1urn:lsid:arphahub.com:pub:F9B2E808-C883-5F47-B276-6D62129E4FF4urn:lsid:zoobank.org:pub:245B00E9-BFE5-4B4F-B76E-15C30BA74C02Biodiversity Data JournalBDJ1314-28361314-2828Pensoft Publishers10.3897/BDJ.11.e986329863221346Taxonomy & InventoriesPiscesTaxonomyFreshwater Biota & EcosystemsBiodiversity & ConservationSouth AmericaChecklist of the fish fauna of the Munim River Basin, Maranhão, north-eastern BrazilVieiraLucas O.https://orcid.org/0000-0002-1448-064512CamposDiego S.https://orcid.org/0000-0001-8262-413X23OliveiraRafael F.https://orcid.org/0000-0002-1659-292324SouthJosie5CoelhoMarcony S. P.2PaivaMaurício J. S.2BragançaPedro H. N.https://orcid.org/0000-0002-8357-701046GuimarãesErick C.https://orcid.org/0000-0003-4480-5452789KatzAxel M.https://orcid.org/0000-0002-2933-716310BritoPâmella S.718SantosJadson P.8OttoniFelipe P.fpottoni@gmail.comhttps://orcid.org/0000-0002-9390-09181243Universidade Federal do Maranhão, Centro de Ciências de Chapadinha, Campus de Chapadinha, Programa de Pós-Graduação em Ciências Ambientais, BR-222, KM 04, Boa Vista, CEP: 65500-000, Chapadinha, BrazilUniversidade Federal do Maranhão, Centro de Ciências de Chapadinha, Campus de Chapadinha, Programa de Pós-Graduação em Ciências Ambientais, BR-222, KM 04, Boa Vista, CEP: 65500-000ChapadinhaBrazilUniversidade Federal do Maranhão, Centro de Ciências de Chapadinha, Campus de Chapadinha, Laboratório de Sistemática e Ecologia de Organismos Aquáticos, BR-222, KM 04, S/N, Boa Vista, CEP: 65500-000, Chapadinha, BrazilUniversidade Federal do Maranhão, Centro de Ciências de Chapadinha, Campus de Chapadinha, Laboratório de Sistemática e Ecologia de Organismos Aquáticos, BR-222, KM 04, S/N, Boa Vista, CEP: 65500-000ChapadinhaBrazilUniversidade Federal do Maranhão, Programa de Pós-Graduação em Biodiversidade e Biotecnologia da Amazônia Legal, Av. dos Portugueses, 1966, Cidade Universitária Dom Delgado, 65080-805, São Luís, BrazilUniversidade Federal do Maranhão, Programa de Pós-Graduação em Biodiversidade e Biotecnologia da Amazônia Legal, Av. dos Portugueses, 1966, Cidade Universitária Dom Delgado, 65080-805São LuísBrazilUniversidade Federal do Maranhão, Programa de Pós-Graduação em Biodiversidade e Conservação, Av. dos Portugueses, 1966, CEP: 65085-580, São Luís, BrazilUniversidade Federal do Maranhão, Programa de Pós-Graduação em Biodiversidade e Conservação, Av. dos Portugueses, 1966, CEP: 65085-580São LuísBrazilSchool of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomSchool of Biology, Faculty of Biological Sciences, University of LeedsLeedsUnited KingdomSouth African Institute for Aquatic Biodiversity, Grahamstown, South AfricaSouth African Institute for Aquatic BiodiversityGrahamstownSouth AfricaUniversidade Federal do Maranhão, Departamento de Biologia, Laboratório de Genética e Biologia Molecular, Av. dos Portugueses 1966, Cidade Universitária do Bacanga, CEP: 65080-805, São Luís, BrazilUniversidade Federal do Maranhão, Departamento de Biologia, Laboratório de Genética e Biologia Molecular, Av. dos Portugueses 1966, Cidade Universitária do Bacanga, CEP: 65080-805São LuísBrazilUniversidade Estadual do Maranhão, Laboratório de Ictiofauna e Piscicultura Integrada, Centro de Ciências Agrárias, Campus Paulo VI, avenida Lourenço Vieira da Silva, n. 1000, bairro Jardim São Cristóvão, CEP: 65.055-310, São Luís, BrazilUniversidade Estadual do Maranhão, Laboratório de Ictiofauna e Piscicultura Integrada, Centro de Ciências Agrárias, Campus Paulo VI, avenida Lourenço Vieira da Silva, n. 1000, bairro Jardim São Cristóvão, CEP: 65.055-310São LuísBrazilUniversidade Federal do Oeste do Pará, Instituto de Ciências da Educação, Programa de Pós-graduação Sociedade Natureza e Desenvolvimento, Av. Marechal Rondon s/n, CEP: 68040-070, Santarém, PA, Brasil, Belém, BrazilUniversidade Federal do Oeste do Pará, Instituto de Ciências da Educação, Programa de Pós-graduação Sociedade Natureza e Desenvolvimento, Av. Marechal Rondon s/n, CEP: 68040-070, Santarém, PA, BrasilBelémBrazilUniversidade Federal do Rio de Janeiro, Laboratório de Sistemática e Evolução de Peixes Teleósteos, Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva, Instituto de Biologia, CEP: 21.941-902, Rio de Janeiro, BrazilUniversidade Federal do Rio de Janeiro, Laboratório de Sistemática e Evolução de Peixes Teleósteos, Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva, Instituto de Biologia, CEP: 21.941-902Rio de JaneiroBrazil
Corresponding author: Felipe P. Ottoni (fpottoni@gmail.com).
Academic editor: Rupert Collins
20231002202311e986328BD83233-1C86-54A9-9688-7F07EC9A44260912202203022023Lucas O. Vieira, Diego S. Campos, Rafael F. Oliveira, Josie South, Marcony S. P. Coelho, Maurício J. S. Paiva, Pedro H. N. Bragança, Erick C. Guimarães, Axel M. Katz, Pâmella S. Brito, Jadson P. Santos, Felipe P. OttoniThis is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Background
The Maranhão State harbours great fish diversity, but some areas are still undersampled or little known, such as the Munim River Basin in the northeast of the State. This lack of knowledge is critical when considering anthropogenic impacts on riverine systems especially in the face of major habitat destruction. These pressing threats mean that a comprehensive understanding of diversity is critical and fish checklists extremely relevant. Therefore, the present study provides a checklist of the fish species found in the Munim River Basin, Maranhão State, north-eastern Brazil, based on collected specimens.
New information
A total of 123 species were recorded for the Munim River Basin, with only two non-native species, Oreochromisniloticus and Colossomamacropomum, showing that the fish assemblage has relatively high ecological integrity. In addition, 29 species could not be identified at the species level, indicating the presence of species that are probably new to science in the Basin. A predominance of species belonging to the fish orders Characiformes and Siluriformes, with Characidae being recovered as the most species-rich family (21 species) agrees with the general pattern for river basins in the Neotropical Region. The total fish diversity was estimated by extensive fieldwork, including several sampling gears, carried out in different seasons (dry and rainy) and exploring different environments with both daily and nocturnal sampling, from the Basin's source to its mouth. A total of 84 sites were sampled between 2010 and 2022, resulting in 12 years of fieldwork. Fish assemblages were distinct in the Estuary and Upper river basin sections and more similar in the Lower and Middle sections indicating environmental filtering processes. Species were weakly nested across basin sections, but unique species were found in each section (per Simpsons Index). High variability of species richness in the Middle river basin section is likely due to microhabitat heterogeneity supporting specialist fish communities.
biodiversityendemismfreshwatermigratory speciestaxonomy.Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Finance Code 001), Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), Conselho Nacional de Desenvolvimento (CNPQ), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), and Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA)Introduction
The Neotropical Region comprises the most biodiverse freshwater ichthyofauna on the planet, with more than 6000 described species (Reis et al. 2016, Albert et al. 2020). Within the Neotropics, South America harbours the world's greatest diversity of freshwater fishes, including about 5160 described species, which represents about one-third of all known freshwater species (Reis et al. 2016, Pelicice et al. 2017, Castro and Polaz 2020). Studies on diversity of the region have produced estimates which are much higher, predictions being between 8000 to 9000 described and undescribed freshwater fish species (Reis et al. 2016, Birindelli and Sidlauskas 2018, Castro and Polaz 2020, Albert et al. 2020, Koerber et al. 2022). This high diversity is mainly comprised of medium- to small-sized species (species that do not surpass 15 cm standard length), corresponding to 70% of the species (Reis et al. 2003, Castro and Polaz 2020). Small and medium-sized species are broadly distributed throughout all aquatic habitats, which is most likely due to niche partitioning, life history traits adapted to stochastic environments and high trophic plasticity (Vazzoler 1996, Castro 1999, Lowe-Mcconnell 1999, Abelha et al. 2001, Guimarães et al. 2020, Castro and Polaz 2020, Corrêa and Castro 2021). Despite the description of small- and medium-sized fish diversity in scientific journals, they remain largely unnoticed by the general public and neglected by conservation agencies and policies (Castro 1999, Castro et al. 2005, Abell et al. 2011, Albert et al. 2011, Castro and Polaz 2020).
Brazil possesses the highest number of freshwater fish species in South America (Buckup et al. 2007, Castro and Polaz 2020), with about 100 new species being described every year over the last decade (Nelson et al. 2016, Reis et al. 2016, Fricke et al. 2022). However, several of these species represent endemics, with narrow distributions and some are highly threatened due to increased anthropogenic pressure on their natural habitats (Reis et al. 2003, Nogueira et al. 2010, Darwall et al. 2018, Reid et al. 2019). Brazilian freshwaters are subject to multitude anthropogenic threats, such as: deforestation resulting in suppression or reduction of the original vegetation cover, due to logging and expansion of agricultural and urban areas; release of domestic and industrial effluents and chemical products from agricultural activities in aquatic environments, resulting in pollution; irregular water abstraction for different urban, industrial and agricultural uses; soil erosion and silting of the environments; river damming and construction of hydroelectric power plants, disrupting fish migration routes and destroying the natural habitats of fish species; extraction of sand from the riverbeds; mining, resulting in modification of habitats and water pollution and contamination; modification and diversion of the river channels; introduction of non-native species; overharvesting for the aquarium trade; ghost fishing; and overfishing of food fishes (Dudgeon et al. 2006, Pereira et al. 2016, Pelicice et al. 2017, Reid et al. 2019, Zarfl et al. 2019, Zeni et al. 2019, Bergmann et al. 2020, Castro and Polaz 2020, Ottoni et al. 2021, Azevedo-Santos et al. 2021, Doria et al. 2021, Vitorino et al. 2022, Rocha et al. 2023). Despite the high freshwater native fish diversity, non-native fish species have proliferated in Brazil and in Brazilian hydrographic systems where they do not occur naturally due to several human activities, such as: aquaculture, intentional introductions and release, aquarium trade, mosquito larvae biological control interventions, transposition of water between isolated river basins, sport fishing, amongst other activities (Figueredo and Giani 2005, Azevedo-Santos et al. 2011, Vitule et al. 2015, Latini et al. 2016, Padial et al. 2017, Bragança et al. 2020, Doria et al. 2021, Ottoni et al. 2021, Franco et al. 2022, Rocha et al. 2023). Non-native species have caused changes in the local assemblage composition and in the abundance of native species populations, causing major environmental impacts (Giacomini et al. 2011, Latini et al. 2016, Padial et al. 2017, Doria et al. 2021, Ottoni et al. 2021, Rocha et al. 2023).
Maranhão is the westernmost state in north-eastern Brazil, bordered by the Piauí State in the east, from whom it is separated by the Parnaíba River; by Tocantins State in the south and southeast, from which it is separated by the Tocantins River; and by Pará State in the west, from which it is separated by the Gurupi River (Rebêlo et al. 2003). Maranhão total area is about 330000 km2, corresponding to 3.9% of Brazil's territory (Rebêlo et al. 2003, Rios 2005, Batistella et al. 2014, Spinelli-Araújo et al. 2016). Maranhão is an extremely important State in terms of biodiversity, housing three of the main Brazilian biomes, as well as transition areas between them. The Cerrado biome is present in the central, eastern and southern portion of the State; the Amazon biome is present in the western and central portion; and the Caatinga biome is found in the easternmost portion of the State (Rebêlo et al. 2003, Rios 2005, Batistella et al. 2014, Spinelli-Araújo et al. 2016). Thus, Maranhão includes a phytogeographic mosaic due to the presence and overlap of floral elements typical of these three distinct biomes, besides the presence of complex transition areas, making the State extremely biodiverse, ecologically relevant and a key area for conservation (Rebêlo et al. 2003, Rios 2005, Batistella et al. 2014, Spinelli-Araújo et al. 2016).
In the past two decades, several fish surveys were carried out in Maranhão, in both freshwater and estuarine environments, increasing the knowledge of the State's fish fauna (Castro 2001, Castro et al. 2002, Piorski et al. 2003, Pinheiro-Júnior et al. 2005, Soares 2005, Piorski et al. 2007, Castro et al. 2010, Barros et al. 2011, Sousa et al. 2011, Fraga et al. 2012, Almeida et al. 2013, Ribeiro et al. 2014, Ramos et al. 2014, Lima et al. 2015, Matavelli et al. 2015, Melo et al. 2016, Nascimento et al. 2016, Piorski et al. 2017, Brito et al. 2019, Lima et al. 2019, Teixeira et al. 2019, Nunes et al. 2019, Guimarães et al. 2020, Brito et al. 2020, Oliveira et al. 2020, Guimarães et al. 2021c, Guimarães et al. 2021a, Guimarães et al. 2021b). Information about the ichthyofauna of the coastal Munim River Basin, however, is scarce. At the same time, this river basin is under severe anthropogenic pressure from deforestation of marginal vegetation, pollution, contamination of the water, erosion, siltation and even the loss of water bodies (Ribeiro et al. 2006, Ribeiro and Nunes 2017). The Munim River Basin has only five published studies documenting its fish diversity (Ribeiro et al. 2014, Matavelli et al. 2015, Nunes et al. 2019, Oliveira et al. 2020, Guimarães et al. 2021c). These, however, focused on specific localities and environments and, in many cases, surveying only similar and neighbouring sites within this river basin. As a consequence, the fish fauna of the Munim River Basin still awaits a more comprehensive checklist.
The main goal of the present study is to present a detailed inventory of the fish diversity in the Munim River Basin, through the analysis and study of data sampled over 12 years of fieldwork, providing species-level identifications when possible. The study covered the entire river basin and includes relevant information about the importance of checklists in contributing to the knowledge of the river basin, species conservation and distribution. In addition, we provide here ecological and biogeographical comments.
Materials and methodsStudy area
Sampling was carried out in rivers, streams, lagoons, swamps, marshes, lakes and the estuary of the Munim River Basin, northeast of the Maranhão State, north-eastern Brazil. The Munim River Basin source is at the Caxias Municipality, in the Cerrado Biome and its mouth is at baía of São José in a region known as "Golfão Maranhense" between the Axixá and Icatu municipalities, within the Cerrado and Amazon biomes (Fig. 1). The Munim River Basin has an area of about 15918.04 km2, with 331.74 km from its source to its mouth (Nugeo 2016, Rios 2005).
Sampling sites
Sampling was carried out in 84 collecting sites, covering four different sections of the Munim River Basin, in both rainy (January to May) and dry (June to December) seasons according to Passos et al. (2016). The sampling was done between 2010 and 2022 (about 65% of the surveys were carried out between 2019 and 2022), including sites close to its source and to its mouth (Fig. 1). The sampled environments included rivers, streams, lagoons, swamps, marshes, lakes and the estuary (Table 1, Fig. 2, Suppl. material 1).
Sampling and specimens identification
All (about 160) sampling events were carried under the permits issued by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO; License nº 54949, 57258, 57787, 64415, 73267). In addition, material already housed at the Coleção Ictiológica do Centro de Ciências Agrárias e Ambientais (CICCAA) of the Universidade Federal do Maranhão, was also used in this study. The specimens were sampled by using different sampling gear, such as fishing line, hand net, seine net, cast net, gill nets and crayfish-type traps (Souza and Auricchio 2002). All the sampling activities and procedures followed the best practices and standards for animal welfare as presented in Leary et al. (2020). Specimens were euthanised by immersion in a 250 mg/l Tricaine methane sulphonate (MS-222) solution until the cessation of opercular movements.
Following the euthanasia, the specimens for morphological studies were preserved in formalin (10%) and moved to a 70% ethanol solution after 10-15 days. Specimens selected for future molecular studies were preserved in 99% ethanol. The processing and identification of specimens were made at the Laboratório de Sistemática e Ecologia de Organismos Aquáticos (LASEOA), at the Universidade Federal do Maranhão, by the use of specialised bibliography for each taxonomic group and by consulting specialists. The specimens were identified to the lowest taxonomic rank possible. All biological material is catalogued and housed at the Coleção Ictiológica do Centro de Ciências Agrárias e Ambientais (CICCAA) of the Universidade Federal do Maranhão (UFMA) (Suppl. materials 1, 2). The taxonomic classifications, species names, authorship and year, original descriptions, habitat of occurrence and geographic distributions were verified and presented according to Fricke et al. (2022a), Fricke et al. (2022b) and Froese and Pauly (2022).
Map and Munin River Basin sections distinction
The geographic coordinates of each collection site along the Munim River Basin were registered from a GPS device and then converted to the shapefile format, with place names and respective codes in the attribute table. Additional data on boundaries from river basins and political division of territory were acquired from the official data service IBGE (Brazilian Institute for Geography and Statistics). The map was composed in QGIS 3.22.12 (Qgis development team 2022). Due to scale, each point on the map may correspond to one or more collection sites, depending on the geographic proximity.
The Munim River Basin was divided into four sections: Estuary section with an area of 78.89 km2, comprising one collecting site; Lower river basin section with an area of 2891.89 km2, comprising 13 collecting sites; Middle river basin section with an area of 10722.29 km2, comprising 62 collecting sites; and Upper river basin section with an area of 2224.90 km2, comprising eight collecting sites (Fig. 1, Table 1, Suppl. material 2). The criterion for the sectorisation of the basin was based on the average slope calculated from the elevation values (meters above sea level) of the digital elevation model SRTM/USGS, available at the TOPODATA/INPE project (http://www.dsr.inpe.br/topodata/). Based on the analysed area, this river basin varies from 0 to 162 meters above the sea level. The parameters considered for the sectorisation were: Estuary section - average slope of 1.09 (standard deviation 1.59); Lower river basin section - average slope of 1.41 (standard deviation 1.33); Middle river basin section - average slope of 2.63 (standard deviation: 2.43); and Upper river basin section - average slope of 3.11 (standard deviation 2.61) (Fig. 1, Table 1, Suppl. material 2).
Species photographs
Specimens of some species were photographed in the laboratory to illustrate the diversity of species that occur in the Munim River Basin (Fig. 3, Fig. 4 and Fig. 5). Additional photographs of Munim River fish species can be seen in Guimarães et al. (2018b): figs. 1, 2, Oliveira et al. (2020): fig. 3, Guimarães et al. (2021c) and Aguiar et al. (2022): fig.2b.
Migratory species
Species were classified as migratory based on Carolsfeld et al. (2003). When any species was not listed in Carolsfeld et al. (2003), we considered the genus to indicate if it is a migratory species.
General species accumulation curve
A matrix of occurrence and abundance data over the sampling period, for this study, was used to plot the general species accumulation curve with Primer-e statistical software (Clarke and Gorley 2006), based on a spreadsheet containing relevant data for this analysis (Suppl. material 2). Given that the order of samples in the analysis affects the shape of the curve produced, due to heterogeneity amongst the species in the samples (Ugland et al. 2003), 1000 permutations were calculated to overcome this effect.
Species Richness and Fish assemblage composition
The statistical and ecological analyses were based on a spreadsheet containing relevant data for these analyses (Suppl. material 2).
Species Richness
Species richness (Sprich) (i.e. number of species in each river basin section) was compared using Kruskal-Wallis tests, on account of non-normal distribution (per Shapiro-Wilk test) and Dunn post-hocs with Holm adjusted p-values to account for multiple comparisons were used to determine section level differences. Visualisation was completed through the R package '“ggstatsplot'” (Patil 2021).
Fish assemblage composition
Fish assemblage composition was compared between basin sections, at the basin section level, using presence-absence data due to surveys not being standardised for sampling methods. Only native species were included in the analysis. First, nestedness was assessed using the NODF method (Almeida-Neto et al. 2008), which is bound between 0 and 100 where 100 is perfect nestedness, via vegan::nestednodf, then Sørensen dissimilarity and Simpsons Index were calculated using vegan::nestedbetasor. Sørensen dissimilarity closer to 0 indicates more shared species. Simpsons Index is not affected by species richness and represents true turnover, i.e. the the replacement of some species by other species from section to section, independent of potential differences in species richness between the sections. Areas with Simpsons Index values over 66% are considered to have similar faunal composition (Sánchez and López 1988). Jaccard Index was calculated using vegan::nestedbetajac where values closer to one indicate higher similarity. A cluster analysis and dendrogram was completed on the section Jaccard coefficients using the Ward.D2 method. All statistical analyses were performed within the R software environment version 4.0.2 and the package “vegan” (Oksanen et al. 2019, R Core Team 2020).
ChecklistsChecklist of the fish fauna of the Munim River BasinBECF9992-741F-5B58-82A8-2E86F1450CC2ActinopteriNotes
The checklist is presented in Table 2.
Analysis
The present study recorded about 32500 specimens belonging to 123 fish species (94 identified at the species level) for the Munim River Basin, divided into 49 families and 14 orders (Table 2, Suppl. materials 1, 2). The most diverse orders are the Characiformes, with 43 species (35%); Siluriformes, with 38 species (30.9%); Acanthuriformes, with 11 (8.9%); Cichliformes, with seven species (5.7%) and Gymnotiformes, with six species (4.9%), representing 85.4% of all species known from the river basin. The remaining orders (Clupeiformes, Carangiformes, Cyprinodontiformes, Batrachoidiformes, Beloniformes, Mugiliformes, Scombriformes, Synbranchiformes and Tetraodontiformes) together represent only 14.6% of the Munim River Basin species.
The most diverse family was the Characidae, with 21 species (17.1%), followed by the Loricariidae, with nine (7.3%) and the Cichlidae, with seven (5.7%). Further, from all 123 recorded species, only two, Oreochromisniloticus and Colossomamacropomum are non-native species for the studied region and 13 are migratory species (see Table 2). Amongst the species identified at the species level, 16 are endemic to the hydrographic regions of Maranhão and Parnaíba sensuHubert and Renno (2006) (Mrn and Prn, respectively).
According to the General plotted curves (General species accumulation curve), the sampling effort can be considered sufficient (Fig. 6), given that the observed values of Sobs (125 ±14) are aligned with those calculated in the estimator Chao1 (136.25) and the asymptote estimates of the Michaelis-Menten equation (113), as well as the Bootstrap (140.8) and Jackknife1 (162.85) variation indicators (Fig. 6).
Species Richness
There were significant differences in species richness between sections (X2= 16.207, df = 3, p < 0.001) where the Lower and Upper river basin sections had significantly more species than the Middle river basin section (p < 0.05, p < 0.01 respectively; Fig. 7).
Fish assemblage composition
There was weak nestedness across the four basin sections (NODF = 37.67) and indices of species composition similarity and dissimilarity were moderate. Where Sørensen dissimilarity was 0.70 and Simpsons Index (i.e. true turnover) was 56%, suggesting that fish assemblage is distinct between basin sections but only moderately. Jaccard similarity was 83% indicating many shared species compared to unique species across river basin sections. Cluster analysis showed that the Estuary and Upper river sections were more distinct from the Lower and Middle river sections, which formed their own cluster (Fig. 8).
Discussion
This long-term icthyological survey, covering 12 years, conducted between 2010 and 2022 (65% of the surveys were carried out between 2019 and 2022), applied different sampling gears over different water bodies and environments along the Munim River Basin and recorded a predominance of fishes belonging to the Characiformes and Siluriformes, agreeing with a pattern expected for the Neotropics (Lowe-Mcconnell 1999, Pelicice et al. 2005, Langeani et al. 2007, Polaz et al. 2014, Reis et al. 2016, Brito et al. 2019, Dagosta and de Pinna 2019, Guimarães et al. 2020, Castro and Polaz 2020). The study also recorded the predominance of small-sized characid fishes, which have a great diversity in the Neotropical Region, due to several traits, such as their high trophic plasticity (Abelha et al. 2001, Van Der Sleen and Albert 2018, Dagosta and de Pinna 2019, Castro and Polaz 2020, Guimarães et al. 2020, Corrêa and Castro 2021).
A total of 123 species were recorded, with only two of them representing introduced species to the studied river basin (Table 2 and Suppl. materials 1, 2). Colossomamacropomum (tambaqui) occurs naturally in the Amazon and Orinoco River Basins, thus being native to Brazil, but not the Munim River Basin (Latini et al. 2016, Fricke et al. 2022b); and Oreochromisniloticus (tilápia) which is native to northern and eastern Africa (Figueredo and Giani 2005, Latini et al. 2016, Fricke et al. 2022b). All the other 121 species are native to the studied area. Therefore, the fish assemblage composition of the Munim River Basin is currently little affected by the presence of alien fish species. However, the policy regarding non-native species and push for economic development indicates this may soon change (Azevedo-Santos et al. 2011, Doria et al. 2021, Faria et al. 2022).
The occurrence of non-native fish species usually comes from fish farming and, in some cases, from intentional release and aquarium trade (Latini et al. 2016, Rocha et al. 2023). Oreochromisnilotus is an omnivorous fish which has broad abiotic tolerances, rapid growth and high survival in environments with high population density, traits which facilitate invasiveness and are favoured in aquaculture species (Figueredo and Giani 2005, Latini et al. 2016). In Brazil, the cultivation of this species is increasing, frequently without any control (Figueredo and Giani 2005, Latini et al. 2016). The species C.macropomum was recorded at only one collection site (a single specimen) (see Suppl. materials 1, 2). This makes us believe that the specimen had probably accidentally escaped from local or home fish-farming. On the other hand, O.niloticus was recorded in four locations (some of these locations far from each other), on different dates (i.e. several specimens). These data suggest establishment in the river basin and, thus, should be considered an established species in the Munim River Basin. Aquaculture initiatives with poor biosecurity are the probable pathway of invasion and rapid expansion facilitated by favourable climatic conditions should be expected and monitored in the Munim River Basin (Charvet et al. 2021, Wilgen et al. 2022). There is likelihood of negative ecological impacts as a result of this burgeoning invasion, in particular O.niloticus is a highly efficient filter feeder and may disrupt the food-web (Vasconcelos et al. 2018, Charvet et al. 2021). Biological invasions are a direct cause of biodiversity decline globally and are an increasing threat, especially in aquatic systems with high endemicity (Havel et al. 2015, Gallardo et al. 2016).
This study reported 13 migratory fish species occurring in the Munim River Basin. Therefore, the eventual construction of dams and hydroelectric plants will undoubtedly negatively impact these species as migration routes will be interrupted. Locally, Oliveira et al. (2020) have already reported this situation occurring in the Mata de Itamacaoca, Chapadinha Municipality, State of Maranhão. They verified that the reservoir dam constructed in the Mata de Itamacaoca inhibits the dispersion of fish occurring below the dam, which possesses higher species diversity. In addition, migratory species were also not found by Oliveira et al. (2020) above the dam, in the reservoir, which would be a suitable habitat for these species. This may illustrate the effects of increased dam construction along the Munim River Basin.
When comparing the present checklist with previous ones listing the fish species found in the hydrographic regions of Maranhão and Parnaíba sensuHubert and Renno (2006) (Mrn and Prn, respectively) (e.g. Soares (2005), Barros et al. (2011), Nascimento et al. (2016), Piorski et al. (2017), Brito et al. (2019), Brito et al. (2020), Guimarães et al. (2020)), it is evident that the fish diversity from the Munim River Basin has been underestimated. In fact, the present study showed a surprisingly high fish species diversity occurring in the Munim River Basin, when compared to the species richness found in other larger drainage systems and river basins from Maranhão. For example, Munim River Basin outnumbered the Itapecuru River Basin, a larger river basin, with 29 more species being recorded, where 94 fish species are known to occur (e.g. Barros et al. (2011), Nascimento et al. (2016), Koerber et al. (2022)). In addition, we recorded 67 more species than in the Preguiças and Periá River Basin, where 56 fish species are known to occur (e.g. Piorski et al. (2017), Brito et al. (2019), Brito et al. (2020), Koerber et al. (2022)); 22 more fish species than Guimarães et al. (2020) recorded for the Pindaré River drainage (101 fish species); and more than twice the number of fish species for the coastal river basins of Gurupi, Maracaçumé, and Turiaçu, where less than 50 species are known for each of these river basins (Koerber et al. 2022). There are only three studies surveying Maranhão coastal drainage systems, which presented a higher number of species than this study. Ramos et al. (2014), who recorded 146 species for the Parnaíba River Basin and, later, Silva et al. (2015) provided an updated list with six additional species (152). Koerber et al. (2022) published a checklist of the freshwater species in Maranhão (CLOFFBR-MA), listing 136 species for the Mearim River Basin. The Munim River Basin had 13 fewer species than those recorded in the Mearim River Basin, one of the largest river basins in Maranhão and 29 fewer species than the Parnaíba River Basin, which is the largest hydrographic basin in north-eastern Brazil (Ramos et al. 2014, Silva et al. 2015, Koerber et al. 2022).
When analysing the present results in light of the previous surveys in the Munim River Basin, it is clear that all previous studies were geographically restricted to specific localities, extremely close to each other, thus were not able to depict and represent the wider basin diversity. Ribeiro et al. (2014) recorded only 20 fish species (103 less than the present study), using a traditional fishing technique called "moita" commonly used by local traditional communities in the Chapadinha Municipality. However, this method is biased toward the capture of medium to large-sized fishes and is generally applied by subsistence fisheries. Matavelli et al. (2015) surveyed the tadpoles occurring in lentic and lotic environments in Cerrado and Restinga vegetation types, sampling in localities in the Munim and Parnaíba river basins. Fish species were also sampled and a total of 13 species were recorded from the Munim River Basin (110 less than the present study). Nunes et al. (2019) carried out a weight-length ratio study of the fish community in one locality in Munim River Basin, recording 15 fish species (108 less than the present study). More recently, Oliveira et al. (2020) published a freshwater fish species list of a conservation unit in the Chapadinha Municipality after a long monitoring period, with 23 species (100 less than the present study). However, the survey was focused on small streams and consequently recorded mainly small-size species. Guimarães et al. (2021b) published a book from the same area studied by Oliveira et al. (2020), directed at the general public, which focused on species with an estimated high ornamental value. Finally, in the CLOFFBR-MA, which relied upon literature information, 59 species were identified in the Munim River Basin (64 less than the present study) (Koerber et al. 2022). None of these previous studies had the main goal of identifying the entire species diversity of the Munim River Basin.
Within the 121 native species listed in the present study, 29 were not able to be identified to the species level. Guimarães et al. (2018a) and Guimarães et al. (2020), hypothesised that probably this is a result of the lack of taxonomic knowledge and information about these species and groups occurring in Maranhão. The taxa which could not be identified to the species level, likely belong to species complexes or represent taxonomically challenging and poorly defined groups and may represent new species to science (see Table 2).
Median species richness in the Middle river basin section was lower than in the Upper and Lower river basin sections; however, the Middle section had both more sampling sites and much higher range of species richness. Environmental filtering across river gradients has a strong influence on species richness and diversity (López‐Delgado et al. 2019, Walsh et al. 2022). By grouping by section, we are missing local habitat-specific variables which are likely to be driving differences in fish assemblages across a highly heterogenous river network. Investigating habitat specific associations and drivers of beta diversity will vastly improve our understanding of drivers of fish assemblages in the Munim River Basin. Moderate nestedness and similarity/dissimilarity trends, combined with the lack of clear clustering between sites within river basin sections, indicate that fish assemblage structuring in the Munim River Basin is probably driven by both the river continuum concept as well as environmental filtering (Vannote et al. 1980, Heino et al. 2015). However, unobstructed flows facilitating dispersal likely drive high similarity throughout each basin section (Leitão et al. 2018). The Munim River Basin is not high altitude and has neither large rapids nor large waterfalls; therefore, the flow conditions through the sections are also relatively similar, with the lower river section differing through estuarine influence. Further research is needed to understand the specific microhabitats and fish associations throughout the river basin as this is undoubtedly a driving factor of diversity. For example, river slope and flow conditions exert strong environmental filters on fish community and traits in Neotropical and Afrotropical freshwaters and dispersal between heterogenous habitats may be limited by side channels and swamp habitats (Caetano et al. 2021, Walsh et al. 2022). A higher concentration of specialist species is expected to be found in the Upper section as there is more competition for niches (Sternberg and Kennard 2013). The cluster analysis indicated that the Upper section sites were on distinct branches from the other sites, but a standardised sampling methodology combined with implementation of functional trait-based approaches will facilitate our understanding of finer scale processes of environmental filtering in each section (Bower and Winemiller 2019a, Bower and Winemiller 2019b).
Considering all 92 native species which were identified to the species level, 30 of them (Achirusachirus, Amphiariusrugispinis, Anablepsanableps, Anchoviasurinamensis, Anchoviellaguianensis, Anchoviellalepidentostole, Aspistorquadriscutis, Aspredoaspredo, Bagrebagre, Batrachoidessurinamensis, Cathoropsspixii, Centropomusparallelus, Chaetodipterusfaber, Chloroscombruschrysurus, Conodonnobilis, Cynoscionsteindachneri, Eugerresplumieri, Genyatremusluteus, Hyporhamphusroberti, Lutjanusjocu, Macrodonancylodon, Menticirrhusamericanus, Micropogoniasfurnieri, Mugilcurema, Oligoplitespalometa, Opisthonemaoglinum, Peprilusparu, Plagioscionsquamosissimus, Rhinosardiniaamazonica and Stellifernaso) are commonly found in brackish water or estuaries. Due to this, no biogeographical considerations will be made about them. From the remaining 62 species identified to the species level, 16 are only known from river drainage systems and basins of the Maranhão State and the Parnaíba River Basin (Anablepsoidesvieirai, Apistogrammapiauiensis, Auchenipterusmenezesi, Charaxawa, Cichlasomazarskei, Corydorasvittatus, Eigenmanniarobsoni, Geophagusparnaibae, Hassaraffinis, Hemiodusparnaguae, Hyphessobryconpiorskii, Pimelodellaparnahybae, Prochiloduslacustris, Rhamphichthysatlanticus, Roeboidesmargareteae and Roeboidessazimai). Three other species (Platydorasbrachylecis, Poeciliasarrafae and Schizodondissimilis) are also known from other drainages in the northeast of Brazil (Teixeira et al. 2017, Silva et al. 2020, Fricke et al. 2022b). The remaining 43 species are also known from different Amazonian drainage systems (Fricke et al. 2022b), a pattern clearly showing the influence and presence of Amazonian fauna in the Munim River Basin. In addition, when comparing the species listed for the Munim River Basin to the list of species in the Parnaíba River (Ramos et al. 2014, Silva et al. 2015), there are 53 native species co-occurring in both drainage systems, showing a high influence of the larger Parnaíba River Basin over smaller coastal drainage systems. Finally, there are a total of 64 new records of fish species for the Munim River Basin and 48 new records considering only the number of taxa identified at the species level (Table 2), showing that, until the present study, the drainage's diversity was underestimated.
The Munim River Basin, previously a neglected river system, similar to many other coastal systems in Maranhão, is now one of the better known river basins relative to its fish diversity. A detailed taxonomic investigation of specimens sampled over a 12 year period revealed a much diverse fish fauna. The present study is the most comprehensive carried out in the Munim River Basin so far, adding 64 species (including species identified at the species level and species not identified at species level), which were previously considered not to occur in the drainage, resulting in a total of 123 species. Within this species richness, there was a large number of taxa, which could not be identified at the species level, indicating the urgent need for dedicated taxonomic research in the region. This study puts emphasis on the importance of compiling ichthyofaunal lists for poorly-studied or subsampled areas. This achievement represents a first step in understanding the diversity in the Munim River Basin, with the information presented herein allowing the development of future ecology, biogeography and conservation studies. Thus, this is an essential contribution to the effort to better understand the fish diversity of Maranhão in the face of rapid global change and habitat alteration. Despite the high number of species found for the Munim River Basin, more collection efforts are recommended, especially in the Lower and Estuary sections. New collection expeditions may find species that may not have been recorded by this work.
Acknowledgements
We thank Ananda Saraiva for helping to identify some specimens of Loricariinae; Elioenai Oliveira, Antônio Bezerra and Brenda Lima for laboratory assistance; four anonymous reviewers for their important contributions to the manuscript; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Finance Code 001), Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), Conselho Nacional de Desenvolvimento (CNPQ), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA) for providing the scholarship under the process (CNPq-FAPEMA, grant PDCTR-08797/22 to PSB), (FAPESPA; grant 028/2021 to ECG), (CNPq; grant 307974/2021-9 to FPO), (CNPq-IC; grant 134775/2020-1 to RFO), (FAPEMA; grant BM-00809/22 to LOV), (FAPEMA-IC; grants BIC-01958/20 and BIC-04123/21 to MSPC), (FAPERJ; grant E–26/202.005/2020 to AMK) and (CAPES; grant 88887.674455/2022-00 to DSC). This study was supported by the projects “PROCESSO UNIVERSAL-00724/17” and “Processo UNIVERSAL-00437/19”, from FAPEMA.
Author contributions
Conceptualisation: Felipe Ottoni, Erick Guimarães, Lucas Vieira. Data collecting, organising and curation: Lucas Vieira, Rafael Oliveira, Diego Campos, Marcony Coelho, Maurício Paiva, Erick Guimarães, Pâmella Brito, Felipe Ottoni. Specimens identification: Lucas Vieira, Rafael Oliveira, Diego Campos, Marcony Coelho, Maurício Paiva, Erick Guimarães, Pâmella Brito, Axel Katz, Felipe Ottoni. Supplementary material: Lucas Vieira. Ecological and statistics analyses: Josie South, Diego Campos. Manuscript writing: Lucas Vieira, Felipe Ottoni, Josie South, Pedro Bragança, Diego Campos, Marcony Coelho, Maurício Paiva, Rafael Oliveira, Erick Guimarães, Pâmella Brito, Jadson Santos, Axel Katz. Map and river basin sectorisation: Diego Campos. Photographs: Lucas Vieira and Rafael Oliveira. Photographs editing: Axel Katz. Supervision: Felipe Ottoni, Pedro Bragança, Josie South. English language review: Pedro Bragança, Josie South. All authors have read and agreed to the published version of the manuscript.
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Map with sampling sites along the Munim River Basin. Sample sites are listed in Table 1 and illustrated on the map as L1-L84. MA = State of Maranhão and PI = State of Piauí. In the highlighted squares are the geographically close sample sites, for better visualisation. River basin sections: Estuary section (green), Lower section (orange), Middle section (lilac) and Upper section (pink).
Samples sites: L1, L18, L19, L30, L31, L36, L38, L43, L49, L53, L54, L55, L62, L65, L66, L69, L75, L77, L78 and L84 according to Table 1. Photographed by Lucas Vieira and Rafael Oliveira, edited by Axel Katz.
Selected fish species collected in the Munim River Basin of the Order Characiformes: AAcestrorhynchusfalcatus (CICCAA 06398, 112.60 mm SL), BAphyocharax sp. (CICCAA 06636, 32.91 mm SL), CCharaxawa (CICCAA 06430, 80.22 mm SL), DGasteropelecussternicla (CICCAA 06366, 39.50 mm SL), EHemiodusparnaguae (CICCAA 06238, 94.99 mm SL), FLeporinusaff.friderici (CICCAA 02755, 102.31 mm SL), GMetynnislippincottianus (CICCAA 06383, 64.06 mm SL), HMoenkhausiacf.intermedia (CICCAA 06634, 50.38 mm SL), IMoenkhausia sp. (CICCAA 06635, 35.10 mm SL), JPoptellacompressa (CICCAA 06429, 42.46 mm SL), KProchiloduslacustris (CICCAA 06340, 84.94 mm SL), LPsectrogasterrhomboides (CICCAA 06270, 121.08 mm SL), MPygocentrusnattereri (CICCAA 06271, 138.08 mm SL), NSchizodondissimilis (CICCAA 06344, 99.03 mm SL), OSerrasalmusrhombeus (CICCAA 06269, 70.99 mm SL), PTriportheussignatus (CICCAA 06339, 86.62 mm SL). Photographed by Lucas Vieira and Rafael Oliveira, edited by Axel Katz.
Selected fish species collected in the Munim River Basin of the Order Siluriformes: AAncistrus sp. (CICCAA 06652, 76.85 mm SL), BAuchenipterusmenezesi (CICCAA 06534, 98.38 mm SL), CBatrochoglanis sp. (CICCAA 06654, 64.16 mm SL), D - Callichthyscallichthys (CICCAA 03927, 102.12 mm SL), ECorydorasjulii (CICCAA 06378, 34.33 mm SL), FCorydorasvittatus (CICCAA 06418, 34.19 mm SL), GHassaraffinis (CICCAA 06263, 109.79 mm SL), HHoplosternumlittorale (CICCAA 06657, 81.91 mm SL), IHypoptopomaincognitum (CICCAA 06315, 70.81 mm SL), JItuglaniscf.amazonicus (CICCAA 06643, 30.53 mm SL), KLoricariacf.cataphracta (CICCAA 06628, 105.80 mm SL), LLoricariichthys sp. (CICCAA 06328, 160.18 mm SL), MPimelodella sp.1 (CICCAA 06629, 83.02 mm SL), NPlatydorasbrachylecis (CICCAA 04608, 58.36 mm SL), OPseudoplatystomafasciatum (CICCAA 04549, 208.39 mm SL), PSorubimlima (CICCAA 06272, 204.01 mm SL), QTatiaintermedia (CICCAA 02736, 46.17 mm SL), RTrachelyopterusgaleatus (CICCAA 06243, 122.56 mm SL). Photographed by Lucas Vieira and Rafael Oliveira, edited by Axel Katz.
Selected fish species collected in the Munim River Basin of the Orders Cichliformes and Gymnotiformes: AGeophagusparnaibae (CICCAA 06229, 98.62 mm SL), BSatanopercajurupari (CICCAA 06377, 105.36 mm SL), CApteronotusalbifrons (CICCAA 06266, 168.59 mm TL), DEigenmanniarobsoni (CICCAA 06631, 180.36 mm TL), ESternopygusmacrurus (CICCAA 06261, 183.50 mm TL). Photographed by Lucas Vieira and Rafael Oliveira, edited by Axel Katz.
Hierachial cluster diagram of fish assemblage based on Jaccard Index per basin section using species presence-absence data.
https://binary.pensoft.net/fig/804159
Sampling sites at the Munim River Basin, Maranhão, Brazil. *Localities with the presence of non-native species.
Locality number (L)
Locality
Municipality
Coordinates
Altitude
River basin section
01
Stream in the balneário at the entrance of Anapurus
Anapurus - MA
03°40'15.28"S 043°07'9.7"W
81 m
Middle
02
*Stream at balneário São Lourenço
Anapurus - MA
03°39'16.30"S 043°6'50.2"W
75 m
Middle
03
Stream at balneário Recanto do Buriti
Anapurus - MA
03°40'53.04"S 043°7'23.0"W
76 m
Middle
04
Riacho crossing the road at Poços community
Anapurus - MA
03°33'44.61"S 043°3'52.4"W
71 m
Middle
05
Stream at Caraíbas community
Chapadinha - MA
03°56'7.71"S 043°26'14.8"W
51 m
Middle
06
Riacho Xororó at Aparecida neighbourhood
Chapadinha - MA
03°44'2.23"S 043°22'1.21"W
81 m
Middle
07
Stream at Aldeia neighbourhood
Chapadinha - MA
03°45'7.75"S 043°21'32.7"W
74 m
Middle
08
Stream at Aldeia neighbourhood
Chapadinha - MA
03°44'53.1"S 043°21'32.6"W
80 m
Middle
09
Stream at Terra Duras neighbourhood
Chapadinha - MA
03°45'6.42"S 043°22'24.7"W
65 m
Middle
10
Riacho Feio, Boa Vista community
Chapadinha - MA
03°50'51.8"S 043°18'50.5"W
44 m
Middle
11
*Riacho Feio, Boa Vista community
Chapadinha - MA
03°50'46.8"S 043°18'48.9"W
40 m
Middle
12
Riacho Feio, São José community
Chapadinha - MA
03°51'6.30"S 043°17'53.0"W
45 m
Middle
13
*Riacho Feio, São José community
Chapadinha - MA
03°51'18.7"S 043°17'14.4"W
47 m
Middle
14
Riachinho, Cumbre community
Chapadinha - MA
03°51'46.8"S 043°17'10.2"W
52 m
Middle
15
Riachinho, Água Branca community
Chapadinha - MA
03°53'13.5"S 043°16'37.1"W
59 m
Middle
16
Riacho Feio, Riacho Feio community
Chapadinha - MA
03°51'42.84"S 043°16'1.7"W
52 m
Middle
17
Rio Iguará, Malhadinha community
Vargem Grande - MA
03°54'27.8"S 043°44'55.8"W
30 m
Middle
18
Rio Iguará, Malhadinha community
Vargem Grande - MA
03°54'3.25"S 043°44'55.8"W
32 m
Middle
19
Rio Iguará, Poço Cumprido community
Chapadinha - MA
04°2'54.24"S 043°34'58.4"W
41 m
Middle
20
Stream at Itamacaoca forest
Chapadinha - MA
03°44'45.2"S 043°19'15.0"W
90 m
Middle
21
Stream at balneário Repouso do Guerreiro
Chapadinha - MA
03°44'57.4"S 043°20'24.0"W
66 m
Middle
22
Stream at Itamacaoca forest
Chapadinha - MA
03°44'27.2"S 043°19'36.5"W
85 m
Middle
23
Itamacaoca dam
Chapadinha - MA
03°44'56.5"S 043°19'55.8"W
74 m
Middle
24
Stream just after Itamacaoca dam
Chapadinha - MA
03°45'7.42"S 043°20'4.05"W
68 m
Middle
25
Jabuti community, Tinguis road
Chapadinha - MA
03°46'11.9"S 043°20'25.2"W
50 m
Middle
26
Rio Preto at Bom Sucesso community
Mata Roma - MA
03°34'0.40"S 043°19'0.40"W
45 m
Middle
27
Swampy areas at Brejo do Meio community
Chapadinha - MA
03°55'38.7"S 043°30'13.1"W
53 m
Middle
28
Stream behind the Mix Atacarejo Mateus store
Chapadinha - MA
03°45'6.00"S 043°20'23.0"W
59 m
Middle
29
Rio Munim, Carnaúba Amarela community
Chapadinha - MA
03°51'51.3"S 043°19'36.8"W
39 m
Middle
30
Rio Munim, Porções bridge
Chapadinha - MA
03°50'50.0"S 043°19'19.4"W
41 m
Middle
31
*Rio Munim, Cedro community
Chapadinha - MA
03°50'15.5"S 043°19'41.1"W
41 m
Middle
32
Rio Munim, Riacho Fundo community
Chapadinha - MA
03°42'22.7"S 043°31'47.1"W
25 m
Middle
33
Rio Munim, bridge at Mangabeira community
Chapadinha - MA
03°48'34.1"S 043°24'33.2"W
33 m
Middle
34
Stream at Pai Gonçalo community
Chapadinha - MA
04°2'38.12"S 043°28'40.7"W
82 m
Middle
35
Stream at Mucambo community
São Benedito do Rio Preto - MA
03°29'1.01"S 043°33'39.5"W
92 m
Middle
36
Riacho da Raiz
Chapadinha - MA
03°53'45.1"S 043°29'21.3"W
45 m
Middle
37
Riacho São João, São João dos Pilão
Brejo - MA
03°41'2.64"S 042°56'31.9"W
89 m
Middle
38
Riacho Pau Preto, Pau Preto community
Brejo - MA
03°39'54.9"S 042°56'35.5"W
84 m
Middle
39
Riacho da Cruz, close to Palestina
Brejo - MA
03°41'18.0"S 042°58'39.8"W
88 m
Middle
40
Rio Preto, Água Rica community
Brejo - MA
03°41'34.92"S 043°0'56.1"W
78 m
Middle
41
Córrego Água Rica
Anapurus - MA
03°41'41.24"S 043°1'44.8"W
86 m
Middle
42
Riacho do Muquém
Mata Roma - MA
03°42'21.2"S 043°13'57.1"W
68 m
Middle
43
Stream, Laranjeira community
Buriti - MA
03°52'31.09"S 043°3'0.60"W
96 m
Middle
44
Rio Munim, Capoeira Grande community
Afonso Cunha - MA
04°10'2.79"S 043°13'28.0"W
54 m
Upper
45
Rio São Gonçalo
Afonso Cunha - MA
04°7'58.77"S 043°19'16.1"W
64 m
Upper
46
Stream crossing the road
Afonso Cunha - MA
04°10'53.63"S 043°14'1.5"W
58 m
Upper
47
Stream crossing the road
Afonso Cunha - MA
04°12'23.9"S 043°14'46.8"W
68 m
Upper
48
Riacho barrigudinho
Afonso Cunha - MA
04°18'46.1"S 043°13'39.1"W
67 m
Upper
49
Riacho do boi
Afonso Cunha - MA
04°19'12.38"S 043°13'9.8"W
67 m
Upper
50
Stream crossing the road
Aldeias Altas - MA
04°22'14.3"S 043°12'17.6"W
69 m
Upper
51
Riacho do boi
Aldeias Altas - MA
04°26'4.96"S 043°11'46.9"W
82 m
Upper
52
*Rio Bandeira, Belágua
Belágua - MA
03° 9'22.7"S 043°30'35.4"W
65 m
Middle
53
Riacho Água Fria on the road MA-110
Belágua - MA
03°10'9.49"S 043°28'45.3"W
68 m
Middle
54
Rio Bandeira
Urbano Santos - MA
03°11'49.0"S 043°24'29.3"W
41 m
Middle
55
Rio Mocambo
Urbano Santos - MA
03°12'34.6"S 043°24'23.8"W
38 m
Middle
56
Stream on the road MA-224
São Benedito do Rio Preto - MA
03°18'46.2"S 043°30'25.1"W
40 m
Middle
57
Rio Preto, São Benedito do Rio Preto
São Benedito do Rio Preto - MA
03°19'59.0"S 043°31'34.8"W
29 m
Middle
58
Stream on the road MA-224
São Benedito do Rio Preto - MA
03°29'29.0"S 043°35'25.9"W
50 m
Middle
59
Rio Munim, on the road MA-224
Nina Rodrigues - MA
03°35'14.1"S 043°39'50.4"W
21 m
Middle
60
Rio Munim, at the quilombola community Evienã
Presidente Vargas - MA
03°22'31.0"S 043°58'18.5"W
14 m
Middle
61
Riacho Paulica on the road MA-020
Presidente Vargas - MA
03°25'54.98"S 043°58'1.0"W
16 m
Middle
62
Rio Munim at Nina Rodrigues City
Nina Rodrigues - MA
03°27'36.1"S 043°54'15.1"W
14 m
Middle
63
Riacho Paulica on the road BR-222
Vargem Grande -MA
03°31'11.5"S 043°58'30.7"W
23 m
Middle
64
Rio Iguará on the road BR-222
Vargem Grande - MA
03°33'9.64"S 043°52'23.0"W
22 m
Middle
65
Rio Munim mouth at Icatu
Icatu - MA
02°46'33.86"S 044° 4'1.3"W
1 m
Estuary
66
Rio Una, between the municipalities of Morro and Icatu
Morros - MA
02°50'3.06"S 044°2'24.82"W
8 m
Lower
67
Rio das Cobra, Santa Helena community
Morros - MA
02°49'22.1"S 044° 2'34.8"W
9 m
Lower
68
Riacho at the entrance to Icatu
Icatu - MA
02°46'58.50"S 044°2'48.2"W
19 m
Lower
69
Rio Munim, Cachoeira Grande
Cachoeira Grande - MA
02°55'36.25"S 044°3'39.2"W
4 m
Lower
70
Stream crossing the road MA-020
Cachoeira Grande - MA
02°55'14.62"S 044°2'31.5"W
34 m
Lower
71
Stream next to the road MA-402
Axixá - MA
02°51'37.1"S 044° 3'14.5"W
4 m
Lower
72
Rio Munim between the municipalities of Axixá and Presidente Juscelino
Axixá - MA
02°52'35.63"S 044°3'41.8"W
15 m
Lower
73
Stream between the municipalities of Axixá and Presidente Juscelino
Axixá - MA
02°53'50.06"S 044°4'15.9"W
4 m
Lower
74
Rio Munim, Presidente Juscelino
Presidente Juscelino - MA
02°55'39.38"S 044°3'50.5"W
6 m
Lower
75
Rio Una, Cachoeira do Arruda
Morros - MA
02°53'31.5"S 043°58'13.8"W
28 m
Lower
76
Riacho das Pacas
Morros - MA
02°51'4.94"S 043°57'52.1"W
28 m
Lower
77
Stream next to the road MA-402
Morros - MA
02°51'19.5''S 044°01'03.0''W
19 m
Lower
78
Rio Munim, Axixá
Axixá - MA
02°50'14.60"S 044°3'3.81"W
1 m
Lower
79
Rio Munim, Balceiro community
Chapadinha - MA
03°46'44.9"S 043°26'42.7"W
33 m
Middle
80
Stream at the Paiol community
Chapadinha - MA
04°1'13.56"S 043°29'27.6"W
74 m
Middle
81
Stream at São Pedro community
Chapadinha - MA
03°54'4.66"S 043°35'12.3"W
73 m
Middle
82
Stream crossing a road in the Resex
Chapadinha - MA
03°56'10.0"S 043°30'29.5"W
61 m
Middle
83
Riacho Xororó at Aparecida neighbourhood
Chapadinha - MA
03°44'7.77"S 043°22'8.94"W
69 m
Middle
84
Riachinho, Água Branca community
Chapadinha - MA
03°52'37.67"S 043°16'59.37"W
60 m
Middle
List of fish species recorded for the Munim River Basin in the present study. *endemic species to the hydrological units Maranhão and Parnaíba sensuHubert and Renno (2006).