BRIEF COMMUNICATIONS First record of Barbonymus schwanenfeldii (Bleeker) in the Iberian Peninsula

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Journal of Fish Biology (2008) 72, 1089 1094 doi:10.1111/j.1095-8649.2007.01773.x, available online at http://www.blackwell-synergy.com BRIEF COMMUNICATIONS First record of Barbonymus schwanenfeldii (Bleeker) in the Iberian Peninsula H. F. GANTE*, L. MOREIRA DA COSTA k, J. MICAEL* AND M. J. ALVES* *Centro de Biologia Ambiental and Museu Bocage Museu Nacional de História Natural, Rua da Escola Politecnica n 58, 1269-102 Lisboa, Portugal, School of Life Sciences, LSC 274, Arizona State University, Tempe, AZ85287-4601, U.S.A., Centro de Biologia Ambiental and Departamento de Biologia Ambiental, Faculdade de Ci^encias, Universidade de Lisboa, Campo Grande, C2, 1749-016 Lisboa, Portugal and ksouth African Institute for Aquatic Biodiversity (SAIAB), Somerset Street, Private Box 1015, 6140 Grahamstown, South Africa (Received 2 November 2006, Accepted 14 November 2007) The South-east Asian cyprinid Barbonymus schwanenfeldii is recorded for the first time in the Iberian Peninsula from two specimens collected in the Guadiana River Basin in 2005. Their presence is probably due to release from aquaria. Key words: Cyprinidae; introduced species; Portugal; tinfoil barb. Journal compilation # 2008 The Fisheries Society of the British Isles The freshwater ichthyofauna of the Iberian Peninsula is extremely rich in smallto medium-sized endemic species. While new species are still being formally described, native species face a growing threat from habitat destruction and introduction of alien species (Elvira & Almodo var, 2001). At least two-thirds of the freshwater and migratory fish species in Portugal and Spain are threatened (Doadrio, 2001; Cabral et al., 2005). In the present paper the first observation of tinfoil barb Barbonymus schwanenfeldii (Bleeker, 1853) is reported in Iberia from Portuguese inland waters. During 2005, Iberia experienced severe drought conditions which led to diminishing water levels in rivers and reservoirs. To reduce fish density in the Lucefecit Reservoir, Lucefecit River (Guadiana River basin, southern Iberia, 38 389050 N; 7 249300 W), c. 5000 kg of fishes were collected in August by professional fishermen using gillnets (CS2005, 2005). Species captured included the native Barbus comizo Steindachner, 1864 (sensu Doadrio, 1988), Barbus sclateri Author to whom correspondence should be addressed. Tel.: þ351 213921886; fax: þ351 213969784; email: hfgante@fc.ul.pt 1089 Journal compilation # 2008 The Fisheries Society of the British Isles

1090 H. F. GANTE ET AL. Günther, 1868 and Chondrostoma willkommii Steindachner, 1866 and the exotic Cyprinus carpio L., 1758, Lepomis gibbosus (L., 1758), Micropterus salmoides (Lacepède, 1802) and Sander lucioperca (L., 1758). Additionally, two specimens of an unreported exotic species (1399 and 1659 mm in standard length L S ) were collected and deposited in the collection of the Museu Bocage, Lisbon, Portugal (MB05-2193). Both specimens are males and show undeveloped gonads. These specimens were identified as B. schwanenfeldii (Fig. 1), following a combination of meristic criteria given by Bleeker (1853), Gunther (1868) and Kottelat (2001) (Table I), as well as the body shape and colouration patterns noted below. The two specimens have a whitish margin and a black submarginal stripe along the length of both caudal-fin lobes, which distinguish them from any other Barbonymus species, including the similar Barbonymus altus (Gunther, 1868) (Kottelat, 1998, 2001). Both specimens have a highly compressed, deep body [v. fusiform shape of Barbonymus collingwoodii (Gunther, 1868) (Kottelat et al., 1993)], and are greenish on the back and silvery on the ventral parts. The dorsal fin has a black blotch on the apex and all fins, except the pectorals, have an intense red colour [v. plain greyish to yellowish grey dorsal and caudal fins, and light orange anal and pelvic fins in Barbonymus gonionotus (Bleeker, 1850), although the tips of the anal and pelvic fins can sometimes be reddish in this species; Taki, 1974]. Additionally, both specimens have barbels longer than the eye diameter and snout shorter than the eye diameter, which are characteristic of B. schwanenfeldii (Bleeker, 1853; Gunther, 1868). Barbonymus schwanenfeldii is native to the Mekong and Chao Phraya basins (Cambodia, Laos, Thailand and Vietnam), the Malay Peninsula, Borneo and Sumatra (Kottelat, 2001). It is a schooling species growing up to 340 mm standard length (L S ) (Kottelat, 2001) with an omnivorous and detritivorous habit, feeding on aquatic and terrestrial macrophytes, filamentous algae, small fishes and occasionally insects (Siaw-Yang, 1988; Rainboth, 1996). It is a highly fecund species with females producing 7900 16 000 eggs for fish weighing 220 382 g (Christensen, 1992) and a spawning frequency of three times per year in a regulated river (McAdam et al., 1999). In its natural range, adult specimens (>240 mm L S ) undertake upriver spawning migrations during the rainy season; larvae (<25 mm L S ) and juveniles (25 70 mm L S ) congregate in flooded forest and grassland, and lakes, respectively (Christensen, 1992). FIG. 1. Barbonymus schwanenfeldii (MB 05-2193), male, 1659 mm standard length, (L S ) Portugal, Lucefecit Reservoir, Lucefecit River, Guadiana River basin. Recently preserved specimen. Scale bar ¼ 10 mm.

TINFOIL BARB IN IBERIA 1091 TABLE I. Meristic characters of two Barbonymus schwanenfeldii specimens collected in Lucefecit Reservoir, Portugal and congeneric species [B. altus, B. collingwoodii and B. gonionotus in G unther (1868)]. Range values given in the original description of B. schwanenfeldii (Bleeker, 1853) and subsequent references shown for comparison. Discrepancy between Bleeker s (1853) and the other authors transverse series scale counts probably reflects methodological differences, as Günther (1868) examined Bleeker s (1853) original material B. schwanenfeldii Present study Bleeker (1853) G unther (1868) Kottelat (2001) B. altus B. collingwoodii B. gonionotus Lateral line scales 36 35 36 35 36 32 30 32 29 30 75/4 14 15 75 8/4 75/ 8/7 6/45 6/5 Transverse series scales Dorsal-fin rays IV/9 IV/8 9 11 11 11 11 Pectoral-fin rays I/14 I/14 Pelvic-fin rays I/8 I/8 Anal-fin rays III/6 III/5 6 8 7 8 9 Caudal-fin rays 18 19 19, No data.

1092 H. F. GANTE ET AL. For many years, the aquarium fish trade has been utilizing numerous wild species from South-east Asia (Ng & Tan, 1997), where >2100 species are recognized (Lundberg et al., 2000). Barbonymus schwanenfeldii is commercially important in the aquarium hobby trade, as well as for commercial aquaculture, subsistence farming, and is occasionally used as bait (Lambert, 1997). Recorded introductions of B. schwanenfeldii include the south-east of the U.S.A. (Benson et al., 2001) and the Philippines (ASAP, 1996), both associated with the ornamental fish trade, and the Ivory Coast, linked to aquacultural practises (Welcomme, 1988). In the northern Mediterranean region it was introduced in Italy, where it nonetheless failed to establish (Holc ı k, 1991). This species is sometimes seen in the ornamental fish trade in Portugal, and release of outgrown specimens seems to be the most probable source of the fish in the present study. This is consistent with the propagule pressure hypothesis, which predicts that introduced and established specimens have greater lengths than those typically found in the aquarium trade (Duggan et al., 2006). Although direct evidence about the species establishment and successful reproduction in the Guadiana River basin is lacking (both specimens were immature males), both events seem possible as the specimens were found in favourable habitats. The Lucefecit River drains to the Alqueva Reservoir, the largest artificial lake in Europe, which should be a more thermally stable environment than nearby streams. Additionally, inflowing rivers could provide breeding areas for adults and the seasonally flooded marginal areas of the reservoir could provide feeding grounds for the young. Should this generalist species become established, the potential impacts on the native fauna and flora are obvious both in terms of competition for resources and predation. An additional and often overlooked impact would be the potential introduction of new diseases and parasites, against which the natives might have no resistance to (Holc ı k, 1991; Salgado-Maldonado & Pineda-Lo pez, 2003; Gozlan, et al., 2005). For instance, Bassleer (1997) and Bu & Seng (1997) reported the protozoan Ichthyophthirius sp. and several nematode species parasitizing B. schwanenfeldii. Parasites might need only the occasional introduction rather than the successful establishment of the host species (B. schwanenfeldii in this case) to infect native species and complete their life cycle. Careful attention should be given to new introductions, as human-mediated habitat modifications potentially open new corridors for alien species to become successfully established, and hence threaten the native species (Moyle & Light, 1996). The authors are grateful to A. C. Gill (ASU) for his suggestions on the early version of the manuscript, to I. Harrison and to three anonymous reviewers for comments that improved the manuscript s quality. The authors also thank D. Catita (EDIA) for permission to keep representatives of the species collected during the fish collection in the Lucefecit Reservoir. References ASAP (1996). Aquarium Species in the Philippines. Quezon City: Aquarium Science Association of the Philippines. Bassleer, G. (1997). Color Guide of Tropical Fish Diseases: on Freshwater Fish. Westmeerbeek: Bassleer Biofish.

TINFOIL BARB IN IBERIA 1093 Benson, A. J., Fuller, P. L. & Jacono, C. C. (2001). Summary Report of Nonindigenous Aquatic Species in U.S. Fish and Wild Service Region 4. Arlington, VA: US Fish and Wild Service. Bleeker, P. (1853). Nieuwe tientallen diagnostische beschrijvingen van nieuwe of weinig bekende vischsoorten van Sumatra. Natuurkundig Tijdschrift voor Nederlandsch Indië 5, 495 534. Bu, S. S. H. & Seng, L. T. (1997). Fish parasite communities in tropical reservoirs along the Perak River, Malaysia. Hydrobiologia 356, 175 181. doi: 10.1023/ A:1003158700538 Cabral, M. J., Almeida, J., Almeida, P. R., Dellinger, T., Ferrand de Almeida, N., Oliveira, M. E., Palmeirim, J. M., Queiroz, A. I., Rogado, L. & Santos-Reis, M. (Eds) (2005). Livro Vermelho dos Vertebrados de Portugal. Lisboa: Instituto de Conservacx ao da Natureza. Christensen, M. S. (1992). Investigations on the ecology and fish fauna of the Mahakam River in east Kalimantan (Borneo), Indonesia. Internationale Revue der Gesamten Hydrobiologie 77, 593 608. Doadrio, I. (1988). Sobre la taxonomia de Barbus comiza Steindachner, 1865 (Ostariophysi: Cyprinidae). Doñana, Acta Vertebrata 15, 19 28. Doadrio, I. (Ed.) (2001). Atlas y Libro Rojo de los Peces Continentales de España. Madrid: Direccio n General de la Natureza Museo Nacional de Ci^encias Naturales. Duggan, I. C., Rixon, C. A. M. & MacIsaac, H. J. (2006). Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biological Invasions 8, 377 382. doi: 10.1007/s10530-004-2310-2 Elvira, B. & Almodo var, A. (2001). Freshwater fish introductions in Spain: facts and figures at the beginning of the 21st century. Journal of Fish Biology 59 (Suppl. A), 323 331. doi: 10.1111/j.1095-8649.2001.tb01393.x Gozlan, R. E., St-Hilaire, S., Feist, S. W., Martin, P. & Kent, M. L. (2005). Disease threat to European fish. Nature 435, 1046. Günther, A. (1868). Catalogue of the Physostomi, Containing the Families Heteropygii, Cyprinidae, Gonorhynchidae, Hyodontidae, Osteoglossidae, Clupeidae, Chirocentridae, Alepocephalidae, Notopteridae, Halosauridae, in the Collection of the British Museum. London: The British Museum. Holc ík, J. (1991). Fish introductions in Europe with particular reference to its central and eastern part. Canadian Journal of Fisheries and Aquatic Sciences 48 (Suppl. 1), 13 23. Kottelat, M. (1998). Fishes of the Nam Theun and Xe Bangfai basins, Laos, with diagnoses of twenty-two new species (Teleostei: Cyprinidae, Balitoridae, Cobitidae, Coiidae and Odontobutidae). Ichthyological Exploration of Freshwaters 9, 1 128. Kottelat, M. (2001). Fishes of Laos. Colombo: WHT Publications (Pte). Kottelat, M., Whitten, A. J., Kartikasari, S. N. & Wirjoatmodjo, S. (1993). Freshwater Fishes of Western Indonesia and Sulawesi. Hong Kong: Periplus Editions. Lambert, D. J. (1997). Freshwater Aquarium Fish. Edison, NJ: Chartwell Books. Lundberg, J. G., Kottelat, M., Smith, G. R., Stiassny, M. L. J. & Gill, A. C. (2000). So many fishes, so little time: an overview of recent ichthyological discoveries in continental waters. Annals of Missouri Botanical Garden 87, 26 62. McAdam, D. S. O., Liley, N. R. & Tan, E. S. P. (1999). Comparison of reproductive indicators and analysis of the reproductive seasonality of the tinfoil barb, Puntius schwanenfeldii, in the Perak River, Malaysia. Environmental Biology of Fishes 55, 369 380. doi: 10.1023/A:1007563914300 Moyle, P. B. & Light, T. (1996). Biological invasions of fresh water: empirical rules and assembly theory. Biological Conservation 78, 149 162. doi: 10.1016/0006-3207(96)00024-9 Ng, P. K. L. & Tan, H. H. (1997). Freshwater fishes of Southeast Asia: potential for the aquarium fish trade and conservation issues. Aquarium Sciences and Conservation 1, 79 90. doi: 10.1023/A:1018335617835 Rainboth, W. J. (1996). Fishes of the Cambodian Mekong. Rome: FAO.

1094 H. F. GANTE ET AL. Salgado-Maldonado, G. & Pineda-Lo pez, R. F. (2003). The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions 5, 261 268. doi: 10.1023/A:1026189331093 Siaw-Yang, Y. (1988). Food resource utilization partitioning of fifteen fish species at Bukit Merah Reservoir, Malaysia. Hydrobiologia 157, 143 160. Taki, Y. (1974). Fishes of the Lao Mekong Basin. Vientiane: United States Agency for International Development Mission to Laos Agriculture Division. Welcomme, R. L. (1988). International introductions of inland aquatic species. FAO Fisheries Technical Paper No. 294. Electronic Reference CS2005 (2005). Relatório quinzenal (15 de Agosto). Lisboa: Comissão para a Seca 2005. Available from http://www.inag.pt/inag2004/port/divulga/actualidades/seca/ relatorios/relatorio15agosto.pdf (downloaded 22 March, 2007).