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Visual navigation in starfish: first evidence
for the use of vision and eyes in starfish
Anders Garm1 and Dan-Eric Nilsson2
rspb.royalsocietypublishing.org
Research
Cite this article: Garm A, Nilsson D-E. 2014
Visual navigation in starfish: first evidence
for the use of vision and eyes in starfish.
Proc. R. Soc. B 281: 20133011.
http://dx.doi.org/10.1098/rspb.2013.3011
Received: 19 November 2013
Accepted: 27 November 2013
Subject Areas:
behaviour, evolution, neuroscience
Keywords:
echinoderm, Linckia, compound eye,
coral reef, navigation
Author for correspondence:
Anders Garm
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.3011 or
via http://rspb.royalsocietypublishing.org.
1
Section of Marine Biology, Department of Biology, University of Copenhagen, Universitetsparken 4,
Copenhagen Ø 2100, Denmark
2
Lund Vision Group, Department of Biology, Lund University, Sölvegatan 35, Lund 22362, Sweden
Most known starfish species possess a compound eye at the tip of each arm,
which, except for the lack of true optics, resembles an arthropod compound
eye. Although these compound eyes have been known for about two centuries,
no visually guided behaviour has ever been directly associated with their
presence. There are indications that they are involved in negative phototaxis
but this may also be governed by extraocular photoreceptors. Here, we
show that the eyes of the coral-reef-associated starfish Linckia laevigata are
slow and colour blind. The eyes are capable of true image formation although
with low spatial resolution. Further, our behavioural experiments reveal that
only specimens with intact eyes can navigate back to their reef habitat when
displaced, demonstrating that this is a visually guided behaviour. This is, to
our knowledge, the first report of a function of starfish compound eyes. We
also show that the spectral sensitivity optimizes the contrast between the
reef and the open ocean. Our results provide an example of an eye supporting
only low-resolution vision, which is believed to be an essential stage in eye
evolution, preceding the high-resolution vision required for detecting prey,
predators and conspecifics.
1. Introduction
Though still debated, there are many indications of image-forming eyes having
evolved several times within Metazoa [1–3]. One example of assumed independently evolved eyes is found in the cnidarian lineage peaking in complexity in the
image-forming lens eyes in cubozoans [4,5]. Another example is found within
echinoderms, where only starfish and a single species of holothurian possess
true eyes with putative image-forming capacity [6,7]. Interestingly, there is
evidence of image formation without eyes in sea urchins possibly using directional shading of epidermal opsin by the spines [8,9]. The behavioural
significance of the image formation in sea urchins has not yet been established.
Although certainly convergently evolved, the compound eyes of starfish
resemble the compound eyes of arc clams, which also lack lenses [10] in contrast
to the more advanced compound eyes of arthropods. Depending on species, the
fully grown starfish eyes are composed of 50 –200 ommatidia, each holding
several photoreceptors. The eye is presumably supporting true image vision,
but this has not been verified. From immunocytochemistry and physiology, it
has been indicated that vision in these eyes is opsin based as in all other
known animal eyes [11 –13]. Relatively few behavioural experiments have
been conducted with starfish and almost none dealing with their visual performance. In the 1960s, Yoshida & Ohtsuki [14] made experiments studying
their phototaxis and found some indications that the eyes are possibly involved
in this behaviour. Still, no behaviour has ever been directly associated with the
eyes and image formation, and today it is still unknown why they possess such
prominent eyes.
Here, we studied the eyes and behaviour of Linckia laevigata, a circum tropical
species of starfish closely associated with coral reefs [15]. We tested the hypothesis
that they use vision to find their way back to the reef if displaced. We also
obtained functional data on the physiology and spatial resolution of their eyes,
and correlated this with the behavioural data.
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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2. Material and methods
For the morphological and optical studies, animals were purchased from an aquarium store in Copenhagen, Denmark. For
the electrophysiological and behavioural experiments, animals
were collected in their natural habitat on the coral reef at Akajima,
Okinawa, Japan, and kept in a 300 l holding tank with running seawater at 298C and salinity of 34 psu at Akajima Marine Science
Laboratory. These animals were used for the experiments within
2 days of collection.
Pictures of the eyes were taken in vivo using a Nikon D300 camera
equipped with a 105 mm Micro Nikkor lens and a Leica dissection
microscope equipped with a digital camera (Evolution MP v. 5.0,
MediaCybernetics, MD, USA). These pictures were used to determine possible influence on the visual field by the ossicles, etc.
sitting next to the eye. Further, the pictures revealed in which
direction the eye pointed relative to the long axis of the arm.
Four eyes from four specimens were fixed in 2.5% glutaraldehyde,
1.5% paraformaldehyde and 3% sucrose in 0.1 M phosphate
buffered saline (PBS) overnight. The eyes were postfixed in 1%
osmium tetraoxide in 0.1 M PBS overnight at 48C, dehydrated in
a series of ethanol and acetone, and embedded in Epon 812 resin
following standard procedures. Two eyes were cut in 2 mm sections, stained with toluidine blue and used for light microscopy
(LM). The two last eyes were used for ultrathin sections (70 nm)
and contrasted with lead citrate and uranyl acetate and observed
in a Jeol 1010 transmission electron microscope (TEM) equipped
with a SC1000 Gatan digital camera. Longitudinal sections of
three randomly chosen, fully developed ommatidia were used to
estimate ommatidial receptive fields.
(c) Visual field measurements
Two eyes from two different specimens were placed in a custommade underwater goniometer, and observed through a dissection
microscope. The visual field of the bilaterally symmetric eye was
determined by finding the midline of the eye along with the optical
centres of six peripheral ommatidia situated at regular intervals
along one-half of the eye (figure 3). As the eyes are bilaterally symmetric, we mirrored the data from the one-half to obtain the
complete visual field, which was too large for the range of the goniometer. We also measured the angles between the optical axes of
neighbouring ommatidia in different parts of the eye (n ¼ 16),
and used this to calculate the average sampling density.
(d) Electrophysiology
Extracellular electroretinogram (ERG) recordings were obtained
from seven ommatidia from five individuals. The eye including
the modified tube foot was dissected from an animal and transferred to a Petri dish in the electrophysiological set-up
containing seawater at 298C and a salinity of 3.4%. A custommade glass suction electrode was placed on the edge of one of
the fully developed ommatidia and suction was applied until a
slight migration of pigment into the electrode was observed. The
pore diameter of the electrode was 1–3 mm, resulting in an impedance of 2–5 Mohm. Recordings were amplified 1000 times and
filtered (0.01 Hz high pass and 1000 Hz low pass) via a differential
alternating current amplifier (1700, A-Msystems Inc., WA, USA)
and recorded using a custom-made program for LABVIEW (LABVIEW
v. 8.5, National Instruments, TX, USA). The light stimulus was provide by an ultra bright white LED (Luxeon III star, Philips, San
Jose, CA, USA) placed in a Linos microbench system (Linos, Goettingen, Germany). The microbench was equipped with a series of
neutral density filters and interference colour filters (half-width ¼
(e) Behavioural experiments
The behavioural experiments were performed on two different
coral reefs at Akajima, Okinawa, Japan. A first set of experiments
was made with three groups of intact specimens of L. laevigata
placed at 4, 2 and 1 m in front of the reef front, respectively (locality 1,
reef front facing east). The reef was approximately 6 m wide at
the base and 3 m tall at the middle part. The vertical slope of the
front was about 458, which resulted in the tallest central part of
the reef taking up about 238, 318 and 408 of the visual field vertically depending on the distance. Only at 1 m (visual angle ¼ 408)
did the starfish walk straight back to the reef (see the electronic
supplementary material, figure S2), and here all starfish reached
it in less than 25 min. Accordingly, 1 m was chosen to be the distance to the reef in the following experiments. Five adult-sized
specimens (25–30 cm) had their eyes removed with a pair of scissors (two ossicles also had to be removed to get access to the eyes),
while five others were sham operated (each arm had two tube feet
and two ossicles removed from the middle part). The animals were
left to recover and were tested the day after. The five animals
having the same treatment were tested simultaneously, placing
them 1 m from the reef front with 1 m in between (locality 1).
Their movements were then monitored for 25 min using an underwater video camera (GoPro HERO3, Woodman Laboratories, Inc.,
USA). The water depth was 5 m and the observer was lying at the
surface. The experiments were repeated with 10 new animals at
another location (locality 2, reef front facing south). The water
depth here was 6 m. The average speed of movements was determined in each experimental trial by path integration.
For analysing the behavioural data, still pictures were grabbed
from the videos with 5 min intervals (at 0, 5, 10, 15, 20 and 25 min)
to calculate the speed of movement. The direction perpendicular to
the reef front from their starting position was determined for each
individual and set to 08. Their overall direction of movement was
then measured in degrees relative to this 0. For the individuals
reaching the reef, the direction of movement was determined to
the point of first contact with the reef. For the others, the direction
of movement was determined to the end position after the 25 min.
The results were then analysed with circular statistics. First, a Rayleigh test was performed to test whether the animals moved
randomly or not. If this test returned the direction to be nonrandom, a V-test was used to check whether the direction was
different from 0 (towards the reef front).
3. Results and discussion
(a) Eye morphology
To better understand the functional significance of the
compound eyes present in most starfish, we started out by
Proc. R. Soc. B 281: 20133011
(b) Eye morphology
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(a) Experimental animals
12 nm, CVI Laser, Bensheim, Germany). The stimulus was presented to the ommatidium of interest using a 1 mm light guide
to assure a close to even illumination of its entire field of view.
The experimental protocol started with 15 min of dark adaptation. Then an intensity series was presented covering 5 log units
in steps of 0.3 or 0.7 log units starting at the low intensity end
(1.1 W sr21 m22). This was followed by an equal quanta (6 1018
photons s21 sr22 m22) spectral series covering 400–660 nm in 22
steps, and the protocol ended with a second intensity series to
ensure that the sensitivity had not changed during the experiment.
Each stimulus lasted 100 ms and the stimuli were presented with
2 min in between. Only data from eyes lasting a full protocol,
where the second intensity series differed less than 10% from the
first, were used for the analysis. The data were analysed manually
in the program IGOR PRO v. 6.12A (Wavematrics, Lake Oswego, OR,
USA). The spectral data were transformed by the V/logI-curve to
obtain the relative sensitivity (see [16] for details on this procedure).
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(a)
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Proc. R. Soc. B 281: 20133011
1 cm
(c)
(d)
100 µm
(e)
(f)
(g)
(h)
Figure 1. Visual system of the starfish L. laevigata. (a) Linckia laevigata in its natural coral reef habitat at Akajima, Japan, where it feeds on detritus and algae.
(b) As in other starfish species, the compound eye of L. laevigata is situated on the tip of each arm (arrowhead). It sits in the ambulaceral groove which continues to
the top of the arm tip. (c) Lateral view of the compound eye, also called the optical cushion, which is sitting on the base of a modified tube foot. The eye has
approximately 150 separate ommatidia with bright red screening pigment. (d ) Frontal view of the compound eye showing its bilateral symmetry. (e) The tip of the
arm seen from below. The view of the compound eye is obscured by a double row of modified black tube feet (arrow). ( f ) The arm tip seen straight from above.
Note that the eye is again obscured from view by a modified black tube foot (arrow). (g) The compound eye (arrowhead) seen from 458 above horizontal in a freely
behaving animal. When the animal is active, the modified black tube feet spread out to allow vision. (h) If the animal is disturbed, it closes the ambulaceral groove
(broken line) at the arm tip and withdraws the modified tube feet. The compound eye is then completely covered, leaving the animal blind.
examining the eye morphology, and used this for estimations of
receptive fields and spatial resolution. As in all other known starfish, the eyes of L. laevigata are situated at the very tip of each arm
and in moving animals the tip bends 808–1208 upwards which
raise the eyes from the substrate (figure 1a,b). The eye sits on a
modified tube foot, and fully grown it holds 150–200 ommatidia, distributed in a bilaterally symmetric pattern on the
so-called optical cushion (figure 1c,d). As the eye is sitting on
the base of a modified tube foot, it is drawn into the ambulaceral
groove so that the visual field is narrowed laterally (figure 1b).
The visual field is further shaped by two rows of modified
black tube feet surrounding the eye (figure 1e–h), potentially
blocking light coming from below (figure 1e) and from above
(figure 1f). These tube feet are spread out when the animal is
active (figure 1g), but interestingly when the animal is disturbed
they can be withdrawn into the ambulaceral groove which closes
and covers the eye leaving the animal blind (figure 1h).
The ommatidia vary in size, with the largest being 25 mm
wide and 60 mm deep (figure 2a). The large ommatidia have
about 120 photoreceptors and a similar number of pigment
cells arranged in seven to eight layers along the long axis
(figure 2b,e). This is in good accordance with what is known
from the similar-sized starfish Patiria miniata and Nepanthia
belcheri [17,18]. From the LM and TEM-micrographs, it is
evident that the ommatidia lack any focusing optics, which
contrasts with earlier suggestions from a range of species
[7,19]. They are covered by a single layer of epithelial cells
(figure 2a), and the receptive fields are thus determined by
the screening pigment alone, just as in a pinhole eye. Because
the outer segments of the photoreceptors are arranged in
layers, the width of their receptive fields depends on their
position in the ommatidia (figure 3b). Interestingly, it looks
as though visual information is already being processed in
the retina, as indicated by afferent synapses contacting the
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EC
(a)
(b)
(e)
Pr
PC
PC
PC
OS
OS
PC
OS
Pr
10 µm
10 µm
(d )
(c)
Pr
PC
PC
Pr
PrN
PC
Pr
2 µm
1 µm
Figure 2. Morphology of the starfish eye. (a) LM of two ommatidia sectioned longitudinally. Each of the fully developed ommatidia is composed of 100 –150
photoreceptors and about the same number of pigment cells (PC). Note the thin layer of epithelial cells (EC, arrowhead) covering the outer segments (OS). The
receptors are arranged in seven to eight layers perpendicular to the surface (b). (c) Longitudinal section of a photoreceptor (Pr, dashed black line). Interestingly, it
receives feedback from the nervous system as indicated by afferent synapses (insert, arrowhead indicates synapse, arrows indicate synaptic vesicles). PrN, photoreceptor nucleus. (d ) The outer segments of the starfish photoreceptors are morphologically a mixture of the rhabdomeric- and ciliary-type receptors. They are
formed by microvilli coming both directly from the cell membrane (arrows) and from a modified cilium (arrowhead). (e) Schematic drawing of an ommatidium
showing the layered arrangement of the photoreceptors and pigment cells.
(a)
(b)
right
26°
30°
26°
14°
16°
14°
30°
left half
half
midlin
e
30°
Figure 3. The visual field of a starfish compound eye. (a) Visual field measured with a goniometer. The left ( pink) and right (blue) halves of the eye are symmetric around
the midline. Altogether, the eye covers about 1708 vertically and 1208–2108 horizontally. To illustrate the sampling array, optical axes from a central and six neighbouring
ommatidia are plotted. The average separation between the central ommatidia and the neighbours is 168. The dashed circles illustrate the estimated acceptance cone of
individual receptors in the middle and bottom of an ommatidium, respectively. (b) Estimates of acceptance angles from the middle and bottom part of the ommatidia.
photoreceptors at the soma (figure 2c). It is not known, though,
whether the synaptic contacts are made by interneurons or by
neighbouring photoreceptors. Morphologically, the receptors
are of an intermediate type with microvilli originating both
from the cell surface and from a modified cilium (figure 2d).
(b) Low spatial resolution
From the goniometric measurements of the visual field, each
compound eye is shown to cover about 2108 horizontally and
about 1708 vertically (figure 3). When the position of the eye
on the bent arm tip is taken into account, it is clear that the
starfish eyes monitor the surroundings from the water surface
to the substrate just in front of it. Horizontally, there is a large
overlap between eyes on neighbouring arms. In total, this
gives the animals the ability to simultaneously view their
entire surroundings. However, the visual field is probably
dynamic, because the eyes are surrounded by the highly flexible black tube feet in all directions, potentially narrowing the
visual field.
The optical axes of the ommatidia are more or less evenly
distributed in the visual field, resulting in a sampling density of 108 –208 across the eye, with an average of 168 + 4.58
(n ¼ 16; figure 3a). Together with the large acceptance
angles of 158 –308, this means that the eyes can only resolve
low spatial frequencies, and thus only detect large structures
in the environment. In their natural habitat, this would
be large coral structures. It eliminates the possibility that
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(a)
(b)
time (ms)
600
400
1000
800
200
0
200
0
1
2
3
4
0
5
0
1
2
3
log intensity (W sr–1m–2)
4
5
650
700
(d )
relative sensitivity
1.0
0.8
0.6
0.4
0.2
0
0
1
2
3
log intensity (W sr–1m–2)
4
5
1.0
0.8
0.6
0.4
0.2
0
400
450
500
550
600
wavelength (nm)
Figure 4. Temporal resolution and spectral sensitivity. (a) The temporal resolution of the photoreceptors was examined with ERGs. The half-width of the impulse
response had a minimum of approximately 250 ms, which is comparatively very slow. (b) The slow response is supported by the time to peak measurements of the
impulse response. Again the minimal time to peak was about 250 ms. (c) It is seen from the V/logI-curve that the dynamic range of the eyes was at least 4 log
units, but it is also seen from the curve that the receptors were not saturated at the maximum test intensity (1.1 105 W sr21 m2). (d) The spectral sensitivity of
the receptors showed a single and relatively narrow peak in the deep blue (450 nm) part of the spectrum. The half-width is about 50 nm, which is somewhat
narrower than the typical opsin, indicating the presence of spectral filters.
L. laevigata uses vision to detect fine details in the habitat e.g.
for finding food, predators or conspecifics. Such low spatial
resolution is similar to that found in other animals with
limited brain power [5].
(c) Temporal and spectral response
Using ERGs, we went on to test the temporal response from
the photoreceptors and their spectral sensitivity (figure 4;
electronic supplementary material, S1). The response time
turned out to be very long and with flashes shorter than
50 ms; there was almost no response even at the highest
intensity used (1.1 105 W sr21 m22). We therefore used
100 ms flashes, but at the highest intensity, the time to peak
was still 250 ms and the half-width of the response was
about the same (figure 4). These very slow responses did
not come as a surprise, because they make a good match
with the slow behaviour of the animals. The slow responses
will remove any fast-moving objects from sight. Further, the
ERGs suggest that the eyes of L. laevigata are colourblind
and use a single opsin with peak sensitivity in the blue
part of spectrum around 450 nm (figure 4). The spectral sensitivity curve is somewhat narrower than for a typical opsin
with the best fit to the absorption curve for a theoretical
452 nm opsin [20], resulting in a regression coefficient (r 2)
of 0.69. We speculate that this is owing to some kind of spectral filter present in the eye. It is not unusual that the lens or
cornea absorb damaging ultraviolet-light [21]. Our morphological data show that no lens is present, only a thin layer
of epithelial cells (figure 2a,e), making us unable to point to
a specific structure responsible for the filtering.
Interestingly, the maximum sensitivity at 450 nm matches
the dominant wavelength of clear ocean water in the horizontal
and upward directions [22]. This means that the open ocean
will appear bright to the starfish. But the coral reef will
appear dark, because light reflected from it mostly contains
the longer wavelength part of the spectrum [23,24]. In general,
little light below 470 nm is reflected from reef components.
(d) Navigation
From the optical and physiological results, we hypothesize
that L. laevigata starfish use vision to detect large stationary
objects. Given their ecology and close association with coral
reefs, it seems likely that they use visual cues to discriminate
reef structures from the open sea in order to navigate towards
their preferred habitat. We initially tested this hypothesis by
placing intact specimens at different distances (1, 2 and 4 m)
in front of a reef front taking up between 238 and 408 vertically of the visual space (see the electronic supplementary
material, figure S2). At 4 m, they walked randomly (length
of mean vector ¼ 0.31, Rayleigh test: p ¼ 0.4) but a distance
of 2 m seemed to be very close to the limit of successful navigation (length of mean vector ¼ 0.46, Rayleigh test: p ¼ 0.1). At
2 m, the reef takes up 31o of the visual field vertically which is
approaching the resolving power of the eyes as indicated by
our morphological and goniometry data. When the animals
were placed 1 m in front of the same reef front (maximum
height approx. 408), they all walked more or less straight
back to the reef (length of mean vector ¼ 0.99, Rayleigh test
p ¼ 0.008, V-test p , 0.001; electronic supplementary material,
figure S2). It was obvious, therefore, that at short distances,
they were able to detect the reef and find their way back.
Next, we made a new series of experiments at two different
localities, one with the reef front facing south and one with
the front facing east. At both localities, the navigational abilities
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Figure 5. Navigation experiments. In the behavioural experiments, the test animals were removed from their natural reef habitat and placed 1 m from the reef edge.
(a) The visual scene away from the coral reef habitat was the open ocean. (b) The visual scene towards the natural habitat (coral reef) at a distance of 1 m. (c) Trajectories
from the sham-operated animals tested at locality 1 (reef front to the east). Most of the animals quickly found their way back to the habitat. (d) Trajectories from the eyeablated animals tested at locality 2 (reef front to the south). They moved at the same pace as the intact and sham-operated animals but in random directions. (e) Circular
statistics of the behavioural experiments show that the direction of movement of the sham-operated animals differed significantly from random and correlated with the
direction to the reef front. The direction of movement of the eye-ablated animals did not differ significantly from random. Blue dots represent animals reaching the reef
within the 25 min, red dots represent animals that did not. See experimental procedure for details of the statistical analysis.
of five blinded (modified tube foot with the eye and two
ossicles surgically removed from each arm) and five shamoperated (two tube feet and two ossicles removed from the
middle of each arm) animals were tested at a distance of 1 m
from the reef front (maximum height approx. 408). While the
blinded starfish walked randomly (length of mean vector ¼
0.25, Rayleigh test p ¼ 0.56), the sham operated were still able
to navigate back to the reef (length of mean vector ¼ 0.57, Rayleigh test p ¼ 0.034, V-test p ¼ 0.005; figure 5). To verify that the
blinded starfish were not just impaired by the surgery, we compared the walking speed during the experiments from intact,
sham-operated and blinded animals. The average walking
speeds were 5.2, 4.0 and 4.3 cm min21, respectively, and
none of the differences were significant (one-way ANOVA,
F2,21 ¼ 3.34, p ¼ 0.25). This allowed us to conclude that the
blinded animals were just as active but walked in random
directions. To get additional evidence for visual navigation,
we tested the ability of 10 intact animals during a starry but
moonless night where our V/logI-curve (figure 4a) suggests
they can no longer see. Indeed, they also walked randomly in
the dark (length of mean vector ¼ 0.08, Rayleigh test p ¼
0.94, electronic supplementary material, figure S3). Previous
studies have found that another starfish Oreaster reticulates
is also able to walk more or less straight back to their
feeding grounds, but here is was suggested to be based on
olfaction [25,26].
(e) Eye evolution
In the light of eye evolution, echinoderms are interesting
because they constitute an early branch within the deuterostomes and might therefore shed light on the split between the
two major photoreceptor types, ciliary and rhabdomeric,
with their different photo-transduction pathways [3,27]. Morphologically, the starfish eyes are unusual, because their
photoreceptors are neither ciliary nor rhabdomeric but a
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4. Conclusion
To our knowledge, the results we present here are the first to
directly demonstrate a visually guided behaviour in starfish
involving their compound eyes. We show that if displaced
from their natural coral habitat, L. laevigata uses vision to navigate back, but only when the reef takes up more than 308
vertically, which matches our estimates of a 158–308 resolution.
Acknowledgements. The authors are grateful for all the help supplied by
Dr Kenji Iwao at AMSL and the input offered by MSc Jan Bielecki
and Dr Ronald Petie.
Funding statement. A.G. acknowledges financial support from the
VILLUM Foundation (grant no. VKR022166). D.-E.N. is supported
by the Swedish Research Council and the Knut and Alice Wallenberg
Foundation.
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Interestingly, this means that the behaviour only works at relatively short distances from the reef, and we suggest that the
importance of the behaviour is not primarily to seek new
reefs, or to handle major displacements from the reef, but
rather to ensure that they do not move away from the reef.
Our data also show that the physiology and morphology
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The spectral sensitivity, with a single peak at about 450 nm,
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rspb.royalsocietypublishing.org
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