Mesophotic coral refuges following multiple disturbances

Coral Reefs (2021)Cite this article

Abstract

As coral populations on shallow reefs decline globally, mesophotic coral ecosystems (MCE) have been proposed as potential coral refugia from thermal, storm, and anthropogenic disturbances in the face of climate change. The current study assesses the refuge potential of MCEs in the U.S. Virgin Islands (USVI) for Montastraea cavernosa by extrapolating reproductive potential through depth-stratified coral loss following regional storm, disease, and bleaching perturbations. Fecundity of this depth-generalist coral from 4 to 40 m was measured histologically, and polyp, population, and total habitat fecundities were then extrapolated across the species’ depth range. The number of reproductively active female gonads per polyp and oocyte size experienced a significant, though small, decrease with depth, potentially due to energetic limitations. Notably, the population sex ratio was not different from 1:1 on shallow and mid-depth reefs, but it became significantly male-biased (3.6:1) at mesophotic depths. Population-level differences in oocyte production over depth were primarily driven by changes in coral cover and sex ratio. The large spatial extent of mesophotic reefs relative to shallow reefs in the USVI makes MCEs the primary contributor of oocytes, despite the reduced proportion of females at depth. Following Hurricanes Irma and Maria in 2017, the outbreak of Stony Coral Tissue Loss Disease in 2019, and a bleaching event in 2019, shallow and mid-depth M. cavernosa populations experienced severe coral cover declines. Shallow and mid-depth population fecundities were predicted to decline correspondingly. Coral cover in MCEs remained relatively stable following these largely shallow water perturbations, and predicted population and total habitat fecundities remained constant as well. Thus, MCEs in the USVI currently appear to be reproductive refuges for M. cavernosa, but the persistence of that refuge remains in question as disease perturbation begins to affect deeper reefs.

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References

  1. Acosta A, Zea S (1997) Sexual reproduction of the reef coral Montastraea cavernosa (Scleractinia: Faviidae) in the Santa Marta area, Caribbean coast of Colombia. Mar Biol 128:141–148

    Article  Google Scholar 

  2. Aeby GS, Ushijima B, Campbell JE, Jones S, Williams GJ, Meyer JL, Häse C, Paul VJ (2019) Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front Mar Sci 6:678

    Article  Google Scholar 

  3. Arai I, Kato M, Heyward A, Ikeda Y, Iizuka T, Maruyama T (1993) Lipid composition of positively buoyant eggs of reef building corals. Coral Reefs 12:71–75

    Article  Google Scholar 

  4. Babcock RC, Mundy CN, 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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  5. 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 24:475–479

    Article  Google Scholar 

  6. Benayahu Y, Loya Y (1983) Surface brooding in the Red Sea soft coral Parerythropodium fulvum (Forskål, 1775). Biol Bull 165:353–369

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. Bongaerts P, Smith TB (2019) Beyond the “Deep Reef Refuge” Hypothesis: a conceptual framework to characterize persistence at depth. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 881–895

    Google Scholar 

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

    Article  Google Scholar 

  9. 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. https://doi.org/10.1126/sciadv.1602373

    Article  PubMed  PubMed Central  Google Scholar 

  10. Brazeau DA, Lasker HR (1990) Sexual reproduction and external brooding by the Caribbean gorgonian Briareum asbestinum *. Mar Biol 104:465–474

    Article  Google Scholar 

  11. Budd AF, Nunes FLD, Weil E, Pandolfi JM (2012) Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications. Evol Ecol 26:265–290

    Article  Google Scholar 

  12. Cerrano C, Arillo A, Azzini F, Calcinai B, Castellano L, Mutt C, Valisano L, Zego G, Bavestrelloa G (2005) Gorgonian population recovery after a mass mortality event. Aquat Conserv Mar Freshw Ecosyst 15:147–157

    Article  Google Scholar 

  13. Costa B, Kracker LM, Battista T, Sautter W, Mabrouk A, Edwards K, Taylor C, Ebert E. (2017) Benthic Habitat Maps for the Insular Shelf South of St. Thomas and St. John. NOAA Technical Memorandum NOS NCCOS 241, Silver Spring, MD, pp 59

  14. 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 36:913–925

    Article  Google Scholar 

  15. Day T, Nagel L, Van Oppen MJH, Caley MJ (2008) Factors affecting the evolution of bleaching resistance in corals. Am Nat 171:E72–E88

    PubMed  Article  PubMed Central  Google Scholar 

  16. Edmunds PJ (2019) The demography of hurricane effects on two coral populations differing in dynamics. Ecosphere 10:e02836

    Article  Google Scholar 

  17. Feldman B, Shlesinger T, Loya Y (2018) Mesophotic coral-reef environments depress the reproduction of the coral Paramontastraea peresi in the Red Sea. Coral Reefs 37:201–214

    Article  Google Scholar 

  18. FKNMS/DEP (2018) Case Definition: Stony Coral Tissue Loss Disease (SCTLD).

  19. Foster NL, Baums IB, Mumby PJ (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76:384–391

    PubMed  Article  PubMed Central  Google Scholar 

  20. Frade PR, Reyes-Nivia MC, Faria J, Kaandorp JA, Luttikhuizen PC, Bak RPM (2010) Semi-permeable species boundaries in the coral genus Madracis: introgression in a brooding coral system. Mol Phylogenet Evol 57:1072–1090

    CAS  PubMed  Article  Google Scholar 

  21. Gintert BE, Precht WF, Fura R, Rogers K, Rice M, Precht LL, D’Alessandro M, Croop J, Vilmar C, Robbart ML (2019) Regional coral disease outbreak overwhelms impacts from a local dredge project. Environ Monit Assess 191:630

    PubMed  Article  Google Scholar 

  22. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509

    Article  Google Scholar 

  23. Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141:39–46

    Article  Google Scholar 

  24. Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar Ecol Prog Ser 346:89–96

    CAS  Article  Google Scholar 

  25. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 59–85

    Google Scholar 

  26. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    CAS  PubMed  Article  Google Scholar 

  27. Holland G, Bruyère CL (2014) Recent intense hurricane response to global climate change. Clim Dyn 42:617–627

    Article  Google Scholar 

  28. Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:1–12

    Article  CAS  Google Scholar 

  29. Holstein DM, Paris CB, Vaz AC, Smith TB (2016a) Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35:23–37

    Article  Google Scholar 

  30. Holstein DM, Smith TB, Paris CB (2016b) Depth-independent reproduction in the reef coral Porites astreoides from shallow to mesophotic zones. PLoS ONE 11:e0146068

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JPA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. Kahng SE, Akkaynak D, Shlesinger T, Hochberg EJ, Wiedenmann J, Tamir R, Tchernov D (2019) Light, temperature, photosynthesis, heterotrophy, and the lower depth limits of mesophotic coral ecosystems. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic Coral Ecosystems. Springer, New York, pp 801–828

    Google Scholar 

  33. Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404

    Article  Google Scholar 

  34. Knutson TR, Mcbride JL, Chan J, Emanuel K, Holland G, Landsea C, Held I, Kossin JP, Srivastava AK, Sugi M (2010) Tropical cyclones and climate change. Nat Geosci 3:157–163

    CAS  Article  Google Scholar 

  35. Kobluk DR, Lysenko MA (1992) Storm features on a southern Caribbean fringing coral reef. Palaios 7:213–221

    Article  Google Scholar 

  36. Kramer PR, Roth L, Lang J (2019) Map of stony coral tissue loss disease outbreak in the Caribbean. ArcGIS Online. www.agrra.org

  37. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest Package: tests in linear mixed effects models. J Stat Softw 82:1–16

    Article  Google Scholar 

  38. Lasker HR (1979) Light dependent activity patterns among reef corals: Montastraea cavernosa. Biol Bull 156:196–211

    Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  41. Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531

    PubMed  Article  PubMed Central  Google Scholar 

  42. Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Bio Ecol 251:41–57

    CAS  Article  Google Scholar 

  43. Lunz K, Landsberg J, Kiryu Y, Brinkhuis V (2017) Investigation of the Coral Disease Outbreak Affecting Scleractinian Corals of the Florida Reef Tract. Florida DEP

  44. Marchini C, Airi V, Fontana R, Tortorelli G, Rocchi M, Falini G, Levy O, Dubinsky Z, Goffredo S (2015) Annual reproductive cycle and unusual embryogenesis of a temperate coral in the Mediterranean Sea. PLoS ONE 10:1–17

    Article  CAS  Google Scholar 

  45. Maynard J, Van Hooidonk R, Eakin CM, Puotinen M, Garren M, Williams G, Heron SF, Lamb J, Weil E, Willis B, Harvell CD (2015) Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat Clim Chang 5:688–694

    Article  Google Scholar 

  46. Meyer JL, Castellanos-Gell J, Aeby GS, Häse CC, Ushijima B, Paul VJ (2019) Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front Microbiol 10:2244

    PubMed  PubMed Central  Article  Google Scholar 

  47. Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937

    Article  Google Scholar 

  48. Muller EM, Sartor C, Alcaraz NI, van Woesik R (2020) Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front Mar Sci 7:163

    Article  Google Scholar 

  49. Polato NR, Concepcion GT, Toonen RJ, Baums IB (2010) Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol Ecol 19:4661–4677

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  50. Prasetia R, Sinniger F, Hashizume K, Harii S (2017) Reproductive biology of the deep brooding coral Seriatopora hystrix: implications for shallow reef recovery. PLoS ONE 12:1–17

    Article  CAS  Google Scholar 

  51. Precht WF, Gintert BE, Robbart ML, Fura R, Van Woesik R (2016) Unprecedented disease-related coral mortality in Southeastern Florida. Sci Rep 6:1–11

    Article  CAS  Google Scholar 

  52. Richmond RH (1987) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533

    Article  Google Scholar 

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

    Article  Google Scholar 

  54. Rinkevich B, Loya Y (1987) Variability in the pattern of sexual reproduction of the coral Stylophora pistillata at Eilat, Red Sea: a long-term study. Biol Bull 173:335–344

    Article  Google Scholar 

  55. Robbart ML, RB Aronson, KJP Deslarzes, WF Precht, L Duncan, B Zimmer, T DeMunda. (2009) Post-hurricane assessment of sensitive habitats of the Flower Garden Banks vicinity. U.S. Dept. of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans, Louisiana, OCS Study MMS 2009–032, pp 160

  56. Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P (2018) Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science 361:281–284

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. Ruiz Torres HJ (2004) Morphometric Examination of Corallite and Colony Variability in the Caribbean Coral Montastraea cavernosa. University of Puerto Rico Mayaguez

  58. 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 23:4226–4240

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  59. 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 6:21619

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Shlesinger T, Loya Y (2019) Sexual reproduction of scleractinian corals in mesophotic coral ecosystems vs. shallow reefs tom. Mesophotic Coral Ecosystems. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic Coral Ecosystems. Springer, New York, pp 653–666

    Google Scholar 

  61. Shlesinger T, Grinblat M, Rapuano H, Amit T, Loya Y (2018) Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt. Ecology 99:421–437

    PubMed  Article  Google Scholar 

  62. 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 

  63. 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

    CAS  PubMed  Article  Google Scholar 

  64. Smith TB, Gyory J, Brandt ME, Miller WJ, Jossart J, Nemeth RS (2016) Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Glob Chang Biol 22:2756–2765

    PubMed  Article  Google Scholar 

  65. Smith TB, Brandtneris VW, Canals M, Brandt ME, Martens J, Brewer RS, Kadison E, Kammann M, Keller J, Holstein DM (2016) Potential structuring forces on a shelf edge upper mesophotic coral ecosystem in the US Virgin Islands. Front Mar Sci 3:115

    Google Scholar 

  66. Smith TB, Brandt ME, Brandtneris VW, Ennis RS, Groves SH, Habtes S, Holstein DM, Kadison E, Nemeth RS (2019) The United States Virgin Islands. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 131–147

    Google Scholar 

  67. Smith TB, Holstein DM, Ennis RS (2019) Disturbance in mesophotic coral ecosystems and linkages to conservation and management. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic Coral Ecosystems. Springer, New York, pp 911–1003

    Google Scholar 

  68. Soong K (1991) Sexual reproductive patterns of shallow-water reef corals in Panama. Bull Mar Sci 49:832–846

    Google Scholar 

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

    Article  Google Scholar 

  70. Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25

    Article  Google Scholar 

  71. Szmant-Froelich A, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892

    Google Scholar 

  72. Van Veghel MLJ (1993) Multiple species spawning on Curacao reefs. Bull Mar Sci 52:1017–1021

    Google Scholar 

  73. Vargas-Angel B, Colley SB, Hoke SM, Thomas JD (2002) Sexual reproduction of Acropora cervicornis in nearshore waters off Fort Lauderdale, Florida, USA. Coral Reefs 21:25–26

    Article  Google Scholar 

  74. 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 

  75. Ward S, Harrison P, Hoegh-guldberg O (2000) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. Proc 9th Int Coral Reef Symp, 2:1123–1128

  76. Weil E, Cróquer A, Urreiztieta I (2009) Yellow band disease compromises the reproductive output of the Caribbean reef-building coral Montastraea faveolata (Anthozoa, Scleractinia). Dis Aquat Organ 87:45–55

    PubMed  Article  PubMed Central  Google Scholar 

  77. 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 

  78. Woodley JD, Chornesky EA, Clifford PA, Jackson JBC, Kaufman LS, Knowlton N, Lang JC, Pearson MP, Porter JW, Rooney MC, Rylaarsdam KW, Tunnicliffe VJ, Wahle CM, Wulff JL, Curtis ASG, Dallmeyer MD, Jupp BP, Koehl MAR, Neigel J, Sides EM (1981) Hurricane Allen’s impact on Jamaican coral reefs. Science 214:749–755

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  79. Wyers SC, Barnes HS, Smith SR (1991) Spawning of hermatypic corals in Bermuda: a pilot study. Hydrobiologia 216(217):109–116

    Article  Google Scholar 

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Acknowledgements

We thank the University of the Virgin Islands Search Center for Marine and Environmental Studies for use of their facilities and M. Brandt, T. Smith, R. Ennis, V. Brandtneris, A. Galhan, S. Heidman, and D. Mele for assistance and field support, and access to TCRMP datasets. We thank B. Green for help with laboratory histology. This study was partially supported by NSF OCE-BIO 1927277 to D Holstein.

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    Jeanne Bloomberg & Daniel M. Holstein

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Bloomberg, J., Holstein, D.M. Mesophotic coral refuges following multiple disturbances. Coral Reefs (2021). https://doi.org/10.1007/s00338-021-02087-w

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Keywords

  • Mesophotic coral ecosystems
  • Deep reef refugia hypothesis
  • Coral reproduction
  • Fecundity
  • Montastraea cavernosa