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Rapid coloration changes of manta rays (Mobulidae)
CSILLA ARI1,2*
1Foundation for the Oceans of the Future, Budapest, 1108, Hungary
2Hyperbaric Biomedical Research Laboratory, Department of Molecular Pharmacology and
Physiology, University of South Florida, Tampa, FL 33612, USA
Received 9 February 2014; revised 26 March 2014; accepted for publication 26 March 2014
Changes of body coloration have not been described in manta rays (genus Manta) so far; therefore, their natural
body coloration is used to distinguish species and their ventral spot markings are used to identify individuals
worldwide to estimate their population size or seasonal migration. The present study describes the first evi-
dence of rapid coloration changes of manta rays based on observations of captive individuals. Body coloration
changes were observed most intensely on the dorsal surface and on the head, which occurred within minutes
prior to feeding and during intense social interactions. The coloration intensity drastically changed for the white
markings of the shoulder bars, the chevron-shaped marking on the back, the dorsal side of fin tips, the area
around the eyes, the upper margin of mouth, and the inner side of cephalic fins. Three out of five of the captive
specimens have been identified as a putative third manta ray species, and detailed description about their rapid
coloration changes is provided. The present observational study confirms the ability of manta rays to rapidly
change body coloration during exposure to certain environmental stimuli. Understanding the dynamics of these
rapid coloration changes is essential for accurate species identification and to perhaps gain insight into more
advanced forms of communication. © 2014 The Linnean Society of London, Biological Journal of the Linnean
Society, 2014, 113, 180–193.
ADDITIONAL KEYWORDS: adaptive – Atlantic – behavioural ecology – Cephalopterus giorna –Manta
birostris –Manta sp. cf. birostris – marine conservation – natural markings – photo-identification – species
classification – visual communication.
INTRODUCTION
It has long been known that many animals show
adaptive coloration in response to environmental cues
(Linnaeus, 1758; Ramachandran et al., 1996), in asso-
ciation with developmental stages (Dugas, 2012;
Diamond and Bond 2013), to communicate or to
provide camouflage (O’Day, 2008; Mäthger et al.,
2009; Stevens, Rong & Todd, 2013). However, no
coloration changes have been reported on manta rays
so far over the lifespan of an individual, and photo
identification (photo-ID) studies on manta rays have
reported that their ventral spot markings do not
change for extended periods of time (Homma et al.,
1999; Yano, Sato & Takahashi, 1999; Clark, 2001;
Marshall & Bennett, 2010; Deakos, Baker & Bejder,
2011). Photo-ID and visual sight-re-sight techniques
using manta rays’ natural, distinctive ventral spot
markings are commonly used to identify and count
individuals in the wild (Marshall, Compagno &
Bennett, 2009; Kitchen-Wheeler, 2010) and have
become accepted techniques for population estimates
of manta rays. Natural body coloration and spot
markings are similarly used in other large bodied,
pelagic marine species as well (Castro & Rosa, 2005;
Auger-Methe & Whitehead, 2007; Graham & Roberts,
2007; Dudgeon, Noad & Lanyon, 2008; Silva et al.,
2009). Although the white patterns on the dorsal side
of manta rays are quite variable, these patterns have
not been extensively studied and have not been
reported in individual identification studies.
Recently, two (and a putative third) manta ray
species have been separated that were distinguished,
in part based on their body coloration: the coloration
of their dorsal surface, ventral surface, and mouth
*E-mail: csari2000@yahoo.com
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Biological Journal of the Linnean Society, 2014, 113, 180–193. With 6 figures
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193180
area, and the presence of distinct white-colored shoul-
der patches were described as distinguishing identi-
fication keys (Marshall et al., 2009). Specifically,
among the character keys of Manta birostris, the
shoulder patches are very distinct and mouth colora-
tion is dark. Manta alfredi is characterized by white
to light grey mouth, whereas the mouth of Manta sp.
cf. birostris (a putative third species; Lesueur, 1824;
Mitchill, 1824; Bancroft, 1829; Coles, 1916; Bigelow &
Schroeder, 1953, Notarbartolo-di Sciara & Hillyer,
1989, Marshall et al., 2009) is described as cream to
white in coloration.
As a result of population estimates that are partly
based on photo-ID studies using their patterns of
markings, M. alfredi and M. birostris are listed as
vulnerable species on the International Union for
Conservation of Nature red list (IUCN, 2013). Despite
their vulnerable status, these species are still heavily
fished in many parts of the world for their meat,
gill rakers, and cartilage (Compagno & Last, 1999;
Homma et al., 1999; Stevens et al., 2000; Alava et al.,
2002; Dewar, 2002; Marshall, Dudgeon & Bennett,
2011; Couturier et al., 2012). In addition, they are
often caught as bycatch (White et al., 2006), whereas,
to date, there has been no population estimate on the
third, putative species. To enable their more effective
conservation, a more complete understanding of the
characteristics of the natural coloration and markings
of manta rays is essential for accurate population
estimates and the identification of species.
Vision plays an important sensory role in species
that change body coloration (Chen et al., 2013). Visual
centres are enlarged in the Mobulid brain (Amaral,
2003; Ari, 2011) and manta rays have recently been
shown to have relatively good visual abilities (Ari &
Correia, 2008). The latter study implies that vision
most likely plays an important role in foraging,
although it may have other important behavioural
aspects as well, such as communication or courtship.
It is interesting to note that manta rays possess the
largest brain of all fish (Striedter, 2005; Ari, 2011)
and also that their brain weight to body weight
ratio far exceeds that of other large-bodied plankton
feeders including basking and whale sharks
(Northcutt, 1977, 1978; Striedter, 2005; Ari, 2008; Ari
2011; Kruska, 1988; Yopak & Frank, 2009) and is
close to that of predatory elasmobranchs (hammer-
head shark, Yopak et al., 2007; Ari, 2011). Taken
together, these observations suggest that their
enlarged brain did not develop primarily to perform
their feeding strategy. A large brain weight has been
associated with highly social animals (Dunbar &
Shultz, 2007), although no study to date has been
published on the social life or communication of
manta rays, except for a description of their repro-
ductive behaviour (Yano et al., 1999; Marshall &
Bennett, 2010).
The present observational study provides the first
evidence of rapid coloration changes of giant manta
rays, with an emphasis on the natural markings that
are used for species identification.
MATERIAL AND METHODS
STUDIED SPECIMENS
The observations made during the present study were
made in compliance with all ethical standards and
were approved by the Kerzner Marine Foundation
and the Atlantis Aquarium, Bahamas. The tank
where the manta rays were kept was approximately
165 m long, with the narrowest point being approxi-
mately 4.5 m wide and the widest part approximately
21 m wide, and contained an estimated number of
20 000 reef and pelagic fish of species commonly
found in the manta ray’s natural habitat.
The rapid coloration changes were observed on two
M. birostris and three M. sp. cf. birostris specimens
in captivity. Photographs and video recordings taken
at the Atlantis Aquarium, Bahamas were analyzed
for all manta rays in the present study. Two of these
specimens (Manta 1 and 2) were also directly
observed in July 2011 for 24 days and in March 2012
for 16 days. Table 1 provides information on the
specimens discussed in the present study, which were
numbered in reverse chronological order with the
time interval of data collection and the method of
observation.
Table 1. The specimens analyzed in the present study are listed along with the time interval of data collection and the
method of observation
Species Number Observation period Observation method
Manta birostris Manta1 July 2011 to March 2012 Photography/video + direct
Manta sp. cf. birostris Manta2 July 2011 to March 2012 Photography/video + direct
Manta birostris Manta3 May 2009 to Nov 2009 Photography/video
Manta sp. cf. birostris Manta4 2006–2009 Photography/video
Manta sp. cf. birostris Manta5 2006–2009 Photography/video
RAPID COLORATION CHANGES OF MANTA RAYS 181
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A male (stage of maturation uncertain, claspers for
which the calcification degree could not be deter-
mined, extended beyond the posterior margin of the
pelvic fins, clasper gland structure visibly apparent
from the ventral surface situated laterally to the
cloacal opening) M. birostris (Manta 1) was estimated
to be 3.5 m wide during the first observation period
and approximately 4.2 m during the second observa-
tion phase. The species M. birostris was identified
based on distinctive shoulder patch characteristics,
ventral coloration and spot markings, the presence of
caudal spine and mouth coloration (sensu Marshall
et al., 2009). Skin denticles and dentition could not be
analyzed microscopically.
A female manta ray (Manta 2) was measured 2.6 m
wide in July 2011 (stage of maturation uncertain,
most likely immature based on body size), whereas it
was estimated to be 3.3 m in March 2012. The taxo-
nomical classification of this individual remains
uncertain to date. The morphological characteristics,
such as caudal spine, white mouth region, brownish
back coloration, and lack of large white shoulder bars
suggests that it belongs to a putative third manta
ray species, noted as Manta sp. cf. birostris
(Cephalopterus giorna Lesueur, 1824), the Atlantic or
Caribbean manta ray (Marshall et al., 2009).
Archived photographs and videos taken of a male
M. birostris (Manta 3) that lived in captivity at the
Atlantis Aquarium between May 2009 and November
2009, and two male Manta sp. cf. birostris (Manta 4,
5) between 2006 and 2009 have also been used to
analyze rapid coloration changes. Details on the col-
oration changes of both species are presented on the
specimens that were observed directly (Manta 1 and
2).
PHOTOGRAPHY,VIDEOGRAPHY,
AND SIZE MEASUREMENTS
Photographs and video recordings of Mantas 1 and
2 were collected from outside of the tank through
the aquarium windows, from the surface, and inside
the tank with an underwater still and video camera
system (Canon S100 with Fisheye Fix S100 housing
for underwater use). Their size was estimated by a
snorkeller measuring the interorbital distance with
a measuring tape and extrapolating their total
width using frontal photographs of the whole body.
Direct observations were conducted from outside of
the tank, from the side of the tank, and from behind
aquarium windows and by snorkelling inside
the tank. Photographs and video recordings of
Mantas 3, 4, and 5 that were taken at the Atlantis
Aquarium between 2006 and 2009 were analyzed as
well.
QUANTIFICATION OF COLORATION CHANGES
PHOTOSHOP CS5, version 9.0.2 (Adobe Systems
Inc.) was used to quantify the relative darkness of
body areas in each coloration state. To calculate the
difference in darkness of defined body areas, the
images were converted to greyscale and the lightness
value (L) was measured and compared in each
coloration state (0 = black; 100 = white), similar to
methods employed by Robbins & Fox (2012): the areas
were selected and an average blur function was
applied to obtain the mean L value for that area. Five
images per animal were analyzed in each coloration
state for each species. To eliminate the variation in
lighting differences of the photographs potentially
caused by depth, clarity of the water, use of flash, and
the relative position of the sun, control areas were
selected and compared with the areas of coloration
changes in question. The control areas were selected
on the body in close proximity to the areas in ques-
tion, and were oriented at the same angle to assure
similar lighting conditions. Furthermore, the control
areas were areas that did not, themselves, noticeably
change in colour during the study period. The body
areas selected for measurement were: (1) on the
dorsal side; the shoulder bar, pectoral fin tip, chevron
mark, pelvic fin tip, and dorsal fin tip; (2) on the head;
the periorbital region and the edge of mouth. Body
areas to be used as light intensity comparison con-
trols were: (1) black regions on the top of the head; (2)
the middle of the back; (3) and medially from the
pectoral fin tip. For statistical analyses, two-way
analysis of variance was used with Tukey’s post-hoc
multiple comparison test. Changes of lightness value
for certain body regions over the years are presented
as the mean ± SEM. Statistical analysis was
conducted using GRAPHPAD PRISM, version 6
(GraphPad Software Inc.).
RESULTS
Captive manta rays were observed to undergo rapid
changes (within a few minutes) in their body colora-
tion. Specifically, white markings appeared and
changed intensity on certain body regions (Figs 1, 2,
3, 4; the two most representative specimens from each
species are shown). The intensity of the white mark-
ings would increase rapidly to the ‘intense coloration
state’ (Figs 1D, E, F, G, H, 2D, E, F) more times
during the day within a few minutes, and then return
to the normal ‘baseline coloration state’. Changes in
coloration were observed to occur in temporal prox-
imity to a variety of situations, including at feeding
times (Fig. 1H), whenever a new manta ray was intro-
duced to the tank, and during intense social interac-
tion between the two manta rays (Fig. 1G). Feeding
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© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193
occurred twice a day and the rapid coloration changes
started shortly (5–10 min) before each feeding on both
specimens. The ‘intense coloration state’ was most
intense during feeding and slowly returned to the
‘baseline coloration state’ over a period of 20–30 min
after the end of the feedings. In addition, rapid col-
oration changes were observed in association with
intense social interaction; for example, when Manta 2
was introduced into the tank or when mantas were
chasing each other rapidly and closely, which
appeared to comprise courtship behaviour.
In the ‘baseline coloration’ state, the dorsal surface
and the head of Manta 1 was almost completely black,
with only a slightly lighter shade indicating the
shoulder bars and the chevron shaped marking ante-
rior to the dorsal fin (Figs 1A, B, C, 2A, B, C). In the
‘intense coloration state’, the increased intensity of
the white markings was most obvious on the dorsal
supra-branchial shoulder patch markings of Manta 1
(Figs 1, 2), and on the chevron shaped marking ante-
rior to the dorsal fin (Fig. 1D, E, F), the periorbital
region, and the upper margin of the mouth (Fig. 2D,
E, F). At this state, white patches could be observed
close to the dorsal end of the pectoral fins (Figs 1D, E,
H, 2D), and on the tip of the dorsal and pelvic fins
(Fig. 1F).
The back and head areas of Manta 2 were almost
completely black in the ‘baseline coloration state’
(Figs 3A, B, C, 4A, B, C), whereas rapid coloration
changes occurred in these areas during feeding times
(Fig. 3F) and intense social interaction (Fig. 4E).
Similar to Manta 1, the periorbital region, upper
margin of the mouth (Figs 3D, E, 4D, E, F), small
shoulder bar, and dorsal side of pectoral fin tips
turned white in the ‘intense coloration state’ (Figs 3F,
G, 4E). In addition, the inner side of the cephalic lobe
turned to white with a black edge (Figs 3D, E, F, G,
4D, E, F) in the ‘intense coloration state’ from almost
uniformly dark grey in the ‘baseline coloration state’
(Figs 3A, B, C, 4A, B, C), whereas the intensity of the
black coloration decreased somewhat on the ventral
side of the pectoral fin margins (Fig. 3B, E).
Manta 3 showed similar rapid coloration changes as
Manta 1, whereas Manta 4 and 5 showed similar
coloration changes as Manta 2 at feeding times.
In between the two distinct coloration states, inter-
mediate states could be observed for all animals
(Figs 2B, 3K). It is important to note that no rapid
coloration changes were found on the ventral spot
markings in the area posterior to the gill slits on any
of the specimens, comprising the area that is largely
relied upon by investigators for photo-ID purposes.
The white shoulder bar marking of Manta 1 was
peeling; for example, skin layers appeared to be
missing at certain regions of the white shoulder bar
markings, although this phenomenon did not change
significantly over the observation periods (Figs 1D, E,
F, G, H, 2D, E, F) and was more prominently detect-
able during the intense coloration state.
Movies 1–6 show the two different coloration states
on M. birostris (Manta 1) and on the putative third
species (Manta 2). The difference in darkness of the
changing body regions between the two coloration
states is quantified for M. birostris and M. sp. cf.
birostris in Figure 5. In M. birostris, the most signifi-
cant changes in lightness value were observed on the
shoulder bars and dorsal fin tip, whereas, in M. sp. cf.
birostris, they were observed on the pectoral fin tip,
periorbital region, and inside of the cephalic fins be-
tween the ‘baseline’ and the ‘intense coloration state’.
DISCUSSION
The present study provides the first description of
coloration changes on the body of manta rays, which
were rapid (within minutes), reversible, and repeat-
edly observed. It is most likely that they show adap-
tive coloration changes; however, the exact cause
of these rapid coloration changes needs further
investigation. Possible causes could be an indication
of excitement, aggression, and courting, or perhaps
stress related to hormonal changes. It could be
speculated that these coloration changes might give
adaptive advantages for prey capture, be used as a
communication signal between individuals or help to
avoid potential predators.
Previous studies reported that manta rays have
natural markings from birth (Beebe & Tee-Van, 1941;
Marshall, Pierce & Bennett, 2008) and their ventral
spot patterns are considered permanent over their
lifespan (Deakos, 2010; Kitchen-Wheeler, 2010;
Marshall & Bennett, 2010; Deakos et al., 2011;
Marshall & Pierce, 2012). Taxonomic classification,
population estimates, and recent studies on manta
ray seasonal migration also use natural coloration of
manta rays (Kitchen-Wheeler 2008; Luiz et al. 2009;
Marshall et al., 2009; Deakos et al., 2011; Marshall
et al., 2011; Kitchen-Wheeler, Ari & Edwards, 2011;
Marshall & Pierce, 2012); therefore, the present
results should be considered in the future if research-
ers intend to use the body regions where rapid col-
oration changes occur.
The observed rapid changes show that certain body
coloration patterns are potentially not distinctive
characteristics between species, such as the coloration
of cephalic fins, the periorbital region, and the mouth,
as well as the intensity of the shoulder bar markings.
It is important to note that the distinct white shoul-
der patches that are distinguishing character keys of
M. birostris were only present at the ‘intense colora-
tion state’ and were not present most of the day,
during the ‘baseline coloration state’. In addition, the
RAPID COLORATION CHANGES OF MANTA RAYS 183
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© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193
mouth area was dark in the ‘baseline coloration state’
in M. birostris, although the margin of the mouth
turned intensely white in the ‘intense coloration
state’, which therefore would not satisfy the species
description because the white mouth area is a dis-
tinctive feature of M. alfredi and the putative third
species (Marshall et al., 2009). At present, three out of
five identification keys to distinguish manta ray
Figure 1. Rapid coloration changes are presented on the dorsal region of Manta 1 (Manta birostris). During the ‘baseline
coloration state’ (A, B, C), the shoulder bar markings were pale on the dorsal surface, the head and the rest of the dorsal
side was uniformly black, and no white marking could be observed on the fin tips (arrows). During the ‘intense coloration
state’ (D, E, F, G, H), and for the same animal, intense coloration was observed for the white markings of the shoulder
bars, the chevron shaped marking on the dorsal surface anterior to the dorsal fin, the white coloration of the pectoral,
dorsal, and pelvic fin tips (F), and the circular area around the eyes and the upper margin of the mouth. Arrows indicate
areas with high-intensity white coloration at this state. Note the intense white markings during social interaction (G) and
during feeding (H).
◀
Figure 2. Rapid coloration changes are presented on the head region of Manta 1 (Manta birostris). During ‘baseline
coloration state’ (A, B, C), the shoulder bars were pale and the coloration was almost completely black.Arrows indicate areas
that change intensity. During the ‘intense coloration state’ (D, E, F), the shoulder bars had intense white coloration, and the
dorsal side of the pectoral fin tips (D), the upper margin of the mouth, and a circular area around the eyes turned white.
RAPID COLORATION CHANGES OF MANTA RAYS 185
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species are based on body coloration and one of the
keys can be evaluated only by microscopy (Marshall
et al., 2009); therefore, it is very important to clarify
the extent of these rapid coloration changes in each
species to distinguish them properly.
Similar coloration states were also observed on
wild M. alfredi, suggesting that all manta ray
species likely have similar, rapid coloration changes.
Figure 6A presents an example of wild M. alfredi
specimens with intense white coloration on their
dorsal surface and pectoral fin tips, around the eyes,
mouth, and inside of the cephalic fins, as observed
during feeding and social interaction in the Maldives.
An example of a different, solitary individual in the
wild that was not feeding shows rather pale shoulder
bar markings, as well as dark fin tips, head, and
cephalic fin, with a coloration that resembles the
‘baseline coloration state’ of the captive animals
(Fig. 6B). Another example of such coloration states in
M. alfredi was observed in Hawaii, where a specimen
was videotaped with intense white markings on the
dorsal surface when entangled in a fishing line
(Fig. 6C). The same individual (confirmed by using
the unchanging ventral spot markings) was later seen
on a night dive with much less intense white dorsal
markings, long after the line had been cut from its
body (Fig. 6D). Unfortunately, because the light con-
ditions and image quality were not comparable in
Figure 3. Rapid coloration changes are presented on the dorsal region of Manta 2 (Manta sp. cf. birostris). At the
‘baseline coloration state’ (A, B, C), the head, the inside of the cephalic lobes, and the dorsal surface coloration were
completely black (arrows indicate areas that change intensity), whereas, at the ‘intense coloration state’ (D, E, F, G), the
inside of the cephalic fins, the circular area around the eyes, and the upper margin of the mouth were white (arrows).
The black pectoral fin margin on the ventral side was also less intense at the ‘brightly colored state’ (E), whereas small
white patches could be observed on the shoulder and on the fin tips (F, G, arrows).
186 C. ARI
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193
these scenarios, the difference could not be quantified
with the above method in the present study. This
observation, however, also supports the hypothesis
proposing that the white markings most likely inten-
sify as a response to excitement-related stimuli, as
triggered by food, mate, competition or danger.
Individual variation in colour patterns has poten-
tially important implications from an ecological per-
spective. Previous population studies used the ventral
spot markings to identify individuals. Rapid colora-
tion changes were not observed on these ventral spot
markings posterior from the gill slits; however, if
the dorsal surface and head area are intended to be
used for individual identification in the future, the
potential influence of coloration changes in these
areas should be considered. Documentation of both
the dorsal and ventral sides of the same individual
within minutes/hours is difficult in the wild, which
increases the risk of an inaccurate identification if the
areas subject to change, as described in the present
study, are to be used for species or individual identi-
fication. If the identification of manta ray specimens
or species is to be based on these changing regions, it
will be important to consider whether the photo-ID
studies are conducted at feeding areas or during
social interaction because these situations may
produce changes in coloration states in wild animals
as well. The markings that showed intense, rapid
coloration changes might be slightly different in size,
shape or location for each specimen, although
thechanges in intensity are most likely similar to the
observed animals.
Figure 4. Rapid coloration changes are presented on the head region of Manta 2 (Manta sp. cf. birostris). At the ‘baseline
coloration state’ (A, B, C), the inner side of the cephalic fins, the upper edge of the mouth, and the area around the eyes
were black. At the ‘intense coloration state’ (D, E, F), the inner side of the cephalic fins was white with a narrow black
edge, and the upper edge of the mouth and the area around the eyes turned white. Arrows indicate changing areas.
RAPID COLORATION CHANGES OF MANTA RAYS 187
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The observed peeling on the white shoulder bar
areas might be connected to the white marking inten-
sity changes because no similar peeling could be
observed on other parts of the body. It is also possible
that regular sloughing of the skin cells occurred more
intensely in that area or that a general sloughing was
more visible on the white shoulder bar than on the
black parts of the body. Fungus or another infection
was not reported by the aquarium veterinary staff;
therefore, it is unlikely that such a cause contributed
to the peeling phenomenon.
The fact that the manta rays started to show a
more intense white marking coloration just a short
time before feeding started may indicate the antici-
pation of food at exact times of the day, which sup-
ports the hypothesis that manta rays have a long-
Figure 5. The difference in darkness of the changing body areas is presented between the two coloration states.
Differences in lightness value are presented in Manta birostris (A) and Manta sp. cf. birostris (B) where 0 = black and
100 = white. *P<0.05, **P<0.005, ***P<0.0005.
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term memory and are able to perform associative
learning (Ari & Correia, 2008).
Previous studies describing the large visual centres
of the Mobulid brain suggest that vision plays
an important role in social communication or prey
capture; however, very little is known about the role of
vision in the natural behaviour of elasmobranch
species (Ari, 2011; Lisney et al., 2012; Jordan et al.,
2013). For example, billfish (Xiphiidae) can rapidly
change coloration when excited during hunting,
showing bright blue bars along the side of their
body, which is mediated by adrenergic stimulation
(Davie, 1990; Fritsches et al., 2000). These predators
also have well developed colour vision (Fritsches et al.,
2000). Their brightly colored bars are assumed to
break up their large dark silhouette, disguising an
attack, or the presence of conspicuous coloration on the
flanks of sailfish circling a prey fish school might
confuse the schooling fish (Fritsches et al., 2000). Con-
spicuous patterns of other predators are reported
to have a destabilizing effect on schooling fish as
well (Wilson et al., 1987; Fritsches et al., 2000); there-
fore, manta rays might employ a similar strategy,
using strong coloration changes to gain advantage
when foraging, by breaking up their silhouette with
white markings when somersaulting or to gather
plankton more efficiently by attracting them to the
lighter areas.
These coloration changes might also help mantas
communicate because they are often encountered
with an intense coloration state at large feeding
aggregations or when swimming in mating trains.
For example, at feeding aggregation sites on the
Maldives where intense feeding and social interac-
tions are present, the majority of the manta rays
(M. alfredi) have intense white markings on their
back (Fig. 6A; C. Ari, pers. observ.; A.-Ma. Kitchen-
Wheeler, pers. comm.; Guy Stevens, pers. comm.),
whereas nonfeeding, solitary specimens were
observed with less intense white markings, similar to
the ‘baseline coloration state’ of the described animals
(Fig. 6B; C. Ari, pers. observ.). These theories cannot
be confirmed until we know more about their visual
abilities and natural feeding behaviour. It is unlikely
that these white marking intensity changes would
be connected to environmental factors, developmental
Figure 6. Wild Manta alfredi specimens were documented in the Maldives and Hawaii with different intensity white
markings. The photograph presents an example of the wild M. alfredi specimens that were observed during feeding and
social interaction in the Maldives (A). Note the intense white coloration on the dorsal surface and pectoral fin tips, around
the eyes and mouth, and inside the cephalic fins (arrows). An example of a different, nonfeeding, solitary individual that
was observed in the wild, with coloration resembling the ‘baseline coloration state’ of the captive animals (B). Note the
rather pale shoulder bar markings, as well as dark fin tips, head, and cephalic fin. A M.alfredi was observed in Hawaii
with very intense white markings on the dorsal surface when entangled in a fishing line (C). The same individual
(confirmed by using the unchanging ventral spot markings) was later seen on a night dive with much less intense white
dorsal markings, long after the line had been cut from its body (D).
RAPID COLORATION CHANGES OF MANTA RAYS 189
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193
stages or camouflage because they are very strongly
and predictably correlated with every feeding event.
Coloration changes commonly occur in the animal
kingdom for a variety of reasons (Vroonen et al., 2012;
Isaac & Gregory, 2013; Rudh, Breed & Qvarnström,
2013). As the seasons change, some arctic mammals,
such as the arctic fox (Alopex lagopus), change
the colour of their coat to match the surrounding
environment (Linnaeus, 1758). Ramachandran et al.
(1996) reported that the tropical flatfish Bothus
ocellatus can achieve pattern-matching with surpris-
ing fidelity by adjusting the contrast of different sets
of ‘splotches’ of different grain size (or spatial fre-
quency) on the skin and can blend into a wide range
of background textures in just 2–8 s. During the life
stages of development, many mammals, birds and
insects shed their outer layers of hair, feather or
exoskeleton and replace them with new ones to
alter their appearance (Diamond and Bond 2013).
Both terrestrial (chameleons, family Chamaeleonidae:
O’Day, 2008; Stuart-Fox & Moussalli, 2008) and
marine animals (cephalopods: Mäthger et al., 2009)
use colour changes as communication signals (e.g.
during courtship) and for camouflage (O’Day, 2008;
Stuart-Fox & Moussalli, 2008; Mäthger et al., 2009).
Cuttlefish change colour and light polarization to
communicate with other cuttlefish and to camouflage
themselves from predators (Mäthger et al., 2009),
whereas colour changes also have important function
in reef fish communication during territorial behav-
iour (damselfish; Siebeck, 2004). Chameleons (family
Chamaeleonidae) are able to change their colora-
tion depending on the dominant and submissive
state (O’Day, 2008; Stuart-Fox & Moussalli, 2008),
whereas, in elasmobranchs, sharks also display sub-
ordinate behaviour to larger individuals (Myrberg &
Gruber, 1974; Klimley, 1983). Kline, Khan & Holt
(2011) observed a rapid temporary colour display
in rock hind (Epinephelus adscensionis) that could
be turned on and off within 3 s and was used when
confronting territory intruders and during displays of
aggression towards females. Similarly, the coloration
changes observed in manta rays may be part of a
system of communication in which intense colour
patterning is used to display territoriality and domi-
nance. This notion is strengthed in light of the fact
that intense patterns were very prominent when a
new individual was placed in the tank and during
putative courting events. Although these coloration
changes connected to chasing behaviour might
suggest dominance hierarchy, further research is
needed on this topic. It is tempting to speculate that
these rapid coloration changes are a result of acute
hormonal or neuronal changes induced by specific
behavioral responses that may function as an evolu-
tionary advantage for the manta rays.
The results of the present study show that the
areas used to separate species may vary in appear-
ance depending on the state of the animal. Observers
should be aware of the potential range of appearance
for individuals of a particular species. Therefore,
based on the present results, if future identification or
classification studies on giant manta rays intend to
use the changing body regions, these rapid changes in
coloration must be considered. Further studies are
needed to clarify both the mechanism and role of
rapid coloration changes and to confirm the assumed
permanence of coloration at other body regions as
well, with the aim of assisting with classification and
conservation efforts.
ACKNOWLEDGEMENTS
I am very thankful for the generous funding provided
by the Save Our Seas Foundation (http://www
.saveourseas.com), which made this research possible.
I thank the Atlantis Aquarium, Bahamas, for provid-
ing me the opportunity to study the manta rays at
their exhibition, especially Michelle Liu and Dave
Wert, as well as all of the aquarium staff for their
support during the observations. I also thank Keller
Laros (Manta Pacific Research Foundation) who pro-
vided the photographs of the entangled Manta alfredi
(Fig. 6C, D). Thanks are extended to Dr Dominic
D’Agostino and Dr Huntington Potter for their
continuous and irreplaceable support during the
present study. Divers Alert Network Europe provided
essential support during this research. I express
sincere thanks to Dr Dominic D’Agostino, Dr Chris-
topher Rogers and the anonymous reviewers for their
thoughtful comments that greatly improved the
manuscript.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Movie S1. Note the coloration of Manta 1 (1–5 s) and Manta 2 (7–19 s) at the ‘intense coloration’ state from
outside of the tank.
Movie S2. Note the coloration of Manta 1 (1–7 s) and Manta 2 (8–25 s) at the ‘baseline coloration’ state from
outside of the tank.
Movie S3. Note the coloration of Manta 1 (8–37 s) and Manta 2 (1–11 s, 38–52 s) at the ‘intense coloration’ state
from inside the tank. The ventral markings are visible for both animals to enable identification of the same
individuals at the ‘baseline coloration’ state in Movie 6.
Movie S4. Note the coloration of Manta 1 (1–3 s, 28–52 s) and Manta 2 (4–27 s, 52–58 s) at the ‘baseline
coloration’ state from inside the tank.
Movie S5. Note the coloration of Manta 1 (1–12 s) and Manta 2 (13–24 s) at the ‘intense coloration’ state from
inside the tank.
Movie S6. Note the coloration of Manta 1 (6–27 s, 44–51 s) and Manta 2 (1–5 s, 28–43 s, 51–69 s) at the
‘baseline coloration’ state from inside the tank. The ventral markings are visible for both animals to enable
identification of the same individuals at the ‘intense coloration’ state in Movie 3.
RAPID COLORATION CHANGES OF MANTA RAYS 193
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 180–193
