Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-26T12:15:25.460Z Has data issue: false hasContentIssue false
  • English
  • Français

Low salinity negatively affects early larval development of Nile tilapia, Oreochromis niloticus: insights from skeletal muscle and molecular biomarkers

Published online by Cambridge University Press:  13 August 2019

Luis Henrique Melo ,
Yuri Simões Martins ,
Rafael Magno Costa Melo ,
Paula Suzanna Prado ,
Ronald Kennedy Luz ,
Nilo Bazzoli  and
Elizete Rizzo Open the ORCID record for Elizete Rizzo [Opens in a new window]
Luis Henrique Melo
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Yuri Simões Martins
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Rafael Magno Costa Melo
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Paula Suzanna Prado
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Ronald Kennedy Luz
Affiliation:
Laboratório de Aquacultura, Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Nilo Bazzoli
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
Elizete Rizzo*
Affiliation:
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
*
Address for correspondence: Elizete Rizzo. Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901 Belo Horizonte, Minas Gerais, Brasil. E-mails: [email protected]; [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The present study evaluated the effects of low salinity on the early larval development of Oreochromis niloticus, specifically histological damage to white muscle, morphology of the yolk-sac surface and trunk area, and molecular expression of apoptosis and cell proliferation biomarkers. Newly hatched larvae were submitted to four salinity treatments for a period of 48 or 72 h, in duplicate: (S0) freshwater, (S2) 2 g l−1, (S4) 4 g l−1, and (S6) 6 g l−1NaCl. Larval development was examined using histology, electron microscopy, enzyme-linked immunosorbent assay (ELISA), and morphometry. At the yolk-sac surface, larvae of S4 and S6 displayed alterations to the apical opening of chloride cells that may be related to osmotic expenditure caused by the increased salinity. Caspase-3 expression did not differ significantly among treatments, however significantly lower proliferating cell nuclear antigen (PCNA) expression (P < 0.05) suggested minor cell proliferation in larvae of S4 and S6 compared with S0 and S2. Furthermore, there was a significant reduction in both trunk area and percentage of normal white muscle fibres (WF) in larvae of S4 and S6. Vacuolated areas and myofibrils concentrated at the cell periphery and found in the white muscle from larvae exposed to saline environments suggested disturbance to muscle development. Oedema and mononuclear infiltrate were also observed in the white muscle of S4 and S6 larvae. Together these results indicated that treatments with 4 and 6 g l−1 NaCl may cause osmoregulation expenditure, morphological alterations to the yolk-sac surface and histological damage to skeletal muscle that negatively affected the early larval development of O. niloticus.

Keywords

Caspase-3LarvaePCNASkeletal muscleYolk sac
Type
Research Article
Information
Zygote , Volume 27 , Issue 6 , December 2019 , pp. 375 - 381
Copyright
© Cambridge University Press 2019 

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

Alderdice, DF (1988) Osmotic and ionic regulation in teleost eggs and larvae. In Fish Physiology (eds Hoar, WS and Randall, DJ), pp. 163–251, Academic Press.Google Scholar
Altinok, I and Grizzle, JM (2001) Effects of low salinities on Flavobacterium columnare infection of euryhaline and freshwater stenohaline fish. J Fish Dis 24, 361–7.CrossRefGoogle Scholar
Betancor, MB, Caballero, MJ, Benítez-Santana, T, Saleh, R, Atalah, E and Izquierdo, M (2013) Oxidative status and histological changes in sea bass larvae muscle in response to high dietary content of docosahexanoic acid DHA. J Fish Dis 36, 453–65.CrossRefGoogle Scholar
Beux, LF and Zaniboni-Filho, E (2007) Survival and the growth of pintado (Pseudoplatystoma corruscans) post-larvae on different salinities. Braz Arch Biol Tech 5, 821–9.CrossRefGoogle Scholar
Bhujel, RC (2000) A review of strategies for the management of Nile tilapia (Oreochromis niloticus) broodfish in seed production systems, especially hapa-based systems. Aquaculture 181, 37–59.CrossRefGoogle Scholar
Borode, AO, Balogun, AM and Omoyeni, BA (2002) Effect of salinity on embryonic development, hatchability, and growth of African catfish, Clarias gariepinus, eggs and larvae. J Appl Aquacult 12, 89–93.CrossRefGoogle Scholar
Brodeur, JC, Peck, LS and Johnston, IA (2002) Feeding increases MyoD and PCNA expression in myogenic progenitor cells of Notothenia coriiceps . J Fish Biol 60, 1475–85.Google Scholar
Food and Agriculture Organization of the United Nations (FAO) (2016) Cultured aquatic species information programme: Oreochromis niloticus (Linnaeus, 1758). Available at: http://www.fao.org/fishery/culturedspecies/Oreochromis_niloticus/en. Accessed on 9 December 2016.Google Scholar
Fridman, S, Bron, JE and Rana, KJ (2011) Ontogenetic changes in location and morphology of chloride cells during early life stages of the Nile tilapia Oreochromis niloticus adapted to fresh and brackish water. J Fish Biol 79, 597–614.10.1111/j.1095-8649.2011.03043.xCrossRefGoogle ScholarPubMed
Fridman, S, Bron, JE and Rana, KJ (2012a) Influence of salinity on embryogenesis, survival, growth and oxygen consumption in embryos and yolk-sac larvae of the Nile tilapia. Aquaculture 334–337, 182–90.10.1016/j.aquaculture.2011.12.034CrossRefGoogle Scholar
Fridman, S, Bron, JE and Rana, KJ (2012b) Ontogenetic changes in the osmoregulatory capacity of the Nile tilapia Oreochromis niloticus and implications for aquaculture. Aquaculture 356–357, 243–9.CrossRefGoogle Scholar
Fridman, S, Rana, KJ and Bron, JE (2013) Confocal scanning laser microscopy 3D image analysis allows quantitative studies of functional state of ion regulatory cells in the Nile tilapia (Oreochromis niloticus) following salinity challenge. Microsc Res Tech 76, 412–8.10.1002/jemt.22181CrossRefGoogle Scholar
Fuchs, Y and Steller, H (2011) Programmed cell death in animal development and disease. Cell 147, 742–58.CrossRefGoogle ScholarPubMed
Garcia, LO, Becker, AG, Copatti, CE and Baldisserotto, B (2007) Salt in the food and water as a supportive therapy for Ichthyophthirius multifilii infestation on silver catfish, Rhamdia quelen, fingerlings. J World Aquacult Soc 38, 1–11.CrossRefGoogle Scholar
Hiroi, J, Kaneko, T, Uchida, K, Hasegawa, S and Tanaka, M (1998) Immunolocalization of vacuolar-type H+-ATPase in the yolk-sac membrane of Tilapia (Oreochromis mossambicus) larvae. Zool Sci 16, 447–53.Google Scholar
Hirose, S, Kaneko, T, Naito, N and Takei, Y (2003) Molecular biology of major components of chloride cells. Comp Bioch Physiol B 136, 593–620.CrossRefGoogle ScholarPubMed
Jenkins, VK, Timmons, AK and McCall, K (2013) Diversity of cell death pathways: insight from the fly ovary. Trends Cell Biol. 332, 159–70.Google Scholar
Johnston, IA (1999) Muscle development and growth: potential implications for flesh quality in fishes. Aquaculture 177, 99–115.10.1016/S0044-8486(99)00072-1CrossRefGoogle Scholar
Johnston, IA (2006) Environmental and plasticity of myogenesis in teleost fish. J Exp Biol 209, 2249–64 CrossRefGoogle ScholarPubMed
Jomori, RK, Luz, RK and Portella, MC (2012) Effect of salinity on larval rearing of pacu, Piaractus mesopotamicus, a freshwater species. J World Aquacult Soc 43, 423–32.CrossRefGoogle Scholar
Jun, Q, Pao, X, Haizhen, W, Ruiwei, L and Hui, W (2012) Combined effect of temperature, salinity and density on the growth and feed utilization of Nile tilapia juveniles (Oreochromis niloticus). Aquacult Res 43, 1344–56.CrossRefGoogle Scholar
Kelman, Z (1997) PCNA: structure, functions and interactions. Oncogene 14, 629–40.CrossRefGoogle ScholarPubMed
Likongue, JS, Stecko, TD, Stauffer, JR Jr and Carline, RF (1996) Combined effects of water temperature and salinity on growth and feed utilization of juvenile Nile tilapia Oreochromis niloticus (Linnaeus). Aquaculture 146, 37–46.CrossRefGoogle Scholar
Little, DC and Hulata, G (2000) Strategies for tilapia seed production. In Tilapia: Biology and Exploitation (eds Beveridge, MCM and McAndrew, BJ), pp 226–326, Kluwer Academic Publisher.Google Scholar
Loppion, G, Crespel, A, Martinez, AS, Auvray, P and Sourdaine, P (2008) Study of the potential spermatogonial stem cell compartment in dogfish testis, Scyliorhinus canicula L. Cell Tissue Res 332, 533–42.CrossRefGoogle ScholarPubMed
Martins, YS, Melo, RMC, Campo-Junior, PHA, Santos, JCE, Luz, RK, Rizzo, E and Bazzoli, N (2014) Salinity and temperature variations reflecting on cellular PCNA, IGF-I and II expressions, body growth and muscle cellularity of a freshwater fish larvae. Gen Comp Endocr 202, 50–8.CrossRefGoogle ScholarPubMed
Meier, P, Finch, A and Evan, G (2000) Apoptosis in development. Nature 47, 796–801.CrossRefGoogle Scholar
Melo, RMC, Martins, YS, Luz, RK, Rizzo, E and Bazzoli, N (2015) PCNA and apoptosis during post-spawning ovarian remodeling in the teleost Oreochromis niloticus . Tissue Cell 47, 541–9.CrossRefGoogle ScholarPubMed
Rowlerson, A, Radaelli, G, Mascarello, F and Veggetti, A (1997) Regeneration of skeletal muscle in two teleost fish: Sparus aurata and Brachydanio rerio . Cell Tissue Res 289, 311–22.CrossRefGoogle ScholarPubMed
Schultz, E and McCormick, KM (1994) Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123, 213–57 10.1007/BFb0030904CrossRefGoogle ScholarPubMed
Shiraishi, K, Kaneko, T, Hasegawa, S and Hirano, T (1997) Development of multicellular complexes of chloride cells in the yolk-sac membrane of tilapia (Oreochromis mossambicus) embryos and larvae in seawater. Cell Tissue Res 288, 583–90.10.1007/s004410050844CrossRefGoogle Scholar
Souza-Bastos, LR and Freire, CA (2009) The handling of salt by the neotropical cultured freshwater catfish Rhamdia quelen . Aquaculture 289, 167–74.10.1016/j.aquaculture.2009.01.007CrossRefGoogle Scholar
Suresh, AV and Lin, CK (1992) Tilapia culture in saline water: a review. Aquaculture 106, 201–26.CrossRefGoogle Scholar
Takle, H and Andersen, Ø (2007) Caspases and apoptosis in fish. J Fish Biol 71, 326–49.CrossRefGoogle Scholar
Thomé, RG, Domingos, FFT, Santos, HB, Martinelli, PM, Sato, Y, Rizzo, E and Bazzoli, N (2012) Apoptosis, cell proliferation and vitellogenesis during the folliculogenesis and follicular growth in teleost fish. Tissue Cell 44, 54–62.CrossRefGoogle ScholarPubMed
Villegas, CT (1990) Evaluation of the salinity tolerance of Oreochromis mossambicus, O. niloticus and their F1 hybrids. Aquaculture 85, 281–92.CrossRefGoogle Scholar
Wang, Ji-Q, Lui, H, Po, H and Fan, L (1996) Influence of salinity on food consumption, growth and energy conversion efficiency of common carp (Cyprinus carpio) fingerlings. Aquaculture 148, 115–24.CrossRefGoogle Scholar
Watanabe, WO, Kuo, CM and Huang, MC (1985) The ontogeny of salinity tolerance in the tilapias Oreochromis aureus, O. niloticus and O. mossambicus × O. niloticus hybrid, spawned and reared in freshwater. Aquaculture 47, 353–67.CrossRefGoogle Scholar
Zadunaisky, JA (1996) Chloride cells and osmoregulation. Kidney Int 49, 1563–7.CrossRefGoogle ScholarPubMed