Bemerkungen zur Evolution von., Sprachen bei Säugetieren1 Zur Variabilität innerartlicher Kommunikation bei Caniden

Remarks on the evolution of “languages” of mammals. The variability of the intraspecific communication of canids The canid species mainly considered in this study, the golden jackal (Canis aureus), the cojote (Canis latrans), and especially the wolf (Canis lupus) have an extremely variable species-specific intraspecific communication. Communities, but also differences between the species become evident; the wolf with its distinct social behavior has the greatest differentiation. These results make also clear, that forms of communication in mammals develop in evolutionary processes and events. A safe statement on the beginning of the forms of communication in canids cannot be given so far. This is also true for humans. The ideas of Lenneberg (1967) of the parallel and disjunct origin of the forms of communication in mammals has a high probability for higher systematic units, but on lower systematic level a gradual change can be observed. The forms of communication in mammals are highly differentiated structures, where specific pecularities of the brain are of a special importance. The observations on the variability of intraspecific communication of canids, representing nonhuman mammals, suggest to define “language” in a very general form. In this way, similarities, analogies, and differences between the species of mammals, inclusive man, can be seen more clearly. In only this way the material can be gained to answer the question, if the language of man has in principle exceptional position biologically. It is important for the valuation of forms of intraspecific communication, the “languages”, of mammals not to choose human theory of life and human thinking as a basis, but to start with the biological pecularities of the species. Also canids, as higher mammals, have the ability to abstract, a form of thinking. In their special, species-specific way also non-human mammals arrange their area of experience and thinking. They form for themselves a species-specific “theory of live”. This will of course be different from the human one, according to the systematic position and the biological environment of the species. It is generally accepted that man has special abilities of thinking, he possesses an extraordinary developed brain, compared to all other mammals. This must effect his communication, his language, and result in differences to other mammal species. Gipper (1977) pointed out especially these differences, but they should not be interpreted as differences in principle. Canids use different gestures and sounds for communication within the species; dialog relations can be observed. Different connections of gestures and sounds have different contents of information. It is remarkable that canids do not use their total abilities in using the means of communication in the same way. This is very striking in the change from the wolf, as the only ancestor, to the domestic dog. It is evident that the brain has a greater importance in developing intraspecific communication, than do the peculuarities of organs causing the understanding. A dependanc of intraspecific communication from the environment can be observed either in differences of wird species of canids as well as in the domestication. In the domestic dog, but also in other domestic animals, there is an increase in vocalisations. But the content of information of sounds and gestures decreases in domestication, expressions of arousal become more important. A remarkable plasticity of intraspecific communication becomes evident by domestication. The transformations can be evaluated in the sense of Kosswig (1963, 1965) as first stages of a regressive evolution. Experiments of cross-breeding canid species show exemplarily that forms of communication within these mammal species have a highly polygene regulation, and that processes of learning have an influence. Also from this point of view, no basic differences between nonhuman mammals and humans can be assured, especially when taking into account the facts and thoughts described by Lenneberg. The findings in the canids give useful hints for a better understanding of the human language and its relations to the forms of communication in other mammals. Altogether one can conclude that genetic variability, numerous recombinations, the synorganisation of the processes caused in this way, and natural selection plays definite role in the evolution of “languages”.     

Distal Humeral Morphology Indicates Locomotory Divergence in Extinct Giant Kangaroos

Previous studies of the morphology of the humerus in kangaroos showed that the shape of the proximal humerus could distinguish between arboreal and terrestrial taxa among living mammals, and that the extinct “giant” kangaroos (members of the extinct subfamily Sthenurinae and the extinct macropodine genus Protemnodon) had divergent humeral anatomies from extant kangaroos. Here, we use 2D geometric morphometrics to capture the shape of the distal humerus in a range of extant and extinct marsupials and obtain similar results: sthenurines have humeral morphologies more similar to arboreal mammals, while large Protemnodon species (P. brehus and P. anak) have humeral morphologies more similar to terrestrial quadrupedal mammals. Our results provide further evidence for prior hypotheses: that sthenurines did not employ a locomotor mode that involved loading the forelimbs (likely employing bipedal striding as an alternative to quadrupedal or pentapedal locomotion at slow gaits), and that large Protemnodon species were more reliant on quadrupedal locomotion than their extant relatives. This greater diversity of locomotor modes among large Pleistocene kangaroos echoes studies that show a greater diversity in other aspects of ecology, such as diet and habitat occupancy.

     

Communication between domestic dogs (Canis familiaris) and humans: Dogs are good learners

Communication involves a wide range of behaviours that animals emit in their daily lives and can take place between different species, as is the case of domestic dogs (Canis familiaris) and humans. Dogs have shown to be successful at following human cues to solve the object choice task. The question is what are the mechanisms involved in these communicative abilities. This article presents a review of studies about the communicative capacities of domestic dogs emphasizing the ones that considered the effect of associative learning upon these skills. In addition, evidence about differences in dogs’ performance in following physical or social cues is summarized and two studies where both signals compete are presented here. The obtained results suggest that the training of a colour cue reverses the dogs’ preference for the social one. These results are discussed in light of the findings that gave importance to the learning effect, concluding that the dogs fundamentally follow those cues that allowed them to obtain reinforcers in their previous learning history.     

Natural gaze signaling in a social context

Evolutionary theory, augmented by a vast literature on gaze cuing and gaze following, suggests that the unique high-contrast morphology of the human eye evolved for rapid and silent communication between conspecifics. While this theory rests on the fundamental idea that humans use their eyes to signal information, empirical studies have focused exclusively on the effects of gaze cues on human receivers. In a series of three experiments we examined the other side of the communication dynamic by investigating if, and when, humans signal gaze information to other humans in a natural, but controlled, situation involving food consumption. First, we established that there is a normative behavior to look away when someone begins to bite. Second, we found that participants were significantly more likely to look down at their food before taking a bite when they were eating with another person versus alone. Lastly, we found that in pairs where a social connection has been established, when one person looks down signaling that a bite is forthcoming, the other person tends to look away. These results demonstrate that natural gaze signaling occurs in the context of eating, and it can, dependent on the relationship between the pair, trigger a gaze response that is different from gaze following. Our study shows that natural social attention between individuals is a two-way street, where each person can signal and read gaze information, consistent with the idea that human eye morphology evolved to facilitate communication between conspecifics.     

Do more sociable dogs gaze longer to the human face than less sociable ones?

Domestic dogs (Canis familiaris) are especially skillful in communicating with humans, and they rely on special abilities to do that. One of these skills involves gazing at human faces in cases of uncertainty or when seeking for something out of reach. In this study, we evaluated the relationship between dogs' sociability level and the ability to learn to gaze in a situation with food in sight but out of their reach. Thirty-nine adult dogs were tested in two procedures: (1) a sociability test that involved interacting with an unknown person, and (2) a learning task that consisted of training trials in which gazing at the experimenter's face was food reinforced, followed by extinction trials in which gazing was not followed by food. A significant positive correlation was found between the duration of physical contact with the unknown person in the sociability test and gaze duration during extinction. Moreover, high sociability dogs gazed significantly longer at humans during extinction trials. We discuss the possibility that, more sociable animals, such as those who pay more attention to the person in our sociability test, may be more persistent in their communicative attempts because the presence of the human is intrinsically reinforcing to them. Finally, we comment on the importance of these findings for training purposes.     

Do American Crows Pay Attention to Human Gaze and Facial Expressions?

Interactions between species can lead to the evolution of interspecific communication. Non‐verbal communication by humans, both intentional and unintentional, can be interpreted by other species. We tested whether American crows (Corvus brachyrhynchos) were sensitive to human facial features under field conditions by comparing flight initiation distances and urgency of escape behavior to human approaches varying in eye contact and facial expression. We first examined whether crows distinguish between an approaching human who is directly gazing at them and a human approaching them with an averted gaze. In a second experiment, we tested whether crows differentiate a smiling from scowling human approaching them with direct or averted gaze. In the first experiment, we found that crows fled sooner and more urgently when humans were directly gazing at them. Similarly, in the second experiment, crows responded sooner to a direct vs. averted gaze; however, they did not react differently to varying human facial expressions. We suggest that crows use human gaze as a reliable visual cue compared with facial expressions when making decisions about responding to approaching humans. This is the first study to show that a wild corvid species changes its behavior based on human gaze, possibly representing an adaptation to living in human‐dominated urban areas and suggesting crows might perceive human intention by this visual cue.     

What Are You or Who Are You? The Emergence of Social Interaction between Dog and an Unidentified Moving Object (UMO)

Robots offer new possibilities for investigating animal social behaviour. This method enhances controllability and reproducibility of experimental techniques, and it allows also the experimental separation of the effects of bodily appearance (embodiment) and behaviour. In the present study we examined dogs’ interactive behaviour in a problem solving task (in which the dog has no access to the food) with three different social partners, two of which were robots and the third a human behaving in a robot-like manner. The Mechanical UMO (Unidentified Moving Object) and the Mechanical Human differed only in their embodiment, but showed similar behaviour toward the dog. In contrast, the Social UMO was interactive, showed contingent responsiveness and goal-directed behaviour and moved along varied routes. The dogs showed shorter looking and touching duration, but increased gaze alternation toward the Mechanical Human than to the Mechanical UMO. This suggests that dogs’ interactive behaviour may have been affected by previous experience with typical humans. We found that dogs also looked longer and showed more gaze alternations between the food and the Social UMO compared to the Mechanical UMO. These results suggest that dogs form expectations about an unfamiliar moving object within a short period of time and they recognise some social aspects of UMOs’ behaviour. This is the first evidence that interactive behaviour of a robot is important for evoking dogs’ social responsiveness.     

From overlooking to concealed: predator avoidance in an apex carnivore

Many prey species select bed sites that reduce the risk of being caught off guard. We investigated bed sites used by an apex predator (gray wolf, Canis lupus) before and after individuals were approached by humans (N?=?48 trials). On 9 out of 10?days, the unprovoked wolves rested at sites high in the terrain with a good overview (overlooking sites). After being approached, they resettled on more concealed sites lower in the terrain. Solitary yearlings used less overlooking sites than adults both before and after disturbance. The study provides experimental evidence that wolves’ behavioural response to approaching humans is analogous to predator avoidance in prey species.     

Female but not male dogs respond to a size constancy violation

Differences between sexes in cognitive processes are widespread in humans and permeate many, if not most, cognitive domains. In animal cognition research, however, possible sex differences are still often neglected. Here, we provide striking evidence for a sex-specific response in an object permanence task in domestic dogs (Canis familiaris). Female dogs responded with significantly increased looking times to a violation of expectancy--a ball 'magically' changing size while temporarily occluded. By contrast, male dogs, irrespective of their neuter status, did not respond to the size constancy violation. These results indicate that sex differences in basic cognitive processes may extend to mammals in general, and call for increased consideration of possible sex effects when analysing and interpreting data in animal cognition.     

On the evolution of noise-dependent vocal plasticity in birds

Signal plasticity is considered an important step in the evolution of animal communication. In acoustic communication, signal transmission is often constrained by background noise. One adaptation to evade acoustic signal masking is the Lombard effect, in which an animal increases its vocal amplitude in response to an increase in background noise. This form of signal plasticity has been found in mammals, including humans, and some birds, but not frogs. However, the evolution of the Lombard effect is still unclear. Here we demonstrate for the first time the Lombard effect in a phylogentically basal bird species, the tinamou Eudromia elegans. By doing so, we take a step towards reconstructing the evolutionary history of noise-dependent vocal plasticity in birds. Similar to humans, the tinamous also raised their vocal pitch in noise, irrespective of any release from signal masking. The occurrence of the Lombard effect in a basal bird group suggests that this form of vocal plasticity was present in the common ancestor of all living birds and thus evolved at least as early as 119 Ma.     

Frustration Behaviors in Domestic Dogs

During extinction a previously learned behavior stops being reinforced. In addition to the decrease in the rate of the instrumental response, it produces an aversive emotional state known as frustration. This state can be assimilated with the fear reactions that occur after aversive stimuli are introduced at both the physiological and behavioral levels. This study evaluated frustration reactions of domestic dogs (Canis familiaris) during a communicative situation involving interactions with a human. The task included the reinforcement and extinction of the gaze response toward the experimenter's face when the dogs tried to obtain inaccessible food. The dog's frustration reactions during extinction involved an increase in withdrawal and side orientation to the location of the human as well as lying down, ambulation, sniffing, and vocalizations compared with the last acquisition trial. These results are especially relevant for domestic dog training situations in which the extinction technique is commonly used to discourage undesirable behaviors.     

Breed differences in dogs’ (Canis familiaris) gaze to the human face

Domestic dogs (Canis familiaris) have been submitted to a vast process of artificial selection and to date, there are hundreds of breeds that differ in their physical and behavioral features. In addition, dogs possess important skills to communicate with humans. Previous evidence indicates that those abilities are related to the domestication process and are modulated by instrumental learning processes. Very few studies, however, have evaluated breed differences in the use and learning of interspecific communicative responses. In Study 1 Retrievers, German Shepherds and Poodles were compared in the acquisition and extinction of their gaze toward the human face, in a conflict situation involving food within sight but out of reach. The groups did not differ in the acquisition of the response, but throughout the extinction phase Retrievers gazed to the human significantly more than the other groups. In Study 2, similar results were obtained in a test without any previous explicit training. These results suggest that these three major popular breeds differ in gazing to humans in a communicative situation.     

Learning interspecific communicative responses in Pampas foxes (Lycalopex gymnocercus)

Domestic dogs show remarkable communicative abilities in their interaction with people. These skills maybe explained by the interaction between the domestication process and learning experiences during ontogeny. Studies carried out on other species of canids, which have not been domesticated are relevant to this topic. The purpose of this article is to study the effect of instrumental learning on captive Pampas foxes’ (Lycalopex gymnocercus) communicative responses to humans. Seven foxes were tested in a conflict situation involving food within sight but out of their reach. In these situations dogs typically gaze at the human face to ask for food. In Study 1, there was an increase in gaze duration as a consequence of reinforcement and a decrease during extinction, when animals did not receive any more food. In Study 2, all of the four foxes tested successfully followed proximal pointing gesture to find hidden food. When a distal pointing cue was given, three out of four followed it in the first session and one in the second session. These results are consistent with those previously found in dogs, and suggest that learning experiences allow the development of communicative skills, even in not domesticated canid species.     

Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis

As compared with other primates, humans have especially visible eyes (e.g., white sclera). One hypothesis is that this feature of human eyes evolved to make it easier for conspecifics to follow an individual's gaze direction in close-range joint attentional and communicative interactions, which would seem to imply especially cooperative (mututalistic) conspecifics. In the current study, we tested one aspect of this cooperative eye hypothesis by comparing the gaze following behavior of great apes to that of human infants. A human experimenter "looked" to the ceiling either with his eyes only, head only (eyes closed), both head and eyes, or neither. Great apes followed gaze to the ceiling based mainly on the human's head direction (although eye direction played some role as well). In contrast, human infants relied almost exclusively on eye direction in these same situations. These results demonstrate that humans are especially reliant on eyes in gaze following situations, and thus, suggest that eyes evolved a new social function in human evolution, most likely to support cooperative (mututalistic) social interactions.     

Intranasal oxytocin and a polymorphism in the oxytocin receptor gene are associated with human-directed social behavior in golden retriever dogs

The oxytocin system may play an important role in dog domestication from the wolf. Dogs have evolved unique human analogue social skills enabling them to communicate and cooperate efficiently with people. Genomic differences in the region surrounding the oxytocin receptor (OXTR) gene have previously been associated with variation in dogs' communicative skills. Here we have utilized the unsolvable problem paradigm to investigate the effects of oxytocin and OXTR polymorphisms on human-directed contact seeking behavior in 60 golden retriever dogs. Human-oriented behavior was quantified employing a previously defined unsolvable problem paradigm. Behaviors were tested twice in a repeated, counterbalanced design, where dogs received a nasal dose of either oxytocin or saline 45 min before each test occasion. Buccal DNA was analysed for genotype on three previously identified SNP-markers associated with OXTR. The same polymorphisms were also genotyped in 21 wolf blood samples to explore potential genomic differences between the species. Results showed that oxytocin treatment decreased physical contact seeking with the experimenter and one of the three polymorphisms was associated with degree of physical contact seeking with the owner. Dogs with the AA-genotype at this locus increased owner physical contact seeking in response to oxytocin while the opposite effect was found in GG-genotype individuals. Hence, intranasal oxytocin treatment, an OXTR polymorphism and their interaction are associated with dogs' human-directed social skills, which can explain previously described breed differences in oxytocin response. Genotypic variation at the studied locus was also found in wolves indicating that it was present even at the start of dog domestication.     

Cryptosporidium in wild placental mammals

Cryptosporidium species are common parasites of wild placental mammals. Recent parasitological studies combined with molecular genotyping techniques have been providing valuable new insight into the host specificity and potential transmission of various Cryptosporidium species/genotypes among animals and between these animals and humans. Although Cryptosporidium in wild animals may possess a potential public health problem due to oocyst contamination in the environment, studies at various regions of the world have indicated a strong host-adaptation by these parasites and a limited potential of cross-species transmission of cryptosporidiosis among placental mammals, suggesting that these animals are probably not a major reservoir for human infection. However, Cryptosporidium species/genotypes in placental animals have been reported occasionally in humans. Therefore, public health significance of some Cryptosporidium species in wild placental mammals, such as the cervine genotype, should not be overlooked and should be further studied.     

Gaze direction - a cue for hidden food in rooks (Corvus frugilegus)?

Other individual's head- and eye-directions can be used as social cues indicating the presence of important events. Among birds, ravens and rooks have been shown to co-orient with conspecifics and with humans by following their gaze direction into distant space and behind visual screens. Both species use screens to cache food in private; also, it had been suggested that they may rely on gaze cues to detect hidden food. However, in an object-choice task, ravens failed to do so, and their competitive lifestyle may have prevented them from relying on these cues. Here we tested closely related and cooperative rooks. Food was hidden in one of two cups and the experimenter gazed at the baited cup. In a second experiment, we aimed to increase the birds’ motivation to choose correctly by increasing the investment needed to obtain the reward. To do so, the birds had to pull on a string to obtain the cup. Here, the birds as a group tended to rely on gaze cues. In addition, individual birds quickly learned to use the cue in both experiments. Although rooks may not use gaze cues to find hidden food spontaneously, they may quickly learn to do so.     

Developmental and Post-Eruptive Defects in Molar Enamel of Free-Ranging Eastern Grey Kangaroos (Macropus giganteus) Exposed to High Environmental Levels of Fluoride

Dental fluorosis has recently been diagnosed in wild marsupials inhabiting a high-fluoride area in Victoria, Australia. Information on the histopathology of fluorotic marsupial enamel has thus far not been available. This study analyzed the developmental and post-eruptive defects in fluorotic molar enamel of eastern grey kangaroos (Macropus giganteus) from the same high-fluoride area using light microscopy and backscattered electron imaging in the scanning electron microscope. The fluorotic enamel exhibited a brownish to blackish discolouration due to post-eruptive infiltration of stains from the oral cavity and was less resistant to wear than normally mineralized enamel of kangaroos from low-fluoride areas. Developmental defects of enamel included enamel hypoplasia and a pronounced hypomineralization of the outer (sub-surface) enamel underneath a thin rim of well-mineralized surface enamel. While the hypoplastic defects denote a disturbance of ameloblast function during the secretory stage of amelogenesis, the hypomineralization is attributed to an impairment of enamel maturation. In addition to hypoplastic defects, the fluorotic molars also exhibited numerous post-eruptive enamel defects due to the flaking-off of portions of the outer, hypomineralized enamel layer during mastication. The macroscopic and histopathological lesions in fluorotic enamel of M. giganteus match those previously described for placental mammals. It is therefore concluded that there exist no principal differences in the pathogenic mechanisms of dental fluorosis between marsupial and placental mammals. The regular occurrence of hypomineralized, opaque outer enamel in the teeth of M. giganteus and other macropodids must be considered in the differential diagnosis of dental fluorosis in these species.     

Dogs' looking times and pupil dilation response reveal expectations about contact causality

Contact causality is one of the fundamental principles allowing us to make sense of our physical environment. From an early age, humans perceive spatio-temporally contiguous launching events as causal. Surprisingly little is known about causal perception in non-human animals, particularly outside the primate order. Violation-of-expectation paradigms in combination with eye-tracking and pupillometry have been used to study physical expectations in human infants. In the current study, we establish this approach for dogs (Canis familiaris). We presented dogs with realistic three-dimensional animations of launching events with contact (regular launching event) or without contact between the involved objects. In both conditions, the objects moved with the same timing and kinematic properties. The dogs tracked the object movements closely throughout the study but their pupils were larger in the no-contact condition and they looked longer at the object initiating the launch after the no-contact event compared to the contact event. We conclude that dogs have implicit expectations about contact causality.     

To Beg,or Not to Beg? That Is the Question: Mangabeys Modify Their Production of Requesting Gestures in Response to Human’s Attentional States

Background

Although gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys.

Methodology/Principal Findings

The present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human’s attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human’s attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter’s eyes state.

Conclusions/Significance

These results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.