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Check List 10(4): 864–869, 2014 © 2014 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution

Ichthyofauna of the Sumidouro system, state of Minas pecies S

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Ruanny Casarim * ists L Gerais, , Débora Reis de Carvalho, Rafaela Bastos Pereira and Paulo Santos Pompeu [email protected] Universidade Federal de , Departamento de Biologia. Campus Universitário, s/n. CEP 37200-000. Lavras, , Brazil. * Corresponding author: E-mail: Abstract:

Alterations in environmental conditions may cause changes to fish assemblages regarding their composition and distribution. This study aimed to describe the composition the ichthyofauna of the Sumidouro system and to compare it with the ichthyofauna found in the Lagoa Central. The Sumidouro system is a preserved aquatic biome located on the assemblagesRio das Velhas of drainage both systems on central was evaluated Brazil while in four the Lagoadifferent Central scenarios, is an environmentbuilt from recently under publishedanthropogenic data, impactand compared located inside the Lagoa Santa city. Sampling of the Sumidouro system was carried out, in October 2012. The similarity of the fish

by a cluster analysis using Sorensen similarity index. The Sumidouro system is more similar to the historical fauna of the SumidouroLagoa Central system or after may its be isolation causing fromloss of Rio aquatic das Velhas. biodiversity, This indicates as observed that ina cavethe Lagoa located Central. at this region (Sumidouro Cave) may act as a barrier to fish movements. The results also allow us to infer that the intensification of urbanization around the

DOI: 10.15560/10.4.864

Introduction the habitat use by native species (Zaret and Paine 1973; Welcomme 1988; Canonico et al. 2005; Vitule 2009), leading to local extinction (Welcomme 1988). Since most Biological communities vary through timeet andal. 2012). space invasive exotic species do not have natural predators as a result of differences in habitat structure (Gorman and where they are introduced, they may proliferate fast, thus Karr 1978; Ferreira and Casatti 2006; Dubey competing with, or even feeding directly on, native species The recognition of mechanisms and factors responsible for (Agostinho et al. 2007). Sutherlandsuch differences et al. 2013).is one of the most important objectives Comparative studies of lagoons that involve substantial of community ecology (Angermeier and Karr 1984; variations of abiotic conditions are excellent opportunities physical and biological factors as responsible for the to examine the effects of factors responsible for There is a discussion regarding the importance of et al. 1998). point that the spatial distribution of results from complexdistribution ecological of freshwater relationships fishes among and species, some authors which thestructuring ichthyofauna fish assemblages in the Sumidouro (Tejerina-Garro system, a preserved environmentThe aim of this located study at is tothe describe protected the area composition of Parque of ecosystem, habitat connectivity (individual species turnover),are influenced and byhabitat environmental availability, characteristics allied to species of the SumidouroEstadual do system Sumidouro and compare(Minas Gerais it with state, the Brazil).fauna of Also, the Lagoathis study Central aim of tothe characterize Lagoa Santa thecity, ichthyofaunalocated in the of same the anthropogeniccomposition (Welcomme actions leading 1979; to habitat Werner changes 1986; may Wootton have basin, and which has been suffering several environmental 1998; Grenouillet and Hérissé 2004). Consequently, impacts. Currently, the fast expansion of urban centers has beendeep influencecausing alterations on species to composition aquatic environment on ecosystems. through Materials and Methods Study area et alcanalization,. 2012). Such dams, activities siltation, directly and affect the reduction the geomorphology of vegetal comprising Sumidouro lagoon and Samambaia stream. ofcover the (Malmqvist channel , leadingand Rundle to changes 2002; Allan in the 2004; original Casarim lotic This study was developed in the Sumidouro system, characteristics, and causing the loss of biodiversity and a Estadual do Sumidouro, Rio das Velhas basin (Figure 1). et Studied areas are located at 19°32′ S and 43°56′ W, in Parque al. 2005; Cunico et al decrease in the abundance of fishes (Sale 1985; Pompeu The park is 50 Km from Belo Horizonte, in municipalities of the community structure. 2006). Another due to frequentlythe introduction observed of of aLagoa Federal Santa Conservation and Pedro UnitLeopoldo, and belongs state of to Minas the category Gerais, exoticproblem species in intensively in the watercourse. inhabited areas is the modification ‘sustainablecentral Brazil. use The of Parque natural Estadual resources’ do Sumidouro – APA Carste consists de Lagoa Santa. Such conservation units aim to promote the to the environment in which they are introduced due to conservation of nature through the sustainable use of part theirThe facility non-native to reproduce species and with disperse, invasive they potential may preclude adapt of available resources (MMA 2000).

864 Casarim et al. | Ichthyofauna of Sumidouro system, Brazil

six meters with the aim of collecting the ichthyofauna. Fish collections were performed from downstream to The Sumidouro lagoon is a temporary lake that has upstream with sieves made from mosquito netting (80 cm multiannual cycles. The lagoon may achieve a perimeter of 15 Km when full, or be completely devoid of water in drought periods (Figure 2A and 2B). This drought and asin diameter,standard 1mmtime for mesh sampling. size) and with trawl nets (3 m long, flood cycle is a natural phenomenon. The lagoon lies in 5 mm mesh size). For each point, 20 min was established a karstic region, a type of relief formed by the corrosive effect of water on soluble rocks such as limestone (IEF- The Sumidouro lagoon was also sampled once in MG 2010). Due to the peculiar characteristics of this October 2012 (Figure 3). For fish collections, trawl nets region many phenomena of karstic hydrography, such were used (3 m long, 50 mm mesh size) and two sets of as upwellings and sinkholes, are present at the Parque 150gillnets m2 with 2.4 - 14 centimeters-mesh between opposite Estadual do Sumidouro. There are sinkholes within the 18:00knots h and with 10 gillnets; meters these long. were Each set set up had in approximatelythe afternoon Sumidouro lagoon, which gave the place its name (IEF-MG and removed. A total the of followingten drags morning,were performed giving a at total 6:00 of h 12 and h 2010). The water from the Samambaia stream is the main of sampling. Specimens of each species were deposited in water source of the lagoon, flowing into these sinkholes the Ichthyological Collection of the Federal University of and then rising, debouching into the Rio das Velhas (IEF- Lavras (UFLA). Fish were collected under the IEF license MG 2010; Pereira and Caldeira 2011). The Lagoa Central is located downtown in the Fishes from the Sumidouro system (Sumid) were municipality of Lagoa Santa, 19°38′ S and 43°53′ W, compared#UC127/12. with those from the Lagoa Central of the Lagoa 40 km north of Belo Horizonte, and is part of the Rio max.= 7 m), situated at das Velhas basin, Brazil (Pompeu and Alves 2003).2 Theand different human impacts, including isolation from the lagoon is relatively shallow (depth 2 et al. 1998). Santa city. Because Lagoa Central has been submitted to an altitude of 740 m, covering a total area of 1.31 km fauna in four different scenarios based on Pompeu and highwith diversity a drainage of basinaquatic of life, 11.34 excellent km (Parizzi water quality and main river, we considered the Lagoa Central (LC) fish The Lagoa Central was considered an ecosystem with the region has suffered increasing transformations as a historicalAlves (2003): fauna historicalminus lost fauna species (LC-Hist: (migratory) 17 species); due to great transparency. However, since the end of the 1970s, thecurrent current fauna interruption (LC-Curr: 10 of species, communication including withexotic Rio ones); das onlyconsequence caused changes of disordered in the water urbanization quality and (Coutinho transparency, and butBarbosa also in 1986). its communication Such increase with in humanRio das occupationVelhas through not Velhas (LC-Isol: 14 species); and current fauna minus lost species (others) by introduction of exotic species (LC-Exot: decrease in biological diversity due to the introduction of 6 species). In the last scenario, we considered lost due to the Bebedouro stream. Furthermore, studies show a the exotic fish introduction all the lost species that do not depend on the communication between the lake and the Dataexotic collection fish species (Pompeu and Alves 2003). throughriver to complete a Cluster their analysis life cycle. based These on the four similarity scenarios index and the fishes from the Sumidouro system were compared Samambaia stream, in October 2012 (Figure 3). At each point,Twenty-three two trawl nets points were were used sampledto isolate once a stretch in the of of Sorensen, UPGMA groupinget (Davisal. (1988). and Greenes 1983). Identification of the sampled fishes in the Sumidouro system was based on Britski

Figure 1. Location map of the Sumidouro System highlighting the Sumidouro Lagoon, Samambaia stream and the sample sites.

865 Casarim et al. | Ichthyofauna of Sumidouro system, Brazil

Figure 2.

The Sumidouro lagoon when full (A) and completely devoid of water (B) in October 2012 and July 2013, respectively (Photos Ruanny Casarim andResults Parque Estadual do Sumidouro-IEF) of the Lagoa Central of the Lagoa Santa city and the SumidouroThe greater system similarity may be betweenexplained the by historicalthe obstruction fauna the Overall,Sumidouro 16021 lagoon fish specimens, and Samambaia belonging stream, to five which, orders, at of the natural communication between Lagoa Central and leastnine families,two of these 12 genera species and are 16 exotic species, to the were Rio collected das Velhas in basin: Tilapia rendalli and Hoplosternum littorale the rio das Velhas, formerly provided by the Bebedouro (Table characteristicsstream. This obstructionof the stream caused (Pompeu the and isolation Alves 2003). of the At 1) (Godinho and Godinho 2003). The greatest biodiversity Lagoa Central and the extinction of some fish species was found in the Characiformes (68%) and Siluriformes are still present (Characidium zebra and Trachelyopterus (25%) orders. galeatus)the Sumidouro. In addition, system thesome similarity of these foundstream between fish species the Ten species were known for the Lagoa Central system(Pompeu of andthis Alvesregion. 2003). By adding nine species found in the Rio das Velhas and the Sumidouro system may be the present study, 19 species are identified for the karstic explainedfish fauna byfrom the the fact Lagoa that the Central Lagoa after Central its isolation isolation from also with the different scenarios built for the Lagoa Central, greaterWhen similarity comparing was the found fishes with of thethe Sumidourohistorical fauna system of as Prochilodus costatus and Pimelodus maculatus (Pompeu caused the extinction of the migratory fish species, such situation with Sumidouro system may be explained by the the Lagoa Central (LC-Hist), or after its isolationA. lacustris, from the A. and Alves 2003). Besides, the greater similarity of this taeniatus,Rio das Velhas H. nana, (LC-Isol) H sanctae (53%) and C.(Figure zebra), 4). a native Both predatorsystems share(H. malabaricus originally five small sized R.characins quelen and ( T. galeatus) drainagefact that thisunderground. karstic system In fact, is naturallyany migratory isolated, species since were the and G. carapo recordedwhole system in this flows study. to the Sumidouro Cave, continuing his occurrence in the), two Lagoa catfishes Central ( (L. reinhardti, P. costatus and P. maculatus. However,), which migratory were lost speciesdue to interruptionwith historical of Samambaia stream are in an environmental protection communication with Rio das Velhas, were not found in the areaDespite (APA – theÁrea fact, de Proteção that the Ambiental), Sumidouro both lagoon suffer and with the

Sumidouro system. Only 35% of the similarity was founded problems related to urbanization such as the non-native thebetween Lagoa the Central. studied system with the current fauna (LC- species presence. The species introduction is one of the Curr) and after introduction of exotic species (LC-Exot) of Invasivemain problems species forgenerally freshwater reduce fish native conservation inland (Cowxwater Discussion 2002; Cambray 2003; Collares-Pereira and Cowx 2004). parasitism or competition (Canonico et al. 2005). Even beforespecies the abundance creation of throughthe Parque predation, Estadual do hybridization, Sumidouro, The greatest richness found in the region is represented Characiformesby the order is Characiformes, one of the largest a pattern groups widely of freshwater known for (Lowe-Mcconnell 1987). The order waterthe lake contamination was indiscriminately (Pereira used and byCaldeira predatory 2011) and et al. and urbanization of the margins facing, as a consequence, fishes,Siluriformes with species was more found frequent both in lenticthe studied and lotic stream systems than region, which are still constant, have contributed to the (Buckupin the lagoon. Species 2000; Nelsonof this order 2006). may However, present the small order or colonization by exotic species. Anthropic actions in the

deterioration of water, vegetation and relief (IEF- MG 1981).large size Among and arethe foundadded mainlyspecies, in only fast flowingtwo were habitats, found 2010). The comparison between the two systems made inriver the bottomslagoon, and and the among other rocks seven and were vegetation found in (Britskistream, in this study allows one to infer that the intensification of withurbanization the Lagoa around Central, the especially Sumidouro if new system exotic may species cause theare small water courses (Casarim et al. 2012). introduced.significant loss of richness of fish, as had already occurred indicating that most of the unknown fauna is found in

866 Casarim et al. | Ichthyofauna of Sumidouro system, Brazil

Table 1.

Fish species collected in Rio das Velhas basin, per sampled environment, Sumidouro Lagoon, Samambaia stream, Historical and Current Lagoa Santa Lagoon (CI-UFLA = number of species deposited in the Ichthyological Collection of UFLA, *Exotic species, ϴFishes with migratory behavior). Valid names according to Eigenmann (1918), Buckup (1992), Mago-Leccia (1994), Britski (2001), Godinho and Godinho (2003).LAGOA CENTRAL TAXON SUMIDOURO LAGOON SAMAMBAIA STREAM Current CHARACIFORMES Hist. Acestrorhynchidae Acestrorhynchus lacustris X Anostomidae (Lütken,1875) Leporinus reinhardti ϴ X Characidae Lütken,1875 Astyanax aff. eigenmanniorum Astyanax lacustres X X (Cope,1894) CI-UFLA 0730 Astyanax rivularis X (Lütken,1875) CI-UFLA 0719 CI-UFLA 0719 Astyanax taeniatus (Lütken,1875) CI-UFLA 0720 Hasemania nana X (Jenyns, 1842) CI-UFLA 0718 CI-UFLA 0718 Hyphessobrycon gracilis X (Lütken,1875) CI-UFLA 0717 CI-UFLA 0717 Hyphessobrycon santae (Eigenmann, 1907) X (Lütken,1875) Serrasalmus brandtii X CI-UFLA 0716 CI-UFLA 0716 Crenuchidae Lütken,1875 Characidium zebra Eigenmann, 1909 X Characidium lagosantensis X CI-UFLA 0722 Erythrinidae Travassos, 1947 Hoplias malabaricus X X Hoplias intermedius X (Bloch, 1794) CI-UFLA 0724 CI-UFLA 0724 CYPRINODONTIFORMES (Günther, 1864) CI-UFLA 0731 Poeciliidae Pamphorichthys hollandi X Poecilia reticulata Peters, 1859 (Henn, 1916) Prochilodontidae CI-UFLA 0727 Prochilodus costatus ϴ Valenciennes 1850 X Tetragonopterinae Serrapinnus heterodon (Eigenmann, 1915) X GYMNOTIFORMES Gymnotidae Gymnotus carapo Linnaeus, 1758 X PERCIFORMES CI-UFLA 0725 Cichlidae Cichla cf. monoculus* X Tilapia rendalli* X Agassiz, 1831 SILURIFORMES (Boulenger 1877) CI-UFLA 0721 CI-UFLA 0721 Auchenipteridae Trachelyopterus galeatus X Callichthyidae (Linnaeus,1766) CI-UFLA 0729 Hoplosternum littorale* X Heptapteridae (Hancock, 1828) CI-UFLA 0728 CI-UFLA 0728 Pimelodella lateristriga (Lichtenstein, 1823) Rhamdia quelen X X CI-UFLA 0726 Pimelododidae (Quoy and Gaimard, 1824) CI-UFLA 0723 Pimelodus maculatus ϴ X Sternopygidae Lacépède, 1803 Eigenmannia microstoma (Reinhardt, 1852) X X Total of species 9 17 10

14

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Figure 3.

Scheme of study points, Sumidouro Lagoon (A – E) and Samambaia stream (1-23), located in the Parque Estadual do Sumidouro, Minas Gerais, Brazil.

Figure 4.

Percentage of similarity of the historical (LC – Hist) and current fauna (LC – Curr), presence of exotic species (LC – Exot) and the scenario after isolation of the Lagoa Santa (LC – Isol) in relation to the fishes found in the Sumidouro system (Sumid.). Acknowledgments: Fishes 9: 117–135 (doi: ). Ecology of UFLA and Parque Estadual do Sumidouro for providing logistic support. We thank the Graduate program in Applied Atlas da fauna brasileira10.1007/BF00690857. : Melhoramentos. Britski, H.A. 1981. Peixes de água doce; pp.Manual 84-93, in:de identificaçãoJ.C.M. Carvalho. de We also thank Polyanne Aguiar for drawing the map. peixes da região de Três Marias: Com chaves de identificação para os Authors received financial support from CNPq (Conselho Nacional de Britski,peixes H.A., da Y.bacia Sato do and São A.B.S. Francisco Rosa. 1988. Desenvolvimento Científico e Tecnológico) and CAPES (Coordenação de Codevasf. 115 pp. LiteratureAperfeiçoamento Cited de Pessoal de Nível Superior). . Brasília: Câmara dos Deputados/ Ecologia e manejo de Peixes do recursos pesqueiros em reservatórios do Brasil. Britski,rio dasH.A. Velhas: 2001. PassadoSobre a eobra presente Velhas-Flodens Fiske [Peixes do rio das Agostinho,pp. A.A., L.C. Gomes and F.M. Pelicice. 2007. Velhas], pp. 15–22, in: C.B.M. Alves and P.S. Pompeu. (ed.). EDUEM: Maringá. 501 . Belo Horizonte:Copeia SEGRAC. land use on Stream Ecosystems. Annual Review of Ecology, Buckup,1073 P.A. (doi: 1992. Redescription of). Characidium fasciatum, type species Allan,Evolution, J. D. 2004.and SystematicsLandscapes and Riverscapes: The influence of of the Characidiinae (Teleostei, Characiformes). 2000. 1992: Waterfall 1066– ecolsys.35.120202.110122). climbing in10.2307/1446639 Characidium (Crenuchidae: Characidiinae) from eastern . 35: 257–84 (doi: 10.1146/annurev. Buckup, P.A.,Icththyological C. Zamprogno, Explorations F. Vieira and Freshwaters R.L. Teixeira. 11(3): 273–278 gradients in a system of tropical streams. Environmental Biology of ( Angermeier, P.L. and J.R. Karr. 1984. Fish communities along environmental Brazil. http://www.academia.edu/1831320/Waterfall_climbing_in_ 868 Casarim et al. | Ichthyofauna of Sumidouro system, Brazil

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