Marine Biology

, Volume 162, Issue 5, pp 957–968 | Cite as

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

  • Katrina M. Pagenkopp Lohan
  • Kristina M. Hill-Spanik
  • Mark E. Torchin
  • Ellen E. Strong
  • Robert C. Fleischer
  • Gregory M. Ruiz
Original Paper

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.

Supplementary material

227_2015_2637_MOESM1_ESM.pdf (298 kb)
Supplementary material 1 (PDF 297 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. Carlton JT (1992) Introduced marine and estuarine mollusks of North America: an end-of-the-20th-century perspective. J Shellfish Res 11:489–505Google Scholar
  4. Carnegie RB, Cochennec-Laureau N (2004) Microcell parasites of oysters: recent insights and future trends. Aquat Living Resour 17:519–528CrossRefGoogle Scholar
  5. 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 10–18Google Scholar
  6. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefGoogle Scholar
  7. 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 BarbaraGoogle Scholar
  8. Coen LD, Brumbaugh RD, Bushek D et al (2007) Ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307CrossRefGoogle Scholar
  9. 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 135:147–158CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. Coutts AD, Moore KM, Hewitt CL (2003) Ships’ sea-chests: an overlooked transfer mechanism for non-indigenous marine species? Mar Pollut Bull 46:1510–1513CrossRefGoogle Scholar
  13. 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
  14. 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 CrossRefGoogle Scholar
  15. de Melo AGC, Varela ES, Beasley CR et al (2010) Molecular identification, phylogeny and geographic distribution of Brazilian mangrove oysters (Crassostrea). Genet Mol Biol 33:564–572CrossRefGoogle Scholar
  16. Donald KM, Kennedy M, Spencer HG (2005) Cladogenesis as the result of long-distance rafting events in South Pacific topshells (Gastropoda, Trochidae). Evolution 59:1701–1711CrossRefGoogle Scholar
  17. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acid Res 32:1792–1797. doi:10.1093/nar/gkh340 CrossRefGoogle Scholar
  18. 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 83:159–168CrossRefGoogle Scholar
  19. 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 325–336CrossRefGoogle Scholar
  20. 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 44:1589–1601CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 217–231CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Haupt TM, Griffiths CL, Robinson TB et al (2010) The history and status of oyster exploitation and culture in South Africa. J Shellfish Res 29:151–159CrossRefGoogle Scholar
  26. Hedgecock D, Li G, Banks MA, Kain Z (1999) Occurrence of the Kumamoto oyster Crassostrea sikamea in the Ariake Sea, Japan. Mar Biol 133:65–68CrossRefGoogle Scholar
  27. Kaplan E (1982) Coral Reefs: Caribbean and Florida. Houghton Mifflin Company, New YorkGoogle Scholar
  28. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings Bioinform 9:286–298CrossRefGoogle Scholar
  29. 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 30:3059–3066CrossRefGoogle Scholar
  30. Kemp WM, Boynton WR, Adolf JE et al (2005) Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Prog Ser 303:1–29CrossRefGoogle Scholar
  31. 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 7:306–317CrossRefGoogle Scholar
  32. 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 228:1–13CrossRefGoogle Scholar
  33. Lam K, Morton B (2006) Morphological and mitochondrial-DNA analysis of the Indo-west Pacific rock oysters (Ostreidae: Saccostrea species). J Molluscan Stud 72:235–245CrossRefGoogle Scholar
  34. 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 202:232–242CrossRefGoogle Scholar
  35. 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 426:197–212CrossRefGoogle Scholar
  36. Littlewood TJ, Donovan SK (1988) Variation of recent and fossil Crassostrea in Jamaica. Palaeontol 31:1013–1028Google Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 26:281–294CrossRefGoogle Scholar
  39. Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61Google Scholar
  40. 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 196:122–126CrossRefGoogle Scholar
  41. Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 2:155–161CrossRefGoogle Scholar
  45. Romashko S (1992) The shell book: Florida, Gulf, and Caribbean. Windward Publishing, LakevilleGoogle Scholar
  46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574. doi:10.1093/bioinformatics/btg180 CrossRefGoogle Scholar
  47. 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 291–299Google Scholar
  48. Scheltema RS (1986) Long-distance dispersal by planktonic larvae of shoal-water benthic invertebrates among central Pacific islands. Bull Mar Sci 39:241–256Google Scholar
  49. 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 8:443–448CrossRefGoogle Scholar
  50. 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 79:61–76CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 ppGoogle Scholar
  53. Tack JF, Vanden Berghe E, Polk P (1992) Ecomorphology of Crassostrea cucullata (Born, 1778) (Ostreidae) in a mangrove creek (Gazi, Kenya). Hydrobiol 247:109–117CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Tëmkin I (2010) Molecular phylogeny of pearl oysters and their relatives (Mollusca, Bivalvia, Pterioidea). BMC Evol Biol 10:342CrossRefGoogle Scholar
  56. Tucker Abbott R, Morris PA (1995) Shells of the Atlantic and Gulf Coasts and the West Indies, 4th edn. Houghton Mifflin Company, New YorkGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 19:213–223CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • Katrina M. Pagenkopp Lohan
    • 1
    • 2
  • Kristina M. Hill-Spanik
    • 1
    • 2
    • 3
  • Mark E. Torchin
    • 4
  • Ellen E. Strong
    • 5
  • Robert C. Fleischer
    • 1
  • Gregory M. Ruiz
    • 2
  1. 1.Center for Conservation and Evolutionary GeneticsSmithsonian Conservation Biology InstituteWashingtonUSA
  2. 2.Marine Invasions LaboratorySmithsonian Environmental Research CenterEdgewaterUSA
  3. 3.Grice Marine LabCollege of CharlestonCharlestonUSA
  4. 4.Smithsonian Tropical Research InstituteBalboa, AnconRepublic of Panama
  5. 5.Department of Invertebrate ZoologyNational Museum of Natural History, Smithsonian InstitutionWashingtonUSA

Personalised recommendations