Selection of mesophotic habitats by Oculina patagonica in the Eastern Mediterranean Sea following global warming.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 09 2021
13 09 2021
Historique:
received:
03
06
2021
accepted:
24
08
2021
entrez:
14
9
2021
pubmed:
15
9
2021
medline:
16
12
2021
Statut:
epublish
Résumé
Globally, species are migrating in an attempt to track optimal isotherms as climate change increasingly warms existing habitats. Stony corals are severely threatened by anthropogenic warming, which has resulted in repeated mass bleaching and mortality events. Since corals are sessile as adults and with a relatively old age of sexual maturity, they are slow to latitudinally migrate, but corals may also migrate vertically to deeper, cooler reefs. Herein we describe vertical migration of the Mediterranean coral Oculina patagonica from less than 10 m depth to > 30 m. We suggest that this range shift is a response to rapidly warming sea surface temperatures on the Israeli Mediterranean coastline. In contrast to the vast latitudinal distance required to track temperature change, this species has migrated deeper where summer water temperatures are up to 2 °C cooler. Comparisons of physiology, morphology, trophic position, symbiont type, and photochemistry between deep and shallow conspecifics revealed only a few depth-specific differences. At this study site, shallow colonies typically inhabit low light environments (caves, crevices) and have a facultative relationship with photosymbionts. We suggest that this existing phenotype aided colonization of the mesophotic zone. This observation highlights the potential for other marine species to vertically migrate.
Identifiants
pubmed: 34518595
doi: 10.1038/s41598-021-97447-5
pii: 10.1038/s41598-021-97447-5
pmc: PMC8438053
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
18134Informations de copyright
© 2021. The Author(s).
Références
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).
pubmed: 22615406
pmcid: 3384199
doi: 10.1073/pnas.1118364109
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).
doi: 10.1126/science.1206432
Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
doi: 10.1111/j.1600-0706.2010.18270.x
Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).
doi: 10.1038/nclimate1958
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).
doi: 10.1111/j.1600-0706.2010.18270.x
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).
pubmed: 23951016
pmcid: 3741371
doi: 10.1371/journal.pone.0070820
Rodolfo-Metalpa, R. et al. Thermally tolerant corals have limited capacity to acclimatize to future warming. Glob. Change Biol. 20, 3036–3049 (2014).
doi: 10.1111/gcb.12571
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).
doi: 10.1111/j.1365-2486.1996.tb00063.x
Price, N. N. et al. Global biogeography of coral recruitment: Tropical decline and subtropical increase. Mar. Ecol. Prog. Ser. 621, 1–17 (2019).
doi: 10.3354/meps12980
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).
doi: 10.1371/journal.pone.0052739
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).
pubmed: 29710655
doi: 10.1016/j.scitotenv.2018.04.032
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).
doi: 10.1357/002224006778715711
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).
doi: 10.1007/s00338-021-02095-w
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).
doi: 10.1007/s00338-016-1530-0
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).
doi: 10.1038/s42003-021-01727-9
pubmed: 33589736
pmcid: 7884412
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).
pubmed: 25859324
pmcid: 4377262
doi: 10.1002/ece3.1324
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).
doi: 10.3389/fmars.2018.00445
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).
doi: 10.1007/s00338-009-0581-x
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).
pubmed: 20581269
doi: 10.1242/jeb.040147
Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: Metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007).
doi: 10.3354/meps334093
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).
pubmed: 28074021
pmcid: 5241398
doi: 10.1128/mBio.02058-16
Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).
pubmed: 16641995
doi: 10.1038/nature04565
Tremblay, P. et al. Controlling effects of irradiance and heterotrophy on carbon translocation in the temperate coral Cladocora caespitosa. PLoS ONE 7, e44672 (2012).
pubmed: 22970284
pmcid: 3438184
doi: 10.1371/journal.pone.0044672
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).
pubmed: 30718370
doi: 10.1242/jeb.189225
Shenkar, N., Fine, M. & Loya, Y. Size matters: Bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294, 181–188 (2005).
doi: 10.3354/meps294181
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).
doi: 10.3389/fmars.2019.00662
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).
doi: 10.1007/s10530-013-0424-0
Fine, M., Zibrowius, H. & Loya, Y. Oculina patagonica: A non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar. Biol. 138, 1195–1203 (2001).
doi: 10.1007/s002270100539
Sartoretto, S. et al. The alien coral Oculina patagonica De Angelis, 1908 (Cnidaria, Scleractinia) in Algeria and Tunisia. Aquat. Invasions 3, 173–180 (2008).
doi: 10.3391/ai.2008.3.2.7
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).
doi: 10.1016/j.gloplacha.2016.04.001
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).
doi: 10.3354/meps07908
Goodbody-Gringley, G. & Waletich, J. Morphological plasticity of the depth generalist coral, Montastraea cavernosa, on mesophotic reefs in Bermuda. Ecology 99, 1688–1690 (2018).
pubmed: 29608800
doi: 10.1002/ecy.2232
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).
doi: 10.1016/j.actbio.2020.01.010
pubmed: 31954936
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).
doi: 10.1007/s00338-008-0406-3
Lesser, M. P. et al. Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: Light, food, and genetics. Ecology 91, 990–1003 (2010).
pubmed: 20462114
doi: 10.1890/09-0313.1
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).
doi: 10.1371/journal.pone.0059596
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).
doi: 10.3389/fmars.2020.00013
pubmed: 33409285
pmcid: 7116548
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).
doi: 10.1007/s00338-016-1409-0
Rubio-Portillo, E. et al. Eukarya associated with the stony coral Oculina patagonica from the Mediterranean Sea. Mar. Genom. 17, 17–23 (2014).
doi: 10.1016/j.margen.2014.06.002
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).
Ben-Zvi, O. et al. Photophysiology of a mesophotic coral 3 years after transplantation to a shallow environment. Coral Reefs 39, 903–913 (2020).
doi: 10.1007/s00338-020-01910-0
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).
doi: 10.1007/s00338-020-02029-y
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).
doi: 10.1007/s00338-009-0558-9
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).
doi: 10.3389/fmars.2020.561568
Wall, C. B., Wallsgrove, N. J., Gates, R. D. & Popp, B. N. Amino acid δ
doi: 10.1002/lno.11742
pubmed: 34248204
pmcid: 8252108
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).
doi: 10.3390/microorganisms9010182
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).
doi: 10.1016/j.ecss.2020.106652
Leal, M. C. et al. Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar. Ecol. Prog. Ser. 504, 171–179 (2014).
doi: 10.3354/meps10750
Ferrier-Pagès, C. et al. Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol. Oceanogr. 56, 1429–1438 (2011).
doi: 10.4319/lo.2011.56.4.1429
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).
doi: 10.3389/fmars.2017.00102
Martinez, S. et al. Energy sources of the depth-generalist mixotrophic coral Stylophora pistillata. Front. Mar. Sci. 7, 1–16 (2020).
doi: 10.3389/fmars.2020.566663
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).
pubmed: 31900444
pmcid: 7082336
doi: 10.1038/s41396-019-0570-1
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).
doi: 10.1111/1365-2435.13441
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).
pubmed: 21795572
doi: 10.1242/jeb.054239
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).
doi: 10.1016/j.dib.2019.104809
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).
doi: 10.1016/j.marenvres.2020.105215
pubmed: 33360640
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).
doi: 10.1016/S0015-3796(17)30778-3
Marsh, J. A. Primary productivity of reef-building calcareous red algae. Ecology 51, 255–263 (1970).
doi: 10.2307/1933661
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).
doi: 10.4319/lo.1991.36.6.1232
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).
doi: 10.4319/lo.2006.51.3.1284
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).
pubmed: 7881515
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).
pubmed: 25052021
pmcid: 4285332
doi: 10.1111/mec.12869
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
pubmed: 17846036
doi: 10.1093/bioinformatics/btm404
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).
pubmed: 30740899
pmcid: 6618109
doi: 10.1111/1755-0998.13004
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).
doi: 10.4319/lo.2002.47.3.0782
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).
pubmed: 22442377
doi: 10.1242/jeb.065201
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).
doi: 10.1016/0304-4203(92)90079-P
Docherty, G., Jones, V. & Evershed, R. P. Practical and theoretical considerations in the gas chromatography/combustion/isotope ratio mass spectrometry δ
pubmed: 11319796
doi: 10.1002/rcm.270
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).