Fish fauna of the Pandeiros River , a region of environmental protection for fish species in Minas Gerais state , Brazil

The Area of Environmental Protection of the Pandeiros River is the largest unit for sustainable use in Minas Gerais state, Brazil. The Pandeiros Wetland in the lower part of this river is considered a nursery for most migratory fish species of the São Francisco River and it is currently threatened by the introduced peacock-bass Cichla piquiti (Kullander & Ferreira, 2006). In this study, a list of fish species from the Pandeiros River was developed and compared with data for populations from other regions in the São Francisco basin. The presence of a new species record for the São Francisco River basin in the Pandeiros, and the particular local biotic and abiotic conditions of that river, support its recognition as an important conservation unit within the basin.


INTRODUCTION
The São Francisco River is 2,780 km long and drains 450 municipalities of seven Brazilian states (Franco de Camargo and Petrere 2001).The headwaters of the Pandeiros River, an important tributary of the middle São Francisco River, are in northern Minas Gerais state, Brazil.This river is 145 km long and its flow rate ranges from 8 m³/s in the dry season to 24 m³/s in the rainy season.The tributaries of the Pandeiros River are the Pindaibal I and II, São Pedro, Alegre, and Mandins rivers on the left bank and the Catolé, Borrachudo, Macaúbas, and São Domingos rivers on the right bank.The area where the Pandeiros River reaches the São Francisco River is known as the Pandeiros Wetland (Lopes et al. 2010).
The Area of Environmental Protection of the Pandeiros River (AEP-Pandeiros) was established by State Law No.11.901 in 1995.It encompasses 393,060 hectares and is the largest unit for sustainable use in Minas Gerais state.AEP-Pandeiros covers the entire basin of the Pandeiros River in the municipalities of Januária, Bonito de Minas, and Cônego Marinho (Lopes et al. 2010).This AEP has global conservation relevance because freshwater ecosystems are the most threatened biodiversity hotspots (Strayer and Dudgeon 2010).The objective of the AEP-Pandeiros is to protect the Pandeiros Wetland and the biological diversity in the surrounding area for development and reproduction of native fish species.Wetlands are home to large assemblages of species (Gibbs 2000), and the Pandeiros Wetland, with an area of 3,000 ha in the dry season to 5,000 ha in the wet season, is considered to be the nursery of most migratory fishes of the São Francisco Basin (Godinho and Godinho 2003).The ecotone of the AEP-Pandeiros contains three vegetation types (savannah is the predominant vegetation, but Caatinga and dry forest are also present), which increases local diversity and provides suitable conditions for species that require large habitat ranges.The area, therefore, is a priority for conservation (Kark et al. 2007), as established by the Atlas of Biodiversity Conservation of Minas Gerais state (Drummond et al. 2005).Although the local fauna is poorly studied, 315 bird species were listed in this conservation unit (Lopes et al. 2010).The fish fauna of the Pandeiros River is less well known than that of the Velhas River (Alves and Pompeu 2001) and the Três Marias Dam (Britski et al. 1986), both in the São Francisco River basin.
The decline of fish fauna at a global scale can be attributed to factors such as habitat alteration, water extraction, pollution, commercial exploitation, and the introduction of exotic species (Paiva et al. 2006;Barros et al. 2012), but their cumulative effects are less predictable.Lists of species are one of the tools used to establish priorities for conservation (Jowett and Richardson 2003;Raghavan et al. 2008) and to guide use of financial resources for biodiversity management (Grammont and Cuarón 2006).
In this study, an inventory of the Pandeiros River fishes was undertaken and compared with other fish assemblages from the São Francisco basin region.The results underscore the importance of the AEP-Pandeiros for conservation of fish species of the São Francisco River basin.

MATERIALS AND METHODS
Collecting permit SISBIO14975-1 was provided by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio); this authorization is valid for the collection, transport, and sacrifice of an unlimited number of specimens of all fish taxa from Pandeiros River basin.Four field campaigns were conducted: two in the dry season (July) et al. 1986;Alves and Pompeu, 2010, and original species descriptions), with taxonomic classification following Eschmeyer (2013).Prior to preservation, specimens captured alive were anaesthetized and euthanized with clove oil following Inoue et al. (2003).

RESULTS
Forty-four fish species were identified in the Pandeiros River basin (Table 1), including the large piscivorous catfish, Pseudoplatystoma corruscans, and the minute Planaltina sp.(Figure 2).Sixteen species were collected upstream of the three waterfalls of the Pandeiros River and nine of them occurred only in this region: Acestrorhynchus lacustris, Myl eus altipinnis, Characidium aff.zebra, Hoplias intermedius, Pimelodella cf.lateristriga, Corydoras multimaculatus, Hart tia longipinna, Planaltina sp. and Trichomycterus sp.On the other hand, Trachelyopterus galeatus, Pterygoplichtys etentaculatus, Salminus franciscanus, Prochilodus argenteus, Pimelodus maculatus, Leporinus reinhardtii, Brycon orthotae nia, Pseudoplatystoma corruscans, and Leporinus elongatus were only recorded downstream of the three waterfalls.Bryconops affinis, Bryconamericus stramineus and Piabina argentea were only recorded at the beach of the Pandeiros Resort.Hoplosternum littorale and Cichla piquiti, which are non-natives to the São Francisco River basin, were captured in the Pandeiros Wetland.and two in the rainy season (February and December) of 2008 and 2009.Fish were caught with trolling nets, seines, fishing rods, and mesh nets (mesh sizes 3,4,5,7,8,10,12,14 mm between opposite knots) from dusk to dawn in different habitats in the basin.The two sites upstream of the three waterfalls of the Pandeiros River were Catolé Stream, a tributary of the Pandeiros River at the Santa Maria da Vereda Farm (15°24'43" S, 044°50'32" W), and at the bridge over the Pandeiros River (15°26'27.0"S, 044°49'19.2"W).Collections downstream of the three water falls were made at the Pandeiros Resort (15°26'48.7"S, 044°49'32.0"W) and the Pandeiros Wetland in Três Irmãs Farm (15°40'01.8"S, 044°37'99.3"W) (Figure 1).Tissue samples from captured specimens were deposited in the public tissue collection of the Laboratory of Molecular Systematics at the Universidade Federal de Viçosa (UFV) in Viçosa, Minas Gerais state, Brazil, which is an authorized depository of the Brazilian Genetic Heritage (Ministério do Meio Ambiente, decision no 23 of 24 April 2003).Voucher specimens were fixed in 10% formalin, stored in 70% alcohol, and deposited in the ichthyological collection of the João Moojen Zoology Museum at the UFV, the ichthyological collection of the Universidade Federal do Rio Grande do Sul (UFRGS), and the ichthyological collection of the Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS).Fish specimens were identified following specialized literature (e.g., Britski     (Britski et al. 1986), 21 in marginal lakes of the São Francisco River in the municipalities of Jaíba, and Itacarambi (Minas Gerais) (Pompeu and Godinho 2003), 19 in the Juramento River (Silva et al. 2006), and 13 in Itapecerica River (Domingos et al. 2013).This pattern indicates that the fishes of the Pandeiros River are widely distributed in the São Francisco River basin.However, the presence of the nearthreatened species Pseudoplatystoma corruscans, included in the list of endangered species in Minas Gerais state (Vieira et al. 2008), underscores the importance of the AEP-Pandeiros as environmental protection region for the conservation of the ichthyofauna of the São Francisco basin.The relevance of the AEP-Pandeiros also applies to small-sized, poorly known species: the occurrence of Planaltina sp. in the Pandeiros River for example, represents the first record of this genus in the São Francisco River basin.Currently, only three species of this genus have been described: Planaltina myersi from the Corumbá River (a tributary of the Paranaíba River), and Planaltina glandipedis and Planaltina britskii from tributaries of the Grande and Tietê rivers, all tributaries of the Upper Paraná River (Menezes et al. 2003).Based on a bibliographic review undertaken for this study, and including Planaltina sp., the number of known freshwater fish species in the basin is 233 (Britski et al. 1986;Malabarba andWeitzman 1999, 2000;Alves and Pompeu 2001;Lütken 2001;Reis et al. 2003;Pompeu and Godinho 2003;Costa 2005Costa , 2006Costa , 2013Costa , 2014;;Silva et al. 2006;Costa and Brasil 2006;Bockmann and Castro 2010;Nielsen et al. 2010;Costa and Amorim 2011;Costa et al. 2012;Ottoni 2012;Lehmann and Reis 2012;Bichuette and Rizzato 2012).
Of the sixteen species collected upstream of the three waterfalls, Myleus altipinnis, Characidium aff.zebra, Hoplias intermedius, Pimelodella cf.lateristriga, Corydoras multimacu latus, Harttia longipinna, Planaltina sp. and Trichomycterus sp. were not found anywhere else.This suggests their preference for water rapids which are characteristic of this river section.According to reports from locals, Acestrorhynchus lacustris, another species recorded only in this part of the river, was recently stocked in the upper Pandeiros River.This species has generalist piscivorous habits (Hahn et al. 2000), which may impact natural fish populations upstream.The lack of sampling of the migratory species Brycon orthotaenia, Pimelodus maculatus, Pseudoplatystoma corruscans, Salminus franciscanus, Leporinus elongatus, and Prochilodus argenteus upstream of the three waterfalls suggests that these constitute a barrier for some species of the fish fauna of the Pandeiros River.The occurrence of Trachelyopterus galeatus, Pterygoplichtys etentac ulatus, and the migratory fishes S. franciscanus, P. argenteus, P. maculatus and Leporinus reinhardtii in the Pandeiros Wetland and the Pandeiros Resort are likely due to the physical continuity without waterfalls.In the Pandeiros Wetland and the Pandeiros Resort it was possible to see schools of P. argenteus closely followed by S. franciscanus, which is an efficient predator in lotic environments (Rodríguez-Olarte and Taphorn 2006).The migration of fishes in the São Francisco River basin occurs with greater intensity from October to January, probably due to the greater water volume in the river, higher temperature, and longer days.Salminus franciscanus, P. argen teus, P. maculatus, L. reinhardtii, L. elongatus, B. orthotaenia, and P. corruscans ascend the river channel and reproduce in the tributaries (Godinho and Godinho 2003).In a mark and recapture study of P. argenteus, 10% of the specimens were recaptured 800 km upstream 85 days after release (Sato and Godinho 2003), thus demonstrating the great migratory capacity of this species.
Bryconops affinis was collected in all campaigns immediately downstream of the lower waterfall.Juveniles of this species apparently prey on Bryconamericus stramineus and Piabina argentea juveniles, which were observed in the shallow, clear water along the beach of Pandeiros Resort.Bryconamericus species are omnivorous, may reach 10 cm in length, live in diverse environments, and are an important food item for larger fishes (Lima et al. 2003).
The presence of the invasive species Hoplosternun littorale and Cichla piquiti in the AEP-Pandeiros may affect native biodiversity due to competition for resources (H.littorale) or predation (C.piquiti) (Duncan and Williams 2002).Fish communities of native species have declined in parts of the São Francisco River basin in association with exotic species introduction.For example, populations of small fishes such as Astyanax lacustris, Curimatella lepidura, and Triportheus guentheri are declining, whereas non-native species have increased their populations in the Três Marias Dam (Sato and Godinho 2003).
The wetland formed by the Pandeiros River can be considered a nursery for migratory fish species of the São Francisco River.High temperatures and large amounts of nutrients, macrophytes, phytoplankton, and zooplankton are present in the Pandeiros River.These are favorable biotic conditions for the reproduction of fish species, and they provide food sources for fish larvae of the São Francisco River.Thus, the Pandeiros River helps maintain temporal processes and biodiversity in this basin (Ward and Tockner 2001).
The diversity of fish of the Pandeiros River and local biotic conditions (ecotone regions) are consistent that AEP-Pandeiros is an important conservation unit for the ichthyofauna of the São Francisco River basin, in Brazil.

ACKNOWLEDGMENTS
Our thanks go to Asia Science and Journal Editors of America LLC for English revision and editing this manuscript.We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq) and Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG) for financial support.Our thanks also to Fernando Carvalho for help with some species identifications and Melanie L. Stiassny for valuable suggestions on manuscript revision.

Table 1 .
Fish species collected and place of capture in the Environmental Protection Area Pandeiros.