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.

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.

Delayed recovery and host specialization may spell disaster for coral-fish mutualism.

Mutualisms are prevalent in many ecosystems, yet little is known about how symbioses are affected by ecological pressures. Here, we show delayed recovery for 13 coral-dwelling goby fishes (genus Gobiodon) compared with their host Acropora corals following four consecutive cyclones and heatwaves. While corals became twice as abundant in 3 years postdisturbances, gobies were only half as abundant relative to predisturbances and half of the goby species disappeared. Although gobies primarily occupied one coral species in greater abundance predisturbances, surviving goby species shifted hosts to newly abundant coral species when their previously occupied hosts became rare postdisturbances. As host specialization is key for goby fitness, shifting hosts may have negative fitness consequences for gobies and corals alike and affect their survival in response to environmental changes. Our study is an early sign that mutualistic partners may not recover similarly from multiple disturbances, and that goby host plasticity, while potentially detrimental, may be the only possibility for early recovery.

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.

Further Insights into Invasion: Field Observations of Behavioural Interactions between an Invasive and Critically Endangered Freshwater Crayfish Using Baited Remote Underwater Video (BRUV).

Competitive behavioural interactions between invasive and native freshwater crayfish are recognised as a key underlying mechanism behind the displacement of natives by invaders. However, in situ investigations into behavioural interactions between invasive and native crayfish are scarce. In Australian freshwater systems, the invasive Cherax destructor has spread into the ranges of many native Euastacus species, including the critically endangered Euastacus dharawalus. Staged contests between the two species in a laboratory setting found E. dharawalus to be the dominant competitor, however, this has yet to be corroborated in situ. Here, we used baited remote underwater video (BRUV) to examine in situ intra- and inter-specific behavioural interactions between E. dharawalus and C. destructor. We sought to evaluate patterns of dominance and differential contest dynamics between the species to provide indications of competition between the two species. We found E. dharawalus to be dominant over C. destructor based on pooled interspecific interaction data and size-grouped interactions where C. destructor was the smaller opponent. Alarmingly, however, when C. destructor was within a 10% size difference the dominance of E. dharawalus was lost, contrasting with the outcomes of the laboratory-staged study. In addition, we report that small C. destructor initiated significantly more contests than larger conspecifics and larger E. dharawalus, a pattern that was not observed in smaller E. dharawalus. Further, intraspecific interactions between C. destructor were significantly longer in duration than intraspecific interactions between E. dharawalus, indicating a willingness to continue fighting. Concerningly, these outcomes point towards inherent and greater aggressiveness in C. destructor relative to E. dharawalus and that only larger E. dharawalus hold a competitive advantage over C. destructor. Therefore, we conclude that C. destructor represents a substantial threat to E. dharawalus through competitive behavioural interactions. Further, due to the disparity between our findings and those produced from laboratory-staged contests, we recommend the use of in situ studies when determining the behavioural impacts of invasive crayfish on natives.

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.

Uneven declines between corals and cryptobenthic fish symbionts from multiple disturbances.

With the onset and increasing frequency of multiple disturbances, the recovery potential of critical ecosystem-building species and their mutual symbionts is threatened. Similar effects to both hosts and their symbionts following disturbances have been assumed. However, we report unequal declines between hosts and symbionts throughout multiple climate-driven disturbances in reef-building Acropora corals and cryptobenthic coral-dwelling Gobiodon gobies. Communities were surveyed before and after consecutive cyclones (2014, 2015) and heatwaves (2016, 2017). After cyclones, coral diameter and goby group size (i.e., the number of gobies within each coral) decreased similarly by 28-30%. After heatwave-induced bleaching, coral diameter decreased substantially (47%) and gobies mostly inhabited corals singly. Despite several coral species persisting after bleaching, all goby species declined, leaving 78% of corals uninhabited. These findings suggest that gobies, which are important mutual symbionts for corals, are unable to cope with consecutive disturbances. This disproportionate decline could lead to ecosystem-level disruptions through loss of key symbiont services to corals.

Behavioural plasticity in a native species may be related to foraging resilience in the presence of an aggressive invader.

Competition between invasive and native species can result in the exploitation of resources by the invader, reducing foraging rates of natives. However, it is increasingly recognized that multiple factors can enhance the resilience of native species competing for limiting resources with invaders. Although extensively studied in terrestrial species, little research has focused on behavioural plasticity in aquatic ecosystems and how this influences native species resilience. Here, we examined the role of behavioural plasticity in interactions between a native Australian fish, Pseudomugil signifer, and a widespread invasive fish, Gambusia holbrooki. To determine whether P. signifer displays behavioural plasticity that may mitigate competition with G. holbrooki, we first quantified social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups. Second, we compared the feeding rates of both species in these groups to ascertain if any modulation of social behaviours and cohesion related to foraging success. We found that aggressive and submissive behaviours of G. holbrooki and P. signifer showed plasticity in the presence of heterospecifics, but social affiliation, shoaling and, most importantly, foraging, remained inflexible. This variation in the degree of plasticity highlights the complexity of the behavioural response of a native species and suggests that both behavioural modulation and consistency may be related to sustaining foraging efficiency in the presence of an invader.

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.

Predation avoidance and foraging efficiency contribute to mixed-species shoaling by tropical and temperate fishes.

The formation of mixed-species social groups, whereby heterospecifics form and maintain either transient or stable groups with each other, can confer substantial fitness benefits to individuals. Such benefits may arise via multiple mechanisms associated with both predation avoidance and foraging efficiency. In fishes, mixed-species shoaling reportedly occurs where displaced tropical species (known as "vagrants") interact with resident temperate species, although little is known about the nature and frequency of such interactions. To investigate this phenomenon, we used displaced tropical Indo-pacific Sergeant Abudefduf vaigiensis settling in temperate south-eastern Australia as a model system. Underwater visual surveys revealed shoal composition and size differed significantly between open-water and reef habitats, with shoals in open habitats being larger and more speciose. Shoals containing A. vaigiensis were mainly mixed-species, and larger and more speciose in open habitats than nearer to reef. Since both foraging efficiency (via access to plankton) and predation threat likely increase with increasing distance from reef habitat, we suggest that mixed-species shoaling mitigates predation risk whilst allowing increased foraging opportunities for A. vaigiensis in open areas. These findings provide support for the importance of mixed-species shoaling to the persistence of tropical reef fishes in temperate regions.

Elevated CO2 and food ration affect growth but not the size-based hierarchy of a reef fish.

Under projected levels of ocean acidification, shifts in energetic demands and food availability could interact to effect the growth and development of marine organisms. Changes to individual growth rates could then flow on to influence emergent properties of social groups, particularly in species that form size-based hierarchies. To test the potential interactive effects of (1) food availability, (2) elevated CO2 during juvenile development, and (3) parental experience of elevated CO2 on the growth, condition and size-based hierarchy of juvenile fish, we reared orange clownfish (Amphiprion percula) for 50 days post-hatching in a fully orthogonal design. Development in elevated CO2 reduced standard length and weight of juveniles, by 9% and 11% respectively, compared to ambient. Development under low food availability reduced length and weight of juveniles by 7% and 15% respectively, compared to high food. Parental exposure to elevated CO2 restored the length of juveniles to that of controls, but it did not restore weight, resulting in juveniles from elevated CO2 parents exhibiting 33% lower body condition when reared in elevated CO2. The body size ratios (relative size of a fish from the rank above) within juvenile groups were not affected by any treatment, suggesting relative robustness of group-level structure despite alterations in individual size and condition. This study demonstrates that both food availability and elevated CO2 can influence the physical attributes of juvenile reef fish, but these changes may not disrupt the emergent group structure of this social species, at least amongst juveniles.

Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history.

What drives the evolution of sociality in animals? Many robust studies in terrestrial organisms have pointed toward various kinship-based, ecological and life-history traits or phylogenetic constraint which have played a role in the evolution of sociality. These traits are not mutually exclusive and the exact combination of traits is likely taxon-specific. Phylogenetic comparative analyses have been instrumental in identifying social lineages and comparing various traits with non-social lineages to give broad evolutionary perspectives on the development of sociality. Few studies have attempted this approach in marine vertebrate systems. Social marine fishes are particularly interesting because many have a pelagic larval phase and non-conventional life-history strategies (e.g. bi-directional sex-change) not often observed in terrestrial animals. Such strategies provide novel insights into terrestrially-derived theories of social evolution. Here, we assess the strength of the phylogenetic signal of sociality in the Gobiodon genus with Pagel's lambda and Blomberg's K parameters. We found some evidence of a phylogenetic signal of sociality, but factors other than phylogenetic constraint also have a strong influence on the extant social state of each species. We then use phylogenetic generalized least squares analyses to examine several ecological and life-history traits that may have influenced the evolution of sociality in the genus. We found an interaction of habitat size and fish length was the strongest predictor of sociality. Sociality in larger species was more dependent on coral size than in smaller species, but smaller species were more social overall, regardless of coral size. Finally, we comment on findings regarding the validity of the species G. spilophthalmus which arose during the course of our research. These findings in a group of marine fishes add a unique perspective on the evolution of sociality to the excellent terrestrial work conducted in this field.

Comparison of efficiency of direct observations by scuba diver and indirect observations via video camera for measuring reef-fish behaviour.

The present study investigates how the humbug damselfish Dascyllus aruanus, subject of a large number of ecological, evolutionary and behavioural studies, responds to the presence of human observers (effect of scuba diver presence-absence) and how the method of data collection (directly by a scuba diver v. indirectly via video camera) may affect the quality of behavioural data. Scuba diver presence had only subtle effects on fish behaviour. The efficiency of the method of scoring fish behaviour depended on the behaviour under consideration: those behaviours that occur in close proximity to the corals were scored more effectively directly by a scuba diver while those that are performed in a more rapid or repetitive fashion were scored more effectively indirectly via video camera. These results provide a foundation for future behavioural research on D. aruanus and other fishes where scuba divers or video cameras are the prevalent means of data collection.

Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes.

Social organization is a key factor influencing a species' foraging and reproduction, which may ultimately affect their survival and ability to recover from catastrophic disturbance. Severe weather events such as cyclones can have devastating impacts to the physical structure of coral reefs and on the abundance and distribution of its faunal communities. Despite the importance of social organization to a species' survival, relatively little is known about how major disturbances such as tropical cyclones may affect social structures or how different social strategies affect a species' ability to cope with disturbance. We sampled group sizes and coral sizes of group-forming and pair-forming species of the Gobiid genus Gobiodon at Lizard Island, Great Barrier Reef, Australia, before and after two successive category 4 tropical cyclones. Group sizes of group-forming species decreased after each cyclone, but showed signs of recovery four months after the first cyclone. A similar increase in group sizes was not evident in group-forming species after the second cyclone. There was no change in mean pair-forming group size after either cyclone. Coral sizes inhabited by both group- and pair-forming species decreased throughout the study, meaning that group-forming species were forced to occupy smaller corals on average than before cyclone activity. This may reduce their capacity to maintain larger group sizes through multiple processes. We discuss these patterns in light of two non-exclusive hypotheses regarding the drivers of sociality in Gobiodon, suggesting that benefits of philopatry with regards to habitat quality may underpin the formation of social groups in this genus.

Social motivation and conflict resolution tactics as potential building blocks of sociality in cichlid fishes.

Even closely related and ecologically similar cichlid species of Lake Tanganyika exhibit an impressive diversity of social systems, and therefore these fishes offer an excellent opportunity to examine the evolution of social behaviour. Sophisticated social relationships are thought to have evolved via a building block design where more fundamental social behaviours and cognitive processes have been combined, incrementally modified, and elaborated over time. Here, we studied two of these putative social building blocks in two closely related species of cichlids: Neolamprologus pulcher, a group-living species, and Telmatochromis temporalis, a non-grouping species. Otherwise well matched in ecology, this pair of species provide an excellent comparison point to understand how behavioural processes may have been modified in relation to the evolution of sociality. Using social assays in both the laboratory and in the field, we explored each species' motivation to interact with conspecifics, and each species' conflict resolution tactics. We found that individuals of the group living species, N. pulcher, displayed higher social motivation and were more likely to produce submission displays than were individuals of the non-grouping species, T. temporalis. We argue that the motivation to interact with conspecifics is a necessary prerequisite for the emergence of group living, and that the use of submission reduces the costs of conflict and facilitates the maintenance of close social proximity. These results suggest that social motivation and conflict resolution tactics are associated with social complexity, and that these behavioural traits may be functionally significant in the evolution and maintenance of sociality.

Developmental exposure of zebrafish (Danio rerio) to bisphenol-S impairs subsequent reproduction potential and hormonal balance in adults.

In the recent years, there has been a growing concern about the production and use of bisphenol-A substitute, namely bisphenol-S (BPS). Due to its novel nature, there have been few studies addressing the ability of BPS to disrupt the endocrine system of animals. In the present study, zebrafish (Danio rerio) embryos were exposed to and reared in various concentrations of BPS (0, 0.1, 1, 10 and 100 µg/l) for 75 days. Then adult males and females were paired in spawning tanks for 7 days in clean water and the consequent effects on fish development, reproduction, plasma vitellogenin (VTG), sex steroids and thyroid hormone levels were investigated as endpoints. After 75 days of exposure, there was a skewed sex ratio in favor of females. The results also showed that body length and weight significantly decreased in males exposed to 100 µg/l of BPS. Gonadosomatic index was significantly reduced in fish at ≥ 10 µg/l. Hepatosomatic index exhibited a significant increase in both male and female fish. At ≥ 1 µg/l of BPS, plasma 17ß-estradiol levels were significantly increased in both males and females. However, plasma testosterone showed a significant reduction in males exposed to 10 and 100 µg/l of BPS. A significant induction in plasma VTG level was observed in both males and females at ≥ 10 µg/l of BPS. Plasma thyroxine and triiodothyronine levels were significantly decreased at 10 and 100 µg/l of BPS in males, and at 100 µg/l in females. Egg production and sperm count were also significantly decreased in groups received 10 and 100 µg/l of BPS. Moreover, once time to hatching and hatching rates were calculated for fertilized eggs the postponed and decreased rates of hatching were observed. Taken together, these results suggest that developmental exposure to low concentrations of BPS has adverse effects on different parts of the endocrine system in zebrafish.

Ecological constraints and benefits of philopatry promote group-living in a social but non-cooperatively breeding fish.

Why non-breeding subordinates of many animal societies tolerate group-living remains a pertinent question in evolutionary biology. The ecological constraints and benefits of philopatry hypotheses have the potential to explain the maintenance of group-living by specifying the ecological conditions favouring delayed dispersal over independent breeding by subordinates. In this study, I used field and laboratory experiments to investigate the role of ecological and social factors on the dispersal decisions of non-breeding subordinates in the coral-dwelling fish, Paragobiodon xanthosomus (Gobiidae). Subordinate dispersal was strongly influenced by ecological constraints (habitat saturation and risks of movement) and benefits of philopatry (relative coral size). Social factors, namely social rank and forcible eviction, did not affect the occurrence of subordinate dispersal. These results suggest that selection has favoured subordinate P. xanthosomus, which employ a mixed strategy-switching tactics in response to three ecological factors-despite having low mobility and extreme habitat-specific requirements. Furthermore, this study demonstrates the generality of the ecological constraints and benefits of philopatry hypotheses as explanations for group-living in species where subordinates are unrelated to breeders, provide no help and do not strictly delay dispersal.

The effects of familiarity and social hierarchy on group membership decisions in a social fish.

Members of animal groups face a trade-off between the benefits of remaining with a familiar group and the potential benefits of dispersing into a new group. Here, we examined the group membership decisions of Neolamprologus pulcher, a group-living cichlid. We found that subordinate helpers showed a preference for joining familiar groups, but when choosing between two unfamiliar groups, helpers did not preferentially join groups that maximized their social rank. Rather, helpers preferred groups containing larger, more dominant individuals, despite receiving significantly more aggression within these groups, possibly owing to increased protection from predation in such groups. These results suggest a complex decision process in N. pulcher when choosing among groups, dependent not only on familiarity but also on the social and life-history consequences of joining new groups.

Genetic relatedness in groups of the humbug damselfish Dascyllus aruanus: small, similar-sized individuals may be close kin.

Kin selection plays an important role in the evolution of social behaviour in terrestrial systems. The extent to which kin selection influences the evolution of social behaviour in marine systems is largely unexplored. Generally, it is considered that kin selection is irrelevant in marine systems, because it is assumed that the dispersing larval phase of marine organisms will break up kin associations. Here, we challenge this assumption and investigate the opportunity for kin selection in a coral reef fish: the humbug damselfish Dascyllus aruanus. This fish lives in groups composed of a large male and a number of smaller females and nonbreeders. We use 10 polymorphic microsatellite loci to assess the relatedness of 265 individuals from 35 groups. The mean coefficient of relatedness among group members is 0.01 +/- 0.04, suggesting that individuals are not associated with close relatives. However, the distribution of pairwise relatedness of individuals within groups has an overabundance of positive values, and indicates that there might be 35 pairs of close relatives within groups. Further analyses reveal that close relatives likely are similar in size and small in size, suggesting that they might have recruited together. We conclude that it is possible for kin selection to operate in D. aruanus, but kin recognition will be a prerequisite for such selection. This study reveals that individuals can be associated with close relatives, and there is a hidden potential for kin selection, during certain parts of the life cycle of coral reef fishes.