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.
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
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
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
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
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
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
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
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
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
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
Chornesky E, Peters E (1987) Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Biol Bull 172:161–177
Collingham Y, Huntley B (2000) Impacts of habitat fragmentation and patch size upon migration rates. Ecol Appl 10:131–144
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
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
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
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
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
Freeman LC (1977) A set of measures of centrality based on betweenness. Sociometry 40:35–41
Gardner T, Côté IM, Gill J, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Gleason DF (1993) Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol Oceanogr 38:1452–1463
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
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
Gleason DF, Danilowicz BS, Nolan CJ (2009) Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals. Coral Reefs 28:549–554
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 1:177–509
Goldberg W (1983) Cay Sal Bank: a biologically impoverished physically controlled environment. Atoll Res Bull 271:1–36
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
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
Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature 404:755–758
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
Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407
Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263
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
Johnson DB (1977) Efficient algorithms for shortest paths in sparse networks. Journal of the Association for Computing Machinery 24:1–13
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
Kough AS, Paris CB (2015) The influence of spawning periodicity on population connectivity. Coral Reefs. doi:10.1007/s00338-015-1311-1
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
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8
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
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
Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Rev Biol Trop 56:11–24
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
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
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
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422
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
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
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
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
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
Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531
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
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
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
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
Szmant A (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54
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
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
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
Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66
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
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
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
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
Wellington GM, Fitt WK (2003) Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals. Mar Biol 143:1185–1192
West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ecology Editor Dr. Michael Berumen
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-015-1339-2