Development of Gaze Following Abilities in Wolves (Canis Lupus): Friederike Range, Zsófia Virányi (2011)

Abstract

Según esta investigación los lobos son capaces de seguir

la mirada de un humano para encontrar objetos ocultos

 

"The ability to coordinate with others' head and eye orientation to look in the same direction is considered a key step towards an understanding of others mental states like attention and intention. Here, we investigated the ontogeny and habituation patterns of gaze following into distant space and behind barriers in nine hand-raised wolves. We found that these wolves could use conspecific as well as human gaze cues even in the barrier task, which is thought to be more cognitively advanced than gazing into distant space. Moreover, while gaze following into distant space was already present at the age of 14 weeks and subjects did not habituate to repeated cues, gazing around a barrier developed considerably later and animals quickly habituated, supporting the hypothesis that different cognitive mechanisms may underlie the two gaze following modalities. More importantly, this study demonstrated that following another individuals' gaze around a barrier is not restricted to primates and corvids but is also present in canines, with remarkable between-group similarities in the ontogeny of this behaviour. This sheds new light on the evolutionary origins of and selective pressures on gaze following abilities as well as on the sensitivity of domestic dogs towards human communicative cues."

Introduction

"One central feature of social life and communication in humans is the monitoring of others' head and eye orientation (gaze). The abilities to coordinate with others and look in the same direction (gaze following) or at a specific target (joint attention) develop early during ontogeny. […] Due to these theoretical implications and in order to understand the evolutionary roots of such capabilities, gaze-following abilities in non-human animal species have recently received increased attention."

Layout of the barrier test, showing the position of the human E 1 and the start position of the test subject. E2 held the subject on the collar or leash until the gaze cue was given. The arrows indicate where E 1 looked in the test and control conditions respectively.

"Interestingly, while most animals have difficulties in interpreting the gaze of others as a communicative intentional cue and fail to choose a food container indicated by the gaze of a cooperative partner, animals are quite successful in using others' gaze to detect significant events in their environment. These later gaze following abilities have been observed in several animal species.
[…] While several species have been shown to successfully follow another's gaze into distant space […] have been reported to successfully follow another's gaze geometrically around a visual barrier by repositioning themselves to follow a gaze cue when faced with a barrier blocking their view. […] This mosaic of results is strongly connected to theoretical considerations concerning the underlying cognitive mechanism of gaze following. Povinelli and Eddy suggest that gaze following into distant space may be a socially facilitated orientation response (i.e. a predisposition to look where others are looking). This would probably require no more than an intrinsic tendency to co-orient with others, combined with associative learning. However, when faced with a barrier blocking their view, individuals need to reposition themselves to look behind the obstacle thus assessing the difference in visual perception between the cue-giver and themselves. [...] It has been hypothesized that especially species with high levels of cooperative and competitive interactions may develop the ability to track another's gaze around obstacles, whereas the capability to follow another's gaze into distant space is likely to be adaptive for most socially living vertebrates since it will allow detecting predators or food resources earlier. [...]"

Seguir la dirección de la mirada de los otros es una importante fuente de información que ayuda al lobo a detectar a sus presas o depredadores, a percibir eventos relevantes dentro de su grupo social y predecir las próximas acciones de los demás.

"[...] Wolves (Canis lupus), the ancestors of domestic dogs, are well known for their cooperative hunting. Visual coordination, including following their partner's gaze into distant space and around barriers, should thus be very adaptive to their survival. It has been hypothesized, however, that, compared to domestic dogs, wolves may be less ready to accept humans as social partners. In line with this argument, one can expect that, similarly to ravens, wolves follow the gaze of humans later in development than the gaze of conspecifics. Therefore, in experiment 1, we tested the wolves across several ages to determine if they follow the gaze of both a human experimenter and a conspecific partner around a barrier, and, if so, when this ability emerges during development. Both to verify that wolves have the ability to follow humans' gaze direction as shown in experiment 1 and to determine the possible mechanisms involved, experiment 2 was designed to test the wolves' ability to follow the gaze of a human experimenter into distant space. According to the theoretical considerations outlined above, we expected this ability to develop earlier during ontogeny than following human gaze around the barrier. To gather additional information in regard to the underlying mechanisms, we also compared the habituation pattern of the two gaze following modalities using a human experimenter. Based on the only available data, we expected that wolves would quickly cease responding to repeated gaze cues into distant space but would show no habituation to repeated trials in the barrier task."

Box plots showing the latency of wolves to look behind the barrier in the control and test trials according to whether a dog or a human demonstrated the gaze cue. Each test was repeated at the age of 4, 5 and 6 months of age. Shaded boxes represent the interquartile range, bars within shaded boxes are median values and whiskers indicate the 5th and 95th percentile.

General Methods

Subjects 

"All wolves (n = 9) that participated in this study originated from North America and were born in captivity. [...] All of them were hand-raised [...] after being separated from their mothers in the first 10 days after birth. They were bottle-fed and later hand-fed by humans and had continuous access to humans the first 5 months of their life. When the second generation was five months old, they were introduced to the pack of the 1.5 year-old wolves. [...] From this age on, there were no humans continuously present in the enclosure, but the wolves participated in training and/or cognitive and behavioural experiments at least once a day and hence had intensive social contact with humans. Also, five adult dogs of various breeds were present during the hand-raising of the wolves. They established close relationships with the wolves and until the end of this study all wolves readily submitted to the dogs. [...]"

Median latency of individual wolves to follow the gaze in the first 5 and last 5 trials of the habituation experiments. A: Gaze following around the barrier; B: Gaze following into distant space.

Experiment 1: Gaze following around the barrier Top

"In experiment 1, we aimed at testing if wolves would follow the gaze of a human and/or a conspecific experimenter around a barrier and how this ability develops over ontogeny. Furthermore, we tested if the animals habituated to repeated trials. [...]"

Discussion

"The results of experiment 1 show that gaze following around the barrier appears in wolves reliably only at the age of 6 months. [...] Overall the results indicate that by 6 months of age, wolves reliably follow the gaze of conspecifics and to a certain degree also of humans around a barrier. [...]"

Gaze following into distant space. A: control trial; B: test trial.

Experiment 2: Gaze following into distant space

"In this experiment we aimed at testing whether wolves' ability to follow human into distant space develops earlier than following human gaze around a barrier and whether wolves would habituate to these gaze cues differently."

Discussion
"The wolves followed the gaze of the human demonstrator into distant space significantly more often in the first 2 seconds and faster in the entire test condition compared to the control condition. This ability was already present at an age of 14 weeks when the wolves were tested the first time. [...] As argued in the introduction, it seems to confirm that simpler mechanisms underlie this form of gaze following in contrast to geometrical gaze follow. [...]  At the age of 14 weeks, wolf pups already spend a lot of time out of the den and engage in complex interactions with their fellow pack members including playing where they should keep track of each other. [...] In contrast to our expectation, the wolves showed a lack of habituation in the gaze following task into distant space."

General Discusion

"Taken together, our results provide the first evidence that a non-primate mammalian species, the wolf, is also able to follow the gaze of others' not only into distant space but also around barriers. Moreover, while the wolves did not habituate to the gaze following cue into distant space within 10 trials, they rapidly habituated towards gaze following in the barrier task. 

While the ontogeny of the two different gaze following abilities was in line with our expectation supporting the theoretical consideration that these two abilities may have different underlying cognitive mechanisms, habituation patterns differed from our expectations based on published data in corvids."

"[...] Wolves live in closed social groups with social interactions changing constantly and rapidly. Thus, following the cue of another individual repeatedly might still be adaptive since it might reveal new information every time. [...]

Overall, our data suggest that wolves are excellent at using conspecifics' as well as human gaze cues (if properly socialized) even to track gaze behind barriers, showing that this ability is not restricted to primate and corvid species. Relying on gaze cues to understand other individuals as intentional beings or, alternatively, to learn to use others' gaze cues, as predictors for their future behaviour, may be a crucial prerequisite for the highly cooperative social system in which wolves live. However, these new results raise questions as why dogs do not follow gaze into distant space but do so in object choice tasks and call for further tests in dogs and wolves to get a better understanding of the effect of domestication on dogs' sensitivity towards human communicative cues. Finally, the patterns of ontogeny and habituation found in our wolves provide further evidence that the underlying cognitive mechanisms in the two gaze following abilities differ."

Supporting Information

"Video S1. Gaze following around the barrier. The video illustrates a test and control trial of the gaze following around a barrier response of a wolf. (M4V)
Video S2. Gaze following into distant space. The video illustrates a test and control trial of the gaze following response of a wolf. (M4V)"

(Nota:Para visualizar los videos es necesario descargarlos desde el archivo original y cambiar la extensión a m4v)

Development of Gaze Following Abilities in Wolves (Canis Lupus): Friederike Range, Zsófia Virányi (2011) PLoS ONE 6(2): e16888.doi:10.1371/journal.pone.0016888 http://bit.ly/Szshf1 (Publicado en http://www.plosone.org/ )