Spatial vision in the echinoid genus Echinometra
Biology Department, Box 90338, Duke University, Durham, NC 27708, USA
* Author for correspondence (e-mail: sjohnsen{at}duke.edu)
Accepted 15 September 2004
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Summary |
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Key words: vision, acuity, echinoderm, echinoid, visual
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Introduction |
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The anatomical and behavioral characteristics of echinoderms make them
likely candidates for this form of limited spatial vision. Although discrete
photoreceptive organs are found only in certain asteroids and one holothurian,
all examined echinoderms have behavioral responses to light mediated by
photosensitivity of the body wall and nervous system
(Millot and Yoshida, 1958;
Yoshida, 1966
;
Reese, 1966
;
Moore and Cobb, 1985
). These
responses range from seeking shelter to covering reactions, oriented movement
and daily migrations (Thornton,
1956
; Johnsen 1994
;
Hendler et al., 1995
;
Johnsen and Kier, 1999
).
Because the photosensitive tissue is found within and below the transparent
calcite endoskeleton, echinoderms have the potential for lenses and filters.
Indeed, the aboral plates of the ophiuroid Ophiocoma wendtii contain
modified ossicles and migrating screening pigments that act as sophisticated
lenses and filters (Aizenberg et al.,
2001
). The ophiuroid Ophioderma brevispinum has ossicles
that polarize light and appear to affect the locomotion of the animal
(Johnsen, 1994
;
Johnsen and Kier, 1999
). These
anatomical modifications and relatively complex behaviors suggest that at
least some echinoderm species have spatial vision.
All spatial vision ultimately depends on restricting the angular width over
which light can reach each region of a photosensitive surface
(Land and Nilsson, 2002).
Woodley (1982
) suggested that
the opaque spines of echinoids could restrict the directions over which light
could reach the dermis, much as the screening pigments in insect ommatidia
restrict the light reaching the photosensitive rhabdomeres. The entire
echinoid could then act as a large compound eye, with a resolution determined
by the angular spacing of the spines.
This hypothesis was tested in two species of the echinoid genus Echinometra, chosen because they leave and return to small, dark crevices and thus may benefit from limited spatial vision. The ability of the echinoids to find dark targets of different sizes was examined and the results analyzed to predict their spatial resolution.
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Materials and methods |
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Two species were chosen rather than one due to availability issues. Both,
however, have similar habits and ranges
(McGeehee, 1992). Both also
inhabit small crevices, the primary ecological difference between the two
species being that E. lucunter can slowly excavate its own shelter
while E. viridis cannot. Their orientation behavior was not
significantly different (see Results), so the data from the two species were
combined.
Experimental apparatus
The experimental arena was essentially identical to the one described by
Johnsen and Kier (1999). It
consisted of a covered fiberglass tank (1.2 m diameter) with an opening in the
top and a glass bottom (Fig.
1). A circular wall (0.6 m diameter, 4.5 cm high) was centered on
the bottom, and white paper marked in 10° increments was placed underneath
the glass. A cylinder (15 cm diameter, 9.5 cm high) suspended on a string was
used to hold and then remotely release the echinoids in the centre of the
arena. The arena was placed on blocks so that the echinoids' motion could be
viewed from below through the paper. Ten 20 W fluorescent bulbs (0.6 m long)
were mounted in parallel 6 cm apart and 0.6 m above the floor of the arena.
The light passed through a wax paper diffuser, resulting in an irradiance at
the arena floor of 3.3x1015 photons cm-2
s-1 (integrated from 400 to 700 nm;
Fig. 1). This is approximately
equal to the downwelling irradiance during early morning or late
afternoon.
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Three circular targets with diameters of 8.6, 13.5 and 17 cm were constructed from matt black plastic. During trials, the targets were affixed to the circular wall within the arena, 30 cm from where the echinoids were released. Thus, they had angular diameters of 16°, 26° and 33° and subtended solid angles of 0.065, 0.17 and 0.30 sr, respectively.
Experimental procedure
Experiments were conducted from November 2003 to February 2004. Before each
day of trials, the experimental arena was rinsed and filled with artificial
seawater to a depth of 6-8 cm. One of the three targets was chosen at random,
and each echinoid was tested four times with the target at four randomly
ordered positions (0°, 90°, 180° or 270°, relative to the back
of the room). At the beginning of each trial, the echinoid was placed into the
release cylinder. The lights were turned on and the echinoid was released by
lifting the cylinder using a line. Echinoids typically moved within 20 s of
being released and continued in a straight line to the circular wall. An
observer beneath the arena monitored the echinoid's movement and recorded the
bearing (within ±5°) when its center was 4 cm from the circular
wall. The light was then turned off and the echinoid was returned to the
release cylinder. The arena surface was scrubbed with a brush (to minimize the
potential for trail following), the target was moved to its second position,
and the testing process was repeated. A trial was terminated and no bearing
recorded if an echinoid did not move within 60 s or changed direction more
than once. Four trials out of a total of 88 were terminated. In addition, one
echinoid, which only moved once in four trials, was removed from the study.
After all four target positions were tested, a mean vector
for the four bearings (relative to the
position of the target) was calculated using:
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Data analysis
The mean vectors for each echinoid were bivariate, having both direction
and length. In addition, there was a predicted direction (the position of the
target). Thus, the ideal statistical test would have been a bivariate
equivalent of the V-test
(Batschelet, 1981). Because
there is no such test, the data were analyzed using Monte Carlo methods
(Diggle, 1983
). Essentially,
the experiment was simulated many times using random data, and a distribution
of a test statistic was created using the following procedure.
Four random bearings were chosen and averaged into one vector. This was
repeated N times, where N was the number of echinoids tested
for a particular target size. A mean of the N vectors,
, was then
calculated. The mean vector for perfect orientation toward the target,
, has a
bearing of 0° and a length of 1. The distance between the endpoints of
and
was used as
the test statistic (i.e.
).
This process was repeated 100 000 times to create a distribution of distances.
The mean vector from the empirical data
(
) was
calculated and the test statistic (ddata) determined. The
position of ddata in the distribution then gave the
P-value, with a low ddata indicating a
significant departure from randomness. 95% confidence ellipses were also
calculated to ensure that the bearing of mean vector
was not
significantly different from the bearing of the target
(Batschelet, 1981
).
The absolute bearings of the echinoids (not normalized by the position of
the target, but instead to the back wall of the room) were also analyzed to
ensure that there was no spurious orientation to some feature of the arena or
room. Since there was no predicted direction for the absolute bearings, they
were analyzed using the Hotelling T2 test
(Batschelet, 1981).
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Results |
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Discussion |
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The half of the arena containing the black target was, of course, darker
than the half without the target, so it is possible that Echinometra
is simply undergoing phototaxis. There are two arguments against this. First,
the half of the arena with the target is only slightly darker than the half
without the target (assuming that the target reflects no light), requiring the
echinoid to have extremely good contrast sensitivity (2.4%;
Fig. 3). Some vertebrates can
detect radiance differences of approximately 1-2% under ideal conditions
(Douglas and Hawryshyn, 1990
).
However, the regions with the differing radiances must be adjacent and
separated by a sharp border (Land and
Nilsson, 2002
). Gradual changes in radiance, particularly over a
large field of view, are far more difficult to detect. Continual movement
towards slightly darker directions would also be maladaptive, given that the
echinoids' environment has many subtle (and ecologically meaningless) changes
in brightness. Second, the echinoid's orientation towards the target was quite
strong, with a third of the animals hitting the target itself, suggesting that
they were able to accurately determine its location.
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The exact spatial resolution of the echinoid cannot be determined from the results of this study because a single object on an empty background can be detected by visual systems with lower resolution than the object's size. However, this requires a very high contrast sensitivity. Fig. 3 shows the minimum contrast threshold required to detect the presence of the 33° target as a function of spatial resolution. For example, if the echinoid has a spatial resolution of 90°, a minimum contrast threshold of 9.5% is required to detect the 33° target. This is still quite low for the detection of graded boundaries. It is only when the spatial resolution drops to approximately the angular size of the target that it becomes readily detectable, requiring a minimum contrast threshold of 50%.
The highly significant orientation towards the 33° target and the
complete absence of orientation towards the 26° target is intriguing.
While the area of the latter target is only 54% of the area of the former, one
might expect weak orientation towards the smaller target. Both species of
Echinometra seek shelter in rock crevices
(McClanahan, 1999). It is
therefore possible that the smaller targets are detected but not considered
large enough to provide adequate shelter. However, while the 16° target is
indeed smaller than the typical shelter for these species, the 26° target
is not. In addition, smaller crevices are often preferred because they offer
increased protection (Schneider,
1985
). Thus, a behavioral explanation for the lack of orientation
to the 26° target appears less likely than a physiological one.
The spatial resolution of Echinometra may be due to light screening by the spines. Much like the screening pigments in the ommatidia of compound eyes, the spines limit the angular field of view of each portion of the photosensitive body wall by absorbing and reflecting light that does not hit the surface more or less perpendicularly (Fig. 4A). The aboral surfaces of E. viridis and E. lucunter have approximately 100-150 spines, resulting in a mean angular distribution of one spine every 12-16°. From signal theory, detail can be resolved over angles that are double the angular resolution of the detector. Thus, the predicted spatial resolution is 24-32°, suggesting that the spines may be responsible for the observed resolution. Caution is required, however, because the angular distribution of the spines is quite variable. In addition, the photosensitive regions under the test may themselves have directional sensitivity.
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Spatial vision has a clear ecological function in E. lucunter and E.
viridis. Unlike Lytechinus, Tripneustes, Arbacia and many other
Atlantic epibenthic echinoids, both species of Echinometra rely on
small dark crevices for protection from predators and turbulence
(Schneider, 1985;
Thomas, 1991
;
Schoppe, 1996
). They inhabit
shallow forereef and offshore reef areas, as well as the rims of cup reefs -
turbulent areas with high exposure to predation. In rare systems with low
predation pressure, Echinometra communities persist without shelter,
but in typical environments mortality is dramatically increased if no
protection is available (Schneider,
1985
; McClanahan,
1999
). Both species move to and from these shelters to graze on
algae and retreat from predators (Hendler
et al., 1995
). If either is removed from its shelter, it returns
immediately (Abbot et al.,
1974
; McClanahan,
1999
). The ability to detect the direction of distant shelter is
thus advantageous in these species, decreasing the time spent exposed
(Fig. 4B,C). Thus, the spatial
vision observed in this study is unlikely to be an artifact of laboratory
conditions.
It is not known whether spatial vision exists in other echinoderms. Other epibenthic echinoids with large numbers of spines are natural candidates. Ecological similarities and close evolutionary relationships suggest that other crevice-dwelling echinometrids (e.g. E. mathei) may possess spatial vision. The diadematoids are also promising, due to their complex photobehaviors and large number of closely packed spines (over double that found in Echinometra). Many echinoids are also known to aggregate. While the most likely cue for this behavior is olfactory, it is possible that vision plays a role, particularly since many echinoids are far darker than their environment. Ophiuroids, with their cryptic habits and complex optical structures, are also obvious candidates.
The presence of spatial vision in Echinometra also has larger implications, because it demonstrates that a diffuse sensory system can provide a level of spatial information typically associated with specialized sense organs. Although diffuse sensory systems are almost certainly found in all species, they generally receive less attention than specialized sense organs because they are harder to study and are considered to be more primitive. However, as shown by this study, at least some of these diffuse systems may have more sophisticated abilities than previously considered.
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Acknowledgments |
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References |
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