Ocean warming and acidification modify top-down and bottom-up control in a tropical seagrass ecosystem

Listiawati V., Kurihara H.

Faculty of Science, University of the Ryukyus, Okinawa, 903-0123, Japan; Master of Marine Science, Universitas Diponegoro, Semarang, 50275, Indonesia; Department of Biology Education, Universitas Muhammadiyah Surakarta, Surakarta, 57162, Indonesia


Seagrass ecosystem is one of the most productive ecosystems in coastal waters providing numerous ecological functions and supporting a large biodiversity. However, various anthropogenic stressors including climate change are impacting these vulnerable habitats. Here, we investigated the independent and combined effects of ocean warming and ocean acidification on plant–herbivore interactions in a tropical seagrass community. Direct and indirect effects of high temperature and high pCO2 on the physiology of the tropical seagrass Thalassia hemprichii and sea urchin Tripneustes gratilla were evaluated. Productivity of seagrass was found to increase under high pCO2, while sea urchin physiology including feeding rate decreased particularly under high temperature. The present study indicated that future climate change will affect the bottom-up and top-down balance, which potentially can modify the ecosystem functions and services of tropical seagrass ecosystems. © 2021, The Author(s).


Scientific Reports

Publisher: Nature Research

Volume 11, Issue 1, Art No 13605, Page – , Page Count

Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85109129624&doi=10.1038%2fs41598-021-92989-0&partnerID=40&md5=aa4d50b2455fd738a019241c9c6b3307

doi: 10.1038/s41598-021-92989-0

Issn: 20452322

Type: All Open Access, Gold, Green


Duarte, C.M., Chiscano, C.L., Seagrass biomass and production: A reassessment (1999) Aquat. Bot., 65, pp. 159-174; Boon, P.I., Moriarty, D.J.W., Saffigna, P.G., Rates of ammonium turnover and the role of amino-acid deamination in seagrass (Zostera capricorni) beds of Moreton Bay, Australia (1986) Mar. Biol., 91, pp. 259-268. , COI: 1:CAS:528:DyaL28Xkt1WnurY%3D; Smith, S.V., Marine macrophytes as a global carbon sink (1981) Science, 211, pp. 838-840. , COI: 1:CAS:528:DyaL3MXkt12hu7w%3D, PID: 17740399; Scoffin, T.P., The trapping and binding of subtidal carbonate sediments by marine vegetation in Bimini Lagoon, Bahamas (1970) J. Sediment. Res., 40, pp. 249-273; Robblee, M.B., Zieman, J.C., Diel variation in the fish fauna of a tropical seagrass feeding ground (1984) Bull. Mar. Sci., 34, pp. 335-345; Orth, R.J., A global crisis for seagrass ecosystems (2006) Bioscience, 56, pp. 987-996; Short, F.T., Neckles, H.A., The effects of global climate change on seagrasses (1999) Aquat. Bot., 63, pp. 169-196; Unsworth, R.K.F., Nordlund, L.M., Cullen-Unsworth, L.C., Seagrass meadows support global fisheries production (2019) Conserv. Lett., 12; Barber, B.J., Behrens, P.J., Effects of elevated temperature on seasonal in situ leaf productivity of Thalassia testudinum Banks ex König and Syringodium filiforme Kützing (1985) Aquat. Bot., 22, pp. 61-69; Marsh, J.A., Dennison, W.C., Alberte, R.S., Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.) (1986) J. Exp. Mar. Biol. Ecol., 101, pp. 257-267; Lee, K.S., Park, S.R., Kim, Y.K., Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: A review (2007) J. Exp. Mar. Biol. Ecol., 350, pp. 144-175; Marbà, N., Duarte, C.M., Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality (2010) Glob. Change Biol., 16, pp. 2366-2375; Kim, M., Influence of water temperature anomalies on the growth of Zostera marina plants held under high and low irradiance levels (2020) Estuaries Coasts, 43, pp. 463-476; Zimmerman, R.C., Kohrs, D.G., Steller, D.L., Alberte, R.S., Impacts of CO2 enrichment on productivity and light requirements of eelgrass (1997) Plant Physiol., 115, pp. 599-607. , COI: 1:CAS:528:DyaK2sXntFSlsrc%3D, PID: 12223828; Palacios, S.L., Zimmerman, R.C., Response of eelgrass Zostera marina to CO2 enrichment: Possible impacts of climate change and potential for remediation of coastal habitats (2007) Mar. Ecol. Prog. Ser., 344, pp. 1-13; Jiang, Z.J., Huang, X.P., Zhang, J.P., Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers (2010) J. Integr. Plant Biol., 52, pp. 904-913. , COI: 1:CAS:528:DC%2BC3cXhtlGjs7nM, PID: 20883442; Beer, S., Koch, E., Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments (1996) Mar. Ecol. Prog. Ser., 141, pp. 199-204; Repolho, T., Seagrass ecophysiological performance under ocean warming and acidification (2017) Sci. Rep., 7, p. 41443. , COI: 1:CAS:528:DC%2BC2sXitVyitro%3D, PID: 28145531; Tomas, F., Martínez-Crego, B., Hernán, G., Santos, R., Responses of seagrass to anthropogenic and natural disturbances do not equally translate to its consumers (2015) Glob. Change Biol., 21, pp. 4021-4030; 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 (2013) Mar. Ecol. Prog. Ser., 485, pp. 37-46. , COI: 1:CAS:528:DC%2BC3sXhtlCqsb%2FJ; Kurihara, H., Yin, R., Nishihara, G.N., Soyano, K., Ishimatsu, A., Effect of ocean acidification on growth, gonad development and physiology of the sea urchin Hemicentrotus pulcherrimus (2013) Aquat. Biol., 18, pp. 281-292; Catarino, A.I., Bauwens, M., Dubois, P., Acid-base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures (2012) Environ. Sci. Pollut. Res., 19, pp. 2344-2353. , COI: 1:CAS:528:DC%2BC38XhtVShsLjE; Arnold, T., Ocean acidification and the loss of phenolic substances in marine plants (2012) PLoS One, 7. , COI: 1:CAS:528:DC%2BC38XntFWltr0%3D, PID: 22558120; Hernán, G., Seagrass (Posidonia oceanica) seedlings in a high-CO2 world: from physiology to herbivory (2016) Sci. Rep., 6, p. 38017. , PID: 27905514, COI: 1:CAS:528:DC%2BC28XitFWnsr7O; Nguyen, K.D.T., Upper temperature limits of tropical marine ectotherms: Global warming implications (2011) PLoS ONE, 6. , COI: 1:CAS:528:DC%2BC38XjtFOqsw%3D%3D; Agawin, N.S.R., Duarte, C.M., Fortes, M.D., Uri, J.S., Vermaat, J.E., Temporal changes in the abundance, leaf growth and photosynthesis of three co-occurring Philippine seagrasses (2001) J. Exp. Mar. Biol. Ecol., 260, pp. 217-239. , PID: 11358580; Kurihara, H., Wouters, J., Yasuda, N., Seasonal calcification of the coral Acropora digitifera from a subtropical marginal Okinawa reef under ocean acidification (2019) Coral Reefs, 38, pp. 443-454; Koch, M., Bowes, G., Ross, C., Zhang, X.H., Climate change and ocean acidification effects on seagrasses and marine macroalgae (2013) Glob. Change Biol., 19, pp. 103-132; Sage, R.F., Kubien, D.S., The temperature response of C3 and C4 photosynthesis (2007) Plant Cell Environ., 30, pp. 1086-1106. , COI: 1:CAS:528:DC%2BD2sXhtVeiurrP, PID: 17661749; O’Connor, M.I., Warming strengthens an herbivore–plant interaction (2009) Ecology, 90, pp. 388-398. , PID: 19323223; Campbell, J.E., Fourqurean, J.W., Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum (2013) Mar. Biol., 160, pp. 1465-1475. , COI: 1:CAS:528:DC%2BC3sXovVSjtbw%3D; Moulin, L., Grosjean, P., Leblud, J., Batigny, A., Dubois, P., Impact of elevated pCO2 on acid-base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean acidification: A study in mesocosms (2014) J. Exp. Mar. Biol. Ecol., 457, pp. 97-104. , COI: 1:CAS:528:DC%2BC2cXhtVaksLrF; Stumpp, M., Trübenbach, K., Brennecke, D., Hu, M.Y., Melzner, F., Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification (2012) Aquat. Toxicol., 110-111, pp. 194-207. , PID: 22343465, COI: 1:CAS:528:DC%2BC38Xjt1Olsrg%3D; Thomsen, J., Melzner, F., Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis (2010) Mar. Biol., 157, pp. 2667-2676; Marčeta, T., Do males and females respond differently to ocean acidification? An experimental study with the sea urchin Paracentrotus lividus (2020) Environ. Sci. Pollut. Res., 27, pp. 39516-39530. , COI: 1:CAS:528:DC%2BB3cXhsVersrbF; Uthicke, S., Soars, N., Foo, S., Byrne, M., Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei (2013) Mar. Biol., 160, pp. 1913-1926. , COI: 1:CAS:528:DC%2BC3sXht1Ggt77E; Atwood, T.B., Predators help protect carbon stocks in blue carbon ecosystems (2015) Nat. Clim. Change, 5, pp. 1038-1045; Scott, A.L., The role of herbivory in structuring tropical seagrass ecosystem service delivery (2018) Front. Plant Sci., 9, p. 127. , PID: 29487606; Lewis, E., Wallace, D., Program developed for CO2 system calculations (1998) Ornl/Cdiac, 105, pp. 1-21; Dickson, A.G., Millero, F.J., A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media (1987) Deep Sea Res. Part A Oceanogr. Res. Pap., 34, pp. 1733-1743. , COI: 1:CAS:528:DyaL1cXotFGjsg%3D%3D; Short, F.T., Duarte, C.M., Methods for the measurement of seagrass growth and production Global Seagrass Research Methods, pp. 155-182. , https://doi.org/10.1016/b978-044450891-1/50009-8, Short, F. T., Coles, R. G., (Elsevier Science, 2001); Platt, T., Gallegos, C.L., Harrison, W.G., Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton (1980) J. Mar. Res., 38, pp. 103-111; Silsbe, G.M., Malkin, S.Y., Phytotools: Phytoplankton production tools (2015) An R Packag., , https://cran.r-project.org/web/packages/phytotools/index.html, available CRAN., Accessed 7 July 2020; Holmes, R.M., Aminot, A., Kérouel, R., Hooker, B.A., Peterson, B.J., A simple and precise method for measuring ammonium in marine and freshwater ecosystems (1999) Can. J. Fish. Aquat. Sci., 56, pp. 1801-1808. , COI: 1:CAS:528:DyaK1MXnslGitbc%3D; R: A Language and Environment for Statistical Computing (2020) R Foundation for Statistical Computing; Rstudio: Integrated Development for R., , (RStudio, Inc., 2015); Hothorn, T., Bretz, F., Westfall, P., Simultaneous inference in general parametric models (2008) Biom. J., 50, pp. 346-363. , PID: 18481363

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