IPCC: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate [Pörtner, H.-O. et al.] In press (2019).Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
Gibble, C. et al. Investigation of a largescale Common Murre (Uria aalge) mortality event in California, USA, in 2015. J. Wildl. Dis. 54, 569–574 (2018).PubMed
Article
Google Scholar
Brodeur, R. D., Auth, T. D. & Phillips, A. J. Major shifts in pelagic micronekton and macrozooplankton community structure in an upwelling ecosystem related to an unprecedented marine heatwave. Front. Mar. Sci. 6, 212 (2019).Article
Google Scholar
Le Nohaïc, M. et al. Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia. Sci. Rep. 7, 1–11 (2017).ADS
Article
CAS
Google Scholar
Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS
CAS
PubMed
Article
Google Scholar
Genevier, L. G., Jamil, T., Raitsos, D. E., Krokos, G. & Hoteit, I. Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea. Glob. Change Biol. 25, 2338–2351 (2019).ADS
Article
Google Scholar
Leggat, W. P. et al. Rapid coral decay is associated with marine heatwave mortality events on reefs. Curr. Biol. 29, 2723–2730 (2019).CAS
PubMed
Article
Google Scholar
Green, E. P. & Short, F. T. World Atlas of Seagrasses (University of California Press, 2003).Duarte, C. M. The future of seagrass meadows. Environ. Conserv. 29, 192–206 (2002).Article
Google Scholar
Alongi, D. M. Blue Carbon: Coastal Sequestration for Climate Change Mitigation (Springer, Berlin, 2018).Book
Google Scholar
Blandon, A. & ZuErmgassen, P. S. Quantitative estimate of commercial fish enhancement by seagrass habitat in southern Australia. Estuarine Coast. Shelf Sci. 141, 1–8 (2014).ADS
Article
Google Scholar
Boudouresque, C. F., Mayot, N. & Pergent, G. The outstanding traits of the functioning of the Posidonia oceanica seagrass ecosystem. Biol. Mar. Medit. 13, 109–113 (2006).
Google Scholar
Carr, J., D’odorico, P., McGlathery, K. & Wiberg, P. L. Stability and bistability of seagrass ecosystems in shallow coastal lagoons: Role of feedbacks with sediment resuspension and light attenuation. J. Geophys. Res. Biogeosci. https://doi.org/10.1029/2009JG001103 (2010).Article
Google Scholar
Welsh, D. T. Nitrogen fixation in seagrass meadows: regulation, plant–bacteria interactions and significance to primary productivity. Ecol. Lett. 3, 58–71. https://doi.org/10.1046/j.1461-0248.2000.00111.x (2000).Article
Google Scholar
Duarte, C. M. et al. Seagrass community metabolism: Assessing the carbon sink capacity of seagrass meadows. Glob. Biogeochem. Cycles. https://doi.org/10.1029/2010GB003793 (2010).Article
Google Scholar
Cabaço, S. & Santos, R. Human-induced changes of the seagrass Cymodocea nodosa in Ria Formosa lagoon (Southern Portugal) after a decade. Cah. Biol. Mar. 55, 101–108 (2014).
Google Scholar
Marbà, N., Krause-Jensen, D., Masqué, P. & Duarte, C. M. Expanding Greenland seagrass meadows contribute new sediment carbon sinks. Sci. Rep. 8, 1–8 (2018).Article
CAS
Google Scholar
Bañolas, G., Fernández, S., Espino, F., Haroun, R. & Tuya, F. Evaluation of carbon sinks by the seagrass Cymodocea nodosa at an oceanic island: Spatial variation and economic valuation. Ocean Coast. Manag. 187, 105112 (2020).Article
Google Scholar
Duarte, C. M. & Krause-Jensen, D. Export from seagrass meadows contributes to marine carbon sequestration. Front. Mar. Sci. 4, 13 (2017).
Google Scholar
Duarte, C. M., Middelburg, J. J. & Caraco, N. Major role of marine vegetation on the oceanic carbon cycle. Biogeosci. 2, 1–8 (2005).ADS
CAS
Article
Google Scholar
Kennedy, H. et al. Seagrass sediments as a global carbon sink: Isotopic constraints. Glob. Biogeochem. Cycles https://doi.org/10.1029/2010GB003848 (2010).Article
Google Scholar
Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996 (2006).Article
Google Scholar
Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. 106, 12377–12381 (2009).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
Arias-Ortiz, A. et al. A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat. Clim. Change 8, 338 (2018).ADS
CAS
Article
Google Scholar
Collier, C. J. et al. Optimum temperatures for net primary productivity of three tropical seagrass species. Front. Plant Sci. 8, 1446 (2017).PubMed
PubMed Central
Article
Google Scholar
George, R., Gullström, M., Mangora, M. M., Mtolera, M. S. & Björk, M. High midday temperature stress has stronger effects on biomass than on photosynthesis: a mesocosm experiment on four tropical seagrass species. Ecol. Evol. 8, 4508–4517 (2018).PubMed
PubMed Central
Article
Google Scholar
Savva, I., Bennett, S., Roca, G., Jordà, G. & Marbà, N. Thermal tolerance of Mediterranean marine macrophytes: Vulnerability to global warming. Ecol. Evol. 8, 12032–12043 (2018).PubMed
PubMed Central
Article
Google Scholar
Massa, S. I., Arnaud-Haond, S., Pearson, G. A. & Serrão, E. A. Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in Southern Europe (Ria Formosa, Portugal). Hydrobiologia 619, 195–201 (2009).Article
Google Scholar
Bergmann, N. et al. Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming. Mol. Ecol. 19, 2870–2883 (2010).PubMed
Article
Google Scholar
Franssen, S. U. et al. Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types. Mar. Genomics 15, 65–73 (2014).PubMed
Article
Google Scholar
Qin, L. Z. et al. Influence of regional water temperature variability on the flowering phenology and sexual reproduction of the seagrass Zostera marina in Korean coastal waters. Estuaries Coasts 43, 449–462 (2020).CAS
Article
Google Scholar
Gao, Y. et al. Photosynthetic and metabolic responses of eelgrass Zostera marina L. to short-term high-temperature exposure. J. Oceanol. Limnol. 37, 199–209 (2019).ADS
CAS
Article
Google Scholar
Marín-Guirao, L. et al. Carbon economy of Mediterranean seagrasses in response to thermal stress. Mar. Pollut. Bull. 135, 617–629 (2018).PubMed
Article
CAS
Google Scholar
Costa, M. M., Silva, J., Barrote, I. & Santos, R. Heatwave effects on the photosynthesis and antioxidant activity of the seagrass Cymodocea nodosa under contrasting light regimes. Oceans 2, 448–460 (2021).Article
Google Scholar
de los Santos, C. et al. Recent trend reversal for declining European seagrass meadows. Nat. Commun. 10, 3356 (2019).Cunha, A. H., Assis, J. F. & Serrão, E. A. Reprint of “Seagrasses in Portugal: A most endangered marine habitat”. Aquat. Bot. 115, 3–13 (2014).Article
Google Scholar
Olsen, Y. S., Sánchez-Camacho, M., Marbà, N. & Duarte, C. M. Mediterranean seagrass growth and demography responses to experimental warming. Estuaries Coasts 35, 1205–1213 (2012).Article
Google Scholar
Marín-Guirao, L., Ruiz, J. M., Dattolo, E., Garcia-Munoz, R. & Procaccini, G. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses. Sci. Rep. 6, 1–13 (2016).Article
CAS
Google Scholar
Lüning, K. Seaweeds. Their Environment, Biogeography, and Ecophysiology (Wiley-Interscience, New York, 1990).Lee, K. S., Park, S. R. & Kim, Y. K. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. J. Exp. Mar. Biol. Ecol. 350, 144–175 (2007).Article
Google Scholar
Franssen, S. U. et al. Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proc. Natl. Acad. Sci. 108, 19276–19281 (2011).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
Winters, G., Nelle, P., Fricke, B., Rauch, G. & Reusch, T. B. H. Effects of a simulated heat wave on photophysiology and gene expression of high- and low-latitude populations of Zostera marina. Mar. Ecol. Prog. Ser. 435, 83–95 (2011).ADS
Article
Google Scholar
Maxwell, K. & Johnson, G. N. Chlorophyll fluorescence—A practical guide. J. Exp. Bot. 51, 659–668 (2000).CAS
PubMed
Article
Google Scholar
Schubert, N. et al. Photoacclimation strategies in northeastern Atlantic seagrasses: Integrating responses across plant organizational levels. Sci. Rep. 8, 1–14 (2018).CAS
Article
Google Scholar
Miyake, C., Yonekura, K., Kobayashi, Y. & Yokota, A. Cyclic electron flow within PSII functions in intact chloroplasts from spinach leaves. Plant Cell Physiol. 43, 951–957 (2002).CAS
PubMed
Article
Google Scholar
Rasmusson, L. M., Gullström, M., Gunnarsson, P. C. B., George, R. & Björk, M. Estimation of a whole plant Q10 to assess seagrass productivity during temperature shifts. Sci. Rep. 9, 1–9 (2019).CAS
Article
Google Scholar
Buapet, P. & Björk, M. The role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L. Photosynth. Res. 129, 59–69 (2016).CAS
PubMed
Article
Google Scholar
Mehler, A. H. Studies on reactions of illuminated chloroplasts. II Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys. 34, 339–51 (1951).CAS
PubMed
Article
Google Scholar
Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).CAS
PubMed
Article
Google Scholar
Chalanika De Silva, H. C. & Asaeda, T. Effects of heat stress on growth, photosynthetic pigments, oxidative damage and competitive capacity of three submerged macrophytes. J. Plant Interact. 12, 228–236 (2017).Article
CAS
Google Scholar
Beer, S., Björk, M., Gademann, R. & Ralph, P. Measurements of photosynthetic rates in seagrasses. In Global Seagrass Research Methods pp. 183–198 (Elsevier Science, 2001).Brodersen, K. E., Kühl, M., Nielsen, D. A., Pedersen, O. & Larkum, A. W. Rhizome, root/sediment interactions, aerenchyma and internal pressure changes in seagrasses. In Seagrasses of Australia pp. 393–418; https://doi.org/10.1007/978-3-319-71354-0_13 (Springer, Cham, 2018).Purnama, P. R., Purnama, E. R., Manuhara, Y. S. W., Hariyanto, S. & Purnobasuki, H. Effect of high temperature stress on changes in morphology, anatomy and chlorophyll content in tropical seagrass Thalassia hemprichii. AACL Bioflux 11, 1825–1833 (2018).
Google Scholar
Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D. & Risjani, Y. Anatomical changes in the roots, rhizomes and leaves of seagrass (Cymodocea serrulata) in response to lead. Biodiversitas 20, 2583–2588; https://doi.org/10.13057/biodiv/d200921 (2019).Beca-Carretero, P., Olesen, B., Marbà, N. & Krause-Jensen, D. Response to experimental warming in northern eelgrass populations: comparison across a range of temperature adaptations. Mar. Ecol. Progr. Ser. 589, 59–72; https://doi.org/10.3354/meps12439 (2018).Beca-Carretero, P., Guihéneuf, F., Krause-Jensen, D. & Stengel, D. B. Seagrass fatty acid profiles as a sensitive indicator of climate settings across seasons and latitudes. Mar. Env. Res. 161, 105075; https://doi.org/10.1016/j.marenvres.2020.105075 (2020).Pérez, M. & Romero, J. Photosynthetic response to light and temperature of the seagrass Cymodocea nodosa and the prediction of its seasonality. Aquat. Bot. 43, 51–62; https://doi.org/10.1016/0304-3770(92)90013-9 (1992).Saha, M. et al. Response of foundation macrophytes to near‐natural simulated marine heatwaves. Global Change Biol. 26, 417–430; https://doi.org/10.1111/gcb.14801 (2020).Tutar, O., Marín-Guirao, L., Ruiz, J. M. & Procaccini, G. Antioxidant response to heat stress in seagrasses. A gene expression study. Mar. Environ. Res. 132, 94–102; https://doi.org/10.1016/j.marenvres.2017.10.011 (2017).Moreno‐Marín, F., Brun, F. G. & Pedersen, M. F. Additive response to multiple environmental stressors in the seagrass Zostera marina L. Limnol. Oceanogr. 63, 1528–1544; https://doi.org/10.1002/lno.10789 (2018).Kim, M. et al. Influence of water temperature anomalies on the growth of Zostera marina plants held under high and low irradiance levels. Estuaries Coasts 43, 463–476; https://doi.org/10.1007/s12237-019-00578-2 (2020).Egea, L. G., Jiménez-Ramos, R., Vergara, J. J., Hernández, I. & Brun, F. G. Interactive effect of temperature, acidification and ammonium enrichment on the seagrass Cymodocea nodosa. Mar. Pollut. Bull. 134, 14–26; https://doi.org/10.1016/j.marpolbul.2018.02.029 (2018).Newton, A. & Mudge, S. M. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuarine Coastal Shelf Sci. 57, 73–85; https://doi.org/10.1016/S0272-7714(02)00332-3 (2003).Instituto Hidrográfico. Marés 81/82 Ria de Faro. Estudo das marés de oito estacões da Ria de Faro pp. 13 (Lisbon: Instituto Hidrográfico, 1986).Andrade, J. P. Aspectos Geomorfológicos, Ecológicos e Socioeconómicos da Ria Formosa pp. 91 (Faro: Universidade do Algarve, 1985).Hobday, A.J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238; https://doi.org/10.1016/j.pocean.2015.12.014 (2016).Hobday, A. J. et al. Categorizing and naming marine heatwaves. Oceanogr. 31, 162–173; https://doi.org/10.5670/oceanog.2018.205 (2018).Cunha, A. H., Paulo, D. S., Sousa, I. & Serrão, E. The rediscovery of Caulerpa prolifera in Ria Formosa, Portugal, 60 years after the previous record. Cah. Biol. Mar. 54, 359–364 (2013).
Google Scholar
Huang, B. et al. Improvements of the daily optimum interpolation sea surface temperature (DOISST) Version 2.1. J. Clim. 34, 2923–2939 (2020).ADS
Article
Google Scholar
Reynolds, R. W. et al. Daily high-resolution-blended analyses for sea surface temperature. J. Clim. 20, 5473–5496 (2007).ADS
Article
Google Scholar
Banzon, V., Smith, T. M., Chin, T. M., Liu, C. & Hankins, W. A long-term record of blended satellite and in situ sea-surface temperature for climate monitoring, modelling and environmental studies. Earth Syst. Sci. Data 8, 165–176 (2016).ADS
Article
Google Scholar
Schlegel, R. W. Marine Heatwave Tracker. http://www.marineheatwaves.org/tracker; 10.5281/zenodo.3787872 (2020).Field, C. B., Barros, V., Stocker, T. F. & Dahe, Q. (Eds.). Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change (IPCC) (Cambridge University Press, 2012).Silva, J., Barrote, I., Costa, M. M., Albano, S. & Santos, R. Physiological responses of Zostera marina and Cymodocea nodosa to light-limitation stress. PLoS One 8, e81058 (2013).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
Silva, J. & Santos, R. Can chlorophyll fluorescence be used to estimate photosynthetic production in the seagrass Zostera noltii?. J. Exp. Mar. Biol. Ecol. 307, 207–216 (2004).CAS
Article
Google Scholar
Jassby, A. D. & Platt, T. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547 (1976).ADS
CAS
Article
Google Scholar
Henley, W. J. Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29, 729–739 (1993).Article
Google Scholar
Genty, B., Briantais, J. M. & Baker, N. R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92 (1989).CAS
Article
Google Scholar
Folin, O. & Ciocalteu, V. On tyrosine and tryptophane determinations in proteins. J. Biol. Chem. 73, 627–650 (1927).CAS
Article
Google Scholar
Booker, F. L. & Miller, J. E. Phenylpropanoid metabolism and phenolic composition of soybean [Glycine max (L) Merr] leaves following exposure to ozone. J. Exp. Bot. 49, 1191–1202 (1998).CAS
Article
Google Scholar
Re, R. et al. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 26, 1231–1237 (1999).CAS
Article
Google Scholar
Gillespie, K. M., Chae, J. M. & Ainsworth, E. A. Rapid measurement of total antioxidant capacity in plants. Nat. Protoc. 2, 867–870 (2007).CAS
PubMed
Article
Google Scholar
Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J. A. & Prior, R. L. High-Throughput Assay of Oxygen Radical Absorbance Capacity (ORAC) Using a Multichannel Liquid Handling System Coupled with a Microplate Fluorescence Reader in 96-Well Format. J. Agric. Food Chem. 50, 4437–4444 (2002).CAS
PubMed
Article
Google Scholar
Hodges, D. M., DeLong, J. M., Forney, C. F. & Prange, R. K. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611 (1999).CAS
Article
Google Scholar
Rasband, W.S. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, 1997–2018. https://imagej.nih.gov/ij/ (1997).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2014).Devore, J. & Farnum, N. Applied Statistics for Engineers and Scientists (ed. Brooks/Cole) pp. 656 (Pacific Grove, CA, USA, 1999). More