Abstract
Following major stress events such as storms, bleaching events, or disease outbreaks, surviving corals must regenerate tissue to recover. We aimed to understand how this recovery changes across depth, hypothesizing that deeper corals would regenerate more slowly and that this may limit resilience to acute stressors. Two species of reef-building coral, Orbicella franksi (an intermediate-depth species) and Agaricia lamarcki (a depth-generalist), were tagged at selected sites across their overlapping depth range of 13–41 m and directly monitored for recovery from experimentally generated lesions across time. Overall, recovery rates were distinct between species and across depths, with O. franksi recovery rates showing high variability and declining at depth. In contrast, A. lamarcki maintained similar rates of recovery across the examined depth range. The consistent response of A. lamarcki suggests that it can attenuate its biology with changing light resources to maintain healing abilities in different environments. Recovery rates were additionally compared against environmental and biological covariates and it was found that only increased initial lesion size had a significant positive effect on tissue regeneration rates for A. lamarcki. Collectively, this suggests that some mesophotic coral reefs, despite having high coral cover, may be slower to recover from stress events if dominated by non-depth-generalist species, such as O. franksi, resulting in increased vulnerability to repeated stress events.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All DNA sequence data collected during this study is available in Genbank. Remaining datasets generated and analyzed during the current study are included in this publication [and its supplementary information files.
References
Bongaerts P, Frade PR, Ogier JJ, Hay KB, Van Bleijswijk J, Englebert N, 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 Evolutionary Biology. https://doi.org/10.1186/1471-2148-13-205
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. Scientific Reports. https://doi.org/10.1038/srep07652
Booij N, Ris RC, Holthuijsen LH (1999) A third-generation wave model for coastal regions, Part I, model description and validation. Journal of Geophysical Research C4(104):7649–7666
Brandt ME, Ennis RS, Meiling SS, Townsend J, Cobleigh K, Glahn A, Quetel J, Brandtneris V, Henderson LM, Smith TB (2021) The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Frontiers in Marine Science 8:715329. https://doi.org/10.3389/fmars.2021.715329
Cairns SD (1982) Stony corals (Cnidaria: Hydrozoa, Scleractinia) of Carrie Bow Cay, Belize. Smithsonian Contributions to the Marine Sciences. https://doi.org/10.1002/iroh.19840690135
Carilli J, Donner SD, Hartmann AC (2012) Historical temperature variability affects coral response to heat stress. PLoS ONE 7(3):1–9. https://doi.org/10.1371/journal.pone.0034418
Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek CJ, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzman HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Palidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AR, Sanciango J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321(5888):560–563. https://doi.org/10.1126/science.1159196
Chaves-Fonnegra A, Panassiti B, Smith TB, Brown E, Clemens E, Sevier M, Brandt ME (2021) Environmental and biological drivers of white plague disease on shallow and mesophotic coral reefs. Ecography. https://doi.org/10.1111/ecog.05527
Counsell CWW, Johnston EC, Sale TL (2019) Colony size and depth affect wound repair in a branching coral. Marine Biology. https://doi.org/10.1007/s00227-019-3601-6
Crandall JB, Teece MA, Estes BA, Manfrino C, Ciesla JH (2016) Nutrient acquisition strategies in mesophotic hard corals using compound specific stable isotope analysis of sterols. Journal of Experimental Marine Biology and Ecology 474:133–141. https://doi.org/10.1016/j.jembe.2015.10.010
Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecology Letters 15:1378–1386. https://doi.org/10.1111/j.1461-0248.2012.01861.x
Dollar SJ (1982) Wave stress and coral community structure in Hawaii. Coral Reefs 1(2):71–81
Dustan P (1975) Growth and form in the reef-building coral Montastrea annularis. Marine Biology 33(2):101–107. https://doi.org/10.1007/BF00390714
Egan KE, Viehman TS, Holstein DM, Poti M, Groves SH, Smith TB (2021) Predicting the distribution of threatened orbicellid corals in shallow and Mesophotic reef ecosystems. Marine Ecology Progress Series 667:61–81. https://doi.org/10.3354/meps13698
Enríquez S, Méndez ER, -Prieto, R. I. (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnology and Oceanography 50(4):1025–1032. https://doi.org/10.4319/lo.2005.50.4.1025
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50(2):125–146. https://doi.org/10.1016/j.marpolbul.2004.11.028
Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Marine Ecology Progress Series 234:119–125
Fisher EM, Fauth JE, Hallock P, Woodley CM (2007) Lesion regeneration rates in reef-building corals Montastraea spp. as indicators of colony condition. Marine Ecology Progress Series 339:61–71. https://doi.org/10.3354/meps339061
Groves SH, Holstein DM, Enochs IC, Kolodzeij G, Manzello DP, Brandt ME, Smith TB (2018) Growth rates of Porites astreoides and O. franksi in mesophotic habitats surrounding St. Thomas US Virgin Islands. Coral Reefs 37:345–354
Hall VR (1997) Interspecific differences in the regeneration of artificial injuries on scleractinian corals. Journal of Experimental Marine Biology and Ecology 212(1):9–23. https://doi.org/10.1016/S0022-0981(96)02760-8
Helmuth B, Sebens K (1993) The influence of colony morphology and orientation to flow on particle capture by the scleractinian coral Agaricia agaricites (Linnaeus). Journal of Experimental Marine Biology and Ecology 165(2):251–278
Henry L-A, Hart M (2005) Regeneration from Injury and resource allocation in sponges and corals—a Review. Internaltional Review of Hydrobiology 90(2):125–158. https://doi.org/10.1002/iroh.200410759
Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic Coral Ecosystems: Characterization Ecology and Management”. Coral Reefs 29(2):247–251. https://doi.org/10.1007/s00338-010-0614-5
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318(5857):1737–1742. https://doi.org/10.1126/science.1152509
Holstein DM, Paris CB, Vaz AC, Smith TB (2016) Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35(1):23–37. https://doi.org/10.1007/s00338-015-1339-2
Kramarsky-Winter, E, Loya Y (2000) Tissue regeneration in the coral Fungia granulosa: the effect of extrinsic and intrinsic factors. Marine Biology 867–873. Retrieved from http://link.springer.com/article/https://doi.org/10.1007/s002270000416
Laverick JH, Andradi-Brown DA, Rogers AD (2017) Using light-dependent scleractinia to define the upper boundary of mesophotic coral ecosystems on the reefs of Utila Honduras. PLOS ONE 12(8):e0183075. https://doi.org/10.1371/journal.pone.0183075
Laverick JH, Piango S, Andradi-Brown DA, Exton DA, Bongaerts P, Bridge TCL, Lesser MP, Pyle RL, Slattery M, Wagner D, Rogers AD (2018) To what extent do mesophotic coral ecosystems and shallow reefs share species of conservation interest? A systematic review. Environmental Evidence 7:15
Laverick JH, Green TK, Burdett HL, Newton J, Rogers AD (2019) Depth alone is an inappropriate proxy for physiological change in the mesophotic coral Agaricia lamarcki. Journal of the Marine Biological Association of the United Kingdom 99(7):1535–1546. https://doi.org/10.1017/S0025315419000547
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. Journal of Experimental Marine Biology Ecology 375(1–2):1–8
Loya Y (1976) Skeletal regeneration in a Red Sea scleractinian coral population. Nature 261(5560):490–491
Lugo-Fernández A, Gravois M (2010) Understanding impacts of tropical storms and hurricanes on submerged bank reefs and coral communities in the northwestern Gulf of Mexico. Continental Shelf Research 30(10–11):1226–1240. https://doi.org/10.1016/j.csr.2010.03.014
Meesters E, Wesseling I, Bak RPM (1996) Partial mortality in three species of reef-building corals and the relation with colony morphology. Bulletin of Marine Science 58(3):838–852
Meesters EH, Bak RPM (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. Marine Ecology Progress Series 96(2), 189–198. Retrieved from http://www.jstor.org/sTable/24833544
Meesters EH, Noordeloos M, Bak RPM (1994) Damage and regeneration: links to growth in the reef-building coral Montastrea annularis. Marine Ecology Progress Series 112(1/2), 119–128. Retrieved from http://www.jstor.org.ezaccess.libraries.psu.edu/sTable/24847643
Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecological Economics 29(2):215–233. https://doi.org/10.1016/S0921-8009(99)00009-9
Nagelkerken I, Meesters EH, Bak RPM (1999) Depth-related variation in regeneration of artificial lesions in the Caribbean corals Porites astreoides and Stephanocoenia michelinii. Journal of Experimental Marine Biology and Ecology 234(1):29–39. https://doi.org/10.1016/S0022-0981(98)00147-6
NOAA, (2016). “Coral laceration regeneration assay”. Coral disease & health consortium. https://cdhc.noaa.gov/education/coral_assay.aspx. Accessed 16 March 2016
Oren U, Benayahu Y, Loya Y (1997) Effect of lesion size and shape on regeneration of the red sea coral Faviafavus. Marine Ecology Progress Series 146:101–107
Plaisance L, Caley MJ, Brainard RE, Knowlton N (2011) The diversity of coral reefs: What are we missing? PLoS ONE. https://doi.org/10.1371/journal.pone.0025026
Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical pacific and the red sea. Marine Ecology Progress Series 60:185–203
Ruiz-Diaz CP, Toledo-Hernandez C, Mercado-Molina AE, Pérez ME, Sabat AM (2016) The role of coral colony health state in the recovery of lesions. PeerJ 2016(1):1–13. https://doi.org/10.7717/peerj.1531
Sabine AM, Smith TB, Williams DE, Brandt ME (2015) Environmental conditions influence tissue regeneration rates in scleractinian corals. Marine Pollution Bulletin 95(1):253–264. https://doi.org/10.1016/j.marpolbul.2015.04.006
Smith TB, Blondeau J, Nemeth RS, Pittman SJ, Calnan JM, Kadison E, Gass J (2010) Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the hind bank marine conservation district US Virgin Islands. Coral Reefs 29(2):289–308. https://doi.org/10.1007/s00338-009-0575-8
Smith TB, Brandtneris VW, Canals M, Brandt ME, Martens J, Brewer RS, Holstein DM (2016a) Potential structuring forces on a shelf edge upper mesophotic coral ecosystem in the US Virgin Islands. Frontiers in Marine Science. https://doi.org/10.3389/fmars.2016.00115
Smith TB, Gyory J, Brandt ME, Miller WJ, Jossart J, Nemeth RS (2016b) Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Global Change Biology 22(8):2756–2765. https://doi.org/10.1111/gcb.13175
Smith TB, Brandt ME, Brandtneris VW, Ennis RS, Groves SH, Habtes S, Holstein DM, Kadison E, Nemeth RS (2019a) Disturbance in mesophotic coral ecosystems and linkages to conservation and management. In: Loya Y, Puglise KA, Bridge T (eds) Coral reefs of the world: mesophotic coral ecosystems. Springer, Berlin
Smith TB, Brandt ME, Brandtneris VW, Ennis RS, Groves SH, Habtes S, Holstein DM, Kadison E, Nemeth RS (2019b) The United States Virgin Islands. In: Loya Y, Puglise KA, Bridge T (eds) Coral reefs of the world: mesophotic coral ecosystems. Springer, Berlin
Smith TB, Ennis RS, Kadison E, Weinstein DW, Jossart J, Gyory J, Henderson L (2015) The United States Virgin Islands territorial coral reef monitoring program. p. 288 Year 15 Annual Report
Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5(1):43–53
Tamir R, Eyal G, Kramer N, Laverick JH, Loya Y (2019) Light environment drives the shallow-to-mesophotic coral community transition. Ecosphere 10:e02839
Terán E, Méndez ER, Enríquez S, Iglesias-Prieto R (2010) Multiple light scattering and absorption in reef-building corals. Applied Optics 49(27):5032–5042. https://doi.org/10.1364/AO.49.005032
Todd PA (2008) Morphological plasticity in scleractinian corals. Biological Reviews 83(3):315–337. https://doi.org/10.1111/j.1469-185X.2008.00045.x
Van Moorsel G (1983) Reproductive strategies in two closely related stony corals (Agaricia, Scleractinia). Marine Ecology Progress Series 13:273–283. https://doi.org/10.3354/meps013273
Weinstein DK, Sharifi A, Klaus JS, Smith TB, Giri SJ, Helmle KP (2016) Coral growth, bioerosion, and secondary accretion of living orbicellid corals from mesophotic reefs in the US Virgin Islands. Marine Ecology Progress Series 559:45–63. https://doi.org/10.3354/meps11883
Acknowledgements
The authors would like to acknowledge the funding support from the following entities: The National Oceanic and Atmospheric Administration (NOAA), The Black Coral Penalty Fund, the Wottowa Fund, the Lana Vento Charitable Trust, and The National Science Foundation. The authors would like to acknowledge the contribution and efforts by members of the Smith Lab for completion of fieldwork: Kyle Jerris, Rosmin Ennis, Viktor Brandtneris, Sarah Heidmann, and Kristen Ewen. The authors would also like to acknowledge members of the Baums lab and Lajeunesse lab for their assistance and insight into laboratory analysis and technique. Additionally authors acknowledge the support from the University of the Virgin Islands Masters of Marine and Environmental Sciences cohort of 2017, as well as family, dear friends, and pets who have all supported the completion of this work whenever and however possible. All views expressed are those of the authors and do not necessarily reflect the views of the granting agencies and support personnel. This is contribution 262 from the Center for Marine and Environmental Science, University of the Virgin Islands
Funding
This work was funded by the US Virgin Islands Territorial Coral Reef Monitoring Program (GC021PNR15/NA17NOS4820033), the Black Coral Penalty Fund, the Wottowa Fund, the Lana Vento Charitable Trust, the NSF INCLUDES Supporting Emerging Aquatic Scientists (SEAS) Islands Alliance (NSF Award #1930991), and the VI Established Program to Stimulate Competitive Research (NSF Award #1355437).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, field data collection were completed by JET and TBS. Computational data collection was completed by SM. Data analysis was performed by JET and MB. The first draft of the manuscript was written by JET and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose. On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Townsend, J.E., Brandt, M.E., Mukherjee, S. et al. Differing lesion recovery rates of two Caribbean stony coral species across a shallow water to mesophotic depth gradient suggest different sensitivity to repeated disturbance. Coral Reefs 42, 1067–1077 (2023). https://doi.org/10.1007/s00338-023-02414-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-023-02414-3