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The anatomy and fine structure of the eye in teleost. III. The structure of the lentiform body in Fundulus grandis
Exp. Eye Res. (1975) 21, 515-521
The Anatomy and Fine Structure of the Eye in Teleost. III. The Structure of the Lentiform Body in Fundulus grandis D. EUGENE COPELAND AND Bidogy
Lkpartrnent,
Marine
Tdane
l7hcersity,
AUSTIK
T.
FITZJARRELL
Xezo OrleansF La. 70118, and the
Biological Laboratory, WoodsHole, Mass. 02543: U.X.A. (Received14 July 1975, Boston)
The lentiform body in conjunction with the much larger choroidal body is concerned with the elevation of oxygen tensions in the eyes of some teleost fishes. The lentiform body of Eundulus grandis is a counter-current system of afferent capillaries interspaced with irregular efferent sinusoids. It is significantly smaller than the choroidal body and much less efficient in that the vascular components are shorter in length and larger in diameter, reducing the exchange capability. The fine structure of the vessels in the lentiform body is much like that of the choroidal body.
1. Introduction Many teleost fishes have a choroidal body in the vascular system of their eyes. This is a compact structure located on the back surface of the eye and composedof man? thousands of capillaries arranged so that afferent and efferent vesselsinterdigitate to form a counter-current system (rete mirabile) or wundernetze). General morphological studies have been done by Walls (1942): Allen (1949) and Barnett (1951). Taxonomically, the choroidal body has been found in only one non-teleost, bony fish, t#hc Holostean bow-fin (Amia calva). Representatives of the Brachiopterygii, Dipnoi anti (‘hondrostei do not possessthe body (Wittenberg and Haedrich, 1974). The choroidal body has been linked functionally to the exceptional elevation of oxygen tensions in t!he vitreous humor (Wittenberg and Wittenberg, 1962, 1974). The fine structure of’ the gland has been described for Amia (Fawcett and Wittenberg, 1959; Wittenberg and Wittenberg, 1974) and for Pun&&s grandis (Copeland, 1974a). A much smaller counter-current arrangement, the lentiform body, is founcl associatedwith the choroidal body in somefish. There is little in the literature on tht> nature of the body or its distribution. Walls (1942) states that, when present,, it i> interposed in the circulation to the falciform process. When the falciform process i\ missing, there is no lentiform body. Barnett (1951) and Hanyu (1962) diagram the I)ody in their studies of the choroidal body and falciform processes,respectively, hut (10 not go into detail. The killifish, P. grandis, does not possessa falciform process, but does possessN well-developed lentiform body. I have described the rather complicated vascular c:onnection of it to the general circulation, to the choriocapillaris, to the hyaloitl vesselswithin the eye and to the choroidal body itself (Copeland, 1974b). The following is a description of the anatomy and fine structure of the lentiform body in 8’. grandis. 2. Materials and Methods Fish
were
Two minor
perfused and fixed by methods previously described (Copeland, 1974a, 1~). subst,itutions were made in the procedures. Grumbacher white ink was used
FIGS l-2. The upper photograph is a top view of lentifwm body; aRerent suspension; cleared in toluene so the efferent sinusoid complex is transparent. lower photograph is a ventral view of the same lentiform body. H-4, hyaloid
rete injected with ~hitc i~,i, LA, lentiform artery. Thc~ artery connections ( ,’ 100).
LENTIFORM
BODY
OF
TELEOST
EYE
FIGS 3-4. Light microscope photographs. The upper photograph is a cross-section lentiform body. The lower photograph is a cross-section of the rete in the choroidal !ish. Roth taken at the same magnification. The bar equals 0.1 mm.
?)
c II
of the rete in 1 I\(* body of the sall)t.
528
D. E. COPELASD
XSD
A. T.
FI’CZ,JARREI,I,
in place of Pelikan white ink and Plasmanate (Cutter) in place of Plmnatein ( A/)l)ot t 1. Since it may be a misnomer to refer to capillaries zu “srterid” ;~nd “~enotl~“. t ht* choroidal and lentiform capillaries that introduce blood to the eye are called ~~;lfferv~~f” and those that conduct blood away, “efferent”.
3. Results The lentiform body is a rounded, slightly flattened body approximately O-7mm in diameter and O-3mm in thickness, in fish of lo-12 cm length. Figures 1 and 2 show the dorsal and ventral views of a typical organ. See Fig, 1 of Copeland, 1974h for
FIG. 5. Electron micrograph of the rete in the lentiform body. A, afferent capillary. E, elltercnt sinusoid. Arrows indicate thickened endothelia with endoplasmic reticulum (see Fig. 6) ( \* 3150).
LENTIFORM
BODY OFTELEOSTEYE
519
details of the vascular connections. The afferent vessels are injected with the white ink suspension. The efferent sinusoids are transparent and clear. Note that the manifold developed from the lentiform artery occupies a significant portion of the upper surface of the body and, conversely, the manifold giving rise to the hyaloid artery is tucked into the lower surface. As a result, it is difficult to obtain a cross-section of the entire body that does not include elements of one or the other manifold system. Nevertheless, the individual efferent capillaries are much the same length. Figure 3 is a light micrograph cross-section of the rete of a lentiform body and Fig. 4 is a cross-section of the choroidal body from the same fish and pictured at the same magnification. There is striking difference in the size of vascular elements. The diameter of the afferent capillaries in the rebe proper average 8.3 ,um in the choroidal body and 18 pm in the lentiform body. Not only are the rete elements of the lentiform body much larger, they are also much shorter. They are about lG1.7 mm long in the choroidal body and only about 0.5-0.6 mm long in the lentiform body. At the fine structural level, the vascular tissues of the lentiform body have much the same pattern as described for the choroidal body in the same fish (Copeland. 1974a). The afferent capillaries are well-defined, evenly spaced tubular elements surrounded by irregular, sinusoidal efferent spaces. Other than size, about the only noticeable difference from the choroidal rete is the presence of more connective tissue space between the vessels and the presence of more tubular endoplasmic reticulum in the endothelial cells, The lentiform vessels in Fig. 5 should be compared with thth choroidal vessels described in Fig. 8 (Copeland, 1974a). The irregular, sinusoid-like, efferent vessels of the lentiform body frequently have cytoplasmic thickenings at the points where the contour of the vessels is sharply bent (Figs 5 and 6). At first glance, many of the round profiles in the cytoplasm look like
FIG. tubules
6. Electron micrograph of thickened area of the endothelia (ER) and a few microtubules (MT) ( x 43 250).
showing
endoplasmic
reticulunl
I)ynocytotic vesicles but study of a number of sections reveals that most structures are tubular and therefore better named as endoplasmic reticulum tend to run parallel to the long dimension of the vessel and usually contain small ikmounts of flocculent material.
4. Discussion The lentiform body in P. gra&is is obviously structured to serve a counter-current function similar to that in the choroidal body. However, as commented in my carlie publication (Copeland, 19’74b), the lentiform body is probably dependent on the choroidal body complex for the basic incremental mechanism 1,~ which the countercurrent rete conditions the incoming blood. The choroidal body receives systenlic blood by way of the ophthalmic artery after it has passed through the pseudobranch gland, a relationship apparently essential for oxygen increment (Dehatlrai, 1966 : Fairbanks, Hoffert and Fromm, 1969; Hoffert, Fairbanks and Fromm, 1971 ; Former. Hoffert and Fromm, 1973). The lentiform body, however, receives blooct directl! from the carotid artery and this incoming systemic blood is conditioned by countercurrent flow provided by the choroid-choriocapillaris complex (i.e. blood that has already been conditioned by the choroidal body). The present observations further substantiate that though the lentiform body ma! be a counter-current mechanism, it does not approach the efficiency of the choroitlal body. Two factors are quite important in a counter-current system (Hargitay and Kuhn, 1951; Scholander, 1954; Kuhn and Kuhn, 1961). First, the longer the matched tubules, the longer the two blood flows are in contact and the more an exchange can occur. Second, the smaller and more numerous the tubules in a given cross-section, the great,er are the surface areas across which exchange can occur. The lentifornl afl’erent rete is at a disadvantage in both respects when compared to the choroidal elements, being shorter (0.5-06 mm compared to l-6-lm’i mm) and wider (18 PHI compared to 8.3 pm). Gross inspection shows that the entire lentiform structure is much smaller than that of the choroidal body. This was roughly quantitated by the following procedure. The two structures were dissected free, blotted on Whatman paper and weighed on a Mettler M-5 microbalance. Excess vessels were trimmed from the choroidal body. but because of its small size the lentiform body was weighed intact. In five eyes, the weight of the choroidal body ranged from 4.055 mg to 11.570 mg and the weight of the lentiform body from 0.180 mg to 0.345 mg. The individual ratios of choroidal weight to lentiform weight ranged from 21 to 33 with 27 as the average. Thus the lentiform body is not only less efficiently arranged as a counter-current system, lr)ut it, also has much less total tissue devoted to the function. The choroidal body-choriocapillaris complex is Essociated with the most met,abolically active part of the eye, namely the rod and cone layer with its packed mitochondria. The demand for oxygen is greatest on this system. The lentiform b0c-l.v conditions blood for the vitreous humor and the inner nerve la,yers of the retina, areas which require less oxygen. On this basis, we may consider that the discrepancies in the two systems are linked to the differing functional needs. The presence of the two separate counter-current systems may find an explanation\ in the evolution of the eye. That is: if the eye evolved with independent external and internal circulatory patterns, it was then “easier” to evolve the two counter-current systems, rather than modify the primitive dual pattern to a single one. In short this might be considered an interesting example of convergent, evolution to achieve similar function within the individual. ACKNOWLEDGMENT
This work was supported by NH-HEW
grant EY-Oc%l.
LENTIFORM
BODY
OF
TELEOST
E\-E
?52I
REFERENCES Xllen.
W. F. (1949). Blood-vascular system of the eye of a deep water fish (Ophiodon rlonqnfus) considered as a pressure mechanism. An&. Rec. 103, 205. Barnet,t, C. H. (1951). The structure and function of the choroidal gland of the teleostean fisll. J. And. 85, 113. Copeland, D. E. (1974a). The anatomy and fine struct’ure of the eye of teleost. I. The choroid 1~~1) in Fund&us qmndis. Exp. Eye Res. 18, 547. (‘opeland, D. E. (1974b). The anatomy and fine structure of the eye in teleost. II. The vatsc*ular connections of the lentiform body in Fundulus grandis. Exp. Eye Res. 19, 58X I)ehadrai, P. V. (1966). Mechanism of gaseous esophthalmia in thcb Atlantic cod, Gn(1u.s nlorhurr I,. .I. Fish. Res. Board Can. 23, 909. Fairbanks, M. B., Hoffert, J. R. and Fromm, P. 0. (1969). The deprndence on the oxygen (‘OIIcentrating mechanism of the teleost eye (Srlmo gairdmzeri) on the tknzyme carbonic anhydrascs. J. ({en. Physiol. 54, 203. Fawcchtt, D. W. and Wittenberg, J. B. (1959). The fine structure of capillaries in the rete mirabik of the swim bladder of Opsanus tau. Amt. Rec. 113, 27d. Fonncbr. D. B., Hoffert, J. Russell and Fromm, I’. 0. (1973). The importance of the counter current oxygen multiplier mechanism in maintaining retinal function in the teleost. (‘art//). Bioch.em. Ph.ysiol. 45A, 559. Hanyu. I. (1962). Intraocular vascularization in some fishes. (‘ctn. J. Zool. 40, 87. Hargitay. B. and Kuhn. W. (1951). Das Multiplikationsprinzip als Grundlnge der Harnkonzentierung in der Niere. 2. Elektrochem. 55, Ti49. Hoff&t, ,J. Russell, Fairbanks, M. B. and Fromm, I?. 0. (1971). @ular oxygen concentrations :tc*caompanying severe chronic ophthalmic pathology in the lake trout (Snlz~elinus nmwtycush ). (‘(orap.
Hiochern.
Physiol.
39A, 137.
Kuhn.
1V. and Kuhn. H. J. (1961). Multiplikation von &ssaltzund anderen Einzeleff’ekten fiir (tic Bereitung hoher Gasdrucke in der Schwimmblase. %. Elektrochern. 65, 426. Scholander, P. F. (1954). Secretion of gases against high pressures in the swim bladdcbr of dechl) SC’;1 fishes. 11. The ret,e mirabile. Biol. Bull. 107, 26i 1. Il’alls, (:. I,. (1942). The vertebrate eye and its adaptivt3 radiation. (‘mr~brool; Inst. S-i. Hull. 19. 1lichigan (reprinted Hafner Publishing Co., K.Y., 1963). \Vittcbnber,a, J. B. and Haedrich, R. L. (1974). The choroid rcte mirabile of the fish eye. IL. Dist rihution and relation to the pseudobranch and to the swimbladder rete mirabile. 13iol. Hull.
146, 137. l’l’ittc~nberg. S(lturP IVittc~nbcrg, Oxygen
146.
,J. B. and Wittenberg, (Londm) 194, 106. J. B. ad Wittenberg, secretion and st#rricture 116.
B. A. (1962).
Xctivch
sec*rc$ion
of oxygen
into
the eye ot’ fish.
B. A. (1974). The choroid rete mirabile of the : comparison \vith the s~zimbladder retch mirabile.
fish eye. I. Ijiol. Hvll.
The Anatomy and Fine Structure of the Eye in Teleost. III. The Structure of the Lentiform Body in Fundulus grandis D. EUGENE COPELAND AND Bidogy
Lkpartrnent,
Marine
Tdane
l7hcersity,
AUSTIK
T.
FITZJARRELL
Xezo OrleansF La. 70118, and the
Biological Laboratory, WoodsHole, Mass. 02543: U.X.A. (Received14 July 1975, Boston)
The lentiform body in conjunction with the much larger choroidal body is concerned with the elevation of oxygen tensions in the eyes of some teleost fishes. The lentiform body of Eundulus grandis is a counter-current system of afferent capillaries interspaced with irregular efferent sinusoids. It is significantly smaller than the choroidal body and much less efficient in that the vascular components are shorter in length and larger in diameter, reducing the exchange capability. The fine structure of the vessels in the lentiform body is much like that of the choroidal body.
1. Introduction Many teleost fishes have a choroidal body in the vascular system of their eyes. This is a compact structure located on the back surface of the eye and composedof man? thousands of capillaries arranged so that afferent and efferent vesselsinterdigitate to form a counter-current system (rete mirabile) or wundernetze). General morphological studies have been done by Walls (1942): Allen (1949) and Barnett (1951). Taxonomically, the choroidal body has been found in only one non-teleost, bony fish, t#hc Holostean bow-fin (Amia calva). Representatives of the Brachiopterygii, Dipnoi anti (‘hondrostei do not possessthe body (Wittenberg and Haedrich, 1974). The choroidal body has been linked functionally to the exceptional elevation of oxygen tensions in t!he vitreous humor (Wittenberg and Wittenberg, 1962, 1974). The fine structure of’ the gland has been described for Amia (Fawcett and Wittenberg, 1959; Wittenberg and Wittenberg, 1974) and for Pun&&s grandis (Copeland, 1974a). A much smaller counter-current arrangement, the lentiform body, is founcl associatedwith the choroidal body in somefish. There is little in the literature on tht> nature of the body or its distribution. Walls (1942) states that, when present,, it i> interposed in the circulation to the falciform process. When the falciform process i\ missing, there is no lentiform body. Barnett (1951) and Hanyu (1962) diagram the I)ody in their studies of the choroidal body and falciform processes,respectively, hut (10 not go into detail. The killifish, P. grandis, does not possessa falciform process, but does possessN well-developed lentiform body. I have described the rather complicated vascular c:onnection of it to the general circulation, to the choriocapillaris, to the hyaloitl vesselswithin the eye and to the choroidal body itself (Copeland, 1974b). The following is a description of the anatomy and fine structure of the lentiform body in 8’. grandis. 2. Materials and Methods Fish
were
Two minor
perfused and fixed by methods previously described (Copeland, 1974a, 1~). subst,itutions were made in the procedures. Grumbacher white ink was used
FIGS l-2. The upper photograph is a top view of lentifwm body; aRerent suspension; cleared in toluene so the efferent sinusoid complex is transparent. lower photograph is a ventral view of the same lentiform body. H-4, hyaloid
rete injected with ~hitc i~,i, LA, lentiform artery. Thc~ artery connections ( ,’ 100).
LENTIFORM
BODY
OF
TELEOST
EYE
FIGS 3-4. Light microscope photographs. The upper photograph is a cross-section lentiform body. The lower photograph is a cross-section of the rete in the choroidal !ish. Roth taken at the same magnification. The bar equals 0.1 mm.
?)
c II
of the rete in 1 I\(* body of the sall)t.
528
D. E. COPELASD
XSD
A. T.
FI’CZ,JARREI,I,
in place of Pelikan white ink and Plasmanate (Cutter) in place of Plmnatein ( A/)l)ot t 1. Since it may be a misnomer to refer to capillaries zu “srterid” ;~nd “~enotl~“. t ht* choroidal and lentiform capillaries that introduce blood to the eye are called ~~;lfferv~~f” and those that conduct blood away, “efferent”.
3. Results The lentiform body is a rounded, slightly flattened body approximately O-7mm in diameter and O-3mm in thickness, in fish of lo-12 cm length. Figures 1 and 2 show the dorsal and ventral views of a typical organ. See Fig, 1 of Copeland, 1974h for
FIG. 5. Electron micrograph of the rete in the lentiform body. A, afferent capillary. E, elltercnt sinusoid. Arrows indicate thickened endothelia with endoplasmic reticulum (see Fig. 6) ( \* 3150).
LENTIFORM
BODY OFTELEOSTEYE
519
details of the vascular connections. The afferent vessels are injected with the white ink suspension. The efferent sinusoids are transparent and clear. Note that the manifold developed from the lentiform artery occupies a significant portion of the upper surface of the body and, conversely, the manifold giving rise to the hyaloid artery is tucked into the lower surface. As a result, it is difficult to obtain a cross-section of the entire body that does not include elements of one or the other manifold system. Nevertheless, the individual efferent capillaries are much the same length. Figure 3 is a light micrograph cross-section of the rete of a lentiform body and Fig. 4 is a cross-section of the choroidal body from the same fish and pictured at the same magnification. There is striking difference in the size of vascular elements. The diameter of the afferent capillaries in the rebe proper average 8.3 ,um in the choroidal body and 18 pm in the lentiform body. Not only are the rete elements of the lentiform body much larger, they are also much shorter. They are about lG1.7 mm long in the choroidal body and only about 0.5-0.6 mm long in the lentiform body. At the fine structural level, the vascular tissues of the lentiform body have much the same pattern as described for the choroidal body in the same fish (Copeland. 1974a). The afferent capillaries are well-defined, evenly spaced tubular elements surrounded by irregular, sinusoidal efferent spaces. Other than size, about the only noticeable difference from the choroidal rete is the presence of more connective tissue space between the vessels and the presence of more tubular endoplasmic reticulum in the endothelial cells, The lentiform vessels in Fig. 5 should be compared with thth choroidal vessels described in Fig. 8 (Copeland, 1974a). The irregular, sinusoid-like, efferent vessels of the lentiform body frequently have cytoplasmic thickenings at the points where the contour of the vessels is sharply bent (Figs 5 and 6). At first glance, many of the round profiles in the cytoplasm look like
FIG. tubules
6. Electron micrograph of thickened area of the endothelia (ER) and a few microtubules (MT) ( x 43 250).
showing
endoplasmic
reticulunl
I)ynocytotic vesicles but study of a number of sections reveals that most structures are tubular and therefore better named as endoplasmic reticulum tend to run parallel to the long dimension of the vessel and usually contain small ikmounts of flocculent material.
4. Discussion The lentiform body in P. gra&is is obviously structured to serve a counter-current function similar to that in the choroidal body. However, as commented in my carlie publication (Copeland, 19’74b), the lentiform body is probably dependent on the choroidal body complex for the basic incremental mechanism 1,~ which the countercurrent rete conditions the incoming blood. The choroidal body receives systenlic blood by way of the ophthalmic artery after it has passed through the pseudobranch gland, a relationship apparently essential for oxygen increment (Dehatlrai, 1966 : Fairbanks, Hoffert and Fromm, 1969; Hoffert, Fairbanks and Fromm, 1971 ; Former. Hoffert and Fromm, 1973). The lentiform body, however, receives blooct directl! from the carotid artery and this incoming systemic blood is conditioned by countercurrent flow provided by the choroid-choriocapillaris complex (i.e. blood that has already been conditioned by the choroidal body). The present observations further substantiate that though the lentiform body ma! be a counter-current mechanism, it does not approach the efficiency of the choroitlal body. Two factors are quite important in a counter-current system (Hargitay and Kuhn, 1951; Scholander, 1954; Kuhn and Kuhn, 1961). First, the longer the matched tubules, the longer the two blood flows are in contact and the more an exchange can occur. Second, the smaller and more numerous the tubules in a given cross-section, the great,er are the surface areas across which exchange can occur. The lentifornl afl’erent rete is at a disadvantage in both respects when compared to the choroidal elements, being shorter (0.5-06 mm compared to l-6-lm’i mm) and wider (18 PHI compared to 8.3 pm). Gross inspection shows that the entire lentiform structure is much smaller than that of the choroidal body. This was roughly quantitated by the following procedure. The two structures were dissected free, blotted on Whatman paper and weighed on a Mettler M-5 microbalance. Excess vessels were trimmed from the choroidal body. but because of its small size the lentiform body was weighed intact. In five eyes, the weight of the choroidal body ranged from 4.055 mg to 11.570 mg and the weight of the lentiform body from 0.180 mg to 0.345 mg. The individual ratios of choroidal weight to lentiform weight ranged from 21 to 33 with 27 as the average. Thus the lentiform body is not only less efficiently arranged as a counter-current system, lr)ut it, also has much less total tissue devoted to the function. The choroidal body-choriocapillaris complex is Essociated with the most met,abolically active part of the eye, namely the rod and cone layer with its packed mitochondria. The demand for oxygen is greatest on this system. The lentiform b0c-l.v conditions blood for the vitreous humor and the inner nerve la,yers of the retina, areas which require less oxygen. On this basis, we may consider that the discrepancies in the two systems are linked to the differing functional needs. The presence of the two separate counter-current systems may find an explanation\ in the evolution of the eye. That is: if the eye evolved with independent external and internal circulatory patterns, it was then “easier” to evolve the two counter-current systems, rather than modify the primitive dual pattern to a single one. In short this might be considered an interesting example of convergent, evolution to achieve similar function within the individual. ACKNOWLEDGMENT
This work was supported by NH-HEW
grant EY-Oc%l.
LENTIFORM
BODY
OF
TELEOST
E\-E
?52I
REFERENCES Xllen.
W. F. (1949). Blood-vascular system of the eye of a deep water fish (Ophiodon rlonqnfus) considered as a pressure mechanism. An&. Rec. 103, 205. Barnet,t, C. H. (1951). The structure and function of the choroidal gland of the teleostean fisll. J. And. 85, 113. Copeland, D. E. (1974a). The anatomy and fine struct’ure of the eye of teleost. I. The choroid 1~~1) in Fund&us qmndis. Exp. Eye Res. 18, 547. (‘opeland, D. E. (1974b). The anatomy and fine structure of the eye in teleost. II. The vatsc*ular connections of the lentiform body in Fundulus grandis. Exp. Eye Res. 19, 58X I)ehadrai, P. V. (1966). Mechanism of gaseous esophthalmia in thcb Atlantic cod, Gn(1u.s nlorhurr I,. .I. Fish. Res. Board Can. 23, 909. Fairbanks, M. B., Hoffert, J. R. and Fromm, P. 0. (1969). The deprndence on the oxygen (‘OIIcentrating mechanism of the teleost eye (Srlmo gairdmzeri) on the tknzyme carbonic anhydrascs. J. ({en. Physiol. 54, 203. Fawcchtt, D. W. and Wittenberg, J. B. (1959). The fine structure of capillaries in the rete mirabik of the swim bladder of Opsanus tau. Amt. Rec. 113, 27d. Fonncbr. D. B., Hoffert, J. Russell and Fromm, I’. 0. (1973). The importance of the counter current oxygen multiplier mechanism in maintaining retinal function in the teleost. (‘art//). Bioch.em. Ph.ysiol. 45A, 559. Hanyu. I. (1962). Intraocular vascularization in some fishes. (‘ctn. J. Zool. 40, 87. Hargitay. B. and Kuhn. W. (1951). Das Multiplikationsprinzip als Grundlnge der Harnkonzentierung in der Niere. 2. Elektrochem. 55, Ti49. Hoff&t, ,J. Russell, Fairbanks, M. B. and Fromm, I?. 0. (1971). @ular oxygen concentrations :tc*caompanying severe chronic ophthalmic pathology in the lake trout (Snlz~elinus nmwtycush ). (‘(orap.
Hiochern.
Physiol.
39A, 137.
Kuhn.
1V. and Kuhn. H. J. (1961). Multiplikation von &ssaltzund anderen Einzeleff’ekten fiir (tic Bereitung hoher Gasdrucke in der Schwimmblase. %. Elektrochern. 65, 426. Scholander, P. F. (1954). Secretion of gases against high pressures in the swim bladdcbr of dechl) SC’;1 fishes. 11. The ret,e mirabile. Biol. Bull. 107, 26i 1. Il’alls, (:. I,. (1942). The vertebrate eye and its adaptivt3 radiation. (‘mr~brool; Inst. S-i. Hull. 19. 1lichigan (reprinted Hafner Publishing Co., K.Y., 1963). \Vittcbnber,a, J. B. and Haedrich, R. L. (1974). The choroid rcte mirabile of the fish eye. IL. Dist rihution and relation to the pseudobranch and to the swimbladder rete mirabile. 13iol. Hull.
146, 137. l’l’ittc~nberg. S(lturP IVittc~nbcrg, Oxygen
146.
,J. B. and Wittenberg, (Londm) 194, 106. J. B. ad Wittenberg, secretion and st#rricture 116.
B. A. (1962).
Xctivch
sec*rc$ion
of oxygen
into
the eye ot’ fish.
B. A. (1974). The choroid rete mirabile of the : comparison \vith the s~zimbladder retch mirabile.
fish eye. I. Ijiol. Hvll.