Trait gradients inform predictions of seagrass meadows changes to future 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:
18
05
2021
accepted:
17
08
2021
entrez:
14
9
2021
pubmed:
15
9
2021
medline:
15
9
2021
Statut:
epublish
Résumé
Comparing populations across temperature gradients can inform how global warming will impact the structure and function of ecosystems. Shoot density, morphometry and productivity of the seagrass Posidonia oceanica to temperature variation was quantified at eight locations in Sardinia (western Mediterranean Sea) along a natural sea surface temperature (SST) gradient. The locations are spanned for a narrow range of latitude (1.5°), allowing the minimization of the effect of eventual photoperiod variability. Mean SST predicted P. oceanica meadow structure, with increased temperature correlated with higher shoot density, but lower leaf and rhizome width, and rhizome biomass. Chlorophyll a (Chl-a) strongly impacted seagrass traits independent of SST. Disentangling the effects of SST and Chl-a on seagrass meadow shoot density revealed that they work independently, but in the same direction with potential synergism. Space-for-time substitution predicts that global warming will trigger denser seagrass meadows with slender shoots, fewer leaves, and strongly impact seagrass ecosystem. Future investigations should evaluate if global warming will erode the ecosystem services provided by seagrass meadows.
Identifiants
pubmed: 34518602
doi: 10.1038/s41598-021-97611-x
pii: 10.1038/s41598-021-97611-x
pmc: PMC8438026
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
18107Informations de copyright
© 2021. The Author(s).
Références
Lovejoy, T. E. & Hannah, L. Biodiversity and Climate Change: Transforming the Biosphere (Yale University Press, 2005).
Bellard, C., Berttelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).
pubmed: 22257223
pmcid: 3880584
doi: 10.1111/j.1461-0248.2011.01736.x
Hawkins, B. A. et al. Energy, water, and broad scale geographic patterns of species richness. Ecology 84, 3105–3117 (2003).
doi: 10.1890/03-8006
Pearce, A. & Feng, M. Observation of warming on the western Australia continental shelf. Mar. Freshwater Res. 58, 914–920 (2007).
doi: 10.1071/MF07082
Ridgway, K. R. Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys. Res. Lett. 34, L13613 (2007).
doi: 10.1029/2007GL030393
Chen, L., Huang, J. G., Ma, Q. & Hanninen, H. Long-term changes in the impacts of global warming on leaf phenology of four temperature tree species. Glob. Change Biol. 25(3), 997–1004 (2018).
doi: 10.1111/gcb.14496
Harley, C. D. G. et al. The impacts of climate change in coastal marine systems. Ecol. Lett. 9, 228–241 (2006).
pubmed: 16958887
doi: 10.1111/j.1461-0248.2005.00871.x
Poloczanska, E. S. et al. Climate change and Australian marine life. Oceanogr. Mar. Biol. 45, 407–478 (2007).
Maltby, K. M. et al. Projected impacts of warming seas on commercially fished species at a biogeographic boundary of the European continental shelf. J. Appl. Ecol. 57, 2222–2233 (2019).
doi: 10.1111/1365-2664.13724
Melzner, F., Buchholz, B., Wolf, F., Panknin, U. & Wall, M. Ocean winter warming induced starvation of predator and prey. Proc. R. Soc. B 287, 20200970 (2020).
pubmed: 32673558
pmcid: 7423679
doi: 10.1098/rspb.2020.0970
He, H. et al. Turning up the heat: Warming influences plankton biomass and spring phenology in subtropical waters characterized by extensive fish omnivory. Oecologia 194, 251–265 (2020).
pubmed: 32964292
doi: 10.1007/s00442-020-04758-x
Pagès-Escolà, M. et al. Divergent responses to warming of two common co-occurring Mediterranean bryozoans. Sci. Rep. 8, 17455 (2018).
pubmed: 30498253
pmcid: 6265274
doi: 10.1038/s41598-018-36094-9
Gómez-Gras, D. et al. Response diversity in Mediterranean coralligenous assemblages facing climate change: Insights from a multispecific thermotolerance experiment. Ecol. Evol. 9(7), 4168–4180 (2019).
pubmed: 31015996
pmcid: 6468064
doi: 10.1002/ece3.5045
Huret, M., Bourriau, P., Doray, M., Gohin, F., Petitgas, P. Survey timing vs. ecosystem scheduling: Degree-days to underpin observed interannual variability in marine ecosystems. Progr. Oceanogr. 166, 30–40 (2018).
Strelkov, P., Katolikova, M. & Väinolä, R. Temporal change of the Baltic sea-North Sea mussle hybrid zone over two decades. Mar. Biol. 164, 1–14 (2017).
doi: 10.1007/s00227-017-3249-z
Chiba, S. et al. Temperature and zooplankton size structure: Climate control and basin-scale comparison in the North Pacific. Ecol. Evol. 5(4), 968–978 (2015).
pubmed: 25750722
pmcid: 4338978
doi: 10.1002/ece3.1408
Wernberg, T. et al. Seaweed communities in retreat from ocean warming. Curr. Biol. 21, 1–5 (2011).
doi: 10.1016/j.cub.2011.09.028
Block, S. E., Olesen, E. & Krause-Jensen, D. Life history events of eelgrass Zostera marina L. populations across gradients of latitude and temperature. Mar. Ecol. Progr. Ser. 590, 79–93 (2018).
doi: 10.3354/meps12479
Cure, K. et al. Spatiotemporal patterns of abundance and ecological requirements of a labrid’s juveniles reveal conditions for establishment success and range shift capacity. J. Exp. Mar. Biol. Ecol. 500, 34–45 (2018).
doi: 10.1016/j.jembe.2017.12.006
Smale, D. A. et al. Environmental factors influencing primary productivity of the forest-forming kelp Laminaria hyperborea in the northeast Atlantic. Sci. Rep. 10, 12161 (2020).
pubmed: 32699214
pmcid: 7376248
doi: 10.1038/s41598-020-69238-x
Ruiz, J. M. et al. Experimental evidence of warming-induced flowering in the Mediterranean seagrass Posidonia oceanica. Mar. Pollut. Bull. 134, 49–54 (2018).
pubmed: 29102072
doi: 10.1016/j.marpolbul.2017.10.037
Rasconi, S., Winter, K. & Kainz, M. J. Temperature increase and fluctuation induce phytoplankton biodiversity loss—Evidence from a multi-seasonal mesocosm experiment. Ecol. Evol. 7, 2936–2946 (2017).
pubmed: 28479993
pmcid: 5415537
doi: 10.1002/ece3.2889
Smale, D. A., Wernberg, T., Yunnie, A. L. E. & Vance, T. The rise of Laminaria ochroleuca in the Western English Channel (UK) and preliminary comparisons with its competitor and assemblage dominant Laminaria hyperborea. Mar. Ecol. 36, 1033–1044 (2015).
doi: 10.1111/maec.12199
Pansch, C. & Hibenthal, C. A new mesocosm system to study the effects of environmental variability on marine species and communities. Limnol. Oceanogr. Methods 17, 145–162 (2019).
doi: 10.1002/lom3.10306
Doo, S. S. The challenges of detecting and attributing ocean acidification impacts on marine ecosystems. ICES J. Mar. Sci. 77, 2411–2422 (2020).
doi: 10.1093/icesjms/fsaa094
Kim, J.-H. et al. Global warming offsets the ecophysiological stress of ocean acidification on temperate crustose coralline algae. Mar. Pollut. Bull. 157, 111324 (2020).
pubmed: 32658689
doi: 10.1016/j.marpolbul.2020.111324
Bonaviri, C., Graham, M., Gianguzza, P. & Shears, N. T. Warmer temperatures reduce the influence of an important keystone predator. J. Anim. Ecol. 86, 490–500 (2017).
pubmed: 28075025
doi: 10.1111/1365-2656.12634
Carr, L. A., Gittman, R. K. & Bruno, J. F. Temperature influences herbivory and algal biomass in the Galápagos Islands. Front. Mar. Sci. 5, 279 (2018).
doi: 10.3389/fmars.2018.00279
De Frenne, P. et al. Latitudinal gradients as natural laboratories to infer species’ responses to temperature. J. Ecol. 101, 784–795 (2013).
doi: 10.1111/1365-2745.12074
Behrenfeld, M. J. Climate-mediated dance of the plankton. Nat. Clim. Change 4(10), 880–887 (2014).
doi: 10.1038/nclimate2349
Behrenfeld, M. J. et al. Climate-driven trends in contemporary ocean productivity. Nature 444(7120), 752–755 (2006).
pubmed: 17151666
doi: 10.1038/nature05317
Bricaud, A., Morel, A., Babin, M., Allali, K. & Hervè, C. Variations of light absorption by suspended particles with chlorophyll a concentration in oceanic waters: Analysis and implications for bio-optical models. J. Geophys. Res. 103, 31033–31044 (1998).
doi: 10.1029/98JC02712
Jaud, T., Dragon, A. C., Garcia, J. V. & Guinet, C. Relationship between chlorophyll a concentration, light attenuation and diving depth of the southern elephant seal Mirounga leonina. PLoS ONE 7(10), e47444 (2012).
pubmed: 23082166
pmcid: 3474817
doi: 10.1371/journal.pone.0047444
Dunstan, P. K. et al. Global patterns of change and variation in sea surface temperature and chlorophyll a. Sci. Rep. 8, 14624 (2018).
pubmed: 30279444
pmcid: 6168485
doi: 10.1038/s41598-018-33057-y
Sanford, E. & Kelly, M. W. Local adaptation of marine invertebrates. Annu. Rev. Mar. Sci. 3, 509–535 (2011).
doi: 10.1146/annurev-marine-120709-142756
Oliver, T. A. & Palumbi, S. R. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 30, 429–440 (2011).
doi: 10.1007/s00338-011-0721-y
Baumann, H. & Conover, D. O. Adaptation to climate change: Contrasting patterns of thermal-reaction-norm evolution in Pacific versus Atlantic silversides. Proc. R. Soc. B 278(1716), 2265–2273 (2011).
pubmed: 21208956
pmcid: 3119017
doi: 10.1098/rspb.2010.2479
Castillo, K. D., Ries, J. B., Weiss, J. M. & Lima, F. P. Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat. Clim. Change 2(10), 756–760 (2012).
doi: 10.1038/nclimate1577
Thomas, M. K., Kremer, C. T., Klausmeier, C. T. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 6110 (2012).
doi: 10.1126/science.1224836
Chefaoui, R. M., Duarte, C. M. & Serrao, E. A. Dramatic loss of seagrass habitat under projected climate change in the Mediterranean Sea. Glob. Change Biol. 24(10), 4919–4928 (2018).
doi: 10.1111/gcb.14401
Duarte, B. et al. Climate change impacts on seagrass meadows and macroalgal forests: an integrative perspective on acclimation and adaptation potential. Front. Mar. Sci. 5, 190 (2018).
doi: 10.3389/fmars.2018.00190
Hemminga, M. A. & Duarte, C. M. Seagrass Ecology (Cambridge University Press, 2000).
doi: 10.1017/CBO9780511525551
Larkum, A. W. D., Orth, R. J. & Duarte, C. M. Seagrasses: Biology, Ecology and Conservation (Springer, 2006).
Fourqurean, J. W. et al. Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 5(7), 505–509 (2012).
doi: 10.1038/ngeo1477
Fonseca, M. S. & Cahalan, J. A. A preliminary evaluation of wave attenuation by four species of seagrass. Estuar. Coast. Shelf Sci. 35, 565–576 (1992).
doi: 10.1016/S0272-7714(05)80039-3
Fonseca, M. S. & Koehl, M. A. R. Flow in Seagrass canopies: the influence of patch width. Estuar. Coast. Shelf Sci. 67, 1–9 (2006).
doi: 10.1016/j.ecss.2005.09.018
Telesca, L. et al. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep. 5, 12505 (2015).
pubmed: 26216526
pmcid: 4516961
doi: 10.1038/srep12505
Marbà, N. & Duarte, C. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Glob. Change Biol. 16, 2366–2375 (2010).
Beca-Carretero, P., Guiheneuf, F., Krause-Jensen, D. & Stengel, D. B. Seagrass fatty acid profiles as a sensitive indicator of climate settings across seasons and latitudes. Mar. Environ. Res. 161, 105075 (2020).
pubmed: 32739623
doi: 10.1016/j.marenvres.2020.105075
Marín-Guirao, L., Ruiz, J., Dattolo, E., Garcia-Munoz, R. & Procaccini, G. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses. Sci. Rep. 6, 28615 (2016).
pubmed: 27345831
pmcid: 4921816
doi: 10.1038/srep28615
Marín-Guirao, L., Entrambasaguas, L., Dattolo, E., Ruiz, J. M. & Procaccini, G. Mechanisms of resistance to intense warming events in an iconic seagrass species. Front. Plant Sci. 8, 1142 (2017).
pubmed: 28706528
pmcid: 5489684
doi: 10.3389/fpls.2017.01142
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 (2017).
pubmed: 29126631
doi: 10.1016/j.marenvres.2017.10.011
Marín-Guirao, L., Entrambasaguas, L., Ruiz, J. M. & Procaccini, G. Heat-stress induced flowering can be a potential adaptive response to ocean warming for the iconic seagrass Posidonia oceanica. Mol. Ecol. 28, 2486–2501 (2019).
pubmed: 30938465
doi: 10.1111/mec.15089
Peirano, A. et al. Phenology of the Mediterranean seagrass Posidonia oceanica (L.) Delile: Medium and long-term cycles and climate inferences. Aquat. Bot. 94(2), 77–92 (2011).
doi: 10.1016/j.aquabot.2010.11.007
Walker, L. R., Wardle, D. A., Bardgett, R. D. & Clarkson, B. D. The use of chronosequences in studies of ecological succession and soil development. J. Ecol. 98(4), 725–736 (2010).
doi: 10.1111/j.1365-2745.2010.01664.x
Shaltaut, M. & Omstedt, A. Recent sea surface temperature trends and future scenarios for the Mediterranean. Oceanologia 56(3), 441–443 (2014).
Adloff, F. et al. Mediterranean sea response to climate change in an ensemble of twenty first century scenarios. Clim. Dyn. 45, 2775–2802 (2015).
doi: 10.1007/s00382-015-2507-3
E.C. Marine Strategy Framework Directive 2008/56/EC of the European Parliament and of the Council, of 17 June 2008, establishing a framework for Community action in the field of marine environmental policy (Marine Strategy Framework Directive). OJEU 164, 19–40 (2008).
Montefalcone, M. Ecosystem health assessment using the Mediterranean seagrass Posidonia oceanica: A review. Ecol. Indic. 9, 595–604 (2009).
doi: 10.1016/j.ecolind.2008.09.013
Steinacher, M. et al. Projected 21st century decrease in marine productivity: A multi-model analysis. Biogeosciences 7, 979–1005 (2010).
doi: 10.5194/bg-7-979-2010
Taucher, J. & Oschlies, A. Can we predict the direction of marine primary production change under global warming?. Geophys. Res. Lett. 38, LO2603 (2011).
doi: 10.1029/2010GL045934
Dutkiewicz, S. et al. Ocean colour signature of climate change. Nat. Commun. 10, 578 (2019).
pubmed: 30718491
pmcid: 6362115
doi: 10.1038/s41467-019-08457-x
Kim, G.-U., Seo, K.-H. & Chen, D. Climate change over the Mediterranean and current destruction of marine ecosystem. Sci. Rep. 9, 18813 (2019).
pubmed: 31827188
pmcid: 6906505
doi: 10.1038/s41598-019-55303-7
Kimball, S., Angert, A. L., Huxman, T. E. & Venable, D. L. Contemporary climate change in the Sonoran Desert favors cold-adapted species. Glob. Change Biol. 16, 1555–1565 (2010).
doi: 10.1111/j.1365-2486.2009.02106.x
Graae, B. J. et al. On the use of weather data in ecological studies along altitudinal and latitudinal gradients. Oikos 121, 3–19 (2012).
doi: 10.1111/j.1600-0706.2011.19694.x
Pergent, G., Pergent-Martini, C. & Boudouresque, C. F. Utilisation de l’herbier a Posidonia oceanica comme indicateur biologique de la qualite du milieu littoral en Mediterranee: etat des connaissances. Mesogee 54, 3–27 (1995).
Pergent-Martini, C. & Pergent, G. Spatio-temporal dynamics of Posidonia oceanica beds near a sewage outfall (Mediterranean, France). in Seagrass Biology: Proceeding of an International Workshop, Rottnest Island, Australia, 25–29 January 1996. Faculty of Sciences, the University of Western Australia Publications: Nedlands, Australia, pp. 299–306 (Kuo, J., Phillips, R. C., Walker, D. I., Kirkman, H. eds.) (1996).
Scardi, M., Chessa, L. A., Fresi, E., Pais, A. & Serra, S. Optimizing interpolation of shoot density data from a Posidonia oceanica seagrass bed. Mar. Ecol. 27, 339–349 (2006).
doi: 10.1111/j.1439-0485.2006.00116.x
Kun-Seop, L., Sang, R. P. & Young, K. K. Effects of irradiance, temperature and nutrients on growth dynamics of seagrasses: A review. J. Exp. Mar. Biol. Ecol. 350(1), 144–175 (2007).
Molenaar, H., Barthélémy, D., de Reffye, P., Meinesz, A. & Mialet, I. Modelling architecture and growth patterns of Posidonia oceanica. Aquat. Bot. 66, 85–99 (2000).
doi: 10.1016/S0304-3770(99)00071-6
Olesen, B., Enrìquez, S., Duarte, C. M. & Sand-Jensen, K. Depth-acclimation of photosynthesis, morphology and demography of Posidonia oceanica and Cymodocea nodosa in the Spanish Mediterranean Sea. Mar. Ecol. Progr. Ser. 236, 89–97 (2002).
doi: 10.3354/meps236089
Ralph, P. J., Durako, M. J., Enriquez, S., Collier, C. J. & Doblin, M. A. Impact of light limitation on seagrasses. J. Exp. Mar. Biol. Ecol. 350, 176–193 (2007).
doi: 10.1016/j.jembe.2007.06.017
Ekstam, B. Ramet size equalization in a clonal plant, Phragmites australis. Oecologia 104, 440–446 (1995).
pubmed: 28307659
doi: 10.1007/BF00341341
Van Kleunen, M., Fischer, M. & Schmid, B. Effects of intraspecific competition on size variation and reproductive allocation in a clonal plant. Oikos 94, 515–524 (2001).
doi: 10.1034/j.1600-0706.2001.940313.x
Campagne, C. S., Salles, J. M., Boissery, P. & Deter, J. The seagrass Posidonia oceanica: Ecosystem services identification and economic evaluation of goods and benefits. Mar. Pollut. Bull. 97, 391–400 (2015).
pubmed: 26028167
doi: 10.1016/j.marpolbul.2015.05.061
Nordlund, L. M., Koch, E. W., Barbier, E. B. & Creed, J. C. Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 1(10), e0163091 (2016).
doi: 10.1371/journal.pone.0163091
Repolho, T. et al. Seagrass ecophysiological performance under ocean warming and acidification. Sci. Rep. 7, 41443 (2017).
pubmed: 28145531
pmcid: 5286439
doi: 10.1038/srep41443
Adams, M. P. et al. Predicting seagrass decline due to cumulative stressors. Environ. Model. Softw. 130, 104717 (2020).
doi: 10.1016/j.envsoft.2020.104717
Pazzaglia, J., Reusch, T. B. H., Terlizzi, A., Marín-Guirao, L. & Procaccini, G. Phenotypic plasticity under rapid global changes: The intrinsic force for future seagrasses survival. Evol. Appl. 00, 1–21 (2021).
Olita, A., Ribotti, A., Fazioli, L., Perilli, A. & Sorgente, R. Surface circulation and upwelling in the Sardinia Sea: A numerical study. Cont. Shelf Res. 71, 95–108 (2013).
doi: 10.1016/j.csr.2013.10.011
Pinardi, N. et al. Mediterranean Sea large-scale low-frequency ocean variability and water mass formation rates from 1987 to 2007: A retrospective analysis. Prog. Oceanogr. 132, 318–332 (2015).
doi: 10.1016/j.pocean.2013.11.003
Smale, D. A. & Wernberg, T. Satellite-derived SST data as a proxy for water temperature in nearshore benthic ecology. Mar. Ecol. Progr. Ser. 387, 27–37 (2009).
doi: 10.3354/meps08132
Giraud, G. Contribution à la description et à la phénologie quantitative des herbiers de Posidonia oceanica (L.) Delile. Thèse de Doctorat de Spécialité en Océanologie, Université d’Aix-Marseille, Marseille (1977).
Pergent, G. Lepidochronological analyses of the seagrass Posidonia oceanica (L.) Delile: a standardized approach. Aquat. Bot. 37, 39–54 (1990).
Pagès, J. F. et al. Indirect interactions in seagrasses: Fish herbivores increase predation risk to sea urchins by modifying plant traits. Funct. Ecol. 26, 1015–1023 (2012).
doi: 10.1111/j.1365-2435.2012.02038.x
Zuur, A. F., Leno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).
doi: 10.1111/j.2041-210X.2009.00001.x
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2018).
Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S 4th edn. (Springer, 2002).
doi: 10.1007/978-0-387-21706-2