Abstract
Photosymbiotic corals inhabit depths 0–170 + m and form the foundation of coral reef ecosystems by creating complex habitats with their calcium carbonate skeletons. While well studied in shallow waters, almost nothing is known about their basic biology & ecology at depths > 60 m. Here, we report on the first measurements of skeletal density and coral calcification rates from Leptoseris spp. growing at depths of 70–111 m in Hawaii. These corals have very thin, nonporous, skeletons that are considerably denser (2.7 g cm−3) than most shallow water corals. Their calcification rates (0.042–0.085 g cm−2 yr−1) are the lowest ever reported for a photosymbiotic scleractinian coral and ~ 20–40 times lower than the dominant shallow water corals in Hawaii. Given their colony geometry, calcification rate and tissue biomass productivity (per unit area) are tightly coupled, and a constant calcification rate leads to an increasing radial extension rate with colony size. These growth parameter relationships contrast sharply with hemispheroidal colonies in shallow water. Despite their extremely low calcification rates, these corals are very productive at increasing planar area over time, which is consistent with their phototrophic strategy at depth.
This is a preview of subscription content, access via your institution.



Change history
25 September 2023
A Correction to this paper has been published: https://doi.org/10.1007/s00338-023-02421-4
References
Álvarez-Noriega M, Baird AH, Dornelas M, Madin JS, Cumbo VR, Connolly SR (2016) Fecundity and the demographic strategies of coral morphologies. Ecology 97:3485–3493
Atkinson MJ (2011) Biogeochemistry of nutrients. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 199–206
Babcock RC (1988) Age-structure, survivorship and fecundity in populations of massive corals. In: Proc 6th Int Coral Reef Symp 2:625–633
Barnes DJ, Lough JM (1993) On the nature and causes of density banding in massive coral skeletons. J Exp Mar Biol Ecol 167(1):91–108
Bongaerts P, Ridgway T, Sampayo EM et al (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327
Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KR, Bak RP, 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
Carlot J, Rouzé H, Barneche DR, Mercière A, Espiau B, Cardini U, Brandl SJ, Casey JM, Pérez-Rosales G, Adjeroud M, Hédouin L, Parravicini V (2022) Scaling up calcification, respiration, and photosynthesis rates of six prominent coral taxa. Ecol Evol 12:e8613. https://doi.org/10.1002/ece3.8613
Cooper TF, O’Leary RA, Lough JM (2012) Growth of Western Australian corals in the Anthropocene. Science 335:593–596
Cornwall CE, Comeau S, Kornder NA, Perry CT, van Hooidonk R, DeCarlo TM et al (2021) Global declines in coral reef calcium carbonate production under ocean acidification and warming. Proc Natl Acad Sci USA 118:e2015265118
Crossland CJ (1984) Seasonal variations in the rates of calcification and productivity in the coral Acropora formosa on a high-latitude reef. Mar Ecol Prog Ser 15:135–140
Davis KL, Colefax AP, Tucker JP, Kelaher BP, Santos IR (2021) Global coral reef ecosystems exhibit declining calcification and increasing primary productivity. Communications Earth & Environment 2:105
De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119
De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27 year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999
Dornelas M, Madin JS, Baird AH, Connolly SR (2017) Allometric growth in reef-building corals. Proc R Soc B-Biol Sci 284:20170053. https://doi.org/10.1098/rspb.2017.0053
Dubinsky Z, Falkowski PG (2011) Light as a source of information and energy in zooxanthellate corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 107–118
Eddy TD, Lam VWY, Reygondeau G, Cisneros-Montemayor AM, Greer K, Palomares MLD, Bruno JF, Ota Y, Cheung WWL (2021) Global decline in coral reefs to provide ecosystem services. OneEarth 4:1278–1285
Englebert N, Bongaerts P, Muir PR, Hay KB, Pichon M, Hoegh-Guldberg O (2017) Lower mesophotic coral communities (60–125 m depth) of the Northern Great Barrier Reef and Coral Sea. PLoS ONE 12:e0170336
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43:606–611
Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274
Fletcher C, Bochicchio C, Conger C, Engels M et al (2008) Geology of Hawaii reefs. In: Riegl B, Dodge R (eds) Coral reefs of the USA. Springer, pp 435–488
Franklin EC, Jokiel PL, Donahue MJ (2013) Predictive modeling of coral distribution and abundance in the Hawaiian Islands. Mar Ecol Prog Ser 481:121–132
Fricke HW, Vareschi E, Schlichter D (1987) Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible). Oecologia 73:371–381
Goldberg WM (2018) Coral food, feeding, nutrition, and secretion: A Review. In: Kloc M, Kubiak J (eds) Marine Organisms as Model Systems in Biology and Medicine. Results and Problems in Cell Differentiation. Springer, Cham, pp 377–421
Grigg RW (1982) Darwin point: a threshold for atoll formation. Coral Reefs 1:29–34
Grigg RW (1983) Community structure, succession and development of coral reefs in Hawaii. Mar Ecol Prog Ser 11:1–14
Hughes TP (1987) Skeletal density and growth form of corals. Mar Ecol Prog Ser 35:259–266
Kahng SE (2013) Growth rate for a zooxanthellate coral (Leptoseris hawaiiensis) at 90 m. Galaxea J Coral Reef Stud 15:39–40
Kahng SE, García-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275
Kahng SE, Hochberg EJ, Apprill A, Wagner D, Luck DG, Perez D, Bidigare RR (2012b) Efficient light harvesting in deep-water zooxanthellate corals. Mar Ecol Prog Ser 455:65–77
Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81
Kahng SE, Akkaynak D, Shlesinger T, Hochberg E, Wiedenmann J, Tamir R, Tchernov D (2019) Light, temperature, photosynthesis, heterotrophy, and the lower depth limits of mesophotic coral ecosystems (MCEs). In: Loya Y, Bridge T, Puglise K (eds) mesophotic coral ecosystems. Springer, Berlin, pp 799–826
Kahng SE, Watanabe TK, Hu H-M, Watanabe T, Shen C-C (2020) Moderate zooxanthellate coral growth rate at mesophotic depths. Coral Reefs 39:1273–1284
Kahng SE, Wagner D, Lantz C, Vetter O, Gove J, Merrifield M (2012a) Temperature related depth limits of warm-water corals. In: Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia, 9C
Kramer N, Tamir R, Ben-Zvi O, Jacques SL, Loya Y, Wangpraseurt D (2022) Efficient light-harvesting of mesophotic corals is facilitated by coral optical traits. Funct Ecol 36:406–441
Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Berlin, pp 405–420
Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, Gorbunov MY (2004) Diurnal hysteresis in coral photosynthesis. Mar Ecol Prog Ser 268:105–117
Lough JM (2008) Coral calcification from skeletal records revisited. Mar Ecol Prog Ser 373:257–264
Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243
Lough JM, Cantin NE (2014) Perspectives on massive coral growth rates in a changing ocean. Biol Bull 226:187–202
Lough JM, Cantin NE, Benthuysen JA, Cooper TF (2016) Environmental drivers of growth in massive Porites corals over 16 degrees of latitude along Australia’s northwest shelf. Limnol Oceanogr 61:684–700
Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R (2016) Theme section on mesophotic coral ecosystems: Advances in knowledge and future perspectives. Coral Reefs 35:1–9
Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480
Madin JS, Baird AH, Dornelas M, Connolly SR (2014) Mechanical vulnerability explains size dependent mortality of reef corals. Ecol Lett 17:1008–1015
Madin JS, Baird AH, Baskett ML, Connolly SR, Dornelas MA (2020) Partitioning colony size variation into growth and partial mortality. Biol Let 16:20190727. https://doi.org/10.1098/rsbl.2019.0727
Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224
Medellín-Maldonado F, López-Pérez A, Ruiz-Huerta L, Carricart-Ganivet JP (2022) Understanding corallite demography to comprehend potential bias in sclerochronology: analysis of coral modular growth by micro-computed tomography. Oceanogr Limnol 67(12):2665–2676. https://doi.org/10.1002/lno.12229
Naumann MS, Richter C, Mott C, el-Zibdah M, Manasrah R, Wild C, (2012) Budget of coral-derived organic carbon in a fringing coral reef of the Gulf of Aqaba, Red Sea. J Mar Syst 105:20–29
Pérez-Rosales G, Rouzé H, Torda G, Bongaerts P, Pichon M, Parravicini V, Hédouin L, Consortium Under The Pole (2021) Mesophotic coral communities escape thermal coral bleaching in French Polynesia. R Soc Open Sc 8:210139
Pérez-Rosales G, Hernández-Agreda A, Bongaerts P, Rouzé H, Pichon M, Carlot J, Torda G, Parravicini V, Hédouin L (2022) Mesophotic depths hide high coral cover communities in French Polynesia. Sci Total Environ 844:157049
Portner HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79:295–313
Pratchett MS, Anderson KD, Hoogenboom MO, Widman E, Baird AH (2015) Spatial, temporal and taxonomic variation in coral growth—implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol Annu Rev 53:215–295
Pyle RL (2019) Advanced Technical Diving. In: Loya Y, Bridge T, Puglise K (eds) Mesophotic Coral Ecosystems. Springer Publishing, Berlin, pp 959–972
Rodgers KS, Jokiel PL, Brown EK et al (2015) Over a decade of change in spatial and temporal dynamics of hawaiian coral reef communities. Pac Sci 69:1–13. https://doi.org/10.2984/69.1.1
Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceangr 52:1874–1882
Rouzé H, Galand PE, Medina M, Bongaerts P, Pichon M, Pérez-Rosales G, Torda G, Moya A, Bardout G, Périé-Bardout E, Marivint E, Lagarrigue G, Leblond J, Gazzola F, Pujolle S, Mollon N, Mittau A, Fauchet J, Paulme N, Pete R, Peyrusse K, Ferucci A, Magnan A, Horlaville M, Breton C, Gouin M, Markocic T, Jubert I, Herrmann P, Raina JB, Hédouin L (2021) Symbiotic associations of the deepest recorded photosynthetic scleractinian coral (172 m depth). ISME J 15:1564–1568
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089
Souter D, Serge P, Wicquart J, Logan M, Obura D, Staub F (2021) Status of coral reefs of the world: 2020 Executive Summary, (Townsville, Australia: Coral Reef Initiative, Global Coral Reef Monitoring Network)
Acknowledgements
This research was made possible by funding from the JSPS Invitational Fellowship for Research in Japan (Fellowship ID L20527) and by the Hawaii Undersea Research Laboratory (HURL). Special thanks to T. Kirby, M. Cremer and the HURL staff for operational support with the Pisces IV/V submersibles.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
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.
The original online version of this article was revised: Several equations were wrongly typeset by the published in the original article and have now been updated to their final version.
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
Kahng, S., Kishi, T., Uchiyama, R. et al. Calcification rates in the lower photic zone and their ecological implications. Coral Reefs 42, 1207–1217 (2023). https://doi.org/10.1007/s00338-023-02410-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-023-02410-7