Abstract:
Aim
To investigate reproductive characteristics in a small population of Psalidodon aff. fasciatus living in isolation in an environment with a unique geological configuration, a doline-shaped depression (known as Furna 2), with a mean diameter of 80 m and water depth of 50 m, a natural heritage of the Vila Velha State Park (VVSP).
Methods
The fish were collected between February 2019 and January 2020 using nets and pots; standard length and total weight were measured. The gonads were also removed for histological analysis. Estimates were made for the weight-length ratio, the relative condition factor, the sex ratio, and the size at first maturity (L50 and L95) for males and females.
Results
The five gonadal stages that were characterized (resting, early mature, mature, partially empty, and totally empty) were consistent with what was expected for the species. The results obtained here indicate that these lambaris have an opportunistic (r) life strategy. Compared to previous studies, we discovered that fish of this population start maturing at smaller sizes. Indicating negative allometric growth, the length-weight ratio was WT = 0.0002 * LT2.3039, and the condition index (Kn = 0.95) showed no significant gender differences. When compared to other non-isolated populations of the same species, the population's sex ratio showed an unexpectedly significant male predominance (1M: 0.6 F).
Conclusions
Our results show an imbalance in the sex ratio, contrary to what would be expected for non-isolated populations. This imbalance may be related to the complete isolation of this environment, suggesting that females may be affected by some evolutionary force, such as inbreeding. However, other factors cannot be ruled out, as the underlying genetic mechanisms remain unknown, and only future investigations can reveal a more complete understanding of reproduction in isolated populations.
Keywords:
lambari; reproduction; sex ratio; gonads; inbreeding
Resumo:
Objetivo
Investigar caracteres reprodutivos em uma pequena população natural de Psalidodon aff. fasciatus que está isolada em um ambiente com rara configuração geológica, uma depressão em forma de dolina (conhecida como Furna 2), com diâmetro médio de 80 m e lâmina d'água de 50 m, patrimônio natural do Parque Estadual de Vila Velha.
Métodos
Os peixes foram coletados entre fevereiro de 2019 e janeiro de 2020 com redes e covos; foram determinados o comprimento padrão e o peso total, além da remoção das gônadas para análises histológicas. Também, foram estimadas a relação peso-comprimento, o fator de condição relativo, a proporção sexual e o tamanho da primeira maturação (L50 e L95) para machos e fêmeas.
Resultados
Caracterizamos cinco estádios de desenvolvimento gonadal: repouso, maduro inicial, maduro, parcialmente vazio e totalmente vazio, não diferindo do esperado para a espécie. Os resultados aqui obtidos indicam que esses lambaris possuem estratégia de vida do tipo oportunística (r). Comparado a estudos anteriores, descobrimos que os peixes desta população começam a amadurecer em tamanhos menores. Indicando crescimento alométrico negativo, a relação peso-comprimento foi WT = 0.0002 * LT2.3039, e o fator de condição (Kn = 0.95) não diferiu significativamente entre os sexos. A proporção sexual revelou uma predominância significativa e inesperada de machos (1M: 0,6 F) dentro da população, e também quando comparada com outras populações não isoladas da mesma espécie.
Conclusões
Nossos resultados revelam um desequilíbrio na proporção sexual, contrastando com o esperado para a espécie em condições de não isolamento. Esse desequilíbrio pode estar relacionado ao isolamento completo desse ambiente, sugerindo que as fêmeas podem estar sendo afetadas por alguma força evolutiva, como a endogamia. No entanto, não podem ser descartados outros fatores, pois, os mecanismos genéticos subjacentes permanecem ainda desconhecidos, somente investigações futuras poderão revelar uma compreensão mais completa da reprodução em populações isoladas.
Palavras-chave:
lambari; reprodução; razão sexual; gônadas; endogamia
1. Introduction
The most diverse group of vertebrates are fishes, which also display a variety of reproductive strategies that ensure the fitness of a species in a given environment (Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.; Lassala & Renesto, 2007Lassala, M.D.P., & Renesto, E., 2007. Reproductive strategies and genetic variability in tropical freshwater fish. Genet. Mol. Biol. 30(3), 690-697. http://dx.doi.org/10.1590/S1415-47572007000400030.
http://dx.doi.org/10.1590/S1415-47572007...
; Azevedo, 2010Azevedo, M.A., 2010. Reproductive characteristics of characid fish species (Teleostei, Characiformes) and their relationship with body size and phylogeny. Iheringia Ser. Zool. 100(4), 469-482. http://dx.doi.org/10.1590/S0073-47212010000400020.
http://dx.doi.org/10.1590/S0073-47212010...
). Much remains to be known about the reproductive biology of species in the Neotropical region (Waddell et al., 2019Waddell, J.C., Njeru, S.M., Akhiyat, Y.M., Schachner, B.I., Correa-Roldán, E.V., & Crampton, W.G.R., 2019. Reproductive life-history strategies in a species-rich assemblage of Amazonian electric fishes. PLoS One 14(12), e0226095. PMid:31805125. http://dx.doi.org/10.1371/journal.pone.0226095.
http://dx.doi.org/10.1371/journal.pone.0...
), presumably because this region having the planet’s highest variety of freshwater ichthyofauna (Lowe-McConnel, 1999Lowe-McConnel, R.H. 1999. Estudos ecológicos de comunidades de peixes tropicais. São Paulo: Edusp, 534 p.; Reis et al., 2003Reis, R.E., Kullander, S.O., & Ferraris, C., 2003. Check list of the freshwater fishes of South and Central America (CLOFFSCA). Porto Alegre: EDIPUCRS, 729 p., 2016Reis, R.E., Albert, J.S., Di Dario, F., Mincarone, M.M., Petry, P., & Rocha, L.A., 2016. Fish biodiversity and conservation in South America. J. Fish Biol. 89(1), 12-47. PMid:27312713. http://dx.doi.org/10.1111/jfb.13016.
http://dx.doi.org/10.1111/jfb.13016...
; Albert et al., 2020Albert, J.S., Tagliacollo, V.A., & Dagosta, F., 2020. Diversification of neotropical freshwater fishes. Annu. Rev. Ecol. Evol. Syst. 51(1), 27-53. http://dx.doi.org/10.1146/annurev-ecolsys-011620-031032.
http://dx.doi.org/10.1146/annurev-ecolsy...
). The Characiformes, along with the Siluriformes, are the largest group in the Neotropical region, with a wide range of morphologies, behaviors, and life histories that reflect their interactions with other species and the ecosystem (Nelson, 2006Nelson, J.S., 2006. Fishes of the World. New York: John Wiley & Sons, 601 p.; Albert et al., 2012Albert, J., Albert, J.S., & Reis, R.E., 2012. Historical biogeography of neotropical freshwater fishes. Berkeley: University of California Press. http://dx.doi.org/10.1525/california/9780520268685.001.0001.
http://dx.doi.org/10.1525/california/978...
; Toussaint et al., 2016Toussaint, A., Charpin, N., Brosse, S., & Villéger, S., 2016. Global functional diversity of freshwater fish is concentrated in the Neotropics while functional vulnerability is widespread. Sci. Rep. 6(1), 22125. PMid:26980070. http://dx.doi.org/10.1038/srep22125.
http://dx.doi.org/10.1038/srep22125...
; Antonelli et al., 2018Antonelli, A., Ariza, M., Albert, J., Andermann, T., Azevedo, J., Bacon, C., Faurby, S., Guedes, T., Hoorn, C., Lohmann, L.G., Matos-Maraví, P., Ritter, C.D., Sanmartín, I., Silvestro, D., Tejedor, M., ter Steege, H., Tuomisto, H., Werneck, F.P., Zizka, A., & Edwards, S.V., 2018. Conceptual and empirical advances in Neotropical biodiversity research. PeerJ 6, e5644. PMid:30310740. http://dx.doi.org/10.7717/peerj.5644.
http://dx.doi.org/10.7717/peerj.5644...
). With 1245 species and 142 genera, the family Characidae is the most diverse among the Characiformes (Fricke et al., 2022Fricke, R., Eschmeyer, W.N., & Van der Laan, R., 2022. Eschmeyer's catalog of fishes: genera, species [online]. Retrieved in 2022, November 16, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
http://researcharchive.calacademy.org/re...
). They are mostly small (15 cm) fish with a variety of reproductive and feeding strategies (Reis et al., 2016Reis, R.E., Albert, J.S., Di Dario, F., Mincarone, M.M., Petry, P., & Rocha, L.A., 2016. Fish biodiversity and conservation in South America. J. Fish Biol. 89(1), 12-47. PMid:27312713. http://dx.doi.org/10.1111/jfb.13016.
http://dx.doi.org/10.1111/jfb.13016...
).
Psalidodon Eigenmann, 1911 is a genus with 43 species (Fricke et al., 2022Fricke, R., Eschmeyer, W.N., & Van der Laan, R., 2022. Eschmeyer's catalog of fishes: genera, species [online]. Retrieved in 2022, November 16, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
http://researcharchive.calacademy.org/re...
) that has recently been revalidated by four molecular and two morphological synapomorphies (Terán et al., 2020Terán, G.E., Benitez, M.F., & Mirande, J.M., 2020. Opening the Trojan horse: phylogeny of Astyanax, two new genera and resurrection of Psalidodon (Teleostei: Characidae). Zool. J. Linn. Soc. 190(4), 1217-1234. http://dx.doi.org/10.1093/zoolinnean/zlaa019.
http://dx.doi.org/10.1093/zoolinnean/zla...
). These fish can be found in Argentina, Bolivia, Brazil, Paraguay, and Uruguay, where they live in large rivers, streams, and headwaters (Baumgartner et al., 2012Baumgartner, G., Pavanelli, C.S., Baumgartner, D., Bifi, A.G., Debona, T., & Frana, V.A., 2012. Peixes do baixo rio Iguaçu. Maringá: Eduem, 203 p. http://dx.doi.org/10.7476/9788576285861.
http://dx.doi.org/10.7476/9788576285861...
; Reis et al., 2020Reis, R.B., Frota, A., Carvalho Deprá, G., Ota, R.R., & Graça, W.J., 2020. Freshwater fishes from Paraná state, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa 4868(4), zootaxa.4868.4.1. PMid:33311378.; Dos Santos & de Britto, 2021Santos, S.A., & de Britto, M.R., 2021. The ichthyofauna of a poorly known area in the middlesouthern espinhaço mountain range, state of Minas Gerais, Brazil: diagnostics and identification keys. ZooKeys 1054, 25-66. PMid:34393562. http://dx.doi.org/10.3897/zookeys.1054.67554.
http://dx.doi.org/10.3897/zookeys.1054.6...
). Psalidodon fasciatus (Cuvier, 1819), popularly known as lambari, is a species complex that occurs in several Brazilian hydrographic systems. Because the São Francisco population is the type locality, much of the closely related species are likely to be P. aff. fasciatus (Gavazzoni et al., 2023Gavazzoni, M., Pavanelli, C.S., Graça, W.J., Oliveira, E., Moreira-Filho, O., & Margarido, V.P., 2023. Species delimitation in Psalidodon fasciatus (Cuvier, 1819) complex (Teleostei: Characidae) from three hydrographic basins. Biol. J. Linn. Soc. Lond. 138(1), 51-67. http://dx.doi.org/10.1093/biolinnean/blac139.
http://dx.doi.org/10.1093/biolinnean/bla...
). Chromosome variation has also been reported in some P. fasciatus populations, indicating the presence of cryptic species (Medrado et al., 2015Medrado, A.S., Affonso, P.R., Carneiro, P.L.S., Vicari, M.R., Artoni, R.F., & Costa, M.A., 2015. Allopatric divergence in Astyanax aff. fasciatus Cuvier, 1819 (Characidae, Incertae sedis) inferred from DNA mapping and chromosomes. Zool. Anz. 257, 119-129. http://dx.doi.org/10.1016/j.jcz.2015.05.005.
http://dx.doi.org/10.1016/j.jcz.2015.05....
). Most of the differences are found in the amount of satellite DNA (As51) (Medrado et al., 2015Medrado, A.S., Affonso, P.R., Carneiro, P.L.S., Vicari, M.R., Artoni, R.F., & Costa, M.A., 2015. Allopatric divergence in Astyanax aff. fasciatus Cuvier, 1819 (Characidae, Incertae sedis) inferred from DNA mapping and chromosomes. Zool. Anz. 257, 119-129. http://dx.doi.org/10.1016/j.jcz.2015.05.005.
http://dx.doi.org/10.1016/j.jcz.2015.05....
; Gavazzoni et al., 2023Gavazzoni, M., Pavanelli, C.S., Graça, W.J., Oliveira, E., Moreira-Filho, O., & Margarido, V.P., 2023. Species delimitation in Psalidodon fasciatus (Cuvier, 1819) complex (Teleostei: Characidae) from three hydrographic basins. Biol. J. Linn. Soc. Lond. 138(1), 51-67. http://dx.doi.org/10.1093/biolinnean/blac139.
http://dx.doi.org/10.1093/biolinnean/bla...
) and the number of diploid chromosomes (2n=46, 48, and 50 chromosomes) (Pansonato-Alves et al., 2013Pansonato-Alves, J.C., Hilsdorf, A.W.S., Utsunomia, R., Silva, D.M.Z.A., Oliveira, C., & Foresti, F., 2013. Chromosomal mapping of repetitive DNA and Cytochrome C Oxidase I sequence analysis reveal differentiation among sympatric samples of Astyanax fasciatus (Characiformes, Characidae). Cytogenet. Genome Res. 141(2-3), 133-142. PMid:24081020. http://dx.doi.org/10.1159/000354885.
http://dx.doi.org/10.1159/000354885...
).
External fertilization, opportunistic reproductive strategies, batch-spawning, and no parental care are common among these characids, with some exceptions such as insemination and large investments in fecundity (Menni & Almirón, 1994Menni, R.C., & Almirón, A.E., 1994. Reproductive seasonality in fishes of manmade ponds in temperate South America. Neotropica 40(103-104), 75-85.; Azevedo, 2010Azevedo, M.A., 2010. Reproductive characteristics of characid fish species (Teleostei, Characiformes) and their relationship with body size and phylogeny. Iheringia Ser. Zool. 100(4), 469-482. http://dx.doi.org/10.1590/S0073-47212010000400020.
http://dx.doi.org/10.1590/S0073-47212010...
; Malabarba & Malabarba, 2020Malabarba, L.R., & Malabarba, M.C., 2020. Phylogeny and classification of neotropical fish. In: Baldisserotto, B., Criscuolo Urbinati, E. & Cyrino, J.E.P., eds. Biology and physiology of freshwater neotropical fish. Amsterdam: Academic Press, 1-19. http://dx.doi.org/10.1016/B978-0-12-815872-2.00001-4
http://dx.doi.org/10.1016/B978-0-12-8158...
; Quirino et al., 2021Quirino, P.P., Siqueira-Silva, D.H., Silva Rodrigues, M., Santos-Silva, A.P., Delgado, M.L.R., Senhorini, J.A., & Veríssimo-Silveira, R., 2021. Gonadal morphology and difference in reproductive development of two isolated populations of Astyanax rivularis (Teleostei, Characidae). J. Fish Biol. 99(5), 1719-1728. PMid:34392530. http://dx.doi.org/10.1111/jfb.14879.
http://dx.doi.org/10.1111/jfb.14879...
). Some researches on the reproductive strategies of the lambaris indicates that they breed throughout the year, with peaks in the warmer months (Abilhoa, 2007Abilhoa, V., 2007. Aspectos da história natural de Astyanax scabripinnis Jenyns (Teleostei, Characidae) em um riacho de floresta com araucária no sul do Brasil. Rev. Bras. Zool. 24(4), 997-1005. http://dx.doi.org/10.1590/S0101-81752007000400016.
http://dx.doi.org/10.1590/S0101-81752007...
; Baumgartner et al., 2016Baumgartner, M.T., Rogério, P., Da Silva, L., & Baumgartner, G., 2016. Population structure and reproductive biology of Astyanax gymnodontus (Characiformes: Characidae), a poorly known endemic fish of the Iguaçu River basin, Brazil. Rev. Biol. Trop. 64(1), 69-77. PMid:28862403. http://dx.doi.org/10.15517/rbt.v64i1.18100.
http://dx.doi.org/10.15517/rbt.v64i1.181...
; Silveira et al., 2020Silveira, E.L., Aranha, J.M.R., Menezes, M.S., & Vaz-Dos Santos, A.M., 2020. Reproductive dynamics, age and growth of Astyanax aff. fasciatus in a Neotropical basin. Mar. Freshw. Res. 71(6), 670-683. http://dx.doi.org/10.1071/MF19100.
http://dx.doi.org/10.1071/MF19100...
; Portella et al., 2021Portella, A.C., Arsentales, A.D., Cavallari, D.E., & Welber, S.S., 2021. Effect of seasonality on the reproduction of characiformes fish in a neotropical river. Iheringia Ser. Zool. 111, e2021012. http://dx.doi.org/10.1590/1678-4766e2021012.
http://dx.doi.org/10.1590/1678-4766e2021...
).
In the Vila Velha State Park (VVSP), a protected area located in the upper Tibagi River basin in southern Brazil, a small population of the characin P. aff. fasciatus (Cuvier, 1819) can be found (Shibatta & Artoni, 2005Shibatta, O.A., & Artoni, R.F., 2005. Sobre a identidade das populações alopátricas de Astyanax (Characiformes, Characidae) das formações Furna 1 e Furna 2 do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Publ. UEPG Biol. Health Sci. 11(2), 7-12. https://doi.org/10.5212/publicatio%20uepg.v11i2.410.
https://doi.org/10.5212/publicatio%20uep...
). This naturally isolated population lives in the VVSP's Furna 2, a doline-shaped sandstone depression with an average diameter of 80 meters, a water depth of 50 meters, and walls reaching 110 meters (Campos & Dalcomune, 2011Campos, J.B., & Dalcomune, M.A., 2011. O Parque Estadual de Vila Velha. In: Carpanezi, O.T.B., & Campos, J.B., eds. Coletânea de pesquisas: Parques Estaduais de Vila Velha, Cerrado e Guartelá. Curitiba: Instituto Ambiental do Paraná, 66-79.). Furnas are among the most prominent landforms in the region, and they represent a unique geological heritage in the VVSP (Melo & Giannini, 2007Melo, M.S., & Giannini, P.C.F., 2007. Sandstone dissolution landforms in the furnas formation, southern Brazil. Earth Surf. Process. Landf. 32(14), 2149-2164. http://dx.doi.org/10.1002/esp.1520.
http://dx.doi.org/10.1002/esp.1520...
). The Furnas Formation, which formed between 395 and 421 million years ago in the Paraná Basin during the Siluro-Devonian period (Guimarães et al., 2007Guimarães, G.B., Melo, M.S., Giannini, P.C.F., & Melek, P.R., 2007. Geologia dos campos gerais. In: Melo, M.S., Moro, R.S., & Guimarães, G.B., eds. Patrimônio natural dos campos gerais do Paraná. Ponta Grossa: UEPG, 23-32, cap. 2.), consists of crater-like depressions formed by the karstification of sandstone rocks (Melo et al., 2011Melo, M.S., Guimarães, G.B., Pontes, H.S., Massuqueto, L.L., Pigurim, I., Bagatim, H.Q., & Giannini, P.C.F., 2011. Carste em rochas não-carbonáticas: o exemplo dos arenitos da Formação Furnas, Campos Gerais do Paraná/Brasil e as implicações para a região. Espeleo-Tema 22(1), 81-97.). Because of the environment geological configuration and lack of contact with nearby river drainages, this population of P. aff. fasciatus experienced clear isolation and restriction of gene flow (Artoni et al., 2006Artoni, R.F., Shibatta, O.A., Gross, M.C., Schneider, C.H., Almeida, M.C., Vicari, M.R., & Bertollo, L.A.C., 2006. Astyanax aff. fasciatus Cuvier, 1819 (Teleostei; Characidae): evidences of a species complex in the upper rio Tibagi Basin (Paraná, Brazil). Neotrop. Ichthyol. 4(2), 197-202. http://dx.doi.org/10.1590/S1679-62252006000200005.
http://dx.doi.org/10.1590/S1679-62252006...
). Previous research on this population has indicated that a percentage of individuals have malformed vertebrae as a result of isolation and likely inbreeding (Kerniske et al., 2021Kerniske, F.F., Pena Castro, J., De la Ossa-Guerra, L.E., Mayer, B.A., Abilhoa, V., Paiva-Affonso, I., & Artoni, R.F., 2021. Spinal malformations in a naturally isolated Neotropical fish population. PeerJ 9, e12239. PMid:34721968. http://dx.doi.org/10.7717/peerj.12239.
http://dx.doi.org/10.7717/peerj.12239...
).
Inbreeding tends to reduce intrapopulation genetic variability by increasing the frequency of deleterious alleles that are normally expressed in recessive homozygosis (Keller & Waller, 2002Keller, L.F., & Waller, D.M., 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17(5), 230-241. http://dx.doi.org/10.1016/S0169-5347(02)02489-8.
http://dx.doi.org/10.1016/S0169-5347(02)...
). Genetic variability may be reduced in populations distributed in distinct areas, this reduces their evolutionary potential and raises their extinction risk (Meffe & Carroll, 1994Meffe, G.K., & Carroll, C.R., 1994. Principles of conservation biology. Sunderland: Sinauer Associates Inc., 600 p.). Although the underlying mechanisms are poorly understood, the effects on fitness in inbred populations are highly variable, including body size reduction, changes in primary and secondary sexual characters, and morphological traits (Gilpin & Soulé, 1986Gilpin, M.E., & Soulé, M.E., 1986. Minimum viable populations: the processes of species extinctions. In: Soulé, M.E., ed. Conservation biology: the science of scarcity and diversity. Sunderland, MA: Sinauer Associates.; Keller & Waller, 2002Keller, L.F., & Waller, D.M., 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17(5), 230-241. http://dx.doi.org/10.1016/S0169-5347(02)02489-8.
http://dx.doi.org/10.1016/S0169-5347(02)...
; Mariette et al., 2006Mariette, M., Kelley, J.L., Brooks, R., & Evans, J.P., 2006. The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112(8), 807-814. http://dx.doi.org/10.1111/j.1439-0310.2006.01236.x.
http://dx.doi.org/10.1111/j.1439-0310.20...
; Ala-Honkola et al., 2009Ala-Honkola, O., Uddström, A., Pauli, B.D., & Lindström, K., 2009. Strong inbreeding depression in male mating behaviour in a poeciliid fish. J. Evol. Biol. 22(7), 1396-1406. PMid:19486236. http://dx.doi.org/10.1111/j.1420-9101.2009.01765.x.
http://dx.doi.org/10.1111/j.1420-9101.20...
; Fitzpatrick & Evans, 2009Fitzpatrick, J.L., & Evans, J.P., 2009. Reduced heterozygosity impairs sperm quality in endangered mammals. Biol. Lett. 5(3), 320-323. PMid:19324650. http://dx.doi.org/10.1098/rsbl.2008.0734.
http://dx.doi.org/10.1098/rsbl.2008.0734...
; Losdat et al., 2014Losdat, S., Chang, S.M., & Reid, J.M., 2014. Inbreeding depression in male gametic performance. J. Evol. Biol. 27(6), 992-1011. PMid:24820115. http://dx.doi.org/10.1111/jeb.12403.
http://dx.doi.org/10.1111/jeb.12403...
).
The primary goal of this study was to characterize the reproductive biology of this naturally isolated population of P. aff. fasciatus, describing traits such as sex ratio, reproductive activity, sexual maturity, and length-weight ratio, and to determine if isolation could be associated with differences in reproductive tactics and possibly inbreeding (Kerniske et al., 2021Kerniske, F.F., Pena Castro, J., De la Ossa-Guerra, L.E., Mayer, B.A., Abilhoa, V., Paiva-Affonso, I., & Artoni, R.F., 2021. Spinal malformations in a naturally isolated Neotropical fish population. PeerJ 9, e12239. PMid:34721968. http://dx.doi.org/10.7717/peerj.12239.
http://dx.doi.org/10.7717/peerj.12239...
).
2. Material and Methods
2.1. Study area
This research followed the international standards of animal experimentation, approved by the Ethics Committee for Animal Use of the Universidade Tecnológica Federal do Paraná (CEUA process N °. 2018-025/2018). The collection was authorized by the Ministério do Meio Ambiente (MMA/ICMbio nº 15115-1) and the Instituto Ambiental do Paraná (IAP nº 15.190.528-5; authorization 15.18).
Specimens of P. aff. fasciatus were collected in the Furna 2 of Vila Velha State Park (VVSP), a protected area located in the upper Tibagi River basin, Ponta Grossa, southern Brazil, at coordinates 25º 15'01 53” S and 50º 00'19 38” E (Figure 1). Precipitation and air temperature data for the time period were obtained from SIMEPAR (Sistema Meteorológico do Paraná; http://www.simepar.br/).
2.2. Sampling methods and data analysis
Except for March 2019, sampling was done monthly using seine nets between February 2019 and January 2020. Specimens of P. aff. fasciatus were transported to the UTFPR's Laboratório de Ecologia Aquática, where they were anaesthetised with benzocaine (0.1 g/L) and sacrificed. The presence (male) or absence (female) of bony hooks on the pelvic fin was used to determine sex (Porto-Foresti et al., 2005Porto-Foresti, F., Castilho-Almeida, R.B., & Foresti, F., 2005. Biologia e criação do lambari-do-rabo-amarelo (Astyanax altiparanae). In: Baldisserotto, B., & Gomes, L.C., eds. Espécies nativas para piscicultura. Santa Maria: Editora UFMS, 468 p.), which was later confirmed by histological analysis of the gonads.
Each captured individual's standard length (SL) and total weight (TW) were measured in the laboratory to the nearest 0.1 cm and 1 g, respectively. Fresh gonads were removed, and sex and maturity were determined macroscopically based on gonad size, color, vascularity, and the presence of lateral spermathecae or oocytes. Following macroscopic classification, gonads were fixed in Bouin's solution for 48 hours before being stored in 70% ethanol for histological preparation (Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.; Bazzoli, 2003Bazzoli, N., 2003. Parâmetros reprodutivos de peixes de interesse comercial na região de Pirapora. In: Godinho, H.P., & Godinho, A.L., eds. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas, 291-306.). Microscopically, histological sections from 69 males and 26 females were examined and classified into five developmental stages: Regenerating (I), Developing (II), Spawning Capable 1 (III), Spawning Capable 2 (IV), and Regressing (V), as adapted from Brown-Peterson et al. (2011)Brown-Peterson, N.J., Wyanski, D.M., Saborido-Rey, F., MacEwicz, B.J., & Lowerre-Barbieri, S.K., 2011. A standardized terminology for describing reproductive development in fishes. Mar. Coast. Fish. 3(1), 52-70. http://dx.doi.org/10.1080/19425120.2011.555724.
http://dx.doi.org/10.1080/19425120.2011....
.
For the entire study population, the total length at maturity (L50, the length in which 50% of individuals were mature; and L95, the length in which most of the individuals reached sexual maturity) was estimated. The L50 and L95 analysis took into account sexually mature individuals (adults). The logistic regression model shown below was used: PM = 1[11+e(a+𝛽L)]-1, where PM denotes the proportion of mature individuals in length class L, a denotes a constant, and L50 = -a𝛽-1. Binary maturity observations (0=immature, 1=mature) and total length were fitted to binary logistic models (logit function) to construct maturity ogives (maturity-at-length probability plots) based on logistic regression to predict the probability that an individual was mature at a given length (Hazelton, 2007Hazelton, M.L., 2007. Bias reduction in kernel binary regression. Comput. Stat. Data Anal. 51(9), 4393-4402. http://dx.doi.org/10.1016/j.csda.2006.06.012.
http://dx.doi.org/10.1016/j.csda.2006.06...
). The 95% confidence interval was estimated using a bootstrap method with 1000 interactions. The R package was used for statistical procedures (R Core Team, 2019R Core Team, 2019. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved in 2022, November 16, from https://www.R-project.org/
https://www.R-project.org/...
).
The reproductive season was determined by the relative frequency of reproductive stages, and the sex ratio was calculated for each month, with the 𝜒2 test determining significant differences (df = 1; p = 0.05; 𝜒2 < 3.84). To compare the sex ratio, we employed the Bayesian approach, estimating the proportion of females in comparison to external populations by applying a conjugate beta-binomial statistical model. Within this model, we established an uninformative beta distribution (1,1) as the prior, signifying the absence of prior knowledge about the female proportion within the population. The posterior distribution was then modeled using the beta distribution (f + 1, n - f + 1), where “f” denotes the number of observed females and “n” represents the total sample size, encompassing both females and males. Statistical inferences concerning the female proportion were subsequently derived from the resulting posterior beta distribution (Gelman et al., 2013Gelman, A., Carlin, J.B., Stern, H.S., Dunson, D.B., Vehtari, A., & Rubin, D.B., 2013. Bayesian data analysis (3rd ed.). New York: Chapman and Hall/CRC. http://dx.doi.org/10.1201/b16018.
http://dx.doi.org/10.1201/b16018...
).
The length-weight ratios were calculated using the least-squares fit to log-transformed data function: WT = aLTb, where WT is the total weight, LT is the total length, a is a body shape coefficient, and b is an exponent indicating isometric growth when equal to 3 (Le Cren, 1951Le Cren, E.D., 1951. The length-weight relationship and seasonal cycle in gonadal weight condition in the perch Perca fluviatilis. J. Anim. Ecol. 20(2), 201-219. http://dx.doi.org/10.2307/1540.
http://dx.doi.org/10.2307/1540...
; Lima-Junior et al., 2002Lima-Junior, S.E., Cardone, I.B., & Goitein, R., 2002. Determination of a method for calculation of allometric condition factor of fish. Acta Scientiarum 24(2), 397-400. https://doi.org/10.4025/actascibiolsci.v24i0.2311.
https://doi.org/10.4025/actascibiolsci.v...
). The mean value of the relative condition factor (Kn), which is the quotient of the observed weight and the theoretically expected weight for a given length (Kn=Wt/We), was then estimated (Le Cren, 1951Le Cren, E.D., 1951. The length-weight relationship and seasonal cycle in gonadal weight condition in the perch Perca fluviatilis. J. Anim. Ecol. 20(2), 201-219. http://dx.doi.org/10.2307/1540.
http://dx.doi.org/10.2307/1540...
). Using the Student's t-test (p < 0.05), the values obtained for males and females were statistically compared with the standard Kn = 1.00.
3. Results
A total of 254 P. aff. fasciatus individuals were collected and analyzed, with the presence of males (N=154; 60.6%) and females (N=100; 39.4%). During the sampling period, the average temperature values were highest from October to March (spring-summer), the months from June to October (winter) were the driest of the year, and the month of May (autumn) had the highest precipitation index.
The stages of gonadal development in females and males were identified (Figure 2), and the relative frequency in relation to the months of the year was calculated (Figure 3). Histological examination of reproductively active ovaries revealed the presence of oocytes at various stages of maturation at the same time, indicating multiple spawning patterns. Individuals in the capable of spawning 1 stage (III) were recorded between September 2019 and February 2020, implying that spawning activity peaks occur between spring and summer. In June 2019, females capable of spawning capable 2 stage (IV), with partially empty gonads, post-ovulatory follicles, and regressing (V) were observed. In July, the total number of individuals collected was represented by regenerating females (I).
Histological sections of ovaries (A) and testes (B) of P. aff. fasciatus. (A) I - Regenerating stage containing early and advanced perinuclear oocytes with basophilic cytoplasm and several nucleoli in the nucleus (highlighted), II - Developing stage besides perinuclear oocytes presents pre-vitellogenic oocytes with characteristic cortical alveoli (highlighted - arrow), III - Spawning Capable 1stage predominantly vitellogenic oocytes filled with yolk granules, IV - Spawning Capable 2 stage with oocytes in all growth stages and also post-ovulatory follicles (highlighted - arrow), V - Regressing stage containing perinuclear oocytes, post-ovulatory follicle and atresic oocyte (highlighted); (B) Testes of P. aff. fasciatus stained with HE. I - Regenerating stage organized in cysts containing spermatogonia in the seminiferous tubule and occluded lumen, II - Developing stage with presence of spermatozoa in small proportion within the lumen and spermatogenic cell cysts in the seminiferous tubule, III - Spawning Capable 1 stage exhibiting lumen filled with sperm embedded in acidophilic secretion and some spermatogenic cell cysts, IV - Spawning Capable 2 stage containing few sperm,V - Regressing stage with only residual sperm. Arrow = spermatogonia, * = spermatozoa.
Relative frequency distribution of gonadal maturation stages for females (A) and males (B) of the naturally isolated population of P. aff. fasciatus collected between Feb/2019 - Jan/2020 in Furna 2 (n=95). Monthly average of air temperature and precipitation for the city of Ponta Grossa from 02/2019 to 01/2020.
Males, on the other hand, had spermatozoa-filled testes throughout the sampling period, but the frequency of stage (III) increased in October (spring) and decreased in June (winter). In September, individuals in stage (V) were more frequently observed, with gonads containing only residual spermatozoa.
Females had an L50 of 5.59 cm, and all females over 6.81 cm LT were mature (L95). L50 was estimated to be 5.47 cm for males, and all males > 6.73 cm LT were mature (L95). L50 and L95 were estimated to be 5.56 and 6.64 cm LT for the entire population, respectively (Figure 4).
Length at maturity (L50 and L95) with fitted logistic regression model of males, females and the entire study population of the naturally-isolated population of P. aff. fasciatus captured.between February/2019 and January/2020 in Furna 2.
The overall monthly sex ratio differed significantly (χ2 = 21.885, p = 0.025). Females outnumbered males in July 2019 (χ2 = 8.00, p = 0.01), but males outnumbered females in August 2019 (χ2 = 6.4, p = 0.04) (Figure 5A). Beta-Binomial modeling of sex ratio data revealed that the proportion of females in the naturally isolated population of P. aff. fasciatus was lower than estimates reported in the literature (Figure 5B).
(A) Relative frequency distribution of males and females of P. aff fasciatus collected in Furna 2 of the VVSP in the period 2019-2020; (B) Posterior distribution of the proportion of females in the naturally-isolated population of P. aff. fasciatus, estimated through the Beta-binomial model using the overall sex ratio captured between February/2019 and January/2020 collected in Furna 2 of VVSP compared with the estimates from the literature (Carvalho et al., 2009Carvalho, P.A., Paschoalini, A.L., Santos, G.B., Rizzo, E., & Bazzoli, N., 2009. Reproductive biology of Astyanax fasciatus (Pisces: Characiformes) in a reservoir in southeastern Brazil. J. Appl. Ichthyology 25(3), 306-313. http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x.
http://dx.doi.org/10.1111/j.1439-0426.20... ; Silveira et al., 2020Silveira, E.L., Aranha, J.M.R., Menezes, M.S., & Vaz-Dos Santos, A.M., 2020. Reproductive dynamics, age and growth of Astyanax aff. fasciatus in a Neotropical basin. Mar. Freshw. Res. 71(6), 670-683. http://dx.doi.org/10.1071/MF19100.
http://dx.doi.org/10.1071/MF19100... ).
The weight-length relationship was estimated for all individuals grouped, and the equation obtained was WT = 0.0002 * LT2.3039, indicating that the parameter b of 2.3. Also, the weight-length relationship was estimated for females (b = 2.3) and males (b = 2.2) indicating negative allometric growth (b < 3); it means more energy expenditure in length than in mass. There was no statistically significant difference in body condition between genders (Figure 6), with both presenting an average value of Kn = 0.95.
Individual values for the relative condition factor (Kn) considering the standard value (Kn=1.0) in males (M) and females (F).
4. Discussion
Except for the sex ratio, which seems unbalanced and unexpectedly favorable to males, the general pattern observed in this study of the reproductive period and sexual maturity of a naturally isolated population of P. aff. fasciatus from southern Brazil is similar to others small characins (e.g., Hojo et al., 2004Hojo, R.E.S., Santos, G.B., & Bazzoli, N., 2004. Reproductive biology of Moenkhausia intermedia (Eigenmann) (Pisces, Characiformes) in Itumbiara Reservoir, Goiás, Brazil. Rev. Bras. Zool. 21(3), 519-524. http://dx.doi.org/10.1590/S0101-81752004000300015.
http://dx.doi.org/10.1590/S0101-81752004...
; Carvalho et al., 2009Carvalho, P.A., Paschoalini, A.L., Santos, G.B., Rizzo, E., & Bazzoli, N., 2009. Reproductive biology of Astyanax fasciatus (Pisces: Characiformes) in a reservoir in southeastern Brazil. J. Appl. Ichthyology 25(3), 306-313. http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x.
http://dx.doi.org/10.1111/j.1439-0426.20...
; Portella et al., 2021Portella, A.C., Arsentales, A.D., Cavallari, D.E., & Welber, S.S., 2021. Effect of seasonality on the reproduction of characiformes fish in a neotropical river. Iheringia Ser. Zool. 111, e2021012. http://dx.doi.org/10.1590/1678-4766e2021012.
http://dx.doi.org/10.1590/1678-4766e2021...
). This species can spawn throughout the year, with peak spawning activity in spring and summer, with an increase in air temperature associated with precipitation, as evidenced by numerous studies (Baroiller et al., 2009Baroiller, J.F., D’Cotta, H., & Saillant, E., 2009. Environmental Effects on Fish Sex Determination and Differentiation. Sex Dev. 3(2-3), 118-135. PMid:19684457. http://dx.doi.org/10.1159/000223077.
http://dx.doi.org/10.1159/000223077...
; Bartolini et al., 2015Bartolini, T., Butail, S., & Porfiri, M., 2015. Temperature influences sociality and activity of freshwater fish. Environ. Biol. Fishes 98(3), 825-832. http://dx.doi.org/10.1007/s10641-014-0318-8.
http://dx.doi.org/10.1007/s10641-014-031...
; Firkus et al., 2018Firkus, T., Rahel, F.J., Bergman, H.L., & Cherrington, B.D., 2018. Warmed winter water temperatures alter reproduction in two fish species. Environ. Manage. 61(2), 291-303. PMid:29124337. http://dx.doi.org/10.1007/s00267-017-0954-9.
http://dx.doi.org/10.1007/s00267-017-095...
; Quirino et al., 2021Quirino, P.P., Siqueira-Silva, D.H., Silva Rodrigues, M., Santos-Silva, A.P., Delgado, M.L.R., Senhorini, J.A., & Veríssimo-Silveira, R., 2021. Gonadal morphology and difference in reproductive development of two isolated populations of Astyanax rivularis (Teleostei, Characidae). J. Fish Biol. 99(5), 1719-1728. PMid:34392530. http://dx.doi.org/10.1111/jfb.14879.
http://dx.doi.org/10.1111/jfb.14879...
). This characin's reproductive characteristics indicate an opportunistic (r) strategy, which is common in small-sized species, particularly Characiformes, with no or little parental care and a long reproductive period (Winemiller, 1989Winemiller, K.O., 1989. Patterns of variation in life history among South American fishes in seasonal environmentals. Oecologia 81(2), 225-241. PMid:28312542. http://dx.doi.org/10.1007/BF00379810.
http://dx.doi.org/10.1007/BF00379810...
; Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.; Quirino et al., 2021Quirino, P.P., Siqueira-Silva, D.H., Silva Rodrigues, M., Santos-Silva, A.P., Delgado, M.L.R., Senhorini, J.A., & Veríssimo-Silveira, R., 2021. Gonadal morphology and difference in reproductive development of two isolated populations of Astyanax rivularis (Teleostei, Characidae). J. Fish Biol. 99(5), 1719-1728. PMid:34392530. http://dx.doi.org/10.1111/jfb.14879.
http://dx.doi.org/10.1111/jfb.14879...
).
Growth was negatively allometric (b = 2.3), which means that more energy was expended on length than on weight. This could be due to inbreeding, as body weight is affected in inbred individuals (Fessehaye et al., 2007Fessehaye, Y., Komen, H., Rezk, M.A., Van Arendonk, J.A.M., & Bovenhuis, H., 2007. Effects of inbreeding on survival, body weight and fluctuating asymmetry (FA) in Nile tilapia, Oreochromis niloticus. Aquaculture 264(1-4), 27-35. http://dx.doi.org/10.1016/j.aquaculture.2006.12.038.
http://dx.doi.org/10.1016/j.aquaculture....
). Beyond that, the maximum observed total length was 9.2 cm, which is less than that reported for the species (13.2 cm) (Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.). Despite their smaller sizes, females had the highest values recorded, which could be related to fecundity, because the size of the peritoneal cavity allows for a greater or lesser number of oocytes (Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.; Araújo et al., 2019Araújo, F.G., Nascimento, A.A., Gomes, I.D., Sales, A., & Oliveira, B.A.C., 2019. Gonadal development and reproductive period of the characin Astyanax aff. bimaculatus (Characiformes: Characidae) in a tropical reservoir in southeastern Brazil. Zoologia 36, 1-14. http://dx.doi.org/10.3897/zoologia.36.e30610.
http://dx.doi.org/10.3897/zoologia.36.e3...
). Studies with Characiformes suggest that detrimental effects on Kn may reflect seasonal changes or even be a consequence of parasitism (Gomiero et al., 2012Gomiero, L.M., Souza, U.P., & Braga, F.M.S., 2012. Condition factor of Astyanax intermedius Eigenmann, 1908 (Osteichthyes, Characidae) parasitised by Paracymothoa astyanaxi Lemos de Castro, 1955 (Crustacea, Cymothoidae) in the Grande River, Serra do Mar State Park - Santa Virgínia Unit, São Paulo, Brazil. Braz. J. Biol. 72(2), 379-388. PMid:22735147. http://dx.doi.org/10.1590/S1519-69842012000200020.
http://dx.doi.org/10.1590/S1519-69842012...
; Ito, 2013Ito, K. M., 2013. Histopatologia de brânquia e fator de condição de Astyanax aff. paranae (PISCES) como indicadores de contaminação aquática no centro-noroeste do Paraná [Trabalho de Conclusão de Curso em Engenharia Ambiental]. Campo Mourão: Universidade Tecnológica Federal do Paraná.; Antunes et al., 2022Antunes, D.F., Silva, B.A.F., & Yamada, F.H., 2022. Effect of parasitism on the relative condition factor of Astyanax bimaculatus (Characiformes: Characidae) a freshwater fish from Caatinga domain, Brazil. Int. J. Aquat. Biol. 10(5), 370-377. https://doi.org/10.22034/ijab.v10i5.1560.
https://doi.org/10.22034/ijab.v10i5.1560...
). Nonetheless, the mean value of Kn = 0.95 was not significant in our study, both individually and when the genders were combined, indicating that these lambaris have a high body condition. This could be due to the intra and interspecific isolation of this population (Shibatta & Artoni, 2005Shibatta, O.A., & Artoni, R.F., 2005. Sobre a identidade das populações alopátricas de Astyanax (Characiformes, Characidae) das formações Furna 1 e Furna 2 do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Publ. UEPG Biol. Health Sci. 11(2), 7-12. https://doi.org/10.5212/publicatio%20uepg.v11i2.410.
https://doi.org/10.5212/publicatio%20uep...
; Artoni et al., 2006Artoni, R.F., Shibatta, O.A., Gross, M.C., Schneider, C.H., Almeida, M.C., Vicari, M.R., & Bertollo, L.A.C., 2006. Astyanax aff. fasciatus Cuvier, 1819 (Teleostei; Characidae): evidences of a species complex in the upper rio Tibagi Basin (Paraná, Brazil). Neotrop. Ichthyol. 4(2), 197-202. http://dx.doi.org/10.1590/S1679-62252006000200005.
http://dx.doi.org/10.1590/S1679-62252006...
; Matoso et al., 2013Matoso, D.A., Silva, M., Artoni, R.F., & Torres, R.A., 2013. Molecular taxonomy and evolutionary hypothesis concerning Astyanax fasciatus (Characiformes, Characidae) from Vila Velha State Park and Tibagi and Iguaçu Rivers. Genet. Mol. Res. 12(1), 631-638. PMid:23546944. http://dx.doi.org/10.4238/2013.March.7.1.
http://dx.doi.org/10.4238/2013.March.7.1...
), which reflects the lack of competition among different species, and, as a result, the abundance of available food in Furna 2 (Mayer et al., in preparation).
The standard length at which 50% of the population reached maturity (L50=5.56 cm SL) was 60.3% of the maximum recorded length (9.22 cm). The length at first maturity was estimated to be 5.47 cm for males and 5.59 cm for females, which is lower than the values reported by Carvalho et al. (2009)Carvalho, P.A., Paschoalini, A.L., Santos, G.B., Rizzo, E., & Bazzoli, N., 2009. Reproductive biology of Astyanax fasciatus (Pisces: Characiformes) in a reservoir in southeastern Brazil. J. Appl. Ichthyology 25(3), 306-313. http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x.
http://dx.doi.org/10.1111/j.1439-0426.20...
, who reported 6.4 and 6.5 cm for males and females, respectively, and Prado et al. (2011)Prado, P.S., Souza, C.C., Bazzoli, N., & Rizzo, E., 2011. Reproductive disruption in lambari Astyanax fasciatus from a Southeastern Brazilian reservoir. Ecotoxicol. Environ. Saf. 74(7), 1879-1887. PMid:21831433. http://dx.doi.org/10.1016/j.ecoenv.2011.07.017.
http://dx.doi.org/10.1016/j.ecoenv.2011....
, who reported a total length at maturity of 8.8 cm. According to our findings, the naturally isolated population of P. aff. fasciatus reaches sexual maturity at smaller sizes, which is typical of fast-growing fish (Winemiller, 1989Winemiller, K.O., 1989. Patterns of variation in life history among South American fishes in seasonal environmentals. Oecologia 81(2), 225-241. PMid:28312542. http://dx.doi.org/10.1007/BF00379810.
http://dx.doi.org/10.1007/BF00379810...
).
One of the most important indicators for understanding fish population dynamics is the sex ratio. In natural populations, the number of males is expected to be statistically equal to the number of females (1:1) (Nikolsky, 1969Nikolsky, G.V., 1969. Theory of fish population dynamics. Edinburgh: Oliver and Boyd, 323 p.; Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.). Deviations in the ratio, on the other hand, are relatively common in fish populations and can be caused by factors that affect the genders differently, such as reproductive behavior, birth rates, mortality, and growth rates (Vazzoler, 1996Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.; Araújo et al., 2019Araújo, F.G., Nascimento, A.A., Gomes, I.D., Sales, A., & Oliveira, B.A.C., 2019. Gonadal development and reproductive period of the characin Astyanax aff. bimaculatus (Characiformes: Characidae) in a tropical reservoir in southeastern Brazil. Zoologia 36, 1-14. http://dx.doi.org/10.3897/zoologia.36.e30610.
http://dx.doi.org/10.3897/zoologia.36.e3...
). It is important to note that a skewed sex ratio towards one of the genders reduces effective population size and leads to genetic diversity loss (Zajitschek et al., 2009Zajitschek, S.R.K., Lindholm, A.K., Evans, J.P., & Brooks, R.C., 2009. Experimental evidence that high levels of inbreeding depress sperm competitiveness. J. Evol. Biol. 22(6), 1338-1345. PMid:19344380. http://dx.doi.org/10.1111/j.1420-9101.2009.01738.x.
http://dx.doi.org/10.1111/j.1420-9101.20...
). The higher the number of males in inbred populations, the lower the reproductive success, because the effects of inbreeding are exacerbated when males compete with each other (Fessehaye et al., 2009Fessehaye, Y., Bovenhuis, H., Rezk, M.A., Crooijmans, R., Van Arendonk, J.A.M., & Komen, H., 2009. Effects of relatedness and inbreeding on reproductive success of Nile tilapia (Oreochromis niloticus). Aquaculture 294(3-4), 180-186. http://dx.doi.org/10.1016/j.aquaculture.2009.06.001.
http://dx.doi.org/10.1016/j.aquaculture....
).
Psalidodon aff. fasciatus from Furna 2 showed a male predominance, which contrasts with the typical P. aff. fasciatus female predominance (Carvalho et al., 2009Carvalho, P.A., Paschoalini, A.L., Santos, G.B., Rizzo, E., & Bazzoli, N., 2009. Reproductive biology of Astyanax fasciatus (Pisces: Characiformes) in a reservoir in southeastern Brazil. J. Appl. Ichthyology 25(3), 306-313. http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x.
http://dx.doi.org/10.1111/j.1439-0426.20...
; Silva et al., 2010Silva, J.P.A., Muelbert, A.E., Oliveira, E.C., & Fávaro, L.F., 2010. Reproductive tactics used by the lambari Astyanax fasciatus in three water supply reservoirs in the same geographic region of the upper Iguacu River. Neotrop. Ichthyol. 8(4), 885-892. http://dx.doi.org/10.1590/S1679-62252010000400019.
http://dx.doi.org/10.1590/S1679-62252010...
; Hirt et al., 2011Hirt, L.M., Araya, P.R., & Flores, S.A., 2011. Population structure, reproductive biology and feeding of Astyanax fasciatus (Cuvier, 1819) in an Upper Paraná River tributary, Misiones, Argentina. Acta Limnol. Bras. 23(1), 1-12. http://dx.doi.org/10.4322/actalb.2011.013.
http://dx.doi.org/10.4322/actalb.2011.01...
; Silveira et al., 2020Silveira, E.L., Aranha, J.M.R., Menezes, M.S., & Vaz-Dos Santos, A.M., 2020. Reproductive dynamics, age and growth of Astyanax aff. fasciatus in a Neotropical basin. Mar. Freshw. Res. 71(6), 670-683. http://dx.doi.org/10.1071/MF19100.
http://dx.doi.org/10.1071/MF19100...
), with an exception of Gurgel (2004)Gurgel, H.C.B., 2004. Estrutura populacional e época de reprodução de Astyanax fasciatus (Cuvier) (Characidae, Tetragonopterinae) do Rio Ceará Mirim, Poço Branco, Rio Grande do Norte, Brasil. Rev. Bras. Zool. 21(1), 131-135. http://dx.doi.org/10.1590/S0101-81752004000100022.
http://dx.doi.org/10.1590/S0101-81752004...
who also found a male predominance in a possible oligotrophic environment in the Ceará-Mirim river. The higher number of males found in freshwater fish populations has been linked to oligotrophic environments (Nikolsky, 1969Nikolsky, G.V., 1969. Theory of fish population dynamics. Edinburgh: Oliver and Boyd, 323 p.; Gurgel, 2004Gurgel, H.C.B., 2004. Estrutura populacional e época de reprodução de Astyanax fasciatus (Cuvier) (Characidae, Tetragonopterinae) do Rio Ceará Mirim, Poço Branco, Rio Grande do Norte, Brasil. Rev. Bras. Zool. 21(1), 131-135. http://dx.doi.org/10.1590/S0101-81752004000100022.
http://dx.doi.org/10.1590/S0101-81752004...
), which differs from that found in Furna 2 because the environment is stable and the food resource is abundant. On the other hand, reproductive behavior may have an influence that could explain the higher proportion of males during the reproductive peak, since this is a tactic employed by species with external fertilization related to female fecundity, so the higher proportion of males would increase the number of fertilized oocytes (Veregue & Orsi, 2003Veregue, A.M.L., & Orsi, M.L., 2003. Reproductive biology of Astyanax scabripinnis paranae (Eigenmann) (Ostheichthyes, Characidae) from Marrecas creek of the Tibagi basin, Paraná. Rev. Bras. Zool. 20(1), 97-105. http://dx.doi.org/10.1590/S0101-81752003000100012.
http://dx.doi.org/10.1590/S0101-81752003...
). But, the sex ratio in all samples cannot be fully explained by the previously stated possible causes, leading us to suspect that other factors may act differently on the genders. These may include inbreeding issues, as male and female survival may be affected differently by inbreeding depression (Lacy et al., 1993Lacy, R.C., Petric, A., & Warneke, M., 1993. Inbreeding and outbreeding in captive populations of wild animals. In: Thornhill, N.W., ed. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. Chicago: University of Chicago Press, 352-374.). Similarly, Kerniske et al. (2021)Kerniske, F.F., Pena Castro, J., De la Ossa-Guerra, L.E., Mayer, B.A., Abilhoa, V., Paiva-Affonso, I., & Artoni, R.F., 2021. Spinal malformations in a naturally isolated Neotropical fish population. PeerJ 9, e12239. PMid:34721968. http://dx.doi.org/10.7717/peerj.12239.
http://dx.doi.org/10.7717/peerj.12239...
discovered spinal malformations in females of this population, with inbreeding as a possible cause. For instance, in an inbred tilapia population, deleterious genes were also linked to a sex ratio imbalance, which resulted in higher female lethality (Shirak et al., 2002Shirak, A., Palti, Y., Cnaani, A., Korol, A., Hulata, G., Ron, M., & Avtalion, R.R., 2002. Association Between Loci With Deleterious Alleles and Distorted Sex Ratios in an Inbred Line of Tilapia (Oreochromis aureus). J. Hered. 93(4), 270-276. PMid:12407213. http://dx.doi.org/10.1093/jhered/93.4.270.
http://dx.doi.org/10.1093/jhered/93.4.27...
).
Concluding, this study provides the first information on the reproductive biology of these lambaris discovered in Vila Velha State Park, Paraná's Furna 2. The gonadal development followed the biology of the species, according to the study, and the opportunistic strategy is also common in other small characids, in addition to the expected plasticity of reproductive tactics. However, our findings suggest a sex ratio imbalance that favors males. In an additional way, because this is a small population possibly with limited gene flow, in which the loss of genetic diversity has already been previously reported (Matoso et al., 2004Matoso, D.A., Artoni, R.F., & Galleti, P.M., 2004. Genetic Diversity of the Small Characid Fish Astyanax sp., and its significance for conservation. Hydrobiologia 527(1), 223-225. http://dx.doi.org/10.1023/B:HYDR.0000043303.02986.71.
http://dx.doi.org/10.1023/B:HYDR.0000043...
; Matoso et al., 2010Matoso, D.A., Martins, C., Artoni, R.F., & Galetti Junior, P.M., 2010. Preliminary qualitative analysis on mtDNA in Astyanax fasciatus populations Cuvier, 1819 (Teleostei; Characidae) indicate population distinctiveness. Braz. Arch. Biol. Technol. 53(3), 663-667. http://dx.doi.org/10.1590/S1516-89132010000300022.
http://dx.doi.org/10.1590/S1516-89132010...
), the effects of inbreeding may be amplified, resembling a scenario involving critically endangered individuals.
Acknowledgements
We thank Fabio André dos Santos for laboratory support and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) for the F.F.K and L.E.D.G. grants. We also thank the sampling team that helped us obtain the data.
-
Cite as: Kerniske, F.F. et al. Reproductive aspects of an isolated population of Psalidodon aff. fasciatus (Teleostei: Characidae) from southern Brazil. Acta Limnologica Brasiliensia, 2023, vol. 35, e24.
References
- Abilhoa, V., 2007. Aspectos da história natural de Astyanax scabripinnis Jenyns (Teleostei, Characidae) em um riacho de floresta com araucária no sul do Brasil. Rev. Bras. Zool. 24(4), 997-1005. http://dx.doi.org/10.1590/S0101-81752007000400016
» http://dx.doi.org/10.1590/S0101-81752007000400016 - Ala-Honkola, O., Uddström, A., Pauli, B.D., & Lindström, K., 2009. Strong inbreeding depression in male mating behaviour in a poeciliid fish. J. Evol. Biol. 22(7), 1396-1406. PMid:19486236. http://dx.doi.org/10.1111/j.1420-9101.2009.01765.x
» http://dx.doi.org/10.1111/j.1420-9101.2009.01765.x - Albert, J., Albert, J.S., & Reis, R.E., 2012. Historical biogeography of neotropical freshwater fishes. Berkeley: University of California Press. http://dx.doi.org/10.1525/california/9780520268685.001.0001
» http://dx.doi.org/10.1525/california/9780520268685.001.0001 - Albert, J.S., Tagliacollo, V.A., & Dagosta, F., 2020. Diversification of neotropical freshwater fishes. Annu. Rev. Ecol. Evol. Syst. 51(1), 27-53. http://dx.doi.org/10.1146/annurev-ecolsys-011620-031032
» http://dx.doi.org/10.1146/annurev-ecolsys-011620-031032 - Antonelli, A., Ariza, M., Albert, J., Andermann, T., Azevedo, J., Bacon, C., Faurby, S., Guedes, T., Hoorn, C., Lohmann, L.G., Matos-Maraví, P., Ritter, C.D., Sanmartín, I., Silvestro, D., Tejedor, M., ter Steege, H., Tuomisto, H., Werneck, F.P., Zizka, A., & Edwards, S.V., 2018. Conceptual and empirical advances in Neotropical biodiversity research. PeerJ 6, e5644. PMid:30310740. http://dx.doi.org/10.7717/peerj.5644
» http://dx.doi.org/10.7717/peerj.5644 - Antunes, D.F., Silva, B.A.F., & Yamada, F.H., 2022. Effect of parasitism on the relative condition factor of Astyanax bimaculatus (Characiformes: Characidae) a freshwater fish from Caatinga domain, Brazil. Int. J. Aquat. Biol. 10(5), 370-377. https://doi.org/10.22034/ijab.v10i5.1560
» https://doi.org/10.22034/ijab.v10i5.1560 - Araújo, F.G., Nascimento, A.A., Gomes, I.D., Sales, A., & Oliveira, B.A.C., 2019. Gonadal development and reproductive period of the characin Astyanax aff. bimaculatus (Characiformes: Characidae) in a tropical reservoir in southeastern Brazil. Zoologia 36, 1-14. http://dx.doi.org/10.3897/zoologia.36.e30610
» http://dx.doi.org/10.3897/zoologia.36.e30610 - Artoni, R.F., Shibatta, O.A., Gross, M.C., Schneider, C.H., Almeida, M.C., Vicari, M.R., & Bertollo, L.A.C., 2006. Astyanax aff. fasciatus Cuvier, 1819 (Teleostei; Characidae): evidences of a species complex in the upper rio Tibagi Basin (Paraná, Brazil). Neotrop. Ichthyol. 4(2), 197-202. http://dx.doi.org/10.1590/S1679-62252006000200005
» http://dx.doi.org/10.1590/S1679-62252006000200005 - Azevedo, M.A., 2010. Reproductive characteristics of characid fish species (Teleostei, Characiformes) and their relationship with body size and phylogeny. Iheringia Ser. Zool. 100(4), 469-482. http://dx.doi.org/10.1590/S0073-47212010000400020
» http://dx.doi.org/10.1590/S0073-47212010000400020 - Baroiller, J.F., D’Cotta, H., & Saillant, E., 2009. Environmental Effects on Fish Sex Determination and Differentiation. Sex Dev. 3(2-3), 118-135. PMid:19684457. http://dx.doi.org/10.1159/000223077
» http://dx.doi.org/10.1159/000223077 - Bartolini, T., Butail, S., & Porfiri, M., 2015. Temperature influences sociality and activity of freshwater fish. Environ. Biol. Fishes 98(3), 825-832. http://dx.doi.org/10.1007/s10641-014-0318-8
» http://dx.doi.org/10.1007/s10641-014-0318-8 - Baumgartner, G., Pavanelli, C.S., Baumgartner, D., Bifi, A.G., Debona, T., & Frana, V.A., 2012. Peixes do baixo rio Iguaçu. Maringá: Eduem, 203 p. http://dx.doi.org/10.7476/9788576285861
» http://dx.doi.org/10.7476/9788576285861 - Baumgartner, M.T., Rogério, P., Da Silva, L., & Baumgartner, G., 2016. Population structure and reproductive biology of Astyanax gymnodontus (Characiformes: Characidae), a poorly known endemic fish of the Iguaçu River basin, Brazil. Rev. Biol. Trop. 64(1), 69-77. PMid:28862403. http://dx.doi.org/10.15517/rbt.v64i1.18100
» http://dx.doi.org/10.15517/rbt.v64i1.18100 - Bazzoli, N., 2003. Parâmetros reprodutivos de peixes de interesse comercial na região de Pirapora. In: Godinho, H.P., & Godinho, A.L., eds. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas, 291-306.
- Brown-Peterson, N.J., Wyanski, D.M., Saborido-Rey, F., MacEwicz, B.J., & Lowerre-Barbieri, S.K., 2011. A standardized terminology for describing reproductive development in fishes. Mar. Coast. Fish. 3(1), 52-70. http://dx.doi.org/10.1080/19425120.2011.555724
» http://dx.doi.org/10.1080/19425120.2011.555724 - Campos, J.B., & Dalcomune, M.A., 2011. O Parque Estadual de Vila Velha. In: Carpanezi, O.T.B., & Campos, J.B., eds. Coletânea de pesquisas: Parques Estaduais de Vila Velha, Cerrado e Guartelá. Curitiba: Instituto Ambiental do Paraná, 66-79.
- Carvalho, P.A., Paschoalini, A.L., Santos, G.B., Rizzo, E., & Bazzoli, N., 2009. Reproductive biology of Astyanax fasciatus (Pisces: Characiformes) in a reservoir in southeastern Brazil. J. Appl. Ichthyology 25(3), 306-313. http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x
» http://dx.doi.org/10.1111/j.1439-0426.2009.01238.x - Fessehaye, Y., Bovenhuis, H., Rezk, M.A., Crooijmans, R., Van Arendonk, J.A.M., & Komen, H., 2009. Effects of relatedness and inbreeding on reproductive success of Nile tilapia (Oreochromis niloticus). Aquaculture 294(3-4), 180-186. http://dx.doi.org/10.1016/j.aquaculture.2009.06.001
» http://dx.doi.org/10.1016/j.aquaculture.2009.06.001 - Fessehaye, Y., Komen, H., Rezk, M.A., Van Arendonk, J.A.M., & Bovenhuis, H., 2007. Effects of inbreeding on survival, body weight and fluctuating asymmetry (FA) in Nile tilapia, Oreochromis niloticus. Aquaculture 264(1-4), 27-35. http://dx.doi.org/10.1016/j.aquaculture.2006.12.038
» http://dx.doi.org/10.1016/j.aquaculture.2006.12.038 - Firkus, T., Rahel, F.J., Bergman, H.L., & Cherrington, B.D., 2018. Warmed winter water temperatures alter reproduction in two fish species. Environ. Manage. 61(2), 291-303. PMid:29124337. http://dx.doi.org/10.1007/s00267-017-0954-9
» http://dx.doi.org/10.1007/s00267-017-0954-9 - Fitzpatrick, J.L., & Evans, J.P., 2009. Reduced heterozygosity impairs sperm quality in endangered mammals. Biol. Lett. 5(3), 320-323. PMid:19324650. http://dx.doi.org/10.1098/rsbl.2008.0734
» http://dx.doi.org/10.1098/rsbl.2008.0734 - Fricke, R., Eschmeyer, W.N., & Van der Laan, R., 2022. Eschmeyer's catalog of fishes: genera, species [online]. Retrieved in 2022, November 16, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
» http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp - Gavazzoni, M., Pavanelli, C.S., Graça, W.J., Oliveira, E., Moreira-Filho, O., & Margarido, V.P., 2023. Species delimitation in Psalidodon fasciatus (Cuvier, 1819) complex (Teleostei: Characidae) from three hydrographic basins. Biol. J. Linn. Soc. Lond. 138(1), 51-67. http://dx.doi.org/10.1093/biolinnean/blac139
» http://dx.doi.org/10.1093/biolinnean/blac139 - Gelman, A., Carlin, J.B., Stern, H.S., Dunson, D.B., Vehtari, A., & Rubin, D.B., 2013. Bayesian data analysis (3rd ed.). New York: Chapman and Hall/CRC. http://dx.doi.org/10.1201/b16018
» http://dx.doi.org/10.1201/b16018 - Gilpin, M.E., & Soulé, M.E., 1986. Minimum viable populations: the processes of species extinctions. In: Soulé, M.E., ed. Conservation biology: the science of scarcity and diversity. Sunderland, MA: Sinauer Associates.
- Gomiero, L.M., Souza, U.P., & Braga, F.M.S., 2012. Condition factor of Astyanax intermedius Eigenmann, 1908 (Osteichthyes, Characidae) parasitised by Paracymothoa astyanaxi Lemos de Castro, 1955 (Crustacea, Cymothoidae) in the Grande River, Serra do Mar State Park - Santa Virgínia Unit, São Paulo, Brazil. Braz. J. Biol. 72(2), 379-388. PMid:22735147. http://dx.doi.org/10.1590/S1519-69842012000200020
» http://dx.doi.org/10.1590/S1519-69842012000200020 - Guimarães, G.B., Melo, M.S., Giannini, P.C.F., & Melek, P.R., 2007. Geologia dos campos gerais. In: Melo, M.S., Moro, R.S., & Guimarães, G.B., eds. Patrimônio natural dos campos gerais do Paraná. Ponta Grossa: UEPG, 23-32, cap. 2.
- Gurgel, H.C.B., 2004. Estrutura populacional e época de reprodução de Astyanax fasciatus (Cuvier) (Characidae, Tetragonopterinae) do Rio Ceará Mirim, Poço Branco, Rio Grande do Norte, Brasil. Rev. Bras. Zool. 21(1), 131-135. http://dx.doi.org/10.1590/S0101-81752004000100022
» http://dx.doi.org/10.1590/S0101-81752004000100022 - Hazelton, M.L., 2007. Bias reduction in kernel binary regression. Comput. Stat. Data Anal. 51(9), 4393-4402. http://dx.doi.org/10.1016/j.csda.2006.06.012
» http://dx.doi.org/10.1016/j.csda.2006.06.012 - Hirt, L.M., Araya, P.R., & Flores, S.A., 2011. Population structure, reproductive biology and feeding of Astyanax fasciatus (Cuvier, 1819) in an Upper Paraná River tributary, Misiones, Argentina. Acta Limnol. Bras. 23(1), 1-12. http://dx.doi.org/10.4322/actalb.2011.013
» http://dx.doi.org/10.4322/actalb.2011.013 - Hojo, R.E.S., Santos, G.B., & Bazzoli, N., 2004. Reproductive biology of Moenkhausia intermedia (Eigenmann) (Pisces, Characiformes) in Itumbiara Reservoir, Goiás, Brazil. Rev. Bras. Zool. 21(3), 519-524. http://dx.doi.org/10.1590/S0101-81752004000300015
» http://dx.doi.org/10.1590/S0101-81752004000300015 - Ito, K. M., 2013. Histopatologia de brânquia e fator de condição de Astyanax aff. paranae (PISCES) como indicadores de contaminação aquática no centro-noroeste do Paraná [Trabalho de Conclusão de Curso em Engenharia Ambiental]. Campo Mourão: Universidade Tecnológica Federal do Paraná.
- Keller, L.F., & Waller, D.M., 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17(5), 230-241. http://dx.doi.org/10.1016/S0169-5347(02)02489-8
» http://dx.doi.org/10.1016/S0169-5347(02)02489-8 - Kerniske, F.F., Pena Castro, J., De la Ossa-Guerra, L.E., Mayer, B.A., Abilhoa, V., Paiva-Affonso, I., & Artoni, R.F., 2021. Spinal malformations in a naturally isolated Neotropical fish population. PeerJ 9, e12239. PMid:34721968. http://dx.doi.org/10.7717/peerj.12239
» http://dx.doi.org/10.7717/peerj.12239 - Lacy, R.C., Petric, A., & Warneke, M., 1993. Inbreeding and outbreeding in captive populations of wild animals. In: Thornhill, N.W., ed. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. Chicago: University of Chicago Press, 352-374.
- Lassala, M.D.P., & Renesto, E., 2007. Reproductive strategies and genetic variability in tropical freshwater fish. Genet. Mol. Biol. 30(3), 690-697. http://dx.doi.org/10.1590/S1415-47572007000400030
» http://dx.doi.org/10.1590/S1415-47572007000400030 - Le Cren, E.D., 1951. The length-weight relationship and seasonal cycle in gonadal weight condition in the perch Perca fluviatilis. J. Anim. Ecol. 20(2), 201-219. http://dx.doi.org/10.2307/1540
» http://dx.doi.org/10.2307/1540 - Lima-Junior, S.E., Cardone, I.B., & Goitein, R., 2002. Determination of a method for calculation of allometric condition factor of fish. Acta Scientiarum 24(2), 397-400. https://doi.org/10.4025/actascibiolsci.v24i0.2311
» https://doi.org/10.4025/actascibiolsci.v24i0.2311 - Losdat, S., Chang, S.M., & Reid, J.M., 2014. Inbreeding depression in male gametic performance. J. Evol. Biol. 27(6), 992-1011. PMid:24820115. http://dx.doi.org/10.1111/jeb.12403
» http://dx.doi.org/10.1111/jeb.12403 - Lowe-McConnel, R.H. 1999. Estudos ecológicos de comunidades de peixes tropicais. São Paulo: Edusp, 534 p.
- Malabarba, L.R., & Malabarba, M.C., 2020. Phylogeny and classification of neotropical fish. In: Baldisserotto, B., Criscuolo Urbinati, E. & Cyrino, J.E.P., eds. Biology and physiology of freshwater neotropical fish. Amsterdam: Academic Press, 1-19. http://dx.doi.org/10.1016/B978-0-12-815872-2.00001-4
» http://dx.doi.org/10.1016/B978-0-12-815872-2.00001-4 - Mariette, M., Kelley, J.L., Brooks, R., & Evans, J.P., 2006. The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112(8), 807-814. http://dx.doi.org/10.1111/j.1439-0310.2006.01236.x
» http://dx.doi.org/10.1111/j.1439-0310.2006.01236.x - Matoso, D.A., Artoni, R.F., & Galleti, P.M., 2004. Genetic Diversity of the Small Characid Fish Astyanax sp., and its significance for conservation. Hydrobiologia 527(1), 223-225. http://dx.doi.org/10.1023/B:HYDR.0000043303.02986.71
» http://dx.doi.org/10.1023/B:HYDR.0000043303.02986.71 - Matoso, D.A., Martins, C., Artoni, R.F., & Galetti Junior, P.M., 2010. Preliminary qualitative analysis on mtDNA in Astyanax fasciatus populations Cuvier, 1819 (Teleostei; Characidae) indicate population distinctiveness. Braz. Arch. Biol. Technol. 53(3), 663-667. http://dx.doi.org/10.1590/S1516-89132010000300022
» http://dx.doi.org/10.1590/S1516-89132010000300022 - Matoso, D.A., Silva, M., Artoni, R.F., & Torres, R.A., 2013. Molecular taxonomy and evolutionary hypothesis concerning Astyanax fasciatus (Characiformes, Characidae) from Vila Velha State Park and Tibagi and Iguaçu Rivers. Genet. Mol. Res. 12(1), 631-638. PMid:23546944. http://dx.doi.org/10.4238/2013.March.7.1
» http://dx.doi.org/10.4238/2013.March.7.1 - Medrado, A.S., Affonso, P.R., Carneiro, P.L.S., Vicari, M.R., Artoni, R.F., & Costa, M.A., 2015. Allopatric divergence in Astyanax aff. fasciatus Cuvier, 1819 (Characidae, Incertae sedis) inferred from DNA mapping and chromosomes. Zool. Anz. 257, 119-129. http://dx.doi.org/10.1016/j.jcz.2015.05.005
» http://dx.doi.org/10.1016/j.jcz.2015.05.005 - Meffe, G.K., & Carroll, C.R., 1994. Principles of conservation biology. Sunderland: Sinauer Associates Inc., 600 p.
- Melo, M.S., & Giannini, P.C.F., 2007. Sandstone dissolution landforms in the furnas formation, southern Brazil. Earth Surf. Process. Landf. 32(14), 2149-2164. http://dx.doi.org/10.1002/esp.1520
» http://dx.doi.org/10.1002/esp.1520 - Melo, M.S., Guimarães, G.B., Pontes, H.S., Massuqueto, L.L., Pigurim, I., Bagatim, H.Q., & Giannini, P.C.F., 2011. Carste em rochas não-carbonáticas: o exemplo dos arenitos da Formação Furnas, Campos Gerais do Paraná/Brasil e as implicações para a região. Espeleo-Tema 22(1), 81-97.
- Menni, R.C., & Almirón, A.E., 1994. Reproductive seasonality in fishes of manmade ponds in temperate South America. Neotropica 40(103-104), 75-85.
- Nelson, J.S., 2006. Fishes of the World. New York: John Wiley & Sons, 601 p.
- Nikolsky, G.V., 1969. Theory of fish population dynamics. Edinburgh: Oliver and Boyd, 323 p.
- Pansonato-Alves, J.C., Hilsdorf, A.W.S., Utsunomia, R., Silva, D.M.Z.A., Oliveira, C., & Foresti, F., 2013. Chromosomal mapping of repetitive DNA and Cytochrome C Oxidase I sequence analysis reveal differentiation among sympatric samples of Astyanax fasciatus (Characiformes, Characidae). Cytogenet. Genome Res. 141(2-3), 133-142. PMid:24081020. http://dx.doi.org/10.1159/000354885
» http://dx.doi.org/10.1159/000354885 - Portella, A.C., Arsentales, A.D., Cavallari, D.E., & Welber, S.S., 2021. Effect of seasonality on the reproduction of characiformes fish in a neotropical river. Iheringia Ser. Zool. 111, e2021012. http://dx.doi.org/10.1590/1678-4766e2021012
» http://dx.doi.org/10.1590/1678-4766e2021012 - Porto-Foresti, F., Castilho-Almeida, R.B., & Foresti, F., 2005. Biologia e criação do lambari-do-rabo-amarelo (Astyanax altiparanae). In: Baldisserotto, B., & Gomes, L.C., eds. Espécies nativas para piscicultura. Santa Maria: Editora UFMS, 468 p.
- Prado, P.S., Souza, C.C., Bazzoli, N., & Rizzo, E., 2011. Reproductive disruption in lambari Astyanax fasciatus from a Southeastern Brazilian reservoir. Ecotoxicol. Environ. Saf. 74(7), 1879-1887. PMid:21831433. http://dx.doi.org/10.1016/j.ecoenv.2011.07.017
» http://dx.doi.org/10.1016/j.ecoenv.2011.07.017 - Quirino, P.P., Siqueira-Silva, D.H., Silva Rodrigues, M., Santos-Silva, A.P., Delgado, M.L.R., Senhorini, J.A., & Veríssimo-Silveira, R., 2021. Gonadal morphology and difference in reproductive development of two isolated populations of Astyanax rivularis (Teleostei, Characidae). J. Fish Biol. 99(5), 1719-1728. PMid:34392530. http://dx.doi.org/10.1111/jfb.14879
» http://dx.doi.org/10.1111/jfb.14879 - R Core Team, 2019. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved in 2022, November 16, from https://www.R-project.org/
» https://www.R-project.org/ - Reis, R.B., Frota, A., Carvalho Deprá, G., Ota, R.R., & Graça, W.J., 2020. Freshwater fishes from Paraná state, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa 4868(4), zootaxa.4868.4.1. PMid:33311378.
- Reis, R.E., Albert, J.S., Di Dario, F., Mincarone, M.M., Petry, P., & Rocha, L.A., 2016. Fish biodiversity and conservation in South America. J. Fish Biol. 89(1), 12-47. PMid:27312713. http://dx.doi.org/10.1111/jfb.13016
» http://dx.doi.org/10.1111/jfb.13016 - Reis, R.E., Kullander, S.O., & Ferraris, C., 2003. Check list of the freshwater fishes of South and Central America (CLOFFSCA). Porto Alegre: EDIPUCRS, 729 p.
- Santos, S.A., & de Britto, M.R., 2021. The ichthyofauna of a poorly known area in the middlesouthern espinhaço mountain range, state of Minas Gerais, Brazil: diagnostics and identification keys. ZooKeys 1054, 25-66. PMid:34393562. http://dx.doi.org/10.3897/zookeys.1054.67554
» http://dx.doi.org/10.3897/zookeys.1054.67554 - Shibatta, O.A., & Artoni, R.F., 2005. Sobre a identidade das populações alopátricas de Astyanax (Characiformes, Characidae) das formações Furna 1 e Furna 2 do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Publ. UEPG Biol. Health Sci. 11(2), 7-12. https://doi.org/10.5212/publicatio%20uepg.v11i2.410
» https://doi.org/10.5212/publicatio%20uepg.v11i2.410 - Shirak, A., Palti, Y., Cnaani, A., Korol, A., Hulata, G., Ron, M., & Avtalion, R.R., 2002. Association Between Loci With Deleterious Alleles and Distorted Sex Ratios in an Inbred Line of Tilapia (Oreochromis aureus). J. Hered. 93(4), 270-276. PMid:12407213. http://dx.doi.org/10.1093/jhered/93.4.270
» http://dx.doi.org/10.1093/jhered/93.4.270 - Silva, J.P.A., Muelbert, A.E., Oliveira, E.C., & Fávaro, L.F., 2010. Reproductive tactics used by the lambari Astyanax fasciatus in three water supply reservoirs in the same geographic region of the upper Iguacu River. Neotrop. Ichthyol. 8(4), 885-892. http://dx.doi.org/10.1590/S1679-62252010000400019
» http://dx.doi.org/10.1590/S1679-62252010000400019 - Silveira, E.L., Aranha, J.M.R., Menezes, M.S., & Vaz-Dos Santos, A.M., 2020. Reproductive dynamics, age and growth of Astyanax aff. fasciatus in a Neotropical basin. Mar. Freshw. Res. 71(6), 670-683. http://dx.doi.org/10.1071/MF19100
» http://dx.doi.org/10.1071/MF19100 - Terán, G.E., Benitez, M.F., & Mirande, J.M., 2020. Opening the Trojan horse: phylogeny of Astyanax, two new genera and resurrection of Psalidodon (Teleostei: Characidae). Zool. J. Linn. Soc. 190(4), 1217-1234. http://dx.doi.org/10.1093/zoolinnean/zlaa019
» http://dx.doi.org/10.1093/zoolinnean/zlaa019 - Toussaint, A., Charpin, N., Brosse, S., & Villéger, S., 2016. Global functional diversity of freshwater fish is concentrated in the Neotropics while functional vulnerability is widespread. Sci. Rep. 6(1), 22125. PMid:26980070. http://dx.doi.org/10.1038/srep22125
» http://dx.doi.org/10.1038/srep22125 - Vazzoler, A.E.A.M., 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem, 169 p.
- Veregue, A.M.L., & Orsi, M.L., 2003. Reproductive biology of Astyanax scabripinnis paranae (Eigenmann) (Ostheichthyes, Characidae) from Marrecas creek of the Tibagi basin, Paraná. Rev. Bras. Zool. 20(1), 97-105. http://dx.doi.org/10.1590/S0101-81752003000100012
» http://dx.doi.org/10.1590/S0101-81752003000100012 - Waddell, J.C., Njeru, S.M., Akhiyat, Y.M., Schachner, B.I., Correa-Roldán, E.V., & Crampton, W.G.R., 2019. Reproductive life-history strategies in a species-rich assemblage of Amazonian electric fishes. PLoS One 14(12), e0226095. PMid:31805125. http://dx.doi.org/10.1371/journal.pone.0226095
» http://dx.doi.org/10.1371/journal.pone.0226095 - Winemiller, K.O., 1989. Patterns of variation in life history among South American fishes in seasonal environmentals. Oecologia 81(2), 225-241. PMid:28312542. http://dx.doi.org/10.1007/BF00379810
» http://dx.doi.org/10.1007/BF00379810 - Zajitschek, S.R.K., Lindholm, A.K., Evans, J.P., & Brooks, R.C., 2009. Experimental evidence that high levels of inbreeding depress sperm competitiveness. J. Evol. Biol. 22(6), 1338-1345. PMid:19344380. http://dx.doi.org/10.1111/j.1420-9101.2009.01738.x
» http://dx.doi.org/10.1111/j.1420-9101.2009.01738.x
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Publication Dates
-
Publication in this collection
13 Oct 2023 -
Date of issue
2023
History
-
Received
08 Feb 2023 -
Accepted
16 Aug 2023