Advertisement

Coral Reefs

pp 1–14 | Cite as

Population connectivity among shallow and mesophotic Montastraea cavernosa corals in the Gulf of Mexico identifies potential for refugia

  • M. S. Studivan
  • J. D. Voss
Report

Abstract

Successful management of spatially isolated coral reefs is contingent on an understanding of ecological connections across populations. To investigate genetic connectivity of the depth-generalist coral species Montastraea cavernosa, populations from both shallow (15–30 m) and mesophotic coral ecosystems (30–70 m) in the Gulf of Mexico (GOM) were analyzed with microsatellite genotyping. A series of upstream and downstream sites were chosen in marine protected areas including Carrie Bow Cay, Belize; Flower Garden Banks and nearby mesophotic bank habitats; Pulley Ridge; and Dry Tortugas. Patterns of genetic diversity within the northwest GOM supported relatively open coral populations with high levels of gene flow between shallow and mesophotic depth zones, consistent with strong oceanographic patterns and hypothesized availability of coral reef habitats in the GOM. Conversely, genetic differentiation within Belize and the southeast GOM indicate relative isolation of shallow and mesophotic M. cavernosa populations in these regions. Structure analysis showed dominant genetic clusters within each region that did not correlate strongly with depth zones, and identified a cluster of unknown origin contributing to high differentiation at Pulley Ridge. Migration modeling predicted historical region-wide panmixia for most regions, with Pulley Ridge appearing to be a potential sink population. The GOM appears to demonstrate stronger evidence of vertical connectivity compared to elsewhere in the Tropical Western Atlantic, which may be the result of oceanographic variability and/or lack of local selection at depth. These findings are consistent with previous studies identifying genetic connectivity of broadcast-spawning corals across broad spatial scales and highlight the potential importance of mesophotic habitats in the GOM as larval sources to geographically distant populations.

Keywords

Population genetics Mesophotic coral ecosystems Deep reef refugia hypothesis Vertical connectivity Montastraea cavernosa Marine spatial planning 

Notes

Acknowledgements

We are grateful to the staff of Flower Garden Banks and Florida Keys National Marine Sanctuaries; the crews of the R/V Manta, R/V Walton Smith, and M/V Spree; L. Horn and J. White from the University of North Carolina at Wilmington Undersea Vehicle Program; and the Smithsonian Marine Station. We acknowledge J. Beal, J. Emmert, R. Susen, C. Ledford, J. Polinski, A. Alker, D. Dodge, P. Gardner, M. McCallister, M. Ajemian, R. Christian, and M. Dickson for diving support, and G. O’Corry-Crowe and T. Ferrer for assistance with molecular analyses. Corals were collected from Flower Garden Banks National Marine Sanctuary under permits FGBNMS-2010-005 and FGBNMS-2014-014, and from Carrie Bow Cay under CITES permits 4224 and 7123. This research was funded by the NOAA Office of Ocean Exploration and Research under awards NA09OAR4320073 and NA14OAR4320260 to the Cooperative Institute for Ocean Exploration, Research and Technology (CIOERT) at Harbor Branch Oceanographic Institute and the NOAA National Centers for Coastal Ocean Science under award NA11NOS4780045 to the Cooperative Institute for Marine and Atmospheric Studies (CIMAS) at the University of Miami. Additional funding was provided by a private donation establishing the Robertson Coral Reef Research and Conservation Program at Harbor Branch Oceanographic Institute, and by graduate student fellowships and Grants from Florida Atlantic University. This is contribution number 2149 from Harbor Branch Oceanographic Institute at FAU.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

338_2018_1733_MOESM1_ESM.docx (543 kb)
Supplementary material 1 (DOCX 543 kb)

References

  1. Atchison AD, Sammarco PW, Brazeau DA (2008) Genetic connectivity in corals on the Flower Garden Banks and surrounding oil/gas platforms, Gulf of Mexico. J Exp Mar Biol Ecol 365:1–12CrossRefGoogle Scholar
  2. Bak RPM, Nieuwland G, Meesters EH (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curacao and Bonaire. Coral Reefs 24:475–479CrossRefGoogle Scholar
  3. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390CrossRefPubMedGoogle Scholar
  4. Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345CrossRefPubMedGoogle Scholar
  5. Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326CrossRefPubMedPubMedCentralGoogle Scholar
  6. Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past. Am Zool 39:131–145CrossRefGoogle Scholar
  7. Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KRW, Bak RPM, Vermeij MJA, Hoegh-Guldberg O (2015) Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep 5:7652CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bongaerts P, Frade PR, Ogier JJ, Hay KB, van Bleijswijk J, Englebert N, Vermeij MJA, Bak RPM, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010a) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  10. Bongaerts P, Riginos C, Brunner R, Englebert N, Smith SR, Hoegh-Guldberg O (2017) Deep reefs are not universal refuges: reseeding potential varies among coral species. Sci Adv 3:e1602373CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010b) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5:e10871CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brazeau DA, Lesser MP, Slattery M (2013) Genetic structure in the coral, Montastraea cavernosa: assessing genetic differentiation among and within mesophotic reefs. PLoS ONE 8:e65845CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  14. Chollett I, Garavelli L, Holstein D, Chérubin LM, Fulton S, Box SJ (2017) A case for redefining the boundaries of the Mesoamerican Reef Ecoregion. Coral Reefs 36:1039–1046CrossRefGoogle Scholar
  15. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on. Nat Protoc 1:581–585CrossRefPubMedGoogle Scholar
  16. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  17. Costantini F, Gori A, Lopez-González P, Bramanti L, Rossi S, Gili J-M, Abbiati M (2016) Limited genetic connectivity between gorgonian morphotypes along a depth gradient. PLoS ONE 11:e0160678CrossRefPubMedPubMedCentralGoogle Scholar
  18. Culter JK, Ritchie KB, Earle SA, Guggenheim DE, Halley RB, Ciembronowicz KT, Hine AC, Jarrett BD, Locker SD, Jaap WC (2006) Pulley reef: a deep photosynthetic coral reef on the West Florida Shelf, USA. Coral Reefs 25:228CrossRefGoogle Scholar
  19. Davies SW, Strader ME, Kool JT, Kenkel CD, Matz MV (2017) Modeled differences of coral life-history traits influence the refugium potential of a remote Caribbean reef. Coral Reefs 36:913–925CrossRefGoogle Scholar
  20. Donoghue JF (2011) Sea level history of the northern Gulf of Mexico coast and sea level rise scenarios for the near future. Clim Change 107:17–33CrossRefGoogle Scholar
  21. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  23. 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
  24. Ezer T, Thattai DV, Kjerfve B, Heyman WD (2005) On the variability of the flow along the Meso-American Barrier Reef system: a numerical model study of the influence of the Caribbean current and eddies. Ocean Dyn 55:458–475CrossRefGoogle Scholar
  25. Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642CrossRefGoogle Scholar
  26. 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 MJA, Weil E, Mumby PJ (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol Ecol 21:1143–1157CrossRefPubMedGoogle Scholar
  27. Garavelli L, Studivan MS, Voss JD, Kuba A, Figueiredo J, Chérubin LM (2018) Assessment of mesophotic coral ecosystem connectivity for proposed expansion of a marine sanctuary in the northwest Gulf of Mexico: larval dynamics. Front Mar Sci 5:174CrossRefGoogle Scholar
  28. Gehrels R (2010) Sea-level changes since the Last Glacial Maximum: an appraisal of the IPCC Fourth Assessment Report. J Quat Sci 25:26–38CrossRefGoogle Scholar
  29. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Change Biol 2:495–509CrossRefGoogle Scholar
  30. 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
  31. 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
  32. Gulf of Mexico Fishery Management Council (2016) Final report: 5-year review of essential fish habitat requirements, including review of Habitat Areas of Particular Concern and adverse effects of fishing and non-fishing in the fishery management plans of the Gulf of Mexico. Gulf of Mexico Fishery Management Council, Tampa, FL, p 502Google Scholar
  33. Hammerman NM, Rivera-Vicens RE, Galaska MP, Weil E, Appledoorn RS, Alfaro M, Schizas NV (2018) Population connectivity of the plating coral Agaricia lamarcki from southwest Puerto Rico. Coral Reefs 37:183–191CrossRefGoogle Scholar
  34. Hine AC, Halley RB, Locker SD, Jarrett BD, Jaap WC, Mallinson DJ, Ciembronowicz KT, Ogden NB, Donahue BT, Naar DF (2008) Coral reefs, present and past, on the West Florida Shelf and platform margin. In: Riegl BM, Dodge RE (eds) Coral reefs of the USA. Springer, Dordrecht, pp 127–173CrossRefGoogle Scholar
  35. Holstein DM, Paris CB, Vaz AC, Smith TB (2015) Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35:23–37CrossRefGoogle Scholar
  36. Jaap WC (2015) Stony coral (Milleporidae and Scleractinia) communities in the eastern Gulf of Mexico: a synopsis with insights from the Hourglass collections. Bull Mar Sci 91:207–253CrossRefGoogle Scholar
  37. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  38. Jarrett BD, Hine AC, Halley RB, Naar DF, Locker SD, Neumann AC, Twichell D, Hu C, Donahue BT, Jaap WC, Palandro D, Ciembronowicz K (2005) Strange bedfellows—a deep-water hermatypic coral reef superimposed on a drowned barrier island; southern Pulley Ridge, SW Florida platform margin. Mar Geol 214:295–307CrossRefGoogle Scholar
  39. Johnston MA, Embesi JA, Eckert RJ, Nuttall MF, Hickerson EL, Schmahl GP (2016) Persistence of coral assemblages at East and West Flower Garden Banks, Gulf of Mexico. Coral Reefs 35:821–826CrossRefGoogle Scholar
  40. Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81CrossRefGoogle Scholar
  41. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  42. Kourafalou VH, Kang H (2012) Florida Current meandering and evolution of cyclonic eddies along the Florida Keys Reef Tract: Are they interconnected? J Geophys Res Oceans 117:1–25CrossRefGoogle Scholar
  43. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8CrossRefGoogle Scholar
  44. Locker SD, Armstrong RA, Battista TA, Rooney JJ, Sherman C, Zawada DG (2010) Geomorphology of mesophotic coral ecosystems: current perspectives on morphology, distribution, and mapping strategies. Coral Reefs 29:329–345CrossRefGoogle Scholar
  45. Lugo-Fernández A (1998) Ecological implications of hydrography and circulation to the Flower Garden Banks, northwest Gulf of Mexico. Gulf of Mexico Sci 16:144–160CrossRefGoogle Scholar
  46. 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
  47. Nunes FLD, Norris RD, Knowton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18:4283–4297CrossRefPubMedGoogle Scholar
  48. Oey L, Ezer T, Lee H (2005) Loop Current, rings and related circulation in the Gulf of Mexico: a review of numerical models and future challenges. In: Sturges W, Lugo-Fernandez A (eds) Circulation in the Gulf of Mexico: observations and models. American Geophysical Union, Washington, DC, pp 31–56Google Scholar
  49. Palumbi SR (2003) Population genetics, demography connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  50. Pan C, Jiang M, Dalgleish FR, Reed JK (2017) Modeling the impacts of the Loop Current on circulation and water properties over the Pulley Ridge region on the Southwest Florida shelf. Ocean Model 112:48–64CrossRefGoogle Scholar
  51. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  52. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pochon X, Forsman ZH, Spalding HL, Padilla-Gamiño JL, Smith CM, Gates RD (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawai‘i. R Soc Open Sci 2:140351CrossRefPubMedPubMedCentralGoogle Scholar
  54. Porto-Hannes I, Zubillaga AL, Shearer TL, Bastidas C, Salazar C, Coffroth MA, Szmant AM (2015) Population structure of the corals Orbicella faveolata and Acropora palmata in the Mesoamerican Barrier Reef System with comparisons over Caribbean basin-wide spatial scale. Mar Biol 162:81–98CrossRefGoogle Scholar
  55. Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci 110:3961–3966CrossRefPubMedGoogle Scholar
  56. Precht WF, Deslarzes KJP, Hickerson EL, Schmahl GP, Nuttall MF, Aronson RB (2014) Back to the future: the history of acroporid corals at the Flower Garden Banks, Gulf of Mexico, USA. Mar Geol 349:152–161CrossRefGoogle Scholar
  57. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  58. Puglise KA, Hinderstein LM, Marr J, Dowgiallo MJ, Martinez FA (2009) Mesophotic coral ecosystems research strategy: international workshop to prioritize research and management needs for mesophotic coral ecosystems, Jupiter, Florida, 12–15 July 2008. NOAA National Centers for Coastal Ocean Science, Center for Sponsored Coastal Ocean Research, and Office of Ocean Exploration and Research, NOAA Undersea Research Program. NOAA Technical Memorandum NOS NCCOS 98 and OAR OER 2, Silver Spring, MD, p 24Google Scholar
  59. Reed J, Farrington S, David A, Harter S, Moe H, Horn L, Taylor G, White J, Voss JD, Pomponi S, Hanisak D (2017) Characterization of mesophotic coral/sponge habitats and fish assemblages in the regions of Pulley Ridge and Tortugas from ROV dives during R/V Walton Smith cruises of 2012 to 2015. NOAA CIOERT, NOAA-NOS-NCCOS, NOAA Office of Ocean Exploration and Research. Harbor Branch Oceanographic Technical Report Number 178, Fort Pierce, FL, p 76Google Scholar
  60. Rippe JP, Matz MV, Green EA, Medina M, Khawaja NZ, Pongwarin T, Pinzón CJH, Castillo KD, Davies SW (2017) Population structure and connectivity of the mountainous star coral, Orbicella faveolata, throughout the wider Caribbean region. Ecol Evol 7:9234–9246CrossRefPubMedPubMedCentralGoogle Scholar
  61. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  62. Schmahl GP, Hickerson EL, Precht WF (2008) Biology and ecology of coral reefs and coral communities in the Flower Garden Banks region, northwestern Gulf of Mexico. In: Riegl BM, Dodge RE (eds) Coral reefs of the USA. Springer, Dordrecht, NL, pp 221–261CrossRefGoogle Scholar
  63. Semmler RF, Hoot WC, Reaka ML (2016) Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs? Coral Reefs 36:433–444CrossRefGoogle Scholar
  64. Serrano XM, 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
  65. 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
  66. Sherman C, Nemeth M, Ruíz H, Bejarano I, Appeldoorn R, Pagán F, Schärer M, Weil E (2010) Geomorphology and benthic cover of mesophotic coral ecosystems of the upper insular slope of southwest Puerto Rico. Coral Reefs 29:347–360CrossRefGoogle Scholar
  67. Slattery M, Lesser MP, Brazeau DA, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Biol Ecol 408:32–41CrossRefGoogle Scholar
  68. Slattery M, Moore S, Boye L, Whitney S, Woolsey A, Woolsey M (2018) The Pulley Ridge deep reef is not a stable refugia through time. Coral Reefs 37:391–396CrossRefGoogle Scholar
  69. Stenberg P, Lundmark M, Saura A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes 3:329–331CrossRefGoogle Scholar
  70. Strimmer K (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24:1461–1462CrossRefPubMedGoogle Scholar
  71. Studivan MS, Voss JD (2018a) Assessment of mesophotic coral ecosystem connectivity for proposed expansion of a marine sanctuary in the Northwest Gulf of Mexico: population genetics. Front Mar Sci 5:152CrossRefGoogle Scholar
  72. Studivan MS, Voss JD (2018b) Data from: population connectivity among shallow and mesophotic Montastraea cavernosa corals in the Gulf of Mexico identifies potential for refugia. Dryad Digit Repos.  https://doi.org/10.5061/dryad.tj146fn CrossRefGoogle Scholar
  73. Tang L, Sheng J, Hatcher BG, Sale PF (2006) Numerical study of circulation, dispersion, and hydrodynamic connectivity of surface waters on the Belize shelf. J Geophys Res 111:C01003Google Scholar
  74. van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256CrossRefGoogle Scholar
  75. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660CrossRefPubMedGoogle Scholar
  76. 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. Cont Shelf Res 125:136–146CrossRefGoogle Scholar
  77. 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
  78. Voss JD, Williams MA, Reed JK, Clark R (2014) Benthic and fish communities in the mid and lower mesphotic zone of the sanctuary. In: Clark R, Taylor JC, Buckel CA, Kracker LM (eds) Fish and benthic communities of the Flower Garden Banks National Marine Sanctuary: science to support sanctuary management. NOAA Technical Memorandum NOS NCCOS 179, Silver Spring, MD, pp 201–260Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Florida Atlantic UniversityHarbor Branch Oceanographic InstituteFort PierceUSA

Personalised recommendations