Marine heatwaves and the collapse of marginal North Atlantic kelp forests
1.
Frölicher, T. L. & Laufkötter, C. Emerging risks from marine heat waves. Nat. Commun.9, 650 (2018).
ADS PubMed PubMed Central Google Scholar
2.
Coumou, D. & Rahmstorf, S. A decade of weather extremes. Nat. Clim. Change2, 491–496 (2012).
ADS Google Scholar
3.
Gaines, S. D. & Denny, M. W. The largest, smallest, highest, lowest, longest, and shortest: Extremes in ecology. Ecology74, 1677–1692 (1993).
Google Scholar
4.
Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr.141, 227–238 (2016).
ADS Google Scholar
5.
Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change9, 306–312 (2019).
ADS Google Scholar
6.
Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change8, 579–587 (2018).
ADS Google Scholar
7.
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 Google Scholar
8.
Oliver, E. C. J. et al. The unprecedented 2015/16 Tasman Sea marine heatwave. Nat. Commun.8, 16101 (2017).
ADS PubMed PubMed Central Google Scholar
9.
IPCC. The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press, Cambridge, 2013).
10.
Jentsch, A. & Beierkuhnlein, C. External geophysics, climate and environment. C. R. Geosci.340 (2008).
11.
Wernberg, T., Smale, D. A. & Thomsen, M. S. A decade of climate change experiments on marine organisms: Procedures, patterns and problems. Glob. Change Biol.18, 1491–1498 (2012).
ADS Google Scholar
12.
Kordas, R. L., Harley, C. D. G. & O’Connor, M. I. Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol.400, 218–226 (2011).
Google Scholar
13.
Hobday, A. J. et al. Categorizing and naming marine heatwaves. Oceanography31, 162–173 (2018).
Google Scholar
14.
Wernberg, T. et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change3, 78–82 (2013).
ADS Google Scholar
15.
Wernberg, T., Krumhansl, K. A., Filbee-Dexter, K. & Pedersen, M. F. In World Seas: An Environmental Evaluation, Vol III: Ecological Issues and Environmental Impacts (ed. Sheppard, C.) (Academic Press, Cambridge, 2019).
16.
Lüning, K., Yarish, C. & Kirkman, H. Seaweeds: Their Environment, Biogeography, and Ecophysiology (Wiley, Hoboken, 1990).
Google Scholar
17.
Assis, J., Araújo, M. B. & Serrão, E. A. Projected climate changes threaten ancient refugia of kelp forests in the North Atlantic. Glob. Change Biol.24, e55–e66 (2018).
ADS Google Scholar
18.
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
19.
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).
Google Scholar
20.
Filbee-Dexter, K., Feehan, C. J. & Scheibling, R. E. Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Mar. Ecol. Prog. Ser.543, 141–152 (2016).
ADS CAS Google Scholar
21.
Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science (80-).353, 169–172 (2016).
ADS CAS Google Scholar
22.
Rogers-Bennett, L. & Catton, C. A. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep.9, 1–9 (2019).
CAS Google Scholar
23.
Arafeh-Dalmau, N. et al. Extreme marine heatwaves alter kelp forest community near its equatorward distribution limit. Front. Mar. Sci.6, 499 (2019).
Google Scholar
24.
Starko, S. et al. Environmental heterogeneity mediates scale-dependent declines in kelp diversity on intertidal rocky shores. PLoS ONE14, e0213191 (2019).
CAS PubMed PubMed Central Google Scholar
25.
Cavanaugh, K. C., Reed, D. C., Bell, T. W., Castorani, M. C. N. & Beas-Luna, R. Spatial variability in the resistance and resilience of giant kelp in southern and Baja California to a multiyear heatwave. Front. Mar. Sci.6, 413 (2019).
Google Scholar
26.
Simonson, E., Scheibling, R. & Metaxas, A. Kelp in hot water: I. Warming seawater temperature induces weakening and loss of kelp tissue. Mar. Ecol. Prog. Ser.537, 89–104 (2015).
ADS CAS Google Scholar
27.
Nepper-Davidsen, J., Andersen, D. T. & Pedersen, M. F. Effects of simulated heat wave scenarios on Saccharina latissima: Prolonged exposure to sub-lethal temperatures may cause irreversible damage. Mar. Ecol. Prog. Ser. 630, 25–39 (2020).
ADS Google Scholar
28.
Hollarsmith, J. A., Buschmann, A. H., Camus, C. & Grosholz, E. D. Varying reproductive success under ocean warming and acidification across giant kelp (Macrocystis pyrifera) populations. J. Exp. Mar. Biol. Ecol.522, 151247 (2020).
Google Scholar
29.
Straub, S. C. Effects of marine heatwaves on canopy forming seaweeds and marine forests (University of Western Australia, Perth, 2019).
Google Scholar
30.
Wernberg, T. et al. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep.8, 1851 (2018).
ADS PubMed PubMed Central Google Scholar
31.
Bernhardt, J. R. & Leslie, H. M. Resilience to climate change in coastal marine ecosystems. Ann. Rev. Mar. Sci.5, 371–392 (2013).
PubMed Google Scholar
32.
Filbee-Dexter, K. & Wernberg, T. Rise of Turfs: A new battlefront for globally declining kelp forests. Bioscience68, 64–76 (2018).
Google Scholar
33.
Krause-Jensen, D. & Duarte, C. M. Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci.9, 737–742 (2016).
ADS CAS Google Scholar
34.
Norderhaug, K. M. & Christie, H. Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure. Estuar. Coast. Shelf Sci.95, 135–144 (2011).
ADS Google Scholar
35.
Bertocci, I., Araújo, R., Oliveira, P. & Sousa-Pinto, I. Potential effects of kelp species on local fisheries. J. Appl. Ecol.52, 1216–1226 (2015).
Google Scholar
36.
Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser.612, 209–215 (2019).
ADS Google Scholar
37.
Albretsen, J., Aure, J., Sætre, R. & Danielssen, D. S. Climatic variability in the Skagerrak and coastal waters of Norway. ICES J. Mar. Sci.69, 758–763 (2012).
Google Scholar
38.
Andersen, G. S., Steen, H., Christie, H., Fredriksen, S. & Emil Moy, F. Seasonal patterns of sporophyte growth, fertility, fouling, and mortality of Saccharina latissima in Skagerrak, Norway: Implications for Forest Recovery. J. Mar. Biol.2011, 690375 (2011).
Google Scholar
39.
Krumhansl, K. & Scheibling, R. Detrital production in Nova Scotian kelp beds: Patterns and processes. Mar. Ecol. Prog. Ser.421, 67–82 (2011).
ADS Google Scholar
40.
Brady-Campbell, M. M., Campbell, D. B. & Harlin, M. M. Productivity of kelp (Laminaria spp.) near the southern limit in the Northwestern Atlantic Ocean. Mar. Ecol. Prog. Ser.18, 79–88 (1984).
ADS Google Scholar
41.
Grace, S. P. Ecomorphology of the Temperate Scleractinian Astrangia poculata: Coral–Macroalgal Interactions in Narragansett Bay (University of Rhode Island, South Kingstown, 2004).
Google Scholar
42.
Moy, F. E. & Christie, H. Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar. Biol. Res.8, 309–321 (2012).
Google Scholar
43.
Lee, J.-A. & Brinkhuis, B. H. Reproductive phenology of Laminaria saccharina (L.) Lamour. (Phaeophyta) at the southern limit of its distribution in the northwestern Atlantic Ocean. J. Phycol.22, 276–285 (1986).
Google Scholar
44.
Feehan, C. J., Grace, S. P. & Narvaez, C. A. Ecological feedbacks stabilize a turf-dominated ecosystem at the southern extent of kelp forests in the Northwest Atlantic. Sci. Rep.9, 7078 (2019).
ADS PubMed PubMed Central Google Scholar
45.
Sjøtun, K. Seasonal lamina growth in two age groups of Laminaria saccharina (L.) Lamour. in Western Norway. Bot. Mar.36, 433–442 (1993).
Google Scholar
46.
Martinez, E. A., Cardenas, L. & Pinto, R. Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Nino 1982/831. J. Phycol.39, 504–508 (2003).
Google Scholar
47.
Edwards, M. & Estes, J. Catastrophe, recovery and range limitation in NE Pacific kelp forests: A large-scale perspective. Mar. Ecol. Prog. Ser.320, 79–87 (2006).
ADS Google Scholar
48.
Ummenhofer, C. C. & Meehl, G. A. Extreme weather and climate events with ecological relevance: A review. Philos. Trans. R. Soc. B Biol. Sci.372, 20160135 (2017).
Google Scholar
49.
Hobday, A. J. & Pecl, G. T. Identification of global marine hotspots: Sentinels for change and vanguards for adaptation action. Rev. Fish Biol. Fish.24, 415–425 (2014).
Google Scholar
50.
Sjøtun, K., Fredriksen, S., Lein, T. E., Rueness, J. & Sivertsen, K. Population studies of Laminaria hyperborea from its northern range of distribution in Norway. Hydrobiologia260–261, 215–221 (1993).
Google Scholar
51.
O’Brien, J. M. & Scheibling, R. E. Low recruitment, high tissue loss, and juvenile mortality limit recovery of kelp following large-scale defoliation. Mar. Biol.165, 171 (2018).
Google Scholar
52.
Borum, K., Pedersen, M. F., Krause-Jensen, D. & Christensen, N. Biomass, photosynthesis and growth of Laminaria saccharina in a high-arctic fjord, NE Greenland. Mar. Biol.141, 11–19 (2002).
Google Scholar
53.
Nielsen, M. M. et al. Growth dynamics of Saccharina latissima (Laminariales, Phaeophyceae) in Aarhus Bay, Denmark, and along the species’ distribution range. Mar. Biol.161, 2011–2022 (2014).
CAS Google Scholar
54.
tom Dieck, I. Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta): Ecological and biogeographical implications. Mar. Ecol. Prog. Ser.100, 253–264 (1993).
ADS Google Scholar
55.
Bolton, J. J. & Lüning, K. Optimal growth and maximal survival temperatures of Atlantic Laminaria species (Phaeophyta) in culture. Mar. Biol.66, 89–94 (1982).
Google Scholar
56.
Andersen, G. S., Pedersen, M. F. & Nielsen, S. L. Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales, Phaeophyceae). J. Phycol.49, 689–700 (2013).
CAS PubMed Google Scholar
57.
Jump, A. S. & Penuelas, J. Running to stand still: Adaptation and the response of plants to rapid climate change. Ecol. Lett.8, 1010–1020 (2005).
Google Scholar
58.
Niu, S. et al. Plant growth and mortality under climatic extremes: An overview. Environ. Exp. Bot.98, 13–19 (2014).
Google Scholar
59.
Bennett, S., Wernberg, T., Arackal Joy, B., de Bettignies, T. & Campbell, A. H. Central and rear-edge populations can be equally vulnerable to warming. Nat. Commun.6, 10280 (2015).
ADS CAS PubMed PubMed Central Google Scholar
60.
Gorman, D. & Connell, S. D. Recovering subtidal forests in human-dominated landscapes. J. Appl. Ecol.46, 1258–1265 (2009).
Google Scholar
61.
Burek, K., O’Brien, J. & Scheibling, R. Wasted effort: Recruitment and persistence of kelp on algal turf. Mar. Ecol. Prog. Ser.600, 3–19 (2018).
ADS Google Scholar
62.
Norderhaug, K. M. et al. Effects of climate and eutrophication on the diversity of hard bottom communities on the Skagerrak coast 1990–2010. Mar. Ecol. Prog. Ser.530, 29–46 (2015).
ADS CAS Google Scholar
63.
Gorgula, S. & Connell, S. Expansive covers of turf-forming algae on human-dominated coast: The relative effects of increasing nutrient and sediment loads. Mar. Biol.145, 613–619 (2004).
Google Scholar
64.
Bennett, S., Duarte, C. M., Marbà, N. & Wernberg, T. Integrating within-species variation in thermal physiology into climate change ecology. Philos. Trans. R. Soc. B Biol. Sci.374, 20180550 (2019).
Google Scholar
65.
Lüning, K. Temperature tolerance and biogeography of seaweeds: The marine algal flora of Helgoland (North Sea) as an example. Helgoländer Meeresunters. 38, 305–317 (1984).
Google Scholar
66.
Lee, J. A. & Brinkhuis, B. H. Seasonal light and temperature interaction effects on development of Laminaria saccharina (Phaeophyta) gametophytes and juvenile sporophytes. J. Phycol.24, 181–191 (1988).
Google Scholar
67.
Pedersen, M. F. et al. Detrital carbon production and export in high latitude kelp forests. Oecologia192, 227–239 (2020).
ADS PubMed Google Scholar
68.
Schlegel, R. W. & Smit, A. J. heatwaveR: Detect Heatwaves and Cold-Spells. (2019).
69.
Wasko, C. & Sharma, A. Quantile regression for investigating scaling of extreme precipitation with temperature. Water Resour. Res.50, 3608–3614 (2014).
ADS Google Scholar
70.
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw.67, 1–48 (2015).
Google Scholar
71.
Schlegel, R. W. Marine Heatwave Tracker. https://doi.org/10.5281/zenodo.3787872 (2020).
Article Google Scholar More