Intra-regional transportation of a tugboat fouling community between the ports of recife and natal, northeast Brazil

Abstracts

This study aimed to identify the incrusting and sedentary animals associated with the hull of a tugboat active in the ports of Pernambuco and later loaned to the port of Natal, Rio Grande do Norte. Thus, areas with dense biofouling were scraped and the species then classified in terms of their bioinvasive status for the Brazilian coast. Six were native to Brazil, two were cryptogenic and 16 nonindigenous; nine of the latter were classified as established (Musculus lateralis, Sphenia fragilis, Balanus trigonus, Biflustra savartii, Botrylloides nigrum, Didemnum psammatodes, Herdmania pallida, Microscosmus exasperatus, and Symplegma rubra) and three as invasive (Mytilopsis leucophaeta, Amphibalanus reticulatus, and Striatobalanus amaryllis). The presence of M. leucophaeata, Amphibalanus eburneus and A. reticulatus on the boat's hull propitiated their introduction onto the Natal coast. The occurrence of a great number of tunicate species in Natal reflected the port area's benthic diversity and facilitated the inclusion of two bivalves - Musculus lateralis and Sphenia fragilis - found in their siphons and in the interstices between colonies or individuals, respectively. The results show the role of biofouling on boat hulls in the introduction of nonindigenous species and that the port of Recife acts as a source of some species.

Bioinvasion; vessels hulls; fouling community; harbor area; Nonindigenous species


Este trabalho objetivou identificar os animais incrustantes e sedentários associados ao casco de um rebocador que atuava nos Portos de Pernambuco e foi cedido para o Porto de Natal, Rio Grande do Norte. Áreas com densa bioincrustação foram raspadas e as espécies foram posteriormente classificadas em relação ao status de bioinvasão no litoral brasileiro. Dentre as espécies identificadas, seis eram nativas do Brasil, duas criptogênicas e 16 exóticas. Destas, oito foram classificadas como estabelecidas (Musculus lateralis, Sphenia fragilis, Balanus trigonus, Biflustra savartii, Botrylloides nigrum, Didemnum psammatodes, Herdmania pallida, Microscosmus exasperatus, Symplegma rubra) e três como invasoras (Mytilopsis leucophaeta, Amphibalanus reticulatus e Striatobalanus amaryllis). A presença de M. leucophaeata, Amphibalanus eburneus e A. reticulatus no casco da embarcação, propiciou sua introdução na costa de Natal. A ocorrência de grande número de espécies de tunicados em Natal refletiu a biodiversidade bêntica da área portuária e facilitou a inclusão de dois bivalves, Musculus lateralis e Sphenia fragilis, encontrados em seus sifões e nos interstícios entre colônias ou indivíduos, respectivamente. Os dados obtidos indicam que a incrustação em cascos de embarcações tem um papel preponderante na introdução de espécies exóticas, e que o Porto do Recife atuou como fonte de algumas destas espécies.

Bioinvasão; casco de embarcação; comunidade incrustante; área portuária; espécie exótica


  • ABBOTT, R. T. American Seashells 2nd ed. New York: Van Nostrand Reinhold Co., 1974. 663 p.
  • ALLEN, F. E. Distribution of marine invertebrates by ships. Aust. J. Mar. Freshw. Res, v. 4, p. 307-316, 1953.
  • APTE S.; HOLLAND, B. S.; GODWIN, L. S.; GARDNER, P. A. Jumping ship: A stepping stone event mediating transfer of a nonindigenous species via a potentially unsuitable environment. Biol. Invasions, v. 2, p. 75-79, 2000.
  • BARREIRA, C. A. R.; HIJO, C. A. G.; FERNANDES, D. A. O.; SILVA, H. L.; VIDAL, J. M. A.; RODRIGUES, L.; VIANA, M. G.; JÂNICO, P. R. P. Macroinfauna bentônica de ambientes inconsolidados do estado do Ceará (faixa entre-marés de praias arenosas) Fortaleza: Universidade Federal do Ceará, 2005. 144 p.
  • BEASLEY, C. R.; FERNANDES, C. M.; GOMES, C. P.; BRITO, B. A.; SANTOS, S. M. L.; TAGLIARO, C. H. Molluscan diversity and abundance among coastal habitats of Northern Brazil. Ecotropica, v. 11, p. 9-20, 2005.
  • BERTRAND, G. A. The ecology of the nest-building bivalve Musculus lateralis commensal with the ascidian Molgula occidentalis Veliger, v. 14, p. 23-29, 1971.
  • BISHOP, M. W. H. Establishment of an immigrant barnacle in British costal waters. Nature, v. 159, p. 501, 1947.
  • BISHOP, M. W. H. Distribution of barnacles by ships. Nature, v. 167, p. 531, 1951.
  • CANGUSSU, L. C.; KREMER, L. P.; ROCHA, R. M.; PITOMBO, F. B.; HEYSE, H.; BORNANCIN, E. C. Cracas (Cirripedia, Balanomorpha) introduzidas em um cultivo de mexilhões: Composição de espécies e potencial invasor. In: VIICEB - CONGRESSO DE ECOLOGIA DO BRASIL, 2007, Caxambu. Resumos.. São Paulo: Sociedade de Ecologia do Brasil, 2007. 2 p.
  • CARDIGOS, F.; TEMPERA, F.; ÁVILA, S.; GONÇALVES, J.; COLAÇO, A.; SANTOS, R.S. Non-indigenous marine species of the Azores. Helgol. Mar. Res, v. 60, p. 160-169, 2006.
  • CARLTON, J. T. Transoceanic and intraoceanic dispersal of coastal marine organisms: The biology of ballast water. Oceanogr. Mar. Biol. Annu. Rev, v. 23, p. 313-374, 1985.
  • CARLTON, J. T. Patterns, process, and prediction in marine invasion ecology. Biol. Conserv, v. 78, p. 97-106, 1996.
  • CARLTON, J. T.; GELLER, J.B. Ecological roulette: the global transport of nonindigenous marine organisms. Science, v. 261, p. 78-82, 1993.
  • CARLTON, J. T.; HODDER, J. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th Century sailing vessel. Mar. Biol, v. 121, p. 721-730, 1995.
  • CASTAGNA, M.; CHANLEY, P. Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the Western mid-Atlantic coast. Malacogia, v. 12, n. 1, p. 47-96, 1973.
  • CASTILLA, J. C.; URIBE, M.; BAHAMONDE, N.; CLARKE, M.; DESQUEYROUX-FAÚNDEZ, R.; KONG, I.; MOYANO, H.; ROZBACZYLO, N.; SANTELICES, B.; VALDOVINOS, C.; ZAVALA, P. Down under the southeastern Pacific: Marine non-indigenous species in Chile. Biol. Invasions, v. 7, p. 213-232, 2005.
  • CASTRO, C. B. (Rel.) Projeto Abrolhos: Desenvolvimento de um plano de ação para a conservação dos recursos marinhos do complexo de Abrolhos. Aspectos ambientais Salvador: Conservation International do Brasil, 1997. 104p.
  • CHAMP, M. A. A review of organotin regulatory strategies, pending actions, related costs and benefits. Sci. Total Environ, v. 258, n. 1-2, p. 21-71, 2000.
  • CLARKE, C.; HILLIARD, R.; JUNQUEIRA, A. O. R.; LEAL NETO, A. C.; POLGLAZE, J.; RAAYMAKERS, S. Ballast water risk assessment, Port of Sepetiba, Federal Republic of Brazil, December 2003: Final Report London: GloBallast Monograph Series No.14- IMO, 2004. 131 p. Available from: http://globallast.imo.org [cited 2008 May 13]
  • COHEN, A. N.; CARLTON, J. T. Biological study Nonindigenous aquatic species in a United States estuary: A case study of the biological invasions of the San Francisco Bay and Delta Washington: National Sea Grant Program, 1995. 79 p.
  • COHEN, A. N. An exotic species detection program for Tillamook Bay Garibaldi: Tillamook Estuaries Partnership, 2004. 62 p.
  • COUTTS, A. D. M.; TAYLOR, M. D.; HEWITT, C. L. Novel method for assessing the en route survivorship of biofouling organisms on various vessel types. Mar. Pollut. Bull, v. 54, n. 1, p. 97-100, 2007.
  • DARWIN, C. R. A monograph on the sub-class Cirripedia with figures of all the species. The Balanidae (or Sessile Cirripedes); the Verrucidae, etc London: The Ray Society of London, 1854. 684 p.
  • DAVID, M.; GOLLASCH, S.; CABRINI, M.; PERKOVIC, M.; BOSNJAK, D.; VIRGILIO, D. Results from the first ballast water sampling study in the Mediterranean Sea – the Port of Koper study. Mar. Pollut. Bull, v. 54, p. 53-65, 2007.
  • DAVIDSON, I.; McCANN, L. D.; FOFONOFF, P. W.; SYTSMA, M. D.; RUIZ, G. M. The potential for hull-mediated species transfers by obsolete ships on their final voyages. Diversity Distrib, v. 14, n. 3, p. 518-529, 2008a.
  • DAVIDSON, I. C.; McCANN, L. D.; SYSTMA, M. D.; RUIZ, G. M. Interrupting a multi-species bioinvasion vector: The efficacy of in-water cleaning for removing biofouling on obsolete vessels. Mar. Pollut. Bull, v. 56, p. 1538-1544, 2008b.
  • DePAULA, A. F.; CREED, J. C. Two species of tube coral Tubastraea (Cnidaria, Scleractinia) in Brazil: a case of accidental introduction. Bull. Mar. Sci, v. 74, n. 1, p. 175-183, 2004.
  • ESCOT, C.; BASANTA, A.; COBO, F.; GONZÁLEZ, M.A.A. Sobre la presencia de Mytilopsis leucophaeta (Conrad, 1831) (Bivalvia, Dreissenacea, Dreissenidae) en el río Guadalquivir (sur de la Península Ibérica). Graellsia, v. 59, n. 1, p. 91-94, 2003.
  • FARRAPEIRA, C. M. R. Barnacles (Cirripedia Balanomorpha) of the estuarine region of Recife, Pernambuco, Brazil. Trop. Oceanogr., v. 34, n. 2, p. 100-119, 2006.
  • FARRAPEIRA, C. M. R. Barnacles (Crustacea: Cirripedia) of the estuarine and marine areas of the Port of Recife (Pernambuco-Brazil): a monitoring study for bioinvasion. Cah. Biol. Mar., v. 50, n. 1, p. 119-129, 2009.
  • FARRAPEIRA, C. M. R. Cirripedia Balanomorpha en el estuario del río Paripe (Isla de Itamaracá-Pernambuco-Brasil). Biota Neotrop, v. 8, n. 3, p. 31-39, 2008.
  • FARRAPEIRA, C.M.R.; MELO, A.V.O.M.; BARBOSA, D.F.; SILVA, K.M.E. Ship hull fouling in the Port of Recife, Pernambuco. Braz. J. Oceanogr, v. 55, n. 3, p. 207-221, 2007.
  • FARRAPEIRA, C. M. R.; MELO, A. V. O. M.; TENÓRIO, D. O. Comunidade bentônica de lagunas costeiras impactadas de Recife e Olinda, Pernambuco- possível grupamento biológico bioindicador de poluição orgânica. Arq. Ciênc. Mar, v. 42, n.1, p. 28-38, 2009a.
  • FARRAPEIRA, C. M. R.; RAMOS, C. A. C.; BARBOSA, D. F.; MELO, A. V. O. M.; PINTO, S. L.; VERÇOSA, M. M.; OLIVEIRA, D. A. S.; FRANCISCO, J. A. Zonación vertical de la macrofauna de sustratos sólidos del estuario del Río Massangana, Bahía de Suape – Pernambuco, Brasil. Biota Neotrop, v. 9, n. 1, p. 1-14, 2009b.
  • FARRAPEIRA-ASSUNÇÃO, C. M. Estudo comparativo da macrofauna bentônica de substratos duros em estuários não impactados (Rio Paripe-Itamaracá) e impactados (Rio Capibaribe e Bacia do Pina)- Pernambuco In: ENCONTRO NACIONAL DE ESTUDOS SOBRE O MEIO AMBIENTE, 3, Londrina, 1991. Anais.. Londrina: Universidade Estadual de Londrina, 1991, v. 2, pp. 80-95.
  • FARRAPEIRA-ASSUNÇÃO, C. M. Ocorrência de Chirona (Striatobalanus) amaryllis Darwin, 1854 e de Balanus reticulatus Utinomi, 1967 (Cirripedia, Balanomorpha) no Estado de Pernambuco. In: CONGRESSO BRASILEIRO DE ZOOLOGIA, 17, Londrina, 1990. Resumos.. Londrina: Sociedade Brasileira de Zoologia, 1990. p. 7.
  • FERREIRA, C. E. L.; GONÇALVES, J. E. A.; COUTINHO, R. Ship hulls and oil platforms as potential vectors to marine exotic introduction. J. Coast. Res, v. 39, p. 1340-1345, 2006. (ICS 2004 - Proceedings).
  • FOFONOFF, P.F.; RUIZ, G.G.; STEVES, B.; CARLTON, J. In ships or on ships? Mechanisms of transfer and invasion for nonnative species to the coasts of North America. In: RUIZ, G.M.; CARLTON, J.T. (Eds.) Invasive species: vectors and management strategies Washington: Island Press, 2003. pp. 152-181.
  • FOSTER, B. A.; WILLAN, R. C. Foreign barnacles transported to New Zealand on an oil platform. New Zealand J. Mar. Freshw. Res, v. 13, n. 1, p. 143-150, 1979.
  • FRAZIER, J. G.; MARGARITOULIS, D.; MULDOON, K.; POTTER, C. W.; ROSEWATER, J.; RUCKDESCHEL, C.; SALAS, S. Epizoan communities on marine turtles. I. Bivalve and gastropod mollusks. Mar. Ecol, v. 6, n. 2, p. 127-140, 1985.
  • FREITAS, G. M. R.; LOPES, D. M.; SILVA, K. M. R. G.; SOUZA, J.R.B. Distribuição e abundância do bivalve exótico Mytilopsis leucophaeta (Conrad, 1831) após 4 anos de sua introdução no estuário do Rio Capibaribe - Pernambuco. In: CONGRESSO BRASILEIRO SOBRE BIOINVASÃO, 1, 2009, São Luís, 2009. Anais.. São Luís: Mutual / Instituto Hórus, 2009. pp. 1-4.
  • GAMA, P. B.; LEONEL, R. M. V.; HERNANDEZ, M. I. M.; MOTHES, B. Recruitment and colonization of colonial ascidians (Tunicata: Ascidiacea) on intertidal rocks in Northeastern Brazil. Iheringia, Sér. Zool., v. 96, n. 2, p. 165-172, 2006.
  • GARCÍA-CUBAS, A. Moluscos de un sistema lagunas tropical en el Sur del Golfo de Mexico (Laguna de Términos, Campeche). Publ. Esp. Inst. Cienc. Mar y Limnol, v. 5, n. 458, p. 1-316, 1981.
  • GODWIN, L. S. Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling, v. 19 (Suppl.), p. 123-131, 2003.
  • GODWIN, L. S.; ELDREDGE, L. G.; GAUT, K. The assessment of hull fouling as a mechanism for the introduction and dispersal of marine alien species in the main Hawaiian Islands. Bishop Mus. Tech. Rep., n. 28, p. 1-122. 2004.
  • GOLLASCH, S. The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling, v. 18, p. 105-121, 2002.
  • GOLLASCH, S.; NEHRING, S. National checklist for aquatic alien species in Germany. Aquat. Invasions, v. 1, n. 4, p. 245-269, 2006.
  • GOMES, R. S.; COSTA, P. M. S.; MONTEIRO, J. C.; COELHO, A. C. S.; SALGADO, N. C. Moluscos das ilhas oceânicas brasileiras. In: ALVES, R. J. V.; CASTRO, J. W. A. (Orgs.) Ilhas oceânicas brasileiras: Da pesquisa ao manejo Brasília: Ministério do Meio Ambiente, 2006. p. 179-198.
  • GOODBODY, I. The ascidian fauna of Jamaica lagoon: Thirty years of change. Rev. Biol. Trop, v. 41, n. 1, p. 35-38, 1993.
  • GOULLETQUER, P.; BACHELET, G.; SAURIAU, P. G.; NOEL, P. Open Atlantic coast of Europe - a century of introduced species into French waters. In: LEPPAKOSKI, E.; GOLLASCH, S.; OLENIN, S. Invasive aquatic species of Europe: Distribution, impacts and management Dordrecht: Kluwer Academic Publishers, 2002. pp.276-290.
  • GROSHOLZ, E. D.; RUIZ, G. M. Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas Biol. Conserv, v. 78, p. 59-66, 1996.
  • HEWITT, C. L.; GOLLASCH, S.; MINCHIN, D. The vessel as a vector - biofouling, ballast water and sediments. In: RILOV, G.; CROOKS, J. A. (eds.). Biological invasions in marine ecosystems Ecological Studies 204. Berlin: Springer-Verlag, 2009. pp. 117-131.
  • IGNACIO, B. L., ABSHER, T. M.; LAZOSKI, C.; SOLÉ-CAVA, A. M. Genetic evidence of the presence of two species of Crassostrea (Bivalvia: Ostreidae) on the coast of Brazil. Mar. Biol, v. 136, p. 987-991, 2000.
  • IWASAKI, K. Human-mediated introduction of marine organisms in Japan: a review. In: KOIKE, F.; CLOUT, M.N.; KAWAMICHI, M., De POORTER, M.; IWATSUKI, K. (eds). Assessment and control of biological invasion risks Kyoto: Shoukadoh Book Sellers, 2006. pp. 104-112.
  • KOTT, P. The genus Herdmania Lahille, 1888 (Tunicata, Ascidiacea) in Australian waters. Zool. J. Linn. Soc, v. 134, n. 3, p. 359-374, 2002.
  • LAMBERT, C. C.; LAMBERT, G. Non-indigenous ascidians in southern California harbors and marinas. Mar. Biol., v. 130, p. 675-688, 1998.
  • LAMBERT, C. C.; LAMBERT, G. Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar. Ecol. Progr. Ser, v. 259, p. 145-161, 2003.
  • LAMBERT, G. Ecology and natural history of the protochordates. Can. J. Zool, v. 83, p. 34-50, 2005.
  • LAMBERT, G. A global overview of ascidian introductions and their possible impact on the endemic fauna. In: SAWADA, H.; OKOSAWA, H.; LAMBERT, C. C. (eds.) The biology of ascidians. Tokyo: Springer Verlag, 2001. pp. 249-257.
  • LAPÈGUE, S.; BOUTET, I.; LEITÃO, A.; HEURTEBISE, S.; THIRIOT-QUIÉVREUX, C.; BOUDRY, P. Trans-Atlantic distribution of a mangrove oyster species revealed by 16s mtDNA and karyological analyses. Biol. Bull, v. 202, p. 232-242, 2002.
  • LEONEL, R. M. V.; SILVA, I. N. Estudo da sobrevivência e da capacidade de isolamento de Mytella guyanensis (Mollusca: Bivalvia) em diferentes salinidades. Rev. Nordest. Biol, v. 6, p. 35-41, 1988.
  • LOTUFO, T. M. C. Ascidiacea (Chordata: Tunicata) do litoral tropical brasileiro 2002. 184 f. Tese (Doutorado em Ciências- Zoologia) Universidade de São Paulo, São Paulo.
  • MARELLI, D. C., GRAY, S. Conchological redescriptions of Mytilopsis sallei and Mytilopsis leucophaeata of the brackish Western Atlantic (Bivalvia: Dreissenidae). Veliger, v. 25, p. 185-193, 1983.
  • MILLAR, R. H. Ascidians (Tunicata: Ascidiacea) from the northern and north-eastern Brazilian shelf. J. Nat. Hist, v. 11, n. 2, p. 169-223, 1977.
  • MINCHIN, D. A checklist of alien and cryptogenic aquatic species in Ireland. Aquat. Invasions, v. 2, n. 4, p. 341-366, 2007.
  • MINCHIN, D.; GOLLASCH, S. Fouling and ships' hulls: How changing circumstances and spawning events may result in the spread of exotic species. Biofouling, v. 19 (Suppl.), p. 111-122, 2003.
  • MINCHIN, D.; GOLLASCH, S.; COHEN, A. N.; HEWITT, C. L.; OLENIN, S. Characterizing vectors of marine invasion. In: RILOV, G.; COOKS, J. A. (eds.). Biological invasions in marine ecosystems Ecological Studies 204. Berlin: Springer-Verlag, 2009. pp. 109-116.
  • MONNIOT, C. Stolidobranch ascidians from the tropical western Indian Ocean. Zool. J. Linn. Soc., v. 135, n. 1, p. 65-120, 2002.
  • MONNIOT, C.; MONNIOT, F. Additions to the inventory of eastern tropical Atlantic ascidians; arrival of cosmopolitan species. Bull. Mar. Sci, v. 54, n. 1, p. 71-93, 1994.
  • NAIR, V. R.; SANKARANKUTTY, C. Chaetognaths of the Potengi estuary, Natal, Northeast Brazil. Atlântica, v. 10, n. 1, p. 5-20, 1988.
  • NEHRING, S. Four arguments why so many alien species settle into estuaries, with special reference to the German river Elbe. Helgol. Mar. Res, v. 60, p. 127-134, 2006.
  • NEVES, C. S.; ROCHA, R. M.; PITOMBO, F. B.; ROPER, J. J. Use of artificial substrata by introduced and cryptogenic marine species in Paranaguá Bay, southern Brazil. Biofouling, v. 23, n. 5, p. 319-30, 2007.
  • OKA A. Ueber eine merkwürdige Botryllus Art., Botryllus primigenus n. sp. Proceed. Imperial Acad., v. 4, p. 303-305, 1928.
  • OREN, U; BENAYAHU, Y. Didemnid ascidians: Rapid colonizers of artificial reefs in Eilat (Red Sea). Bull. Mar. Sci, v. 63, n. 1, p. 199-206, 1998.
  • OTANI, M.; OUMI, T.; UWAI, S.; HANYUDA, T.; PRABOWO, R. E.; YAMAGUCHI, T.; KAWAI, H. Occurrence and diversity of barnacles on international ships visiting Osaka Bay, Japan, and the risk of their introduction. Biofouling, v. 23, n. 3-4, p. 277-286, 2007.
  • REIMER, A. A. Succession of invertebrates in vacant test of Tetraclita stalactifera panamensis. Mar. Biol, v. 35, n. 3, p. 239-252, 1976.
  • REISE, K.; OLENIN, S.; THIELTGES, W. A. Are aliens threatening European aquatic coastal ecosystems? Helgol. Mar. Res, v. 60, p. 77-83, 2006.
  • RIOS, E. C. Seashells of Brazil 2nd ed. Rio Grande: Fundação Universidade do Rio Grande, 1994. 368 p.
  • ROCHA, R. M.; COSTA, L. V. G. Ascidians (Urochordata: Ascidiacea) from Arraial do Cabo, Rio de Janeiro, Brazil. Iheringia, Ser. Zool., v. 95, n. 1, p. 57-64, 2005.
  • ROCHA, R. M.; KREMER, L.P. Introduced ascidians in Paranaguá Bay, Paraná, southern Brazil. Rev. Bras. Zool., v. 22, n. 4, p. 1170-1184, 2005.
  • ROCHA, R. M.; KREMER, L. P.; BAPTISTA, M. S.; METRI, R. Bivalve cultures provide habitat for exotic tunicates in southern Brazil. Aquat. Invasions, v. 4, n. 1, p. 195-205, 2009.
  • ROCHA, R. M.; MORENO, T. R.; METRI, R. Ascidians (Tunicata, Ascidiacea) from the Arvoredo Marine Biological Reserve, Santa Catarina, Brazil. Rev. Bras. Zool, v. 22, n. 2, p. 461-476, 2005.
  • RODRIGUES, S. A. Algumas ascídias do litoral sul do Brasil. Bol. Fac. Filos. Cienc. Let. Univ. São Paulo, v. 2, p. 193-216, 1962.
  • RODRIGUES, S. A.; ROCHA, R. M.; LOTUFO, T. M. C. Guia ilustrado para identificação das ascídias do Estado de São Paulo São Paulo: Parma, 1998. 190 p.
  • RODRIGUES DA COSTA, H. Notas sobre os Ascidiacea brasileiros. V. Subclasse Pleurogona. Atas Soc. Biol. Rio J., v. 12, n. 5-6, p. 299-302, 1969.
  • RUPPERT, E. E.; FOX, R. S. Seashore animals of the Southeast Columbia: University of South Carolina Press, 1988. 407 p.
  • RILOV, G.; CROOKS, J. A. Marine bioinvasions: Conservation hazards and vehicles for ecological understanding. In: RILOV, G.; CROOKS, J. A. (eds.). Biological invasions in marine ecosystems Ecological Studies 204. Berlin: Springer-Verlag, 2009. pp. 3-11.
  • SHANKS, A. L. Orientated swimming by megalopae of several eastern North Pacific crab species and its potential role in their onshore migration. J. Exp. Mar. Biol. Ecol, v. 186, p. 1-16, 1995.
  • SHILTS, M. H.; PASCUAL, M. S.; FOIGHIL, D. O. Systematic, taxonomic and biogeographic relationships of Argentine flat oysters. Mol. Phylogenet. Evol, v. 44, n. 1, p. 467-473, 2007.
  • SILVA, C. A. R.; SMITH, B. D., RAINBOW, P. S. Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Mar. Environ. Res, v. 61, n. 4, p. 439-455, 2006.
  • SILVA-BRUM, I. N.; MARTINS, E. M. P. Seasonal variation of the intertidal community of Balanomorpha of Guanabara Bay, Rio de Janeiro, Brazil (Crustacea Cirripedia). Rev. Bras. Biol., v. 57, n. 2, p. 275-288, 1997.
  • SILVEIRA, N. G.; SOUZA, R. C. C. L.; FERNANDES, F. C.; SILVA, E. P. Occurrence of Perna perna, Modiolus carvalhoi (Mollusca, Bivalvia, Mytilidae) and Megabalanus coccopoma (Crustacea, Cirripedia) off Areia Branca, Rio Grande do Norte State, Brazil. Biociências, v. 14, n. 1, p. 89-90, 2006.
  • SIMBERLOFF, D.; VON HOLLE, B. Positive interactions of nonindigenous species: Invasional meltdown? Biol. Invasions, v. 1, p. 21-32, 1999.
  • SKERMAN, T. M. Ship-fouling in New Zealand waters: A survey of marine fouling organisms from vessels of the coastal and overseas trades. New Zealand J. Sci, v. 3, n. 4, p. 620-648, 1960.
  • SOUTHGATE, T.; MYERS, A. A. Mussel fouling on the Celtic Sea Kinsale field gas platforms. Estuar. Coast. Shelf Sci, v. 20, p. 651-659, 1985.
  • SOUZA, A. C. F. F.; VIEIRA, D. M.; TEIXEIRA, S. F. Percepção da influência da espécie exótica Mytilopsis leucophaeta (Conrad, 1831) na atividade pesqueira de duas comunidades de Recife-PE. In: CONGRESSO DE ECOLOGIA DO BRASIL, 9, 2009, São Lourenço. Anais.. Caxambu: Sociedade Brasileira de Ecologia, 2009. 3p.
  • SOUZA, J. R. B.; ROCHA, C. M. C.; LIMA, M. P. R. Ocorrência do bivalve exótico Mytilopsis leucophaeta (Conrad) (Mollusca, Bivalvia), no Brasil. Rev. Bras. Zool, v. 22, n. 4, p. 1204-1206, 2005.
  • STREFTARIS, N.; ZENETOS, A.; PAPATHANASSIOU, E. Globalization in marine ecosystems: The story of non-indigenous marine species across European seas. Oceanogr. Mar. Biol. Annu. Rev, v. 43, p. 419-453, 2005.
  • THERRIAULT, T. W.; DOCKER, M. F.; ORLOVA, M. I.; HEATH, D. D.; MacISAAC, H. J. Molecular resolution of the family Dreissenidae (Mollusca: Bivalvia) with emphasis on Ponto-Caspian species, including first report of Mytilopsis leucophaeata in the Black Sea basin. Mol. Phylogenet. Evol., v. 30, n. 1-2, p. 479-489, 2004.
  • VAN NAME, W. G. The North and South American ascidians. Bull. Am. Mus. Nat. Hist, v. 84, p. 1-476, 1945.
  • VARELA, E. S.; BEASLEY, C. R.; SCHNEIDER, H.; SAMPAIO, I.; MARQUES-SILVA, N. S.; TAGLIARO, C. H. Molecular phylogeny of mangrove oysters (Crassostrea) from Brazil. J. Mollus. Stud, v. 73, p. 229-234, 2007.
  • VERMEIJ, G. J. When biotas meet: Understanding biotic interchange. Science, v. 253, n. 5024 p. 1099-1104, 1991.
  • VERMEIJ, G. J. An agenda for invasion biology. Biol. Conserv, v. 78, p. 3-9, 1996.
  • VERWEEN, A.; VINCX, M.; DEGRAER, S. Growth patterns of Mytilopsis leucophaeata, an invasive biofouling bivalve in Europe. Biofouling, v. 22, n. 4, p. 221-231, 2006.
  • VERWEEN, A.; VINCX, M.; DEGRAER, S. The effect of temperature and salinity on the survival of Mytilopsis leucophaeata larvae (Mollusca, Bivalvia): The search for environmental limits. J. Exp. Mar. Biol. Ecol, v. 348, n. 1-2, p. 111-120, 2007.
  • VERWEEN, A.; VINCX, M.; MEES, J.; DEGRAER, S. Seasonal variability of Mytilopsis leucophaeata larvae in the harbour of Antwerp: Implications for ecologically and economically sound biofouling control. Belg. J. Zool, v. 135, p. 91-93, 2005.
  • VIEIRA, L. M.; MIGOTTO, A. E.; WINSTON, J. E. Synopsis and annotated checklist of Recent marine Bryozoa from Brazil. Zootaxa, v. 1810, p. 1-39, 2008.
  • VISSCHER, J. P. Nature and extent of fouling on ships' bottoms. Bull. Bur. Fish., v. 43, n. 1031, p. 193-252, 1928.
  • WASSON, K.; ZABIN, C. J.; BEDINGER, L.; DIAZ, M. C.; PEARSE, J. S. Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol. Conserv, v. 102, p. 143-153, 2001.
  • WHOI. Marine fouling and its prevention Annapolis: Woods Hole Oceanographic Institution- WHOI, 1952. 381pp.
  • WILLIAMS, S. L.; GROSHOLZ, E. D. The invasive species challenge in estuarine and coastal environments: Marrying management and science. Estuaries & Coasts, v. 331, p. 3-20, 2008.
  • WIJSMAN, J. W. M.; SMAAL, A. C. Risk analysis of mussels transfer Ijmuiden: Wageningen IMARES - Institute for Marine Resources & Ecosystem Studies, Report Number: C044/06, 2006. 105p.
  • WINSTON, J. E. Marine bryozoans (Ectoprocta) of the Indian River area, Florida. Bull. Am. Mus. Nat. Hist, v. 173, p. 99-176, 1982.
  • WWF. Silent Invasion – The spread of marine invasive species via ships' ballast water. Gland: WWF International, 2009. 22 p.
  • YOUNG, P. S. Establishment of an Indo-Pacific barnacle in Brazil. Crustaceana, v. 56, n. 2, p. 212-214, 1989.
  • YOUNG, P. S. Maxillopoda. Thecostraca. In: YOUNG, P.S (Ed.) Catalogue of Crustacea of Brasil Rio de Janeiro: Museu Nacional do Rio de Janeiro, 1998. pp. 263-285.
  • YOUNG, P. S. The Balanoidea (Cirripedia) from the Brazilian coast. Bol. Mus. Nac., n. sér., n. 356, p. 1-36, 1994.
  • ZIBROWIUS, H. Assessing scale and impact of ship-transported alien fauna in the Mediterranean? In: CIESM 2002. Alien Marine Organisms introduced by ships in the Mediterranean and Black Seas, Istambul, 2002 Monaco: CIEMS Workshop Monograph 20. pp. 63-69.
  • ZVYAGINTSEV, A. Y. Fouling of ocean-going shipping and its role in the spread of exotic species in the seas of the Far East. Sessile Org., v. 17, n. 1, p. 31-43, 2000.
  • ZVYAGINTSEV, A. Y. Introduction of species into the Northwestern Sea of Japan and the problem of marine fouling. Russian J. Mar. Biol., v. 29, n. 1, p. S10–S21, 2003.

Publication Dates

  • Publication in this collection
    31 Aug 2010
  • Date of issue
    June 2010

History

  • Reviewed
    06 Apr 2009
  • Received
    26 Feb 2009
  • Accepted
    27 Apr 2010
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