Changing structure of benthic foraminiferal communities due to declining p H: Results from laboratory culture experiments
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摘要
The ocean absorbs large amounts of CO_2 emitted from human activities, which results in a decrease in seawater p H.Marine calcifying organisms such as foraminifera, are most likely to be affected by this declining pH. In this study, we collected sediments from five stations of different depths(34–73 m) in a continental shelf of the Yellow Sea. The entire benthic foraminiferal communities together with sea sediments were cultured under three constant pHs(8.3, 7.8, and 7.3) for 6 and 12 weeks in the laboratory to study their responses to pH or incubation time. The microcosm's experimental results obtained showed that most of the foraminiferal community parameters(abundance, species richness, Margalef index, and Shannon-Wiener diversity) decreased significantly(p<0.05) with the decline in pH in all the tested stations. The responses of foraminifera to the decline in p H were species-specific, for instance, Protelphidium tuberculatum and Cribroelphidiumfrigidum were highly sensitive to declining pH and were finally eliminated at low pH, while some species(e.g., Lagenammina atlantica, Verneuilinulla advena, V. propinqua, Haplophragmoides applanata, and H. canariensis) could tolerate low pH and acted as pH-tolerant species. In addition, the proportion of hyaline taxa showed a significant(p<0.05) positive correlation with pH, while agglutinated type showed a negative response. Furthermore, different incubation times(6 and 12 weeks) showed significant effects on the nearshore communities other than the offshore treatments, which were, however, entirely declined after 6 weeks' incubation under low p H manipulation. Our results indicated that nearshore foraminiferal communities showed rather a resilience to the declining p H and the offshore foraminifera, especially those in the central area of the Yellow Sea Cold Water Mass were found to be more sensitive to the decline in pH in the continental shelf sediments of the Yellow Sea.
The ocean absorbs large amounts of CO_2 emitted from human activities, which results in a decrease in seawater p H.Marine calcifying organisms such as foraminifera, are most likely to be affected by this declining pH. In this study, we collected sediments from five stations of different depths(34–73 m) in a continental shelf of the Yellow Sea. The entire benthic foraminiferal communities together with sea sediments were cultured under three constant pHs(8.3, 7.8, and 7.3) for 6 and 12 weeks in the laboratory to study their responses to pH or incubation time. The microcosm's experimental results obtained showed that most of the foraminiferal community parameters(abundance, species richness, Margalef index, and Shannon-Wiener diversity) decreased significantly(p<0.05) with the decline in pH in all the tested stations. The responses of foraminifera to the decline in p H were species-specific, for instance, Protelphidium tuberculatum and Cribroelphidiumfrigidum were highly sensitive to declining pH and were finally eliminated at low pH, while some species(e.g., Lagenammina atlantica, Verneuilinulla advena, V. propinqua, Haplophragmoides applanata, and H. canariensis) could tolerate low pH and acted as pH-tolerant species. In addition, the proportion of hyaline taxa showed a significant(p<0.05) positive correlation with pH, while agglutinated type showed a negative response. Furthermore, different incubation times(6 and 12 weeks) showed significant effects on the nearshore communities other than the offshore treatments, which were, however, entirely declined after 6 weeks' incubation under low p H manipulation. Our results indicated that nearshore foraminiferal communities showed rather a resilience to the declining p H and the offshore foraminifera, especially those in the central area of the Yellow Sea Cold Water Mass were found to be more sensitive to the decline in pH in the continental shelf sediments of the Yellow Sea.
The ocean absorbs large amounts of CO_2 emitted from human activities, which results in a decrease in seawater p H.Marine calcifying organisms such as foraminifera, are most likely to be affected by this declining pH. In this study, we collected sediments from five stations of different depths(34–73 m) in a continental shelf of the Yellow Sea. The entire benthic foraminiferal communities together with sea sediments were cultured under three constant pHs(8.3, 7.8, and 7.3) for 6 and 12 weeks in the laboratory to study their responses to pH or incubation time. The microcosm's experimental results obtained showed that most of the foraminiferal community parameters(abundance, species richness, Margalef index, and Shannon-Wiener diversity) decreased significantly(p<0.05) with the decline in pH in all the tested stations. The responses of foraminifera to the decline in p H were species-specific, for instance, Protelphidium tuberculatum and Cribroelphidiumfrigidum were highly sensitive to declining pH and were finally eliminated at low pH, while some species(e.g., Lagenammina atlantica, Verneuilinulla advena, V. propinqua, Haplophragmoides applanata, and H. canariensis) could tolerate low pH and acted as pH-tolerant species. In addition, the proportion of hyaline taxa showed a significant(p<0.05) positive correlation with pH, while agglutinated type showed a negative response. Furthermore, different incubation times(6 and 12 weeks) showed significant effects on the nearshore communities other than the offshore treatments, which were, however, entirely declined after 6 weeks' incubation under low p H manipulation. Our results indicated that nearshore foraminiferal communities showed rather a resilience to the declining p H and the offshore foraminifera, especially those in the central area of the Yellow Sea Cold Water Mass were found to be more sensitive to the decline in pH in the continental shelf sediments of the Yellow Sea.
引文
Al-Sabouni N,Kucera M,Schmidt D N.2007.Vertical niche separation control of diversity and size disparity in planktonic foraminifera.Mar Micropaleontol,63:75-90
Allison N,Austin W,Paterson D,Austin H.2010.Culture studies of the benthic foraminifera Elphidium williamsoni:Evaluating pH,?[CO32-]and inter-individual effects on test Mg/Ca.Chem Geol,274:87-93
Allison N,Austin H,Austin W,Paterson D M.2011.Effects of seawater pH and calcification rate on test Mg/Ca and Sr/Ca in cultured individuals of the benthic,calcitic foraminifera Elphidium williamsoni.Chem Geol,289:171-178
Alve E,Goldstein S T.2003.Propagule transport as a key method of dispersal in benthic foraminifera(Protista).Limnol Oceanogr,48:2163-2170
Bernhard J M,Barry J P,Buck K R,Starczak V R.2009.Impact of intentionally injected carbon dioxide hydrate on deep-sea benthic foraminiferal survival.Glob Change Biol,15:2078-2088
Caldeira K,Wickett M E.2003.Anthropogenic carbon and ocean pH.Nature,425:365
Cigliano M,Gambi M C,Rodolfo-Metalpa R,Patti F P,Hall-Spencer J M.2010.Effects of ocean acidification on invertebrate settlement at volcanic CO2vents.Mar Biol,157:2489-2502
Clarke K R,Gorley R N.2006.PRIMER v6:User Manual/Tutorial.Plymouth:PRIMER-E Ltd
Davis C V,Rivest E B,Hill T M,Gaylord B,Russell A D,Sanford E.2017.Ocean acidification compromises a planktic calcifier with implications for global carbon cycling.Sci Rep,7:2225
Di Bella L,Ingrassia M,Frezza V,Chiocci F L,Martorelli E.2016.The response of benthic meiofauna to hydrothermal emissions in the Pontine Archipelago,Tyrrhenian Sea(central Mediterranean Basin).J Mar Syst,164:53-66
Di Bella L,Ingrassia M,Frezza V,Chiocci F L,Pecci R,Bedini R,Martorelli E.2018.Spiculosiphon oceana(Foraminifera)a new bio-indicator of acidic environments related to fluid emissions of the Zannone Hydrothermal Field(central Tyrrhenian Sea).Mar Environ Res,136:89-98
Dias B B,Hart M B,Smart C W,Hall-Spencer J M.2010.Modern seawater acidification:The response of foraminifera to high-CO2conditions in the Mediterranean Sea.J Geol Soc,167:843-846
Dlugokencky E,Tans P.2018.Trends in atmospheric carbon dioxide,National Oceanic&Atmospheric Administration,Earth System Research Laboratory(NOAA/ESRL),available at http://www.esrl.noaa.gov/gmd/ccgg/trends(last access:5 February 2018)
Elderfield H,Yu J,Anand P,Kiefer T,Nyland B.2006.Calibrations for benthic foraminiferal Mg/Ca paleothermometry and the carbonate ion hypothesis.Earth Planet Sci Lett,250:633-649
Fabry V J,Seibel B A,Feely R A,Orr J C.2008.Impacts of ocean acidification on marine fauna and ecosystem processes.ICES J Mar Sci,65:414-432
GB/T 34656-2017.2017.Specifications for Marine Sediment Interstitial Biota Survey,National Standard of the People’s Republic of China(in Chinese).Beijing:Standards Press of China
Gray W R,Weldeab S,Lea D W,Rosenthal Y,Gruber N,Donner B,Fischer G.2018.The effects of temperature,salinity,and the carbonate system on Mg/Ca in Globigerinoides ruber(white):A global sediment trap calibration.Earth Planet Sci Lett,482:607-620
Jian Z,Wang L,Kienast M,Sarnthein M,Kuhnt W,Lin H,Wang P.1999.Benthic foraminiferal paleoceanography of the South China Sea over the last 40000 years.Mar Geol,156:159-186
Joos F,Spahni R.2008.Rates of change in natural and anthropogenic radiative forcing over the past 20000 years.Proc Natl Acad Sci USA,105:1425-1430
K?sakürek B,Eisenhauer A,B?hm F,Garbe-Sch?nberg D,Erez J.2008.Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan,Globigerinoides ruber(white).Earth Planet Sci Lett,273:260-269
Ko G W K,Dineshram R,Campanati C,Chan V B S,Havenhand J,Thiyagarajan V.2014.Interactive effects of ocean acidification,elevated temperature,and reduced salinity on early-life stages of the Pacific oyster.Environ Sci Technol,48:10079-10088
Kuroyanagi A,Kawahata H,Suzuki A,Fujita K,Irie T.2009.Impacts of ocean acidification on large benthic foraminifers:Results from laboratory experiments.Mar Micropaleontol,73:190-195
Kurtarkar S R,Nigam R,Saraswat R,Linshy V N.2011.Regeneration and abnormality in benthic foraminifera Rosalina leei:Implications in reconstructing past salinity changes.Riv Ital Paleontol Stratigr,117:189-196
Le Cadre V,Debenay J P,Lesourd M.2003.Low pH effects on Ammonia beccarii test deformation:Implications for using test deformations as a pollution indicator.J Foraminiferal Res,33:1-9
Lei Y,Li T.2016.Atlas of Benthic Foraminifera from China Seas the Bohai Sea and the Yellow Sea.Beijing:Springer-Verlag GmbH Germany and Science Press.399
Lei Y,Li T,Jian Z,Nigam R.2017.Taxonomy and distribution of benthic foraminifera in an intertidal zone of the Yellow Sea,PR China:Correlations with sediment temperature and salinity.Mar Micropaleontol,133:1-20
Liu S,Liu C,Yan P,Huang Z,Peng T,Zhou Y,Ding H.2013.Research of spectrophotometric pH measurements of sea waters in Jiaozhou Bay and coastal waters of Qingdao(in Chinese).Trans Oceanol Limnol:108-114
Loeblich A R,Tappan H.1988.Foraminiferal Genera and Their Classification.New York:Van Nostrand Reinhold.970
Mahmoudi E,Essid N,Beyrem H,Hedfi A,Boufahja F,Vitiello P,Aissa P.2005.Effects of hydrocarbon contamination on a free living marine nematode community:Results from microcosm experiments.Mar Pollut Bull,50:1197-1204
Manno C,Morata N,Bellerby R.2012.Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma(sinistral).Polar Biol,35:1311-1319
McIntyre-Wressnig A,Bernhard J M,Wit J C,Mccorkle D C.2014.Ocean acidification not likely to affect the survival and fitness of two temperate benthic foraminiferal species:Results from culture experiments.J Foraminiferal Res,44:341-351
Meng Z,Xu K,Lei Y.2011.Community composition,distribution,and contribution of microbenthos in offshore sediments from the Yellow Sea.Cont Shelf Res,31:1437-1446
Milliman J D.1993.Production and accumulation of calcium carbonate in the ocean:Budget of a nonsteady state.Glob Biogeochem Cycle,7:927-957
Muller P H.1974.Sediment production and population biology of the benthic foraminifer Amphistegina madagascariensis.Limnol Oceanogr,19:802-809
Murray J W.2006.Ecology and Applications of Benthic Foraminifera.New York:Cambridge University Press.426
Orr J C,Fabry V J,Aumont O,Bopp L,Doney S C,Feely R A,Gnanadesikan A,Gruber N,Ishida A,Joos F,Key R M,Lindsay K,MaierReimer E,Matear R,Monfray P,Mouchet A,Najjar R G,Plattner G K,Rodgers K B,Sabine C L,Sarmiento J L,Schlitzer R,Slater R D,Totterdell I J,Weirig M F,Yamanaka Y,Yool A.2005.Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms.Nature,437:681-686
Pettit L R,Hart M B,Medina-Sánchez A N,Smart C W,Rodolfo-Metalpa R,Hall-Spencer J M,Prol-Ledesma R M.2013.Benthic foraminifera show some resilience to ocean acidification in the northern Gulf of California,Mexico.Mar Pollut Bull,73:452-462
Pettit L R,Smart C W,Hart M B,Milazzo M,Hall-Spencer J M.2015.Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2gradient.Ecol Evol,5:1784-1793
Qu B,Song J,Yuan H,Li X,Li N.2014.Air-sea CO2exchange process in the southern Yellow Sea in April of 2011,and June,July,October of2012.Cont Shelf Res,80:8-19
Reymond C E,Lloyd A,Kline D I,Dove S G,Pandolfi J M.2013.Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios.Glob Change Biol,19:291-302
Russell A D,H?nisch B,Spero H J,Lea D W.2004.Effects of seawater carbonate ion concentration and temperature on shell U,Mg,and Sr in cultured planktonic foraminifera.Geochim Cosmochim Acta,68:4347-4361
Saalim S M,Saraswat R,Suokhrie T,Nigam R.2018.Assessing the ecological preferences of agglutinated benthic foraminiferal morphogroups from the western Bay of Bengal.Deep-Sea Res Part II-Top Stud Oceanogr,doi:10.1016/j.dsr2.2018.02.002
Sabine C L,Feely R A,Gruber N,Key R M,Lee K,Bullister J L,Wanninkhof R,Wong C S,Wallace D W R,Tilbrook B,Millero F J,Peng TH,Kozyr A,Ono T,Rios A F.2004.The oceanic sink for anthropogenic CO2.Science,305:367-371
Saraswat R,Kouthanker M,Kurtarkar S R,Nigam R,Naqvi S WA,Linshy V N.2015.Effect of salinity induced pH/alkalinity changes on benthic foraminifera:A laboratory culture experiment.Estuar Coast Shelf Sci,153:96-107
SAS Institute Inc..2009.SAS/STAT?9.2 User’s Guide.2nd ed.Cary,NC:SAS Institute Inc
Schneider K,Erez J.2006.The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma.Limnol Oceanogr,51:1284-1293
Sinutok S,Hill R,Doblin M A,Wuhrer R,Ralph P J.2011.Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers.Limnol Oceanogr,56:1200-1212
Sinutok S,Hill R,Kühl M,Doblin M A,Ralph P J.2014.Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis.Mar Biol,161:2143-2154
Uthicke S,Fabricius K E.2012.Productivity gains do not compensate for reduced calcification under near-future ocean acidification in the photosynthetic benthic foraminifer species Marginopora vertebralis.Glob Change Biol,18:2781-2791
Uthicke S,Momigliano P,Fabricius K E.2013.High risk of extinction of benthic foraminifera in this century due to ocean acidification.Sci Rep,3:1769
Wei Q,Zhan R,Zang J,Li R.2010.Distributions and influence factors of the chemical parameters in the Southern Yellow Sea in spring(in Chinese).Mar Sci,34:52-60
Weisse T,Stadler P.2006.Effect of pH on growth,cell volume,and production of freshwater ciliates,and implications for their distribution.Limnol Oceanogr,51:1708-1715
Xin M,Ma D,Wang B.2015.Chemicohydrographic characteristics of the Yellow Sea cold water mass.Acta Oceanol Sin,34:5-11
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Zhao L,Sch?ne B R,Mertz-Kraus R,Yang F.2017.Insights from sodium into the impacts of elevated p CO2and temperature on bivalve shell formation.J Exp Mar Biol Ecol,486:148-154
Allison N,Austin W,Paterson D,Austin H.2010.Culture studies of the benthic foraminifera Elphidium williamsoni:Evaluating pH,?[CO32-]and inter-individual effects on test Mg/Ca.Chem Geol,274:87-93
Allison N,Austin H,Austin W,Paterson D M.2011.Effects of seawater pH and calcification rate on test Mg/Ca and Sr/Ca in cultured individuals of the benthic,calcitic foraminifera Elphidium williamsoni.Chem Geol,289:171-178
Alve E,Goldstein S T.2003.Propagule transport as a key method of dispersal in benthic foraminifera(Protista).Limnol Oceanogr,48:2163-2170
Bernhard J M,Barry J P,Buck K R,Starczak V R.2009.Impact of intentionally injected carbon dioxide hydrate on deep-sea benthic foraminiferal survival.Glob Change Biol,15:2078-2088
Caldeira K,Wickett M E.2003.Anthropogenic carbon and ocean pH.Nature,425:365
Cigliano M,Gambi M C,Rodolfo-Metalpa R,Patti F P,Hall-Spencer J M.2010.Effects of ocean acidification on invertebrate settlement at volcanic CO2vents.Mar Biol,157:2489-2502
Clarke K R,Gorley R N.2006.PRIMER v6:User Manual/Tutorial.Plymouth:PRIMER-E Ltd
Davis C V,Rivest E B,Hill T M,Gaylord B,Russell A D,Sanford E.2017.Ocean acidification compromises a planktic calcifier with implications for global carbon cycling.Sci Rep,7:2225
Di Bella L,Ingrassia M,Frezza V,Chiocci F L,Martorelli E.2016.The response of benthic meiofauna to hydrothermal emissions in the Pontine Archipelago,Tyrrhenian Sea(central Mediterranean Basin).J Mar Syst,164:53-66
Di Bella L,Ingrassia M,Frezza V,Chiocci F L,Pecci R,Bedini R,Martorelli E.2018.Spiculosiphon oceana(Foraminifera)a new bio-indicator of acidic environments related to fluid emissions of the Zannone Hydrothermal Field(central Tyrrhenian Sea).Mar Environ Res,136:89-98
Dias B B,Hart M B,Smart C W,Hall-Spencer J M.2010.Modern seawater acidification:The response of foraminifera to high-CO2conditions in the Mediterranean Sea.J Geol Soc,167:843-846
Dlugokencky E,Tans P.2018.Trends in atmospheric carbon dioxide,National Oceanic&Atmospheric Administration,Earth System Research Laboratory(NOAA/ESRL),available at http://www.esrl.noaa.gov/gmd/ccgg/trends(last access:5 February 2018)
Elderfield H,Yu J,Anand P,Kiefer T,Nyland B.2006.Calibrations for benthic foraminiferal Mg/Ca paleothermometry and the carbonate ion hypothesis.Earth Planet Sci Lett,250:633-649
Fabry V J,Seibel B A,Feely R A,Orr J C.2008.Impacts of ocean acidification on marine fauna and ecosystem processes.ICES J Mar Sci,65:414-432
GB/T 34656-2017.2017.Specifications for Marine Sediment Interstitial Biota Survey,National Standard of the People’s Republic of China(in Chinese).Beijing:Standards Press of China
Gray W R,Weldeab S,Lea D W,Rosenthal Y,Gruber N,Donner B,Fischer G.2018.The effects of temperature,salinity,and the carbonate system on Mg/Ca in Globigerinoides ruber(white):A global sediment trap calibration.Earth Planet Sci Lett,482:607-620
Jian Z,Wang L,Kienast M,Sarnthein M,Kuhnt W,Lin H,Wang P.1999.Benthic foraminiferal paleoceanography of the South China Sea over the last 40000 years.Mar Geol,156:159-186
Joos F,Spahni R.2008.Rates of change in natural and anthropogenic radiative forcing over the past 20000 years.Proc Natl Acad Sci USA,105:1425-1430
K?sakürek B,Eisenhauer A,B?hm F,Garbe-Sch?nberg D,Erez J.2008.Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan,Globigerinoides ruber(white).Earth Planet Sci Lett,273:260-269
Ko G W K,Dineshram R,Campanati C,Chan V B S,Havenhand J,Thiyagarajan V.2014.Interactive effects of ocean acidification,elevated temperature,and reduced salinity on early-life stages of the Pacific oyster.Environ Sci Technol,48:10079-10088
Kuroyanagi A,Kawahata H,Suzuki A,Fujita K,Irie T.2009.Impacts of ocean acidification on large benthic foraminifers:Results from laboratory experiments.Mar Micropaleontol,73:190-195
Kurtarkar S R,Nigam R,Saraswat R,Linshy V N.2011.Regeneration and abnormality in benthic foraminifera Rosalina leei:Implications in reconstructing past salinity changes.Riv Ital Paleontol Stratigr,117:189-196
Le Cadre V,Debenay J P,Lesourd M.2003.Low pH effects on Ammonia beccarii test deformation:Implications for using test deformations as a pollution indicator.J Foraminiferal Res,33:1-9
Lei Y,Li T.2016.Atlas of Benthic Foraminifera from China Seas the Bohai Sea and the Yellow Sea.Beijing:Springer-Verlag GmbH Germany and Science Press.399
Lei Y,Li T,Jian Z,Nigam R.2017.Taxonomy and distribution of benthic foraminifera in an intertidal zone of the Yellow Sea,PR China:Correlations with sediment temperature and salinity.Mar Micropaleontol,133:1-20
Liu S,Liu C,Yan P,Huang Z,Peng T,Zhou Y,Ding H.2013.Research of spectrophotometric pH measurements of sea waters in Jiaozhou Bay and coastal waters of Qingdao(in Chinese).Trans Oceanol Limnol:108-114
Loeblich A R,Tappan H.1988.Foraminiferal Genera and Their Classification.New York:Van Nostrand Reinhold.970
Mahmoudi E,Essid N,Beyrem H,Hedfi A,Boufahja F,Vitiello P,Aissa P.2005.Effects of hydrocarbon contamination on a free living marine nematode community:Results from microcosm experiments.Mar Pollut Bull,50:1197-1204
Manno C,Morata N,Bellerby R.2012.Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma(sinistral).Polar Biol,35:1311-1319
McIntyre-Wressnig A,Bernhard J M,Wit J C,Mccorkle D C.2014.Ocean acidification not likely to affect the survival and fitness of two temperate benthic foraminiferal species:Results from culture experiments.J Foraminiferal Res,44:341-351
Meng Z,Xu K,Lei Y.2011.Community composition,distribution,and contribution of microbenthos in offshore sediments from the Yellow Sea.Cont Shelf Res,31:1437-1446
Milliman J D.1993.Production and accumulation of calcium carbonate in the ocean:Budget of a nonsteady state.Glob Biogeochem Cycle,7:927-957
Muller P H.1974.Sediment production and population biology of the benthic foraminifer Amphistegina madagascariensis.Limnol Oceanogr,19:802-809
Murray J W.2006.Ecology and Applications of Benthic Foraminifera.New York:Cambridge University Press.426
Orr J C,Fabry V J,Aumont O,Bopp L,Doney S C,Feely R A,Gnanadesikan A,Gruber N,Ishida A,Joos F,Key R M,Lindsay K,MaierReimer E,Matear R,Monfray P,Mouchet A,Najjar R G,Plattner G K,Rodgers K B,Sabine C L,Sarmiento J L,Schlitzer R,Slater R D,Totterdell I J,Weirig M F,Yamanaka Y,Yool A.2005.Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms.Nature,437:681-686
Pettit L R,Hart M B,Medina-Sánchez A N,Smart C W,Rodolfo-Metalpa R,Hall-Spencer J M,Prol-Ledesma R M.2013.Benthic foraminifera show some resilience to ocean acidification in the northern Gulf of California,Mexico.Mar Pollut Bull,73:452-462
Pettit L R,Smart C W,Hart M B,Milazzo M,Hall-Spencer J M.2015.Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2gradient.Ecol Evol,5:1784-1793
Qu B,Song J,Yuan H,Li X,Li N.2014.Air-sea CO2exchange process in the southern Yellow Sea in April of 2011,and June,July,October of2012.Cont Shelf Res,80:8-19
Reymond C E,Lloyd A,Kline D I,Dove S G,Pandolfi J M.2013.Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios.Glob Change Biol,19:291-302
Russell A D,H?nisch B,Spero H J,Lea D W.2004.Effects of seawater carbonate ion concentration and temperature on shell U,Mg,and Sr in cultured planktonic foraminifera.Geochim Cosmochim Acta,68:4347-4361
Saalim S M,Saraswat R,Suokhrie T,Nigam R.2018.Assessing the ecological preferences of agglutinated benthic foraminiferal morphogroups from the western Bay of Bengal.Deep-Sea Res Part II-Top Stud Oceanogr,doi:10.1016/j.dsr2.2018.02.002
Sabine C L,Feely R A,Gruber N,Key R M,Lee K,Bullister J L,Wanninkhof R,Wong C S,Wallace D W R,Tilbrook B,Millero F J,Peng TH,Kozyr A,Ono T,Rios A F.2004.The oceanic sink for anthropogenic CO2.Science,305:367-371
Saraswat R,Kouthanker M,Kurtarkar S R,Nigam R,Naqvi S WA,Linshy V N.2015.Effect of salinity induced pH/alkalinity changes on benthic foraminifera:A laboratory culture experiment.Estuar Coast Shelf Sci,153:96-107
SAS Institute Inc..2009.SAS/STAT?9.2 User’s Guide.2nd ed.Cary,NC:SAS Institute Inc
Schneider K,Erez J.2006.The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma.Limnol Oceanogr,51:1284-1293
Sinutok S,Hill R,Doblin M A,Wuhrer R,Ralph P J.2011.Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers.Limnol Oceanogr,56:1200-1212
Sinutok S,Hill R,Kühl M,Doblin M A,Ralph P J.2014.Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis.Mar Biol,161:2143-2154
Uthicke S,Fabricius K E.2012.Productivity gains do not compensate for reduced calcification under near-future ocean acidification in the photosynthetic benthic foraminifer species Marginopora vertebralis.Glob Change Biol,18:2781-2791
Uthicke S,Momigliano P,Fabricius K E.2013.High risk of extinction of benthic foraminifera in this century due to ocean acidification.Sci Rep,3:1769
Wei Q,Zhan R,Zang J,Li R.2010.Distributions and influence factors of the chemical parameters in the Southern Yellow Sea in spring(in Chinese).Mar Sci,34:52-60
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