Coral Reefs

, Volume 37, Issue 2, pp 585–596 | Cite as

Dispersal capacity and genetic relatedness in Acropora cervicornis on the Florida Reef Tract

  • Crawford Drury
  • Claire B. Paris
  • Vassiliki H. Kourafalou
  • Diego Lirman


Sexual reproduction in scleractinian corals is a critical component of species recovery, fostering population connectivity and enhancing genetic diveristy. The relative contribution of sexual reproduction to both connectivity and diversity in Acropora cervicornis may be variable due to this species’ capacity to reproduce effectively by fragmentation. Using a biophysical model and genomic data in this threatened species, we construct potential connectivity pathways on the Florida Reef Tract (FRT) and compare them to inferred migration rates derived from next-generation sequencing, using a link and node-based approach. Larval connectivity on the FRT can be divided into two zones: the northern region, where most transport is unidirectional to the north with the Florida Current, and the southern region that is more dynamic and exhibits complex spatial patterns. These biophysical linkages are poorly correlated with genetic connectivity patterns, which resolve many reciprocal connections and suggest a less sparse network. These results are difficult to reconcile with genetic data which indicate that individual reefs are diverse, suggesting important contributions of sexual reproduction and recruitment. Larval connectivity models highlight potential resources for recovery, such as areas with high larval export like the Lower Keys, or areas that are well connected to most other regions on the FRT, such as the Dry Tortugas.


Acropora cervicornis Coral reef connectivity Biophysical modeling Population structure Demographic inference 



We would like to thank Romain Chaput and Jay Fisch for assistance and advice with CMS setup, Erica Staaterman for the provision of settlement polygons, Mikhail Matz for helpful input regarding Dadi, and Ryan Gutenkunst for maintaining the Dadi forum and software. We would also like to thank three anonymous reviewers who provided constructive feedback.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2018_1683_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1094 kb)
338_2018_1683_MOESM2_ESM.docx (15 kb)
Supplementary material 2 (DOCX 15 kb)


  1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 9:323CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs In The Ecology and Etiology of Newly Emerging Marine Diseases. Springer, pp25-38Google Scholar
  3. Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy‐Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J (2013) From FastQ data to high‐confidence variant calls: the genome analysis toolkit best practices pipeline Current Protocols in Bioinformatics, pp11.10Google 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 (2008) A restoration genetics guide for coral reef conservation. Molecular Ecology 17:2796–2811CrossRefPubMedGoogle Scholar
  6. Baums IB, Miller MW, Hellberg ME (2005a) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Molecular Ecology 14:1377–1390CrossRefPubMedGoogle Scholar
  7. Baums IB, Hughes CR, Hellberg ME (2005b) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Marine Ecology Progress Series 288:115–127CrossRefGoogle Scholar
  8. Baums IB, Johnson ME, Devlin-Durante MK, Miller MW (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29:835–842CrossRefGoogle Scholar
  9. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  10. Botsford L, Hastings A, Gaines S (2001) Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecology Letters 4:144–150CrossRefGoogle Scholar
  11. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711CrossRefPubMedPubMedCentralGoogle Scholar
  12. Burgess SC, Nickols KJ, Griesemer CD, Barnett LA, Dedrick AG, Satterthwaite EV, Yamane L, Morgan SG, White JW, Botsford LW (2014) Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. Ecological Applications 24:257–270CrossRefPubMedGoogle Scholar
  13. Christie MR, Tissot BN, Albins MA, Beets JP, Jia Y, Ortiz DM, Thompson SE, Hixon MA (2010) Larval connectivity in an effective network of marine protected areas. PLoS One 5:e15715CrossRefPubMedPubMedCentralGoogle Scholar
  14. Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101–S113CrossRefGoogle Scholar
  15. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends in Ecology & Evolution 14:405–410CrossRefGoogle Scholar
  16. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1:443–466CrossRefPubMedGoogle Scholar
  17. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527CrossRefPubMedGoogle Scholar
  18. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-yr decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109:17995–17999CrossRefGoogle Scholar
  19. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Del Angel G, Rivas MA, Hanna M (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics 43:491–498CrossRefPubMedPubMedCentralGoogle Scholar
  20. Drury C, Dale KE, Panlilio JM, Miller SV, Lirman D, Larson EA, Bartels E, Crawford DL, Oleksiak MF (2016) Genomic variation among populations of threatened coral: Acropora cervicornis. BMC Genomics 17:1–13CrossRefGoogle Scholar
  21. Drury C, Schopmeyer S, Goergen E, Bartels E, Nedimyer K, Johnson M, Maxwell K, Galvan V, Manfrino C, Lirman D (2017) Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity. Ecology and Evolution 7:6188–6200CrossRefPubMedPubMedCentralGoogle Scholar
  22. Edgar GJ, Stuart-Smith RD, Willis TJ, Kininmonth S, Baker SC, Banks S, Barrett NS, Becerro MA, Bernard AT, Berkhout J (2014) Global conservation outcomes depend on marine protected areas with five key features. Nature 506:216–220CrossRefPubMedGoogle Scholar
  23. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379CrossRefPubMedPubMedCentralGoogle Scholar
  24. Flint M, Than JT (2016) Potential spawn induction and suppression agents in Caribbean Acropora cervicornis corals of the Florida Keys. PeerJ 4:e1982CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fogarty ND (2012) Caribbean acroporid coral hybrids are viable across life history stages. Marine Ecology Progress Series 446:145–159CrossRefGoogle Scholar
  26. Fogarty ND, Vollmer SV, Levitan DR (2012) Weak prezygotic isolating mechanisms in threatened Caribbean Acropora corals. PLoS One 7:e30486CrossRefPubMedPubMedCentralGoogle Scholar
  27. Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Molecular Ecology 21:1143–1157CrossRefPubMedGoogle Scholar
  28. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960CrossRefPubMedGoogle Scholar
  29. Gilmore MD, Hall BR (1976) Life history, growth habits, and constructional roles of Acropora cervicornis in the patch reef environment. Journal of Sedimentary Research 46:519–522Google Scholar
  30. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71CrossRefPubMedGoogle Scholar
  31. Ginsburg R, Shinn E (1995) Preferential distribution of reefs in the Florida reef tract: the past is the key to the present. Oceanographic Literature Review 8:674Google Scholar
  32. Gladfelter WB (1982) White-band disease in Acropora palmata: implications for the structure and growth of shallow reefs. Bulletin of Marine Science 32:639–643Google Scholar
  33. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genetics 5:e1000695CrossRefPubMedPubMedCentralGoogle Scholar
  34. Harrison PL (2011) Sexual reproduction of scleractinian corals In Coral reefs: an ecosystem in transition. Springer, pp59-85Google Scholar
  35. Hellberg ME (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473CrossRefGoogle Scholar
  36. Highsmith RC (1982) Reproduction by fragmentation in corals. Marine Ecology Progress Series 7:207–226CrossRefGoogle Scholar
  37. Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer D, Parmesan C, Possingham HP, Thomas C (2008) Assisted colonization and rapid climate change. Science 321:345–346CrossRefPubMedGoogle Scholar
  38. Hogarth WT (2006) Endangered and threatened species: final listing determinations for elkhorn coral and staghorn coral. Federal Register 71:26852–26861Google Scholar
  39. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  40. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JB, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  41. Hughes AR, Inouye BD, Johnson MT, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecology Letters 11:609–623CrossRefPubMedGoogle Scholar
  42. Jones GP, Almany GR, Russ G, Sale P, Steneck R, Van Oppen M, Willis B (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325CrossRefGoogle Scholar
  43. Kininmonth S, van Oppen MJ, Possingham HP (2010) Determining the community structure of the coral Seriatopora hystrix from hydrodynamic and genetic networks. Ecological Modelling 221:2870–2880CrossRefGoogle Scholar
  44. Knowlton N (2001) The future of coral reefs. Proceedings of the National Academy of Sciences 98:5419–5425CrossRefGoogle Scholar
  45. Kool JT, Paris CB, Andréfouët S, Cowen RK (2010) Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems. Ecography 33:597–606Google Scholar
  46. Kool JT, Moilanen A, Treml EA (2013) Population connectivity: recent advances and new perspectives. Landscape Ecology 28:165–185CrossRefGoogle Scholar
  47. Kourafalou VH, Kang H (2012) Florida Current meandering and evolution of cyclonic eddies along the Florida Keys Reef Tract: Are they interconnected? Journal of Geophysical Research: Oceans 117:1–25CrossRefGoogle Scholar
  48. Kourafalou VH, Peng G, Kang H, Hogan PJ, Smedstad O-M, Weisberg RH (2009) Evaluation of global ocean data assimilation experiment products on South Florida nested simulations with the Hybrid Coordinate Ocean Model. Ocean Dynamics 59:47–66CrossRefGoogle Scholar
  49. Lee TN, Rooth C, Williams E, McGowan M, Szmant AF, Clarke M (1992) Influence of Florida Current, gyres and wind-driven circulation on transport of larvae and recruitment in the Florida Keys coral reefs. Continental Shelf Research 12:971–1002CrossRefGoogle Scholar
  50. Lirman D, Schopmeyer S (2016) Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ 4:e2597CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lirman D, Schopmeyer S, Galvan V, Drury C, Baker AC, Baums IB (2014) Growth dynamics of the threatened Caribbean staghorn coral Acropora cervicornis: influence of host genotype, symbiont identity, colony size, and environmental setting. PLoS One 9:e107253CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lubchenco J, Palumbi SR, Gaines SD, Andelman S (2003) Plugging a hole in the ocean: the emerging science of marine reserves. Ecological Applications 13:S3–S7CrossRefGoogle Scholar
  53. Matz MV, Treml EA, Aglyamova GV, van Oppen MJ, Bay LK. (2017). Potential for rapid genetic adaptation to warming in a Great Barrier Reef coral. bioRxiv Google Scholar
  54. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20:1297–1303CrossRefPubMedPubMedCentralGoogle Scholar
  55. Miller M, Bourque A, Bohnsack J (2002) An analysis of the loss of acroporid corals at Looe Key, Florida, USA: 1983-2000. Coral Reefs 21:179–182Google Scholar
  56. Munday P, Leis J, Lough J, Paris C, Kingsford M, Berumen M, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395CrossRefGoogle Scholar
  57. Neigel JE, Avise JC (1983) Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution 37:437–453PubMedGoogle Scholar
  58. Nozawa Y, Harrison PL (2008) Temporal patterns of larval settlement and survivorship of two broadcast-spawning acroporid corals. Marine Biology 155:347–351CrossRefGoogle Scholar
  59. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications:S146-S158Google Scholar
  60. Pandolfi J (2002) Coral community dynamics at multiple scales. Coral Reefs 21:13–23CrossRefGoogle Scholar
  61. Paris CB, Chérubin LM, Cowen RK (2007) Surfing, spinning, or diving from reef to reef: effects on population connectivity. Marine Ecology Progress Series 347:285–300CrossRefGoogle Scholar
  62. Paris CB, Helgers J, Van Sebille E, Srinivasan A (2013) Connectivity Modeling System: A probabilistic modeling tool for the multi-scale tracking of biotic and abiotic variability in the ocean. Environmental Modelling & Software 42:47–54CrossRefGoogle Scholar
  63. Prada C, Hanna B, Budd AF, Woodley CM, Schmutz J, Grimwood J, Iglesias-Prieto R, Pandolfi JM, Levitan D, Johnson KG (2016) Empty niches after extinctions increase population sizes of modern corals. Current Biology 26:3190–3194CrossRefPubMedGoogle Scholar
  64. Pulliam HR (1988) Sources, sinks, and population regulation. The American Naturalist 132:652–661CrossRefGoogle Scholar
  65. Reusch TB, Ehlers A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences 102:2826–2831CrossRefGoogle Scholar
  66. Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJ, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithsonian Contributions to the Marine Sciences 38:437–457CrossRefGoogle Scholar
  67. Ritson-Williams R, Paul VJ, Arnold S, Steneck R (2010) Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29:71–81CrossRefGoogle Scholar
  68. Sala E, Aburto-Oropeza O, Paredes G, Parra I, Barrera JC, Dayton PK (2002) A general model for designing networks of marine reserves. Science 298:1991–1993CrossRefPubMedGoogle Scholar
  69. Selkoe KA, Aloia CC, Crandall ED, Iacchei M, Liggins L, Puritz JB, von der Heyden S, Toonen RJ (2016) A decade of seascape genetics: contributions to basic and applied marine connectivity. Marine Ecology Progress Series 554:1–19CrossRefGoogle Scholar
  70. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–323CrossRefPubMedGoogle Scholar
  71. Sponaugle S, Lee T, Kourafalou V, Pinkard D (2005) Florida Current frontal eddies and the settlement of coral reef fishes. Limnology and Oceanography 50:1033–1048CrossRefGoogle Scholar
  72. Sponaugle S, Paris C, Walter K, Kourafalou V, Alessandro E (2012) Observed and modeled larval settlement of a reef fish to the Florida Keys. Marine Ecology Progress Series 453:201–212CrossRefGoogle Scholar
  73. Staaterman E, Paris CB, Helgers J (2012) Orientation behavior in fish larvae: a missing piece to Hjort’s critical period hypothesis. Journal of Theoretical Biology 304:188–196CrossRefPubMedGoogle Scholar
  74. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–53CrossRefGoogle Scholar
  75. Tunnicliffe V (1981) Breakage and propagation of the stony coral Acropora cervicornis. Proceedings of the National Academy of Sciences 78:2427CrossRefGoogle Scholar
  76. van Oppen MJ, Lutz A, De’ath G, Peplow L, Kininmonth S (2008) Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral. PLoS One 3:e3401CrossRefPubMedPubMedCentralGoogle Scholar
  77. van Woesik R, Scott WJ, Aronson RB (2014) Lost opportunities: coral recruitment does not translate to reef recovery in the Florida Keys. Marine Pollution Bulletin 88:110–117CrossRefPubMedGoogle Scholar
  78. Vargas-Angel B, Thomas JD, Hoke SM (2003) High-latitude Acropora cervicornis thickets off Fort Lauderdale, Florida, USA. Coral Reefs 22:465–473CrossRefGoogle Scholar
  79. Vargas-Ángel B, Thomas J (2002) Sexual reproduction of Acropora cervicornis in nearshore waters off Fort Lauderdale, Florida, USA. Coral Reefs 21:25–26CrossRefGoogle Scholar
  80. Vargas-Ángel B, Colley SB, Hoke SM, Thomas JD (2006) The reproductive seasonality and gametogenic cycle of Acropora cervicornis off Broward County, Florida, USA. Coral Reefs 25:110–122CrossRefGoogle Scholar
  81. Vaz AC, Paris CB, Olascoaga MJ, Kourafalou VH, Kang H, Reed JK (2016) The perfect storm: Match-mismatch of bio-physical events drives larval reef fish connectivity between Pulley Ridge mesophotic reef and the Florida Keys. Continental Shelf Research 125:136–146CrossRefGoogle Scholar
  82. Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573CrossRefGoogle Scholar
  83. Williams D, Miller M, Kramer K (2008) Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705CrossRefGoogle Scholar
  84. Wood S, Baums I, Paris C, Ridgwell A, Kessler W, Hendy E (2016) El Niño and coral larval dispersal across the eastern Pacific marine barrier. Nature Communications 7:12571CrossRefPubMedPubMedCentralGoogle Scholar
  85. Young CN, Schopmeyer SA, Lirman D (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bulletin of Marine Science 88:1075–1098CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  2. 2.Department of Ocean Sciences, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  3. 3.Hawai’i Institute of Marine BiologyUniversity of Hawai’iKaneoheUSA

Personalised recommendations