Coral Reefs

, Volume 36, Issue 3, pp 701–716 | Cite as

Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic

  • Júlia N. de Souza
  • Flávia L. D. Nunes
  • Carla Zilberberg
  • Juan A. Sanchez
  • Alvaro E. Migotto
  • Bert W. Hoeksema
  • Xaymara M. Serrano
  • Andrew C. Baker
  • Alberto Lindner
Report

Abstract

Fire corals are the only branching corals in the South Atlantic and provide an important ecological role as habitat-builders in the region. With three endemic species (Millepora brazilensis, M. nitida and M. laboreli) and one amphi-Atlantic species (M. alcicornis), fire coral diversity in the Brazilian Province rivals that of the Caribbean Province. Phylogenetic relationships and patterns of population genetic structure and diversity were investigated in all four fire coral species occurring in the Brazilian Province to understand patterns of speciation and biogeography in the genus. A total of 273 colonies from the four species were collected from 17 locations spanning their geographic ranges. Sequences from the 16S ribosomal DNA (rDNA) were used to evaluate phylogenetic relationships. Patterns in genetic diversity and connectivity were inferred by measures of molecular diversity, analyses of molecular variance, pairwise differentiation, and by spatial analyses of molecular variance. Morphometrics of the endemic species M. braziliensis and M. nitida were evaluated by discriminant function analysis; macro-morphological characters were not sufficient to distinguish the two species. Genetic analyses showed that, although they are closely related, each species forms a well-supported clade. Furthermore, the endemic species characterized a distinct biogeographic barrier: M. braziliensis is restricted to the north of the São Francisco River, whereas M. nitida occurs only to the south. Millepora laboreli is restricted to a single location and has low genetic diversity. In contrast, the amphi-Atlantic species M. alcicornis shows high genetic connectivity within the Brazilian Province, and within the Caribbean Province (including Bermuda), despite low levels of gene flow between these populations and across the tropical Atlantic. These patterns reflect the importance of the Amazon–Orinoco Plume and the Mid-Atlantic Barrier as biogeographic barriers, and suggest that, while M. alcicornis is capable of long-distance dispersal, the three endemics have restricted ranges and more limited dispersal capabilities.

Keywords

Biogeographic barriers Endemics Genetic diversity Genetic structure Peripheral populations Phylogenetics 

Supplementary material

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Supplementary material 3 (FAS 40 kb)

References

  1. Amaral FMD, Broadhurst MK, Cairns SD, Schlenz E (2002) Skeletal morphometry of Millepora occurring in Brazil, including a previously undescribed species. Proceedings of the Biological Society of Washington 115:681–695Google Scholar
  2. Amaral FMD, Steiner AQ, Broadhurst MK, Cairns SD (2008) An overview of the shallow-water hydroids from Brazil (Hydrozoa:Cnidaria), including the description of a new species. Zootaxa 1930:56–68Google Scholar
  3. Arrigoni R, Kitano YF, Stolarski J, Hoeksema BW, Fukami H, Stefani F, Galli P, Montano S, Castoldi E, Benzoni F (2014) A phylogeny reconstruction of the Dendrophylliidae (Cnidaria, Scleractinia) based on molecular and micromorphological criteria, and its ecological implications. Zool Scr 43:661–688CrossRefGoogle Scholar
  4. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605CrossRefPubMedGoogle Scholar
  5. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390CrossRefPubMedGoogle Scholar
  6. Benzoni F, Arrigoni R, Stefani F, Reijnen BT, Montano S, Hoeksema BW (2012) Phylogenetic position and taxonomy of Cycloseris explanulata and C. wellsi (Scleractinia: Fungiidae): lost mushroom corals find their way home. Contributions to Zoology 81:125–146Google Scholar
  7. Bertelsen E, Ussing H (1936) Marine tropical animals carried to the Copenhagen Sydhavn on a ship from the Bermudas. Vidensk Medd Dansk Naturhist Foren Kobenhavn 100:237–245Google Scholar
  8. Boekschoten GJ, Borel Best M (1988) Fossil and recent shallow water corals from the Atlantic islands off Western Africa. Zoologische Mededeelingen 62:98–112Google Scholar
  9. Boschma H (1948) The species problem in Millepora. Zoologische Verhandelingen 1:1–115Google Scholar
  10. Boschma H (1962) On Milleporine corals from Brazil. Proc K Ned Akad Wet C 65:302–313Google Scholar
  11. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bourmaud CA-F, Leung JKL, Bollard S, Gravier-Bonnet N (2013) Mass spawning events, seasonality and reproductive features in milleporids (Cnidaria, Hydrozoa) from Reunion Island. Mar Ecol 34:14–24CrossRefGoogle Scholar
  13. Brasil (2014) Ministério do Meio Ambiente, Portaria n° 445, de 17 de dezembro de 2014. Fauna brasileira ameaçada de extinção. Diário Oficial da União 18 dez 2014; Seção 1Google Scholar
  14. Brazeau DA, Sammarco PW, Gleason DF (2005) A multi-locus genetic assignment technique to assess sources of Agaricia agaricites larvae on coral reefs. Mar Biol 147:1141–1148CrossRefGoogle Scholar
  15. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30CrossRefGoogle Scholar
  16. Budd AF, Stolarski J (2009) Searching for new morphological characters in the systematics of scleractinian reef corals: comparison of septal teeth and granules between Atlantic and Pacific Mussidae. Acta Zool 90:142–165CrossRefGoogle Scholar
  17. Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc 166:465–529CrossRefGoogle Scholar
  18. Cabezas MP, Navarro-Barranco C, Ros M, Guerra-García JM (2013) Long-distance dispersal, low connectivity and molecular evidence of a new cryptic species in the obligate rafter Caprella andreae Mayer, 1890 (Crustacea: Amphipoda: Caprellidae). Helgol Mar Res 67:483–497CrossRefGoogle Scholar
  19. Caires RA, Figueiredo JL, Bernardes RÁ (2008) Registros novos e adicionais de teleósteos marinhos na costa brasileira. Pap Avulsos Zool 48:213–225Google Scholar
  20. Capel KCC, Segal B, Bertuol P, Lindner A (2012) Corallith beds at the edge of the tropical South Atlantic. Coral Reefs 31:75CrossRefGoogle Scholar
  21. Carvalho Filho A, Ferreira CEL (2013) A new species of dwarf sea bass, genus Serranus (Serranidae: Actinopterygii), from the southwestern Atlantic Ocean. Neotrop Ichthyol 11:809–814CrossRefGoogle Scholar
  22. Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371Google Scholar
  23. Clemente S, Rodríguez A, Brito A, Ramos A, Monterroso Ó, 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
  24. 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
  25. Coni EOC, Ferreira CM, de Moura RL, Meirelles PM, Kaufman L, Francini-Filho RB (2013) An evaluation of the use of branching fire-corals (Millepora spp.) as refuge by reef fish in the Abrolhos Bank, eastern Brazil. Environ Biol Fishes 96:45–55CrossRefGoogle Scholar
  26. Connell JH (1973) Population ecology of reef building corals. In: Jones OA, Endean R (eds) Biology and geology of coral reefs. Academic Press, New York, pp 204–205Google Scholar
  27. Connolly SR, Baird AH (2010) Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals. Ecology 91:3572–3583CrossRefPubMedGoogle Scholar
  28. Cordeiro RTS, Kitahara MV, Amaral FMD (2012) New records and range extensions of azooxanthellate scleractinians (Cnidaria: Anthozoa) from Brazil. Mar Biodivers Rec 5:e35CrossRefGoogle Scholar
  29. Cordeiro RTS, Neves BM, Rosa-Filho JS, Pérez CD (2015) Mesophotic coral ecosystems occur offshore and north of the Amazon River. Bull Mar Sci 91:491–510CrossRefGoogle Scholar
  30. Cunningham CW, Buss LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the Family Hydractiniidae. Biochem Syst Ecol 21:57–69CrossRefGoogle Scholar
  31. Cunningham CW, Buss LW, Anderson C (1991) Molecular and geologic evidence of shared history between hermit crabs and the symbiotic genus Hydractinia. Evolution 45:1301–1316CrossRefPubMedGoogle Scholar
  32. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  33. de Weerdt WH (1984) Taxonomic characters in Caribbean Millepora species (Hydrozoa, Coelenterata). Bijdragen tot de Dierkunde 54:243–262Google Scholar
  34. DiBattista JD, Berumen ML, Gaither MR, Rocha LA, Eble JA, Choat JH, Craig MT, Skillings DJ, Bowen BW (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. J Biogeogr 40:1170–1181CrossRefGoogle Scholar
  35. Dubé CE, Boissin E, Planes S (2016) Overgrowth of living scleractinian corals by the hydrocoral Millepora platyphylla in Moorea, French Polynesia. Mar Biodivers 46:329–330CrossRefGoogle Scholar
  36. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  37. Edmunds PJ (1999) The role of colony morphology and substratum inclination in the success of Millepora alcicornis on shallow coral reefs. Coral Reefs 18:133–140CrossRefGoogle Scholar
  38. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  39. Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O, Ferrari R, Gonzalez P, Gore S, Guppy R, McCartney MA, McCoy C, Mendes J, Srinivasan A, Steiner S, Vermeij MJ, Weil E, Mumby PJ (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol Ecol 21:1143–1157CrossRefPubMedGoogle Scholar
  40. Fukami H, Budd AF, Paulay G, Sole A, Chen CA, Iwao K, Knowlton N (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835CrossRefPubMedGoogle Scholar
  41. Gasparini JL, Joyeux J-C, Floeter SR (2003) Sparisoma tuiupiranga, a new species of parrotfish (Perciformes: Labroidei: Scaridae) from Brazil, with comments on the evolution of the genus. Zootaxa 384:1–14CrossRefGoogle Scholar
  42. Gittenberger A, Reijnen BT, Hoeksema BW (2011) A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contributions to Zoology 80:107–132Google Scholar
  43. Goodbody-Gringley G, Woollacott RM, Giribet G (2012) Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar Ecol 33:32–48CrossRefGoogle Scholar
  44. Goodbody-Gringley G, Vollmer SV, Woollacott RM, Giribet G (2010) Limited gene flow in the brooding coral Favia fragum (Esper, 1797). Mar Biol 157:2591–2602CrossRefGoogle Scholar
  45. Govindarajan AF, Halanych KM, Cunningham CW (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Mar Biol 146:213–222CrossRefGoogle Scholar
  46. Guimarães RZP, Bacellar ACLH (2002) Review of the Brazilian species of Paraclinus (Teleostei: Labrisomidae), with descriptions of two new species and revalidation of Paraclinus rubicundus (Starks). Copeia 2002:419–427CrossRefGoogle Scholar
  47. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  48. Hoeksema BW (2012) Extreme morphological plasticity enables a free mode of life in Favia gravida at Ascension Island (South Atlantic). Mar Biodivers 42:289–295CrossRefGoogle Scholar
  49. 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
  50. Hoeksema BW, Nunes FLD, Lindner A, de Souza JN (2014) Millepora alcicornis (Hydrozoa: Capitata) at Ascension Island: confirmed identity based on morphological and molecular analyses. J Mar Biol Assoc UK. doi:10.1017/S0025315414001283 Google Scholar
  51. Hoorn C, Guerrero J, Sarmiento GA, Lorente MA (1995) Andean tectonics as a cause for changing drainage patterns in Miocene northern South America. Geology 23:237–240CrossRefGoogle Scholar
  52. Hu C, Montgomery ET, Schmitt RW, Muller-Karger FE (2004) The dispersal of the Amazon and Orinoco River water in the tropical Atlantic and Caribbean Sea: observation from space and S-PALACE floats. Deep Sea Res Part 2 Top Stud Oceanogr 51:1151–1171CrossRefGoogle Scholar
  53. Huang D, Benzoni F, Fukami H, Knowlton N, Smith ND, Budd AF (2014a) Taxonomic classification of the reef coral families Merulinidae, Montastraeidae, and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc 171:277–355CrossRefGoogle Scholar
  54. Huang D, Benzoni F, Arrigoni R, Baird AH, Berumen ML, Bouwmeester J, Chou LM, Fukami H, Licuanan WY, Lovell ER, Meier R, Todd PA, Budd AF (2014b) Towards a phylogenetic classification of reef corals: the Indo-Pacific genera Merulina, Goniastrea and Scapophyllia (Scleractinia, Merulinidae). Zool Scr 43:531–548CrossRefGoogle Scholar
  55. Jokiel PL (1989) Rafting of reef corals and other organisms at Kwajalein Atoll. Mar Biol 101:483–493CrossRefGoogle Scholar
  56. Kitahara MV (2007) Species richness and distribution of azooxanthellate Scleractinia in Brazil. Bull Mar Sci 81:497–518Google Scholar
  57. Laborel J (1969a) Les peuplements de Madréporaires des cotês tropicales du Brésil. Annales de l´Université D’Abidjan Série E II:1–261Google Scholar
  58. Laborel J (1969b) Madréporaires et Hydrocoralliaires récifaux des côtes brésiliennes: systématique, écologie, répartition verticale et géographique. Resultats Scientifiques des Campagnes de la Calypso 9:171–229Google Scholar
  59. Laborel J (1974) West African reef corals: an hypothesis on their origin. Proc 2nd Int Coral Reef Symp 1:425–443Google Scholar
  60. Lang J (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279Google Scholar
  61. Leal ICS, Pereira PHC, De Araujo ME (2013) Coral reef fish association and behaviour on the fire coral Millepora spp. in north-east Brazil. J Mar Biol Assoc UK 93:1703–1711CrossRefGoogle Scholar
  62. Leal ICS, de Araújo ME, da Cunha SR, Pereira PHC (2015) The influence of fire-coral colony size and agonistic behaviour of territorial damselfish on associated coral reef fish communities. Mar Environ Res 108:45–54CrossRefPubMedGoogle Scholar
  63. Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 9–52CrossRefGoogle Scholar
  64. Lewis JB (1989) The ecology of Millepora—a review. Coral Reefs 8:99–107CrossRefGoogle Scholar
  65. Lewis JB (1991) The ampullae and medusae of the calcareous hydrozoan Millepora complanata. Hydrobiologia 216(217):165–169CrossRefGoogle Scholar
  66. Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55CrossRefPubMedGoogle Scholar
  67. Lindner A, Cairns SD, Cunningham CW (2008) From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors. PLoS One 3:e2429CrossRefPubMedPubMedCentralGoogle Scholar
  68. López C, Clemente S, Almeida C, Brito A, Hernández M (2015) A genetic approach to the origin of Millepora sp. in the eastern Atlantic. Coral Reefs 34:631–638CrossRefGoogle Scholar
  69. López-Gappa J, Liuzzi MG (2016) High density of the alien bryozoan Fenestrulina delicia in the fouling assemblage of a South American harbour (Argentina). Mar Biodivers 46:509–513CrossRefGoogle Scholar
  70. Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proc R Soc Lond B Biol Sci 279:1033–1040CrossRefGoogle Scholar
  71. Mayer AG (1910) Medusae of the world. Hydromedusae, vols. I & II. Scyphomedusae, vol III. Carnegie Institution, WashingtonGoogle Scholar
  72. Miller KJ, Ayre DJ (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol 77:713–724CrossRefPubMedGoogle Scholar
  73. Moura CJ, Cunha MR, Porteiro FM, Rogers AD (2011) The use of the DNA barcode gene 16S mRNA for the clarification of taxonomic problems within the family Sertulariidae (Cnidaria, Hydrozoa). Zool Scr 40:520–537CrossRefGoogle Scholar
  74. Moura CJ, Cunha MR, Porteiro FM, Rogers AD (2012) A molecular phylogenetic appraisal of the systematics of the Aglaopheniidae (Cnidaria: Hydrozoa, Leptothecata) from the north-east Atlantic and west Mediterranean. Zool J Linn Soc 164:717–727CrossRefGoogle Scholar
  75. Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM et al (2016) An extensive reef system at the Amazon River mouth. Sci Adv 2:e1501252CrossRefPubMedPubMedCentralGoogle Scholar
  76. Nawrocki AM, Schuchert P, Cartwright P (2010) Phylogenetics and evolution of Capitata (Cnidaria: Hydrozoa), and the systematics of Corynidae. Zool Scr 39:290–304CrossRefGoogle Scholar
  77. Neves E, Johnsson R (2009) Taxonomic revision of the southwestern Atlantic Madracis and the description of Madracis fragilis n. sp. (Scleractinia: Pocilloporidae), a new coral species from Brazil. Sci Mar 73:739–746CrossRefGoogle Scholar
  78. Neves EG, Johnsson R, Sampaio CLS, Pichon M (2006) The occurrence of Scolymia cubensis in Brazil: revising the problem of the Caribbean solitary mussids. Zootaxa 1366:45–54Google Scholar
  79. Neves EG, Andrade SCS, Silveira FL, Solferini VN (2008) Genetic variation and population structuring in two brooding coral species (Siderastrea stellata and Siderastrea radians) from Brazil. Genetica 132:243–254CrossRefPubMedGoogle Scholar
  80. Neves EG, Silveira FL, Pichon M, Johnsson R (2010) Cnidaria, Scleractinia, Siderastreidae, Siderastrea siderea (Ellis and Solander, 1786): Hartt Expedition and the first record of a Caribbean siderastreid in tropical Southwestern Atlantic. Check List 6:505–510CrossRefGoogle Scholar
  81. Nunes F, Norris RD, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18:4283–4297CrossRefPubMedGoogle Scholar
  82. Nunes FLD, Norris RD, Knowlton N (2011) Long distance dispersal and connectivity in amphi-Atlantic corals at regional and basin scales. PLoS One 6:e22298CrossRefPubMedPubMedCentralGoogle Scholar
  83. Nunes F, Fukami H, Vollmer SV, Norris RD, Knowlton N (2008) Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs 27:423–432CrossRefGoogle Scholar
  84. Pereira PHC, Leal ICS, de Araújo ME, Souza AT (2012) Feeding association between reef fishes and the fire coral Millepora spp. (Cnidaria: Hydrozoa). Mar Biodivers Rec 5:e42CrossRefGoogle Scholar
  85. Picciani N, de Lossio e Seiblitz IG, de Paiva PC, Castro CB, Zilberberg C (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the Southwestern Atlantic Ocean. Mar Biol 163:236CrossRefGoogle Scholar
  86. Pinzón JH, Weil E (2011) Cryptic species within the Atlantic-Caribbean genus Meandrina (Scleractinia): a multidisciplinary approach and description of the new species Meandrina jacksoni. Bull Mar Sci 87:823–853CrossRefGoogle Scholar
  87. Pires DO (2007) The azooxanthellate coral fauna of Brazil. In: George RY, Cairns SD (eds) Conservation and adaptative management of seamount and deep-sea coral ecosystems. Rosentiel School of Marine and Atmospheric Science, University of Miami, Miami, pp 265–272Google Scholar
  88. Razak TB, Hoeksema BW (2003) The hydrocoral genus Millepora (Hydrozoa: Capitata: Milleporidae) in Indonesia. Zoologische Verhandelingen 345:313–336Google Scholar
  89. Ros M, Guerra-García JM, Hoffman R (2016) First record of the exotic caprellid amphipod Paracaprella pusilla Mayer, 1890 in the eastern Mediterranean. Mar Biodivers 46:281–284CrossRefGoogle Scholar
  90. Ruiz-Ramos DV, Weil E, Schizas NV (2014) Morphological and genetic evaluation of the hydrocoral Millepora species complex in the Caribbean. Zool Stud 53:4CrossRefGoogle Scholar
  91. Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long-distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6:21619CrossRefPubMedPubMedCentralGoogle Scholar
  92. Serrano X, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL, Nunes FLD, Baker AC (2014) Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol 23:4226–4240CrossRefPubMedGoogle Scholar
  93. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68CrossRefGoogle Scholar
  94. Soong K, Lang JC (1992) Reproductive integration in reef corals. Biol Bull 183:418–431CrossRefGoogle Scholar
  95. Soong K, Cho LC (1998) Synchronized release of medusae from three species of hydrozoan fire corals. Coral Reefs 17:145–154CrossRefGoogle Scholar
  96. Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128CrossRefGoogle Scholar
  97. Verrill AE (1868) Notice of the corals and echinoderms collected by Prof. C. F. Hartt, at the Abrolhos Reefs, Province of Bahia, Brazil, 1867. Transactions of the Connecticut Academy of Arts and Sciences 1:351–364Google Scholar
  98. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50CrossRefPubMedGoogle Scholar
  99. Wahle CM (1980) Detection, pursuit, and overgrowth of tropical gorgonians by milleporid hydrocorals: Perseus and Medusa revisited. Science 209:689–691CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Júlia N. de Souza
    • 1
  • Flávia L. D. Nunes
    • 2
    • 3
  • Carla Zilberberg
    • 4
  • Juan A. Sanchez
    • 5
  • Alvaro E. Migotto
    • 6
  • Bert W. Hoeksema
    • 7
  • Xaymara M. Serrano
    • 8
    • 9
  • Andrew C. Baker
    • 8
  • Alberto Lindner
    • 1
  1. 1.Departamento de Ecologia e ZoologiaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Laboratoire des Sciences de l’Environnement Marin, LEMAR UMR 6539 CNRS/UBO/IRD/Ifremer, Université de Brest (UBO), Université Européenne de Bretagne (UEB)Institut Universitaire Européen de la Mer (IUEM)PlouzanéFrance
  3. 3.Laboratoire d’Écologie Benthique Côtière, DYNECOIfremer Centre BretagnePlouzanéFrance
  4. 4.Departamento de Zoologia, Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  5. 5.BIOMMAR, Department of Biological SciencesUniversidad de los AndesBogotáColombia
  6. 6.Centro de Biologia MarinhaUniversidade de São PauloSão SebastiãoBrazil
  7. 7.Naturalis Biodiversity CenterLeidenThe Netherlands
  8. 8.Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  9. 9.Atlantic Oceanographic and Meteorological LaboratoryNational Oceanic and Atmospheric AdministrationMiamiUSA

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