Changing structure of benthic foraminiferal communities due to declining pH: Results from laboratory culture experiments

  • Shuaishuai Dong
  • Yanli LeiEmail author
  • Tiegang Li
  • Zhimin JianEmail author
Research Paper


The ocean absorbs large amounts of CO2 emitted from human activities, which results in a decrease in seawater pH. 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 pH 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 pH manipulation. Our results indicated that nearshore foraminiferal communities showed rather a resilience to the declining pH 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.


Benthic foraminifera Community pH Laboratory culture experiment Yellow Sea 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



We thank Lina Cao, Man Lyu, Meng Li and the crew of R/V Dongfanghong 2 for help in sampling and technical assistance. We thank two anonymous reviewers for constructive comments on the earlier version of this manuscript. The authors thank to the Jiaozhou Bay Marine Ecosystem Research Station, Chinese Academy of Sciences for sharing the voyage and providing CTD data. This work was supported by the National Natural Science Foundation of China (Grant Nos. 41630965 & 41830539), Monitoring and Protection of Ecology and Environment in the East Pacific Ocean (Granted No. DY135-E2-5), the Senior User Project of RV KEXUE (Grant No. KEXUE2018G27), the Paul Brönnimann Foundation 2014.

Supplementary material

11430_2018_9321_MOESM1_ESM.pdf (5.4 mb)
Supplementary material, approximately 5.44 MB.


  1. Al-Sabouni N, Kucera M, Schmidt D N. 2007. Vertical niche separation control of diversity and size disparity in planktonic foraminifera. Mar Micropaleontol, 63: 75–90CrossRefGoogle Scholar
  2. Allison N, Austin W, Paterson D, Austin H. 2010. Culture studies of the benthic foraminifera Elphidium williamsoni: Evaluating pH, Δ[CO3 2-] and inter-individual effects on test Mg/Ca. Chem Geol, 274: 87–93CrossRefGoogle Scholar
  3. 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: 171–178CrossRefGoogle Scholar
  4. Alve E, Goldstein S T. 2003. Propagule transport as a key method of dispersal in benthic foraminifera (Protista). Limnol Oceanogr, 48: 2163–2170CrossRefGoogle Scholar
  5. 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: 2078–2088CrossRefGoogle Scholar
  6. Caldeira K, Wickett M E. 2003. Anthropogenic carbon and ocean pH. Nature, 425: 365CrossRefGoogle Scholar
  7. 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 CO2 vents. Mar Biol, 157: 2489–2502CrossRefGoogle Scholar
  8. Clarke K R, Gorley R N. 2006. PRIMER v6: User Manual/Tutorial. Plymouth: PRIMER-E LtdGoogle Scholar
  9. 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: 2225CrossRefGoogle Scholar
  10. 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: 53–66CrossRefGoogle Scholar
  11. 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: 89–98CrossRefGoogle Scholar
  12. Dias B B, Hart M B, Smart C W, Hall-Spencer J M. 2010. Modern seawater acidification: The response of foraminifera to high-CO2 conditions in the Mediterranean Sea. J Geol Soc, 167: 843–846CrossRefGoogle Scholar
  13. 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)Google Scholar
  14. 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: 633–649CrossRefGoogle Scholar
  15. 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: 414–432CrossRefGoogle Scholar
  16. 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 ChinaGoogle Scholar
  17. 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: 607–620CrossRefGoogle Scholar
  18. 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: 159–186CrossRefGoogle Scholar
  19. 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: 1425–1430CrossRefGoogle Scholar
  20. Kisakürek B, Eisenhauer A, Böhm F, Garbe-Schönberg D, Erez J. 2008. Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan, Globigerinoides ruber (white). Earth Planet Sci Lett, 273: 260–269CrossRefGoogle Scholar
  21. 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: 10079–10088CrossRefGoogle Scholar
  22. 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: 190–195CrossRefGoogle Scholar
  23. 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: 189–196Google Scholar
  24. 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: 1–9CrossRefGoogle Scholar
  25. 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. 399CrossRefGoogle Scholar
  26. 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: 1–20CrossRefGoogle Scholar
  27. 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: 108–114Google Scholar
  28. Loeblich A R, Tappan H. 1988. Foraminiferal Genera and Their Classification. New York: Van Nostrand Reinhold. 970CrossRefGoogle Scholar
  29. 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: 1197–1204CrossRefGoogle Scholar
  30. Manno C, Morata N, Bellerby R. 2012. Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma (sinistral). Polar Biol, 35: 1311–1319CrossRefGoogle Scholar
  31. 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: 341–351CrossRefGoogle Scholar
  32. 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: 1437–1446CrossRefGoogle Scholar
  33. Milliman J D. 1993. Production and accumulation of calcium carbonate in the ocean: Budget of a nonsteady state. Glob Biogeochem Cycle, 7: 927–957CrossRefGoogle Scholar
  34. Muller P H. 1974. Sediment production and population biology of the benthic foraminifer Amphistegina madagascariensis. Limnol Oceanogr, 19: 802–809CrossRefGoogle Scholar
  35. Murray J W. 2006. Ecology and Applications of Benthic Foraminifera. New York: Cambridge University Press. 426CrossRefGoogle Scholar
  36. 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, Maier-Reimer 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: 681–686CrossRefGoogle Scholar
  37. 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: 452–462CrossRefGoogle Scholar
  38. 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 CO2 gradient. Ecol Evol, 5: 1784–1793CrossRefGoogle Scholar
  39. Qu B, Song J, Yuan H, Li X, Li N. 2014. Air-sea CO2 exchange process in the southern Yellow Sea in April of 2011, and June, July, October of 2012. Cont Shelf Res, 80: 8–19CrossRefGoogle Scholar
  40. 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: 291–302CrossRefGoogle Scholar
  41. Russell A D, Hönisch 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: 4347–4361CrossRefGoogle Scholar
  42. 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.dsr2.2018.02.002Google Scholar
  43. 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 T H, Kozyr A, Ono T, Rios A F. 2004. The oceanic sink for anthropogenic CO2. Science, 305: 367–371CrossRefGoogle Scholar
  44. Saraswat R, Kouthanker M, Kurtarkar S R, Nigam R, Naqvi S W A, Linshy V N. 2015. Effect of salinity induced pH/alkalinity changes on benthic foraminifera: A laboratory culture experiment. Estuar Coast Shelf Sci, 153: 96–107CrossRefGoogle Scholar
  45. SAS Institute Inc. 2009. SAS/STAT® 9.2 User’s Guide. 2nd ed. Cary, NC: SAS Institute IncGoogle Scholar
  46. Schneider K, Erez J. 2006. The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr, 51: 1284–1293CrossRefGoogle Scholar
  47. 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: 1200–1212CrossRefGoogle Scholar
  48. 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: 2143–2154CrossRefGoogle Scholar
  49. 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: 2781–2791CrossRefGoogle Scholar
  50. 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: 1769CrossRefGoogle Scholar
  51. 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: 52–60Google Scholar
  52. 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: 1708–1715CrossRefGoogle Scholar
  53. Xin M, Ma D, Wang B. 2015. Chemicohydrographic characteristics of the Yellow Sea cold water mass. Acta Oceanol Sin, 34: 5–11CrossRefGoogle Scholar
  54. Yu J, Foster G L, Elderfield H, Broecker W S, Clark E. 2010. An evaluation of benthic foraminiferal B/Ca and δ11B for deep ocean carbonate ion and pH reconstructions. Earth Planet Sci Lett, 293: 114–120CrossRefGoogle Scholar
  55. Zhai W D. 2018. Exploring seasonal acidification in the Yellow Sea. Sci China Earth Sci, 61: 647–658CrossRefGoogle Scholar
  56. Zhai W D, Zheng N, Huo C, Xu Y, Zhao H D, Li Y W, Zang K P, Wang J Y, Xu X M. 2014. Subsurface pH and carbonate saturation state of aragonite on the Chinese side of the North Yellow Sea: Seasonal variations and controls. Biogeosciences, 11: 1103–1123CrossRefGoogle Scholar
  57. Zhang M, Fang J, Zhang J, Li B, Ren S, Mao Y, Gao Y. 2011. Effect of Marine Acidification on Calcification and Respiration of Chlamys farreri. J Shellfish Res, 30: 267–271CrossRefGoogle Scholar
  58. Zhao L, Schöne B R, Mertz-Kraus R, Yang F. 2017. Insights from sodium into the impacts of elevated pCO2 and temperature on bivalve shell formation. J Exp Mar Biol Ecol, 486: 148–154CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Marine Organism Taxonomy and Phylogeny, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Key Laboratory of Marine Sedimentology and Environmental GeologyFirst Institute of Oceanography, MNRQingdaoChina
  3. 3.State Key Laboratory of Marine GeologyTongji UniversityShanghaiChina
  4. 4.Laboratory for Marine Biology and BiotechnologyPilot National Laboratory for Marine Science and Technology (Qingdao)QingdaoChina
  5. 5.University of Chinese Academy of SciencesBeijingChina
  6. 6.Center for Ocean Mega-ScienceChinese Academy of SciencesQingdaoChina

Personalised recommendations