Abstract
Calcifying organisms such as benthic foraminifera are susceptible to changes in ocean pH and alkalinity. Responses to these changes include variations in mortality, calcification rates or assemblage composition, which have been observed in field and experimental studies. Here we applied a growth experiment with benthic foraminiferal propagules under different pH conditions to gather insights into the effect of pH on the composition of grown assemblages. A homogeneous propagule assemblage from a local mudflat in Corfu Island (Greece) was exposed to a range of pH conditions (6.5, 7.2, 7.8 and 8.5) for 5 weeks. In a second experiment, the assemblages were first exposed to low and subsequently to high conditions for a total of 8 weeks. After termination of the experiments, we recorded high survivability and growth throughout the treatments. Analysis of the assemblage composition of the first experiments revealed a shift from porcelaneous dominated taxa in the higher pH treatments to an assemblage with higher numbers of agglutinated taxa in the lower pH treatments. Soft-shelled monothalamous species were common throughout. The second experiment revealed assemblages that were significantly dominated by porcelaneous taxa with monothalamous taxa being almost absent. The results of this study are congruent with other observations on changing assemblage compositions with changing pH from both laboratory and field studies. The fast response of the assemblages through activation of potentially dormant propagules adds insights into the mechanisms behind seasonal composition changes in naturally variable environments such as river estuaries. They also shed new light on possible effects of continuous decreases in ocean pH on shallow-water foraminiferal assemblages in future.
Similar content being viewed by others
Availability of data and material
All relevant data will be published as supplementary material along with the article.
References
Allison N, Austin H, Austin W, Paterson DM (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. https://doi.org/10.1016/j.chemgeo.2011.08.001
Alve E, Goldstein ST (2002) Resting stage in benthic foraminiferal propagules: a key feature for dispersal? Evidence from two shallow-water species. J Micropalaeontol 21:95–96. https://doi.org/10.1144/jm.21.1.95
Alve E, Goldstein ST (2003) Propagule transport as a key method of dispersal in benthic foraminifera (Protista). Limnol Oceanogr 48:2163–2170. https://doi.org/10.4319/lo.2003.48.6.2163
Alve E, Goldstein ST (2010) Dispersal, survival and delayed growth of benthic foraminiferal propagules. J Sea Res 63:36–51. https://doi.org/10.1016/j.seares.2009.09.003
Baggini C, Salomidi M, Voutsinas E, Bray L, Krasakopoulou E, Hall-Spencer JM (2014) Seasonality affects macroalgal community response to increases in pCO2. PLoS ONE 9:e106520. https://doi.org/10.1371/journal.pone.0106520
Bentov S, Brownlee C, Erez J (2009) The role of seawater endocytosis in the biomineralization process in calcareous foraminifera. Proc Nat Acad Sci USA 106:21500–21504. https://doi.org/10.1073/pnas.0906636106
Brouillette Price E, Kabengi N, Goldstein ST (2019) Effects of heavy-metal contaminants (Cd, Pb, Zn) on benthic foraminiferal assemblages grown from propagules, Sapelo Island, Georgia (USA). Mar Micropaleontol 147:1–11. https://doi.org/10.1016/j.marmicro.2019.01.004
Camacho S, Moura D, Connor S, Scott D, Boski T (2015) Ecological zonation of benthic foraminifera in the lower Guadiana Estuary (southeastern Portugal). Mar Micropaleontol 114:1–18. https://doi.org/10.1016/j.marmicro.2014.10.004
Carstensen J, Duarte CM (2019) Drivers of pH variability in coastal ecosystems. Environ Sci Technol 53:4020–4029. https://doi.org/10.1021/acs.est.8b03655
Cesbron F, Geslin E, Jorissen FJ, Delgard ML, Charrieau L, Deflandre B et al (2016) Vertical distribution and respiration rates of benthic foraminifera. Contribution to aerobic remineralization in intertidal mudflats covered by Zostera noltei meadows. Estuar Coast Shelf Sci 179:23–38. https://doi.org/10.1016/j.ecss.2015.12.005
Charrieau LM, Filipsson HL, Ljung K, Chierici M, Knudsen KL, Kritzberg E (2018a) The effects of multiple stressors on the distribution of coastal benthic foraminifera: a case study from the Skagerrak-Baltic Sea region. Mar Micropaleontol 139:42–56. https://doi.org/10.1016/j.marmicro.2017.11.004
Charrieau LM, Filipsson HL, Nagai Y, Kawada S, Ljung K, Kritzberg E, Toyofuku T (2018b) Decalcification and survival of benthic foraminifera under the combined impacts of varying pH and salinity. Mar Environ Res 138:36–45. https://doi.org/10.1016/j.marenvres.2018.03.015
Cimerman F, Langer MR (1991) Mediterranean foraminifera. Academia Scientarium et Artium Slovenica, Opera 30, Ljubljana
Debenay JP, Guillou JJ, Redois F, Geslin E (2000) Distribution trends of foraminiferal assemblages in paralic environments. In: Martin RE (ed) Environmental micropaleontology. Topics in geobiology, vol 15. Springer. Boston, MA, pp 40–70. https://doi.org/10.1007/978-1-4615-4167-7_3
Debenay JP, Guiral D, Parra M (2002) Ecological factors acting on the microfauna in mangrove swamps. The case of foraminiferal assemblages in French Guiana. Estuar Coast Shelf Sci 55:509–533. https://doi.org/10.1006/ecss.2001.0906
Debenay JP, Millet B, Angelidis MO (2005) Relationships between foraminiferal assemblages and hydrodynamics in the Gulf of Kalloni, Greece. J Foraminifer Res 35:327–343. https://doi.org/10.2113/35.4.327
Debenay JP, Bicch E, Goubert E, Du Armynot CE (2006) Spatio-temporal distribution of benthic foraminifera in relation to estuarine dynamics (Vie estuary, Vendée, W France). Estuar Coast Shelf Sci 67:181–197. https://doi.org/10.1016/j.ecss.2005.11.014
Dias BB, Hart MB, Smart CW, Hall-Spencer JM (2010) Modern seawater acidification. The response of foraminifera to high-CO2 conditions in the Mediterranean Sea. J Geol Soc 167:843–846. https://doi.org/10.1144/0016-76492010-050
Dimiza MD, Koukousioura O, Triantaphyllou MV, Dermitzakis MD (2016) Live and dead benthic foraminiferal assemblages from coastal environments of the Aegean Sea (Greece): distribution and diversity. Rev Micropaleontol 59:19–32. https://doi.org/10.1016/j.revmic.2015.10.002
Dissard D, Nehrke G, Reichart GJ, 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. https://doi.org/10.5194/bg-7-81-2010
Dong S, Lei Y, Li T, Jian Z (2019) Changing structure of benthic foraminiferal communities due to declining pH. Results from laboratory culture experiments. Sci China Earth Sci 62:1151–1166. https://doi.org/10.1007/s11430-018-9321-6
Dong S, Lei Y, Li T, Jian Z (2020) Response of benthic foraminifera to pH changes. Community structure and morphological transformation studies from a microcosm experiment. Mar Micropaleontol 156:101819. https://doi.org/10.1016/j.marmicro.2019.101819
Erskian MG, Lipps JH (1977) Distribution of foraminifera in the Russian River estuary, northern California. Micropaleontol 23:453–469
Fabry VJ (2008) Marine calcifiers in a high-CO2 ocean. Science 320:1020–1022. https://doi.org/10.1126/science.1157130
Fajemila OT, Sariaslan N, Langer MR (2020) Spatial distribution of benthic foraminifera in the Lagos Lagoon (Nigeria) Tracing the impact of environmental perturbations. PLoS ONE 15:e0243481. https://doi.org/10.1371/journal.pone.0243481
Fischer P, Cl F, Röbke BR, Baika K, Hadler H, Willershäuser T, Rigakou D, Metallinou G, Vött A (2016) Impact of Holocene tsunamis detected in lagoonal environments on Corfu (Ionian Islands, Greece) Geomorphological, sedimentary and microfaunal evidence. Quat Int 401:4–16. https://doi.org/10.1016/j.quaint.2015.07.019
Goldstein ST (1988) On the life cycle of Saccammina alba Hedley, 1962. J Foraminifer Res 18:311–325. https://doi.org/10.2113/gsjfr.18.4.311
Goldstein ST, Alve E (2011) Experimental assembly of foraminiferal communities from coastal propagule banks. Mar Ecol Prog Ser 437:1–11. https://doi.org/10.3354/meps09296
Grell KG (1988) The life-cycle of the monothalamous foraminifer Heterotheca lobata, n. gen., n. sp. J Foraminifer Res 18:54–74. https://doi.org/10.2113/gsjfr.18.1.54
Guamán-Guevara F, Austin H, Hicks N, Streeter R, Austin WEN (2019) Impacts of ocean acidification on intertidal benthic foraminiferal growth and calcification. PLoS ONE 14:e0220046. https://doi.org/10.1371/journal.pone.0220046
Hagens M, Middelburg JJ (2016) Attributing seasonal pH variability in surface ocean waters to governing factors. Geophys Res Lett 43:189. https://doi.org/10.1002/2016GL071719
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol Electronica 4
Hart MB, Molina GS, Smart CW (2020) Estuarine foraminifera from South West England: impact of metal pollution in a mining heritage area. J Sediment Environ 5:1–16. https://doi.org/10.1007/s43217-020-00006-7
Havenhand JN, Filipsson HL, Niiranen S, Troell M, Crépin AS, Jagers S et al (2019) Ecological and functional consequences of coastal ocean acidification. Perspectives from the Baltic–Skagerrak System. Ambio 48:831–854. https://doi.org/10.1007/s13280-018-1110-3
Hayek LAC, Buzas MA (2013) On the proper and efficient use of diversity measures with individual field samples. J Foraminifer Res 43:305–313. https://doi.org/10.2113/gsjfr.43.3.305
Haynert K, Schönfeld J, Riebesell U, Polovodova I (2011) Biometry and dissolution features of the benthic foraminifer Ammonia aomoriensis at high pCO2. Mar Ecol Prog Ser 432:53–67. https://doi.org/10.3354/meps09138
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. https://doi.org/10.5194/bg-11-1581-2014
Hayward BW, Le Coze F, Vachard D, Gross O (2020) World Foraminifera database. Accessed at http://www.marinespecies.org/foraminifera on 2020-11-26. https://doi.org/10.14284/305
Hikami M, Ushie H, Irie T, Fujita K, Kuroyanagi A, Sakai K, Nojiri Y, Suzuki A, Kawahata H (2011) Contrasting calcification responses to ocean acidification between two reef foraminifers harboring different algal symbionts. Geophys Res Lett 38:L19601. https://doi.org/10.1029/2011GL048501
Hoegh-Guldberg O, Cai R, Poloczanska ES, Brewer PG, Sundby S, Hilmi K, Fabry VJ, Jung S (2014) The Ocean. In: Barros, V.R., C.B. Field, D.J. Dokken, M.D. Mastrandrea, K.J. Mach, T.E. Bilir, M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova, B. Girma, E.S. Kissel, A.N. Levy, S. MacCracken, P.R. Mastrandrea, and L.L. White (eds) Climate Change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of working Group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York, NY, USA, pp 1655–1731
Holland K, Eggins SM, Hönisch B, Haynes LL, Branson O (2017) Calcification rate and shell chemistry response of the planktic foraminifer Orbulina universa to changes in microenvironment seawater carbonate chemistry. Earth Planet Sci Lett 464:124–134. https://doi.org/10.1016/j.epsl.2017.02.018
Hottinger L, Halicz E, Reiss Z. (1993) Recent foraminiferida from the Gulf of Aqaba, Red Sea. Slovenska Akademija Znanosti in Umetnosti, Dela Opera, Classics IV, Historia Naturalis, Ljubljana
Howland RJN, Tappin AD, Uncles RJ, Plummer DH, Bloomer NJ (2000) Distributions and seasonal variability of pH and alkalinity in the Tweed Estuary. UK Sci Total Environ 251(252):125–138. https://doi.org/10.1016/S0048-9697(00)00406-X
Khanna N, Godbold JA, Austin WEN, Paterson DM (2013) The impact of ocean acidification on the functional morphology of foraminifera. PLoS ONE 8:e83118. https://doi.org/10.1371/journal.pone.0083118
Knorr PO, Robbins LL, Harries PJ, Hallock P, Wynn J (2015) Response of the miliolid Archaias angulatus to simulated Ocean Acidification. J Foraminifer Res 45:109–127. https://doi.org/10.2113/gsjfr.45.2.109
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS et al (2013) Impacts of ocean acidification on marine organisms. Quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896. https://doi.org/10.1111/gcb.12179
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. https://doi.org/10.1016/j.marmicro.2009.09.003
Le Cadre V, Debenay JP, Lesourd M (2003) Low pH effects on Ammonia beccarii test deformation: implications for using test deformations as a pollution indicator. J Foraminifer Res 33:1–9. https://doi.org/10.2113/0330001
McIntyre-Wressnig A, Bernhard JM, McCorkle DC, Hallock P (2013) Non-lethal effects of ocean acidification on the symbiont-bearing benthic foraminifer Amphistegina gibbosa. Mar Ecol Prog Ser 472:45–60. https://doi.org/10.3354/meps09918
McIntyre-Wressnig A, Bernhard JM, Wit JC, Mccorkle DC (2014) Ocean acidification not likely to affect the survival and fitness of two temperate benthic foraminiferal species: results from culture experiments. J Foraminifer Res 44:341–351. https://doi.org/10.2113/gsjfr.44.4.341
Meric E, Avşar N, Yokeş MB, Dinçer F (2014) Atlas of recent benthic foraminifera from Turkey. Micropaleontol 60:211–398
Milker Y, Schmiedl G (2012) A taxonomic guide to modern benthic shelf foraminifera of the western Mediterranean Sea. Palaeontol Electronica 15:1–134. https://doi.org/10.26879/271
Mouanga GH (2018) Impact and range extension of invasive foraminifera in the NW Mediterranean Sea: implications for diversity and ecosystem functioning. Dissertation, University of Bonn (Germany)
Naeher S, Geraga M, Papatheodorou G, Ferentinos G, Kaberi H, Schubert CJ (2012) Environmental variations in a semi-enclosed embayment (Amvrakikos Gulf, Greece)-Reconstructions based on benthic foraminifera abundance and lipid biomarker pattern. Biogeosciences 9:5081–5094. https://doi.org/10.5194/bg-9-5081-2012
Ohno Y, Iguchi A, Shinzato C, Inoue M, Suzuki A, Sakai K, Nakamura T (2017) An aposymbiotic primary coral polyp counteracts acidification by active pH regulation. Sci Rep 7:40324. https://doi.org/10.1038/srep40324
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. https://doi.org/10.1038/nature04095
Pettit LR, Hart MB, Medina-Sánchez AN, Smart CW, Rodolfo-Metalpa R, Hall-Spencer JM, Prol-Ledesma RM (2013) Benthic foraminifera show some resilience to ocean acidification in the northern Gulf of California, Mexico. Mar Pollut Bull 73:452–462. https://doi.org/10.1016/j.marpolbul.2013.02.011
Pettit LR, Smart CW, Hart MB, Milazzo M, Hall-Spencer JM (2015) Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2 gradient. Ecol Evol 5:1784–1793. https://doi.org/10.1002/ece3.1475
Polovodova I, Schönfeld J (2008) Foraminiferal test abnormalities in the western Baltic Sea. J Foraminifer Res 38:318–336. https://doi.org/10.2113/gsjfr.38.4.318
Prazeres M, Uthicke S, Pandolfi JM (2015) Ocean acidification induces biochemical and morphological changes in the calcification process of large benthic foraminifera. Proc R Soc B 282:20142782. https://doi.org/10.1098/rspb.2014.2782
Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134. https://doi.org/10.1130/G30210A.1
Ross BJ, Hallock P (2016) Dormancy in the foraminifera: A review. J Foraminifer Res 46:358–368. https://doi.org/10.2113/gsjfr.46.4.358
Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL et al (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371. https://doi.org/10.1126/science.1097403
Schmidt C, Kucera M, Uthicke S (2014) Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa. Coral Reefs 33:805–818. https://doi.org/10.1007/s00338-014-1151-4
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. https://doi.org/10.4319/lo.2006.51.3.1284
Schönfeld J (2018) Monitoring benthic foraminiferal dynamics at Bottsand coastal lagoon (western Baltic Sea). J Micropalaeontol 37:383–393. https://doi.org/10.5194/jm-37-383-2018
Schönfeld J, Alve E, Geslin E, Jorissen F, Korsun S, Spezzaferri S et al (2012) The FOBIMO (Foraminiferal BIo-MOnitoring) initiative - Towards a standardised protocol for soft-bottom benthic foraminiferal monitoring studies. Mar Micropaleontol 94–95:1–13. https://doi.org/10.1016/j.marmicro.2012.06.001
Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56:1200–1212. https://doi.org/10.4319/lo.2011.56.4.1200
Smith CW, Goldstein ST (2019) The effects of selected heavy metal elements (arsenic, cadmium, nickel, zinc) on experimentally grown foraminiferal assemblages from Sapelo Island, Georgia and Little Duck Key, Florida, USA. J Foraminifer Res 49:303–317. https://doi.org/10.2113/gsjfr.49.3.303
Tee MZ, Yong YS, Rodrigues KF, Yong WTL (2015) Growth rate analysis and protein identification of Kappaphycus alvarezii (Rhodophyta, Gigartinales) under pH induced stress culture. Aquac Rep 2:112–116. https://doi.org/10.1016/j.aqrep.2015.09.001
Toyofuku T, Matsuo MY, de Nooijer LJ, Nagai Y, Kawada S, Fujita K, Reichart GJ, Nomaki H, Tsuchiya M, Sakaguchi H, Kitazato H (2017) Proton pumping accompanies calcification in foraminifera. Nat Commun 8:14145. https://doi.org/10.1038/ncomms14145
Triantaphyllou MV, Baumann KH, Karatsolis BT, Dimiza MD, Psarra S, Skampa E, Patoucheas P, Vollmar NM, Koukousioura O, Katsigera A, Krasakopoulou E, Nomikou P (2018) Coccolithophore community response along a natural CO2 gradient off Methana (SW Saronikos Gulf, Greece, NE Mediterranean). PLoS ONE 13:e0200012. https://doi.org/10.1371/journal.pone.0200012
van Dijk I, Bernhard JM, de Nooijer LJ, Nehrke G, Wit JC, Reichart GJ (2017) Combined impacts of ocean acidification and dysoxia on survival and growth of four agglutinating foraminifera. J Foraminifer Res 47:294–303. https://doi.org/10.2113/gsjfr.47.3.294
Weinmann AE, Goldstein ST (2016) Changing structure of benthic foraminiferal communities: Implications from experimentally grown assemblages from coastal Georgia and Florida, USA. Mar Ecol 37:891–906. https://doi.org/10.1111/maec.12368
Weinmann AE, Goldstein ST (2017) Landward directed dispersal of benthic foraminiferal propagules at two shallow-water sites in the Doboy Sound area (Georgia, USA). J Foraminifer Res 47:325–336. https://doi.org/10.2113/gsjfr.47.4.325
Weinmann AE, Goldstein ST, Triantyphyllou MV, Langer MR (2019) Effects of sampling site, season, and substrate on foraminiferal assemblages grown from propagule banks from lagoon sediments of Corfu Island (Greece, Ionian Sea). PLoS ONE 14:e0219015. https://doi.org/10.1371/journal.pone.0219015
Wit JC, Davis MM, McCorkle DC, Bernhard JM (2016) A short-term survival experiment assessing impacts of ocean acidification and hypoxia on the benthic foraminifer Globobulimina turgida. J Foraminifer Res 46:25–33. https://doi.org/10.2113/gsjfr.46.1.25
Acknowledgements
The authors wish to thank Michael Kunert for sampling assistance as well as Nadine Blume, Olaf Dülfer and Karen Schmeling for laboratory assistance. Nadine Blume is also acknowledged for producing the SEM images. Further, the authors thank the editor Dr. Télesphore Sime-Ngando, as well as the 2 reviewers for their thoughtful comments and suggestions to improve the manuscript.
Funding
This study was funded by a grant from the Deutsche Forschungsgemeinschaft (DFG, 323009980).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared that no conflicts of interest exist.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Télesphore Sime-Ngando.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Weinmann, A.E., Goldstein, S.T., Triantaphyllou, M.V. et al. Community responses of intertidal foraminifera to pH variations: a culture experiment with propagules. Aquat Ecol 55, 309–325 (2021). https://doi.org/10.1007/s10452-021-09833-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-021-09833-w