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Sea lions’ (Zalophus californianus) use of human pointing gestures as referential cues



This experiment investigated the ability of four human-socialized sea lions to exploit human communicative gestures in three different object-choice tasks based on directional cues emitted by their caretakers. In Study 1, three of the tested subjects were able to generalize their choice of the pointed target to variations of the basic pointing gestures (i.e., cross-body point, elbow point, foot point, and gaze only), from the very first trials. Study 2 showed that the subjects could follow the pointing gestures geometrically and select the correct target among four possible targets, two on each side of the informant. In Study 3, we tested the robustness of their tendency to follow a pointing gesture by hiding targets behind barriers. One subject was able to follow pointing gestures towards targets not visible at the moment of their decision without any training, despite the presence of another visible and directly accessible one. Taken together, these results suggest that sea lions were able to use the referential property of the human pointing gesture, because they were able to rely on extrapolating precise linear vectors along different pointing body parts in order to identify a precise object rather than merely a general direction. These findings support previous arguments that some non-domesticated species might have as great an ability to respond appropriately to pointing gestures as domesticated dogs. The potential roles of human-socialization and specific features of wild sea lions ecology are discussed.
1 23
Learning & Behavior
ISSN 1543-4494
Learn Behav
DOI 10.3758/s13420-014-0165-7
Sea lions’ (Zalophus californianus) use of
human pointing gestures as referential cues
Raphaëlle Malassis & Fabienne Delfour
1 23
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Sea lions(Zalophus californianus) use of human pointing gestures
as referential cues
Raphaëlle Malassis &Fabienne Delfour
#Psychonomic Society, Inc. 2014
Abstract This experiment investigated the ability of four
human-socialized sea lions to exploit human communicative
gestures in three different object-choice tasks based on direc-
tional cues emitted by their caretakers. In Study 1, three of the
tested subjects were able to generalize their choice of the
pointed target to variations of the basic pointing gestures
(i.e., cross-body point, elbow point, foot point, and gaze only),
from the very first trials. Study 2 showed that the subjects
could follow the pointing gestures geometrically and select
the correct target among four possible targets, two on each
side of the informant. In Study 3, we tested the robustness of
their tendency to follow a pointing gesture by hiding targets
behind barriers. One subject was able to follow pointing ges-
tures towards targets not visible at the moment of their deci-
sion without any training, despite the presence of another vis-
ible and directly accessible one. Taken together, these results
suggest that sea lions were able to use the referential property
of the human pointing gesture, because they were able to rely
on extrapolating precise linear vectors along different pointing
body parts in order to identify a precise object rather than
merely a general direction. These findings support previous
arguments that some non-domesticated species might have as
great an ability to respond appropriately to pointing gestures
as domesticated dogs. The potential roles of human-
socialization and specific features of wild sea lions ecology
are discussed.
Keywords Social cognition .Human-given cues .Pointing .
California sea lion
The function of gaze and general body orientation, sometimes
strengthened by pointing with an arm and/or a finger, is crucial
to human referential communication. Referential communica-
tion per se implies Bjoint attention^: a triadic relationship be-
tween an informant, a recipient and a precise object, place, or
event on which the attention of the first individual is fixed
(Butterworth, 1995). Deictic gesture following, as opposed
to merely looking where someone else is looking, implies a
certain degree of comprehension of the communicative and
referential nature of this gesture. The specific informative ges-
ture has to be identified among all other gestures as indicative
of a specific object among other objects. The capacity to fol-
low such gestures is developed quite early in human children
(Lempers, 1979; Morissette, Ricard, & Decarie, 1995), and
plays a crucial role in language learning.
Numerous studies have been conducted to assess this abil-
ity in other species in the last few decades, using the so-called
object-choice task. This task tests the ability to use human-
given cues to find a hidden reward located in one of two (or
more) containers. The question is whether certain animals can
follow human pointing gestures to the correct object without
any prior formal training, and to what extent the distortion of
these cues or the complexity of the situation affect their be-
havior. Dogs have been reported to be particularly sensitive to
human pointing cues in this type of task (Canis familiaris;
Hare, Call, & Tomasello, 1998; Lakatos, Gácsi, Topál, &
Miklósi, 2009; Soproni, Miklosi, Lorand, Topal, & Csanyi,
2002). Other domestic species have been successful in
R. Malassis (*)
Laboratory of Cognitive Psychology, Aix-Marseille University,
Fédération de Recherche 3C, CNRS, 13331 Marseille Cedex, France
F. Delfour
Parc Astérix, Plailly, France
Learn Behav
DOI 10.3758/s13420-014-0165-7
Author's personal copy
exploiting at least some explicit pointing (i.e., with an extend-
ed arm): cats (Felis catus; Miklosi, Pongracz, Lakatos, Topal,
& Csanyi, 2005), horses (Equus caballus; Maros, Gacsi, &
Miklosi, 2008; Proops, Walton, & McComb, 2010), goats
(Capra hircus; Kaminski, Riedel, Call, & Tomasello, 2005),
and pigs (Sus scrofa domestica; Nawroth, Ebersbach, & von
Borell, 2013). Taken together, these results have led some
researchers to hypothesize that successful interpretation of
human communicative cues arises as a side effect of domes-
tication (e.g., see Agnetta, Hare, & Tomasello, 2000;Hare&
Tomasello, 2005; Virányi, Gácsi, Kubinyi, Topál, Belényi,
Ujfalussy, & Miklósi, 2008).
However, this hypothesis has been countered by other find-
ings: human-socialized undomesticated individuals, such as
wolves (Canis lupus; Udell, Dorey, & Wynne, 2008;Udell,
Spencer, Dorey, & Wynne, 2012), African elephants
(Loxodonta africana;Smet&Byrne,2013), dolphins
(Tursiops truncatus; Pack & Herman, 2004,2007; Tschudin,
Call, Dunbar, Harris, & van der Elst, 2001), fur seals
(Arctocephalus pusillus, Schuemann & Call, 2004)andagray
seal (Halichoerus grypus, Shapiro, Janik, & Slater, 2003)have
also been shown to be very successful, some not far from a
dog's level of performance. Great apes are generally unskillful
(e.g., see Call & Tomasello, 2005; Povinelli, Reaux,
Bierschwale, Allain, & Simon, 1997), but recently Lyn,
Russel, and Hopkins (2010) showed that chimpanzees and
bonobos raised in socio-linguistically rich environments per-
form much better than chimpanzees raised in standard
laboratory housing. These findings suggest a comple-
mentary hypothesis: in some species, rich daily interac-
tions with and exposure to human gestural communica-
tion can be sufficient for correctly interpreting pointing
cues. This could be especially the case for species that
have native ability in attending to and exploiting social
cues (Smet & Byrne, 2013).
To further test this hypothesis, we investigated the under-
standing of human pointing gestures in four human-socialized
Californian sea lions (Zalophus californianus). Even though
other social marine mammals have already been reported to
succeed to some degree (Herman, Abichandani, Elhajj,
Sanchez, & Pack, 1999;Pack&Herman,2007; Schuemann
& Call, 2004; Shapiro et al., 2003), only dolphins have been
tested in object-choice tasks involving more than two targets,
unusual body parts (i.e., not associated with any specific com-
mands). The formal training of these four sea lions included
several commands involving arm gestures, and two subjects
had to be trained to respond to proximal points (i.e., with an
extended arm, finger at approximately 30 cm from the target
while pointing) at the beginning of the current experiment
(See BPretraining^, in the Methods section). The aim of this
experiment was to investigate whether they could exploit new
pointing gestures, in relatively complex situations.
Three studies were conducted, using different object-
choice tasks. In Study 1, we tested these sea lionsability to
spontaneously transfer their response from explicit pointing
(i.e., with an extended arm) to variations of the pointing ges-
ture, to select the correct target between two similar objects,
placed on either side of the informant. However, here we
define the ability to use the referential property of the pointing
gesture as the ability to rely on extrapolating precise linear
vectors along the pointing arm in order to identify a precise
object, instead of a general direction. In the basic version of
the object-choice task used in Study 1, it may be possible that
the subject would simply choose the object situated on the side
of the human at which they saw a protruding body part and/or
amovement(Lakatosetal.,2009; Lakatos, Gácsi, Topál, &
Miklósi, 2011; Soproni et al., 2002), without any use of the
referential property of the pointing gesture. This possibility
was addressed by Study 2, where two similar targets were
placed along the same line on each side of the informant
(resulting in two proximal and two distal targets). Finally,
Study 3 tested the sea lionsresponse to pointing to a hidden
target, in the presence of a visible distractor item.
Four subjects were tested in Study 1, but only three partic-
ipated in Studies 2 and 3. Thiswas because one of the subjects
arrived at the dolphinarium only one month prior to the be-
ginning of the experiment, and required a period of familiar-
ization with this new environment before participating in our
experiment. Thus, this subject (Kaï) started participation in the
experiment later than the other three subjects (i.e., when they
were already into Study 2), and completed Study 1 only.
Study 1
The subjects comprised four male sea lions (Zalophus
californianus), housed together at Parc Asterix, France. All
were born in captivity, but came from different zoos and had
different life experiences prior to coming to Parc Asterix. San-
to, Smack, and Gonzo (respectively 6, 5, and 3 years old)
arrived at the park 30 months prior to the experiment. They
were quite familiarized with training sessions and shows, and
knew a wide range of commands. Kaï (2 years old) arrived
only one month prior to the beginning of the experiment, and
had never been trained to any human gestural and/or vocal
command before. None of the subjects had previously partic-
ipated in any behavioral study. They lived in an enclosure of
125 m
, with an outdoor saltwater pool (313 m
), and a set of
two indoor habitats (total over 50 m
). They were fed a mix-
ture of capelin, squid, and herring, distributed during their five
daily training sessions. Typically, they had to respond
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correctly to both vocal and gestural commands to be rewarded
with a whistle blow and pieces of fish. Caretakers proceeded
in such a way that by the end of the session (including exper-
imental sessions), each sea lion had received his planned ra-
tion, regardless of his performance.
Experimental sessions were conducted as much as possible
like usual training sessions. We made the choice not to sepa-
rate the tested individual from the other subjects. The tested
sea lion was simply led to the part of the enclosure where the
experimental setup was placed. He could meanwhile keep
visual and acoustic contact with his conspecifics, as they par-
ticipated in routine training sessions with the other caretakers
(learning new commands and being trained for shows and
medical examinations, without any direct connection with
our pointing experiment).
Along the same line, the informant was not an unfamiliar
experimenter, but one of their customary caretakers. Four
caretakers participated in the experimental sessions, each with
the same animal throughout the experiment. We made sure all
caretakers were previously trained to correctly execute each
cue, and a strong emphasis was put on displaying only the
gestural and verbal cues defined for each experimental condi-
tion throughout each trial in order to avoid unintentional extra
Two identical and familiar green Frisbees (24 cm in diam-
eter) served as the response targets. They were placed on the
ground, at equal distance from the subject, approximately 150
cm, on either side of subject. Each trial began with the sea lion
sitting down at his starting position (represented by a piece of
carpet), the caretaker in front of him between the two Frisbees
(approximately 100 cm from both). He/she obtained visual
contact with the subject (calling him by name if necessary),
demonstrated the cue for 2 s, and then returned to his/her
initial position. If the subject did not move at the first cue,
the experimenter repeated it every 2 s, up to a maximum of
three times. The subject indicated his choice by touching one
of the Frisbees with his muzzle. Correct choices were
rewarded with a whistle blow and a piece of fish. If the subject
made an incorrect choice, no reward was given and he was
simply signaled to return to his starting position. The cues
were presented in a predetermined semi-random order (14
trials per cue), each Frisbee was pointed to an equal number
of times, and the same Frisbee was never pointed to more than
twice in a row.
Six different cues were presented to the subjects, defined as
follows (Fig. 1). In all cases, the caretaker was positioned in
front of the subject and looked at him while pointing, unless
otherwise specified below:
Point and gaze (PG): Caretaker extended his/her ipsilat-
eral arm and index finger toward the target object while
turning his/her head to look at it.
Fig. 1 Experiment setup and
illustration of the six different
pointing cues used in Study 1,
from the sea lion's point of view.
PG : Point and Gaze; P : Point; C :
Cross-body point; E : Elbow
point; G : Gaze; F : Foot point.
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Point (P): Caretaker extended his/her ipsilateral arm and
index finger toward the target object.
Cross-body point (C): Caretaker extended his/her contra-
lateral arm and index finger toward the target object.
Elbow point (E): Caretaker stuck his/her ipsilateral elbow
out toward the target object while keeping the hand be-
hind the back at hip level.
Gaze (G): Caretaker turned only his/her head to look at
the target object.
Foot point (F): Caretaker stood on one foot while pointing
at the target container with his/her ipsilateral foot.
The number of trials per session varied between five and
18, depending on the study, the age of the individual, his
interest in participating in the training and the current state
of the other sea lionstraining sessions. Sessions were con-
ducted until the subject completed the number of trials
planned for each study, over a period of two months. Inter-
trial time varied from approximately 5 to 30 s, during which
the caretaker sometimes gave known and rewarded com-
mands (unrelated to pointing cues) to maintain the sea lions
motivation and attention.
The subjects had previously been trained to respond to several
commands which included arm gesture. Only two of the com-
mands involved an extended arm pointing toward a general
direction: all of the subjects had been trained to return to the
water when the caretaker extend his/her arm inthe direction of
the pool, saying Bwater.^The second one was known only by
Santo, who had been trained to return a floating toy when the
caretaker extended his/her arms in the direction of the water
and formed a square with his two hands. Two other commands
involved an extended arm oriented toward the sea lion: with
the palm open, while saying Bstay,^to make him sit down and
wait at a specific place, and with a finger pointed toward the
animal, while saying "shy", to make him cover his muzzle
with his flipper. They were not trained to any other gestural
command including an extended arm, and more specifically,
had never been previously trained to select (e.g., by touching
with his muzzle) a precise object indicated by an extended arm
and pointed finger. Therefore, considering their previous ex-
perience of commands involving arm gestures, all described
above, the main aim of this study was not to test their ability to
follow gestures to a general direction; it was to assess their
ability to spontaneously generalize their response when other
caretakers body parts were used to emit the pointing cue
(Study 1), and to follow it to a precise object rather than
merely in a general direction (Studies 2 and 3).
Accordingly, the initial session was conducted as follows:
if the subject spontaneously gave a correct response to the first
pointing gesture, the session continued as planned (i.e., with
the six cues presented in a predetermined semi-random order).
If he did not, training sessions with proximal pointing were
conducted until the subject gave eight correct responses in a
row (i.e., moving to the pointed object and touching it with his
muzzle). Trainings to proximal point were conducted in the
same setup as Study 1 (as described below), except that the
caretaker was on his/her knees, with the tip of his/her finger at
approximately 30 cm from the target while pointing.
Data analysis
All trials were recorded by digital camera for post-session
review and analysis. Only individual analyses of perfor-
mances with nonparametric statistical tests were used. Bino-
mial tests were conducted for each individual to determine if
he performed better than chance when using a particular cue.
Permutation tests were used to compare latencies of choices
between the different cues (starting when the caretaker began
to demonstrate the cue until the subject touched the Frisbee).
To test the hypothesis that the sea lions learned to respond
correctly to each cue across trials, the number of correct trials
on the first and the second half of the trials (seven trials each)
for each cue were compared using Fishers test. Additionally,
the response of each individual on the first trial for each one of
the six cues was recorded. Binomial tests were conducted to
determine for each individual whether he performed better
than chance on these first trials (six in total).
Results and discussion
Spontaneous responses to an explicit pointing gesture were
first tested. Santo and Smack responded correctly on the very
first trial, by moving to the pointed target and touching it with
their muzzle. On the other hand, Gonzo and Kaï both
attempted to respond by executing previously learned com-
mands (specifically by touching the caretakerspointinghand
with their muzzle, or by executing the Bshy^behavior, sig-
naled by the caretakers' finger pointed toward the sea lion);
therefore both needed two training sessions to proximal point
to reach the learning criterion (as described above, in the
Pretraining section), while Santo and Smack directly moved
up to the next test sessions.
Figure 2presents the percentage of correct reponses in test
sessions, for each sea lion, across the six pointing cues. All
subjects performed at or near ceiling level to the Point cues,
with or without gaze (binomial tests: p<.001 in both cases,
with 50 % chance). Three of our four subjects also performed
beyond chance in the cross-body point (C), elbow point (E),
gaze (G), and foot point (F) cues (ps.05). However, one
subject, Gonzo, failed to successfully respond to the cross-
body point (C), and another one, Smack, failed to respond to
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the three cues that did not involve the arm (i.e., G, E, and F).
Tab le 1presents the response on the very first trial, and the
number of correct trials on the first and second half of the trials
for each subject. For each correctly interpreted cue (i.e., except
for Smack and Gonzo for the cues cited above), the subjects
very first choice was correct. Santo and Kaï performed beyond
chance level on the overall six first trials (ps<.05 for both), but
Smack and Gonzo did not (ps>.13). There was no significant
difference in number of correct responses between the first
and the second half of the trials (Fishers tests (N = 14),
ps > .19 in all cases).
Latencies (Fig. 2) were shorter with PG, P, and C than with
the less conspicuous cues (G, E, and F). Santo's latencies were
significantly longer with F compared to all pointing gestures
involving the arm; with E versus PG and C; and with F versus
PG and P (permutation tests: ps < .05 in all cases). Smack's
latencies were longer with G than PG, P, C, and E (p< .05 for
C, ps < .01 for the others). It took Gonzo longer to choose with
Fig. 2 Bars represent the
percentage of correct reponses for
each sea lion across the six
pointing cues used in Study 1:
Point and Gaze (PG), Point (P),
Cross-body point (C), Elbow
point (E), Gaze (G), and Foot
point (F). The cues were present-
ed in a predetermined semi-
random order (14 trials per cue for
each subject). Curves represent
their mean latencies (starting
when the caretaker began to pro-
duce the cue and ending when the
subject touched the Frisbee).
Dotted lines represent chance
level (50 %). *p.05, **p.01,
***p.001, binomial tests.
Tabl e 1 Number of correct trials in the first and second half of the trials
(seven trials each) for Study 1, and in the first and last ten-trial blocks for
Studies 23, and response in the very first trial (underlined value: correct;
non-underlined value: incorrect), across conditions for each subject (San-
to, Smack, Gonzo, Kaï).
Study 1 Studies 23
Subjects Trials Point and gaze Point Cross-body point Gaze Elbow point Foot point Subjects Trials Study 2 Study 3
Santo First half 7 7 6 6 6 4 Santo First 10 7 10
Second half 7 7 7 6 6 7 Last 10 10 10
Smack First half 7 6 6 3 6 4 Smack First 10 7 5
Second half 6 7 7 5 3 5 Last 10 10 9
Gonzo First half 7736 5 6 Gonzo First 10 6 6
Second half 7 7 5 6 7 6 Last 10 8 10
KaїFirst half 7 7 7 6 5 6KaїFirst 10 ––
Second half 7 7 7 7 7 5 Last 10 ––
Note that Kaï did not participate in Studies 23 due to his later arrival at the dolphinarium (no data indicated by B^),and that Smack and Gonzosresults
in Study 3 were obtained after having provided them extra training (cf. Study 3 Methods section)
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GversusPG,P(ps <.05)andF(p< .01). It took Kaï longer
with F compared to PG, P and C (ps <.01).During these
intervals, the sea lions typically stayed at their starting
place, or moved very slowly, making gaze alternations
between the caretaker and the Frisbees. As their perfor-
mances show, the sea lions were able to interpret vari-
ations of the pointing gesture correctly, but sometimes
hesitated and waited for cue repetition before acting.
Study 2
Subjects included three of the four previous participants: San-
to, Smack, and Gonzo.
The general procedure was the same as in Study 1, except that
instead of two targets, there were four. We used a similar
design to that of Morissette et al. (1995) and Lakatos et al.
(2011). Four identical Frisbees were placed in front of the
caretaker in such a way that the distances between each Fris-
bee and the tested subject were the same (approximately 1.5
m). In the starting position, the caretaker stood behind the two
inner Frisbees (hereafter called Bproximal^targets), while the
subject faced him behind the two outer (Bdistal^) targets. Con-
sequently, the targets lay along the same visual line, and
pointing gestures towards distal and proximal targets differed
by the angle of the caretakers arm (50° and 20°, respectively).
Thus, even when the caretaker pointed to a distal target, his/
her pointing finger was actually closer to the proximal target
located on the same side (respectively 1.50 m and 0.90 m)
(Fig. 3a). Each Frisbee was pointed to an equal number of
times, in a semi-random order, with a total of 60 trials per
Data analysis
Binomial tests were conducted for each individual to
determine if performance was better than chance. The
ability of sea lions to choose the side (left vs. right) of
the object correctly on the basis of a point and gaze cue
(PG) was not in question (and indeed, they chose the
correct side 100 % of the time in this study); rather,
the question was whether they would choose the indicat-
ed Frisbee between the two present on the correct side.
This is why the level of chance was 50 % and not 25 %.
Learning across trials was investigated by comparing for
each subject the number of correct responses on the first
ten-trial and the last ten-trial blocks of the Study (i.e.,
trials 110 vs. trials 5060), using Fishers test. The re-
sponse of each individual on the first trial was also
Results and discussion
All subjects performed well in this task: Santo was cor-
rect in 85 % of the trials (binomial test: p<.001, with
50 % chance), Smack 67.8 %, and Gonzo 71.7 %
(ps<.01) (Fig. 4a). There was no difference in perfor-
mance between proximal and distal targets (Pearsons
Chi-Square tests (1, N = 60), ps>.14), despite a slight
tendency to be more efficient with distal targets than
proximal ones. Table 1presents the number of correct
trials on the first and the last ten-trial blocks, and the
response on the very first trial for each subject. There
Fig. 3 (a) Experimental setup of Study 2 (left side only), illustrating the
distal pointing cue. (b) Experimental setup of Study 3, illustrating
pointing toward the left hidden target
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was no significant difference between the blocks for any
subject (Fisherstests(N=20),ps>.21). However, none
of the subjects were correct on the first trial.
Study 3
The subjects were the same as in Study 2: Santo, Smack, and
The general procedure and the pointing gesture (point and
gaze cue) were the same as in Study 2. However, here three
instead of four Frisbees were pointed to in a semi-random
order. One Frisbee was placed in front of the caretaker (ap-
proximately 60 cm from him/her) and another on either side of
him/her (approximately 140 cm). Two opaque screens (100
) were placed in such a way that the subject could not see
the two lateral targets while he was at the starting position in
front of the caretaker. Only the Frisbee placed in front of the
subject was visible (Fig. 3b). Each of the three Frisbees was
pointed to an equal number of times, in a semi-random order,
with a total of 42 trials per subject.
We suspected the central Frisbee to be a highly salient
stimulus in Study 3 considering that no other target stimulus
was visible. It was reasoned that strong behavioral inhibition
of responding to that stimulus might be necessary in trials
where the occluded Frisbees were pointed to. Considering
this, we planned the first trials as follows: if the sea lion cor-
rectly moved to the hidden Frisbee when pointed to, the test
session was conducted directly. But in case of systematic
choice of the visible Frisbee, we conducted a training session.
This training session consisted of eight trials without the vis-
ible Frisbee. Therefore only the two hidden Frisbees were
present, and each one pointed to four times, in a semi-
random order. After that, test sessions would be conducted
under the conditions described above.
Data analysis
Given that three Frisbees were present in the testing sessions
of this experiment, binomial tests were conducted for each
individual with a chance level of 33 %. Learning across trials
in the test sessions was investigated by comparing for each
subject the number of correct responses on the first ten-trial
and the last ten-trial blocks of the study (i.e., trials 110 vs.
trials 3242), using Fisherstests.
Results and discussion
The subjectsinitial responses were different: Santo correctly
responded immediately (i.e., in less than 2 s for each trial)
during the first session. Smack was correct but took longer
than Santo during the first four trials. It took him approximate-
ly 10 s to respond, making several gaze-alternations, but, little
by little, he got around the screen (no reinforcement was given
before he finally touched the Frisbee). After that, he always
responded immediately. On the contrary, Gonzo systematical-
ly chose the visible Frisbee on the first session, including in
the trials where the hidden Frisbees were pointed to. Thus,
Gonzo was the only one to be trained for a session of eight
trials without the visible Frisbee. Gonzosresponseattempts
during the first training trials were similar to those of Smack in
his first test trials (e.g., he tried to respond by touching the
screen with his nose). During these training trials, no feed-
Fig. 4 Bars represent the percentage of correct reponses for each sea lion
in Study 2 (a) and Study 3 (b). The total number of trials per subject was
60 for Study 2 and 42 for Study 3. Dotted lines represent the level of
chance (50 % in Study 2: a correct reponse was choosing the indicated
Frisbee between the two present on the pointed side; 33 % in Study 3: a
correct response was choosing the indicated Frisbee between the three
available). *p.05, **p.01, ***p.001, binomial tests.
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back was given to Gonzo until he had chosen a Frisbee. The
same reinforcement procedure as for test trials was applied : in
case of a correct choice, the subject was rewarded, while in
case of an incorrect choice, no reward was given and he was
signaled to return to his starting position to perform the next
trial. At the end of the training session, Gonzo successfully
completed five of eight trials. Results presented hereafter are
from the first test trials for Santo and Smack, and from test
sessions following the training for Gonzo.
The percentage of correct choices for each subject was
significantly above the values expected from chance: Santo
was correct in 92.9 % of the trials (binomial test: p<.001, with
33% chance),Smack in 66.7 %, and Gonzo in 85.7 % (ps<.01)
(Fig. 4b). No better performance was found in their response
to pointing toward the visible target than toward hidden tar-
gets. Table 1presents the number of correct trials in the first
and the last ten-trial blocks, and the response on the very first
trial for each subject. No significant difference between the
blocks was found for any subject, but Smack and Gonzo had a
tendency to perform better in the last block of trials compared
with the first block (Fishers tests (N=20), p=.14 and p=.08,
Because one out of the three tested subjects, Santo,
responded directly (i.e., in less than 2 s, and without any other
attempt at response) to the pointing gestures towards the hid-
den Frisbees, we conclude that this sea lion was able to follow
pointing gestures made towards occluded targets, despite the
presence of a visible and directly accessible target. The two
remaining subjects needed training in order to correctly follow
these pointing gestures. For Gonzo, a training session without
the visible Frisbee had to be conducted, as described in the
Methods section. Smack did not systematically choose the
distractor, and thus did not receive this explicit training. How-
ever, he also made other attempts at response before touching
the pointed hidden Frisbee (e.g., touching the screen). Touch-
ing the visible Frisbee despite the caretakers gesture to a
hidden one was considered as an incorrect choice (no reward
was given and the sea lion was signaled to return to his starting
position), while in the case of touching the opaque screen the
trial continued until the sea lion touched one of the Frisbees. It
may thus be possible to consider the lack of reinforcement in
both cases (touching the visible Frisbee as well as touching the
screen) as a form of training. As Santo was the only tested
subject to not attempt either of those actions, he was the only
one considered to be successful without any prior training.
General discussion
The current findings establish that three of the four tested sea
lions generalized their responses to all novel pointing cues
presented in Study 1: cross-body point, elbow point, foot
point, and gaze only. Because correct responses were
rewarded, it would be tempting to explain such results by
reinforced learning. However, these three subjects were error-
less on the very first trial for each cue, and tests comparing the
number of correct responses between the first and the second
half of trials for each subject for each condition revealed no
difference in performance with time. Increasing latencies re-
lated to decreasing conspicuousness of the cues suggests that
even if three out of the four sea lions performed above chance
level with all the pointing cues, it was easier for them to
respond to the most Bexplicit^ones (i.e., involving an extend-
ed arm).
Their level of generalization was equivalent to that ob-
served in dogs. Sea lions followed the foot point cue, which
is a body part never used before with them to give commands,
an ability that has also been reported in dogs (Lakatos et al.,
2009), half of the tested wolves (Udell et al., 2012), and ele-
phants (Smet & Byrne, 2014). They also correctly exploited
the elbow point cue, while dogs and wolves have been report-
ed to fail to do so (Soproni et al., 2002; Udell et al., 2012).
Unlike the two previously cited studies, in our study we asked
the caretaker to put the hand of the used arm behind his/her
back while producing elbow point. This may have facilitated
elbow point following by reducing the conflict between the
different potential cues (i.e., pointing elbow and hand). Such
interference might also explain why chimpanzees (Povinelli
et al., 1997), dogs (Lakatos et al., 2009; Soproni et al., 2002),
and elephants (Smet & Byrne, 2013) performed below the
level of chance with a cross-elbow point cue (i.e., elbow pro-
tuberance could interfere with the index finger on the midline
of the body, pointing at the opposite target). The sea lions also
used gaze as a directional cue, as do dogs (Hare et al., 1998;
Miklosi, Polgardi, Topal, Csanyi, 1998), dolphins (Pack &
Herman, 2004), fur seals (Schuemann & Call, 2004), and
chimpanzees (Barth, Reaux, & Povinelli, 2005; Povinelli
et al., 1997; Povinelli, Bierschwale, & Cech, 1999). This abil-
ity seems to be restricted: horses (Proops et al., 2010), goats
(Kaminski et al., 2005), wolves (Udell et al., 2012), a gray seal
(Shapiro et al., 2003), and elephants (Smet & Byrne, 2013)
failed. A possible explanation could be that the species that
were unsuccessful in this task have poor eyesight, which does
not allows them to perceive this very subtle cue (Shyan-
Norwalt, Peterson, Milankow King, Staggs, & Dale, 2010,
in Smet & Byrne, 2013). We also suggest that sensitivity to
human head orientation could have been enhanced in the test-
ed sea lions because of the importance of visual contact during
interactions with the caretakers (e.g., during shows, sea lions
have learnt to respond to a caretaker only when being in visual
contact with him/her).
The results of the first experiment show that three sea lions
out of four selectively responded to the only fundamental
characteristic which appears to link the six presented cues:
the target was located in the extension of the pointing body
part. However, subjects could rely on very basic decision-
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making rules to respond correctly in this task. They could
merely move to the unique target located on the side of the
caretaker where they perceived a protruding body part and/or
a movement (Lakatos et al., 2009,2011; Soproni et al., 2002)
or to the closest one, according to a distance-based rule from
hand to target (Povinelli et al., 1997). Therefore, in the second
study we assessed their use of the referential property of the
pointing gesture by testing whether they could not only follow
it in a general direction, but more precisely to the pointed
object, in the presence of two potential targets along the same
line. All the sea lions tested in the current study correctly
selected, beyond the level of chance, the pointed object be-
tween the two present on each side of the informant. There
the first and last ten-trial blocks were not different for any
subject. In studies using only two potential targets, a gray seal
(Shapiro et al., 2003), fur seals (Schuemann & Call, 2004),
wolves (Udell et al., 2012), dogs (Hare et al., 1998; Soproni
et al., 2002), and elephants (Smet & Byrne, 2013)successfully
chose the pointed target even when the informant stood closer
to the incorrect one. These results show that the pointing cue
prevails over body position, and that the hand-to-target
distance-based rule is not sufficient to explain the perfor-
mances of the tested subjects, contrary to some findings in
chimpanzees (Povinelli et al., 1997). The sea lionsperfor-
mance in our setup leads to the same conclusion, because
the informant's hand was closer to the proximal target than
to the distal one, even when pointing to the distal item. But
in these previously cited studies, subjects could still simply
follow the discriminative rule of choosing the object located
on the side in which a body part of the informant is protruding
or moving to be successful. Tasks in which the subject has to
follow a precise linear vector along the pointing arm to a
particular object among several objects located in the same
general direction appear to be more valuable (Pack & Herman,
2007). To our knowledge, only two other species have been
tested in this way. Bottlenose dolphins were tested in a setup
similar to the one we used, with the same positive results
(Pack & Herman, 2007). Results in dogs are more heteroge-
neous: using the same setup, recently Lakatos et al. (2011)
have shown that 14 out of 16 tested dogs failed to select the
correct target between the two present on the pointed side, and
tended to choose the containers closer to the informant; while
Hare et al. (1998), using three instead of four containers, tested
two dogs that succeeded above chance level.
Results of our second study showed that the tested sea lions
understood the pointing cue as indicating a particular object,
rather than merely a general direction. To investigate this more
thoroughly, we tested the subjectspoint following to a target
located outside their visual field. This has been tested in other
studies by placing a third target behind the subject, which has
led to mixed results: dogs succeed in selecting the correct
target (Hare et al., 1998), but the gray seal (Shapiro et al.,
2003) and one of the two tested bottlenose dolphins failed to
do so (Pack & Herman, 2006). The lack of salience of this cue
may represent an additional difficulty, and could make this
setup a weak test of the ability of these animals to follow
pointing gestures to targets located outside their visual field.
Moreover, our limited knowledge of these species' visual field
makes it difficult to be sure that the target is in fact not visible
for them (Pack & Herman, 2006). To our knowledge, the
present study is the first in which barriers and distractors,
commonly used in studies on gaze-following (e.g., see
Tomasello, Hare, & Agnetta, 1999), are used in an object-
choice task on point following. We showed that only one sea
lion out of the three tested was successful from the very first
trial in following the pointing cue past a distractor target (i.e., a
similar item placed in front of him and directly accessible), to
targets located behind opaque screens that prevented him from
seeing the target at the moment of his choosing. The two other
subjects needed extra training as they began by attempting
different responses (i.e., touching the distractor or the
screens). Their subsequent success could thus be explained
in terms of reinforced learning: because these first attempts
were not rewarded, the sea lions continued to search, guided
only by the general direction from the pointing (i.e., left or
right), until finding the rewarded object behind the screen.
Considering these mixed results, we suggest that following
point gestures towards targets situated outside an animals
visual field remains a difficult task, even when the pointing
cuessaliency is improved (i.e., in comparison with studies
placing the target behind the animal).
The current experiment was designed to test the sea lions'
ability to exploit human pointing cues. This necessitated
preventing the animals from basing their responses on inad-
vertent cues instead of, or in addition to, the tested cues. For
example, some unintentional subtle changes in the caretakers
attitude could indicate to the tested sea lion that he is looking
at or moving to the correct target. In our experiment, the
greatest caution was taken to avoid any possible uncontrolled
cueing from the experimenter. For instance, the caretakers
were instructed to avoid any extra changes in their position,
movement, vocalizations, orfacial expression while providing
a pointing cue. Additionally, they repeated the cue if the sub-
ject did not respond every 2 s, totally independently of current
sea lion behavior. Of course, we cannot completely guarantee
that the sea lions could not perceive any subtle and incidental
cuing from the caretakers, including some that human ob-
servers may not perceive. In fact, this limitation is present in
many experiments that use pointing gestures. Future research
will have to be conducted, in sea lions as well as in other
species, in order to directly address this unintentional cues
account. One way would be to use an experimenter made
unaware of the animals behavior (e.g., by asking the experi-
menter acting as informant to close his eyes from the pointing
cue initiation until the final response of the animal, signaled to
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Author's personal copy
him by someone else). Successful animals in pointing exper-
iments involving such types of control would undoubtedly be
argued to be relying on human-given pointing cues to manage
the task. Nonetheless, the current study shows that sea lions
equal dogsperformance reported in previous studies using
similar experimental conditions.
In conclusion, these results obtained in a non-domesticated
species support the hypothesis of a transfer from conspecifics
directional and social cue reading skills to sensitivity to human
communicative cues (Smet & Byrne, 2013;Udell,Dorey,&
Wynne, 2010a). Spontaneous production of pointing cues can
be observed in the species tested successfully in joint-attention
tasks. Several reports have been made about production of
pointing gestures involving an extended arm without any for-
mal training in great apes, both in the wild (Hobaiter, Leavens,
&Byrne,2013; Inoue-Nakamura & Matsuzawa, 1997; Vea &
Sabater-Pi, 1998), and in captivity (Brakke & Savage-
Rumbaugh, 1996;Call&Tomasello,1994;Leavens&Hop-
kins, 1998). African elephants, which have been demonstrated
to successfully interpret human pointing without any prior
training, have been reported to regularly make prominent
trunk gestures (Smet & Byrne, 2013). But whether or not
those motions act in elephants as Bpoints^have to be explored
further. Other researchers demonstrated the ability in
dogs (Miklosi, Polgardi, Topal, & Csanyi, 2000)and
captive dolphins (Xitco, Gory, & Kuczaj, 2001,2004)
to spontaneously indicate the location of a hidden food
item by aligning the axis of their body with a container,
while producing gaze-alternations between its owner (or
caretaker) and the object.
To our knowledge, no such experimental studies had yet
been conducted in California sea lions. However, specific fea-
tures of their ecology and social behaviors would make sensi-
tivity to gaze and body-line orientation of conspecifics highly
adaptive for this species. Their foraging behavior in particular,
which seems to involve precise coordination of high-speed
directional movements among large groups of conspecifics,
appears to be precisely the sort of behavior that would lead
to such sensitivity. As has been suggested for some of the
other species tested successfully in pointing studies, their abil-
ity to exploit varied human communicative cues may be due
to the generalization of conspecific cue reading skills to this
interspecific context (Pack & Herman, 2006, Smet & Byrne,
2013; Shapiro et al., 2003). Smet & Byrne (2013) posed the
hypothesis that some speciesnative ability in interpreting
social cues may have contributed to their effective use by
man, regardless of whether or not domestication has taken
place, with the notable example of elephants. Although sea
lions do not have such a long history of close cooperation with
humans, according to Smet & Byrnes hypothesis (2013), the
extensive use of sea lions nowadays in dolphinariums for
shows and educational programs could be due in part to their
ability to exploit social cues.
In addition to this ecological account for the current find-
ings, it may be interesting to consider the potential influence
of daily interactions with humans. Lyn et al. (2010) have
shown that chimpanzees and bonobos raised in a socio-
linguistically rich environment performed much better in
exploiting human pointing gestures than chimpanzees raised
in standard laboratory housing. In the same way, stray dogs
living in shelters perform very poorly compared to pet dogs
(Udell, Dorey, & Wynne, 2010b), and some recent experimen-
tal data suggest in young pet dogs an inability to exploit such
gestures (Dorey, Udell, & Wynne, 2010), contrary to previous
findings (Hare, Brown, Williamson, & Tomasello, 2002).
Like the majority of the tested marine mammals, the sea lions
tested here had undergone training and participated in public
shows, during which they focus their attention on their care-
takers gestures in order to detect his/her commands. Similar
to pet dogs and primates raised in a socio-linguistically rich
environment, sea lions would have been highly attuned to
human gestural cues in these previous experiences because
of their frequent association with food rewards and social
praise (Elgier, Jakovcevic, Mustaca, & Bentosela, 2012;Pra-
to-Previde, Marshall-Pescini, & Valsecc, 2008). This is sup-
ported by observations in a young gray seal born in the wild
who was trained to follow explicit pointing gesture; while he
was able to respond appropriately to different types of points,
he did not spontaneously exploit more subtle cues such as
head orientation (Shapiro et al., 2003). The results of the pres-
ent experiment support both an ecological and a human-
socialization account of some undomesticated speciesability
to use human pointing gestures. Further exploration of Cali-
fornian sea lionsbehavior in the wild as well as additional
experiments would be needed to disentangle between the two
hypotheses (for example, comparative studies between
human-socialized and wild individuals).
In summary, we have provided evidence that the ability to
exploit varied human pointing gestures can emerge in human-
socialized Californian sea lions, at least when these are per-
formed by their familiar caretakers. However, potential ex-
ploitation by the sea lions of unintended cues that the care-
takers might have provided instead of, or in addition to, the
tested pointing cues still has to be assessed. We suggest that
they understand to some extent the referential property of the
pointing gesture, because they were able to follow a precise
linear vector along the pointing arm to a particular object
among several objects located in the same general direction.
But saying that they understand pointing as referring to a
particular object, place, or event, does not assume that they
comprehend in another social agent the aspect of looking at
and/or indicating an object as having a mental experience
about this object. For instance, 3-year-old children can choose
the correct cup (i.e., the one pointed to by the experimenter),
but cannot explain why they have done so (Povinelli &
deBlois, 1992). This supports the idea that no theory of mind
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(i.e., the ability to interpret the behavior of oneself or others in
terms of internal states as knowledge, beliefs, intents, etc.) is
necessary to explain sea lions' current results. Further investi-
gations would have to be made about the ecological back-
ground and the histories of learning underlying the sophisti-
cated social cue reading skills observed in studies on joint-
attention in some non-human animals, and their relations with
the potential development of high-level representations in
both humans and non-human animals.
Acknowledgments We are grateful to the curator of Parc Asterix,
Birgitta Mercera, and the caretakers, Caroline Lévy, Stéphane Lecki,
Daphné Vergon, Juana Serrano and Bastien Servière, for acting as infor-
mants, and to all the dolphinarium staff for their gracious collaboration.
We also thank Celeste Mason, Ralitsa Todorova and Isabella Clegg for
improving the English in the manuscript. Special thanks to Gilles Gheusi
who kindly collaborated on the figure designs. This experiment complies
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... Pointing is a form of social referencing and is an important stage in child development (Behne, Carpenter, & Tomasello, 2005;Grassmann & Tomasello, 2010;Hodges, Özçalışkan, & Williamson, 2018;Thoermer & Sodian, 2001). Comparative cognition research over the past 20 years has investigated the development of similar point-following behaviors in humans and nonhuman animals (Call, Hare, & Tomasello, 1998;Hall, Udell, Dorey, Walsh, & Wynne, 2011;Kaminski, Riedel, Call, & Tomasello, 2005;Malassis & Delfour, 2015;Maros, Gácsi, & Miklósi, 2008;Miklósi, Pongrácz, Lakatos, Topál, & Csányi, 2005;Smet & Byrne, 2013;Hall et al., 2011). Such research has focused on domestic dogs, as pet dogs generally perform well on point-following tasks (Lazarowski & Dorman, 2015;Miklósi, Polgárdi, Topál, & Csányi, 1998;Udell, Dorey, & Wynne, 2008). ...
... Further, other domesticated species such as goats (Kaminski et al., 2005), horses (Maros et al., 2008), and cats (Miklósi et al., 2005) have all shown success on point following. Point following, however, does not appear limited to domesticated species, as nondomesticated species such as bats (Hall et al., 2011), elephants (Smet & Byrne, 2013), and sea lions (Malassis & Delfour, 2015) can perform well on point-following tasks. ...
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Pet dogs are known to be responsive to human pointing gestures, but shelter dogs have repeatedly demonstrated poor abilities to follow human pointing, although they can be explicitly trained quickly. This study evaluated the time course in which shelter dogs learn to follow points without explicit training, when given typical interactions with humans. In a longitudinal evaluation, the development of point following was tracked in seven shelter dogs in a training program (enriched human exposure), seven dogs in a traditional shelter (control population), and evaluated once in pet dogs. Twice a week for 6 weeks, shelter dogs’ point-following performance was evaluated in 10 probe trials in which an experimenter pointed to one of two containers equidistant from the dog. To avoid direct training, dogs were given a treat for approaching and touching either container; although correct responses were recorded for touching the pointed-towards container within 30 s. Pet dogs were tested in only one session. All shelter dogs initially showed the expected poor performance. However, enriched shelter dogs receiving enriched human exposure showed significant improvements reaching an identical performance to pet dogs within 7 weeks. In comparison, shelter dogs under standard conditions showed an initial improvement, but performance reached asymptote close to chance levels and lower than that of enriched dogs or pet dogs. Together, these results suggest that enriched experiences with humans, typical of pet dogs, is sufficient for dogs to learn to follow points without explicit training.
... The capacity to use human behavioural cues has been demonstrated in numerous non-human species and has remained the focus of extensive research over the last decade (e.g., gulls, Larus argentatus: Goumas et al. 2020; dogs, Canis lupus familiaris: Bhattacharjee et al. 2020; elephants, Elephas maximus: Ketchaisri et al. 2019;goats, Capra hircus: Nawroth et al. 2020 Malassis and Delfour 2015). A widely used method for investigating this capacity is the two-way object-choice paradigm, where subjects are presented with a choice between two containers, only one hiding a food reward, and the identity of the correct container is indicated through experimenter-given cues (such as gazing and pointing, e.g., Clark et al. 2019;Danel et al. 2022a, b). ...
The capacity to follow human cues provides animals with information about the environment and can hence offer obvious adaptive benefits. Most studies carried out so far, however, have been on captive animals with previous experience with humans. Further comparative investigation is needed to properly assess the factors driving the emergence of this capacity under natural conditions, especially in species that do not have longstanding interactions with humans. Wild brown skuas (Catharacta antarctica ssp. lonnbergi) are non-neophobic seabirds that live in human-free habitats. In test 1, we assessed this species’ capacity to use human behavioural cues (i.e., pecking at the same object previously picked up and lifted by a human experimenter) when the items presented were food objects: anthropogenic objects (wrapped muffins) and natural-food-resembling objects (plaster eggs). In test 2, we examined the response of another skua population towards non-food objects (sponges). Although all skuas in test 1 pecked at the objects, they pecked significantly more at the same previously handled items when they resembled natural food (plaster eggs). Most skuas in test 2, however, did not approach or peck at the non-food objects presented. Our results lead us to suggest that the use of human behavioural cues may be influenced by skuas’ foraging ecology, which paves the way to further field studies assessing whether this capacity is directed specifically towards food objects and/or develops after previous interaction with humans.
... They are sociable, demonstrate complex cognitive abilities, and are easily trainable (Brando, 2010), which is valuable when setting up cognitive bias tests. California sea lions (Zalophus californianus) are gregarious animals living in colonies with well-known abilities in memory, attention, and abstraction (Arkwright et al., 2016;Kastak & Schusterman, 2002;Malassis & Delfour, 2015;Penel & Delfour, 2014) and, like bottlenose dolphins, are readily trainable (Schusterman, 1981). ...
In the last 30 years, concerns about animal emotions have emerged from the general public but also from animal professionals and scientists. Animals are now considered as sentient beings, capable of experiencing emotions such as fear or pleasure. Understanding animals’ emotions is complex and important if we want to guarantee them the best care, management, and welfare. The main objectives of the paper are, first, to give a brief overview of various and contemporary assessments of emotions in animals, then to focus on particular zoo animals, that is, marine mammals, since they have drawn a lot of attention lately in regards of their life under professional care. We discuss here 1 approach to monitor their emotions by examining their laterality to finally conclude the importance of understanding animal emotion from a holistic welfare approach.
... In the communication scale, all species performed equally well, suggesting that all species can make use of socio-visual cues given by others. This result is in line with those of several other studies showing the ability to use social-visual cues presented by a human demonstrator in object-choice experiments in birds (Schmitt, Pankau & Fischer, 2012), aquatic mammals (sea lions: Malassis & Delfour, 2015;dolphins: Tschudin et al., 2001), domestic animals (dogs: Kaminski et al., 2005Miklósi et al., 1998);pigs: Nawroth, Ebersbach & von Borell, 2016;goats: Wallis et al., 2015), as well as other primates (Anderson & Mitchell, 1999;Itakura, 1996). ...
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Primates have relatively larger brains than other mammals even though brain tissue is energetically costly. Comparative studies of variation in cognitive skills allow testing of evolutionary hypotheses addressing socioecological factors driving the evolution of primate brain size. However, data on cognitive abilities for meaningful interspecific comparisons are only available for haplorhine primates (great apes, Old-and New World monkeys) although strepsirrhine primates (lemurs and lorises) serve as the best living models of ancestral primate cognitive skills, linking primates to other mammals. To begin filling this gap, we tested members of three lemur species (Microcebus murinus, Varecia variegata, Lemur catta) with the Primate Cognition Test Battery, a comprehensive set of experiments addressing physical and social cognitive skills that has previously been used in studies of haplorhines. We found no significant differences in cognitive performance among lemur species and, surprisingly, their average performance was not different from that of haplorhines in many aspects. Specifically, lemurs' overall performance was inferior in the physical domain but matched that of haplorhines in the social domain. These results question a clear-cut link between brain size and cognitive skills, suggesting a more domain-specific distribution of cognitive abilities in primates, and indicate more continuity in cognitive abilities across primate lineages than previously thought.
... Recently, Malassis and Delfour (2015) showed in a two-alternative distal object-choice task that four sea lions (Zalophus californianus) with previous experience with human pointing responded at or near ceiling levels to direct momentary pointing with and without target gazing, and three of the four responded above chance to long cross-body pointing, elbow pointing, and foot pointing. A second experiment performed with the three more enculturated sea lions tested their understanding of the geometry of human pointing cues using a similar configuration of aligned near and far objects on each side of an informant, as was employed by Lakatos et al. (2012) with dogs. ...
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... In Miklósi and Soproni's (2006) review, two aquatic carnivoran species had the highest rate of success in spontaneous use of human points of all taxa (bottlenose dolphins, Pack & Herman, 2004, and see also Xitco, Gory, & Kuczaj, 2001; and a grey seal, Shapiro, Janik, & Slater, 2003). A recent report of successful use of points by Californian sea lions continues that trend (Malassis & Delfour, 2015). Among the social hunters, there is much more evidence. ...
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The great increase in the study of dog cognition in the current century has yielded insights into canine cognition in a variety of domains. In this review, we seek to place our enhanced understanding of canine cognition into context. We argue that in order to assess dog cognition, we need to regard dogs from three different perspectives: phylogenetically, as carnivoran and specifically a canid; ecologically, as social, cursorial hunters; and anthropogenically, as a domestic animal. A principled understanding of canine cognition should therefore involve comparing dogs’ cognition with that of other carnivorans, other social hunters, and other domestic animals. This paper contrasts dog cognition with what is known about cognition in species that fit into these three categories, with a particular emphasis on wolves, cats, spotted hyenas, chimpanzees, dolphins, horses, and pigeons. We cover sensory cognition, physical cognition, spatial cognition, social cognition, and self-awareness. Although the comparisons are incomplete, because of the limited range of studies of some of the other relevant species, we conclude that dog cognition is influenced by the membership of all three of these groups, and taking all three groups into account, dog cognition does not look exceptional.
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Animals of different taxa can read and respond to various human communicative signals. Such a mechanism facilitates animals to acquire social information and helps them react in a context-dependent manner. Dogs have garnered extensive attention owing to their socio-cognitive skills and remarkable sensitivity to human social cues. For example, dogs readily respond to different human pointing gestures to locate hidden food rewards. However, a general inclination towards testing highly socialized pet dogs has resulted in a dearth of information on other sub-populations of dogs. Free-ranging dogs are one of the least socialized dog populations yet exhibit point-following behaviour flexibly. As a consequence of frequent negative interspecific interactions, they are typically wary of unfamiliar humans; thus, contextual recognition of human actions is paramount for these dogs to avoid potential conflict. However, the mechanisms influencing their point-following behaviour remain unidentified. We asked to what extent the informative-deceptive nature of cues and positive human interactions influence the interspecific communicative behaviour of these minimally socialized dogs. Using a point-following experiment with a 2 × 2 design, we focused on adult free-ranging dogs’ behavioural adjustments. Dogs were randomly divided into two groups, with only one receiving brief social petting. Further, informative and deceptive cues were given to separate subsets within each group. Our findings suggest that brief social petting strongly affects the likelihood of free-ranging dogs’ point-following tendencies. Dogs who received petting followed the pointing cues regardless of their informative or deceptive nature, whereas dogs who did not receive petting discriminated between informative and deceptive pointing. This study highlights the contribution of positive human interaction and informative-deceptive quality of cues in modulating the behavioural responses of free-ranging dogs in an interspecific communicative context.
This chapter contextualizes the dog-human relationship in the dog's origin as a scavenger on the fringes of human settlements over 15,000 years ago. It then reviews the evidence for unique evolved cognitive structures in dogs that could explain their success in a human-dominated world. Failing to find evidence of unique human-like social-cognitive capacities I then review uncontroversial facts of dogs' basic behavioral biology, including reproductive and foraging behavior and, particularly, affiliative and attachment-related behaviors. This leads to consideration of dogs' social behavior, both conspecific and toward other species, especially humans. I draw attention to a seldom-noted apparent contradiction between dogs' stronger affectional bonds toward humans than toward members of their own species. Dogs' social groups also show steeper social hierarchies accompanied by more behaviors indicating formal dominance than do other canid species including wolves. I resolve this contradiction by proposing that dogs' intense sensitivity to social hierarchy contributes to their willingness to accept human leadership. People commonly control resources that dogs need and also unknowingly express behaviors which dogs perceive as formal signs of dominance. This may be what Darwin was referring to when he endorsed the idea that a dog looks on his master as on a god. Whatever the merits of this idea, if it serves to redirect behavioral research on dogs in human society more toward the social interactions of these species in their diverse forms of symbiosis it will have served a useful function.
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Primates have relatively larger brains than other mammals even though brain tissue is energetically costly. Comparative studies of variation in cognitive skills allow testing of evolutionary hypotheses addressing socioecological factors driving the evolution of primate brain size. However, data on cognitive abilities for meaningful interspecific comparisons are only available for haplorhine primates (great apes, Old- and New World monkeys) although strepsirrhine primates (lemurs and lorises) serve as the best living models of ancestral primate cognitive skills, linking primates to other mammals. To begin filling this gap, we tested members of three lemur species (Microcebus murinus, Varecia variegata, Lemur catta) with the Primate Cognition Test Battery, a comprehensive set of experiments addressing physical and social cognitive skills that has previously been used in studies of haplorhines. We found no significant differences in cognitive performance among lemur species and, surprisingly, their average performance was not different from that of haplorhines in many aspects. Specifically, lemurs overall performance was inferior in the physical domain but matched that of haplorhines in the social domain. These results question a clear-cut link between brain size and cognitive skills, suggesting a more domain-specific distribution of cognitive abilities in primates, and indicate more continuity in cognitive abilities across primate lineages than previously thought.
Domestic dogs, Canis familiaris, are highly responsive to human communicative cues and can utilize gestures, such as pointing, to locate hidden rewards. This ability is thought to be the product of both genetic and behavioural selection, allowing dogs to adapt to life with humans. Dogs' responsiveness to human gestures can also lead to suboptimal choices when dogs readily follow misleading cues despite directly contradicting perceptual information such as odour cues. However, this bias likely reflects pet dogs' enculturation with humans and thus may not be representative of other populations of dogs. We investigated the ability of young dogs in training for explosives detection (N ¼ 77) to locate a hidden reward using olfactory cues when presented in conflict with a deceptive communicative gesture in an object-choice task. We assessed performance at 3, 6 and 11 months of age using both cross-sectional and longitudinal designs. We found that, contrary to previous findings with pet dogs, responsiveness to human pointing decreased with age, whereas the ability to locate the reward by scent increased. Furthermore, a lack of susceptibility to deceptive social cues was predictive of future success as a detection dog. These findings further indicate the influence of ontogenetic effects on canine social cognition and demonstrate potential applications for the identification of suitable detection dogs.
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Many studies document the domestic dogs’ responsiveness to human gestures. Reports of success on human guided tasks have led to evolutionary hypotheses that set dogs’ skills apart from other species, including other canids, in terms of their social cognition and comprehension of human communicative stimuli. However, until recently the range of other species tested and the availability of studies using equivalent testing methods between different species and groups have been limited, making it difficult to interpret cross-species comparisons. Here we demonstrate that humansocialized wolves are not only capable of responding to points made with the arm and hand, but are sensitive to a wide range of human gestures when given the opportunity to utilize such gestures in an object-choice task. Claims that domestic dogs are unique in their ability to respond to diverse novel stimuli may be in part due to the absence of data for the same range of gestures in other species. We also provide the first evidence that human-socialized coyotes have the capacity to utilize a human point to locate a target; further demonstrating that domestication is not a prerequisite for canid responsiveness to human actions, and that socialization and life experience are likely more important predictors of success.
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The ability of adolescent chimpanzees and 2- and 3-year-old children to use pointing gestures to locate hidden surprises was examined in two experiments. The results revealed that although young 2-year-old children appeared to have no difficulty extracting referential information from a pointing gesture (independent of gaze or distance cues) and spontaneously using it to search in specific locations, adolescent chimpanzees appeared to rely on cueconfiguration and distance-based rules. Thus, although these chimpanzees were trained to respond appropriately to the pointing gestures of a human by searching in a particular location, this ability did not easily generalize to situations in which the distance between the pointing hand and the location were more distal. Furthermore, even those chimpanzees that were able to generalize in this fashion appeared to use distance-based cues, not ones based on an appreciation of the internal attentional focus or mental referent of the experimenter as indicated by his pointing gesture.
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Since the observations of O. Pfungst the use of human-provided cues by animals has been well-known in the behavioural sciences ("Clever Hans effect"). It has recently been shown that rhesus monkeys (Macaca mulatta) are unable to use the direction of gazing by the experimenter as a cue for finding food, although after some training they learned to respond to pointing by hand. Direction of gaze is used by chimpanzees, however. Dogs (Canis familiaris) are believed to be sensitive to human gestural communication but their ability has never been formally tested. In three experiments we examined whether dogs can respond to cues given by humans. We found that dogs are able to utilize pointing, bowing, nodding, head-turning and glancing gestures of humans as cues for finding hidden food. Dogs were also able to generalize from one person (owner) to another familiar person (experimenter) in using the same gestures as cues. Baseline trials were run to test the possibility that odour cues alone could be responsible for the dogs' performance. During training individual performance showed limited variability, probably because some dogs already "knew" some of the cues from their earlier experiences with humans. We suggest that the phenomenon of dogs responding to cues given by humans is better analysed as a case of interspecific communication than in terms of discrimination learning.
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Research on the comprehension of human-given cues by domesticated as well as non-domesticated species has received considerable attention over the last decade. While several species seem to be capable of utilizing these cues, former work with domestic pigs (Sus scrofa domestica) has shown inconclusive results. In this study, we investigated the use of human-given cues in an object choice task by young domestic pigs (N = 17; 7 weeks of age) who had very limited human contact prior to the experiments. Subjects had to choose between two bowls of which only one was baited with a reward. Over the course of five experiments, pigs were able to use proximal and, with some constraints, also distal pointing cues presented in both a dynamic-sustained and in a momentary manner. When the experimenter was pointing from the incorrect bowl towards the correct one, most of the subjects had problems solving the task-indicating that some form of stimulus/local enhancement affected pigs' decision making. Interestingly, pigs were able to utilize the body and head orientation of a human experimenter to locate the hidden reward but failed to co-orient when head or body orientation of the experimenter was directed into distant space with no bowls present. Control trials ruled out the possibility that other factors (e.g. odour cues) affected subjects' choice behaviour. Learning during experiments played a minor role and only occurred in three out of twelve test conditions. We conclude that domestic pigs, even at a very young age, are skilful in utilizing various human-given cues in an object choice task-raising the question whether pigs only used stimulus/local enhancement and associative learning processes or whether they were able to comprehend the communicative nature of at least some of these cues.
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Recent intense interest in social cognition in dol- phins reflects findings that wild dolphins live in com- plex societies that rely on individual recognition, a protracted period of development, coalition forma- tion, and cooperative, as well as competitive, social behaviors. Laboratory studies have revealed a host of cognitive skills that can support such complex behaviors—for example, broad imitative abilities, abilities to understand another's indicative cues, and spontaneous use of pointing to communicate with human companions. Joint attention is recognized as a key element of social cognition that extends from simply following another's gaze to using pointing or gazing cues of another to select objects or locations. Studies of bottlenose dolphins (Tursiops truncatus) have revealed that they understand (1) human-given direct and cross-body points; (2) human-given dynamic and static pointing and gazing cues within object-choice tasks; (3) the geometry of pointing cues; (4) the referential character of pointing and gazing cues; (5) sequences of direct and/or cross- body points that were instructions to transport one object to another; (6) how to produce pointing cues and the importance of audience attention; and (7) possibly the belief state of another that is engaged in a joint attention task. The evidence suggests that joint attention skills in dolphins are robust and to some degree symmetric across comprehension and production. Comparative analyses indicate that in some areas of joint attention, abilities of dolphins exceed the demonstrated skills of apes. Possibly, a dolphin's capacity for joint attention may be related to the adaptive benefits of being able to attend to the focus of another dolphin's echolocation beam in conjunction with a sophisticated social structure dependent on attention to others.
Domestic dogs have proved to be extremely successful in finding hidden food following a series of human social cues such as pointing (an extended hand and index finger indicating the location of the reward), or body position, among many other variants. There is controversy about the mechanisms responsible for these communicative skills in dogs. On the one hand, a hypothesis states that dogs have complex cognitive processes such as a theory of mind, which allow them to attribute intent to the human pointing gesture. A second, more parsimonious, hypothesis proposes that these skills depend on associative learning processes. The purpose of this paper is to provide data that may shed some light on the discussion by looking into two learning processes by using an object choice task: the effect of interference between stimuli on the preference for human social cues and the effect of generalization of the response to novel human social stimuli. The first study revealed that previous training using a physical cue (container location) may hamper the learning of a novel human social cue (distal cross-pointing). The results of the second study indicated stimulus generalization. Dogs learnt a novel cue (distal cross-pointing) faster due to previous experience with a similar cue (proximal pointing), as compared to dogs confronted by a less similar cue (body position) or dogs with no previous experience. In sum, these findings support the hypothesis about the important role of associative learning in interspecific communication mechanisms of domestic dogs.
Factors influencing the abilities of different animals to use cooperative social cues from humans are still unclear, in spite of long-standing interest in the topic. One of the few species that have been found successful at using human pointing is the African elephant (Loxodonta africana); despite few opportunities for learning about pointing, elephants follow a pointing gesture in an object-choice task, even when the pointing signal and experimenter's body position are in conflict, and when the gesture itself is visually subtle. Here, we show that the success of captive African elephants at using human pointing is not restricted to situations where the pointing signal is sustained until the time of choice: elephants followed human pointing even when the pointing gesture was withdrawn before they had responded to it. Furthermore, elephants rapidly generalised their response to a type of social cue they were unlikely to have seen before: pointing with the foot. However, unlike young children, they showed no sign of evaluating the 'rationality' of this novel pointing gesture according to its visual context: that is, whether the experimenter's hands were occupied or not.
How animals gain information from attending to the behavior of others has been widely studied, driven partly by the importance of referential pointing in human cognitive development [1-4], but species differences in reading human social cues remain unexplained. One explanation is that this capacity evolved during domestication [5, 6], but it may be that only those animals able to interpret human-like social cues were successfully domesticated. Elephants are a critical taxon for this question: despite their longstanding use by humans, they have never been domesticated [7]. Here we show that a group of 11 captive African elephants, seven of them significantly as individuals, could interpret human pointing to find hidden food. We suggest that success was not due to prior training or extensive learning opportunities. Elephants successfully interpreted pointing when the experimenter's proximity to the hiding place was varied and when the ostensive pointing gesture was visually subtle, suggesting that they understood the experimenter's communicative intent. The elephant's native ability in interpreting social cues may have contributed to its long history of effective use by man.
Referential pointing is important in the development of language comprehension in the child and is often considered a uniquely human capacity. Nonhuman great apes do point in captivity, usually for a human audience, but this has been interpreted as an interaction pattern learned from human caretakers, not indicative of natural deictic ability. In contrast, spontaneous pointing for other apes is almost unknown among wild ape populations, supporting doubts as to whether apes naturally have any capacity to point referentially. Here the authors describe and illustrate 4 cases of gestures by juvenile chimpanzees in the Sonso chimpanzee community in Budongo, Uganda, that, at some level, may appear to be deictic and referential. The authors discuss the possible reasons why chimpanzees, if they possess a capacity for referential pointing, do not use it more frequently. (PsycINFO Database Record (c) 2013 APA, all rights reserved).