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.

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.

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.

Negative emotional contagion and cognitive bias in common ravens (Corvus corax).

Emotional contagion is described as an emotional state matching between subjects, and has been suggested to facilitate communication and coordination in complex social groups. Empirical studies typically focus on the measurement of behavioral contagion and emotional arousal, yet, while highly important, such an approach often disregards an additional evaluation of the underlying emotional valence. Here, we studied emotional contagion in ravens by applying a judgment bias paradigm to assess emotional valence. We experimentally manipulated positive and negative affective states in demonstrator ravens, to which they responded with increased attention and interest in the positive condition, as well as increased redirected behavior and a left-eye lateralization in the negative condition. During this emotion manipulation, another raven observed the demonstrator's behavior, and we used a bias paradigm to assess the emotional valence of the observer to determine whether emotional contagion had occurred. Observers showed a pessimism bias toward the presented ambiguous stimuli after perceiving demonstrators in a negative state, indicating emotional state matching based on the demonstrators' behavioral cues and confirming our prediction of negative emotional contagion. We did not find any judgment bias in the positive condition. This result critically expands upon observational studies of contagious play in ravens, providing experimental evidence that emotional contagion is present not only in mammalian but also in avian species. Importantly, this finding also acts as a stepping stone toward understanding the evolution of empathy, as this essential social skill may have emerged across these taxa in response to similar socioecological challenges.

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.

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.

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.

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.

Common marmosets are sensitive to simple dependencies at variable distances in an artificial grammar.

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies ('consistent' and 'inconsistent', respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

Competition is crucial for social comparison processes in long-tailed macaques.

Humans modulate their self-evaluations and behaviour as a function of conspecific presence and performance. In this study, we tested for the presence of human-like social comparison effects in long-tailed macaques ( Macaca fascicularis). The monkeys' task was to extract food from an apparatus by pulling drawers within reach and we measured latency between drawer pulls. Subjects either worked on the task with a partner who could access the apparatus from an adjacent cage, worked in the absence of a conspecific but with food moving towards the partner's side or worked next to a partner who was denied apparatus access. We further manipulated partner performance and competitiveness of the set-up. We found no indication that long-tailed macaques compare their performance to the performance of conspecifics. They were not affected by the mere presence of the partner but they paid close attention to the partner's actions when they were consequential for food availability. If social comparison processes are present in long-tailed macaques, the present study suggests they may only manifest in situations involving direct competition and would thus be different from social comparisons in humans, which manifest also in the absence of direct competition, for example in evaluative contexts.

Attacked ravens flexibly adjust signalling behaviour according to audience composition.

A fundamental attribute of social intelligence is the ability to monitor third-party relationships, which has been repeatedly demonstrated in primates, and recently also in captive ravens. It is yet unknown how ravens make use of this ability when dealing with different types of social relationships simultaneously during complex real-life situations. Free-ranging non-breeder ravens live in societies characterized by high fission-fusion dynamics and structured by age, pair-bond status and kinship. Here, we show that free-ranging ravens modify communication during conflicts according to audience composition. When being attacked by dominant conspecifics, victims of aggression signal their distress via defensive calls. Victims increased call rates when their kin were in the bystander audience, but reduced call rates when the bystanders were bonding partners of their aggressors. Hence, ravens use social knowledge flexibly and probably based on their own need (i.e. alert nearby allies and avoid alerting nearby rivals).

Raven food calls indicate sender's age and sex.

BACKGROUND: Acoustic parameters of animal signals have been shown to correlate with various phenotypic characteristics of the sender. These acoustic characteristics can be learned and categorized and thus are a basis for perceivers' recognition abilities. One of the most demanding capacities is individual recognition, achievable only after repeated interactions with the same individual. Still, class-level recognition might be potentially important to perceivers who have not previously encountered callers but can classify unknown individuals according to the already learned categories. Especially for species with high fission-fusion dynamics that repeatedly encounter unknown individuals it may be advantageous to develop class-level recognition. We tested whether frequency-, temporal-, and amplitude-related acoustic parameters of vocalizations emitted by ravens, a species showing high fission-fusion dynamics in non-breeder aggregations, are connected to phenotypic characteristics and thus have the potential for class-level recognition. RESULTS: The analysis of 418 food calls revealed that some components summarizing acoustic parameters were differentiated by age-classes and sex. CONCLUSIONS: Together, the results provide evidence for the co-variation of vocal characteristics and respective sex and age categories, a prerequisite for class-level recognition in perceivers. Perceivers that are ignorant of the caller's identity can thus potentially recognize these class-level differences for decision-making processes in feeding contexts.

A technological framework for running and analyzing animal head turning experiments.

Head turning experiments are widely used to test the cognition of both human infants and non-human animal species. Monitoring head turns allows researchers to non-invasively assess attention to acoustic or visual stimuli. In the majority of head turning experiments, the head direction analyses have been accomplished manually, which is extremely labor intensive and can be affected by subjectivity or other human errors and limitations. In the current study, we introduce an open-source computer program for measuring head directions of freely moving animals including common marmoset monkeys (Callithrix jacchus), American alligators (Alligator mississippiensis), and Mongolian gerbils (Meriones unguiculatus) to reduce human effort and time in video coding. We also illustrate an exemplary framework for an animal head turning experiment with common marmoset monkeys. This framework incorporates computer-aided processes of data acquisition, preprocessing, and analysis using the aforementioned software and additional open-source software and hardware.

Calls during agonistic interactions vary with arousal and raise audience attention in ravens.

BACKGROUND: Acoustic properties of vocalizations can vary with the internal state of the caller, and may serve as reliable indicators for a caller's emotional state, for example to prevent conflicts. Thus, individuals may associate distinct characteristics in acoustic signals of conspecifics with specific social contexts, and adjust their behaviour accordingly to prevent escalation of conflicts. Common ravens (Corvus corax) crowd-forage with individuals of different age classes, sex, and rank, assemble at feeding sites, and engage in agonistic interactions of varying intensity. Attacked individuals frequently utter defensive calls in order to appease the aggressor. Here, we investigated if acoustic properties of defensive calls change with varying levels of aggression, and if bystanders respond to these changes. RESULTS: Individuals were more likely to utter defensive calls when the attack involved contact aggression, and when the attacker was higher in rank than the victim. Defensive calls produced during intense conflicts were longer and uttered at higher rates, and showed higher fundamental frequency- and amplitude-related measures than calls uttered during low-intensity aggression, indicating arousal-based changes in defensive calls. Playback experiments showed that ravens were more likely to react in response to defensive calls with higher fundamental frequency by orientating towards the speakers as compared to original calls and calls manipulated in duration. CONCLUSIONS: Arousal-based changes are encoded in acoustic parameters of defensive calls in attacked ravens, and bystanders in the audience pay attention to the degree of arousal in attacked conspecifics. Our findings imply that common ravens can regulate conflicts with conspecifics by means of vocalizations, and are able to gather social knowledge from conspecific calls.

Responses of urban crows to con- and hetero-specific alarm calls in predator and non-predator zoo enclosures.

Urban animals and birds in particular are able to cope with diverse novel threats in a city environment such as avoiding novel, unfamiliar predators. Predator avoidance often includes alarm signals that can be used also by hetero-specifics, which is mainly the case in mixed-species flocks. It can also occur when species do not form flocks but co-occur together. In this study we tested whether urban crows use alarm calls of conspecifics and hetero-specifics (jackdaws, Corvus monedula) differently in a predator and a non-predator context with partly novel and unfamiliar zoo animal species. Birds were tested at the Tiergarten Schönbrunn in the city of Vienna by playing back con- and hetero-specific alarm calls and control stimuli (great tit song and no stimuli) at predator (wolf, polar bear) and non-predator (eland antelope and cranes, peccaries) enclosures. We recorded responses of crows as the percentage of birds flying away after hearing the playback (out of those present before the playback) and as the number of vocalizations given by the present birds. A significantly higher percentage of crows flew away after hearing either con- or hetero-specific alarm calls, but it did not significantly differ between the predator and the non-predator context. Crows treated jackdaw calls just as crow calls, indicating that they make proper use of hetero-specific alarm calls. Responding similarly in both contexts may suggest that the crows were uncertain about the threat a particular zoo animal represents and were generally cautious. In the predator context, however, a high percentage of crows also flew away upon hearing the great tit control song which suggests that they may still evaluate those species which occasionally killed crows as more dangerous and respond to any conspicuous sound.

Adjusting foraging strategies: a comparison of rural and urban common mynas (Acridotheres tristis).

Establishment in urbanized environments is associated with changes in physiology, behaviour, and problem-solving. We compared the speed of learning in urban and rural female common mynas, Acridotheres tristis, using a standard visual discrimination task followed by a reversal learning phase. We also examined how quickly each bird progressed through different stages of learning, including sampling and acquisition within both initial and reversal learning, and persistence following reversal. Based on their reliance on very different food resources, we expected urban mynas to learn and reversal learn more quickly but to sample new contingencies for proportionately longer before learning them. When quantified from first presentation to criterion achievement, urban mynas took more 20-trial blocks to learn the initial discrimination, as well as the reversed contingency, than rural mynas. More detailed analyses at the level of stage revealed that this was because urban mynas explored the novel cue-outcome contingencies for longer, and despite transitioning faster through subsequent acquisition, remained overall slower than rural females. Our findings draw attention to fine adjustments in learning strategies in response to urbanization and caution against interpreting the speed to learn a task as a reflection of cognitive ability.

Apes perform like infants in false-belief tasks.

Although the extent to which some nonhuman animals understand mental states is currently under debate, attributing false beliefs has been considered to be beyond their limits. A recent study by Krupenye, Kano, Hirata, Call, and Tomasello (Science, 354, 110-114, 2016) shows that great apes pass a false-belief task when they are tested with an anticipatory-looking paradigm developed for nonverbal human infants.

Loner or socializer? Ravens' adrenocortical response to individual separation depends on social integration.

Non-breeding common ravens (Corvus corax) live in complex social groups with a high degree of fission-fusion dynamics. They form valuable relationships and alliances with some conspecifics, while taking coordinated action against others. In ravens, affiliates reconcile their conflicts, console each other after conflicts with a third party, and provide each other with social support - all behaviors that presumably reduce corticosterone levels and alleviate stress. However, how well an individual is socially integrated in a (sub)group might vary substantially. This raises the question whether the social integration of a raven affects its stress responses to fission-fusion dynamics. The present study aims to investigate this effect experimentally by separating single ravens (n=16) individually from their group for four days and subsequently reintroducing them. To determine stress response patterns in the separated individuals we measured the amounts of immunoreactive corticosterone metabolites (CM) in droppings. We compared two enzyme immunoassays, which we validated by conducting an ACTH challenge, and finally decided to apply an 11-oxoetiocholanolone enzyme immunoassay. Additionally, we determined levels of social integration using focal observations. Our findings suggest that a strong social integration is related to low CM levels when the individuals are within the group and high levels during separations, implying that separation leads to stress in these birds. In contrast, poorly socially integrated ravens seem to exhibit the opposite pattern, indicating that to them group living is more stressful than being temporarily separated. We, therefore, conclude that the birds' adrenocortical activity is modulated by their social integration.