Brain monoaminergic activity during predator inspection in female Trinidadian guppies (Poecilia reticulata).

To understand the processes underpinning social decision-making, we need to determine how internal states respond to information gathered from the social environment. Brain monoamine neurotransmitters are key in the appraisal of the social environment and can reflect the internal state underlying behavioural responses to social stimuli. Here we determined the effects of conspecific partner cooperativeness during predator inspection on brain monoamine metabolic activity in Trinidadian guppies (Poecilia reticulata). We quantified the concentration of dopamine, serotonin and their metabolites across brain sections sampled immediately after ostensibly experiencing cooperation or defection from social partners whilst inspecting a predator model, using a familiar object as a control condition. Our results indicate dopaminergic and serotonergic activity differs with the cooperativeness experienced; these different neurotransmission profiles are likely to affect the expression and regulation of downstream behaviours that ultimately contribute to the patterning of cooperative interactions among individuals in a population.

Leaders of war: modelling the evolution of conflict among heterogeneous groups.

War, in human and animal societies, can be extremely costly but can also offer significant benefits to the victorious group. We might expect groups to go into battle when the potential benefits of victory (V) outweigh the costs of escalated conflict (C); however, V and C are unlikely to be distributed evenly in heterogeneous groups. For example, some leaders who make the decision to go to war may monopolize the benefits at little cost to themselves ('exploitative' leaders). By contrast, other leaders may willingly pay increased costs, above and beyond their share of V ('heroic' leaders). We investigated conflict initiation and conflict participation in an ecological model where single-leader-multiple-follower groups came into conflict over natural resources. We found that small group size, low migration rate and frequent interaction between groups increased intergroup competition and the evolution of 'exploitative' leadership, while converse patterns favoured increased intragroup competition and the emergence of 'heroic' leaders. We also found evidence of an alternative leader/follower 'shared effort' outcome. Parameters that favoured high contributing 'heroic' leaders, and low contributing followers, facilitated transitions to more peaceful outcomes. We outline and discuss the key testable predictions of our model for empiricists studying intergroup conflict in humans and animals. This article is part of the theme issue 'Intergroup conflict across taxa'.

Divergence in social traits in Trinidadian guppies selectively bred for high and low leadership in a cooperative context.

In many animal species, individuals with certain morphological, physiological, or behavioural traits may have a disproportionately large role in determining group behaviour. While most empirical studies of leadership have focused on behaviour of individuals exploring new environments or foraging, little is known about leading behaviour in other ecological contexts. Here, we use a selective breeding design in the Trinidadian guppy (Poecilia reticulata) to quantify the heritability of leadership in a cooperative context, and determine the behavioural traits associated with it. Firstly we found that phenotypic selection for high and low leadership (HL and LL, respectively) over three filial generations resulted in pronounced differences in leadership tendency with a moderate degree of heritability. In our assay of other social traits, LL males were more aggressive and sampled their social environment less than HL males, but HL and LL females did not differ in either aggressiveness or sociability. Traits such as boldness and exploratory tendency did not diverge between the two lines. Leading behaviour was thus associated with social traits in males, but not females; suggesting that there may be sex-specific mechanisms driving the emergence of leadership in this context. We discuss our findings in the context of the evolution of cooperation.

Use of novel sensors combining local positioning and acceleration to measure feeding behavior differences associated with lameness in dairy cattle.

Time constraints for dairy farmers are an important factor contributing to the under-detection of lameness, resulting in delayed or missed treatment of lame cows within many commercial dairy herds. Hence, a need exists for flexible and affordable cow-based sensor systems capable of monitoring behaviors such as time spent feeding, which may be affected by the onset of lameness. In this study a novel neck-mounted mobile sensor system that combines local positioning and activity (acceleration) was tested and validated on a commercial UK dairy farm. Position and activity data were collected over 5 consecutive days for 19 high-yield dairy cows (10 lame, 9 nonlame) that formed a subset of a larger (120 cow) management group housed in a freestall barn. A decision tree algorithm that included sensor-recorded position and accelerometer data was developed to classify a cow as doing 1 of 3 categories of behavior: (1) feeding, (2) not feeding, and (3) out of pen for milking. For each classified behavior the mean number of bouts, the mean bout duration, and the mean total duration across all bouts was determined on a daily basis, and also separately for the time periods in between milking (morning = 0630-1300 h; afternoon = 1430-2100 h; night = 2230-0500 h). A comparative analysis of the classified cow behaviors was undertaken using a Welch t-test with Benjamini-Hochberg post-hoc correction under the null hypothesis of no differences in the number or duration of behavioral bouts between the 2 test groups of lame and nonlame cows. Analysis showed that mean total daily feeding duration was significantly lower for lame cows compared with non-lame cows. Behavior was also affected by time of day with significantly lower mean total duration of feeding and higher total duration of nonfeeding in the afternoons for lame cows compared with nonlame cows. The results demonstrate how sensors that measure both position and acceleration are capable of detecting differences in feeding behavior that may be associated with lameness. Such behavioral differences could be used in the development of predictive algorithms for the prompt detection of lameness as part of a commercially viable automated behavioral monitoring system.

Mortality risk and social network position in resident killer whales: sex differences and the importance of resource abundance.

An individual's ecological environment affects their mortality risk, which in turn has fundamental consequences for life-history evolution. In many species, social relationships are likely to be an important component of an individual's environment, and therefore their mortality risk. Here, we examine the relationship between social position and mortality risk in resident killer whales (Orcinus orca) using over three decades of social and demographic data. We find that the social position of male, but not female, killer whales in their social unit predicts their mortality risk. More socially integrated males have a significantly lower risk of mortality than socially peripheral males, particularly in years of low prey abundance, suggesting that social position mediates access to resources. Male killer whales are larger and require more resources than females, increasing their vulnerability to starvation in years of low salmon abundance. More socially integrated males are likely to have better access to social information and food-sharing opportunities which may enhance their survival in years of low salmon abundance. Our results show that observable variation in the social environment is linked to variation in mortality risk, and highlight how sex differences in social effects on survival may be linked to sex differences in life-history evolution.

Stress and welfare in ornamental fishes: what can be learned from aquaculture?

The ornamental fish trade is estimated to handle up to 1·5 billion fishes. Transportation and handling of fishes imposes a range of stressors that can result in mortality at rates of up to 73%. These rates vary hugely, however, and can be as low as 2%, because they are generally estimated rather than based on experimental work. Given the numbers of ornamental fishes traded, any of the estimated mortality rates potentially incur significant financial losses and serious welfare issues. Industry bodies, such as the Ornamental Aquatic Trade Association (OATA), have established standards and codes of best practice for handling fishes, but little scientific research has been conducted to understand the links between stress, health and welfare in ornamental species. In aquaculture, many of the same stressors occur as those in the ornamental trade, including poor water quality, handling, transportation, confinement, poor social and physical environment and disease and in this sector directed research and some resulting interventions have resulted in improved welfare standards. This review considers the concept of welfare in fishes and evaluates reported rates of mortality in the ornamental trade. It assesses how the stress response can be quantified and used as a welfare indicator in fishes. It then analyses whether lessons from aquaculture can be usefully applied to the ornamental fish industry to improve welfare. Finally, this analysis is used to suggest how future research might be directed to help improve welfare in the ornamental trade.

The effect of familiarity on aggregation and social behaviour in juvenile small spotted catsharks Scyliorhinus canicula.

This study was designed to address whether juvenile small spotted catsharks Scyliorhinus canicula aggregate and to determine whether potential aggregation is underpinned by social preferences for conspecifics. Using controlled and replicated experiments, the role of familiarity as a potential mechanism driving aggregation and social behaviour in this species was considered. Observed S. canicula association data compared to null model simulations of random distributions revealed differences in aggregation under different social contexts. Only familiar juvenile S. canicula aggregated more than would be expected from random distribution across their habitat. Familiarity increased the mean number of groups but did not significantly affect mean group size. Significant preference and avoidance behaviour across all groups were also observed. Furthermore, the strength of social attraction, quantified by the mean association index, was significantly higher in groups containing familiar individuals. Mixed familiar and unfamiliar treatments were also conducted to test for within- and between-group effects, finding high variation across replicates with some groups assorting by familiarity and others not. It is believed that this study is the first to examine experimentally the influence of conspecific familiarity on aggregation behaviour in sharks. These results not only imply a functional benefit to aggregation, but also suggest that persistent social affiliation is likely to influence dispersal following hatching in this small benthic elasmobranch.

Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus.

Association preferences and aggression intensity were investigated in relation to kin and familiarity in the self-fertilizing, clonal vertebrate, the mangrove killifish Kryptolebias marmoratus. Results indicated that fish preferentially associated with and exhibited less intense aggression towards members of their own genotype (kin), compared to members of a different genotype (non-kin). Furthermore, when fish were presented with stimulus groups of the same genotype that were familiar or unfamiliar, fish preferentially associated with and exhibited lower aggression intensity directed towards familiar groups. These results indicate that this species prefer to associate with both kin and familiar individuals and modulate aggression accordingly. These results are discussed with reference to the adaptive benefits of kin recognition and preferences for familiars, and place results within the context of current knowledge of the ecology of K. marmoratus.

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish.

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.

Personality in the context of social networks.

There is great interest in environmental effects on the development and evolution of animal personality traits. An important component of an individual's environment is its social environment. However, few studies look beyond dyadic relationships and try to place the personality of individuals in the context of a social network. Social network analysis provides us with many new metrics to characterize the social fine-structure of populations and, therefore, with an opportunity to gain an understanding of the role that different personalities play in groups, communities and populations regarding information or disease transmission or in terms of cooperation and policing of social conflicts. The network position of an individual is largely a consequence of its interactive strategies. However, the network position can also shape an individual's experiences (especially in the case of juveniles) and therefore can influence the way in which it interacts with others in future. Finally, over evolutionary time, the social fine-structure of animal populations (as quantified by social network analysis) can have important consequences for the evolution of personalities-an approach that goes beyond the conventional game-theoretic analyses that assumed random mixing of individuals in populations.

Predation risk as a driving force for phenotypic assortment: a cross-population comparison.

Frequency-dependent predation has been proposed as a general mechanism driving the phenotypic assortment of social groups via the 'oddity effect', which occurs when the presence of odd individuals in a group allows a predator to fixate on a single prey item, increasing the predator's attack-to-kill ratio. However, the generality of the oddity effect has been debated and, previously, there has not been an ecological assessment of the role of predation risk in driving the phenotypic assortment of social groups. Here, we compare the levels of body length assortment of social groups between populations of the Trinidadian guppy (Poecilia reticulata) that experience differences in predation risk. As predicted by the oddity effect hypothesis, we observe phenotypic assortment by body length to be greater under high predation risk. However, we found that a number of low-predation populations were also significantly assorted by body length, suggesting that other mechanisms may have a role to play.

RISK-SENSITIVE ANTIPREDATOR BEHAVIOR IN THE TRINIDADIAN GUPPY, POECILIA RETICULATA.

The comparative approach has become a powerful tool for understanding how predation has shaped prey behavior. In this study we recorded the occurrence of common aquatic predator species and their densities in seven natural populations of Trinidadian guppies, Poecilia reticulata. We then exposed shoals of guppies from each of these populations to a series of predator treatments. Predator treatments differed in the species of predator used (pike cichlids, Crenicichla frenata; rivulus, Rivulus hartii; and freshwater prawns, Macrobrachium carcinus) and thus in the level of risk posed. We recorded the antipredator responses of guppies in each of these predator treatments. The strength of antipredator behavior shown by guppies was affected by both the type of predator they were exposed to and the level of predation risk they experienced naturally in the wild. Importantly, we found that guppies from high-risk populations showed a heightened response, compared to those from lower risk populations, only when exposed to the predator species that posed the greatest risk. Our results show the importance of individual predator species in shaping the behavioral traits of prey species at the population level. This has implications for prey movement between habitats that are geographically close but differ greatly in predator fauna.

Social network theory in the behavioural sciences: potential applications.

Social network theory has made major contributions to our understanding of human social organisation but has found relatively little application in the field of animal behaviour. In this review, we identify several broad research areas where the networks approach could greatly enhance our understanding of social patterns and processes in animals. The network theory provides a quantitative framework that can be used to characterise social structure both at the level of the individual and the population. These novel quantitative variables may provide a new tool in addressing key questions in behavioural ecology particularly in relation to the evolution of social organisation and the impact of social structure on evolutionary processes. For example, network measures could be used to compare social networks of different species or populations making full use of the comparative approach. However, the networks approach can in principle go beyond identifying structural patterns and also can help with the understanding of processes within animal populations such as disease transmission and information transfer. Finally, understanding the pattern of interactions in the network (i.e. who is connected to whom) can also shed some light on the evolution of behavioural strategies.

Social organization, grouping, and domestication in fish.

The zebrafish (Danio rerio) is now established as one of the pre-eminent model vertebrate study animals in biology, providing an excellent opportunity to integrate the fields of genetics and behavioral ecology. Considerable attention has been paid to the social organization of animals and the study of zebrafish in this context allows behavioral geneticists to gain an insight into this fundamentally important field. This paper reviews the literature on the social organization of fish, with special reference to the zebrafish. The mechanisms and functions of social behavior in fish and the current understanding of the behavioral genetics of these are discussed. Finally, the impact of domestication on the expression of wild-type behavior patterns in laboratory fish is considered.

Assortative interactions and social networks in fish.

The mechanisms underpinning the structure of social networks in multiple fish populations were investigated. To our knowledge this is the first study to provide replication of social networks and therefore probably the first that allows general conclusions to be drawn. The social networks were all found to have a non-random structure and exhibited 'social cliquishness'. A number of factors were observed to contribute to this structuring. Firstly, social network structure was influenced by body length and shoaling tendency, with individuals interacting more frequently with conspecifics of similar body length and shoaling tendency. Secondly, individuals with many social contacts were found to interact with each other more often than with other conspecifics, a phenomenon known as a 'positive degree correlation'. Finally, repeated interactions between pairs of individuals occurred within the networks more often than expected by random interactions. The observed network structures will have ecological and evolutionary implications. For example, the occurrence of positive degree correlations suggests the possibility that pathogens and information (that are socially transmitted) could spread very fast within the populations. Furthermore, the occurrence of repeated interactions between pairs of individuals fulfils an important pre-requisite for the evolution of reciprocal altruism.