Skip to main content
Log in

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

  • Research Paper
  • Published:
Science China Earth Sciences Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allison N, Austin W, Paterson D, Austin H. 2010. Culture studies of the benthic foraminifera Elphidium williamsoni: Evaluating pH, Λ[CO32-] and inter-individual effects on test Mg/Ca. Chem Geol, 274: 87–93

    Google Scholar 

  • 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

    Google Scholar 

  • 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: 171–193

    Google Scholar 

  • Alve E, Murray J W. 2001. Temporal variability in vertical distributions of live (stained) intertidal foraminifera, southern England. J Foraminifer Res, 31: 12–24

    Google Scholar 

  • Basson P W, Murray J W. 1995. Temporal variations in four species of intertidal foraminifera, Bahrain, Arabian Gulf. Micropaleontology, 41: 69–76

    Google Scholar 

  • 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: 369–414

    Google Scholar 

  • 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: 240–261

    Google Scholar 

  • 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: 205–230

    Google Scholar 

  • Bernhard J M. 1988. Postmortem vital staining in benthic foraminifera; duration and importance in population and distributional studies. J Foraminifer Res, 18: 143–146

    Google Scholar 

  • Bernhard J M. 2000. Distinguishing live from dead foraminifera: Methods review and proper applications. Micropaleontology, 46: 38–46

    Google Scholar 

  • 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: 2233–2249

    Google Scholar 

  • 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: 68–92

    Google Scholar 

  • Clarke K R, Gorley R N. 2006. PRIMER: User Manual/Tutorial Version 6

    Google Scholar 

  • 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: 204–211

    Google Scholar 

  • de Rijk S. 1995. Salinity control on the distribution of salt marsh foraminifera (Great Marshes, Massachusetts). J Foraminifer Res, 25: 156–166

    Google Scholar 

  • 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. 378

    Google Scholar 

  • 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. 39–67

    Google Scholar 

  • 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: 181–197

    Google Scholar 

  • 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: 81–93

    Google Scholar 

  • 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: 238–254

    Google Scholar 

  • 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: 145–163

    Google Scholar 

  • 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: 751–785

    Google Scholar 

  • 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: 147–160

    Google Scholar 

  • 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 Press

  • 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: 1592–1599

    Google Scholar 

  • 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: 58–75

    Google Scholar 

  • 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: 17–33

    Google Scholar 

  • Goldstein S, Alve E. 2011. Experimental assembly of foraminiferal communities from coastal propagule banks. Mar Ecol Prog Ser, 437: 1–11

    Google Scholar 

  • Gross O. 2000. Influence of temperature, oxygen and food availability on the migrational activity of bathyal benthic foraminifera: Evidence by microcosm experiments. Hydrobiologia, 426: 123–137

    Google Scholar 

  • 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: 1581–1597

    Google Scholar 

  • 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: 76–89

    Google Scholar 

  • 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: 37–66

    Google Scholar 

  • Horton B P, Edwards R J, Lloyd J M. 1999. UK intertidal foraminiferal distributions: Implications for sea-level studies. Mar Micropaleontol, 36: 205–223

    Google Scholar 

  • 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. 263–326

    Google Scholar 

  • Kitazato H, Bernhard J M. 2014. Approaches to Study Living Foraminifera. Tokyo: Springer. 227

    Google Scholar 

  • 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

    Google Scholar 

  • 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: 461–466

    Google Scholar 

  • 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: 350–362

    Google Scholar 

  • 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: 1–19

    Google Scholar 

  • 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

    Google Scholar 

  • 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: 1–20

    Google Scholar 

  • 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: 49–57

    Google Scholar 

  • 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: 305–318

    Google Scholar 

  • Loeblich A R, Tappan H. 1988. Foraminiferal Genera and Their Classification. New York: Springer. 970

    Google Scholar 

  • 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: 1–7

    Google Scholar 

  • Murray J W. 1991. Ecology and Palaeoecology of Benthic Foraminifera. New York: Longman. 397

    Google Scholar 

  • Murray J W. 2006. Ecology and Applications of Benthic Foraminifera. New York: Cambridge University Press. 426

    Google Scholar 

  • 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: 177–191

    Google Scholar 

  • Nardelli M P, Sabbatini A, Negri A. 2013. Experimental chronic exposure of the foraminifer Pseudotriloculina rotunda to zinc. Acta Protozool, 52: 193

    Google Scholar 

  • Nigam R. 2005. Addressing environmental issues through foraminifera— Case studies from the Arabian Sea. J Palaeontol Soc India, 50: 25–36

    Google Scholar 

  • 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: 41–46

    Google Scholar 

  • 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: 699–704

    Google Scholar 

  • 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: 239–297

    Google Scholar 

  • 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: 121–135

    Google Scholar 

  • 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: 786–793

    Google Scholar 

  • 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: 21936

    Google Scholar 

  • Saad S A, Wade C M. 2016. Seasonal and spatial variations of saltmarsh benthic foraminiferal communities from North Norfolk, England. Microb Ecol, 73: 539–555

    Google Scholar 

  • 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: 105–110

    Google Scholar 

  • SAS Institute Inc.. 2009. SAS/STAT® User’s Guide Version 9.2

  • 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: 149–164

    Google Scholar 

  • 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: 1587–1602

    Google Scholar 

  • Scott D S, Medioli F S. 1978. Vertical zonations of marsh foraminifera as accurate indicators of former sea-levels. Nature, 272: 528–531

    Google Scholar 

  • 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: 190–201

    Google Scholar 

  • 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: 891–906

    Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yanli Lei or Tiegang Li.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, S., Lei, Y., Li, T. et al. Responses of benthic foraminifera to changes of temperature and salinity: Results from a laboratory culture experiment. Sci. China Earth Sci. 62, 459–472 (2019). https://doi.org/10.1007/s11430-017-9269-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11430-017-9269-3

Keywords

Navigation