Abstract

The objective of this study was to provide a comprehensive list of the fish fauna of headwater streams of the Miranda River in the Upper Paraguay River Basin. Our primary data set was constructed from sampling of fish using a rectangular sieve, trawl, and gill nets from 2004 to 2015. Our secondary data were derived from published reports conducted in the Miranda River Basin, in addition to taxonomic and distribution data from other studies conducted in the basin. All data were compiled, which in the end encompassed a period from 1999 to 2015. The datasets yielded a total of 143 species, 104 from the primary data (72.7%) and 39 from the secondary data (27.3%). Species were distributed among seven orders and 30 families were found in the Miranda River Basin. Characiformes and Siluriformes were the predominant orders, and the families Characidae and Loricariidae had the greatest number of species. Our results indicate a greater number of species compared to other studies of the Upper Paraguay Basin headwaters, likely due to the longer time frame covered by our primary and secondary datasets.

Keywords:
Species List; Pantanal; streams ichthyofauna; plateau; Paraguay basin

Resumo

O objetivo deste trabalho é o de prover uma listagem da ictiofauna de riachos de cabeceira da bacia do Rio Miranda, Alto Rio Paraguai. Os peixes foram amostrados utilizando uma peneira retangular, rede de arrasto e rede de espera no período de 2004 a 2015, além disso, outros trabalhos realizados na bacia do Rio Miranda foram compilados e adicionados na listagem total, assim como, artigos de descrição e distribuição de espécies amostradas na bacia compreendendo o período de 1999 a 2015. A bacia do Rio Miranda apresentou um total de 143 espécies, 104 espécies oriundas de dados primários (72,7%) e 39 de dados secundários (27,3%). As espécies estão distribuídas em sete ordens e 30 famílias. Characiformes e Siluriformes foram as ordens predominantes e as famílias Characidae e Loricariidae apresentaram maior número de espécies. Os resultados obtidos neste estudo demonstram um maior número de espécies quando comparados com outros estudos realizados em cabeceiras na bacia do Alto Rio Paraguai decorrente ao longo período de estudo.

Palavras-chave:
Lista de espécies; Pantanal; ictiofauna de riachos; planalto; bacia do Paraguai

Introduction

The Paraguay River Basin is an important drainage of the La Plata River Basin (Lowe-McConnell 1999), and occupies a total area of about 496,000 km² (Junk et al. 2006JUNK, W.J., CUNHA, C.N., WANTZEN, K.M., PETERMANN, P., STRÜSSMANN, C., MARQUES, M.I. & ADIS, J. 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68: 278-309. doi: http://dx.doi.org/10.1007/s00027-006-0851-4.
http://dx.doi.org/10.1007/s00027-006-085... ). The Brazilian Pantanal has a total area of approximately 361,700 km², with 72.7% of the total territory lying in Brazil and the remainder in Bolivia and Paraguay. The upper Paraguay basin in Brazilian divided into two distinct regions: a floodplain known as the ‘Pantanal’, which at approximately 138,200 km² constitutes one of the largest wetland areas in the world; and a plateau comprised of areas with altitudes greater than 200 m encompassing approximately 223,500 km² (Silva & Abdon 1998SILVA, J.S.V. & ABDON, M.M. 1998. Delimitação do Pantanal Brasileiro e suas sub-regiões. Pesq. Agropec. Bras. 33: 1703-1711.). These two regions are distinguished by geological and geomorphological characteristics, however they are also interdependent since the headwaters of the most important rivers draining into the Pantanal are in the plateau region, resulting in strong hydrologic connectivity (Willink et al. 2000WILLINK, P.W., FROEHLICH, O., MACHADO-ALISSON, A., MENEZES, N., OYAKAWA, O., CATELLA, A., CHERNOFF, B., LIMA, F.C.T., TOLEDO-PIZA, M., HORTEGA, H., ZANATA, A.M. & BARRIGA, R. 2000. Diversidade, distribuição e habitats críticos dos peixes dos rios: Negro, Negrinho, Taboco, Taquari e Miranda, e sua importância para conservação e desenvolvimento sustentável do Pantanal, Mato Grosso do Sul, Brasil. Pp. 63-81. In: WILLINK, P. W., CHERNOFF, B., ALONSO, L., MONTAMBAULT, J.R. & LOURIVAL, R. (eds). RAP Bulletin of Biological Assesment, 18: Uma Avaliação Biológica dos Ecossistemas Aquáticos do Pantanal, Mato Grosso do Sul, Brasil. Conservation International, Washington., Teresa et al. 2010TERESA, F.B., ROMERO, R.M. & LANGEANI, F. 2010. Pisces, Aquidauana and Miranda drainages, upper Paraguay River basin, Mato Grosso do Sul, Brazil. Check List 6(4): 596-601.).

Approximately 270 fish species have been identified in the Paraguay River Basin (Britski et al. 2007BRITSKI, H.A., SILIMON, K.Z.S. & LOPES, B.S. 2007. Peixes do Pantanal: manual de identificação. 2 ed. Embrapa, Brasília, 227p.). However, the total number of species would likely be higher if the plateau streams had been included (Alho & Sabino 2012ALHO, C.J.R. & SABINO, J. 2012. Seasonal Pantanal flood pulse: implications for biodiversity conservation – A review. Oecol. Aust. 16(4): 958-978. doi: http://dx.doi.org/10.4257/oeco.2012.1604.17.
http://dx.doi.org/10.4257/oeco.2012.1604... ). Numerous studies have been carried out in the basin over the past two decades, including the floodplain region (Catella & Petrere-Jr 1996CATELLA, A.C. & PETRERE-JR, M. 1996. Feeding patterns in a fish community of Baia da Onça, a foodplain lake of the Aquidauana River, Pantanal, Brazil. Fisheries Manag Ecol 3: 229-237., Willink et al. 2000WILLINK, P.W., FROEHLICH, O., MACHADO-ALISSON, A., MENEZES, N., OYAKAWA, O., CATELLA, A., CHERNOFF, B., LIMA, F.C.T., TOLEDO-PIZA, M., HORTEGA, H., ZANATA, A.M. & BARRIGA, R. 2000. Diversidade, distribuição e habitats críticos dos peixes dos rios: Negro, Negrinho, Taboco, Taquari e Miranda, e sua importância para conservação e desenvolvimento sustentável do Pantanal, Mato Grosso do Sul, Brasil. Pp. 63-81. In: WILLINK, P. W., CHERNOFF, B., ALONSO, L., MONTAMBAULT, J.R. & LOURIVAL, R. (eds). RAP Bulletin of Biological Assesment, 18: Uma Avaliação Biológica dos Ecossistemas Aquáticos do Pantanal, Mato Grosso do Sul, Brasil. Conservation International, Washington., Junk et al. 2006JUNK, W.J., CUNHA, C.N., WANTZEN, K.M., PETERMANN, P., STRÜSSMANN, C., MARQUES, M.I. & ADIS, J. 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68: 278-309. doi: http://dx.doi.org/10.1007/s00027-006-0851-4.
http://dx.doi.org/10.1007/s00027-006-085... , Baginski et al. 2007BAGINSKI, L.J., FLORENTINO, A.C., FERNANDES, I.M., PENHA, J.M.P. & MATEUS, L.A.F. 2007 The spatial and temporal dimension of fish diversity of the vegetated littoral zone of marginal lagoons of the Cuiabá river floodplain, Pantanal, Brazil. Biota Neotrop 7(3): 233-238. http://www.biotaneotropica.org.br/v7n3/pt/abstract?article+bn04007032007 (Accessed 24 Jun 2016).
http://www.biotaneotropica.org.br/v7n3/p... , Pacheco & Silva 2009PACHECO, E.B. & SILVA, C.J. 2009. Fish associated with aquatic macrophytes in the Chacororé-Sinhá Mariana lake system and Mutum River, Pantanal of Mato Grosso Brazil. Braz J Biol 69(1): 101-108. doi: http://dx.doi.org/10.1590/S1519-69842009000100012.
http://dx.doi.org/10.1590/S1519-69842009... , Pains-Silva et al. 2010PAINS-SILVA, H., PETRY, A.C. & DA SILVA, C.J. 2010. Fish communities of the Pantanal wetland in Brazil: evaluating the effects of the Upper Paraguay River flood pulse on baía Caiçara fish fauna. Aquat Ecol 44: 275-288. doi: http://dx.doi.org/10.1007/s10452-009-9289-9.
http://dx.doi.org/10.1007/s10452-009-928... , Tondato et al. 2013TONDATO, K.K., FANTIN-CRUZ, I., PEDROLLO, O.C., SÚAREZ, Y.R. 2013.Spatial distribution of fish assemblages along environmental gradients in the temporary ponds of Northern Pantanal, Brazil. J Limnol 71(1): 95-102. doi: http://dx.doi.org/10.4081/jlimnol.2013.e8.
http://dx.doi.org/10.4081/jlimnol.2013.e... , Súarez et al. 2013SÚAREZ, Y.R., FERREIRA, F.S. & TONDATO, K.K. 2013. Assemblage of fish species associated with aquatic macrophytes in Porto Murtinho Pantanal, Mato Grosso do Sul, Brazil. Biota Neotrop 13(2): 182-189. http://www.biotaneotropica.org.br/v13n2/en/abstract?inventory+bn02313022013 (Accessed 24 Jun 2016)
http://www.biotaneotropica.org.br/v13n2/... , Pains-Silva et al. 2014PAINS-SILVA, H., SOUZA, F. & CORRÊA, F. 2014. Icththyofauna of the Bento Gomes River in the Pantanal Matogrossense, Brazil. Panamjas 9(1): 48-53., Polaz et al. 2014POLAZ, C.N.M., MELO, B.F., BRITZKE, R., RESENDE, E.K., MACHDO, F.A., LIMA, J.A.F. & PETRERE JR, M. 2014. Fishes from the Parque Nacional do Pantanal Matogrossense, upper Paraguai River basin, Brazil. Check List 10(1): 122-130. doi: http://dx.doi.org/10.15560/10.1.122.
http://dx.doi.org/10.15560/10.1.122... , Botini et al. 2015BOTINI, A.F., BARROS, C.A., SOUZA, T.H., BOTINI, N., MOURA, N.A. 2015. Diversidade de peixes no Rio Mutum e baía marginal no Pantanal – Matogrossense através da coleta ativa. Enciclop Biosf 11(21): 2183-2197. and Severo-Neto et al. 2015SEVERO-NETO, F., TENCATT, L.F.C., COSTA-PEREIRA, R. & TAVARES, L.E.R. 2015. Fishes from Baía da Medalha, southern Pantanal, Brazil: A 20 years review. Biota Neotrop 15(2): 1-9. doi: http://dx.doi.org/10.1590/1676-06032015011614.
http://dx.doi.org/10.1590/1676-060320150... ) and plateau waters (Súarez et al. 2007SÚAREZ, Y.R., VALÉRIO, S.B., TONDATO, K.K., FLORENTINO, A.C., FELIPE, T.R.A., XIMENES, L.Q.L. & LOURENÇO, L.S. 2007. Fish species diversity in headwaters streams of Paraguay and Paraná basins. Braz Arch Biol Techn 50(6): 1033-1042. doi: http://dx.doi.org/10.1590-89132007000700014.
http://dx.doi.org/10.1590-89132007000700... , Terra & Sabino 2007TERRA, L.C.C. & SABINO, J. 2007. Composição da ictiofauna de dois riachos, com diferentes graus de conservação, na bacia do Rio Formoso, município de Bonito, Mato Grosso do Sul, Brasil. Redalyc 11(1): 49-58. http://www.redalyc.org/articulo.oa?id=26012838005 (Accessed 24 Jun 2016).
http://www.redalyc.org/articulo.oa?id=26... , Teresa et al. 2010TERESA, F.B., ROMERO, R.M. & LANGEANI, F. 2010. Pisces, Aquidauana and Miranda drainages, upper Paraguay River basin, Mato Grosso do Sul, Brazil. Check List 6(4): 596-601., Casatti et al. 2010CASATTI, L., ROMERO, R.M., TERESA, F.B., SABINO, J. & LANGEANI, F. 2010. Fish community structure along a conservation gradient in Bodoquena Plateau streams, central West of Brazil. Acta Limnol Brasil 22(1): 50-59. doi: http://dx.doi.org/10.4322/actalb.02201007.
http://dx.doi.org/10.4322/actalb.0220100... , Teresa & Romero 2010TERESA, F.B. & ROMERO, R.M. 2010. Influence of the riparian zone phytophysiognomies on the longitudinal distribution of fishes: evidence from a Brazilian savanna stream. Neotrop Ichthyol 8(1): 163-170. doi: http://dx.doi.org/10.1590/S1679-62252010000100019.
http://dx.doi.org/10.1590/S1679-62252010... , Castro & Vizzotto 2013CASTRO, R.J. & VIZZOTTO, P.C. 2013. Fishes of the Vermelho River, São Lourenço River basin, MatoGrosso state, Brazil. Check List 9(1): 001-003., Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292. and Oliveira et al. 2015OLIVEIRA, V.A., MATEUS, L.A., LOVERDE-OLIVEIRA, S. & PIETRO-SOUZA, W. 2015. Fish from urban tributaries to the Vermelho River, upper Paraguay River Basin, Mato Grosso, Brazil. Check List 11(1): 1-6. doi: http://dx.doi.org/10.15560/11.1.1516.
http://dx.doi.org/10.15560/11.1.1516... ). In studies of the plateau portion of the basin, analyses at small spatial scales were the predominant.

Compared to Brazilian hydrographic basins (e.g. the Upper Paraná River system), the fish fauna of central Brazil is poorly described (Casatti et al. 2010CASATTI, L., ROMERO, R.M., TERESA, F.B., SABINO, J. & LANGEANI, F. 2010. Fish community structure along a conservation gradient in Bodoquena Plateau streams, central West of Brazil. Acta Limnol Brasil 22(1): 50-59. doi: http://dx.doi.org/10.4322/actalb.02201007.
http://dx.doi.org/10.4322/actalb.0220100... ). Despite being a hotspot for endemic fauna (Willink et al. 2000WILLINK, P.W., FROEHLICH, O., MACHADO-ALISSON, A., MENEZES, N., OYAKAWA, O., CATELLA, A., CHERNOFF, B., LIMA, F.C.T., TOLEDO-PIZA, M., HORTEGA, H., ZANATA, A.M. & BARRIGA, R. 2000. Diversidade, distribuição e habitats críticos dos peixes dos rios: Negro, Negrinho, Taboco, Taquari e Miranda, e sua importância para conservação e desenvolvimento sustentável do Pantanal, Mato Grosso do Sul, Brasil. Pp. 63-81. In: WILLINK, P. W., CHERNOFF, B., ALONSO, L., MONTAMBAULT, J.R. & LOURIVAL, R. (eds). RAP Bulletin of Biological Assesment, 18: Uma Avaliação Biológica dos Ecossistemas Aquáticos do Pantanal, Mato Grosso do Sul, Brasil. Conservation International, Washington.) the main Pantanal headwater streams are understudied. The goal of this study was thus to describe the ichthyofauna of plateau region streams of the Miranda River Basin by combining primary and secondary data compiled from previous studies on the basin.

Materials and Methods

1. Study site

The Miranda River Basin is entirely within the limits of the Brazilian region, in Mato Grosso do Sul State. The total basin area is 42,993.83 km², with Serra da Bodoquena as the western boundary and the Paraguay River as the northwestern boundary (Plano de Recursos Hídricos da Bacia Hidrográfica do Rio Miranda 2014PLANO DE RECURSOS HÍDRICOS DA BACIA HIDROGRÁFICA DO RIO MIRANDA. 2014. http://www.imasul.ms.gov.br/wp-content/uploads/sites/74/2015/06/Diagn%C3%B3stico-Final-Plano-de-Bacia-Miranda.pdf (Acessed 20 May 2017).
http://www.imasul.ms.gov.br/wp-content/u... ). The main tributaries are the Miranda and Aquidauana Rivers. The rivers and streams of the Aquidauana and Miranda Rivers flow into the Brazilian Cerrado (savanna), which is composed of patches of deciduous, semi-deciduous, and riparian forest that vary in density depending on the ecological drainage system in which they lie (Jesus 2003JESUS, F. 2003. Classificação dos ecossistemas aquáticos do Pantanal e da bacia do Alto Paraguai. Brasília: The Nature Conservancy. p. 136., Junk et al. 2006JUNK, W.J., CUNHA, C.N., WANTZEN, K.M., PETERMANN, P., STRÜSSMANN, C., MARQUES, M.I. & ADIS, J. 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68: 278-309. doi: http://dx.doi.org/10.1007/s00027-006-0851-4.
http://dx.doi.org/10.1007/s00027-006-085... ).

Surveys were conducted at 42 sites in the Miranda River Basin from January 2004 to January 2015 (primary data). Additional secondary data were compiled from 16 collection sites from published work on stream fish assemblages in the Miranda River Basin (Willink et al. 2000WILLINK, P.W., FROEHLICH, O., MACHADO-ALISSON, A., MENEZES, N., OYAKAWA, O., CATELLA, A., CHERNOFF, B., LIMA, F.C.T., TOLEDO-PIZA, M., HORTEGA, H., ZANATA, A.M. & BARRIGA, R. 2000. Diversidade, distribuição e habitats críticos dos peixes dos rios: Negro, Negrinho, Taboco, Taquari e Miranda, e sua importância para conservação e desenvolvimento sustentável do Pantanal, Mato Grosso do Sul, Brasil. Pp. 63-81. In: WILLINK, P. W., CHERNOFF, B., ALONSO, L., MONTAMBAULT, J.R. & LOURIVAL, R. (eds). RAP Bulletin of Biological Assesment, 18: Uma Avaliação Biológica dos Ecossistemas Aquáticos do Pantanal, Mato Grosso do Sul, Brasil. Conservation International, Washington., Casatti et al. 2010CASATTI, L., ROMERO, R.M., TERESA, F.B., SABINO, J. & LANGEANI, F. 2010. Fish community structure along a conservation gradient in Bodoquena Plateau streams, central West of Brazil. Acta Limnol Brasil 22(1): 50-59. doi: http://dx.doi.org/10.4322/actalb.02201007.
http://dx.doi.org/10.4322/actalb.0220100... , Teresa et al. 2010TERESA, F.B., ROMERO, R.M. & LANGEANI, F. 2010. Pisces, Aquidauana and Miranda drainages, upper Paraguay River basin, Mato Grosso do Sul, Brazil. Check List 6(4): 596-601., Teresa & Romero 2010TERESA, F.B. & ROMERO, R.M. 2010. Influence of the riparian zone phytophysiognomies on the longitudinal distribution of fishes: evidence from a Brazilian savanna stream. Neotrop Ichthyol 8(1): 163-170. doi: http://dx.doi.org/10.1590/S1679-62252010000100019.
http://dx.doi.org/10.1590/S1679-62252010... ). These 58 sampling sites are distributed among streams from first to third order in 18 municipalities in Mato Grosso do Sul, Brazil (Figure 1). Taxonomic and distribution data from additional studies were also added to the final species list (Sabino & Trajano 1997SABINO, J. & TRAJANO, E. 1997. A new species of blind armoured catfish, genus Ancistrus, from caves of Bodoquena region, Mato Grosso do Sul, southwestern Brazil (Siluriformes, Loricariidae, Ancistrinae). Revue Fr Aquariol 23: 73-78., Willink et al. 2000WILLINK, P.W., FROEHLICH, O., MACHADO-ALISSON, A., MENEZES, N., OYAKAWA, O., CATELLA, A., CHERNOFF, B., LIMA, F.C.T., TOLEDO-PIZA, M., HORTEGA, H., ZANATA, A.M. & BARRIGA, R. 2000. Diversidade, distribuição e habitats críticos dos peixes dos rios: Negro, Negrinho, Taboco, Taquari e Miranda, e sua importância para conservação e desenvolvimento sustentável do Pantanal, Mato Grosso do Sul, Brasil. Pp. 63-81. In: WILLINK, P. W., CHERNOFF, B., ALONSO, L., MONTAMBAULT, J.R. & LOURIVAL, R. (eds). RAP Bulletin of Biological Assesment, 18: Uma Avaliação Biológica dos Ecossistemas Aquáticos do Pantanal, Mato Grosso do Sul, Brasil. Conservation International, Washington., Ribeiro et al. 2007RIBEIRO, A.C., CAVALLARO, M.R. & FROEHLICH, O. 2007. Oligosarcus perdido (Characiformes, Characidae), a new species of fresh water fish from Serra da Bodoquena, upper Rio Paraguai basin, Brazil. Zootaxa 1560: 43-53., Terra & Sabino 2007TERRA, L.C.C. & SABINO, J. 2007. Composição da ictiofauna de dois riachos, com diferentes graus de conservação, na bacia do Rio Formoso, município de Bonito, Mato Grosso do Sul, Brasil. Redalyc 11(1): 49-58. http://www.redalyc.org/articulo.oa?id=26012838005 (Accessed 24 Jun 2016).
http://www.redalyc.org/articulo.oa?id=26... , Zawadzki et al. 2014ZAWADZKI, C.H., L.F.C. TENCATT, AND O. FROEHLICH. 2014. A new unicuspid-toothed species of Hypostomus Lacépède, 1803 (Siluriformes: Loricariidae) from the rio Paraguai basin. Neotrop Ichthyol 12(1): 97-104. doi: http://dx.doi.org/10.1590/S1679-62252014000100010.
http://dx.doi.org/10.1590/S1679-62252014... , Shibatta 2016SHIBATTA, O.A. 2016. A new species of bumblebee catfish of the genus Microglanis (Siluriformes: Pseudopimelodidae) from the upper rio Paraguay basin, Brazil. Neotrop Ichthyol 14(3): e160031. http://dx.doi.org/10.1590/1982-0224-20160031.
http://dx.doi.org/10.1590/1982-0224-2016... ).

Figure 1
Locations of the sampling points in the Miranda River Basin of the Upper Paraguay River, Mato Grosso do Sul, Brazil. Black dots: Primary data; Red dots: Secondary data.

2. Sampling

For the primary data set, fish were sampled predominantly using a 0.8 x 1.2 m rectangular sieve and 5 x 1.5 m trawl nets, both with 2 mm mesh. In streams with a higher volume, sampling was supplemented with 10 x 1.5 m gill nets with mesh sizes of 15, 25, 30, 40, and 50 mm between adjacent knots. Sampled fish were anesthetized with Eugenol solution and subsequently fixed by immersion in 4% formaldehyde solution for at least 48 hours. Specimens were then washed and transferred to 70% ethanol.

Fish identification was performed mainly using the Pantanal fish identification key of Britski et al. (2007)BRITSKI, H.A., SILIMON, K.Z.S. & LOPES, B.S. 2007. Peixes do Pantanal: manual de identificação. 2 ed. Embrapa, Brasília, 227p., and specific keys were used when necessary. Voucher specimens were deposited in the fish collection at the Universidade Federal de Mato Grosso do Sul (ZUFMS/UFMS) and the Núcleo de Pesquisa em Limnologia, Ictiologia e Aquicultura at the Universidade Estadual de Maringá (Nupelia/UEM). For the secondary data set, obtained by published articles and fish collection, voucher specimens were deposited in the fish collection of the Departamento de Zoologia e Botânica at the Universidade Estadual Paulista, São José do Rio Preto (DZSJRP/UNESP), Fish collection of Laboratório de Ictiologia de Ribeirão Preto (LIRP/USP) and Fish collection of Museu de Zoologia of University of Londrina (MZUEL/UEL). Collections were authorized by IBAMA (collection permit number SISBIO; process number 13458-1). Fish classification follows Eschmeyer et al. (2017)ESCHMEYER, W.N., FRICKE, R. & VAN DER LAAN, R. (eds.). 2017. Catalog of Fishes: Genera, Species, References.http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (Accessed 20 May 2017).
http://researcharchive.calacademy.org/re... .

3. Data analysis

To evaluate sampling efficiency, the total richness in the basin was estimated using a species accumulation curve with the bootstrap method (Smith & Van Belle 1984SMITH, E.P. & VAN BELLE, G. 1984. Nonparametric estimation of species richness. Biometrics 40(1):119-129. doi: http://dx.doi.org/10.2307/2530750.
http://dx.doi.org/10.2307/2530750... ), as well as standard error using the function ‘specaccum’ in the ‘vegan’ package (Oksanen et al. 2011OKSANEN, J., BLANCHET, F.G., KINDT, R., LEGENDRE, P., O’HARA, R.B., SIMPSON, G.L., STEVENS, M.H.H. & WAGNER, H. 2011. Vegan: community ecology package. Version 1.17-11. Available from: http://vegan.r-forge.r-project.org/
http://vegan.r-forge.r-project.org/... ) in R (R Development Core Team 2013R DEVELOPMENT CORE TEAM. 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
http://www.R-project.org/... ).

Results

The datasets yielded a total of 143 species, 104 from the primary data (72.7%) and 39 from the secondary data (27.3%) data. Species were distributed among seven orders and 30 families (Table 1). Characiformes (75 species) and Siluriformes (48 species) were the predominant orders, representing together 86% of the recorded species. Among the families of these orders, the largest numbers of species were from Characidae and Loricariidae, representing 32.2% (46 species) and 15.4% (22 species) of the total sample, respectively (Figure 2).

Figure 2
Frequency of orders and families from to primary and secondary data from the Miranda River Basin of the Upper Paraguay River, Mato Grosso do Sul, Brazil.

The species accumulation curve shows that richness does not reach the asymptotic threshold (Figure 3), indicating the need for further collection efforts (i.e., increasing the number of sampling sites should increase estimates of species richness). The bootstrap method estimated approximately 169 with confidence interval (α=0.05) from 150 to 188 species, represent approximately 84.6% of the estimated by datasets (primary and secondary) the total number of species in the Miranda River basin.

Figure 3
Species accumulated curve generated from to primary and secondary data from the Miranda River Basin of the Upper Paraguay River, Mato Grosso do Sul, Brazil.

In relation the species sampled Piaractus mesopotamicus (Holmberg 1887), Pseudoplatystoma corruscans (Linnaeus 1766) are on the National List of Near-threatened Species. Furthermore Characidium aff. fasciatum Reinhardt 1866, Farlowella cf. isbrueckeri Retzer & Page 1997 are listed as data deficient. The cave fishes Ancistrus formoso Sabino & Trajano 1997 and Trichomycterus dali Rizzato, Costa, Trajano & Bichuette 2011 are listed as vulnerable. We encountered six possible new species, including Astyanax sp. 1, Astyanax sp. 2, Astyanax sp. 3, Characidium sp. 1, Imparfinis sp. 1, Imparfinis sp. 2. Six species from our data sets were reported as only being found in the Paraná River basin, such as Serrapinnus notomelas (Eigenmann 1915), Astyanax aff. fasciatus (Cuvier 1819), Imparfinis mirini Haseman 1911, Imparfinis cf. schubarti (Gomes 1956), Proloricaria prolixa Isbrücker & Nijssen 1978 and Hoplias sp. 1 from our primary data set, and Oligosarcus pintoi Campos 1945, Rineloricaria lanceolata (Günter 1868) from our secondary data set.

Discussion

Studies of fishes from the Paraguay River basin usually concentrate on the main rivers of the Pantanal region (Britski et al. 2007BRITSKI, H.A., SILIMON, K.Z.S. & LOPES, B.S. 2007. Peixes do Pantanal: manual de identificação. 2 ed. Embrapa, Brasília, 227p., Terra & Sabino 2007TERRA, L.C.C. & SABINO, J. 2007. Composição da ictiofauna de dois riachos, com diferentes graus de conservação, na bacia do Rio Formoso, município de Bonito, Mato Grosso do Sul, Brasil. Redalyc 11(1): 49-58. http://www.redalyc.org/articulo.oa?id=26012838005 (Accessed 24 Jun 2016).
http://www.redalyc.org/articulo.oa?id=26... , Polaz et al. 2014POLAZ, C.N.M., MELO, B.F., BRITZKE, R., RESENDE, E.K., MACHDO, F.A., LIMA, J.A.F. & PETRERE JR, M. 2014. Fishes from the Parque Nacional do Pantanal Matogrossense, upper Paraguai River basin, Brazil. Check List 10(1): 122-130. doi: http://dx.doi.org/10.15560/10.1.122.
http://dx.doi.org/10.15560/10.1.122... ), due mainly to the easy access into these areas, when compared to the headwaters, this makes the knowledge of the fauna of streams almost non-existent (Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292.). However, to understand the environmental structural dynamics, the accomplishment of ichthyofauna inventories and systematic studies are extremely important. Besides, they constitute the basis for better understanding the dynamics of species distribution (Vilar et al. 2011VILAR, C.C., SPACH, H.L. & SOUZA-CONCEIÇÃO, J.M. 2011. Fish assemblage in shallow areas of Baía da Babitonga, southern Brazil: structure, spatial and temporal patterns. Panamjas 6(4): 303-319.), providing data on the species composition, management and conservation (Pains-Silva et al. 2014PAINS-SILVA, H., SOUZA, F. & CORRÊA, F. 2014. Icththyofauna of the Bento Gomes River in the Pantanal Matogrossense, Brazil. Panamjas 9(1): 48-53.).

Our results showed predominance of Characiformes and Siluriformes, and the families Characidae and Loricariidae. Other studies conducted in streams of the Paraguay River Basin reported similar results (Oliveira et al. 2015OLIVEIRA, V.A., MATEUS, L.A., LOVERDE-OLIVEIRA, S. & PIETRO-SOUZA, W. 2015. Fish from urban tributaries to the Vermelho River, upper Paraguay River Basin, Mato Grosso, Brazil. Check List 11(1): 1-6. doi: http://dx.doi.org/10.15560/11.1.1516.
http://dx.doi.org/10.15560/11.1.1516... , Vizzotto & Castro 2015VIZZOTO, P.C. & CASTRO, R.J. 2015. Ichthyofauna of tributaries of the Vermelho River, upper Paraguay River basin, region of Rondonópolis, state of Mato Grosso, Brazil. Check List 11(5): 1-5. doi: http://dx.doi.org/10.15560/11.5.1750.
http://dx.doi.org/10.15560/11.5.1750... ), which reflect typical species patterns for Neotropical icthyofauna (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. doi: http://dx.doi.org/10.1111/jfb.13016
http://dx.doi.org/10.1111/jfb.13016... ).

The combination of primary and secondary data for the Miranda River Basin produced a data set from a greater number of sample sites, over longer time periods, and at larger spatial scales, and the end product is a more complete assessment of regional fish fauna. Other studies of fish fauna in the Paraguay River Basin at smaller spatial scales report fewer numbers of species, including studies from streams of the headwaters of the Rio Vermelho (Oliveira et al. 2015OLIVEIRA, V.A., MATEUS, L.A., LOVERDE-OLIVEIRA, S. & PIETRO-SOUZA, W. 2015. Fish from urban tributaries to the Vermelho River, upper Paraguay River Basin, Mato Grosso, Brazil. Check List 11(1): 1-6. doi: http://dx.doi.org/10.15560/11.1.1516.
http://dx.doi.org/10.15560/11.1.1516... , Vizzotto & Castro 2015VIZZOTO, P.C. & CASTRO, R.J. 2015. Ichthyofauna of tributaries of the Vermelho River, upper Paraguay River basin, region of Rondonópolis, state of Mato Grosso, Brazil. Check List 11(5): 1-5. doi: http://dx.doi.org/10.15560/11.5.1750.
http://dx.doi.org/10.15560/11.5.1750... ) and Rio Sepotuba (Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292.) in northern Pantanal. In other words, by increasing spatial scale and the number of sample sites, we also increase the probability of greater among-site variation in species numbers by virtue of including a greater diversity of mesohabitats with different substrate types and riparian vegetation. These differences in habitat structural complexity (Teresa et al. 2010TERESA, F.B., ROMERO, R.M. & LANGEANI, F. 2010. Pisces, Aquidauana and Miranda drainages, upper Paraguay River basin, Mato Grosso do Sul, Brazil. Check List 6(4): 596-601., Teresa Romero & 2010, Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292., Vizzotto & Castro 2015VIZZOTO, P.C. & CASTRO, R.J. 2015. Ichthyofauna of tributaries of the Vermelho River, upper Paraguay River basin, region of Rondonópolis, state of Mato Grosso, Brazil. Check List 11(5): 1-5. doi: http://dx.doi.org/10.15560/11.5.1750.
http://dx.doi.org/10.15560/11.5.1750... ) result in a gradient of heterogeneity that, through niche differentiation, favors a greater number of species.

Some species in the current study should be highlighted due to conservation status. Serrasalmidae and Pimelodidae, Piaractus mesopotamicus and Pseudoplatystoma corruscans are on the National List of Near-threatened Species (NT) in Brazil (data published by ICMBio 2014), despite this, these species have broad distribution in the Paraguay River Basin, in addition, they are important species for artisanal and sports fishing in the region, being P. corruscans represent approximately 32% and P. mesopotamicus 17.3% of artisanal fisheries in 2015 (Catella et al. 2016CATELLA, A.C., CAMPOS, F.L.R., ALBUQUERQUE, S.P. 2016. Sistema de controle de pesca de Mato Grosso do Sul SCPESCA/MS 22- 2015. Corumbá: Boletim de pesquisa e desenvolvimento – Embrapa Pantanal. p. 55.). So, this results suggest a need of effort to better definition of conservation status at upper Paraguay basin scale.

Among the species sampled were Characidium aff. fasciatum and Farlowella cf. isbrueckeri from the families Crenuchidae and Loricariidae, respectively, both of which are listed at Brazilian law as Data Deficient (DD) (data published by ICMBio 2014) due to low numbers of recorded occurrences or absence in study samples. Ancistrus formoso and Trichomycterus dali are the only encountered species listed as vulnerable, likely a result of its limited distribution due to restriction to cave habitats in the karst environments of the Serra da Bodoquena (Cordeiro et al. 2014CORDEIRO, L.M.; BORGHEZAN, R. & TRAJANO, E. 2014. Subterranean biodiversity in the Serra da Bodoquena karst area, Paraguay river basin, Mato Grosso do Sul, Southwestern Brazil. Biota Neotropica14: 1-28. doi: http://dx.doi.org/10.1590/1676-06032014011414.
http://dx.doi.org/10.1590/1676-060320140... ); the restricted range and the frequent change of the landscape to harbor crop fields in the region represent a great menace to these species. The Miranda River Basin seems to offers sufficient resources to maintain numerous species, in particular species of concern with respect to conservation. The collective data thus suggest that preservation of this basin ecosystem is critical for perpetuation of natural resources and biodiversity.

There are roughly 270 described species in the Pantanal floodplain (Britski et al. 2007BRITSKI, H.A., SILIMON, K.Z.S. & LOPES, B.S. 2007. Peixes do Pantanal: manual de identificação. 2 ed. Embrapa, Brasília, 227p.), and our list presents 39 additional species not included in that estimate. Several species from our data sets were reported as only being found in the Paraná River basin, this suggests dispersion during the formation of the Pantanal, and serves as evidence of connectivity between the headwaters of the Paraná and Paraguay River Basins. This finding illustrates the importance of expanding sampling effort for interface regions of the basins, and reviewing the material deposited in biological collections.

In addition to future studies of species richness in the Paraguay River Basin, more detailed information on species distributions is needed to better gauge conservation status of fish in the area. There have been a limited number of studies in the area, particularly in headwater streams and their tributaries (Oyakawa & Menezes 2011OYAKAWA, O.T. & MENEZES, N.A. 2011. Checklist of fresh water fishes from São Paulo State, Brazil. Biota Neotrop 11(1a): 19-32. doi: http://dx.doi.org/10.1590/S1676-06032011000500002.
http://dx.doi.org/10.1590/S1676-06032011... , Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292.). Many species of headwater streams are potentially geographically isolated (Lowe-McConnell 1999) that are specific to these areas (Krinski et al. 2015KRINSKI, D., CARMO, E.J. & MIYAZAWA, C.S. 2015. Ichthyofauna of headwaters from Sepotuba River Basin, Upper Paraguay River Basin, Tangará da Serra, Mato Grosso state, Brazil. Panamjas 10(4): 283-292.), whereby headwaters may host very different fauna than exists in major rivers (Pedroza et al. 2012PEDROZA, W.S., RIBEIRO, F.R.V., TEIXEIRA, T.F., OHARA, W.M. & PY-DANIEL, L.H.R. 2012. Icththyofauna survey of stretches of the Guariba and Roosevelt Rivers, in Guariba State Park and Guariba Extractive Reserve, Madeira River basin, Amazonas, Brazil. Check List 8(1): 8-15., Volcan et al. 2012VOLCAN, M.V., LANÉS, L.E.K., GONÇALVES, A.C., FONSECA, A.P. & CIRNE, M.P. 2012. The fish fauna of the Corrientes stream basin, Patos lagoon system, state of Rio Grande do Sul, southern Brazil. Check List 8(1): 77-82. doi: http://dx.doi.org/10.15560/8.1.077.
http://dx.doi.org/10.15560/8.1.077... ). Based on previous experience and distribution maps from SpeciesLink, we can point out in this whor Astyanax lineatus, A. marionae, Creagrutus meridionalis, Oligosarcus perdido, Hypostomus basilisko, H. perdido and the cave fish Ancistrus formoso and Trichomycterus dali as exclusive species that inhabit headwaters. This understanding of fish fauna in headwater streams and associated tributaries is essential for maintaining fish biodiversity in the Paraguay River Basin. Inventory studies in the basin would also be useful for evaluation of potential environmental impacts on ichthyofauna, as these environments are subject to anthropogenic modification (e.g., due to the construction of hydroelectric dams, which has increased in last years). Such anthropogenic impacts have potential to modify species distribution (Mariano et al. 2012MARIANO, J.R., MAKRAKIS, M.C., KASHIWAQUI, E.A.L., CELESTINO, E.F. & MAKRAKIS, S. 2012. Longitudinal habitat disruption in Neotropical streams: fish assemblages under the influence of culverts. Neotrop Ichthyol 10(4):771-784. doi: http://dx.doi.org/10.1590/S1679-62252012000400010.
http://dx.doi.org/10.1590/S1679-62252012... ), by limiting species dispersion and altering resource availability in the entire plateau region of the Upper Paraguay Basin. In the Miranda River Basin, at least eleven small hydroelectric projects have recently approved for construction, two in Miranda sub-basin and nine in Aquidauana sub-basin. More attention should be given to the actual and potential negative impacts of these and other anthropogenic activities upon fish diversity and distributions in the basin area.

Acknowledgments

We thank the Biota-MS program in association with the Superintendência de Ciência e Tecnologia de MatoGrosso do Sul (SUCITEC), CAPES, CNPq and FUNDECT for financial and logistical support. We are grateful to Walmir B. F. Mundim Jr., Wagner Vicentin, Marcelo S. Maldonado and Gabriel Nakamura for help with field work.

References

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