hepatic IGF-I mRNA, and HSI. These results demonstrate a strong effect of temperature on flounder growth and show that temperature-induced variation in growth is associated with differences in systemic IGF-I and local (i.e., muscle) IGF-I mRNA levels. The results also support the use of plasma IGF-I and HSI as indicators of flounder growth status.     

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.     

Higher levels of aggression are observed in socially dominant toadfish treated with the selective serotonin reuptake inhibitor, fluoxetine

The following study set out to test the hypothesis that acute treatment with the selective serotonin reuptake inhibitor, fluoxetine, would result in a rise in circulating 5-HT levels and consequently a decrease in territorial aggression in the Gulf toadfish, Opsanus beta. Size-matched pairs of toadfish were implanted intraperitoneally with the same dose of fluoxetine (0, 10 or 25 μg g^− 1). After a social interaction between a pair of fish, circulating levels of serotonin (5-HT; 5-hydroxytryptamine) and cortisol were measured and relative mRNA expression of the 5-HT_1A receptor in the toadfish brain was determined using quantitative (real-time) PCR (qPCR). Behavioral endpoints such as the number of aggressive acts and swimming activity were also quantified so that dominant and subordinate fish could be identified. Fluoxetine treatment resulted in an increase in circulating levels of 5-HT, regardless of social status. Circulating cortisol concentrations were unaffected by fluoxetine, but were significantly higher in subordinate individuals when compared to dominant fish. Toadfish brain 5-HT_1A receptor mRNA expression was not affected by treatment or social status. Lastly and contrary to our predictions, fluoxetine treatment resulted in an increase in the number of aggressive acts made by dominant individuals, with no differences in the level of aggression or swimming activity of subordinate fish. This study is the first to describe elevated aggression in a teleost fish with elevated circulating levels of 5-HT.     

Juvenile hormone levels are increased in winners of cockroach fights

In lobster cockroach (Nauphoeta cinerea) adult males, concomitant expression of attack behavior and an increase in juvenile hormone (JH) III titer can be induced by contact with an isolated antenna [Chou et al., 2007. Antenna contact and agonism in the male lobster cockroach, Nauphoeta cinerea. Horm. Behav. 52, 252–260]. In the present study, socially naïve N. cinerea males that were either aggressive posture-adopting (i.e., “ready-for-fight”) or not (i.e., “non-ready-for-fight”) were paired to ask if status was determined by JH III levels before the encounter and if JH III levels were altered in dominants and subordinates after the encounter. The results showed that, although in the non-aggressive posture-adopting male pairs, the one with higher JH titers before the encounter was more likely to become the dominant, this was not the case in pairs formed between aggressive posture-adopting males or between non-aggressive posture-adopting and aggressive posture-adopting males. In all types of male pairs combined, JH III levels in the dominant were significantly increased after the encounter compared with before the encounter and were significantly higher than those in the subordinates, suggesting that the JH III increase in the dominants may serve to sustain aggression. JH III application before rank formation had a significant effect on establishment of dominant status in non-aggressive posture-adopting, but not aggressive posture-adopting, males. After rank formation, JH III application to subordinates had no effect on rank switch. These results indicate that the relationship between JH and aggression in this cockroach species is broadly consistent with the vertebrate challenge hypothesis, which predicts that testosterone levels increase in response to social stimuli to modulate aggression.     

Social Opportunity Rapidly Regulates Expression of CRF and CRF Receptors in the Brain during Social Ascent of a Teleost Fish,Astatotilapia burtoni

In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF₁ receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR₁ and CRFR₂ receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.     

The influence of social rank in the angelfish,Pterophyllum scalare,on locomotor and feeding activities in a novel environment

To investigate differences in behaviour associated with social rank and environmental conditions, a comparison was made between swimming and feeding activities of dominant and subordinate angelfish, housed in groups of six, with those of angelfish housed singly in identical laboratory aquaria. Subordinate individuals were less active, less ready to feed and consumed less food items than dominants, but their feeding and activity levels were still greater than those displayed by isolated fish used as controls. When fish from each of the above categories were transferred to a novel, identical tank to be tested individually for a 6-day period, little change was observed in previously isolated fish. In contrast, the previous social experience had a marked influence on the behaviour of the other individuals, the effects being related to the social status. The strongest initial response to the new environment was shown by subordinate individuals, with a significant increase in swimming and a significant decrease in feeding compared to the group situation. Subordinates were significantly more active than dominants, who in turn moved more than previously isolated fish. Dominants and subordinates were now similarly reluctant to feed, and their food consumption was less than that of previously isolated fish. With time in the novel environment a significant reduction of swimming activity and a recovery of feeding measures were detected, but levels were still depressed in relation to the group condition, and lower in subordinates than in dominants, indicating the long-lasting effects of the previous social interactions. The results have clear implications for laboratory studies using groups of fish in which social hierarchies may be established prior to individuals being tested singly in a novel environment.     

Social Status and Feeding in Atlantic Salmon Salmo salar Parr: The Effect of Visual Exposure to a Dominant

Groups of four Atlantic salmon parr were established and the dominant individual identified. Feeding responses were then observed in the remaining (subordinate) fish housed in one of three conditions: in the same compartment as the dominant fish (full exposure), separated from it by a transparent partition (visual exposure) or behind an opaque partition (isolated). Subordinate parr in the full exposure condition responded to and ate fewer food pellets than did the dominant fish. However, subordinate parr in the visual exposure condition and in the isolation condition fed actively, indicating that neither visual intimidation nor long-term stress-induced reduction of appetite were responsible for the reduced food intake of subordinate parr in direct contact with dominants. Dominant parr and subordinates in the visual exposure condition, but not subordinates in the exposed condition, moved further from their feeding station when attacking food items that were contested by a competitor compared with the distance moved for uncontested items. The presence of a competitor therefore forced both dominant and visually exposed subordinates to pay higher costs while foraging.     

Social status,behavior, and central serotonergic responsivity in female cynomolgus monkeys

The relationship between social status, behavioral characteristics, and central serotonergic function was examined in eight adult female cynomolgus monkeys (Macaca fascicularis). The subjects were housed in four-member social groups for 6 months. Social behavior was observed three times a week. The early follicular phase of the menstrual cycle was determined based on the occurrence of menses, and the prolactin response to acute administration of fenfluramine HCl during the early follicular phase was used as a measure of net brain serotonergic responsivity. Delta prolactin responses (the prolactin response to fenfluramine minus baseline concentrations) were lower in dominant than in subordinate females. Dominant females were more aggressive and less submissive than subordinates. Likewise, females with the lowest delta prolactin concentrations were more aggressive and less submissive than females that had relatively large increases in prolactin. Delta prolactin responses also correlated negatively with percent time eating and investigating in close proximity to penmates, and correlated positively with percent time scanning anxiously while alone. The same pattern of correlation was noted between social status and the aforementioned affiliative behaviors. It was concluded that high central serotonergic responsivity may be associated with low rates of aggression, high rates of submission, and subordinate social status in female cynomolgus monkeys. © 1995 Wiley-Liss, Inc.     

Surface feeding and aggressive behaviour of diploid and triploid brown trout Salmo trutta during allopatric pair‐wise matchings

Diploid and triploid brown trout Salmo trutta were acclimated for 6 weeks on two feeding regimes (floating and sinking). Thereafter, aggression and surface feeding response were compared between pairs of all diploid, all triploid and diploid and triploid S. trutta in an experimental stream. In each pair‐wise matching, fish of similar size were placed in allopatry and rank was determined by the total number of aggressive interactions recorded. Dominant individuals initiated more aggression than subordinates, spent more time defending a territory and positioned themselves closer to the surface food source (Gammarus pulex), whereas subordinates occupied the peripheries. In cross ploidy trials, diploid S. trutta were more aggressive than triploid, and dominated their sibling when placed in pair‐wise matchings. Surface feeding, however, did not differ statistically between ploidy irrespective of feeding regime. Triploids adopted a sneak feeding strategy while diploids expended more time defending a territory. In addition, we also tested whether triploids exhibit a similar social dominance to diploids when placed in allopatry. Although aggression was lower in triploid pairs than in the diploid and triploid pairs, a dominance hierarchy was also observed between individuals of the same ploidy. Dominant triploid fish were more aggressive and consumed more feed items than subordinate individuals. Subordinate fish displayed a darker colour index than dominant fish suggesting increased stress levels. Dominant triploid fish, however, appeared to be more tolerant of subordinate individuals and did not display the same degree of invasive aggression as seen in the diploid and diploid or diploid and triploid matchings. These novel findings suggest that sterile triploid S. trutta feed similarly but are less aggressive than diploid trout. Future studies should determine the habitat choice of triploid S. trutta after release and the interaction between wild fish and triploids during the breeding season prior to utilization of triploids as an alternative management strategy within freshwater fisheries.     

Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout Oncorhynchus mykiss

The effects of food ration and social context, as well as possible interactions, on the antipredator behaviour of juvenile rainbow trout Onchorhynchus mykiss were investigated in a pair of laboratory studies. In experiment 1, pairs of dominant and subordinate O. mykiss were exposed to conspecific alarm cues when maintained under high or low food rations. Under high food rations, dominant individuals responded to predation risk, whereas subordinates used the opportunity to feed. Under low food ration, however, the opposite pattern was observed, where subordinates responded to predation cues and dominants did not. Experiment 2 consisted of performing the same experiment, however separating the dominant and subordinate O. mykiss 3 h before testing. When tested separately, dominant and subordinate individuals did not differ in their responses to alarm cues, regardless of food ration. These results demonstrate that there is a complex interaction between current energy status and social context on decision making by prey animals.     

Effects of previous experience on the agonistic behaviour of male crickets, Gryllus bimaculatus

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