Halpern, B. S. et al. Spatial and temporal changes in cumulative human impacts on the world’s ocean. Nat. Commun. 6, 1–7. https://doi.org/10.1038/ncomms8615 (2015).
Hodgson, E. E. & Halpern, B. S. Investigating cumulative effects across ecological scales. Conserv. Biol. 33, 22–32. https://doi.org/10.1111/cobi.13125 (2018).
Lu, Y. et al. Major threats of pollution and climate change to global coastal ecosystems and enhanced management for sustainability. Environ. Pollut. 239, 670–680. https://doi.org/10.1016/j.envpol.2018.04.016 (2018).
Ostle, C. et al. The rise in ocean plastics evidenced from a 60-year time series. Nat. Commun. 10, 1622. https://doi.org/10.1038/s41467-019-09506-1 (2019).
Doan, N. X. et al. Extreme temperature impairs growth and productivity in a common tropical marine copepod. Sci. Rep. 9, 4550. https://doi.org/10.1038/s41598-019-40996-7 (2019).
Barcelos e Ramos, J., Biswas, H., Schulz, K. G., LaRoche, J. & Riebesell, U. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Glob. Biogeochem. Cycles 21, 2028. https://doi.org/10.1029/2006GB002898 (2007).
Srinivasan, U. T., Cheung, W. W. L., Watson, R. & Sumaila, U. R. Food security implications of global marine catch losses due to overfishing. J. Bioecon. 12, 183–200. https://doi.org/10.1007/s10818-010-9090-9 (2010).
Frommel, A. Y., Stiebens, V., Clemmesen, C. & Havenhand, J. Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua). Biogeosciences 7, 3915–3919. https://doi.org/10.5194/bg-7-3915-2010 (2010).
Harvey, B. P., Gwynn-Jones, D. & Moore, P. J. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol. Evol. 3, 1016–1030. https://doi.org/10.1002/ece3.516 (2013).
Jackson, M. C. Interactions among multiple invasive animals. Ecology 96, 2035–2041. https://doi.org/10.1890/15-0171.1 (2015).
Przeslawski, R., Byrne, M. & Mellin, C. A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob. Change Biol. 21, 2122–2140. https://doi.org/10.1111/gcb.12833 (2015).
Strain, E. M. A., Thomson, R. J., Micheli, F., Mancuso, F. P. & Airoldi, L. Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob. Change Biol. 20, 3300–3312. https://doi.org/10.1111/gcb.12619 (2014).
Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315. https://doi.org/10.1111/j.1461-0248.2008.01253.x (2008).
Didham, R. K., Tylianakis, J. M., Gemmell, N. J., Rand, T. A. & Ewers, R. M. Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol. Evol. 22, 489–496. https://doi.org/10.1016/j.tree.2007.07.001 (2007).
Harley, C. D. G. et al. The impacts of climate change in coastal marine systems. Ecol. Lett. 9, 228–241. https://doi.org/10.1111/j.1461-0248.2005.00871.x (2006).
King, A. Avoiding ecological surprise: Lessons from long-standing communities. Acad. Manag. Rev. 20, 961–985 (1995).
Darling, E. S. & Côté, I. M. Quantifying the evidence for ecological synergies. Ecol. Lett. 11, 1278–1286. https://doi.org/10.1111/j.1461-0248.2008.01243.x (2008).
Côté, I. M., Darling, E. S. & Brown, C. J. Interactions among ecosystem stressors and their importance in conservation. Proc. R. Soc. B Biol. Sci. 283, 1–9. https://doi.org/10.1098/rspb.2015.2592 (2016).
Folt, C. L., Chen, C. Y., Moore, M. V. & Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).
Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952. https://doi.org/10.1126/science.1149345 (2008).
Villazan, B., Pedersen, M. F., Brun, F. G. & Vergara, J. J. Elevated ammonium concentrations and low light form a dangerous synergy for eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 493, 141–154. https://doi.org/10.3354/meps10517 (2013).
Peachey, R. B. J. The synergism between hydrocarbon pollutants and UV radiation: A potential link between coastal pollution and larval mortality. J. Exp. Mar. Biol. Ecol. 315, 103–114. https://doi.org/10.1016/j.jembe.2004.09.009 (2005).
Przeslawski, R., Davis, A. R. & Benkendorff, K. Synergistic effects associated with climate change and the development of rocky shore molluscs. Glob. Change Biol. 11, 515–522. https://doi.org/10.1111/j.1365-2486.2005.00918.x (2005).
Gieswein, A., Hering, D. & Feld, C. K. Additive effects prevail: The response of biota to multiple stressors in an intensively monitored watershed. Sci. Total Environ. 593–594, 27–35. https://doi.org/10.1016/j.scitotenv.2017.03.116 (2017).
McRoy, C. P. & McMillan, C. Seagrass Ecosystems. 53–87 (Marcel Dekker, New York, 1977).
Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. USA 106, 12377–12381. https://doi.org/10.1073/pnas.0905620106 (2009).
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. https://doi.org/10.1016/j.marpolbul.2015.05.061 (2014).
Lau, W. W. Y. Beyond carbon: Conceptualizing payments for ecosystem services in blue forests on carbon and other marine and coastal ecosystem services. Ocean Coast. Manag. 83, 5–14. https://doi.org/10.1016/j.ocecoaman.2012.03.011 (2013).
Watson, R. A., Watson, R. A. & Long, W. J. L. Simulation estimates of annual yield and landed value for commercial penaeid prawns from a tropical seagrass habitat, Northern Queensland, Australia. Mar. Freshw. Res. 44, 211–219. https://doi.org/10.1071/MF9930211 (1993).
Short, F. T. et al. Extinction risk assessment of the world’s seagrass species. Biol. Conserv. 144, 1961–1971. https://doi.org/10.1016/j.biocon.2011.04.010 (2011).
Dewsbury, B. M., Bhat, M. & Fourqurean, J. W. A review of seagrass economic valuations: Gaps and progress in valuation approaches. Ecosyst. Serv. 18, 68–77. https://doi.org/10.1016/j.ecoser.2016.02.010 (2016).
Short, F. T. & Wyllie-Echeverria, S. Natural and human-induced disturbance of seagrasses. Environ. Conserv. 23, 17–27. https://doi.org/10.1017/S0376892900038212 (1996).
García-Redondo, V., Bárbara, I. & Díaz-Tapia, P. Zostera marina meadows in the northwestern Spain: Distribution, characteristics and anthropogenic pressures. Biodivers. Conserv. 28, 1743–1757. https://doi.org/10.1007/s10531-019-01753-4 (2019).
Duarte, C. M. The future of seagrass meadows. Environ. Conserv. 29, 192–206. https://doi.org/10.1017/S0376892902000127 (2002).
Duffy, J. E. Biodiversity and the functioning of seagrass ecosystems. Mar. Ecol. Prog. Ser. 311, 233–250. https://doi.org/10.3354/meps311233 (2006).
Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996. https://doi.org/10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2 (2006).
Deter, J., Lozupone, X., Inacio, A., Boissery, P. & Holon, F. Boat anchoring pressure on coastal seabed: Quantification and bias estimation using AIS data. Mar. Pollut. Bull. 123, 175–181. https://doi.org/10.1016/j.marpolbul.2017.08.065 (2017).
Pereda-Briones, L., Terrados, J. & Tomas, F. Negative effects of warming on seagrass seedlings are not exacerbated by invasive algae. Mar. Pollut. Bull. 141, 36–45. https://doi.org/10.1016/j.marpolbul.2019.01.049 (2019).
Koweek, D. A. et al. Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow. Ecol. Appl. 28, 1694–1714. https://doi.org/10.1002/eap.1771 (2018).
Burnell, O. W., Russell, B. D., Irving, A. D. & Connell, S. D. Eutrophication offsets increased sea urchin grazing on seagrass aused by ocean warming and acidification. Mar. Ecol. Prog. Ser. 485, 37–46. https://doi.org/10.3354/meps10323 (2013).
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).
Han, Q. & Liu, D. Macroalgae blooms and their effects on seagrass ecosystems. J. Ocean Univ. China 13, 791–798. https://doi.org/10.1007/s11802-014-2471-2 (2014).
Willette, D. A. & Ambrose, R. F. Effects of the invasive seagrass Halophila stipulacea on the native seagrass, Syringodium filiforme, and associated fish and epibiota communities in the Eastern Caribbean. Aquat. Bot. 103, 74–82. https://doi.org/10.1016/j.aquabot.2012.06.007 (2012).
Vonk, J. A., Christianen, M. J. A., Stapel, J. & O’Brien, K. R. What lies beneath: Why knowledge of belowground biomass dynamics is crucial to effective seagrass management. Ecol. Ind. 57, 259–267. https://doi.org/10.1016/j.ecolind.2015.05.008 (2015).
Griffiths, L. L., Connolly, R. M. & Brown, C. J. Critical gaps in seagrass protection reveal the need to address multiple pressures and cumulative impacts. Ocean Coast. Manag. https://doi.org/10.1016/j.ocecoaman.2019.104946 (2019).
Clark, D., Goodwin, E., Sinner, J., Ellis, J. & Singh, G. Validation and limitations of a cumulative impact model for an estuary. Ocean Coast. Manag. 120, 88–98. https://doi.org/10.1016/j.ocecoaman.2015.11.013 (2016).
Andersson, S., Persson, M., Moksnes, P. O. & Baden, S. The role of the amphipod Gammarus locusta as a grazer on macroalgae in Swedish seagrass meadows. Mar. Biol. 156, 969–981. https://doi.org/10.1007/s00227-009-1141-1 (2009).
Hemmi, A. & Jormalainen, V. Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83, 1052–1064 (2002).
Kraufvelin, P. et al. Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat. Bot. 84, 199–209. https://doi.org/10.1016/j.aquabot.2005.08.008 (2006).
Burkepile, D. E. & Hay, M. E. Herbivore vs. nutrient control of marine primary producers: Context-dependent effects. Ecology 87, 3128–3139. https://doi.org/10.1890/0012-9658(2006)87[3128:Hvncom]2.0.Co;2 (2006).
Korpinen, S. & Jormalainen, V. Grazing and nutrients reduce recruitment success of Fucus vesiculosus L. (Fucales: Phaeophyceae). Estuar. Coast. Shelf Sci. 78, 437–444 (2008).
Hasler-Sheetal, H., Castorani, M. C. N., Glud, R. N., Canfield, D. E. & Holmer, M. Metabolomics reveals cryptic interactive effects of species interactions and environmental stress on nitrogen and sulfur metabolism in seagrass. Environ. Sci. Technol. 50, 11602–11609. https://doi.org/10.1021/acs.est.6b04647 (2016).
Koch, M. S., Schopmeyer, S. A., Holmer, M., Madden, C. J. & Kyhn-Hansen, C. Thalassia testudinum response to the interactive stressors hypersalinity, sulfide and hypoxia. Aquat. Bot. 87, 104–110. https://doi.org/10.1016/j.aquabot.2007.03.004 (2007).
Touchette, B. W. Seagrass-salinity interactions: Physiological mechanisms used by submersed marine angiosperms for a life at sea. J. Exp. Mar. Biol. Ecol. 350, 194–215. https://doi.org/10.1016/j.jembe.2007.05.037 (2007).
Koch, M. S. & Erskine, J. M. Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: Interactions with light, salinity and temperature. J. Exp. Mar. Biol. Ecol. 266, 81–95. https://doi.org/10.1016/s0022-0981(01)00339-2 (2001).
Lamers, L. P. M. et al. Sulfide as a soil phytotoxin-a review. Front. Plant Sci. https://doi.org/10.3389/fpls.2013.00268 (2013).
Pedersen, O., Binzer, T. & Borum, J. Sulphide intrusion in eelgrass (Zostera marina L.). Plant Cell Environ. 27, 595–602. https://doi.org/10.1111/j.1365-3040.2004.01173.x (2004).
Wahl, M. et al. in Advances in Marine Biology Vol. 59 (ed. Michael L.) 37–105 (Academic Press, London, 2011).
Koch, M. S., Schopmeyer, S., Kyhn-Hansen, C. & Madden, C. J. Synergistic effects of high temperature and sulfide on tropical seagrass. J. Exp. Mar. Biol. Ecol. 341, 91–101. https://doi.org/10.1016/j.jembe.2006.10.004 (2007).
Steen, H. & Scrosati, R. Intraspecific competition in Fucus serratus and F. evanescens (Phaeophyceae: Fucales) germlings: Effects of settlement density, nutrient concentration, and temperature. Mar. Biol. 144, 61–70. https://doi.org/10.1007/s00227-003-1175-8 (2004).
Jenkins, S. R., Norton, T. A. & Hawkins, S. J. Interactions between canopy forming algae in the eulittoral zone of sheltered rocky shores on the Isle of Man. J. Mar. Biol. Assoc. UK 79, 341–349. https://doi.org/10.1017/S0025315498000381 (1999).
Kilminster, K. et al. Unravelling complexity in seagrass systems for management: Australia as a microcosm. Sci. Total Environ. 534, 97–109 (2015).
de Vries, J., Kraak, M. H. S., Verdonschot, R. C. M. & Verdonschot, P. F. M. Quantifying cumulative stress acting on macroinvertebrate assemblages in lowland streams. Sci. Total Environ. 694, 133630. https://doi.org/10.1016/j.scitotenv.2019.133630 (2019).
Halpern, B. S. & Fujita, R. Assumptions, challenges, and future directions in cumulative impact analysis. Ecosphere 4, 1–11. https://doi.org/10.1890/ES13-00181.1 (2013).
Suchanek, T. H. Temperate coastal marine communities: Biodiversity and threats. Am. Zool. 34, 100–114. https://doi.org/10.1093/icb/34.1.100 (1994).
Stock, A. & Micheli, F. Effects of model assumptions and data quality on spatial cumulative human impact assessments. Glob. Ecol. Biogeogr. 25, 1321–1332. https://doi.org/10.1111/geb.12493 (2016).
Korpinen, S. & Andersen, J. H. A global review of cumulative pressure and impact assessments in marine environments. Front. Mar. Sci. 3, 153–164. https://doi.org/10.3389/fmars.2016.00153 (2016).
Coll, M., Steenbeek, J., Sole, J., Palomera, I. & Christensen, V. Modelling the cumulative spatial-temporal effects of environmental drivers and fishing in a NW Mediterranean marine ecosystem. Ecol. Model. 331, 100–114. https://doi.org/10.1016/j.ecolmodel.2016.03.020 (2016).
Griffith, G. P., Fulton, E. A., Gorton, R. & Richardson, A. J. Predicting interactions among fishing, ocean warming, and ocean acidification in a marine system with whole-ecosystem models. Conserv. Biol. 26, 1145–1152. https://doi.org/10.1111/j.1523-1739.2012.01937.x (2012).
Brown, C. J., Saunders, M. I., Possingham, H. P. & Richardson, A. J. Interactions between global and local stressors of ecosystems determine management effectiveness in cumulative impact mapping. Divers. Distrib. 20, 538–546. https://doi.org/10.1111/ddi.12159 (2014).
Andersen, J. H., Halpern, B. S., Korpinen, S., Murray, C. & Reker, J. Baltic Sea biodiversity status vs. cumulative human pressures. Estuar. Coast. Shelf Sci. 161, 88–92. https://doi.org/10.1016/j.ecss.2015.05.002 (2015).
Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).
Hoffman, J. R., Hansen, L. J. & Klinger, T. Interactions between UV radiation and temperature limit inferences from single-factor experiments. J. Phycol. 39, 268–272. https://doi.org/10.1046/j.1529-8817.2003.01111.x (2003).
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G. & Grp, P. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Int. J. Surg. 8, 336–341. https://doi.org/10.1016/j.ijsu.2010.02.007 (2010).
Kahn, A. E. & Durako, M. J. Thalassia testudinum seedling responses to changes in salinity and nitrogen levels. J. Exp. Mar. Biol. Ecol. 335, 1–12. https://doi.org/10.1016/j.jembe.2006.02.011 (2006).
Lange, K., Bruder, A., Matthaei, C. D., Brodersen, J. & Paterson, R. A. Multiple-stressor effects on freshwater fish: Importance of taxonomy and life stage. Fish Fish. 19, 974–983. https://doi.org/10.1111/faf.12305 (2018).
Hedges, L. V. & Olkin, I. Statistical methods for meta-analysis (Academic Press, London, 1985).
Gurevitch, J., Morrison, J. A. & Hedges, L. V. The interaction between competition and predation: A meta-analysis of field experiments. Am. Nat. 155, 435–453. https://doi.org/10.1086/303337 (2000).
Nakagawa, S. & Cuthill, I. C. Effect size, confidence interval and statistical significance: A practical guide for biologists. Biol. Rev. 82, 591–605. https://doi.org/10.1111/j.1469-185X.2007.00027.x (2007).
UNEP-WCMC & Short, F. T. Global Distribution of Seagrasses (version 6). Sixth update to the data layer used in Green and Short (2003), superseding version 5. Cambridge (UK): UN Environment World Conservation Monitoring Centre. https://data.unep-wcmc.org/datasets/7 (2018).
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