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Towards a universal scale to assess sexual maturation and related life history traits in oviparous teleost fishes

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Abstract

The literature presents a confusing number of macroscopic maturation scales for fish gonads, varying from over-simplified scales comprising three to four stages to highly specific and relatively complicated nine-stage scales. The estimation of some important life history traits are dependent on a correct assessment and use of the gonadal maturation scales, and frequent mistakes have been made in many studies. The goal of this report is to provide a synthetic, relatively simple, yet precise maturation scale that works for most oviparous teleost fishes. The synthetic scale proposed here is based on the correspondence between key physiological and cytological processes of gamete development and corresponding modifications observed at the macroscopic level. It is based on previous and ongoing studies of several fish species pertaining to some of the most important African and Neotropical taxa, including Characiformes, Siluriformes, Osteoglossiformes and Perciformes. This scale should allow for standardized protocols of field studies and improve intra- and inter-specific comparisons of life history traits. Guidelines on the correct use of this scale to estimate these life history traits are provided.

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References

  • Arocha F (2002) Oocyte development and maturity classification of swordfish from the north-western Atlantic. J Fish Biol 60:13–27

    Article  Google Scholar 

  • Balon EK (1975) Reproductive guilds of fishes: a proposal and definition. J Fish Res Board Can 32:821–864

    Google Scholar 

  • Barbieri LR, Chittenden JME, Lowerre-Barbieri SK (1994) Maturity, spawning, and ovarian cycle of Atlantic croaker, Micropogonias undulatus, in the Chesapeake Bay and adjacent coastal waters. Fish B-NOAA 92:671–685

    Google Scholar 

  • Bazzoli N, Godinho HP (1991) Reproductive biology of the Acestrorhynchus lacustris (Reinhardt, 1874) (Pisces, Characidae) from Tres-Marias-Reservoir, Brazil. Zool Anz 226:285–297

    Google Scholar 

  • Bazzoli N, Godinho HP (1994) Cortical alveoli in oocytes of freshwater neotropical teleost fish. Boll Zool 61:301–308

    Google Scholar 

  • Bazzoli N, Rizzo E (1990) A comparative cytological and cytochemical study of the oogenesis in ten brazilian teleost fish species. Eur Archiv Biol 101:399–410

    Google Scholar 

  • Bazzoli N, Sato Y, Santos JE, Cruz AMG, Cangussu LCV, Pimenta RS, Ribeiro VMA (1997) Biologia reprodutiva de quatro espécies de peixes forrageiros da represa de Três Marias, MG. Bios Cuadernos Dep Ciências Biol PUC Minas 5:17–28

    Google Scholar 

  • Brito MFG, Bazzoli N (2003) Reproduction of the surubim catfish (Pisces, Pimelodidae) in the São Francisco River, Pirapora Region, Minas Gerais, Brazil. Arq Bras Med Vet Zootec 55:624–633

    Article  Google Scholar 

  • Casadevall M, Bonnet S, Matallanas J (1993) Description of different stages of oogenesis in Ophiodon barbatum (Pisces, Ophidiidae). Environ Biol Fish 36:127–133

    Article  Google Scholar 

  • Coward K, Bromage NR (1998) Histological classification of oocyte growth and the dynamics of ovarian recrudescence in Tilapia zillii. J Fish Biol 53:285–302

    Google Scholar 

  • Crespi BJ, Teo R (2002) Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes. Evolution 56:1008–1020

    PubMed  Google Scholar 

  • da Silva CA, Moraes MF, Pellegrini E (2003) Ovary maturation stages and oocyte features in three species of the neotropical fish Hemiodus (Müller, 1842). Braz Arch Biol Technol 46:433–441

    Google Scholar 

  • Duponchelle F, Legendre M (2001) Rapid phenotypic changes of reproductive traits in response to modification of spatial structure in Nile tilapia, Oreochromis niloticus. Aquat Living Resour 14:145–152

    Article  Google Scholar 

  • Duponchelle F, Panfili J (1998) Variations in age and size at maturity of female Nile tilapia, Oreochromis niloticus, populations from man-made lakes of Côte d’Ivoire. Environ Biol Fish 52:453–465

    Article  Google Scholar 

  • Duponchelle F, Ribbink AJ (2000) Fish ecology report. SADC/GEF Lake Malawi/Nyasa biodiversity conservation project, final report, 325 pp. Available at: http://malawicichlids.com/mw14001.htm#DR00

  • Duponchelle F, Cecchi P, Corbin D, Nunez J, Legendre M (1999) Spawning season variations of female Nile tilapia, Oreochromis niloticus, populations from man-made lakes of Côte d’Ivoire. Environ Biol Fish 56:377–389

    Article  Google Scholar 

  • Duponchelle F, Carvajal F, Renno JF, Dugué R, Nuñez J (2006) Historia de vida del tucunaré, Cichla monoculus, en la Amazonía Boliviana. In: Renno JF, Garcia C, Duponchelle F, Nunez J (eds) Biologia de las poblaciones de Peces de la Amazonía y Piscicultura. IIAP-IRD, Iquitos, pp 13–17

  • Duponchelle F, Lino F, Hubert N, Panfili J, Renno J-F, Baras E, Torrico JP, Dugué R, Nuñez J (2007) Environment-related life history trait variations of the red-bellied piranha, Pygocentrus nattereri, in two river basins of the Bolivian Amazon. J Fish Biol 71:1113–1134

    Article  Google Scholar 

  • Ferreira RMA, Godinho HP (1990) Reproductive biology of the white-piau, Schizodon knerii (Steindachner, 1875) (Anostomidae) from a reservoir in Southeast Brazil. Eur Archiv Biol 101:331–344

    Google Scholar 

  • Ferreira RMA, Bazzoli N, Rizzo E, Sato Y (1996) Aspectos reprodutivos da piranha, Pygocentrus piraya (Teleostei, Characiformes), espécie nativa da bacia do Rio São Francisco. Arq Bras Med Vet Zootec 48:71–76

    Google Scholar 

  • Fonseca Ratton T, Bazzoli N, Bastos Santos G (2003) Reproductive biology of Apareiodon affinis (Pisces: Parodontidae) in the Furnas Reservoir, Minas Gerais, Brazil. J Appl Ichthyol 19:387–390

    Article  Google Scholar 

  • Giulianini PG, Di Marcotullio A, Ferrero EA (1994) Light microscopical and ultrastructural cytology of the ovaries in the sea-grass goby Zosterisessor ophiocephalus (Osteichtyes, Gobiidae). Boll Zool 61:135–144

    Google Scholar 

  • Gomes BVC, Scarpelli RS, Arantes FP, Sato Y, Bazzoli N, Rizzo E (2007) Comparative oocytemorphology and early development in three species of trahiras from the Saõ Francisco River basin, Brazil. J Fish Biol 70:1412–1429

    Google Scholar 

  • Gonçalves TL, Bazzoli N, Brito MFG (2006) Gametogenesis and reproduction of the matrinxã Brycon orthotaenia (Günther, 1864) (Pisces: Characidae) in the São Francisco river, Minas Gerais, Brazil. Braz J Biol 66:513–522

    Article  PubMed  Google Scholar 

  • Grau A, Crespo S, Riera F, Pou S, Sarasquete MC (1996) Oogenesis in the amberjack Seriola dumerili Risso, 1810. An histological, histochemical and ultrastructural study of oocyte development. Sci Mar 60:391–406

    CAS  Google Scholar 

  • Hunter JR, Macewicz BJ (1985) Rates of atresia in the ovary of captive and wild northern anchovy, Engraulis mordax. Fish Bull 83:119–136

    Google Scholar 

  • Jackson LF, Sullivan CV (1995) Reproduction of white perch: the annual gametogenic cycle. Trans Am Fish Soc 124:563–577

    Article  Google Scholar 

  • Lamas IR, Godinho AL (1996) Reproduction in the piranha Serrasalmus spilopleura, a neotropical fish with an unusual pattern of sexual maturity. Environ Biol Fish 45:161–168

    Article  Google Scholar 

  • Legendre M, Ecoutin JM (1989) Suitability of brackish water tilapia species from the Ivory Coast for lagoon aquaculture 1—reproduction. Aquat Living Resour 2:71–79

    Article  Google Scholar 

  • Le Menn F, Davail B, Pelissero C, Ndiaye P, Bon E, Perazzolo L, Nunez Rodriguez J (2000) New approach to fish oocyte vitellogenesis. In: Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds) 6th Int Symp Reprod Physiol Fish. Bergen, Norway, pp 281–284

    Google Scholar 

  • Loubens G, Aquim J L (1986) Sexualidad y reproduccion de los principales peces de la cuenca del Rio Mamoré, Béni, Bolivia. Informe cientifico N° 5. ORSTOM-UTB-BENI, Trinidad, Bolivia

  • Loubens G, Panfili J (1995) Biologie de Prochilodus nigricans (Teleostei: Prochilodontidae) dans le bassin du Mamoré (Amazonie bolivienne). Ichthyol Explor Freshw 6:17–32

    Google Scholar 

  • Loubens G, Panfili J (1997) Biologie de Colossoma macropomum (Teleostei: Serrasalmidae) dans le bassin du Mamoré (Amazonie bolivienne). Ichthyol Explor Freshw 8:1–22

    Google Scholar 

  • Loubens G, Panfili J (2000) Biologie de Pseudoplatystoma fasciatum et P. tigrinum (Teleostei: Pimelodidae) dans le bassin du Mamoré. Ichthyol Explor Freshw 11:13–34

    Google Scholar 

  • Loubens G, Panfili J (2001) Biologie de Piaractus brachypomus (Telostei: Serrasalmidae) dans le bassin du Mamoré (Amazonie bolivienne). Ichthyol Explor Freshw 12:51–64

    Google Scholar 

  • Loubens G, Aquim JL, Robles E (1984) Primeras observaciones sobre la sexualidad y la reproduccion de las principales especies de peces de la region de trinidad, Béni, Bolivia. Informe cientifico N° 1. ORSTOM-UTB-BENI, Trinidad, Bolivia, 34 pp

  • Lowe-McConnell RH (1964) The fishes of the Rupununi savanna district of Bristish Guiana, South America. Part 1. Ecological groupings of fish species and effects of the seasonal cycle on the fish. Zool J Linn Soc Lond 45:103–144

    Article  Google Scholar 

  • Lowe-McConnell RH (1969) The cichlid fishes of Guyana, South America, with notes on their ecology and breeding behaviour. Zool J Lin Soc Lond 48:255–302

    Article  Google Scholar 

  • Lowe-McConnell RH (1987) Ecological studies in tropical fish communities. Cambridge University Press, Cambridge, 382 pp

  • Magalhães ALB, Sato Y, Rizzo E, Ferreira RMA, Bazzoli N (1996) Ciclo reprodutivo do tucunaré Cichla ocellaris (Schneider, 1801) na represa de Três Marias, MG. Arq Bras Med Vet Zootec 48:85–92

    Google Scholar 

  • Mañanos E, Nuñez-Rodriguez J, Le Menn F, Zanuy S, Carrillo M (1997) Identification of vitellogenin receptors in the ovary of a teleost fish, the Mediterranean sea bass (Dicentrarchus labrax). Reprod Nutr Dev 37:51–61

    Article  PubMed  Google Scholar 

  • Miranda ACL, Bazzoli N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tissue Cell 31:480–488

    Article  PubMed  CAS  Google Scholar 

  • Muñoz H, Van Damme PA (1998) Parametros de reproduction de 4 especies de peces comerciales (Pseudoplatystoma fasciatum, P. trigrinum, Colossoma macropomum y Piaractus brachypomum) en la cuenca del Rio Ichilo (Bolivia). Rev Bol Ecol Conserv Ambiental 4:39–54

    Google Scholar 

  • Muñoz H, Van Damme PA, Duponchelle F (2006) Breeding behaviour and distribution of the tucunaré Cichla aff. monoculus in a clear water river of the Bolivian Amazon. J Fish Biol 69:1018–1030

    Article  Google Scholar 

  • Ndiaye P, Forgue J, Lamothe V, Cauty C, Tacon P, Lafon P, Davail B, Fostier A, Le Menn F, Núñez J (2006) Tilapia Oreochromis niloticus vitellogenins: development of homologous and heterologous ELISAs and analysis of vitellogenin pathway through the ovarian follicle. J Exp Zool 305A:576–593

    Article  CAS  Google Scholar 

  • Nunez Rodriguez J, Hem S, Otémé ZJ (1995) Comparative study of vitellogenesis of two African catfish species Chrysichthys nigrodigitatus (Claroteidae) and Heterobranchus longifilis (Clariidae). Aquat Living Resour 8:291–296

    Article  Google Scholar 

  • Nuñez Rodriguez J, Bon E, Le Menn F (1996) Vitellogenin receptors during vitellogenesis in rainbow trout, Oncorhynchus mykiss. J Exp Zool 274A:163–170

    Article  Google Scholar 

  • Nuñez J, Inturias A, Dugue R, Barreto J, Rivera R, Duponchelle F, Renno J F (2006a) Reproducción y crecimiento de Pseudoplatystoma fasciatum en la cuenca amazónica Boliviana. In: Renno JF, Garcia C, Duponchelle F, Nunez J (eds) Biologia de las poblaciones de Peces de la Amazonía y Piscicultura. IIAP-IRD, Iquitos, pp 47–51

  • Nuñez J, Maldonado E, Dugué R, Duponchelle F, Aliaga C, Rivera R, Renno J F (2006b) Reproducción y crecimiento de Colossoma macropomum en las cuencas del Iténez y del Mamoré (Amazonía Boliviana). In: Biologia de las poblaciones de Peces de la Amazonía y Piscicultura. IIAP-IRD, Iquitos, pp 55–60

  • Otemé ZJ, Nuñez Rodriguez J, Kouassi CK, Agnese JF, Hem S (1996) Testicular structure and sperm cryopreservation of the african catfish Heterobranchus longifilis (Clariidae). Aquac Res 27:805–813

    Article  Google Scholar 

  • Perez-Vega MH, Uribe-Aranzabal MC, Garcia-Lorenzana M, Romero-Ramirez MC, Arredondo-Figueroa JL (2006) Description of the ovarian follicle growth of the neotropical cichlids Petenia splendida and Parachromis managuensis (Perciformes: Cichlidae). J Appl Ichthyol 22:515–520

    Article  Google Scholar 

  • Poortenaar CW, Hickman RW, Tait MJ (2001) Seasonal changes in ovarian activity of New Zealand turbot (Colistium nudipinnis) and brill (C. guntheri). N Z J Mar Freshw Res 35:521–529

    Article  Google Scholar 

  • Ravaglia MA, Maggese MC (2003) Ovarian follicle ultrastructure in the teleost Synbranchus marmoratus (B, 1795), with special reference to the vitelline envelope development. Tissue Cell 35:9–17

    Article  PubMed  CAS  Google Scholar 

  • Ricardo MCP, Rizzo E, Sato Y, Bazzoli N (1998) Analise histológica da reprodução de Tetragonopterus chalceus Agassiz, 1829 (Pisces: Characidae) na represa de Três Marias, Minas Gerais. BIOS 6:113–120

    Article  Google Scholar 

  • Rizzo E, Bazzoli N (1995) Follicular atresia in curimatá-pioa Prochilodus affinis Reinhardt, 1874 (Pisces, Characiformes). Rev Bras Biol 55:697–703

    Google Scholar 

  • Robillard E, Reiss CS, Jones CM (2008) Reproductive biology of bluefish (Pomatomus saltatrix) along the East Coast of the United States. Fish Res (in press), corrected proof. Available at: http://www.sciencedirect.com/science/article/B6T6N-4R3BYYC-1/2/cc8fe09e376b3dcc2da3b43cf45bb8fa

  • Selman K, Wallace R (1989) Cellular aspects of oocyte growth in teleosts. Zool Sci 6:211–231

    Google Scholar 

  • Spadella MA, de Castilho-Almeida RB, Quagio-Grassiotto I, Cesario MD (2005) Follicular diameter range based on morphological features in Synbranchus marmoratus (Bloch, 1795) (Teleostei, Synbranchiformes, Synbranchidae) from the South-central region of Brazil. Tissue Cell 37:91–100

    Article  PubMed  Google Scholar 

  • Sumpter JP (1997) Environmental control of fish reproduction: a different perspective. Fish Physiol Biochem 17:25–31

    Article  CAS  Google Scholar 

  • Suzuki HI, Agostinho AA, Winemiller KO (2000) Relationship between oocyte morphology and reproductive strategy in locariid catfishes of the Parana River, Brazil. J Fish Biol 57:791–807

    Google Scholar 

  • Teles MEO, Godinho HP (1997) Ciclo reproductivo da pirampeba Serrasalmus brandtii (Teleostei, Characidae) na represa de Três Marias, Rio Säo Francisco. Rev Bras Biol 57:177–184

    Google Scholar 

  • Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleosts. Rev Fish Biol Fish 6:287–318

    Article  Google Scholar 

  • Wallace RA (1985) Vitellogenesis and oocyte growth in non-mammalian vertebrates. In: Browder LW (ed) Developmental biology. Plenum Press, New York, pp 127–177

    Google Scholar 

  • Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86:25–88

    Article  PubMed  CAS  Google Scholar 

  • Winemiller KO (1989) Patterns of variations in life history among south American fishes in seasonal environments. Oecologia 81:225–241

    Google Scholar 

  • Winemiller KO, Rose KA (1992) Patterns of life history diversification in north American fishes: implications for population regulation. Can J Fish Aquat Sci 49:2196–2218

    Article  Google Scholar 

  • Yamaguchi A, Todoroki T, Kume G (2006) Reproductive cycle, sexual maturity and diel-reproductive periodicity of white croaker, Pennahia argentata (Sciaenidae), in Ariake Sound, Japan. Fish Res 82:95–100

    Article  Google Scholar 

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Acknowledgements

This work has been funded by IRD (UR 081 and 175) and carried out in collaboration with UMSA, La Paz, Bolivia; UMSS, Cochabamba, Bolivia and IIAP, Iquitos Perú in the framework of the RIIP network (Red de Investigacin sobre Ia Ictiofauna Amaznica, http://www.riiaamazonia.org).

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Núñez, J., Duponchelle, F. Towards a universal scale to assess sexual maturation and related life history traits in oviparous teleost fishes. Fish Physiol Biochem 35, 167–180 (2009). https://doi.org/10.1007/s10695-008-9241-2

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