Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task

doi:10.1016/j.anbehav.2004.05.008

Animal Behaviour

Volume 69, Issue 1, January 2005, Pages 11-18

https://doi.org/10.1016/j.anbehav.2004.05.008 Get rights and content

Gaze following is a basic social cognitive skill with many potential benefits for animals that live in social groups. At least five primate species are known to follow the gaze of conspecifics, but there have been no studies on gaze following in other mammals. We investigated whether domestic goats can use the gaze direction of a conspecific as a cue to find food. They were able to do this, at a level comparable to that of primates. In a second experiment, we tested goats' ability to use gaze and other communicative cues given by a human in a so-called object choice situation. An experimenter hid food out of sight of the subject under one of two cups. After baiting the cup the experimenter indicated the location of the food to the subject by using different cues. The goats used communicative cues (touching and pointing) but not gaze by itself. Since domestic dogs are very skilled in this task, whereas wolves are not, one hypothesis is that the use of communicative cues in the object choice task is a side-effect of domestication.

Section snippets

Experiment 1: gaze following

In this experiment we replicated the procedure of Tomasello et al. (1998) using domestic goats as subjects to investigate whether mammals other than primates follow the gaze direction of conspecifics.

Experiment 2: object choice

In experiment 2 we investigated whether goats can use not only cues of conspecifics in a gaze-following situation but also human-given cues to locate hidden food in the so-called object choice task.

General discussion

Our experiments had two basic results. First, domestic goats followed the gaze direction of conspecifics to outside objects/events, and they did this at the same general level as primates. Second, they were able to use some cues in the object choice task to locate hidden food. We discuss the cognitive and evolutionary implications of each finding.

From a cognitive point of view, following the gaze direction of others can reflect a number of different cognitive processes. As noted above, simply

Acknowledgments

We thank Juliane Bräuer and Katrin Schumann for helping with data collection. We also thank the caretakers of the Leipzig Zoo, Tierpark Weissenfels and Tierpark Hirschfeld for their help. In addition we thank Nicholas Mulcahy and Daniel Stahl for helpful comments on the manuscript.

References (39)

F.G. Barroso et al.
Social hierarchy in the domestic goat: effect on food habits and production
Applied Animal Behaviour Science
(2000)
B. Hare et al.
Chimpanzees know what conspecifics do and do not see
Animal Behaviour
(2000)
B. Hare et al.
Do chimpanzees know what conspecifics know?
Animal Behaviour
(2001)
H. Kobayashi et al.
Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye
Journal of Human Evolution
(2001)
A. Miklosi et al.
A simple reason for a big difference: wolves do not look back at humans, but dogs do
Current Biology
(2003)
M. Tomasello et al.
Five primate species follow the visual gaze of conspecifics
Animal Behaviour
(1998)
M. Tomasello et al.
Chimpanzees, Pan troglodytes, follow gaze direction geometrically
Animal Behaviour
(1999)
J.R. Anderson et al.
Macaques but not lemurs co-orient visually with humans
Folia Primatologica
(1999)
R.W. Byrne
The Thinking Ape: Evolutionary Origins of Intelligence
(1995)
J. Call et al.
Chimpanzee gaze in an object-choice task
Animal Cognition
(1998)

J. Call et al.

Domestic dogs (Canis familiaris) are sensitive to the attentional state of humans

Journal of Comparative Psychology

(2003)

R. Coppinger et al.

Differences in the behavior of dog breeds

N.J. Emery et al.

Effects of experience and social context on prospective caching strategies by scrub jays

Nature

(2001)

N.J. Emery et al.

Gaze following and joint attention in rhesus monkeys (Macaca mulatta)

Journal of Comparative Psychology

(1997)

B. Hare et al.

Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food

Journal of Comparative Psychology

(1999)

B. Hare et al.

Communication of food location between human and dog (Canis familiaris)

Evolution of Communication

(1998)

B. Hare et al.

The domestication of social cognition in dogs

Science

(2002)

H. Hemmer

Domestication: The Decline of Environmental Appreciation

(1990)

L.M. Herman et al.

Dolphins (Tursiops truncatus) comprehend the referential character of the human pointing gesture

Journal of Comparative Psychology

(1999)

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Citation Excerpt :
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View full text

Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task

Section snippets

Experiment 1: gaze following

Experiment 2: object choice

General discussion

Acknowledgments

Applied Animal Behaviour Science

Animal Behaviour

Animal Behaviour

Journal of Human Evolution

Current Biology

Animal Behaviour

Animal Behaviour

Macaques but not lemurs co-orient visually with humans

Folia Primatologica

The Thinking Ape: Evolutionary Origins of Intelligence

Chimpanzee gaze in an object-choice task

Animal Cognition

Domestic dogs (Canis familiaris) are sensitive to the attentional state of humans

Journal of Comparative Psychology

Differences in the behavior of dog breeds

Effects of experience and social context on prospective caching strategies by scrub jays

Nature

Gaze following and joint attention in rhesus monkeys (Macaca mulatta)

Journal of Comparative Psychology

Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food

Journal of Comparative Psychology

Communication of food location between human and dog (Canis familiaris)

Evolution of Communication

The domestication of social cognition in dogs

Science

Domestication: The Decline of Environmental Appreciation

Dolphins (Tursiops truncatus) comprehend the referential character of the human pointing gesture

Journal of Comparative Psychology