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Impact of captive conditions on female germinal epithelium of the butterflyfish Chaetodon striatus (Perciformes: Chaetodontidae)

Published online by Cambridge University Press:  15 January 2021

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

Summary

Chaetodon striatus is a cosmopolitan seawater species present in aquaria all over the world and its extractivism is quite high. The lack of studies on the reproductive biology of C. striatus contributes to the difficulty in managing the species outside its natural habitat. Without knowledge of the mechanisms that control or affect gonadal changes, reproduction of C. striatus in captivity has become almost impossible, considering that the species is quite sensitive and the effect of captive conditions on its reproductive biology is unknown. Therefore, this study aimed to evaluate the effect on its reproductive biology of the animal’s confinement and possible alteration in structure of the ovaries. In C. striatus, after oocyte development, for animals confined in small spaces, maturing oocytes undergo atresia. During atresia, ovarian follicles were at different stages of degeneration, characterized by the progressive loss of the basement membrane and disorganization of the follicle complex. In the advanced stage of follicular atresia, there was total loss of the basement membrane, culminating in degradation of the follicle complex. In unconfined animals, oocyte development and maturation were not affected. Confinement also affected the cell structure of the germinal epithelium, which showed large numbers of apoptotic bodies. The difference in cortisol and glucose levels between the unconfined and confined groups was significant, which may have to do with the change found in the ovaries, such as extensive follicular atresia and loss of the basement membrane.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Barton, BA (2000). Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquac 62, 12–8.2.0.CO;2>CrossRefGoogle Scholar
Barton, BA, Peter, RE and Paulencu, CR (1980). Plasma cortisol levels of fingerling rainbow trout (Salmo gairdneri) at rest, and subjected to handling, confinement, transport, and stocking. Can J Fish Aquat Sci 37, 805–11.CrossRefGoogle Scholar
Bayona Perez, IL (2019). Biologia reprodutiva do peixe borboleta Chaetodon striatus (Perciformes: Chaetodontidae) e manutenção em sistema de recirculação. Tese de Doutorado. Universidade Estadual Paulista – UNESP.Google Scholar
Bayona Perez, IL, Mazzoni, TS and Quagio-Grassiotto, I (2020). Cellular development of the germinal epithelium during the female and male gametogenesis of Chaetodon striatus (Perciformes: Chaetodontidae). Zygote 28, 291–9.CrossRefGoogle Scholar
Berumen, ML and Pratchett, MS (2006). Effects of resource availability on the competitive behaviour of butterflyfishes (Chaetodontidae). In Proceedings of Loth 10th International Coral Reef Symposium, pp. 644–50.Google Scholar
Campbell, PM, Pottinger, TG and Sumpter, JP (1992). Stress reduces the quality of gametes produced by rainbow trout. Biol Reprod 47, 1140–50.CrossRefGoogle ScholarPubMed
Courtney Jones, SK, Munn, AJ and Byrne, PG (2018). Effect of captivity on morphology: negligible changes in external morphology mask significant changes in internal morphology. R Soc Open Sci 5, 172470.CrossRefGoogle ScholarPubMed
Eschmeyer, WN, Fricke, F and Van Der Laan, R (2020). Catalog of fishes: genera, species, reference. https://www.calacademy.org/scientists/projects/eschmeyers-catalog-of-fishes (accessed 1 May 2020). [W Eschmeyer (ed.) – 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].Google Scholar
Falahatkar, B, Poursaeid, S, Shakoorian, M and Barton, B (2009). Responses to handling and confinement stressors in juvenile great sturgeon Huso J Fish Biol 75, 784–96.CrossRefGoogle ScholarPubMed
França, GF, Grier, HJ and Quagio-Grassiotto, I (2010). A new vision of the origin and the oocyte development in the Ostariophysi applied to Gymnotus sylvius (Teleostei: Gymnotiformes). Neotrop Ichthyol 8, 787804.CrossRefGoogle Scholar
Gowaty, PA, Anderson, WW, Bluhm, CK, Drickamer, LC, Kim, YK and Moore, AJ (2007). The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Nat Acad Sci USA 104, 15023–7.CrossRefGoogle ScholarPubMed
Grier, H (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, 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
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), vol. 8A, pp. 25–84. Science Publishers, Enfield, New Hampshire, USA.Google Scholar
Holt, GJ (2003). Research on culturing early life stages of marine ornamental fish. In: Marine Ornamental Species – Collection, Culture & Conservation (JC Cato and CL Brown eds.). pp. 251–254. Iowa, USA: Iowa State Press.Google Scholar
Lawrence, M. J., Jain-Schlaepfer, S., Zolderdo, A. J., Algera, D. A., Gilmour, K. M., Gallagher, A. J., & Cooke, SJ (2018). Are 3 min good enough for obtaining baseline physiological samples from teleost fish? Canadian J Zool 96, 774–86.CrossRefGoogle Scholar
Mazzoni, TS and Quagio-Grassiotto, I (2017). Ovary differentiation and activity in teleostei fish. In: Theriogenology (RP Carreira ed.). InTech, pp. 129–56.CrossRefGoogle 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: Cypriniformes). Anat Rec 293, 1581–606.CrossRefGoogle Scholar
Mazzoni, TS, Grier, HJ and Quagio-Grassiotto, I (2015). The basement membrane and the sex establishment in the juvenile hermaphroditism during gonadal differentiation of the Gymnocorymbus ternetzi (Teleostei: Characiformes: Characidae). Anat Rec 298, 19842010.CrossRefGoogle Scholar
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, E34.CrossRefGoogle Scholar
Mazzoni, TS, Junior, HR, Viadanna, RR and Silva, GC (2019). Clown fishes breeding in captivity using low cost resources and water recycling. World J Aquacul Res Dev 1, 1005.Google Scholar
Monteiro-Neto, C, Cunha, FEDA, Nottingham, MC, Araújo, ME, Rosa, IL and Barros, GML (2003). Analysis of the marine ornamental fish trade at Ceará State, northeast Brazil. Biodivers Conserv 12, 1287–95.CrossRefGoogle Scholar
Morgan, KN and Tromborg, CT (2007). Sources of stress in captivity. Appl Anim Behav Sc 102, 262302.CrossRefGoogle Scholar
Motta, PJ (2012). The Butterflyfishes: Success on the Coral Reef (vol. 9). Springer Science & Business Media. 250 pp.Google Scholar
Mylonas, CC, Fostier, A and Zanuy, S (2010). Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165, 516–34.CrossRefGoogle ScholarPubMed
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
Ostrand, KG, Cooke, SJ and Wahl, DH (2004). Effects of stress on largemouth bass reproduction. North Am J Fish Manage 24, 1038–45.CrossRefGoogle Scholar
Pandian, TJ (2010). Sexuality in fishes. FL: Science Publishers, 189 pp.CrossRefGoogle Scholar
Pankhurst, NW (2011). The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170, 265–75.CrossRefGoogle ScholarPubMed
Pottinger, TG, Carrick, TR, Appleby, AYWE and Yeomans, WE (2000). High blood cortisol levels and low cortisol receptor affinity: is the chub, Leuciscus cephalus, a cortisol-resistant teleost? Gen Comp Endocrinol 120, 108–17.CrossRefGoogle ScholarPubMed
Pratap, HB and Wendelaar Bonga, SE (1990). Effects of water-borne cadmium on plasma cortisol and glucose in the cichlid fish Oreochromis mossambicus . Comp Biochem Physiol C Comp Pharmacol 95, 313–7.CrossRefGoogle Scholar
Quagio-Grassiotto, I, Grier, HJ, Mazzoni, TS, Nóbrega, RH and Amorim, JP (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 Morphol 272, 1290–306.CrossRefGoogle Scholar
Quintero-Hunter, I, Grier, H 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. Biotec Histochem 66, 169–72.CrossRefGoogle ScholarPubMed
Ratnasabapathi, D, Burns, J and Souchek, R (1992). Effects of temperature and prior residence on territorial aggression in the convict cichlid Cichlasoma nigrofasciatum . Aggress Behav 18, 365–72.3.0.CO;2-E>CrossRefGoogle Scholar
Santana, JCO and Quagio-Grassiotto, I (2014). Extracellular matrix remodeling of the testes through the male reproductive cycle in Teleostei fish. Fish Physiol Biochem 40, 1863–75.CrossRefGoogle ScholarPubMed
Schreck, CB (2010). Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165, 549–56.CrossRefGoogle ScholarPubMed
Schreck, CB, Contreras-Sanchez, W and Fitzpatrick, MS (2001). Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197, 324.CrossRefGoogle Scholar
Schwindt, AR, Feist, GW and Schreck, CB (2007). Stress does not inhibit induced vitellogenesis in juvenile rainbow trout. Environ Biol Fish 80, 453–63.CrossRefGoogle Scholar
Shourbela, RM, Abd El-Latif, AM and Abd El-Gawad, EA (2016). Are Pre Spawning Stressors Affect Reproductive Performance of African Catfish Clarias gariepinus? Turk J Fish Aquat Sci 16, 651–7.CrossRefGoogle Scholar
Small, BC (2004). Effect of dietary cortisol administration on growth and reproductive success of channel catfish. J Fish Biol 64, 589–96.CrossRefGoogle Scholar
Vidal, BC (1988). Histochemical and anisotropical properties characteristics of silver impregnation: the differentiation of reticulin fibres from the other interstitial collagens. Zool Jb Anat 117, 485–94.Google Scholar
Wabnitz, C, Taylor, M, Green, E and Razak, T (2003). From ocean to aquarium. Cambridge, UK: UNEP-WCMC, 64 pp.Google Scholar
Wildner, DD, Grier, H and Quagio-Grassiotto, I (2013). Female germ cell renewal during the annual reproductive cycle in Ostariophysians fish. Theriogenology 79, 709–24.CrossRefGoogle ScholarPubMed
Wood, E (2001). Collection of coral reef fish aquaria: global trade, conservation issues and management strategies. Londres: Marine Conservation Society.Google Scholar