Abstract
Survival analysis has proven to be a robust tool for studies in humans, and recently, it has been adopted in studies with animals, but very little in fish. The production of uniform fingerlings has been one challenge of aquaculture, influenced by the use of the efficient breeders. We aimed to present, for the first time in aquaculture, a survival analysis as a tool for decision-making by using the relationship between the main morphometric traits and the spawning time of Nile tilapia females up to 28 days after mating in an intensive system. We used 78 females and 26 males from which ten traits were evaluated. A check was made for the presence of eggs in the female mouth (spawning) every seven days until the final twenty-eight days. Confirmation of eggs was defined as uncensored data (C = 1) and absence of eggs as censored (C = 0). The Cox proportional hazards ratio and Kaplan–Meier models were adjusted to analyze the data. Females with a standard length of 19.19 cm (small group) and males with a weight of 259.14 g (small group) reproduced early, being more adapted to 1000 L tanks in a recirculation system. Less heavy egg masses were also related to early spawning. Therefore, the traits, standard length of the female, egg mass weight, and male weight, affected the presence of eggs up to 28 days and should be used as selection criteria for early breeders. Besides, the survival analysis was accurate as a tool for tilapia breeding management in an intensive system.
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References
Agumassie T (2018) Overview of length-weight relationship, condition factor and size at first maturity of Nile tilapia Oreochromis niloticus (L.) in different water bodies of Ethiopia: a review. Greener J 8:021–028. https://doi.org/10.15580/GJBS.2018.3.060618077
Al-Feky SSA, El-Sayed AF, Ezzat AA (2016) Dietary taurine improves reproductive performance of Nile tilapia (Oreochromis niloticus) broodstock. Aquacult Nutr 22:392–399. https://doi.org/10.1111/anu.12256
Alvarenga ERD, França LRD (2009) Effects of different temperatures on testis structure and function, with emphasis on somatic cells, in sexually mature Nile tilapias (Oreochromis niloticus). Biol Reprod 80:537–544. https://doi.org/10.1095/biolreprod.108.072827
Bentsen HB, Gjerde B, Eknath AE, De Vera MSP, Velasco RR, Danting JC, Dionisio EE, Longalong FM, Reyes RA, Abella TA, Tayamen MM, Ponzoni RW (2017) Genetic improvement of farmed tilapias: response to five generations of selection for increased body weight at harvest in Oreochromis niloticus and the further impact of the project. Aquaculture 468:206–217. https://doi.org/10.1016/j.aquaculture.2016.10.018
Beveridge MCM (1996) Cage aquaculture, 2nd edn. Fishing News, Oxford
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. https://doi.org/10.1016/S0044-8486(99)00217-3
Boettcher PJ, Jairath LK, Koots KR, Dekkers JCM (1997) Effects of interactions between type and milk production on survival traits of Canadian Holsteins. J Dairy Sci 80:2984–2995. https://doi.org/10.3168/jds.S0022-0302(97)76265-9
Brummett RE (1995) Environmental regulation of sexual maturation and reproduction in tilapia. Rev Fish Sci 3:231–248. https://doi.org/10.1080/10641269509388573
Caetano SL, Rosa GJM, Savegnago RP, Ramos SB, Bezerra LAF, Lôbo RB, De Paz CCP, Munari DP (2013) Characterization of the variable cow’s age at last calving as a measurement of longevity by using the Kaplan-Meier estimator and the Cox model. Animal 7:540–546
Campos-Mendoza A, McAndrew BJ, Coward K, Bromage N (2004) Reproductive response of Nile tilapia (Oreochromis niloticus) to photoperiodic manipulation; effects on spawning periodicity, fecundity and egg size. Aquaculture 231:299–314. https://doi.org/10.1016/j.aquaculture.2003.10.023
Castañeda-Busto VJ, Montaldo HH, Torres-Hernandez G, Pérez-Elizalde S, Valencia-Posadas M, Hernández-Mendo O, Shepard L (2014) Estimation of genetic parameters for productive life, reproduction, and milk-production traits in US dairy goats. J Dairy Sci 97:2462–2473. https://doi.org/10.3168/jds.2013-7503
Castañeda-Bustos VJ, Montaldo HH, Valencia-Posadas M, Shepard L, Pérez-Elizalde S, Hernández-Mendo O, Torres-Hernández G (2017) Linear and nonlineargenetic relationships between type traits and productive life in US dairy goats. J Dairy Sci 100:1232–1245. https://doi.org/10.3168/jds.2016-11313
Collett D (2003) Modelling survival data in medical research, 2nd edn. Chapman and Hall/CRC, London
Colosimo EA, Giolo SR (2006) Análise de sobrevivência aplicada. Edgard Blucher, São Paulo
Costa DC, De Souza e Silva W, MelilloFilho R, Miranda Filho KC, dos Santos JCE, Luz RK (2015) Capture, adaptation and artificial control of reproduction of Lophiosilurus alexandri: a carnivorous freshwater species. Anim. Reprod. Sci. 159:148–154. https://doi.org/10.1016/j.anireprosci.2015.06.009
Cox DR (1972) Regression models and life tables (with discussion). J R Stat Soc: Series B (Methodological) 34:187–202. https://doi.org/10.1111/j.2517-6161.1972.tb00899.x
Cox DR, Oakes D (1984) Analysis of survival data. Chapman & Hall/CRC, London. https://doi.org/10.1201/9781315137438
Cox DR, Snell EJ (1968) A general definition of residuals. J R Stat Soc: Series B (Methodological) 30:248–275. https://doi.org/10.1111/j.2517-6161.1968.tb00724.x
De Moura PS, Moreira RL, Teixeira EG, Moreira AG, Lima FRDS, Farias WR (2011) Desenvolvimento larval e influência do peso das fêmeas na fecundidade da tilápia do Nilo. Bras Cienc Agrar 6:531–537. https://doi.org/10.5039/agraria.v6i3a1396
Duponchelle F, Cecchi P, Corbin D, Nuñez J, Legendre M (2000) Variations in fecundity and egg size of female Nile tilapia, Oreochromis niloticus, from man-made lakes of Côte d’Ivoire. Environ Biol Fishes 57:155–170. https://doi.org/10.1023/A:1007575624937
Eknath AE, Bentsen HB, Ponzoni RW, Rye M, Nguyen NH, Thodesen J, Gjerde B (2007) Genetic improvement of farmed tilapias: composition and genetic parameters of a synthetic base population of Oreochromis niloticus for selective breeding. Aquaculture 273:1–14. https://doi.org/10.1016/j.aquaculture.2007.09.015
El-Sayed AF, Kawanna M (2008) Optimum water temperature boosts the growth performance of Nile tilapia (Oreochromis niloticus) fry reared in a recycling system. Aquac Res 39:670–672. https://doi.org/10.1111/j.1365-2109.2008.01915.x
El-Sayed AFM, Mansour CR, Ezzat AA (2003) Effects of dietary protein level on spawning performance of Nile tilapia (Oreochromis niloticus) broodstock reared at different water salinities. Aquaculture 220:619–632. https://doi.org/10.1016/s0044-8486(02)00221-1
FAO (2020) The state of world fisheries and aquaculture 2020. Sustainability in action, Rome. https://doi.org/10.4060/ca9229en
Farquharson KA, Hogg CJ, Grueber CE (2018) A meta-analysis of birth-origin effects on reproduction in diverse captive environments. Nat Commun 9:1–10. https://doi.org/10.1038/s41467-018-03500-9
Ferreira TA, Martins PGMA, Gouveia GC, Abreu LRA, Gouveia AMG, Facó O, Colosimo EA, Furusho-Garcia IF, Pereira IG (2020) Proportional hazard models associated with the survival of dairy goats reared in a tropical environment. Small Rumin Res 184:106063. https://doi.org/10.1016/j.smallrumres.2020.106063
Galemoni de Graaf GJ, Huisman EA (1999) Reproductive biology of pond reared Nile tilapia, Oreochromis niloticus L. Aquac Res 30:25–33. https://doi.org/10.1046/j.1365-2109.1999.00295.x
Gwahaba JJ (1973) Effects of fishing on Tilapia nilotica (L.) population in L. George, Uganda, over the past 20 years. Afr J Ecol 11:317–328. https://doi.org/10.1111/j.1365-2028.1973.tb00096.x
He J, Zhao Y, Zhao J, Gao J, Han D, Xu P, Yang R (2017) Multivariate random regression analysis for body weight and main morphological traits in genetically improved farmed tilapia (Oreochromis niloticus). Genet Sel Evol 49:80. https://doi.org/10.1186/s12711-017-0357-7
Hiroi J, Kaneko T, Tanaka M (1999) In vivo sequential changes in chloride cell morphology in the yolk-sac membrane of Mozambique tilapia (Oreochromis mossambicus) embryos and larvae during seawater adaptation. J Exp Biol 202:3485–3495. https://doi.org/10.1242/jeb.202.24.3485
Hurst TS, Neves RC, Boerman JP (2022) Early life indicators of first lactation milk yield and the effect of treatment for bovine respiratory disease on survivability and risk of pregnancy in Holstein dairy cattle. Vet J 282:105826. https://doi.org/10.1016/j.tvjl.2022.105826
ICLARM (1998) International Center for Living Aquatic Resources Management. Manual on: Genetic Improvement of Farmed Tilapia (GIFT) Research Methodologies. vol. 1. Revised version. Filipinas
Kaplan E, Meier P (1958) Nonparametric estimation from incomplete observation. J Am Stat Assoc 53:457–481. https://doi.org/10.1080/01621459.1958.10501452
Keeler AM, Zieger M, Todeasa SH, McCall AL, Gifford JC, Birsak S, Choudhury SR, Byrne BJ, Sena-Esteves M, ElMallah MK (2019) Systemic delivery of AAVB1-GAA clears glycogen and prolongs survival in a mouse model of Pompe disease. Hum Gene Ther 30:57–68. https://doi.org/10.1089/hum.2018.016
Keshari RS, Silasi R, Popescu NI, Georgescu C, Chaaban H, Lupu C, McCarty OJT, Esmon CT, Lupu F (2020) Fondaparinux pentasaccharide reduces sepsis coagulopathy and promotes survival in the baboon model of Escherichia coli sepsis. J Thromb Haemost 18:180–190. https://doi.org/10.1111/jth.14642
King RP (1997) Length-fecundity relationships of Nigerian fish populations. NAGA, ICLARM Quarterly 20:29–33
Kolding J, Haug L, Stefansson S (2008) Effect of ambient oxygen on growth and reproduction in Nile tilapia (Oreochromis niloticus). Can J Fish Aquat Sci 65:1413–1424. https://doi.org/10.1139/f08-059
Kubitza F (2011) Tilápia: tecnologia e planejamento na produção comercial, 2ª. Kubitza, Jundiaí
Lowe-Mcconnell RH (1958) Observations on the biology of Tilapia nilotica (L.) in East African waters. Revue De Zoologie Et De Botanique Africaines 57:129–170
Maluwa AO, Gjerde B (2006) Genetic evaluation of four strains of Oreochromis shiranus for harvest body weight in a diallel cross. Aquaculture 259:28–37. https://doi.org/10.1016/j.aquaculture.2006.06.003
Mashaii N, Rajabipour F, Mohammadi M, Sarsangi H, Bitaraf A, Hossein-Zadeh H, Sharif-Rohani M (2016) Reproduction of Nile tilapia, Oreochromis niloticus in brackish water. J Appl Aquac 28:1–8. https://doi.org/10.1080/10454438.2015.1104943
Mashaii N, Rajabipour F, Bitaraf A, Hosseinzadeh H, Rohani MS, Sarsangi H, Mohammadi M (2022) Reproductive biology of Nile tilapia, Oreochromis niloticus under the brackish water culture condition. Int J Agric Fodd Sci 6:4–7. https://doi.org/10.26855/ijfsa.2022.03.002
Mercante CTJ, Martins YK, Carmo CF, Osti JS, Pinto CSR, Tucci A (2007) Qualidade da água em viveiro de tilápia do Nilo (Oreochromis niloticus): caracterização diurna de variáveis físicas, químicas e biológicas. Bioikos 21:79–88
Mordenti O, Casalini A, Mandelli M, di Biase A (2014) A closed recirculating aquaculture system for artificial seed production of the European eel (Anguilla anguilla): technology development for spontaneous spawning and eggs incubation. Aquac Eng 58:88–94. https://doi.org/10.1016/j.aquaeng.2013.12.002
Parkanzky M, Grimes J, Schmiedt C, Secrest S, Bugbee A (2019) Long-term survival of dogs treated for gallbladder mucocele by cholecystectomy, medical management, or both. J Vet Intern Med 33:2057–2066. https://doi.org/10.1111/jvim.15611
Peixe BR (2021) Anuário PeixeBR de Piscicultura. Associação Brasileira da Piscicultura, São Paulo
Peña-Mendoza B, Gómez-Márquez JL, Salgado-Ugarte IH, Ramírez-Noguera D (2005) Reproductive biology of Oreochromis niloticus (Perciformes: Cichlidae) at Emiliano Zapata dam, Morelos. Mexico Biol Trop 53:515–522
Philippart JC, Ruwet JC (1982) Ecology and distribution of tilapias. In: Pullin RSV, Lowe-McConnell RH (eds) The biology and culture of tilapias. ICLARM Conference Proceedings 7th, 1980. ICLARM-International Center for Living Aquatic Resources Management, Manila, pp 15–59
Pires AV, Pedreira MM, Pereira IG, Fonseca Júnior AD, Araújo CV, Silva e Silva LHD (2011) Prediction of yield and weight of Nile tilapia fillet. Acta Sci. Anim. Sci. 33:315–319. https://doi.org/10.4025/actascianimsci.v33i3.10838
Porto EP, Oliveira CALD, Martins EN, Ribeiro RP, Conti ACM, Kunita NM, Oliveira SN, Porto PP (2015) Respostas à seleção de características de desempenho em tilápia-do-Nilo. Pesqui Agropecu Bras 50:745–752. https://doi.org/10.1590/S0100-204X2015000900002
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Raitt DS (1930) The fecundity of annual egg-production of the haddock (Gadus aeglefinus, l) with special reference to the factors determining or influencing same. University of Aberdeen, United Kingdom
Ridha MT, Cruz EM, Al-Ameeri AA, Al-Ahmed AA (1998) Effects of controlling temperature and light duration on seed production in tilapia, Oreochromis spilurus (Günther). Aquac Res 29:403–410. https://doi.org/10.1046/j.1365-2109.1998.00216.x
Roosevelt RB (1872) Fish Culture compared in importance with agriculture: speech of Hon. Robert B. Roosvelt, of New York, in the House of representatives, 13. F. & J. Rives and Geo. A. Bailey, Wahington
Rutten MJ, Bovenhui H, Komen H (2004) Modeling fillet traits based on body measurements in three Nile tilapia strains (Oreochromis niloticus L.). Aquaculture 231:113–122. https://doi.org/10.1016/j.aquaculture.2003.11.002
Schoenfeld D (1982) Partial residuals for the proportional hazards regression model. Biometrika 69:239–241. https://doi.org/10.1093/biomet/69.1.239
Sewalem A, Kistemaker GJ, Ducrocq V, Van Doormaal BJ (2005) Genetic analysis of herd life in Canadian dairy cattle on a lactation basis using a Weibull proportional hazards model. J Dairy Sci 88:368–375. https://doi.org/10.3168/jds.S0022-0302(05)72696-5
Shalloof KAS, Salama HM (2008) Investigations on some aspects of reproductive biology in Oreochromis niloticus (Linnaeus, 1757) inhabited Abu-zabal Lake, Egypt. Global Veterinaria 2:351–359
Shoko AP, Limbu SM, Mrosso HDJ, Mgaya YD (2015) Reproductive biology of female Nile tilapia Oreochromis niloticus (Linnaeus) reared in monoculture and polyculture with African sharptooth catfish Clarias gariepinus (Burchell). Springerplus 4:1–9. https://doi.org/10.1186/s40064-015-1027-2
Silva ACF, Corrêa Filho RAC, Ventura AS, Nunes AL, Laice LM, Ribeiro RP, Oliveira CAL, Almeida LC, Barbosa PTL, Povh JA (2020) Reproductive traits in different Nile tilapia genetic groups. Arq Bras Med Vet Zootec 72:1797–1804. https://doi.org/10.1590/1678-4162-11764
Suresh V, Bhujel RC (2012) Tilapias. In: Lucas JS, Southgate PC (eds) Aquaculture: farming aquatic animals and plants. Wiley-Blackwell Publishing Company, United Kingdom. https://doi.org/10.1002/9781118687932.ch16
Teame T, Zebib H, Meresa T (2018) Observations on the biology of Nile tilapia, Oreochromis niloticus L., in Tekeze Reservoir, Northern Ethiopia. J Fish Aquat 10:86–94. https://doi.org/10.5897/IJFA2017.0637
Tesema Z, Deribe B, Kefale A, Lakew M, Tilahun M, Shibesh M, Belayneh N, Zegeye A, Worku G, Yizengaw L (2020) Survival analysis and reproductive performance of Dorper x Tumele sheep. Heliyon 6:e03840. https://doi.org/10.1016/j.heliyon.2020.e03840
Turra EM, Oliveira DAA, Teixeira EA, Prado SA, Melo DC, Sousa AB (2010) Uso de medidas morfométricas no melhoramento genético do rendimento de filé da tilápia do Nilo (Oreochromis niloticus). Revista Brasileira De Reprodução Animal 34:29–36
Valencia-Posadas M, Torrero-Garza Y, Torres-Vázquez JA, Ángel-Sahagún CA, Gutiérrez-Chávez AJ, Shepard L, Montaldo HH (2017) Genetic parameters for functional stayability to 24 and 36 months of age and first lactation milk yield in dairy goats. Small Rumin Res 149:209–213. https://doi.org/10.1016/j.smallrumres.2017.02.010
Vollema AR, Van der Beek S, Harbers AGF, de Jong G (2000) Genetic evaluation for longevity of Dutch dairy bulls. J Dairy Sci 83:2629–2639. https://doi.org/10.3168/jds.S0022-0302(00)75156-3
Wald A (1939) Contributions to the theory of statistical estimation and testing hypotheses. Ann Math Stat 10:299–326. https://doi.org/10.1214/aoms/1177732144
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To Idalmo Garcia Pereira, Rúbia Monteiro de Jesus, and Nathalia Fernandino Moreira for invaluable logistical support.
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This project was financially supported by the Minas Gerais Research Funding Foundation (FAPEMIG—process APQ-01530–16), the Coordination for the Improvement of Higher Education Personnel—CAPES (Financing Code 001), the National Council for Scientific and Technological Development (CNPq—Institutional Scientific Initiation Program—PIBIC, EDITAL 001/2021—PBIC/CNPq), and to Banco do Nordeste do Brasil (BNB—FUNDECI 2012/324).
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TAF wrote, conceived the manuscript, and analyzed the data. MMP wrote, conceived the manuscript, and designed the research. ERS wrote, conducted, and collected data for research. CRM conceived, conducted, and collected data for research. LLV wrote, conceived the manuscript, and designed the research.
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Ferreira, T.A., de Souza, E.R., Matos, C.R. et al. Survival analysis as a tool for breeding management of Nile tilapia in an intensive system. Aquacult Int (2023). https://doi.org/10.1007/s10499-023-01289-z
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DOI: https://doi.org/10.1007/s10499-023-01289-z