Science China Earth Sciences

, Volume 62, Issue 2, pp 459–472 | Cite as

Responses of benthic foraminifera to changes of temperature and salinity: Results from a laboratory culture experiment

  • Shuaishuai Dong
  • Yanli LeiEmail author
  • Tiegang LiEmail author
  • Zhimin Jian
Research Paper


The effects of temperature and salinity on intertidal foraminiferal community under laboratory conditions are poorly understood. We designed a two-factor crossed experiment in which foraminiferal communities were cultured at different temperatures (6, 12, and 18°C) and salinities (15, 20, 25, and 30 psu) for 10 weeks. In total, 2616 living (stained) specimens were obtained and analyzed. Foraminiferal abundance ranged from 9 to 202 individuals/10 g wet weight of sediment. The highest abundance was obtained at 12°C, 25 psu and the lowest at 6°C, 15 psu. Statistical results demonstrated that temperature affected foraminiferal community more significantly than salinity. Most foraminiferal community parameters (abundance, species richness, Margalef index, and Shannon-Wiener diversity) were significantly positively correlated to temperature, but not to salinity, whereas Pielou’s evenness was significantly negatively correlated to both temperature and salinity. The interactive effect of temperature and salinity on foraminiferal abundance was significant. In addition, with increasing temperature, the species composition shifted from hyaline Rotaliida to porcellaneous Miliolida. The abundance of dominant species (e.g., Ammonia aomoriensis, A. beccarii, and Quinqueloculina seminula) showed significant positive correlations to temperature. Our study indicated that the intertidal foraminiferal community responds sensitively and rapidly to the changes of salinity and, especially, temperature by shifting foraminiferal species composition and altering the community parameters.


Benthic foraminifera Community parameter Temperature Salinity Culture experiment Intertidal zone 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



We thank the 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. 41476043, 41630965 & 41830539), the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA11030104), the National Program on ‘Global Change and Air-Sea Interaction’ (Grant No. GASI-03-01-03-01), the Continental Shelf Drilling Program of China (Grant No. GZH201100202), the Paul Brönnimann Foundation 2014.

Supplementary material

11430_2017_9269_MOESM1_ESM.pdf (586 kb)
Appendix: Responses of foraminifera to temperature and salinity


  1. Allison N, Austin W, Paterson D, Austin H. 2010. Culture studies of the benthic foraminifera Elphidium williamsoni: Evaluating pH, Λ[CO3 2-] and inter-individual effects on test Mg/Ca. Chem Geol, 274: 87–93CrossRefGoogle Scholar
  2. 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
  3. Alve E, Murray J W. 1999. Marginal marine environments of the Skagerrak and Kattegat: A baseline study of living (stained) benthic foraminiferal ecology. Palaeogeogr Palaeoclimatol Palaeoecol, 146: 171–193CrossRefGoogle Scholar
  4. Alve E, Murray J W. 2001. Temporal variability in vertical distributions of live (stained) intertidal foraminifera, southern England. J Foraminifer Res, 31: 12–24CrossRefGoogle Scholar
  5. Basson P W, Murray J W. 1995. Temporal variations in four species of intertidal foraminifera, Bahrain, Arabian Gulf. Micropaleontology, 41: 69–76CrossRefGoogle Scholar
  6. Bé A W H, Hutson W H. 1977. Ecology of planktonic foraminifera and biogeographic patterns of life and fossil assemblages in the Indian Ocean. Micropaleontology, 23: 369–414CrossRefGoogle Scholar
  7. Berkeley A, Perry C T, Smithers S G, Horton B P. 2008. The spatial and vertical distribution of living (stained) benthic foraminifera from a tropical, intertidal environment, north Queensland, Australia. Mar Micropaleontol, 69: 240–261CrossRefGoogle Scholar
  8. Berkeley A, Perry C T, Smithers S G, Horton B P, Taylor K G. 2007. A review of the ecological and taphonomic controls on foraminiferal assemblage development in intertidal environments. Earth-Sci Rev, 83: 205–230CrossRefGoogle Scholar
  9. Bernhard J M. 1988. Postmortem vital staining in benthic foraminifera; duration and importance in population and distributional studies. J Foraminifer Res, 18: 143–146CrossRefGoogle Scholar
  10. Bernhard J M. 2000. Distinguishing live from dead foraminifera: Methods review and proper applications. Micropaleontology, 46: 38–46Google Scholar
  11. Bernhard J M, Buck K R, Barry J P. 2001. Monterey Bay cold-seep biota: Assemblages, abundance, and ultrastructure of living foraminifera. Deep-Sea Res Part I-Oceanogr Res Pap, 48: 2233–2249CrossRefGoogle Scholar
  12. Buzas M A, Hayek L A C, Reed S A, Jett J A. 2002. Foraminiferal densities over five years in the Indian River Lagoon, Florida: A model of pulsating patches. J Foraminifer Res, 32: 68–92CrossRefGoogle Scholar
  13. Clarke K R, Gorley R N. 2006. PRIMER: User Manual/Tutorial Version 6Google Scholar
  14. Culver S J, Buzas M A. 1995. The effects of anthropogenic habitat disturbance, habitat destruction, and global warming on shallow marine benthic foraminifera. J Foraminifer Res, 25: 204–211CrossRefGoogle Scholar
  15. de Rijk S. 1995. Salinity control on the distribution of salt marsh foraminifera (Great Marshes, Massachusetts). J Foraminifer Res, 25: 156–166CrossRefGoogle Scholar
  16. Debenay J P. 2012. A Guide to 1000 Foraminifera from Southwestern Pacific: New Caledonia. IRD éditions, Institut de recherche pourle développement, Marseille, Publications Scientifiques du Muséum, Muséum national d’Histoire naturelle, Paris. 378Google Scholar
  17. Debenay J P, Guillou J J, Redois F, Geslin E. 2000. Distribution trends of foraminiferal assemblages in paralic environments: A base for using foraminifera as bioindicators. In: Martin R E, ed. Environmental Micropaleontology: The Application of Microfossils to Environmental Geology. Boston: Springer. 39–67CrossRefGoogle Scholar
  18. Debenay J P, Bicchi E, Goubert E, Armynot du Châtelet E. 2006. Spatiotemporal distribution of benthic foraminifera in relation to estuarine dynamics (Vie estuary, Vendée, W France). Estuar Coast Shelf Sci, 67: 181–197CrossRefGoogle Scholar
  19. Dissard D, Nehrke G, Reichart G J, Bijma J. 2010. Impact of seawater pCO2 on calcification and Mg/Ca and Sr/Ca ratios in benthic foraminifera calcite: Results from culturing experiments with Ammonia tepida. Biogeosciences, 7: 81–93CrossRefGoogle Scholar
  20. Dorst S, Schönfeld J. 2013. Diversity of benthic foraminifera on the shelf and slope of the NE Atlantic: Analysis of datasets. J Foraminifer Res, 43: 238–254CrossRefGoogle Scholar
  21. Duros P, Jorissen F J, Cesbron F, Zaragosi S, Schmidt S, Metzger E, Fontanier C. 2014. Benthic foraminiferal thanatocoenoses from the Cap-Ferret Canyon area (NE Atlantic): A complex interplay between hydro-sedimentary and biological processes. Deep-Sea Res Part II-Top Stud Oceanogr, 104: 145–163CrossRefGoogle Scholar
  22. Fontanier C, Jorissen F J, Licari L, Alexandre A, Anschutz P, Carbonel P. 2002. Live benthic foraminiferal faunas from the Bay of Biscay: Faunal density, composition, and microhabitats. Deep-Sea Res Part I-Oceanogr Res Pap, 49: 751–785CrossRefGoogle Scholar
  23. Frontalini F, Margaritelli G, Francescangeli F, Rettori R, Armynot du Châtelet E, Coccioni R. 2013. Benthic foraminiferal assemblages and biotopes in a coastal lake: The case study of Lake Varano (southern Italy). Acta Protozool, 52: 147–160Google Scholar
  24. GB/T 34656–2017. 2017. Specification for Marine Sediment Interstitial Biota Survey. National Standard of the People’s Republic of China (in Chinese). Beijing: China Standard PressGoogle Scholar
  25. Ghosh A, Saha S, Saraswati P K, Banerjee S, Burley S. 2009. Intertidal foraminifera in the macro-tidal estuaries of the Gulf of Cambay: Implications for interpreting sea-level change in palaeo-estuaries. Mar Pet Geol, 26: 1592–1599CrossRefGoogle Scholar
  26. Goineau A, Fontanier C, Jorissen F J, Lansard B, Buscail R, Mouret A, Kerhervé P, Zaragosi S, Ernoult E, Artéro C, Anschutz P, Metzger E, Rabouille C. 2011. Live (stained) benthic foraminifera from the Rhône prodelta (Gulf of Lion, NW Mediterranean): Environmental controls on a river-dominated shelf. J Sea Res, 65: 58–75CrossRefGoogle Scholar
  27. Goineau A, Fontanier C, Mojtahid M, Fanget A S, Bassetti M A, Berné S, Jorissen F. 2015. Live-dead comparison of benthic foraminiferal faunas from the Rhône prodelta (Gulf of Lions, NW Mediterranean): Development of a proxy for palaeoenvironmental reconstructions. Mar Micropaleontol, 119: 17–33CrossRefGoogle Scholar
  28. Goldstein S, Alve E. 2011. Experimental assembly of foraminiferal communities from coastal propagule banks. Mar Ecol Prog Ser, 437: 1–11CrossRefGoogle Scholar
  29. Gross O. 2000. Influence of temperature, oxygen and food availability on the migrational activity of bathyal benthic foraminifera: Evidence by microcosm experiments. Hydrobiologia, 426: 123–137CrossRefGoogle Scholar
  30. Haynert K, Schönfeld J, Schiebel R, Wilson B, Thomsen J. 2014. Response of benthic foraminifera to ocean acidification in their natural sediment environment: A long-term culturing experiment. Biogeosciences, 11: 1581–1597CrossRefGoogle Scholar
  31. Haynert K, Schönfeld J. 2014. Impact of changing carbonate chemistry, temperature, and salinity on growth and test degradation of the benthic foraminifer Ammonia aomoriensis. J Foraminifer Res, 44: 76–89CrossRefGoogle Scholar
  32. Hayward B W, Grenfell H R, Nicholson K, Parker R, Wilmhurst J, Horrocks M, Swales A, Sabaa A T. 2004. Foraminiferal record of human impact on intertidal estuarine environments in New Zealand’s largest city. Mar Micropaleontol, 53: 37–66CrossRefGoogle Scholar
  33. Horton B P, Edwards R J, Lloyd J M. 1999. UK intertidal foraminiferal distributions: Implications for sea-level studies. Mar Micropaleontol, 36: 205–223CrossRefGoogle Scholar
  34. Jorissen F, Fontanier C, Thomas E. 2007. Paleoceanographical proxies based on deep-sea benthic foraminiferal assemblage characteristics. In: Hillaire-Marcel C, Vernal A de, eds. Proxies in Late Cenozoic paleoceanography. Amsterdam: Elsevier Science. 263–326CrossRefGoogle Scholar
  35. Kitazato H, Bernhard J M. 2014. Approaches to Study Living Foraminifera. Tokyo: Springer. 227CrossRefGoogle Scholar
  36. 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
  37. Lee J J, Pierce S, Tentchoff M, McLaughlin J J A. 1961. Growth and physiology of foraminifera in the laboratory: Part 1 Collection and maintenance. Micropaleontology, 7: 461–466CrossRefGoogle Scholar
  38. Lei Y, Li C, Li T, Jian Z. 2016. Laboratorial culture of Ammonia beccarii (Linnaeus, 1758): The effect of temperature and food concentration on chamber growth and ingestion rate on diatom (in Chinese). Acta Micropalaeontol Sin, 33: 350–362Google Scholar
  39. Lei Y, Li T. 2015. Ammonia Aomoriensis (Asano, 1951) and Ammonia Beccarii (Linnaeus, 1758)(Foraminifera): Comparisons on their taxonomy and ecological distributions correlated to temperature, salinity and depth in the Yellow Sea and the East China Sea (in Chinese). Acta Micropalaeontol Sin, 32: 1–19Google Scholar
  40. 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
  41. Lei Y, Li T, Jian Z, Nigam R. 2017a. 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
  42. Lei Y, Li T, Nigam R, Holzmann M, Lyu M. 2017b. Environmental significance of morphological variations in the foraminifer Ammonia aomoriensis (Asano, 1951) and its molecular identification: A study from the Yellow Sea and East China Sea, PR China. Palaeogeogr Palaeoclimatol Palaeoecol, 483: 49–57CrossRefGoogle Scholar
  43. Li T, Xiang R, Li T. 2015. Application of a self-organizing map and canonical correspondence analysis in modern benthic foraminiferal communities: A case study from the Pearl River Estuary, China. J Foraminifer Res, 45: 305–318CrossRefGoogle Scholar
  44. Loeblich A R, Tappan H. 1988. Foraminiferal Genera and Their Classification. New York: Springer. 970CrossRefGoogle Scholar
  45. Lombard F, Labeyrie L, Michel E, Spero H J, Lea D W. 2009. Modelling the temperature dependent growth rates of planktic foraminifera. Mar Micropaleontol, 70: 1–7CrossRefGoogle Scholar
  46. Murray J W. 1991. Ecology and Palaeoecology of Benthic Foraminifera. New York: Longman. 397Google Scholar
  47. Murray J W. 2006. Ecology and Applications of Benthic Foraminifera. New York: Cambridge University Press. 426CrossRefGoogle Scholar
  48. Murray J W, Alve E. 2000. Major aspects of foraminiferal variability (standing crop and biomass) on a monthly scale in an intertidal zone. J Foraminifer Res, 30: 177–191CrossRefGoogle Scholar
  49. Nardelli M P, Sabbatini A, Negri A. 2013. Experimental chronic exposure of the foraminifer Pseudotriloculina rotunda to zinc. Acta Protozool, 52: 193Google Scholar
  50. Nigam R. 2005. Addressing environmental issues through foraminifera— Case studies from the Arabian Sea. J Palaeontol Soc India, 50: 25–36Google Scholar
  51. Nigam R, Saraswat R, Kurtarkar S R. 2006. Laboratory experiment to study the effect of salinity variations on benthic foraminiferal species-Pararotalia nipponica (Asano). J Geol Soc India, 67: 41–46Google Scholar
  52. Nigam R, Kurtarkar S R, Saraswat R, Linshy V N, Rana S S. 2008. Response of benthic foraminifera Rosalina leei to different temperature and salinity, under laboratory culture experiment. J Mar Biol Ass, 88: 699–704CrossRefGoogle Scholar
  53. Ongan D, Algan O, Kapan-Yesilyurt S, Nazik A, Ergin M, Eastoe C, Güneybati K, Holosen S, Topluluklari F. 2009. Benthic faunal assemblages of the Holocene sediments from the southwest Black Sea shelf. Turk J Earth Sci, 18: 239–297Google Scholar
  54. Papaspyrou S, Diz P, García-Robledo E, Corzo A, Jimenez-Arias J. 2013. Benthic foraminiferal community changes and their relationship to environmental dynamics in intertidal muddy sediments (Bay of Cádiz, SW Spain). Mar Ecol Prog Ser, 490: 121–135CrossRefGoogle Scholar
  55. Prazeres M, Pandolfi J M. 2016. Effects of Elevated Temperature on the Shell Density of the Large Benthic Foraminifera Amphistegina lobifera. J Eukaryot Microbiol, 63: 786–793CrossRefGoogle Scholar
  56. Prazeres M, Uthicke S, Pandolfi J M. 2016. Influence of local habitat on the physiological responses of large benthic foraminifera to temperature and nutrient stress. Sci Rep, 6: 21936CrossRefGoogle Scholar
  57. Saad S A, Wade C M. 2016. Seasonal and spatial variations of saltmarsh benthic foraminiferal communities from North Norfolk, England. Microb Ecol, 73: 539–555CrossRefGoogle Scholar
  58. Saraswat R, Nigam R, Pachkhande S. 2011. Difference in optimum temperature for growth and reproduction in benthic foraminifer Rosalina globularis: Implications for paleoclimatic studies. J Exp Mar Biol Ecol, 405: 105–110CrossRefGoogle Scholar
  59. SAS Institute Inc.. 2009. SAS/STAT® User’s Guide Version 9.2Google Scholar
  60. Scavia D, Field J C, Boesch D F, Buddemeier R W, Burkett V, Cayan D R, Fogarty M, Harwell M A, Howarth R W, Mason C, Reed D J, Royer T C, Sallenger A H, Titus J G. 2002. Climate Change Impacts on U.S. Coastal and Marine Ecosystems. Estuaries, 25: 149–164Google Scholar
  61. Schmidt C, Heinz P, Kucera M, Uthicke S. 2011. Temperature-induced stress leads to bleaching in larger benthic foraminifera hosting endosymbiotic diatoms. Limnol Oceanogr, 56: 1587–1602CrossRefGoogle Scholar
  62. Scott D S, Medioli F S. 1978. Vertical zonations of marsh foraminifera as accurate indicators of former sea-levels. Nature, 272: 528–531CrossRefGoogle Scholar
  63. Stefanoudis P V, Bett B J, Gooday A J. 2017. Relationship between ‘live’ and dead benthic foraminiferal assemblages in the abyssal NE Atlantic. Deep-Sea Res Part I-Oceanogr Res Pap, 121: 190–201CrossRefGoogle Scholar
  64. Weinmann A E, Goldstein S T. 2016. Changing structure of benthic foraminiferal communities: Implications from experimentally grown assemblages from coastal Georgia and Florida, USA. Mar Ecol, 37: 891–906CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine Organism Taxonomy & Phylogeny, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Key Laboratory of Marine Sedimentology and Environmental Geology, First Institute of OceanographySOAQingdaoChina
  3. 3.State Key Laboratory of Marine GeologyTongji UniversityShanghaiChina
  4. 4.Laboratory for Marine GeologyQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  5. 5.University of Chinese Academy of SciencesBeijingChina
  6. 6.Center for Ocean Mega-ScienceChinese Academy of SciencesQingdaoChina

Personalised recommendations