The deep vault: a temporary refuge for temperate gorgonian forests facing marine heat waves
Published:
Nov 17, 2023
Keywords:
mass mortality events. sea-fan Mediterranean Sea mesophotic deep refuge extreme events temperate corals habitat-forming species climate change octocorals
Abstract
Climate change poses a significant threat to coastal areas, marked by the increasing intensity and frequency of marine heat waves observed in various ecosystems around the world. Over the last 25 years, a vast number of Mediterranean populations of the red gorgonian Paramuricea clavata have been impacted by marine heatwaves. The last mass mortality occurred during the summer of 2022 in the Western Mediterranean Sea, affecting mostly shallow populations (down to 30 m depth). Here we provide an assessment of the health status of mesophotic P. clavata populations down to 90 m depth to investigate a depth refuge hypothesis. Results show that the impact of marine heat waves decreases with depth, with a significant drop in mortality below 40 m depth. These observations support the hypothesis of a depth refuge from marine heat waves that may allow, at least temporarily, the maintenance of P. clavata in the Western Mediterranean Sea. The present study strongly advocates for further investigations and monitoring of the mesophotic zone to chart potential areas that could serve as deep refuge for gorgonians.
Article Details
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BRAMANTI, L., MANEA, E., GIORDANO, B., ESTAQUE, T., BIANCHIMANI, O., RICHAUME, J., MÉRIGOT, B., SCHULL, Q., SARTORETTO, S., GARRABOU, J. G., & GUIZIEN, K. (2023). The deep vault: a temporary refuge for temperate gorgonian forests facing marine heat waves. Mediterranean Marine Science, 24(3), 601–609. https://doi.org/10.12681/mms.35564
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References
Akaike, H., 1978. On the likelihood of a time series model. Journal of the Royal Statistical Society, 27 (3/4), 217-235.
Arnoux, A., Harmelin, J.-G., Monod, J.L., Romana, L.A., Zibrowius, H., 1992. Altérations des peuplements benthiques de roches profondes en Méditerranée nord-occidentale: quelque aspects biologiques et molysmologiques. Comptes Rendus de l’Académie des Science. Série 3, Sciences de la vie, 314 (5), 219-225.
Bavestrello, G., Cerrano, C., Zanzi, D., Cattaneo-Vietti, R., 1994. Damage by fishing activities to the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquatic Conservation- marine and Freshwater Ecosystems, 7 (3), 253-262.
Bongaerts, P., Ridgway, T., Sampayo, E. M., Hoegh-Guldberg, O., 2010. Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs, 29 (2), 309-327.
Bongaerts, P., Smith, T.B., 2019. Beyond the “Deep Reef Refuge” hypothesis: A conceptual framework to characterize persistence at depth. Mesophotic Coral Ecosystems, 881-895.
Bridge, T.C.L., Hoey, A.S., Campbell, S.J., Muttaqin, E., Rudi, E. et al., 2014. Depth-dependent mortality of reef corals following a severe bleaching event: implications for thermal refuges and population recovery. F1000Research, 2, 187.
Carpine, C., Grasshoff, M., 1975. Les gorgonaires de la Mediterranee. Bulletin de l’Institut océanographique de Monaco, 71 (1430), 1-140.
Cerrano, C., Bavestrello, G., Bianchi, C.N., Cattaneo-vietti, R., Bava, S. et al., 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-Western Mediterranean), summer 1999. Ecology Letters, 3 (4), 284-293.
Crisci, C., Ledoux, J.-B., Mokhtar-Jamaï, K., Bally, M., Bensoussan, N. et al., 2017. Regional and local environmental conditions do not shape the response to warming of a marine habitat-forming species. Scientific Reports, 7 (1), 5069.
Cupido, R., Cocito, S., Sgorbini, S., Bordone, A., Santangelo, G., 2008. Response of a gorgonian (Paramuricea clavata) population to mortality events: recovery or loss? Aquatic Conservation: Marine and Freshwater Ecosystems, 18 (6), 984-992.
Cupido, R., Cocito, S., Barsanti, M., Sgorbini, S., Peirano, A. et al., 2009. Unexpected long-term population dynamics in a canopy-forming gorgonian coral following mass mortality. Marine Ecology Progress Series, 394, 195-200.
Dayan, H., McAdam, R., Juza, M., Masina, S., Speich, S., 2023. Marine heat waves in the Mediterranean Sea: an assessment from the surface to the subsurface to meet national needs. Frontiers in Marine Science, 10, 1045138.
Estaque, T., Richaume, J., Bianchimani, O., Schull, Q., Mérigot, B. et al., 2023. Marine heatwaves on the rise: one of the strongest ever observed mass mortality event in temperate gorgonians. Global Change Biology, 29, 6159-6162.
Figuerola-Ferrando, L., Linares C., Zentner Y., López-Sendino P., Garrabou, J., 2022. A rapid assessment method for citizen- scientists to monitor the conservation status of Mediterranean coralligenous assemblages. p. 47-52. In: Proceedings of the 4th Mediterranean Symposium on the conservation of Coralligenous & other Calcareous Bio-Concretions (Genova, Italy, 20-21 September 2022).
Bouafif, C., Ouerghi, A. (Eds). SPA/RAC publications, Tunis. Garrabou, J., Coma, R., Bensoussan, N., Bally, M., Chevaldonné, P. et al., 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: Effects of the 2003 heat wave. Global Change Biology, 15 (5), 1090-1103.
Garrabou, J., Gómez-Gras, D., Ledoux, J.-B., Linares, C., Bensoussan, N. et al., 2019. Collaborative database to track mass mortality events in the Mediterranean Sea. Frontiers in Marine Science, 6, 707.
Garrabou, J., Ledoux, J.-B., Bensoussan, N., Gómez-Gras, D., Linares, C., 2021. Sliding Toward the collapse of Mediterranean coastal marine rocky ecosystems. Ecosystem Collapse and Climate Change, 241, 291-324.
Garrabou, J., Gómez‐Gras, D., Medrano, A., Cerrano, C., Ponti, M. et al., 2022. Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea. Global Change Biology, 28 (19), 5708-5725.
Glynn, P.W., 1996. Coral reef bleaching: facts, hypotheses and implications. Global Change Biology, 2 (6), 495-509.
Gómez‐Gras, D., Linares, C., Dornelas, M., Madin, J.S., Brambilla, V. et al., 2021. Climate change transforms the functional identity of Mediterranean coralligenous assemblages. Ecology Letters, 24 (5), 1038-1051.
Gómez-Gras, D., Bensoussan, N., Ledoux, J.B., López-Sendino, P., Cerrano, C.F. et al., 2022. Exploring the response of a key Mediterranean gorgonian to heat stress across biological and spatial scales. Scientific Reports, 12 (1), 21064.
Grenier, M., Idan, T., Chevaldonné, P., Pérez, T., 2023. Mediterranean marine keystone species on the brink of extinction. Global Change Biology, 29 (7), 1681-1683.
Guinaldo, T., Voldoire, A., Waldman, R., Saux Picart, S., Roquet, H., 2023. Response of the sea surface temperature to heatwaves during the France 2022 meteorological summer. Ocean Science, 19 (3), 629-647.
Juza, M., Fernández-Mora, À., Tintoré, J., 2022. Sub-regional marine heat waves in the Mediterranean Sea from observations: long-term surface changes, sub-surface and coastal responses. Frontiers in Marine Science, 9, 785771.
Kelly, R., Fleming, A., Pecl, G.T., von Gönner, J., Bonn, A., 2020. Citizen science and marine conservation: a global review. Philosophical Transactions of the Royal Society B, 375 (1814), 20190461.
Linares, C., Coma, R., Diaz, D., Zabala, M., Hereu, B. et al., 2005. Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Marine Ecology Progress Series, 305, 127-137.
Linares, C., Figuerola-Ferrando, L., Gómez-Gras, D., Pagés-Escolà, M., Olvera, A. et al., 2022. CorMedNet: building a database on the distribution, demography and conservation status of sessile species for Mediterranean coralligenous assemblages. p. 80-85. In: Proceedings of the 4th Mediterranean Symposium on the conservation of Coralligenous & other Calcareous Bio-Concretions (Genova, Italy, 20-21 September 2022). Bouafif, C., Ouerghi, A. (Eds). SPA/RAC publications, Tunis.
Martínez, J., Leonelli, F.E., García-Ladona, E., Garrabou, J., Kersting, D. et al., 2023. Evolution of marine heatwaves in warming seas: The Mediterranean Sea case study. Frontiers in Marine Science, 10, 1193164.
Mokhtar-Jamaï, K., Pascual, M., Ledoux, J.-B., Coma, R. et al., 2011. From global to local genetic structuring in the red gorgonian Paramuricea clavata: The interplay between oceanographic conditions and limited larval dispersal. Molecular Ecology, 20 (16), 3291-3305.
Neal, B.P., Condit, C., Liu, G., Dos Santos, S., Kahru, M. et al., 2014. When depth is no refuge: cumulative thermal stress increases with depth in Bocas del Toro, Panama. Coral Reefs, 33 (1), 193-205.
Padrón, M., Costantini, F., Bramanti, L., Guizien, K., Abbiati, M., 2018a. Genetic connectivity supports recovery of gorgonian populations affected by climate change. Aquatic Conservation: Marine and Freshwater Ecosystems, 28 (4), 776-787.
Padrón, M., Costantini, F., Baksay, S., Bramanti, L., Guizien, K., 2018b. Passive larval transport explains recent gene flow in a Mediterranean gorgonian. Coral Reefs, 37 (2), 495-506.
Paoli, C., Montefalcone, M., Morri, C., Vassallo, P., Bianchi, C.N., 2017. Ecosystem Functions and Services of the Marine Animal Forests. In: Marine Animal Forests. Rossi, S., Bramanti, L., Gori, A., Orejas Saco del Valle, C. (Eds). Springer International Publishing, Switzerland.
Perez, T., Garrabou, J., Sartoretto, S., Harmelin, J.-G., Francour, P. et al., 2000. Mortalité massive d’invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. Comptes Rendus de l’Académie des Science, 323 (10), 853-865.
Perez, T., Lejeusne, C., Aurelle, D., Bensoussan, N., Boury-esnault, N. et al., 2006. Évaluation des modifications de la biodiversité marine sous l’influence du changement global en Méditerranée nord-occidentale. In : Colloque de restitution IFB – GICC, Réponses adaptatives au changement global : résultats et prospective, 18-20 septembre 2006.
Pérez-Portela, R., Cerro-Gálvez, E., Taboada, S., Tidu, C., Campillo-Campbell, C. et al., 2016. Lonely populations in the deep: genetic structure of red gorgonians at the heads of submarine canyons in the north-western Mediterranean Sea. Coral Reefs, 35 (3), 1013-1026.
Pilczynska, J., Cocito, S., Boavida, J., Serrão, E., Queiroga, H., 2016. Genetic diversity and local connectivity in the Mediterranean red gorgonian coral after mass mortality events. PLoS ONE, 11 (3), e0150590.
Ponti, M., Perlini, R.A., Ventra, V., Grech, D., Abbiati, M. et al., 2014. Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS ONE, 9 (7), e102782.
Ponti, M., Turicchia, E., Ferro, F., Cerrano, C., Abbiati, M., 2018. The understorey of gorgonian forests in mesophotic temperate reefs. Aquatic Conservation: Marine and Freshwater Ecosystems, 28 (5), 1153-1166.
Rivetti, I., Fraschetti, S., Lionello, P., Zambianchi, E., Boero, F., 2014. Global warming and mass mortalities of benthic invertebrates in the Mediterranean Sea. PLoS ONE, 9 (12), e115655.
Rossi, S., Bramanti, L., Gori, A., Orejas, C. 2017. An Overview of the Animal Forests of the World. In: Marine Animal Forests. Rossi, S., Bramanti, L., Gori, A., Orejas Saco del Valle, C. (Eds). Springer International Publishing, Switzerland.
Rossi, S., Bramanti, L., Horta, P., Allcock, L., Carreiro-Silva, M. et al., 2022. Protecting global marine animal forests. Science, 376 (6596), 929-929.
Santangelo, G., Cupido, R., Cocito, S., Bramanti, L., Priori, C. et al., 2015. Effects of increased mortality on gorgonian corals (Cnidaria, Octocorallia): different demographic features may lead affected populations to unexpected recovery and new equilibrium points. Hydrobiologia, 759 (1), 171-187.
Sciascia, R., Guizien, K., Magaldi, M.G., 2022. Larval dispersal simulations and connectivity predictions for Mediterranean gorgonian species: sensitivity to flow representation and biological traits. ICES Journal of Marine Science, 79 (7), 2043-2054.
Smith, K.E., Burrows, M.T., Hobday, A.J., King, N.G., Moore P.J. et al., 2023. Biological impacts of marine heatwaves. Annual Review of Marine Science, 15 (1), 119-145.
Turicchia, E., Ponti, M., Rossi, G., Milanese, M., Di Camillo, C.G. et al., 2021. The reef check mediterranean underwater coastal environment monitoring protocol. Frontiers in Marine Science, 8, 620368.
Venegas, R.M., Oliver, T., Liu, G., Heron, S.F., Clark, S.J. et al., 2019. The rarity of depth refugia from coral bleaching heat stress in the western and central pacific islands. Scientific Reports, 9 (1), 19710.
Vicioso, M., López-Sendino, P., Espeja, S., Garcia, M., Agell, G. et al., 2021. Observadores del mar: transformative marine citizen science. p. 242-244. In: The ocean we want: inclusive and transformative ocean science. Pelegrí J.L., Gili J.M., Martínez de Albéniz M.V. (Eds.). Institut de Ciències del Mar, CSIC, Barcelona.
Weinberg, S., 1976. Revision of the common Octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia, 24 (313), 63-104.
Zentner, Y., Rovira, G., Margarit, N., Ortega, J., Casals, D. et al., 2023. Marine protected areas in a changing ocean: adaptive management can mitigate the synergistic effects of local and climate change impacts. Biological Conservation, 282, 110048.
