Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2023-0158
Animal Reproduction (AR)
ORIGINAL ARTICLE

Effect of temperature on gonadal differentiation and growth of Leporinus friderici

Thiago Gonçalves de Souza; Mariana Roza de Abreu; Rafael Yutaka Kuradomi; Sergio Ricardo Batlouni

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Abstract

This study aimed to investigate the effect of temperature on gonadal differentiation, growth, survival, and sex ratio of Leporinus friderici reared at 25 °C or 29 °C from 50 to 240 days after eclosion (DAE) in a water recirculation system. A total of 110 fish at 50 DAE (6.7 ± 0.1 cm and 6.1 ± 0.3 g) were equally and randomly distributed in 10 boxes (90 L) (11 fish/box, 5 boxes/temperature). One fish from each experimental unit was randomly sampled at 50, 70, 90, 110, 130, 150, 170, 190, 210 and 240 DAE. Female gonadal differentiation started at 150 DAE (11.4 ± 0.0 cm and 16.4 ± 0.0 g) at 25 °C and at 170 DAE (10.7 ± 0.7 cm and 27.7 ± 8.5 g) at 29 ºC, while testes differentiation only occurred at 29 °C from 190 DAE (12.1 ± 0.0 cm and 38.0 ± 0.0 g). Of 50 fishes sampled in each condition, 17 (12 females and five males) and three (three females) displayed gonadal differentiation at 29 °C and 25 °C, respectively. Final biometric values at 29 °C were twice those obtained at 25 °C, reaching 13.9 ± 0.65 cm and 57.3 ± 10.12 g versus 11.2 ± 0.39 cm and 28.5 ± 2.95 g, respectively. While temperature clearly influenced gonadal differentiation and growth, it had inconclusive effects on sex ratio. The higher temperature (29 °C) has direct implications for the production of this species, as it accelerates growth without causing mortality.

Keywords

sex determination, gonads, females, fish, wild

References

Adolfi MC, Carreira ACO, Jesus LWO, Bogerd J, Funes RM, Schartl M, Sogayar MC, Borella MI. Molecular cloning and expression analysis of dmrt1 and sox9 during gonad development and male reproductive cycle in the lambari fish, Astyanax altiparanae. Reprod Biol Endocrinol. 2015;13(1):2. http://doi.org/10.1186/1477-7827-13-2. PMid:25577427.

Agostinho AA, Gomes LC, Pelicice FM. Ecologia e manejo de recursos pesqueiros em reservatório do Brasil. Maringá: EDUEM; 2007. 501 p.

Albrecht MP, Caramaschi EP. Feeding Ecology of Leporinus friderici (Teleostei; Anostomidae) in the Upper Tocantins River, Central Brazil, before and after Installation of a Hydroelectric Plant. Stud Neotrop Fauna Environ. 2003;3(1):33-40. http://doi.org/10.1076/snfe.38.1.33.14033.

Alix M, Chardard D, Ledoré Y, Fontaine P, Schaerlinger B. An alternative developmental table to describe non-model fish species embryogenesis: application to the description of the Eurasian perch (Perca fluviatilis L. 1758) development. Evodevo. 2015;6(1):39. http://doi.org/10.1186/s13227-015-0033-3. PMid:26688712.

Amaral AC, Lima AF, Ganeco-Kirschnik LN, Almeida FL. Morphological characterization of Pirarucu Arapaima gigas (Schinz, 1822) gonadal differentiation. J Morphol. 2020;281(4-5):491-9. http://doi.org/10.1002/jmor.21116. PMid:32198946.

Amaral-Junior H, Nunes MFS, Garcia S. Análise de diferentes dosagens de hormônio na ração, para definição de um protocolo de feminilização do jundiá Rhamdia quelen. Redvet. 2008;12:1-7.

Barbosa RP, Kuradomi RY, Sato RT, Batlouni SR. Piaractus mesopotamicus gonad differentiation. Aquacult Res. 2022;53(11):4106-15. http://doi.org/10.1111/are.15912.

Baroiller JF, D’Cotta H. Environment and sex determination in farmed fish. Comp Biochem Physiol C Toxicol Pharmacol. 2001;130(4):399-409. http://doi.org/10.1016/S1532-0456(01)00267-8. PMid:11738628.

Bem JC, Fontanetti CS, Senhorini JA, Parise-Maltempi PP. Effectiveness of estradiol valerate on sex reversion in Astyanax altiparanae (Characiformes, Characidae). Braz Arch Biol Technol. 2012;55(2):283-90. http://doi.org/10.1590/S1516-89132012000200015.

Brito MFG, Santos GB, Bazzoli N. Reprodução de Leporinus friderici (Pisces: Anostomidae) no reservatório de Itumbiara, GO. BIOS. 1999;7:33-40.

Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002;208(3-4):191-364. http://doi.org/10.1016/S0044-8486(02)00057-1.

Durães R, Pompeu PS, Godinho AL. Alimentação de quatro espécies de Leporinus (Characiformes, Anostomidae) durante a formação de um reservatório no sudeste do Brasil. Iheringia Ser Zool. 2001;(90):183-91. http://doi.org/10.1590/S0073-47212001000100019.

Fernandino JI, Hattori RS. Sex determination in Neotropical fish: implications ranging from aquaculture technology to ecological assessment. Gen Comp Endocrinol. 2019;273:172-83. http://doi.org/10.1016/j.ygcen.2018.07.002. PMid:29990492.

Furtado MDSC, Queiroz JCB, Bentes B, Yasojima EKK, Thomaz DDO, Pinheiro LDC, Ruffino ML, Isaac V. The hydrological cycle of the lower Amazon in Brazil determines the variation in local fishing patterns. Fishes. 2023;8(7):371. http://doi.org/10.3390/fishes8070371.

Gao Z, Wang HP, Rapp D, O’Bryant P, Wallat G, Wang W, Yao H, Tiu L, MacDonald R. Gonadal sex differentiation in the bluegill sunfish Lepomis macrochirus and its relation to fish size and age. Aquaculture. 2009;294(1-2):138-46. http://doi.org/10.1016/j.aquaculture.2009.05.024.

García-Dávila C, Sánchez Riveiro H, Flores Silva MA, Mejía de Loayza JE, Angulo Chávez CAC, Castro Ruiz D. Peces de consumo de la Amazonía Peruana [Internet]. Iquitos: Instituto de Investigaciones de la Amazonía Peruana (IIAP); 2018 [cited 2023 Dec 4]. Available from: https://borea.mnhn.fr/sites/default/files/pdfs/PECES%20DE%20CONSUMO%20DE%20LA%20AMAZONIA%20PERUANA%20%28WEB%29.pdf

Graeff A, Segalin CA, Pruner EN, Amaral H Jr. Produção de alevinos de Jundiá (Rhamdia quelen) [Internet]. Epagri; 2008. Boletim Técnico Epagri [cited 2023 Dec 4]. Available from: https://docweb.epagri.sc.gov.br/website_epagri/Cedap/Publicacao-Seriada/3-Publicacao-seriada-piscicultura-jundia-alevinagem-reproducao.pdf

Hawkes LA, Broderick AC, Godfrey MH, Godley BJ. Investigating the potential impacts of climate change on a marine turtle population. Glob Change Biol. 2007;13(5):923-32. http://doi.org/10.1111/j.1365-2486.2007.01320.x.

Honeycutt JL, Deck CA, Miller SC, Severance ME, Atkins EB, Luckenbach JA, Buckel JA, Daniels HV, Rice JA, Borski RJ, Godwin J. Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination. Sci Rep. 2019;9(1):6527. http://doi.org/10.1038/s41598-019-42944-x. PMid:31024053.

Imsland AK, Hanssen H, Foss A, Vikingstad E, Roth B, Bjørnevik M, Powell M, Solberg C, Norberg B. Short-term exposure to continuous light delays sexual maturation and increases growth of Atlantic cod in sea pens. Aquacult Res. 2012;44:n/a. http://doi.org/10.1111/j.1365-2109.2012.03171.x.

Instituto Brasileiro de Geografia e Estatística – IBGE. Produção da pecuária municipal [Internet]. Rio de Janeiro; 2021 [cited 2023 Dec 4]. Available from: https://biblioteca.ibge.gov.br/index.php/biblioteca-catalogo?id=784&view=detalhes

Kissil GW, Lupatsch I, Elizur A, Zohar Y. Long photoperiod delayed spawning and increased somatic growth in gilthead seabream (Sparus aurata). Aquaculture. 2001;200(3-4):363-79. http://doi.org/10.1016/S0044-8486(01)00527-0.

Leal MC, Cardoso ER, Nóbrega RH, Batlouni SR, Bogerd J, França LR, Schulz RW. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod. 2009;81(1):177-87. http://doi.org/10.1095/biolreprod.109.076299. PMid:19339708.

Lema SC, Luckenbach JA, Yamamoto Y, Housh MJ. Fish reproduction in a warming world: vulnerable points in hormone regulation from sex determination to spawning. Philos Trans R Soc Lond B Biol Sci. 2024;379(1898):20220516. http://doi.org/10.1098/rstb.2022.0516. PMid:38310938.

Lopes CA, Benedito-Cecilio E, Agostinho AA. The reproductive strategy of Leporinus friderici (Characiformes, Anostomidae) in the Paraná River basin: the effect of reservoirs. Rev Bras Biol. 2000;60(2):255-66. http://doi.org/10.1590/S0034-71082000000200009. PMid:10959109.

Marreta ME, Faldoni FLC, Parise-Maltempi PP. Cytogenetic mapping of the W chromosome in the genus Leporinus (Teleostei, Anostomidae) using a highly repetitive DNA sequence. J Fish Biol. 2012;80(3):630-7. http://doi.org/10.1111/j.1095-8649.2011.03199.x. PMid:22380557.

Martínez P, Viñas AM, Sánchez L, Díaz N, Ribas L, Piferrer F. Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture. Front Genet. 2014;5:340. http://doi.org/10.3389/fgene.2014.00340. PMid:25324858.

Nascimento MHS, Aragão DG, Silva JLN, Lima RC, Birindelli JLO, Fraga EC, Barros MC. The DNA barcode reveals cryptic diversity and a new record for the genus Leporinus (Characiformes, Anostomidae) in the hydrographic basins of central northern Brazil. PeerJ. 2023;11:e15184. http://doi.org/10.7717/peerj.15184. PMid:37250713.

Pereira TSB, Boscolo CNP, Batlouni SR. Use of 17β-estradiol for Leporinus macrocephalus feminization. Bol Inst Pesca. 2020;46:1-7. http://doi.org/10.20950/1678-2305.2020.46.2.547.

Poltronieri J, Marquioni V, Bertollo LAC, Kejnovsky E, Molina WF, Liehr T, Cioffi MB. Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res. 2014;142(1):40-5. http://doi.org/10.1159/000355908. PMid:24217024.

Quirino PP, Delgado MLR, Gomes-Silva L, Benevente CF, Grigoli-Olivio ML, Bianchini BC, Ninhaus-Silveira A, Veríssimo-Silveira R. Female sex inversion as a reason for an unbalanced sex ratio in the neotropical species Brycon orbignyanus. Aquacult Res. 2022;53(5):1706-26. http://doi.org/10.1111/are.15701.

Reading BJ, Andersen LK, Ryu YW, Mushirobira Y, Todo T, Hiramatsu N. Oogenesis and egg quality in Finfish: yolk formation and other factors influencing female fertility. Fishes. 2018;3(4):1-28. http://doi.org/10.3390/fishes3040045.

Rêgo ACL, Pinese OP, Magalhães PA, Pinese JF. Relação peso-comprimento para Prochilodus lineatus (Valenciennes, 1836) e Leporinus friderici (Bloch, 1794) (Characiformes) no reservatório de Nova Ponte - EPDA de Galheiro, rio Araguari, MG. Rev. Bras. Zoociências. 2008;10:13-21.

Rolim GS, Aparecido LE. Camargo, Köppen and Thornthwaite climate classification systems in defining climatical regions of the state of São Paulo, Brazil. Int J Climatol. 2015;36(2):636-43. http://doi.org/10.1002/joc.4372.

Rougeot C, Krim A, Mandiki SNM, Kestemont P, Mélard C. Sex steroid dynamics during embryogenesis and sexual differentiation in Eurasian perch, Perca fluviatilis. Theriogenology. 2007;67(5):1046-52. http://doi.org/10.1016/j.theriogenology.2006.12.006. PMid:17270265.

Santidrián Tomillo P, Spotila JR. Temperature-dependent sex determination in sea turtles in the context of climate change: uncovering the adaptive significance. BioEssays. 2020;42(11):1-6. http://doi.org/10.1002/bies.202000146. PMid:32896903.

Senthilkumaran B, Yoshikuni M, Nagahama Y. A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol. 2004;215(1-2):11-8. http://doi.org/10.1016/j.mce.2003.11.012. PMid:15026170.

Servili A, Canario AVM, Mouchel O, Muñoz-Cueto JA. Climate change impacts on fish reproduction are mediated at multiple levels of the brain-pituitary-gonad axis. Gen Comp Endocrinol. 2020;291:113439. http://doi.org/10.1016/j.ygcen.2020.113439. PMid:32061640.

Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD, Mendelson CR, Bulun SE. Aromatase cytochrome p450, the enzyme responsible for estrogen biosynthesis. Endocr Rev. 1994;15(3):342-55. http://doi.org/10.1210/edrv-15-3-342. PMid:8076586.

Singh AK. Introduction of modern endocrine techniques for the production of monosex population of fishes. Gen Comp Endocrinol. 2013;181:146-55. http://doi.org/10.1016/j.ygcen.2012.08.027. PMid:23063432.

Souza TG, Kuradomi RY, Rodrigues SM, Batlouni SR. Wild Leporinus friderici induced spawning with different dose of mGnRHa and metoclopramide or carp pituitary extract. Anim Reprod. 2020;17(1):e20190078. http://doi.org/10.21451/1984-3143-AR2019-0078. PMid:32399066.

Strüssmann CA, Nakamura M. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol Biochem. 2002;26(1):13-29. http://doi.org/10.1023/A:1023343023556.

Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA, Dufour S, Karlsen Ø, Norberg B, Andersson E, Hansen T. Control of puberty in farmed fish. Gen Comp Endocrinol. 2010;165(3):483-515. http://doi.org/10.1016/j.ygcen.2009.05.004. PMid:19442666.

Valenti WC, Barros HP, Moraes-Valenti P, Bueno GW, Cavalli RO. Aquaculture in Brazil: past, present and future. Aquacult Rep. 2021;19:100611. http://doi.org/10.1016/j.aqrep.2021.100611.

Vidal MV, Batlouni SR. The environmental licensing of hydroelectrics and the interface with migratory fish and aquaculture in Brazil. Bol Inst Pesca. 2023;2023(48):1-12. http://doi.org/10.20950/1678-2305/bip.2022.48.e696.

Ye D, Zhu L, Zhang Q, Xiong F, Wang H, Wang X, He M, Zhu Z, Sun Y. Abundance of early embryonic primordial germ cells promotes zebrafish female differentiation as revealed by lifetime labeling of germline. Mar Biotechnol. 2019;21(2):217-28. http://doi.org/10.1007/s10126-019-09874-1. PMid:30671659.

Zardo ÉL, Fornari DC, Giora J, Rotili DA, Gomes IC, Esquivel-Muelbert JR, Streit DP. Gonadal development period and sexual differentiation through histological analysis in Brycon orbignyanus (Valenciennes, 1850) (Characiformes: Bryconidae). Aquaculture. 2021;539:736636. http://doi.org/10.1016/j.aquaculture.2021.736636.
 


Submitted date:
12/07/2023

Accepted date:
04/29/2024

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