First record of the Saccostrea oyster in Bertioga, São Paulo, Brazil
DOI:
https://doi.org/10.20950/1678-2305.2017v43n4p638Keywords:
Saccostrea, bivalve, exotic species, oyster, molecular identificationAbstract
This study presents the first record of an alien species of oyster in Bertioga, São Paulo State (Southeastern Brazilian coast). Alien oysters were found attached to mangrove roots, rock shores, stones and gravel in the riverbed, forming clusters of 10í 20 individuals and cohabiting with native oyster species (Crassostrea mangle, C. brasiliana and Ostrea sp.). Results are presented based on molecular analysis of specimens collected in the Itaguaré River in June 2014. We used partial sequences of 16S and COI genes to assess the taxonomic identity. The Neighbor-joining method was used to analyze phenetic relationships among samples and the genetic diversity was calculated from the Kimura two-parameter (K2P) distances. The sequences in this work clustered with a sequence of "Saccostrea cucullata†from Madagascar for both genes (COI and 16S) and presented a genetic distance of 1.7í 2.2% and 3.5í 5.3% from other sequences of "S. cucullata group†for 16S and COI fragments respectively. The genetic distances from others Saccostrea species (S. palmula, S. glomerata and S. mordax) ranged from 4.7 to 9.1% for 16S and from 13.8 to 19.0% for COI. The genetic distances from other oysters’ species sequences (genera Ostrea and Crassostrea) are over than 14.0% and 25.0% for 16S and COI respectively. The record is discussed in the context of possible consequences on the environment and probable pathways of introduction. This is the first published record of a Saccostrea species in the southwestern Atlantic Ocean.
References
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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): 281-294.
MELO, C. M. R.; SILVA, F. C.; GOMES, C. H. A. M.; SOLÉ-CAVA, A. M.; LAZOSKI, C. 2010 Crassostrea
gigas in natural oyster banks in southern Brazil. Biological Invasions, 12(3): 441-449.
MORGULIS, A.; COULOURIS, G.; RAYTSELIS, Y.; MADDEN, T. L.; AGARWALA, R.; SCHí"žFFER, A. A. 2008 Database Indexing for Production MegaBLAST Searches. Bioinformatics, 24(16):1757-1764.
NEI, M.; KUMAR, S. 2000 Molecular evolution and phylogenetics. Oxford University Press, New York.352 p.
OLIVEIRA, M. D.; TAKEDA, A. M.; BARROS, L. F.; BARBOSA, D. S.; RESENDE, E. K. 2006 Invasion by Limnoperna fortunei (Dunker, 1857) (Bivalvia, Mytilidae) of the Pantanal Wetland, Brazil.Biological Invasions, 8(1): 97-104.
PALUMBI, S. R. 1996 Nucleic acids II: the polymerase chain reaction. In: HILLIS, D. M.; MORITZ, C.;
MABLE, B. K., Eds. Molecular Systematics. Sinauer & Associates Inc, Sunderland, p. 205-247.
REECE, K. S.; CORDES, J. F.; STUBBS, J. B.; HUDSON, K. L.; FRANCIS, E. A. 2008 Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Marine
Biology, 153(4): 709-721.
RIOS, E.C. 2009. Compendium of brazilian sea shells, Rio Grande, Brasil. Evangraf, Rio Grande, 676p.
RUESINK, J. L.; LENIHAN, H. S.; TRIMBLE, A. C.; HEIMAN, K. W.; MICHELI, F.; BYERS, J. E.; KAY,M. C. 2005 Introduction of non-native oysters: cosystem effects and restoration implications. Annual Review of Ecology and Systematics, 36: 643-689.
RUIZ, G. M.; CARLTON, J. T.; GROSHOLTZ, E. D.; HINES, A. H. 1997 Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent and consequences. American Zoologist, 37(6): 621-632.
SAITOU, N.; NEI, M. 1987 The neighbor-joining method: A new method for reconstructing
phylogenetic trees. Molecular Biology and Evolution, 4(4): 406-425.
SALVI, D.; MACALI, A.; MARIOTTINI, P. 2014 Molecular Phylogenetics and Systematics of the Bivalve Family Ostreidae Based on rRNA Sequence-Structure Models and Multilocus Species Tree. PLoS ONE, 9(9): e108696.
SEKINO, M.; YAMASHITA, H. 2013 Mitochondrial DNA barcoding for Okinawan oysters: a cryptic
population of the Portuguese oyster Crassostrea angulata in Japanese waters. Fisheries Science,
79(1): 61-76.
TAMURA, K.; STECHER, G.; PETERSON, D.; FILIPSKI, A.; KUMAR, S. 2014 MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Molecular Biology and Evolution, 30(12): 2725-2729.
TEIXEIRA, R. M.; BARBOSA, J. S. P.; LÓPEZ, M. S.; FERREIRA-SILVA, M. A. G.; COUTINHO, R.;VILLAí"¡A, R. C. 2010 Bioinvasão Marinha: Os bivalves exóticos de substrato consolidado e suas interações com a comunidade receptora. Oecologia Australis, 14(2): 381-402.
THOMPSON, J. D.; HIGGINS, D. G.; GIBSON, T.J. 1994 CLUSTAL W: improving the sensitivity
of progressive multiple sequence alignment through sequence weighting, position-specific gap
penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4673-4680.
í"¡INAR, M. E.; BILECENOÄžLU, M.; í–ZTíÅ“RK, B.; KATAÄžAN, T.; YOKES, M. B.; AYSEL, V.; DAÄžLI, E.; Aí"¡IK, S.; í–ZCAN, T.; ERDOÄžAN, H. 2011 An updated review of alien species on the coasts of Turkey. Mediterranean Marine Science, 12(2): 257-315.
COLES, S. L.; DeFELICE, R. C.; ELDREDGE, L. G.; CARLTON, J. T. 1999 Historical and recent introductions of nonindigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands. Marine
Biology, 135(1): 147-158.
DARRIGRAN, G.; DRAGO, I. E. 2000 Invasion of the exotic freshwater mussel Limnoperna fortunei
(Dunker, 1857) (Bivalvia: Mytilidae) in South America. The Nautilus, 114(2): 69-73.
DAISIE European Invasive Alien Species Gateway, 2008 Saccostrea cucullata. Available in: <http://
www.europe-aliens.org/speciesFactsheet.do?speciesId=100848> Accessed in: September 21, 2015.
FOLMER, O.; BLACK, M.; HOEH, W.; LUTZ, R.; VRIJENHOEK, R. 1994 DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5): 294-299.
GALTSOFF, P. S. 1964 The American Oyster Crassostrea virginica Gmelin. Fishery Bulletin, 64, United States Government Printing Office, Washington D. C. 480 p.
GALVÃO, M. S. N.; PEREIRA, O. M.; HILSDORF, A. W. S. 2013 Molecular identification and
distribution of mangrove oysters (Crassostrea) in an estuarine ecosystem in Southeast Brazil:
implications for aquaculture and fisheries management. Aquaculture Research, 44(10): 1589-
1601.
GRABOWSKI, J. H.; BRUMBAUGH, R. D.; CONRAD, R. F.; KEELER, A. G.; OPALUCH, J. J.; PETERSON,
C. H.; PIEHLER, M. F.; POWERS, S. P.; SMYTH, A. R. 2012 Economic valuation of ecosystem services
provided by oysters reefs. BioScience, 62(10): 900
í 909.
HAMAGUCHI, M.; SHIMABUKURO, H.; USUKI, H.; HORI, M. 2014 Occurrences of the Indo-West
Pacific rock oyster Saccostrea cucullata in mainland Japan. Marine Biodiversity Records, 7(e84): 1-8.
HEBERT, P. D. N.; CYWINSKA, A.; BALL, S. L.; DEWAARD, J. R. 2003 Biological identifications
through DNA barcodes. Proceedings of the Royal Society of London Series B Biological Sciences,
270(1512): 313-321.
HUBER, M. 2010 Compendium of bivalves. A fullcolor guide to 3,300 of the world’s marine bivalves.A status on Bivalvia after 250 years of research. ConchBooks, Hackenheim. 901 p.
IGNACIO, B. L.; ABSHER, T. M.; LAZOSKI, C.; SOLÉ-CAVA, A. M. 2000 Genetic evidence of the
presence of two species of Crassostrea (Bivalvia: Ostreidae) on the coast of Brazil. Marine Biology,
136(6): 987-991.
JIN, Y.; LI, Q.; KONG, L.; YU, H.; ZHONG, X. 2014 High-resolution melting (HRM) analysis: a
highly sensitive alternative for the identification of commercially important Crassostrea oysters.
Journal of Molluscan Studies, 81(1): 167-170.
KIMURA, M. 1980 A simple method for estimating evolutionary rate of base substitutions through
comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2): 111-120.
LAM, K.; MORTON, B. 2006 Morphological and mitochondrial-DNA analysis of the Indo-West
Pacific rock oysters (Ostreidae: Saccostrea species). Journal of Molluscan Studies, 72(3): 235-245.
LAPíˆGUE, S.; BOUTET, I.; LEITÃO, A.; HEURTEBISE, S.; GARCIA, P.; THIRIOT-QUIÉVREUX, C.;
BOUDRY, P. 2002 Trans-Atlantic distribution of a mangrove oyster species revealed by 16S mtDNA
and karyological analyses. Biological Bulletin, 202(3): 232-242.
LAZOSKI, C.; GUSMÃO, J.; BOUDRY, P.; SOLÉCAVA, A. M. 2011 Phylogeny and phylogeography
of Atlantic oyster species: evolutionary history, limited genetic connectivity and isolation by
distance. Marine Ecology Progress Series, 426(1): 197-212.
LIU, J.; LI, Q.; KONG, L.; YU, H.; ZHENG, X. 2011 Identifying the true oysters (Bivalvia: Ostreidae)
with mitochondrial phylogeny and distance-based DNA barcoding. Molecular Ecology Resources, 11(5):820-830.
LOHAN, K. M. P.; HILL-SPANIK, K. M.; TORCHIN, M. E.; STRONG, E. E.; FLEISCHER, R. C.; GREGORY, M. R. 2015 Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean. Marine Biology, 162(5): 957-968.
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): 281-294.
MELO, C. M. R.; SILVA, F. C.; GOMES, C. H. A. M.; SOLÉ-CAVA, A. M.; LAZOSKI, C. 2010 Crassostrea
gigas in natural oyster banks in southern Brazil. Biological Invasions, 12(3): 441-449.
MORGULIS, A.; COULOURIS, G.; RAYTSELIS, Y.; MADDEN, T. L.; AGARWALA, R.; SCHí"žFFER, A. A. 2008 Database Indexing for Production MegaBLAST Searches. Bioinformatics, 24(16):1757-1764.
NEI, M.; KUMAR, S. 2000 Molecular evolution and phylogenetics. Oxford University Press, New York.352 p.
OLIVEIRA, M. D.; TAKEDA, A. M.; BARROS, L. F.; BARBOSA, D. S.; RESENDE, E. K. 2006 Invasion by Limnoperna fortunei (Dunker, 1857) (Bivalvia, Mytilidae) of the Pantanal Wetland, Brazil.Biological Invasions, 8(1): 97-104.
PALUMBI, S. R. 1996 Nucleic acids II: the polymerase chain reaction. In: HILLIS, D. M.; MORITZ, C.;
MABLE, B. K., Eds. Molecular Systematics. Sinauer & Associates Inc, Sunderland, p. 205-247.
REECE, K. S.; CORDES, J. F.; STUBBS, J. B.; HUDSON, K. L.; FRANCIS, E. A. 2008 Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Marine
Biology, 153(4): 709-721.
RIOS, E.C. 2009. Compendium of brazilian sea shells, Rio Grande, Brasil. Evangraf, Rio Grande, 676p.
RUESINK, J. L.; LENIHAN, H. S.; TRIMBLE, A. C.; HEIMAN, K. W.; MICHELI, F.; BYERS, J. E.; KAY,M. C. 2005 Introduction of non-native oysters: cosystem effects and restoration implications. Annual Review of Ecology and Systematics, 36: 643-689.
RUIZ, G. M.; CARLTON, J. T.; GROSHOLTZ, E. D.; HINES, A. H. 1997 Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent and consequences. American Zoologist, 37(6): 621-632.
SAITOU, N.; NEI, M. 1987 The neighbor-joining method: A new method for reconstructing
phylogenetic trees. Molecular Biology and Evolution, 4(4): 406-425.
SALVI, D.; MACALI, A.; MARIOTTINI, P. 2014 Molecular Phylogenetics and Systematics of the Bivalve Family Ostreidae Based on rRNA Sequence-Structure Models and Multilocus Species Tree. PLoS ONE, 9(9): e108696.
SEKINO, M.; YAMASHITA, H. 2013 Mitochondrial DNA barcoding for Okinawan oysters: a cryptic
population of the Portuguese oyster Crassostrea angulata in Japanese waters. Fisheries Science,
79(1): 61-76.
TAMURA, K.; STECHER, G.; PETERSON, D.; FILIPSKI, A.; KUMAR, S. 2014 MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Molecular Biology and Evolution, 30(12): 2725-2729.
TEIXEIRA, R. M.; BARBOSA, J. S. P.; LÓPEZ, M. S.; FERREIRA-SILVA, M. A. G.; COUTINHO, R.;VILLAí"¡A, R. C. 2010 Bioinvasão Marinha: Os bivalves exóticos de substrato consolidado e suas interações com a comunidade receptora. Oecologia Australis, 14(2): 381-402.
THOMPSON, J. D.; HIGGINS, D. G.; GIBSON, T.J. 1994 CLUSTAL W: improving the sensitivity
of progressive multiple sequence alignment through sequence weighting, position-specific gap
penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4673-4680.
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