Early development of gaze following into distant space in juvenile Greylag geese (Anser anser)

Visual co-orientation with another's gaze direction (gaze following) may provide important information about the location of food, social interactions or predators. Gaze following has been shown in a variety of mammals, but only in few bird species, and has not been tested in precocial birds at all. It has been suggested that gaze following is an anti-predator behaviour, and in Common ravens (Corvus corax) and rooks (C. frugilegus), it emerges shortly after fledging, at a time when young birds leave the predator-safe nest. However, if gaze following is adaptive, the developmental pattern should differ between altricial and precocial birds. Greylag geese (Anser anser) are highly social birds with a precocial development. Goslings move and feed independently within 24 h post-hatching, and they are highly vulnerable to aerial predators. We therefore predicted that greylag geese are capable of gaze following and that they develop this skill already pre-fledging. We experimentally tested 19 hand-raised greylag goslings for their ability to follow a conspecific's gaze when they were between 10 days and 6 weeks old. In line with our predictions, first responses were already detectable in 10-day-old goslings. Our results therefore not only demonstrate that greylag geese follow the gaze of conspecifics into distant space, but that they also develop this ability much earlier than altricial birds.     

Clark’s nutcrackers (<Emphasis Type="Italic">Nucifraga columbiana</Emphasis>) use gestures to identify the location of hidden food

Heterospecific cues, such as gaze direction and body position, may be an important source of information that an animal can use to infer the location of resources like food. The use of heterospecific cues has been largely investigated using primates, dogs, and other mammals; less is known about whether birds can also use heterospecific gestures. We tested six Clark’s nutcrackers in a two-way object-choice task using touch, point, and gaze cues to investigate whether these birds can use human gestures to find food. Most of the birds were able to use a touch gesture during the first trial of testing and were able to learn to use point and gaze (eyes and head alternation) cues after a limited number of trials. This study is the first to test a non-social corvid on the object-choice task. The performance of non-social nutcrackers is similar to that of more social and related corvids, suggesting that species with different evolutionary histories can utilize gestural information.     

Spontaneous social orienting and gaze following in ringtailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>)

Both human and nonhuman primates preferentially orient toward other individuals and follow gaze in controlled environments. Precisely where any animal looks during natural behavior, however, remains unknown. We used a novel telemetric gaze-tracking system to record orienting behavior of ringtailed lemurs (Lemur catta) interacting with a naturalistic environment. We here provide the first evidence that ringtailed lemurs, group-living prosimian primates, preferentially gaze towards other individuals and, moreover, follow other lemurs’ gaze while freely moving and interacting in naturalistic social and ecological environments. Our results support the hypothesis that stem primates were capable of orienting toward and following the attention of other individuals. Such abilities may have enabled the evolution of more complex social behavior and cognition, including theory of mind and language, which require spontaneous attention sharing. This is the first study to use telemetric eye-tracking to quantitatively monitor gaze in any nonhuman animal during locomotion, feeding, and social interaction. Moreover, this is the first demonstration of gaze following by a prosimian primate and the first to report gaze following during spontaneous interaction in naturalistic social environments. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The chimpanzee mind: in search of the evolutionary roots of the human mind

One advantage of living in a social group is the opportunity to use information provided by other individuals. Social information can be based on cues provided by a conspecific or even by a heterospecific individual (e.g., gaze direction, vocalizations, pointing gestures). Although the use of human gaze and gestures has been extensively studied in primates, and is increasingly studied in other mammals, there is no documentation of birds using these cues in a cooperative context. In this study, we tested the ability of three African gray parrots to use different human cues (pointing and/or gazing) in an object-choice task. We found that one subject spontaneously used the most salient pointing gesture (looking and steady pointing with hand at about 20 cm from the baited box). The two others were also able to use this cue after 15 trials. None of the parrots spontaneously used the steady gaze cues (combined head and eye orientation), but one learned to do so effectively after only 15 trials when the distance between the head and the baited box was about 1 m. However, none of the parrots were able to use the momentary pointing nor the distal pointing and gazing cues. These results are discussed in terms of sensitivity to joint attention as a prerequisite to understand pointing gestures as it is to the referential use of labels.     

Face detection in 2‐ to 6‐month‐old infants is influenced by gaze direction and species

Humans detect faces efficiently from a young age. Face detection is critical for infants to identify and learn from relevant social stimuli in their environments. Faces with eye contact are an especially salient stimulus, and attention to the eyes in infancy is linked to the emergence of later sociality. Despite the importance of both of these early social skills—attending to faces and attending to the eyes—surprisingly little is known about how they interact. We used eye tracking to explore whether eye contact influences infants' face detection. Longitudinally, we examined 2‐, 4‐, and 6‐month‐olds' (N = 65) visual scanning of complex image arrays with human and animal faces varying in eye contact and head orientation. Across all ages, infants displayed superior detection of faces with eye contact; however, this effect varied as a function of species and head orientation. Infants were more attentive to human than animal faces and were more sensitive to eye and head orientation for human faces compared to animal faces. Unexpectedly, human faces with both averted heads and eyes received the most attention. This pattern may reflect the early emergence of gaze following—the ability to look where another individual looks—which begins to develop around this age. Infants may be especially interested in averted gaze faces, providing early scaffolding for joint attention. This study represents the first investigation to document infants' attention patterns to faces systematically varying in their attentional states. Together, these findings suggest that infants develop early, specialized functional conspecific face detection.     

Gaze behavior and affect at 6 months: predicting clinical outcomes and language development in typically developing infants and infants at risk for autism

This paper presents follow‐up longitudinal data to research that previously suggested the possibility of abnormal gaze behavior marked by decreased eye contact in a subgroup of 6‐month‐old infants at risk for autism ( Merin, Young, Ozonoff & Rogers, 2007 ). Using eye‐tracking data and behavioral data recorded during a live mother–infant interaction involving the still‐face procedure, the predictive utility of gaze behavior and affective behaviors at 6 months was examined using diagnostic outcome data obtained longitudinally over the following 18 months. Results revealed that none of the infants previously identified as showing lower rates of eye contact had any signs of autism at outcome. In contrast, three infants who were diagnosed with autism demonstrated consistent gaze to the eye region and typical affective responses at 6 months. Individual differences in face scanning and affective responsivity during the live interaction were not related to any continuous measures of symptom frequency or symptom severity. In contrast, results of growth curve models for language development revealed significant relationships between face scanning and expressive language. Greater amounts of fixation to the mother's mouth during live interaction predicted higher levels of expressive language at outcome and greater rates of growth. These findings suggest that although gaze behavior at 6 months may not provide early markers for autism as initially conceived, gaze to the mouth in particular may be useful in predicting individual differences in language development.     

Audience effects on food caching in grey squirrels (<Emphasis Type="Italic">Sciurus carolinensis</Emphasis>): evidence for pilferage avoidance strategies

If food pilferage has been a reliable selection pressure on food caching animals, those animals should have evolved the ability to protect their caches from pilferers. Evidence that animals protect their caches would support the argument that pilferage has been an important adaptive challenge. We observed naturally caching Eastern grey squirrels (Sciurus carolinensis) in order to determine whether they used any evasive tactics in order to deter conspecific and heterospecific pilferage. We found that grey squirrels used evasive tactics when they had a conspecific audience, but not when they had a heterospecific (corvid) audience. When other squirrels were present, grey squirrels spaced their caches farther apart and preferentially cached when oriented with their backs to other squirrels, but no such effect was found when birds were present. Our data provide the first evidence that caching mammals are sensitive to the risk of pilferage posed by an audience of conspecifics, and that they utilise evasive tactics that should help to minimise cache loss. We discuss our results in relation to recent theory of reciprocal pilferage and compare them to behaviours shown by caching birds.     

Social monitoring in a primate group: the relationship between visual attention and hierarchical ranks

Social monitoring has been hypothesized to be an important component of primate social behavior. If the gaze direction of one animal can redirect the gaze of another, visual scanning of conspecifics can provide a more efficient means of locating food or predators than directly scanning the entire nonsocial environment. Social monitoring also allows distance regulation between members of a group, reducing the likelihood of agonistic encounters. Although assessment of gaze direction in freely moving primates is problematic, we were successful in assessing amounts of visual scanning among adult females of a captive, socially housed group of patas monkeys (Erythrocebus patas) using a focal sampling technique with on-the-dot recording (5-s sampling intervals). In study 1, relative amounts of scanning were assessed as subjects gazed at any other member of the group. Percentages of agreement between observers ranged from 80% to 92%, with corresponding κ values ranging from 0.74 to 0.92. In study 2, relative amounts of visual scanning were assessed so that specific targets of gaze were identified. The resultant data supported a long-standing prediction about the role of social monitoring in primate group dynamics. Lower-ranking animals gazed toward higher-ranking animals more often than vice versa. Although the specific cues eliciting social monitoring remain to be determined, visual attention in this social primate group appeared to be systematically related to hierarchical ranks, assessed by displacements. Minimally, these results suggest that patas monkeys structure their visual attention based on previous encounters with other members of their social group. While simple discrimination learning could account for these results, the demonstration of a systematic relationship between visual attention and primate social dynamics is relevant to current discussions of a primate’s understanding of conspecific gaze direction. Received: 26 January 1998 / Accepted after revision: 29 March 1998     

Recognition of partly occluded objects by fish

The ability to visually complete partly occluded objects (so-called “amodal completion”) has been documented in mammals and birds. Here, we report the first evidence of such a perceptual ability in a fish species. Fish (Xenotoca eiseni) were trained to discriminate between a complete and an amputated disk. Thereafter, the fish performed test trials in which hexagonal polygons were either exactly juxtaposed or only placed close to the missing sectors of the disk in order to produce or not produce the impression (to a human observer) of an occlusion of the missing sectors of the disk by the polygon. In another experiment, fish were first trained to discriminate between hexagonal polygons that were either exactly juxtaposed or only placed close to the missing sectors of a disk, and then tested for choice between a complete and an amputated disk. In both experiments, fish behaved as if they were experiencing visual completion of the partly occluded stimuli. These findings suggest that the ability to visually complete partly occluded objects may be widespread among vertebrates, possibly inherited in mammals, birds and fish from early vertebrate ancestors.     

The development and flexibility of gaze alternations in bonobos and chimpanzees

Infants’ early gaze alternations are one of their first steps towards a sophisticated understanding of the social world. This ability, to gaze alternate between an object of interest and another individual also attending to that object, has been considered foundational to the development of many complex social‐cognitive abilities, such as theory of mind and language. However, to understand the evolution of these abilities, it is important to identify whether and how gaze alternations are used and develop in our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Here, we evaluated the development of gaze alternations in a large, developmental sample of bonobos (N = 17) and chimpanzees (N = 35). To assess the flexibility of ape gaze alternations, we tested whether they produced gaze alternations when requesting food from a human who was either visually attentive or visually inattentive. Similarly to human infants, both bonobos and chimpanzees produced gaze alternations, and did so more frequently when a human communicative partner was visually attentive. However, unlike humans, who gaze alternate frequently from early in development, chimpanzees did not begin to gaze alternate frequently until adulthood. Bonobos produced very few gaze alternations, regardless of age. Thus, it may be the early emergence of gaze alternations, as opposed gaze alternations themselves, that is derived in the human lineage. The distinctively early emergence of gaze alternations in humans may be a critical underpinning for the development of complex human social‐cognitive abilities.     

Do common ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>) rely on human or conspecific gaze cues to detect hidden food?

The ability of non-human animals to use experimenter-given cues in object-choice tasks has recently gained interest. In such experiments, the location of hidden food is indicated by an experimenter, e.g. by gazing, pointing or touching. Whereas dogs apparently outperform all other species so far tested, apes and monkeys have problems in using such cues. Since only mammalian species have been tested, information is lacking about the evolutionary origin of these abilities. We here present the first data on object-choice tasks conducted with an avian species, the common raven. Ravens are highly competitive scavengers, possessing sophisticated cognitive skills in protecting their food caches and pilfering others’ caches. We conducted three experiments, exploring (i) which kind of cues ravens use for choosing a certain object, (ii) whether ravens use humans’ gaze for detecting hidden food and (iii) whether ravens would find hidden food in the presence of an informed conspecific who potentially provides gaze cues. Our results indicate that ravens reliably respond to humans’ touching of an object, but they hardly use point and gaze cues for their choices. Likewise, they do not perform above chance level in the presence of an informed conspecific. These findings mirror those obtained for primates and suggest that, although ravens may be aware of the gaze direction of humans and conspecifics, they apparently do not rely on this information to detect hidden food.     

Preference for spatial cues in a non-storing songbird species

Male mammals typically outperform their conspecific females on spatial tasks. A sex difference in cues used to solve the task could underlie this performance difference as spatial ability is reliant on appropriate cue use. Although comparative studies of memory in food-storing and non-storing birds have examined species differences in cue preference, few studies have investigated differences in cue use within a species. In this study, we used a one-trial associative food-finding task to test for sex differences in cue use in the great tit, Parus major. Birds were trained to locate a food reward hidden in a well covered by a coloured cloth. To determine whether the colour of the cloth or the location of the well was learned during training, the birds were presented with three wells in the test phase: one in the original location, but covered by a cloth of a novel colour, a second in a new location covered with the original cloth and a third in a new location covered by a differently coloured cloth. Both sexes preferentially visited the well in the training location rather than either alternative. As great tits prefer colour cues over spatial cues in one-trial associative conditioning tasks, cue preference appears to be related to the task type rather than being species dependent.     

The convergent evolution of neural substrates for cognition

This review describes a case of convergence in the evolution of brain and cognition. Both mammals and birds can organize their behavior flexibly over time and evolved similar cognitive skills. The avian forebrain displays no lamination that corresponds to the mammalian neocortex; hence, lamination does not seem to be a requirement for higher cognitive functions. In mammals, executive functions are associated with the prefrontal cortex. The corresponding structure in birds is the nidopallium caudolaterale. Anatomic, neurochemical, electrophysiologic and behavioral studies show these structures to be highly similar, but not homologous. Thus, despite the presence (mammals) or the absence (birds) of a laminated forebrain, ‘prefrontal’ areas in mammals and birds converged over evolutionary time into a highly similar neural architecture. The neuroarchitectonic degrees of freedom to create different neural architectures that generate identical prefrontal functions seem to be very limited.     

The contribution of private and public information in foraging by Australasian gannets

Predators that forage on foods with temporally and spatially patchy distributions may rely on private or public sources of information to enhance their chances of foraging success. Using GPS tracking, field observations, and videography, we examined potential sites and mechanisms of information acquisition in departures for foraging trips by colonially breeding Australasian gannets (Morus serrator). Analyses of the bill-fencing ceremony between mated pairs of breeding gannets did not detect correlations between parameters of this reciprocal behavior and foraging trips, as would have been predicted if gannets used this behavior as a source of private information. Instead, 60 % of the departing birds flew directly to join water rafts of other conspecific en route to the feeding grounds. The departure of solitary birds from the water rafts was synchronized (within 60 s) with the arrival of incoming foragers and also among departing birds. Furthermore, solitary departing birds from the rafts left in the same directional quadrant (90º slices) as the prior arriving (67 %) and also prior departing forager (79 %). When associated plunge dives of conspecific were visible from the colony, providing a public source of information, gannets more often departed from the water rafts in groups. Our study thus provides evidence for the use of water rafts, but not the nest site, as locations of information transfer, and also confirms the use of local enhancement as a strategy for foraging flights by Australasian gannets.     

Origins of the human pointing gesture: a training study

Despite its importance in the development of children’s skills of social cognition and communication, very little is known about the ontogenetic origins of the pointing gesture. We report a training study in which mothers gave children one month of extra daily experience with pointing as compared with a control group who had extra experience with musical activities. One hundred and two infants of 9, 10, or 11 months of age were seen at the beginning, middle, and end of this one‐month period and tested for declarative pointing and gaze following. Infants’ability to point with the index finger at the end of the study was not affected by the training but was instead predicted by infants’ prior ability to follow the gaze direction of an adult. The frequency with which infants pointed indexically was also affected by infant gaze following ability and, in addition, by maternal pointing frequency in free play, but not by training. In contrast, infants’ ability to monitor their partner’s gaze when pointing, and the frequency with which they did so, was affected by both training and maternal pointing frequency in free play. These results suggest that prior social cognitive advances, rather than adult socialization of pointing per se, determine the developmental onset of indexical pointing, but socialization processes such as imitation and adult shaping subsequently affect both infants’ ability to monitor their interlocutor’s gaze while they point and how frequently infants choose to point.     

Detour behaviour in three species of birds: quails (Coturnix sp.), herring gulls (Larus cachinnans) and canaries (Serinus canaria)

Detour behaviour is the ability of an animal to reach a goal stimulus by moving round any interposed obstacle. It has been widely studied and has been proposed as a test of insight learning in several species of mammals, but few data are available in birds. A comparative study in three species of birds, belonging to different eco-ethological niches, allows a better understanding of the cognitive mechanism of such detour behaviour. Young quails (Coturnix sp.), herring gulls (Larus cachinnans) and canaries (Serinus canaria), 1 month old, 10–25 days old and 4–6 months old, respectively, were tested in a detour situation requiring them to abandon a clear view of a biologically interesting object (their own reflection in a mirror) in order to approach that object. Birds were placed in a closed corridor, at one end of which was a barrier through which the object was visible. Four different types of barrier were used: vertical bar, horizontal bar, grid and transparent. Two symmetrical apertures placed midline in the corridor allowed the birds to adopt routes passing around the barrier. After entering the apertures, birds could turn either right or left to re-establish social contact with the object in the absence of any local sensory cues emanating from it. Quails appeared able to solve the task, though their performance depended on the type of barrier used, which appeared to modulate their relative interest in approaching the object or in exploring the surroundings. Young herring gulls also showed excellent abilities to locate spatially the out-of-view object, except when the transparent barrier was used. Canaries, on the other hand, appeared completely unable to solve the detour task, whatever barrier was in use. It is suggested that these species differences can be accounted for in terms of adaptation to a terrestrial or aerial environment.     

The Umwelt and its relevance to animal communication: introduction to special issue

This introduction applies J. von Uexküll's (1934/1957) concept of the Umwelt to the study of animal communication, particularly as it pertains to studies presented at a recent workshop on animal communication in the context of the environment. The environment is conceived broadly in the articles that follow, including the many physical and social environments in which an animal may find itself. The Umwelt concept is briefly expanded here to include also the personal microenvironment of the signaler in which the signal is embedded into the suite of concurrent nonsignaling behaviors of the individual. Other animals may even infer aspects of the signaler's own immediate Umwelt by noticing accompanying attentional cues such as the direction of eye gaze. In this way, part of the Umwelt can be accessible to companions, facilitating the communication process.     

To see or not to see: infants prefer to follow the gaze of a reliable looker

In two experiments, we examined whether 14‐month‐olds understand the subjective nature of gaze. In the first experiment, infants first observed an experimenter express happiness as she looked inside a container that either contained a toy (reliable looker condition) or was empty (unreliable looker condition). Then, infants had to follow the same experimenter's gaze to a target object located either behind or in front of a barrier. Infants in the reliable looker condition followed the experimenter's gaze behind the barrier more often than infants in the unreliable looker condition, whereas both groups followed the experimenter's gaze to the target object located in front of the barrier equally often. In the second experiment, infants did not generalize their knowledge about the unreliability of a looker to a second ‘naïve’ looker. These findings suggest that 14‐month‐old infants adapt their gaze following as a function of their past experience with the looker.     

Cues that chimpanzees do and do not use to find hidden objects

Chimpanzees follow conspecific and human gaze direction reliably in some situations, but very few chimpanzees reliably use gaze direction or other communicative signals to locate hidden food in the object-choice task. Three studies aimed at exploring factors that affect chimpanzee performance in this task are reported. In the first study, vocalizations and other noises facilitated the performance of some chimpanzees (only a minority). In the second study, various behavioral cues were given in which a human experimenter either touched, approached, or actually lifted and looked under the container where the food was hidden. Each of these cues led to enhanced performance for only a very few individuals. In the third study – a replication with some methodological improvements of a previous experiment – chimpanzees were confronted with two experimenters giving conflicting cues about the location of the hidden food, with one of them (the knower) having witnessed the hiding process and the other (the guesser) not. In the crucial test in which a third experimenter did the hiding, no chimpanzee found the food at above chance levels. Overall, in all three studies, by far the best performers were two individuals who had been raised in infancy by humans. It thus seems that while chimpanzees are very good at “behavior reading” of various sorts, including gaze following, they do not understand the communicative intentions (informative intentions) behind the looking and gesturing of others – with the possible exception of enculturated chimpanzees, who still do not understand the differential significance of looking and gesturing done by people who have different knowledge about states of affairs in the world. Received: 8 November 1999 / Accepted after revision: 24 January 2000     

An ethologist aboard hms beagle: The young darwin's observations on animal behavior

Darwin's notes from the Beagle period abound with observations on animal behavior. Although in places anecdotal and anthropomorphic, they include many detailed, lively comments of the activities of birds, reptiles, mammals, Crustacea, insects, and other invertebrates. In his comparative approach, belief in the importance of heredity, an understanding that behavior might be of assistance in taxonomy, and that it was linked with both the organism's morphology and habitat, and his attempts at experiments, Charles Darwin in his early and mid-twenties was using techniques and concepts that were to be of great significance in his later work.