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Life-History traits of Hollandichthys multifasciatus (Eigenmann & Norris, 1900) (Characiformes: Characidae) in coastal Atlantic Forest blackwater streams from Southeastern Brazil

Abstract

Ecological and life history traits have been used to understand the basic ecology of fishes. This study aimed to examine the existence of plasticity in life history traits of populations of Hollandichthys multifasciatus in ten blackwater streams. This is an inseminating Characidae, endemic to the Atlantic coastal drainages of Brazil. Different aspects of the life-history of the species, such as mean length, sex ratio, absolute and relative fecundity, gonadosomatic index, condition factor, length-weight relationship and the growth parameter (b) of 185 specimens were studied during the period of low precipitation (June-September). Fish samples were obtained along a 100 m stretch of each stream, and some habitat variables recorded. ANOVA and Kruskal-Wallis tests indicated a similarity in most of the analyzed traits, with exception of the mean length of immatures, Gonadosomatic Index of mature males and condition factor of immatures and mature adults. Also, slope tests of the length-weight relationship were significantly different for immatures. The observed differences were attributed to heterogeneity in food availability and/or other site-specific factors, which may influence growth and/or breeding aspects among the studied localities. The approach used herein may improve understanding of trait plasticity under natural conditions, helping to understand fish-community responses to anthropogenic changes.

Keywords.
Length-weight relationship; Condition factor; Humic waters; Baixada Santista

INTRODUCTION

Variations in life-history traits between and within fish populations have been described for several native populations from tropical (Winemiller, 1989Winemiller, K.O. 1989. Patterns of Variation in Life History among South American Fishes in Seasonal Environments. International Association for Ecology, 81(2): 225-241. https://doi.org/10.1007/BF00379810.
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; Grether et al., 2001Grether, G.F.; Millie, D.F.; Bryant, M.J.; Reznick, D.N. & Mayea, W. 2001. Rain Forest Canopy Cover, Resource Availability, and Life History Evolution in Guppies. Ecology, 82(6): 1546. https://doi.org/10.2307/2679799.
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; Gomes & Monteiro, 2007Gomes, J.L. & Monteiro, L.R. 2007. Size and fecundity variation in populations of Poecilia vivipara Block & Schneider (Teleostei; Poeciliidae) inhabiting an environmental gradient. Journal of Fish Biology, 71(6): 1799-1809. https://doi.org/10.1111/j.1095-8649.2007.01653.x.
https://doi.org/10.1111/j.1095-8649.2007...
) and temperate habitats (García & Braña, 1988García, E. & Braña, F. 1988. Reproductive biology of brown trout (Salmo trutta) in the Aller river (Asturias, Northern Spain). Polskie Archiwum Hydrobiologii, 3(3-4): 361-374.; Lobón-Cerviá & Rincón, 1998Lobón-Cerviá, J. & Rincón, P.A. 1998. Field Assessment of the Influence of Temperature on Growth Rate in a Brown Trout Population. Transactions of the American Fisheries Society, 127(5): 718-728. https://doi.org/10.1577/1548-8659(1998)127<0718:FAOTIO>2.0.CO;2.
https://doi.org/10.1577/1548-8659(1998)1...
; Craig et al., 2017Craig, N.; Jones, S.E.; Weidel, B.C. & Solomon, C.T. 2017. Life history constraints explain negative relationship between fish productivity and dissolved organic carbon in lakes. Ecology and Evolution, 7(16): 6201-6209. https://doi.org/10.1002/ece3.3108.
https://doi.org/10.1002/ece3.3108...
), with spatial and temporal patchiness of resources resulting in variation in reproductive traits. Resource availability is considered a major driver for selection of various life-history strategies in organisms and can affect population growth and productivity (Begon et al., 2006Begon, M.; Townsend, C.R. & Harper, J.L. 2006. Ecology: From individuals to ecosystems. Oxford, Blackwell Publishing.). However, other factors, such as environmental stability (e.g., hydrology; Lytle & Poff, 2004Lytle, D.A. & Poff, N.L. 2004. Adaptation to natural flow regimes. Trends in Ecology & Evolution, 19(2): 94-100. https://doi.org/10.1016/j.tree.2003.10.002.
https://doi.org/10.1016/j.tree.2003.10.0...
), light radiance, temperature, and oxygen levels may be related to variations in growth and reproductive strategies (Jobling, 1994Jobling, M. 1994. Fish bioenergetics. London, Chapman & Hall.), and thus life-history traits of fish populations may vary among habitat types (Blanck & Lamouroux, 2007Blanck, A. & Lamouroux, N. 2007. Large-scale intraspecific variation in life-history traits of European freshwater fish. Journal of Biogeography, 34(5): 862-875. https://doi.org/10.1111/j.1365-2699.2006.01654.x.
https://doi.org/10.1111/j.1365-2699.2006...
).

Several studies have shown that organisms in unproductive environments may grow more slowly and allocate their limited energy to growth for a longer time until they become large enough to produce sufficient offspring (Pianka, 1970Pianka, E.R. 1970. On r- and K- selection. American Naturalist, 104: 592-597. https://doi.org/10.1086/282697.
https://doi.org/10.1086/282697...
). Organisms are likely to mature later than those in more productive environments where they can grow faster and get larger quicker (Stearns & Koella, 1986Stearns, S.C. & Koella, J.C. 1986. The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution, 40(5): 893-913. https://doi.org/10.2307/2408752.
https://doi.org/10.2307/2408752...
). In this respect, important drivers of freshwater productivity as Dissolved Organic Carbon (DOC) have been shown to affect life-history characteristics of Lepomis macrochirus Rafinesque, 1819 in North American lakes such that fish in high-DOC lakes reached smaller sizes, but had similar fecundity and egg size, at a given size (Craig et al., 2017Craig, N.; Jones, S.E.; Weidel, B.C. & Solomon, C.T. 2017. Life history constraints explain negative relationship between fish productivity and dissolved organic carbon in lakes. Ecology and Evolution, 7(16): 6201-6209. https://doi.org/10.1002/ece3.3108.
https://doi.org/10.1002/ece3.3108...
).

Since streams exhibit variation in physiographic and physicochemical factors, which are often patchily distributed (Pringle et al., 1988Pringle, C.M.; Naiman, R.J.; Gretschko, G.; Karr J.R.; Oswood, M.W.; Webster, J.R.; Welcomme, R.L. & Winterbourn, M.L. 1988. Patch dynamics in lotic systems; the stream as a mosaic. Journal of the North American Benthological Society, 7(4): 503-524. https://doi.org/10.2307/1467303.
https://doi.org/10.2307/1467303...
), shifts in resource availability are important in predicting the adaptiveness of traits of species populations. Blackwater Atlantic Forest rivers and streams present some environmental heterogeneity, low pH (Camargo et al., 1997Camargo, A.F.M.; Nucci, P.R.; Bini, L.M. & Silva, U.L. 1997. The influence of the geology on the limnological characteristics of some lotic ecosystems of the Itanhaém River Basin, SP, Brazil. SIL Proceedings, 26(2): 860-864. https://doi.org/10.1080/03680770.1995.11900840.
https://doi.org/10.1080/03680770.1995.11...
; Gonçalves & Braga, 2012Gonçalves, C.S.S. &; Braga, F.M.S. 2012. Changes in ichthyofauna composition along a gradient from clearwaters to blackwaters in coastal streams of Atlantic forest (southeastern Brazil) in relation to environmental variables. Neotropical Ichthyology, 10(3): 675-684. https://doi.org/10.1590/S1679-62252012000300022.
https://doi.org/10.1590/S1679-6225201200...
) and varied levels of DOC concentrations (Felisberto, 2020Felisberto, M.L.G. 2020. Estrutura da comunidade de peixes em riachos costeiros de águas pretas da Mata Atlântica no Sudeste do Brasil (Master’s Dissertation). Instituto de Pesca/APTA/SAA, São Paulo (SP).), owing to high humic acid contents (Por, 1992Por, F.D. 1992. Sooretama, the Atlantic rainforest of Brazil. The Hague, SPB Academic Publishing.). They are also part of Atlantic Forest coastal drainages, which correspond to a system of isolated streams that originate at different points in a region between marine and coastal environments, draining directly into the Atlantic Ocean. Freshwater fishes in these coastal basins have evolved in isolation with sporadic dispersal with inland basins of Brazil (Ribeiro, 2006Ribeiro, A.C. 2006. Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotropical Ichthyology, 4(2): 225-46. https://doi.org/10.1590/S1679-62252006000200009.
https://doi.org/10.1590/S1679-6225200600...
). As small and/or non-migratory species with specific habitat requirements may be susceptible to variation in habitat across the landscape, limiting their dispersal between populations (Waters & Burridge, 2016Waters, J.M. & Burridge, C.P. 2016. Fine-scale habitat preferences influence within-river population connectivity: a case-study using two sympatric New Zealand Galaxias fish species. Freshwater Biology, 61: 51-56. https://doi.org/10.1111/fwb.12675.
https://doi.org/10.1111/fwb.12675...
), isolated streams may be good model ecosystems for understanding how intraspecific traits vary in response to different conditions.

Hollandichthys multifasciatus (Eigenmann & Norris, 1900) is an endemic characid to the Atlantic coastal drainages of Brazil, occurring from Rio de Janeiro to Rio Grande do Sul states, and in the upper Tietê river (Lima et al., 2007Lima, F.C.T.; Buckup, P.A.; Menezes, N.A.; Lucena, C.A.S.; Lucena, Z.M.S.; Toledo-Piza M. & Zanata, A. 2007. Família Characidae: gêneros incertae sedis. In: Buckup PA, Menezes NA, Ghazzi MS (Eds.). Catálogo das espécies de peixes de água doce do Brasil. Rio de Janeiro, Museu Nacional. p. 44-62.; Menezes et al., 2007Menezes, N.A.; Weitzman, S.H.; Oyakawa, O.T.; Lima, F.C.T.; Castro, R.M.C. & Weitzman, M.J. 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce neotropicais. MZUSP, São Paulo.). Despite being one of the most representative species in several coastal stream surveys (Ferreira & Petrere, 2009Ferreira, F.C. & Petrere, M. 2009. The fish zonation of the Itanhaém river basin in the Atlantic forest of southeast Brazil. Hydrobiologia, 636(1): 11-34. https://doi.org/10.1007/s10750-009-9932-4.
https://doi.org/10.1007/s10750-009-9932-...
; Gonçalves & Braga, 2012Gonçalves, C.S.S. &; Braga, F.M.S. 2012. Changes in ichthyofauna composition along a gradient from clearwaters to blackwaters in coastal streams of Atlantic forest (southeastern Brazil) in relation to environmental variables. Neotropical Ichthyology, 10(3): 675-684. https://doi.org/10.1590/S1679-62252012000300022.
https://doi.org/10.1590/S1679-6225201200...
; Lemos, 2019Lemos, C.A. 2019. Biologia de populações de peixes do Riachos da Vila de Itatinga, Bertioga, São Paulo (Doctoral Thesis). Universidade Federal de São Carlos, São Carlos (SP).; Felisberto, 2020Felisberto, M.L.G. 2020. Estrutura da comunidade de peixes em riachos costeiros de águas pretas da Mata Atlântica no Sudeste do Brasil (Master’s Dissertation). Instituto de Pesca/APTA/SAA, São Paulo (SP).), biological aspects of H. multifasciatus are still poorly known. It is an inseminating species found in clear and blackwater streams (Sabino & Castro, 1990Sabino, J. & Corrêa e Castro, R. 1990. Alimentação, período de atividade e distribuição espacial dos peixes de um riacho da Floresta Atlântica (Sudeste do Brasil). Revista Brasileira de Biologia, 50(1): 23-36.; Esteves & Lobón-Cerviá, 2001Esteves, K.E. & Lobón-Cerviá, J. 2001. Composition and trophic structure of a fish community of a clear water Atlantic rainforest stream in southeastern Brazil. Environmental Biology of Fishes, 62(4): 429-440. https://doi.org/10.1111/j.1600-0633.2011.00518.x.
https://doi.org/10.1111/j.1600-0633.2011...
; Esteves et al., 2019Esteves, K.E.; Silva, M.H.C.; Nanini-Costa, M.H. & Petesse, M.L. 2019. Organization of fish assemblages in blackwater Atlantic Forest streams. Neotropical Ichthyology, 17(1): e180120. https://doi.org/10.1590/1982-0224-20180120.
https://doi.org/10.1590/1982-0224-201801...
) with little running water and a muddy bottom, associated with preserved Atlantic Forest riparian vegetation (Bertaco, 2003Bertaco, V.A. 2003. Taxonomia e filogenia do gênero Hollandichthys Eigenmann, 1909 (Teleostei: Characidae) do sul e sudeste do Brasil (Master’s Dissertation). Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre (RS).). Adults display solitary habits, while juveniles form shoals of three to six individuals (Bertaco & Malabarba, 2013Bertaco, V.A. & Malabarba, L.R. 2013. A new species of the characid genus Hollandichthys Eigenmann from coastal rivers of southern Brazil (Teleostei: Characiformes) with a discussion on the diagnosis of the genus. Neotropical Ichthyology, 11(4): 767-778. https://doi.org/10.1590/S1679-62252013000400004.
https://doi.org/10.1590/S1679-6225201300...
). It is considered an omnivore which consumes few autochthonous items and great proportions of plants and terrestrial insects (Abilhoa et al., 2009Abilhoa, V.; Bornatowski, H. & Otto, G. 2009. Temporal and ontogenetic variations in feeding habits of Hollandichthys multifasciatus (Teleostei: Characidae) in coastal Atlantic rainforest streams, southern Brazil. Neotropical Ichthyology, 7(3): 415-420. https://doi.org/10.1590/S1679-62252009005000001.
https://doi.org/10.1590/S1679-6225200900...
; Gonçalves et al., 2018Gonçalves, C.S; de Souza Braga, F.M. & Casatti, L. 2018. Trophic structure of coastal freshwater stream fishes from an Atlantic rainforest: evidence of the importance of protected and forest-covered areas to fish diet. Environmental Biology of Fishes, 101(6): 1-16. https://doi.org/10.1007/s10641-018-0749-8.
https://doi.org/10.1007/s10641-018-0749-...
), displaying a surface picking behavior as described for several characin species (Sazima, 1986Sazima, I. 1986. Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities. Journal of Fish Biology, 29(1): 53-65. https://doi.org/10.1111/j.1095-8649.1986.tb04926.x.
https://doi.org/10.1111/j.1095-8649.1986...
). Hollandichthys multifasciatus is classified as Data Deficient (DD) by the Brazilian federal list of endangered species (ICMBio/MMA, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)/Ministério do Meio Ambiente (MMA). 2018. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasília, ICMBio/MMA.) and as Least Concern (LC) in the regional list of São Paulo State (Oyakawa et al., 2009Oyakawa, O.T.; Menezes, N.A.; Shibatta, O.A.; Lima, F.C.T.; Langeani, F.; Pavanelli, C.S.; Nielsen, D.T.B. & Hilsdorf, A.W.S. 2009. Peixes. In: Bressan P.M.; Kierulff, M.C.M.; Sugieda A.M. (Eds.). Fauna ameaçada de extinção no Estado de São Paulo: vertebrados; Fundação Parque Zoológico de São Paulo. São Paulo, Secretaria do Meio Ambiente.).

Here we examined the existence of plasticity in life history traits of populations of H. multifasciatus from ten preserved blackwater streams, assessing their mean length, absolute and relative fecundity, condition factor, length-weight relationship, type of growth (b), sex ratio and gonadal-somatic index among the streams.

MATERIAL AND METHODS

The present study was carried out in the coastal region of São Paulo State (southeast Brazil) in the municipalities of Bertioga and São Sebastião, comprising ten blackwater streams which belong to the Guaratuba, Itapanhaú, Itaguaré and Una sub-basins (Figs. 1, 2, Table 1). The first three sub-basins are located in the Baixada Santista Hydrographic Basin (Ribeiro, 2018Ribeiro, R.B. 2018. Relatório de situação dos recursos hídricos da Baixada Santista 2018. Available: Available: https://sigrh.sp.gov.br/public/uploads/documents/CBH-BS/13787/rs-2018-bs.pdf . Access: 22/11/2021.
https://sigrh.sp.gov.br/public/uploads/d...
), and the Una sub-basin in the Northern Coast, all of them included in the Ribeira do Iguape Ecoregion sensuAbell et al. (2008Abell, R.; Thieme, M.L.; Revenga, C.; Bryer, M.; Kottelat, M.; Bogutskaya, N.; Coad, B.; Mandrak, N.; Balderas, S.C.; Bussing, W.; Stiassny, M.L.J.; Skelton, P.; Allen, G.R.; Unmack, P.; Naseka, A.; Ng., R.; Sindorf, N.; Robertson, J.; Armijo, E.; Higgins, J.V.; Heibel, T.J.; Wikramanayake, E.; Olson, D.; López, H.L.; Reis, R.E.; Lundberg, J.G.; Pérez, M.H.S. & Paulo Petry. 2008. Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 58(5): 403-414. https://doi.org/10.1641/B580507.
https://doi.org/10.1641/B580507...
). Sampled streams are independent coastal slow-moving acidic environments with high humic acid content. They have their origins at low altitudes in the alluvial plains, also called Coastal Plain Forest, which represents one of the faces of the Atlantic Forest biome, commonly found in the region of the Serra do Mar hills (Marques et al., 2015Marques, M.C.M.; Silva, S.M. & Liebsch, D. 2015. Coastal plain forests in southern and southeastern Brazil: ecological drivers, floristic patterns and conservation status. Brazilian Journal of Botany, 38(1): 1-18. https://doi.org/10.1007/s40415-015-0132-3.
https://doi.org/10.1007/s40415-015-0132-...
). The area consists of Dense Ombrophilous Forest and Pioneer Formations, with emphasis on Restinga vegetation (coastal sand-dune habitats) (Instituto Ekos Brasil, 2008Instituto Ekos Brasil. 2008. Diagnóstico socioambiental para criação de unidades de conservação polígono Bertioga: relatório final. Available: Available: http://assets.wwfbr.panda.org/downloads/diagnostico_socioambiental_para_criacao_de_unidades_de_conservacao.pdf . Access: 20/12/2017.
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), which range from grasslands and shrublands to forests, with a maximum canopy height of 20 m (Bonilha et al., 2012Bonilha, R.M.; Casagrande, J.C. & Soares, M.R. 2012. Characterization of the soil fertility and root system of restinga forests. Revista Brasileira de Ciências do Solo, 36(1): 1804-1813. https://doi.org/10.1590/S0100-06832012000600014.
https://doi.org/10.1590/S0100-0683201200...
).

Figure 1
Study area, coastal region of the State of São Paulo. Sampled streams (JP1, JP2 - Itapanhaú); (P1-P6 - Guaratuba); Itaguaré (MP) and Una (BB1 - Una). Adapted from Esteves et al. (2019Esteves, K.E.; Silva, M.H.C.; Nanini-Costa, M.H. & Petesse, M.L. 2019. Organization of fish assemblages in blackwater Atlantic Forest streams. Neotropical Ichthyology, 17(1): e180120. https://doi.org/10.1590/1982-0224-20180120.
https://doi.org/10.1590/1982-0224-201801...
).

Figure 2
View of one of the sampling sites (JP1, Itapanhaú sub-basin), showing block nets at the 100 m sampled stretch.

Table 1
Characteristics of the sampling sites in the municipalities of Bertioga and São Sebastião, SP. FaR - High dry Restinga Forest; FODT - Lowland Rainforest; FODM - Dense Sub-Montana rainforest (Adapted from Esteves et al., 2019Esteves, K.E.; Silva, M.H.C.; Nanini-Costa, M.H. & Petesse, M.L. 2019. Organization of fish assemblages in blackwater Atlantic Forest streams. Neotropical Ichthyology, 17(1): e180120. https://doi.org/10.1590/1982-0224-20180120.
https://doi.org/10.1590/1982-0224-201801...
).

Samplings were performed during the low rainfall season (July-September/2016). The criteria used to select the sampling sites were accessibility, the adequacy for electrofishing, salinity ≤ 0.05 ppm and good conservation status of the streams, for instance, with preserved vegetation and with a minimum of anthropic influences.

Streams were characterized according to its dominant terrestrial vegetation, based on França & Rolim (2000França, F.S. & Rolim, S.G. 2000. Estrutura de um trecho de floresta de restinga no município de Bertioga (SP). In: Watanabe S. (Ed.). Simpósio de Ecossistemas Brasileiros: Conservação, 5º. Anais. São Paulo, ACIESP. p. 84-91.), Instituto Ekos Brasil (2008Instituto Ekos Brasil. 2008. Diagnóstico socioambiental para criação de unidades de conservação polígono Bertioga: relatório final. Available: Available: http://assets.wwfbr.panda.org/downloads/diagnostico_socioambiental_para_criacao_de_unidades_de_conservacao.pdf . Access: 20/12/2017.
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), Guedes et al. (2006Guedes, D.; Barbosa, L.M. & Martins, S.E. 2006. Composição florística e estrutura fitossociológica de dois fragmentos de Floresta de restinga no município de Bertioga, SP, Brasil. Acta Botanica Brasilica, 20: 299-311. https://doi.org/10.1590/S0102-33062006000200006.
https://doi.org/10.1590/S0102-3306200600...
) and Pinto-Sobrinho et al. (2011Pinto-Sobrinho, F.A.; Souza, C.R.D.G. & Mogollón, J.E.J.B. 2011. Análise Estrutural de Florestas de Restinga associadas a Depósitos Marinhos Pleistocênicos e Holocênicos na Bacia do Rio Itaguaré, Bertioga (SP). Revista do Instituto Geológico, 32: 27-40. https://doi.org/10.5935/0100-929X.20110003.
https://doi.org/10.5935/0100-929X.201100...
). A physical assessment of some habitat variables was conducted along a 100 m stretch of each stream. The following descriptors were considered and scored according to Callisto et al. (2014Callisto, M.; Pompeu, O.S.; Alves, C.B.M.; Santos, G.B. 2014. Perspectivas na abordagem de Índices de Integridade Biótica com peixes e bentos em bacias hidrográficas no cerrado. In: Callisto, M.; Alves, C.B.M.; Lopes, J.M. & Castro, M.A. (Eds.). Condições ecológicas em bacias hidrográficas de empreendimentos hidrelétricos. Belo Horizonte, Companhia Energética de Minas Gerais. p. 235-240.): percentage of high canopy (Diameter at Breast Height > 0.3 m); leaf banks (%); overhanging vegetation (< 1 m from the surface) (%); sand (0.6-2 mm) (%); silt/clay (%). Some water variables as temperature, pH, dissolved oxygen and electrical conductivity were recorded at each stream with a HORIBA multiparameter probe, model U-5000G. Dissolved Organic Carbon (DOC) was analyzed according to APHA/AWWA/WEF (2012American Public Health Association (APHA); American Water Works Association (AWWA) & Water Environment Federation (WEF). 2012. Standard methods for the examination of water and freshwater. Washington DC, APHA/AWWA/WEF.).

Each stream was sampled three times along a 100 m stretch isolated with block nets, where electrofishing was performed using a Honda EUi10 Generator (CA, 1000 W). Fish were separated into containers, anesthetized in eugenol solution, fixed in a 10% formalin solution, and transferred to 70% ethanol after 10 days. Specimens were deposited at the ichthyological collection of the Museu de Zoologia da Universidade Estadual de Campinas “Adão José Cardoso” (ZUEC 16629).

Specimens were measured (total length, mm) and weighed (W, g) in the laboratory. Sex was determined through macroscopic analysis of the gonads, which were removed, weighed, and fixed in 70% ethanol. The degree of maturation was determined according to Vazzoler (1996Vazzoler, A.E.A.M. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Maringa, EDUEM.). Specimens were considered immature/juveniles if it was not possible to distinguish sex through gonads or secondary characteristics. The gonadosomatic index (GSI) was calculated for mature females and males according to Santos (1978Santos, E.P. 1978. Dinâmica de populações aplicada à pesca e piscicultura. São Paulo, Hucitec.), following the formula GSI = 100 GW. TW -1, where GW is the gonad weight and TW is the total weight. Fecundity was estimated by direct counts of fixed mature ovarian subsamples. Oocytes were sub-sampled three times with a Hensel-Stempel pipette, samples counted and measured in a Sedgewick Rafter chamber (Sá-Oliveira & Chelappa, 2002Sá-Oliveira, J.C. & Chellappa, S. 2002. Fecundidade e tipo de desova do tamuatá, Hoplosternum littorale Hancock (Osteichthyes, Siluriformes) no Rio Curiaú, Macapá, Amapá. Revista Brasileira de Zoologia, 19(4): 1053-1056. https://doi.org/10.1590/S0101-81752002000400009.
https://doi.org/10.1590/S0101-8175200200...
). A minimum of 50 oocytes were measured for each female according to Gomes et al. (2011Gomes, I.D.; Araújo, F.G.; Uehara, W. & Sales, A. 2011. Reproductive biology of the armoured catfish Loricariichthys castaneus (Castelnau, 1855) in Lajes reservoir, southeastern Brazil. Journal of Applied Ichthyology, 27(6): 1322-1331. https://doi.org/10.1111/j.1439-0426.2011.01874.
https://doi.org/10.1111/j.1439-0426.2011...
). Absolute fecundity was calculated considering the total of vitellogenic oocytes (Vazzoler, 1981Vazzoler, A.E.A.M. 1981. Manual de Métodos para estudos biológicos de populações de peixes. Reprodução e crescimento. Brasília, CNPq, Programa Nacional de Zoologia.), herein considered those with a diameter ≥ 0.6 mm. To calculate the relative fecundity, the absolute fecundity of each female was divided by its weight (g) (Adebisi, 1987Adebisi, A.A. 1987. The relationships between fecundities, gonadosomatic indices and egg sizes of some fishes of the Ogun River, Nigeria. Archiv für Hydrobiologie, 111(1): 151-156.), and then the average relative fecundity per stream was calculated. The sex ratio was determined by the distribution of male and female frequencies in each stream.

The length-weight relationship (LWR) was calculated for mature and immature specimens separately. We calculated the regression for each stream according to the equation W = a Lb, where W = weight, L = Length, a = intersection with y-axes and b = slope (angular coefficient). After logarithmic transformation of the data we obtained the coefficient A and B by the least squares method for the equation log (W) = log A + log Bx, where a = eA and b = B (Santos, 1978Santos, E.P. 1978. Dinâmica de populações aplicada à pesca e piscicultura. São Paulo, Hucitec.; Braga, 1986Braga, F.M.S. 1986. Estudo entre fator de condição e relação peso-comprimento para alguns peixes marinhos. Brazilian Journal of Biology, 46(2): 339-346.). Prior to regression analysis, log10-log10 plots of W and L were used to detect and exclude outliers (Froese, 2006Froese, R. 2006. Cube law, condition factor and weight-length relationships: History, meta-analysis and recommendations. Journal of Applied Ichthyology, 22(4): 241-53. https://doi.org/10.1111/j.1439-0426.2006.00805.x.
https://doi.org/10.1111/j.1439-0426.2006...
). Initially, to test for significant differences between males and females, we compared the slope (B) of the linearized regressions for grouped streams using PAST 4.05 software. When slopes were statistically similar, males and females were grouped for each stream in the subsequent analysis. Linearized equations of the LWR were performed to compare the slopes (b) obtained for immatures and adults of the different streams, using the PAST 4.08 software (Hammer et al., 2001Hammer, O.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paelontological Statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9p. https://doi.org/10.1590/1982-0224-20180120.
https://doi.org/10.1590/1982-0224-201801...
). The coefficient of determination R² was used as a measure of the strength of the straight-line relationship.

The allometric condition factor (K = W/Lb) was assessed for comparisons among adults (females and males) and immatures (Le Cren, 1951Le Cren, E.D. 1951. The length-weight relationship and seasonal cycle in gonad weight and conditions in the perch (Perca fluviatilis). Journal of Animal Ecology, 20(2): 201-219.; Weatherley, 1972Weatherley, A.H. 1972. Growth and ecology of fish populations. London, Academic Press.) from the different streams, where b is the allometry coefficient related with the form of the individuals’ growth calculated from the length-weight relationship. A Student t-test (one-tailed; p < 0.025) was performed to test whether the estimated b values differed significantly from a value of 3. The species growth was considered isometric when the value of b = 3, and allometric when this value was lower or higher than 3 (Ricker & Carter, 1958Ricker, W.E. & Carter, N.M. 1958. Handbook of computations for biological statistics of fish populations, Bullletin. Fishery Research Board of Canada, 119.).

Data analysis

We performed a Principal Component Analysis (PCA) from the linear correlation matrix of the environmental variables on the PC-ORD v.6.0 software (McCune & Mefford, 2011McCune, B. & Mefford, M.J. 2011. PC-ORD. Multivariate Analysis of Ecological Data. Version 6.0 MjM Software, Gleneden Beach, Oregon, U.S.A.). Data in percentage were arcsin square-root transformed, and the axes retained for interpretation chosen through the Broken-stick criterion (McCune & Mefford, 2011McCune, B. & Mefford, M.J. 2011. PC-ORD. Multivariate Analysis of Ecological Data. Version 6.0 MjM Software, Gleneden Beach, Oregon, U.S.A.).

The Shapiro-Wilks test of normality and Levene’s test of homoscedasticity were used to determine whether parametric ANOVA or the non-parametric Kruskal-Wallis test should be used to test for differences between mean oocyte diameter, gonadal-somatic index, condition factor and total length of females, males and immatures. When data fit assumptions of normality and/or homogeneity of variance, we employed a one-way ANOVA considering the streams as independent samples. A post hoc Tukey test was used to determine which streams showed significant differences (p < 0.05). For non-parametric data, the Kruskal-Wallis ANOVA and Dunn’s post-hoc test were employed. A chi-square test (α = 0.05) was applied to verify the existence of significant differences between the number of males and females, and a ‘two sample’ t-test to compare mean lengths between males and females (grouped streams), with significance at the 5% level. All analyses were performed with PAST 4.08 software (Hammer et al., 2001Hammer, O.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paelontological Statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9p. https://doi.org/10.1590/1982-0224-20180120.
https://doi.org/10.1590/1982-0224-201801...
).

RESULTS

Environmental variables presented high variation among sites as shown by Table 2 and Fig. 3. The first PCA axis retained for interpretation (eigenvalue = 2.78) explained 27.9% of total variance, and the second axis (eigenvalue = 2.64) 26.4% (Fig. 3). Axis 1 reflected habitat characteristics related to substrate type, with sand (r = 0.950) and silt/clay (-0.834) showing the highest loadings, to which P5 was associated. Sites from the Itaguaré and Itapanhaú sub-basins (MP, JP1, JP2) were associated to high canopy and pH on the positive side of Axis 2, while most of the sites of the Guaratuba sub-basin were related to higher temperature (r = -0.863) and leaf banks (r = -0.698) on the negative side.

Figure 3
Principal Components Analysis (PCA) plot of environmental variables measured at 10 blackwater streams in the Baixada Santista and Northern Coast Basins, São Paulo state. Environmental variables are indicated by vectors. DOC = Dissolved Organic Carbon; Temp = Temperature; C = Conductivity; DO = Dissolved Oxygen; HC = High Canopy; S = Sand; SC = Silt/Clay; LB = Leaf Banks; OV = Overhanging vegetation. For stream acronyms see Table 1.

Table 2
Basic environmental characteristics of ten coastal blackwater streams sampled in in the municipalities of Bertioga and São Sebastião, SP, in the low pluviosity season, indicating the range of values, mean and Standard Deviation (SD).

A total of 185 specimens were analyzed, comprising 82 adults (37 males and 45 females) and 103 immature individuals. Mean length of females and males was similar among streams (Table 3), while for immatures, the Kruskal-Wallis test indicated significant differences among sites. The highest values were observed in streams P2, P3 and MP (Table 4). The two sample t-test on mean length between males and females, showed no significant differences between them (t = 0.229; p = 0.81).

Table 3
Intraspecific variation of life-history traits in streams where mature adults of Hollandichthys multifasciatus were found, and results of the ANOVA and Chi-Squared test (χ²). F = Females; M = Males; GSI = Gonado-Somatic Index; RF = Relative Fecundity; AF = Absolute Fecundity. Means with different superscripts were significantly different (p < 0.05). For stream acronyms see Table 1.
Table 4
Intraspecific variation of mean length and condition factor (K) in streams where immature specimens of Hollandichthys multifasciatus were obtained, and results of the Kruskal-Wallis (H) test. Means with different superscripts were significantly different (p < 0.05). For stream acronyms see Table 1.

The sex ratio (male: female) varied among streams, however the values did not depart significantly from the expected 1:1 ratio in the different streams according to the χ² test (p ≥ 0.05). The mean Gonadosomatic Somatic Index (GSI) of the females was similar between stream samples, while significant differences were found between males according to the ANOVA (Table 3). The mean absolute fecundity for 25 females varied between 604 and 708 oocytes (SD = 98.7) and the relative fecundity between 132 and 192 oocytes (SD = 65.3). ANOVA did not show significant differences between these variables among streams (Table 3).

The condition factor of mature adults was significantly different among streams as indicated by the ANOVA, with exception of P4 and P6 from the Guaratuba sub-basin (Table 3). For immatures, the condition factor also differed significantly among streams, as shown by the Kruskal-Wallis test (Table 4), with highest value observed at MP (0.068) and the lowest value at JP2 (1.3 × 10-5). Dunn?s post hoc comparisons showed that P1 and P2 presented similar values.

Fecundity data was obtained from the analysis of 25 mature females which ranged from 58.0 to 99?mm TL. They were obtained at streams P2 (N = 4), P3 (N = 3), P4 (N = 10), P5 (N = 4), P6 (N = 4). Oocyte diameter varied from 0.35 mm to 0.90 mm, showing a more developed group ready to be released, with mode at 0.6 mm observed in all streams (Fig. 4).

Figure 4
Frequency distribution of oocytes diameter (mm) of mature females of Hollandichthys multifasciatus sampled at the different coastal blackwater streams in the Baixada Santista and Northern Coast Basins, São Paulo state. P2 (N = 4); P3 (N = 3); P4 (N = 10); P5 (N = 4); P6 (N = 4).

The high coefficient of determination values obtained in the assessment of LWRs for adults and immatures at the different streams indicated a good quality of the prediction of the linear regression for (R² > 0.88) (Table 5). The slope test (b) between the LWR obtained for the different streams indicated no significant differences between adults (p = 0.259), but significant differences between immatures (p = 0.001). The b coefficient, which is indicative of the type of growth, varied from 2.7 to 3.09 for adults (males and females) and 1.04 to 3.01 for immatures. The growth was predominantly isometric in streams P4, BB1, P2 and P6, and allometric in P5, JP1, P1 and MP.

Table 5
Coefficients of the length-weight regressions of mature adults (females + males) (A) and immatures (B), according to the equation: log (TW) = log (a) + b * log (TL), where “a” is the intercept (coefficient related to condition factor), “b” is the regression coefficient (indicative of growth type), and R² is the coefficient of determination, or proportion of variance explained by the model; t = t-test for the results of b values compared to the theoretical value (b = 3, p < 0.025). For stream acronyms see Table 1.

DISCUSSION

Streams were located in preserved areas with some heterogeneity of environmental conditions, which distinguished streams from the Guaratuba sub-basin from the other sub-basins due to higher values of temperature and leaf banks. Compared to other Atlantic Forest coastal plain rivers (Ferreira et al., 2014Ferreira, F.C.; Silva, A.T.; Gonçalves, C.D.S. & Petrere-Jr., M. 2014. Disentangling the influences of habitat structure and limnological predictors on stream fish communities of a coastal basin, southeastern Brazil. Neotropical Ichthyology, 12(1): 177-186. https://doi.org/10.1590/S1679-62252014000100019.
https://doi.org/10.1590/S1679-6225201400...
), lower values of pH and higher conductivity were observed in our study. For DOC values, no information was found for Atlantic Forest backwater streams, but when they are compared to those observed in blackwaters of the Rio Negro, the major tributary to the Amazon, we obtained higher values than Duarte et al. (2016Duarte, R.M.; Smith, D.; Val, A.L. & Wood, C.M. 2016. Dissolved organic carbon from the upper Rio Negro protects zebrafish (Danio rerio) against ionoregulatory disturbances caused by low pH exposure. Scientific Reports, 6: (20377): 1-10. https://doi.org/10.1038/srep20377.
https://doi.org/10.1038/srep20377...
), who recorded concentrations between 8-12 mg C L-1, but up to 35 mg C L-1.

Most of the analyzed life-history traits of H. multifasciatus were similar among streams, suggesting that site-specific factors did not influence size of adults, maturation, sex ratio or fecundity. Resource availability seems to play an important role in life-history aspects of different species, being considered theoretically a potent agent of selection on life history traits (Grether et al., 2001Grether, G.F.; Millie, D.F.; Bryant, M.J.; Reznick, D.N. & Mayea, W. 2001. Rain Forest Canopy Cover, Resource Availability, and Life History Evolution in Guppies. Ecology, 82(6): 1546. https://doi.org/10.2307/2679799.
https://doi.org/10.2307/2679799...
). High levels of dissolved organic carbon (DOC) reduce ecosystem productivity and resource availability (Craig et al., 2015Craig, N.; Jones, S.E.; Weidel, B.C. & Solomon, C.T. 2015. Habitat, not resource availability, limits consumer production in lake ecosystems. Limnology and Oceanography, 60(6): 2079-2089. https://doi.org/10.1002/lno.10153.
https://doi.org/10.1002/lno.10153...
), and such relations were observed by Craig et al. (2017Craig, N.; Jones, S.E.; Weidel, B.C. & Solomon, C.T. 2017. Life history constraints explain negative relationship between fish productivity and dissolved organic carbon in lakes. Ecology and Evolution, 7(16): 6201-6209. https://doi.org/10.1002/ece3.3108.
https://doi.org/10.1002/ece3.3108...
) for populations of bluegill (Lepomis macrochirus). They found a strong negative relationship between maximum size and DOC concentration and lower fecundity in a set of lakes with DOC concentrations ranging from 3 to 24 mg. L-1. Guppies (Poecilia reticulata Peters, 1859) from Trinidad streams living in resource-rich streams were able to grow faster, reach larger sizes, and allocate more resources to reproduction (Grether et al., 2001Grether, G.F.; Millie, D.F.; Bryant, M.J.; Reznick, D.N. & Mayea, W. 2001. Rain Forest Canopy Cover, Resource Availability, and Life History Evolution in Guppies. Ecology, 82(6): 1546. https://doi.org/10.2307/2679799.
https://doi.org/10.2307/2679799...
), and in this case, stream differences in canopy cover could translate into stream differences in resource availability. Although these aspects must be further investigated in blackwater streams, the similarity in the several life-history traits of H. multifasciatus, suggests that the preserved riparian conditions of the different streams may be more important than the high DOC levels in determining resource availability for this species. This may be explained by the food habits of H. multifasciatus, which is considered an omnivorous species that consumes great proportions of plants and terrestrial insects, due to its surface picking behavior (Abilhoa et al., 2009Abilhoa, V.; Bornatowski, H. & Otto, G. 2009. Temporal and ontogenetic variations in feeding habits of Hollandichthys multifasciatus (Teleostei: Characidae) in coastal Atlantic rainforest streams, southern Brazil. Neotropical Ichthyology, 7(3): 415-420. https://doi.org/10.1590/S1679-62252009005000001.
https://doi.org/10.1590/S1679-6225200900...
).

We observed that mature females with vitellogenic oocytes displayed a similar spawning pattern among sites during the sampling period, suggesting that mature oocytes are spawned at once within this reproductive event. This agrees with Lemos (2019Lemos, C.A. 2019. Biologia de populações de peixes do Riachos da Vila de Itatinga, Bertioga, São Paulo (Doctoral Thesis). Universidade Federal de São Carlos, São Carlos (SP).) who found that H. multifasciatus had high frequencies of mature females in the rainy and dry seasons in coastal streams of Bertioga (SP). Frequency distribution of oocyte diameter indicated total spawning, and size was higher than that observed by Oliveira (2019Oliveira, I.F. 2019. Aspectos reprodutivos do lambari-listrado Hollandichthys multifasciatus (Characiformes: Characidae) de riachos Costeiros da Mata Atlântica, São Paulo, Brasil. (Undergraduate Monography), Universidade Estadual Paulista, Rio Claro.) for this species (0.15-0.7 mm). Nevertheless, fecundity was lower than the mean values recorded by this author in clear and blackwater Atlantic Forest streams (860.2), which may be attributed to a higher size attained by the species in their study, since larger fish have large gonads and consequently can produce more oocytes and more offspring (Wootton, 1992Wootton, R.J. 1992. Life-Histories and Population Dynamics. In: Fish Ecology. Dordrecht, Springer. p. 132-160. https://doi.org/10.1007/978-94-011-3832-1_6.
https://doi.org/10.1007/978-94-011-3832-...
). Observed fecundity values can be considered low when compared to non-inseminating characids, as found by Mazzoni et al. (2005Mazzoni, R.; Mendonça, R.S. & Caramaschi, E.P. 2005. Reproductive biology of Astyanax janeiroensis (Osteichthyes, Characidae) from the Ubatiba River, Maricá, RJ, Brazil. Brazilian Journal of Biology, 65(4): 643-649. https://doi.org/10.1590/S1519-69842005000400012.
https://doi.org/10.1590/S1519-6984200500...
) for Astyanax janeiroensis Eigenmann, 1908 (3.169-18.714 oocytes) in coastal streams of Rio de Janeiro State. This may be explained by the fact that among small sized species, lower relative fecundity values may be associated with the presence and efficiency of insemination (Azevedo, 2010Azevedo, M.A. 2010. Reproductive characteristics of characid fish species (Teleostei, Characiformes) and their relationship with body size and phylogeny. Iheringia, Série Zoologia, 100(4): 469-482. https://doi.org/10.1590/S0073-47212010000400020.
https://doi.org/10.1590/S0073-4721201000...
).

Environmental factors may also regulate variations in either egg size or number between and within populations of freshwater fish, as reported by Lobón-Cerviá et al. (1997Lobón-Cerviá, J.; Utrilla, C.G.; Rincón, P.A. & Amezcua, F. 1997. Environmentally induced spatio-temporal variations in the fecundity of brown trout Salmo trutta: Trade-offs between egg size and number. Freshwater Biology, 38(2): 277-288. https://doi.org/10.1046/j.1365-2427.1997.00217.x.
https://doi.org/10.1046/j.1365-2427.1997...
), who found that trout at sites which were fully covered by canopy spawned fewer, but larger, eggs than fast-growers in unshaded sites. In coastal streams, rainfall regime may be considered an important factor as pointed out by Menezes & Caramaschi (1994Menezes, M.S. de & Caramaschi, E.P. 1994. Características reprodutivas de Hypostomus grupo H. punctatus no rio Ubatiba, Maricá, RJ (Osteichthyes, Siluriformes). Revista Brasileira de Biologia, 54(3): 503-513.). Braga et al. (2008Braga, M.R.; Aranha, J.M.R. & Vitule, J.R.S. 2008. Reproduction period of Mimagoniates microlepis, from an Atlantic Forest stream in southern Brazil. Brazilian Archives of Biology and Technology, 51(2): 345-351. https://doi.org/10.1590/s1516-89132008000200014.
https://doi.org/10.1590/s1516-8913200800...
) for example, reported that insemination of the Glandulocaudinae Mimagoniates microlepis (Steindachner, 1877) seems to occur in the dry season, when the habitat is reduced and encounters between males and females are most probable. As H. multifasciatus and M. microlepis are both inseminating and related species (Thomaz et al., 2010Thomaz, A.T.; Malabarba, L.R. & Bonatto, S.L. 2010. The phylogenetic placement of Hollandichthys Eigenmann, 1909 (Teleostei: Characidae) and related genera. Molecular Phylogenetics and Evolution, 57(3): 1347-1352. https://doi.org/10.1016/j.ympev.2010.10.006.
https://doi.org/10.1016/j.ympev.2010.10....
), it is possible that the low water level during the period of our study may also influence the reproductive behavior of H. multifasciatus.

The condition factor of adults, immatures and the mean length of immatures were the only parameters that showed intraspecific variations, which can be related to differences in such factors as temperature and food supply, as condition factor is an index that indicates the “well-being” of the fish (Froese, 2006Froese, R. 2006. Cube law, condition factor and weight-length relationships: History, meta-analysis and recommendations. Journal of Applied Ichthyology, 22(4): 241-53. https://doi.org/10.1111/j.1439-0426.2006.00805.x.
https://doi.org/10.1111/j.1439-0426.2006...
). The higher condition factor observed for immatures suggests that they are in a rapid growth phase, directing the feeding resources to their growth. This has been observed for other Neotropical species, as several characids in the Upper Paraná River floodplain (Lizama & Ambrósio, 2002Lizama, M.L. & Ambrósio, A.M. 2002. Condition factor in nine species of fish of the Characidae family in the Upper Paraná river floodplain, Brazil. Brazilian Journal of Biology, 62(1): 113-124. https://doi.org/10.1590/S1519-69842002000100014.
https://doi.org/10.1590/S1519-6984200200...
) and Micropogonias furnieri (Desmarest, 1823), with higher condition independent of the time and distribution area (Costa & Araújo, 2003Costa, M.R. da & Araújo, F.G. 2003. Length-weight relationship and condition factor of Micropogonias furnieri (Desmarest) (Perciformes, Sciaenidae) in the Sepetiba Bay, Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia, 20(4): 685-690. https://doi.org/10.1590/s0101-81752003000400022.
https://doi.org/10.1590/s0101-8175200300...
).

Spatial differences in the condition factor among adults were observed even at nearby streams like P2 and P4, which showed similar environmental conditions, suggesting that site-specific factors other than food availability may have influenced these values. In fact, differences in the condition factor have been interpreted as a measure of several biological events, such as fat reserves, adaptation to the environment and gonadal development (Le Cren, 1951Le Cren, E.D. 1951. The length-weight relationship and seasonal cycle in gonad weight and conditions in the perch (Perca fluviatilis). Journal of Animal Ecology, 20(2): 201-219.). It is known that fish usually decrease their feeding activity and use their lipid reserves during spawning which results in a decrease in condition (Lizama & Ambrósio, 2002Lizama, M.L. & Ambrósio, A.M. 2002. Condition factor in nine species of fish of the Characidae family in the Upper Paraná river floodplain, Brazil. Brazilian Journal of Biology, 62(1): 113-124. https://doi.org/10.1590/S1519-69842002000100014.
https://doi.org/10.1590/S1519-6984200200...
). Thus, it is possible that the observed dissimilarities in condition were related to differences in growth and/or breeding of fish between localities, as confirmed by the difference in slopes of the LWR for immatures. Similar observations were found for trout, by Lobón-Cerviá & Rincón (1998Lobón-Cerviá, J. & Rincón, P.A. 1998. Field Assessment of the Influence of Temperature on Growth Rate in a Brown Trout Population. Transactions of the American Fisheries Society, 127(5): 718-728. https://doi.org/10.1577/1548-8659(1998)127<0718:FAOTIO>2.0.CO;2.
https://doi.org/10.1577/1548-8659(1998)1...
) who observed differences in growth between localities 1-2 km apart.

It can be concluded that H. multifasciatus showed few intraspecific variations of the analyzed life-history traits under natural conditions during the low precipitation period, despite variations in some environmental conditions among sub-basins. Although other aspects of the biology of H. multifasciatus should be further investigated, the obtained results may help to document natural variations of traits of an endemic fish species, providing foundation for future efforts to examine the biotic and abiotic factors associated with the life histories of imperiled fishes.

ACKNOWLEDGMENTS

We thank Maria Letizia Petesse for comments on the manuscript. We also thank Maressa Helena Nanini Costa, Marcelo Horikoshi Candido da Silva, Sergio Luiz da Silva, Ronaldo de Flores Bernardino, Luiz Evangelista and Renato Horikoshi Candido da Silva for help in the fieldwork. João Batista Pinheiro da Silva, Marizete Ramos dos Santos and Bolivar Barbanti assisted us during the collections. The Peralta group allowed us to perform part of the study on their property. We thank the Forestry Institute of São Paulo State (SMA Process: 30 260108-003286/2016). Permissions for collecting specimens and experimentation were granted by ICMBio/SISBIO (Nº 54432-1) and the Animal Experimentation Ethics Committee from the Fisheries Institute (Nº 05/2016), respectively.

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  • FUNDING INFORMATION: Funding for this work was provided by FAPESP (grant #2015/26728-6). VCC was funded by CNPq (PIBIC #03/2018).
  • Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP"
  • Erratum

    In the article "Life-History traits of Hollandichthys multifascitus (Eigenmann & Norris, 1900) (Characiformes: Characidae) in coastal Atlantic Forest blackwater streams from Southeastern Brazil", http://doi.org/10.11606/1807-0205/2022.62.016, published in the Journal Papéis Avulsos de Zoologia, Volume 62: e202262016,
    In the title:
    Where you read:
    Life-History traits of Hollandichthys multifascitus (Eigenmann & Norris, 1900) (Characiformes: Characidae) in coastal Atlantic Forest blackwater streams from Southeastern Brazil
    Read it:
    Life-History traits of Hollandichthys multifasciatus (Eigenmann & Norris, 1900) (Characiformes: Characidae) in coastal Atlantic Forest blackwater streams from Southeastern Brazil

Edited by

EDITED BY: Murilo Nogueira de Lima Pastana.

Publication Dates

  • Publication in this collection
    16 May 2022
  • Date of issue
    2022

History

  • Received
    11 Aug 2021
  • Accepted
    17 Dec 2021
  • Published
    10 Mar 2022
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