Anim Cogn (2008) 11:475–483 DOI 10.1007/s10071-008-0138-3 ORIGINAL PAPER How do guide dogs of blind owners and pet dogs of sighted owners (Canis familiaris) ask their owners for food? Florence Gaunet Received: 15 March 2007 / Revised: 3 January 2008 / Accepted: 17 January 2008 / Published online: 16 February 2008 © Springer-Verlag 2008 Abstract Although there are some indications that dogs (Canis familiaris) use the eyes of humans as a cue during human–dog interactions, the exact conditions under which this holds true are unclear. Analysing whether the interactive modalities of guide dogs and pet dogs diVer when they interact with their blind, and sighted owners, respectively, is one way to tackle this problem; more speciWcally, it allows examining the eVect of the visual status of the owner. The interactive behaviours of dogs were recorded when the dogs were prevented from accessing food that they had previously learned to access. A novel audible behaviour was observed: dogs licked their mouths sonorously. Data analyses showed that the guide dogs performed this behaviour longer and more frequently than the pet dogs; seven of the nine guide dogs and two of the nine pet dogs displayed this behaviour. However, gazing at the container where the food was and gazing at the owner (with or without sonorous mouth licking), gaze alternation between the container and the owner, vocalisation and contact with the owner did not diVer between groups. Together, the results suggest that there is no overall distinction between guide and pet dogs in exploratory, learning and motivational behaviours and in their understanding of their owner’s attentional state, i.e. guide dogs do not understand that their owner cannot see (them). However, results show that guide dogs are subject to incidental learning and suggest that they supplemented their way to trigger their owners’ attention with a new distal cue. F. Gaunet (&) Laboratoire “Eco-Anthropologie et Ethnobiologie” UMR 5145, Muséum National d’Histoire Naturelle, CP 135, 57 rue Cuvier, 75231 Paris Cedex 05, France e-mail: gaunet@mnhn.fr Keywords Human–dog interaction · Interactive behaviours · Social cognition · Guide dogs · Socialisation Introduction Over the past few years, it has been shown that dogs can read human social-communicative signals. For example, dogs use the direction of attention of humans to obtain food from the appropriate person and to perform forbidden actions (e.g. Call et al. 2003; Virányi et al. 2004). They understand human pointing, pointing and gazing, and gazing above chance level to locate hidden food or toys (e.g. Hare et al. 1998; Miklósi et al. 1998; Agnetta et al. 2000; Soproni et al. 2001, 2002). It has further been shown that dogs can indicate to a human the location of a hidden target (Miklósi et al. 2000). Together, these data conWrm folk psychology that there is an actual common space of communication between humans and dogs, based on perceiving the direction of attention of the partner, triggering his/her attention and indicating the location of an object. The present study focuses on dogs’ social-communicative signals for interacting with humans, and more speciWcally, with their owners. In an experiment by Miklósi et al. (2000), in which the owner was naive about the location of a hidden target (food or a toy located in one of three bowls unreachable by the dogs), dogs displayed intentional communicative behaviours towards their owner. SpeciWcally, when both the desired target and the owner were present, the dogs tended to gaze at their owner and at the target, sniV and lick their mouths, and alternately gaze at the target and the owner. Vocalisations were also observed and were always associated with gazing at the owner or at the location of the target (see also Hare et al. 1998, Study 3). These signals were successfully used by the humans to locate the 123 476 hidden target, conWrming that they were attention-getting and directional signals. Additionally, Miklósi et al. (2003) found that the dogs looked longer at their caregiver than wolves did when prevented from accessing food in a way they had previously learned. The use of human gaze by dogs as a social cue is thus a key to their interaction with humans. These studies show that dogs have a propensity to request help from humans using various types of signals when they encounter an unsolvable problem (Cooper et al. 2003; Hare 2004), and that dogs use humans as tools (Hare 2004). Convergent evolutionary and domestication processes have been deemed to be involved in the expression of human-like social skills in dogs (Hare and Tomasello 2005; Hare et al. 2005; see also Miklósi and Soproni 2006 for a discussion). The early, daily and long-standing closeness of domesticated dogs to humans further provides dogs a special niche for the development of socio-communicative skills (for a review, see Miklósi and Soproni 2006). Indeed, because dogs learn to communicate and collaborate throughout their lives with humans, they have ample opportunity to learn to use human behaviours, both intentional and unintentional, to predict future events as a result of simple learned contingencies (Cooper et al. 2003). Because primary interactions between dogs and humans focus on the management of a shared space (e.g. the human directs the dog to come or to leave, the dog asks the human for food or to go out, the dog or the human asks to play), communicative behaviours take place between the two species. Communicative behaviours are indeed viewed as a kind of control system that allows group members to synchronize activities and collaborate (Csányi 2000; see also Kerepesi et al. 2005). Domestic dogs’ social-communicative skills may thus be subject to learning, because they are exposed to, and immersed in, the human world. Importantly, dogs’ ability to use the most common human deictic cues is not acquired (e.g. Hare et al. 1998; Miklósi et al. 1998; Hare and Tomasello 1999; McKinley and Sambrook 2000; Agnetta et al. 2000; Soproni et al. 2001, 2002). Even puppies with little prior human contact use communicative signals such as gazing, and pointing and gazing (Hare et al. 2002). However, Hare and Tomasello (1999) found that in a group of dogs ranging from 6 months to 4 years of age, only the youngest (a 6-monthold dog) was able to use a directional cue given by a conspeciWc, whereas the oldest dogs (two of 4-year-olds) used only human cues. Miklósi et al. (1998) found that the dogs learned to use bowing, nodding and head-turning, and one dog learned to use directional glancing (see experiment 1); the use of glancing improved signiWcantly in the group, but the youngest dog never achieved the learning criteria (see experiment 2). Soproni et al. (2001) also observed that the ability to use eye direction as a cue developed across 123 Anim Cogn (2008) 11:475–483 sessions. In McKinley and Sambrook’s study (2000), two dogs out of 11 succeeded in using eye direction; moreover, trained gundogs were better at using arm pointing than untrained gundogs. Consequently, inter-individual variability among dogs’ social-communicative and learning and developmental processes may not be ruled out as factors in the ability of dogs to use some human-given cues, especially glancing. Even if dogs seldom use human eye direction as a cue for Wnding a toy or hidden food, a question that remains unanswered concerns the exact conditions allowing the sensitivity of dogs to human eyes in referential communication, but also in perceiving the spatial locus of human attention. For instance, when dogs are forced to choose between two humans holding food, they prefer to beg from a human whose head and eyes are visible and not covered (Gácsi et al. 2004). Dogs are also more likely to avoid approaching forbidden food when human eyes are open than when they are closed (Call et al. 2003). Moreover, dogs ignore a human’s gaze when the person stares into space above the correct hiding location (Soproni et al. 2001) and they do not follow eye direction at all if there is no attractive object (Agnetta et al. 2000). Finally, in the presence of eVective and ineVective barriers, dogs make the decision not to approach forbidden food when they cannot see the human or when the human cannot see them (Bräuer et al. 2004); dogs apparently project what the human can see through a small window. Thus, although there are some indications that human eyes, per se, are used by dogs as a cue, the exact conditions under which this holds true remain unknown. To address this issue, we chose a novel approach (Cooper et al. 2003; Bering 2004; Tomasello and Call 2004) to determine whether dogs use their owner’s eyes as a cue for inferring the direction of attention of their owner towards them. In the present study, guide dogs of blind owners are compared with pet dogs of sighted owners. Guide dogs and pet dogs obtain diVerent lifetime experiences depending on the visual status of their owner. Our goal was to determine whether dogs are sensitive to the visual status of their owner, and whether, as a consequence, dogs have somehow set up a way to trigger their owner’s attention when the owner is blind. The question of apprenticeship (Bering 2004) as the result of enculturation or socialisation (Tomasello and Call 2004) among dogs is raised here. Socialisation is the sensitive period for the formation of primary social relationships or attachments (Serpell 1995). On this basis, the two groups of the present study were similarly socialised, as they were reared in similar conditions at the earlier stage of their life (i.e. in sighted families). However, they diVered in terms of their adult living conditions. Guide dogs begin to get “blind-socialised” later in life (after generally about 1.5– 2 years). Though some studies have shown the eVects of Anim Cogn (2008) 11:475–483 early enculturation/socialisation on social-communicative skills in apes (Bering 2004; Tomasello and Call 2004; Miklósi and Soproni 2006), to date, no studies have compared groups of animals that were owned late in their life by caregivers diVering in their perceptual skills, primarily due to methodological issues (Bering 2004; Cooper et al. 2003). The present study is aimed to provide such data, with a focus on the eVect of “blind-socialisation” among dogs. Guide dogs present a unique opportunity to study such eVects on social-communicative behaviours in dogs: blind owners and guide dogs have extensive interaction during free time periods, and when synchronizing their actions with humans during navigation, dogs have the ability to interactively exchange roles with the human as the initiator of actions (Naderi et al. 2001). Moreover sighted and blind owners attend and respond to their dogs diVerently. As a consequence, the daily interactions between guide dogs and their blind owners could aVect the interspecies interactive modalities of guide dogs, in a diVerent fashion from that of pet dogs. To test for any apprenticeship of social-communicative cues, we adapted Miklósi et al.’s experiment (2003) and measured exploratory and interactive behaviours during the unsolvable test trial to get a broad overview of the dogs’ behavioural proWle. We expect that if a dog’s social cognition is attuned to the owner’s (non) visual status, then sound and contact should replace to some extent the function of staring at the owner to trigger his/her attention. Consequently, less gazing at the owner and more sound emissions and contacts in the guide dog group than in the pet dog group should be observed. Further, guide dogs should gaze less at the container where the unreachable food is, and engage in less-sequential gazing between their owners and the container, than pet dogs do. Methods Participants One group of nine pet dogs of sighted owners and one group of nine guide dogs of blind owners matched for breed, age (t16 = 0.45, P = 0.66) and duration of the dyads’ common life (t16 = ¡0.25, P = 0.81) were involved in the experiment (see Table 1 for the characteristics of the dogs). Guide dogs were raised in a sighted family before receiving their education between the ages of 6 and 18–24 months and were transferred to the ownership of blind persons when they were adults (1.83 years old on average). Five guide dogs were from the same school and four other guide dogs were from four other diVerent schools. On average, pet dogs spent 2 h per day interacting with their owner 477 Table 1 Characteristics of the dogs (ages are in years) Dog breed Sex Age Number of years living together (owner and dog) Guide dog Gold. £ Lab. F 10 8 Golden F 3 1 Labrador F 3 1 Labrador F 12 10 Labrador M 5 3.5 Labrador M 10 8.5 Labrador F 5 3.5 Australian shepherd M 7 5.5 Howavart F 5.5 3 Gold. £ Lab. F 7.5 7.1 Golden M 7 2 Labrador F 2.5 2.25 Labrador M 8 7.75 Labrador M 5.5 5.33 Labrador F 7 5.5 Labrador M 4 3.6 Pet dogs Lab. £ shepherd M 7 6.5 Golden M 7 6.8 (e.g., play, educational games, obedience training, etc.), in addition to morning, night and weekend walks and play. Dog were not fed 4 h before the experiment. Owners received a gratiWcation of 12 Euros for their participation. Experimental settings The dogs were tested in a large novel experimental room in which the experimental area (3.88 m £ 2.70 m) was deWned (Fig. 1). For future analysis, the whole experiment was videotaped by two cameras. Two identical 30-cm high plastic containers (30 cm in diameter) with two identical lids covering the containers were used, as well as 17 pieces of dry dog-food per dog. One of the two lids could be physically locked onto one of the containers by an invisible fastener, and a piece of food was hidden in this container just before the training phase (cf. below). Procedure Before starting the experiment, the dogs were allowed to explore the experimental room and area, including the two lid-covered containers. The experimenter and owner discussed and agreed upon the verbal instruction that owners would use to ask their dog to retrieve the food. The owners were told to stand up during the experiment, and that during 123 478 Anim Cogn (2008) 11:475–483 (C1, C2, C3; C for “covered”). The experimenter then hid behind the high fence (Fig. 1), asked the owner to remove the piece of cloth from the dog’s eyes and to give the instruction. The dog was allowed to go and open the container on its own. 80 cm high fence Cont ainer Experimental phase Cont ainer 1.40 cm h ig h w a l l ner Dog O(Dw oorma t) Ro om Ex pe r im en ta la re a 80 cm high fence Experimenter The diVerence between the last six trials and the Wnal one (with the lid secured on the container, i.e. namely the locked-container test trial) was that while the dog was blindfolded, the experimenter exchanged the openable container with the locked one (hidden behind the 80 cm high fence), and that the duration of the trial was 2 min and not 1.5 min. The duration between the moment when the dog was blindfolded and when it was unmasked was held consistent throughout the 17 trials. At the end of each trial, the dog returned to sit or stand close to its owner. 80 cm high fence 1.60 cm high fence Fig. 1 Experimental arrangement Data collection Learning and motivation behaviours (1) the Wrst ten identical trials, the experimenter would lift the lid so that the dog could go and get the food, (2) the next six trials lasting 1.5 min, the dog would have to lift the lid by itself and (3) the last trial (2 min) involving the lid secured to the container, the dog would try to remove the lid by itself. The owners were asked not to move and interact with their dogs and to look ahead after giving the instruction, especially during the last seven trials. They were subjected to one or two training trials without their dog to ensure they understood the task. The dogs were unleashed. Each of the 17 trials was started by asking the dog to sit close to or to stand by its owner; the owner then covered its eyes with a piece of cloth. Training phase For the Wrst ten trials, out of the dog’s view, the experimenter silently put one piece of food in the container, put the lid on the top of the container and asked the owner to remove the piece of cloth from the dog’s eyes. The owner gave the instruction and the experimenter immediately removed the lid after the dog had looked at her; the dog was allowed to go and eat the food. Next, during the following six trials, the experimenter stopped demonstrating the opening action: the food was hidden while the dog was blindfolded; for the Wrst three trials the container was half covered (HC1, HC2, HC3; HC for “half covered”) and for the last three trials the container was fully covered 123 In order to assess any diVerence in the speed of learning between the two groups of dogs during the block of six learning trials (2 £ 3 trials), we measured: • the latency to get the piece of food, which is the time elapsed between the instruction given by the owner to the dog and the time when the dog had the piece of food in its mouth. For the 2-min locked-container test trial, two variables were measured to ensure that both groups were equally motivated to solve the task on their own, and two others ensured equal food motivation: • the latency to get to the container, which is the duration between the owner’s instruction and the moment the dog touched the edge of the lid with its nose to lift it. • the number of attempts to lift the lid during the stays at the container. • the number of occurrences and duration of the dog staying at the container with its head bowed towards the container (a few cm) and sniVing it, or when it attempted to lift the lid. Behavioural observations during the 2-min locked-container test trial The number and duration of occurrences of the following behaviours were measured and submitted to inter-group analyses. Anim Cogn (2008) 11:475–483 • Exploratory behaviour: this behaviour refers to any activity directed towards non-movable aspects of the environment, including gazing at the ground with or without sniVing, distal visual inspection (staring or scanning), and close visual or oral examination and looking towards the non-visible experimenter. The number of occurrences and duration of the following interactive behaviours were measured: • GazeOwner: the dog’s head/nose was oriented towards the owner’s head. • Vocalisations: the dog barked and/or whined. • Contact: the dog pawed the owner, or touched him/her with its nose or head or performed any form of bodily contact. • MouthLickingS: a noisy mouth-licking behaviour was performed by the dog. • MouthLickingNS: a silent mouth-licking behaviour was displayed by the dog. Combinations of some of the interactive behaviours were also observed and recorded: GazeOwner + Vocalisation, GazeOwner + MouthLickingS and GazeOwner + Contact. Gazing at the container (GazeContainer) and gazing at the container with sonorous mouth licking (GazeContainer + MouthLickingS) were also observed and recorded. The sum of the durations of all 11 behaviours plus the latency to get to the container and the duration of stay at the container is 2 min for each dog. Finally, the number of gazes at the owner followed directly by a gaze at the container within 2 s, or vice versa was recorded in both groups (GazeAlternation). Two trained observers recorded the occurrences of behaviours independently (one of them was naive with respect to the aim of the experiment). In a few occurrences (totalling 22 s out of the 120 s £ 18 dyads), the owner did not follow the instruction to look ahead; the corresponding dog’s behaviours were taken as exploratory behaviour. Before data analyses, we assessed inter-observer agreements for the most frequent behaviours by means of parallel coding of 100% of the sample of durations. We calculated Kappa coeYcients (Martin and Bateson 1986) for durations and found relatively high values for Exploration: 0.81, GazeOwner: 0.83, Contact: 0.89, MouthLickingS: 0.85, GazeContainer: 1.00 and staying at the container: 0.86. We Wnally examined inter-group diVerences for the latency for gazing at the owner and latency for the Wrst interactive behaviour to be displayed (Wrst gaze at owner, contact, vocalisation, sonorous mouth licking or combination of these behaviours). 479 Results Learning and motivation behaviours Non-parametric statistics were applied to the latencies to get the piece of food (see Table 2 for medians). Mann– Whitney tests did not reveal a group eVect for any of the trials (HC1: U = 27, P = 0.23; HC2: U = 38.5, P = 0.85; HC3: U = 21, P = 0.08; C1: U = 36.5, P = 0.72; C2: U = 23.5, P = 0.13; C3: U = 32.5, P = 0.47), with N guide dogs = N pet dogs = 9. For each of the six trials, groups have thus been pooled for the next analysis. Wilcoxon matched pairs signed ranks tests revealed that the latencies for HC1&C1 pooled and HC2&C2 pooled did not diVer (n = 17, T = 47.50, P = 0.16), nor did they diVer for HC2&C2 pooled and HC3&C3 pooled (n = 16, T = 49.0, P = 0.32); however, the diVerence of latencies for HC1&C1 pooled and HC3&C3 pooled was signiWcant, with HC1&C1 being longer than HC3&C3 (n = 16, T = 30.50, P = 0.05) (see the medians on the second part of Table 2). Group comparisons for the four variables recorded during the 2-min locked-container test trial as an indication for learning and motivation behaviours were carried out using Mann–Whitney U tests, with N guide dogs = N pet dogs = 9. The groups did not diVer for the latency to get to the container (median = 1 for both groups; U = 40.50, P = 0.99), for the number of attempts to lift the lid (median = 3 for both groups; U = 34.00, P = 0.56), for the number of occurrences of the dog staying at the container (median = 2 for the guide dogs; median = 3 for the pet dogs; U = 32.00, P = 0.45) and for the duration of the dog staying at the container (median = 16 for the guide dogs; median = 24 for the pet dogs; U = 20.50, P = 0.08). These results show that the learning process does not diVer between the groups of dogs and that the dogs were equally motivated, both for attempting to solve the task on their own, and for food in general. Table 2 Medians of the latencies for getting the food according to the dogs and trials First set of trials Second set of trials HC1 HC2 HC3 C1 C2 C3 Guide dogs 3 3 2 5 5 4 Pet dogs 2 3 2 5 3 5 Two groups pooled 3 3 2 5 4.5 4.5 Two groups pooled HC1&C1 HC2&C2 HC3&C3 10 8 7.5 123 480 Anim Cogn (2008) 11:475–483 Behavioural observations during the 2-min locked-container test trial The guide dogs and the pet dogs explored the experimental area for 61.29 and 61.57% of the time, respectively. The number and duration of exploratory behaviours did not diVer between the guide dogs (median = 20 for number; median = 79 for duration) and the pet dogs (median = 19 for number; median = 72 for duration); see Table 3 for the results of the Mann–Whitney analyses. This test revealed that the guide dogs exhibited more and longer instances of MouthLickingS (median = 3 for both variables) than the pet dogs (median = 0 for both variables). The number and duration of GazeOwner, Vocalisation, Contact, MouthLickingNS, GazeOwner + Vocalisation, GazeOwner + MouthLickingS and GazeOwner + Contact did not diVer between the groups (Table 3; Fig. 2). Table 3 also shows that the groups did not diVer in terms of the number and duration of GazeContainer and GazeContainer + MouthLickingS: the median of GazeContainer equals one for the guide dogs and the three other medians equal two; for GazeContainer + MouthLickingS, the median equals zero for both variables of both groups. Further, the number of GazeAlternation did not diVer between the guide and pet dogs (median = 0 for both variables). Finally, it was found that the latency to gaze at the owner did not signiWcantly diVer between the guide dogs (median = 15) and the pet dogs (median = 29) (U = 15, P = 0.13); two guide dogs and one pet dog did not look at their owner at all. The latency for the Wrst interactive behaviour (gaze at the owner, contact, vocalisation, sonorous mouth licking or combination of these behaviours) did not diVer between the guide dogs (median = 15) and the pet Table 3 Mann–Whitney tests results for between-group analyses, with N guide dogs = N pet dogs = 9 123 dogs (median = 27.5) (U = 25, P = 0.28). Among the guide dogs, the Wrst interactive behaviour was to look at the owner (for seven dogs) and to touch the owner (for two dogs); among the pet dogs, six pet dogs looked at their owner Wrst, one touched its owner Wrst, one vocalized Wrst, and one did not gaze, touch, vocalize, mouth lick with sound, or combine the two modalities at all. Discussion The aim of this study was to determine whether the behaviour of dogs, and more speciWcally the modalities of interaction of dogs, is attuned to the visual status of their owners. We addressed this issue by comparing guide dogs and pet dogs prevented from accessing food that they had previously learned to access. Learning and motivational behaviours did not diVer between the groups and both groups explored the experimental area in a similar fashion. These results conWrm that in a situation similar to a context commonly experienced by dogs, working dogs such as guide dogs display an exploratory repertoire with learning and motivational behaviours that are similar to those of pet dogs. Further, none of the main interactive behaviours (gazing at the owner, vocalisations, contact with the owner and any combination of these behaviours), and neither the gaze at the container nor alternate gaze, diVered between groups. However, a new audible behaviour was observed, namely sonorous mouth licks. These were signiWcantly greater in number and duration in the guide dog group than in the pet dog group. Cognitive innovations devised by animals in the wild or in the human environment are indeed numerous (Lestel 2004; Tomasello 2004; Bates and Byrne 2007). But how may the behavioural pattern of the two groups be inter- DiVerences between the guide and pet dogs Duration Number U P U P Exploratory behaviour 37.00 0.75 37.50 0.79 GazeOwner 38.50 0.86 37.50 0.78 Vocalisation 36.00 0.32 36.00 0.32 Contact 24.00 0.08 24.00 0.08 MouthLickingS 13.00 0.009 14.00 0.012 MouthLickingNS 38.50 0.83 40.00 0.95 GazeOwner + Vocalisation 40.00 0.93 40.50 0.99 GazeOwner + MouthLickingS 31.50 0.14 31.50 0.14 GazeOwner + Contact 40.00 0.95 40.00 0.95 GazeContainer 39.00 0.89 40.00 0.96 GazeContainer + MouthLickingS 31.50 0.42 31.50 0.42 GazeAlternation – – 31.00 0.40 Anim Cogn (2008) 11:475–483 (a) 481 11 Guide dogs Pet dogs 10 Number of behaviors 9 8 7 6 ** 5 4 3 2 1 0 t ner tion ontac kingS ingNS ation kingS ntact o Ow alisa c k lis C Lic c h Lic Voca hLi ner+C t o u V uth out Mo Mo wner+ erM+ zeOw Ga wn zeO Ga GazeO ze Ga Duration of behaviors (sec.) (b) 70 65 60 55 50 45 40 35 30 25 20 15 10 5 0 Guide dogs Pet dogs * t t ner tion ontac kingS ingNS sation kingS ontac Ow alisa li c r+C k ic C i e a c L i L z c c h L o ut Ga uth ne Vo uth +V Mo Mo Ow Mo wner er+ Gaze n O e w z Ga zeO Ga Fig. 2 The behavioural proWle of the dogs. a Number of behaviours for the guide dogs and the pet dogs. b Duration of the interactive behaviours for the guide dogs and the pet dogs. Non-parametric data are represented as medians, and the box indicates the interquartile range of 50% of the data. Whiskers extend to the smallest and largest values and exclude outliers preted, and what is the meaning of the sonorous mouth licks? At the outset, it is striking that gazing at the owner was by far the most common interactive behaviour displayed in both groups, and that this behaviour did not diVer between groups. This conWrms that gazing at the owner is a key factor in dogs’ social cognition when interacting with humans (Miklósi et al. 2000, 2003), especially when seeking help from the owner (Cooper et al. 2003; Hare 2004). This is further supported by the Wnding that the latency to gaze at the owner (i.e. the Wrst gaze) did not diVer between groups, and that the Wrst interactive modality was gazing at the owner for the vast majority of the dogs in both groups. Second, the display of an increased number and duration of sonorous mouth licks in the guide dog group may not be as unexpected as it initially sounds, for several reasons. First, the present task concerns food retrieval with the owner present, which itself triggers mouth licking in dogs (Miklósi et al. 2000). Second, touching the blind owner would be too far from the referential object and the ears replace the eyes in blind individuals for attending to space and events (for a review of perceptual abilities of blind individuals, see the introductory section of Gaunet and BriVault 2005). Finally, guide dogs are taught neither to beg and bark, nor to beg and whine. The only directly available clue to tackle the meaning of audible mouth licks and to interpret the diVerence between the two groups is given by Miklósi et al. (2000). The authors found that both mouth licking and sniVing behaviours signiWcantly increased when the dogs knew the location of a hidden and inaccessible piece of food and when the owner—naive of that location—was present with the dog. Since these authors did not observe these behaviours when the dog was left alone with the hidden food, the emergence of these behaviours were attributed to the joint presence of the owner and food, and might indicate increased levels of motivation because dogs associate the arrival of the human with the retrieval of food (Miklósi et al. 2000). There are indeed many opportunities for learning such signals as operant. For instance, noticing changes in the dog’s behaviour, the owners may suppose that the dog might be hungry, and “reward” this behaviour by providing food, or they may respond to the directional gazing by dogs what would cause dogs to conventionalize their gazing as a communicative exchange aimed at desired objects (Miklósi et al. 2000). Both mouth licking—including a fortiori sonorous mouth licking—and staring at the owner may thus be signals that draw the owner’s attention towards the dog and/or a target (Fox 1971; Bradshaw and Nott 1995). These signals may be a fortiori operant when both the owner and the dog know that there is an inaccessible piece of food in the room, though these signals do not provide a spatial reference to the target. These behaviours may, however, be motivational signals per se, or signals aimed at triggering the owner’s attention to a “desired” target. Overall, because the groups did not diVer in terms of gazing at the owner or gaze alternation, sonorous mouth licking simply supplemented such behaviours rather than replacing them, perhaps with the goal of capturing the owner’s attention or to display motivation and/or interest. Sonorous mouth licks would then be an addition, which could be learned as a useful action to get help from the owner. The fact that seven of nine guide dogs exhibited sonorous mouth licks while only two pet dogs did, is never- 123 482 theless an argument that guide dogs may develop special signals as a result of their owners’ diVerent attentional state. Guide dogs may thus have supplemented a reduced reaction of their owners to the visual signals they emit with a new distal cue (or the greater number and the longer duration of contacts with the owner—a proximal cue—in guide dogs would have signiWcantly diVered from that of the pet dogs). It might thus be that because blind owners cannot see the dog trying to trigger his/her attention (e.g. by using the distal cue of staring) or see changes in the dog’s motivation, dogs have incidentally developed an alternative tactic and learned to use a new sound for triggering their owners’ attention from a distal location. Analysing whether this behaviour would emerge when the target is inaccessible and the owner is absent would tell whether this behaviour is intentional. Finally, because guide dogs were just as likely to gaze at the owner, to gaze at the container and to exhibit gaze alternation as were the pet dogs, guide dogs were not actually sensitive to the fact that their owners were not responding to their gaze signals. The results thus suggest that guide dogs did not understand their owner’s diVerent attentional state (i.e. that their owners could not recognize the visual signals dogs emit); if the dogs understood this, presumably the guide dogs would have used MouthLickingS in place of visual signals to gain their owner’s attention. Overall, and in other words, the guide dogs did not detect that their owners could not see (them), but dogs have modiWed their interactive behaviours slightly, to adjust to their owners. Further, the behavioural proWles of the dogs (Fig. 2) happened to superimpose fairly well in terms of the number and duration of the interactive behaviours, for each group. This shows that a constant duration of social-communicative behaviours is associated with the occurrence of each behaviour, and further suggests that the behavioural modalities displayed when interacting with humans—once triggered—is regular in duration among the behaviours. Taken together, the results suggest that the guide dogs’ behaviour is not attuned to the non-visual status of their owner, but that sonorous mouth licking may supplement staring at the owner to get the owner’s attention. The development of another attention-getting behaviour through experience and the persistence of a generalized form of gazing behaviour can be explained by a combination of reasons: Wrst, guide dogs grew up among sighted families and still live surrounded by sighted people, and second, they have an extensive experience of living with their blind owners during their adulthood and are fed only by their owner. The abilities of Philip, a 3-year-old male dog, who was able to adjust his communicative behaviour to his disabled human partner to solve a cooperative problem-solving task (Topál et al. 2006), may also be the result of Philip’s extensive experience with attending to his owner 123 Anim Cogn (2008) 11:475–483 and of the cognitive innovations that he has to perform regularly. Further, the development of another attention-getting behaviour through experience can also be explained by the cooperative features of human–dog relationships and the type of attachment of dogs to humans (Topál et al. 1998; Naderi et al. 2001, 2002; Kerepesi et al. 2005), and by the sophisticated social-cognitive skills dogs posses (see Hare and Tomasello 2005; Miklósi and Soproni 2006). It must be emphasized that this is the Wrst study comparing social-communicative skills of groups of animals that are owned late in their life by caregivers diVering in their perceptual skills. This study is thus the Wrst evidence of incidental learning in the adult dogs’ social-communicative skills in an interspecies context, and the present evidence of behavioural plasticity converges with Pongrácz-Rossi and Ades’s (2008) study showing that an adult dog can learn to use arbitrary signs to communicate requests to its owner. To conclude, at this point, sonorous mouth licking may be a motivational signal or a signal intended to trigger the owner’s attention to a target (i.e. a communicative signal). However, recent studies on vocalisations produced by dogs and on the categorization by humans of these productions have started to provide insights into the characteristics and meanings of sound production in dogs. Yin and McCowan (2004) analysed barking spectrograms in three diVerent contexts. A discriminant analysis revealed that dog barks are divided into diVerent subtypes based on context. Moreover, in another study, people were asked to describe the emotional content of several artiWcially assembled bark sequences on the basis of Wve emotional states (aggressiveness, fear, despair, playfulness, happiness) (Pongrácz et al. 2007). The scoring of the emotional content of the bark sequences was in accordance with the so-called Morton’s structural–acoustic rules (e.g. low-pitched and atonal vocalisations signal aggressive intentions, in contrast to highpitched and tonal vocalisations signalling friendly/submissive intentions), suggesting that dog barks may present a functional system for communication (see also Molnar et al. 2008). Studying the perception of sonorous mouth licking by blind owners and the spontaneous reaction of blind owners to such sound may thus allow to clarify the role of this behaviour in the context of human–dog interaction. Acknowledgments This work was supported by Centre National de la Recherche ScientiWque and conducted at the “Laboratoire Eco-Anthropologie et Ethnobiologie”, Muséum National d’Histoire Naturelle, Paris, France. The experiments comply with the current laws in France for animal and human research. Author thanks the guide and pet dogowner dyads for their interest and cooperation. Author is especially grateful to B. Sauzeau and S. Reis for their contribution in the design of the experiment and their help in determining behaviours to be collected, and to D. Sulinski for her contribution in the analysis of the videos. The author is also grateful to I. Guaitella for her comments on a previous version of the manuscript and to J. Philbeck for his feed-backs and corrections on the manuscript. Anim Cogn (2008) 11:475–483 References Agnetta B, Hare B, Tomasello M (2000) Cues to food locations that domestic dogs (Canis familiaris) of diVerent ages do and do not use. 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