The spread of the introduced ascidians Ciona robusta Hoshino & Tokioka, 1967 and Rhodosoma turcicum (Savigny, 1816) in the southwestern Atlantic

Authors

  • Danielle Fernandes Barboza Universidade do Estado do Rio de Janeiro
  • Luis Felipe Skinner Universidade do Estado do Rio de Janeiro

DOI:

https://doi.org/10.1590/2675-2824069.20-303dfb

Keywords:

Ascidiacea, Marine fouling, Introduced species, Marine activities

Abstract

New records of the introduced solitary ascidians, Ciona robusta and Rhodosoma turcicum, have been added to the southwestern Atlantic Ocean, from Cabo Frio to Ilha Grande Bay, Brazil, in surveys conducted since 2009. Both species occurred on natural and artificial substrates, in predator-protected habitats, and regions close to harbors or other maritime activities. The distribution of Ciona robusta was related to water temperature, influenced by upwelling intensity and temperatures below 25ºC, while R. turcicum was not sensitive to the range of recorded water temperatures. The occurrence of both species on sites close to maritime terminals suggests vessels as potential vectors.

References

BNDO (Base Nacional de Dados Oceanográficos). 2020. Centro de Hidrografia da Marinha - Dados PNBOIA [online]. Brasil: Marinha do Brasil. Available at: https://www.marinha.mil.br/chm/dados-do-goos-brasil/pnboia-mapa [Accessed 8 May 2020].

» https://www.marinha.mil.br/chm/dados-do-goos-brasil/pnboia-mapa

BATISTA, D., GONÇALVES, J. E. A., MESSANO, H. F., ALTVATER, L., CANDELLA, R., ELIAS, L. M. C., MESSANO, L. V. R., APOLINÁRIO, M. & COUTINHO, R. 2017. Distribution of the invasive orange cup coral Tubastraea coccinea Lesson, 1829 in an upwelling area in the South Atlantic Ocean fifteen years after its first record. Aquatic Invasions, 12(1), 23-32, DOI: https://doi.org/10.3391/ai.2017.12.1.03

» https://doi.org/10.3391/ai.2017.12.1.03

BAYLON, C. B. 1990. Culture of bivalve molluscs. Selected papers on mollusc culture [online]. Bangkok: NDP/FAO Regional Seafarming Development and Demonstration Project (RAS/90/002). Available at: http://www.fao.org/3/ab737e/AB737E02.htm#ch2 [Accessed 10 May 2020].

» http://www.fao.org/3/ab737e/AB737E02.htm#ch2

BLACKBURN, T. M., BELLARD, C. & RICCIARDI, A. 2019. Alien versus native species as driver of recent extinction. Frontiers in Ecology and the Environment, 17(4), 203-207, DOI: https://doi.org/10.1002/fee.2020

» https://doi.org/10.1002/fee.2020

BOLTOVSKOY, D. & VALENTIN, J. L. 2018. Overview of the history of biological oceanography in the southwestern Atlantic, with emphasis on plankton. In: HOFFMEYER, M. S., SABATINI, M. E., BRANDINI, F. P., CALLIARI, D. L. & SANTINELLI, N. H. Plankton ecology of the southwestern Atlantic [ebook]. Cham: Springer, pp. 3-34. Available at: https://link.springer.com/book/10.1007%2F978-3-319-77869-3#about [Accessed 15 Apr. 2020].

» https://link.springer.com/book/10.1007%2F978-3-319-77869-3#about

BOLTOVSKOY, D., SYLVESTER, F. & PAOLUCCI, E. M. 2018. Invasive species denialism: sorting out facts, beliefs, and definitions. Ecology and evolution, 8(22), 11190-11198, DOI: https://doi.org/10.1002/ece3.4588

» https://doi.org/10.1002/ece3.4588

BOUCHEMOUSSE, S., BISHOP, J. D. & VIARD, F. 2016. Contrasting global genetic patterns in two biologically similar, widespread and invasive Ciona species (Tunicata, Ascidiacea). Scientific Reports, 6, 24875, DOI: https://doi.org/10.1038/srep24875

» https://doi.org/10.1038/srep24875

BRASIL. Ministério da Infraestrutura. 2019. Plano Mestre - Complexo portuário de Forno/RJ - Sumário Executivo [online]. Rio de Janeiro: Ministério da Infraestrutura. Available at: http://antigo.infraestrutura.gov.br/images/planos-mestres-sumarios-executivos/FNO-Sum_Exec_simples.pdf [Accessed 15 Dec. 2019].

» http://antigo.infraestrutura.gov.br/images/planos-mestres-sumarios-executivos/FNO-Sum_Exec_simples.pdf

BRUNETTI, R., GISSI, C., PENNATI, R., CAICCI, F., GASPARINI, F. & MANNI, L. 2015. Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis Journal of Zoological Systematics and Evolutionary Research, 53(3), 186-193, DOI: https://doi.org/10.1111/jzs.12101

» https://doi.org/10.1111/jzs.12101

CAPUTI, L., TOSCANO, F., ARIENZO, M., FERRARA, L., PROCACCINI, G. & SORDINO, P. 2019. Temporal correlation of population composition and environmental variables in the marine invader Ciona robusta Marine Ecology, 40(2), e12543, DOI: https://doi.org/10.1111/maec.12543

» https://doi.org/10.1111/maec.12543

CAPUTI, L., CROCETTA, F., TOSCANO, F., SORDINO, P. & CIRINO, P. 2015. Long-term demographic and reproductive trends in Ciona intestinalis sp. A. Marine Ecology, 36(1), 118-128, DOI: https://doi.org/10.1111/maec.12125

» https://doi.org/10.1111/maec.12125

CARLTON, J. T. & ELDREDGE, L. G. 2009. Marine bioinvasions of Hawai’i: the introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian archipelago. Bishop Museum Bulletin in Cultural and Environmental Studies, 4, 1-203.

CLANCEY, L. & HINTON, R. 2003. Distribution of the tunicate, Ciona intestinalis Nova Scotia: Nova Scotia Department Agriculture and Fisheries.

COE, H. H., CARVALHO, C. N., SOUZA, L. O. & SOARES, A. 2007. Peculiaridades ecológicas da região de Cabo Frio. Revista Tamoios, 3(2), 1-20.

COLARUSSO, P., NELSON, E., AYVAZIAN, S., CARMAN, M. R., CHINTALA, M., GRABBERT, S. & GRUNDEN, D. 2016. Quantifying the ecological impact of invasive tunicates to shallow coastal water systems. Management of Biological Invasions, 7(1), 33-42, DOI: http://dx.doi.org/10.3391/mbi.2016.7.1.05

» http://dx.doi.org/10.3391/mbi.2016.7.1.05

COMAP (Companhia Municipal de Administração Portuária). 2008. Atualização do plano de desenvolvimento e zoneamento do Porto do Forno - 2008-2012 [online]. Arraial do Cabo: COMAP. Available at: http://www.transportes.gov.br/images/SNP/planejamento_portuario/pdz/pdz09.pdf[Accessed 15 Dec. 2019].

» http://www.transportes.gov.br/images/SNP/planejamento_portuario/pdz/pdz09.pdf

COSTA, H. R. 1969. Notas sobre os Ascidiacea brasileiros. IV. Ordem Phlebobranchia (Lahille, 1887). Atas da Sociedade de Biologia do Rio de Janeiro, 12(5-6), 289-292.

CREED, J. C., FENNER, D., SAMMARCO, P., CAIRNS, S., CAPEL, K., JUNQUEIRA, A. O. R., CRUZ, I., MIRANDA, R. J., CARLOS JUNIOR, L., MANTELATTO, M. C. & OIGMAN-PSZCZOL, S. 2017. The invasion of the azooxanthellate coral Tubastraea (Scleractinia: Dendrophylliidae) throughout the world: history, pathways and vectors. Biological Invasions, 19(1), 283-305, DOI: https://doi.org/10.1007/s10530-016-1279-y

» https://doi.org/10.1007/s10530-016-1279-y

CREED, J. C., PIRES, D. O. & FIGUEIREDO, M. A. O. 2007. Biodiversidade marinha da baía da Ilha Grande Brasília: Ministério do Meio Ambiente (MMA)/Secretaria de Biodiversidade e Florestas (SBF).

CROOKS, J. A., CHANG, A. L. & RUIZ, G. M. 2011. Aquatic pollution increases the relative success of invasive species. Biological Invasions, 13(1), 165-176, DOI: https://doi.org/10.1007/s10530-010-9799-3

» https://doi.org/10.1007/s10530-010-9799-3

DALEY, B. A. & SCAVIA, D. 2008. An integrated assessment of the continued spread and potential impacts of the colonial ascidian, Didemnum sp. A, in US waters. NOAA Technical Memorandum NOS NCCOS, 78, 1-70.

DARBYSON, E. A., HANSON, J. M., LOCKE, A. & WILLISON, J. H. M. 2009. Settlement and potential for transport of clubbed tunicate (Styela clava) on boat hulls. Aquatic Invasions, 4(1), 95-103.

DIAS, G. M., ROCHA, R. M., LOTUFO, T. M. C. & KREMER, L. P. 2013. Fifty years of ascidian biodiversity research in São Sebastião, Brazil. Journal of the Marine Biological Association of the United Kingdom, 93(1), 273-282, DOI: https://doi.org/10.1017/S002531541200063X

» https://doi.org/10.1017/S002531541200063X

DIAS, P. J., CARMAN, M. R. & BULLARD, S. G. 2019. All for one and one for all: research from the 6th International Invasive Sea Squirt Conference and the 10th International Conference on Marine Bioinvasions. Management of Biological Invasions, 10(4), 597-601, DOI: https://doi.org/10.3391/mbi.2019.10.4.01

» https://doi.org/10.3391/mbi.2019.10.4.01

DUMONT, C. P., GAYMER, C. F. & THIEL, M. 2011. Predation contributes to invasion resistance of benthic communities against the non-indigenous tunicate Ciona intestinalis Biological Invasions, 13(9), 2023-2034, DOI: https://doi.org/10.1007/s10530-011-0018-7

» https://doi.org/10.1007/s10530-011-0018-7

EPELBAUM, A., PEARCE, C. M., BARKER, D. J., PAULSON, A. & THERRIAULT, T. W. 2009. Susceptibility of non-indigenous ascidian species in British Columbia (Canada) to invertebrate predation. Marine Biology, 156(6), 1311-1320, DOI: https://doi.org/10.1007/s00227-009-1172-7

» https://doi.org/10.1007/s00227-009-1172-7

FOFONOFF, P. W., RUIZ, G. M., STEVES, B., HINES, A. H. & CARLTON, J. T. 2019. National exotic marine and estuarine species information system. Nemesis [online]. Available at: http://invasions.si.edu/nemesis/ [Accessed 13 Dec. 2019].

» http://invasions.si.edu/nemesis/

FOWLER, A. E., BLAKESLEE A. M. H., BORTOLUS A., DIAS, J., TEPOLT, C. K. & SCHWINDT, E. 2020 Current research, pressing issues, and lingering questions in marine invasion science: lessons from the Tenth International Conference on Marine Bioinvasions (ICMB-X). Aquatic Invasions, 15(1), 1-10, DOI: https://doi.org/10.3391/ai.2020.15.1.01

» https://doi.org/10.3391/ai.2020.15.1.01

FREESTONE, A. L., OSMAN, R. W., RUIZ, G. M. & TORCHIN, M. E. 2011. Stronger predation in the tropics shapes species richness patterns in marine communities. Ecology, 92(4), 983-993.

GISD (Global Invasive Species Database). 2019. Species profile: Ciona intestinalis [online]. Abu Dhabi: GISD. Available at: http://www.iucngisd.org/gisd/speciesname/Ciona+intestinalis [Accessed 10 May 2020].

» http://www.iucngisd.org/gisd/speciesname/Ciona+intestinalis

GRANOT, I., SHENKAR, N. & BELMAKER, J. 2017. Habitat niche breadth predicts invasiveness in solitary ascidians. Ecology and Evolution, 7(19), 7838-7847, DOI: https://doi.org/10.1002/ece3.3351

» https://doi.org/10.1002/ece3.3351

GRANTHOM-COSTA, L. V., FERREIRA, C. G. W. & DIAS, G. M. 2016. Biodiversity of ascidians in a heterogeneous bay from southeastern Brazil. Management of Biological Invasions, 7(1), 5-12, DOI: https://doi.org/10.3391/mbi.2016.7.1.02

» https://doi.org/10.3391/mbi.2016.7.1.02

GREY, E. K. 2010. Effects of large enemies on success of exotic species in marine fouling communities of Washington, USA. Marine Ecology Progress Series, 411, 89-100, DOI: https://doi.org/10.3354/meps08645

» https://doi.org/10.3354/meps08645

HOSHINO, Z. & TOKIOKA, T. 1967. An unusually robust Ciona from the northeastern coast of Honsyu Island, Japan. Publications of the Seto Marine Biological Laboratory, 15(4), 275-290.

IGNACIO, B. L., JULIO, L. M., JUNQUEIRA, A. O. R. & FERREIRA-SILVA, M. A. G. 2010. Bioinvasion in a Brazilian bay: filling gaps in the knowledge of southwestern Atlantic biota. PLoS ONE, 5(9), e13065, DOI: https://doi.org/10.1371/journal.pone.0013065

» https://doi.org/10.1371/journal.pone.0013065

INEA (Instituto Estadual do Ambiente). 2015. Diagnóstico do setor costeiro da Baía da Ilha Grande: Subsídios à elaboração do zoneamento ecológico-econômico costeiro - Volume I [online]. Rio de Janeiro: INEA. Available at: http://www.inea.rj.gov.br/cs/groups/public/documents/document/zwew/mdcz/~edisp/inea0073532.pdf [Acessed 12 Nov. 2019].

» http://www.inea.rj.gov.br/cs/groups/public/documents/document/zwew/mdcz/~edisp/inea0073532.pdf

JUNQUEIRA, A. O. R. 2013. Guilty or innocent? The need to improve the assessment of impacts caused by non-native species. Aquatic Conservation: Marine and Freshwater Ecosystems, 23(5), 641-645, DOI: https://doi.org/10.1002/aqc.2392

» https://doi.org/10.1002/aqc.2392

KAKKONEN, J. E., WORSFOLD, T. M., ASHELBY, C. W., TAYLOR, A. & BEATON, K. 2019. The value of regular monitoring and diverse sampling techniques to assess aquatic non-native species: a case study from Orkney. Management of Biological Invasions, 10(1), 46-79, DOI: https://doi.org/10.3391/mbi.2019.10.1.04

» https://doi.org/10.3391/mbi.2019.10.1.04

KAUANO, R. V., ROPER, J. J. & ROCHA, R. M. 2017. Small boats as vectors of marine invasion: experimental test of velocity and desiccation as limits. Marine Biology, 164, 27, DOI: https://doi.org/10.1007/s00227-016-3057-x

» https://doi.org/10.1007/s00227-016-3057-x

KIM, M. K., KIM, D. H., PARK, J. U., KIM, D. H., YOON, T. J., KIM, D. G., LEE, Y. & SHIN, S. 2019. Effects of temperature and salinity on the egg development and larval settlement of Ciona robusta (Ascidiacea, Phlebobranchia, Cionidae). Ocean Science Journal, 54, 97-106, DOI: https://doi.org/10.1007/s12601-018-0056-5

» https://doi.org/10.1007/s12601-018-0056-5

KOTT, P. 1985. The Australian Ascidiacea part I: Phlebobranchia and Stolidobranchia. Memoirs of the Queensland Museum, 23, 1-440.

KOTT, P. 2005. Catalogue of Tunicata in Australian waters Canberra: Australian Biological Resources Study.

KREMER, L. P. & ROCHA, R. M. 2011. The role of Didemnum perlucidum F. Monniot, 1983 (Tunicata, Ascidiacea) in a marine fouling community. Aquatic Invasions, 6(4), 441-449, DOI: https://doi.org/10.3391/ai.2011.6.4.09

» https://doi.org/10.3391/ai.2011.6.4.09

LAMBERT, G. 2005. Ecology and natural history of the protochordates. Canadian Journal of Zoology, 83(1), 34-50.

MARINS, F. O., OLIVEIRA, C. S., MACIEL, N. M. V. & SKINNER, L. F. 2009. Reinclusion of Ciona intestinalis (Ascidiacea: Cionidae) in Brazil - a methodological view. Marine Biodiversity Records, 2, e112.

MARINS, F. O., NOVAES, R. L. M., ROCHA, R. M. & JUNQUEIRA, A. O. R. 2010. Non indigenous ascidians in port and natural environments in a tropical Brazilian bay. Zoologia (Curitiba), 27(2), 213-221, DOI: https://doi.org/10.1590/S1984-46702010000200009

» https://doi.org/10.1590/S1984-46702010000200009

MCKINDSEY, C. W., LANDRY, T., O’BEIRN, F. X. & DAVIES, I. M. 2007. Bivalve aquaculture and exotic species: a review of ecological considerations and management issues. Journal of Shellfish Research, 26(2), 281-295.

MILLAR, R. H. 1958. Some ascidians from Brazil. Annals and Magazine of Natural History, 1(8), 497-514.

MILLAR, R. H. 1971. The biology of ascidians. Advances in Marine Biology, 9, 1-100.

MONNIOT, C., MONNIOT, F. & LABOUTE, P. 1991. Coral reef ascidians of New Caledonia (No. 30). Paris: Editions de I’ORSTOM.

NOAA. National Weather Service. Climate Prediction Center. 2019. El Niño/Southern oscillation (ENSO) diagnostic discussion [online]. Maryland: NOAA. Available at: https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ [Accessed 5 Dec. 2019].

» https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/

OBIS (Ocean Biodiversity Information System). 2019. Rhodosoma turcicum (Savigny, 1815) [online]. New Jersey: OBIS. Available at: https://obis.org/taxon/103749 [Accessed 20 Nov. 2019].

» https://obis.org/taxon/103749

O’BRIEN, C. E., JOHNSTON, M. W. & KERSTETTER, D. W. 2017. Ports and pests: assessing the threat of aquatic invasive species introduced by maritime shipping activity in Cuba. Marine Pollution Bulletin, 125(1-2), 92-102, DOI: https://doi.org/10.1016/j.marpolbul.2017.07.071

» https://doi.org/10.1016/j.marpolbul.2017.07.071

ORICCHIO, F., MARQUES, A., HAJDU, E., PITOMBO, F., AZEVEDO, F., PASSOS, F., VIEIRA, L., STAMPAR, S., ROCHA, R. & DIAS, G., 2019. Exotic species dominate marinas between the two most populated regions in the southwestern Atlantic Ocean. Marine Pollution Bulletin, 146, 884-892.

PAETZOLD, S. C., GIBERSON, D. J., HILL, J., DAVIDSON, J. D. P. & DAVIDSON, J. 2012. Effect of colonial tunicate presence on Ciona intestinalis recruitment within a mussel farming environment. Management of Biological Invasions, 3(1), 15-23, DOI: https://doi.org/10.3391/mbi.2012.3.1.02

» https://doi.org/10.3391/mbi.2012.3.1.02

PERKOL-FINKEL, S., ZILMAN, G., SELLA, I., MILOH, T. & BENAYAHU, Y. (2006). Floating and fixed artificial habitats: effects of substratum motion on benthic communities in a coral reef environment. Marine Ecology Progress Series, 317, 9-20.

RAMSAY, A., DAVIDSON, J., LANDRY, T. & STRYHN, H. 2008. The effect of mussel seed density on tunicate settlement and growth for the cultured mussel, Mytilus edulis Aquaculture, 275(1-4), 194-200, DOI: https://doi.org/10.1016/j.aquaculture.2008.01.024

» https://doi.org/10.1016/j.aquaculture.2008.01.024

ROCHA, R. M. 1995. Abundance and distribution of sessile invertebrates under intertidal boulders (São Paulo, Brazil). Boletim do Instituto Oceanográfico, 43(1), 71-88.

ROCHA, R. M. & COSTA, L. V. G. 2005. Ascidians (Urochordata: Ascidiacea) from Arraial do Cabo, Rio de Janeiro, Brazil.Iheringia. Sries Zoologia, 95(1), 57-64, DOI: https://doi.org/10.1590/S0073-47212005000100009

» https://doi.org/10.1590/S0073-47212005000100009

ROCHA, R. M., BONNET, N. Y. K., BAPTISTA, M. S. & BELTRAMIN, F. S. 2012. Introduced and native Phlebobranch and Stolidobranch solitary ascidians (Tunicata: Ascidiacea) around Salvador, Bahia, Brazil. Zoologia (Curitiba), 29(1), 39-53, DOI: https://doi.org/10.1590/S1984-46702012000100005

» https://doi.org/10.1590/S1984-46702012000100005

ROCHA, R. M., ZANATA, T. B. & MORENO, T. R. 2012. Keys for the identification of families and genera of Atlantic shallow water ascidians. Biota Neotropica, 12(1), 269-303, DOI: https://doi.org/10.1590/S1676-06032012000100022

» https://doi.org/10.1590/S1676-06032012000100022

ROCHA, R. M., CASTELLANO, G. C. & FREIRE, C. A. 2017. Physiological tolerance as a tool to support invasion risk assessment of tropical ascidians. Marine Ecology Progress Series, 577, 105-119, DOI: https://doi.org/10.3354/meps12225

» https://doi.org/10.3354/meps12225

ROCHA, R. M., KREMER, L. P., BAPTISTA, M. S. & METRI, R. 2009. Bivalve cultures provide habitat for exotic tunicates in southern Brazil. Aquatic invasions, 4(1), 195-205, DOI: https://doi.org/10.3391/ai.2009.4.1.20

» https://doi.org/10.3391/ai.2009.4.1.20

ROCHA, R. M. & BONNET, N. Y. K. 2009. Ascídias (Tunicata, Ascidiacea) introduzidas no Arquipélago de Alcatrazes, São Paulo. Iheringia. Series Zoologie, 99(1), 27-35.

ROTH, F., STUHLDREIER, I., SÁNCHEZ-NOGUERA, C., CARVALHO, S. & WILD, C. 2017. Simulated overfishing and natural eutrophication promote the relative success of a non-indigenous ascidian in coral reefs at the Pacific coast of Costa Rica. Aquatic Invasions, 12, 435-446, DOI: https://doi.org/10.3391/ai.2017.12.4.02

» https://doi.org/10.3391/ai.2017.12.4.02

SARDAIN, A., SARDAIN, E. & LEUNG, B. 2019. Global forecasts of shipping traffic and biological invasions to 2050. Nature Sustainability, 2, 274-282.

SAVIGNY, J., 1816. Mémoires sur les Animaux sans vertèbres Paris.

SATO, A., SATOH, N. & BISHOP, J. D. D. 2012. Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry. Marine Biology, 159(7), 1611-1619, DOI: https://doi.org/10.1007/s00227-012-1898-5

» https://doi.org/10.1007/s00227-012-1898-5

SEEBENS, H., GASTNER, M. T. & BLASIUS, B. 2013. The risk of marine bioinvasion caused by global shipping. Ecology Letters, 16(6), 782-790, DOI: https://doi.org/10.1111/ele.12111

» https://doi.org/10.1111/ele.12111

SHENKAR, N. & LOYA, Y. (2009). Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel. Marine Biodiversity Records, 2, e166, DOI: https://doi.org/10.1017/S1755267209990753

» https://doi.org/10.1017/S1755267209990753

SHENKAR, N., SHMUEL, Y. & HUCHON, D. 2018. The invasive ascidian Ciona robusta recorded from a Red Sea marina. Marine Biodiversity, 48(4), 2211-2214, DOI: https://doi.org/10.1007/s12526-017-0699-y

» https://doi.org/10.1007/s12526-017-0699-y

SILVA, A. C. P., SPATA, A. O. & LIMA, M. S. C. 2018. Gestão ambiental integrada na Região Metropolitana do Rio de Janeiro: a avaliação de impactos cumulativos e sinérgicos entre cidades milionárias - o exemplo da baia de Sepetiba (RJ). Confins, 38, DOI: https://doi.org/10.4000/confins.16960

» https://doi.org/10.4000/confins.16960

SKINNER, L. F. 2018a. Sea surface temperature measured since 2012 for Ponta leste, Angra dos Reis, Rio de Janeiro, Brazil. Researchgate [online]. Available at: https://www.researchgate.net/project/Conhecendo-e-Divulgando-a-Biodiversidade-Marinha-da-Baia-da-Ilha-Grande [Accessed 10 Oct. 2019], DOI: https://doi.org/10.13140/RG.2.2.19686.27205

» https://www.researchgate.net/project/Conhecendo-e-Divulgando-a-Biodiversidade-Marinha-da-Baia-da-Ilha-Grande

» https://doi.org/10.13140/RG.2.2.19686.27205

SKINNER, L. F. 2018b. Sea surface temperature measured since 2012 for Dois Rios cove, Ilha Grande, Rio de Janeiro, Brazil. Researchgate [online]. Available at: https://www.researchgate.net/project/Conhecendo-e-Divulgando-a-Biodiversidade-Marinha-da-Baia-da-Ilha-Grande [Accessed 10 Oct. 2019], DOI:https://doi.org/10.13140/RG.2.2.12975.38560

» https://www.researchgate.net/project/Conhecendo-e-Divulgando-a-Biodiversidade-Marinha-da-Baia-da-Ilha-Grande

» https://doi.org/10.13140/RG.2.2.12975.38560

SKINNER, L. F., BARBOZA, D. F. & ROCHA, R. M. 2016. Rapid assessment survey of introduced ascidians in a region with many marinas in the southwest Atlantic Ocean, Brazil. Management of Biological Invasions, 7(1), 13-20, DOI: http://dx.doi.org/10.3391/mbi.2016.7.1.03

» http://dx.doi.org/10.3391/mbi.2016.7.1.03

SKINNER, L. F., MACHARET, H. K. L. & COUTINHO, R. 2011. Influence of upwelling and tropical environments on the breeding development of the intertidal barnacle Tetraclita stalactifera (Lamarck, 1818). Brazilian Journal of Oceanography, 59(4), 349-356, DOI: https://doi.org/10.1590/S1679-87592011000400005

» https://doi.org/10.1590/S1679-87592011000400005

SKINNER, L. F., ROCHA, R. M. & COUNTS, B. K. 2019. Pyura gangelion and Pyura beta Sp. Nov. (Ascidiacea: Pyuridae): An exotic and a new tunicate from the west Atlantic. Zootaxa 4545 (2): 264. doi:10.11646/zootaxa.4545.2.6.

» https://doi.org/0.11646/zootaxa.4545.2.6

SKINNER, L. F., OLIVEIRA, G. C. M., BARBOZA, D. F., TENÓRIO, A. A. & SOARES, D. C. 2013. First record of the Ascidiacea Rhodosoma turcicum in the south-west Atlantic Ocean. Marine Biodiversity Records, 6, e37, DOI: https://doi.org/10.1017/S1755267213000092

» https://doi.org/10.1017/S1755267213000092

SPALDING, M. D., FOX, H. E., ALLEN, G. R., DAVIDSON, N., FERDAÑA, Z. A., FINLAYSON, M., HALPERN, B. S., JORGE, M. A., LOMBANA, A., LOURIE, S. A., MARTIN, K. D., MCMANUS, E., MOLNAR, J., RECCHIA, C. A. & ROBERTSON, J. 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience, 57(7), 573-583, DOI: https://doi.org/10.1641/B570707

» https://doi.org/10.1641/B570707

TARALLO, A., YAGI, M., OIKAWA, S., AGNISOLA, C. & D’ONOFRIO, G. 2016. Comparative morphophysiological analysis between Ciona robusta and Ciona savignyi Journal of Experimental Marine Biology and Ecology, 485, 83-87, DOI: https://doi.org/10.1016/j.jembe.2016.09.001

» https://doi.org/10.1016/j.jembe.2016.09.001

UNDERWOOD, A. J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance Cambridge: Cambridge University Press, DOI: https://doi.org/10.1017/CBO9780511806407

» https://doi.org/10.1017/CBO9780511806407

VALENTIN, J. L. 2001. The Cabo Frio upwelling system, Brazil. In: SEELIGER, U. & KJERFVE, B. (eds.). Coastal marine ecosystems of Latin America Berlin: Springer. pp. 97-105.

VAN NAME, W. G. 1945. North and South American ascidians. Bulletin of the American Museum of Natural History, 84, 1-462.

VIEIRA, E. A., DUARTE, L. F. L. & DIAS, G. M. 2012. How the timing of predation affects composition and diversity of species in a marine sessile community?. Journal of Experimental Marine Biology and Ecology, 412, 126-133, DOI: https://doi.org/10.1016/j.jembe.2011.11.011

» https://doi.org/10.1016/j.jembe.2011.11.011

ZABIN, C. J., ASHTON, G. V., BROWN, C. W., DAVIDSON, I. C., SYTSMA, M. D. & RUIZ, G. M. 2014. Small boats provide connectivity for nonindigenous marine species between a highly invaded international port and nearby coastal harbors. Management of Biological Invasions, 5(2), 97-112, DOI: https://doi.org/10.3391/mbi.2014.5.2.03

» https://doi.org/10.3391/mbi.2014.5.2.03

ZHAN, A., BRISKI, E., BOCK, D. G., GHABOOLI, S. & MACISAAC, H. J. 2015. Ascidians as models for studying invasion success. Marine Biology, 162(12), 2449-2470, DOI: https://doi.org/10.1007/s00227-015-2734-5

» https://doi.org/10.1007/s00227-015-2734-5

Downloads

Published

2021-06-15

How to Cite

Barboza, D. F., & Skinner, L. F. (2021). The spread of the introduced ascidians Ciona robusta Hoshino & Tokioka, 1967 and Rhodosoma turcicum (Savigny, 1816) in the southwestern Atlantic. Ocean and Coastal Research, 69, 13. https://doi.org/10.1590/2675-2824069.20-303dfb

Issue

Section

Original Article