Social regulation of arginine vasopressin and oxytocin systems in a wild group-living fish.

The neuropeptides arginine vasopressin (AVP) and oxytocin (OXT) are key regulators of social behaviour across vertebrates. However, much of our understanding of how these neuropeptide systems interact with social behaviour is centred around laboratory studies which fail to capture the social and physiological challenges of living in the wild. To evaluate relationships between these neuropeptide systems and social behaviour in the wild, we studied social groups of the cichlid fish Neolamprologus pulcher in Lake Tanganyika, Africa. We first used SCUBA to observe the behaviour of focal group members and then measured transcript abundance of key components of the AVP and OXT systems across different brain regions. While AVP is often associated with male-typical behaviours, we found that dominant females had higher expression of avp and its receptor (avpr1a2) in the preoptic area of the brain compared to either dominant males or subordinates of either sex. Dominant females also generally had the highest levels of leucyl-cystinyl aminopeptidase (lnpep)-which inactivates AVP and OXT-throughout the brain, potentially indicating greater overall activity (i.e., production, release, and turnover) of the AVP system in dominant females. Expression of OXT and its receptors did not differ across social ranks. However, dominant males that visited the brood chamber more often had lower preoptic expression of OXT receptor a (oxtra) suggesting a negative relationship between OXT signalling and parental care in males of this species. Overall, these results advance our understanding of the relationships between complex social behaviours and neuroendocrine systems under natural settings.

Galanin expression varies with parental care and social status in a wild cooperatively breeding fish.

As many busy parents will attest, caring for young often comes at the expense of having time to feed and care for oneself. Galanin is a neuropeptide that regulates food intake and modulates parental care; however, the relative importance of galanin in the regulation of feeding versus caring by parents has never been evaluated before under naturalistic settings. Here, we assessed how expression of the galanin system varied in two brain regions, the hypothalamus (which regulates feeding) and the preoptic area (which modulates social behaviours including care) in a wild cichlid fish, Neolamprologus pulcher. Females with young had higher hypothalamic expression of galanin receptor 1a, and the highest expression of galanin and galanin receptor 1a was observed in females that foraged the least. However, expression of five other feeding-related neuropeptides did not change while females were caring for young suggesting that changes in the hypothalamic galanin system may not have been directly related to changes in food intake. The preoptic galanin system was unaffected by the presence of young, but preoptic galanin expression was higher in dominant females (which are aggressive, regularly reproduce and care for young) compared to subordinate females (which are submissive, rarely reproduce but often help care for young). Additionally, preoptic galanin expression was higher in fish that performed more territory defense. Overall, our results indicate that galanin has brain-region-specific roles in modulating both parental care and social status in wild animals.

Glucocorticoids do not promote prosociality in a wild group-living fish.

Individuals often respond to social disturbances by increasing prosociality, which can strengthen social bonds, buffer against stress, and promote overall group cohesion. Given their importance in mediating stress responses, glucocorticoids have received considerable attention as potential proximate regulators of prosocial behaviour during disturbances. However, previous investigations have largely focused on mammals and our understanding of the potential prosocial effects of glucocorticoids across vertebrates more broadly is still lacking. Here, we assessed whether experimentally elevated glucocorticoid levels (simulating endogenous cortisol responses mounted following disturbances) promote prosocial behaviours in wild groups of the cichlid fish, Neolamprologus pulcher. Using SCUBA in Lake Tanganyika, we observed how subordinate group members adjusted affiliation, helping, and submission (all forms of prosocial behaviour) following underwater injections of either cortisol or saline. Cortisol treatment reduced affiliative behaviours-but only in females-suggesting that glucocorticoids may reduce overall prosociality. Fish with elevated glucocorticoid levels did not increase performance of submission or helping behaviours. Taken together, our results do not support a role for glucocorticoids in promoting prosocial behaviour in this species and emphasize the complexity of the proximate mechanisms that underlie prosociality.

Rank- and sex-specific differences in the neuroendocrine regulation of glucocorticoids in a wild group-living fish.

Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glucocorticoid dynamics in wild groups are poorly understood, making it difficult to determine the functional consequences of differences in glucocorticoid levels. Therefore, we observed wild social groups of a cooperatively breeding fish (Neolamprologus pulcher) and evaluated how scale cortisol content (an emerging method to evaluate cortisol dynamics in fishes) and expression of glucocorticoid-related genes varied across group members. Scale cortisol was detectable in ~50% of dominant males (7/17) and females (7/15)-but not in any subordinates (0/16)-suggesting that glucocorticoid levels were higher in dominants. However, the apparent behavioural and neuroendocrine factors regulating cortisol levels varied between dominant sexes. In dominant females, higher cortisol was associated with greater rates of territory defense and increased expression of corticotropin-releasing factor in the preoptic and hypothalamic regions of the brain, but these patterns were not observed in dominant males. Additionally, transcriptional differences in the liver suggest that dominant sexes may use different mechanisms to cope with elevated cortisol levels. While dominant females appeared to reduce the relative sensitivity of their liver to cortisol (fewer corticosteroid receptor transcripts), dominant males appeared to increase hepatic cortisol breakdown (more catabolic enzyme transcripts). Overall, our results offer valuable insights on the mechanisms regulating rank- and sex-based glucocorticoid dynamics, as well as the potential functional outcomes of these differences.

Understanding fish cognition: a review and appraisal of current practices.

With over 30,000 recognized species, fishes exhibit an extraordinary variety of morphological, behavioural, and life-history traits. The field of fish cognition has grown markedly with numerous studies on fish spatial navigation, numeracy, learning, decision-making, and even theory of mind. However, most cognitive research on fishes takes place in a highly controlled laboratory environment and it can therefore be difficult to determine whether findings generalize to the ecology of wild fishes. Here, we summarize four prominent research areas in fish cognition, highlighting some of the recent advances and key findings. Next, we survey the literature, targeting these four areas, and quantify the nearly ubiquitous use of captive-bred individuals and a heavy reliance on lab-based research. We then discuss common practices that occur prior to experimentation and within experiments that could hinder our ability to make more general conclusions about fish cognition, and suggest possible solutions. By complementing ecologically relevant laboratory-based studies with in situ cognitive tests, we will gain further inroads toward unraveling how fishes learn and make decisions about food, mates, and territories.

Colorful facial markings are associated with foraging rates and affiliative relationships in a wild group-living cichlid fish.

Many animals use color to signal their quality and/or behavioral motivations. Colorful signals have been well studied in the contexts of competition and mate choice; however, the role of these signals in nonsexual, affiliative relationships is not as well understood. Here, we used wild social groups of the cichlid fish Neolamprologus pulcher to investigate whether the size of a brightly colored facial patch was related to 1) individual quality, 2) social dominance, and/or 3) affiliative relationships. Individuals with larger patches spent more time foraging and tended to perform more aggressive acts against conspecific territory intruders. We did not find any evidence that the size of these yellow patches was related to social rank or body size, but dominant males tended to have larger patches than dominant females. Additionally, patch size had a rank-specific relationship with the number of affiliative interactions that individuals engaged in. Dominant males with large patches received fewer affiliative acts from their groupmates compared to dominant males with small patches. However, subordinates with large patches tended to receive more affiliative acts from their groupmates while performing fewer affiliative acts themselves. Taken together, our results suggest that patch size reflects interindividual variation in foraging effort in this cichlid fish and offer some of the first evidence that colorful signals may shape affiliative relationships within wild social groups.

Rapid spatial learning in cooperative and non-cooperative cichlids.

The number, duration and depth of social relationships that an individual maintains can impact social cognition, but the connection between sociality and other aspects of cognition has hardly been explored. To date, the link between social living and intelligence has been mainly supported by studies on primates, and far fewer tests connecting sociality to cognitive abilities have used other taxa. Here, we present the first comparative study in fishes that examines whether complex social living is associated with better performance on a cognitively demanding spatial task. Using three cooperative, group-living cichlid fish species and three of their non-cooperative, more solitary close relatives, we studied maze learning and employed a new statistical extension for the 'lme4' and 'glmmTMB' packages in R that allows phylogeny to be included as a random effect term. Across trials, the three cooperative and the three non-cooperative species completed the maze faster, made fewer mistakes, and improved their inhibitory control. Although fish improved their performance, we did not detect any differences in the extent of improvement between cooperative and non-cooperative species. Both the cooperative species and the non-cooperative species took similar amounts of time to complete the maze, had comparable numbers of mistakes, and exhibited similar inhibitory control while in the maze. Our results suggest that living and breeding in complex social groups does not necessarily imply enhancement of other forms of cognition nor, more specifically, an enhanced spatial learning capacity.

Municipal wastewater as an ecological trap: Effects on fish communities across seasons.

Municipal wastewater treatment plant (WWTP) effluents are a ubiquitous source of contamination whose impacts on fish and other aquatic organisms span across multiple levels of biological organization. Despite this, few studies have addressed the impacts of WWTP effluents on fish communities, especially during the winter-a season seldom studied. Here, we assessed the impacts of wastewater on fish community compositions and various water quality parameters during the summer and winter along two effluent gradients in Hamilton Harbour, an International Joint Commission Area of Concern in Hamilton, Canada. We found that fish abundance, species richness, and species diversity were generally highest in sites closest to the WWTP outfalls, but only significantly so in the winter. Fish community compositions differed greatly along the effluent gradients, with sites closest and farthest from the outfalls being the most dissimilar. Furthermore, the concentrations of numerous contaminants of emerging concern (CECs) in the final treated effluent were highest during the winter. Water quality of sites closer to the outfalls was poorer than at sites farther away, especially during the winter. We also demonstrated that WWTPs can significantly alter the thermal profile of effluent-receiving environments, increasing temperature by as much as ~9 °C during the winter. Our results suggest that wastewater plumes may act as ecological traps in winter, whereby fish are attracted to the favourable temperatures near WWTPs and are thus exposed to higher concentrations of CECs. This study highlights the importance of winter research as a key predictor in further understanding the impacts of wastewater contamination in aquatic ecosystems.

Social memory and quantity discrimination: A cross cichlid species comparison.

Cooperation is a highly complex social interaction that often requires coordination and communication between two individuals. Reciprocity is one explanation for how cooperation evolves and is maintained; help now will eventually be repaid in kind. For reciprocity to work, individuals must be able to differentiate between those who helped previously versus those who cheated. However, there is little empirical evidence that cooperative species have an enhanced recognition capacity compared to noncooperative species. Here we conducted a comparative study to address this question using three cooperatively breeding cichlids and three of their close relatives that are not cooperative breeders, all from Lake Tanganyika. In a first experiment, we offered fish a choice between spending time with a familiar versus an unfamiliar conspecific and found that while cooperative cichlids spent more time with familiar individuals, the noncooperative cichlids spent more time with unfamiliar individuals. In a second experiment, we provided a choice between affiliating with one versus three individuals (all unfamiliar) and found that 2/3 cooperative and 3/3 noncooperative cichlids strongly preferred to affiliate with larger groups. Our results suggest that both cooperative and noncooperative cichlids have evolved the ability to recognise familiar individuals and have affiliative preferences; however, the nature of these preferences differ. (PsycInfo Database Record (c) 2020 APA, all rights reserved).