The Functional Significance of the Avian Pecten: a Review

THE FUNCTIONAL SIGNIFICANCE OF THE AVIAN PECTEN: A REVIEW

VINCENT BRACH

The pecten oculi of the avian eye is an in- tic species, especially the domestic chicken triguing structure which, despite intensive (Gallus domesticus) and the domestic pigeon study, has defied conclusive functional analy- ( Columha hia). sis for over 300 years. The reviews of ORa-’ Embryologically, the pecten arises as an ec- hilly and Meyer (1961) and Wingstrand and todermal (glial) process- from the edges of Munk (1965) summarized research done on the optic fissure (Mann 1922). The ectoder- the pecten up to 1965. Both of these reviews ma1 elements are largely replaced later in confirmed the observation of Walls (1942) development by an extensive invasion of meso- that although anatomical studies and purely dermal vascular tissue. In most birds, the pec- speculative accounts of the function of the ten is largely complete at hatching, although pecten abound in the literature, the number in some species full pigmentation may be de- of experimental investigations has been small. layed for some time (Hailman 1964). In his classic study of the vertebrate eye, The gross appearance of the typical pecten Walls (1942) marshalled considerable ana- is suggestive of a steam radiator. Woods’ atlas tomical and circumstantial evidence for the ( 1917) demonstrates the remarkable vari- hypothesis that the pecten, which is the only ability of a number of external pecten features vascular structure within the posterior cham- such as color, length, thickness, and number ber of the avian eye, serves as a replacement of pleats. Early anatomical investigations for the direct vascularization of the retina (Rabl 1900, quoted in Walls 1942, Bacsich found in most other vertebrates. In recent and Gellert 1935) showed that the gross years, the ablation experiments of Wingstrand morphology of the pecten was highly variable and Munk (1965) have been taken by most even among related genera, but tended to- ornithologists and physiologists (e.g., Jasinki ward three distinct patterns: the “pleated 1973, Sillman 1973) as positive proof of this fan,” the commonest type, found in most neo- hypothesis. However, my recent investiga- gnathous birds; the “pleated cone” of some tions of the physiology of the pecten (Brach ratites, which has a radiate appearance due 1975a, b) have produced results which cast to the circular cross-section of the optic nerve doubt on the trophic theory of pecten func- head; and the bridgeless, often greatly reduced tion. In this review, I summarize what is pectens of kiwis, owls, and the caprimulgi- presently known about the structure and func- forms. Except for the degenerate pectens of tion of the pecten with the aim of providing kiwis, the pectens of all birds are folded or a fresh look at the problems and partial an- pleated. The purpose of these pleats is ap- swers which have arisen in studies of the pec- parently to increase the surface area of the ten since 1965. pecten rather than to produce rigidity as proposed by Tucker ( 1975), because the pecten DESCRIPTION is supported entirely by the vitreous body and collapses limply against the retina when the The structure of the pecten has been de- vitreous body is excised. scribed exhaustively on every level. The atlas The histological features of the pectens of of avian ophthalmoscopy by Wood (1917) is all birds are remarkably similar. The pecten still the best survey of the gross appearance consists of a thin, pleated plexus of rather large of the pectens and retinas of non-domestic capillaries held together by a sparse matrix of species. The light and electron microscopy of pigmented stroma cells (Fig. 1). In most the pecten have been described by many birds, the pecten apex is held together by a workers (Bacsich and Gellert 1935, Seaman densely-pigmented, fibrous “bridge” of tissue and Storm 1963, Bacsich et al. 1966, Seaman which has a reduced vascularization with re- 1966, Nguyen H. Anh et al. 1967, Raviola and spect to the pecten pleats. The pecten is at- Raviola 1967, Porte et al. 1968, Fielding 1972, tached basally to the optic nerve head and Fischlschweiger and ORahilly’ 1972, Welsch distally to the vitreous body by fine strands 1972, Dieterich et al. 1973, Jasinki 1973, Han- of vitreous tissue which interdigitate with zely et al. 1976). Much of this work was per- processes of the bridge cells. formed on a small number of primarily domes- Ultrastructural investigations of the pecten 13211 The Condor 79:321-327, 1977 322 VINCENT BRACH

However, Dieterich et al. ( 1976) reported the presence of some primitive smooth muscle cells in the walls of the pre-fold vessels in Passer domesticus. The absence of nervous tissue is especially significant as it renders unlikely the numerous sense-organ theories of pecten function. A scanning electron microscope study by Dieterich et al. (1973) showed that the pecten capillaries form an extensively anas- tomosed network, but neither this study nor that of Tucker (1975) disclosed any regular arrangement of vessels which might suggest the presence of a rete system. The pecten also shows a number of interesting biochemical features. Several enzymes, including carbonic anhydrase (Leiner 1951, Kauth and Sommer 1953, Welsch 1972), alkaline and acid phosphatases (Seaman and Storm 1963, Bawa and YashRoy 1972), and aminopeptidase (Welsch 1972) have been found in large amounts in the pecten. The relatively large amount of carbonic anhydrase prompted the study of Seaman and Himelfarb ( 1963), in which the carbonic anhydrase in- hibitor acetazolamide was administered to FIGURE 1. 1Opm vertical section of the pecten and chickens in large doses and the effect on the optic nerve head of the Burrowing Owl, Athene cprni- ultrastructures of the pecten and ciliary body culuria. Note the extensive vascularization of the pec- explored. The principle finding of this study ten-optic nerve junction (arrow) as well as the pec- was that the amount of infolding of the apical ten pleats. In this species, the bridge of the pecten is lacking. ( 125X ). and basal plasmalemma of the capillary endothelium in both the pecten and the ciliary body increased greatly after administration of reveal one of its most unusual features, the ex- acetazolamide. However, because the quan- tensively reduplicated apical and basal plas- tity of acetazolamide administered was greatly malemma of the capillary endothelium (Fig. in excess of the recommended therapeutic 2). This condition has no known parallel in dose, these results easily could have been the animal kingdom except in the capillaries caused by nonspecific tissue damage and must of the lizard conus papillaris, which exhibits be viewed with caution. Bawa and YashRoy a remarkable histological similarity to the pec- (1972) found that the alkaline phosphatase ten ( Brach 1976). The nature of this infolding activity of pecten tissue changes markedly is that of microfolds rather than microvilli upon dark adaptation, about which more will (Dieterich et al. 1973). The basal folds are be said below. oriented perpendicular to the apical folds, the latter being pointed in the direction of the HYPOTHESIZED FUNCTIONS blood flow. Wingstrand and Munk (196.5) found that capillaries having an endothelium The intriguing shape of the pecten has proof this type are restricted to the folds of the voked more than 30 ingenious hypotheses of pecten. Surrounding each capillary is a multi- pecten function, many of which directly link layered lamina of fibrous material with a dis- the pecten with the proverbial acuity of avian tinct outer boundary which has been shown vision. Most of these proposed functions are histochemically to be composed of polysac- either physical (usually in reference to op- charide or mucopolysaccharide material tics) or metabolic. Walls (1942) and Wing- ( O’Rahilly and Meyer 1961). Except for the strand and Munk (1965) discussed many of pigment-containing stroma cells, a few spin- these extensively. dle-shaped cells within the fibrous laminae A number of the hypotheses for pecten ( fibroblasts or pericytes), and an occasional function in both the physical and the meta- mast cell, no other cell types have been re- bolic categories seem speculative and highly ported from the pecten folds and bridge. unlikely. For example, the pecten has been AVIAN PECTEN 323

FIGURE 2. Electron micrograph of glutaraldehyde-osmium fixed pecten tissue from the domestic chicken. E = extravascular space, EC = endothelial cell, F = fibroblast, L = vessel lumen, M = mast cell, PL = perivascular lamina, RBC = red blood cell, S = stroma. Note the extensively reduplicated endothelial cell plasmalemma.

implicated as the seat of an avian magnetic pecten cast a sharp, grid-like shadow on the “sense” by at least one group (Danilov et al. retina, which in fact is not the case. My own 1970). As the pecten is devoid of nervous tis- observations confirm those of Wingstrand and sue (Ehinger 1967)) it is improbable that the Munk ( 1965) that the pecten is so situated in pecten is the seat of any sort of sensory sys- the eye as to cast a minimal, rather un-grid- tem, although the possibility remains that like shadow on the retina, which in any case photic environmental cues could be trans- falls almost exclusively on the photoreceptor- duced through humoral rather than neurologi- free optic nerve head. This suggests that birds cal routes, should the pecten be directly photo- may not actually perceive the presence of sensitive with respect to its function. their pectens. The dark pigmentation and “Optical” hypotheses of pecten function somewhat velvety texture of the pecten sur- tend to ignore the histological and ultrastruc- face, especially on the bridge, indicate that tural features of the pecten and concentrate the pecten absorbs light. This led Barlow and instead on its form, position, or color. The Ostwald (1972) to suggest that light absorp- most ingenious of these hypotheses is that of tion might actually be the pectens’ function, Menner ( 1938). With the aid of models, Men- making it analogous to the light baffles found ner argued that a grid-like pattern of shadows in many cameras. However, because “grid,” was cast upon the retina by the pecten, in- “baffle,” and other purely optical hypotheses creasing the sensitivity of the retina to small of pecten function account for only the exter- moving objects by causing their images to nal shape and coloration of the pecten and flicker. This theory was developed further by ignore its unique histological and physiologi- Crozier and Wolff (1943a, b) who were able cal features, they are incomplete. to increase the flicker response contour of the The most thoroughly developed explana- human eye to a level comparable to that of tions of the pecten relate to the hypothesis the House Sparrow (Passer domesticus) by that the pecten replaces the missing central re- throwing a grid-like shadow onto the retina. tinal artery system in the avian eye. Walls However, this hypothesis requires that the (1942) and Wingstrand and Munk (1965) 324 VINCENT BRACH presented the most thorough analyses of the tention of retinal and some visual integrity various trophic hypotheses. Their conclusions, after varying degrees of pecten destruction in and the conclusions of almost all other work- domestic pigeons, although neither study con- ers to date, perhaps have been expressed firmed these findings by demonstration of his- most succinctly by Jasinki (1973:281) : “The tologically intact retina or total lesion of the pecten oculi of birds is a nutritive organ sup- pecten. However, all of these data suggest plying the inner layers of the retina with oxy- that the pecten does not perform any func- gen.” Other investigators have suggested the tions vital to the survival of the retina. Addi- possibility of glucose secretion (Kuwabara tional experiments, perhaps using different and Cogan 1961, Pedler 1963, Uga and Smel- ablation techniques on non-domestic species, ser 1973). are needed before this can be considered Wingstrand and Munk (1965) were the proven. first to develop a controllable technique for Following the ablation of the pecten, I ob- the ablation of the pecten, which involved served a small but significant (P = .05, paired surgical cautery of the retrobulbar supplying t-test) reduction in the normal pH of the arteries of the pecten in the domestic pigeon. vitreous humor. The possibility that the pec- This operation produced a rapid, irreversible ten may have a role in the regulation of intra- degeneration of the inner retinal layers. ocular pH was first suggested by A. Hughes These investigators also made a small number (in King-Smith 1971) and elaborated by of intraocular measurements of vitreal oxygen Brach ( 197513). This hypothesis would also tension before and after pecten ablation, which explain why the pecten is so extraordinarily demonstrated that an oxygen gradient from rich in carbonic anhydrase as this enzyme the pecten to the retina had been destroyed. catalyzes the equilibration of the three species A relative anoxia in the vitreous humor fol- of carbonic acid. The need for a pH regulator lowing pecten ablation was advanced as the within the avian eye may be linked to an un- probable cause of retinal atrophy, even usual retinal metabolism. In the mammalian though the measured difference in oxygen retina, although a substantial portion of the tension at the retina was only 3-5 mm Hg in energy-generating metabolism is dependent normal birds (three measurements) and 3 mm upon aerobic glycolysis (Krebs 1927, 1972, Hg in a single operated bird (one measure- Noel1 1956, 1963), a vascular supply is still ment) . When the sensing electrode was essential for retinal maintenance, and a sig- pushed against or slightly into the retina, the nificant portion of the retinal ATP is generated oxygen tension recorded in both classes of by oxidative phosphorylation. In the avas- bird was always three- to four-fold higher than cular avian retina, typical mitochondria in- at the vitreous-retina boundary. This suggests ward to the photoreceptor layer (which abuts that the source of oxygen being measured at the vascular choriocapillaris) are reduced or the vitreous-retina boundary may have been possibly even absent (Hughes et al. 1972). the richly vascular choriocapillaris behind the If mitochondria’ are present in the avian inner retina rather than the pecten. The retinal retina, they are so deficient in oxidative en- atrophv observed by these workers may actu- zyme capacity that these investigators were ally have been caused by embarrassment of unable to demonstrate the presence of bound the circulation of the optic nerve head which succinic acid dehydrogenase over much of the appears to receive some supply from the ar- width of the retina in the domestic pigeon, terioles at the pecten base (Fig. l), rather even though the same techniques revealed than by a loss of pecten function. Hence, the abundant, typical mitochondria in the photo- explanations advanced by Wingstrand and receptor layer. If the avian retina employs Murlk are questionable. glucose as a source of energy but lacks the Recently, I devised a new technique for pec- capacitv for oxidative phosphorylation, rela- ten ablation in the domestic chicken which tively large amounts of pyruvic and/or lactic involves intraocular electrocautery with acid would be generated in the glycolytic specially-designed electric forceps (Brach production of ATP, and some system serving 1975b). Essentially no change in retinal his- the retina would be expected to be present to tology was produced from 13 total and 7 remove both excess hydrogen ions and the ac- partial ablations of the pecten, and consider- cumulation of lactate. Brach (197%) specu- able visual capacity was retained. These related that vitreal lactate might be actively sults tend to confirm the less precise experi- exchanged for blood bicarbonate across the ments of Kauth and Sommer (1953) and the pecten vessels, which would simultaneously preliminary report of Frangois and Neetens eliminate both wastes. ( 1974). Both of these studies reported the re- Since the classic fluorescein permeability ex- AVIAN PEGTEN 325

-- FIGURE 4. Head-on view of normal (left) and glaucomatous (right) chicken eyes in birds of equal ages. The bird on the right was reared in 24 h light for I4 weeks prior to this photograph. Note the reduction in the anterior chamber space.

anhydrase-independent source of fluid secretion within the avian eye although he did not FIGURE 3. Representative stages from a typical mention the possibility that this might be the fluorescein angiogram of the pecten and fundus of pecten. The extensively reduplicated pecten the domestic chicken after 0.5 ml of 5% sodium capillary endothelium is quite suggestive of a fluorescein was injected into the brachial vein. Times water-transport device, the most likely direc- in set from the start of the injection are: a) 1.0, b) 2.0. c) 4.0. d) 6.0. e) 10.0. f) 16.0. Note the dve tion of movement being from the vessel lumen plumes resulting from ’ bulk flow within the vitreous into the vitreous humor. Normally, the secre- in e and f. Some dye can also be seen in the choroidal tion of aqueous humor by vertebrate eyes is circulation beneath the retina in c and d. performed by the posterior portion of the ciliary body. The aqueous humor is therefore secreted into the posterior chamber of the eye; periments of Abelsdorff and Wessely ( 1999), from there it flows around the lens through it has been known that the pecten is grossly the pupil into the anterior chamber where it permeable to a variety of dyes (especially is drained into the venous circulation at the fluorescein) and some other substances, edge of the cornea by the canal of Schlemm. which suggests a high permeability to water If the pecten also secretes fluid, a bulk flow (Seaman 1966, Fielding 1972, Bellhom and through the vitreous would produce a Bellhorn 1975, Brach 1975b). Fluorescein in- “sweeping” effect that might facilitate the re- jected into the heart or brachial vein in chick- moval of retinal metabolic wastes. ens begins to leak out of the pecten into the Fluid secretion by the pecten may have an vitreous within 1.0 set and appears to be additional role in the vegetative physiology caught up in a bulk flow or current, perhaps of the eye. For at least 20 years, it has been from the pecten itself (Fig. 3). Recently, R. known that chicks (G. domesticus) reared W. Bellhorn and M. S. Bellhorn (pers. comm. ) under continuous illumination develop a glau- found that the pecten is essentially imperme- comatous condition characterized by bulbar able to fluorescein-labeled dextrans which sug- enlargement, raised intraocular pressure, re- gests that the selective permeability of the duced cornea1 curvature and aqueous volume pecten capillaries may be due to discrimina- (Fig. 4), and eventual blindness (Lauber tion by molecular size, perhaps by pores. In 1974). Curiously, eye enlargement precedes this, the permeability characteristics of the a measureable increase in intraocular pressure pecten resemble those of the ciliary body more by several weeks, and no primary lesions of closely than those of mammalian retinal ves- the sort usually associated with glaucoma, sels. Sears (1960) demonstrated a carbonic such as reduced outflow of aqueous humor 326 VINCENT BRACH

caused by the iris adhering to the lens or by involving experimental surgery, may produce blocking of the cornea1 angle, are found in a satisfactory answer within the next few the early stages of the disease. All known years. In my opinion, the functional signifi- human glaucomas are the result of impaired cance of the avian pecten holds considerable outflow facility; a theoretically possible “hy- interest for medicine as well as ornithology persecretion glaucoma” has never been found and is well-deserving of intensive study. (D. R. Anderson, pers. comm.). However, investigations by Bawa and YashRoy (1972) ACKNOWLEDGMENTS demonstrated that alkaline phosphatase, an enzyme implicated in some forms of active Support and facilities for my investigations of the avian pecten were graciously provided at the Uni- transport, shows decreased activity in the pec- versity of Miami, Coral Gables, Florida, by 0. T. ten upon dark adaptation of the eye. Al- Owre, D. Anderson, and the Robert E. Maytag Chair though purely speculative at the present, it in Ornithology at the University of Miami. This work would be most interesting if fluid secretion was performed at the Bascom Palmer Eye Institute, by the pecten were directly influenced by Miami, Florida, under U.S.P.H.S. Grant EY00031, awarded from the National Institutes of Health, light, making the “primary lesion” of light- Bethesda, Maryland. Discussions with D. H. Evans, induced avian glaucoma a hypersecretion by J. S. Clegg, D. I. Hamasaki, and B. Davis aided in an overstimulated pecten. Assuming that the the development of many of the ideas in this paper. outflow facility of the eye is relatively fixed, I also wish to thank my wife for her continued support. hypersecretion beginning soon after hatching might cause the rapidly growing eye to “bal- loon” in response to a chronic but small ele- LITERATURE CITED vation in intraocular pressure which becomes AAELSWRFF, G., ANU K. WESSELY. 1909. Vergleic- measurable only after the eye is no longer hend-physiologische Untersuchungen iiber der able to enlarge. Fliissigkeitwechel des Aunes in der Wirbeltier- reihe.-I. Vogel. Arch. Augenheilk. 64:65-124. The question might well be asked, “Why BACSICH, P., AND A. GELLERT. 1935. Beitrage zur has a pecten-like structure evolved in the Kenntnis der Struktur und Funktion des Pectens avian eye in lieu of the more conventional ret- im Vogelauge. Graefes Arch. Ophthalmol. 133: inal vascularization found in most other verte- 448460. brates?” Actually, the presence of blood ves- BACSICH, P., I. A. CHISHOLM, AND A. GELLERT. 1966. The riddle of the pecten in the birds’ eye and sels on and within the mammalian retina is the probable usefulness of the laser in the analy- an impediment to sharp vision, and one finds sis of its function, p. 299-316. In British Small that in those mammals having the best vision, Animals Veterinary Assoc. [ed.], Aspects of com- the fovea1 region is supplied from the chorio- gnative ophthalmology. Pergamon Press, Lon- capillaris and is devoid of‘ blood vessels. Walls BARLOW, H. B., AND T. J. OS~VALD. 1972. Pecten ( 1942), Hughes et al. ( 1972), Krebs ( 1972)) of the pigeons’ eye as an inter-ocular eye shade. and Brach (1975b) argued that the evolution Nature 236: 88-90. of the pecten may be one of a suite of several BAWA, S. R., AND R. C. YASHROY. 1972. Effect of adaptations for improving retinal image qual- light and dark adaptation on the retina and pecten of the chicken. Exp. Eye Res. 13:92-97. ity and transparency, including the loss of BELLHORN, R. W., AND M. S. BELLHORN. 1975. The blood vessels and mitochondria from the re- avian pecten. I. Fluorescein permeability. Oph- tina. In this regard it is interesting to recall thalmic Res. 7:1-7. that the eyes of most diurnal lizards are served BRACH, V. 1975a. The effect of intraocular ablation of the necten oculi of the chicken. Invest. by the histologically similar conus papillaris Ophthalmol. 14: 166-168. ( Brach 1976). However, both nocturnal birds BRACN. V. 1975b. The functional sienificance of and lizards have a reduced pecten or conus, the pecten oculi in the domestic fo&, Gallus do- perhaps the result of retinal “noctumaliza- mesticus, with comparative studies on the lacer- tion” (sensu Walls 1942). The typical “noc- tilian conus papillaris. Ph.D. diss., University of Miami, Florida. turnalized” retina sacrifices visual acuity for BRACH, V. 1976. Structure and function of the ocu- photic sensitivity and is relatively thinner than lar conus papillaris in Anolis equestris ( Sauria: the diurnal retina due to the reduced number Iguanidae). Copeia 1976:552-559. of retinal ganglion cells. In those nocturnal CROZIER, W. J., AND E. WOLFF. 1943a. Modifica- tions of the flicker response contour and the sig- birds and lizards which have come to depend nificance of the avian pecten. J. Gen. Physiol. largely upon tactile and olfactory senses (e.g., 27:287-313. kiwis and the Gila monster, Heloderm su- CROZIER, W. J., AND E. WOLFF. 194313. Flicker re- spectum), both the pecten and the eye itself sponse contours for the sparrow, and the theory have become greatly reduced. of the avian pecten. J. Gen. Physiol. 27:315- 324. Although the enigma of the pecten is far DANILOV, V., G. DERMOCHAGYLAN, Z. AVETISYAN, M. from solved, future research, especially that AELAKHNYERDYAN, S. GRIGORYAN, AND G. SARI- AVIAN PECTEN 327

BEKHYAN. 1970. Possible mechanisms of mag- MENNER, E. 1938. Die Bedeutung des Pecten im netic sensitivity in birds. Biol. Zh. Arm. 23: Auge der Vogel fiir die Wahrnehmung von Bewe- 2634. gungen. Zool. Jahr. Abt. Allg. Zool. Physiol. DIETERICH, C. E., H. J. DIETERICH, M. A. SPYCHER, Tiere 58:481-538. AND M. PFAUTSCH. 1973. Fine structural ob- NGUYEN H. ANH, J., A. DELAVILLE, AND R. COUJAIUX servations of the pecten oculi capillaries of the 1967. Lendothelium’ capillaire du peigne de chicken. Z. Zellforsch. Mikrosk. Anat. 146:473- Ioeil’ des oiseaux. Z. Zellforsch. Mikrosk. Anat. 489. 77:432441. DIETERICH, H. J., K. A. ROCENBAUER AND C. E. DIE- NOELL, W. K. 1956. Differentiation, metabolic or- TERICH. 1976. The blood vessel svstem of the ganization, and viability of the visual cell. Arch. pecten ocuh in the House Sparrow ’ (Passer do: Ophthalmol. 60:702-733. mesticus ) : its architecture and fine structure NOELL, W. K. 1963. Cellular physiology of the studied by light, transmission and scanning elec- retina. J. Opt. Sot. Am. 53:3648. tron microscopy. Cytobiologie 13:57-73. ORAHILLY,’ R., AND D. B. MEYER. 1961. The de- EHINGER, B. 1967. Adrenergic nerves in the avian velopment and histochemistry of the pecten oculi. eye and cihary ganglion. Z. Zellforsch. Mikrosk. D. 207-219. In G. K. Smelser Ted.1. The struc- Anat. 82:577-588. Fure of the eye. Academic Press, New York. FIELDING, M. 1972. The ultrastructure of the pec- PEDLER, P. 1963. The fine structure of the radial ten oculi in the domestic fowl. J. Anat. 113:295- fibers in the reptile retina. Exp. Eye Res. 2:296- 297. 303. FISCHLSCHWEIGER, W., AND R. ORAHILLY.’ 1968. PORTE, A., M. E. STOECKEL, AND A. BRINI. 1968. The ultrastructure of the pecten oculi in the chick. Structure du pecten oculi chez le poulet. Arch. Z. Zellforsch. Mikrosk. Anat. 92:313-324. Ophtalmol. (Paris) 28:7-26. FRANCOIS, J., AND A. NEETENS. 1974. Comparative RAVIOLA, E., AND G. RAVIOLA. 1967. A light and anatomy of the vascular supply of the eye in ver- electron microscope study of the pecten of the tebrates. In H. Dawson, and L. T. Graham [eds.], pigeon eye. Am.- J. Anat. 120:427-462. The Eye, 5:1-70. Academic Press, New York. SEAMAN. A. R. 1966. Ultrafine architecture of the HAILMAN, J. P. 1964. The Galapagos Swallow- avian “pecten oculi.” Graefes Arch. Ophthalmol. tailed Gull is nocturnal. Wilson Bull. 76:347- 170: l-15. 354. SEAMAN, A. R., AND T. M. HIMELFARB. 1963. Cor- HANZELY, L., W. E. SOUTHERN, AND D. MQLSEN. related ultrafine structural changes of the avian 1976. Ultrastructure of the Ring-billed Gull eye pecten oculi and ciliary body of Gallus domesti- pecten. Cytobios 12: 191-202. GUS. Am. J. Ophthalmol. 56:278-296. HUGHES, P. T., P. JERROME, AND H. A. KREBS. 1972. SEAMAN, A. R., AND H. STORM. 1963. A correlated Ultrastructure of the avian retina: an anatomical light and electron microscope study on the pec- study of the retina of the domestic pigeon, Co- ten oculi of the domestic fowl (Gallus domesti- Zumba Zivia, with particular reference to the dis- cus). Exp. Eye Res. 2:163-172. tribution of mitochondria. Exp. Eye Res. 14: SEARS, M. L. 1960. Intraocular pressure of the un- 189-195. anaesthetized hen. Arch. OnhthaImoI.- 63:212- JASINKI, A. 1973. Fine structure of capillaries in 216. the pecten oculi of the sparrow, Passer domesti- SILLMAN, A. J. 1973. Avian vision. In D. S. Far- cus. Z. Zellforsch. Mikrosk. Anat. 146:281-292. ner, T. R. King, and K. C. Parkes [eds.], Avian KAUTH, H., AND H. SOMMER. 1953. Das Ferment biologv 3:349-387. Academic Press. New York. Kohlensaureanydrase im Tierkorper. IV. Uber TUCKER, K 1975. The surface of the pecten ocuh die Funktion des Pekten im Vogelauge.- - Biol. in the pigeon. Cell Tissue Res. 157:457-465. Zentralbl. 72: 196-209. UGA, S., AND 6. K. SMELSER. 1973. Comparative KING-SMITH, P. E. 1971. Special senses. In D. J. study of the fine structure of retinal Muller cells Bell, and B. M. Freeman [eds.], Physiology and in various vertebrates. Invest. Ophthalmol. 12: biochemistry of the domestic fowl 2:1039-1083. 434-488. Academic Press, New York. WALLS, G. L. 1942. The vertebrate eye and its KREBS, H. A. 1927. Uber den Stoffwechsel der adaptive radiation. Cranbrook Inst. Sci. Bull. 19, Netzhaut. Biochem. Z. 189:57-59. Bloomfield Hills, Michigan. KnEBS, H. A. 1972. The Pasteur effect and the re- WELSCH, U. 1972. Enzymehistochemische und fein- lation between respiration and fermentation. In strukturelle Beobactungen am Pecten Oculi von F. Dickens, and P. N. Campbell teds.], Essays Taube (Columba livia) und LachmSwe (Law in biochemistry 8:1-34. Academic Press, Lon- &bun&s). Z. Zellforsch. Mikrosk. Anat. 132: don. 231-244. KUWABARA, T., AND D. C. COGAN. 1961. Retinal WINGSTRAND, K. G., AND 0. MUNK. 1965. The pec- glycogen. Arch. Ophthalmol. 66:680-688. ten oculi of the pigeon with particular regard to LAUBER, J. K. 1974. Genesis of light-induced avian its function. Biol. Skr. Danske Viden. Selsk. (Co- glaucoma. Invest. Ophthalmol. 13:872-875. penhagen) 14:1-64. LEINER, M. 1951. Uber die Bedeutung des Pectens WOOD, C. A. 1917. The fundus oculi of birds. im Vogelauge. Zool. Anz., Suppl. 15:117-123. Lakeside Press, Chicago. MANN, I. C. 1922. On the morphology of certain developmental structures associated with the up- Department of Biology, Texas Eastern University, Ty- per end of the choroidal fissure. Br. J. Ophthamol. ler, Texas 75701. Accepted for publication 5 October 6: 145-163. 1976.