Corneal power and underwater accommodation in great cormorants (Phalacrocorax carbo sinensis)
1 Department of Biology, University of Haifa, Oranim, Tivon 36006,
Israel
2 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY
14850, USA
* Author for correspondence (e-mail: gkatzir{at}research.haifa.ac.il)
Accepted 13 November 2002
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Summary |
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Key words: keratometry, IR photorefraction, lens, cornea, accommodation, refractive power, amphibious vision, great cormorant, Phalacrocorax carbo sinensis
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Introduction |
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The refractive power of the cornea underwater is virtually lost, as the
media bathing its inner and outer surfaces (the aqueous humor and water,
respectively) are of similar refractive indices. In a submerged eye, the lens
becomes the sole agent for accommodative adjustments and must provide for the
refractive power lost by the cornea if image quality is to be retained
(Fernald, 1990;
Land, 1990
; but see
Pettigrew et al., 2000
). The
lenses of fish (Fernald, 1990
),
amphibians (Mathis et al.,
1988
), penguins (Sivak,
1980
) and seals (Sivak et al.,
1989
) tend to be spherical with an internal gradient of refractive
indices. This allows for the continuous refraction of light within the lens
itself and not merely at its surfaces
(Fernald, 1990
;
Sivak et al., 1989
). These
lenses exhibit a high level of correction for spherical aberrations
(Fernald, 1990
;
Land, 1990
;
Sivak and Millodot, 1977
).
In all vertebrate classes, there are species that perform visually guided
motor tasks in both air and water. Eyes that are better adapted for
terrestrial vision and are emmetropic (i.e. in focus) in air tend to be
hyperopic (i.e. far sighted) underwater, while eyes better adapted for aquatic
vision and are emmetropic in water will tend to be myopic (i.e. near sighted)
in air. If retinal image is to remain sharp in both media, the eye must cope
with large changes in external refractive indices
(Martin, 1998;
Sivak and Millodot, 1977
;
Howland et al., 1997
;
Howland and Sivak, 1984
;
Land, 1990
;
Fleishman et al., 1988
;
Glasser and Howland, 1996
).
The corneas of penguins (Sphenisciformes) and albatrosses
(Procelariiformes) are relatively flattened and have refractive powers lower
than those of avian species of comparable eye size (Tables
3,
4). Such corneas suffer
relatively little loss of power when submerged. Penguins, with corneal
refractive powers of 11-30 D (Sivak and
Millodot, 1977; Howland and
Sivak, 1984
) are emmetropic in air and slightly hyperopic in
water, which is well within the compensatory power of the lens
(Sivak, 1976
;
Sivak et al., 1987
;
Howland and Sivak, 1984
;
Table 3). Seals have flattened
corneas and, in common with penguins, make use of spherical lenses
(Sivak et al., 1989
).
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Several other bird species that are pursuit-divers have strongly curved
corneas. Such corneas have a high refractive power in air, and, indeed,
pronounced capacities for lenticular accommodation are observed in these
species, indicating their capacity to compensate for corneal loss of power
during dives. Accommodation in these species involves considerable changes in
lens curvature and is associated with highly developed muscular mechanisms. In
his pioneering studies, Hess (1909, 1913; cited in
Glasser and Howland, 1996)
demonstrated that, in cormorants (Phalacrocorax sp.), the lens, when
stimulated electrically, undergoes pronounced changes in shape. The changes
result in the lens being literally squeezed into, and partially through, the
rigid iris by the ciliary muscle. The front surface of the now strongly curved
lens produces a region of high refractive power (>60 D). Subsequent studies
have verified the extent of lenticular accommodation (e.g.
Sivak et al., 1977
;
Levy and Sivak, 1980
;
Table 3), although there is
still no agreement as to the precise muscular mechanisms involved.
Two important aspects have been left open in studies of lenticular
capacities in pursuit-diving birds. First, a prevailing assumption to date is
that, when diving, pursuit divers such as cormorants and mergansers
(Mergus spp.) keep the retinal image sharply focused. However, this
assumption has not been verified experimentally to date, while examples from
other vertebrate groups indicate that pursuit and capture of fish is not
necessarily coupled with high visual acuity. Thus, while otters (Amblonyx
cinerea cinerea; Schusterman and
Barrett, 1973; Balliet and
Schusterman, 1971
) and sea lions (Zalophus californianus;
Schusterman and Balliet, 1970
)
retain similar grating acuity in air and in water, crocodiles (including
Gavialis, which feed exclusively on fish) do not accommodate
underwater (Fleishman et al.,
1988
), implying that crocodiles can manage with blurred
images.
The second aspect relates to methods of experimentation on which
conclusions on accommodation have been drawn. In most experiments, drugs or
electrical stimulation were employed to elicit accommodation, or conditions of
submergence were achieved by forcibly holding the birds' head underwater (e.g.
Goodge, 1960;
Sivak et al., 1977
;
Levy and Sivak, 1980
;
Table 3). To the best of our
knowledge, states of accommodation during voluntary dives of birds have been
recorded, to date, in penguins only
(Howland and Sivak, 1984
;
Sivak et al., 1987
) and not in
bird species that are said to have curved corneas and may employ pronounced
lenticular accommodation.
In the present study, we aimed to determine, in great cormorant, P. carbo sinensis, (1) the refractive power of the cornea in air, and thus the extent of compensatory power required by the lens upon submergence, and (2) the capacity to accommodate and the refractive range when freely diving.
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Materials and methods |
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Photokeratometry
The photokeratometer used to determine corneal curvature was that described
by Howland and Sayles (1985;
also Howland et al., 1997
). It
consisted of a 35 mm Nikon SLR camera, with an f/1.2, 55 mm Nikkor lens
mounted on a 31 mm extension tube, and operated at full aperture to minimize
depth of field. Eight light sources (the tips of fiberoptic light guides, 1.5
mm diameter) were embedded in an aluminum ring, 75 mm in diameter, at the
radii of a 67.5 mm circle around the optic axis, and the ring was mounted on
the camera's objective lens. The proximal tips of the light guides were held
in a bundle directly in front of an electronic flash.
For calibration, we used a set of 10 steel ball bearings of various
diameters. Each ball was measured to the nearest 0.05 mm using vernier
calipers, and its photograph (Kodakchrome/Ektachrome 100/200 ASA) was taken
with the photokeratometer mounted on a tripod. The focus of the camera lens
was set at infinity, yet, because of the extension tubes, the actual focus was
at 150 mm. In taking the photographs, the camera-to-ball distance was adjusted
for the sharpest image. For each ball, the distances between opposite
reflections of the eight keratometeric reflection points were determined with
a measuring microscope accurate to 1.0 µm. This resulted in four
measurements along the 0°, 45°, 90° and 135° meridians. The
mean of the four measurements was calculated and we then regressed the ball
bearing diameters against the mean reflection distances measured on the film
plane. We used this regression equation to estimate the corneal radii
(corresponding to half of the diameters of the calibration ball bearings). To
determine the dioptric power, F, of a cornea (measured in diopters),
the following equation was used: F=337.5/R, where R
is the corneal radius (measured in mm). This equation expresses the power of
the human cornea as a function of the radius of its first surface
(Borish, 1995) and is
frequently applied in animal work.
The bird to be tested was held by one investigator, while another investigator photographed each of the bird's eyes with the hand-held photokeratoscope. The room was lit by two 60 W incandescent bulbs, positioned 2.5 m above the bird. In taking the photographs, the camera-to-bird distance was adjusted for the sharpest image. Each eye of each of the five cormorants was photographed 12 times. Pronounced eye movements and rapid flicking of the nictitating membrane resulted in a proportion of the slides being unsuitable for analysis. For each eye of each bird, the two slides that provided the sharpest and best-centered images of the photokeratometric light reflections were used for extracting the values of the distances between opposite reflections along the four meridians.
Infrared photorefractions
Photoretinoscopy was performed on the cormorants to measure their natural
accommodation with the use of an infrared (IR) video photoretinoscope
(Fig. 1). The principles
underlying the retinoscope are detailed elsewhere
(Schaeffel et al., 1987). In
brief, the IR retinoscope is based on a light source adjacent, and eccentric,
to a video-camera lens' axis that projects light rays parallel to the camera's
axis and records the reflection from the fundus. IR is used to minimize
disturbance to the animals. The reflected light appears as a crescent in the
pupil, and the position of the reflex indicates the sign of the defocus
relative to the camera. In hyperopia, the reflex appears at the top of the
pupil, while in myopia the reflex appears at the bottom of the pupil. The
amount of defocus (D) may be obtained from the size of the reflex:
D=E/(2xAxDFxR),
where E is the eccentricity of the light source, A is the
distance of the camera to the eye, DF is the dark fraction in the
pupil and R is the pupil radius (all dimensions in meters). To
improve the precision of the measurements, light sources at five different
eccentricities are employed in a row, consecutively providing five different
crescents. Due to the high mobility of the birds' head and eyes, no attempt
was made to verify the amount of defocus by the use of correction lenses.
Filming was conducted when the bird was 1.2-1.4 m from the camera lens, and
the horizontal distance of the eye to the glass wall was approximately 5 cm.
This provides an optical distance (distance in air + distance in water/1.33)
of approximately 1.0 m.
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Seven cormorants were tested over two consecutive days (Table 1). A single bird was allowed into the test room from its home cage and was encouraged to climb a short sloping gangway, leading to a test aquarium. The room was lit by four 100 W lamps and by indirect daylight from the open door. The aquarium (80 cmx40 cmx50 cm; length x width x height) was kept three-quarters full of water, and the bird could perch comfortably on its narrow side. One investigator then held a small fish (Tilapia sp. or carp Cyprinus carpio) at the side farthest from the bird and moved it to attract the bird's attention. He then dipped the fish and kept it underwater. The bird would submerge its head, search for the fish and capture it. Often, the fish was held against the outside of the aquarium glass wall, and, if the bird attempted to capture it from within, it was rewarded with a fish. The cormorants were acquainted with this procedure and were continuously rewarded for climbing the gangway and searching for fish in the experimental aquarium. During the week preceding the tests, they were fed daily in this manner.
As the cormorant climbed the gangway, the second investigator, positioned so as to view the aquarium's long axis and to be level with the water surface, filmed the bird. Filming was with the video camera held by hand, with the filming axis perpendicular to the plane of approach of the bird. Filming was continuous and conducted for as long as the bird searched for fish. The termination of a test session was when the bird left the aquarium and attempted to get back to the home cage. Video films (Sony 8 mm) were digitized, and selected sequences were captured using Adobe Premier 6. From these sequences, the states of accommodation were determined.
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Results |
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Photorefraction
All cormorants readily climbed onto the side of the test aquarium and took
fish from the hand, both in air and underwater. They searched for fish
underwater and attempted to capture them, even when the fish were presented
beyond the aquarium's glass wall. Approximately 300 sequences of accommodation
footage were acquired for the five cormorants tested for both air and
water.
Photorefraction in air
In most recorded sequences, the eyes appeared to be in a state of
hyperopia, while emmetropia and myopia were observed less frequently. An
example of a state of myopia, with a bird holding a fish halfway down its bill
immediately prior to swallowing, is depicted in
Fig. 3B. Mean pupil diameter in
air during myopia and hyperopia did not differ (9.9±0.9 mm and
9.7±1.1 mm, respectively). Mean refractive states ranged from -0.44 D
to +0.45 D (Table 2).
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Photorefraction in water
The eyes appeared to be focused hyperopically relative to the camera, while
emmetropia and myopia were observed less frequently. Mean pupil diameter did
not differ between myopia and hyperopia (8.7±2.3 mm and 8.9±0.7
mm, respectively). Mean refractive states ranged from -0.56 D to +0.50 D
(Table 2). Most sequences of a
state of myopia occurred when the target (fish) was close to the plane of the
eye, one to two bill lengths (approximately 6-12 cm) away
(Fig. 3B,C).
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Discussion |
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The demanding nature of amphibious vision in mammals (e.g.
Ballard et al., 1989) and birds
(e.g. Glasser and Howland,
1996
) has attracted attention for nearly a century
(Glasser and Howland, 1996
).
Hess (1909, 1913) first elucidated the capacity of the highly pliable lens of
a diving bird (cormorant) to undergo dramatic changes in shape through the
exceptionally well-developed iris and ciliary muscles. Hess (loc.
cit.) concluded that these changes compensated for the approximately 60 D
of corneal loss of power caused by submergence. Subsequent studies indicated
that, in penguins, the corneas tend to be flattened and a penguin's lens must
consequently accommodate for 10-30 D lost during eye submergence
(Howland and Sivak, 1984
).
In pursuit-diving bird species (but not penguins) tested to date, the
corneas seem to be curved and there exists a capacity for marked change in
lens shape through the action of highly developed intraocular muscles. Thus,
in the hooded merganser (Mergus cucullatus), red headed duck
(Aythya americana), double crested cormorant and black guillemot
(Cepphus grylle), the ranges of accommodation span 40-80 D
(Table 3), while in non-divers
[e.g. pigeon (Columba livia) and chicken (Gallus gallus)],
the total range of accommodation is approximately 10-20 D. A high range of
accommodation is also found in the dipper (Cinclus mexicanus), a
passerine that captures insects underwater
(Goodge, 1960). The capacity
of these species to accommodate underwater has been supported, to date, by
anatomical and histological characteristics of the intraocular muscles and by
changes in the lens shape elicited by stimulation of intraocular muscles.
The ciliary muscle in birds comprises three muscle fiber groups: the
anterior muscle group (Crampton), the posterior muscle group (Brücke) and
the internal muscle group (Müller). The Crampton muscle group is
responsible for enhancing the steepness of the central cornea and thus
increasing the corneal power, the Brücke group reduces the lens radius of
curvature, while the Müller group affects both cornea and lens. Comparing
four avian species, Pardue and Sivak
(1997) found that, in the
hooded merganser, the majority of the ciliary muscle fibers are in the
posterior and internal fiber groups, suggesting predominance of lenticular
accommodation. By contrast, in the pigeon, kestrel (Falco sparverius)
and chicken, the majority of muscle fibers are in the anterior muscle group,
suggesting emphasis on corneal accommodation. Hooded mergansers also exhibit
an especially large number of muscle fibers in the peripheral iris, the region
that is supposed to be responsible for lens squeezing
(Glasser et al., 1995
). These
authors conclude that mergansers have the largest structures associated with
lenticular accommodation of the species studied.
Accommodation in the hooded merganser is achieved by the pressure of the
malleable lens against the rigid iris plate, thus resulting in the bulging of
the lens through the pupil (Levy and
Sivak, 1980). The iris sphincter muscles presumably aid the
formation of a rigid ring or plate against which the lens is pushed to create
lenticonus (Sivak and Vrablic,
1982
). Studies in the cormorant, double crested cormorant, dipper
and red headed duck (Hess, 1909, 1913;
Goodge, 1960
; Sivak et al.,
1977
,
1985
;
Pardue and Sivak, 1997
) lend
support to the existence of an iris accommodative mechanism capable of
producing dramatic lens changes in these species. Such phenomena were not
observed in non-diving species.
Curved corneas coupled with strong muscular mechanisms have been
demonstrated in otters as well as in several species of pursuit-diving birds.
Sea otters (Enhydra lutris;
Murphy et al., 1990), with a
corneal refractive power of 59 D, are nearly emmetropic in both air and water.
Based on their findings that the iris musculature, meridional ciliary muscle
and corneal scleral plexus are highly developed in this species, Murphy et al.
(loc. cit.) concluded that sea otters rely on a powerful
accommodation mechanism for underwater vision. Similar conclusions were drawn
for the Canadian river otter (Lutra canadensis;
Ballard et al., 1989
), although
in this species the states of accommodation while diving were not
recorded.
Several studies point to a marked constriction of the pupil while
accommodating. Thus, Levy and Sivak
(1980) reported a fivefold
decrease in pupil diameter in the red headed duck and a threefold decrease in
the hooded merganser during accommodation stimulated with nicotine sulfate
(Table 3). Reduction of pupil
aperture increases image quality and may also be part of the formation of a
rigid plate by the iris, against which the lens is pressed. However, in the
present study, we observed only a slight constriction of the pupil
(Fig. 3;
Table 2), suggesting that the
coupling of pupillary changes and underwater accommodation should be further
investigated. The initial large pupil diameter seen here was most probably
related to the dim illumination in the room, because, under bright light,
pupil diameters are less than 2 mm (G. Katzir and H. C. Howland, personal
observation).
Certain important areas of amphibious vision are, however, in need of
further investigation. One area pertains to the actual refractive power lost
upon submergence in pursuit-diving birds. Most studies imply that
approximately 60 D of corneal refractive power is lost upon submergence, yet
data on corneal curvature and refractive power in air are usually lacking
(Tables 3,
4; but see Sivak et al.,
1977,
1985
). While the results in
the present study indicate that, indeed, the corneal refractive power of the
great cormorant may exceed 60 D, both intra- and interspecific differences are
expected as a function of eye size.
Another area is related to the manner of eliciting accommodation. Two
approaches have been used to determine states of accommodation: (1) by
recording naturally occurring changes in accommodation from a distance and (2)
by stimulating intraocular muscles. The former method, using photorefraction
and retinoscopy, was mostly employed in studies of penguins (e.g.
Howland and Sivak, 1984;
Sivak and Millodot, 1977
;
Sivak et al., 1987
;
Table 4), while the latter was
used predominately for other pursuit-diving species
(Table 3). Thus, studies that
demonstrated changes in the lens during accommodation were performed by
electrical or chemical stimulation of the eyes of anaesthetized or dead birds
(Hess, 1909, 1913; Goodge,
1960
; Sivak et al.,
1985
; Levy and Sivak,
1980
). Simulation of submergence was obtained by forceful holding
of birds' heads underwater (Goodge,
1960
; Sivak et al.,
1977
,
1978
). Such methods may have
yielded results somewhat different from naturally occurring phenomena. For
example, the results in the present study indicate that, in the great
cormorant, transitions from hyperopia in air to myopia underwater, i.e. over
60 D, may occur within 40-80 ms (1-2 frames), while such changes obtained by
electrical or chemical stimulation were an order of magnitude longer
(Sivak et al., 1985
).
Moreover, while states of emmetropia or myopia underwater were retained for
only tens of milliseconds in the present study, those achieved through
electrical stimulation (Sivak et al.,
1985
) were in the order of hundreds of milliseconds.
Finally, visual performance underwater must be considered. Amphibious
animals that actively pursue fish underwater are assumed to retain a sharp
image on the retina. However, neither the eyes of crocodiles
(Fleishman et al., 1988) nor
those of the amphibious snakes studied by Schaeffel and Mathis
(1991
) were well accommodated
underwater, and, while clawless otters (A. cinerea cinerea) are
emmetropic in both air and water, their acuity in either media is not high
(Schusterman and Barrett,
1973
). Thus, during underwater pursuits, animals may `make do'
with blurred images or make use of non-visual information. Moreover, visual
acuity, the capacity of the visual system to extract detailed information, is
determined not only by the eye's optics but also by the underlying neural
structures (retina and brain), neural processing and the environment. Compared
with air, the underwater light environment has much more deleterious effects
on acuity, due to turbidity, pronounced attenuation and chromatic absorption
of light (Loew and McFarland,
1990
). To date, there are relatively few behavioral studies on
visual acuity, the performance of visually guided tasks
(Schusterman and Barrett,
1973
) and the effects of the underwater light environment in
amphibious animals and none, to the best of our knowledge, in pursuit-diving
birds.
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Acknowledgments |
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