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Journal of Ethology
ISSN 0289-0771
J Ethol
DOI 10.1007/s10164-016-0462-z
Contingency checking and self-directed
behaviors in giant manta rays: Do
elasmobranchs have self-awareness?
Csilla Ari & Dominic P.D’Agostino
1 23
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ARTICLE
Contingency checking and self-directed behaviors in giant manta
rays: Do elasmobranchs have self-awareness?
Csilla Ari
1,2,3
•Dominic P. D’Agostino
1,2,3
Received: 30 November 2015 / Accepted: 20 February 2016
ÓJapan Ethological Society and Springer Japan 2016
Abstract Elaborate cognitive skills arose independently in
different taxonomic groups. Self-recognition is conven-
tionally identified by the understanding that one’s own
mirror reflection does not represent another individual but
oneself, which has never been proven in any elasmobranch
species to date. Manta rays have a high encephalization
quotient, similar to those species that have passed the mirror
self-recognition test, and possess the largest brain of all fish
species. In this study, mirror exposure experiments were
conducted on two captive giant manta rays to document their
response to their mirror image. The manta rays did not show
signs of social interaction with their mirror image. However,
frequent unusual and repetitive movements in front of the
mirror suggested contingency checking; in addition, unusual
self-directed behaviors could be identified when the manta
rays were exposed to the mirror. The present study shows
evidence for behavioral responses to a mirror that are pre-
requisite of self-awareness and which has been used to
confirm self-recognition in apes.
Keywords Self-recognition Mirror test Comparative
cognition Mobulidae Cognition
Introduction
Animal cognition is the process by which animals acquire,
process, store and act on information gathered from the
environment (Shettleworth 2010; Brown 2014). Con-
sciousness includes sentience, intelligence and self-
awareness (Brown 2014), or, in other words, awareness of
internal and external stimuli, having a sense of self and
some understanding of one’s place in the world (Chandroo
et al. 2004; Bekoff and Sherman 2004; Brown 2014).
Animal consciousness has been a long-time interest and
a debated field among cognitive ethologists (Heyes 1994,
1998; Povinelli et al. 1997). The mirror self-recognition
(MSR) test initially developed by Gallup (1970) is con-
sidered to be a reliable behavioral index to show an ani-
mal’s ability for self-recognition/self-awareness (SA;
Platek and Levin 2004; Prior et al. 2008). Recognizing
oneself in a mirror is a rare capacity among animals (Reiss
and Marino 2001), while no species of fish has so far
passed this test. There has been only one report on self-
recognition in fish using chemosensory recognition
(Thu
¨nken et al. 2009). However, studies conducted on
other fish species reported that the response to their mirror
images differed from responses to conspecifics (Verbeek
et al. 2007; Desjardins and Fernald 2010; Suddendorf and
Butler 2013; Balzarini et al. 2014). The only nonhuman
species which demonstrated MSR are the great apes (i.e.,
chimpanzees, Pan troglodytes,Pan paniscus; orangutans,
Pongo pygmaeus; gorilla, Gorilla gorilla), asian elephants
(Elephas maximus), bottlenose dolphins (Tursiops trunca-
tus) and a non-mammal species, the magpie (Pica pica)
(Gallup 1970; Amsterdam 1972; Lethmate and Ducker
1973; Povinelli et al. 1993; Miles 1994; Patterson and
Cohn 1994; Walraven et al. 1995; Prior et al. 2008).
Electronic supplementary material The online version of this
article (doi:10.1007/s10164-016-0462-z) contains supplementary
material, which is available to authorized users.
&Csilla Ari
csari2000@yahoo.com
1
Hyperbaric Biomedical Research Laboratory, Department of
Molecular Pharmacology and Physiology, Morsani College
of Medicine, University of South Florida, 12901 Bruce B.
Downs Blvd., MDC 8, Tampa, FL 33612, USA
2
Foundation for the Oceans of the Future, Budapest, Hungary
3
Manta Pacific Research Foundation, Kona, HI, USA
123
J Ethol
DOI 10.1007/s10164-016-0462-z
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Those species that passed the MSR test to date share
common characteristics, such as large, complex and highly
foliated brain, complex social behavior, cooperative and
empathic behavior. The largest brain of all fish species is
possessed by manta rays with high encephalization quotient
and highly foliated cerebellum (Ari 2009,2011), they often
form large feeding aggregations suggesting complex social
system, and are often referred to as being intelligent; therefore,
manta rays may beconsidered the most likely candidates from
any fish species to pass the MSRtest. The universal use of this
test has attracted controversy, because it is biased for vision,
but not other sensory modalities. Although it has been sug-
gested that olfactory recognition using chemical cues is more
appropriate for fish (Thu
¨nken et al. 2009;Brown2014), this
might not be the case for Mobulids. Manta rays have excep-
tionally large optic tectum and telencephalon among elas-
mobranchs, and the high importance of vision during their
foraging activity has also been recently described (Ari 2009,
2011;AriandCorreia2008), which further supports the
possibility that evaluating their self-awareness based on the
MSR test is likely a suitable technique.
The definitive test of MSR is the mark test focusing the
animal’s behaviors on the newly marked area of their body
when exposed to a mirror (Sarko et al. 2002). However,
similarly to marine mammals, fish species also have the
disadvantage that they are not able to touch the marked
area of their body; therefore, it is more challenging to
evaluate their behavioral response. Exploratory and social
behavior can be observed at first when animals are exposed
to a mirror, which stage is followed by contingency
checking when the animals engage in highly repetitive or
unusual movements to understand their own image. In the
next stage, the animals might show self-directed behavior
(e.g., dolphins blowing bubbles, chimpanzee picking teeth;
Gallup 1970; Reiss 2012; Sarko et al. 2002; de Veer and
van den Bos 1999), before the mark test would be initiated.
Mirror exposure experiments were conducted on two
captive giant manta rays to document their responses to
their mirror image in order to predict whether they would
be a candidate for the mark test and whether they use a
mirror to understand their own image. The present study
shows evidence for manta rays’ contingency checking and
self-directed behavior when exposed to a mirror, which are
the prerequisites of self-awareness.
Materials and methods
Subjects
Two giant manta ray specimens were exposed to a mirror at
the Atlantis Aquarium, Bahamas, in March 2012 during a
16-day period. The first subject (M1) was a mature male
Manta birostris (estimated disc width 4.2 m) which had
been living in the exhibit for over 2 years, while the second
subject (M2) was a female (estimated disc width 3.3 m)
that had been at the Aquarium for 1 year. This individual’s
taxonomical classification is uncertain to date, because her
characteristics almost completely fulfill the criteria for M.
birostris, except for a white mouth region, brownish back
coloration and the lack of large white shoulder bars.
The two manta rays showed similar responses through-
out the study, and therefore their data were merged in most
cases during the representation of the results, unless there
was significant difference between their behaviors, in
which case their data are presented separately.
Apparatus and procedure
The observation area (OA) was selected to be the widest
area in the tank that was free of underwater decoration
obstacles, where the animals were able to turn and
maneuver comfortably when necessary (Fig. 1). The two
manta rays’ behavior was documented in a rectangular area
of the tank (OA) that was approximately 10 m wide, 15 m
long and 5.5 m deep, where the mirror was considered
visible to the manta rays (Fig. 1).
Three experimental conditions were tested: (1) mirror
placed in the water (MI); (2) control conditions when the
mirror was either removed completely (MO), or (3) a
mirror-sized, non-reflective white board was placed in the
water (WB). Seven trials were performed in each experi-
mental condition during 16 days. Each trial was conducted
between feeding times and lasted for 10 min. The test was
performed with a 0.9 m 91.5 m mirror which was tem-
porarily installed in a horizontal orientation on the side of
Fig. 1 The observation area (OA, rectangle) of the tank is presented,
where the mirror was considered visible to the manta rays, from
dorsal view. The elongated tank continues on both sides for
approximately 55 and 35 m (Mmirror, polygon location of the
underwater camera, circle location of the camera outside the tank)
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the tank in the manta rays’ regular swimming path, *1m
below water level. The placement of the mirror was made
to ensure that the manta rays would have a frequent and
predictable visual image of their reflection, and thus the
potential to exhibit a behavioral response. The white board
condition was achieved by reversing the mirror to the white
surface facing the pool. The duration of the experimental
sessions was between 10 and 50 min per day. The manta
rays’ behavior was video-recorded and viewed by two
independent analysts. Observations during the study were
recorded from inside the tank using a Canon S100 camera
with Fisheye Fix S100 underwater housing and from out-
side the tank by using an Olympus FE360 camera.
The reported variables were determined as the total time
spent in the observation area, number of cephalic fin
movements and circling behavior in the observation area. A
continuous record of the manta ray’s behavior during each
condition was also created for the total duration of the
sessions, and the total time spent in the observation area
was presented for every 10 min interval. The time of
occurrence of specific behaviors, its onset (from a counter
on the videotape), its duration and any additional com-
ments were noted. The analysis of the video recordings
were done by the independent observers.
Behavioral categories were identified, using the MSR
test reported on bottlenose dolphins by Reiss and Marino
(2001) and modified to manta ray specific behaviors, which
are described in Table 1. Social behaviors (S) were defined
when the animals were closely following, chasing or
touching each other inside the OA. Surfacing behavior
(when the animals swam up breaking the water surface)
was considered to be feeding related behavior (F) inde-
pendently of whether or not the mouth or cephalic lobes
were open. Contingency checking behaviors (when the
animal is testing to see whether, when it moves, the image
also moves, CC) included performing unusual or repetitive
body movements in front of the mirror while visually ori-
ented to it (e.g., circling in front of the mirror, repetitive
cephalic fin movements or bubble blowing in front of the
mirror). Self-directed behavior (SD) occurs when a subject
uses a mirror to investigate parts of its body that would not
be visible without the mirror while visually oriented to the
mirror. Based on this definition which has been used in
previous studies on dolphins, when a posture or movement
exposing the ventral side to the mirror otherwise not visible
to the animal could be observed, while the manta ray was
visually oriented to the mirror, this behavior was identified
as SD, while it could also be classified as CC. Other
behaviors (O) that were unusual but not strictly classifiable
included sudden speed or swimming direction change,
stopping or twitching of fins.
Coding was done by two coders (C.A. and D.D.) who
independently scored the same ten sessions. The coding of
C.A. was considered the standard which was to be achieved
by D.D. Coding was considered reliable when the sequence
and duration of specific behaviors coded by C.A. and D.D.
was of the same (duration could differ by a few seconds).
Statistical comparisons were made using an unpaired
ttest ±standard error (SEM) with GraphPad Prism 6.
Results
The manta rays spent 67.88 % of the total observation time
in the OA when the mirror was in the tank, while they spent
18.54 % of the time in the OA when the mirror was not in
the tank. Overall, the manta rays spent 265 % more time in
the OA when the mirror was in compared to when the
mirror was out of the tank (unpaired ttest, P=0.0001,
t=4.086, n=28; Fig. 2a). They also spent significantly
more time in the OA than when WB was presented to them
(unpaired ttest, P=0.0066, t=2.826, n=28). The time
the manta rays spent in the OA was not significantly dif-
ferent between the specimens, except when the white board
was present (unpaired ttest, MI: P=0.384, t=0.879,
n=28; MO: P=0.12, t=1.586, n=20). In that con-
dition, M2 spent more time in the OA compared to M1
(unpaired ttest, WB: P=0.0002, t=4.282, n=15).
The average duration of time spent at the mirror was
also measured for every subsequent 10-min interval. Dur-
ing the first 10 min, the manta rays spent 549 % more time
at the mirror, which decreased during the 2–4th sessions.
Table 1 Description of behavioral categories used during the study
Behavioral category Abbreviation Definition/examples
Social S Closely following, chasing or touching each other
Feeding related F Surfacing behavior
Contingency checking CC Unusual or repetitive behavior while visually oriented to the mirror, e.g., circling in front of the
mirror, repetitive cephalic fin movement, bubble blowing
Self-directed SD Posture or movement exposing the ventral side/a body part to the mirror that otherwise would not
be visible without the mirror while visually oriented to the mirror
Other behaviors not strictly
classifiable
O Sudden change in swimming speed or direction, body twitching
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Following the 4th session, the time increased again by
more than 1400 % within the period of the 5th session
which was significantly higher in the 4–5th sessions than in
the control conditions (unpaired ttest, 40 min MI/MO:
P=0.018, t=3.244, n=4; 50 min MI/MO:
P=0.0297, t=2.641, n=5; Fig. 2b).
During the time spent at the mirror, their cephalic fin
movements were frequent, and they opened their cephalic
fins significantly more often when the mirror was in the
tank, compared to when the mirror was removed (unpaired
ttest, MI/MO: P\0.0001, t=5.954, n=19; MI/WB:
P\0.0001, t=4.677, n=19; Fig. 3a). They also closed
their cephalic fins more often when the mirror was in the
tank, compared to when the mirror was removed (unpaired
ttest, MI/MO: P\0.0001, t=6.142, n=18; MI/WB:
P\0.0001, t=5.363, n=18; Fig. 3a).
The manta rays showed significantly higher frequency
of other repetitive behavior, such as circling at the mirror
when the mirror was placed in the tank compared to either
control conditions (unpaired ttest, MI/MO: P=0.0006,
t=3.776, n=19; MI/WB: P=0.0012, t=3.51,
n=19, Fig. 3b).
No aggressive displays by any of the specimens were
seen towards the mirror. Social/sexual behaviors remained
at a low frequency throughout the study with following
each other at four occasions and touching each other by
their cephalic fins two times. No rapid coloration changes
were observed and the white markings on the back and
head of the animals did not intensify in response to the
mirror on either of the specimens (Fig. 4a, b), as previously
reported to occur during feeding, intense social interaction
and in response to the presence of a new individual (Ari
2014).
Feeding-related (MI:14; MO:3; WB:2), mirror-directed,
self-directed, and other unusual behaviors together (MI:22;
MO:2; WB:3) were more frequent when the mirror was
present compared to when the mirror was absent (unpaired
ttest, P=0.0294, t=2.539, n=6) or when the white
board was present (unpaired ttest, P=0.0251, t=2.631,
n=6; Table 2). Speed change was divided into unusually
slow or fast swimming and stopping/stationing behaviors.
More frequent slow swimming (MI:7; MO:0; WB:1) and
even more frequent fast swimming (MI:17; MO:3; WB:0)
could be observed when the mirror was present. Swimming
up and surfacing behaviors happened more often when the
mirror was present (MI:20; MO:4; WB:5).
Some contingency checking (CC) and SD behaviors
were exclusively present when the mirror was in the tank,
which included body turns into a vertical direction,
exposing the ventral side of the body to the mirror while
visually oriented to it (MI:3; MO:0; WB:0) and bubble
blowing (MI:2; MO:0; WB:0) in front of the mirror, while
other, repetitive behaviors were more frequent, such as
cephalic fin movements and circling (Fig. 3). Figure 4and
Movies 1–5 of the Electronic Supplementary Material
show some of the behaviors observed with and without the
mirror.
These spontaneous CC and SD behaviors could be
observed in both individuals except exposing the ventral
side and bubble blowing which was performed by only one
of them (M2).
Discussion
The present study provides a qualitative and quantitative
description of two manta rays’ behavioral responses in
front of a mirror by employing protocols adapted from
primate and bottlenose dolphin MSR studies. Similar to
that observed in primate studies, the manta rays showed
Fig. 2 a The manta rays (Manta birostris) spent significantly more
time in the observation area when the mirror was placed in the water
compared to control conditions. bDuring the first 10-min session, the
manta rays spent 549 % more time at the mirror than without the
mirror. The time spent in the OA was significantly more in the 3rd,
5th and 6th 10-min sessions when the mirror was present, compared
to control conditions. MI mirror in the tank, MO mirror out of the
tank, WB white board in the tank, *P\0.05; **P\0.005;
***P\0.0005
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exploratory, contingency checking and self-directed
behavior when exposed to the mirror. Intelligence is often
defined as behavioral flexibility, by abilities such as rea-
soning, planning, learning from past experiences and
applying this knowledge to solve problems in novel con-
texts (Brown 2014). To assess the intelligence (cognitive
complexity) of an animal, since it is difficult to measure
mental states or feelings, subjective behavioral responses
that imply consciousness are measured instead (Dawkins
2001; Brown 2014).
The presented data show that the manta rays gave
selective attention to the mirror by displaying significantly
more repetitive movements than in control conditions and
several unusual contingency checking behaviors exclu-
sively at the mirror. The manta rays’ white markings on
their back and head did not change; it was recently
described that the white markings rapidly increase in
intensity when a ray meets a new individual (Ari 2014).
Therefore, we can speculate that the animals did not per-
ceive their mirror image as a new individual, suggesting
that the observed behaviors in the OA were not part of
social behaviors towards the mirror. Aggressive behavior
directed specifically toward the mirror could not be
identified.
Social behaviors between the animals remained at
extremely low frequency during exposure to the mirror
which is similar to what was found with bottlenose dol-
phins (Reiss and Marino 2001). Gallup (1970) and Povi-
nelli et al. (1993) also showed that, in chimpanzees, social
responsiveness declines and contingency checking increa-
ses over time of exposure to the mirror.
Cephalic fin movements, especially on the side that was
facing the mirror, increased greatly in frequency, which
might suggest that manta rays used their cephalic fin
movements for contingency checking (testing to see whe-
ther when it moves, the image also moves). It is also
possible that the cephalic fin movements are helping the
exploration of new objects, so their role is not exclusively
channeling plankton into their mouth during foraging.
Bubble blowing behavior was never observed other than
during MI condition, suggesting that bubble blowing while
staying visually oriented to the mirror was possibly con-
tingency checking.
Among other marine species, in killer whales (Orcinus
orca) and false killer whales (Pseudorca crassidens; Del-
four and Marten 2001) the response to an applied mark on
their body is likely not the only proof of SA, especially if
indeed many levels of self-consciousness exist. An African
Grey parrot (Psittacus erithacus) was described as
exhibiting mirror mediated object discrimination in an
earlier study (Pepperberg et al. 1995), while all monkey
species so far tested (Anderson 1986; Itakura 1987) have
been shown to exhibit mirror- guided behavior (i.e., using
the mirror to guide a part of their body towards hidden
food; Sarko et al. 2002), but no compelling evidence was
found in these species for CC and/or SD responses. In
humans and great apes, CC behaviors are represented as
repetitive head or hand motions (Povinelli et al. 1993),
while in dolphins CC behaviors usually involved head or
body cocking, repetitive horizontal and vertical head
movements, and head circling (Reiss and Marino 2001;
Marino et al. 1994). In dolphins, SD behavior was repre-
sented as unusual neck stretching, body flexing and bubble
blowing (Reiss and Marino 2001; Marino et al. 1994), a
behavior which resembles manta rays exposing their ven-
tral surface to the mirror and bubble blowing in front of the
mirror. Contrary to studies of chimpanzees reported by
Gallup (1970) and others, the manta rays showed a
decrease in the amount of time at the mirror after the first
two sessions, but after the 4th session it dramatically
increased. This trend was similar to that observed in bot-
tlenose dolphins (Sarko et al. 2002). In apes, SD behavior
in response to a mirror has been taken as evidence of self-
recognition (Prior et al. 2008); therefore, the recorded
observations on manta rays possibly show their ability to
self-awareness. However, to further confirm this
Fig. 3 The frequency of repetitive behaviors: acephalic fin move-
ments and bcircling in front of the mirror was significantly higher
when the mirror was present compared to control conditions. MI
mirror in the tank, MO mirror out of the tank, WB white board in the
tank, **P\0.005; ***P\0.0005
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possibility, a MSR mark test might need to be completed
and more animals will need to be tested. Although the full
MSR test could not be completed due to technical diffi-
culties, previous studies suggest that those individuals that
showed mark-directed behavior were the same that had
shown a high interest in the standard mirror exploration test
(Prior et al. 2008).
Primates, cetaceans and elasmobranchs all possess
elaborated brains which show a dispersed morphological
convergence that may also be linked to cognitive conver-
gence. Social intelligence is also believed to be an expla-
nation for the evolution of the primate brain (Whiten and
Byrne 1997). The brain of elasmobranchs has analogous
structures and functions similar to other vertebrates; for
example, the telencephalic dorsal pallium in fish, which is
greatly enlarged in Mobulids (Ari 2011), is considered to
be homologous to the tetrapod hippocampus, amygdala and
neocortex (Broglio et al. 2011; Demski 2013; Brown
Fig. 4 a,bManta rays swim in front of the mirror; c,dDisplaying
the ventral side to the mirror while staying visually oriented;
esurfacing behavior; fopening of cephalic fin in front of the mirror;
g,hBubble blowing behavior in front of the mirror while displaying
the ventral side and staying visually oriented (Mthe location of the
mirror, large arrows point to bubbles)
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2014). Those species with elaborated brains that have
passed the MSR test to date, have large, complex and
highly foliated brains, complex social behaviors, coopera-
tive behaviors and the ability to empathize (Reiss 2012;
Plotnik et al. 2006). If manta rays are entering the small
group of species with self-awareness, we might speculate
that they also share the same common characteristics and
are able to perform complex social understandings, coop-
erative and empathic behaviors.
Self-recognition is also essential for the ability to use
one’s own experience to predict the behavior of con-
specifics (Prior et al. 2008) which might be a unique ability
for an elasmobranchs species. However, these findings
should be interpreted with caution because of the small
sample size and because the MSR test might demonstrate
only a specific level of consciousness (Panksepp 2005;
Brown 2014).
Studies on fish intelligence are largely restricted to bony
fishes, while we have very little knowledge about the
cognitive abilities of sharks and rays (Brown 2014).
Therefore, these results on manta ray cognition are aimed
at stimulating new research directions. In addition, the
perception of an animal’s cognitive abilities and intelli-
gence influences the views and drives decisions about
captive animal welfare and wildlife conservation. There-
fore, our hope is that a greater understanding of manta
rays’ cognitive abilities will support the rationale for pro-
tective legislation in the future.
Conclusion
This paper presents the first analysis of manta rays’
behavioral response to a mirror, including the description
of their contingency checking and self-directed behaviors
which can serve as a basis for similar studies with manta
rays and other elasmobranchs in the future. Further studies
are needed to assess whether the mirror-induced, self-di-
rected behavior is atypical or frequent in manta rays and
whether manta rays are the first elasmobranch species to
exhibit self-awareness, which would imply their potential
for an ability to higher order brain function, and sophisti-
cated cognitive and social skills.
Acknowledgments This study was funded by the Save Our Seas
Foundation. We are very grateful to Michelle Liu, Dave Wert and the
staff of the Aquarium for the possibility and logistical support to
conduct this research at the Atlantis Aquarium, Bahamas. The Divers
Alert Network Europe and Dr. Huntington Potter provided essential
support. The observations during this study were in compliance with
all ethical standards and were approved by the Kerzner Marine
Foundation and the Atlantis Aquarium, Bahamas. We thank three
anonymous reviewers for their thoughtful comments on the
manuscript.
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Table 2 Summarized
frequencies of feeding-related
and other behaviors
Feeding-related Speed change Stopping Direction change
Slow Fast Up Down
M1 M2 M1 M2 M1 M2 M1 M2 M1 M2 M1 M2
MI5 9 161071171310
MO1 2 00 21001 300
WB2 0 01 00003 200
Unpaired ttest, MI/MO: P=0.0294, t=2.539, n=6; MI/WB: P=0.0251, t=2.631, n=6
MI mirror in the tank, MO mirror out of the tank, WB white board in the tank, M1 Manta1, M2 Manta2
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