Download “AQUATIC” vs. “TERRESTRIAL” EYE DESIGN. A FUNCTIONAL

Analele Științifice ale Universității „Alexandru Ioan Cuza” din Iași, s. Biologie animală, Tom LXI, 2015
“AQUATIC” vs. “TERRESTRIAL” EYE DESIGN.
A FUNCTIONAL ECOMORPHOLOGICAL APPROACH
Anca-Narcisa NEAGU1 and Ozana-Maria PETRARU1
1
Faculty of Biology, “Alexandru Ioan Cuza” University of Iași, Carol I Bvd, no. 20 A, 700505 Iași, Romania,
[email protected], [email protected]
Abstract. The eye ecomorphological design in vertebrates reflects the environment characteristics and the life
style of species, into an evolutionary context. The light level is considered the decisive factor involved in
morphological, structural and physiological adaptation plan of the camera eye. However, the convergence on
favorable phenotypes principle is available also for the eye design. An “aquatic” pattern emphasizes some
common features present in fish and in secondary aquatic mammals, like cetaceans, and also in some reptiles,
birds and land mammals, concerning the “terrestrial” eye design. A general pattern available for the “aquatic” eye,
emmetropic in water, could be described: a thick and flattened cornea, with a low refractive index, a spherical lens,
with a high refractive power, and a refractive index gradient due to its very high protein core content, a welldeveloped sclera, presence of different types and highly developed tapetum lucidum, an all-rod retina or a roddominante retina, with few cones, sustaining a monochromatic vision, a low density of retinal ganglion cells in
areas with highest spatial resolution and a high spatial summation of rods on the ganglionar cells. The “terrestrial”
eye, emmetropic in air, has as general features: a curved or a strongly curved cornea with a high refractive index,
an elliptical lens, a duplex retina, cone-dominant for diurnal species and rod-dominant for those with nocturnal
habits, presence of foveae typically found in species with acute vision as birds (bifoveate) or primates
(monofoveate), a dichromatic vision for most of mammals, trichromatic vision in human, cat and nocturnal species
of birds to pentachromatic vision in pigeon, the high density of retinal ganglion cells in areas with highest
resolution. An “intermediate” eye design, adapted for terrestrial and aquatic vision, “two-in-one” designs, is also
described: a duplicate cornea, lens, iris and retina could solve the air myopic tendency for the “aquatic” eye and
the underwater hyperopia for the “terrestrial” eye.
Keywords: aquatic, terrestrial, “two-in-one” eye, vision, adaptations, ecomorphology, cornea, retina.
Rezumat. „Ochiul acvatic” vs. „ochiul terestru”. O abordare ecomorfologică și funcțională. Design-ul
ecomorfologic al ochiului la vertebrate reflectă caracteristicile mediului și stilul de viață al speciilor, într-un
context evolutiv. Lumina este considerată factorul decisiv implicat în adaptările morfologice și funcționale ale
ochiului. Cu toate acestea, principiul convergenței fenotipurilor favorabile este valabil și pentru design-ul globului
ocular. Un model de „ochi acvatic” prezintă o serie de trăsături comune, convergente, ale globului ocular la pești și
la mamiferele secundar acvatice, ca cetaceele, sau, pentru modelul „terestru”, trăsături comune ale ochiului la
păsări, reptile și mamifere. Un model general valabil al „ochiului acvatic”, emetrop în apă, include: o cornee
groasă, aplatizată, cu un indice de refracție redus, un cristalin sferic, cu un indice de refracție ridicat, datorită
conținutului mare în proteine al miezului cristalinian, dar și unui gradient al indicelui de refracție dinspre centru
spre periferie, o sclerotică groasă, prezența a diferite tipuri bine dezvoltate de tapetum lucidum, o retină formată
numai din celule cu bastonaș sau cu celule cu bastonaș dominante, cu foarte puține celule cu con, o vedere în
general monocromatică, o densitate redusă a celulelor ganglionare în zonele retiniene cu acuitate ridicată, și cu o
mare rată de sumație a celulelor cu bastonaș pe celulele ganglionare. „Ochiul terestru”, emetrop în aer, are ca
trăsături generale: o cornee curbată sau foarte curbată, cu un indice de refracție ridicat, un cristalin eliptic, convex
sau biconvex, o retină de tip duplex, având celule cu con dominante la speciile diurne și celule cu bastonaș
dominante la speciile cu regim de viață nocturn, prezența uneia sau a două arii retiniene cu acuitate vizuală ridicată
de tip fovea, la speciile cu acuitate vizuală ridicată ca păsările (bifoveate) sau primatele (monofoveate), cu o
vedere bicromatică la cele mai multe specii de mamifere, tricromatică la om și la speciile nocturne de păsări, dar
pentacromatică la porumbel, cu o mare densitate a celulelor ganglionare în retină, în zonele cu acuitate vizuală
ridicată. Un design intermediar care reunește trăsături comune ochiului acvatic, dar și celui terestru, pe principiul
doi ochi într-unul singur este, de asemenea, descris: două porțiuni ale corneei, irisului, cristalinului și retinei, fapt
care rezolvă acceptabil tendința „ochiului acvatic” de a fi miop în aer și a „ochiului terestru” de a fi hipermetrop în apă.
Cuvinte cheie: ochi acvatic, terestru și „doi în unu”, vedere, adaptări, ecomorfologie, cornee, retină.
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Introduction
Vision is an important source of information and the visual adaptations reflect well
the ecological diversity in vertebrate world, predicting differences in habitat (aquatic,
amphibious/semi-aquatic and terrestrial, dim or light environments), diurnal, nocturnal or
cathemeral behavior, predator or prey lifestyle and the ontogenetic growth of eye
(Litherland et al., 2009). The “terrestrial”, “intermediate” and the “aquatic” designs of eye
could be described from ecomorphological point of view and studied as a good example for
sustaining the “eco-devo-evo” theory (Gilbert & Epel, 2009). The eyes reflect the
environment and the life style of species (Akat & Arikan, 2013), into an evolutionary
context. Being an important source of information in aquatic and also in terrestrial world,
the eye sustains important physiological processes, such as feeding, locomotion and
reproduction. Lifestyles affect also the overall eyeball shape (Schmitz & Motani, 2010).
In 1975, Kerr and James, examining the relationships between morphological
features of organisms and their environment, introduced the term “ecomorphology” (Bock,
1994) as an “analysis of the adaptativeness of morphological features and all depend,
correlated topics such as the comparisons of adaptations in different organisms,
modification of adaptive features due to competition and other causes, structure of
ecological communities, diversity within taxa, etc.”, emphasizing that the ecomorphology is
a different field from the functional morphology because is based on the biological role
rather than the function concept, organisms must be observed in their natural environment
not in captivity conditions and ecomorphology depends on the functional morphology
studies, whereas the functional morphology is independent of any information from
ecomorphology.
The functional morphology of the eye could be considered similar in all
vertebrates, but the organogenesis and ecomorphological, structural and functional
complexity varies greatly according to the specific ecological context of each species.
The ecomorphological design of the eye reflects and sustains its physiological
activities (refraction power, biochemical reactions, accommodation etc.) during the
interactions between photoreceptor neurons and the photons of light. Light is the decisive
factor affecting the morphology and structural plans of the eye (Schmitz & Weinwright,
2011).
According to Gilbert & Epel (2009), numerous environmental agents contribute to
producing a phenotype: temperature, nutrition, pressure and gravity, predators or stress, the
presence/absence of conspecifics. Water is not a good visual medium. Light is attenuated in
water and turbidity accentuates this problem. Besides light and turbidity, there is a variety
of other factors that affect the “aquatic” vision: temperature, pressure, light scattered from
planktonic organisms, scales and particles suspended in the water and bioluminescence
(Landgren et al., 2014). The “terrestrial” eye also adapts to variable light
environments, strongly depending on the diurnal or nocturnal activity patterns of organisms
(Schmitz & Motani, 2010). An “intermediate” amphibious/semi-aquatic eye design could
be described for vertebrates living both in water and in air and dealing with a large
variation of the really diverse environmental factors.
This paper offers a lot of photomicrographs of the eye’s structures, compared and
integrated with the reviewed published results, and three types of eye designs were
documented: “terrestrial”, “aquatic” and “intermediate” or “two-in-one”.
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Analele Științifice ale Universității „Alexandru Ioan Cuza” din Iași, s. Biologie animală, Tom LXI, 2015
Material and Methods
“Aquatic”, “terrestrial” and “intermediate” eyes from dead animals were used for
this study: for aquatic pattern, Cyprinus carpio; for intermediate amphibious eye, Rana
ridibunda; and for terrestrial pattern bird eye, Columba livia, reptile eye, Lacerta viridis
and mammal eye: Bos taurus and Ovis aries. Each eye was removed from the orbit and
fixed with 10% formaldehyde solution. Ethyl alcohol was used for dehydration in a series
upgrading from over night of 60%, and 2 h in 70%, 80%, 90%, 95% and 100%. After
clearing with xylene, some samples were embedded in paraffin. Other eyes were directly
sliced using a Leica cryotome CM 1850, in the Laboratory of Histology. The frontal,
sagittal or transverse serial sections were taken and stained with hematoxylin & eosin (HE).
The micrographs were taken with a Confocal Laser Scanning Microscope CLSM - Leica
TCS SPE DM 5500Q, using different types of light microscopy (bright field, fluorescence
and DIC - differential interference contrast).
Results and Discussion
“Terrestrial” eye ecomorphological design
“Terrestrial” eye (Table 1) is emmetropic in air and tends to be hyperopic
underwater (Katzir & Howland, 2003). The terrestrial species acquire a predominant
spherical form of the eye. Among the terrestrial vertebrates, the ostrich has the largest eye
(50 mm in diameter), twice that of the human eye (Jones et al., 2012). Between the
“terrestrial” eyes, the bird’s eye has the greater visual acuity, birds being exceptionally
visual animals. Bird eyes are emmetropic on land, and cornea plays an important role in
accommodation. The avian eye is very large, representing about 50% of the cranial volume
(Jones et al., 2007), allowing a large image projected onto the retina. Some predator birds
have large eyes directed frontally and prey species usually have smaller, more flattened and
laterally places eyes.
Cornea and lens forms a complex unity, transparent and equipped with refractive
power, known as a refracton (Jonasova & Kozmik, 2008). Refraction occurs when light
radiation passes from a medium with a certain refractive index (air – 1) into a medium with
a different refractive index (aqueous humor – 1.33). The refractive power is expressed in
diopters (D). In the “terrestrial” eye cornea is curved or even strongly curved in nocturnal
birs, with a very high refrative index. In human (Gislen et al., 2003) and birds (Jones et al.,
2007), 2/3 of the refractive power of the eye is assured by the curved corneal surface.
The structure of cornea in most vertebrates is similar. It consists of an anterior
corneal epithelium, an underlying basement membrane – Bowman’s membrane, a stroma, a
basement membrane – Descemet’s membrane, and an endothelium (Fig. 1 A-F).
Diurnal, some nocturnal and crepuscular terrestrial animals have large, circular
pupils and monofocal lens. In mammals, a circular pupil is correlated with monofocal optic
system (Canis lupus lupus, C. lupus familiaris, Panthera leo, P. tigris) or with a multifocal
optical system (Mus musculus) (Malmström & Kröger, 2006; Lind et al., 2008). The lens
consists of a thin acellular capsule, a cuboidal monocellular epithelium which provides
dehydration and maintains sodium and potassium gradients by an active sodium-potassium
adenosine triphosphatase pump. The fibers form the cortex and the core’s lens, in avian lens
are separated by vesicula lentis.
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Some nocturnal and diurnal reptiles (i.g. ophidians) have a spherical lens (Rival et
al., 2015; Hall et al., 2012) or a biconvex one. In birds, the lens is convex and differs from
that of mammals.
The nocturnal eye adapted also to diurnal conditions have usually a slit vertical
pupil (geckos, snakes) that enables a more effective closure, with a maximum pupillary
dilatation under scotopic light (Hall et al., 2012).
In diurnal birds the pupil is circular or oval and in cathemeral species is slit
vertical (Banks et al., 2015).
Tapetum lucidum is a biological intraocular coat or a reflective screen with a
special microanatomy, responsible for "glow" feature of the vertebrate eye. Its role is to
increase the amount of light that reaches the photoreceptor cells in the retina. Tapetum
provides only 30% of the light that returns to the photoreceptor cells, 70% of radiation light
reaches directly to the photoreceptor cells. Tapetum lucidum is absent in birds, primates,
squirrels and pig. Some terrestrial mammals present a choroidal tapetum fibrosum or
cellulosum.
Vision required functional integrity of different retinal cell types. The retina of
vertebrates consists of ten layers: retinal pigmentar epithelium (RPE), photoreceptor cell
layer (PCL), outer limiting membrane (OLM), outer nuclear layer (ONL), outer plexiform
layer (OPL), inner nuclear layer (INL), inner plexiform layer (IPL), ganglion cell layer
(GCL), nerve fiber layer (NFL) and the inner limiting membrane (ILM) (Fig. 1 K, L).
Reptiles and birds have a blood supply as a substitute for the anangiotic retina: in
reptiles – conus papilaris (Fig. 1 H) and in birds (Fig. 1 G) – pecten oculi.
Conus papilaris is considered a well developed choroid which contains venous
sinuses, melanocytes with melanin pigmentation (spherical melanosomes, Fig. 1 J) and
connective tissue.
The pecten oculi is an anatomical structure of the avian eye. Morphologically, it
consists by a base (situated in the lower posterior temporal quadrant of the fundus (Kiama
et al., 2001), a vary number of pleats (15-16 in diurnal bird Columba livia; 5-6 in nocturnal
bird Bubo bubo africanus) and a bridge. There are tree types of pecten: the conical type
(pecten oculi conicus), the vaned type (pecten oculi vanellus) and the pleated type (pecten
oculi plicatus) (Pourlis, 2013). Structurally, it is composed by many blood vessels,
melanosomes protecting the blood cells against UV radiation, connective tissue and a
vitreopectinal membrane (Fig. 1 I). This blood supply structures provides oxygen for the
anangiotic retina, maintains the acid-base balance and a constant intraocular temperature.
The retina of diurnal birds is thicker than the most of vertebrates (630 µm thick in
diurnal bird Circaetus gallicus and 360 µm in Bubo bubo) (Kiama et al., 2001).
Birds have a duplex-retina, cone-dominant in diurnal birds and rod-dominant in
nocturnal ones. The double-cone is the dominant photoreceptor in diurnal animals. The
most birds are tetrachromats, having multiple spectral clasess of cones with spectral
sensitivity in the region of red, green, blue and ultraviolet, but the diurnal birds could be
possible pentachromic (pigeon) and the nocturnal birds are mainly trichromatic, having also
primarily rods in foveas.
Foveae are typically found in species with a great visual acuity, absolutely
necessary for their survival. Birds are usually bifoveate, mainly having a centrally located
fovea - with a high photoreceptors density, for monocular vision, and a temporal smaller
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fovea, for binocular vision. Nearly all avian species present foveae. Primates are the only
foveate mammals, many animal species being afoveate (Jones et al., 2012).
On terrestrial mammals, retina has been described two areas characterized by a
high density of ganglion cells: fovea centralis – in mammals with frontal view (including
human), and a horizontal strip – in mammals with lateral eyes. Also in some birds, the
central and temporal fovea is encompassed by a horizontal visual streak.
“Aquatic” eye ecomorphological design
The “aquatic” (Table 2) eye is emmetropic underwater and tend to be myopic in
air (Katzir & Howland, 2003; Jones et al., 2012). The challanges for an “aquatic” eye in
order to mantain the visual aquity are diverse: turbidity, attenuation and chromatic
absorbtion of light with depth, temperature and underwater pressure.
In some species of epipelagic sharks the eyeballs are situated lateral, and dorsolateral, in some benthopelagical species. The eyeball form is predominantly spherical in
fish, flattened – hemispherical in cetaceans, tubular in some mesopelagic species (Partridge
et al., 2014). The size and location of the eyes are related to the amount of light which
decreases exponentially with depth; 1% of the surface light reaches a depth of 255 m (El
Said & El Bakary, 2014). A larger eye presents an increased sensitivity to light due to a
higher degree of summative neural convergence of signals from multiple photoreceptors,
stimulated by a greater amount of light. The diameter of scotopic reef species teleost eyes is
1.4 times higher than photopic species (Schmitz & Weinwright, 2011). Also nocturnal
species of fish present well developed eyes and retina compared with diurnal species
(Darwish et al., 2015).
The ecomorphology and ecophysiology of cetacean eye, for example, are also
significantly different from those in terrestrial mammals (Mass & Supin, 2007).
Underwater, the refractive power of the cornea is negligible, the water and the
aqueous humor having almost the same refractive index. Lens remain the main structure to
assure the accommodative adjustements. The “aquatic” eye has a cornea usually flattened
(Gonzales et al., 2014). The refraction index of “aquatic” cornea is about the same as that
of water: 1.33. In cetaceans the cornea has also an appropriate refractive index: 1.37 (Mass
& Supin, 2007).
The anterior corneal epithelium surface is covered, particularly in fish, with
cytoplasmatic projections such as: microvilli – in ratfish Hidrolagus colliei; microvilli and
microplicae – tiger shark Galeocerdo cuvier, spiny dogfish Squalus acanthias (Collin &
Collin, 2001), Mugil cephalus (El Said & El Bakary, 2014); or microholes of about 300 nm,
in Neoceratodus forsteri or Lepidogalaxias salamandroides. The anterior corneal
epithelium is composed of a stratified cuboidal epithelium in teleost fish Siganus javus
(Mansoori et al., 2012), Mugil cephalus (El Said & El Bakary, 2014), and a single cuboidal
row to a short columnar basal cells in aquatic frog Xenopus laevis (Nakayama et al., 2015).
The anterior epithelium of the “aquatic” cornea, as well as epidermis, includes also mucus –
secreting goblet cells. The basal cells from the anterior epithelium of cornea are followed
by several layers of intermediate cells, and one to three layers of flattened apical cells (Fig.
2 A, C). The density of surface cells in the corneal epithelium is greater in aquatic
vertebrates than those in terrestrial or air (Collin & Collin, 2001). In some species of fish
there are two distinct corneal stroma: a dermal one, which continues with the connective
tissue of skin, and a scleral stroma, which continues with the connective dense tissue of
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sclera. Between these two stromas may be a region filled with granular material or mucous
tissue (Collin & Collin, 2001). In fish, sometimes, sclera is accompanied by a cartilaginous
tissue (Fig. 2 F).
Refraction and image formation on the eye “aquatic” retina depends almost
entirely on the lens. In the aquatic eye, the lens are spherical – in elasmobranch and
cetaceans (Mass & Supin, 2007), spherical or elliptical – in teleosts (Darwish et al., 2015),
with a parabolic refractive index: 1.55 in center, 1.35 to periphery (Landgren et al., 2014)
and a high protein content in center – 100%, compared to mammals 40%, and birds 35%
(Jonasova & Kozmik, 2008).
In fish, the pupil autonomously reacts to light (no neural mechanisms are involved
therefore the miofibroblasts reacts directly) (Gonzales-Martin-Moro et al., 2014). The pupil
diameter is about the same as the lens diameter. In cetaceans, the iris presents a
protuberance called operculum, which is contracted or raised in dim light, such that pupil,
as well as other mammals, is circular expended or slightly oval. In high light the operculum
descents so that the pupil takes the form of the letter U. Under high light intensity
conditions, the pupil contracts more and it turns into a double pupil composed of two small
openings in photopic vision (nasal and temporal) (Mass & Supin, 2007).
Elasmobranches inhabit predominantly marine habitats and have largely adapted
eyes for scotopic vision. The photoreceptors are composed by rods (all-rod retina). Some
elasmobranches have mixed cones and rods (duplex-retina) with different proportional
density: 3 rods/1 cone (Dasyatis sabina); 40 rods/1 cone (Trygonorhina fasciata); more
than 100 rods/1 cone (Mustelus canis). Microspectrofotometric measurements showed the
presence of three distinct spectral types of visual pigments of cones, raising a possible
trichromatic vision in sharks.
Teleost fishes show that the PCL is composed mainly of single, duble, and triple
rods (all-rod retina) (Darwish et al., 2015). Some teleost fish are adapted for hight light
vision and possess a duplex retina or a all-con retina. Light and dark adaptation is
accomplished by migration of rod shaped melanosomes in RPE (Fig. 1 B, D).
Melanosomes are considered organelles like lysosomes, containing large amounts of acid
phosphatase (Dell’Angelica et al., 2000), which presents a distribution from the cell body
pigment toward rods. This movement is not present in the mammal’s retina. Under high
light, the eye adapts by movement of melanosomes toward the outer segment of the rods. In
dim light melanosomes are drawn back and the rods are exposed to light. Investigation
revealed also a dark-light adaptation movements of rods. In Lepidocybium flavobrunneum,
retina has two special areas characterized by a high ganglion cell density: a temporal (600
ganglionar cells/mm2) and nasal area (400 ganglionar cells/mm2 (Landgren et al., 2014).
The mammal aquatic eye resemble some fish eye features such as duplex retina
and monochromatic vision. In cetacean retina were found giant ganglion cells (75 µm
comparative to terrestrial giant ganglion cells: 15-35 µm) which suggest high functional
integrity of different retinal cell. In pinnipeds and cetaceans, the photoreceptor layer is
present in one type of con containing L – opsin. The cetacean’s retina is about 2-4 times
thicker than diurnal terrestrial mammals (Mass & Supin, 2007).
“Intermediate” eye ecomorphological design
Gonzales et al. (2014) define this type of eye present to Anableps anableps as:
“two different optical systems integrated in the same eye”; Mass & Supin, 2007, show that:
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“the visual system features adaptation to both aquatic and terrestral habitats” in pinnipeds
or eye “represents an example of terrestrial carnivores to an aquatic life style”, in sea otter.
The “intermediate”, amphibious eye (Table 3), show both terrestrial and aquatic
features, adapted for both environments. In particular, an epipelagic fish, Anableps
anableps, has a double cornea: dorsal – for aerial view, curved and thick, with high
protein, collagen and gycogen content and a high refractive power, that projects light to the
ventral retinal area; ventral – for aquatic vision, flattened, with a low refractive power, that
projects light to the dorsal area of retina (Schwab et al., 2001; Gonzales et al., 2014).
The amphibian cornea (Fig. 2 E) possesses 70-75% of the eye’s total refractive
power (Akat & Arikan, 2013). Several diver bird species have an underwater accomodation
by changing the curvature of the cornea, because “the greather the curvature, the greather
the refractive power is” (Jones et al., 2007). In penguins and albatross, the cornea is
flattened with an accommodatory range from 11D to 30D (emmetropic in air); in great
cormorant, the cornea is curved with a 62-64D (emmetropic in air and water) (Katzir &
Howland, 2003). Some aquatic & terrestrial mammals presents a specialized cornea: central
flat surface as an “emetropic window” with almost similar refraction in water and air (in
pinnipeds) (Mass & Supin, 2007).
The lens of Anableps anableps is also adapted to amphibious vision. The lens is
fusiform, pyriform, oval/egg shape, oblique, adapted for the water light to pass through
major axis and air light through minor axis (Gonzales et al., 2014; Jonasova & Kozmik,
2008; Schwab et al., 2001). Aquatic birds and mammals have spherical (penguin), spherical
or slightly elliptical (pinnipeds) and lenticular (sea otters) lens.
Pinnipeds have developed better cilliary muscle than cetaceans (Mass & Supin,
2007). The teleost fish Anableps anableps presents also two pupilary apertures: dorsal
aerial pupil and ventral aquatic pupil.
The amphibian iris possesses autonomous contractions, as the iris of fish, and also
a nervous mechanisms, as in terrestrial mammals, and the pupil shape can be round,
horizontal, vertical, triangular, star-shaped (Gonzales et al., 2014).
Because the curved cornea lose strongly the refractive power when submerged,
there are two ecomorphological compensatory strategies in diving animals for mentaining
the emmetropic eye in submerssion:
 A passive one, similar with a typical aquatic eye: flatted cornea with a lower refractive
power, for example in some aquatic birds (penguin) or seals, correlated with a
spherical lens; eye suffers relatively little loss of refraction power in submerssion.
 An active one, similar with the strategy of a typical terrestrial eye when submerge:
curved corneas with a high refractive power, for example in sea otters, correlated with
a powerful iris accomodative mechanism, due to highly developed intraocular muscle
(iris and ciliary muscles); eye adapts by lenticular accommodation. The iris
contraction have two consequences: iris become rigid determinig the maleable lens to
be pressed against to it and to curve with an increse of the refractive power and pupil
reduces it aperture increasing the image quality.
The multifocal optical systems are present in aquatic, as well as in crepuscular and
nocturnal vertebrates (Lind et al., 2008).
Due to amphibious life, Anableps anableps retina is split in two: superior and
inferior hemiretina, with 2 different types of opsins.
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Table 1. “Terrestrial” eye ecomorphological design.
Anca-Narcisa Neagu & Ozana-Maria Petraru
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Table 2. “Aquatic” eye ecomorphological design.
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Table 3. “Intermediate” eye ecomorphological design.
Anca-Narcisa Neagu & Ozana-Maria Petraru
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A
B
C
D
E
F
F
Figure 1. A – cornea (Bos taurus) (HE); B – cornea (Columba livia) (HE); C – anterior corneal
epithelium (DIC) (Bos taurus); D – anterior corneal epithelium (DIC) (Columba livia); E –
Descemet’s membrane & endothelium (DIC) (Bos taurus); F – Descemet’s membrane & endothelium
(DIC) (Columba livia); Epi – anterior corneal epithelium; Bc – basal cell layer; Wc – wing cell layer;
S – squamous cell layer; Str – stroma; Fb – fibrocytes; Dm – Descemet’s membrane; End –
endothelium.
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G
H
I
J
KK
L
L
Figure 1. G, I – pecten oculi plicatus (Columba livia) (HE/FLUO); H, J – conus papillaris (Laceta
viridis) (HE/DIC); Bv – blood vessel; Ec – endothelial cell; Er – erythrocytes; Fo – fold; Sm –
spherical melanosomes; K – retina (Ovis aries) (FLUO & DIC); L – retina (Columba livia) (HE);
RPE – retinal pigmentar epithelium; PCL – photoreceptor cell layer; ONL – outer nuclear layer; OPL
– outer plexiform layer; INL – inner nuclear layer; IPL – inner plexiform layer.
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A
B
C
D
E
F
Figure 2. A – anterior corneal epithelium (DIC) (Cyprinus carpio); B – retina (HE) (Cyprinus
carpio); C – stroma (DIC) (Cyprinus carpio); D – rod like melasomes in RPE (HE) (Cyprinus
carpio); E – cornea (Rana ridibunda) (DIC); F – sclera with cartilaginous tissue (HE) (Cyprinus
carpio); Bc – basal cell layer; Wc – wing cell layer; S – squamous cell layer; Str – stroma; Fb –
fibrocytes; Cf – collagen fiber; Sl – sclera; Ct – cartilaginous tissue; RPE – retinal pigmentar
epithelium, PCL – photoreceptor cell layer; ONL – outer nuclear layer; OPL – outer plexiform layer;
INL – inner nuclear layer; IPL – inner plexiform layer; GCL – ganglion cell layer; Rlm – rod shape
melanosomes; R – rod.
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Anca-Narcisa Neagu & Ozana-Maria Petraru
Conclusions
The “terrestrial” eye, emmetropic in air, has as general features: a curved or a
strongly curved cornea with a high refractive index, an elliptical lens, a duplex retina, conedominant for diurnal species and rod-dominant for those with nocturnal habits, presence of
foveae typically found in species with acute vision as birds (bifoveate) or primate
(monofoveate), a trichromatic vision in nocturnal species to pentachromatic vision in some
birds, the high density of retinal ganglion cells in areas with highest resolution. Commonly,
the terrestrial eye of diurnal species have monofocal optical system, showing no zones of
different refractive powers in the lens and a unique focal point for monochromatic light of a
certain wavelenght and crepuscular and nocturnal animals have multifocal system, the lens
having concentric zones with different refractive powers. The terrestrial nocturnal eye
adapted to diurnal conditions, with multifocal optical system, has a slit vertical pupil.
An “aquatic” eye pattern, emmetropic in water, emphasizes: a thick and flattened
cornea, with a low refractive index, a spherical lens, with a high refractive power, and a
refractive index gradient due to its very high protein core content, a well-developed sclera,
presence of different types and highly developed tapetum lucidum, an all-rod retina or a
rod-dominante retina, with few cones, sustaining a monochromatic vision, a low density of
retinal ganglion cells in areas with highest spatial resolution and a high spatial summation
of rodes on the ganglionar cells.
An “intermediate” eye design, adapted for terrestrial and aquatic vision, two-inone designs, is also described: a duplicate cornea, lens, iris and retina could solve the air
myopic tendency for the “aquatic” eye and the underwater hyperopia for the “terrestrial”
eye.
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