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Neotropical Biology and Conservation 3(2):73-77, may - august 2008 © by Unisinos

Ornamental exotic introduced into Atlantic Forest water bodies, Brazil

Peixes ornamentais exóticos introduzidos em corpos d’água na Mata Atlântica, Brasil

André Lincoln Barroso de Magalhães1,2 [email protected] Claudia Maria Jacobi3 [email protected]

Abstract

Specimens of Puntius arulius, P. ticto, P. titteya, P. oligolepis, Nannostomus beckfordi, Poecilia latipinna, P. velifera, Trichogaster pectoralis, and Betta splendens were recorded in the largest ornamental aquaculture center in Brazil. These were introduced in the study sites by accidental escape and intentional release. There is evidence that six are reproducing. Measures are proposed to prevent further spread of ornamental exotic fishes in the region.

Key words: Brazil, species introduction, exotic fishes, ornamental aquaculture.

Resumo

1 Centro Universitário UNA, 30455-590, Belo Exemplares de Puntius arulius, P. ticto, P. titteya, P. oligolepis, Nannostomus beckfordi, Horizonte, MG, Brazil. 2 Universidade Federal de , Poecilia latipinna, P. velifera, Trichogaster pectoralis e Betta splendens foram registrados Programa de Pós-Graduação em Ecologia, no maior centro de piscicultura ornamental do Brasil. Estes peixes alcançaram os locais Conservação e Manejo de Vida Silvestre, de estudo devido a fugas acidentais e liberação intencional. Há evidências de que seis 31250-970, , MG, Brazil. espécies estejam se reproduzindo. Medidas são propostas para se prevenir futuras intro- 3 Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal duções de peixes ornamentais exóticos na região. de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil. Palavras-chave: Brasil, fugas, peixes exóticos, piscicultura ornamental. André Lincoln Barroso de Magalhães, Claudia Maria Jacobi

Introduction Material and methods Specimens were captured with 0.5 cm-mesh sieves, killed by over- Among the twenty-seven Brazilian Fishes were collected monthly from anaesthetization with ether, fixed in a states, Minas Gerais is one of the January to December 2005 in four 10% formalin solution, and preserved in largest. It is slightly bigger than sites: (i) Santo Antônio creek (20o56’S 70% alcohol. Species identification was France, with an area of 585528 km2 and 42o17’W), Vieiras municipality, (ii) based on Nelson (1994) and Axelrod et (IBGE, 2002). It is drained by thirteen Pinheiros creek (20o51’S and 42o23’W), al. (1998). Fish pictures and descriptions different river basins, including two municipality, (iii) of colors on the websites Froese of the largest Brazilian basins, the São creek (20o57’S and 42o28’W), Muriaé and Pauly (2006), FishIndex (2006), Francisco basin and the High Paraná municipality, Glória river sub-basin, Badman’s Tropical Fish (2006), and basin, and contains more than 2000 and (iv) Maurício dam (21o23’S Aquatic Community (2006) were used small, medium, large and megadams and 42o41’W), to confirm the fish species identification. (Alves et al., 2007). The native municipality, Pinho river sub-basin In laboratory, all individuals were ichthyofauna in the state is estimated (Figure 1). All sites belong to the measured, adult females and males were in 354 species, which represents Paraíba do Sul basin (length: 1080 km, dissected and their gonads checked for approximately 12% of the total found drainage area: 55,400 km2), which is indications of reproductive activity. in Brazil (McAllister et al., 1997). one of South America´s largest river Fish were classified as rest, mature, The native fish fauna includes systems (Lundberg et al., 1998) and spawned for females and spermiated some of Brazil´s most endangered drains part of Brazil’s southeast region for males (in oviparous species) species such as Matrinchã Brycon including the States of São Paulo according to Magalhães and Ratton orbignyanus (Valenciennes), Andirá (drainage area: 13,500 km2), Minas (2005), and as gravid/non-gravid for Henochilus weatlandii, Garman, Gerais (drainage area: 20,900 km2), females of viviparous species according Armored catfish Pogonopoma and Rio de Janeiro (drainage area: to Milton and Arthington (1983). parahybae (Steindachner), Killifish 21,000 km2) (Pfeiffer et al., 1986). Voucher specimens used in this study Simpsonichthys zonatus (Costa and Brasil), Surubim Steindachneridion parahybae (Steindachner), Jaú Zungaro jahu (Ihering) (Fundação Biodiversitas, 2007). Furthermore, Minas Gerais ranks high in the list of states in number of fish introductions, with 69 detected exotic species already, more than 50 of which are ornamental (Alves et al., 2007; Magalhães, 2007a; Magalhães and Carvalho, 2007). The number of non-native species for the main river basins in the state is: 47 in Paraíba do Sul (Magalhães, 2007b; Magalhães and Carvalho, 2007), 30 in Doce, 20 in High Paraná, 16 in São Francisco, 12 in Mucuri, and 5 in (Alves et al., 2007). The high level of introductions in Paraíba do Sul is associated with an ornamental fish farming center, the largest in Brazil (Magalhães et al., 2002). The aims of this communication are: (i) to record the occurrence of exotic fishes in three creeks and in one dam of the Paraíba do Sul basin, (ii) to analyze evidence of reproduction and (iii) to propose guidelines to Figure 1. Map showing the four study sites in the state of Minas Gerais, Brazil: Pinheiros circumvent further introductions. creek (PI), Santo Antônio creek (SA), Pratinha creek (PR), and Maurício dam.

74 Volume 3 number 2 may - august 2008 Ornamental exotic fish introduced into Atlantic Forest water bodies, Brazil are deposited under their respective captured, totaling 583 specimens (Table P. oligolepis and N. beckfordi females catalogue numbers (Table 1) in the 1). The occurrence of alevins, juveniles and males showed reproductive activity. Museum of Science and Technology and adults of the Arulius Puntius The single male specimens of the Cherry (MCP), Pontifical Catholic University arulius (Jerdon), Ticto barb Puntius ticto barb Puntius titteya Deraniyagala and of Rio Grande do Sul, Brazil. (Hamilton), Checkered barb Puntius the Snakeskin gourami Trichogaster oligolepis (Bleeker), Golden pencilfish pectoralis (Regan), and the only female Results and Nannostomus beckfordi Günther, Sailfin caught of the Siamese fighting fishBetta discussion mollies Poecilia latipinna (Lesueur), splendens Regan were with the gonads and Poecilia velifera (Regan) was in rest. Most P. latipinna and P. velifera Nine exotic species belonging to four evidenced by the heterogeneity of the females were pregnant with developing families, native to four continents were standard length. Puntius arulius, P. ticto, embryos (Table 1).

Table 1. General data about the nine ornamental exotic fishes.

Standard Species * N Family * Native range * Site Gonads of adult specimens length (mm)

Oviparous Min. Max.

Ovaries: rest (26%), mature (56%), Puntius arulius Pinheiros spawned (18%) Arulius barb 37 India 35 72 creek Testes: rest (32%), mature (50%), MCP 39006 spermiated (18%) India, Thailand, Ovaries: rest (20%), mature (70%), Puntius ticto Nepal, Pakistan, Pinheiros spawned (10%) Ticto barb 14 Cyprinidae Sri-Lanka, 22 54 creek Testes: rest (25%), mature (50%), MCP 39005 Bangladesh, spermiated (25%) Myanmar Puntius titteya Pinheiros 1 Cyprinidae Sri Lanka 33 Rest testis (100%) creek MCP 38998 Puntius oligolepis Ovaries: mature (67%), Sumatra, Pinheiros Checkered barb 4 Cyprinidae 10 46 spawned (33%) Indonesia creek MCP 38999 Mature testes (100%)

Nannostomus Ovaries: rest (22%), mature (67%), beckfordi Guyana, Maurício spawned (11%) 167 Lebiasinidae 21 45 Golden pencilfish N Brazil dam Testes: rest (32%), mature (39%), MCP 39000 spermiated (29%)

Trichogaster Cambodia, pectoralis Pinheiros 1 Osphronemidae Laos, Thailand, 128 Rest testis (100%) Snakeskin gourami creek Vietnam MCP 38996

Betta splendens Laos, Thailand, Pratinha Siamese fighting fish 1 Osphronemidae Cambodia, 40 Rest ovary (100%) creek MCP 39001 Malaysia

Viviparous

Poecilia latipinna Santo Sailfin molly 24 Poeciliidae U.S.A., Mexico Antônio 8 61 Gravid (61%), non-gravid (39%) MCP 39008 creek

Poecilia velifera Santo Sailfin molly 334 Poeciliidae Mexico Antônio 9 69 Gravid (52%), non-gravid (48%) MCP 39003 creek

* Scientific and common names; Family and Native range from Froese and Pauly (2006).

Neotropical Biology and Conservation 75 André Lincoln Barroso de Magalhães, Claudia Maria Jacobi

The region where these exotic screens in the effluent pipes to prevent the presence of non-native fish species. fishes were recorded comprises 12 escapes); (ii) heavy rains that often Therefore, records of exotic fish are municipalities and has around 250 flood fish farms, flushing fishes into necessary to create a database for producers who breed approximately non-managed waters; (iii) disposal of mitigatory purposes and the conservation 60 different ornamental species, such specimens of low commercial value of the native freshwater fauna. Also, as the GoldfishCarassius auratus (L.), (undersized individuals of P. latipinna, studies of diet and reproduction overlap Common Cyprinus carpio L., P. velifera and B. splendens) into and relative density of all species Common serpa tetra Hyphessobrycon nearby creeks; and (iv) intentional are needed to assess the negative eques (Steindachner), Guppy Poecilia release of commercially important impacts upon native fish species in the reticulata Peters, P. velifera, Green species so that their offspring be region, such as the Twospot astyanax swordtail Xiphophorus hellerii Heckel, collected for sale. Astyanax bimaculatus (L.), Yellow Southern platyfish X. maculatus The release of adult forms may have tetra Hyphessobrycon bifasciatus (Günther), Dwarf gourami Colisa benefited representatives of fish Ellis, Armored catfishes Hypostomus lalia (Hamilton), Freshwater angelfish families that display survival strategies affinis (Steindachner), Neoplecostomus Pterophyllum scalare (Schultze), and such as uni-parental care (Poeciliidae, microps (Steindachner), Parotocinclus Ram ramirezi Osphronemidae), school formation maculicauda (Steindachner), Catfishes (Myers and Harry), in more than 3000 (Lebiasinidae), and broad dietary habits Rhamdioglanis transfaciatus Miranda earthen and concrete ponds (Rasguido (Cyprinidae, Lebiasinidae, Poeciliidae, Ribeiro, Trichomycterus spp., Pearl and Albanez, 2000; Vidal Júnior and Osphronemidae), considered important cichlid Geophagus brasiliensis (Quoy Costa, 2000). Besides fish, there are strategies for the survival of teleost and Gaimard) (Magalhães, personal small-scale cultures of ornamental species introduced into new habitats observation), and the endangered , crustaceans, snails and frogs (Welcomme, 1988). The differences in endemic P. parahybae (Fundação (Magalhães, personal observation). standard length observed in P. arulius, Biodiversitas, 2007). For 40% of these producers, this P. ticto, P. oligolepis, N. beckfordi, The release of exotic organisms is a activity is the main source of income, P. latipinna and P. velifera, along federal offense according to Brazilian which makes this region the largest with the presence of mature/spawned legislation and ornamental aquaculture ornamental aquaculture center in South females, mature/spermiated males, in Brazil should be conducted strictly in America since the end of the 1970’s and pregnancy attest that they are accordance with specific regulations, (Vidal Júnior and Costa, 2000), and the reproducing in the wild. Reproductive control and effective inspections main source of , , fish evidence in females and males of the (Magalhães et al., 2002). Some and frog introductions in the continent exotic Sumatra barb Puntius tetrazona immediate remedial measures to (Magalhães et al., 2002; Magalhães, (Bleeker), C. carpio, Black tetra prevent further introductions from 2006, 2007b). Paradoxically, the region Gymnocorymbus ternetzi (Boulenger), farm ponds should be: (i) to reroute where these exotic fish are grown is Spotted metynnis Metynnis maculatus all effluent waters from fish rearing enclosed in an area of Atlantic Forest, (Kner), M. ramirezi, Flag acara facilities through an underground a hotspot classified by the Brazilian curviceps (Ahl), P. scalare, or above-ground dry well; (ii) to Ministry of Environment (2000) as a X. maculatus, and X. hellerii have install adequate sand and gravel priority for native fish conservation. already been recorded in the region filter which will allow passage of The present study raised the number of (Magalhães et al., 2002). Special water but not livestock; (iii) outdoor exotic fish species to 56 (51 of which attention should be given to P. latipinna fish ponds located on floodable land ornamental) for the basin, and to 78 and T. pectoralis, as they are considered should be diked; and (iv) to promote in the state of Minas Gerais (before pests in other countries (Froese and environmental awareness of those the present study: 47 for Paraíba do Pauly, 2006). The Sailfin molly directly involved with ornamental fish Sul basin, 69 for the state of Minas competes for food with the native farms. Otherwise, fish escapes out of Gerais). For comparison purposes, 72 Milkfish Chanos chanos (Forsskål) in most of the 3000 ponds will negatively exotic fish species had been detected the Philippines (Juliano et al., 1989), change the native diversity scenario in in Chinese inland waters (Ma et al., and the Snakeskin gourami competes the near future. 2003). In the study area, the presence for reproductive sites with the native of adult individuals in the dam and Three spot gourami Trichogaster Acknowledgements in the three creeks can be due to: trichopterus (Pallas) in Malaysia (Ang (i) accidental release during pond et al., 1989). The authors thank fisherman Jorge drainage, discharging water directly According to Hilsdorf and Petrere Clementino de Farias for field into adjacent water bodies (most of Jr. (2002), one of the main threats to assistance, Roberto Esser dos Reis the ponds do not have protective the Paraíba do Sul basin diversity is (Museum of Science and Technology,

76 Volume 3 number 2 may - august 2008 Ornamental exotic fish introduced into Atlantic Forest water bodies, Brazil

Pontifical Catholic University of Rio FUNDAÇÃO BIODIVERSITAS. 2007. Revi­ Stream, Paraíba do Sul river basin, state of Minas Grande do Sul) for the species catalogue são das Listas das Espécies da Flora e da Gerais, southeastern Brazil. Comunicações do number, Myrian M. Duarte for the Fauna Ameaçadas de Extinção do Estado de Museu de Ciências e Tecnologia, Série Zoologia, Minas Gerais. Belo Horizonte, relatório final, 15:265-278. drawing, the Graduate Program in 142 p. MAGALHÃES, A.L.B.; CARVALHO, P.A. Ecology, Conservation and Management HILSDORF, A.W.S.; PETRERE JR., M. 2002. 2007. Occurrence of exotic ornamental fish in of Wildlife (Federal University of Minas Conservação de peixes na bacia do rio Paraíba streams in the states of Minas Gerais and Rio Gerais) and the US Fish and Wildlife do Sul. Ciência Hoje, 30:62-65. de Janeiro, Brazil. Natureza & Conservação, Service for financial support. IBGE - INSTITUTO BRASILEIRO DE 5:124-129. GEOGRAFIA E ESTATÍSTICA. 2002. 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