Facial Recognition in a Group-Living Cichlid Fish

The theoretical underpinnings of the mechanisms of sociality, e.g. territoriality, hierarchy, and reciprocity, are based on assumptions of individual recognition. While behavioural evidence suggests individual recognition is widespread, the cues that animals use to recognise individuals are established in only a handful of systems. Here, we use digital models to demonstrate that facial features are the visual cue used for individual recognition in the social fish Neolamprologus pulcher. Focal fish were exposed to digital images showing four different combinations of familiar and unfamiliar face and body colorations. Focal fish attended to digital models with unfamiliar faces longer and from a further distance to the model than to models with familiar faces. These results strongly suggest that fish can distinguish individuals accurately using facial colour patterns. Our observations also suggest that fish are able to rapidly (≤ 0.5 sec) discriminate between familiar and unfamiliar individuals, a speed of recognition comparable to primates including humans.     

Crows cross-modally recognize group members but not non-group members

Recognizing other individuals by integrating different sensory modalities is a crucial ability of social animals, including humans. Although cross-modal individual recognition has been demonstrated in mammals, the extent of its use by birds remains unknown. Herein, we report the first evidence of cross-modal recognition of group members by a highly social bird, the large-billed crow (Corvus macrorhynchos). A cross-modal expectancy violation paradigm was used to test whether crows were sensitive to identity congruence between visual presentation of a group member and the subsequent playback of a contact call. Crows looked more rapidly and for a longer duration when the visual and auditory stimuli were incongruent than when congruent. Moreover, these responses were not observed with non-group member stimuli. These results indicate that crows spontaneously associate visual and auditory information of group members but not of non-group members, which is a demonstration of cross-modal audiovisual recognition of group members in birds.     

Social learning spreads knowledge about dangerous humans among American crows

Individuals face evolutionary trade-offs between the acquisition of costly but accurate information gained firsthand and the use of inexpensive but possibly less reliable social information. American crows (Corvus brachyrhynchos) use both sources of information to learn the facial features of a dangerous person. We exposed wild crows to a novel 'dangerous face' by wearing a unique mask as we trapped, banded and released 7-15 birds at five study sites near Seattle, WA, USA. An immediate scolding response to the dangerous mask after trapping by previously captured crows demonstrates individual learning, while an immediate response by crows that were not captured probably represents conditioning to the trapping scene by the mob of birds that assembled during the capture. Later recognition of dangerous masks by lone crows that were never captured is consistent with horizontal social learning. Independent scolding by young crows, whose parents had conditioned them to scold the dangerous mask, demonstrates vertical social learning. Crows that directly experienced trapping later discriminated among dangerous and neutral masks more precisely than did crows that learned through social means. Learning enabled scolding to double in frequency and spread at least 1.2 km from the place of origin over a 5 year period at one site.     

Categorical learning between 'male' and 'female' photographic human faces in jungle crows (Corvus macrorhynchos)

We trained jungle crows to discriminate among photographs of human face according to their sex in a simultaneous two-alternative task to study their categorical learning ability. Once the crows reached a discrimination criterion (greater than or equal to 80% correct choices in two consecutive sessions; binomial probability test, p < .05), they next received generalization and transfer tests (i.e., greyscale, contour, and ‘full’ occlusion) in Experiment 1 followed by a ‘partial’ occlusion test in Experiment 2 and random stimuli pair test in Experiment 3. Jungle crows learned the discrimination task in a few trials and successfully generalized to novel stimuli sets. However, all crows failed the greyscale test and half of them the contour test. Neither occlusion of internal features of the face, nor randomly pairing of exemplars affected discrimination performance of most, if not all crows. We suggest that jungle crows categorize human face photographs based on perceptual similarities as other non-human animals do, and colour appears to be the most salient feature controlling discriminative behaviour. However, the variability in the use of facial contours among individuals suggests an exploitation of multiple features and individual differences in visual information processing among jungle crows.     

Formation of linear dominance relationship in captive jungle crows (Corvus macrorhynchos): implications for individual recognition

Jungle crows (Corvus macrorhynchos) flexibly change their social forms depending on their age, time of the day, and the season. In the daytime, paired adults behave territorially and unpaired subadults form small flocks of ten birds, whereas at night hundreds of birds roost together. In the breeding season, pairings remain in their nest all day. This fission-fusion raises questions about the underlying social structure and the cognitive capability of jungle crows. In this study, dyadic encounters were used to investigate dominance relationships (linear or non-linear) and the underlying mechanisms in captive jungle crows. Fourteen crows were tested in 455 encounters (i.e., 5 encounters per dyad), and a stable linear dominance relationship emerged. Sex and aggressiveness were determinants as individual characteristics for dominance formation. Males dominated females, and more aggressive individuals dominated less aggressive ones. Aggressive interactions in dyads occurred primarily during the first encounter and drastically declined during subsequent encounters without any signs of a confidence effect. These results suggest that, in captive jungle crow, a linear form of dominance is intrinsically determined by sex and aggressiveness and maintained extrinsically by memories of past outcomes associated with specific individuals, implying individual recognition.     

Acoustic communication in the Kittiwake <Emphasis Type="Italic">Rissa tridactyla</Emphasis>: potential cues for sexual and individual signatures in long calls

Sex and individual recognition systems vary among species and can have various functions in different contexts. In order to determine the basis of identification by voice in the Kittiwake (Rissa tridactyla), the greeting calls of 32 individuals (18 males and 14 females) were recorded in May–June 2004 on the Kittiwake colony of Hornøya island (Barents sea) and analysed. On the basis of coefficient of variation calculations and discriminant analyses, we show (1) that calls are sexually dimorphic and that the dimorphism is mainly based on the value of the fundamental frequency, and (2) that calls are individually distinct, individuality being due to a complex of temporal and frequency parameters located in different parts of the signal. This coding strategy is discussed in the context of the colonial breeding habitat of the species.     

Diverse sensory cues for individual recognition

To be social, the ability to recognize and discriminate conspecific individuals is indispensable in social animals, including primates, rodents, birds, fish, and social insects which live in societies or groups. Recent studies using molecular biology, genetics, in vivo and in vitro physiology, and behavioral neuroscientific approaches have provided detailed insights into how animals process and recognize the information of individuals. Here, we review the most distinct sensory modalities for individual recognition in animals, namely, olfaction and vision. In the case of rodents, two polymorphic gene complexes have been identified in their urine as the key and essential pheromonal components for individual recognition: the major histocompatibility complex (MHC) and the major urinary protein (MUP). Animals flexibly utilize MHC and/or MUP, which are detected by the main olfactory epithelium (MOE) and/or the vomeronasal organ (VNO) for various types of social recognition, such as strain recognition, kin recognition, and individual recognition. In contrast, primates, including humans, primarily use facial appearance to identify others. Face recognition in humans and other animals is naturally unique from genetic, cognitive, developmental, and functional points of view. Importantly note that nurture effects during growth phase such as social experience and environment can also shape and tune this special cognitive ability, in order to distinguish subtle differences between individuals. In this review, we address such unique nature and nurture mechanisms for individual recognition.     

Morphology of the Hooded crow Corvus corone cornix in relation to age, sex and latitude

The morphological variation of the Hooded crow at Trondheim, Norway, was studied, based on a sample of 734 birds collected during a six year period. Mouth colour, plumage colour, skull thickness and feather length were found to be characters which could readily be used to separate juveniles from adults. Females aged 15–19 months had a thinner skull roof than older female birds. Low coefficients of variation were found for the lengths of the third primary and of the tail feathers. A discriminant analysis showed that of the various body dimensions studied bill height and bill length distinguished the sexes most precisely. A high degree of sexual dimorphism was also found to exist in body weight and in the thickness of the skull roof.
Those body structures which develop at about the same stage during the juvenile growth period were associated with the same principal component, viz. the lengths of bony structures, parts that develop early on in life, were intercorrelated (wing bones, tarsus, bill basis and the width of foramen magnum). The lengths of the primaries and of tail feathers were also intercorrelated, structures which develop late.
The mean body weight of the Hooded crow population studied in Norway was intermediate between that of the Hooded crow in Germany and of the Carrion and Hooded crows in England and Scotland. No such differences were found in wing length. Norwegian Hooded crows have shorter tails than German ones, but their bills are much larger, in particular for the females. Therefore, the degree of sexual dimorphism in bill size seems to be reduced at high latitudes.     

Individuality of contact calls in the Greater Flamingo Phoenicopterus ruber and the problem of background noise in a colony

Acoustic communication has great importance in social relationships and especially in individual recognition in the Greater Flamingo Phoenicopterus ruber. However, it is constrained by the noisy environment of the colony. I performed an analysis of both the temporal and frequency patterns of contact calls and showed that the use of both is essential for discrimination between individuals. I made a search for the acoustic parameters which are used by the flamingos. It appears that the call duration, the slow amplitude modulation, the spectrum bandwidth and the repartition of energy among harmonics exhibit individuality. Recognition between the birds must be based on a multiparametric analysis, taking into account both spectral and temporal features of the calls. Indeed, no single parameter was sufficient to discriminate between individual birds used in my research. In the noisy environment of the colony, the transmission of individuality in a message is improved by this multiparametric coding, which can be considered as an adaptation to these extreme acoustic conditions. Moreover, the study revealed numerous acoustic convergences with another colonial bird species, the Emperor Penguin Aptenodytes forsteri , and both species seemed to use the same method to encode individuality in their vocalizations.     

Do Zebra Finch Parents Fail to Recognise Their Own Offspring?

Individual recognition systems require the sender to be individually distinctive and the receiver to be able to perceive differences between individuals and react accordingly. Many studies have demonstrated that acoustic signals of almost any species contain individualized information. However, fewer studies have tested experimentally if those signals are used for individual recognition by potential receivers. While laboratory studies using zebra finches have shown that fledglings recognize their parents by their "distance call", mutual recognition using the same call type has not been demonstrated yet. In a laboratory study with zebra finches, we first quantified between-individual acoustic variation in distance calls of fledglings. In a second step, we tested recognition of fledgling calls by parents using playback experiments. With a discriminant function analysis, we show that individuals are highly distinctive and most measured parameters show very high potential to encode for individuality. The response pattern of zebra finch parents shows that they do react to calls of fledglings, however they do not distinguish between own and unfamiliar offspring, despite individual distinctiveness. This finding is interesting in light of the observation of a high percentage of misdirected feedings in our communal breeding aviaries. Our results demonstrate the importance of adopting a receiver's perspective and suggest that variation in fledgling contact calls might not be used in individual recognition of offspring.     

Vocal individuality of large-tailed nightjar (Caprimulgus macrurus) in Peninsular Malaysia

All four nightjar species resident in Peninsular Malaysia are vocally distinct, yet they remain little studied. Conventional field methods based on visual cues to study diurnal species may be impractical for nightjars. Alternatively, aural survey can potentially be applied on nightjars provided that individuality in their vocalisations can be proven. Our study aimed to determine the vocal individuality of the common, large-tailed nightjar (Caprimulgus macrurus) in oil palm smallholdings and an isolated forest patch located in Selangor, Peninsular Malaysia. From the call recordings obtained from 22 individuals, results of the Kruskal-Wallis analysis revealed significant differences in all the nine vocal parameters (call length, interquartile range bandwidth, low, high, average, centre and peak frequencies as well as first and third quartile frequencies) measured among individual nightjars (p < 0.001) regardless of study sites. Discriminant Function Analysis showed that more than 94.5% of original grouped cases were correctly classified. This implied that the majority of vocalizations can be assigned to individual birds based on the parameters measured. This study demonstrated the occurrence of vocal individuality in the large-tailed nightjar and such a finding pertaining to distinct vocalisations at the individual level will compensate for the limited access to visual cues in field surveys, as with the case for all nocturnal birds.     

Lateralized tool use in wild New Caledonian crows

Many vertebrate species exhibit sensory and motor asymmetries. Laterality studies of tool use have focused on primates, where hemispheric asymmetries, manifested behaviourally in hand preferences, are thought to be associated with complex motor tasks. Here we report strong individual lateralization for tool use in birds. New Caledonian crows, Corvus moneduloides, hold stick tools with their bills while foraging, often with the nonworking end laterally positioned on one side of the head and the working end possibly positioned in the binocular field. We observed four wild crows to determine whether tools were consistently held on one side. All crows showed a significant preference (two right, two left). This preference was independent of any asymmetry in tool manufacture and held for artificial holes similarly accessible for tools held on either side. This is the first demonstration of lateralized tool use in a nonprimate. In addition, all 173 tools used unilaterally were held only on a crow's preferred side. Such pronounced individual laterality for tool use in natural conditions has previously been reported only in humans and chimpanzees.     

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.     

Plain faces are more expressive: comparative study of facial colour,mobility and musculature in primates

Facial colour patterns and facial expressions are among the most important phenotypic traits that primates use during social interactions. While colour patterns provide information about the sender''s identity, expressions can communicate its behavioural intentions. Extrinsic factors, including social group size, have shaped the evolution of facial coloration and mobility, but intrinsic relationships and trade-offs likely operate in their evolution as well. We hypothesize that complex facial colour patterning could reduce how salient facial expressions appear to a receiver, and thus species with highly expressive faces would have evolved uniformly coloured faces. We test this hypothesis through a phylogenetic comparative study, and explore the underlying morphological factors of facial mobility. Supporting our hypothesis, we find that species with highly expressive faces have plain facial colour patterns. The number of facial muscles does not predict facial mobility; instead, species that are larger and have a larger facial nucleus have more expressive faces. This highlights a potential trade-off between facial mobility and colour patterning in primates and reveals complex relationships between facial features during primate evolution.     

Carotenoid-based plumage colouration is associated with blood parasite richness and stress protein levels in blue tits (Cyanistes caeruleus)

Carotenoids are molecules that birds are not able to synthesize and therefore, must be acquired through their diet. These pigments, besides their function of giving birds red and yellow colouration when deposited in feathers, seem to act as immune-stimulators and antioxidants in the organism. Hence, only the healthiest individuals would be able to express carotenoid-based ornaments to a larger extent without compromising the physiological functions of carotenoids. Various studies have reported that birds infected by parasites are paler than those uninfected, but, to our knowledge, none of them has assessed the possible effect of multiple infections by blood parasites on plumage colour. By comparing the yellow colour in the breast plumage of blue tits, Cyanistes caeruleus, between birds infected by different numbers of blood parasite genera, we found that those birds infected by more than one genus were paler than those parasitized just by one. In addition, we examined the potential role of carotenoid-based plumage colour of blue tits as a long-term indicator of other parameters of health status, such as body condition and immunoglobulin and heat shock protein (HSP) levels. Our results indicate that more brightly coloured birds had lower HSP70 levels than paler birds, but we did not find any significant association between colour and body condition or immunoglobulin levels. In addition, we found a positive significant association between Haemoproteus density of infection and HSP60 levels. Overall, these results support the role of carotenoid-based colours as indicators of health status in blue tits and show detrimental effects of parasitism on this character.     

Double cones are used for colour discrimination in the reef fish,Rhinecanthus aculeatus

Double cones (DCs) are the most common cone types in fish, reptiles and birds. It has been suggested that DCs are used for achromatic tasks such as luminance, motion and polarization vision. Here we show that a reef fish Rhinecanthus aculeatus can discriminate colours on the basis of the difference between the signals of individual members of DCs. This is the first direct evidence that individual members of DCs are used in colour vision as independent spectral channels.     

Population genetic structure and colonisation history of the tool-using New Caledonian crow

New Caledonian crows exhibit considerable variation in tool making between populations. Here, we present the first study of the species' genetic structure over its geographical distribution. We collected feathers from crows on mainland Grande Terre, the inshore island of Toupéti, and the nearby island of Maré where it is believed birds were introduced after European colonisation. We used nine microsatellite markers to establish the genotypes of 136 crows from these islands and classical population genetic tools as well as Approximate Bayesian Computations to explore the distribution of genetic diversity. We found that New Caledonian crows most likely separate into three main distinct clusters: Grande Terre, Toupéti and Maré. Furthermore, Toupéti and Maré crows represent a subset of the genetic diversity observed on Grande Terre, confirming their mainland origin. The genetic data are compatible with a colonisation of Maré taking place after European colonisation around 1900. Importantly, we observed (1) moderate, but significant, genetic differentiation across Grande Terre, and (2) that the degree of differentiation between populations on the mainland increases with geographic distance. These data indicate that despite individual crows' potential ability to disperse over large distances, most gene flow occurs over short distances. The temporal and spatial patterns described provide a basis for further hypothesis testing and investigation of the geographical variation observed in the tool skills of these crows.     

Note-, phrase- and song-specific acoustic variables contributing to the individuality of male duet song in the Bornean southern gibbon (Hylobates albibarbis)

In this study, we examine acoustic individuality in male duet songs of wild, non-habituated Bornean southern gibbons (Hylobates albibarbis) and identify contributing acoustic variables. We recorded 174 male duet songs from nine groups in a rainforest in Central Kalimantan, Indonesia. Each male portion of the duet was analysed for 14 acoustic variables at three levels of variation, including six note-specific variables (start frequency, end frequency, minimum frequency, maximum frequency, average frequency and duration), four phrase-specific variables (minimum frequency, maximum frequency, duration and number of syllables) and four song-specific variables (minimum frequency, maximum frequency, duration and number of syllables). Principal component analysis was performed to summarise each of these sets of variables into a total of six principal components (PCs). Strong acoustic individuality was found in all PCs and at all three levels: note, phrase and song (all p < 0.001). Furthermore, a particularly high magnitude of individuality was found in PC 1 of the song-specific analysis, defined by the acoustic variables of duration and number of syllables. Due to the high levels of individuality, we suggest that these acoustic variables may be used by Bornean southern gibbons for individual discrimination. As well as furthering our biological understanding of male gibbon song with regards to individuality and associated conspecific recognition, these findings also have the potential to help improve population survey methods, such as the acoustic sampling method using listening points, by offering a more accurate method of individual recognition.     

Individuality in Corncrake Crex crex vocalizations

Vocal individuality has potential for the monitoring of bird species that are otherwise difficult to observe. In this study we assessed the potential of this technique for the monitoring of the globally threatened Corncrake Crex crex based on the analysis of calls recorded in Ireland and Scotland in 1993 and 1994. Discriminant function analysis correctly attributed >80% of individual calls based on five temporal parameters. A high level of individual distinctiveness was also found in the fine temporal structure of calls. When information on fine structure was added to the discriminant function analysis, classification of calls to individuals was improved to 100%. The structure of an individual's call was found to be consistent over the 2-year period. This study highlighted the problemsassociated with setting criteria for re-identifying individuals by calls. The consequences of these problems and the potential of vocal individuality for providing monitoring information in this species are discussed.     

Activity profiles and hook-tool use of New Caledonian crows recorded by bird-borne video cameras

New Caledonian crows are renowned for their unusually sophisticated tool behaviour. Despite decades of fieldwork, however, very little is known about how they make and use their foraging tools in the wild, which is largely owing to the difficulties in observing these shy forest birds. To obtain first estimates of activity budgets, as well as close-up observations of tool-assisted foraging, we equipped 19 wild crows with self-developed miniature video cameras, yielding more than 10 h of analysable video footage for 10 subjects. While only four crows used tools during recording sessions, they did so extensively: across all 10 birds, we conservatively estimate that tool-related behaviour occurred in 3% of total observation time, and accounted for 19% of all foraging behaviour. Our video-loggers provided first footage of crows manufacturing, and using, one of their most complex tool types—hooked stick tools—under completely natural foraging conditions. We recorded manufacture from live branches of paperbark (Melaleuca sp.) and another tree species (thought to be Acacia spirorbis), and deployment of tools in a range of contexts, including on the forest floor. Taken together, our video recordings reveal an ‘expanded’ foraging niche for hooked stick tools, and highlight more generally how crows routinely switch between tool- and bill-assisted foraging.