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The ability of dogs to follow human communicative cues

Author Name: Emma Walters, BSc (Hons) Animal Behaviour and Welfare

 

Abstract

Humans and dogs share a unique relationship, where the dogs’ ability to interpret human communicative skills outperform both humans’ and dogs’ closest living ancestors. Dogs are particularly skilled at following human pointing gestures. Researchers question whether this skill developed due to domestication or learning during ontogeny. Object-choice tasks are used to assess the dogs’ ability to follow human pointing. However, differences between methods used in the studies mean results cannot be compared and some are biased, questioning the validity of the hypothesis they support. The procedure used to carry out object-choice tasks should be consistent, as differences may affect motivation and performance and different species may respond differently. The type of point may also influence results through varying the levels of difficulty, and easier points may cause bias through local enhancement. Momentary distal points may be appropriate as a baseline measure, as this controls for local enhancement and may be more representative of a communicative interaction. When comparing different species, rearing backgrounds should be similar to ensure comparable results and control for performance bias caused by previous training, or fear. Stress should be considered during testing, as this may affect the subjects’ performance and measuring stress levels during testing may be beneficial. When analysing data, individual and group results should be included for subjects’ performance and ability to follow specific gestures, so reliable results are obtained. Ensuring object-choice tasks use the same procedure between studies and provide clear, detailed methods can ensure comparable results, minimise bias and ensure tests are repeatable.

 

1.0 Introduction

Dogs (Canis lupus familiaris) have developed remarkable abilities to use human social behaviour and communication (Miklósi, 2009; Phillips Buttner, 2016). Dogs have been found able to interpret human emotional (Buttelman and Tomasello, 2013; Nagasawa et al. 2011) and attentional states (Call et al. 2003; Virányi et al. 2004), comprehend human visual perception (Kaminski et al. 2009; MacLean, Krupenye and Hare, 2014) and learn socially from copying human behaviour (Tópal et al. 2006). Dogs are particularly skilled at following human ostensive signals (e.g. pointing) (Riedel et al. 2008; Gácsi et al. 2009a), showing similar performance to human infants (aged 2 years old) (Lakatos et al. 2009). Dogs outperform humans’ closest living ancestors, chimpanzees (Pan troglodytes) (MacLean et al. 2017) and wolves (Canis lupus) (Viryáni et al. 2008). This questions how a distantly related species developed social skills comparable to humans (Elgier et al. 2009; Hare, 2017). Researchers have suggested domestication enabled this ability (Hare et al. 2010; Wobbler et al. 2009), though what part of the domestication process, or if domestication at all is involved, is debated (Wynne, Udell and Lord, 2008; Helton and Helton, 2010; Range and Viryáni, 2015; Udell et al. 2014).

 

2.0 Critical Review

2.1 Communication

The ethological approach to communication defines it as a sender altering its behaviour to elicit a response from the receiver, benefiting sender and receiver, or just sender (Krebs and Davies, 1993; Miklósi, 2009). Visual communication (e.g. pointing, gaze) has been used to test dogs’ ability to follow human communicative cues (Reid, 2009). This review focuses on the ability to follow human pointing. Pointing is a behaviour unique to humans (Miklósi and Soproni, 2006; Tauzin et al. 2015). For a different species to be able to interpret human pointing suggests a form of interspecific communication (Miklósi and Soproni, 2006).

 

2.1.1 Hypotheses for dogs’ socio-cognitive abilities

Conflicting hypotheses question how dogs developed their socio-cognitive abilities to interpret human communicative cues. The domestication hypothesis argues that it developed through direct and/or indirect selection during domestication (Kaminski and Nitzschner, 2013); while the two-stage hypothesis claims domestication is not necessary for these skills to develop and they are learned from sharing a human environment during ontogeny (Udell, Dorey and Wynne, 2010a); and the synergistic hypothesis maintains learning during ontogeny and domestication enable dogs’ abilities (Gácsi et al. 2009c). Evidence supporting these hypotheses is based on the reliability and validity of the methodology used to assess them (Pongrácz et al. 2013), yet methodologies vary between studies, meaning results may be biased (Reid, 2009; Miklósi and Topál, 2011).

 

2.2 Object-choice tasks

Object-choice tasks (OCT) assess the ability of a subject to follow human pointing (Reid, 2009). The general design of an OCT is to have 2 opaque containers where one is baited (usually with food), and the other is sham-baited. Subjects are aware that a reward is hidden but not its location. The experimenter gestures to the baited container and the subject chooses between the containers (see figure 1) (Oliva et al. 2015). The subject is only rewarded if they choose correctly. For a subject to be considered as interpreting the signal, they must perform at above chance levels (e.g. 15 out of 20 correct trials) (Udell, Dorey and Wynne 2010).

 

Figure 1 EW

Figure 1: An example of an OCT set-up (Pet Behaviour Science, 2016).

 

2.2.1 Procedure

For most OCTs the reward is hidden, and subjects are aware of this (Hare et al. 2010). One method uses a different procedure where a container is pointed at, but no bait is hidden. If the subject chooses correctly the experimenter drops the reward (Udell, Dorey and Wynne, 2008; 2010a; Zaine, Domeniconi and Wynne, 2015). This approach is used to account for the subjects using olfactory cues (Udell, Dorey and Wynne, 2008). Although this procedure follows the same principle of following a human point to obtain a reward, the motivation for doing so may differ, e.g. following the point to a correct location then being rewarded, compared to locating the hidden reward. In addition, as the subject does not have to find food indicated by pointing there is no link between the reward and the pointing gesture (Pongrácz et al. 2013). Additionally, control trials in previous studies have found olfactory cues do not influence choice (Riedel et al. 2008; Viryáni et al. 2008). A pre-trial is required for this design, whereby the experimenter gains the subject’s attention, then places the reward on a container, repeating both sides until the subject approaches. This builds association with the reward and container and helps control for neophobia (Dorey, Udell and Wynne, 2010; Udell, Dorey and Wynne, 2008). However, this may reinforce an association between the hand and container, potentially influencing performance (Pongrácz et al. 2013).

Furthermore, some studies use clickers to mark correct choices (Udell, Dorey and Wynne, 2008). Clickers are secondary reinforcers (Wilson et al. 2017) used to mark desired behaviour (Feng, Howell and Bennett, 2017). Clicking may reinforce approach behaviour instead of interpreting the pointing gesture, potentially affecting performance (Gácsi et al. 2009c; Pongrácz et al. 2013). These methods have been used to argue for the two-stage hypothesis, but this may be biased for the reasons stated above. Pongrácz et al. (2013) tested these confounding factors, finding no significant improvement for using a clicker alone, even if dogs were clicker trained. Instead, they suggest the clicker, dropping food, and methods used in pre-trials combined may influence performance. Furthermore, testing these variables on wolves’ performance may be interesting, as Udell, Dorey and Wynne (2008) found wolves performed better using this method, although factors such as previous training experience may have influenced this (Hare et al. 2010). This highlights the need for consistency amongst OCTs, to control for potential influences and ensure comparable results.

 

2.2.2 Type of point

Different points have been used for different studies, potentially influencing results due to varying degrees of difficulty as they can be easier or more difficult to interpret (Miklósi and Soproni, 2006; Viryáni et al. 2008). This means studies using different points may be incomparable and results from studies using easier points may be biased (Gacsi et al. 2009c). Proximal (fingertip is 10-40cm away from the container), dynamic (subject views point occurring, remaining in place until the subject choses), and static points (the point is in place when the subject approaches, remaining until the subject chooses) may cause bias through local enhancement, i.e. the physical association between the point and food location (Miklósi and Soproni, 2006; Viryáni et al. 2008), or the subject approaching the closest part of the experimenter (Reid, 2009). Momentary (point lasts no more than 2 seconds and ends before the subject can choose) distal (container is more than 50cm away from fingertip) points (MDPs) may be most suitable as baseline points for OCTs when assessing the communicative ability to follow pointing. Although the subject may be influenced by the movement of the point, local enhancement is controlled for due to the distance of the point to the container (Viryáni et al. 2008). Furthermore, as the subject must remember the signal before choosing, it is more in line with communicative interaction, where a sender emits a short discrete signal (Miklósi and Soproni, 2006; Viryáni et al. 2008). By setting baseline measures, it may be easier to compare studies assessing different factors more reliably (Viryáni et al. 2008). Gaze and head turning should also be considered during pointing tasks (e.g. looking at subject, not looking at the subject) (Udell, Dorey and Wynne, 2010b; Cunningham and Ramos, 2014) as this can also influence performance, as dogs appear sensitive to human attentional states and whether the cue is intended for them (Kaminski et al. 2012). This highlights the importance of providing clear methods, to ensure that studies are repeatable and comparable (Miklósi and Soproni, 2006; Hare et al. 2010; Udell, Dorey and Wynne, 2010b).

 

2.2.3 Subjects’ history

To assess whether domestication impacted dogs’ ability to follow human communicative gestures, it might be useful to consider whether their wild ancestors, wolves, can perform this task (Viryáni et al. 2008; Miklósi and Topál, 2011). However, dogs may have an advantage over wolves in their ability to interpret human communicative gestures as living in an anthropogenic environment gives them the opportunity to learn about human social behaviour (Gacsi et al. 2013; Viryáni and Range, 2014, p.35). In addition, if wolves and dogs share genes which emerge indirectly from environmental factors (e.g. exposure to human gestures), different rearing conditions may mean that these are expressed differently, potentially affecting performance (Miklósi and Topál, 2011). Similarly, performance bias may occur if subjects are fearful due to not being socialised to humans, or human environments (Viryáni et al. 2008), or if subjects have already learned similar tasks (Hare et al, 2010). To compare the communicative skills of wolves and dogs, they should be reared similarly, with exposure to humans to control for fear responses.

Viryáni et al (2008) raised 9 wolves and 8 puppies under an intensive socialisation programme, raised by humans without their mothers and littermates shortly after birth (4-7 days wolves, 4-10 days puppies). Both had the same upbringing until 2 months, when the wolves moved into a wolf park, receiving 2 days a week of contact with their carer and daily contact with other people at the park responsible for their husbandry, and the puppies remained with their human. These groups were compared to 9 pet dogs in an OCT using MDP. All subjects were 4 months at the time of testing. None of the wolves performed above chance in the OCT, but 4 pet dogs and 3 hand-raised puppies were successful. This suggests that the ability to follow human pointing cannot be attributed to learning during ontogeny, supporting the domestication hypothesis. Although, at 2 months old the wolves were raised differently, potentially giving the hand-raised puppies an advantage due to spending extra time in human social environments (Udell and Wynne, 2010). However, Gácsi et al. (2009c) compared pet dogs to hand-raised wolves, kept until 3-4 months of age, using MDP. Both were 4 months when tested. They found wolves did not perform above chance but dogs did, supporting Viryáni et al.‘s (2008) findings.

Breed, age and background should also be considered when comparing human-dog communication, to compare how experience with humans, breed traits and development affect dogs’ performance in OCTs (Gácsi et al. 2009b; Riedel et al. 2008; Lazarowski and Dorman, 2015). Studies have compared shelter and pet dogs to assess how experience with humans affects performance (Udell, Dorey and Wynne, 2010a; Barrera et al. 2015). Poor performance of shelter dogs is thought to indicate that learning from experience around humans is a factor in dogs’ social-cognitive abilities (Udell, Dorey and Wynne, 2008; Zaine, Domeniconi and Wynne, 2015). However, caution should be taken when interpreting these results. Shelters are stressful environments (Barnard et al., 2015; Protopopova, 2016) and stress may affect dogs’ cognitive abilities during OCTs (Phillips Buttner, 2016). Furthermore, dogs may be relinquished to shelters due to behavioural problems (Diesel, Brodbert and Pfeiffer, 2009; Kwan and Bain, 2013), or cognitive impairments (Udell et al. 2010; Miklósi and Topal, 2011).

Zaine, Domeniconi and Wynne (2015) compared puppies at a shelter aged 8-12 weeks to those aged 20-24 weeks, finding that younger puppies outperformed older. This did not support their argument for the two-stage hypothesis. Upon further investigation they found that 18 out of 20 younger puppies were given up by their owner, compared to 5 out of 20 older puppies, suggesting that prior experience in a human environment affected younger dogs’ ability. However, this conclusion alone is an assumption as the dogs’ exact rearing history cannot be known (Cunningham and Ramos, 2014; Lazarowski and Dorman, 2015). Another explanation for this result could be due to the socialisation period for puppies which is between 3-12 weeks (Case, 2005, pp. 149-150; Landsberg, Hunthausen and Ackerman, 2013, p.15). During this period puppies are less fearful of new experiences and situations (Landsberg, Hunthausen and Ackerman, 2013, p.15). Due to this reduction in fear, the younger puppies would likely be less stressed than older puppies, who had finished their socialisation period (Phillips Buttner, 2016), supporting the suggestion of stress affecting performance. To investigate the impact stress may have upon performance, experiments could include an independent observer assessing stress-related behaviours.

 

2.2.4 Statistical analysis

When analysing the results of OCTs for several subjects, individual and group performance should be assessed. Results from group performance may indicate overall success even if only a few individuals perform above chance, or most individuals score just above 50% (random choice) as suggested by Gácsi et al. (2009a). Grouping different gestures together should also be considered. Wynne, Udell and Lord (2008) re-analysed data from Riedel et al. (2008). By grouping together 3 different gestures they found a significant effect on performance, despite the group only performing above chance for one of the cues (Riedel et al. 2008; Hare et al. 2010). Differences have also been found between studies when including no-choices (subject does not choose a container) as an incorrect choice during analysis. Hare et al. (2010) re-analysed data from Udell, Dorey and Wynne (2008) who originally included no-choices as incorrect. When these tests were not included in the statistical analysis, results changed from not significant to significant. No-choices may be related to the subject experiencing fatigue or lack of motivation instead of an inability to interpret the cue (Hare et al. 2010). Interestingly most of the subjects scoring no-choice were shelter dogs, which may indicate stress affecting performance. However, it is debatable as to what constitutes an incorrect choice over a no-choice. Udell et al. (2014) found that one no-choice response was to approach the experimenter. However, in this experiment no food was hidden, but the experimenter dropped the food for the correct choice. Although an incorrect choice was made, the subjects may have approached the experimenter for food, potentially being a previously reinforced behaviour (e.g. begging for food from someone known to have food) (Udell and Wynne, 2010). This highlights the importance of detailed methods and the impact previous experience may have on performance.

 

3.0 Conclusion

Interspecific communication between humans and dogs has been identified through their ability to follow human pointing. OCTs offer insight into how dogs developed this skill. Differences between methodologies and limitations of OCTs may cause biased results questioning the validity of the hypothesis they support and making studies incomparable. Procedures used by studies should remain the same to control for differences in motivation, performance and between species. MDPs were suggested as a baseline measure when testing point following as this controls for local enhancement. Comparing dogs and wolves may offer insight into the role domestication or living in an anthropogenic environment has on the ability to follow human pointing. However, caution should be taken to ensure that subjects have similar rearing backgrounds to obtain comparable results. Furthermore, subjects’ history, age and breed should be considered. Stress may influence performance, so monitoring stress-related behaviours during trials may be beneficial. Performance and cues should be analysed on an individual level, as grouping subjects together may influence results. Authors should clearly state how they assess correct and incorrect choices. No-choices should be clearly defined as they may not indicate misinterpretation of the pointing cue. Future OCTs should consider the methods used and include detailed methodologies to minimise bias and ensure tests are repeatable and comparable.

 

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