Abstract
Domestication is an important factor driving changes in animal cognition and behaviour. In particular, the capacity of dogs to communicate in a referential and intentional way with humans is considered a key outcome of how domestication as a companion animal shaped the canid brain. However, the lack of comparison with other domestic animals makes general conclusions about how domestication has affected these important cognitive features difficult. We investigated human-directed behaviour in an ‘unsolvable problem’ task in a domestic, but non-companion species: goats. During the test, goats experienced a forward-facing or an away-facing person. They gazed towards the forward-facing person earlier and for longer and showed more gaze alternations and a lower latency until the first gaze alternation when the person was forward-facing. Our results provide strong evidence for audience-dependent human-directed visual orienting behaviour in a species that was domesticated primarily for production, and show similarities with the referential and intentional communicative behaviour exhibited by domestic companion animals such as dogs and horses. This indicates that domestication has a much broader impact on heterospecific communication than previously believed.
1. Introduction
Domestication is an important factor driving changes in animal cognition and behaviour. In particular, the capacity of dogs (Canis familiaris), but not wolves (C. lupus), to communicate in a referential and intentional way with humans is considered a key outcome of how domestication shaped the canid brain. Referential and intentional communication is defined as the persistent use and elaboration of successive orienting between a communicative partner and the target, and takes into account not only the presence but also the attentional stance of an audience [1].
Dogs are capable of using gazing behaviour as a form of referential and intentional communication [2,3]. This has often been tested with a so-called ‘unsolvable problem’ paradigm in which subjects (after a training phase) are offered a task with an inaccessible food reward [2]. Although young dogs also show some human-directed gazing behaviour, this trait seems to be influenced by developmental factors during their ontogeny [4]. In addition, both adult dogs and human toddlers (Homo sapiens) take into account the attentional stance of a human and increase their use of gaze alternations during an ‘unsolvable problem’ task, indicating the communicative and referential nature of the behavioural outcome in this task [5].
Two other domestic species have been tested using the ‘unsolvable problem’ paradigm. Cats (Felis catus) performed poorly and barely looked at humans, potentially owing to their rather solitary lifestyle [6]. Recently, horses (Equus caballus) were found to not only look towards humans, but they were also sensitive to the attentional state of the experimenter [7]. However, both dogs and horses have been domesticated to work closely with humans, which may explain their higher inclination to rely on human information. To date, no research on animals that have been domesticated for food and related products, rather than companionship, has been conducted to investigate whether these enhanced communication skills underlie a broader effect of domestication. To answer this question, we investigated goat behaviour in an ‘unsolvable problem’ task, in which subjects that were highly habituated to human presence and handling were either confronted with a forward-facing or away-facing human experimenter.
2. Material and methods
(a) Animals, keeping and management
The study was carried out at Buttercups Sanctuary for Goats (http://www.buttercups.org.uk), UK. We tested 34 adult goats (17 females and 17 castrated males; 2–15 years; various breeds), which were fully habituated owing to previous research [8]. In addition, the goats have experienced many positive interactions with staff, volunteers and visitors at the sanctuary, as well as circumstances in which food is inaccessible [8]. Routine care of the animals was provided by sanctuary employees and volunteers. The goats had ad libitum access to hay and were not food restricted before testing.
(b) Test procedure
Goats were tested individually in a familiar test pen. A plastic box lid was attached to a wooden board and placed in the middle of the pen. The main part of the transparent plastic box could be fixed to the board by catches on the box lid. During all trials, one experimenter (Experimenter 1) was positioned on either the left or right side of the wooden board while a second experimenter (Experimenter 2) was positioned approximately 250 cm away. In training trials, Experimenter 1 placed a food reward on the lid and covered it with the plastic box. Subjects could retrieve the reward by moving or overturning the box in three training trials that lasted for 60 s. If a subject did not complete two consecutive training trials within 60 s, then it was removed from the experiment (two subjects). Thus, a total of 32 subjects (15 females and 17 males) were used in the tests. Test trials (‘unsolvable’) were similar to the training trials, except that the box was fixed to the lid, rendering the food reward visible but inaccessible. Each subject received only one test trial, which lasted 120 s, and goats were assigned to one of two groups (16 goats per group). One group received a test trial in which Experimenter 1 faced the box (‘FORWARD’, figure 1a), whereas the other group received a test trial in which Experimenter 1 faced away from the box (‘BACK’, figure 1b). Experimenter 2 always looked straight at the box and thus served as a control for the general inclination of subjects in both test groups to gaze at humans. Throughout the duration of the training and test trials, both experimenters did not interact with the goat (see the electronic supplementary material for a detailed description).
Experimenter 1 in the test arena demonstrating the group conditions: (a) FORWARD condition and (b) BACK condition; Experimenter 2 (not in the image) was positioned on the right side of the camera in both test conditions. (Online version in colour.)
(c) Data scoring and analysis
All trials were videotaped (Sony HCR-CX190E Camcorder) and analysed using Kinovea 0.8.15. For training trials, a Friedman test was carried out in order to evaluate whether there was a reduction in the latencies to retrieve the food reward across the three training trials. Bonferroni-corrected Wilcoxon signed-rank tests were used for later pairwise comparisons. In test trials, subjects' interactions with the box were recorded as an indicator of motivation to retrieve the food reward. Human-directed behaviours such as general gazes towards the two experimenters and gaze alternations between experimenter and box (and vice versa) within 2 s were analysed (see electronic supplementary material for a detailed description). One quarter of the training and test trials was double-coded by C.N. and J.M.B. for the time to solve the task (training), frequency, latency and total duration of gaze and gaze alternating behaviours towards each of the experimenters (test). These were highly reliable (all at or above rs = 0.89, p < 0.01). Because data from test trials were not normally distributed, we used Mann–Whitney U tests to compare groups in each behavioural variable. Age, sex and breed were counterbalanced between groups, and therefore these parameters were not included in the analysis. Alpha was set at 0.05. All statistical analyses were conducted in R. 3.1.0 [9].
3. Results
(a) Training
The time taken to retrieve the food reward was significantly reduced over the training trials (median times for first trial: 9.18 s, second trial: 6.16 s, third trial: 5.36 s; Friedman χ² = 28.65, d.f. = 2, p < 0.001). There were significant reductions in the time taken for the goats to retrieve the reward from Trial 1 to Trial 2, and from Trial 2 to Trial 3 (both p's < 0.025). The latencies to retrieve the food reward in training trials did not differ between groups (all p's > 0.4). Goats never looked back during training trials.
(b) Test
There were no significant differences between groups regarding their interactions with the box (duration: U = 91, p = 0.17; latency: U = 123, p = 0.87; frequency: U = 119, p = 0.75). Thus, subjects from both groups were equally motivated to retrieve the reward. In general, goats gazed towards the forward-facing Experimenter 1 earlier (U = 61, p < 0.001; figure 2a), for longer (U = 187, p = 0.02; figure 2b) and more frequently (U = 191, p = 0.013; figure 2c) than towards Experimenter 1 facing away. Goats also performed their first gaze alternation earlier (U = 76, p = 0.038; figure 2d) and performed gaze alternations more frequently (U = 181, p = 0.033; figure 2e) when Experimenter 1 was forward-facing compared with the away-facing experimenter. Importantly, no behavioural differences between groups were found regarding Experimenter 2 (all p's > 0.4, figure 2).
Boxplots presenting the median times for (a) gaze latencies, (b) gaze durations, (c) gaze frequencies, (d) latencies until first gaze alternation and (e) frequencies of gaze alternations towards either Experimenter 1 or Experimenter 2. Dark grey bars: FORWARD group; light grey bars: BACK group. Asterisk indicates significant differences between groups.
4. Discussion
We investigated human-directed behaviour of goats in the ‘unsolvable problem’ paradigm [2]. Goats often exhibited gazing and gaze alternations at both experimenters during the test and clearly adjusted their behaviour depending on the attentional stance of Experimenter 1. Our results show that animals domesticated primarily for production show audience-dependent human-directed behaviour in a similar manner to companion animals such as dogs and horses [2,7]. Thus, domestication has probably had a much broader impact on heterospecific communication than previously believed.
Goats gazed earlier and for longer towards a forward-facing experimenter compared with an experimenter who had his back turned towards them. Goats also showed a higher frequency of gaze alternations and a lower latency until the first gaze alternation when the experimenter was facing forward. This has previously been shown for human toddlers, dogs and horses [5,7] and is in line with previous findings showing that goats alter their behaviour depending on human body and head orientation [10]. Importantly, no such difference between groups occurred for the second experimenter, who always faced the subjects, indicating no difference in the general predisposition of either group to gaze at humans.
All subjects physically interacted with one or both experimenters, most commonly to beg for food. Interestingly, we observed an additional, very specific type of approach behaviour. Here, goats stopped for approximately 2–3 s, 20–40 cm in front of the experimenter (see electronic supplementary material, video) with little or no physical contact, before returning to the box. This specific approach behaviour might be considered as an elaboration of the previously used gaze alternations. However, only 14/32 of goats (six in the FORWARD and eight in the BACK condition) exhibited this behaviour, making more detailed analysis impossible.
Goats in our study have experienced a history of positive long-term interactions with humans (e.g. receiving food) as well as circumstances in which food is inaccessible. Thus, this specific ontogeny, leading to an additional reduction of fear responses and/or the establishment of a referential problem space [11], may have affected the expression of human-directed behaviours that we report. It would be intriguing to test both hypotheses by comparing the behaviour of tame non-domesticated goats with domestic ones that are kept under similar husbandry conditions. Research that compared canids in the unsolvable task points towards a strong effect of domestication [2], although results in related tasks, like following human pointing gestures, indicated that previous experiences with humans can be a strong factor affecting the performance of canids [12].
5. Conclusion
Goats show human-directed visual orienting behaviour similar to the referential and intentional communication shown in hominoids, which is also evident in companion animals such as dogs and horses. This challenges the view that a specific kind of domestication, i.e. the selection for companionship, has led to the development of complex communication with humans in domestic animals.
Ethics
Animal care and all experimental procedures were in accordance with the ASAB/ABS Guidelines for the Use of Animals in Research. The study was approved by the Animal Welfare and Ethical Review Board committee of Queen Mary University of London (Ref. QMULAWERB032015).
Data accessibility
The data underlying this study are available from Dryad: http://dx.doi.org/10.5061/dryad.t6d26 [13].
Authors' contribution
C.N., J.M.B. and A.G.M. conceived/designed the study; J.M.B. and C.N. conducted experiments and analysed the data; C.N., J.M.B. and A.G.M. wrote the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed.
Competing interests
The authors have no competing interests.
Funding
This work was supported by grants from the Deutsche Forschungsgemeinschaft (NA 1233/1-1) to C.N. and Farm Sanctuary ‘Someone, not Something Project’ to A.G.M. and C.N.
Acknowledgements
We thank Robert Hitch and all staff and volunteers of Buttercups Sanctuary for Goats (www.buttercups.org.uk) for their excellent help and free access to the animals. We thank Natalia Albuquerque, Luigi Baciadonna and Claudia Wascher for helpful comments on the manuscript.
- Received April 6, 2016.
- Accepted June 14, 2016.
- © 2016 The Author(s)
Published by the Royal Society. All rights reserved.
Volume 12, issue 7
Keywords
