Histological and Ultrastructural Characterization of the Gonads of the Grunting Toadfish Allenbatrachus grunniens (Linnaeus, 1758) from the Pranburi River Estuary, Thailand

Authors

  • Tappadit Mitparian Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand
  • Sinlapachai Senarat Department of Marine Science and Environment, Faculty of Science and Fisheries Technology, Rajamangala University of Technology Srivijaya, Trang 92150, Thailand
  • Jes Kettratad Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand
  • Wannee Jiraungkoorskul Division of Pathology, Preclinical Health Science Center, Faculty of Medicine, Bangkokthonburi University, Bangkok 10170, Thailand
  • Gen Kaneko School of Arts and Sciences, University of Houston - Victoria, Texas 77901, USA
  • Niwat Kangwanrangsan Department of Pathobiology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
  • Sumate Ampawong Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand

DOI:

https://doi.org/10.48048/tis.2021.489

Keywords:

Batrachoididae, Histology, Oocytes, Reproductive cycle, Sperm, Thailand

Abstract

Information on the reproductive biology of toadfish remains limited. In this study, we examined the structure and development of gonads in the grunting toadfish Allenbatrachus grunniens (Linnaeus, 1758) using morphological, histological and ultrastructural methods. The fish were collected from the Pranburi River Estuary, Thailand, during the annual reproductive period for this species (January to December 2018). The ovary of this species was paired and had elongated sac-like structures parallel to the kidneys and the digestive tract. In females, we identified 4 oocyte differentiation phases in the ovary including oogonia proliferation phase, a primary growth phase that was further classified into 2 steps (perinucleolar and oil droplets-cortical alveolar steps), and a secondary growth phase that also contained 2 steps (secondary growth and full-grown oocyte steps) and post-ovulatory phases, indicating an asynchronous pattern in ovarian development for this species. Transmission electron microscopy showed the 4 layers including the zona pellucida, basement membrane, granulosa cells and theca cells, all of which initially appeared in the oil droplets-cortical alveolar stage. The zona pellucida and the granulosa cells were highly developed during the secondary growth stage. The granulosa cells contained abundant smooth endoplasmic reticulum near the mitochondria. In males, the spermatogenesis was classified into spermatogonium to spermatozoa. Finally, we associated the morphological gonadal developments (stage I - IV) and the gonadosomatic index (GSI value) with the cellular developmental processes in both sexes. These results help integrate various levels of reproductive observations, which will be applied to understanding the reproductive cycle and development for aquaculture.

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References

JA Munoz-Cueto, M Alvarez, M Blanco, MLGD Canales, A Garcia-Garcia and C Sarasquete. Histochemical and biochemical study of lipids during the reproductive cycle of the toadfish, Halobatrachus didactylus (Schneider, 1801). Sci. Mar. 1996; 60, 289-96.

A Arias and P Drake. Estados juveniles de la ictiofauna en los caños de las salinas de309 la Bahía de Cádiz. Instituto de Ciencias Marinas de Andalucía, Cádiz, Spain, 1990.

MAB Rubio. Estudio histológico, histoquímico y bioquímico durante la reproducción del pez sapo, Halobatrachus didactylus, (Schneider, 1801) de la Bahía de Cádiz. Reprodut 1991; 123, 355-36.

S Gupta. The development of carp gonads in warm water aquaria. J. Fish Biol. 1975; 7, 775-82.

NK Al‐Daham and MN Bhatti. Annual changes in the ovarian activity of the freshwater teleost, Barbus luteus (Heckel) from Southern Iraq. J. Fish Biol. 1979; 14, 381-7.

I Mayer, SE Shackley and JS Ryland. Aspects of the reproductive biology of the bass, Dicentrarchus labrax L. I. An histological and histochemical study of oocyte development. J. Fish Biol. 1988; 33, 609-22.

S Senarat, J Kettratad and W Jiraungkoorskul. Structure and ultrastructure of oogenic stage in short mackerel Rastrelliger brachysoma (Teleostei: Scombidae). J. Morphol. Sci. 2017; 34, 23-30

JM Wilson, RM Bunte and AJ Carty. Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J. Am. Assoc. Lab. Anim. Sci. 2009; 48, 785-9.

M Moslemi-Aqdam, JI Namin, M Sattari, S Abdolmalaki, A Bani and B Rochowski. Reproductive characteristics of nothern pike, Esox lucius (Actinopterygii: Esociformes: Esocidae), in the Anzali Wetland, southwest Caspian Sea. Acta Ichthyologica et Piscatoria 2016; 46, 313-23.

M King. Fisheries biology assessment and management. Fishing News Books, Oxford, 1995.

I Sulistyo, P Fontaine, J Rincarh, JN Gardeur, H Migaud, B Capdeville and P Kestemont. Reproductive Cycle and Plasma Level of Steroid in Male Eurasian Perch (Perca fluviatilis). Aqua. Liv. Res. 2000; 13, 99-106.

JK Presnell and MP Schreibman. Humason's animal tissue techniques. Johns Hopkins University Press, Maryland, 1997.

KS Suvarnam, C Layton, and JD Bancroft. Bancroft’s theory and practice of histological techniques. Churchill Livingstone, London, 2013.

MC Uribe, HJ Grier and LR Parenti. Ovarian structure and oogenesis of the oviparous goodeids Crenichthys baileyi (Gilbert, 1893) and Empetrichthys latos Miller, 1948 (teleostei, Cyprinodontiformes). J. Morphol. 2012; 273, 371-87.

D Dietrich and HO Krieger. Histological analysis of endocrine disruptive effects in small laboratory fish. John Wiley & Sons, New Jersey, 2009.

M Cassel, M Mehanna, L Mateus and A Ferreira. Gametogenesis and reproductive cycle of Melanorivulus aff. punctatus (Boulenger, 1895) (Cyprinodontiformes, Rivulidae) in Chapada dos Guimarães, Mato Grosso, Brazil. Neotrop. Ichthyol. 2013; 11, 179-92.

CFA Culling. Handbook of histopathological and histochemical techniques: Including museum techniques. Butterworth-Heinemann, Oxford, 1974.

G Rowden and MG Lewis. Experience with a three-hour electron microscopy biopsy service. J. Clin Pathol. 1974; 27, 505-10.

J Lahaye. Les cycles sexuels chez les poissons marins. Oceanis 1980; 6, 637-54.

RA Wallace and K Selman. Cellular and dynamic aspects of oocyte growth in teleosts. Am. Zool. 1981; 21, 325-43.

K Selman and RA Wallace. Cellular aspects of oocyte growth in teleosts. Zool. Sci. 1989; 6, 211-31.

S Senarat, J Kettratad and W Jiraungkoorskul. Testicular structure and spermatogenesis of short mackerel, Rastrelliger brachysoma (Bleeker, 1851) in The Upper Gulf of Thailand. Asia. Pac. J. Mol. Biol. Biotechnol. 2018; 26, 30-43.

K Selman, RA Wallace, QI X and A Sarka. Stages of oocyte development in the zebra fish, Brachydanio rerio. J. Morphol. 1993; 218, 203-24.

H Grier. Ovarian germinal epithelium and folliculogenesis in the common snook, Centropomus undecimalis (Teleostei: Centropomidae). J. Morphol, 2000; 243, 265-81.

RA Wallace and K Selman. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron. Microsc. Tech. 1990; 16, 175-201.

A Mandich, A Massari, S Bottero and G Marino. Histological and histochemical study of female germ cell development in the dusky grouper Epinephelus marginatus (Lowe, 1834). Eur. J. Histochem. 2002; 46, 87-100.

KS Chen, P Crone and CC Hsu. Reproductive biology of female Pacific bluefin tuna Thunnus orientalis from south‐western North Pacific Ocean. Fish. Sci. 2006; 72, 985-94.

C Sarasquete, S Cárdenas, MLGD Canales and E Pascual. Oogenesis in the bluefin tuna, Thunnus thynnus L.: A histological and histochemical study. Histol. Histopathol. 2002; 17, 775-88.

M Wiegand. Composition, accumulation and utilization of yolk lipids in teleost fish. Rev. Fish Biol. Fish. 1996; 6, 259-86.

Y Nagahama. The functional morphology of teleost gonads. In: WS Hoar, DJ Randall and EM Donaldson (Eds.). Fish physiology. Academic Press, New York, 1983, p. 223-75.

SE Shackley and PE King. Oogenesis in a marine teleost, Blennius pholis L. Cell. Tissue. Res. 1977; 181, 105-28.

Y Nagahama, H Kagawa and G Young. Cellular sources of sex steroids in teleost gonad. Can. J. Fish. Aquat. Sci. 1982; 39, 56-64.

A Fostier, B Jalabert, R Billard, B Breton and Y Zohar. The gonadal steroids. In: WS Hoar, DJ Randall and EM Donaldson (Eds.). Fish physiology. Academic Press, New York, 1983, p. 277-372.

AP Santos-Silva, DH Siqueira-Silva, A Ninhaus-Silveira and R Veríssimo-Silveira. Oogenesis in Laetacara araguaiae (Ottoni and Costa, 2009) (Labriformes: Cichlidae). Zygote 2015; 24, 502-10.

HJ Grier, CL Neidig and I Quagio‐Grassiotto. Development and fate of the postovulatory follicle complex, postovulatory follicle, and observations on folliculogenesis and oocyte atresia in ovulated common snook, Centropomus undecimalis (Bloch, 1792). J. Morphol. 2017; 278, 547-62.

JA Rodrigues-Filho, RM Honji, PH Mello, MI Borella, AWS Hilsdorf and RG Moreira. Reproductive biology of Pseudotocinclus tietensis (Siluriformes: Loricariidae: Hypoptopomatinae), a threatened fish species. Int. J. Aquat. Biol. 2017; 5, 218-27.

BJV Voorhis. Follicular Steroidogenesis. Encyclopedia of reproduction. Vol II. Academic Press, Massachusetts, 1999, p. 389-95.

H Fliigel. Licht und elektronenmikroskopische Untersuchungen an Oozyten und Eiern einiger Knochenfische. Zeitschrift für Zellforschung und Mikroskopische Anatomie 1967; 83, 82-116

Y Nagahama, WC Clarke and WS Hoar. Ultrastructure of putative steroid-producing cells in the gonads of coho (Oncorhynchus kisutch) and pink salmon (Oncorhyzchzu gorhuscha). Can. J. Zool. 1978; 56, 2508-19.

H Kagawa, K Takano and Y Nagahama. Correlation of plasma estradiol-17β and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the white-spotted char, Salvelinus leucomaenis. Cell Tissue Res. 1981; 218, 315-29.

R Cárdenas, M Chávez, JL González, P Aley, J Espinosa and LF Jiménez-García. Oocyte structure and ultrastructure in the Mexican silverside fish Chirostoma humboldtianum (Atheriniformes: Atherinopsidae). Rev. Biol. Trop. 2008; 56, 1371-80.

G Young, H Ueda and Y Nagahama. Estradiol-17 alpha, 20 beta-dihydroxy-4-pregnen-3-one production by isolated ovarian follicle of amago salmon (Oncorhynchus rhodurus) in response to mammalian pituitary and placental hormones and salmon gonadotropin. Gen. Comp. Endocrinol. 1983; 52, 329-35.

G Young, S Adachai and Y Nagahama. Role of ovarian thecal and granulosa layers in gonadotropininduced synthesis of a salmonid maturation-inducing substance (17 alpha, 20 beta-dihydroxy-4pregnen-3-one). Dev. Biol. 1986; 118, 1-8.

R Billard. Reproduction in rainbow trout: Sex differentiation, dynamics of gametogenesis, biology and preservation of gametes. Aquaculture 1992; 100, 263-98.

D Dietrich and HO Krieger. Histological analysis of endocrine disruptive effects in small laboratory fish. John Wiley & Sons, New Jersey, 2009.

R Cinquetti and L Dramis. Histological, histochemical, enzyme histochemical and ultrastructural investigations of the testis of Padogobius martensi between annual breeding seasons. J. Fish Biol. 2003; 63, 1402-28.

FLL Nostro, FN Antoneli, I Quagio-Grassiotto and GA Guerrero. Testicular interstitial cells, and steroidogenic detection in the protogynous fish, Synbranchus marmoratus (Teleostei, Synbranchidae). Tissue Cell 2004; 36, 221-31.

MC Uribe, HJ Grier and V Mejia-Roa. Comparative testicular structure and spermatogenesis in bony fishes. Spermatogenesis 2014; 4, e983400.

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Published

2021-11-11

How to Cite

Mitparian, T. ., Senarat, S. ., Kettratad, J. ., Jiraungkoorskul, W. ., Kaneko, G. ., Kangwanrangsan, N. ., & Ampawong, S. . (2021). Histological and Ultrastructural Characterization of the Gonads of the Grunting Toadfish Allenbatrachus grunniens (Linnaeus, 1758) from the Pranburi River Estuary, Thailand . Trends in Sciences, 18(22), 489. https://doi.org/10.48048/tis.2021.489