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Heatwaves during low tide are critical for the physiological performance of intertidal macroalgae under global warming scenarios

  • 1.

    Umanzor, S., Ladah, L. & Calderon-aguilera, L. E. Testing the relative importance of intertidal seaweeds as ecosystem engineers across tidal heights. J. Exp. Mar. Bio. Ecol. 511, 100–107 (2018).

    Article  Google Scholar 

  • 2.

    Smale, D. A., Burrows, M. T., Moore, P., O’Connor, N. & Hawkins, S. J. Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecol. Evol. 3, 4016–4038 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 3.

    Krause-Jensen, D. & Duarte, C. M. Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci. 9, 737–742 (2016).

    ADS  CAS  Article  Google Scholar 

  • 4.

    King, N. G., McKeown, N. J., Smale, D. A. & Moore, P. J. The importance of phenotypic plasticity and local adaptation in driving intraspecific variability in thermal niches of marine macrophytes. Ecography (Cop.) 41, 1469–1484 (2018).

    Article  Google Scholar 

  • 5.

    Helmuth, B., Mieszkowska, N., Moore, P. & Hawkins, S. J. Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu. Rev. Ecol. Evol. Syst. 37, 373–404 (2006).

    Article  Google Scholar 

  • 6.

    Fernández, Á. et al. Additive effects of emersion stressors on the ecophysiological performance of two intertidal seaweeds. Mar. Ecol. Prog. Ser. 536, 135–147 (2015).

    ADS  Article  Google Scholar 

  • 7.

    IPCC. Summary for Policymakers. In: Climate Change 2014, Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds. Edenhofer, O. et al.). (Cambridge University Press, Cambridge, 2014).

  • 8.

    Meehl, G. A. & Tebaldi, C. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997 (2004).

    ADS  CAS  Article  PubMed  Google Scholar 

  • 9.

    Koffi, B. & Koffi, E. Heat waves across Europe by the end of the 21st century: multiregional climate simulations. Clim. Res. 36, 153–168 (2008).

    Article  Google Scholar 

  • 10.

    Lüning, K. Temperature, salinity and other abiotic factors in Seaweeds. Their Environment, Biogeography and Ecophysiology (Wiley, New York, 1990).

    Google Scholar 

  • 11.

    Pang, S. J., Jin, Z. H., Sun, J. Z. & Gao, S. Q. Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture 262, 493–503 (2007).

    Article  Google Scholar 

  • 12.

    Nielsen, S. L., Nielsen, H. D. & Pedersen, M. F. Juvenile life stages of the brown alga Fucus serratus L. Are more sensitive to combined stress from high copper concentration and temperature than adults. Mar. Biol. 161, 1895–1904 (2014).

    CAS  Article  Google Scholar 

  • 13.

    Schonbeck, M. W. & Norton, T. A. The effects on intertidal fucoid algae of exposure to air under various conditions. Bot. Mar. 23, 141–148 (1980).

    Article  Google Scholar 

  • 14.

    Pearson, G. A., Lago-Leston, A. & Mota, C. Frayed at the edges: Selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. J. Ecol. 97, 450–462 (2009).

    Article  Google Scholar 

  • 15.

    Ferreira, J. G., Arenas, F., Martínez, B., Hawkins, S. J. & Jenkins, S. R. Physiological response of fucoid algae to environmental stress: comparing range centre and southern populations. New Phytol. 202, 1157–1172 (2014).

    Article  PubMed  Google Scholar 

  • 16.

    Smale, D. A. & Wernberg, T. Extreme climatic event drives range contraction of a habitat-forming species. Proc. R. Soc. B. 280, 20122829 (2013).

    Article  PubMed  Google Scholar 

  • 17.

    Jueterbock, A. et al. Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: Acclimatization potential to climate change. Mar. Genomics 13, 27–36 (2014).

    Article  PubMed  Google Scholar 

  • 18.

    Hurd, K., Harrison, P.J., Bischof, K. & Lobban, C.S. Light and photosynthesis in Seaweed Ecology and Physiology (eds. Hurd, K., Harrison, P.J., Bischof, K. & Lobban, C.S.) 176–237. (Cambridge University Press, Cambridge, 2014).

  • 19.

    Mota, C. F. et al. Differentiation in fitness-related traits in response to elevated temperatures between leading and trailing edge populations of marine macrophytes. PLoS ONE 13, 1–17 (2018).

    Article  CAS  Google Scholar 

  • 20.

    Martínez, B. et al. Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit. Oecologia 170, 341–353 (2012).

    ADS  Article  PubMed  Google Scholar 

  • 21.

    Pereira, T. R., Engelen, A. H., Pearson, G. A., Valero, M. & Serrão, E. A. Response of kelps from different latitudes to consecutive heat shock. J. Exp. Mar. Bio. Ecol. 463, 57–62 (2015).

    Article  Google Scholar 

  • 22.

    Madsen, T. V. & Maberly, S. C. A comparison of air and water as environments for photosynthesis by the intertidal alga Fucus spiralis (Phaeophyta). J. phycol. 26(1), 24–30 (1990).

    Article  Google Scholar 

  • 23.

    Contreras-Porcia, L., López-Cristoffanini, Meynard, A., & Kumar, M. Tolerance pathways to desiccation stress in seaweeds. In Systems Biology of Marine Ecosystems (eds. Kumar, M. & Ralhp, P.) 13–29. (Springer, Berlin, 2017).

  • 24.

    Helmuth, B. et al. Climate change and latitudinal patterns of intertidal thermal stress. Science 298, 1015–1017 (2002).

    ADS  CAS  Article  PubMed  Google Scholar 

  • 25.

    King, N. G. et al. Cumulative stress restricts niche filling potential of habitat-forming kelps in a future climate. Funct. Ecol. 32, 288–299 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 26.

    Hereward, H. F. R., King, N. G. & Smale, D. A. Intra-annual variability in responses of a canopy forming kelp to cumulative low tide heat stress: implications for populations at the trailing range edge. J. Phycol. 56, 146–158 (2019).

    Article  PubMed  Google Scholar 

  • 27.

    Fernández, C. The retreat of large brown seaweeds on the north coast of Spain: the case of Saccorhiza polyschides. Eur. J. Phycol. 46, 352–360 (2011).

    Article  Google Scholar 

  • 28.

    Méndez-Sandín, M. & Fernández, C. Changes in the structure and dynamics of marine assemblages dominated by Bifurcaria bifurcata and Cystoseira species over three decades (1977–2007). Estuar. Coast. Shelf Sci. 175, 46–56 (2016).

    ADS  Article  Google Scholar 

  • 29.

    Wilson, K. L., Skinner, M. A. & Lotze, H. K. Projected 21st-century distribution of canopy-forming seaweeds in the Northwest Atlantic with climate change. Divers. Distrib. 25, 582–602 (2019).

    Article  Google Scholar 

  • 30.

    Martínez, B., Viejo, R. M., Carreño, F. & Aranda, S. C. Habitat distribution models for intertidal seaweeds: Responses to climatic and non-climatic drivers. J. Biogeogr. 39, 1877–1890 (2012).

    Article  Google Scholar 

  • 31.

    Nyström, M. et al. Confronting feedbacks of degraded marine ecosystems. Ecosystems 15, 695–710 (2012).

    Article  Google Scholar 

  • 32.

    O’Brien, B. S., Mello, K., Litterer, A. & Dijkstra, J. A. Seaweed structure shapes trophic interactions: a case study using a mid-trophic level fish species. J. Exp. Mar. Biol. Ecol. 506, 1–8 (2018).

    Article  Google Scholar 

  • 33.

    Voerman, S. E., Llera, E. & Rico, J. M. Climate driven changes in subtidal kelp forest communities in NW Spain. Mar. Environ. Res. 90, 119–127 (2013).

    CAS  Article  PubMed  Google Scholar 

  • 34.

    Duarte, L. et al. Recent and historical range shifts of two canopy-forming seaweeds in North Spain and the link with trends in sea surface temperature. Acta Oecol. 51, 1–10 (2013).

    ADS  Article  Google Scholar 

  • 35.

    Viejo, R. M., Martínez, B., Arrontes, J., Astudillo, C. & Herna, L. Reproductive patterns in central and marginal populations of a large brown seaweed: drastic changes at the southern range limit. Ecography 34, 75–84 (2011).

    Article  Google Scholar 

  • 36.

    Duarte, L. & Viejo, R. M. Environmental and phenotypic heterogeneity of populations at the trailing range-edge of the habitat-forming macroalga Fucus serratus. Mar. Environ. Res. 136, 16–26 (2018).

    CAS  Article  PubMed  Google Scholar 

  • 37.

    Thomsen, M. S. et al. Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front. Mar. Sci. 6, 1–10 (2019).

    Article  Google Scholar 

  • 38.

    Darling, E. S. & Côté, I. M. Quantifying the evidence for ecological synergies. Ecol. Lett. 11, 1278–1286 (2008).

    Article  Google Scholar 

  • 39.

    Gómez-Gesteira, M. et al. The state of climate in NW Iberia. Clim. Res. 48, 109–144 (2011).

    Article  Google Scholar 

  • 40.

    Kersting, D.K. Cambio Climático en El Medio Marino Español: Impactos, Vulnerabilidad y Adaptación. Oficina Española de Cambio Climático, Ministerio de Agricultura, Alimentación y Medio Ambiente. Madrid. http://cort.as/-HXq9 (2016).

  • 41.

    Philippart, C. J. M. et al. Impacts of climate change on European marine ecosystems: observations, expectations and indicators. J. Exp. Mar. Biol. Ecol. 400, 52–69 (2011).

    Article  Google Scholar 

  • 42.

    Lima, F. P., Ribeiro, P. A., Queiroz, N., Hawkins, S. J. & Santos, A. M. Do distributional shifts of northern and southern species of algae match the warming pattern?. Glob. Chang. Biol. 13, 2592–2604 (2007).

    ADS  Article  Google Scholar 

  • 43.

    Díez, I., Muguerza, N., Santolaria, A., Ganzedo, U. & Gorostiaga, J. M. Seaweed assemblage changes in the eastern Cantabrian Sea and their potential relationship to climate change. Estuar. Coast. Shelf Sci. 99, 108–120 (2012).

    ADS  Article  Google Scholar 

  • 44.

    Piñeiro-Corbeira, C., Barreiro, R. & Cremades, J. Decadal changes in the distribution of common intertidal seaweeds in Galicia (NW Iberia). Mar. Environ. Res. 113, 106–115 (2016).

    Article  CAS  PubMed  Google Scholar 

  • 45.

    García-Fernández, A. & Bárbara, I. Studies of Cystoseira assemblages in Northern Atlantic Iberia. Ann. del Jard. Bot. Madrid 73, 1–21 (2016).

    Google Scholar 

  • 46.

    García, A. G., Olabarria, C., Arrontes, J., Álvarez, Ó. & Viejo, R. M. Spatio-temporal dynamics of Codium populations along the rocky shores of N and NW Spain. Mar. Environ. Res. 140, 394–402 (2018).

    Article  CAS  PubMed  Google Scholar 

  • 47.

    Fernández, C. Current status and multidecadal biogeographical changes in rocky intertidal algal assemblages: the northern Spanish coast. Estuar. Coast. Shelf Sci. 171, 35–40 (2016).

    ADS  Article  Google Scholar 

  • 48.

    Eggert, A. Seaweed responses to temperature. In Seaweed Biology. Novel Insights into Ecophysiology, Ecology and Utilization (eds. Wiencke, C. & Bischof, K) 47–66 (Springer, Berlin, 2012).

  • 49.

    Karsten, U. Seaweed acclimation to salinity and desiccation stress. In Seaweed biology. Novel Insights into Ecophysiology, Ecology and Utilization (eds. Wiencke, C. & Bischof, K) 87–108 (Springer, Berlin, 2012).

  • 50.

    Phelps, C. M., Boyce, M. C. & Huggett, M. J. Future climate change scenarios differentially affect three abundant algal species in southwestern Australia. Mar. Environ. Res. 126, 69–80 (2017).

    CAS  Article  PubMed  Google Scholar 

  • 51.

    Olabarria, C., Arenas, F., Fernández, Á., Troncoso, J. S. & Martínez, B. Physiological responses to variations in grazing and light conditions in native and invasive fucoids. Mar. Environ. Res. 139, 151–161 (2018).

    CAS  Article  PubMed  Google Scholar 

  • 52.

    Schagerl, M. & Möstl, M. Drought stress, rain and recovery of the intertidal seaweed. Fucus spiralis. Mar. Biol. 158, 2471–2479 (2011).

    Article  Google Scholar 

  • 53.

    Lamela-Silvarrey, C., Fernández, C., Anadón, R. & Arrontes, J. Fucoid assemblages on the north coast of Spain: Past and present (1977–2007). Bot. Mar. 55, 199–207 (2012).

    Article  Google Scholar 

  • 54.

    Martínez, B., Arenas, F., Trilla, A., Viejo, R. M. & Carreño, F. Combining physiological threshold knowledge to species distribution models is key to improving forecasts of the future niche for macroalgae. Glob. Change Biol. 21, 1422–1433 (2014).

    ADS  Article  Google Scholar 

  • 55.

    Piñeiro-Corbeira, C., Barreiro, R., Cremades, J. & Arenas, F. Seaweed assemblages under a climate change scenario: Functional responses to temperature of eight intertidal seaweeds match recent abundance shifts. Sci. Rep. 8, 1–9 (2018).

    Article  CAS  Google Scholar 

  • 56.

    Figueroa, F. L. et al. Yield losses and electron transport rate as indicators of thermal stress in Fucus serratus (Ochrophyta). Algal Res. 41, 101560 (2019).

    Article  Google Scholar 

  • 57.

    Davison, I. R. & Pearson, G. A. Stress tolerance in intertidal seaweeds. J. Phycol. 32, 197–211 (1996).

    Article  Google Scholar 

  • 58.

    Schreiber, U., Bilger, W. & Neubauer, C. Chlorophyll Fluorescence as a Nonintrusive Indicator for Rapid Assessment of In Vivo Photosynthesis. In Ecophysiology of photosynthesis (eds. Schulze, E.D. & Caldwell, M.M.) 49–70 (Springer, Berlin, 2003).

  • 59.

    Hurd, K., Harrison, P.J., Bischof, K. & Lobban, C.S. Physico-chemical factors as environmental stressors in seaweed biology. In Seaweed Ecology and Physiology (eds. Hurd, K., Harrison, P.J., Bischof, K. & Lobban, C.S.) 294–348 (Cambridge University Press, Cambridge, 2014).

  • 60.

    Kumar, M. et al. Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ. Exp. Bot. 72, 194–201 (2011).

    CAS  Article  Google Scholar 

  • 61.

    Bischof, K. & Rautenberger, R. Seaweed responses to environmental stress: Reactive oxygen and antioxidative strategies. In Seaweed biology. Novel insights into Ecophysiology, Ecology and Utilization (eds. Wiencke, C., Bischof, K.) 109–134 (Springer, Berlin, 2012).

  • 62.

    Allakhverdiev, S. I. et al. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 98, 541–550 (2008).

    CAS  Article  PubMed  Google Scholar 

  • 63.

    Mota, C. F., Engelen, A. H., Serrão, E. A. & Pearson, G. A. Some don’t like it hot: Microhabitat-dependent thermal and water stresses in a trailing edge population. Funct. Ecol. 29, 640–649 (2015).

    Article  Google Scholar 

  • 64.

    Hunt, L. J. H. & Denny, M. W. Desiccation protection and disruption: A trade-off for an intertidal marine alga. J. Phycol. 44, 1164–1170 (2008).

    Article  PubMed  Google Scholar 

  • 65.

    Staehr, P. A. & Wernberg, T. Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J. Phycol. 45, 91–99 (2009).

    CAS  Article  PubMed  Google Scholar 

  • 66.

    Davison, I. R. & Davison, J. O. The effect of growth temperature on enzyme activities in the brown alga Laminaria saccharina. Br. Phycol. J. 22, 77–87 (1987).

    Article  Google Scholar 

  • 67.

    Young, E. B., Dring, M. J., Savidge, G., Birkett, D. A. & Berges, J. A. Seasonal variations in nitrate reductase activity and internal N pools in intertidal brown algae are correlated with ambient nitrate concentrations. Plant, Cell Environ. 30, 764–774 (2007).

    CAS  Article  Google Scholar 

  • 68.

    Monteiro, C. et al. Canopy microclimate modification in central and marginal populations of a marine macroalga. Mar. Biodivers. 49, 415–424 (2019).

    Article  Google Scholar 

  • 69.

    Dawes, C. J. Physiological ecology. In Marine Botany (ed. Dawes, C.J.) (Wiley, New York, 1998).

  • 70.

    Rohde, S., Hiebenthal, C., Wahl, M., Karez, R. & Bischof, K. Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: Effects of light deficiency and epibionts on growth and photosynthesis. Eur. J. Phycol. 43, 143–150 (2008).

    Article  Google Scholar 

  • 71.

    Lüning, K. Seaweed vegetation of the cold and warm temperate regions of the northern hemisphere. In Seaweeds. Their Environment, Biogeography and Ecophysiology. (ed. Lüning, K.) (Wiley, New York, 1990).

  • 72.

    Schiel, D. R., Lilley, S. A., South, P. M. & Coggins, J. H. J. Decadal changes in sea surface temperature, wave forces and intertidal structure in New Zealand. Mar. Ecol. Prog. Ser. 548, 77–95 (2016).

    ADS  Article  Google Scholar 

  • 73.

    Fernández de la Hoz, C. F. et al. OCLE: a European open access database on climate change effects on littoral and oceanic ecosystems. Prog. Oceanogr. 168, 222–231 (2018).

    ADS  Article  Google Scholar 

  • 74.

    Fernández de la Hoz, C., Ramos, E., Puente, A. & Juanes, J. A. Climate change induced range shifts in seaweeds distributions in Europe. Mar. Environ. Res. 148, 1–11 (2019).

    Article  CAS  Google Scholar 

  • 75.

    Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • 76.

    Halekoh, U., Højsgaard, S. & Yan, J. The R package geepack for generalized estimating equations. J. Stat. Softw. 15, 1–11 (2006).

    Article  Google Scholar 

  • 77.

    Fox, J. Applied Regression Analysis and Generalized Linear Models 3rd edn. (Sage, Thousand Oaks, 2016).

    Google Scholar 


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