Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T18:39:23.310Z Has data issue: false hasContentIssue false

Cellular development of the germinal epithelium during the female and male gametogenesis of Chaetodon striatus (Perciformes: Chaetodontidae)

Published online by Cambridge University Press:  13 April 2020

Isabelle Leite Bayona Perez
Affiliation:
Aquaculture Center of São Paulo State University – CAUNESP – Centro de Aquicultura da Universidade Estadual Paulista ‘Julio de Mesquita Filho’, Prof. Paulo Donato Castellane s/n, 14884-900Jaboticabal-SP, Brazil
Talita Sarah Mazzoni
Affiliation:
Department of Cell and Developmental Biology, Institute of Biomedical Sciences, Federal University of Alfenas (UNIFAL), Gabriel Monteiro da Silva 700, 37130-001Alfenas-MG, Brazil
Irani Quagio-Grassiotto*
Affiliation:
Aquaculture Center of São Paulo State University – CAUNESP – Centro de Aquicultura da Universidade Estadual Paulista ‘Julio de Mesquita Filho’, Prof. Paulo Donato Castellane s/n, 14884-900Jaboticabal-SP, Brazil Department of Morphology, Institute of Biosciences of Botucatu, São Paulo State University (UNESP), Prof. Dr. Antonio Celso Wagner Zanin 250, 18618-689Botucatu-SP, Brazil
*
Author for correspondence: Irani Quagio-Grassiotto. Department of Morphology, Institute of Biosciences of Botucatu, São Paulo State University (UNESP), Prof. Dr. Antonio Celso Wagner Zanin 250, 18618-689 Botucatu-SP, Brazil. Tel: +55 14 3880 0468. E-mail: [email protected]

Summary

Butterflyfish Chaetodon striatus is highly sought after in the marine ornamental aquarium, although studies about its reproductive biology are scarce. Therefore, to contribute to a better understanding of the reproductive aspects of C. striatus, we describe in detail with the use of high resolution histology the cellular dynamics of the germinal epithelium during the reproductive life history of this species. Based on the activity of the germinal epithelium, this study describes different stages of the gonadal development, similar to the reproductive phases found in other fish, to determine the reproductive period of C. striatus. In characterization of gonadal development, the following germ cells are described for males: spermatogonia, spermatocytes, spermatids and spermatozoa. Oogonia, early, primary, secondary, full-grown and maturing oocytes are described for females. Female germinal epithelium of C. striatus showed substantial changes over the study period, indicating that there was an active spawning period. Male germinal epithelium also presented relevant alterations, indicating reproductive activity in the testicular lobules. Morphological data confirm how informative was the cellular dynamics of the germinal epithelium for understanding gonadal development during adult reproductive life of fish in general. Although Chaetodon are a popular species, previous studies have only produced superficial and rough histological analyses. Therefore, this study demonstrates important information on germinal epithelium of Chaetodon. This knowledge could be a fundamental tool for development of new strategies for breeding of several species in captivity, especially butterflyfishes.

Type
Research Article
Copyright
© Cambridge University Press 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Brown-Peterson, NJ, Wyanski, DM, Saborido-Rey, F, Macewicz, B and Lowerre-barbieri, SKA (2011) Standardized terminology for describing reproductive development in fishes. Mar Coast Fish 3, 5270.CrossRefGoogle Scholar
Colin, PL (1989) Aspects of the spawning of western Atlantic butterflyfishes (Pisces: Chaetodontidae). Environ Biol Fishes 25, 131–41.CrossRefGoogle Scholar
Degidio, JML, Yanong, RP, Watson, CA, Ohs, CL, Cassiano, EJ and Barden, K (2017) Spawning, embryology, and larval development of the milletseed butterflyfish Chaetodon miliaris in the laboratory. N Am J Aquac 79, 205–15.CrossRefGoogle Scholar
Eschmeyer, WN, Fricke, R and Van der Laan, R (2018) Catalog of fishes: genera, species, reference. [This version was edited by Bill Eschmeyer – Recalculated with each new version; based on current literature, this provides all available species names, valid species, and species described in the last 10 years by family/subfamily]. Available at: ”http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp”. Accessed July 2018.Google Scholar
Fowler, AJ (1991) Reproductive biology of bisexual and all-female populations of chaetodontid fishes from the southern Great Barrier Reef. Environ Biol Fishes 31, 261–74.CrossRefGoogle Scholar
Grier, HJ (1981) Cellular organization of the testis and spermatogenesis in fishes. Am Zool 21, 345–57CrossRefGoogle Scholar
Grier, HJ (2000) Ovarian germinal epithelium and folliculogenesis in the common snook, Centropomus undecimalis (Teleostei: Centropomidae). J Morphol 243, 265–81.3.0.CO;2-I>CrossRefGoogle Scholar
Grier, HJ (2002) The germinal epithelium: its dual role in establishing male reproductive classes and understanding the basis for indeterminate egg production in female fishes. In: Proceedings of the fifty-third annual Gulf and Caribbean Fisheries Institute. Fort Pierce: Mississippi/Alabama Sea Grant Consortium, pp. 537–52.Google Scholar
Grier, HJ and Taylor, RG (1998) Testicular maturation and regression in the common snook. J Fish Biol 53, 521–42.CrossRefGoogle Scholar
Grier, HJ and Uribe-Aranzábal, MC (2009) The testis and spermatogenesis in teleosts. In Reproductive Biology and Phylogeny of Fishes (Agnathans and Bony Fishes): Phylogeny Reproductive System Viviparity Spermatozoa, vol. 8 (ed. Jamieson, BJM), pp. 119–42. Enfield: Science Publishers.Google Scholar
Grier, HJ, Uribe-Aranzábal, MC and Patino, R (2009) The ovary, folliculogenesis, and oogenesis in teleosts. In Reproductive Biology and Phylogeny of Fishes (Agnathans and Bony Fishes): Phylogeny Reproductive System Viviparity Spermatozoa, vol. 8. (ed. Jamieson, BJM), pp. 2584. Enfield: Science Publishers.Google Scholar
Grier, HJ, Uribe, MC and Parenti, LR (2007) Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout, Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, Protacanthopterygii, Salmoniformes). J Morphol 268, 293310.CrossRefGoogle Scholar
Lubzens, E, Young, G, Bobe, J and Cerdà, J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165, 367–89.CrossRefGoogle ScholarPubMed
Mazzoni, TS and Quagio-Grassiotto, I (2017) Ovary differentiation and activity in teleostei fish. Chapter 7. In Theriogenology (ed. Carreira, RP), pp. 129–56. InTech,Google Scholar
Mazzoni, TS, Grier, HJ and Quagio-Grassiotto, I (2010) Germline cysts and the formation of the germinal epithelium during the female gonadal morphogenesis in Cyprinus carpio (Teleostei: Ostariophysi). Anat Rec 293, 1581–606.CrossRefGoogle Scholar
Mazzoni, TS, Grier, HJ and Quagio-Grassiotto, I (2014) Male gonadal differentiation and the paedomorphic evolution of the testis in Teleostei. Anat Rec 297, 1137–62.CrossRefGoogle ScholarPubMed
Mazzoni, TS, Lo Nostro, FL, Antoneli, FN and Quagio-Grassiotto, I (2018) Action of the metalloproteinases in gonadal remodeling during sex reversal in the sequential hermaphroditism of the teleostei fish Synbranchus marmoratus (Synbranchiformes: Synbranchidae). Cells 7, 34.CrossRefGoogle Scholar
Motta, PJ (2012) The Butterflyfishes: Success on the Coral Reef. Springer Science & Business Media, 251 pp.Google Scholar
Murua, H and Saborido-Rey, F (2003) Female reproductive strategies of marine fish species of the North Atlantic. J Northw Atl Fish Sci 33, 2331.CrossRefGoogle Scholar
Mylonas, CC, Fostier, A and Zanuy, S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 3, 516–34.CrossRefGoogle Scholar
Nagahama, Y (1983) The functional morphology of teleost gonads. In Fish Physiology (eds Hoar, WS, Randall, DJ and Donaldson, EM, pp. 223–75. New York: Academic Press.Google Scholar
Nagpure, NS, Kumar, R, Srivastava, SK, Kushwaha, B, Gopalakrishnan, A and Basheer, VS (2006) Cytogenetic characterization of two marine ornamental fishes, Chaetodon collare and Stegastes insularis. J Mar Biol Ass India 48, 267–9.Google Scholar
Nowicki, JP, O’Connell, LA, Cowman, PF, Walker, SP, Coker, DJ and Pratchett, MS (2018) Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding. PLoS One 13, e0194465.CrossRefGoogle ScholarPubMed
Pandian, TJ (2010) Sexuality in Fishes. FL: Science Publishers, 189 pp.CrossRefGoogle Scholar
Parenti, LR and Grier, HJ (2004) Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 44, 333–48.CrossRefGoogle ScholarPubMed
Quagio-Grassiotto, I, Grier, HJ, Mazzoni, TS, Nóbrega, RH and Amorim, JPA (2011) Activity of the ovarian germinal epithelium on the follicle formation and the oocyte development in the freshwater catfish Pimelodus maculatus (Teleostei: Ostariophysi: Siluriformes). J Morph 272, 1290–306.CrossRefGoogle Scholar
Quintero-Hunter, I, Grier, HJ and Muscato, M (1991) Enhancement of histological detail using Metanil Yellow as counterstain in periodic acid/Schiff´s hematoxylin staining of glycol methacrylate tissue sections. Biotech Histochem 66, 169–72.CrossRefGoogle Scholar
Ralston, S (1981) Aspects of the reproductive biology and feeding ecology of Chaetodon miliaris, a Hawaiian endemic butterflyfish. Environ Biol Fishes 6, 167–76.CrossRefGoogle Scholar
Rising Tide Conservation (2019) Successful aquaculture of the banded butterflyfish, Chaetodon striatus! Available at https://www.risingtideconservation.org/successful-aquaculture-of-the-banded-butterflyfish-chaetodon-striatus/Accessed October 2019.Google Scholar
Schulz, RW, França, LR, Lareyre, JJ, Legac, F, ChiarinI-Garcia, H, Nóbrega, RH and Miura, T (2010). Spermatogenesis in fish. Gen Comp Endocrinol 165, 390411.CrossRefGoogle ScholarPubMed
Selman, K and Wallace, RA (1986) Gametogenesis in Fundulus heteroclitus. Amer Zool 26, 173192.CrossRefGoogle Scholar
Tyler, CR and Sumpter, JP (1996) Oocyte growth and development in teleosts. Rev Fish Biol Fish 6, 287318.CrossRefGoogle Scholar
Vazzoler, AEAM (1996) Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 pp.Google Scholar