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First published online February 1, 2008
Journal of Experimental Biology 211, 482-490 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014506
Visual fields of four batoid fishes: a comparative study
Biological Sciences, Florida Atlantic University, Boca Raton, FL 33431, USA
* Author for correspondence (e-mail: dmccomb{at}fau.edu)
Accepted 12 December 2007
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Summary |
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Key words: vision, elasmobranch, skate, ray, binocular, convergence, Dasyatis sabina, Raja eglanteria, Rhinoptera bonasus, Urobatis jamaicensis
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Hueter et al., 2004). These
are characteristics of a much more complex system than previously reported
(Hueter, 1991). Despite recent
advances in our understanding of elasmobranch vision, numerous aspects remain
unexplored, including such fundamental elements as the extent of the visual
field. An organism's visual field is the entire expanse of space visible at a given instant without moving the eyes. There are three measures of the visual field, which include the field of view of a single eye (monocular); the combined field of view of both eyes (cyclopean); and the overlap of the monocular fields (binocular). The point at which the monocular visual fields overlap is termed the binocular convergence point, and the distance from this point to the central point between the eyes (in the transverse plane) is called the convergence distance. A relatively short convergence distance provides depth perception beginning closer to the eyes, whereas with a longer convergence distance binocular vision is achieved further from the eyes.
The visual field is an integral component of the visual sensory system and
is central to an organism's perception of its environment. Herbivorous animals
that are heavily preyed upon often possess laterally positioned eyes with
large monocular fields that facilitate motion detection of predators
(Guillemain et al., 2002). By
contrast, predators typically have frontally positioned eyes with a large
binocular overlap to facilitate accurate depth perception, which is vital for
spatially tracking and acquiring prey
(Blumstein et al., 2000).
Surprisingly, the importance of the visual field appears to have been
overlooked as data on the extent of the monocular and binocular visual fields
of vertebrates are limited to a small group including rabbits
(Hughes, 1972), rats
(Hughes, 1979), humans
(Emsley, 1948), frogs and
toads (Collett, 1977;
Fite, 1973) and avians
(Martin, 1999), with most
visual field assessments limited to birds. Among aquatic organisms, the visual
field has again been determined in relatively few species, including the
harbor seal (Hanke et al.,
2006), cuttlefish (Watanuki et
al., 2000), parrotfish (Rice
and Westneat, 2005), spiny dogfish
(Harris, 1965) and lemon shark
(Hueter and Gruber, 1982).
Because visual fields have been examined in so few species and very few
closely related species, the lack of cohesion and comparable methods have
hindered the ability to formulate and test hypotheses regarding evolutionary
adaptations of visual fields within phylogenetic and ecological contexts.
Therefore, we chose to examine visual fields within a monophyletic clade of
morphologically and ecologically diverse aquatic vertebrates, the batoid
fishes.
Batoid fishes are dorsoventrally flattened elasmobranchs that constitute a
monophyletic group nested within the shark clade
(Douady et al., 2003). There
are over 500 batoid species that exhibit tremendous diversity in head
morphology, eye position, swimming behavior and ecology
(Fig. 1). We hypothesized that
visual field topography would correlate with all of these factors. To test
this hypothesis we selected four representative species that differ in those
characteristics and for which a well-determined phylogeny exists
(Fig. 1).
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Raja eglanteria
The clearnose skate (Raja eglanteria Bosc 1802; Rajidae) is the
most phylogenetically basal species in this study
(Akbulut, 2006;
McEachran and Dunn, 1998). The
skate is a sub-tropical demersal, benthic forager found in the inshore areas
of the western Atlantic and northeastern Gulf of Mexico
(Smith, 1997;
Stehmann and McEachran, 1978).
It has low-profile dorsally positioned eyes set upon a dorso-ventrally
compressed disk mottled with dark irregular markings (presumably for
camouflage). Based upon the position of the eyes and the presence of cryptic
markings, we predicted that R. eglanteria would have large lateral
monocular fields for vigilance against predators, and its sedentary benthic
lifestyle would not necessitate a large anterior binocular overlap.
Urobatis jamaicensis
The yellow stingray (Urobatis jamaicensis Cuvier 1816;
Urolophidae) is a small tropical, reef- and seagrass-associated ray that
commonly buries itself under sand or lies sedentary in seagrass
(Young, 1993). It is found
along the western Atlantic from North Carolina to northern South America in a
depth range of 1–25 m (Smith,
1997). Its body has yellow coloration with elaborate white
spotting, most probably associated with camouflage. It is a benthic forager
and has been documented to raise the anterior portion of its disk to attract
refuge-seeking prey items (Robins and Ray,
1986). The dorsally positioned eyes are periscopic, enabling them
to protrude above the substrate when the ray is buried. Based upon the eye
position and presence of camouflage, we predicted that U. jamaicensis
is heavily preyed upon and would be vigilant against predators. Therefore, it
likely possesses large lateral monocular fields, including good overhead and
binocular vision.
Dasyatis sabina
The Atlantic stingray (Dasyatis sabina Leseur 1824;
Dasyatidae) is a medium-sized subtropical ray with dorsally
positioned eyes, a prominent triangular snout and a counter-shaded disk with
the dorsal surface a deep brown and the ventral surface white. It inhabits
coastal lagoons and seagrass habitats shallower than 25 m
(Snelson et al., 1988) from
the Gulf of Mexico, and Chesapeake Bay through southern Florida, where it
feeds upon benthic invertebrates (Michael,
1993; Cook, 1994).
It is taxonomically intermediate within the assemblage and demonstrates an
undulatory/oscillatory swimming pattern that allows for fast continuous
locomotion (Rosenberger,
2001a). Because of its fast swimming and frontally canted eyes, we
predicted that D. sabina would have a large binocular overlap and
good overhead vision for predator detection.
Rhinoptera bonasus
The cownose ray (Rhinoptera bonasus Mitchill 1815; Myliobatidae)
is the most derived ray in the assemblage and possesses several attributes
that distinguish it from the other species. It is a large tropical ray that
inhabits the eastern and western Atlantic, Gulf of Mexico and northern South
America in waters shallower than 22 m
(Robins and Ray, 1986). It is
the only species with laterally positioned eyes, the only one to exhibit
schooling behavior, the only benthopelagic ray, and the only species to
exhibit true oscillatory swimming. The head extends rostrally well beyond the
margins of the pectoral fins, and the laterally placed eyes provide the
potential for vision ventral to the body. Because of its propensity to form
large schools in the water column, we predicted that R. bonasus would
have binocular vision dorsally, anteriorly and ventrally.
The goal of this study was to quantify the horizontal and vertical visual fields of four batoid species. We asked three primary questions: (1) how do visual fields differ among species that possess different head morphology and eye position, (2) how do their visual fields correlate with their behavioral ecology and (3) are similarities in visual fields retained in morphologically similar, yet phylogenetically distant, species of skate and ray?
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experimental apparatus
An electroretinogram (ERG) technique was utilized to determine the extent
of the horizontal and vertical visual fields. The ERG uses a recording
electrode placed within the vitreal component of the eye to detect a change in
electrical potential when light impinges upon the photoreceptive layer of the
retina. The experimental light source was a white light-emitting diode (LED)
(5 mm diameter/1100 millicandella) that delivered a beam of light through an
acrylic cylinder, which was beveled to terminate in a 1-mm-wide slit. The
acrylic cylinder light guide was painted black so light could emanate only
from the slit. The light guide was mounted within a mobile track that was
fitted upon a protractor, which permitted the light guide to be freely rotated
around the eye in exact degree increments. The protractor light guide
apparatus was positioned with a micromanipulator over the dorsal surface of
the batoid with the center of the protractor carefully aligned at the lateral
margin of the cornea. This permitted the light guide to be rotated around the
eye in the horizontal plane and to deliver a vertical slit of light that
illuminated the cornea from the dorsal to the ventral margins. To determine
the vertical visual field, the protractor device was repositioned orthogonally
to allow the light guide to rotate around the eye in the vertical plane. We
did not determine the visual field in the sagittal plane because the dorsal
positioning and dorsal exposure of the eye resulted in all positive responses
in that plane (pilot data not shown).
The ERG was recorded with 100 µm tip glass electrodes filled with 2 mol l–1 NaCl in 5% agar. A recording electrode was placed within the vitreal component of the eye, and a reference electrode upon the skin of the batoid. The electrodes were differentially amplified to detect the electrical potential of the photoreceptors when light impinged upon the retina. The output from the electrodes was amplified (100–1000x) and filtered (low-pass 1 kHz, high-pass 0.1 Hz) with a differential amplifier (DP-304; Warner Instruments, Hamden, CT, USA). The data were acquired and digitized with Power Lab® 16/30 model ML 880 (AD Instruments, Colorado Springs, CO, USA) and recorded at 1 kHz using ChartTM Software (AD Instruments).
Experimental protocol
To assess the visual field, animals were anesthetized with tricaine
methanesulphonate (MS-222) (1:15 000 w/v). After respiration ceased (2–4
min), animals were quickly transferred to an acrylic experimental tank
(89x43x21 cm) and secured with Velcro® straps to a submerged
plastic stage. The animal was immediately fitted with an oral ventilation tube
that delivered a recirculating maintenance dose (1:20 000 w/v) of MS-222
throughout the experiment. The spiracles were plugged with small form-fitting
pieces of sponge to ensure that water flowed over the gills. Micromanipulators
were then fixed over the tank to hold the two electrodes and the
protractor/light guide apparatus. Light leakage into the room was eliminated
and a light-tight box was created to cover the computer and experimenter
recording the ERG data. The animals were allowed to adapt to the darkened
experimental room for 30 min to ensure maximal pupillary dilation and
therefore greatest retinal exposure (Cohen
and Gruber, 1977).
After full dark adaptation, the trial began with a computer-controlled 2-s flash of the LED directed at the pupil. A clear ERG response was obtained immediately upon activation of the LED (Fig. 2). After a 3-min delay (to allow the eye to recover), the light guide was repositioned in 10° increments and the procedure repeated. A low-power hand-held red LED torch was used by the experimenter to illuminate the protractor and reposition the light guide. The visual field was determined by directing the light around the eye and establishing whether or not there was an ERG waveform response. As the limit of the field was approached, the testing was reduced from 10 to 1° increments. The last angle to produce an ERG response was defined as the limit of the visual field. All measures were taken on anesthetized animals whose eyes were in a static relaxed state. At the conclusion of each experiment, animals were ventilated with fresh seawater and all animals revived and recovered fully.
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) to calculate the angle from the midline of the eye to the
disc wingtip.
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To determine the extent of eye rotation, we used surgical forceps to fully
retract the medial and lateral rectus muscles for a minimum of six freshly
dead individuals of each species. Eyes were photographed dorsally in the
natural, converged and diverged positions, and the angle of rotation
determined using Image J software
(Rasband, 1997).
To determine differences in the visual fields among the four batoid species, the monocular and binocular visual fields, convergence distance, blind area, visual field demarcations (AH, PH, DV, VV) and eyeball rotations of all individuals were compared using one-way ANOVA (Systat Software, Inc., San Jose, CA, USA) with pairwise multiple comparisons by Tukey post-hoc tests. The cyclopean visual field data were non-normal and analyzed with a Kruskal-Wallis ANOVA on ranks with multiple comparisons using Dunn's method.
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RESULTS |
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The visual field demarcations and inter-ocular distance (cm) for each individual were utilized to construct the convergence distance (cm) and blind area (cm2). Both convergence distance and blind area were calculated using a standardized inter-ocular distance to eliminate the effects of body size (Table 1). The standardized convergence distance and blind area differed significantly among the four batoid species in both the horizontal and vertical planes (Fig. 4) (standardized convergence distance: horizontal ANOVA, F=16.0, P<0.001; vertical ANOVA, F=14.0, P<0.001) (blind area: horizontal ANOVA, F=16.0, P<0.001; vertical ANOVA, F=14.0, P<0.001). Pairwise comparisons are provided in Table 2.
The visual field topography changes with eyeball rotation; therefore, we measured the maximum anterior and posterior eyeball rotation in the horizontal plane (Table 1). The degree of eyeball rotation differed significantly among species in both anterior (ANOVA, F=22.1, P<0.001) and posterior directions (ANOVA, F=11.5, P<0.001). Pairwise comparisons are provided in Table 2. Given the data on eyeball rotation, we constructed the dynamic visual fields with the eyes converged (positioned anterior) and with the eyes diverged (positioned posterior) (Fig. 5).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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50°) that are
coupled with large posterior blind areas and are seen in fast-moving predators
that may simultaneously utilize other sensory modalities
(Martin and Katzir, 1999) just
prior to prey capture. Although anatomical features, such as the structure of
the retina, differ between birds and elasmobranchs, both groups face the
common challenges of predator vigilance and optimizing frontal vision for
locomotion, feeding and mate detection. Therefore, it would not be surprising
to find the convergence of visual field types in terrestrial and aquatic
organisms. The visual field characteristics of both U. jamaicensis
and R. eglanteria were similar to the Type I and II visual fields in
birds, whereas D. sabina and R. bonasus were more similar to
Type III visual fields. Both U. jamaicensis and R.
eglanteria possess distinct body markings and elaborate pupillary
structures (both presumably for camouflage), which suggests that predator
vigilance is paramount, a behavioral characteristic found in birds with Type
II visual fields. Additionally, D. sabina and R. bonasus
move faster than the other species and may utilize other sensory modalities to
search for prey, which is a shared behavioral characteristic of birds that
possess Type III visual fields.
Morphology
All four batoid species possessed horizontal anterior binocular overlaps
that confer frontal vision. The overlaps were largest in R. bonasus
and D. sabina and were comparable to those of species with nearly
frontal-facing eyes such as the frog Rana pipiens (90°)
(Grobstein et al., 1980).
However, the large binocular overlaps apparently came at the expense of
reduced posterior visual fields, as D. sabina and R. bonasus
had the largest posterior blind areas. The horizontal anterior binocular
overlaps in U. jamaicensis and R. eglanteria were smaller
than the other species but large enough to allow visually guided locomotion
and feeding. Urobatis jamaicensis was the only species to have a full
360° panoramic view on the horizontal plane. A dorsal binocular overlap
was measured in all species, and U. jamaicensis had the largest
overlap (38°). Rhinoptera bonasus had the greatest morphological
departure from all species in the study, and its laterally positioned eyes,
set anterior to the pectoral wings, allow for a full 360° vertical
cyclopean field around the head.
Dasyatis sabina is the only batoid for which there are some
existing visual field data in the literature
(Nicol, 1978). The visual
fields in Nicol's study were determined by utilizing photographs of the eyes.
Despite differences in methodology, the monocular visual field of D.
sabina obtained in the present study (199°) is very similar to that
reported by Nicol (190°). Sivak described a ramp retina in D.
sabina (Sivak, 1975),
which permits simultaneous focus of images at various distances, and Logiudice
and Laird reported the presence of rods, cones and a horizontal visual streak
(Logiudice and Laird, 1994).
The horizontal visual streak would likely enhance the visual acuity within the
horizontal monocular visual field of D. sabina, which was the largest
measured in this study.
The extent of exposure of the globe of the eye and the position of the eye within the socket partially determine the expansiveness of the visual field. The eye of U. jamaicensis protrudes from the eye cup more than other species, and the posterior and dorsal skin is positioned further from the globe of the eye. This direct exposure may contribute to U. jamaicensis possessing the widest measured vertical binocular overlap. The eye of D. sabina is canted slightly forward and skin surrounding the anterior portion of the eye is retracted, resulting in the largest measured anterior binocular overlap.
Eyeball rotation changes visual field topography, and all four species demonstrated anterior binocular convergence with the eyes in the relaxed and converged states. However, even in the diverged state, D. sabina and R. bonasus still retained anterior binocular convergence but they did not achieve posterior binocular convergence. By contrast, the 16° posterior blind area in R. eglanteria is abolished and replaced by an 8° binocular overlap when the eyes are moved from a relaxed to a diverged state (Fig. 5). Even in the diverged state, R. eglanteria retains anterior binocular overlap, providing it with full 360° vision.
Locomotion
The convergence distance and blind areas are measures of special interest
within the context of locomotion. In fast-moving species, the possession of
short convergence distances and small blind areas would confer an advantage in
optimizing visual information. The four batoids demonstrate three distinct
locomotory patterns (Rosenberger,
2001a). Both R. eglanteria and U. jamaicensis
utilize an undulatory (more than one wave present on the fin at a time)
swimming pattern that is associated with a more sedentary lifestyle. The skate
had the longest horizontal anterior convergence distance (10 cm), followed by
U. jamaicensis (8 cm). For both of these sedentary species, binocular
vision starting near the head may not be as important as for faster swimming
species. Dasyatis sabina, which has a large anterior binocular
overlap and the shortest horizontal anterior convergence distance (3 cm),
demonstrates an intermediate swimming pattern that is a blend of undulation
and oscillation (between half a wave and one wave present on the fin)
(Rosenberger, 2001a). The most
derived ray in the assemblage, R. bonasus, is the only one to exhibit
true oscillatory swimming (fin moves up and down with less than half a wave
present on the fin) and has a large anterior binocular overlap similar to that
found in D. sabina. This binocular overlap is important, as they tend
to form large schools in the water column
(Blaylock, 1989).
Ecology
The habitat associations of the batoids are different and correlate to
aspects of their visual fields. Raja eglanteria is demersal,
inhabiting mudflats, estuaries and rubble bottoms, which allows the skate to
bury and protrude the eyes from the bottom
(Bigelow and Schroeder, 1953).
Urobatis jamaicensis often buries in the substrate
(Michael, 1993), giving its
periscopic eyes a panoramic 360° view of the complex reef environment. The
large anterior binocular overlap found in D. sabina is beneficial as
it negotiates turbid shallow coastal lagoons with sea grass and sandy bottoms
(Snelson et al., 1988).
Rhinoptera bonasus is the only bentho-pelagic ray with ventral
binocular vision, which permits viewing of the oyster beds and estuarine sea
grass common to its habitat (Blaylock,
1989). Additionally, R. bonasus is known to school in
large numbers (Clarke, 1963), and the 360° vertical field would allow for
viewing of conspecifics while swimming.
All three demersal species bury themselves in the substratum, presumably to
avoid detection by predators. Both R. eglanteria and U.
jamaicensis possess camouflage coloration and an elaborate pupillary
operculum (Fig. 6). The
pupillary operculum has been suggested to enhance camouflage of the eyes in
these substrate-dwelling species (Douglas
et al., 2002) in addition to controlling the amount of light that
enters the eye and maintaining a shallow depth of field
(Murphy and Howland, 1991;
Sivak and Luer, 1991). We
predicted that the demersal species should therefore possess good overhead
vision to enable them to remain vigilant while buried. We found that U.
jamaicensis and D. sabina both possessed a greater (larger)
dorsal visual field than the clearnose skate. This may be a reflection of the
skate's basal phylogenetic position or the evolution of more periscopically
positioned eyes in the more recently derived rays.
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Because the three demersal species feed primarily upon benthic infauna,
vision does not likely play an important role in prey detection. Indeed, with
their dorsally positioned eyes and ventrally positioned mouth, these species
can never see what they eat and rely instead upon exquisitely sensitive touch
receptors (Maruska and Tricas,
1998) and electroreceptors
(Sisneros and Tricas, 2002;
Blonder and Alevizon, 1988) to
localize their prey. Unlike the benthically associated species, R.
bonasus often swims in the water column
(Blaylock, 1989), where its
lateral line and electrosensory systems, which both operate at close range,
would be unable to provide it with spatial information about the location of
its benthic prey. The diet of R. bonasus is composed primarily of
benthic mollusks with a small percentage of teleosts
(Smith and Merriner, 1985).
Therefore, the expanded ventral visual field may enable R. bonasus to
visually locate the oyster and clam beds upon which it feeds.
Raja eglanteria was discovered to have the most reduced visual field in comparison with the more derived rays. However, the clearnose skate does possess one specialization that the rays do not: the translucent panes of rostral tissue from which they derive their common name. To our knowledge, the functional significance of the translucent rostral tissue has never been addressed in the literature. The fact that the horizontal visual field overlaps the rostral panes led us to hypothesize that R. eglanteria may have the ability to see through its own translucent tissue. To this end, we directed a beam of light from beneath the translucent pane and impinged the light onto the retina and recorded a positive ERG response. This response simply demonstrates that light can be detected through the rostral tissue; whether this corresponds to a visual or behavioral function remains to be tested. However, it is interesting to note that the mouth of R. eglanteria is located ventrally and immediately posterior to the rostral panes. These windows may allow for last-second visual tracking and acquisition of prey. Although clear image formation through the panes is unlikely, they may at least permit the detection of motion. Rostral translucency is not limited to this species and is found within several skate species and has independently evolved in the guitarfish (Rhinobatidae). A future goal is to investigate a possible visual function of these panes.
Whereas vision may not play as important a role as electroreception in
locating benthic or cryptic prey, it may be most important in vigilance
against predators and in detecting potential mates. Both R.
eglanteria and U. jamaicensis were determined to have large
monocular fields and an approximately 20–30° binocular overlap. This
has been described as the optimal functional width in birds, as it allows
sufficient optic flow field information to ensure accurate locomotion and prey
capture while still maximizing the peripheral view
(Martin, 2007). The horizontal
anterior binocular overlap in D. sabina and R. bonasus are
large (50°) and are coincident with large blind areas behind the head.
This Type III visual field is characteristic of predators with large eyes that
show a reduction in vigilance behavior. This is supported by the fact that
neither of these species possesses the elaborate body camouflage or pupillary
operculum structures that are present in R. eglanteria and U.
jamaicensis.
Evolution
The finding that the most limited visual field was present in the most
basal species in our assemblage, R. eglanteria, has relevance in an
evolutionary context. All of the rays in this study had larger visual fields
on the horizontal plane and, in the case of R. bonasus, in the
vertical plane. This discovery suggests that skates may have had a smaller
visual field that expanded during the radiation of the rays, which in turn
shifted the visual field to suit each species' particular ecological niche.
However, since the visual field of only one skate was determined in this
study, more assessments are needed to resolve the question.
To determine whether a species' visual field shifts as a result of its
ecological niche, it would be interesting to determine visual fields of other
species that are further morphological departures from the species examined in
the present study. For example, the manta (Manta birostris), a huge
derived pelagic ray, has truly unique head morphology with large cephalic
lobes that aid in feeding. The manta has laterally positioned eyes, yet they
are canted slightly forward, which most likely results in a binocular overlap
that would be beneficial to the ray as it continually swims and feeds on
plankton. However, unfurling the cephalic lobes during feeding may partially
occlude the frontal visual field. To compensate for this visual field
reduction, the manta may rotate the eyes anteriorly, as independent eye
movement has been observed in this species in the wild
(Coles, 1916).
A visual field assessment of guitarfish would be relevant, as the Atlantic guitarfish (Rhinobatos lentiginosus) and the shovelnose guitarfish (Rhinobatos productus) both posses rostral translucency similar to that observed in R. eglanteria. If there is a visual function associated with the presence of rostral translucency, a visual field overlap of the rostral tissue would be predicted, as was demonstrated in R. eglanteria.
It is possible that the benthic batoids have a capacity for greater ventral
visual fields and that the constraint is merely due to occlusion by the
pectoral fins and not a limitation of the visual apparatus. This could be
verified by examining a morphologically similar species that is not
constrained to a benthic environment and demonstrates a more oscillatory
swimming pattern. The pelagic stingray, Pteroplatytrygon violacea,
has a nearly worldwide distribution and is commonly found in the top 100 m
over deep waters (Mollet,
2002). It is closely related to D. sabina and has similar
body morphology and eye position. However, P. violacea is pelagic and
its pectoral fins are wider and more flexible than those of D. sabina
(Rosenberger, 2001a). The
greater ventral excursion of the pectoral fins while swimming will likely
result in an expanded ventral visual field.
The goals of the present study were to test whether visual fields varied
among batoid species, if the extent of the visual fields correlated with their
behavioral ecology, and if visual fields demonstrated greater similarity among
closely related species compared with phylogenetically distant ones. The four
batoid species in this study differ in head morphology, eye position
(Compagno, 1977), pectoral fin
locomotion (Rosenberger,
2001b), feeding dynamics (Dean
et al., 2005; Smith and
Merriner, 1985) and habitat associations
(Snelson et al., 1988).
Whereas our data suggest interesting correlations between visual fields and
ecology, data from other species, especially those that possess morphological
distinctions, are needed to definitively correlate the visual fields of
elasmobranch fishes with aspects of their ecology.
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Acknowledgments |
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