Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human

In this study we investigated the communicative abilities of 10 orangutans (Pongo pygmaeus) and seven western lowland gorillas (Gorilla gorilla gorilla), and particularly focused on their sensitivity to the attentional state of a human experimenter when choosing from a repertoire of both auditory and visual communication strategies. In experiment 1 a banana was placed in front of the subject's cage and a human experimenter was either present or absent. The subject's behavior was recorded for 60 sec. Both gorillas and orangutans gestured (t(16)=-3.58, P<.005) and vocalized (t(16)=-2.47, P<.05) more when the experimenter was present. In experiment 2 a human experimenter held a banana in front of the subject's cage and was oriented either toward or away from the subject. Again the subject's behavior was recorded for 60 sec. In this experiment both gorillas and orangutans gestured significantly more frequently (t(16)=3.40, P<.005) when the experimenter was oriented toward them. In addition, gorillas and orangutans used other forms of visual communication signals, such as lip pout (t(16)=3.66, P<.005), barter/trade (t(16)=2.31, P<.05), and body present (t(16)=2.31, P<.05) significantly more when an experimenter was facing them. The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention. These results are also similar to previous findings on communicative behaviors in chimpanzees.     

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.     

Effect of others' attentional states on vocalizations in Japanese monkeys (Macaca fuscata)

We investigated the effects of other's attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter's body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly.     

Do dogs mind the dots? Investigating domestic dogs' (Canis familiaris) preferential looking at human-shaped point-light figures

It is generally assumed that dogs show increased attention towards humans. A major part of this includes attention towards visual cues such as bodily gestures. We tested empirically whether dogs are visually attentive towards human body movement. Based on methods from visual perception research in humans, we used point-light figures (PLFs) to investigate whether dogs attend to human body movement compared to other forms of motion. We investigated dogs' attentiveness towards vocalisation-paired PLFs by adopting a preferential looking paradigm. Results indicate that dogs show increased attention towards vocalisation-paired human-shaped PLFs in comparison with inverted and non-inverted scrambled configurations of the same PLFs. This increased attention, however, was only present in the case of PLFs that simulated a human in frontal orientation but not for PLFs in lateral orientation. We conclude that dogs prefer to look at PLFs of socially relevant (i.e. frontally facing) human body (i.e. natural) movement rather than scrambled (i.e. unnatural) displays. Our results indicate that PLFs may function as a promising tool to investigate dogs' visual perceptual preferences and mechanisms.     

Visual Cues Given by Humans Are Not Sufficient for Asian Elephants (Elephas maximus) to Find Hidden Food

Recent research suggests that domesticated species – due to artificial selection by humans for specific, preferred behavioral traits – are better than wild animals at responding to visual cues given by humans about the location of hidden food. \Although this seems to be supported by studies on a range of domesticated (including dogs, goats and horses) and wild (including wolves and chimpanzees) animals, there is also evidence that exposure to humans positively influences the ability of both wild and domesticated animals to follow these same cues. Here, we test the performance of Asian elephants (Elephas maximus) on an object choice task that provides them with visual-only cues given by humans about the location of hidden food. Captive elephants are interesting candidates for investigating how both domestication and human exposure may impact cue-following as they represent a non-domesticated species with almost constant human interaction. As a group, the elephants (n = 7) in our study were unable to follow pointing, body orientation or a combination of both as honest signals of food location. They were, however, able to follow vocal commands with which they were already familiar in a novel context, suggesting the elephants are able to follow cues if they are sufficiently salient. Although the elephants’ inability to follow the visual cues provides partial support for the domestication hypothesis, an alternative explanation is that elephants may rely more heavily on other sensory modalities, specifically olfaction and audition. Further research will be needed to rule out this alternative explanation.     

Development of a Body Condition Scoring Index for Female African Elephants Validated by Ultrasound Measurements of Subcutaneous Fat

Obesity-related health and reproductive problems may be contributing to non-sustainability of zoo African elephant (Loxodonta africana) populations. However, a major constraint in screening for obesity in elephants is lack of a practical method to accurately assess body fat. Body condition scoring (BCS) is the assessment of subcutaneous fat stores based on visual evaluation and provides an immediate appraisal of the degree of obesity of an individual. The objective of this study was to develop a visual BCS index for female African elephants and validate it using ultrasound measures of subcutaneous fat. To develop the index, standardized photographs were collected from zoo (n = 50) and free-ranging (n = 57) female African elephants for identifying key body regions and skeletal features, which were then used to visually determine body fat deposition patterns. This information was used to develop a visual BCS method consisting of a list of body regions and the physical criteria for assigning an overall score on a 5-point scale, with 1 representing the lowest and 5 representing the highest levels of body fat. Results showed that as BCS increased, ultrasound measures of subcutaneous fat thickness also increased (P<0.01), indicating the scores closely coincide with physical measures of fat reserves. The BCS index proved to be reliable and repeatable based on high intra- and inter-assessor agreement across three assessors. In comparing photographs of wild vs. captive African elephants, the median BCS in the free-ranging individuals (BCS = 3, range 1–5) was lower (P<0.001) than that of the zoo population (BCS = 4, range 2–5). In sum, we have developed the first validated BCS index for African elephants. This tool can be used to examine which factors impact body condition in zoo and free-ranging elephants, providing valuable information on how it affects health and reproductive potential of individual elephants.     

Are Dogs Able to Communicate with Their Owners about a Desirable Food in a Referential and Intentional Way?

The ability of dogs to use human communicative signals has been exhaustively studied. However, few studies have focused on the production of communicative signals by dogs. The current study investigated if dogs are able to communicate by using directional signals towards some desirable object in the environment and also if they show an apparent intention to manipulate their owner’s behavior in order to receive it. Some operational criteria were used to investigate referential and intentional communication: the signal should be influenced by the audience and by the recipient’s direction of visual attention; the sender should display gaze alternations between the recipient and the object and attention-getting behaviors, and, finally, the sender should persist and elaborate the communication when attempts to manipulate the recipient failed. Aiming to investigate these criteria in dogs, 29 subjects were tested using an experimental set up in which they could see a desirable but unreachable food and they needed the cooperation of their owners in order to receive it. This study found evidence of all operational criteria, especially for gaze alternation between the owner and the food, which suggested that some dogs’ communicative behaviors could be functionally referential and intentional. Nevertheless, similar to other studies about social cognition in animals, it is not possible to distinguish if the dog’s behaviors are based on simple mechanisms or on a theory of mind about their owners.     

Weigh and see—Body mass recordings versus body condition scoring in European zoo elephants (Loxodonta africana and Elephas maximus)

Regular body mass (BM) monitoring plays a key role in preventative health care of zoo animals. In some species, including African (Loxodonta africana) and Asian elephants (Elephas maximus), the process of weighing can be challenging, and alternative methods such as visual body condition scoring (BCS) have been developed. We investigated the temporal development of both parameters regarding correlation patterns between them, and their suitability as monitoring measures in dependence of an elephant's life stage. While BM is more suitable in calves and juveniles under the age of 8 years, both BM and BCS are considered equally reliable in adult elephants. In elephants over the age of 40 years, BCS might be more suitable for assessing the physical status. Independent of species and sex, juvenile zoo elephants grow in BM nearly linearly with age, and reach a higher BM at an earlier age compared with conspecifics of free-ranging and semi-captive populations in the countries of origin. The BCS typically remains constant during this life stage, seemingly unaffected by growth. In adult animals, breeding females have a lower BM and BCS than nonbreeders, and BM and BCS typically indicate fluctuations in the same direction. In geriatric elephants (>40 years) a drop in BCS occurs commonly, while BM may even increase in this life stage. We recommend regular body mass recording in zoo elephants to enhance our knowledge of body mass development and allow the formulation of objective practical recommendations. BCS presents a valuable and simple tool for complementary monitoring of an elephant's condition, especially in adult and geriatric individuals.     

Am I seeing my hand? Visual appearance and knowledge of controllability both contribute to the visual capture of a person's own body

When confronted with complex visual scenes in daily life, how do we know which visual information represents our own hand? We investigated the cues used to assign visual information to one''s own hand. Wrist tendon vibration elicits an illusory sensation of wrist movement. The intensity of this illusion attenuates when the actual motionless hand is visually presented. Testing what kind of visual stimuli attenuate this illusion will elucidate factors contributing to visual detection of one''s own hand. The illusion was reduced when a stationary object was shown, but only when participants knew it was controllable with their hands. In contrast, the visual image of their own hand attenuated the illusion even when participants knew that it was not controllable. We suggest that long-term knowledge about the appearance of the body and short-term knowledge about controllability of a visual object are combined to robustly extract our own body from a visual scene.     

Sexy Faces in a Male Paper Wasp

Sexually selected signals are common in many animals, though little reported in social insects. We investigated the occurrence of male visual signals mediating the dominance relationships among males and female choice of sexual partner in the paper wasp Polistes simillimus. Males have three conspicuous, variable and sexually dimorphic traits: black pigmentation on the head, a pair of yellow abdominal spots and body size differences. By conducting behavioral assays, we found that none of the three visual traits are associated with male-male dominance relationship. However, males with higher proportion of black facial pigmentation and bigger yellow abdominal spots are more likely chosen as sexual partners. Also, after experimentally manipulating the proportion of black pigment on males'' face, we found that females may evaluate male facial coloration during the choice of a sexual partner. Thus, the black pigmentation on P. simillimus male''s head appears to play a role as a sexually selected visual signal. We suggest that sexual selection is a common force in Polistes and we highlight the importance of this group as a model for the study of visual communication in insects.     

Eye-Catching Odors: Olfaction Elicits Sustained Gazing to Faces and Eyes in 4-Month-Old Infants

This study investigated whether an odor can affect infants'' attention to visually presented objects and whether it can selectively direct visual gaze at visual targets as a function of their meaning. Four-month-old infants (n = 48) were exposed to their mother''s body odors while their visual exploration was recorded with an eye-movement tracking system. Two groups of infants, who were assigned to either an odor condition or a control condition, looked at a scene composed of still pictures of faces and cars. As expected, infants looked longer at the faces than at the cars but this spontaneous preference for faces was significantly enhanced in presence of the odor. As expected also, when looking at the face, the infants looked longer at the eyes than at any other facial regions, but, again, they looked at the eyes significantly longer in the presence of the odor. Thus, 4-month-old infants are sensitive to the contextual effects of odors while looking at faces. This suggests that early social attention to faces is mediated by visual as well as non-visual cues.     

Macaques (Macaca nemestrina) recognize when they are being imitated

This study investigated whether monkeys recognize when a human experimenter imitates their actions towards an object. Two experimenters faced 10 pigtailed macaques, who were given access to an interesting object. One experimenter imitated the monkeys' object-directed actions, the other performed temporally contingent but structurally different object-directed actions. Results show a significant visual preference for the imitator during manual object manipulations, but not mouthing actions. We argue that the ability to match actions could be based on both visual-visual and kinaesthetic-visual matching skills, and that mirror neurons, which have both visual and motor properties, could serve as a neural basis for recognizing imitation. However, imitation recognition as assessed by visual preference does not necessarily imply the capacity to attribute imitative intentionality to the imitator. The monkeys might implicitly recognize when they are being imitated without deeper insight into the mental processes of others.     

Oestrous state dynamics in chemical communication by captive female Asian elephants

In many mammals, reproductive status is revealed through chemical cues in urine. The reproductive status of receivers may influence their interest in such signals. For social mammals that live in matrilineal groups, females may benefit by detecting the reproductive condition of herdmates. Responses to urine during oestrous cycles of senders and receivers are potential indicators of signal functions. We examined the chemosensory responses, first by four captive female Asian elephants,Elephas maximus , over their oestrous cycles to familiar follicular and luteal phase urine and second by 14 different female Asian elephants to unfamiliar conspecific follicular and luteal phase urine. We asked whether females could distinguish the reproductive state of another female as measured by their differential response to luteal- and follicular-phase urine. We further examined the influence of the receiver's reproductive status on response levels. Females responded more with specific tactolfactory trunk behaviours to follicular- than to luteal-phase urine, but only when the receiving female was in her follicular phase. Like their male conspecifics, Asian elephant females can detect changes in the reproductive state of conspecifics. The functional significance of this ability has yet to be determined but may be related more to the resource holding power of females in follicular phase than to a means for females to synchronize oestrous cycles. Such female-female communication may have important effects on social group dynamics. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

The Social and Ecological Integration of Captive-Raised Adolescent Male African Elephants (Loxodonta africana) into a Wild Population

Background

A rapid rise in the number of captive African elephants (Loxodonta africana) used in the tourism industry in southern Africa and orphaned elephants in human care has led to concerns about their long-term management, particularly males. One solution is to release them into the wild at adolescence, when young males naturally leave their herd. However, this raises significant welfare concerns: little is known about how well released elephants integrate into wild populations and whether they pose a greater threat to humans than wild elephants. We document the release of three captive-raised adolescent male African elephants in the Okavango Delta, Botswana.

Methodology/Principal Findings

Despite having been part of a herd of working elephants for at least eight years, the three males progressively integrated into the complex fission-fusion society of wild bull elephants. In the three years following release, they showed no tendency to be closer to human habitation, and there were no significant differences between wild and captive-raised adolescent males in the total number of social interactions, size of ranges and habitat use. However, the captive-raised elephants sparred less and vocalised more, and spent more time alone and in smaller social groups. Thereafter the released elephants continued to expand their ranges and interact with both mixed-sex herds and males. One male was shot by farmers 94 months after release, along with ten wild elephants, on a ranch outside the protected area.

Conclusions/Significance

We show that captive-raised adolescent male elephants can integrate into a wild population. Long-term studies are required to determine the longevity, breeding success, and eventual fate of released male elephants, but we identified no significant short-term welfare problems for the released elephants or recipient population. Release of captive-raised mammals with complex social systems is a husbandry option that should be explored further.     

Perceived object stability depends on multisensory estimates of gravity

Background

How does the brain estimate object stability? Objects fall over when the gravity-projected centre-of-mass lies outside the point or area of support. To estimate an object''s stability visually, the brain must integrate information across the shape and compare its orientation to gravity. When observers lie on their sides, gravity is perceived as tilted toward body orientation, consistent with a representation of gravity derived from multisensory information. We exploited this to test whether vestibular and kinesthetic information affect this visual task or whether the brain estimates object stability solely from visual information.

Methodology/Principal Findings

In three body orientations, participants viewed images of objects close to a table edge. We measured the critical angle at which each object appeared equally likely to fall over or right itself. Perceived gravity was measured using the subjective visual vertical. The results show that the perceived critical angle was significantly biased in the same direction as the subjective visual vertical (i.e., towards the multisensory estimate of gravity).

Conclusions/Significance

Our results rule out a general explanation that the brain depends solely on visual heuristics and assumptions about object stability. Instead, they suggest that multisensory estimates of gravity govern the perceived stability of objects, resulting in objects appearing more stable than they are when the head is tilted in the same direction in which they fall.     

The Impact of Social Context and Language Comprehension on Behaviour: A Kinematic Investigation

We investigated whether and how comprehending sentences that describe a social context influences our motor behaviour. Our stimuli were sentences that referred to objects having different connotations (e.g., attractive/ugly vs. smooth/prickly) and that could be directed towards the self or towards “another person” target (e.g., “The object is ugly/smooth. Bring it to you/Give it to another person”). Participants judged whether each sentence was sensible or non-sensible by moving the mouse towards or away from their body. Mouse movements were analysed according to behavioral and kinematics parameters. In order to enhance the social meaning of the linguistic stimuli, participants performed the task either individually (Individual condition) or in a social setting, in co-presence with the experimenter. The experimenter could either act as a mere observer (Social condition) or as a confederate, interacting with participants in an off-line modality at the end of task execution (Joint condition). Results indicated that the different roles taken by the experimenter affected motor behaviour and are discussed within an embodied approach to language processing and joint actions.     

The relationship between social behaviour and habitat familiarity in African elephants (Loxodonta africana)

Social associations with conspecifics can expedite animals'' acclimation to novel environments. However, the benefits gained from sociality may change as the habitat becomes familiar. Furthermore, the particular individuals with whom animals associate upon arrival at a new place, familiar conspecifics or knowledgeable unfamiliar residents, may influence the type of information they acquire about their new home. To examine animals'' social dynamics in novel habitats, we studied the social behaviour of African elephants (Loxodonta africana) translocated into a novel environment. We found that the translocated elephants'' association with conspecifics decreased over time supporting our hypothesis that sociality provides added benefits in novel environments. In addition, we found a positive correlation between body condition and social association, suggesting that elephants gain direct benefits from sociality. Furthermore, the translocated elephants associated significantly less than expected with the local residents and more than expected with familiar, but not necessarily genetically related, translocated elephants. The social segregation between the translocated and resident elephants declined over time, suggesting that elephants can integrate into an existing social setting. Knowledge of the relationship between sociality and habitat familiarity is highly important in our constantly changing world to both conservation practice and our understanding of animals'' behaviour in novel environments.     

Rhesus macaques use probabilities to predict future events

Humans can use an intuitive sense of statistics to make predictions about uncertain future events, a cognitive skill that underpins logical and mathematical reasoning. Recent research shows that some of these abilities for statistical inferences can emerge in preverbal infants and non-human primates such as apes and capuchins. An important question is therefore whether animals share the full complement of intuitive reasoning abilities demonstrated by humans, as well as what evolutionary contexts promote the emergence of such skills. Here, we examined whether free-ranging rhesus macaques (Macaca mulatta) can use probability information to infer the most likely outcome of a random lottery, in the first test of whether primates can make such inferences in the absence of direct prior experience. We developed a novel expectancy-violation looking time task, adapted from prior studies of infants, in order to assess the monkeys' expectations. In Study 1, we confirmed that monkeys (n = 20) looked similarly at different sampled items if they had no prior knowledge about the population they were drawn from. In Study 2, monkeys (n = 80) saw a dynamic ‘lottery’ machine containing a mix of two types of fruit outcomes, and then saw either the more common fruit (expected trial) or the relatively rare fruit (unexpected trial) fall from the machine. We found that monkeys looked longer when they witnessed the unexpected outcome. In Study 3, we confirmed that this effect depended on the causal relationship between the sample and the population, not visual mismatch: monkeys (n = 80) looked equally at both outcomes if the experimenter pulled the sampled item from her pocket. These results reveal that rhesus monkeys spontaneously use information about probability to reason about likely outcomes, and show how comparative studies of nonhumans can disentangle the evolutionary history of logical reasoning capacities.     

The extent of visual control in the courtship tracking of D. melanogaster

The courtship tracking behaviour of male D. melanogaster was filmed in a range of visual mutants and in wild type flies under white and infra-red light. The absence of visual input severely restricts the velocity at which the female may be tracked but does not remove the male's ability to discriminate the female's abdomen from her head. Degradation of visual processing, such as occurs in certain visual mutants, leads mainly to disruption of the control of orientation in tracking. The gain control of translation may only be meaningfully assessed when vision is enabled. Courtship tracking does not depend upon the presence of a binocular field of vision; one eyed flies court with a lateral displacement of the body, and loose visual contact with the female readily when her image moves from the sighted towards the blind eye. The selection of the left or right wing for extension follows a distinct pattern with the male's position and orientation around the female; this may be controlled collateral to locomotor output and after interlateral comparison of sensory input.     

Mutual assessment via visual status signals in Polistes dominulus wasps

Many animals use signals to assess the fighting ability of rivals and reduce the cost of aggressive competition. However, little is known about how an individual''s own quality influences their signal assessment decisions. Polistes dominulus wasps have visual signals of fighting ability that provide a good model for testing the dynamics of rival choice. We found that rival assessment behaviour was influenced by the advertised quality of the individual, their rivals, and the interaction between individual and rival quality. Individuals of high advertised quality were more likely to challenge rivals and individuals of low advertised quality were more likely to be challenged. However, when choosing among two rivals with different advertised quality, individuals did not simply choose the lower quality rival. Instead, they only preferred the lower quality rival when there was a small difference between their own advertised quality and that of their rivals. Individuals were not choosy when both rivals advertised relatively high or relatively low quality. Therefore, although P. dominulus facial patterns function as conventional signals of fighting ability that provide valuable information about their bearer''s behavioural strategy, there is substantial variation in signal responses based on the relative intensity of the senders'' and receivers'' signals.