Histological and ultrastructural investigation of early gonad development and sex differentiation in adriatic sturgeon (Acipenser naccarii, acipenseriformes, chondrostei)

Journal of Morphology

Volumn 269, Issue 10, 2008, Pages 1238-1262

  Grandi, Gilberto ^a   Chicca, Milvia ^a  

^a UNIVERSITY OF FERRARA   (Italy)

Author keywords

Acipenseridae; Chondrostei; Gonadogenesis; Histology; Sex differentiation; Ultrastructure

Indexed keywords

ANIMAL; ARTICLE; CYTOLOGY; FEMALE; FISH; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; OVARY; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEX DIFFERENTIATION; TESTIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; FEMALE; FISHES; LARVA; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; OVARY; SEX DIFFERENTIATION; TESTIS;

ACIPENSER NACCARII; ACIPENSERIDAE; ACIPENSERIFORMES; CHONDROSTEI;

EID: 53549096801     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10657     Document Type: Article

References (67)

1. Akhundov MM. 1988. Early gametogenesis and gonadogenesis in Russian sturgeon. Acipenser güeldenstädti. Brandt. Izvest Akad Nauk Azerbaid Ser Biol Nauk 2:76-31.
2. Akhundov MM, Fedorov KY. 1991. Early gametogenesis and gonadogenesis in sturgeons, Part 1: On criteria for comparative assessment of juvenile gonadal development in the example of the Russian sturgeon. Acipenser gueldenstaedtii. J Ichthyol 31:101-114.
3. Akimova NV, Malyutin VS, Smolyanov II, Sokolov LI. 1979. Growth and gametogenesis of the Siberian sturgeon (Acipenser baeri Brandt) under experimental and natural conditions. In the Proceedings of the 7th Japan-Sovietic Joint Symposium on Aquaculture, Tokyo, p 179-183.
4. Arlati G, Bronzi P, Colombo L, Giovannini G. 1988. Induzione della riproduzione nello storione italiano (Acipenser naccarii) allevato in cattività. Riv Ital Acquacol 23:94-96.
5. Azevedo C. 1984. Development and ultrastructural autoradiographic studies of nucleolus-like bodies (nuage) in oocytes of a viviparous teleost (Xiphophorus helleri). Cell Tissue Res 238:121-128.
6. Begovac PC, Wallace RA. 1988. Stages of oocyte development in the pipefish. Syngnathus scovelli. J Morphol 197:353-369.
7. Braat AK, Speksnijder JE, Zivkovic D. 1999. Germ line development in fishes. Int J Dev Biol 43:745-760.
8. Bruslè S. 1980. Fine structure of early previtellogenic oocytes in Mugil (Liza) auratus Risso, 1810 (Teleostei. Mugilidae). Cell Tissue Res 207:123-134.
9. Bruslè-Sicard S, Reinboth S, Fourcault B. 1994. Germinal potentialities during sexual state changes in a protandric hermaphrodite. (Teleostei, Pomacentridae) J Fish Biol 36:383-390.
10. Bruslè-Sicard S, Debas, Fourcault B, Fuchs J. 1992. Ultrastructural study of sex inversion in a protogynous hermaphrodite Epinephelus microdon (Teleostei Serranidae). Reprod Nutr Dev 32:393-406.
11. Carlson JG, Handel MA. 1988. Intercellular bridges and factors determining their patterns in the grasshopper testis. J Morphol 196:173-185.
12. Chieffi G. 1975. The reproductive system of elasmobranches: Development and endocrinological aspects. In: Gilbert PW, Mathewson RS, Rall DP, editors. Sharks, Skates and Rays. Baltimore Maryland: Johns Hopkins Press. pp 553-589.
13. Cruz-Höfling MA, Cruz-Landim C. 1984. Ultrastructural and histological studies on the Leydig and Sertoli cell homologues in the testis of Triportheus elongatus (Sardinhão) and Mylossoma aureum (Pacu). Cytobios 41:161-174.
14. Dettlaff TA, Ginsburg AS, Schmalhausen OL 1993. Sturgeon Fishes: Developmental Biology and Aquaculture. Berlin, Heidelberg: Springer-Verlag. p 300.
15. Devlin RH, Nagahama Y. 2002. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture 208:191-364.
16. Doroshov JN, Moberg GP, Van Eenennaam JP. 1997. Observations on the reproductive cycle of cultured white sturgeon. Acipenser transmontanus. Environ Biol Fish 48:265-278.
17. Doroshov JN, Van Eenennaam JP, Chapman FA, Doroshov SI. 1991. Histological study of the ovarian development in wild white sturgeon, Acipenser transmontanus. In: Williot PR, editor. Acipenser. Bordeaux: CEMAGREF Publ. pp 129-135.
18. Eddy EM. 1975. Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229-280.
19. Fedorov KY, Zubova SZ, Semenov VV, Burlakov AB. 1990. Secretory cells in the gonad of juvenile sterlet sturgeon Acipenser ruthenus, during sexual differentiation. J Ichthyol 30: 65-75.
20. Flores JA, Burns JR. 1993. Ultrastructural study of embryonic and early adult germ cells and their support cells in both sexes of Xiphophorus (Teleostei: Poeciliidae). Cell Tissue Res 271:263-270.
21. Flynn SR, Matsuoka M, Reith M, Martin-Robichaud DJ, Benfey TJ. 2006. Gynogenesis and sex determination in shortnose sturgeon. Acipenser brevirostrum Lesuere. Aquaculture 353: 721-727.
22. Fontana F, Colombo G. 1974. The chromosomes of Italian sturgeons. Experientia 30:739-742.
23. Godin I, Wylie C, Heasman J. 1990. Genital ridges exert long-range effects on mouse primordial germ cell number and direction of migration in culture. J Development 108:357-363.
24. Grandi G, Chicca M. 2004. Early development of the pituitary gland in Acipenser naccarii (Chondrostei. Acipenseriformes): An immunocytochemical study. Anat Embryol 208:311-321.
25. Grandi G, Giovannini S, Chicca M. 2007. Gonadogenesis in early developmental stages of Acipenser naccarii and influence of estrogen immersion on feminization. J Appl Ichthyol 23:3-8.
26. Gresik EW. 1973. Fine structural evidence for the presence of nerve terminals in the testis of the teleost. Oryzias latipes. Gen Com Endocrinol 21:210-213.
27. Grier H. 2000. Ovarian germinal epithelium and folliculogenesis in the common snook. Centropomus undecimalis (Teleostei, Centropomidae). J Morphol 243:265-281.
28. Grier HJ, Uribe MC, Parenti LR. 2007. Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout. Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, Protacanthopterygii, Salmoniformes). J Morphol 268:293-310.
29. Hamaguchi S. 1985. Changes in the morphology of the germinal dense bodies in primordial germ cells of the teleost. Oryzias latipes. Cell Tissue Res 240:669-673.
30. Hoar WS. 1969. Reproduction. In: Hoar WS, Randall DJ, Donaldson EM, editors. Fish Physiology, Vol. 3. New York: Academic Press. pp 1-72.
31. Le Menn F, Pelissero C. 1991. Histological and ultrastructural studies of oogenesis of the Siberian sturgeon (Acipenser baeri). In: Williot PR, editor. Acipenser. Bordeaux: CEMAGREF Publ. pp 129-135.
32. Lin F, Dabrowski K, Timmermans LPM. 1997. Early gonadal development and sexual differentiation in muskellunge (Esox masquinongy). Can J Zool 75:1262-1269.
33. Mattei X, Mattei I, Marchand B, Kit DLT. 1982. Ultrastructure des cellules de Sertoli d'un poisson téléostéèn: Abudefdul marginatus. J Ultras Res 81:333-340.
34. Mattei X, Siau Y, Thiaw OT, Thain D. 1993. Peculiarities in the organization of testis Ophidion sp. (Pisces Teleosts). Evidence for two types of spermatogenesis in teleost fish. J Fish Biol 43:931-937.
35. Meijide FJ, Lo Nostro FL, Guerrero GA. 2005. Gonadal development and sex differentiation in the cichlid fish Cichlasoma dimerus (Teleostei. Perciformes): A light and electron-microscopic study. J Morphol 264:191-210.
36. Mojazi Amiri B, Maebayashi M, Adachi S, Yamauchi K. 1996a. Testicular development and serum sex steroid profiles during the annual sexual cycle of the male sturgeon hybrid, the bester. J Fish Biol 48:1039-1050.
37. Mojazi Amiri B, Maebayashi M, Hara A, Adachi S, Yamauchi K. 1996b. Ovarian development and serum sex steroid and vitellogenin profiles in the female cultured sturgeon hybrid, the bester. J Fish Biol 48:1164-1178.
38. Nakamura M, Nagahama Y. 1989. Differentiation and development of Leydig cells, and changes of testosterone levels during testicular differentiation in tilapia Oreochromis niloticus. Fish Physiol Biochem 7:211-219.
39. Nakamura M, Nagahama Y 1993. Ultrastructural study on the differentiation and development of steroid-producing cells during ovarian differentiation in the amago salmon. Oncorhynchus rhodurus. Aquaculture 112:237-251.
40. Nakamura M, Nagahama Y 1995. Innervation of testes in the tilapia Oreochromis niloticus. Aquaculture 133:41-49.
41. Nakamura M, Specker JL, Nagahama Y 1993. Ultrastructural analysis of the developing follicle during early vitellogenesis in tilapia. Oreochromis niloticus, with special reference to the steroid producing cells. Cell Tissue Res 272:33-39.
42. Nakamura M, Kobayashi T, Chang XT, Nagahama Y 1998. Gonadal sex differentiation in teleost fish. J Exp Zool 281:362-372.
43. Omoto N, Maebayashi M, Hara A, Adachi S, Yamauchi K. 2004. Gonadal maturity in wild sturgeons; Huso dauricus. Acipenser mikadoi and A. schrenckii caught near Hokkaido, Japan. Environ Biol Fish 70:381-391.
44. Omoto N, Maebayashi M, Mitsuhashi E, Yoshitomi K, Adachi S, Yamauchi K. 2001. Histological observations of gonadal sex differentiation in the F2 hybrid sturgeon, the bester. Fish Sci 67:1104-1110.
45. Peplin ME, Spradling AC. 1998. Female mouse germ cells form synchronously dividing cysts. Development 125:3323-3328.
46. Reynolds ES. 1963. The use of lead citrate at high pH as electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.
47. Rossi R, Grandi G, Trisolini R, Franzoi P, Carrieri A, Dezfuli BS, Vecchietti E. 1992. Osservazioni sulla biologia e la pesca dello storione cobice Acipenser naccarii Bonaparte nella parte terminale del flume Po. Atti Soc It Sci Nat Mus St Nat Milano 132:121-142.
48. Ruby JR, Dyer RF, Skalko RG. 1969. The occurence of intercellular bridges during oogenesis in the mouse. J Morphol 127:307-340.
49. Satoh N. 1974. Intercellular bridges between oocytes in developing ovary of the teleost. Oryzias latipes. Annot Zoolog Jap 47:215-220.
50. Schulz RW, Miura T. 2002. Spermatogenesis and its endocrine regulation. Fish Physiol Biochem 26:43-56.
51. Selman K, Wallace RA, Sarka A, Qi X. 1993. Stages of oocyte development in the zebrafish, Brachydanio rerio. J Morphol 218:203-224.
52. Skalko RG, Kerrigan JM, Ruby JR, Dyer RF. 1972. Intercellular bridges between oocytes in the chicken ovary. Z Zeilforsch 128:31-41.
53. Strüssmann CA, Nakamura M. 2002. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol Biochem 26:13-29.
54. Strüssmann CA, Takashima F, Toda K. 1996. Sex differentiation and hormonal feminization in pejerrey Odontesthes bonarien-sis. Aquaculture 139:31-45.
55. Toury R, Clérot JC, André J. 1977. Les groupements mitochon-driaux des cellules germinales des poissons Télé ostéens Cypri-nidés IV Analyses biochémique des constituants du 'ciment' intermitochondrial isolé. Biol Cell 30:225-232.
56. Tyler CR, Sumpter JP. 1996. Oocyte growth and development in teleosts. Rev Fish Physiol Fish 6:287-318.
57. Van Eenennaam JP, Doroshov SI. 1998. Effects of age and body size on gonadal development of Atlantic sturgeon. J Fish Biol 83:624-637.
58. Van Eenennaam AL, Van Eenennaam JP, Medrano JF, Doroshov SI. 1999. Evidence of female heterogametic genetic sex determination in white sturgeon. J Hered 90:231-233.
59. Van Winkoop A, Booms GHR, Dulos GJ, Timmermans LPM. 1992. Ultrastructural changes in primordial germ cells during early gonadal development of the common carp (Cyprinus carpio L. Teleostei). Cell Tissue Res 267:337-346.
60. Ventelä S, Toppari J, Parvinen M. 2003. Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: Mechanism of haploid gene product sharing. Mol Biol Cell 14:2768-2780.
61. Wallace RA, Selman K. 1990. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J Electron Microsc Tech 16:175-201.
62. Wibbels T, Bull JJ, Crews D. 1994. Temperature-dependent sex determination: A mechanistic approach. J Exp Zool 270:71-78.
63. Williot PR, Brun R, Rouault T, Rooryck O. 1991. Management of female spawners of the Siberian sturgeon, Acipenser baeri Brandt: First results. In: Williot PR, editor. Acipenser. Bordeaux: CEMAGREF publ. pp 365-380.
64. Wrobel KH, Jouma S. 2004. Morphology, development and comparative anatomical evaluation of the testicular excretory pathway in Acipenser. Ann Anat 186:99-113.
65. Wrobel KH, Hees I, Geseres S, Schimmed M. 2002a. The genus Acipenser as a model for a model for vertebrate urogenital development: Ultrastructure of nephrostomial tubule formation and of initial gonadogenesis. Ann Anat 184:443-454.
66. Wrobel KH, Hees I, Schimmed M, Stauber E. 2002b. The genus Acipenser as a model for vertebrate urogenital development: Nephrostomial tubules and their significance for the origin of the gonad. Anat Embryol 205:67-80.
67. Yamamoto T. 1969. Sex differentiaton. In: Hoar WS, Randall DJ, editors. Fish Physiology, Vol. 3. New York: Academic Press. pp 117-175.