Brief report: Inverse sex effects on performance of domestic dogs (Canis familiaris) in a repeated problem-solving task

Abstract

The authors investigated differences between female and male pet dogs in physical cognition using an object manipulation task. Subjects (24 females and 23 males of different breeds) had to open a box in order to obtain a food reward during 3 consecutive trials, and latency times before success were measured. Males were significantly more successful in opening the box during the first trial. However, this sex difference was inversed when successful individuals were retested. During the following 2 trials, females were more successful than males, indicating that they were able to improve their skills more quickly once they had managed to succeed for a first time. Sex-specific dynamics in repeated problem-solving tasks might be an important contributor to individual differences in cognitive performance of pet dogs.

Full text

BRIEF REPORT
Inverse Sex Effects on Performance of Domestic Dogs (Canis Familiaris)
in a Repeated Problem-Solving Task
Charlotte Duranton
Laboratory of Experimental and Comparative Ethology EA4443,
University of Paris 13, Sorbonne Paris Cité, France and
Association Aide aux Vieux Animaux (AVA),
Cuy-Saint-Fiacre, France
Heiko G. Rödel
Laboratory of Experimental and Comparative Ethology EA4443,
University of Paris 13, Sorbonne Paris Cité, France
Thierry Bedossa
Association Aide aux Vieux Animaux (AVA),
Cuy-Saint-Fiacre, France
Séverine Belkhir
Laboratory of Experimental and Comparative Ethology EA4443,
University of Paris 13, Sorbonne Paris Cité, France and
Association Aide aux Vieux Animaux (AVA),
Cuy-Saint-Fiacre, France
The authors investigated differences between female and male pet dogs in physical cognition using an object
manipulation task. Subjects (24 females and 23 males of different breeds) had to open a box in order to obtain
a food reward during 3 consecutive trials, and latency times before success were measured. Males were
significantly more successful in opening the box during the first trial. However, this sex difference was
inversed when successful individuals were retested. During the following 2 trials, females were more
successful than males, indicating that they were able to improve their skills more quickly once they had
managed to succeed for a first time. Sex-specific dynamics in repeated problem-solving tasks might be an
important contributor to individual differences in cognitive performance of pet dogs.
Keywords: sex difference, pet dog, dog cognition, physical cognition, object manipulation
Supplemental materials: http://dx.doi.org/10.1037/a0037825.supp
Females and males differ in several aspects of their cognitive
abilities to solve physical problems (Healy, Bacon, Haggis, Harris,
& Kelley, 2009). For example, it has been shown that men perform
better in mental rotation or navigation, whereas women outperform
men in object location memory tasks (Andreano & Cahill, 2009;
Caplan, Crawford, Hyde, & Richardson, 1997). Similar differences
are also found in many nonhuman animals, for instance in rodents
(Hawley, Grissom, Barratt, Conrad, & Dohanich, 2012; Jonasson,
2005). These differences are still not fully understood and are
subject to controversial discussions. One of the widely accepted
explanations is the “range size hypothesis,” proposing that males
are under high selection pressure to remember landmarks as they
have larger home ranges than females, thus leading to an improve-
ment in their physical and spatial cognitive abilities (Healy et al.,
2009). However, in some other taxa such as canids, home range
does not appear to differ between males and females (e.g., Kamler
& MacDonald, 2014). And in free-ranging dogs (Canis familiaris)
sex does not influence home range size (Daniels, 1983) or disper-
sal distance (Pal, Ghosh, & Roy, 1998) either. Moreover, little is
known about the presence or absence of the above-mentioned
sex-specific cognitive differences in the domestic dog (Marshall-
Pescini, Barnard, Branson, & Valsecchi, 2013; Miklósi, 2007;
Passalacqua, Marshall-Pescini, Merola, Palestrini, & Prato Pre-
vide, 2013). This is particularly surprising because various aspects
of dog cognition were intensively studied during the last decades
(reviewed in Bensky, Gosling, & Sinn, 2013). A recent study
focusing on this subject showed that female dogs were more likely
than males to respond to violations of the expected size of an
object (Müller, Mayer, Dörrenberg, Huber, & Range, 2011). But to
This article was published Online First September 1, 2014.
Charlotte Duranton, Laboratory of Experimental and Comparative
Ethology EA4443, University of Paris 13, Sorbonne Paris Cité, France and
Association Aide aux Vieux Animaux (AVA), Cuy-Saint-Fiacre, France;
Heiko G. Rödel, Laboratory of Experimental and Comparative Ethology
EA4443, University of Paris 13; Thierry Bedossa, AVA Association;
Séverine Belkhir, Laboratory of Experimental and Comparative Ethology
EA4443, University of Paris 13 and AVA Association.
We are grateful to all owners and their dogs who volunteered in this
study. We also sincerely thank Cécile Arnault, who carried out the reli-
ability coding. Finally, we thank the staff of the Veterinary School of
Maisons-Alfort and especially Karine Reynaud for kindly lending us the
room for experimentation. Charlotte Duranton is now affiliated with Lab-
oratory of Cognitive Psychology UMR7290, Marseille, France.
Correspondence concerning this article should be addressed to Char-
lotte Duranton, Laboratory of Cognitive Psychology UMR 7290, Uni-
versity of Aix-Marseille, 13 331 Marseille Cedex 03, France. E-mail:
charlotte.duranton@cegetel.net
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Journal of Comparative Psychology © 2014 American Psychological Association
2015, Vol. 129, No. 1, 84–87 0735-7036/15/$12.00 http://dx.doi.org/10.1037/a0037825
84

the best of our knowledge, so far no study has focused on whether
female and male dogs differ in their success to solve a physical
cognitive problem.
In this article, we proposed to explore this understudied field,
testing for sex differences in the domestic dog using a problem-
solving task, defined as “the use of a novel means to reach a goal
when direct means are unavailable” (Seed & Call, 2010). To this
end, subjects had to repeatedly open a box in order to obtain food
and we studied their performance with respect to latency time until
success. Based on the results of studies in other mammalian
species (Healy et al., 2009), we expected that male dogs will
outperform females during a repeated problem-solving task as
applied here. Furthermore, we studied whether this purported male
advantage was constant across time, that is, when initially success-
ful animals were retested in consecutive trials.
Method
Subjects and Experimental Setting
We tested 47 pet dogs (24 females and 23 males) of 28 different
breeds or mixed breeds, with sex ratio balanced across breeds (see
Table S1 in the online supplemental materials). Subjects were
between 1- and 8-years-old (on average: 3.7 years; no significant
age differences between males and females: t ⫽ .26, p ⫽ .79), and
did not show any signs of visual or physical impairment. Owners
participated on a voluntary basis and were recruited via the Inter-
net and by personal communication. As verified by interviews with
the owners, all dogs were naïve to the kind of problem-solving task
used in this study.
Experiments were conducted in a closed and silent room (5.0 ⫻
4.6 m). The experimenter was always the same woman for all dogs
(see Figure S2 in the online supplemental materials). Owners were
present during the experiments, but remained silent, immobile and
did not directly look at their dogs. Furthermore, owners wore dark
sunglasses to avoid giving any gaze cue to the dogs during the
trials. During the experiments, dogs wore their usual collars or
harnesses.
The apparatus consisted of a wooden box (15 cm ⫻ 15 cm ⫻ 5
cm), not fixed to the ground. A food reward was hidden inside the
box (a handful of mince and cooked chicken meat), which was
then closed by a plastic cover. A handle (3 cm ⫻ 3 cm cylindrical
plastic stick) fixed on the top of the cover, allowed the dogs to
remove it (with mouth or front paw) in order to get the reward.
General Procedure and Data Collection
The procedure consisted of two consecutives phases:
1. Familiarization phase: The owner, the dog and the ex-
perimenter entered the room and the dog got unleashed in
order to allow it to explore the room and to get familiar
with the experimenter.
2. Testing phase: The owner and the dogs were on their
predefined location (see Figure S2 in the online supple-
mental materials time until success within each trial were
noted.time until success within each trial were noted.),
with the empty apparatus (i.e., no reward inside) placed
on the floor in front of them. The experimenter attracted
the dog’s attention and let it smell the reward she had in
the hand. Then she put the meat inside the box, and put
the cover on it to close the apparatus, with clear and large
gestures, to ensure that the dog could observe and be
interested in it. Finally, the experimenter went to her own
predefined location and asked the owner to unleash the
dog. This was repeated three times (Trials 1–3). The
experiment was terminated (whether or not the dog was
successful in opening the box) after 120 s during Trial 1,
and after 60 s during Trials 2 and 3. The dog was leashed
at the end of a trial and waited 30 s between each trial.
All trials were video recorded and videos were analyzed by the
same experimenter. For all trials, analysis began when the dog was
unleashed. From this moment on, latency time before first contact
with the box, the dogs’ success in opening the box (yes/no) and the
latency time until success within each trial were noted. See online
supplement materials for details on validation of accuracy of video
analysis.
Statistical Analysis
Analyses were done using the program R, version 3.0.1 (R Core
Team, 2013). Differences between females and males with respect
to the latency time in approaching the box were tested by linear
mixed-effects models (LMM). Sex differences with respect to the
time to open the box were tested using Cox proportional hazards
regression models. By the latter analysis, we adjusted for the
censored character of the data, that is, that some of the dogs did not
manage to open the box during the respective trials. See the online
supplemental materials for details.
To test for sex-specific differences in the success in opening the
box across time (see Figure 1), we considered data from all
individuals during the first trial. This was done in order to test for
sex-specific differences in success in a novel problem solving task.
During the following trials, we only considered individuals for
analysis, which were successful during at least one of the previous
trials. This was done in order to test whether the probability of
repeated success (i.e., in an already mastered problem-solving
task) differs between females and males. Thus sample size de-
creased between trial one and the following trials, however slightly
increased between Trial 2 and Trial 3, as some animals were
successful during Trial 2 but not during Trial 1.
Results
Latency to Approach the Box
The latency of approaching the object did not differ between
females and males and was not affected by the reproductive status
(neutered/intact) or the age of the dogs, either when considering all
individuals or only focusing on dogs which were successful during
the respective trial (p ⬎ .05). Furthermore, there was no significant
interaction between sex and trial, indicating that there were no sex
specific differences among trials (p ⬎ .10).
The latency of approach differed significantly across trials
(LMM: ␹
2
2
⫽ 7.60, n ⫽ 141, p ⫽ .022) when considering all
individuals. Post hoc comparisons revealed that latencies during
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85
SEX DIFFERENCES IN PROBLEM SOLVING IN DOGS

the third trial (on average 7.9 s ⫾ 4.1 CI
90%
) were significantly
higher than during the first trial (4.8 s ⫾ 4.3 CI
90%
); ␹
2
2
⫽ 5.39,
p ⫽ .020) and during the second trial (5.2 s ⫾ 3.5 CI
90%
); ␹
2
2
⫽
6.16, p ⫽ .013). The first and second trials did not differ (␹
2
2
⫽ .16,
p ⫽ .70). These differences among trials disappeared when only
considering subjects, which were successful during the respective
trial (Trial 1: 1.5 s ⫾ .7 CI
90%
; Trial 2: 1.3 s ⫾ .2 CI
90%
; Trial 3:
1.3 s ⫾ .2 CI
90%
;␹
2
2
⫽ .32, p ⫽ .85).
Opening the Box
First trial. During the first trial males were significantly more
successful than females in opening the box (Cox proportional
hazards regression: ␹
2
2
⫽ 7.67, n ⫽ 47, p ⫽ .006; Figure 1A). Note
that this kind of model integrates the latency time as well as the
probability of success as dependent variable for analysis. There
were no significant effects of the dogs’ age and reproductive status
(␹
2
2
⫽ .08, p ⫽ .77) with respect to their success (␹
2
2
⫽ .11, p ⫽ .74)
and also no significant interactions among the three predictor
variables (p ⬎ .10).
Repeated trials. The sex-dependent performance was in-
versed when successful subjects were repeatedly tested in a second
and third trial. During Trial 2 (␹
2
2
⫽ 4.10, n ⫽ 21, p ⫽ .043; Figure
1B) as well as during Trial 3 (␹
2
2
⫽ 7.40, n ⫽ 26, p ⫽ .007; Figure
1C) the proportion of successful females was significantly higher
than the proportion of successful males. Again, there were no
significant effects of age and of reproductive status, and also the
interactions between the 3 predictor variables were not significant
(p ⬎ .05).
Discussion
Although sex differences in physical problem-solving skills
have been intensively studied in various mammalian species (Seed
& Call, 2010), to our knowledge this is the first study reporting
differences between females and males in problem-solving abili-
ties in the domestic dog. Most importantly, our results indicate
inversed sex-specific differences in success across repeated trials.
During the first trial, males outperformed females and such a male
advantage in physical cognition is in line with previous findings in
other mammals (Benson-Amram, Weldele, & Holekamp, 2013;
Healy et al., 2009). This initial difference was unlikely due to
females’ lower degree of motivation because both sexes did not
differ in their latency to approach the box in any of the trials. We
suggest that male dogs were less affected by the experimental
setting as studies on dog temperament using nonsocial objects
have frequently reported comparatively higher boldness scores in
males in such situations (Starling et al., 2013).
Different nonexclusive mechanisms might be considered in or-
der to explain this observed sex difference (Müller et al., 2011).
First and as already mentioned, sex-specific selection might have
led to different cognitive abilities. It is possible that such differ-
ence was selected and present in dogs’ and wolves’ common
ancestor. And even if no evidence exists that different selective
pressures, home range size or breeding strategies have shaped male
and female pet dogs’ behavior in a contrasting way (Miklósi,
2007), sex-specific cognitive abilities might originate from the
dog’s ancestral species. Second, sex-specific environment during
ontogeny might have induced different cognitive capacities of
adult females and males. And indeed, sex-specific differences in
early developmental environment are for example reported in
humans, since children of different gender are frequently raised
in a different way according to cultural traditions (Wood & Eagly,
2012). As many owners consider their dogs as family members
(Archer, 1997), a “social gender consideration,” that is, differences
in the way owners might interact with female and male dogs, could
be potentially relevant here. Third, sex difference in cognition
might also be a by-product of other sex-dependent differences,
such as hormone levels (Kimura, 1999). For example, a study in
men indicates that increased testosterone levels have differential
effects on spatial abilities and verbal fluency (O’Connor, Archer,
Hair, & Wu, 2001). But in general, the interaction between tes-
tosterone levels and cognitive abilities is far from being clear.
Most importantly, when retesting individuals that were initially
successful, females outperformed males during these successive
trials. Such a higher performance in female dogs as compared with
males has been already reported in previous studies, although
Figure 1. Kaplan-Meier curves showing the increase in the proportion of successful females and males during
repeated trials. Differences between females and males were significant during all trials; but note the inversed
effects between the first and the following trials. Sample sizes increase from the second to the third trial, as we
considered all individuals for analysis during the repeated trials, which were successful in one of the previous
trials. See text for details on statistics. See the online article for the color version of this figure.
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86
DURANTON, RÖDEL, BEDOSSA, AND BELKHIR

never in the context of repeated trials (Müller et al., 2011; Rooi-
jakkers et al., 2009). We propose that this inversed sex effect
across time could be due to sex-specific differences in the way of
remembering the successful strategy of problem solving. Indeed,
such differences in learning performance between males and fe-
males in social as well as in nonsocial contexts have been de-
scribed in primates. For example, female rhesus monkeys (Macaca
mulatta) outscored males in a learning task related to the utiliza-
tion of local markers (Herman & Wallen, 2007). Moreover, studies
in humans indicate that females remember precise object or local
features better than males (Lejbak et al., 2009; Voyer et al., 2007).
We propose that similar sex-specific processes could be present in
the dog.
Although this study only focuses on a single task, it provides a
significant piece of evidence emphasizing the existence of sex-
specific differences in problem-solving skills in the domestic dogs.
Most importantly, the study reveals that the direction of differ-
ences between males and females is not necessarily stable across
repeated trials. We hope that our findings will stimulate others to
include such interactive changes across time in the study of cog-
nitive abilities in mammals and birds.
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Received February 27, 2014
Revision received July 28, 2014
Accepted July 30, 2014 䡲
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