Fine structure of neurosecretory cells and sinus gland in the eyestalk of the freshwater crab Travancoriana schirnerae Bott, 1969 (Decapoda: Gecarcinucidae)

Sudha Devi Arath Raghavan , Aswani Ayanath and Bhadravathi Kenchappa Chandrasekhar Sagar

Abstract
This study elucidated the fine structure of neurosecretory cells and sinus gland in the optic ganglia of the freshwater crab Travancoriana schirnerae Bott, 1969 (Decapoda: Gecarcinucidae). The eyestalk ganglion showed the presence of four well defined ganglia arranged below the ommatidium: lamina ganglionaris, medulla externa, medulla interna and medulla terminalis of which the lamina ganglionaris, was devoid of neurosecretory cells. Groups of neurosecretory cells seen distributed along the medulla externa, interna and terminalis regions constitute the X-organs. Electron microscopic observations of the eyestalk ganglia revealed ten types of neurosecretory cells, mostly apolar with a few unipolar and bipolar cells classified according to the size, shape and density of the cell and nucleus, cell organelles/inclusions, together with the arrangement and properties of chromatin. These cells were characterized by the presence of large nuclei with unusually condensed chromatin, inclusions like vacuoles and vesicles of varying size, shape and density and organelles like Golgi, endoplasmic reticulum, ribosomes and mitochondria and neurosecretory material. The sinus gland of T. schirnerae was positioned laterally between the externa and interna regions, composed of axonal endings of the neurosecretory cells of the optic ganglia with interspersed glial cells. The axon terminals were enclosed with several small to large membrane bound homogenously dense neurosecretory granules which also occur in the preterminal areas of the axons. Based on size, shape and density of granules and axoplasmic matrix, seven terminal types could be distinguished in the sinus gland of T. schirnerae. Mostly, the granules contained in a terminal were of the same type; rarely, the same terminal enclosed granules of varying size, shape and density. The neurosecretory cell types and axon terminal types represent the types of neurohormones they contained. A precise knowledge of the morphology and cytology of neurosecretory cells in the XO-SG complex of the eyestalk that secrete neurohormones controlling major physiological processes such as growth and reproduction is imperative for successful captive breeding of a species of aquaculture potential.

Keywords
Eyestalk; Freshwater crab; Neurosecretory cells; Sinus gland; Travancoriana schirnerae.

DOI
10.21472/bjbs.061406

Full text
PDF

References
Andrew, R. D.; Orchard, I.; Salleudin, S. S. M. Structural re-evaluation of the neurosecretory system in the crayfish eyestalk. Cell and Tissue Research, v. 190, p. 235-246, 1978. http://doi.org/10.1007/BF00218172

Andrews, P. M.; Copeland, D. E.; Fingerman, M. Ultrastructural study of the neurosecretory granules in the sinus gland of the blue crab, Callinectes sapidus. Zeitschrift für Zellforschung und Mikroskopische Anatomie, v. 113, p. 461-471, 1971. http://doi.org/10.1007/BF00325666

Beams, H. W.; Kessel, R. G. The Golgi apparatus: Structure and function. International Review of Cytology, v. 23, p. 209-276, 1968. https://doi.org/10.1016/S0074-7696(08)60273-9

Bellon-Humbert, C.; Van Herp, F.; Strolenberg, G. E.; Denucé, J. M. Histological and physiological aspects of the medulla externa X organ, a neurosecretory cell group in the eyestalk of Palaemon serratus Pennant (Crustacea, Decapoda, Natantia). The Biological Bulletin, v. 160, no. 1, p. 11-30, 1981. http://doi.org/10.2307/1540897

Beltz, B. S. Crustacean neurohormones. In: Beltz, B. S.; Laufer, H.; Downer, R. G. H. (Eds.). Endocrinology of selected invertebrate types. New York: A. R. Liss, 1988. p. 235-258.

Bharathi, A.; Sarojini, N.; Padmaja, M. Comparative study of neurosecretory cells in female Penaeus indicus after unilateral eyestalk ablation. International Journal of Scientific and Research Publications, v. 4, no. 7, p. 1-4, 2014.

Bliss, D. E.; Welsh, J. H. The neurosecretory system of brachyuran Crustacea. The Biological Bulletin, v. 103, p. 157-169, 1952. https://doi.org/10.2307/1538442

Bressac, C. Etude ultrastructurale de la glande du sinus du crabe, Pachygrapsus marmoratus. Comptes Rendus de l'Académie des Sciences - Series D, v. 282, p. 1529-1531, 1976.

Bunt, A. H.; Ashby, E. A. Ultrastructure of the sinus gland of the crayfish Procambarus clarkii. General and Comparative Endocrinology, v. 9, no. 3, p. 334-342, 1967. https://doi.org/10.1016/0016-6480(67)90027-5

Carlisle, D. B. Note preliminaire sur la structure du systeme neurosecreteur du pedoncle oculaire de Lysmata seticaudata Risso (Crustacea). Comptes Rendus de l'Académie des Sciences - Series D, v. 236, p. 2541-2542, 1953.

Carlisle, D. B. On the sexual biology of Pandalus borealis (Crustacea Decapoda). I. Histology of incretory elements. Journal of the Marine Biological Association of the United Kingdom, v. 38, p. 381-394, 1959. https://doi.org/10.1017/S0025315400006160

Carlisle, D. B.; Knowles, F. G. W. Endocrine control in crustaceans. London: Cambridge University Press, 1959.

Castany, J.; Van Herp, F.; Charmantier, G.; Trilles, J. P.; Charmantier-Daures, M. Ultrastructural study of the neurosecretory granules and crustacean hyperglycemic hormone (CHH) immunolocalization in the sinus gland of Homarus gammarus. Journal of Crustacean Biology, v. 17, no. 1, p. 6-12, 1997. http://doi.org/10.1163/193724097X00025

Chandy, J. P.; Kolwalker, D. G. Neurosecretion in the marine crab, Charybdis lucifera. Indian Journal of Marine Science, v. 14, p. 31-34, 1985.

Charmantier, G.; Charmantier-Daures, M.; Van Herp, F. Hormonal regulation of growth and reproduction in crustaceans. In: Fingerman, M.; Nagabhushanam, R.; Thompson, M. F. (Eds.). Endocrinology and reproduction. Enfield, NH: Science Publishers, 1997. v. 1. p. 109-201.

Charmantier-Daures, M.; Segonzac, M. Organ of Bellonci and sinus gland in three decapods from Atlantic hydrothermal vents: Rimicaris exoculata, Chorocaris chacei, and Segonzacia mesatlantica. Journal of Crustacean Biology, v. 18, no. 2, p. 213-223, 1998. http://doi.org/10.2307/1549315

Dietz, R. A. Eyestalk histology and the effects of eyestalk ablation on the gonads of the shrimp, Macrobrachium rosenhergii (De Man). Texas A&M University, College Station, 1982. (Ph.D. thesis).

Dircksen, H. Fine structure of the neurohemal sinus gland of the shore crab, Carcinus maenas, and immuno-electron-microscopic identification of neurosecretory endings according to their neuropeptide contents. Cell and Tissue Research, v. 269, p. 249-266, 1992. http://doi.org/10.1007/BF00319616

Diwan, A. D.; Nagabhushanam, R. The neurosecretory cells of the central nervous system of the freshwater crab Barytelphusa cunicularis (Westwood 1836). Rivista di Biologia, v. 68, p. 79-99, 1975.

Durand, J. B. Neurosecretory cell types and their neurosecretory activities in the crayfish. The Biological Bulletin, v. 111, p. 62-76, 1956.

Enami, M. The sources and activities of two chromatophorotropic hormones in crabs of the genus Sesarma. II. Histology of incretory elements. Cell and Tissue Research, v. 101, p. 241-258, 1951.

Fernandez, R.; Radhakrishnan, E. V. Classification and mapping of neurosecretory cells in the optic, supraoesophageal and thoracic ganglia of the female spiny lobster Panulirus homarus (Linnaeus, 1758) and their secretory activity during vitellogenesis. Journal of the Marine Biological Association of India, v. 52, no. 2, p. 237-248, 2010.

Fingerman, M.; Nagabhushanam, R.; Sarojini, R. Vertebrate-type hormones in crustaceans: Localization, identification and functional significance. Zoological Science, v. 10, p. 13-29, 1993.

Frasca, J. M.; Parks, V. R. A routine technique for double-staining ultrathin sections using uranyl and lead salts. The Journal of Cell Biology, v. 25, no. 1, p. 157-161, 1965. http://doi.org/10.1083/jcb.25.1.157

Giulianini, P. G.; Smullen, R. P.; Bentley, M. G.; Ferrero, E. A. Cytological and immunocytochemical study of the sinus gland in the Norway lobster Nephrops norvegicus (L.). Invertebrate Reproduction & Development, v. 33, no. 1, p. 57-68, 1998. http://doi.org/10.1080/07924259.1998.9652342

Gunawardene, Y. I. N. S.; Tobe, S. S.; Bendena, W. G.; Chow, B. K. C.; Yagi, K. J.; Chan, S.-M. Function and cellular localization of farnesoic acid O-methyltransferase (FAMeT) in the shrimp, Metapenaeus ensis. European Journal of Biochemistry, v. 269, p. 3587-3595, 2002. http://doi.org/10.1046/j.1432-1033.2002.03048.x

Heuser, J. E.; Doggenweiler, C. F. The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. Journal of Cell Biology, v. 30, no. 2, p. 381-403, 1966. http://doi.org/10.1083/jcb.30.2.381

Hisano, S. Neurosecretory cell types in the eyestalk of the freshwater prawn Palaemon paucidens. An electron microscopic study. Cell and Tissue Research, v. 166, p. 511-520, 1976. http://doi.org/10.1083/jcb.30.2.381

Hisano, S. The eyestalk neurosecretory cell types in the freshwater prawn Palaemon paucidens: I. A light microscopical study. Journal of the Faculty of Science, Hokkaido University, Series 6, Zoology, v. 19, p. 503-514, 1974.

Hodge, M. H.; Chapman, G. B. Some observations on the fine structure of the sinus gland of a land crab Gecarcinus lateralis. The Journal of Biophysical and Biochemical Cytology, v. 4, no. 5, p. 571-575, 1958. http://doi.org/10.1083/jcb.30.2.381

Hopkins, C. R. The fine localization of acid phosphatase in the prolactin cell of the teleost pituitary following the stimulation and inhibition of secretory activity. Tissue and Cell, v. 1, no. 4, p. 653-671, 1969. https://doi.org/10.1016/S0040-8166(69)80039-X

Hsu, K.; Song, X.; Zhang, T. Microtubular structure of the specific axon wall in the nerve fiber of the shrimp (Penaeus orientalis). Acta Zoologica Sinica, v. 26, p. 220-221, 1980.

Knowles, F. G. W. Crustacean colour change and neurosecretion. Endeavour, v. 14, no. 54, p. 95-104, 1955.

Knowles, F. G. W.; Carlisle, D. B. Endocrine control in the Crustacea. Biological Reviews, v. 81, p. 396-473, 1956. http://doi.org/10.1111/j.1469-185X.1956.tb01556.x

Kuffier, S. W.; Nichols, J. G. The physiology of neuroglial cells. Ergebnisse der Physiologie, Biologischen Chemie und Experimentellen Pharmakologie, v. 57, p. 1-90, 1966.

Lake, P. S. Histochemical studies of the neurosecretory system of Chirocephalus diaphanus Prevost (Crutacea: Anostraca). General and Comparative Endocrinology, v. 14, p. 1-15, 1970. https://doi.org/10.1016/0016-6480(70)90001-8

Lederis, K. Ultrastructure of the hypothalamo-neurohypophysial system in teleost fishes and isolation of hormone containing granules from the neurohypophysis of the cod (Gadus morrhua). Zeitschrift für Zellforschung und Mikroskopische Anatomie, v. 58, p. 192-213, 1962. http://doi.org/10.1007/BF00320184

Matsumoto, K. Morphological studies on the neurosecretion in crabs. Biological Journal of Okayama University, v. 4, p. 103-176, 1958.

Matsumoto, K. Neurosecretion in the thoracic ganglion of the crab, Eriocheir japonicus. The Biological Bulletin, v. 106, p. 60-68, 1954. https://doi.org/10.2307/1538779

McAlear, J. H.; Milburn, N. S.; Chapman, G. B. The fine structure of Schwann cells, nodes of Ranvier and Schmidt-Lanterman incisures in the central nervous system of the crab, Cancer irroratus. Journal of Ultrastructure Research, v. 2, no. 2, p. 171-176, 1958. https://doi.org/10.1016/S0022-5320(58)90015-7

Meusy, J. J. Precisions nouvelles sur l'ultrastructure de la glande du sinus d'un Crustace Decapode Brachyoure. Carcinus maenas L. Bulletin de la Société Zoologique de France, v. 93, p. 291-299, 1968.

Mohamed, K. S.; Diwan, A. D. Neuroendocrine regulation of ovarian maturation in the Indian white prawn Penaeus indicus H. Milne Edwards. Aquaculture, v. 98, p. 381-393, 1991. http://doi.org/10.1016/0044-8486(91)90320-7

Mohamed, K. S.; Vijayan, K. K.; Diwan, A. D. Histomorphology of the neurosecretory system in the Indian white prawn Penaeus indicus H. Milne Edwards. Bulletin of the Institute of Zoology, Academia Sinica, v. 32, no. 1, p. 39-53, 1993.

Nagabhushanam, R.; Sarojini, R. Neurosecretion in the central nervous system of the hermit crab, Diogenes bicristimanus. Proceedings of the Indian Academy of Sciences - Section B, v. 69, p. 20-28, 1969.

Nagabhushanam, R.; Sarojini, R.; Joshi, P. K. Observations on the neurosecretory cells on the marine penaeid prawn, Parapenaeopsis stylifera. Journal of Advanced Zoology, v. 7, no. 2, p. 63-70, 1986.

Nakamura, K. Studies on the neurosecretion of the prawn, Penaeus japonicus. I. Positional relationship of the cell groups located on the supra oesophageal and optic ganglion. Memoirs of the Faculty of Fisheries, Kagoshima University, v. 23, p. 175-184, 1974.

Naylor, E.; Smith, G.; Williams, B. G. The role of the eyestalk in the tidal activity rhythm of the shore crab Carcinus maenas (L). Neurobiology of Invertebrates, v. 1971, p. 423-429, 1993.

Nishiitsutsuji-Uwo, J. Fine structure of neurosecretory system in Lepidoptera. Nature, v. 188, p. 953-954, 1960. https://doi.org/10.1038/188953b0

Padmaja, M.; Deecaraman, M.; Jaganathbose, M. T. Study of neurosecretory cells in sand lobster Thenus orientalis of Royapuram Coast-Chennai. World Journal of Fish and Marine Sciences, v. 2, no. 2, p. 82-85, 2010.

Pandey, A. K.; Pandey, S.; Sridar, N.; Singh, S. P. Studies of neurosecretory cells of eyestalk, brain and thoracic ganglia of Metapenaeus dobsoni (Miers, 1878) in relation to ovarian maturation. Journal of Experimental Zoology, v. 18, no. 1, p. 417-428, 2015.

Parameswaran, R. Neurosecretory cells of the central nervous system of the crab, Paratelphusa hydrodromous. Journal of Cell Science, v. 3, no. 37, p. 75-82, 1956.

Pentreath, V. W. Invertebrate glial cells. Comparative Biochemistry and Physiology Part A: Physiology, v. 93, no. 1, p. 77-83, 1989. https://doi.org/10.1016/0300-9629(89)90194-1

Potter, D. D. Histology of the neurosecretory system of the blue crab, Callinecres sapidus. The Anatomical Record, v. 120, p. 216, 1954.

Potter, D. D. Observations on the neurosecretory system of portunid crabs. In: Bargmann, W.; Hanstrom, B.; Scharrer, B.; Scharrer, E. (Eds.). Zweites Internationales Symposium über Neurosekretion. Berlin: Springer, 1958. http://doi.org/10.1007/978-3-642-53252-8_23

Rajendiran, S.; Vasudevan, S. Localization and identification of crustacean hyperglycemic hormone producing neurosecretory cells in the eyestalk of blue swimmer crab, Portunus pelagicus. Microscopy Research & Technique, v. 79, no. 11, p. 1024-1030, 2016. http://doi.org/10.1002/jemt.22737

Rehm, M. Observations on the localisation and chemical constitution of neurosecretory material in nerve terminals in Carcinus maenas. Acta Histochemica, v. 7, p. 88-106, 1959.

Roots, B. I. The evolution of myelinating cells. In: Vernadakis, A.; Roots, B. (Eds.). Neuronglia interrelations during phylogeny: I. Phylogeny and ontogeny of glial cells. Totawa, New Jersey: Humana Press, 1995. p. 223-248.

Shivers, R. R. Fine structure of crayfish optic ganglia. University Kansas Science Bulletin, v. 47, p. 666-733, 1967.

Silverthorn, U. S. Neurosecretion in the sinus gland of the fiddler crab, Uca pugnax. Cell and Tissue Research, v. 165, p. 129-133, 1975. http://doi.org/10.1007/BF00222805

Smith, G. The ultrastructure of the sinus gland of Carcinus maenas (Crustacea: Decapoda). Cell and Tissue Research, v. 155, no. 1, p. 117-125, 1974. http://doi.org/10.1007/BF00220288

Smith, G. The neurosecretory cells of the optic lobe in Carcinus maenas (L). Cell and Tissue Research, v. 156, no. 3, p. 403-409, 1975. https://doi.org/10.1007/BF00225368

Upadhyaya, R. K. Correlative cyclic changes in neurosecretory cells and gonads of a freshwater prawn M. malcolmsonii (H. Milne Edwards) and its fishery in Weinganga River. Bhopal: Berktullah University, 2000. (Thesis of doctorate).

Van Herp, F.; Bellon Humbert, C.; Luub, J. T. M.; Van Wormhoudt, A. A histophysiological study of the eyestalk of Palaemon serratus (Pennant) with special reference to the impact of light and darkness. Archives de Biologie, v. 88, p. 257-278, 1977.

Weatherby, T. M. Ultrastructural study of the sinus gland of the crab, Cardisoma carnifex. Cell and Tissue Research, v. 220, p. 293-312, 1981. http://doi.org/10.1007/BF00210510

Wigglesworth, V. B. The nutrition of the central nervous system in the cockroach Periplaneta americana L: The role of perineurium and glial cells in the mobilization of reserves. Journal of Experimental Biology, v. 37, no. 3, p. 500-512, 1960.

Xu, H.; Terakawa, S. Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. Journal of Experimental Biology, v. 202, p. 1979-1989, 1999.


ISSN 2358-2731