Cook, B. I., Wolkovich, E. M. & Parmesan, C. Divergent responses to spring and winter warming drive community level flowering trends. Proc. Natl. Acad. Sci. USA 109, 9000–9005 (2012).
Google Scholar
Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science (80-). 333, 1024–1026 (2011).
Google Scholar
Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
Google Scholar
Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).
Google Scholar
Suggitt, A. J., et al. Habitatmicroclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8. https://doi.org/10.1111/j.1600-0706.2010.18270.x (2011).
Google Scholar
Kersting, D. K., Bensoussan, N. & Linares, C. Long-term responses of the endemic reef-builder cladocora caespitosa to mediterranean warming. PLoS ONE 8, e70820 (2013).
Google Scholar
Rodolfo-Metalpa, R. et al. Thermally tolerant corals have limited capacity to acclimatize to future warming. Glob. Change Biol. 20, 3036–3049 (2014).
Google Scholar
Fine M., & Loya Y. Coral bleaching in a temperate sea: From colony physiology to population ecology. In: Coral Health and Disease (eds. Rosenberg, E., & Loya, Y). https://doi.org/10.1007/978-3-662-06414-6_6 (Springer, Berlin, Heidelberg 2004).
Liu, G., Strong, A. E., Skirving, W. J. & Arzayus, L. F. Overview of NOAA Coral Reef Watch Program’s near-real-time satellite global coral bleaching monitoring activities. Proc. 10th Int. Coral Reef Symp. 1793, 1783–1793 (2006).
Glynn, P. W. Coral reef bleaching: Facts, hypotheses and implications. Glob. Change Biol. 2, 495–509 (1996).
Google Scholar
Price, N. N. et al. Global biogeography of coral recruitment: Tropical decline and subtropical increase. Mar. Ecol. Prog. Ser. 621, 1–17 (2019).
Google Scholar
Serrano, E. et al. Rapid northward spread of a zooxanthellate coral enhanced by artificial structures and sea warming in the Western Mediterranean. PLoS One 8(1), e52739. https://doi.org/10.1371/journal.pone.0052739 (2013).
Google Scholar
Grupstra, C. G. B. et al. Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 2017 363. 36, 981–985 (2017).
Serrano, E., Ribes, M. & Coma, R. Demographics of the zooxanthellate coral Oculina patagonica along the Mediterranean Iberian coast in relation to environmental parameters. Sci. Total Environ. 634, 1580–1592 (2018).
Google Scholar
Leichter, J. J., Helmuth, B. & Fischer, A. M. Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J. Mar. Res. 64, 563–588 (2006).
Google Scholar
Gould, K., Bruno, J. F., Ju, R. & Goodbody-Gringley, G. Upper-mesophotic and shallow reef corals exhibit similar thermal tolerance, sensitivity and optima. Coral Reefs https://doi.org/10.1007/s00338-021-02095-w (2021).
Google Scholar
Semmler, R. F., Hoot, W. C. & Reaka, M. L. Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs?. Coral Reefs 36, 433–444 (2017).
Google Scholar
Shlesinger, T. & Loya, Y. Depth-dependent parental effects create invisible barriers to coral dispersal. Commun. Biol. 4(202), https://doi.org/10.1038/s42003-021-01727-9 (2021).
Google Scholar
Ledoux, J.-B. et al. Potential for adaptive evolution at species range margins: Contrasting interactions between red coral populations and their environment in a changing ocean. Ecol. Evol. 5, 1178–1192 (2015).
Google Scholar
Liberman, R., Shlesinger, T., Loya, Y. & Benayahu, Y. Octocoral sexual reproduction: Temporal disparity between mesophotic and shallow-reef populations. Front. Mar. Sci. 5, 1–14 (2018).
Google Scholar
Rapuano, H., Shlesinger, T., Loya, Y., Amit, T. & Grinblat, M. Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt. Ecology 99, 421–437 (2017).
Bongaerts, P., Ridgway, T., Sampayo, E. M. & Hoegh-Guldberg, O. Assessing the ‘deep reef refugia’ hypothesis: Focus on Caribbean reefs. Coral Reefs 29, 1–19 (2010).
Google Scholar
Hoogenboom, M., Rodolfo-Metalpa, R. & Ferrier-Pagès, C. Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J. Exp. Biol. 213, 2399–2409 (2010).
Google Scholar
Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: Metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007).
Google Scholar
Bednarz, V. N., Grover, R., Maguer, J. F., Fine, M. & Ferrier-Pagès, C. The assimilation of diazotroph-derived nitrogen by scleractinian corals depends on their metabolic status. MBio 8, e02058-16 (2017).
Google Scholar
Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).
Google Scholar
Tremblay, P. et al. Controlling effects of irradiance and heterotrophy on carbon translocation in the temperate coral Cladocora caespitosa. PLoS ONE 7, e44672 (2012).
Google Scholar
Aichelman, H. E., Zimmerman, R. C. & Barshis, D. J. Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. J. Exp. Biol. 222, jeb189225 (2019).
Google Scholar
Shenkar, N., Fine, M. & Loya, Y. Size matters: Bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294, 181–188 (2005).
Google Scholar
Zaquin, T., Zaslansky, P., Pinkas, I. & Mass, T. Simulating bleaching: Long-term adaptation to the dark reveals phenotypic plasticity of the Mediterranean Sea coral Oculina patagonica. Front. Mar. Sci. 6, 662 https://doi.org/10.3389/fmars.2019.00662 (2019).
Google Scholar
De Angelis d’Ossat, G. Altri Zoantari del Terziario della Patagonia. (1908).
Fine, M. & Loya, Y. The coral Oculina patagonica a new immigrant to the Mediterranean coast of Israel. Isr. J. Zool. 41, 84 (1995).
Salomidi, M., Katsanevakis, S., Issaris, Y., Tsiamis, K. & Katsiaras, N. Anthropogenic disturbance of coastal habitats promotes the spread of the introduced scleractinian coral Oculina patagonica in the Mediterranean Sea. Biol. Invasions 15, 1961–1971 (2013).
Google Scholar
Fine, M., Zibrowius, H. & Loya, Y. Oculina patagonica: A non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar. Biol. 138, 1195–1203 (2001).
Google Scholar
Sartoretto, S. et al. The alien coral Oculina patagonica De Angelis, 1908 (Cnidaria, Scleractinia) in Algeria and Tunisia. Aquat. Invasions 3, 173–180 (2008).
Google Scholar
Ozer, T., Gertman, I., Kress, N., Silverman, J. & Herut, B. Interannual thermohaline (1979–2014) and nutrient (2002–2014) dynamics in the Levantine surface and intermediate water masses, SE Mediterranean Sea. Glob. Planet. Change 151, 60–67 (2017).
Google Scholar
Leydet, K. P. & Hellberg, M. E. The invasive coral Oculina patagonica has not been recently introduced to the Mediterranean from the western Atlantic. BMC Evol. Biol. 15(79), https://doi.org/10.1186/s12862-015-0356-7 (2015).
Veron, J. E. N. Título: Corals of the world. P.imprenta: Australia. Australian Institute of Marine Science. 463, 31 (2000).
Einbinder, S. et al. Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar. Ecol. Prog. Ser. 381, 167–174 (2009).
Google Scholar
Goodbody-Gringley, G. & Waletich, J. Morphological plasticity of the depth generalist coral, Montastraea cavernosa, on mesophotic reefs in Bermuda. Ecology 99, 1688–1690 (2018).
Google Scholar
Malik, A. et al. Molecular and skeletal fingerprints of scleractinian coral biomineralization: From the sea surface to mesophotic depths. Acta Biomater. https://doi.org/10.1016/j.actbio.2020.01.010 (2020).
Google Scholar
Frade, P. R., Englebert, N., Faria, J., Visser, P. M. & Bak, R. P. M. Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: Is there more to it than total irradiance?. Coral Reefs 27, 913–925 (2008).
Google Scholar
Lesser, M. P. et al. Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: Light, food, and genetics. Ecology 91, 990–1003 (2010).
Google Scholar
Byler, K. A., Carmi-Veal, M., Fine, M. & Goulet, T. L. Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS ONE 8, 1–7 (2013).
Google Scholar
Scucchia, F., Nativ, H., Neder, M., Goodbody-Gringley, G. & Mass, T. Physiological characteristics of Stylophora pistillata larvae across a depth gradient. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00013 (2020).
Google Scholar
Leydet, K. P. & Hellberg, M. E. Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus, Oculina. Coral Reefs 35, 583–595 (2016).
Google Scholar
Rubio-Portillo, E. et al. Eukarya associated with the stony coral Oculina patagonica from the Mediterranean Sea. Mar. Genom. 17, 17–23 (2014).
Google Scholar
Brakel, W. H. Small-scale spatial variation in light available to coral reef benthos: Quantum irradiance measurements from a Jamaican reef. Bull. Mar. Sci. 29, 406–413 (1979).
Google Scholar
Ben-Zvi, O. et al. Photophysiology of a mesophotic coral 3 years after transplantation to a shallow environment. Coral Reefs 39, 903–913 (2020).
Google Scholar
Wang, C., Arneson, E. M., Gleason, D. F. & Hopkinson, B. M. Resilience of the temperate coral Oculina arbuscula to ocean acidification extends to the physiological level. Coral Reefs 40, 201–214 (2021).
Google Scholar
Hoogenboom, M., Béraud, E. & Ferrier-Pagès, C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29, 21–29. https://doi.org/10.1007/s00338-009-0558-9 (2010).
Google Scholar
Martinez, S. et al. Effect of different derivatization protocols on the calculation of trophic position using amino acids compound-specific stable isotopes. Front. Mar. Sci. 7, 1–7. https://doi.org/10.3389/fmars.2020.561568 (2020).
Google Scholar
Wall, C. B., Wallsgrove, N. J., Gates, R. D. & Popp, B. N. Amino acid δ 13C and δ 15N analyses reveal distinct species‐specific patterns of trophic plasticity in a marine symbiosis. Limnol. Oceanogr. 66, 2033–2050. https://doi.org/10.1002/lno.11742 (2021).
Google Scholar
Ferrier-Pagès, C. et al. Tracing the trophic plasticity of the coral-dinoflagellate symbiosis using amino acid compound-specific stable isotope analysis. Microorganisms 9, 1–16 (2021).
Google Scholar
Grossowicz, M., Shemesh, E., Martinez, S., Benayahu, Y. & Tchernov, D. New evidence of Melithaea erythraea colonization in the Mediterranean. Estuar. Coast. Shelf Sci. 236, 106652 (2020).
Google Scholar
Leal, M. C. et al. Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar. Ecol. Prog. Ser. 504, 171–179 (2014).
Google Scholar
Ferrier-Pagès, C. et al. Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol. Oceanogr. 56, 1429–1438 (2011).
Google Scholar
Ezzat, L., Fine, M., Maguer, J.-F., Grover, R. & Ferrier-Pagès, C. Carbon and nitrogen acquisition in shallow and deep holobionts of the Scleractinian coral S. pistillata. Front. Mar. Sci. 4, 1–12. https://doi.org/10.3389/fmars.2017.00102 (2017).
Google Scholar
Martinez, S. et al. Energy sources of the depth-generalist mixotrophic coral Stylophora pistillata. Front. Mar. Sci. 7, 1–16 (2020).
Google Scholar
Wall, C. B., Kaluhiokalani, M., Popp, B. N., Donahue, M. J. & Gates, R. D. Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient. ISME J. 14, 945–958 (2020).
Google Scholar
Fox, M. D., Elliott Smith, E. A., Smith, J. E. & Newsome, S. D. Trophic plasticity in a common reef-building coral: Insights from δ13C analysis of essential amino acids. Funct. Ecol. 33, 2203–2214 (2019).
Google Scholar
Godinot, C., Grover, R., Allemand, D. & Ferrier-Pagès, C. High phosphate uptake requirements of the scleractinian coral Stylophora pistillata. J. Exp. Biol. 214, 2749–2754 (2011).
Google Scholar
Kersting, D. K. et al. Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral. Sci. Rep. 2015 51 5, 1–8 (2015).
Suari, Y. et al. A long term physical and biogeochemical database of a hyper-eutrophicated Mediterranean micro-estuary. Data Br. 27, 104809 (2019).
Google Scholar
Liberman, R., Fine, M. & Benayahu, Y. Simulated climate change scenarios impact the reproduction and early life stages of a soft coral. Mar. Environ. Res. 163, 105215. https://doi.org/10.1016/j.marenvres.2020.105215 (2021).
Google Scholar
Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191–194 (1975).
Google Scholar
Marsh, J. A. Primary productivity of reef-building calcareous red algae. Ecology 51, 255–263 (1970).
Google Scholar
Chisholm, J. R. M. & Gattuso, J.-P. Validation of the alkalinity anomaly technique for investigating calcification of photosynthesis in coral reef communities. Limnol. Oceanogr. 36, 1232–1239 (1991).
Google Scholar
Schneider, K. & Erez, J. The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol. Oceanogr. 51, 1284–1293 (2006).
Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).
Google Scholar
Arif, C. et al. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol. Ecol. 23, 4418–4433 (2014).
Google Scholar
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
Google Scholar
Hume, B. C. C. et al. SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080 (2019).
Google Scholar
Grover, R., Maguer, J.-F., Reynaud-Vaganay, S. & Ferrier-Pagès, C. Uptake of ammonium by the scleractinian coral Stylophora pistillata : Effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 47, 782–790 (2002).
Google Scholar
Tremblay, P., Grover, R., Maguer, J. F., Legendre, L. & Ferrier-Pagès, C. Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation. J. Exp. Biol. 215, 1384–1393 (2012).
Google Scholar
Cowie, G. L. & Hedges, J. I. Improved amino acid quantification in environmental samples: Charge-matched recovery standards and reduced analysis time. Mar. Chem. 37, 223–238 (1992).
Google Scholar
Docherty, G., Jones, V. & Evershed, R. P. Practical and theoretical considerations in the gas chromatography/combustion/isotope ratio mass spectrometry δ 13C analysis of small polyfunctional compounds. Rapid Commun. Mass Spectrom. 15, 730–738 (2001).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing. (2020).
Fox, J. W., & Weisberg, S. An R companion to applied regression. 3rd ed. (Los Angeles: SAGE Publications, Inc, 2019)
Villanueva, R. A. M. & Chen, Z. J. ggplot2: Elegant graphics for data analysis (2nd ed.), Measurement: Interdisciplinary Research and Perspectives, 17(3), 160–167. https://doi.org/10.1080/15366367.2019.1565254 (2019).
Wilke, C. O. cowplot: Streamlined Plot Theme and Plot Annotations for “ggplot2” (R 74 package version 1.1.0) [Computer software]. https://CRAN.Rproject.org/package=cowplot (2020).
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