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Inventory • Biota Neotrop. 17 (3) • 2017 • https://doi.org/10.1590/1676-0611-BN-2017-0344 linkcopy

Open-access Survey of fish species from plateau streams of the Miranda River Basin in the Upper Paraguay River Region, Brazil

Levantamento das espécies de peixes da bacia do Rio Miranda em riachos do planalto, Alto Rio Paraguai, Brasil

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    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. 2006). 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 1998). 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. 2000, Teresa et al. 2010).

    Approximately 270 fish species have been identified in the Paraguay River Basin (Britski et al. 2007). However, the total number of species would likely be higher if the plateau streams had been included (Alho & Sabino 2012). Numerous studies have been carried out in the basin over the past two decades, including the floodplain region (Catella & Petrere-Jr 1996, Willink et al. 2000, Junk et al. 2006, Baginski et al. 2007, Pacheco & Silva 2009, Pains-Silva et al. 2010, Tondato et al. 2013, Súarez et al. 2013, Pains-Silva et al. 2014, Polaz et al. 2014, Botini et al. 2015 and Severo-Neto et al. 2015) and plateau waters (Súarez et al. 2007, Terra & Sabino 2007, Teresa et al. 2010, Casatti et al. 2010, Teresa & Romero 2010, Castro & Vizzotto 2013, Krinski et al. 2015 and Oliveira et al. 2015). 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. 2010). Despite being a hotspot for endemic fauna (Willink et al. 2000) 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 2014). 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 2003, Junk et al. 2006).

    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. 2000, Casatti et al. 2010, Teresa et al. 2010, Teresa & Romero 2010). 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 1997, Willink et al. 2000, Ribeiro et al. 2007, Terra & Sabino 2007, Zawadzki et al. 2014, Shibatta 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), 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).

    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 1984), as well as standard error using the function ‘specaccum’ in the ‘vegan’ package (Oksanen et al. 2011) in R (R Development Core Team 2013).

    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).

    Thumbnail
    Table 1
    Final list of species from sampled and compiled data from the Miranda River Basin, Upper Paraguay River. Location of voucher deposition: DZSJRP (Departamento de Zoologia e Botânica da Universidade Estadual Paulista, São José do Rio Preto – UNESP); ZUFMS (Coleção Zoológica da Universidade Federal do Mato Grosso do Sul – UFMS); LIRP (Coleção de Peixes do Laboratório de Ictiologia de Ribeirão Preto, Universidade de São Paulo - USP); MZUEL (Museu de Zoologia da Universidade Estadual de Londrina - UEL); NUP (Núcleo de Pesquisa em Limnologia, Ictiologia e Aquicultura da Universidade Estadual de Maringá – Nupelia/UEM).
    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. 2007, Terra & Sabino 2007, Polaz et al. 2014), 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. 2015). 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. 2011), providing data on the species composition, management and conservation (Pains-Silva et al. 2014).

    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. 2015, Vizzotto & Castro 2015), which reflect typical species patterns for Neotropical icthyofauna (Reis et al. 2016).

    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. 2015, Vizzotto & Castro 2015) and Rio Sepotuba (Krinski et al. 2015) 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. 2010, Teresa Romero & 2010, Krinski et al. 2015, Vizzotto & Castro 2015) 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. 2016). 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. 2014); 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. 2007), 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 2011, Krinski et al. 2015). Many species of headwater streams are potentially geographically isolated (Lowe-McConnell 1999) that are specific to these areas (Krinski et al. 2015), whereby headwaters may host very different fauna than exists in major rivers (Pedroza et al. 2012, Volcan et al. 2012). 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. 2012), 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.

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    Publication Dates

    • Publication in this collection
      2017

    History

    • Received
      15 Mar 2017
    • Reviewed
      20 July 2017
    • Accepted
      21 July 2017
    Creative Common - by 4.0
    This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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