Fish Physiology and Biochemistry vol. 8 no. 5 pp 355-364 (1990) Kugler Publications, Amsterdam/Berkeley

Development of the hypophysis of the arctic lamprey, Lampetra japonica Y. Honma l, A. Chiba 2 and U. Welsch 3 ISado Marine Biological Station, Faculty of Science, Niigata University, Niigata, 952-21 Japan; 2 Department of Biology, Nippon Dental University, Niigata, 1-8 Hamaura-cho, Niigata, 951 Japan; 3 Department of Anatomy, Chair II Microscopical Anatomy, University of Munich, Pettenkoferstr. 11, 8000 Miinchen 2, FRG Keywords: arctic lamprey, Lampetrajaponica,hypophysis, pituitary, adenohypophysis, neurohypophysis, development, ultrastructure

Abstract The hypophysis of early larval stages, from the moment of hatching on the 18th day after fertilization to the 101st day of larval life, of the arctic lamprey Lampetrajaponica was studied with scanning and transmission electron microscopes. A solid cord of cells of the distal part of the nasopharyngeal duct represents the early adenohypophysis. On the 20th day after fertilization, several of the epithelial cells of this structure showed first indications of secretory activity with an extensive Golgi apparatus and small electron-dense secretory granules. On the 26th day, non-secretory, stellate ( = supporting) cells and secretary cells can be distinguished. Already on the 39th day, two different parts can be distinguished in the adenohypophysis: the pars distalis with cells containing small dense granules, and the pars intermedia with cells containing larger granules of medium density. The number of granulated cells increases steadily; on the 101st day two pars distalis cell types can be distinguished. The neurohypophysis consists of a thin anterior and a thick posterior part. Already on the 20th day single nerve terminals in the ependymal layer of the diencephalic ( = infundibular) floor contain dense elementary granules. The number of granule-containing terminals increases steadily; on the 101st day almost all terminals contain granules. The present observations suggest an early secretory function of the lamprey hypophysis.

Introduction Because of the remarkable life history and the important phylogenetic position of the extant Agnatha, developmental studies of their various organ systems have attracted the attention of numerous scientists since the first half of the 19th century. For example, the studies of Karl von Kupffer (1894) of the pituitary gland form the basis of our present knowledge both in lampreys and hagfish. In Lampetra planeri v. Kupffer (1894) observed that the adenohypophysis arises from a prestomodeal ectodermal invagination the anterior parts of which give rise to the olfactory organ. The adenohypo-

physis develops from the terminal sections of a rather long duct-like structure, the naso-pharyngeal (= naso-hypophyseal) duct, which is a posteriorlydirected extension of the above mentioned ectodermal invagination. The neurohypophysis is represented by a shallow depression of the floor of the forebrain. Recently, Gorbman and Tamarin (1985a,b) critically re-examined with the light and the scanning electron microscope the early stages of development of the adenohypophysis in the sea lamprey, Petromyzon marinus, and found important details clarifying the situation. These authors observed the essential morphogenetic role which is played by three ectodermal folds, the middle one of

356 which transforms into the large specialized upper -lip of these animals, growing dorsally over the ectodermal epithelium which is in contact with the infundibulum. According to Gorbman and Tamarin (1985a, b) the nasopharyngeal duct is in fact not formed by an inwards growing finger-like structure (suggestive of a close similarity to Rathke's pouch) but it is the growing upper lip which is the principal structure in its formation. Virtually no information is available on the functional differentiation of the early pituitary gland of lampreys, most studies concentrating on the gland of adult animals (Tilney 1937; Leach 1951; Tsuboi 1953; Honma 1960, 1969; Wingstrand 1966; Ball and Baker 1969; Larsen and Rothwell 1972). Recently, Sholdice and McMillan (1985) described that the large adenohypophysis of adult P. marinus is formed before and during metamorphosis by proliferation from the nasopharyngeal duct, which for most of the larval period (several years) of this animal is a solid cord of tissue and only in the late metamorphosis develops a lumen. It appeared worthwhile to study the pituitary gland of various well defined early stages of "in vitro" fertilized eggs of arctic lampreys by scanning and transmission electron microscopy, since these techniques provide some indication on the functional organization of the cells of the developing structures in question.

Materials and methods The embryos and larvae used in this study were obtained by fertilization "in vitro". The sexually mature arctic lamprey L. japonica (Martens), were caught in early and mid May 1987, in the middle reaches of the Miomote River. Miomote River flows into the Sea of Japan through Murakami City, located in the northern part of Niigata Prefecture in the central part of the Japanese mainland. Soon after capture, the animals were transported to the Niigata Prefectural Inlandwater Fisheries Experimental Station (Nagaoka City) and reared for several days prior to use in tanks supplied with running well water. Ovulated eggs were allowed by extrude, laid on a large petri dish and moistened with

water. Fertilization was accomplished by the dry method. Immediately after fertilization, eggs were gently rinsed with filtered water, laid on the sheet of fine mesh Saran net, settled in glass tanks which contained well water, and maintained at 15°C. The larvae were fed yeast and rotifers. For transmission electron microscopy, the embryos and larvae at different age and developmental stages (Piavis 1971; Tahara 1988, Table 1) were immersed overnight in Karnovsky's solution, postfixed in 1% OsO4 for 2 h, dehydrated through an ethanol series, and embedded in Araldite-Epon or Spurr resins. Ultrathin sections, cut with an LKB ultratome, were double-stained with uranyl acetate and lead citrate, and examined in JEOL 1200 EX and Zeiss EM 10 electron microscopes. For scanning electron microscopy, the materials prefixed as described above were osmicated, dehydrated, critical point-dried, sputter-coated with platinum-palladium, and observed with a Hitachi S 800 electron microscope. Semi-thin sections of resin-embedded materials were cut sagittally, stained with 0.1% toluidine blue in borax and examined in the light microscope to obtain a general topographic orientation.

Results The present observations focus 1) on the fine structure of the terminal part of the nasohypophyseal duct which transforms into the early adenohypophysis and 2) on the secretory nerve terminals of the neurohypophysis. The general topographical anatomy of the head region of the early larval stages of the arctic lamprey is recognizable on the light micrographs (Figs. 2, 10, 13).

Adenohypophysis In 18 day old larvae (equivalent to Tahara's stage 25), the hatching stage, which were the youngest animals studied, the future nasopharyngeal duct was still relatively short (Figs. 1 and 2), originating from the posterior part of a flat prestomodeal depression. It ran roughly in parallel to the antero-

357 Table 1. The size and days after artificial insemination of the embryos and larvae of Lampetrajaponica, and a comparison of developmental phases and subdivision of the stages in L. japonica with those in Petromyzon marines and Lampetra reissneri. Data on Lampetra japonica

Date of fixation

Days after insemination

May 21 23 25 28 29 Jun. 1 3 6 9 12 22 Jul. 2 22 Aug. 24

7 9 11 14 15 18 20 23 26 29 39 49 69 101

Developmental phases and subdivision of stages in Petromyzon marinus* and Lampetra reissneri** Body length (mm)

4.0 5.0 5.5 5.5- 6.5 7.0 9.0- 9.5 9.5-10.0 10.5-11.5 17.0-18.0

Phase*

Stage*

Stage**

Gastrula Neural rod Head Prehatching Prehatching Hatching Hatching Pigmentation Gill-cleft Gill-cleft Burrowing, Larva Larva Larva Larva

9 11 12 13 13 14 14 15 16 16 17, 18 18 18 18

16 20 21 22 23 25 26 27 28 28 29, 30

*Piavis (1971); **Tahara (1988).

Fig. 1. Scanning electron micrograph; ventral view of the head of a larva of the arctic lamprey, Lampetrajaponica,immediately after hatching (the 18th day after fertilization) showing the nasopharyngeal opening (Np) and the stomodeal cleft (Sc) (x 100). Fig. 2. Sagittal section of the 18 day old lamprey larva to show the nasopharyngeal duct, the wedge-shaped structure extending posteriorly from the nasopharyngeal opening (Np). The distal portion of the nasopharyngeal duct (arrow) represents the early adenohypophysis closely apposed to the infundibular floor (I). Oc, optic chiasma; S, stomodeum (x 100).

358

Fig. 3. A part of the epithelial cell cord in the distal portion of the nasopharyngeal duct (= early adenohypophysis) to show a pale round nucleus (N) with a prominent nucleolus (arrow), yolk (y), plenty of glycogen particles (gl), and a well-developed Golgi apparatus (G). This picture was taken from a hatching larva on the 18th day (x 8,000). Fig. 4. A part of an epithelial cell in the early adenohypophysis of the 20 days old larva. Note a small number of electron dense granules (arrows) in the vicinity of the Golgi apparatus (G) (x 23,000).

ventral margin of the forebrain, and its terminal part, which is considered to represent the early adenohypophysis, had no lumen and was composed of medium sized epithelial cells interconnected by desmosomes. This epithelial structure was surrounded by a continuous basal lamina. The pale, large nuclei were of irregular shape and contained a prominent nucleolus. Mitotic figures occurred regularly. The cytoplasm was marked by yolk inclusions and glycogen. Several cells contained numerous rough endoplasmic reticulum (ER) cisternae and a well-developed Golgi apparatus (Fig. 3). On the 20th day (Tahara's stage 26), some cells containing small dense granules in the vicinity of the Golgi apparatus (Fig. 4) were encountered. Occasionally, some of these cells possessed one or more kinocilia which extended into the narrow intercellu-

lar space. On the 26th day (Tahara's stage 28), there were numerous mitotic figures in the early adenohypophysis and in the epithelial stalk (Figs. 5 to 7). In addition, two cell types could be distinguished in the early adenohypophysis: 1) voluminous oval or roundish secretory cells with a pale nucleus marked by a prominent nucleolus and with cytoplasm containing yolk, glycogen, ribosomes, rough ER cisterns, a large Golgi field and small groups of dense secretory granules (Fig. 8), 2) smaller cells of irregular outline with denser cytoplasm and smaller nuclei; these cells represent the future stellate cells (Fig. 8). At this stage of development, the early adenohypophysis was closely apposed to the floor of the wide diencephalic infundibulum, from which it was separated by only a narrow connective tissue space (300 nm in thickness). In sagittal sections, the

359

Figs. 5, 6 and 7. Mitotic figure (arrows) in epithelial cells of the developing adenohypophysis, all from 26 days old larvae (x 4,700). Fig. 8. A part of the early adenohypophysis of a larva on the 26th day to show two types of the epithelial cells: the roundish secretory cell (Sl ) containing small dense granules (arrow) and the small nonsecretory cell (S2) with relatively dense cytoplasm (x 9,600). Fig. 9. A part of the stalk-like epithelial cell cord (Cc) which connects the early adenohypophysis (the distal part of the nasopharyngeal duct) with the proximal part of the nasopharyngeal duct (nasal sack) with a lumen. 26 days old larva (x 7,500).

adenohypophysis was thicker than the narrow epithelial stalk (Figs. 5, 6, 7, 9 and 10) which connects it with the anterior part of the nasopharyngeal duct which contains a lumen. No major changes in histology and ultrastructure of the adenohypophysis could be observed until the 29th day (Tahara's stage 28). On the 39th day (Tahara's stage 29/30), an anterior (the future pars distalis) and a posterior part (the future pars intermedia) of the adenohypophysis could be distinguished (Fig. 10). Both parts contained secretory (Fig. 11) and non-secretory (stel-

late) cells. The secretory cells of the anterior part had a medium-dense cytoplasm, small dense granules (mean diameter 110 nm, Fig. 11) and variable numbers of organelles; their large nuclei were rich in euchromatin and marked by prominent nucleoli. The secretory cells of the posterior part were marked by pale cytoplasm and larger granules (210 nm in diameter) of medium- or low-density (Fig. 12). On the 49th day (no stage classification of Tahara; Piavis's stage 18), both parts of the adenohypophysis were increased in volume, and the number of granulated cells was also increased. The

360

Fig. 10. Sagittal section of 39 days old larva to show the early regional differentiation of the adeno- and neurohypophysis. In both adenoand neurohypophysis, two portions are distinguishable, respectively: the anterior adenohypophysis (aAH, the future pars distalis) and the posterior adenohypophysis (pAH, the future pars intermedia); and the anterior neurohypophysis (aNH) and the posterior neurohypophysis (pNH). Oc, optic chiasma; N, notochord; arrows: cell cord connecting adenohypophysis and nasal sack (Na) (x 250). Fig. 11. High power electron micrograph to show the secretory granules of an epithelial cell in the future pars distalis of the adenohypophysis of the 39 days old larva (x 23,000). Fig. 12. High power electron micrograph to show the secretory granules of an epithelial cell in the future pars intermedia of the adenohypophysis of the 39 days old larva (x 23,000).

stellate cells extended slender processes between the secretory cells and often covered part of the surface of the organ. On the 101st day (not in the stage classification of Tahara; Piavis's stage 18), the adenohypophysis had further increased in size. The pars intermedia was comprised of numerous pale secretory cells (Fig. 13), many of which contained secretory granules (Fig. 12). Among the secretory cells of the pars

distalis, possibly two types could be distinguished on the basis of ultrastructural criteria of the granules: one cell type was marked by larger ovoid granules (180 nm in diameter), the other by smaller polymorphic ones (110 nm in diameter). The adenohypophysis continued to be directly connected with the anterior part of the nasopharyngeal duct (the nasal sack, which contained a lumen) by the slender stalk-like epithelial structure.

361

Fig. 13. Sagittal section of the ventral hypothalamus of the 101 days old larva showing the further developed hypophysis. (Oc) optic chiasma, (Cc) cell cord connecting adenohypophysis with nasal sack, (aNH) anterior neurohypophysis, (pNH) posterior neurohypophysis, (aAH) anterior adenohypophysis (pars distalis), (pAH) posterior adenohypophysis (pars intermedia). Note the capillaries or venules (arrows) (x 300).

Neurohypophysis In the neurohypophysis, anterior and posterior parts could be distinguished (Figs. 10, 13). Both contained nerve fibres and terminals with elementary granules, the posterior part being larger. The nerve fibres and nerve terminals were usually divided into groups by the processes of tanycytes. Many terminals reached the outer surface of the infundibulum and were directly apposed to the basal lamina of the infundibulum. By the 20th day (Tahara's stage 26), single nerve terminals containing secretory granules occurred in the ependymal layer of the diencephalon. On the 26th day (Tahara's stage 28), in addition, nerve profiles with a cilium and small dense granules were seen in the lumen of the infundibulum overlying the ependymal cells. These structures may correspond to the intraventricular end-bulb of so-called liquor contacting neurons. On the 39th day (Tahara's stage 29/30), the anterior flat neurohypophysis was located dorsally to the pars distalis (Fig. 10) and contained nerve terminals, comprising both dense granules (90-100 nm) and clear vesicles (60 nm in diameter, Fig. 14). The posterior neurohypophysis had enlarged considera-

bly; its terminals mainly contained dense elementary granules (150 nm in diameter). On the 49th, 69th and 101st days (not in the stage classification of Tahara; in Piavis's classification stage 18), the number of fibre profiles had increased, especially in the posterior part of the neurohypophysis. On the 101st day, almost all fibres contained dense elementary granules (Fig. 15). The fibres were divided into groups by tanycytic processes.

Blood vessels Blood vessels were only present in the narrow connective tissue space anterior and posterior to the adenohypophysis, and between infundibular floor and adenohypophysis. The vessels were sinusoidal capillaries, their wall formed by thin continuous endothelial cells (Fig. 15). These vessels were surrounded by a basal lamina and were often accompanied by melanocytes. They closely approach the basal lamina bordering adenohypophysis and neurohypophysis.

362

Fig. 14. High power electron micrograph to show (upper part of photo) the nerve fibers and their terminals in the anterior neurohypophysis (aNH) of the 39 days old larva. Note small vesicles and single dense granules in the nerve terminals. C, connective tissue space between the adeno- (below) and neurohypophysis; Sc, stellate cell in the adenohypophysis (x 36,000). Fig. 15. A part of the neurohypophysis of the 101 days old larva to show the neurosecretory fibers containing abundant elementary granules. Note the thin continuous endothelium (En) and the erythrocytes (E) in the capillary (x 8,000).

Discussion The light microscopical findings of the present study on the early development of the pituitary gland of the arctic lamprey (L. japonica) are in agreement with the observations on the early pituitary development of L. planeri (v. Kupffer 1894) and of P. marinus (Gorbman and Tamarin 1985a, b). Thus, the pituitary of all lamprey species seem to follow a similar development pattern in early life. However, in addition, the present study provides new insights into the differentiation at the cellular level indicative of the initiation of function at an early stage. With regard to the development of the early adenohypophysis, we provide evidence to support Gorbman and Tamarin's (1985a, b) view of the important morphogenetic role of the rapidly developing upper lip of lampreys. This prominent structure represents a specialization of lampreys which has a marked influence on the morphology of the developing adjacent structures. However, our observation of mitotic figures in the epithelia of the developing nasohypophyseal duct and the early adenohypophysis also point to active growth of these epithelial structures, as had been assumed by von Kupffer (1894).

The findings of the present study show that immediately after hatching the lamprey larvae develop an adenohypophysis from the distal, posteriorlydirected tip of the nasopharyngeal duct. In the developmental intervals examined, the duct is mostly represented by a solid cord of flat epithelial cells the cytoplasmic organization of which appears to be undifferentiated and does not allow speculations about a specific function. While this slender epithelial cord of cells is observed between adenohypophysis and the anterior part of the nasopharyngeal duct with a lumen (nasal sack) in all stages that we examined, the fate of this cell cord is uncertain. Percy et al. (1975), do not mention it in their study of the adenohypophysis of 2.5-9 cm long larvae, whereas Sholdice and McMillan (1985) describe it in older larvae of P. marinus larvae and found that distally it forms a lumen in premetamorphosis. These latter authors observed that the dorsal epithelium of this distal part of the nasopharyngeal duct is the site of origin of the adult adenohypophysis. However, they do not specifically indicate the position of the larval adenohypophysis. During the first few days after hatching, there appears to be a steady increase in numbers of cells in

363 the early adenohypophysis of the arctic lamprey. As in the adenohypophysis of adult lampreys (BAge 1967; BAge and Fernholm 1975; van de Kamer and Schreurs 1959; Percy et al. 1975), these cells contain characteristic small secretory granules which suggest a very early endocrine activity of the gland. Taking the ultrastructure of these epithelial cells as a basis for speculation, one can assume that secretory granules are formed immediately after hatching (20th day), and that the appearance of such secretory cells is the first visible indication of the presence of an adenohypophysis. On the basis of location and ultrastructure, a pars distalis and a pars intermedia can already be distinguished on the 39th day of development. Both regions possess cells with structural features which imply some functional activity. In the cells of the primordial pars intermedia granules of intermediate or low electron density occur, a finding which differs from the adult condition, in which the cells of the pars intermedia of lampreys often contain dense granules (Percy et al. 1975; Tsuneki and Gorbman 1975a). Indirect evidence for a functional pars intermedia and hence, melanocyte stimulating hormone, is provided by the presence of melanocytes in the early larvae, which in the present study were found in the neighbourhood of blood vessels of the developing adenohypophysis. It is noteworthy that Gorbman (1980) proposes that the pars intermedia may have been the first adenohypophysial structure to evolve in vertebrates. In the pars distalis of 101 day old larvae, presumably already two secretory cell types occur. In the anterior adenohypophysis of adult P. marinus Percy et al. (1975) found at least 4 secretory cell types. These cells have been mainly characterized on the basis of the fine structure of their secretory granules, but a correlation with the production of specific hormone is not yet certain. A recent discussion of several of the hormones produced in the adult lamprey adenohypophysis is given by Nozaki (1985), who described many cells containing hormones of the pro-opiocortin family. As had been pointed out by Tsuneki and Gorbman (1975a,b), the neurohypophysis of lampreys is composed of an anterior and posterior part. The

present study has shown that this division is already established in very young larvae. While classical studies have shown the presence of arginine vasotocin in the adult lamprey neurohypophysis (Fontaine 1985; Nozaki 1985), recent evidence (Nozaki 1985; Chiba and Honma 1989) points to the additional presence of LHRH-positive fibres in the anterior part of the neurohypophysis of P. marinus, and L. japonica. Chiba and Honma (1989) also found somatostatin-immunoreactive fibres in the anterior neurohypophysis of the arctic lamprey. In this connection, Tsuneki and Gorbman's observation of 4 morphological types of axonal endings in the pars nervosa of Lampetra tridentatais of interest. Thus, both ultrastructural and immunohistochemical evidence point to the existence of several types of nerve fibre terminals in the neurohypophysis of lampreys which may represent a primitive situation. Nevertheless, it can be assumed that the majority of elementary granules in the larval neurohypophysis are associated with arginine vasotocin, which, thus, is secreted very early in ontogeny. The arrangement of the blood vascular system which is associated with the larval hypophysis appears to be strikingly simple, as is also the case in adults (Gorbman 1965). Also, the present ultrastructural study shows a simple design for the vascular endothelia which are characterized by a cytoplasm without fenestrations.

Acknowledgements We wish to express our thanks to Mr. Naoya Mori for keeping and supplying the embryos and larvae of arctic lamprey.

References cited Bage, G. 1967. Ultrastructure of the adenohypophysis of adult migrating Lampetra fluviatilis. Gen. Comp. Endocrinol. 9: 429-430. Bage, G. and Fernholm, Bo. 1975. Ultrastructure of the proadenohypophysis of the river lamprey, Lampetra fluviatilis, during gonad maturation. Acta Zool. 56: 95-118. Ball, J.N. and Baker, B.I. 1969. The pituitary gland: anatomy and histophysiology. In Fish Physiology, Vol. 2 pp. 1-110.

364 Edited by W.S. Hoar and D.J. Randall. Academic Press, New York. Chiba, A. and Honma, Y. 1989. Somatostatin- and luteinizing hormone-releasing hormone-like immunoactivities in the brains of the arctic lamprey and the gummy shark. In Abstracts of Xlth Internat. Symposium on Comparative Endocrinology, Malaga. Fontaine, Y.-A. 1985. Hormonal peptide evolution. In Evolutionary Biology of Primitive Fishes. pp. 413-432. Edited by R.E. Foreman, A. Gorbman, J.M. Dodd and R. Olsson. Plenum Press, New York. Gorbman, A. 1980. Endocrine regulation in Agnatha: Primitive or degenerate? In Hormones, Adaptation and Evolution. pp. 81-92. Edited by S. Ishii, T. Hirano and M. Wada. Japan Sci. Soc. Press, Tokyo/Springer-Verlag, Berlin. Gorbman, A. 1965. Vascular relations between the neurohypophysis and adenohypophysis of cyclostomes and the problem of evolution of hypothalamic endocrine control. Arch. Anat. Microsc. Morphol. Exp. 54: 163-194. Gorbman, A. and Tamarin, A. 1985a. Head development in relation to hypophysial development in a myxinoid, Eptatretus and a petromyzontid, Petromyzon. In The Pars Distalis: Structure, Function and Regulation. pp. 3-14. Edited by F. Yoshimura and A. Gorbman. Elsevier, Amsterdam. Gorbman, A. and Tamarin, A. 1985b. Early development of oral, olfactory and adenohypophyseal structures of agnathans and its evolutionary implications. In Evolutionary Biology of Primitive Fishes. pp. 165-185. Edited by R.E. Foreman, A. Gorbman, J.M. Dodd and R. Olsson. Plenum Press, New York and London. Honma, Y. 1960. The morphology of the pituitary gland of the sea-lamprey, Lampetra (= Entosphenus)japonica (Martens), during its anadromous period. Jap. J. Ichthyol. 8: 29-34 (in Japanese with English summary). Honma, Y. 1969. Some evolutionary aspects of the morphology and role of the adenohypophysis in fishes. Gunma Symp. Endocrinol. 6: 19-37. Kamer, J.C. van de and Schreurs, A.F. 1959. The pituitary gland of the brook lamprey (Lampetra planeri) before, during and after metamorphosis (a preliminary, qualitative investigation). Z. Zellforsch. 49: 605-630.

Kupffer, C. von. 1894. Studien zur vergleichenden Entwicklungsgeschichte des Kopfes der Kranioten. II. Die Entwicklung des Kopfes von Ammocoetes planeri. Verlag J.F. Lehmann, Muinchen. Larsen, L.O. and Rothwell, B. 1972. Adenohypophysis. In The Biology of Lampreys. Vol. 2, pp. 1-62. Edited by M.W. Hardisty and I.C. Potter, Academic Press, New York. Leach, W.J. 1951. The hypophysis of lampreys in relation to the nasal apparatus. J. Morphol. 89: 217-246. Nozaki, M. 1985. Tissue distribution of hormonal peptides. In Evolutionary Biology of Primitive Fishes. pp. 433-454. Edited by R.E. Foreman, A. Gorbman, J.M. Dodd and R. Olsson. Plenum Press, New York. Percy, R., Leatherland, J.F. and Beamish, F.W.H. 1975. Structure and ultrastructure of the pituitary gland in the sea lamprey, Petromyzon marinus, at different stages in its life cycle. Cell Tiss. Res. 157: 141-164. Piavis, G.W. 1971. Embryology. In The Biology of Lampreys. pp. 361-400. Edited by M.W. Hardisty and I.C. Potter. Academic Press, New York. Sholdice, J.A. and McMillan, D.B. 1985. Pituitary cysts in the sea lamprey of the Great Lakes, Petromyzon marinus. Gen. Comp. Endocrinol. 57: 135-149. Tahara, Y. 1988. Normal stages of development in the lamprey Lampetra reissneri (Dybowski). Zool. Sci. 5: 109-118. Tilney, F. 1937. The hypophysis cerebri in Petromyzon marinus dorsatus Wilder. Bull. Neur. Inst. New York 6: 70-117. Tsuboi, K. 1953. A cyto-histological study of the hypophysis of cyclostomes. Acta Inst. Anat. Niigataensis, 25: 97-145 (In Japanese). Tsuneki, K. and Gorbman, A. 1975a. Ultrastructure of pars nervosa and pars intermedia of the lamprey, Lampetra tridentata. Cell Tiss. Res. 157: 165-184. Tsuneki, K. and Gorbman, A. 1975b. Ultrastructure of the anterior neurohypophysis and the pars distalis of lamprey, Lampetra tridentata.Gen. Comp. Endocrinol. 25: 487-508. Wingstrand, K.G. 1966. Comparative anatomy and evolution of the hypophysis. In The Pituitary Gland. Edited by G.W. Harris and B.T. Donovan. pp. 58-126. Butterworths, London.

Development of the hypophysis of the arctic lamprey, Lampetra japonica.

The hypophysis of early larval stages, from the moment of hatching on the 18th day after fertilization to the 101st day of larval life, of the arctic ...
1MB Sizes 0 Downloads 0 Views