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The morphology of the pecten oculi of the ostrich, Struthio camelus
ARTICLE IN PRESS Ann Anat 188 (2006) 519—528
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The morphology of the pecten oculi of the ostrich, Struthio camelus S.G. Kiamaa,b,, J.N. Mainac, J. Bhattacharjeed, D.K. Mwangia, R.G. Machariae, K.D. Weyrauchf a
Department of Veterinary Anatomy and Physiology, University of Nairobi, P.O. Box 30197, Nairobi, Kenya Institute of Anatomy, University of Bern, Baltzerstrasse 2, 3012-Bern, Switzerland c Department of Anatomical Sciences, University of Witwatersrand, 7 York Road, Parktown, Johannesburg 2193, South Africa d Department of Biological Sciences, Kigali Institute of Education, P.O. Box 5039, Kigali, Rwanda e Veterinary Basic Sciences, Royal Veterinary College Street, London NV1 OTU, UK f Institute of Veterinary Anatomy, Free University of Berlin, Koserstrasse 20, D-14195 Berlin, Germany b
Received 24 April 2006; accepted 11 May 2006
KEYWORDS Pecten oculi; Avian eye; Ostrich; Retina
Summary The pecten oculi is a structure peculiar to the avian eye. Three morphological types of pecten oculi are recognized: conical type, vaned type and pleated type. The pleated type has been well studied. However, there exists only scanty data on the morphology of the latter two types of pectens. The structure of the vaned type of pecten of the ostrich, Struthio camelus was investigated with light and electron microscope. The pecten of this species consists of a vertical primary lamella that arises from the optic disc and supports 16–19 laterally located secondary lamellae, which run from the base and confluence at the apex. Some of the secondary lamellae give rise to 2 or 3 tertiary lamellae. The lamellae provide a wide surface, which supports 2–3 layers of blood capillaries. Pigmentation is highest at the distal ends of the secondary and tertiary lamella where blood capillaries are concentrated and very scanty on the primary and the proximal ends of the secondary lamella where the presence of capillaries is much reduced. In contrast to the capillaries of the pleated pecten, the endothelium of the capillaries in the pecten of the ostrich exhibits very few microvilli. These observations suggest that the morphology of the pecten of the ostrich, a flightless ratite bird is unique to the pleated pecten and is designed to meet the balance between optimal vision and large surface area for blood supply and yet ensuring it is kept firmly erect within the vitreous. & 2006 Elsevier GmbH. All rights reserved.
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E-mail address: [email protected] (S.G. Kiama). 0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.06.004
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Introduction One important consequence of sunlight striking our planet has been the evolution of eyes. Scientists have always been fascinated by the design, function and adaptations of the eye to different habitats. A thorough description of the structure, design and adaptive radiation of the eye in vertebrates may be found in Walls (1942) and Duke-Elder (1958). The retina, a direct extension of the central nervous system, is the visual sensory component of the eye and consists of a layer of pigmented epithelium and a neurosensory layer (Kardon, 1998). It exhibits a high rate of oxygen consumption and lactic acid production (Futterman and Kinoshita, 1959; Pasantes-Morales et al., 1972; Yu and Cringle, 2001) which is thought to parallel that of the brain and of tumours (Sickel, 1972). This high metabolic activity of the retina demands an efficient system of delivery of the nutrients required and removal of the by-products of metabolism. However, with the exception of the members of Anguilliformes, for example the common eel, Anguilla anguilla (Locket, 1977) and the Colubrid snake, Tarbophis (Duke-Elder, 1958), it is only within the class of mammals among vertebrates that the retina is supplied with blood vessels (Duke-Elder, 1958; Francois and Neetens, 1962). Where present the retinal circulation supplies nutrients to the neural layers of the retina while the photoreceptors are maintained by the choroidal circulation (Hill, 1989; Bill and Sperber, 1990; Samuelson, 1991). In most cases where the retinal circulation is missing, an alternative vascularized supplemental nutritive device is often developed (Walls, 1942; Duke-Elder, 1958). The supplemental nutritive devices include: the choroid body, the lentiform body and the falciform process of teleost (Copeland and Brown, 1976); the membrana vasculosa retinae of some fishes, anurans and snakes (Miodonski and Bar, 1987); the conus papillaries of lizards (Duke-Elder, 1958; Braekevelt, 1989); and the pecten oculi of birds (Duke-Elder, 1958; Walls, 1942). In all birds so far studied, the pecten is situated in the lower posterior temporal quadrant of the fundus (Thomson, 1929; Kiama et al., 1998) and corresponds embryologically to the position of the choroid fissure (Uehara et al., 1990) and morphologically to an elongated optic disc (Bhattacharjee, 1993). Three morphological types of pecten oculi are recognized: the conical type reported in the brown kiwi (Apteryx australis mantelli); the vaned type present in ostriches and rheas (Walls, 1942); and the pleated form widely reported in modern birds (Neognathae) (Duke-Elder, 1958; Kiama et al.,
S.G. Kiama et al. 1994; Braekevelt, 1993). The pleated form of the pecten is the most investigated perhaps because of the wide geographical distribution of the Neognathous (Barlow and Ostwald, 1972; Bawa and YashRoy, 1974; Uehara et al., 1990; Kiama et al, 2001; Braekevelt, 1998). Save for the information provided by Walls (1942), there is scanty information available on the pecten of the ostrich. The present study investigated the morphology of the pecten oculi of a flightless ratite bird, the ostrich, in an attempt to elucidate how it is designed to meet the demand placed on it by the retina.
Materials and methods The pecten oculi of five adult ostriches, Struthio camelus was investigated. The ostriches were bred in captivity for human consumption. After the animals were killed in slaughterhouse, they were promptly decapitated and the eyeballs carefully removed, washed in phosphate buffered saline and immersed in 2.5% phosphate-buffered glutaraldehyde solution. The eyeball was pierced behind the cornea–scleral junction before immersion to allow the fixative to penetrate the vitreous chamber. The posterior half of the eyeball was then removed, the vitreous body washed carefully and immersed briefly into the same fixative. Each pecten was carefully dissected out and cut into smaller pieces for light and electron microscopy processing. Some of the pectens were left intact for paraffin embedding and for scanning electron microscopy. Intact fixed pectens were dehydrated in increasing concentrations of ethanol (50% ,70%, 80%, 96% and twice in 100%), cleared using methyl benzoate, infiltrated in liquid paraffin and embedded in wax. The embedded tissues were mounted on wooden blocks and 7 mm thick sections cut using a microtome. The sections were stained using haematoxylin and eosin and viewed and photographed under a light microscope. For electron microscopy, the tissues were postfixed in 1% osmium tetroxide in 0.1 M sodium cacodylate buffer and contrasted in 0.5% uranyl acetate in 0.05 M maleate buffer. Dehydration was done as for paraffin embedding and the ethanol gradually replaced with propylene oxide and finally infiltrated and embedded in epoxy resin. Semithin and ultrathin sections were cut using a ultramicrotome (Reichert Austria). The semithin sections were collected on glass slides, stained with 0.5% toluidine blue, and viewed under a light microscope. The ultrathin sections were picked on 200mesh carbon-coated copper grids, stained with lead citrate, and observed with a Phillip 300
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Figure 1. A photograph of the pecten oculi of the ostrich, Struthio camelus. Note the cone shape and the high degree of pigmentation. 7.
transmission electron microscope under an accelerating voltage of 60 Kv. However, after dehydration, some sections were selected for scanning electron microscopy, critical point dried, mounted on aluminium stubs with silver conductive points and coated with gold palladium complex. The coated pectens were examined with a scanning electron microscope at 17 Kv (JEOL JSM 35SF or a Zeiss DSM 950).
Figure 2. Scanning electron micrograph of the lateral view of the pecten oculi of the ostrich, Struthio camelus illustrating the secondary lamellae (S) as they arise from the base (stars) and attach to the primary lamellae (arrows). 18.
Results The pecten oculi of the ostrich is a cone-shaped structure projecting from the optic disc at the lower temporal quadrant of the fundus (Fig. 1). The apex of the pecten was directed toward the lens. The height from the base to the apex and the volume of the pecten measured about 11 mm and 185 mm3 respectively. The pecten was made up of a thick central primary lamella from which arose a series of laterally located thinner secondary lamella that were also attached at the optic disc (Figs. 2 and 3). The secondary lamellae confluence at the narrow apex (Fig. 4). Serial light microscopy sections of the pecten oculi from the base to the apex revealed that the central lamella had an uneven thickness (Figs. 5–7). It was generally thicker at the base and the points of origin of the secondary lamella. The secondary lamellae were about 16–19 in number and some gave rise to 2–3 short tertiary lamellae mainly from their distal extremities. The tertiary lamellae did not run through the entire length of the pecten as they were lacking at the apical end (Fig. 5). Each secondary lamella was generally thicker at the proximal end and narrow at the distal extremity. However, some of the secondary lamellae were
Figure 3. Scanning electron micrograph of the transversely cut surface of the pecten oculi of the ostrich, Struthio camelus. Note the thick primary lamella (P) giving rise to laterally located secondary lamellae (S). Some of the secondary lamella give rise to two branches immediately after emerging from the primary lamellae. 18.
thickened at the point where they gave rise to tertiary lamella (Fig. 6). Large blood vessels were observed within the primary lamella. The blood vessels bore an attenuated endothelium and a thick basement membrane (Figs. 8–10). These vessels were difficult to categorize into either arterioles or venules as they
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Figure 4. Scanning electron micrograph of the apex of the pecten oculi of the ostrich, Struthio camelus illustrating how the secondary lamellae (S) converge at the apex. 26.
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Figure 7. Light Micrograph of a transverse section from near the base of the pecten oculi of the Ostrich, Struthio camelus. Note the elongated secondary lamellae (S) and the tertiary lamellae (arrows) arising from them. Note also the increase tertiary lamellae as compared to Fig. 5 above. Primary Lamella (P). 8.
Figure 5. Light Micrograph of a transverse section from near the apical end of the pecten oculi of the Ostrich, Struthio camelus. Note the thick primary lamella (P) giving rise to laterally located secondary lamellae (S). 17. Figure 8. Light Micrograph of a large blood vessel of the pecten oculi of the Ostrich, Struthio camelus illustrating the attenuated endothelium (Arrows) and the thick basement membrane (M). Erythrocytes (arrow heads). 550.
Figure 6. Light Micrograph of a transverse section from the middle of the pecten oculi of the Ostrich, Struthio camelus. Note the elongated secondary lamellae (S) and the tertiary lamellae (arrows) arising from them. Primary lamella (P). 10.
had no smooth muscles on their wall. The endothelial cells had short scanty microvilli on both the luminal and basal surfaces and were joined together by tight junctions (Fig. 10). Pericytes
were often observed enclosed within the basal lamina of the blood vessels (Fig. 10). These blood vessels gave rise to smaller branches that supplied the blood capillaries in the secondary and tertiary lamellae (Fig. 9). Cementing the blood vessels in the body of the secondary and primary lamellae were pigmented cells (Fig. 11). The blood capillaries were more concentrated in the distal ends and less frequent in proximal ends of the secondary and tertiary lamellae and very scanty on the central primary lamella (Figs. 12 and 13). The wall of the blood capillary consisted of a high endothelium lined by a thick basement membrane (Figs. 12–14). The endothelial cells were joined by tight junctions and displayed few microfolds on the luminal and basal surface (Fig. 15). The distribution of pigmentation was
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Figure 9. Light Micrograph showing a large blood vessel (V) of the pecten oculi of the Ostrich, Struthio camelus giving a smaller branch (B) to the lamellae. Erythrocytes (arrow heads). Basement membrane (M). Pigment granules (G). 290.
Figure 11. Transmission electron micrograph showing pigmented cells of the pecten oculi of the ostrich, Struthio camelus. Note the thin peripectineal membrane (arrows) lining the pecten. Melanin granules (stars). Processes of melanocytes (R). 8700.
related to the presence of blood capillaries and the position in the pecten. The concentration of the pigment granules was more intense on the distal ends of the secondary and tertiary lamellae where the blood capillaries were concentrated and very scanty on the proximal ends of the secondary lamellae and even less on the surface and the core of the primary lamella where few blood capillaries were found (Figs. 12 and 13). Delineating the pecten from the vitreous body was a thin vitreopectineal membrane (Fig. 11). Figure 10. Transmission electron micrograph of a large blood vessel of the pecten oculi of the ostrich, Struthio camelus. Note the short microvilli (Stars) on the luminal and basal surface of the blood vessels. Lumen (L), Basement membrane (M). Pericyte (P), Endothelial cells (E). Nuclears (N). Processes of melanocytes (R). 6990.
Discussion In birds where the retina is avascular, the presence of the pecten, a highly vascularised
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Figure 12. Light Micrograph of the distal end of the secondary lamella of the pecten oculi of the ostrich, Struthio camelus illustrating the thick walled capillaries (C) possessing a high endothelium (arrows). Note the branching of the capillaries and the high degree of pigmentation (arrow heads) between and around the blood vessel. Note also the thick basement membrane (stars) surrounding the blood capillaries. 420.
Figure 13. Light Micrograph of the primary (P) and proximal end of the secondary lamellae (S) of the pecten oculi of the ostrich, Struthio camelus illustrating the distribution of the blood vessels (C) and pigmentation (arrow heads). Note the low pigmentation and the decreased number of blood capillaries as compared to the distal end of the secondary lamella (Fig. 12 above). 196.
intraocular organ with sparse pigmented tissue, strongly suggests a nutritive role (Duke-Elder, 1958; Meyer, 1977). A trophic role calls for an expansive surface area of the diffusion surfaces and a high blood supply. This must, however, be achieved after obviating certain constraints: the pecten must not be too large to interfere with the optical function of the eye and must also be stable enough to resist lateral swing. Our findings from a study of pectens from birds with diverse habitats and differing visual acuity (Kiama et al., 2001) and our present observation on the pecten of the ostrich, S. camelus suggest that the pecten has been designed to overcome these constraints. The location of the pecten oculi of the ostrich conforms to that reported in birds possessing a pleated type of pecten (Meyer, 1977; Duke-Elder, 1958, Bhattacharjee, 1993). It overlies the optic disc and the apex projects into the vitreous humour in form of a cone. Since the optic disc constitutes a blind spot on the retina, it of great advantage that the pecten
is so located to optimize the extent of the retinal available for image capture. Although the location of the pecten is constant in all birds so far studied, specific characteristics of the organ such as size, form and number of pleats vary greatly (Thomson, 1929; Meyer, 1977). The variations are believed to depend on the behaviour of birds in relation to its general activity and visual pattern (Braekevelt, 1994; Kiama et al., 2001). Consistent with the earlier classification of the pecten of the ostrich as of vaned type (Walls, 1942), the pecten of the ostrich, S. camelus consist of a primary middle lamella that gives rise to 16–19 laterally located secondary lamellae running from the optic disc to the apex, all folded up into a black cone-shaped structure. Some of the secondary lamellae also give rise to 2–3 short tertiary lamellae from their distal ends. The peculiar construction of the pecten oculi of the ostrich appears to be in such a way as to increase surface area, occupy minimal space and yet ensure maximal physical rigidity against lateral
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Figure 14. Transmission electron micrograph of a blood capillary of the pecten oculi of the ostrich, Struthio camelus illustrating the high endothelium (E) and the thick basement membrane (M). Lumen (L). Processes of melanocytes (R). 6700.
swing. These attributes are ensured by the lateral secondary and tertiary lamellae that attach on the optic disc at the base and on the primary lamella. As cited by Pumphrey (1948), Menner (1938) examined several birds and concluded that the pleats in the pecten cast shadows on the functional part of the retina and that the extent of the pleats, and consequently of the shadows, is directly related to life-style. He thus inferred that the role of the avian pecten might be to increase the sensory effect of small moving images through creation of flicker response. This suggestion was later supported by Crozier and Wolf (1944). However, Barlow and Ostwald (1972) showed that the shadow of the pecten is cast on the base but not on the sensitive retina and hence would be expected to cause little disturbance to the optical function of the eye. The folding of the lamellae in the pecten oculi of the ostrich into a cone-shaped structure may be seen as an attempt to minimize the size of the shadow falling on the retina. This is apparently critical for the ostrich pecten, which at 11 mm in height is large in absolute terms. Light and transmission electron microscopic studies on the pleated form of pecten oculi have shown that the pecten consists exclusively of highly specialized blood vessels, extravascular pigmented cells and a superficial covering membrane (Meyer, 1977; Braekevelt, 1998). One of the most striking features of the pectineal blood capillaries is the presence of luminal and basal microplicae that
Figure 15. Transmission electron micrograph of the endothelium of a blood capillary in the pecten oculi of the ostrich, Struthio camelus showing the endothelial specializations (stars) on the luminal and basal borders. Nuclears (N). Lumen (L), Pericyte (P). Basement membrane (M). 14990.
amplify the surface areas (Kiama et al., 2001). The development of the microfolds is thought to reflect the demand placed on the pecten by the retina for nutrient delivery (Meyer, 1977; Braekevelt, 1993; Kiama et al., 1997). In the ostrich pecten, the blood capillaries were almost devoid of such endothelial specializations. Studies done in the pecten of the Emu, Dromaius novaehollandie (Braekevelt, 1998) reported reduced or no microfolds in some pectineal blood capillaries. That was interpreted to mean that vision is not of paramount importance in the bird. Reduced microfolds have also been reported in the nocturnal birds such as the great horned owl, Bubo virginanus (Braekevelt, 1993), barred owl, Strix avaria (Smith et al., 1996) and the spotted eagle owl, Bubo bubo africanus (Kiama et al., 2001). The ostrich, S. camelus, a terrestrial flightless bird belongs to the avian subclass Ratitae (Storer, 1971). Birds in this subclass which include
ARTICLE IN PRESS 526 ostrich, emu, rhea, cassowary, kiwis and tinamous are said to share interesting common anatomical, physiological and behavioural attributes (Maina and Nathaniel, 2001) and similarity in the morphology of the blood capillary of the pecten oculi may reflect the common phylogeny of the two species. Little is known about the visual capacities of the ostrich eye. Some authors have suggested that the ostrich has excellent visual activity (Campbell and Lack, 1985; Del Hoyo et al., 1992). However, a recent study estimated the theoretical maximum acuity of the ostrich to range between 17.04 and 22.55 cycles/degree (Boire et al., 2001). These values are low compared to the estimate in the eagle Aquila audax, whose eyes are comparable in size to those of the ostrich, with an axial length of 35 mm and a visual acuity of 157 cycles/degree (Reymond, 1985). This may indicate the low demand placed on the pecten by the retina and suggest that the large surface area provided by the secondary and tertiary lamellae for support of capillaries is adequate to meet the requirements of the retina without a need for further specialization of the endothelium. It has been suggested that the large eye size of the ostrich might not be equipped with the high visual acuity necessary for prey detection but as in owls, might enable the bird to function in a wide range of environmental illumination (Boire et al., 2001). The presence of pigmented cells is a constant feature of all pectens described to date (Bawa and YashRoy, 1974; Braekevelt, 1994; Kiama et al. 2001). As the only cell type found between the blood vessels, most authors have attributed a structural role to the pigmented cells. Bawa and YashRoy, 1974) suggested that the role of the pigmented cells is to absorb light and therefore increase the pectineal temperature for increased physiological activity of the pecten. In the ostrich, the distribution of pigmentation was related to the presence of blood capillaries and the position in the pecten. The concentration of the pigment granules was more intense on the distal ends of the secondary and tertiary lamellae where the blood capillaries were more abundant but very scanty on the proximal ends of the secondary lamellae and the primary lamella where only few blood capillaries were found. Although, undoubtedly the pigmented cells would be expected to play a functional structural role in the ostrich pecten, the coupling of the melanin granules which are suggested to be photoprotective (Schmitz et al., 1995; Krol and Liebler, 1998; Kadekaro et al., 2003) with the blood capillaries suggests that they may also play a role in shielding the blood vessels from the brunt of ultraviolet light (Kiama et al., 1994).
S.G. Kiama et al. The cornea and lens of the ostrich are relatively transparent to light although they show a steep rise in absorbance below a wavelength of 370 nm (Wright and Bowmaker, 2001). However, the predominant form of solar ultraviolet light that reaches the earth is in the form of long wavelength ultraviolet A (UVA) (320–400 nm) and only a minor portion is in the range of ultraviolet B (280–320 nm) and Ultraviolet C (200–280 nm) (Dillman, 1993) suggesting that the ocular media of the ostrich eye may allow ultraviolet light (UVA) transmission. Moreover, the illumination of the eye of the ostrich, a diurnal bird, has been estimated to be only half that of an owl, a nocturnal bird (Martin et al., 2001). Ultraviolet light from the sun is known to induce production of oxygen free radicals (Delmelle, 1979; van-Kuijk, 1991, Kadekaro et al., 2003). When tissues are exposed to reactive oxygen radicals, a variety of pathological changes may occur such as protein denaturation, lipid peroxidation and cell death (Fridovich, 1978). Ultraviolet light exposure to the eye has also been reported to cause cataract formation and retinal degeneration (Weiter, 1987; van-Kuijk, 1991). Cytotoxic effects of reactive oxygen species have also been reported in endothelial cells in vitro (Knepler et al., 2001, Kwon et al., 2001). It could safely be inferred that the presence of the melanin granules could in fact serve a protective function particularly for the endothelial cells from the destructive effects of ultraviolet radiation. In conclusion, for a flightless ratite bird, morphologically, the pecten of the ostrich appears to present a unique design from all the other birds studied so far. These features conform to the demand placed on it by the retina where its form and size must not interfere with the optical function of the eye.
Acknowledgments We wish to thank Mrs Hindorf from the Institute of Anatomy, Free University of Berlin, Germany, Thomas Weissbach and Barbara Krieger, University of Bern, Switzerland, and J. Gachoka of the Department of Veterinary Anatomy and Physiology, University of Nairobi for their excellent Technical Assistance. Part of this Work was funded by the German Academic Exchange Program (DAAD).
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ARTICLE IN PRESS 528 Miodonski, A.J., Bar, T., 1987. The superficial vascular hyaloid system in the eye of the frogs, Rana temporaria and Rana esculenta: scanning electronmicroscopic study of vascular corrosion casts. Cell Tissue Res. 250, 465–473. Pasantes-Morales, Kiethi, J., Urban, F.F., Mandel, P., 1972. Changes in the lactate and malate dehydrogenase isoenzyme pappers of chicken embryo brain and retina. J. Biochem. 19, 1183–1188. Pumphrey, R.J., 1948. The sense organs of birds. Ibis 90, 177–199. Reymond, L., 1985. Spatial visual acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation. Vision Res. 25, 1477–1491. Samuelson, D.A., 1991. Ophthalmic embryology and anatomy. In: Gelatt, G.N. (Ed.), Veterinary Ophthalmology, second ed. Lea and Febiger, Philadelphia, pp. 3–123. Schmitz, S., Thomas, P.D., Allen, T.M., Poznansky, M.J., Jimbow, K., 1995. Dual role of melanins and melanin precursors as photoprotective and phototoxic agents: inhibition of ultraviolet radiation-induced lipid peroxidation. Photochem. Photobiol. 61, 650–655. Sickel, W., 1972. Retinal metabolism in dark and light. In: Crescitelli, F. (Ed.), Handbook of Sensory Physiology, vol. VII/2: Physiology of Photoreceptor Organs. Springer, Berlin, pp. 667–727.
S.G. Kiama et al. Smith, B.J., Smith, S.A., Braekevelt, C.R., 1996. Fine structure of the pecten oculi of the barred owl (Strix varia). Histol. Histopathol. 11, 89–96. Storer, R.W., 1971. Classification of birds. In: Farner, D.S., King, Jr. (Eds.), Avian Biology, vol. 1. Academic Press, New York, pp. 1S–17S. Thomson, A., 1929. The pecten considered from an environmental point of view. Ibis 12, 608–639. Uehara, M., Oomori, S., Kitagawa, H., Ueshima, T., 1990. The development of the pecten oculi in the chick. Jpn. J. Vet. Sci. 52, 503–512. van-Kuijk, F.J., 1991. Effect of ultraviolet light on the eye: role of protective glasses. Environ. Health Perspectives 96, 177–184. Walls, G.L., 1942. The Vertebrate Eye and its Adaptive Radiation. Cranbrook Institute of Science, Bloomfield Hills. Weiter, J.J., 1987. Phototoxic changes in the retina. In: Miller, D. (Ed.), Clinical Light Damage to the Eye. Springer, New York, pp. 77–125. Wright, M.W., Bowmaker, J.K., 2001. Retinal photoreceptors of paleognathous birds: the ostrich (Struthio camelus) and rhea (Rhea americana). Vision Res. 41, 1–12. Yu, D.Y., Cringle, S.J., 2001. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog. Retin. Eye Res. 20, 175–208.
www.elsevier.de/aanat
The morphology of the pecten oculi of the ostrich, Struthio camelus S.G. Kiamaa,b,, J.N. Mainac, J. Bhattacharjeed, D.K. Mwangia, R.G. Machariae, K.D. Weyrauchf a
Department of Veterinary Anatomy and Physiology, University of Nairobi, P.O. Box 30197, Nairobi, Kenya Institute of Anatomy, University of Bern, Baltzerstrasse 2, 3012-Bern, Switzerland c Department of Anatomical Sciences, University of Witwatersrand, 7 York Road, Parktown, Johannesburg 2193, South Africa d Department of Biological Sciences, Kigali Institute of Education, P.O. Box 5039, Kigali, Rwanda e Veterinary Basic Sciences, Royal Veterinary College Street, London NV1 OTU, UK f Institute of Veterinary Anatomy, Free University of Berlin, Koserstrasse 20, D-14195 Berlin, Germany b
Received 24 April 2006; accepted 11 May 2006
KEYWORDS Pecten oculi; Avian eye; Ostrich; Retina
Summary The pecten oculi is a structure peculiar to the avian eye. Three morphological types of pecten oculi are recognized: conical type, vaned type and pleated type. The pleated type has been well studied. However, there exists only scanty data on the morphology of the latter two types of pectens. The structure of the vaned type of pecten of the ostrich, Struthio camelus was investigated with light and electron microscope. The pecten of this species consists of a vertical primary lamella that arises from the optic disc and supports 16–19 laterally located secondary lamellae, which run from the base and confluence at the apex. Some of the secondary lamellae give rise to 2 or 3 tertiary lamellae. The lamellae provide a wide surface, which supports 2–3 layers of blood capillaries. Pigmentation is highest at the distal ends of the secondary and tertiary lamella where blood capillaries are concentrated and very scanty on the primary and the proximal ends of the secondary lamella where the presence of capillaries is much reduced. In contrast to the capillaries of the pleated pecten, the endothelium of the capillaries in the pecten of the ostrich exhibits very few microvilli. These observations suggest that the morphology of the pecten of the ostrich, a flightless ratite bird is unique to the pleated pecten and is designed to meet the balance between optimal vision and large surface area for blood supply and yet ensuring it is kept firmly erect within the vitreous. & 2006 Elsevier GmbH. All rights reserved.
Corresponding author. Tel.: +41 31 631 8434; fax: +41 31 631 3807.
E-mail address: [email protected] (S.G. Kiama). 0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.06.004
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Introduction One important consequence of sunlight striking our planet has been the evolution of eyes. Scientists have always been fascinated by the design, function and adaptations of the eye to different habitats. A thorough description of the structure, design and adaptive radiation of the eye in vertebrates may be found in Walls (1942) and Duke-Elder (1958). The retina, a direct extension of the central nervous system, is the visual sensory component of the eye and consists of a layer of pigmented epithelium and a neurosensory layer (Kardon, 1998). It exhibits a high rate of oxygen consumption and lactic acid production (Futterman and Kinoshita, 1959; Pasantes-Morales et al., 1972; Yu and Cringle, 2001) which is thought to parallel that of the brain and of tumours (Sickel, 1972). This high metabolic activity of the retina demands an efficient system of delivery of the nutrients required and removal of the by-products of metabolism. However, with the exception of the members of Anguilliformes, for example the common eel, Anguilla anguilla (Locket, 1977) and the Colubrid snake, Tarbophis (Duke-Elder, 1958), it is only within the class of mammals among vertebrates that the retina is supplied with blood vessels (Duke-Elder, 1958; Francois and Neetens, 1962). Where present the retinal circulation supplies nutrients to the neural layers of the retina while the photoreceptors are maintained by the choroidal circulation (Hill, 1989; Bill and Sperber, 1990; Samuelson, 1991). In most cases where the retinal circulation is missing, an alternative vascularized supplemental nutritive device is often developed (Walls, 1942; Duke-Elder, 1958). The supplemental nutritive devices include: the choroid body, the lentiform body and the falciform process of teleost (Copeland and Brown, 1976); the membrana vasculosa retinae of some fishes, anurans and snakes (Miodonski and Bar, 1987); the conus papillaries of lizards (Duke-Elder, 1958; Braekevelt, 1989); and the pecten oculi of birds (Duke-Elder, 1958; Walls, 1942). In all birds so far studied, the pecten is situated in the lower posterior temporal quadrant of the fundus (Thomson, 1929; Kiama et al., 1998) and corresponds embryologically to the position of the choroid fissure (Uehara et al., 1990) and morphologically to an elongated optic disc (Bhattacharjee, 1993). Three morphological types of pecten oculi are recognized: the conical type reported in the brown kiwi (Apteryx australis mantelli); the vaned type present in ostriches and rheas (Walls, 1942); and the pleated form widely reported in modern birds (Neognathae) (Duke-Elder, 1958; Kiama et al.,
S.G. Kiama et al. 1994; Braekevelt, 1993). The pleated form of the pecten is the most investigated perhaps because of the wide geographical distribution of the Neognathous (Barlow and Ostwald, 1972; Bawa and YashRoy, 1974; Uehara et al., 1990; Kiama et al, 2001; Braekevelt, 1998). Save for the information provided by Walls (1942), there is scanty information available on the pecten of the ostrich. The present study investigated the morphology of the pecten oculi of a flightless ratite bird, the ostrich, in an attempt to elucidate how it is designed to meet the demand placed on it by the retina.
Materials and methods The pecten oculi of five adult ostriches, Struthio camelus was investigated. The ostriches were bred in captivity for human consumption. After the animals were killed in slaughterhouse, they were promptly decapitated and the eyeballs carefully removed, washed in phosphate buffered saline and immersed in 2.5% phosphate-buffered glutaraldehyde solution. The eyeball was pierced behind the cornea–scleral junction before immersion to allow the fixative to penetrate the vitreous chamber. The posterior half of the eyeball was then removed, the vitreous body washed carefully and immersed briefly into the same fixative. Each pecten was carefully dissected out and cut into smaller pieces for light and electron microscopy processing. Some of the pectens were left intact for paraffin embedding and for scanning electron microscopy. Intact fixed pectens were dehydrated in increasing concentrations of ethanol (50% ,70%, 80%, 96% and twice in 100%), cleared using methyl benzoate, infiltrated in liquid paraffin and embedded in wax. The embedded tissues were mounted on wooden blocks and 7 mm thick sections cut using a microtome. The sections were stained using haematoxylin and eosin and viewed and photographed under a light microscope. For electron microscopy, the tissues were postfixed in 1% osmium tetroxide in 0.1 M sodium cacodylate buffer and contrasted in 0.5% uranyl acetate in 0.05 M maleate buffer. Dehydration was done as for paraffin embedding and the ethanol gradually replaced with propylene oxide and finally infiltrated and embedded in epoxy resin. Semithin and ultrathin sections were cut using a ultramicrotome (Reichert Austria). The semithin sections were collected on glass slides, stained with 0.5% toluidine blue, and viewed under a light microscope. The ultrathin sections were picked on 200mesh carbon-coated copper grids, stained with lead citrate, and observed with a Phillip 300
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Figure 1. A photograph of the pecten oculi of the ostrich, Struthio camelus. Note the cone shape and the high degree of pigmentation. 7.
transmission electron microscope under an accelerating voltage of 60 Kv. However, after dehydration, some sections were selected for scanning electron microscopy, critical point dried, mounted on aluminium stubs with silver conductive points and coated with gold palladium complex. The coated pectens were examined with a scanning electron microscope at 17 Kv (JEOL JSM 35SF or a Zeiss DSM 950).
Figure 2. Scanning electron micrograph of the lateral view of the pecten oculi of the ostrich, Struthio camelus illustrating the secondary lamellae (S) as they arise from the base (stars) and attach to the primary lamellae (arrows). 18.
Results The pecten oculi of the ostrich is a cone-shaped structure projecting from the optic disc at the lower temporal quadrant of the fundus (Fig. 1). The apex of the pecten was directed toward the lens. The height from the base to the apex and the volume of the pecten measured about 11 mm and 185 mm3 respectively. The pecten was made up of a thick central primary lamella from which arose a series of laterally located thinner secondary lamella that were also attached at the optic disc (Figs. 2 and 3). The secondary lamellae confluence at the narrow apex (Fig. 4). Serial light microscopy sections of the pecten oculi from the base to the apex revealed that the central lamella had an uneven thickness (Figs. 5–7). It was generally thicker at the base and the points of origin of the secondary lamella. The secondary lamellae were about 16–19 in number and some gave rise to 2–3 short tertiary lamellae mainly from their distal extremities. The tertiary lamellae did not run through the entire length of the pecten as they were lacking at the apical end (Fig. 5). Each secondary lamella was generally thicker at the proximal end and narrow at the distal extremity. However, some of the secondary lamellae were
Figure 3. Scanning electron micrograph of the transversely cut surface of the pecten oculi of the ostrich, Struthio camelus. Note the thick primary lamella (P) giving rise to laterally located secondary lamellae (S). Some of the secondary lamella give rise to two branches immediately after emerging from the primary lamellae. 18.
thickened at the point where they gave rise to tertiary lamella (Fig. 6). Large blood vessels were observed within the primary lamella. The blood vessels bore an attenuated endothelium and a thick basement membrane (Figs. 8–10). These vessels were difficult to categorize into either arterioles or venules as they
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Figure 4. Scanning electron micrograph of the apex of the pecten oculi of the ostrich, Struthio camelus illustrating how the secondary lamellae (S) converge at the apex. 26.
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Figure 7. Light Micrograph of a transverse section from near the base of the pecten oculi of the Ostrich, Struthio camelus. Note the elongated secondary lamellae (S) and the tertiary lamellae (arrows) arising from them. Note also the increase tertiary lamellae as compared to Fig. 5 above. Primary Lamella (P). 8.
Figure 5. Light Micrograph of a transverse section from near the apical end of the pecten oculi of the Ostrich, Struthio camelus. Note the thick primary lamella (P) giving rise to laterally located secondary lamellae (S). 17. Figure 8. Light Micrograph of a large blood vessel of the pecten oculi of the Ostrich, Struthio camelus illustrating the attenuated endothelium (Arrows) and the thick basement membrane (M). Erythrocytes (arrow heads). 550.
Figure 6. Light Micrograph of a transverse section from the middle of the pecten oculi of the Ostrich, Struthio camelus. Note the elongated secondary lamellae (S) and the tertiary lamellae (arrows) arising from them. Primary lamella (P). 10.
had no smooth muscles on their wall. The endothelial cells had short scanty microvilli on both the luminal and basal surfaces and were joined together by tight junctions (Fig. 10). Pericytes
were often observed enclosed within the basal lamina of the blood vessels (Fig. 10). These blood vessels gave rise to smaller branches that supplied the blood capillaries in the secondary and tertiary lamellae (Fig. 9). Cementing the blood vessels in the body of the secondary and primary lamellae were pigmented cells (Fig. 11). The blood capillaries were more concentrated in the distal ends and less frequent in proximal ends of the secondary and tertiary lamellae and very scanty on the central primary lamella (Figs. 12 and 13). The wall of the blood capillary consisted of a high endothelium lined by a thick basement membrane (Figs. 12–14). The endothelial cells were joined by tight junctions and displayed few microfolds on the luminal and basal surface (Fig. 15). The distribution of pigmentation was
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Figure 9. Light Micrograph showing a large blood vessel (V) of the pecten oculi of the Ostrich, Struthio camelus giving a smaller branch (B) to the lamellae. Erythrocytes (arrow heads). Basement membrane (M). Pigment granules (G). 290.
Figure 11. Transmission electron micrograph showing pigmented cells of the pecten oculi of the ostrich, Struthio camelus. Note the thin peripectineal membrane (arrows) lining the pecten. Melanin granules (stars). Processes of melanocytes (R). 8700.
related to the presence of blood capillaries and the position in the pecten. The concentration of the pigment granules was more intense on the distal ends of the secondary and tertiary lamellae where the blood capillaries were concentrated and very scanty on the proximal ends of the secondary lamellae and even less on the surface and the core of the primary lamella where few blood capillaries were found (Figs. 12 and 13). Delineating the pecten from the vitreous body was a thin vitreopectineal membrane (Fig. 11). Figure 10. Transmission electron micrograph of a large blood vessel of the pecten oculi of the ostrich, Struthio camelus. Note the short microvilli (Stars) on the luminal and basal surface of the blood vessels. Lumen (L), Basement membrane (M). Pericyte (P), Endothelial cells (E). Nuclears (N). Processes of melanocytes (R). 6990.
Discussion In birds where the retina is avascular, the presence of the pecten, a highly vascularised
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Figure 12. Light Micrograph of the distal end of the secondary lamella of the pecten oculi of the ostrich, Struthio camelus illustrating the thick walled capillaries (C) possessing a high endothelium (arrows). Note the branching of the capillaries and the high degree of pigmentation (arrow heads) between and around the blood vessel. Note also the thick basement membrane (stars) surrounding the blood capillaries. 420.
Figure 13. Light Micrograph of the primary (P) and proximal end of the secondary lamellae (S) of the pecten oculi of the ostrich, Struthio camelus illustrating the distribution of the blood vessels (C) and pigmentation (arrow heads). Note the low pigmentation and the decreased number of blood capillaries as compared to the distal end of the secondary lamella (Fig. 12 above). 196.
intraocular organ with sparse pigmented tissue, strongly suggests a nutritive role (Duke-Elder, 1958; Meyer, 1977). A trophic role calls for an expansive surface area of the diffusion surfaces and a high blood supply. This must, however, be achieved after obviating certain constraints: the pecten must not be too large to interfere with the optical function of the eye and must also be stable enough to resist lateral swing. Our findings from a study of pectens from birds with diverse habitats and differing visual acuity (Kiama et al., 2001) and our present observation on the pecten of the ostrich, S. camelus suggest that the pecten has been designed to overcome these constraints. The location of the pecten oculi of the ostrich conforms to that reported in birds possessing a pleated type of pecten (Meyer, 1977; Duke-Elder, 1958, Bhattacharjee, 1993). It overlies the optic disc and the apex projects into the vitreous humour in form of a cone. Since the optic disc constitutes a blind spot on the retina, it of great advantage that the pecten
is so located to optimize the extent of the retinal available for image capture. Although the location of the pecten is constant in all birds so far studied, specific characteristics of the organ such as size, form and number of pleats vary greatly (Thomson, 1929; Meyer, 1977). The variations are believed to depend on the behaviour of birds in relation to its general activity and visual pattern (Braekevelt, 1994; Kiama et al., 2001). Consistent with the earlier classification of the pecten of the ostrich as of vaned type (Walls, 1942), the pecten of the ostrich, S. camelus consist of a primary middle lamella that gives rise to 16–19 laterally located secondary lamellae running from the optic disc to the apex, all folded up into a black cone-shaped structure. Some of the secondary lamellae also give rise to 2–3 short tertiary lamellae from their distal ends. The peculiar construction of the pecten oculi of the ostrich appears to be in such a way as to increase surface area, occupy minimal space and yet ensure maximal physical rigidity against lateral
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Figure 14. Transmission electron micrograph of a blood capillary of the pecten oculi of the ostrich, Struthio camelus illustrating the high endothelium (E) and the thick basement membrane (M). Lumen (L). Processes of melanocytes (R). 6700.
swing. These attributes are ensured by the lateral secondary and tertiary lamellae that attach on the optic disc at the base and on the primary lamella. As cited by Pumphrey (1948), Menner (1938) examined several birds and concluded that the pleats in the pecten cast shadows on the functional part of the retina and that the extent of the pleats, and consequently of the shadows, is directly related to life-style. He thus inferred that the role of the avian pecten might be to increase the sensory effect of small moving images through creation of flicker response. This suggestion was later supported by Crozier and Wolf (1944). However, Barlow and Ostwald (1972) showed that the shadow of the pecten is cast on the base but not on the sensitive retina and hence would be expected to cause little disturbance to the optical function of the eye. The folding of the lamellae in the pecten oculi of the ostrich into a cone-shaped structure may be seen as an attempt to minimize the size of the shadow falling on the retina. This is apparently critical for the ostrich pecten, which at 11 mm in height is large in absolute terms. Light and transmission electron microscopic studies on the pleated form of pecten oculi have shown that the pecten consists exclusively of highly specialized blood vessels, extravascular pigmented cells and a superficial covering membrane (Meyer, 1977; Braekevelt, 1998). One of the most striking features of the pectineal blood capillaries is the presence of luminal and basal microplicae that
Figure 15. Transmission electron micrograph of the endothelium of a blood capillary in the pecten oculi of the ostrich, Struthio camelus showing the endothelial specializations (stars) on the luminal and basal borders. Nuclears (N). Lumen (L), Pericyte (P). Basement membrane (M). 14990.
amplify the surface areas (Kiama et al., 2001). The development of the microfolds is thought to reflect the demand placed on the pecten by the retina for nutrient delivery (Meyer, 1977; Braekevelt, 1993; Kiama et al., 1997). In the ostrich pecten, the blood capillaries were almost devoid of such endothelial specializations. Studies done in the pecten of the Emu, Dromaius novaehollandie (Braekevelt, 1998) reported reduced or no microfolds in some pectineal blood capillaries. That was interpreted to mean that vision is not of paramount importance in the bird. Reduced microfolds have also been reported in the nocturnal birds such as the great horned owl, Bubo virginanus (Braekevelt, 1993), barred owl, Strix avaria (Smith et al., 1996) and the spotted eagle owl, Bubo bubo africanus (Kiama et al., 2001). The ostrich, S. camelus, a terrestrial flightless bird belongs to the avian subclass Ratitae (Storer, 1971). Birds in this subclass which include
ARTICLE IN PRESS 526 ostrich, emu, rhea, cassowary, kiwis and tinamous are said to share interesting common anatomical, physiological and behavioural attributes (Maina and Nathaniel, 2001) and similarity in the morphology of the blood capillary of the pecten oculi may reflect the common phylogeny of the two species. Little is known about the visual capacities of the ostrich eye. Some authors have suggested that the ostrich has excellent visual activity (Campbell and Lack, 1985; Del Hoyo et al., 1992). However, a recent study estimated the theoretical maximum acuity of the ostrich to range between 17.04 and 22.55 cycles/degree (Boire et al., 2001). These values are low compared to the estimate in the eagle Aquila audax, whose eyes are comparable in size to those of the ostrich, with an axial length of 35 mm and a visual acuity of 157 cycles/degree (Reymond, 1985). This may indicate the low demand placed on the pecten by the retina and suggest that the large surface area provided by the secondary and tertiary lamellae for support of capillaries is adequate to meet the requirements of the retina without a need for further specialization of the endothelium. It has been suggested that the large eye size of the ostrich might not be equipped with the high visual acuity necessary for prey detection but as in owls, might enable the bird to function in a wide range of environmental illumination (Boire et al., 2001). The presence of pigmented cells is a constant feature of all pectens described to date (Bawa and YashRoy, 1974; Braekevelt, 1994; Kiama et al. 2001). As the only cell type found between the blood vessels, most authors have attributed a structural role to the pigmented cells. Bawa and YashRoy, 1974) suggested that the role of the pigmented cells is to absorb light and therefore increase the pectineal temperature for increased physiological activity of the pecten. In the ostrich, the distribution of pigmentation was related to the presence of blood capillaries and the position in the pecten. The concentration of the pigment granules was more intense on the distal ends of the secondary and tertiary lamellae where the blood capillaries were more abundant but very scanty on the proximal ends of the secondary lamellae and the primary lamella where only few blood capillaries were found. Although, undoubtedly the pigmented cells would be expected to play a functional structural role in the ostrich pecten, the coupling of the melanin granules which are suggested to be photoprotective (Schmitz et al., 1995; Krol and Liebler, 1998; Kadekaro et al., 2003) with the blood capillaries suggests that they may also play a role in shielding the blood vessels from the brunt of ultraviolet light (Kiama et al., 1994).
S.G. Kiama et al. The cornea and lens of the ostrich are relatively transparent to light although they show a steep rise in absorbance below a wavelength of 370 nm (Wright and Bowmaker, 2001). However, the predominant form of solar ultraviolet light that reaches the earth is in the form of long wavelength ultraviolet A (UVA) (320–400 nm) and only a minor portion is in the range of ultraviolet B (280–320 nm) and Ultraviolet C (200–280 nm) (Dillman, 1993) suggesting that the ocular media of the ostrich eye may allow ultraviolet light (UVA) transmission. Moreover, the illumination of the eye of the ostrich, a diurnal bird, has been estimated to be only half that of an owl, a nocturnal bird (Martin et al., 2001). Ultraviolet light from the sun is known to induce production of oxygen free radicals (Delmelle, 1979; van-Kuijk, 1991, Kadekaro et al., 2003). When tissues are exposed to reactive oxygen radicals, a variety of pathological changes may occur such as protein denaturation, lipid peroxidation and cell death (Fridovich, 1978). Ultraviolet light exposure to the eye has also been reported to cause cataract formation and retinal degeneration (Weiter, 1987; van-Kuijk, 1991). Cytotoxic effects of reactive oxygen species have also been reported in endothelial cells in vitro (Knepler et al., 2001, Kwon et al., 2001). It could safely be inferred that the presence of the melanin granules could in fact serve a protective function particularly for the endothelial cells from the destructive effects of ultraviolet radiation. In conclusion, for a flightless ratite bird, morphologically, the pecten of the ostrich appears to present a unique design from all the other birds studied so far. These features conform to the demand placed on it by the retina where its form and size must not interfere with the optical function of the eye.
Acknowledgments We wish to thank Mrs Hindorf from the Institute of Anatomy, Free University of Berlin, Germany, Thomas Weissbach and Barbara Krieger, University of Bern, Switzerland, and J. Gachoka of the Department of Veterinary Anatomy and Physiology, University of Nairobi for their excellent Technical Assistance. Part of this Work was funded by the German Academic Exchange Program (DAAD).
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