AMER. ZOOL., 17:453-469 (1977).
The Visual System of Sharks: Adaptations and Capability
SAMUELH. GRUBER
Division of Biology and Living Resources, University of Miami, Rosenstiel School of
Marine and Atmospheric Science, Miami, Florida 33149
SYNOPSIS. The visual system of elasmobranchs is reviewed with primary emphasis on recent
investigations. Starting with the ocular adnexa and the whole eye and working through the
cornea, uvea, ciliary zone, lens, and retina, the structure of the eye peculiar to sharks is
described. Visual function as revealed by electrophysiology, photochemistry, and behavioral studies is also reviewed. The discussion ends with a description of structure and
function of the elasmobranch median eye. The overall impression is that far from having
poor vision, these extremely successful marine predators apparently have been provided
with a high degree of visual development. While advances in our understanding of the
shark eye have been impressive, much work remains, and, for example, entire areas such
as resolution and spatial vision are unstudied. Probably the greatest mystery is the relation
between the apparently exquisitely adapted visual system and the natural behavior of
sharks. Thus what is needed is a linking hypothesis between laboratory studies of vision
and the natural behavior of sharks as observed in the field.
rather quickly. For example, no less than
Interest in the visual system of elasmo- eight histological descriptions of the elasbranchs as an object of study extends back mbbranch retina appeared between 1890
at least 200 years. In his pioneer treatise on and 1905.
In the early 20th century two workers,
the visual system of man and animals
Soemmerring (1818) described and V. Franz and M-L. Verrier, devoted much
figured the eye of sharks and even discuss- effort to investigations of the elasmoed the tapetum lucidum, a mirror-like struc- branch visual system and thus influenced
ture behind the retina which produces the development of that discipline. Their
eyeshine. By 1839, the direct autonomic work on sharks and rays culminated in
action of light on constriction of the elas- important contributions from each (Franz,
mobranch iris had been demonstrated 1934; Verrier, 1930). By the mid-20th
(Duke-Elder, 1958), and in 1866 the great century the elasmobranch visual system
retinal anatomist Schultze published a re- was reasonably well known and informalatively detailed account of the shark reti- tion had been summarized several times
(Walls, 1942; Rochon-Duvigneaud, 1943,
na.
1958; Prince, 1956; Duke-Elder, 1958;
Thereafter, information on the visual and Gilbert, 1963). Then, by the 1960s,
system of sharks began to accumulate something happened with which we are all
familiar: namely, an explosion in research
This paper was prepared with support to the
author from the Office of Naval Research, Contract effort and publication in the life sciences.
N000 14-75-C-0173. The author gratefully acknowl- Consequently, more publications on the
edges F. Williams, Chairman, Division of Biology and elasmobranch visual system have appeared
Living Resources and E. Man, Dean, Research Coor- since 1960 than before that date. This is
dination, University of Miami, Miami, Florida; and not entirely without merit, since it has
the American Society of Zoologists, for providing
funds for attending the symposium. The author is permitted a reevaluation of the role of
indebted to J. L. Cohen for detailed discussions on vision in the life of sharks and has clearly
the electrophysiology section. Thanks are due to D. P. demonstrated the diversity of visual sysde Sylva and D. I. Hamasaki for critically reviewing tems within the elasmobranchs, radically
the article; and to Marie Gruber for preparing all of
altering some of the often contradictory
the line drawings.
INTRODUCTION
453
454
SAMUEL H. GRUBER
views expressed in the earlier summary
articles.
Research in the 1960s also opened new
areas of the shark visual system to investigation. These included studies on visual
pigments, visual psychophysics, and retinal
electrophysiology. This summary will draw
primarily on these modern investigations.
For example, some sharks have fixed
eyelids while others have a completely
mobile third lid, or nictitating membrane.
Variability of pupil types and shapes
characterizes the elasmobranchs. The
pupil size of some species is fixed, while
others can stop the pupil down to one or
more stenopaic or pinhole apertures.
Many sharks have a partially or totally
occlusible tapetum, while the tapetum of
DISCUSSION
the cat shark (Scyliorhinidae) is fixed. And
Sharks have been evolving as an inde- so the list could be continued. Thus, it is
pendent group for several hundred mill- difficult to describe the "average" elasmoion years and presently occupy the major branch eye in a meaningful way.
habitats of the sea, with a few species even
restricted to fresh waters. Thus it is not Structural analysis of the lateral eye
surprising that their ocular specializations
are as uniquely characteristic of sharks as
In this section the eye is broken down to
are their naked gill slits, placoid scales, and its component parts and each is briefly
cartilaginous skeletons. In fact, the eye of discussed from the viewpoint of anatomy
elasmobranchs differs in several major and function.
ways from its teleostean counterpart; for
Adnexa and the eye as a whole. Little modexample, in mode of accommodation, ern work has been directed to the ocular
pupilary mobility, ocular adnexa (lids), adnexa of sharks. Yet the palpebrael comand tapetal structure. Most astonishing is plex (upper and lower lids, nictitating
that many of the adaptations which charac- membrane) immediately separates elasterize the visual system of sharks, such as mobranchs from bony fishes. While a lachmobile eyelids, ciliary folds, and a flat- rymal system is unknown, cartilaginous
tened lens drawn back from an arched fishes possess well-formed eyelids which
cornea, are extremely reminiscent of the are mobile in some species (Ginglymostoma,
aerial eye. This was first pointed out by CephaloscyIlium), but relatively immobile in
Walls (1942) and is no less true today. others. In still other species the lower lid is
Actually, recent studies have strengthened secondarily folded longitudinally into a
this view by providing further examples of third eyelid. The original lower lid then
similarity between the eyes of sharks and develops into a structure similar to the
those of mammals. Why the eye should nictitating membrane of amphibians,
have evolved in these directions is un- birds, and mammals. However, unlike the
known. However, it is hoped that in- transparent nictitating membrane of tercreased study of the ecology, natural his- restrial vertebrates, that of sharks is dense,
tory, and behavior of elasmobranchs will opaque, and its outer surface is covered
provide the insight needed to interpret the with placoid scales. Nictitating membranes
biological significance of many of these are especially well developed in the Carunexpected visual adaptations. While the charhinidae and in their allies (Fig. 1).
evolutionary factors leading to the present
form of the shark eye are not well known, ' Most authors studying eyelids of the
much information is available on the struc- / elasmobranchs (Bell and Satchell, 1963;
Gilbert, 1963; Harris, 1965; Gruber and
ture and function of that system.
Schneiderman, 1975; reject Walls' (1942)
Additionally within the elasmobranchs, suggestion that sharks blink in bright light
the visual system is by no means to reduce the amount of light entering the
homogeneous. Although many ocular fea- eye. Rather, the blink reflex is thought of
tures are shared, many more are unique to as a protective mechanism for guarding
the various taxa within the elasmobranchs, the cornea against mechanical damage.
The eyes of sharks are aimed with six
ranging from the species to ordinal level.
VISION IN SHARKS
455
FIG. 1. Head of a lemon shark (Negaprion breviros- retracted state. When fully extended it covers the eye.
tris) showing the nictitating membrane in partially Drawing by R. Hueter.
extrinsic muscles, standard to the verte- received much attention since Smelser's
brate eye (Oliva, 1967). An exception is the (1962) rediscovery of its non-swelling
unusual "e" muscle, first observed by properties. The cornea of elasmobranchs
Johannes Muller more than one hundred is simple in the sense that it does not
years ago, which briefly appears during contain colored substances or other
embryological development of some specialized structures for modulating the
species, then disappears.
light passing through it. Yet it contains all
The eyes of sharks are set with a fair the standard vertebrate layers including a
degree of binocular overlap—up to 45° in thick epithelium, Bowman's membrane, a
Squalus. While visual fixation on an object well-organized, lamellated stroma, Descehas not been reported, the combination of ment's membrane, and a monolayer of
head movements during swimming and endothelial cells (Goldman and Benedek,
coordinated eye movements eliminates the 1967). The so-called sutural fibers discovapproximately 60° blind spot below and ered by Ranvier (1878) set this cornea
astern and provides the shark with stable apart from that of nearly all other verteand nearly panoramic vision (Harris, brates. These fibers mechanically bind the
layers together with the result that the
1965).
The eyes of most elasmobranchs are shark's cornea will not swell or delaminate
prominent organs placed laterally or dor- in unfavorable environments (Smelser,
sally on the head and varying from less 1962). This fact was put to clinical use by
than one percent of the total length in the Payrau (1965), who reported that corneal
whale shark, Rhincodon, to several percent heterografts between shark (Scyliorhinus
in the big-eye thresher (Alopias super- canicula) and man were successful in cases
in which all other tissue
ciliosus) whose eye can attain a horizontal of severe edema
r
failed.
'
diameter of 125 mm or more..
Cornea. The cornea, which is the interEdelhauser (1968) reported that the
face between the external environment cornea is an effective barrier against the
and the internal media of the eye, has - passage of water and sodium into the eye.
456
SAMUEL H. GRUBER
Greatest resistance to the passage of material was offered by the thick corneal
epithelium, known to be coated with a
viscous precorneal film (Harding et al.,
1974).
Uvea. The uveal tract, composed of
choroid and parts of the ciliary body, lines
the globe just internal to the sclera and is
the only vascularized tissue of the adult
eye. Francois and Neetans (1974) briefly
summarized knowledge of the vascular
supply of the elasmobranch eye. Perhaps
the most noteworthy feature of the uveal
tract is the tapetum lucidum, which is located
in the choroid layer behind the retina.
This structure, described in detail by Franz
(1931), is responsible for the eyeshine of
sharks.
Elasmobranchs possess the most highly
evolved tapetum known in the animal
world (Fig. 2). Not only is tapetal reflection
specular, thus reducing scattered light and
internal glare, but it is twice as efficient as
the system in the cat (Weale, 1953), approaching 90% reflection at certain
wavelengths. The tapetal plates contain up
to 1 mg/cm2 pure guanine crystals (Nicol
and Van Baalen, 1968), and are specifically
oriented to direct light back through the
path of entry (Denton and Nicol, 1964).
Finally, the tapetal cells of most elasmobranchs possess fixed channels through
which melanin pigment (Fox and
Kuchnow, 1965) flows during light adaptation, effectively screening the tapetum
from light. The exact mechanism of
tapetal occlusion remains unknown.
Ciliary zone. The ciliary zone, part uvea
and part non-sensory retina, comprises
iris, ciliary body, ciliary folds, and the
ciliary papilla upon which the lens rests.
Ciliary structures are important in regulating the amount of light entering the eye,
movement of the lens in accommodation,
and maintenance of intraocular pressure.
Intraocular pressure directly affects ocular
dimensions, which must be stable for
image quality. Finally, ciliary structures are
active in nutrition of the avascular cornea
and lens. The ciliary body of elasmobranchs is well organized compared to that
of teleosts and can be thought of as the
prototype for "higher vertebrates" (Doolittle and Stone, 1960; Jampol and Forrest,
1972).
Elasmobranchs are among the few fishes
to possess extensive iris movements. The
pupil shapes of elasmobranchs are probably the most varied in the animal kingdom.
light
Shapes range from the familiar circular to
horizontal, vertical and oblique slit pupils,
to pinhole, to multiple pinhole, and finally
•to the unique operculum pupillare of skates
(Fig. 3). Young (1933) showed that excised
iris
muscle will contract autonomously to
light
light. He believed that dilation of the iris
was under CNS control. However, in 1972
Kuchnow and Martin established that the
elasmobranch iris contains smooth muscle
and neurons. In a series of physiological
studies, Kuchnow and his co-workers
(Kuchnow and Gilbert, 1967; Kuchnow,
1970, 1971; Kuchnow and Martin, 1972)
investigated pupillary mechanisms and
kinetics in a variety of elasmobranchs. ReFIG. 2. Perspective diagram of the elasmobranch
sults indicated that most sharks have slow,
tapetum. Unabsorbed light enters and passes through
extensive pupillary responses, but Apristhe eye, retina and retinal epithelium (RE) and
chonocapiUaris (CC) to impinge upon the tapetal plates turus, for example, has fixed pupils while
the pupils of Carcharhinus dilate and con(TP). If the melanin pigment (M) is withdrawn into
the pigment cell (PC) light will reflect from the
strict relatively quickly, taking less than
hexagonal guanine crystals (RC) back through the
one minute for the complete response.
retina. Modified from Best & Nichol (1967). Contr.
Kuchnow presented evidence for an irisMar. Sci. Univ. Texas, 12:172-201, by permission.
VISION IN SHARKS
457'
FIG. 3. The unique operculum pupillare of the thorny operculum rises to expose a circular pupil. Photo by
skate (Raja radiata) in fully light-adapted condition. C. Warner.
As the animal becomes dark-adapted, the digitform
retina reflex, and disproved Franz's (1931) the shark lens is simple, consisting of a
suggestion that melanin is the activating single line running vertically in the anpigment for pupillary constriction. Rather, terior pole and horizontally in the posterpupillary activity under monochromatic ior pole of the eye (Duke-Elder, 1958).
light yielded an action spectrum similar to
The ocular lens is composed of 65%
that of normal rhodopsin, further sup- water and 34% structural protein. The
porting the notion of interaction between protein fraction of the elasmobranch lens
retina and iris.
has been intensively studied during recent
Lens. Elasmobranchs, as all aquatic ver- years. One area of interest lies in the
tebrates, possess a voluminous lens. This is relation between insoluble crystallinnecessary because the cornea, principal protein and cataract formation (Lerman,
refractor of the aerial eye, is optically ab- 1970); the other deals with imsent under water. Thus, the lens must munochemistry and the tracing of verteassume all the refractive power of the eye. brate phylogeny through biochemical
The elasmobranch lens is unusual in two similarities (Manski and Halbert, 1965).
ways: It is aspheric, or more precisely, Lens proteins differ from other structural
elliptical in vertical cross section (Hueter proteins of the body in that crystallins are
and Gruber, unpubl. data), and quite restricted to the lens. This is called tissue
transparent especially in the ultraviolet specificity. Additionally, evolution of lens
(Kennedy and Milkman, 1956). In addi- proteins has been extremely conservative
tion, the complex of sutural lines forming and it appears that crystallins first originat-
458
SAMUEL H. GRUBER
ing in the Agnatha were transferred
through evolution to be shared by shark
and man. This is called organ specificity
(Uhlenhuth, 1903). The crystallins thus
present a unique system upon which the
phylogeny of vertebrates may be traced
(Manski etal, 1967).
Refraction and accommodation in elasmobranchs are primarily functions of the
lens and associated ciliary structures. The
body of knowledge regarding these two
factors is both minute and contradictory
(Sivak, in press). Refraction refers to the
refractive power of individual optical elements of the eye and how they combine to
bring light to a focus at the retina. Refractive error refers to whether the focal point
lies in front of or behind the retina, and
accommodation is the ability of the eye to
change focus, thus maintaining the image
in focus on the retina for targets at varying
distances.
The elasmobranch eye has variously
been labeled as myopic (Beer, 1894) or
hypermetropic (Verrier, 1930; Franz,
1931) in the half dozen papers ever published on its optics. Various attempts have
been made to induce lens movement in
sharks, but most of these have failed (Beer,
1894; Verrier, 1930; Franz, 1931; Somiya
and Tamura, 1973; and Sivak, 1974).
Franz claimed some success at lens movement by electrically stimulating the eye of a
ray and torpedo. But Sivak and Gilbert
(1976) have presented clear evidence of
lens movements in sharks during Tricane
anesthesia.
Resolution of these problems will come
with a concerted effort. Such effort is
being accomplished in our laboratory and
also by Sivak and his colleagues. Thus, we
expect to publish a mathematical model of
the shark eye including physiological and
behavioral studies of visual resolution
within the near future.
Retina and visual pigments. From a visual
standpoint, the retina is the most important element in the vertebrate eye, the
other structures serving to place an image
on that issue. Thus, it is fortunate that the
efforts of several gifted researchers have
been directed toward understanding structure and function of the elasmobranch
retina. This has resulted in real advances
over the past fifteen years.
The structural organization of the elasmobranch retina conforms to the usual
vertebrate plan (Fig. 4); i.e., three cellular
and two synaptic layers (Dowling, 1970).
However, it is unusual in several ways.
Along with cyclostomes, adult elasmobranchs are the only vertebrates whose
retina is entirely devoid of blood vessels.
Retinal nutrition is apparently mediated
by the so-called pigment epithelium, which
is actually unpigmented in sharks. The
only light-screening material in the elasmobranch eye resides in the choroid behind the retina. Receptor cells constitute
about 50% of the retinal thickness in
sharks, a figure somewhat greater than for
other vertebrates. But most notable is the
enormous size of several retinal elements
such as horizontal cells, amacrineprocesses, and some ganglion cells.
The first event of vision, namely absorption of a photon by a visual pigment, takes
place in specialized, ciliated, ependymalike cells known as photoreceptors (Cohen,
1972). Early anatomists, realizing the importance of this retinal layer, noted that
vertebrate photoreceptors were of two
sorts: rods and cones. Retinas could contain either type or a mixture. Further, a
correlation was made between the behavior of the species and whether its retina
contained a predominance of one receptor
or a mixture. These observations led to the
formulation of a theory of vision (Schultze,
1866) known today as the duplexity theory
(Shipley, 1964). From the inception of this
theory, sharks were placed in a category of
animals said to possess pure rod or rod
dominated retinas. This is incorrect, as has
been recently shown and confirmed under
both light and electron optics. Retinal
studies from contemporary literature have
adequately demonstrated that representative elasmobranchs from all orders possess
duplex retinas; i.e., rods and cones. Thus,
the notion based on receptor types, that
sharks are visually inferior, nocturnal
animals without the possibility of dayvision mechanisms, must be abandoned
{Gvuber etal., 1975).
As mentioned, visual pigments reside in
459
VISION IN SHARKS
RE
RL
ELM
ENL
EPL
INL
£•.
IPL
•V.
GCL
•
'
/
ILM
FIG. 4. Gluteraldehyde and osmium fixed retina of
the lemon shark, showing the three cellular (RL =
receptor layer; INL = inner nuclear layer containing
cell bodies of horizontal and bipolar cells; and GCL
containing cell bodies of ganglion and some amacrine
cells) and two synaptic layers (EPL = external
plexiform layer; IPL = internal plexiform layer)
standard to the vertebrate retina. Other labeled structures include retinal epithelium (RE); external limiting "membrane" (ELM); external nuclear layer (ENL
containing receptor nuclei) and the internal limiting
membrane (ILM) separating the retina from the
vitreous body. Histology and photograph by J. L.
Cohen from unpublished work.
the photoreceptors; more specifically, in
their outer segments, which contain up to
35% dry weight of rhodopsin in rods
(Kropf, 1972). Visual pigments of sharks
and rays were incidentally known from the
work of Boll (1876) and Krause (1889).
Detailed studies were not reported until
the work of Bayliss et al., (1936), and the
chromophore was not finally identified as
Vitamin Aj based retinine until Wald's
460
SAMUEL H. GRUBER
(1939) report. Since then about 15 species
have been studied and found to possess
rhodopsin with a maximum light absorption around 500 nm. Perhaps most
noteworthy is the discovery by Denton and
Shaw (1963) that visual pigments of deepsea sharks are environmentally tuned to
the restricted wavelengths of light which
occur at great depths. This is a remarkable
example of parallel evolution, since Denton and Warren (1956) had earlier shown
that certain mesopelagic teleosts contained
a golden pigment termed chrysopsin
which was very similar to that found in the
sharks Centroscymnus, Centrophorus and
Deania (Crescitelli, 1972).
Characterization of the visual pigments
residing in the outer segments of" elasmobranch cones has not yet been accomplished. Thus nothing at all is known
of presumptive cone pigments in the elasmobranchs.
The structure and relations of other
retinal neurons have been studied. Cell
bodies of horizontal and bipolar cells form
the internal nuclear layer of the retina.
Horizontal cells of elasmobranchs are
axonless and among the largest retinal
elements known (up to 200 /urn in horizontal cross section). In Mustelus three layers
of horizontal cells interconnect with the
output terminals of the photoreceptors.
Stell and Witkovsky (19736) observed that
the most proximal layer of horizontal cells
contacted only to cone photoreceptors,
while the distal two sent processes to rods
exclusively. Broad opposition between
horizontal cells of each layer (but not between layers) was demonstrated by
Yamada and Ishikawa (1965), who
suggested that the horizontal cells could
form an electrical syncitium. This was
physiologically confirmed by Kaneko
(1971).
Bipolar cells are also arranged into subtypes and layers, but their relationships are
less well known. Their dendrites, along
with those of horizontal cells, form typically invaginating contacts with receptor
terminals. Witkovsky and Stell (1973) have
shown that certain bipolar subtypes are
provided with Landolt's clubs, which are
digitiform cellular extensions reaching up
into the receptor layer. The function of
these processes is entirely unknown. Bipolar axons course toward the internal
plexiform layer and there synapse with
ganglion and probably amacrine cell processes.
The structure and organization of
amacrine cells is poorly known. According
to Stell and Witkovsky (1973a) they are
axonless fusiform cells with incredibly long
processes, spanning up to 5,000 /u,m. Witkovsky (1971) reported myelinated fibers
of unknown origin which he believed entered the eye of Mustelus from the brain
and ran to the internal nuclear layer, there
synapsing with amacrine and ganglion
cells.
Ganglion cells of elasmobranchs have
recently been treated in detail by Shibkova
(1971), Stell and Witkovsky (1973a), and
Dunn (1973). They form the most proximal layer of the retina and represent its
final output. Their myelinated axons comprise the optic nerve and thus communicate directly with the brain. Ganglion cells
receive information from amacrine and
bipolar cells through synapses in the internal plexiform layer. As with other retinal neurons, several subgroups of ganglion cells have been described dependent
on size, retinal location, and dendritic arborization. For example, in the retina of
Squalus, Shibkova (1971) estimated that the
ratio of giant ganglion cells, to intermediate ganglion cells, to small ganglion
cells was 1:3:50. Stell and Witkovsky
suggested that the numerous small ganglion cells observed are non-neuronal,
perhaps sheath cells associated with the
myelinated axons of true ganglion cells.
This would agree with Franz's (1931) observation that the number of larger ganglion cells increases dramatically in the area
centralis of Mustelus, while that of small
"glial" cells remains constant. Based on
cytoarchitecture and histochemistry, Shibkova (1971) also felt that the giant ganglion cells were the primary visual neurons of
this layer.
Central pathways of this vision in the
shark are now reasonably well known from
work in several laboratories and these have
been covered elsewhere in this symposium.
461
VISION IN SHARKS
zontal cells was never observed. Such a
mechanism implies very large receptive
Electrophysiology of vision. Investigation of fields and broad lateral integration of inthe physiology of the elasmobranch retina formation at the early stages of signal
by electrode penetration and recording processing in the shark retina. Also imwas only first attempted in 1962 by plied is the segregation of signals from the
Kobayashi. Since then a number of studies rod and cone system; i.e., Stell and Withave been accomplished by extracellular kovsky's 19736 work mentioned above.
techniques, intercellular recordings, and Electrical responses from elasmobranch
intracellular penetration of neurons with bipolar cells (Fig. 7) have also been remicroelectrodes. Experiments recording corded by Kaneko (1971) and Ashmore
the massed electrical response of the retina and Falk (1976).
(electroretinogram, Fig. 5) to photic
All neurons in the elasmobranch retina
stimuli have been reported by Kobayashi with the exception of ganglion cells trans(1962), Hamasaki and Bridges (1965), mit information by graded, slow potenO'Gower and Mathewson (1967), Dowling tials, primarily hyperpolarization in recepand Ripps (1970), Gruber (1969, 1975), tors and horizontal cells and transient
and Cohen et al. (1977). These studies biphasic depolarization in bipolars. It is
attempted to answer questions of ecology, only in the ganglion cells that the output
behavior, physiology and pharmacology as signal is at the same time modified for
they pertain to the vision of sharks.
travel over distance and pulse frequency
Records have also been obtained from coded (except see Chan and Naka, 1976).
individual retinal neurons. Thus, Tamura That is, of all retinal neurons, only ganget al. (1966), Tamura and Niwa (1967), lion cells fire propagating all-or-none
Dowling and Ripps (19716) and Niwa and spikes along the axon (Fig. 8). This apTamura (1975) recorded the S-potential of pears to be true for all vertebrate retinas.
horizontal cells from a number of elasmo- However, the organization of this activity
branch species (Fig. 6), finding evidence for is not simple. Depending on how a particucolor coding of responses in at least the red lar ganglion cell is wired into the retina, it
ray, Dasyatis akajei. As mentioned above, may either fire spikes (excitation) or fall
Kaneko (1971) confirmed that horizontal silent (inhibition) to the pattern of photic
cells are electrically coupled by injecting stimulation. The major features of this
current (and procion fluorescent dye) into organization in the retina of Mustelus were
one cell and observing responses of its demonstrated by Naka and Witkovsky
neighbors. He found that electrical stimu- (1972) and Stella al. (1975), but have been
lation of a cell polarized other horizontal well.known from other vertebrate retinas
cells separated by up to five cells. Elec- at least since the work of Kuffler (1953).
trotonic spread between the layers of hori- The so-called receptive field organization
Visual experiments with the elasmobranchs
Negapnon
Dasyatis
Ginglymostoma
light adapted
dark adapted
Isec
FIG. 5. Comparison of the light- and dark-adapted
electroretinogram waveforms in three elasmobranchs. Calibrationrstimulus = 2.5 sec; ramp = 250
V. Modified from Hamasaki and Bridges (1965) by
permission.
462
SAMUEL H . GRUBER
stimulus/time
20mV
FIG. 6. Relation between stimulus intensity and
amplitude of the S-potential recorded from horizontal cells in the dark-adapted skate (Raja) retina.
Stimulus intensity decreases toward the top. Both
amplitude and duration are directly proportional to
stimulus magnitude. Modified from Dowling and
Ripps (1971) by permission.
into such a receptive field organization is
not exactly known, but it is only by such an
antagonistic center-surround mechanism
that the retina talks to the brain. Naka and
Witkovsky (1972) attempted to work out
the role of horizontal cells in organizing
the receptive field of ganglion cells in the
retina of Mustelus. They concluded that all
ganglion cells received input from horizontal cells which were in turn mediated by
bipolar cells.
The receptive fields of ganglion cells in
several vertebrates are color coded. For
example, the RFC might fire to red and
fall silent to green. Such an organization is
termed a chromatic-opponent receptive
field. No evidence of receptive fields with
color coding has been obtained in the two
elasmobranchs (Raja and Mustelus) thus far
studied.
Electrophysiological studies of the elasmobranch retina have provided data on
visual mechanisms of adaptation (Hamasaki et al., 1967; Dowling and Ripps,
1970, 1972, 1976; Green et al., 1975),
flicker (O'Gower and Mathewson, 1967;
-6 1 log at 495 i
of elasmobranchs does not differ substantially from that of other vertebrates. Receptive fields are large (up to 3 mm in
diameter) but are organized into the familiar concentric center-surround type of
overlapping areas of excitation and inhibition. For example, if photoreceptors connected through other neurons to the
center of a particular ganglion cell's receptive field (RFC) are stimulated with light,
that ganglion cell might fire a burst of
spikes. Such a cell is termed an "on-center"
type. If the stimulating light is moved away
from the RFC, a point will be reached
where stimulation has the opposite effect,
i.e., the spontaneous firing of the cell is
inhibited, and the record is now coming
from the "off-surround." "Off-center" and
"on-off center" represent other basic receptive field organizations. Dowling and
Ripps (1970) found an equal number of
on- and off-center ganglion cell receptive
fields in the all-rod retina of Raja. How the
distal retina processes the receptor signals
5mV
FIG. 7. Relation between stimulus intensity and
bipolar cell responses in the retina of the cat shark
(Scyliorhinus canicula). The stimulus was a 0.54 mm
circle of blue light (495 nm) attenuated by neutral
filters. Stimulus magnitude increases toward the bottom. Modified from Ashmore and Falk (1976) by
permission.
VISION IN SHARKS
463
GANGLION CELL RESPONSES
'ON" UNIT
"OFF'UNIT
light alone
light and
depolarizing
current
polarization of
horizontal
cell
light and
hyperpolarizing
20nA\
0.5 sec
FIG. 8. Electrical responses of ganglion cells in the
retina of the smooth dogfish (Mustelus cants). Scheme
shows interaction between light and injection of electrical current into a horizontal cell connected to the
ganglion cell being studied. For example, subliminal
depolarization of a horizontal cell enhances spike
production to photic stimuli in an interconnected
ganglion (middle trace, left-hand column). Taken
from Naka and Witkovsky (1972) by permission.
Gruber, 1969, 1975; Green and Siegel,
1975), and spectral sensitivity (Tamura
and Niwa, 1967; Dowling and Ripps, 1972;
Niwa and Tamura, 1975; Stella al., 1975;
Gruber, 1973; and Cohen et al., 1977), as
well as on the pharmacology synaptic
transmission (Cervetto and MacNichol,
1971; Dowling and Ripps, 1973; and Ripps
et al., 1976). The work on spectral sensitivity indicates that many elasmobranchs apparently have simple retinas with a
monotonous spectral response irrespective
of state of adaptation. These include Mustelus, Raja, and some other batoids. In
contrast, the retinas of Negaprion and
Dasyatis respond differently to color variations of light depending upon state of
adaptation or wavelength. For example,
the peak sensitivity of the lemon shark
shifts from blue-green in the fully darkadapted state (Fig. 9) to green in the lightadapted state. This so-called Purkinje
phenomenon has been correlated with the
presence, in other vertebrates, of a duplex
(rod-cone) retina and the shift is interpreted as the point when the cone system
dominates rod activity under daylight
conditions.
The work on flicker is less clear. The
visual system's ability to resolve flashes of
light into discrete events has been correlated with receptor-type. Thus, Porter
(1902) described a relation between
flicker-fusion and stimulus intensity such
that, for man, as brightness increased by
the log10, the number of resolvable flashes
increased linearly up to a point of 20
flashes per second. With brighter stimuli,
464
SAMUEL H. GRUBER
X= 550
30-
I 2-5|
O — — - O KOtOP*
UJ
•
• acotopic
-photopi.
I"
o
1-0
,
2.4
* •
WAVE NUMBER (cm" 1 )
that an animal with a pure rod retina
would be able to follow such high flicker
rates.
The work by Dowling and his colleagues
on adaptational properties of the vertebrate retina has demonstrated the dependence of state of adaptation on the kinetics
of rhodopsin bleaching and regeneration
in the receptor outer segments. Also, using
the simple all-rod retina of Raja as their
model, they have shown that factors controlling retinal sensitivity are for the most
part located in the receptors. However,
two mechanisms of adaptation were noted:
one is associated with early adaptation to
intense backgrounds which probably results from neural switching within the retina; the other follows bleaching of the
visual pigment and relates visual sensi1.6 xio' tivity to concentration of rhodopsin in the
receptor outer segments.
FIG. 9. Spectral sensitivity of the lemon shark in the
light-adapted (filled circles) and dark-adapted (open
circles) state. These electroretinographically determined results, confirmed behaviorally, demonstrate a
small Purkinje shift (i.e., change in sensitivity as the
animal adapts to light) toward the red end of the
spectrum and can be taken as evidence for two
functional receptor types. Taken from Gruber
(1973).
an abrupt shift occurred in the slope of the
curve which relates flash fusion rate (or
critical frequency of flicker-fusion) to
stimulus brightness. Temporal resolution
then reached another plateau at about
45-60 flashes per second. This relation,
known as the Ferry-Porter law, was later
shown to depend upon retinal position of
stimulation, stimulus wavelength, and a
host of other variables. But from comparative and human work, the general conclusion was that rods have a much lower
temporal resolution than cones, and this
has been reasonably confirmed in the
elasmobranch work (Fig. 10). The one
exception is the study by Green and Siegel
(1973, 1975). They demonstrated that the
all-rod retina of Raja can follow stimuli up
to 30 flashes per second, producing a
double-branched curve reminiscent of a
retina provided with both rods and cones.
It should be noted that special conditions
of adaptation were required to obtain the
higher flicker rates, but it is still unusual
Behavioral studies of vision. Psychophysical
iguana (cone)
c
o
man (rod-cone)
shark (rod-cone)
.2 30
gecko (rod)
2
3
4
LOG RELATIVE
5
6
INTENSITY
FIG. 10. Relation between CFF and stimulus intensity in four vertebrate species. The electroretinographic data from the non-human species were taken
under identical conditions and are thus comparable.
The lemon shark data were also confirmed
psychophysically. Human data are shown for reference only. The duplex retinas show a so-called rodcone break while the pure rod and cone retina produce a monotonous curve. Taken from Gruber
(1969).
465
VISION IN SHARKS
studies of elasmobranch vision have been
carried out in conjunction with electrophysiological investigations (i.e.,
Gruber, 1975) and independently (Aronson et al., 1967; Tester and Kato, 1966;
Graeber and Ebbesson, 1972; Graeber,
Ebbesson and Jane, 1973). The only
studies involving visual thresholds and
subsequent generation of visual parameters were those of Gruber and his coworkers (Gruber, 1966, 1967, 1969, 1973;
Cohen et al., 1977; and Gruber and
Hamasaki, in prep.)- These investigations
were designed to separate the relative contribution of rods and cones to vision in the
lemon shark, Negaprion, and have provided evidence for extremely sensitive nocturnal vision as well as a daylight (photopic) visual mechanism in at least this
species. The experiments have also provided quantitative data on the limits of
vision in this animal. A complete review of
this work can be found in Gruber (1975).
Several studies on light-entrained
periodic activity including laboratory experiments on circadian rhythms have been
carried out by Nelson and his colleagues
(Finstad and Nelson, 1975; Nelson, 1974;
Nelson and Johnson, 1970). Complementary field investigations have demonstrated
the importance of light levels on activity
1968, 1969) has shown that the pineal eye
of Scyliorhinus is provided with rather typical photoreceptors whose structure conforms to the criteria set up by Nilsson
(1964) for retinal cones. Among the six
other cell-types comprising the pineal of
Scyliorhinus were a few ganglion cells which
appeared to project tracts to the posterior
and habenular commissures of the brain.
On this basis, Rudeberg (1969) concluded
that the pineal of sharks is a photosensitive
organ. Yet, unlike other fish, the skull over
the pineal endplate did not appear modified for light transmission to the epiphyseal photoreceptors. However, in a careful
study of the light transmission properties
of the chondrocranium, Gruber et al.,
(1975) demonstrated that a "window" over
the epiphysis permits about seven times
more light to strike the epiphyseal photoreceptors of Negaprion, Mustelus, and Car-
charhinus compared to surrounding areas
of the brain.
In an electrophysiological study, Hamasaki and Streck (1971) demonstrated the
extreme photosensitivity of the epiphysis
in Scyliorhinus. Stimulation of the pineal by
one-second flashes of light evoked a slow
positive potential lasting up to 15 seconds.
All spike activity in the ganglion cell tracts
was promptly inhibited. The illumination
6
rates in the sharks Heterodontus, Cephaloscyl- at threshold of this response was 4 x 10~
2
lium, Squatina, and Prionace. In all cases a lm/m , which is far below ambient moonmarked nocturnality was demonstrated. In light and even approaches the sensitivity of
one example, a horn shark remained ac- the lateral eye. The spectral sensitivity of
tive for over 10 days in darkness, ceasing this system is very similar to that of the
swimming immediately upon return to lateral eye (peaking at about 500 nm) and
light. However, not all sharks are noctur- is probably based upon rhodopsin. Why
nal. Based upon field observations, Hob- the pineal receptors are morphologically
son (1968) and Starck (1968) believe that cone-like but behave like rods and contain
Carcharhinus and Negaprion, respectively, rhodopsin is not clear. The exact role of
are crepuscular or equally active during the pineal eye in the activities of the shark
daylight. Clearly, further observations are is also unknown.
needed to resolve the question of periods
of peak activity in the elasmobranchs.
CONCLUDING REMARKS
In the short space allotted I have been
able to review only the highlights of the
In addition to well-developed lateral visual system in the elasmobranchs. Yet,
eyes, elasmobranchs possess an extremely the overall impression is that evolution has
sensitive median or pineal eye, the epiphysis provided many of these animals with a
cerebri (Studnicka, 1905). Recent anatomi- high degree of visual development and
cal evidence (Altner, 1965; Rudeberg, capacity. This is clearly different from the
Structure and function of the median eye
466
SAMUEL H. GRUBER
viewpoint of the older literature, in which lex visual system would enable it to see in
sharks were labeled as "swimming noses" daylight. The weak link in this hypothesis
with crude sensory organs and a poor formation is our almost complete ignorvisual system. The increasing importance ance of field behavior of these animals (see
in visual science of elasmobranchs as ob- Gruber and Myrberg; Nelson, this Voljects of study has been amply demonstrat- ume). In addition, field studies concentrated by the number and quality of laboratory ing on a particular sensory modality are
studies published within the past fifteen conceptually difficult to design. How
years. These investigations have provided might one assess vision in an uncontrolled
concrete information on structure, multi-stimulus environment? However,
mechanisms and biochemistry of the visual with knowledge of the limits of vision
system, and the resultant data base has derived from controlled studies and comradically altered our views on vision in bined with an overview of ecology and
sharks. The data have also provided a basis behavior, insight into the role of vision in
for insight into the private perceptual the lives of sharks could be gained.
world or Merkwelt of sharks, a necessary
first step in attempting to understand their
normal behavior.
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