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Sciknow Publications Ltd. ABC 2014, 1(4)434-445
Animal Behavior and Cognition DOI: 10.12966/abc.11.01.2014
©Attribution 3.0 Unported (CC BY 3.0)
Are California Sea Lions (Zalophus californianus) Sensitive
to the Attentional State of their Caretakers?
Marie Penel1* and Fabienne Delfour2
1Université de Rennes
2 Parc Asterix
*Corresponding author (Email: marie-penel@orange.fr)
Citation – Penel, M., & Delfour, F. (2014). Are California sea lions (Zalophus californianus) sensitive to the
attentional state of their caretakers? Animal Behavior and Cognition, 1(4), 434-441. doi: 10.12966/abc.11.01.2014
Abstract - Human-animal relations appear in various contexts (homes, farms, zoos, aquatic parks, etc.) possibly
favoring the emergence of the ability to understand heterospecific communication signals in several species. Studies
show that dogs (Canis familiaris) have developed the ability to attribute attention to humans, reading their body,
head and gaze cues. Horses (Equus caballus) and other species including African gray parrots (Psittacus erithacus)
show this ability too. Here, we asked if California sea lions (Zalophus californianus) can discriminate the attentional
state of their caretakers. Four sea lions were tested in three increasingly complex experiments requiring them to
make a choice between an attentive versus an inattentive caretaker. The first test asked whether sea lions could
attribute attention to a human facing them versus facing away. In the second test, the caretaker’s head orientation
towards the sea lion served as the attentional cue. In the final test, the inattentive caretaker wore dark sunglasses.
The results were heterogeneous and showed a higher rate of success than failure in the test 1, but the opposite in test
2. The results in the test 3 were not significant. Furthermore, the latency measures suggested that the subjects did not
understand the tasks. It therefore appears that in the situation used here sea lions mainly focused their attention on
the experimenter’s body orientation; the head did not seem to be a pertinent cue.
Keywords - Attention, Choice task, Gaze, Sea lions, Zalophus californianus
Primatologists Premack and Woodruff (1978) specified theory of mind as the ability to attribute
mental state to oneself and others, i.e., thinking about a parameter which is not visible and also predicting
the future acts of others. One such mental state is attention, as in paying attention to someone. A human
child acquires the ability to attribute attention between 0 and 2 years old (Baron-Cohen, 1994). This
development occurs in the context of the intraspecific relation between the child and people around him.
The question arises whether similar phenomena occur within interspecific relations. Numerous human
societies include nonhuman animals, and not only for food or protection; for example most of our dogs
(Canis familiaris) and cats (Felis silvestris catus) are chosen for their companionship (Miklósi, Polgárdi,
Topál, & Csányi, 1998). Human-animal relations appear in various contexts: farms, zoos, aquatic parks,
etc. These contexts could have favored the emergence of the ability to understand heterospecific
communication signals in several species.
Humans have become social partners for dogs over time, and the latter have learned to
discriminate various cues of human attention including body, facial and visual cues (Kaminski, Bräuer,
Call, & Tomasello, 2009; Riedel, Schumann, Kaminski, Call, & Tomasello, 2008, as cited in Udell,
Dorey, & Wynne, 2010; Soproni, Miklósi, Topál, & Csányi, 2001). Dogs are able to use these human
cues to solve an object choice task, to localize or beg for food (Bräuer, Call, & Tomasello, 2004; Gásci,
Penel & Delfour 435
Miklósi, Varga, Topál, & Csányi, 2004; Miklósi et al., 1998; Soproni et al., 2001; Virányi, Topál, Gásci,
Miklósi, & Csányi, 2004). Some nonhuman primates, for example gorillas (Gorilla gorilla) have
demonstrated this ability too: they used body cues, but also focused on a human’s gaze to make their
choice (Bania & Stromberg, 2013). Orangutans (Pongo pygmaeus) understand human head cues
(Tempelmann, Kaminski, & Liebal, 2011), and cotton-top tamarins (Saguinus oedipus oedipus) use
human body and gaze cues to discriminate human attention (Santos & Hauser, 1999). Even some birds
such as African gray parrots (Psittacus erithacus) can discriminate human gaze cues (with head
orientation) (Giret, Miklósi, Kreutzer, & Bovet, 2009) and are able to use them in the same choice task as
primates do (Péron, Chardard, Nagle, & Bovet, 2011). Bottlenose dolphins’ (Tursiops truncatus) pointing
and monitoring behaviors are linked to human receiver’s attentional behavior (Xitco, Gory, & Kuczaj,
2004). Horses are also able to discriminate human attention using body, head and gaze cues (Proops &
McComb, 2010). The horse “Clever Hans” could “solve” simple equations by discriminating various
unintentional body cues sent by the audience, such as breathing, when the owner voiced numbers.
According to some authors (Buttelman, Carpenter, Call, & Tomasello, 2007; Call, 2001;
Kaminski, Riedel, Call, & Tomasello, 2005; Kaminski et al., 2009), the ability to understand
heterospecific communication signals could be due to the species enculturation or domestication.
However, Udell, Dorey, & Wynne (2011) demonstrated sensitivity to human attentional state in some
non-domesticated animals. Nonetheless there is general agreement that proximity between animals and
humans could have contributed to several species’ ability to infer human mental states.
In some environments (e.g., zoos, farms, dolphinaria, etc.), animals live close to humans.
California sea lions (Zalophus californianus) are commonly housed in zoos or amusement parks. These
pinnipeds naturally live in the North Pacific and belong to the family Otariidae. They can weigh as much
as 390 kg and can be up to 2.20 m tall. They are sexually dimorphic, with males being bigger than
females, reach sexual maturity between 4 and 5 years of age, and live about 15 years. These animals
congregate during the breeding season, forming large herds subdivided into harems, composed of one
male and 3 to 40 females. Males defend their harem aggressively. Young animals stay close to their
mother until they are at least 5 months old, learning to recognize them using smell, sight and
vocalizations (Riedman, 1990). There have been studies of these animals’ anatomical and functional
characteristics (Schusterman, 1969; Wells, Irwin, & Hepper, 2006) but few behavioral studies have been
conducted, particularly regarding their interactions with humans.
In this study, we wanted to know if California sea lions (called “sea lions” here) understand
human attentional signs, and which signs are pertinent for them. We conducted three experiments using
three different attentional cues used in previous studies (Proops & McComb, 2010). In the first test, one
human was facing the subjects (attentive) while another was facing away (inattentive). In the second test,
the human’s head orientation towards the sea lion was the attentional cue. In the final test the inattentive
caretaker wore opaque sunglasses.
Method
Subjects
The four California sea lions (Zalophus californianus) tested here all born and bred under human
care. They were 4 males: Santo (7 years old), Smack (6), Gonzo (4) and Kaï (3), living at Parc Asterix
Delphinarium (France). Their enclosure measured 12 x 31 m with a 5 x 15 m outdoor pool and a 3 x 5 m
indoor enclosure. They were fed with herring, mackerel, capelin and squid distributed in 6 daily rations
including one given during a session without training or show. The sea lions were familiar with a range of
communication signs used by their caretakers and were trained by each team member. The study took
place during regular training sessions.
Penel & Delfour 436
General procedure
Three familiar caretakers participated in each trial: one caretaker (A) stood by the sea lion and
gave him the command “to go to a person” which allows the sea lion to leave caretaker A and go to
caretakers B or C who, about 2 m from each other, stood in front of the sea lion at a distance of 4 m
(Figure 1). Following Proops and McComb’s (2010) procedure, we started with a warm-up phase with
two attentive caretakers to show their attentional state, caretakers B and C looked at the subject until
caretaker A sent him to make his choice. After the subject was sent, caretakers B and C did not look at
him as he moved to avoid influencing his response (except for experiment 3). The choice was considered
made when the subject stood close to one of the caretakers. Only the attentive trainer gave a vocal and/or
tactile reward; the inattentive experimenter did not move or look at the subject. Finally, the sea lion was
called back by caretaker A. A then gave him a few commands and rewarded him with food. We used
vocal rewards rather than food rewards in order to prevent sea lions learning to look for food instead of
signs of attention. A Samsung ® 65X Intelli-Zoom video camera was used to record the experiments and
the videos were analyzed with Windows Live Movie Maker®.
Figure 1. Pictures of the different postures used in this study. For each picture, the attentive caretaker is on the left. Picture 1
represents the body orientation, pictures 2.1 and 2.2, the head orientation and picture 3, the eye visibility.
Shaping phase 1. During this phase the trainers desensitized the subjects to the new procedures.
By facing and looking at the sea lion, caretakers B and C were both showing the “attentive state.” First,
the reward was only vocal and/or tactile to test different places in the enclosure and avoid bias (5 days)
(e.g., confusion arising from the fact that the signs for “go to a person” and “go to the water” were
similar). Then, caretakers B and C alternated positions and status (attentive vs. inattentive) and for 3 days
Penel & Delfour 437
they added food reward to their vocal/tactile reward. We did not want the sea lions to learn a route or a
particular location. Finally, neither caretaker B nor C rewarded the subject with fish (2 days); only
caretaker A did so. From this phase, the caretakers wore sunglasses on their head to habituate subjects for
experiment 3. This phase lasted for 10 days and subjects received variable numbers of trials (Santo: 47;
Smack: 38; Gonzo: 42 and Kaï: 36) depending on availability.
The statistical analysis of the choice of any of the three caretakers, or side (left/right) was non-
significant for each sea lion (Binomial, p > 0.05).
Statistical analysis
For each experiment and each subject, comparisons of the choice of the attentive / inattentive
caretaker (Exp. 1, face forward vs. back turned; Exp. 2, face forward/body turned vs. face turned/body
forward and face forward/body forward vs face turned/body forward; Exp. 3, eyes open vs. sunglasses)
and the choice of caretakers and side (left/right) were analyzed with a binomial test. Latency (time
between the subjects leaving caretaker A and choosing caretaker B or C), and the duration of the behavior
“looks at caretakers” before choosing were analyzed using the Mann-Whitney-U test. Inter-individual
variation and daily patterns of response rates were analyzed using Chi Square tests, but for all
experiments, they were non-significant, and there was no bias for any subject selecting a specific
caretaker (p > 0.05).
Experiment 1: Body Orientation
Face forward vs. back turned
Procedure. During this test, two caretakers were in front of the subject with one of them looking
forward (“attentive state”) and the other with his/her back facing the subject (inattentive state). Each
subject received 42 trials.
Results. The four sea lions successfully passed the first test (Test 1) (N = 168, k = 121, p < 0.01;
Santo: N = 42, k = 28, p < 0.05; Gonzo: N = 42, k = 29, p < 0.05; and Kaï: N = 42, k = 30, p < 0.05;
Smack: N = 42, k = 34, p < 0.01) (Figure 2). They also looked significantly longer at the attentive
caretaker than the inattentive one before choosing (W = 16926.5, p < 0.001).
However, the sea lions did not choose the attentive caretaker faster than the inattentive one (p >
0.05) except for Smack, who took longer to go to the attentive caretaker (Table 1) (W = 51.5, p < 0.02).
Finally, three sea lions preferentially chose a particular side: left for Santo (N = 42, k = 32, p <
0.001) and Kaï (N = 42, k = 28, p < 0.05), right for Gonzo (N = 42, k = 31, p < 0.01).
Experiment 2: Head Orientation
Part 1: Face forward/body turned vs. face turned/body forward
The attentive caretaker turned her head to face the sea lion with her body turned 90° (always
facing away from the inattentive caretaker). The inattentive caretaker had her body facing the sea lion but
her head turned away (not towards the attentive caretaker). Each subject made 42 trials.
Penel & Delfour 438
Figure 2. Test 1: body orientation. For each sea lion, Success / Failure rate and place (top) and mean time (s) of the response time
(latency) and duration (s) of looking at the caretakers (down) during experiment 1. The line shows the random level with 50%. *
= p<0.05; ** = p<0.01; *** = p<0.001
Results. The 4 sea lions failed this test (N = 168, k = 102, p < 0.01), and they did not
preferentially look at the attentive caretaker vs. the inattentive one before choosing (Santo: W = 753.5, p
= 0.23; Smack: W = 672.5, p = 0.21; Gonzo: W = 834.5, p = 0.96) (Figure 3). Kaï not only significantly
chose the inattentive caretaker (N = 42, k = 31, p < 0.01), he also looked at her for significantly longer
before choosing (Figure 3) (W = 429, p < 0.01). Santo (N = 42, k = 37, p < 0.001), Smack (N = 42, k =
37, p < 0.001), and Gonzo (N = 42, k = 35, p < 0.001) showed a side preference (Figure 3) (right, left, and
right, respectively).
Penel & Delfour 439
Figure 3. Test 2.1: head orientation. For each sea lion, Success / Failure rate and place (top) and mean time (s) of the response
time (latency) and duration (s) of looking at the caretakers (down) during experiment 2.1. The line shows the random level with
50%. * = p<0.05; ** = p<0.01; *** = p<0.001
Part 2: Face forward/body forward vs. face turned/body forward
For this test, the attentive caretaker had her body and head facing the sea lion, while the
inattentive caretaker had her body oriented towards the animal but her head turned away. The subjects
received a variable number of trials (Santo: 37; Smack: 43; Gonzo: 46; and Kaï: 44).
Results. The four sea lions failed this test (N = 171, k = 87, p = 0.82), and did not show any
difference in their latencies to choose a caretaker (W = 3304, p = 0.99) (Figure 4). Only Santo looked
longer at the attentive caretaker versus the inattentive one before choosing (W = 885, p < 0.05). All four
subjects showed a significant side bias in this experiment (Test 2.1): Santo and Gonzo went to the left (N
= 37, 46, k = 36, 35, p < 0.001, respectively), while Smack and Kaï went to the right (N = 43, 44, k = 39,
30, p < 0.001, 0.05, respectively).
Penel & Delfour 440
Figure 4. Test 2.2: head orientation. For each sea lion, Success / Failure rate and place (top) and mean time (s) of the response
time (latency) and duration (s) of looking at the caretakers (down) during experiment 2.2. The line shows the random level with
50%. * = p<0.05; ** = p<0.01; *** = p<0.001
Experiment 3: Eye visibility
Eyes open vs. sunglasses
Shaping phase 2 and procedure. Before experiment 3, a second shaping phase introduced a new
posture to the animals: caretakers knelt down in front of the sea lions and looked at them. This posture
allowed the subjects to see their caretakers’ eyes (Figure 1). The attentive caretaker wore sunglasses
without tinted lens, whereas the inattentive caretaker wore the normal, dark sunglasses. The subjects
received 42 trials.
Results. The four sea lions failed this test (N = 168, k = 90, p = 0.39), and their latencies to
choose between the two trainers did not show any significant difference (W = 3375.5, p = 0.76). Nor did
Penel & Delfour 441
they look longer at the attentive versus inattentive caretaker before choosing (W =14505.5, p = 0.28)
(Figure 5). They again all showed a particular side bias, Santo and Gonzo choosing right (N = 42, k = 38,
37, p < 0.001, respectively) and Smack and Kaï choosing left (N = 42, 50, k = 37, 40, p < 0.001,
respectively).
Figure 5. Test 3: eye visibility. For each sea lion, Success / Failure rate and place (top) and mean time (s) of the response time
(latency) and duration (s) of looking at the caretakers (down) during experiment 3. The line shows the random level with 50%. *
= p<0.05; ** = p<0.01; *** = p<0.001
Discussion
The four tested sea lions preferentially chose an attentive caretaker who had her body turned
towards them, but they did not seem to be able to discriminate attentional cues when the caretakers took a
more ambiguous posture. In the latter case, they demonstrated significant side biases by “choosing a
particular side.”
Penel & Delfour 442
Before discussing each test, we would like to mention that of course the four sea lions have been
exposed to their caretakers’ gestures: they were not naïve. However, they have never been subjects in
experiments testing their theory of mind and they have never seen their caretakers wearing sunglasses. Of
course, one could think that some situations are more encountered by the sea lions that others throughout
their training history (e.g., body forward vs back turned) and their choice could be influenced by
neophobia. However at this state, this would be pure speculation since no scientific data is available.
More information on the sea lions’ daily life and history of exposure to humans’ gestures are needed to
answer this point. However, we were interested in conducting situated cognitive experiments by testing
the four subjects’ sensibility to their caretakers’ attentional states in situations they have never
experienced before but in contexts they know (i.e., familiar humans, known location, test occurring
during regular training session and mixed with known exercises, etc).
In the facing versus back turned test the sea lions preferentially chose the attentive caretaker,
recalling results reported in dogs (Virányi et al., 2004) and horses (Proops & Mc Comb, 2010). The
subjects seemed to base their choice on their experience of this human body orientation being correlated
with ability to give food. Moreover, previous studies showed that dogs beg for food more often when a
human is facing them versus facing away (Miklósi et al., unpublished data, as cited in Bräuer et al., 2004;
Kaminski, Call, & Tomasello, 2004). Bottlenose dolphins (Tursiops truncatus), South African fur seals
(Arctocephalus pusillus) and grey seal (Halichoerus grypus) show similar results in a similar task
(Schudin et al., 2001, as cited in Kaminski et al., 2005; Scheumann & Call, 2004; Shapiro et al., 2003).
Interestingly, some authors have explained the good performance of dogs in terms of their long history of
co-habitation with humans and selective breeding (Call, 2001). However, wolves (Canis lupus), reared
and socialized by humans, were also able to understand some attentional states of humans (Udell et al.,
2011). Domestication is therefore not a prerequisite for understanding human attentional states; our
results are in agreement with this. However, unlike in similar studies with horses (Proops & McComb,
2010) and dogs (Gásci et al., 2004), three sea lions did not take more time to choose the attentive
caretaker, even although all four subjects looked longer at the attentive caretaker before making their
choice. One individual (Smack) showed a longer latency when choosing the attentive caretaker compared
to the inattentive one, and he also looked longer at the attentive trainer. Similar results were found with
capuchin monkeys (Cebus apella) (Hattori, Kurosima, & Fujita, 2007): they looked longer at the
experimenter looking at them vs. looking at the ceiling. Conceivably, Smack was looking for the “right”
caretaker, but his inability to find the attentive caretaker might have been due to some caretakers’
ambiguous and/or inadvertent cues or some trouble discriminating the two cues.
When both caretakers’ bodies were oriented towards the subject but one was looking away, and
when one was fully oriented towards the subject while the other’s body was oriented away but her head
faced the subjects, the attentive trainer was not preferentially selected or looked at for longer. The sea
lions did not appear to notice or understand the importance of the head orientation. Bottlenose dolphins
showed similar results, paying more attention to the body than the head of their caretakers (Tomonaga,
Uwano, Ogura, & Saito, 2010). Bonobos (Pan paniscus), gorillas and orangutans understand human
attentive states using head cues (Bania & Stromberg, 2013; Tempelman et al., 2011). Moreover, these
primates selected humans who were in the best position to give them food (e.g., body turned but hand
towards the subject) (Tempelman et al., 2011). California sea lions, like some great apes (Kaminski et al.,
2004), appeared to process cues from the human body in hierarchical fashion. For our subjects, the body
might be a more important cue than the head, meaning that the inattentive caretaker could therefore be a
good choice for them. Interestingly, in test 2.1, Kaï looked longer at the inattentive caretaker with her
body oriented towards him than the attentive before choosing, and he did not choose a particular side,
indicating that his choice was mainly based on the caretaker’s body orientation.
The sea lions’ size should be taken into consideration when examining the present results. These
animals are between 50 cm and 1 m tall (from head to ground), while the caretakers are about 1.70 to 1.75
m tall. When moving forward, sea lions do not look up beyond 1.20 m, so they only see the caretakers’
abdominal belt, not the head. Moreover, sea lions do not only “walk”; they can slide along or combine
these two methods. According to Emery (2000), when the head is not accessible for an animal, body cues
Penel & Delfour 443
are used to discriminate attentive states. Replicating the set of experiments 2.1 and 2.2 with trainers
kneeling down might bring different results. In order to make sure the trainers’ head and eyes were
visually accessible in test 3, the caretakers knelt down. When confronted with eyes accessible versus not
accessible conditions, the four sea lions again failed to discriminate; this suggest that, contrary to horses,
dogs and baboons (Papio papio) (Bräuer et al., 2004; Proops & McComb, 2010; Soproni et al., 2001), sea
lions may not be sensitive to human gaze. As the subjects previously failed to appreciate that the head cue
was a more salient cue than body orientation, this result is not surprising. Several factors could explain
these results. First, eyes may simply be a non-pertinent stimulus for the sea lions. Like orangutans
(Gretscher, Haun, Liebal, & Kaminski, 2012) but unlike chimpanzees (Bräuer, Call, & Tomasello, 2007),
sea lions might need more salient cues to infer if someone is looking at them or not. Their limited
understanding of what humans can and cannot see might mean that they did not understand that the
attentive caretaker was paying attention to them (Emery, 2000). Alternatively, they might not have
understood that the sunglasses blocked the caretaker gaze; in contrast dogs show a better understanding of
humans’ visual perception and that an opaque barrier will block human’s experience of seeing an object
(Bräuer et al., 2004).
Our data suggest that from test 2.1 the subject did not understand what was required of them and
they instead adopt an alternative strategy, namely choosing a particular side. Considering their latencies
and their looking behavior, their side choices became increasingly stronger. Wells et al. (2006) showed
that California sea lions have a different lateralized swimming pattern according to gender: males swim
preferentially in a clockwise direction whereas females swim counterclockwise. The possible lateralized
behaviors of the four sea lions could have influenced the results obtained here. In other words, they might
have adopted a behavior based on some stimuli (a side) instead of the caretakers’ posture, as did dogs
(Kaminski et al., 2009).
Our results do not support the idea that young sea lions possess a concept of “social attention”.
According to Chance (1967; as cited in Emery, 2000), each individual of a social group gives and
receives attention according to its social position (dominant/subordinate). Studies of captive sea lions
have shown hierarchical relationships among individuals of the same sex (Hanggi & Schusterman, 1990;
Schusterman, 1968). Our subjects were young and of a similar ages, and as yet we have no information
about their relationships. Another set of experiments should be conducted to bring more information on
that topic.
Although, the sea lions did not seem to attend to physical signs of caretaker’s attentional states,
several parameters might have compromised the subjects’ understanding of the situation. First, the layout
of the test arena could have influenced our results (Hare, 2001); studies shown that social tensions are
diminished in large arenas. Second, using an opaque barrier (Braüer et al., 2004) instead of sunglasses
might make it easier for the subjects to infer the humans’ perspective. Third, more detailed analysis of the
sea lions’ behaviors might clarify what they understand of the test. For instance, caretakers reported that
the subjects sometimes tried to get their attention by touching their hands. Similar behaviors were
described in horses (Proops & McComb, 2010) and chimpanzees (Theall & Povinelli, 1999). Finally,
delivery of food rewards by the attentive caretaker might facilitate the task. In other studies (Bräuer et al.,
2004; 2007; Proops & McComb, 2010; Tempelman et al., 2011; Udell et al., 2011), experimenters used
food as a primary reward.
To conclude, our results call for testing California sea lions in other experimental situations, and
more naturalistic ones. According to Gásci et al. (2004), gazing as a sign of attention is a specifically
human trait, but ignorance of gaze cues by other species does not mean complete ignorance of attention.
Our sea lions subjects were born in captivity and raised by humans, a situation that is particularly useful
for investigating interspecific communication.
Acknowledgements
The authors would like to thank dolphinarium curator Birgitta Mercera and the following Sea lion
trainers: Caroline Lévy, Stéphane Lecki, Déborah Mallet, Bastien Servières, Daphné Vergon, Juana
Penel & Delfour 444
Serrano, Julie Lovato, Lauranne Torres and Fleur Besnoiy who alternatively were experimenters A, B and
C or took care of the non-tested sea lions while the experiment was conducted. The authors are indebted
to James Anderson for his careful review. They also would like to acknowledge the contributions made
by two ABC anonymous reviewers.
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