Skip to main content

Advertisement

Log in

Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Taxonomic uncertainty often limits our ability to resolve biogeographic patterns and discern biological invasions. Within the bivalve mollusks, this uncertainty is particularly acute for oysters, as the high degree of phenotypic plasticity of their shells creates taxonomic confusion. The integration of molecular data with shell morphology can differentiate species, providing new insights into biogeography, invasions, and ecology of this functionally important group. As an initial step in resolving the identities and current geographic distributions of oyster species, sequence data from the mitochondrial cytochrome oxidase I gene were combined with morphological criteria to confirm the identities of ten oyster species of Ostreidae, Isognomonidae, and Pteriidae, focusing on the Pacific and Caribbean coasts of Panama, since tropical biota have received the least study. The results indicate that Crassostrea virginica, previously only reported from this region along the Yucatan Peninsula and coast of Venezuela, also occurs in the Caribbean waters of Panama. We also document the first record for a species of Saccostrea, a genus native to the Pacific, suggesting an invasion by an unknown non-native Saccostrea species that is now widespread along the Caribbean from the Panama Canal west to Bocas del Toro. Sequences of the internal transcribed spacer region (ITS1) of the ribosomal gene complex (rDNA) did not reveal any hybridization. Considering the high connectivity of shipping and boating in Panama, Saccostrea sp. may have been introduced to the Caribbean by either recreational or commercial vessels, but the timing and potential ecological effects of this invasion remain unknown.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Briski E, Ghabooli S, Bailey SA, MacIsaac HJ (2012) Invasion risk posed by macroinvertebrates transported in ships’ ballast tanks. Biol Invasions 14:1843–1850. doi:10.1007/s10530-012-0194-0

    Article  Google Scholar 

  • Burreson EM, Ford SE (2004) A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquat Living Resour 17:499–517. doi:10.1051/alr:2004056

    Article  Google Scholar 

  • Carlton JT (1992) Introduced marine and estuarine mollusks of North America: an end-of-the-20th-century perspective. J Shellfish Res 11:489–505

    Google Scholar 

  • Carnegie RB, Cochennec-Laureau N (2004) Microcell parasites of oysters: recent insights and future trends. Aquat Living Resour 17:519–528

    Article  Google Scholar 

  • Carriker MR, Gaffney PM (1996) A catalogue of selected species of living oysters (Osteacea) of the world. In: Kennedy VS, Newell RIE, Ebele AF (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 10–18

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  Google Scholar 

  • Coan EV, Valentich-Scott P (2012) Bivalve seashells of tropical west America: marine bivalve mollusks from Baja California to northern Perú, 1st edn. Santa Barbara Museum of Natural History, Santa Barbara

    Google Scholar 

  • Coen LD, Brumbaugh RD, Bushek D et al (2007) Ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307

    Article  Google Scholar 

  • Coles SL, DeFelice RC, Eldredge LG, Carlton JT (1999) Historical and recent introductions of non-indigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands. Mar Biol 135:147–158

    Article  Google Scholar 

  • Cordes JF, Xiao J, Reece KS (2008) Discrimination of nine Crassostrea oyster species based upon restriction fragment-length polymorphism analysis of nuclear and mitochondrial DNA markers. J Shellfish Res 27:1155–1161. doi:10.2983/0730-8000-27.5.1155

    Article  Google Scholar 

  • Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886. doi:10.1016/j.marpolbul.2007.03.011

    Article  CAS  Google Scholar 

  • Coutts AD, Moore KM, Hewitt CL (2003) Ships’ sea-chests: an overlooked transfer mechanism for non-indigenous marine species? Mar Pollut Bull 46:1510–1513

    Article  CAS  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nat Methods. doi:10.1038/nmeth.2109

    Google Scholar 

  • Davidson IC, Brown CW, Sytsma MD, Ruiz GM (2009) The role of containerships as transfer mechanisms of marine biofouling species. Biofouling 25:645–655. doi:10.1080/08927010903046268

    Article  Google Scholar 

  • de Melo AGC, Varela ES, Beasley CR et al (2010) Molecular identification, phylogeny and geographic distribution of Brazilian mangrove oysters (Crassostrea). Genet Mol Biol 33:564–572

    Article  Google Scholar 

  • Donald KM, Kennedy M, Spencer HG (2005) Cladogenesis as the result of long-distance rafting events in South Pacific topshells (Gastropoda, Trochidae). Evolution 59:1701–1711

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acid Res 32:1792–1797. doi:10.1093/nar/gkh340

    Article  CAS  Google Scholar 

  • Ford SE, Allam B, Xu Z (2009) Using bivalves as particle collectors with PCR detection to investigate the environmental distribution of Haplosporidium nelsoni. Dis Aquat Org 83:159–168

    Article  Google Scholar 

  • Galil BS, Zenetos A (2002) A sea change—exotics in the eastern Mediterranean. In: Olenin S, Leppäkoski E, Gollasch S (eds) Invasive aquatic species of Europe. Kluwer, Dordrecht, pp 325–336

    Chapter  Google Scholar 

  • Galvão MSN, Pereira OM, Hilsdorf AWS (2013) Molecular identification and distribution of mangrove oysters (Crassostrea) in an estuarine ecosystem in Southeast Brazil: implications for aquaculture and fisheries management. Aquac Res 44:1589–1601

    Article  Google Scholar 

  • Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol Res 13:851–861. doi:10.1111/1755-0998.12138

    Article  CAS  Google Scholar 

  • Gollasch S (2002) The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling 18:105–121. doi:10.1080/08927010290011361

    Article  Google Scholar 

  • Gollasch S, MacDonald E, Belson S et al (2002) Life in ballast tanks. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive Aquatic Species of Europe. Kluwer Academic Publishers, Netherlands, pp 217–231

    Chapter  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  CAS  Google Scholar 

  • Haupt TM, Griffiths CL, Robinson TB et al (2010) The history and status of oyster exploitation and culture in South Africa. J Shellfish Res 29:151–159

    Article  Google Scholar 

  • Hedgecock D, Li G, Banks MA, Kain Z (1999) Occurrence of the Kumamoto oyster Crassostrea sikamea in the Ariake Sea, Japan. Mar Biol 133:65–68

    Article  Google Scholar 

  • Kaplan E (1982) Coral Reefs: Caribbean and Florida. Houghton Mifflin Company, New York

    Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings Bioinform 9:286–298

    Article  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066

    Article  CAS  Google Scholar 

  • Kemp WM, Boynton WR, Adolf JE et al (2005) Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Prog Ser 303:1–29

    Article  Google Scholar 

  • Klinbunga S, Khamnamtong B, Puanglarp N et al (2005) Molecular taxonomy of cupped oysters (Crassostrea, Saccostrea, and Striostrea) in Thailand based on COI, 16S, and 18S rDNA polymorphism. Mar Biotechnol 7:306–317

    Article  CAS  Google Scholar 

  • Lam K, Morton B (2003) Mitochondrial DNA and morphological identification of a new species of Crassostrea (Bivalvia: Ostreidae) cultured for centuries in the Pearl River Delta, Hong Kong, China. Aquaculture 228:1–13

    Article  CAS  Google Scholar 

  • Lam K, Morton B (2006) Morphological and mitochondrial-DNA analysis of the Indo-west Pacific rock oysters (Ostreidae: Saccostrea species). J Molluscan Stud 72:235–245

    Article  Google Scholar 

  • Lapegue S, Boutet I, Leitão A et al (2002) Trans-Atlantic distribution of a mangrove oyster species revealed by 16S mtDNA and karyological analyses. Biol Bull 202:232–242

    Article  CAS  Google Scholar 

  • Lazoski C, Gusmão J, Boudry P, Solé-Cava AM (2011) Phylogeny and phylogeography of Atlantic oyster species: evolutionary history, limited genetic connectivity and isolation by distance. Mar Ecol Prog Ser 426:197–212

    Article  Google Scholar 

  • Littlewood TJ, Donovan SK (1988) Variation of recent and fossil Crassostrea in Jamaica. Palaeontol 31:1013–1028

    Google Scholar 

  • Liu J, Li Q, Kong L et al (2011) Identifying the true oysters (Bivalvia: Ostreidae) with mitochondrial phylogeny and distance-based DNA barcoding. Mol Ecol Res 11:820–830. doi:10.1111/j.1755-0998.2011.03025.x

    Article  Google Scholar 

  • McKindsey CW, Landry T, O’Beirn FX, Davies IM (2007) Bivalve aquaculture and exotic species: a review of ecological considerations and management issues. J Shellfish Res 26:281–294

    Article  Google Scholar 

  • Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61

    Google Scholar 

  • Ó Foighil D, Marshall BA, Hilbish TJ, Pino MA (1999) Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biol Bull 196:122–126

    Article  Google Scholar 

  • Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138

    Article  Google Scholar 

  • Polson MP, Hewson WE, Eernisse DJ et al (2009) You say Conchaphila, I say Lurida: molecular evidence for restricting the Olympia oyster (Ostrea lurida Carpenter 1864) to temperate western North America. J Shellfish Res 28:11–21. doi:10.2983/035.028.0102

    Article  Google Scholar 

  • Reece KS, Cordes JF, Stubbs JB et al (2008) Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Mar Biol 153:709–721. doi:10.1007/s00227-007-0846-2

    Article  Google Scholar 

  • Roche DG, Torchin ME (2007) Established population of the North American Harris mud crab, Rhithropanopeus harrisii (Gould, 1841) (Crustacea: Brachyura: Xanthidae) in the Panama Canal. Aquat Invasions 2:155–161

    Article  Google Scholar 

  • Romashko S (1992) The shell book: Florida, Gulf, and Caribbean. Windward Publishing, Lakeville

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  Google Scholar 

  • Ruiz GM, Torchin ME, Grant K (2009) Using the Panama Canal to test predictions about tropical marine invasions. In: Proceedings of Smithson marine science symposium, pp 291–299

  • Scheltema RS (1986) Long-distance dispersal by planktonic larvae of shoal-water benthic invertebrates among central Pacific islands. Bull Mar Sci 39:241–256

    Google Scholar 

  • Schlöder C, Canning-Clode J, Saltonstall K et al (2013) The Pacific bivalve Anomia peruviana in the Atlantic: a recent invasion across the Panama Canal? Aquat Invasions 8:443–448

    Article  Google Scholar 

  • Sekino M, Yamashita H (2013) Mitochondrial DNA barcoding for Okinawan oysters: a cryptic population of the Portuguese oyster Crassostrea angulata in Japanese waters. Fish Sci 79:61–76

    Article  CAS  Google Scholar 

  • Shilts MH, Pascual MS, Ó Foighil D (2007) Systematic, taxonomic and biogeographic relationships of Argentine flat oysters. Mol Phylogenetics Evol 44:467–473. doi:10.1016/j.ympev.2006.11.009

    Article  CAS  Google Scholar 

  • Stanley JG, Sellers MA (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico)—American oyster. US Fish and Wildlife Service biological report 82(11.64). US Army Corps of Engineers. TR EL-82-4, 25 pp

  • Tack JF, Vanden Berghe E, Polk P (1992) Ecomorphology of Crassostrea cucullata (Born, 1778) (Ostreidae) in a mangrove creek (Gazi, Kenya). Hydrobiol 247:109–117

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  Google Scholar 

  • Tëmkin I (2010) Molecular phylogeny of pearl oysters and their relatives (Mollusca, Bivalvia, Pterioidea). BMC Evol Biol 10:342

    Article  Google Scholar 

  • Tucker Abbott R, Morris PA (1995) Shells of the Atlantic and Gulf Coasts and the West Indies, 4th edn. Houghton Mifflin Company, New York

    Google Scholar 

  • Villalba A, Reece KS, Camino Ordás M et al (2004) Perkinsosis in molluscs: a review. Aquat Living Res 17:411–432. doi:10.1051/alr:2004050

    Article  Google Scholar 

  • Weigle SM, David Smith L, Carlton JL, Pederson J (2005) Assessing the risk of introducing exotic species via the live marine species trade. Conserv Biol 19:213–223

    Article  Google Scholar 

  • Wilk J, Bieler R (2009) Ecophenotypic variation in the flat tree oyster, Isognomon alatus (Bivalvia: Isognomonidae), across a tidal microhabitat gradient. Mar Biol Res 5:155–163. doi:10.1080/17451000802279644

    Article  Google Scholar 

Download references

Acknowledgments

We thank Gabriel Jacome and Plinio Gondola at the Smithsonian Bocas del Toro Marine Station for assistance and discussions on local bivalve species. Dr. Carmen Schlöder assisted with field collections and obtaining permits. We thank Dr. Ilya Tëmkin (NOVA) for assistance with identifying members of the Isognomonidae and John Wilk (UIC) for sharing his data and confirming the identity of the second species of Isognomon. Dr. Mark Minton assisted with the creation of maps in ArcGIS. Nancy Rotzel McInerney provided lab logistical support at CCEG. A Smithsonian Institution Grand Challenges Grant funded this project. A Smithsonian Institution MarineGEO Postdoctoral Fellowship funded KM Pagenkopp Lohan. This is contribution number 2 from the Smithsonian’s Tennenbaum Marine Observatories Network.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katrina M. Pagenkopp Lohan.

Additional information

Communicated by C. Riginos.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 297 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pagenkopp Lohan, K.M., Hill-Spanik, K.M., Torchin, M.E. et al. Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean. Mar Biol 162, 957–968 (2015). https://doi.org/10.1007/s00227-015-2637-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2637-5

Keywords

Navigation