BEHAVIOUR

Prey size preference in the tokay gecko ()
Probst A, Ringler E and Szabo B
The optimal foraging theory posits that animals aim to maximize energy intake while minimizing predation and handling costs during foraging. Most observed animal behaviour supports this theory, but occasional deviations provide insights into the ecological factors that shape foraging decisions. We tested prey-size preference using a two-choice test between different prey sizes in tokay geckos. We expected geckos to prefer larger prey and decision latencies to be longer when discrimination was more difficult and when small prey was offered. Geckos preferred larger prey when the size difference was large, although decision latency remained consistent. This aligns with prior research on sit-and-wait predators. Together with previous findings showing freezing behaviour after prey capture in tokay geckos, our findings suggest a strong influence of predator avoidance on foraging decisions opening up a new avenue for future research investigating the link between decision making and predator avoidance in tokay geckos.
The link between animal personality and habitat selection in males of the Neotropical poison frog
Bégué L, Peignier M and Ringler E
Environmental variation plays a key role in the evolution and maintenance of animal personality. Individuals with different personality types might exhibit different habitat preferences. Alternatively, variation in individual behaviour across space could arise as a plastic adaptation to distinct habitats. Our study aims to investigate if habitat choice is influenced by an individual's personality. We assessed individual levels of activity, boldness, and exploration in male poison frogs, and performed a habitat choice test under controlled laboratory conditions. Individuals were consistent in their behaviours, but all tested frogs chose the complex over the simple habitat. Individuals that were characterized as bold and very explorative also showed more movements between the two different habitats in the choice test. These results indicate that personality measured in a highly standardized artificial setup, such as a novel environment test, indeed can reflect boldness and exploration related behaviours measured in a more naturalistic setup.
Female social structure influences, and is influenced by, male introduction and integration success among captive rhesus macaques ()
Balasubramaniam KN, Beisner BA, McCowan B and Bloomsmith MA
Animal social structure is influenced by multiple socioecological factors. Of these, the links between changes to group demography through the arrival of new individuals and residents' social structure remain unclear. Across seven groups of captive rhesus macaques (), we examine how male introductions may be influenced by, and in-turn influence, aspects of female social structure. GLMMs revealed that males integrated more successfully into groups in which females showed more 'despotic' social structures, i.e., higher aggression rates, steeper dominance hierarchies, and greater rank-skew in allogrooming network connectedness. Yet during periods that followed males' social integration, females increased their social tolerance (decreased aggression and shallower hierarchies) and group cohesivity (less clustered allogrooming networks), but retained their tendencies to groom dominants. Our findings, independent of group size and matrilineal relatedness, help better understand how dispersal/immigration may influence social structure, and how assessing changes to social structure may inform macaque welfare and management.
The role of personality traits in pair bond formation: pairing is influenced by the trait of exploration
Faust KM and Goldstein MH
In species with long-term pair bonds, such as zebra finches, evaluating the quality of potential mates is critically important. Courtship is an opportunity to evaluate information from dynamic behavioural cues. Personality traits, as stable individual differences in behaviour, could predict the quality of a potential mate. How might personality traits influence mate choice? We examined the influence of several personality traits, including exploration, aggression, and social preference, on pair formation in zebra finches. We provided birds with a variety of potential mates and allowed them to select a pair partner. Our semi-naturalistic mate choice paradigm allowed birds to observe social information over an extended period, simulating the challenges of social evaluation that birds encounter in the wild. We found that pairing is influenced by personality, with birds selecting mates similar to them in exploration. The partner's exploration score relative to their own was more important than the absolute exploration score.
Incorporating genomic methods into contact networks to reveal new insights into animal behavior and infectious disease dynamics
Gilbertson MLJ, Fountain-Jones NM and Craft ME
Utilization of contact networks has provided opportunities for assessing the dynamic interplay between pathogen transmission and host behavior. Genomic techniques have, in their own right, provided new insight into complex questions in disease ecology, and the increasing accessibility of genomic approaches means more researchers may seek out these tools. The integration of network and genomic approaches provides opportunities to examine the interaction between behavior and pathogen transmission in new ways and with greater resolution. While a number of studies have begun to incorporate both contact network and genomic approaches, a great deal of work has yet to be done to better integrate these techniques. In this review, we give a broad overview of how network and genomic approaches have each been used to address questions regarding the interaction of social behavior and infectious disease, and then discuss current work and future horizons for the merging of these techniques.
The neuroscience of social relations. A comparative-based approach to empathy and to the capacity of evaluating others' action value
Ferrari PF
One of the key questions in understanding human morality is how central are emotions in influencing our decisions and in our moral judgments. Theoretical work has proposed that empathy could play an important role in guiding our tendencies to behave altruistically or selfishly. Neurosciences suggest that one of the core elements of empathic behavior in human and nonhuman primates is the capacity to internally mimic the behavior of others, through the activation of shared motor representations. Part of the neural circuits involves parietal and premotor cortical regions (mirror system), in conjunction with other areas, such as the insula and the anterior cingulate cortex. Together with this embodied neural mechanism, there is a cognitive route in which individuals can evaluate the social situation without necessary sharing the emotional state of others. For example, several brain areas of the prefrontal cortex track the effects of one's own behavior and of the value of one's own actions in social contexts. It is here proposed that, moral cognition could emerge as the consequence of the activity of emotional processing brain networks, probably involving mirror mechanisms, and of brain regions that, through abstract-inferential processing, evaluate the social context and the value of actions in terms of abstract representations. A comparative-based approach to the neurobiology of social relations and decision-making may explain how complex mental faculties, such as moral judgments, have their foundations in brain networks endowed with functions related to emotional and abstract-evaluation processing of goods. It is proposed that in primate evolution these brain circuits have been coopted in the social domain to integrate mechanisms of self-reward, estimation of negative outcomes, with emotional engagement.
Integration of multiple cues allows threat-sensitive anti-intraguild predator responses in predatory mites
Walzer A and Schausberger P
Intraguild (IG) prey is commonly confronted with multiple IG predator species. However, the IG predation (IGP) risk for prey is not only dependent on the predator species, but also on inherent (intraspecific) characteristics of a given IG predator such as its life-stage, sex or gravidity and the associated prey needs. Thus, IG prey should have evolved the ability to integrate multiple IG predator cues, which should allow both inter- and intraspecific threat-sensitive anti-predator responses. Using a guild of plant-inhabiting predatory mites sharing spider mites as prey, we evaluated the effects of single and combined cues (eggs and/or chemical traces left by a predator female on the substrate) of the low risk IG predator and the high risk IG predator on time, distance and path shape parameters of the larval IG prey . IG prey discriminated between traces of the low and high risk IG predator, with and without additional presence of their eggs, indicating interspecific threat-sensitivity. The behavioural changes were manifest in distance moved, activity and path shape of IG prey. The cue combination of traces and eggs of the IG predators conveyed other information than each cue alone, allowing intraspecific threat-sensitive responses by IG prey apparent in changed velocities and distances moved. We argue that graded responses to single and combined IG predator cues are adaptive due to minimization of acceptance errors in IG prey decision making.
Individual variation in habituation: behaviour over time toward different stimuli in threespine sticklebacks ()
Bell AM and Peeke HV
Habituation, or the relatively permanent waning of a response as a result of repeated stimulation, is a form of behavioural plasticity that allows animals to filter out irrelevant stimuli and to focus selectively on important stimuli. Individuals that fail to habituate might be at a disadvantage if they continue to respond to irrelevant stimuli; therefore, habituation can have adaptive significance. In this study we compared rates of behaviour over time toward three different ecologically-relevant stimuli (food, a male intruder and a gravid female) in threespine sticklebacks (). We detected evidence for habituation to the stimuli, and males in this study were especially aggressive toward both male and female conspecifics. Although there were some clear temporal patterns that could be detected by looking at average behaviour, not all individuals behaved in the same 'average' way. We detected substantial inter-individual variation in behaviour toward all three stimuli, inter-individual variation in rates of habituation to both male and female conspecifics, but no evidence for correlations between behaviours across stimuli (behavioural syndromes). These results suggest that individual animals vary in rates of habituation, and prompt hypotheses about the causes and consequences of variation in rates of habituation.
Population structure influences sexual conflict in wild populations of water striders
Eldakar OT, Dlugos MJ, Holt GP, Wilson DS and Pepper J
In sexual conflict, aggressive males frequently diminish the long-term reproductive success of females in efforts to gain a short-term advantage over rival males. This short-term advantage can selectively favour high-exploitation males. However, just as the over-exploitation of resources can lead to local extinction, the over-exploitation of females in the form of harassment by aggressive males can yield similar consequences resulting in reduced female fecundity, increased female mortality and overall decline in mating activity. This outcome may often be prevented by selection acting at multiple levels of biological organization. Directional selection favouring aggressive exploitation within groups can be balanced by directional selection amongst groups opposing exploitation. Such between-group selection has recently been demonstrated in laboratory studies of water striders, where the conditional dispersal of individuals increased variation amongst groups and influenced the balance of selection toward reduced male aggression. This multilevel selection (MLS) framework also provides predictive value when investigating natural populations differing in their relative strength of selection within versus among groups. For water striders, the consequences of local exploitation cause fitness differences between groups, favouring less aggressive males. Inconsistently flowing ephemeral streams consist of isolated pools that prevent aggressive male water striders from escaping the consequences of local exploitation. We, therefore, predicted that inconsistently flowing ephemeral streams would favour the evolution of less aggressive males than would perennial streams, which allow aggressive males to move more freely and to escape the group-level costs of their aggression. Comparing two neighbouring streams during the mating season, we found that males dispersed naturally between pools at much higher rates in the perennial stream than in the ephemeral stream. As predicted, we found that males from the perennial stream were significantly more aggressive than those from the ephemeral stream. We also found that dispersers were significantly more aggressive than non-dispersers within each stream. These field results illustrate the relevance of the MLS framework in our understanding of the evolution of sexual conflict.
Handedness for tool use in captive chimpanzees (Pan troglodytes): Sex differences, performance, heritability and comparison to the wild
Hopkins WD, Russell JL, Schaeffer JA, Gardner M and Schapiro SJ
There is continued debate over the factors influencing handedness in captive and wild primates, notably chimpanzees. Previous studies in wild chimpanzees have revealed population-level left handedness for termite fishing. Here we examined hand preferences and performance on a tool use task designed to simulate termite fishing in a sample of 190 captive chimpanzees to evaluate whether patterns of hand use in captive chimpanzees differed from those observed for wild apes. No population-level handedness was found for this task; however, significant sex differences in preference and performance were found, with males showing greater left handedness and poorer performance compared to females. We also found that the hand preferences of offspring were significantly positively correlated with the hand preferences of their mothers. Lastly, older females performed more slowly on the task compared to younger individuals. The overall results neither confirm nor reject previous hypotheses claiming that raising chimpanzees in captivity induces right-handedness, but rather suggest that other factors may account for differences in hand preferences for tool use seen in wild and captive chimpanzees.
Active and passive social support in families of greylag geese (Anser anser)
Scheiber IB, Weiß BM, Frigerio D and Kotrschal K
In general, support by social allies may reduce stress, increase success in agonistic encounters and ease access to resources. Social support was mainly known from mammals, particularly primates, and has been studied in birds only recently. Basically two types are known: (i) 'active social support', which describes the participation of a social ally in agonistic encounters, and (ii) 'passive social support' in which the mere presence of a social ally reduces behavioural and physiological stress responses. In greylag geese (Anser anser) offspring stay with their parents for an entire year or even longer and therefore are a candidate avian model to study support by social allies. We investigated the effects of active and passive social support in ten families (ten males, ten females, 33 juveniles) in a free-roaming, semi-tame flock of greylag geese. Focal individuals were observed during three time periods: (i) re-establishment of the flock in the fall, (ii) stable winter flock, and (iii) disintegration of the flock and break-up of family bonds. We recorded all agonistic interactions of the members of one focal family during morning feedings for two consecutive days: a control day, in which food was distributed widely, and a social density stress situation, in which the same amount of food was spread over a much smaller area. In addition, we collected faeces of all individuals within this family for three hours from the beginning of the feeding situation for determining excreted corticosterone immuno-reactive metabolites by enzyme immuno assay. We found that the small families, i.e. pairs with one or two accompanying young, were involved in more agonistic interactions, mainly through the lack of active social support, as compared to large families in the same situation. Members of greylag goose families lost agonistic encounters significantly less often when actively supported. In addition, the excretion of corticosterone metabolites was significantly decreased in large families during a social density stress situation, probably as an effect of passive social support. Via such a socially induced decrease in hormonal stress response during challenging situations, an individual's long term energy management may benefit.
Perceptual determinants of gaze aversion by normal and psychotic children: the role of two facing eyes
Coss RG
The induction of aggressive behaviour by electrical stimulation in the hypothalamus of male rats
Kruk MR, van der Poel AM and de Vos-Frerichs TP
Chronic perchlorate exposure impairs stickleback reproductive behaviour and swimming performance
Bernhardt RR and von Hippel FA
We describe behavioural changes in two generations of threespine stickleback (Gasterosteus aculeatus) exposed to environmentally relevant concentrations of perchlorate. The first generation (G(0,2002)) was exposed as two-year-old adults to perchlorate in experimental groups ranging in concentration from less than the method detection limit (<1.1 ppb) to 18.6 ppm for up to 22 days during their courtship, spawning, egg guarding, and first five days of fry guarding. No differences were noted in the behaviour or reproductive output of these fish that were exposed as adults. However, perchlorate exposure throughout development caused widespread effects in the second generation (G(1,2003)), which was spawned and raised through sexual maturity in one of four nominal experimental groups (0, 30 and 100 ppm, and a 'variable' treatment that progressively increased from <1.1 ppb to approximately 60 ppm perchlorate). Dose-dependent effects were found during the G(1,2003)'s swimming and behavioural evaluations, including higher mortality rates among treated fish following stressful events. Perchlorate-exposed fish had higher failure rates during swimming trials and failed at lower flow rates than control fish. A number of treated fish exhibited seizures. Progressively fewer males completed benchmark metrics, such as nest building, spawning, nursery formation, or fry production, in a dose-dependent manner. Fewer males from higher treatments courted females, and those that did initiated courtship later and had a reduced behavioural repertoire compared to fish from lower treatments. The lowest observed adverse effect level (LOAEL) for swimming performance, reproductive behaviour, survivorship and recruitment was 30 ppm perchlorate (our lowest G(1,2003) treatment), and near complete inhibition of reproductive activity was noted among males raised in 100 ppm perchlorate. A small number of treated G(1,2003) females were isolated in aquaria, and some performed reproductive behaviour typical of males, such as biting, leading and zig-zagging in the presence of gravid females. These findings have profound implications for recruitment in wild fish populations exposed to perchlorate, and suggest that perchlorate may disrupt behaviour in other vertebrates as well.
Evolution of advertisement calls in African clawed frogs
Tobias ML, Evans BJ and Kelley DB
For most frogs, advertisement calls are essential for reproductive success, conveying information on species identity, male quality, sexual state and location. While the evolutionary divergence of call characters has been examined in a number of species, the relative impacts of genetic drift or natural and sexual selection remain unclear. Insights into the evolutionary trajectory of vocal signals can be gained by examining how advertisement calls vary in a phylogenetic context. Evolution by genetic drift would be supported if more closely related species express more similar songs. Conversely, a poor correlation between evolutionary history and song expression would suggest evolution shaped by natural or sexual selection. Here, we measure seven song characters in 20 described and two undescribed species of African clawed frogs (genera and ) and four populations of . We identify three call types - click, burst and trill - that can be distinguished by click number, call rate and intensity modulation. A fourth type is biphasic, consisting of two of the above. Call types vary in complexity from the simplest, a click, to the most complex, a biphasic call. Maximum parsimony analysis of variation in call type suggests that the ancestral type was of intermediate complexity. Each call type evolved independently more than once and call type is typically not shared by closely related species. These results indicate that call type is homoplasious and has low phylogenetic signal. We conclude that the evolution of call type is not due to genetic drift, but is under selective pressure.
Behavioral characteristics of pair bonding in the black tufted-ear marmoset ()
Ågmo A, Smith AS, Birnie AK and French JA
The present study describes how the development of a pair bond modifies social, sexual and aggressive behavior. Five heterosexual pairs of marmosets, previously unknown to each other, were formed at the beginning of the study. At the onset of pairing, social, sexual, exploratory and aggressive behaviors were recorded for 40 min. The animals were then observed for 20 min, both in the morning and afternoon for 21 days. The frequency and/or duration of behaviors recorded on Day 1 were compared to those recorded at later observations. The behavior displayed shortly after pairing should be completely unaffected by the pair bond, while such a bond should be present at later observations. Thus, it was possible to determine how the behavior between the pair was modified by the development of a pair bond. Social behaviors increased from Day 1 to Days 2-6 and all subsequent days observed. Conversely, other behaviors, such as open mouth displays (usually considered to be an invitation to sexual activity), had a high frequency during the early part of cohabitation but declined towards the end. Consequently, pair bonding manifests itself in an increased intensity of social behaviors. It is suggested that the intrinsically rewarding properties of grooming and perhaps other social behaviors turn the pair mate into a positive incentive, activating approach and further interactions when possible. Thus, the pair bond may be a motivational state activated by the conditioned incentive properties of the partner. This notion can explain all forms of pair bonds, including those occurring between individuals of the same sex and in promiscuous species.
Exploring novelty: a component trait of behavioural syndromes in a colonial fish
Martins CIM, Schaedelin FC, Mann M, Blum C, Mandl I, Urban D, Grill J, Schößwender J and Wagner RH
Individual differences in exploratory behaviour have been shown to be consistent across contexts and suggested to be part of behavioural syndromes in a diversity of species, including fish. Exploration has also been shown to be a key factor in understanding complex ecological processes such as sexual selection and cooperation. Another important question in ecology is why animals breed in colonies. Exploration syndromes, by affecting prospecting behaviour, dispersal and public information use may also contribute to our understanding of coloniality. This study aims at investigating whether an exploration syndrome exists in a colonial fish species, . Individuals of this species were subjected to two consecutive tests, a novel environment and a novel object test. Results show that more explorative individuals in a novel environment are also less neophobic in the presence of a novel object, suggesting that the tendency to engage with novelty per se is a consistent trait and part of an exploration syndrome. These results are discussed in light of the contribution of an exploration syndrome to explain colony formation in animals.
The misbehaviour of a metacognitive monkey
Sayers K, Evans TA, Menzel E, Smith JD and Beran MJ
Metacognition, the monitoring of one's own mental states, is a fundamental aspect of human intellect. Despite tests in nonhuman animals suggestive of uncertainty monitoring, some authors interpret these results solely in terms of primitive psychological mechanisms and reinforcement regimes, where "reinforcement" is invariably considered to be the delivery and consumption of earned food rewards. Surprisingly, few studies have detailed the trial-by-trial behaviour of animals engaged in such tasks. Here we report ethology-based observations on a rhesus monkey completing sparse-dense discrimination problems, and given the option of escaping trials (i.e., responding "uncertain") at its own choosing. Uncertainty responses were generally made on trials of high objective difficulty, and were characterized by long latencies before beginning visible trials, long times taken for response, and, even after controlling for difficulty, high degrees of wavering during response. Incorrect responses were also common in trials of high objective difficulty, but were characterized by low degrees of wavering. This speaks to the likely adaptive nature of "hesitation," and is inconsistent with models which argue or predict implicit, inflexible information-seeking or "alternative option" behaviours whenever challenging problems present themselves, Confounding models which suggest that nonhuman behaviour in metacognition tasks is driven solely by food delivery/consumption, the monkey was also observed allowing pellets to accumulate and consuming them during and after trials of all response/outcome categories (i.e., whether correct, incorrect, or escaped). This study thus bolsters previous findings that rhesus monkey behaviour in metacognition tasks is in some respects disassociated from mere food delivery/consumption, or even the avoidance of punishment. These and other observations fit well with the evolutionary status and natural proclivities of rhesus monkeys, but weaken arguments that responses in such tests are solely associated with associative mechanisms, and instead suggest more derived and controlled cognitive processing. The latter interpretation appears particularly parsimonious given the neurological adaptations of primates, as well as their highly flexible social and ecological behaviour.
A Brain Motivated to Play: Insights into the Neurobiology of Playfulness
Siviy SM
Play is an important part of normal childhood development and is seen in varied forms among many mammals. While not indispensable to normal development, playful social experiences as juveniles may provide an opportunity to develop flexible behavioral strategies when novel and uncertain situations arise as an adult. To understand the neurobiological mechanisms responsible for play and how the functions of play may relate to these neural substrates, the rat has become the model of choice. Play in the rat is easily quantified, tightly regulated, and can be modulated by genetic factors and postnatal experiences. Brain areas most likely to be involved in the modulation of play include regions within the prefrontal cortex, dorsal and ventral striatum, some regions of the amygdala, and habenula. This paper discusses what we currently know about the neurobiological substrates of play and how this can help illuminate functional questions about the putative benefits of play.
Morality, Intentionality, and Intergroup Attitudes
Killen M and Rizzo MT
Morality is at the core of what it means to be social. Moral judgments require the recognition of intentionality, that is, an attribution of the target's intentions towards another. Most research on the origins of morality has focused on intragroup morality, which involves applying morality to individuals in one's own group. Yet, increasingly, there has been new evidence that beginning early in development, children are able to apply moral concepts to members of an outgroup as well, and that this ability appears to be complex. The challenges associated with applying moral judgments to members of outgroups includes understanding group dynamics, the intentions of others who are different from the self, and having the capacity to challenge stereotypic expectations of others who are different from the ingroup. Research with children provides a window into the complexities of moral judgment and raises new questions, which are ripe for investigations into the evolutionary basis of morality.
Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks
Bell AM, Bukhari SA and Sanogo YO
Within many species, some individuals are consistently more aggressive than others. We examine whether there are differences in brain gene expression between aggressive versus nonaggressive behavioural types of individuals within a natural population of male three-spined sticklebacks (). We compared gene expression profiles of aggressive male sticklebacks to nonaggressive males in four regions of the brain (brainstem, cerebellum, diencephalon and telencephalon). Relatively few genes were differentially expressed between behavioural types in telencephalon, cerebellum and diencephalon, but hundreds of genes were differentially expressed in brainstem, a brain area involved in detecting threats. Six genes that were differentially expressed in response to a territorial intrusion in a previous study were also differentially expressed between behavioural types in this study, implying primarily non-shared but some shared molecular mechanisms. Our findings offer new insights into the molecular causes and correlates of behavioural plasticity and individual variation in behaviour.