Investigating the effects of prenatal testosterone exposure (via 2D:4D) and socio-relational factors on 3-6-year-old preschoolers' prosocial choices.

BACKGROUND AND AIMS: Prosocial behavior such as helping and sharing develops early in childhood. Yet very few studies have investigated physiological and relational factors shaping prosociality among children. Here, we systematically examined the role of prenatal androgen exposure alongside prestige, dominance, and friendship in 3-6-year-old preschoolers' prosocial sharing with familiar peers. METHODS: We tested a sample of 65 children, predominately of European descent. We used a cost-free direct-interaction prosocial choice task to assess children's prosocial tendencies. Second-to-fourth digit ratio (2D:4D) was used as a retrospective biomarker for prenatal androgen exposure. Prestige was measured through behavioral observations of interaction partners and visual regard, dominance through teacher questionnaires, and friendship via peer preference assessments. RESULTS: We found that children acted prosocially when tested with a familiar peer. Children with lower 2D:4D (higher prenatal androgen exposure) behaved more prosocially. Further, there were marginal associations between the donors' prosocial tendencies and their visual regard as a proxy of their prestige (positive effect) and their teacher-rated dominance relative to the recipient (negative effect). Neither age, sex, nor friendship influenced prosocial choices. CONCLUSIONS: Prenatal androgen exposure, approximated via 2D:4D, was associated with prosocial behavior. In contrast to previous research in older children, higher exposure was related to stronger prosocial tendencies, which corresponds to earlier findings on fairness in adults. Our findings point towards a potential role of sex steroids in the early development of children's social behavior, but they have to be interpreted with caution due to the small sample size of the current study. Nevertheless, they underscore the importance of integrating biological and psychological perspectives, while also highlighting the significance of studying the development of prosocial behavior within peer groups.

Why are ravens smart? Exploring the social intelligence hypothesis.

Ravens and other corvids are renowned for their 'intelligence'. For long, this reputation has been based primarily on anecdotes but in the last decades experimental evidence for impressive cognitive skills has accumulated within and across species. While we begin to understand the building blocks of corvid cognition, the question remains why these birds have evolved such skills. Focusing on Northern Ravens Corvus corax, I here try to tackle this question by relating current hypotheses on brain evolution to recent empirical data on challenges faced in the birds' daily life. Results show that foraging ravens meet several assumptions for applying social intelligence: (1) they meet repeatedly at foraging sites, albeit individuals have different site preferences and vary in grouping dynamics; (1) foraging groups are structured by dominance rank hierarchies and social bonds; (3) individual ravens memorize former group members and their relationship valence over years, deduce third-party relationships and use their social knowledge in daily life by supporting others in conflicts and intervening in others' affiliations. Hence, ravens' socio-cognitive skills may be strongly shaped by the 'complex' social environment experienced as non-breeders.

Kea, bird of versatility. Kea parrots (Nestor notabilis) show high behavioural flexibility in solving a demonstrated sequence task.

Social learning is an important aspect of dealing with the complexity of life. The transmission of information via the observation of other individuals is a cost-effective way of acquiring information. It is widespread within the animal kingdom but may differ strongly in the social learning mechanisms applied by the divergent species. Here we tested eighteen Kea (Nestor notabilis) parrots on their propensity to socially learn, and imitate, a demonstrated sequence of steps necessary to open an apparatus containing food. The demonstration by a conspecific led to more successful openings by observer birds, than control birds without a demonstration. However, all successful individuals showed great variation in their response topography and abandoned faithfully copying the task in favour of exploration. While the results provide little evidence for motor imitation they do provide further evidence for kea's propensity towards exploration and rapidly shifting solving strategies, indicative of behavioural flexibility. Supplementary Information: The online version contains supplementary material available at 10.1007/s10336-023-02127-y.

Two-action task, testing imitative social learning in kea (Nestor notabilis).

Social learning is an adaptive way of dealing with the complexity of life as it reduces the risk of trial-and-error learning. Depending on the type of information acquired, and associations formed, several mechanisms within the larger taxonomy of social learning can be distinguished. Imitation is one such process within this larger taxonomy, it is considered cognitively demanding and is associated with high-fidelity response matching. The present study reproduced a 2002 study conducted by Heyes and Saggerson, which successfully illustrated motor imitation in budgerigars (Melopsittacus undulatus). In our study, eighteen kea (Nestor notabilis) that observed a trained demonstrator remove a stopper from a test box (1) took less time from hopping on the box to feeding (response duration) in session one and (2) were faster in making a vertical removal response on the stopper once they hopped on the box (removal latency) in session one than non-observing control group individuals. In contrast to the budgerigars (Heyes and Saggerson, Ani Behav. 64:851-859, 2002) the present study could not find evidence of motor imitation in kea. The results do illustrate, however, that there were strong social effects on exploration rates indicating motivational and attentional shifts. Furthermore, the results may suggest a propensity toward emulation in contrast to motor imitation or alternatively selectivity in the application of imitation.

A comparative study of mirror self-recognition in three corvid species.

Mirror self-recognition (MSR) assessed by the Mark Test has been the staple test for the study of animal self-awareness. When tested in this paradigm, corvid species return discrepant results, with only the Eurasian magpies and the Indian house crow successfully passing the test so far, whereas multiple other corvid species fail. The lack of replicability of these positive results and the large divergence in applied methodologies calls into question whether the observed differences are in fact phylogenetic or methodological, and, if so, which factors facilitate the expression of MSR in some corvids. In this study, we (1) present new results on the self-recognition abilities of common ravens, (2) replicate results of azure-winged magpies, and (3) compare the mirror responses and performances in the mark test of these two corvid species with a third corvid species: carrion crows, previously tested following the same experimental procedure. Our results show interspecies differences in the approach of and the response to the mirror during the mirror exposure phase of the experiment as well as in the subsequent mark test. However, the performances of these species in the Mark Test do not provide any evidence for their ability of self-recognition. Our results add to the ongoing discussion about the convergent evolution of MSR and we advocate for consistent methodologies and procedures in comparing this ability across species to advance this discussion.

Social dynamics impact scolding behaviour in captive groups of common ravens (Corvus corax).

BACKGROUND: Predator avoidance can have immense impacts on fitness, yet individual variation in the expression of anti-predator behaviour remains largely unexplained. Existing research investigating learning of novel predators has focused either on individuals or groups, but not both. Testing in individual settings allows evaluations of learning or personality differences, while testing in group settings makes it impossible to distinguish any such individual differences from social dynamics. In this study, we investigate the effect of social dynamics on individual anti-predator behaviour. We trained 15 captive ravens to recognize and respond to a novel experimental predator and then exposed them to this predator in both group and isolation settings across 1.5 years to tease apart individual differences from social effects and evaluate two hypotheses: (1) weaker anti-predator responses of some individuals in the group occurred, because they failed to recognize the experimental predator as a threat, leading to weak responses when separated, or (2) some individuals had learned the new threat, but their scolding intensity was repressed in the group trials due to social dynamics (such as dominance rank), leading to increased scolding intensity when alone. RESULTS: We found that dominance significantly influences scolding behaviour in the group trials; top-ranked individuals scold more and earlier than lower ranking ones. However, in the separation trials scolding duration is no longer affected by rank. CONCLUSIONS: We speculate that, while top-ranked individuals use their anti-predator responses to signal status in the group, lower-ranking ravens may be suppressed from, or are less capable of, performing intense anti-predator behaviour while in the group. This suggests that, in addition to its recruitment or predator-deterrent effects, alarm calling may serve as a marker of individual quality to conspecifics.

Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus).

The proximate mechanisms underlying animal personalities, i.e. consistent inter-individual differences in behaviour, are a matter of discussion. Brain lateralization, expressed as the preferred use of the contralateral limb, has been suggested as one of these mechanisms. In this study, we measured a proxy of brain lateralization in captive common marmosets (N = 28) by testing hand preference in a simple food-reaching task and evaluated personality by coding a wide range of behaviours observed in daily situations. We explored the links between personality and both direction and strength of hand preference, as well as age and sex, using linear models. Principal component analysis revealed that the stable behavioural variables were organized in three personality dimensions: Agreeableness, Extraversion and Neuroticism. Regarding hand preference, 14 individuals were left-handed, seven were right-handed and seven were ambilateral. Contrary to our predictions, we did not find any relationship between personality scores and hand preference or sex. Instead, age was a significant predictor of personality scores, with older individuals being more agreeable and less extraverted. The link between brain lateralization and personality seems to be equivocal and dependent on personality and brain lateralization assessment methods. Further examinations of other proximate mechanisms, such as physiology or (epi)genetics, may elucidate what drives personality variation in common marmosets.

The spatial and temporal exploitation of anthropogenic food sources by common ravens (Corvus corax) in the Alps.

BACKGROUND: Anthropogenic food sources (AFSs) are widespread in human-transformed landscapes and the current scale at which they occur drives ecological change at the individual, population, and community levels. AFSs are exploited extensively by common ravens, Corvus corax. Understanding how raven populations use AFSs can provide insight into their ecological responses to AFSs. METHODS: We equipped 81 ravens in the Austrian Alps with GPS-transmitters over a period of 2.75 years. Using these tracking data, we investigated how cohort differences (i.e., age, sex, and origin) and seasonal changes influence raven movement patterns (i.e., occurrence distribution and maximum daily displacement) and AFS-use (i.e., number of AFSs visited and probability of being present at any AFS) at 45 extensively exploited sites. RESULTS: We found that proxies for experience and dominance, inferred by age (i.e., juvenile versus adult) and origin (i.e., wild-caught versus captive-bred-released) cohorts, influenced movement patterns and the number of AFSs visited. However, all individuals were equally likely to be present at AFSs, highlighting the importance of AFSs for non-breeders in the study population. Seasonal changes in environmental conditions that affect energetic demands, the availability of natural and anthropogenic food, and foraging competition,  influenced individuals' occurrence distributions and AFS-use. We found that under harsher conditions in autumn and winter, individuals ranged wider and depended on AFSs to a larger degree. However, contrary to expectation, they were less likely to be present at AFSs in these seasons compared to spring and summer, suggesting a trade-off between time spent moving and exploiting resources. We attribute the small ranging movements exhibited by non-breeders in spring and summer to the presence of highly territorial and socially dominant breeders. As breeders mostly stay and forage within their territories during these seasons, competition at AFSs decrease, thereby increasing the likelihood of individuals being present at any AFS. CONCLUSIONS: We emphasize that movement and AFS-use differ according to cohort differences and the seasonality of the environment. Our results highlight that predictable AFSs affect foraging strategies among non-breeding ravens. The extent of AFS-exploitation among non-breeding ravens in our study emphasize the potential of AFSs in shaping raven movement and resource-use.

Early social environment affects attention to social cues in juvenile common ravens, Corvus corax.

Social competence, i.e. defined as the ability to adjust the expression of social behaviour to the available social information, is known to be influenced by early-life conditions. Brood size might be one of the factors determining such early conditions, particularly in species with extended parental care. We here tested in ravens whether growing up in families of different sizes affects the chicks' responsiveness to social information. We experimentally manipulated the brood size of 13 captive raven families, creating either small or large families. Simulating dispersal, juveniles were separated from their parents and temporarily housed in one of two captive non-breeder groups. After five weeks of socialization, each raven was individually tested in a playback setting with food-associated calls from three social categories: sibling, familiar unrelated raven they were housed with, and unfamiliar unrelated raven from the other non-breeder aviary. We found that individuals reared in small families were more attentive than birds from large families, in particular towards the familiar unrelated peer. These results indicate that variation in family size during upbringing can affect how juvenile ravens value social information. Whether the observed attention patterns translate into behavioural preferences under daily life conditions remains to be tested in future studies.

No Evidence for Contagious Yawning in Juvenile Ravens (Corvus corax): An Observational Study.

The overt and reflexive matching of behaviors among conspecifics has been observed in a growing number of social vertebrates, including avian species. In general, behavioral contagion-such as the spread of yawning-may serve important functions in group synchronization and vigilance behavior. Here, we performed an exploratory study to investigate yawn contagion among 10 captive juvenile ravens (Corvus corax), across two groups. Using observational methods, we also examined the contagiousness of three other distinct behaviors: stretching, scratching, and shaking. A total of 44 20 min observations were made across both groups, including 28 in the morning and 16 in the afternoon. The time and occurrence of all the behaviors from each bird were coded, and the temporal pattern of each behavior across both groups was then analyzed to assess the degree of social contagion. Overall, we found no evidence for contagious yawning, stretching, scratching, or shaking. However, yawns were relatively infrequent per observation (0.052 ± 0.076 yawns/bird) and thus experimental methods should be used to support this finding.

Personality and social environment predict cognitive performance in common marmosets (Callithrix jacchus).

Consistent inter-individual variation in cognition has been increasingly explored in recent years in terms of its patterns, causes and consequences. One of its possible causes are consistent inter-individual differences in behaviour, also referred to as animal personalities, which are shaped by both the physical and the social environment. The latter is particularly relevant for group-living species like common marmosets (Callithrix jacchus), apt learners that display substantial variation in both their personality and cognitive performance, yet no study to date has interlinked these with marmosets' social environment. Here we investigated (i) consistency of learning speed, and (ii) whether the PCA-derived personality traits Exploration-Avoidance and Boldness-Shyness as well as the social environment (i.e., family group membership) are linked with marmosets' speed of learning. We tested 22 individuals in series of personality and learning-focused cognitive tests, including simple motor tasks and discrimination learning tasks. We found that these marmosets showed significant inter-individual consistency in learning across the different tasks, and that females learned faster than males. Further, bolder individuals, and particularly those belonging to certain family groups, learned faster. These findings indicate that both personality and social environment affect learning speed in marmosets and could be important factors driving individual variation in cognition.

Dominance in a socially dynamic setting: hierarchical structure and conflict dynamics in ravens' foraging groups.

Dominance hierarchies typically emerge in systems where group members regularly encounter and compete for resources. In birds, the 'open' and dynamic structure of foraging groups may prevent the emergence of structured hierarchies, although this assumption have hardly been tested. We report on agonistic data for ravens Corvus corax, collected over two 18-month periods for 183 marked individuals of a wild (fluid) population and 51 birds from six captive (stable) groups. We show that the dominance structure (steep and transitive) in wild foraging groups is strikingly similar to that found in captivity. In the wild, we found that higher ranks are mainly occupied by males, older and more aggressive individuals that also tend to receive fewer aggressions. Exploring the mechanisms sustaining the wild dominance structure, we confirmed that males are more aggressive than females and, with age, tend to receive fewer aggressions than females. Males that are about to leave the foraging groups for some months are less aggressive than newcomers or locals, while newcomers are specifically targeted by aggressions in their first year (as juveniles). Taken together, our results indicate that the socially dynamic conditions ravens face during foraging do not hinder, but provide opportunities for, using (advanced) social cognition. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Socio-ecological correlates of neophobia in corvids.

Behavioral responses to novelty, including fear and subsequent avoidance of novel stimuli, i.e., neophobia, determine how animals interact with their environment. Neophobia aids in navigating risk and impacts on adaptability and survival. There is variation within and between individuals and species; however, lack of large-scale, comparative studies critically limits investigation of the socio-ecological drivers of neophobia. In this study, we tested responses to novel objects and food (alongside familiar food) versus a baseline (familiar food alone) in 10 corvid species (241 subjects) across 10 labs worldwide. There were species differences in the latency to touch familiar food in the novel object and novel food conditions relative to the baseline. Four of seven socio-ecological factors influenced object neophobia: (1) use of urban habitat (versus not), (2) territorial pair versus family group sociality, (3) large versus small maximum flock size, and (4) moderate versus specialized caching (whereas range, hunting live animals, and genus did not), while only maximum flock size influenced food neophobia. We found that, overall, individuals were temporally and contextually repeatable (i.e., consistent) in their novelty responses in all conditions, indicating neophobia is a stable behavioral trait. With this study, we have established a network of corvid researchers, demonstrating potential for further collaboration to explore the evolution of cognition in corvids and other bird species. These novel findings enable us, for the first time in corvids, to identify the socio-ecological correlates of neophobia and grant insight into specific elements that drive higher neophobic responses in this avian family group. VIDEO ABSTRACT.

Carrion Crows and Azure-Winged Magpies Show No Prosocial Tendencies When Tested in a Token Transfer Paradigm.

To study the evolution of humans' cooperative nature, researchers have recently sought comparisons with other species. Studies investigating corvids, for example, showed that carrion crows and azure-winged magpies delivered food to group members when tested in naturalistic or simple experimental paradigms. Here, we investigated whether we could replicate these positive findings when testing the same two species in a token transfer paradigm. After training the birds to exchange tokens with an experimenter for food rewards, we tested whether they would also transfer tokens to other birds, when they did not have the opportunity to exchange the tokens themselves. To control for the effects of motivation, and of social or stimulus enhancement, we tested each individual in three additional control conditions. We witnessed very few attempts and/or successful token transfers, and those few instances did not occur more frequently in the test condition than in the controls, which would suggest that the birds lack prosocial tendencies. Alternatively, we propose that this absence of prosociality may stem from the artificial nature and cognitive complexity of the token transfer task. Consequently, our findings highlight the strong impact of methodology on animals' capability to exhibit prosocial tendencies and stress the importance of comparing multiple experimental paradigms.

Measuring salivary mesotocin in birds - Seasonal differences in ravens' peripheral mesotocin levels.

Oxytocin is involved in a broad array of social behaviours. While saliva has been used regularly to investigate the role of oxytocin in social behaviour of mammal species, so far, to our knowledge, no-one has tried to measure its homolog, mesotocin, in birds' saliva. Therefore, in this study we measured salivary mesotocin in common ravens (Corvus corax), and subsequently explored its link to three aspects of raven sociality. We trained ravens (n = 13) to voluntarily provide saliva samples and analysed salivary mesotocin with a commercial oxytocin enzyme-immunoassay kit, also suitable for mesotocin. After testing parallelism and recovery, we investigated the effect of bonding status, sex and season on mesotocin levels. We found that mesotocin was significantly more likely to be detected in samples taken during the breeding season (spring) than during the mating season (winter). In those samples in which mesotocin was detected, concentrations were also significantly higher during the breeding than during the mating season. In contrast, bonding status and sex were not found to relate to mesotocin detectability and concentrations. The seasonal differences in mesotocin correspond to behavioral patterns known to be associated with mesotocin/oxytocin, with ravens showing much more aggression during the mating season while being more tolerant of conspecifics in the breeding season. We show for the first time that saliva samples can be useful for the non-invasive determination of hormone levels in birds. However, the rate of successfully analysed samples was very low, and collection and analysis methods will benefit from further improvements.

Brain size and neuron numbers drive differences in yawn duration across mammals and birds.

Recent studies indicate that yawning evolved as a brain cooling mechanism. Given that larger brains have greater thermolytic needs and brain temperature is determined in part by heat production from neuronal activity, it was hypothesized that animals with larger brains and more neurons would yawn longer to produce comparable cooling effects. To test this, we performed the largest study on yawning ever conducted, analyzing 1291 yawns from 101 species (55 mammals; 46 birds). Phylogenetically controlled analyses revealed robust positive correlations between yawn duration and (1) brain mass, (2) total neuron number, and (3) cortical/pallial neuron number in both mammals and birds, which cannot be attributed solely to allometric scaling rules. These relationships were similar across clades, though mammals exhibited considerably longer yawns than birds of comparable brain and body mass. These findings provide further evidence suggesting that yawning is a thermoregulatory adaptation that has been conserved across amniote evolution.

Temporal consistency and ecological validity of personality structure in common marmosets (Callithrix jacchus): A unifying field and laboratory approach.

Personality in animals has been extensively researched in recent decades. Temporal consistency of behaviors is almost always part of the personality definition and is usually explored in several different testing sessions or observation periods. However, it is still unclear whether the obtained personality constructs are stable across several years, which might be especially important for long-living animals, such as primates. Further, little is known on whether the personality structures obtained in the laboratory reflect the structures obtained under ecologically relevant conditions in the wild. Therefore, we conducted a battery of personality tests on common marmosets (Callithrix jacchus) (N = 27), compared it with a test battery conducted 4 years beforehand on a subset of animals in captivity (N = 13) and ran an adapted version under field conditions at Baracuhy Biological Field Station, Brazil (N = 18). Under captive conditions, we found a remarkably similar personality structure across 4 testing years. Further, we found high long-term temporal consistency in the first two personality components, Boldness and Exploration; however, monkeys that changed their social (i.e., breeding) status between the two testing periods showed a significant increase in Boldness scores. Under field conditions, we found a somewhat similar personality structure as compared to the laboratory, which to some extent corroborates ecological validity of our personality test design. Nevertheless, whether the structure in the wild is suppressed or expanded in comparison to captivity, and in which way the social setting influences personality structure, should be further explored. Taken together, our results contribute to the discussion about the reliability and ecological validity of personality structures in nonhuman primates.

Who is crying wolf? Seasonal effect on antipredator response to age-specific alarm calls in common ravens, Corvus corax.

Communication about threats including those posed by the presence of predators occurs mainly through acoustic signals called alarm calls. The comprehension of these calls by receivers and their rapid antipredator response are crucial in terms of survival. However, to avoid overreaction, individuals should evaluate whether or not an antipredator response is needed by paying attention to who is calling. For instance, we could expect adults to be more experienced with predator encounters than juveniles and thus elicit stronger antipredator responses in others when alarming. Similarly, we could expect a stronger response to alarm calls when more than one individual is calling. To test these assumptions, we applied a playback experiment to wild ravens, in which we manipulated the age class (adult or juvenile) and the number (one or two) of the callers. Our results revealed a seasonal effect of age class but no effect of number of callers. Specifically, the ravens responded with stronger antipredator behaviour (vigilance posture) towards alarm calls from adults as compared to juveniles in summer and autumn, but not in spring. We discuss alternative interpretations for this unexpected seasonal pattern and argue for more studies on call-based communication in birds to understand what type of information is relevant under which conditions.

Early evidence for emotional play contagion in juvenile ravens.

Perceiving, evaluating and reacting towards conspecifics' emotional states are important challenges of social group living. Emotional contagion describes an alignment of emotional states between individuals and is widely believed to be based on behavioral synchronization, i.e., behavioral contagion. As basic empathy-like processes, the occurrence of both forms of contagion seems to underlie early ontogenetic trajectories in humans and non-human species. In the present study, we assessed play as a context for studying the development of emotional contagion and its interlink with behavioral contagion in ten juvenile common ravens. Ravens are exceptional players that engage in all three forms of play: object, locomotion and social play. To assess potential ontogenetic patterns of both behavioral and emotional contagion, we tested juvenile ravens at two different periods of early development, at three- and six-month post-hatching. We elicited object play in one or several ravens (demonstrators) in a standardized experimental environment, using a playground setup. At both test ages, we found evidence for emotional contagion as observer ravens showed an increase of locomotion and social play after we provided the demonstrator(s) with the playground setup, but no significant changes in the amount of object play. Hence, observers did not copy motor patterns from demonstrator(s) but engaged in other forms of play. Our findings speak for a transfer of a general mood state in the context of play in ravens as young as 3 months and against behavioral mimicry as a precondition for emotional contagion.