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Modeling vertical coral connectivity and mesophotic refugia

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Abstract

Whether mesophotic reefs will behave as refugia for corals threatened by global climate change and coastal development depends on vertical exchange of larvae between diverse habitats. Here we use a biophysical model of larval dispersal to estimate vertical connectivity of a broadcasting (Orbicella faveolata) and a brooding (Porites astreoides) species of coral in the US Virgin Islands. Modeling predicts subsidy to shallow areas by mesophotic larvae of both species based on local hydrology, adult reproductive characteristics, larval traits, and a wide range of scenarios developed to test depth-sensitive factors, such as fertilization rates and post-settlement survivorship. In extreme model scenarios of reduced fertilization and post-settlement survivorship of mesophotic larvae, 1–10 % local mesophotic subsidy to shallow recruitment is predicted for both species, which are demographically significant. Although direct vertical connectivity is higher for the broadcaster, the brooder demonstrates higher local multigenerational vertical connectivity, which suggests that local P. astreoides populations are more resilient than those of O. faveolata, and corroborates field studies. As shallow habitat degrades, mesophotic–shallow subsidy is predicted to increase for both species. This study is the first of its kind to simulate larval dispersal and settlement between habitats of different depths, and these findings have local, regional, and global implications for predicting and managing coral reef persistence in a changing climate.

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References

  • Babcock R, Mundy C, Whitehead D (1994) Sperm diffusion models and in situ confirmation of long-distance fertilization in the free- spawning asteroid Acanthaster planci. Biol Bull 186:17–28

    Article  Google Scholar 

  • Bak R, Nieuwland G, Meesters E (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curacao and Bonaire. Coral Reefs 24:475–479

    Article  Google Scholar 

  • Baums IB, Paris CB, Cherubin LM, Che LM (2006) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnol Oceanogr 51:1969–1981

    Article  Google Scholar 

  • Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010a) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327

    Article  Google Scholar 

  • 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:e10871

    Article  PubMed Central  PubMed  Google Scholar 

  • Bongaerts P, Riginos C, Hay KB, van Oppen MJ, Hoegh-Guldberg O, Dove S (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol Biol 11:303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bongaerts P, Frade PR, Ogier JJ, Hay KB, van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, 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 13:205

    Article  PubMed Central  PubMed  Google Scholar 

  • Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KRW, Bak RPM, Vermeij MJ, Hoegh-Guldberg O (2015) Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep 5:7652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Botsford LW, White JW, Coffroth MA, Paris CB, Planes S, Shearer TL, Thorrold SR, Jones GP (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28:327–337

    Article  PubMed Central  PubMed  Google Scholar 

  • Cherubin LM, Nemeth RS, Idrisi N (2011) Flow and transport characteristics at an Epinephelus guttatus (red hind grouper) spawning aggregation site in St. Thomas (US Virgin Islands). Ecol Modell 222:3132–3148

    Article  Google Scholar 

  • Chornesky E, Peters E (1987) Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Biol Bull 172:161–177

    Article  Google Scholar 

  • Collingham Y, Huntley B (2000) Impacts of habitat fragmentation and patch size upon migration rates. Ecol Appl 10:131–144

    Article  Google Scholar 

  • Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecol Monogr 77:3–18

    Article  Google Scholar 

  • Edmunds PJ, Gates RD, Gleason DF (2001) The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar Biol 139:981–989

    Article  Google Scholar 

  • Edmunds PJ, Ross CLM, Didden C (2011) High, but localized recruitment of Montastraea annularis complex in St. John, United States Virgin Islands. Coral Reefs 30:123–130

    Article  Google Scholar 

  • Foster NL, Baums IB, Sanchez JA, Paris CB, Chollett I, Agudelo CL, Vermeij MJA, Mumby PJ (2013) Hurricane-Driven Patterns of Clonality in an Ecosystem Engineer: The Caribbean Coral Montastraea annularis. PLoS One 8:e53283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 21:1143–1157

    Article  PubMed  Google Scholar 

  • Freeman LC (1977) A set of measures of centrality based on betweenness. Sociometry 40:35–41

    Article  Google Scholar 

  • Gardner T, Côté IM, Gill J, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    Article  CAS  PubMed  Google Scholar 

  • Gleason DF (1993) Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol Oceanogr 38:1452–1463

    Article  Google Scholar 

  • Gleason DF, Wellington GM (1995) Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar Biol 123:693–703

    Article  Google Scholar 

  • Gleason DF, Edmunds PJ, Gates RD (2005) Ultraviolet radiation effects on the behavior and recruitment of larvae from the reef coral Porites astreoides. Mar Biol 148:503–512

    Article  Google Scholar 

  • Gleason DF, Danilowicz BS, Nolan CJ (2009) Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals. Coral Reefs 28:549–554

    Article  Google Scholar 

  • Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 1:177–509

    Google Scholar 

  • Goldberg W (1983) Cay Sal Bank: a biologically impoverished physically controlled environment. Atoll Res Bull 271:1–36

    Article  Google Scholar 

  • Green DH, Edmunds PJ (2011) Spatio-temporal variability of coral recruitment on shallow reefs in St. John, US Virgin Islands. J Exp Mar Bio Ecol 397:220–229

    Article  Google Scholar 

  • Green D, Edmunds P, Carpenter R (2008) Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Mar Ecol Prog Ser 359:1–10

    Article  Google Scholar 

  • Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature 404:755–758

    Article  CAS  PubMed  Google Scholar 

  • Holstein DM (2013) Vertical connectivity in mesophotic coral ecosystems. Ph.D. thesis, University of Miami, FL, USA

  • Holstein DM, Paris CB, Mumby PJ (2014) Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Mar Ecol Prog Ser 499:1–18

    Article  Google Scholar 

  • Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Article  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  CAS  PubMed  Google Scholar 

  • Johnson DB (1977) Efficient algorithms for shortest paths in sparse networks. Journal of the Association for Computing Machinery 24:1–13

    Article  Google Scholar 

  • Kendall MS, Monaco ME, Buja KR, Christensen JD, Kruer CR, Finkbeiner M, Warner RA (2001) Methods used to map the benthic habitats of Puerto Rico and the U.S. Virgin Islands. U.S. National Oceanic and Atmospheric Administration. National Ocean Service, National Centers for Coastal Ocean Science Biogeography Program, Silver Spring, MD. 46 pp

  • Kool JT, Nichol SL (2015) Four-dimensional connectivity modelling with application to Australia’s north and northwest marine environments. Environ Model Softw 65:67–78

    Article  Google Scholar 

  • Kough AS, Paris CB (2015) The influence of spawning periodicity on population connectivity. Coral Reefs. doi:10.1007/s00338-015-1311-1

    Google Scholar 

  • Lasker HRH, Brazeau D, Calderon J, Coffroth MA, Coma R, Kim K (1996) In situ rates of fertilization among broadcast spawning gorgonian corals. Biol Bull 190:45–55

    Article  Google Scholar 

  • Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8

    Article  Google Scholar 

  • Levitan D, Fukami H, Jara J, Kline D, McGovern T (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution (N Y) 58:308–323

    Google Scholar 

  • Locker SD, Armstrong R, Battista T, Rooney JJ, Sherman C, Zawada DG (2010) Geomorphology of mesophotic coral ecosystems: current perspectives on morphology, distribution, and mapping strategies. Coral Reefs 29:329–345

    Article  Google Scholar 

  • Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Rev Biol Trop 56:11–24

    Google Scholar 

  • Miller MW, Weil E, Szmant AM (2000) Coral recruitment and juvenile mortality as structuring factors for reef benthic communities in Biscayne National Park, USA. Coral Reefs 19:115–123

    Article  Google Scholar 

  • Mumby PJ, Elliott IA, Eakin CM, Skirving W, Paris CB, Edwards HJ, Enríquez S, Iglesias-Prieto R, Cherubin LM, Stevens JR (2011) Reserve design for uncertain responses of coral reefs to climate change. Ecol Lett 14:132–140

    Article  PubMed  Google Scholar 

  • NOAA (2014) Endangered and threatened wildlife and plants: final listing determinations on proposal to list 66 reef-building coral species and to reclassify elkhorn and staghorn corals: Federal Register 79(175). National Oceanic and Atmospheric Administration. Office of the Federal Register, National Archives and Records Administration

  • Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–417

    Article  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  PubMed  Google Scholar 

  • Paris C, Chérubin L, Cowen R (2007) Surfing, spinning, or diving from reef to reef: effects on population connectivity. Mar Ecol Prog Ser 347:285–300

    Article  Google Scholar 

  • Paris CB, Cowen RK, Claro R, Lindeman KC (2005) Larval transport pathways from Cuban snapper (Lutjanidae) spawning aggregations based on biophysical modeling. Mar Ecol Prog Ser 296:93–106

    Article  Google Scholar 

  • 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. Environ Model Softw 42:47–54

    Article  Google Scholar 

  • Paris CB, Le Hénaff M, Aman ZM, Subramaniam A, Helgers J, Wang D-P, Kourafalou VH, Srinivasan A (2012) Evolution of the Macondo well blowout: simulating the effects of the circulation and synthetic dispersants on the subsea oil transport. Environ Sci Technol 46:13293–13302

    Article  CAS  PubMed  Google Scholar 

  • Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci USA 110:3961–3966

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531

    Article  Google Scholar 

  • Rivera JA, Prada MC, Arsenault JL, Moody G, Benoit N (2006) Detecting fish aggregations from reef habitats mapped with high resolution side scan sonar imagery. Professional Paper NMFS 88–104

  • 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 23:4226–4240

    Article  CAS  PubMed  Google Scholar 

  • Shchepetkin AF, McWilliams JC (2005) The regional oceanic modeling system (ROMS): a split-explicit, free-surface, topography-following-coordinate oceanic model. Ocean Modelling 9:347–404

    Article  Google Scholar 

  • Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 408:32–41

    Article  Google Scholar 

  • Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb S (2008) Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Mar Pollut Bull 56:1983–1991

    Article  CAS  PubMed  Google Scholar 

  • Szmant A (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54

    Article  Google Scholar 

  • Szmant AM, Meadows MG (2006) Developmental changes in coral larval buoyancy and vertical swimming behavior: Implications for dispersal and connectivity. Proc 10th Int Coral Reef Symp 1:431–437

    Google Scholar 

  • Szmant AM, Weil E, Miller MW, Colon DE (1997) Hybridization within the species complex of the scleractinian coral Montastraea annularis. Mar Biol 129:561–572

    Article  Google Scholar 

  • Tay YC, Guest JR, Chou LM, Todd P (2011) Vertical distribution and settlement competencies in broadcast spawning coral larvae: Implications for dispersal models. J Exp Mar Bio Ecol 409:324–330

    Article  Google Scholar 

  • Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  • Treml EA, Halpin PN, Urban DL, Pratson LF (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landsc Ecol 23:19–36

    Article  Google Scholar 

  • Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Article  CAS  PubMed  Google Scholar 

  • 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 20:1647–1660

    Article  PubMed  Google Scholar 

  • 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 310:119–128

    Article  Google Scholar 

  • Wellington GM, Fitt WK (2003) Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals. Mar Biol 143:1185–1192

    Article  CAS  Google Scholar 

  • West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967

    Article  Google Scholar 

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Acknowledgments

Research was supported by the National Science Foundation (NSF OCE-0928423 to CBP), Natural Environment Research Council (Exeter University partially supported DMH, under subcontract to CBP) and NOAA (NOAA-Pulley Ridge to CBP supported ACV).

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Correspondence to Daniel M. Holstein.

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Communicated by Ecology Editor Dr. Michael Berumen

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Holstein, D.M., Paris, C.B., Vaz, A.C. et al. Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35, 23–37 (2016). https://doi.org/10.1007/s00338-015-1339-2

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