Gazing toward humans: A study on water rescue dogs using the impossible task paradigm

Publishing Authors : Biagio D’Anielloa,∗, Anna Scandurra b, Emanuela Prato-Previdec, Paola Valsecchi d

a Department of Biology, University of Naples Federico II, via Cinthia, 80126 Italy
b Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, Second University of Naples, via Vivaldi, 81100 Caserta, Italy
c Department of Pathophysiology and Transplantation (DEPT), University of Milan, Via F.lli Cervi 93, 20090 Segrate (MI), Italy
d Department of Neuroscience, University of Parma, viale Usberti 11 A, 43125 Parma, Italy

Date Published : 13/09/2014

 

a b s t r a c t
Various studies have assessed the role of life experiences, including learning opportunities, living conditions
and the quality of dog-human relationships, in the use of human cues and problem-solving ability.
The current study investigates how and to what extenttraining affects the behaviour of dogs and the communication
of dogs with humans by comparing dogs trained for a water rescue service and untrained pet
dogs in the impossible task paradigm. Twenty-three certified water rescue dogs (the water rescue group)
and 17 dogs with no training experience (the untrained group) were tested using a modified version
of the impossible task described by Marshall-Pescini et al. in 2009. The results demonstrated that the
water rescue dogs directed their first gaze significantly more often towards the owner and spent more
time gazing toward two people compared to the untrained pet dogs. There was no difference between
the dogs of the two groups as far as in the amount of time spent gazing at the owner or the stranger;
neither in the interaction with the apparatus attempting to obtain food. The specific training regime,
aimed at promoting cooperation during the performance of water rescue, could account for the longer
gazing behaviour shown toward people by the water rescue dogs and the priority of gazing toward the
owner.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
In recent years, evidence has accumulated indicating that dogs
are particularly skilful in comprehending and using different types
of human communicative signals, such as gazing, nodding and
pointing (Agnetta et al., 2000; Hare and Tomasello, 2005; Hare
et al., 2002; Miklósi and Soproni, 2006; Reid, 2009; Soproni et al.,
2001), but also actively and effectively communicate with humans
through a variety of visual and auditory signals (Gaunet, 2010,
2008; Gaunet and Deputte, 2011; Kaminski et al., 2011; MarshallPescini
et al., 2012, 2009; Miklósi et al., 2003, 2000). Such findings
have stimulated an active debate concerning how these abilities
of dogs have evolved. Based upon studies showing that wolves
are more skilled than dogs in using human communicative cues
in a food retrieval task (Udell et al., 2008), it was suggested that
differences among canid species in their social skills are largely
due to environmental factors (Wynne et al., 2008). Particularly, a
“Two Stage Hypothesis” has been proposed, which states that the
∗ Corresponding author. Tel.: +39 081 679177; fax: +39 081 679233.
E-mail address: biagio.daniello@unina.it (B. D’Aniello).
sensitivity of canids to human social cues depends on the interaction
with humans during a sensitive developmental period, and
that learning is not restricted to a particular phase of development
(Udell and Wynne, 2010, 2008; Udell et al., 2010a; Wynne et al.,
2008). Some authors, however, have underlined the importance of
the domestication process attributing the domestic dog’s sensitivity
to human social cues to an human-like social cognition selected
during domestication, considering such dog abilities neither simply
inherited from wolves nor the result of ontogeny (Hare and
Tomasello, 2005; Hare et al., 2010, 2002). Within an approach to
socio-cognitive skills in dogs, which demonstrate the importance
of selection (natural and artificial) and individual ontogenetic experiences
(Miklósi and Topál, 2013; Udell et al., 2010b), a number of
studies have assessed the role of learning, living conditions and the
quality of the dog–human relationship in shaping the behaviour
of dogs in different contexts, such as problem-solving tasks (e.g.,
Barrera et al., 2011; Bentosela et al., 2009, 2008; Cunningham and
Ramos, 2013; Horn et al., 2013; Marshall-Pescini et al., 2009, 2008;
Passalacqua et al., 2013; Range et al., 2009; Topál et al., 1997).
Studies have evaluated the effect of intensive training on
communicative skills and problem-solving abilities. It has been
reported that highly trained dogs are more proficient in using
http://dx.doi.org/10.1016/j.beproc.2014.09.022
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Please cite this article in press as: D’Aniello, B., et al., Gazing toward humans: A study on water rescue dogs using the impossible task
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human cues than untrained dogs (McKinley and Sambrook, 2000;
Range et al., 2009); however, Cunningham and Ramos (2013)
obtained no evidence that intensive training improved performance
on a cue-following task.
The effect oftraining on the behaviour of dogs has been reported
by Marshall-Pescini et al. (2008), who compared trained and
untrained pet dogs in a problem-solving task, in which a food-box
could be accessed by pressing a paw-pad or opening the lid with
themuzzle. The results indicatedthattraineddogs (i.e.,dogs trained
for agility, search and rescue, schutzhund, freestyle, and gun-dog
working trials) had a lower tendency to look at the owner during
the problem-solving task; the trained dogs interacted more with
the apparatus to solve the problem independently and were more
successful in accessing the box than were the untrained dogs;there
was no direct relationship between the dogs’ training experience
and the task presented in the study (see also Osthaus et al., 2003).
Dogs trained for different social uses appeared to be less prone than
untrained dogs to follow their owners’ misleading indications in a
food choice task (Prato-Previde et al., 2008), suggesting that training
experiences might reduce dependency on the owner, thereby
favouring more independent decision-making. These results are
in contrast with a previous paper which reported that obedience
training (i.e. dogs had a certificate of official obedience training)
does not influence the behaviour of the dogs in problem solving;
whereas, dogs kept with less direct contact with humans behaved
more independently in a problem-solving task (Topál et al., 1997).
A small number of studies have investigated the potential influence
ofthe training of dogs on the manifestation of human-directed
gazing behaviour. Bentosela et al. (2008) showed that learning
and reinforcement contingencies play an important role in shaping
looking behaviour in dogs, reporting that schutzhund trained
dogs, who are specifically reinforced to gaze at the face of the handler
while they walk, look at their owner/trainer significantly more
than do untrained dogs during a short walk.
Marshall-Pescini et al. (2009) compared untrained dogs and
dogs trained in two substantially different activities (i.e., agility
and search and rescue training) using an impossible task paradigm
(Miklósi et al., 2003), in which an initially accessible apparatus containing
food becomes impossible to access. It emerged that the
untrained and trained dogs were comparable in interacting with
the apparatus, whereas they differed in their human-directed gazing
behaviour, with agility-trained dogs gazing longer at humans
than did the search-and-rescue and untrained dogs. In another
impossible task study, guide dogs for visually impaired people, as
well as search-and-rescue dogs (Marshall-Pescini et al., 2009), did
not differ in gazing behaviour from the untrained group (Gaunet,
2008). Apparently, the type of experiences that agility dogs had
during the training process affected their gazing behaviour.
Water rescue dogs are interesting subjects for studying the
potential effects oftraining on the social-communicative behaviour
of dogs because they undergo intense training to optimise their
cooperation with humans. The aim of the Italian water rescue
school is to form dog-human dyads specialised in rescuing drowning
people, and upon completion of training and a successful
final examination, dog–human dyads are qualified as water rescue
teams (obtaining a Water Rescue Certificate®). Each member
of the dyad plays a specific role while rescuing people: the owner
is responsible for calming and grasping the drowning person and
then supporting and preparing him/her for the journey back; the
dog tows both people to safety (to shore or to an emergency boat).
Water rescue training implies the formation of strong, long-lasting
cooperation and synchronisation between dogs and handlers. An
important component of both training stages involves focusing the
dog’s attention on unknown people who scream for help and wave
their arms, simulating people in distress (during land obedience
stage) and simulating drowning (during water stage). Dogs must
also be highly attentive to their handler/owner and ready to obtain
information from him/her;they are strongly rewarded for carefully
looking at the handler during the obedience exercises. Therefore,
a successful training program will produce water rescue dogs that
not only are strongly bonded with their owner, with whom they
work in a cooperative manner, but that also have strong positive
attitudes towards strangers, without being scared of or aggressive
towards them. All of the dogs live with their handlers/owners as
pets.
Water rescue involves a social use of dogs and developed in Italy
more than 20 years ago, although only recently it became object of
scientific inquiries (Merola et al., 2013). Testing trained dogs in different
experimental contexts allows a better comprehension of the
actual behavioural outcomes of training methods. This can be usefulto
understand whether the objectives ofthe training are actually
achieved, and possibly to improve the efficiency of the training
method and prepare better dogs for this social service. Thus, in
this study, we explored the effect of training on the socio-cognitive
abilities of dogs by testing water rescue dogs in a well-established
testing protocol, the impossible task paradigm, and subsequently
comparing their performance with that of a group of untrained pet
dogs tested as the control.
First of all, we assessed whether water rescue dogs due to their
training, showed an increased use of gazing compared to pet dogs.
Since some studies suggest that dogs show preferential attention
and gazing toward their owner compared to an unfamiliar experimenter
(Miklósi et al., 2005; Mongillo et al., 2010), a second goal
of this study was to evaluate whether water rescue training would
determine a greater tendency of dogs to gaze toward their reference
figure (the owner), rather than toward a stranger when facing
an unsolvable task. Recently, it has been demonstrated that dogs
direct their attention significantly more to a familiar human than
to a stranger only when the familiar person has a close relationship
with them, based on joint activities and frequent feeding (Horn
et al., 2013), as is the case of a water rescue team. However, water
rescue dogs during their training,through a positive reinforcement,
are strongly focused on a stranger, who might have acquired gazerelated
relevance.
Finally, we investigated whether water rescue training makes
dogs more proactive in trying to solve the task. Despite the evidence
that trained dogs in a problem task might be more independent
and proactive compared with untrained pet dogs (Marshall-Pescini
et al., 2008; Prato-Previde et al., 2008), a recent study on water
rescue dogs indicated that in an unexpected situation perceived as
unfamiliar and potentially ‘dangerous’, these dogs depend on their
owners’ instructions more than do pet dogs (Merola et al., 2013);
thus, we not expect that these dogs would be more proactive than
untrained dogs in attempting to obtain
Please cite this article in press as: D’Aniello, B., et al., Gazing toward humans: A study on water rescue dogs using the impossible task
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Fig. 1. Experimental room, with the handler (left) and a stranger (right) during the
insolvable task trial. The dog is gazing at its handler. The insert shows the experimental
apparatus. The box was open (left) during the insolvable task trial and locked
(right) during the impossible task phases.
The untrained group included 17 subjects (eight females and
nine males; mean age = 6.0 ± 3.1 years; 14 Labrador Retrievers and
3 Golden Retrievers), kept for companionship and thus with no formal
training implying reinforcement for gazing at humans. These
dogs lived in the human households at the time of testing.
2.2. Apparatus and procedure
The apparatus consisted of a glass food container
(10.5 × 10.5 cm), placed on a rectangular wooden platform
(77 × 34.5 cm), comparable to the apparatus used by MarshallPescini
et al. (2009) and Passalacqua et al. (2013, 2011). The lid was
fixed on the platform, whereas the container was placed upside
down on the tracks of the lid during the solvable task trials and
was locked during the unsolvable task trial (Fig. 1, insert). The
wooden platform was fixed to the floor by double-sided adhesive
tape. After each test, the apparatus and the container were washed
with a slightly perfumed and non-toxic disinfectant. The tests
were conducted at the University of Naples “Federico II” (Naples)
and at the training centre of the Italian School of Water Rescue
Dogs (Velletri, Rome) in rooms ranging in size from 12 to 16 m2.
Both rooms were unfamiliar and novel to dogs.
The owners were asked not to feed their dogs during the four
hours prior to testing to enhance the interest of the dogs toward
the food used as bait during the test. The food palatability of the
dogs was ascertained by administering small bits of food to them
before the test.
The test consisted of three ‘solvable’ trials in which the dogs
could obtain the food by manipulating the container followed
by an ‘unsolvable’ trial, in which the container was fixed onto
the wooden board. In all the trials, the owner and an unfamiliar
researcher (hereinafter referred to as the stranger) were present
and maintained the identical position standing at either side of
and one step back (30 cm) from the wooden board on which the
container was placed. During the entire test period, these humans
looked straight ahead and ignored the dog (e.g., neither spoke,
looked at or touched the dog; Fig. 1). Two different researchers
handled each dog in the following manner during the testing:
one researcher held the dog and the other placed the food below
the glass container during solvable trials, ensuring that the dog
observed the procedure and blocked the apparatus in the unsolvable
trial; then, both researchers left the room. During all the trials,
the stranger and the owner had no contact with the dog or with
the food/food container. The duration of the unsolvable trial was
60 s.
No specific permission for the use of animals (dogs) in this
type of behaviour study is required in Italy; however, an in-depth
description ofthe test was presented by the researcher and consensus
was sought prior to testing. The relevant ethical committee is
the Ethical Committee for Animal Experimental Procedures (CESA)
of the University of Naples “Federico II”.
2.3. Data analysis
The entire experimental procedure was recorded using two
video cameras (Sony Handycam HDR-CX115 and HDR-PJ260VE)
positioned at two adjacent corners of the rooms.
The goal of this study was to assess the potential effect of training
experience on the behaviour of gazing towards humans and on
problem-solving strategies in an unsolvable task, and we focused
our attention on the following mutually exclusive behaviours: (1)
gazing at the stranger or at the owner: the dog does not approach
the unfamiliar person/owner, however, the dog turns/lifts its head
towards the stranger or the owner faces. According to Smith and
Litchfield (2013) all gazing recorded in this paper has been considered
task-directed (i.e. they followed or preceded a direct action
on the apparatus); (2) direct interaction with the container: any
behaviour aimed at obtaining the food, e.g., grasping, scratching,
nosing, biting and pushing the experimental apparatus. A random
selection of trials (25%) was coded by a second observer and the
interobserver reliability on the duration of the behaviours was calculated
using Cronbach’s alpha (gazing at the stranger: ˛= 0.95;
gazing at the owner: ˛= 0.98; interaction with the food container:
˛= 0.98). To test whether the dogs, as a group, directed their first
gaze significantly more often towards the owner once the task was
made unsolvable we used a two-tailed binomial test with a test
value of 0.5; we used the Wilcoxon test to determine whether
there was a difference in the time spent gazing at the owner vs. the
stranger within each group. Next, to test whether the water rescue
dogs would gaze at people for longer than the untrained dogs or
would be more independent than the untrained dogs, as shown by
interacting with the apparatus longer and trying to obtain the food
reward, we used a Mann-Whitney U test to compare the duration
of gazing at people (the owner plus stranger) and of interaction
with the apparatus between the two groups. The alpha was set at
0.05. All of the statistical analyses were conducted only for the data
collected in the unsolvable trial and were implemented in SPSS 21
software.
3. Results
All of the dogs in the study exhibited notably high motivation to
approach the apparatus and obtain the food, and they succeeded in
obtaining the food reward at least two times in the solvable trials
and were thus exposed to the unsolvable trial. The following results
concern only the unsolvable trial.
3.1. Owner vs. stranger: preference in gazing
Two dogs ofthe water rescue group and one dog ofthe untrained
group did not gaze at people during the unsolvable trial and were
excluded from this analysis. Of the remaining 37 subjects, 15 of the
21 water rescue dogs (71%) gazed at their owner first and then at
the stranger during the test (binomial test: p = 0.02), whereas only
seven of the 16 dogs of the untrained group (44%) did so (binomial
test: p = 0.17; Fig. 2A). The comparison of the amount of time
spent gazing at the owner vs the stranger did not reveal any significant
differences by neither in water rescue nor in untrained
dogs (Wilcoxon test: water rescue: z = −0.57, p = 0.57; untrained:
z = −0.56, p = 0.57; Fig. 2B).
Please cite this article in press as: D’Aniello, B., et al., Gazing toward humans: A study on water rescue dogs using the impossible task
paradigm. Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.09.022
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Fig. 2. A. Gazing towards the owner by the dog in the unsolvable trial; 71% of the
water rescue dogs gazed at their owner first and then at the stranger (binomial
test: p = 0.02), whereas the untrained group was selected randomly (binomial test:
p = 0.17). B. The duration of gazing towards the owner or stranger in the unsolvable
task trial. No significant differences were found in the water rescue dogs or in the
untraineddogs.Wilcoxontest: water rescue: z = −0.57, p = 0.57;untrained: z = −0.56,
p = 0.57. Bold horizontal lines: medians; gray boxes: quartiles; thin vertical lines:
minimum and maximum values.
3.2. Water rescue vs. untrained dogs: gazing at people and acting
independently
During the unsolvable trial the water rescue dogs gazed at the
people (owner and stranger) standing near the apparatus significantly
longer than did the dogs of the untrained group (Mann
Whitney test: U = 79.5, z = −2.72, p = 0.007; Fig. 3A). All the dogs,
except for one in the untrained group, immediately interacted with
the food container, touching it with the muzzle or paw and trying
to open itto obtain the food reward. The latency to interact with the
apparatus was not analysed. No difference in the amount of time
spent interacting with the apparatus emerged between the dogs of
the two groups (Mann Whitney test: U = 166.5, z = −0.79, p = 0.43;
Fig. 3B).
4. Discussion
Various studies have investigated the use of gaze by dogs to
communicate with humans, demonstrating that gazing behaviour
is influenced by several factors, including learning opportunities,
training and living conditions (Prato-Previde and Marshall-Pescini,
2014 for a review).
In this study, dogs trained for water rescue and untrained pet
dogs were compared using an ‘unsolvable task paradigm’ suitable
for assessing independent problem-solving abilities and the
Fig. 3. A. The duration of gazing at people in the unsolvable task trial. The water
rescue dogs gazed at people significantly more than did the untrained dogs. Mann
Whitney test: U = 79.5, z = −2.72, p = 0.007. B. The duration ofthe interaction with the
experimental apparatus in the unsolvable task trial. No significant differences were
found between the water rescue dogs and the untrained dogs. Mann Whitney test:
U = 166.5, z = −0.79, p = 0.43. Bold horizontal lines: medians; gray boxes: quartiles;
thin vertical lines: minimum and maximum values.
propensity of dogs to seek human intervention (Marshall-Pescini
et al., 2009; Miklósi et al., 2003; Passalacqua et al., 2013, 2011).
Whereas water rescue dogs gazed at humans for significantly
longer periods than untrained dogs, there were no intragroup differences
in the duration of gazing towards the owner and the
stranger.In the water rescue group, a significantly higher number of
dogs looked attheir owners first and later atthe experimenter. Thus
it appears that the training aimed at focusing dogs’ attention on the
stranger had no effect in our experimental situation. The strong
partnership of the water rescue dog-human dyad could account for
the dogs’ priority in directing visual interest toward their owner.
Horn et al.(2013) recently demonstrated that dogs’ visual attention
toward a human partner is not affected by social familiarity per se;
it depends on the quality of the relationship, and dogs attend significantly
more to a familiar human from their household than to
an unfamiliar experimenter only when the familiar person has a
relationship with them, characterised by many joint activities and
Please cite this article in press as: D’Aniello, B., et al., Gazing toward humans: A study on water rescue dogs using the impossible task
paradigm. Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.09.022
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frequent feeding, which is the case with water rescue team. However,
despite the water rescue dogs’ first gaze was for their owners,
we did not observe differences between the two groups in the duration
of gazing at the owner vs a stranger in the unsolvable trial. This
finding could be observed because in the study, the stranger and
owner were instructed not to provide any cue to the dogs; thus,
after an initial preferential gaze at the owner, the stranger might
become comparable in salience for the dogs. However, we cannot
exclude that focusing on a stranger during water rescue training
reduced the differences with the control group. This result suggest
that water rescue dogs are differentfrom agility dogs, which in similar
experimental conditions clearly preferred their owner gazing
at him/her for significantly longer periods (Marshall-Pescini et al.,
2009).
Human-directedgazing aptitude appears to be affectedby learning
and can be shaped through positive reinforcement (Bentosela
et al., 2008; Protopopova et al., 2012) during a specific training
program (as in water rescue dog training); however, it could be
inadvertently promoted during everyday interactions with humans
(e.g., by giving attention, food, care or a toy when a dog engages
in human directed gazing). Water rescue and untrained dogs,
except for training, are exposed to comparable social contexts
and lifestyles, and they both grow up in families from puppyhood
and live in the household as pets, sharing daily activities
with humans. The water rescue dogs spent more time gazing
at people than did the untrained dogs, which suggests an effect
of training. It should be noted that in water rescue dogs gazing
behaviour is reinforced to increase dogs’ attention to the owner,
but not in the context of problem solving. Whether dogs were
gazing to seek for help in solving the task, as proposed in other
studies (Cooper et al., 2003; Marshall-Pescini et al., 2013, 2009;
Miklósi et al., 2003, 2000; Passalacqua et al., 2013, 2011) and/or
were waiting to receive commands and instruction, as they are
trained to do, is unclear, thereby warranting further investigation.
No difference emerged between the dogs in the two groups in
the problem-solving strategies, as well as in the duration of interaction
with the apparatus, confirming our prediction that water
rescue dogs are not more prone to act independently from their
owners than are untrained dogs, most likely because of the training
received (Merola et al., 2013). Even though our finding are in
agreement with the data of Topál (1997) showing no differences
in problem solving strategies between dogs with a certificate of
obedience training and pet dog, they are in contrast with some
other studies indicating that the training experience might affect
the performance of dogs, with trained dogs for social service and
sport being more independent and proactive problem-solvers (e.g.,
Marshall-Pescini et al., 2008; Prato-Previde et al., 2008). It seems
that different training methods can result in different behavioural
outcomes.
The results of this study provide further insight on the complex
factors influencing and modulating dog-human interspecific communication,
confirming that gazing behaviour in dogs is affected
by environmental and life experiences, as has been shown in
the literature (Barrera et al., 2011; Bentosela et al., 2009, 2008;
Marshall-Pescini et al., 2009; Passalacqua et al., 2011; Udell and
Wynne, 2010). They indicate that specific training regimes aimed at
promoting cooperation on a specific task that provide many learning
opportunities might further enhance this ability in dogs. The
more independent andproactive attitude oftraineddogs whenconfronted
with a cognitive task remains questionable. In this study,
water rescue dogs appeared not more proactive than untrained
dogs. Further studies comparing dogs not specifically trained for
human-directed gazing during their training and trained to be more
independentin decision making would facilitate clarification ofthis
aspect.
In a broader context, our results point out that specific training
regimes can affect the working dog behavioural responses in
very different ways, emphasising the wide ontogenetic behavioural
plasticity of the dog. Whether such characteristic is also related to
the domestication process is not clear. However,this adaptability is
one of the key factors accounting for the great evolutionary success
of this species, closely linked to humans.
Acknowledgments
We are grateful to all the dog handlers, to Roberto Gasbarri, the
director of the Italian School of Water Rescue Dogs and the dog
trainer Serenella Loreti, for their great support in the organisation
of the testing.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/j.beproc.
2014.09.022.
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