Coral Reefs

, Volume 34, Issue 2, pp 631–638 | Cite as

A genetic approach to the origin of Millepora sp. in the eastern Atlantic

  • C. LópezEmail author
  • S. Clemente
  • C. Almeida
  • A. Brito
  • M. Hernández


Many species have experienced recent range expansions due to human-mediated processes, such as the unintentional transport on ships or plastic waste and ocean warming, which facilitates many tropical species to tolerate living beyond their normal limit of distribution, with a potential impact on autochthonous assemblages. In September 2008, three colonies of the fire coral Millepora sp. (Cnidaria: Hydrozoa) were found on the southeastern coast of Tenerife (Canary Islands), though this species had been previously described to have a circumtropical distribution with Cape Verde Islands as its northern limit of distribution in the eastern Atlantic. The aim of this study was to determine the origin of these new colonies in the Canary Islands (11°N of its previously known northernmost limit of distribution) using variation in the cytochrome oxidase subunit I (COI) gene as a molecular marker. In order to do that, Millepora samples from Tenerife and Cape Verde Islands were collected for molecular analyses, and COI sequences from Caribbean samples listed in GenBank were also included in the analysis. Our results showed that all the specimens from Tenerife were genetically identical, suggesting that the colonization of the Canary Islands was the result of a very recent and strong founder effect. The nucleotide sequences of the samples from the Cape Verde and the Canary Islands were closer to the Caribbean than between themselves, pointing to the Caribbean population as the source population for both archipelagos, through independent founder events. The fact that Millepora sp. arrived to Cape Verde long before arriving to the Canaries (pleistocene fossils have been found in that archipelago) suggests that the habitat requirements for this species did not exist before in the Canarian archipelago. Therefore, the rising seawater temperatures recently registered in the Canary Islands could have facilitated the settlement of reef-forming corals drifting across the two basins of the Atlantic.


Millepora sp. COI Canary Islands Cape Verde Coral distribution 



This research has been supported by a grant from Gobierno de Canarias ACIISI “PROYECTO ESTRUCTURANTE EN CIENCIAS MARINAS: GENMOLBIO” (FEDER) to C. López and by the Programa de Cooperación Transnacional Madeira-Azores-Canarias (MAC 2007-2013), in the context of the Canarias-Campus de Excelencia Internacional: ‘Educar para Conservar el Mar’ (ECOMAR-SEMACA). We would like to thank José Carlos Mendoza, José Carlos Hernández, Carlos Sangil and David Martínez for making the trip to Cape Verde a great trip and to the anonymous reviewers for their suggestions and comments.


  1. Boekschoten GJ, Best MB (1988) Fossil and recent shallow water corals from the Atlantic islands off western Africa. Zool Meded 8:99–112Google Scholar
  2. Boschma H (1948) The species problem in Millepora. Zoologische Verhandelingen 1:1–115Google Scholar
  3. Boschma H (1956) Milleporina and Stylasterina. In: Moore RC (ed) Treatise on invertebrate paleontology. Geological Society of America, University of Kansas, Lawrence, pp F90–F106Google Scholar
  4. Brito A, Falcón JM, Herrera R (2005) Sobre la tropicalización reciente de la ictiofauna litoral de las islas Canarias y su relación con cambios ambientales y actividades antrópicas. Vieraea 33:515–525Google Scholar
  5. Brito A, Clemente S, Herrera R (2011) On the occurrence of the African hind, Cephalopholis taeniops, in the Canary Islands (eastern subtropical Atlantic): introduction of large-sized demersal littoral fishes in ballast water of oil platforms? Biol Invansions 13:2185–2189CrossRefGoogle Scholar
  6. Bullart SG, Lambert G, Carman MR, Byrnes J, Whitlatcha RB, Ruiz G, Miller RJ, Harris L, Valentine PC, Collie JS, Pederson J, McNaught, Cohen AN, Rg Asch, Dijkstra J, Heinonen K (2007) The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. J Exp Mar Bio Ecol 342:99–108CrossRefGoogle Scholar
  7. Burns TP (1985) Hard-coral distribution and cold-water disturbances in South Florida. Coral Reefs 4:117–124CrossRefGoogle Scholar
  8. Chapin FS III, Sala OE, Burke IC, Grime JP, Hooper DU, Laurenroth WK, Lombard A, Mooney HA, Moiser AR, Naeem S, Pacala SW, Roy J, Steffen WL, Tilman D (1998) Ecosystem consequences of changing biodiversity. Bioscience 48:45–52CrossRefGoogle Scholar
  9. Clemente S, Rodríguez A, Brito A, Ramos A, Monterroso O, Hernández JC (2011) On the occurrence of the hydrocoral Millepora (Hydrozoa: milleporidae) in the subtropical eastern Atlantic (Canary Islands): is the colonization related to climatic events? Coral Reefs 30:237–240CrossRefGoogle Scholar
  10. Coffroth MA, Lasker HR, Diamond ME, Bruenn JA, Bermingham E (1992) DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species. Mar Biol 114:317–325CrossRefGoogle Scholar
  11. De Paula AF, Creed JC (2004) Two species of the coral Tubastraea (Cnidaria, Scleractinia) In Brazil: a case of accidental introduction. Bull Mar Sci 74:175–183Google Scholar
  12. Done TJ (1982) Patterns in the distribution of coral communities across the Central Great Barrier Reef. Coral Reefs 1:95–107CrossRefGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  14. Excoffier L, Larval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  15. Fields RA, Graham JB, Rosenblatt RH, Somero GN (1993) Effects of expected global climate change on marine faunas. TREE 8:361–367PubMedGoogle Scholar
  16. Fishelson L (1973) Ecological and biological phenomena influencing coral species composition on the reef tables at Eilat (Gulf of Aqaba, Red Sea). Mar Biol 19:183–196CrossRefGoogle Scholar
  17. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337CrossRefPubMedGoogle Scholar
  18. Freitas R, Luiz OJ, Silva PN, Floeter SR, Bernardi G, Ferreira CEL (2013) The occurrence of Sparisoma frondosum (Teloestei: Labridae) in the Cape Verde Archipelago, with a summary of expatriated Brazilian endemic reef fishes. Mar Biodivers 44:173–179CrossRefGoogle Scholar
  19. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodríguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241CrossRefPubMedGoogle Scholar
  20. Hernández JC, Clemente S, Sangil C, Brito A (2008) The key role of the sea urchin Diadema aff. antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): a spatio-temporal approach. Mar Environ Res 66:259–270CrossRefPubMedGoogle Scholar
  21. Hernández JC, Clemente S, Girard D, Pérez-Ruzafa A, Brito A (2010) Effect of temperature of settlement and postsettlement survival in a barrens-forming sea urchin. Mar Ecol Prog Ser 413:69–80CrossRefGoogle Scholar
  22. Hoeksema BW, Roos PJ, Cadée GC (2012) Trans-Atlantic rafting by the brooding reef coral Favia fragum on man-made flotsam. Mar Ecol Prog Ser 445:209–218CrossRefGoogle Scholar
  23. Jackson JBC (1985) Distribution and ecology of clonal and aclonal benthic invertebrates. In: Jackson JBC, Buss LW, Cook RF, Ashmun JW (eds) Population biology and evolution of clonal organism. Yale University Press, New Haven, Connecticut USA, pp 297–355Google Scholar
  24. Jackson JBC (1986) Modes of dispersal of clonal benthic invertebrates: consequences for species’ distributions and genetic structure of local populations. Bull Mar Sci 39:588–606Google Scholar
  25. Jokiel PL (1989) Rafting of reef corals and other organisms at Kwajalein Atoll. Mar Biol 101:483–493CrossRefGoogle Scholar
  26. Lasker HR (1990) Asexual reproduction, fragmentation, and skeletal morphology of a plexaurid gorgonian. Mar Ecol Prog Ser 19:261–268CrossRefGoogle Scholar
  27. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  28. Lewis JB (1989) The ecology of Millepora. Coral Reefs 8:99–107CrossRefGoogle Scholar
  29. Lewis JB (2006) Biology and Ecology of the Hydrocoral Millepora on Coral Reefs. Adv Mar Biol 50:1–55CrossRefPubMedGoogle Scholar
  30. Librado P, Rozas J (2009) DnaSP v5 A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  31. Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–894CrossRefPubMedGoogle Scholar
  32. Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137CrossRefPubMedGoogle Scholar
  33. McManus JW, Vergara SG (1998) ReefBase: a global database on coral reefs and their resources. Version 3.0 ICLARM Manila, PhilippinesGoogle Scholar
  34. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci 98:5446–5451CrossRefPubMedCentralPubMedGoogle Scholar
  35. Morri C, Bianchi CN (1995) Cnidarian zonation at llha do Sal (Arquipelago de Cabo Verde). Beiträge zur Paläontologie Wien 20:41–49Google Scholar
  36. Morri C, Cattaeno-Vietti R, Sartoni G, Banchi CN (2000) Shallow epibenthic communities of Ilha do Sal (Cape Verde Archipelago, eastern Atlantic). Life Mar Sci Supplement Part 2A:157–165Google Scholar
  37. Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and assemblage theory. Biol Conserv 78:149–161CrossRefGoogle Scholar
  38. Nunes FLD, Norris RD, Knowlton N (2011) Long distance dispersal and connectivity in amphi-atlantic corals at regional and basin scales. PLoS ONE 6:e22298CrossRefPubMedCentralPubMedGoogle Scholar
  39. Ramos AG, Martel A, Codd GA, Soler E, Coca J, Redondo A, Morrison LF, Metcalf JS, Ojeda A, Suárez S, Petit M (2005) Bloom of the marine diazotrophic cyanobacterium Richodesmium erythraceum in the Northwest African Upwelling. Mar Ecol Prog Ser 301:303–305CrossRefGoogle Scholar
  40. Reichard SH, Hamilton CV (1997) Predicting invasions of woody plants introduced into North America. Conserv Biol 11:193–203CrossRefGoogle Scholar
  41. Reimer JD, Hirose M, Wirtz P (2010) Zoanthids of the Cape Verde Islands and their symbionts: previously unexamined diversity in the Northeastern Atlantic. Contrib Zool 79:147–163Google Scholar
  42. Richards ZT, Oppen MJH, Wallace CC, Willis BL, Miller DJ (2008) Some rare Indo-Pacific coral species are probable hybrids. PLoS ONE 3:e3240CrossRefPubMedCentralPubMedGoogle Scholar
  43. Ruiz-Ramos DV (2009) Morphological and genetic variation in the Caribbean species of the hydrocoral genus Millepora. Ph.D. thesis, University of Puerto Rico, MayagüezGoogle Scholar
  44. Ruiz-Ramos DV, Weil E, Schizas NV (2014) Morphological and genetic evaluation of the hydrocoral Millepora species complex in the Caribbean. Zool Stud 53:1–15CrossRefGoogle Scholar
  45. Serrano E, Coma R, Ribes M, Weitzmann B, García M, Ballesteros E (2013) Rapid northward spread of a zooxanthellate coral enhanced by artificial structures and sea warming in the western Mediterranean. PLoS ONE 8:e52739CrossRefPubMedCentralPubMedGoogle Scholar
  46. Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974CrossRefGoogle Scholar
  47. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579CrossRefPubMedGoogle Scholar
  48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedCentralPubMedGoogle Scholar
  49. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedCentralPubMedGoogle Scholar
  50. Van Oppen MJH, Willis BL, Van Vugt HWJA, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinian, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373CrossRefPubMedGoogle Scholar
  51. Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. University of New South Wales Press, SydneyGoogle Scholar
  52. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359CrossRefGoogle Scholar
  53. Wonham MJ, Carlton JT, Ruiz GM, Smith LD (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Mar Biol 136:1111–1121CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • C. López
    • 1
    Email author
  • S. Clemente
    • 1
  • C. Almeida
    • 2
  • A. Brito
    • 1
  • M. Hernández
    • 3
  1. 1.Departamento de Biología Animal, Edafología y Geología, Facultad de BiologíaUniversidad de La Laguna (ULL)La Laguna (Tenerife)Spain
  2. 2.Departamento de Engenharias e Ciências do Mar.Universidad de Cabo VerdePraiaCape Verde
  3. 3.Instituto de Enfermedades Tropicales y Salud Pública de CanariasGenética. Universidad de La Laguna (ULL)La Laguna (Tenerife)Spain

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