Abstract
With shallow coral reefs suffering from an ongoing rapid decline in many regions of the world, the interest in studies on mesophotic coral ecosystems (30–150 m) is growing rapidly. While most photoacclimation responses in corals were documented within the upper 30 m of reefs, in the present study we transplanted fragments of a strictly mesophotic species from the Red Sea, Euphyllia paradivisa, from 50 m to 5 m for a period of 3 years. Following the retrieval of the corals, their physiological and photosynthetic properties of the corals were tested. The transplanted corals presented evidence of photosynthetic acclimation to the shallow habitat, lower sensitivity to photoinhibition, and a high survival percentage, while also demonstrating a reduced ability to utilize low light compared to their mesophotic counterparts. This long-term successful transplantation from a mesophotic depth to a shallow habitat has provided us with insights regarding the ability of mesophotic corals and their symbionts to survive and withstand shallow environments, dominated by a completely different light regime. The extensive characterization of the photobiology of E. paradivisa, and its photoacclimation response to a high-light environment also demonstrates the plasticity of corals and point out to mechanisms different than those reported previously in shallower corals.
This is a preview of subscription content, access via your institution.





References
Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342
Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009) Carbon and nitrogen utilization in two species of Red Sea corals along a depth gradient: insights from stable isotope analysis of total organic material and lipids. Geochimica et Cosmochimica Acta 73:5333–5342
Anthony KRN, Hoegh-Guldberg O (2003) Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Funct Ecol 17:246–259
Anthony KRN, Hoogenboom MO, Connolly SR (2005) Adaptive variation in coral geometry and the optimization of internal colony light climates. Funct Ecol 19:17–26
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Beer S, Bjork M, Beardall J (2014) Photosynthesis in the marine environment. Wiley, New York
Benayahu Y, Loya Y (1985) Settlement and recruitment of a soft coral: why is Xenia macrospiculata a successful colonizer? Bull Mar Sci 36:177–188
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
Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325
Chalker B (1981) Simulating light-saturation curves for photosynthesis and calcification by reef-building corals. Mar Biol 63:135–141
Chalker BE, Dunlap WC, Oliver JK (1983) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. II. Light saturation curves for photosynthesis and respiration. J Exp Mar Bio Ecol 73:37–56
Cohen I, Dubinsky Z (2015) Long term photoacclimation responses of the coral Stylophora pistillata to reciprocal deep to shallow transplantation: photosynthesis and calcification. Front Mar Sci 2:45
Cohen I, Dubinsky Z, Erez J (2016) Light enhanced calcification in hermatypic corals: New insights from light spectral responses. Fronts Mar Sci 2:122
Edwards MS, Kim KY (2010) Diurnal variation in relative photosynthetic performance in giant kelp Macrocystis pyrifera (Phaeophyceae, Laminariales) at different depths as estimated using PAM fluorometry. Aquat Bot 92:119–128
Einbinder S, Gruber DF, Salomon E, Liran O, Keren N, Tchernov D (2016) Novel adaptive photosynthetic characteristics of mesophotic symbiotic microalgae within the reef-building coral, Stylophora pistillata. Front Mar Sci 3:195
Enríquez S, Méndez ER, Hoegh-Guldberg O, Iglesias-Prieto R (2017) Key functional role of the optical properties of coral skeletons in coral ecology and evolution. Proc R Soc Lond B Biol Sci 284(1853):20161667
Eyal-Shaham L, Eyal G, Tamir R, Loya Y (2016) Reproduction, abundance and survivorship of two Alveopora spp. in the mesophotic reefs of Eilat, Red Sea. Sci Rep 6:20964
Eyal G, Wiedenmann J, Grinblat M, D’Angelo C, Kramarsky-Winter E, Treibitz T, Ben-Zvi O, Shaked Y, Smith TB, Harii S, Denis V, Noyes T, Tamir R, Loya Y (2015) Spectral diversity and regulation of coral fluorescence in a mesophotic reef habitat in the Red Sea. PLoS One 10:e0128697
Eyal G, Eyal-Shaham L, Cohen I, Tamir R, Ben-Zvi O, Sinniger F, Loya Y (2016) Euphyllia paradivisa, a successful mesophotic coral in the northern Gulf of Eilat/Aqaba, Red Sea. Coral Reefs 35:91–102
Eyal G, Cohen I, Eyal-Shaham L, Ben-Zvi O, Tikochinski Y, Loya Y (2019) Photoacclimation and induction of light-enhanced calcification in the mesophotic coral Euphyllia paradivisa. R Soc Open Sci 6:180527
Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174
Falkowski PG, Jokiel PL, Kinzie RA (1990) Irradiance and corals. Ecosystems of the world 25:89–107
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
Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Bio Ecol 373:102–110
Gleason D, Wellington G (1995) Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar Biol 123:693–703
Groves SH, Holstein DM, Enochs IC, Kolodzeij G, Manzello DP, Brandt ME, Smith TB (2018) Growth rates of Porites astreoides and Orbicella franksi in mesophotic habitats surrounding St. Thomas, US Virgin Islands. Coral Reefs 37:345–354
Hinderstein M, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG (2010) Theme section on “mesophotic coral ecosystems: characterization, ecology, and management”. Coral Reefs 29:247–251
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 E (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: Deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407
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, Prachett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
Iluz D, Alexandrovich I, Dubinsky Z (2012) The enhancement of photosynthesis by fluctuating light. In: Artificial photosynthesis. BoD-Books on demand, pp 115–134
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a1, b1, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
Jokiel PL (1978a) Effects of water motion on reef corals. J Exp Mar Bio Ecol 35:87–97
Jokiel PL (1978b) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO, Paris
Kahng SE, Garcia-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, 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 EJ, Wiedenmann J, Tamir R, Tchernov D (2019) Light, temperature, photosynthesis, heterotrophy, and the lower depth limits of mesophotic coral ecosystems. Mesophotic coral ecosystems. Springer, Berlin, pp 801–828
Kaiser P, Schlichter D, Fricke HW (1993) Influence of light on algal symbionts of the deep water coral Leptoseris fragilis. Mar Biol 117:45–52
Kinzie RA, Jokiel PL, York R (1984) Effects of light of altered spectral composition on coral zooxanthellae associations and on zooxanthellae in vitro. Mar Biol 78:239–248
Kinzie RA, Hunter T (1987) Effect of light quality on photosynthesis of the reef coral Montipora verrucosa. Mar Biol 94:95–109
Kramer N, Eyal G, Tamir R, Loya Y (2019) Upper mesophotic depths in the coral reefs of Eilat, Red Sea, offer suitable refuge grounds for coral settlement. Sci Rep 9:2263
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580
Laverick JH, Rogers AD (2018) Experimental evidence for reduced mortality of Agaricia lamarcki on a mesophotic reef. Mar Environ Res 134:37–43
Lenth R (2018) emmeans: Estimated marginal means, aka least-squares means, R package Version 1.4.3. https://CRAN.R-project.org/package=emmeans
Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283
Lesser PM (2000) Depth-dependent photoacclimatization to solar ultraviolet radiation in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 192:137–151
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8
Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003
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
Maida M, Coll JC, Sammarco PW (1994) Shedding new light on scleractinian coral recruitment. J Exp Mar Bio Ecol 180:189–202
Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102
Mundy CN, Babcock RC (1998) Role of light intensity and spectral quality in coral settlement: implications for depth-dependent settlement? J Exp Mar Bio Ecol 223:235–255
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world: coral reefs. Elsevier, New York, pp 75–78
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460
Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611
Nir O, Gruber DF, Einbinder S, Kark S, Tchernov D (2011) Changes in scleractinian coral Seriatopora hystrix morphology and its endocellular Symbiodinium characteristics along a bathymetric gradient from shallow to mesophotic reef. Coral Reefs 30:1089
Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS One 7:e29816
Polinski JM, Voss JD (2018) Evidence of photoacclimatization at mesophotic depths in the coral-Symbiodinium symbiosis at Flower Garden Banks National Marine Sanctuary and McGrail Bank. Coral Reefs 37:779–789
Scheufen T, Iglesias-Prieto R, Enriquez S (2017) Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front Mar Sci 4:309
Schreiber U, Neubauer C, Schliwa U (1993) PAM fluorometer based on medium-frequency pulsed Xe-flash measuring light: a highly sensitive new tool in basic and applied photosynthesis research. Photosynth Res 36:65–72
Schubert H, Sagert S, Forster RM (2001) Evaluation of the different levels of variability in the underwater light field of a shallow estuary. Helgol Mar Res 55:12–22
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
Smith EG, D’Angelo C, Sharon Y, Tchernov D, Wiedenmann J (2017) Acclimatization of symbiotic corals to mesophotic light environments through wavelength transformation by fluorescent protein pigments. Proc R Soc Lond B Biol Sci 284:1858
Team RC (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Tamir R, Eyal G, Kramer N, Laverick JH, Loya Y (2019) Light environment drives the shallow-to-mesophotic coral community transition. Ecosphere 10:e02839
Titlyanov EA, Titlyanova TV, Yamazato K, van Woesik R (2001) Photo-acclimation dynamics of the coral Stylophora pistillata to low and extremely low light. J Exp Mar Bio Ecol 263:211–225
Trench RK, Harley JL (1971) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. liberation of fixed 14C by zooxanthellae in vitro. Proc R Soc Lond B Biol Sci 177:237–250
Veron JEN (1990) New scleractinia from Japan and other Indo-West Pacific countries. Galaxea 9:95–173
Veron JEN (1995) Corals in time and space. University New South Wales Press, Sydney
Wangpraseurt D, Lichtenberg M, Jacques SL, Larkum AWD, Kühl M (2019) Optical properties of corals distort variable chlorophyll fluorescence measurements. Plant Physiol 179:1608–1619
Wijgerde T, van Melis A, Silva CIF, Leal MC, Vogels L, Mutter C, Osinga R (2014) Red light represses the photophysiology of the scleractinian coral Stylophora pistillata. PLoS ONE 9:e92781–e92781
Yamashiro H, Nishira M (1995) Phototaxis in Fungiidae corals (Scleractinia). Mar Biol 124:461–465
Acknowledgements
We would like to thank the Interuniversity Institute for Marine Sciences in Eilat (IUI) for logistical support and making their facilities available to us. We thank M. Fine and his lab for assisting us with the Imaging-PAM measurements and I. Cohen for his assistance in analyzing the respiration metabolic chambers results. We are grateful to the Marine Photosynthesis Course in the IUI for their contribution to the final stage of this research. We also thank N. Paz for her proofreading and the anonymous reviewers for their much-appreciated comments.
Funding
Funding was provided by the Israel Science Foundation (Grant No. 1191/16), Ministry of Science and Technology, Israel (Grant No. 3-18487), European Union’s Horizon 2020 research and innovation program under a Marie Skłodowska-Curie (Grant No. 796025).
Author information
Affiliations
Corresponding authors
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.
Topic Editor Simon Davy
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ben-Zvi, O., Tamir, R., Keren, N. et al. Photophysiology of a mesophotic coral 3 years after transplantation to a shallow environment. Coral Reefs 39, 903–913 (2020). https://doi.org/10.1007/s00338-020-01910-0
Received:
Accepted:
Published:
Issue Date:
Keywords
- Mesophotic coral ecosystems (MCEs)
- Euphyllia paradivisa
- Photosynthesis
- Photoacclimation
- Photophysiology