Nutraceutical supplementation increases mobility in aged captive non-domesticated felids.

BACKGROUND: Musculoskeletal diseases (MSDs) are an increasing issue as the lifespan of captive animals increases. Extracts of green-lipped mussels have been linked to alleviation of MSDs in domestic carnivores. Understanding their efficacy in non-domestic felids could provide another tool to improve the welfare of aged individuals in collections. METHODS: A within-subject study design quantified steps per minute in each of 18 cats of 13 species before and after the addition of a nutraceutical containing green-lipped mussel extract (Antinol) to their diets. The age structure of four commonly kept subspecies of non-domestic cats was quantified to provide a demographic context to the need for managing aged individuals. RESULTS: Each of the 18 cats exhibited a higher number of steps per minute after the addition of Antinol to their diet. At the group level, a paired t-test showed that the step rate was significantly increased after the addition of Antinol to the diet. LIMITATIONS: While our results showed a strong significant increase in step rate following Antinol supplementation, further studies that incorporate a placebo, more individuals and more detailed metrics of mobility would provide a more detailed evidence base for practitioners. CONCLUSION: Nutraceuticals may yield benefits to aged individual felids, including species kept widely in European collections. Their use warrants further, detailed research in collections.

Heart and brain: Change in cardiac entropy is related to lateralised visual inspection in horses.

Cerebral lateralisation is the tendency for an individual to preferentially use one side of their brain and is apparent in the biased use of paired sensory organs. Horses vary in eye use when viewing a novel stimulus which may be due to different physiological reactions. To understand the interplay between physiology and lateralisation, we presented a novel object (an inflated balloon) to 20 horses while electrocardiogram traces were collected. We measured the amount of time each horse looked at the balloon with each eye. We calculated 'sample entropy' as a measure of non-linear heart rate variability both prior to and during the stimulus presentation. A smaller drop in sample entropy values between the habituation phase and the sample presentation indicates the maintenance of a more complex signal associated with a relaxed physiological state. Horses that spent longer viewing the balloon with their left eye had a greater reduction in sample entropy, while time spend looking with the right eye was unrelated to the change in sample entropy. Therefore, the horses that exhibited a greater reduction in sample entropy tended to use their right hemisphere more, which may take precedence in emotional reactions. These results may help to explain the variation in lateralisation observed among horses.

Fellowship of the fin: Fish empathy and oxytocin.

Zebrafish exhibit fear contagion, a basic form of empathy, and when observing social fellows that have been exposed to predation cues, will themselves exhibit similar distress behaviours. As in mammals, the nonapeptide hormone oxytocin is essential for this empathic response, and homologous areas of the brain are involved, suggesting that the mechanistic basis of empathy may be conserved among vertebrates.

Horses show individual level lateralisation when inspecting an unfamiliar and unexpected stimulus.

Animals must attend to a diverse array of stimuli in their environments. The emotional valence and salience of a stimulus can affect how this information is processed in the brain. Many species preferentially attend to negatively valent stimuli using the sensory organs on the left side of their body and hence the right hemisphere of their brain. Here, we investigated the lateralisation of visual attention to the rapid appearance of a stimulus (an inflated balloon) designed to induce an avoidance reaction and a negatively valent emotional state in 77 Italian saddle horses. Horses' eyes are laterally positioned on the head, and each eye projects primarily to the contralateral hemisphere, allowing eye use to be a proxy for preferential processing in one hemisphere of the brain. We predicted that horses would inspect the novel and unexpected stimulus with their left eye and hence right hemisphere. We found that horses primarily inspected the balloon with one eye, and most horses had a preferred eye to do so, however, we did not find a population level tendency for this to be the left or the right eye. The strength of this preference tended to decrease over time, with the horses using their non-preferred eye to inspect the balloon increasingly as the trial progressed. Our results confirm a lateralised eye use tendency when viewing negatively emotionally valent stimuli in horses, in agreement with previous findings. However, there was not any alignment of lateralisation at the group level in our sample, suggesting that the expression of lateralisation in horses depends on the sample population and testing context.

Head up displays are a submission signal in the group-living daffodil cichlid.

Dominance hierarchies can reduce conflict within social groups and agonistic signals can help to establish and maintain these hierarchies. Behaviours produced by subordinates in response to aggression are often assumed to function as signals of submission, however, these behaviours may serve other purposes, for example, defence or escape. For a behaviour to act as a submission signal, the receiver must respond by reducing their likelihood of further aggression towards the signaller. In the current study, we examine the receiver response to a putative signal of submission, the head up display, within established social groups of the cooperatively breeding fish, the daffodil cichlid (Neolamprologus pulcher). We found that when subordinate signallers produce the head up display in response to aggression from the breeder male, he exhibited a longer latency to behave aggressively towards that individual again. We also report that head up displays are rarely produced without being elicited by aggression, and the number of head up displays correlates with the amount of aggression received. Our results demonstrate that the head up display is used as a signal of submission in the daffodil cichlid and provide insight into intragroup communication in an emerging model system for the study of social behaviour.

Consistency and flexibility in solving spatial tasks: different horses show different cognitive styles.

Individual animals vary in their behaviour and reactions to novel situations. These differences may extend to differences in cognition among individuals. We tested twenty-six horses for their ability to detour around symmetric and asymmetric obstacles. All of the animals were able to get around the barrier to reach a food target, but varied in their approach. Some horses moved slowly but were more accurate in choosing the shortest way. Other horses acted quickly, consistently detoured in the same direction, and did not reliably choose the shortest way. The remaining horses shifted from a faster, directionally consistent response with the symmetric barrier, to a slower but more accurate response with the asymmetric barrier. The asymmetric barrier induced a reduction in heart rate variability, suggesting that this is a more demanding task. The different approaches used to solve the asymmetric task may reflect distinct cognitive styles in horses, which vary among individuals, and could be linked to different personality traits. Understanding equine behaviour and cognition can inform horse welfare and management.

Isotocin neuronal phenotypes differ among social systems in cichlid fishes.

Social living has evolved numerous times across a diverse array of animal taxa. An open question is how the transition to a social lifestyle has shaped, and been shaped by, the underlying neurohormonal machinery of social behaviour. The nonapeptide neurohormones, implicated in the regulation of social behaviours, are prime candidates for the neuroendocrine substrates of social evolution. Here, we examined the brains of eight cichlid fish species with divergent social systems, comparing the number and size of preoptic neurons that express the nonapeptides isotocin and vasotocin. While controlling for the influence of phylogeny and body size, we found that the highly social cooperatively breeding species (n = 4) had fewer parvocellular isotocin neurons than the less social independently breeding species (n = 4), suggesting that the evolutionary transition to group living and cooperative breeding was associated with a reduction in the number of these neurons. In a complementary analysis, we found that the size and number of isotocin neurons significantly differentiated the cooperatively breeding from the independently breeding species. Our results suggest that isotocin is related to sociality in cichlids and may provide a mechanistic substrate for the evolution of sociality.

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.

Within-group relatedness is correlated with colony-level social structure and reproductive sharing in a social fish.

In group-living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within-group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group-living cichlid fish. We used restriction site-associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony-level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same-sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within-group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.

Social cichlid fish change behaviour in response to a visual predator stimulus, but not the odour of damaged conspecifics.

Predation is one of the primary drivers of fitness for prey species. Therefore, there should be strong selection for accurate assessment of predation risk, and whenever possible, individuals should use all available information to fine-tune their response to the current threat of predation. Here, we used a controlled laboratory experiment to assess the responses of individual Neolamprologus pulcher, a social cichlid fish, to a live predator stimulus, to the odour of damaged conspecifics, or to both indicators of predation risk combined. We found that fish in the presence of the visual predator stimulus showed typical antipredator behaviour. Namely, these fish decreased activity and exploration, spent more time seeking shelter, and more time near conspecifics. Surprisingly, there was no effect of the chemical cue alone, and fish showed a reduced response to the combination of the visual predator stimulus and the odour of damaged conspecifics relative to the visual predator stimulus alone. These results demonstrate that N. pulcher adjust their anti-predator behaviour to the information available about current predation risk, and we suggest a possible role for the use of social information in the assessment of predation risk in a cooperatively breeding fish.

Demasculinization of male guppies increases resistance to a common and harmful ectoparasite.

Parasites are detrimental to host fitness and therefore should strongly select for host defence mechanisms. Yet, hosts vary considerably in their observed parasite loads. One notable source of inter-individual variation in parasitism is host sex. Such variation could be caused by the immunomodulatory effects of gonadal steroids. Here we assess the influence of gonadal steroids on the ability of guppies (Poecilia reticulata) to defend themselves against a common and deleterious parasite (Gyrodactylus turnbulli). Adult male guppies underwent 31 days of artificial demasculinization with the androgen receptor-antagonist flutamide, or feminization with a combination of flutamide and the synthetic oestrogen 17 ß-estradiol, and their parasite loads were compared over time to untreated males and females. Both demasculinized and feminized male guppies had lower G. turnbulli loads than the untreated males and females, but this effect appeared to be mainly the result of demasculinization, with feminization having no additional measurable effect. Furthermore, demasculinized males, feminized males and untreated females all suffered lower Gyrodactylus-induced mortality than untreated males. Together, these results suggest that androgens reduce the ability of guppies to control parasite loads, and modulate resistance to and survival from infection. We discuss the relevance of these findings for understanding constraints on the evolution of resistance in guppies and other vertebrates.

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish.

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group(e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge,the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.

Brain nonapeptide levels are related to social status and affiliative behaviour in a cooperatively breeding cichlid fish.

The mammalian nonapeptide hormones, vasopressin and oxytocin, are known to be potent regulators of social behaviour. Teleost fishes possess vasopressin and oxytocin homologues known as arginine vasotocin (AVT) and isotocin (IT), respectively. The role of these homologous nonapeptides in mediating social behaviour in fishes has received far less attention. The extraordinarily large number of teleost fish species and the impressive diversity of their social systems provide us with a rich test bed for investigating the role of nonapeptides in regulating social behaviour. Existing studies, mostly focused on AVT, have revealed relationships between the nonapeptides, and both social behaviour and dominance status in fishes. To date, much of the work on endogenous nonapeptides in fish brains has measured genomic or neuroanatomical proxies of nonapeptide production rather than the levels of these molecules in the brain. In this study, we measure biologically available AVT and IT levels in the brains of Neolamprologus pulcher, a cooperatively breeding cichlid fish, using high performance liquid chromatography with fluorescence detection. We found that brain AVT levels were higher in the subordinate than in dominant animals, and levels of IT correlated negatively with the expression of affiliative behaviour. We contrast these results with previous studies, and we discuss the role the nonapeptide hormones may play in the regulation of social behaviour in this highly social animal.

A comparative study of an innate immune response in Lamprologine cichlid fishes.

Social interactions facilitate pathogen transmission and increase virulence. Therefore, species that live in social groups are predicted to suffer a higher pathogen burden, to invest more heavily in immune defence against pathogens, or both. However, there are few empirical tests of whether social species indeed invest more heavily in immune defence than non-social species. In the current study, we conducted a phylogenetically controlled comparison of innate immune response in Lamprologine cichlid fishes. We focused on three species of highly social cichlids that live in permanent groups and exhibit cooperative breeding (Julidochromis ornatus, Neolamprologus pulcher and Neolamprologus savoryi) and three species of non-social cichlids that exhibit neither grouping nor cooperative behaviour (Telmatochromis temporalis, Neolamprologus tetracanthus and Neolamprologus modestus). We quantified the innate immune response by injecting wild fishes with phytohaemagglutinin (PHA), a lectin that causes a cell-mediated immune response. We predicted that the three highly social species would show a greater immune reaction to the PHA treatment, indicating higher investment in immune defence against parasites relative to the three non-social species. We found significant species-level variation in immune response, but contrary to our prediction, this variation did not correspond to social system. However, we found that immune response was correlated with territory size across the six species. Our results indicate that the common assumption of a positive relationship between social system and investment in immune function may be overly simplistic. We suggest that factors such as rates of both in-group and out-group social interactions are likely to be important mediators of the relationship between sociality and immune function.

Water pH during early development influences sex ratio and male morph in a West African cichlid fish, Pelvicachromis pulcher.

Environmental sex determination (ESD) is one of the most striking examples of phenotypic plasticity. Individuals from species that exhibit ESD can develop as either males or females depending on the particular environmental conditions they experience during early development. In fish, ESD species often show a relatively subtle effect of environment, resulting in a substantial number of both sexes being produced in both male- and female-biasing conditions, rather than the unisex clutches that are typical of many reptiles. This less dramatic form of ESD allows the opportunity to study the effects of sexual differentiation on within-sex variation in behavior and morphology by comparing same-sex individuals produced in male- and female-biasing conditions. Here, we confirm that sex determination in the West African cichlid, Pelvicachromis pulcher, is influenced by pH during early development. We show that pH also affects the ratio of two alternative male reproductive types with the polygynous morph being overproduced in male-biasing conditions and the monogamous male morph being overproduced in female-biasing conditions. Our results suggest that the sexual differentiation process may be an important force in maintaining individual variation in behavior and reproductive tactics.

Probing aggressive motivation during territorial contests in a group-living cichlid fish.

Many animals fight to win resources, repel competitors or establish dominance in a social group. Mutual-assessment of fighting ability, where competitors gather and compare information about their opponent's as well as their own fighting ability has been the dominant theoretical framework for understanding decision-making during fights. However, self-assessment, where each individual has a cost threshold and fights up until that point, may be more common than previously appreciated. In this study, we attempted to discriminate between these two potential assessment mechanisms in a group-living cichlid fish, Neolamprologus pulcher by probing aggressive motivation during a territorial contest. We measured aggressive motivation, and used this metric to investigate assessment rules during an ongoing contest. We predicted that if these social fish use self-assessment, we would observe a positive correlation between the fighting ability of the probed animal and its aggressive motivation. Alternatively, if mutual-assessment is used then we predicted we would find a negative effect of the opponent's fighting ability on the aggressive motivation of the probed fish because fish should be less motivated to fight against formidable opponents. Our results did not support either of these predictions. In contrast we found that small individuals were more aggressively motivated regardless of their opponent's size. We discuss this result in the context of theoretical models of aggression in individuals of small body size.

Lateralized behaviour of a non-social cichlid fish (Amatitlania nigrofasciata) in a social and a non-social environment.

Cerebral lateralization, the partitioning of cognitive function preferentially into one hemisphere of the brain, is a trait ubiquitous among vertebrates. Some species exhibit population level lateralization, where the pattern of cerebral lateralization is the same for most members of that species; however, other species show only individual level lateralization, where each member of the species has a unique pattern of lateralized brain function. The pattern of cerebral lateralization within a population and an individual has been shown to differ based on the stimulus being processed. It has been hypothesized that sociality within a species, such as shoaling behaviour in fish, may have led to the development and persistence of population level lateralization. Here we assessed cerebral lateralization in convict cichlids (Amatitlania nigrofasciata), a species that does not shoal as adults but that shoals briefly as juveniles. We show that both male and female convict cichlids display population level lateralization when in a solitary environment but only females show population level lateralization when in a perceived social environment. We also show that the pattern of lateralization differs between these two tasks and that strength of lateralization in one task is not predictive of strength of lateralization in the other task.

Variation in asymmetry of the habenular nucleus correlates with behavioural asymmetry in a cichlid fish.

Asymmetries in brain and behaviour have been demonstrated in numerous species representing all major vertebrate taxa, and may be a universal feature of the vertebrate nervous system. While descriptions of lateralization at the behavioural and neuroanatomical level are widespread, examples of correlation between asymmetries in behaviour and neural structures remain relatively scarce. In the past few years, the habenular nucleus has emerged as a potential site for the neural basis of some lateralized behaviours. Here we investigate the relation between continuous individual variation in asymmetry of the habenulae and behaviour in the detour task in the convict cichlid (Amatitlania nigrofasciata). We found that both male and female convicts show a significant population-level bias towards relatively larger left habenulae. We also show that habenular asymmetry is correlated with behavioural lateralization in both males and females, but in opposite directions. This adds to previous studies showing both in convict cichlids and other vertebrates an interaction between sex and lateralized behaviour. The results of this study increase our understanding of the role of the habenula in lateralized behaviour and highlight the importance of a comparative approach to understanding the development and evolution of habenular asymmetry.

Sex differences in the relationship between aggressiveness and the strength of handedness in humans.

Cerebral lateralisation, the partitioning of cognitive functioning into one hemisphere of the brain, was once considered unique to humans; however, recent research in a variety of taxa suggests that lateralisation is an evolutionarily ancient adaptation. Handedness is the most obvious manifestation of cerebral lateralisation in humans. Much of the literature on handedness has focused on the direction, rather than the strength, of this lateralisation. From both genetic and evolutionary perspectives it may be more informative to study degrees of cerebral lateralisation rather than direction. Strong evidence suggests that the strength may be more closely associated with individual differences in behaviour in humans than the direction, and individual variation in the degree of lateralisation has been found to correlate with personality-like characteristics such as aggressiveness in fish. The association between different patterns of lateralisation and personality characteristics may help explain how variation in the strength of lateralisation is evolutionarily stable in natural populations. The present study investigated the relationship between aggression and strength of handedness in humans. We found a significant interaction between sex and lateralisation with respect to aggression. In males, trait aggression was significantly higher in strong-handers than in mixed-handers, while no difference was seen in females. This finding highlights the importance of considering sex as a factor when investigating relationships between cerebral lateralisation and personality characteristics. Potential causes and consequences of the sex interaction as well as future directions for research are discussed.

Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task.

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.