Citation: | Claire E. Reymond, Frances Patel, Sven Uthicke. Stable Adult Growth but Reduced Asexual Fecundity in Marginopora vertebralis, under Global Climate Change Scenarios. Journal of Earth Science, 2022, 33(6): 1400-1410. doi: 10.1007/s12583-022-1657-6 |
Large benthic foraminifera are an integral component of shallow-water tropical habitats and like many marine calcifiers, are susceptible to ocean acidification (OA) and ocean warming (OW). In particular, the prolific Symbiodiniaceae-bearing and high-magnesium calcite
Bates, D., Mächler, M., Bolker, B., et al., 2015. Fitting Linear Mixed-Effects Models Using Lme4. Journal of Statistical Software, 67(1): 1–48. https://doi.org/10.18637/jss.v067.i01 |
Beavington-Penney, S. J., Racey, A., 2004. Ecology of Extant Nummulitids and other Larger Benthic Foraminifera: Applications in Palaeoenviron-mental Analysis. Earth-Science Reviews, 67(3/4): 219–265. https://doi.org/10.1016/j.earscirev.2004.02.005 |
Bernhard, J. M., Blanks, J. K., Hintz C. J., et al., 2004. Use of the Fluorescent Calcite Marker Calcein to Label Foraminiferal Tests. Journal of Foraminiferal Research, 34(2): 96–101. https://doi.org/10.2113/0340096 |
Botté, E. S., Luter, H. M., Marangon, E., et al., 2020. Simulated Future Conditions of Ocean Warming and Acidification Disrupt the Microbiome of the Calcifying Foraminifera Marginopora vertebralis across Life Stages. Environmental Microbiology Reports, 12(6): 693–701. https://doi.org/10.1111/1758-2229.12900 |
Brandano, M., Cuffaro, M., Gaglianone, G., et al., 2016. Evaluating the Role of Seagrass in Cenozoic CO2 Variations. Frontiers in Environmental Science, 4: 72. https://doi.org/10.3389/fenvs.2016.00072 |
Briguglio, A., Hohenegger, J., 2014. Growth Oscillation in Larger Forami-nifera. Paleobiology, 40(3): 494–509. https://doi.org/10.1666/13051 |
Chave, K. E., 1954. Aspects of the Biogeochemistry of Magnesium 1. Calcareous Marine Organisms. The Journal of Geology, 62(3): 266–283. https://doi.org/10.1086/626162 |
Doo, S. S., Fujita, K., Byrne, M., et al., 2014. Fate of Calcifying Tropical Symbiont-Bearing Large Benthic Foraminifera: Living Sands in a Changing Ocean. Biological Bulletin, 226(3): 169–186. https://doi.org/10.1086/bblv226n3p169 |
Doo, S. S., Hamylton, S., Finfer, J., et al., 2017. Spatial and Temporal Variation in Reef-Scale Carbonate Storage of Large Benthic Foraminifera: A Case Study on one Tree Reef. Coral Reefs, 36(1): 293–303. https://doi.org/10.1007/s00338-016-1506-0 |
Doo, S. S., Leplastrier, A., Graba-Landry, A., et al., 2020. Amelioration of Ocean Acidification and Warming Effects through Physiological Buffering of a Macroalgae. Ecology and Evolution, 10(15): 8465–8475. https://doi.org/10.1002/ece3.6552 |
Fabricius, K. E., Langdon, C., Uthicke, S., et al., 2011. Losers and Winners in Coral Reefs Acclimatized to Elevated Carbon Dioxide Concentrations. Nature Climate Change, 1(3): 165–169. https://doi.org/10.1038/nclimate1122 |
Fujita, K., Okai, T., Hosono, T., 2014. Oxygen Metabolic Responses of Three Species of Large Benthic Foraminifers with Algal Symbionts to Temperature Stress. PLoS One, 9(3): e90304. https://doi.org/10.1371/journal.pone.0090304 |
Fujita, K., Osawa, Y., Kayanne, H., et al., 2009. Distribution and Sediment Production of Large Benthic Foraminifers on Reef Flats of the Majuro Atoll, Marshall Islands. Coral Reefs, 28(1): 29–45. https://doi.org/10.1007/s00338-008-0441-0 |
Fujita, K., Nishi, H., Saito, T., 2000. Population Dynamics of Marginopora Kudakajimensis Gudmundsson (Foraminifera: Soritidae) in the Ryukyu Islands, the Subtropical Northwest Pacific. Marine Micropaleontology, 38(3/4): 267–284. https://doi.org/10.1016/s0377-8398(99)00042-0 |
Galdies, C., Bellerby, R., Canu, D., et al., 2020. European Policies and Legislation Targeting Ocean Acidification in European Waters—Current State. Marine Policy, 118: 103947. https://doi.org/10.1016/j.marpol.2020.103947 |
Garcia-Cuetos, L., Pochon, X., Pawlowski, J., 2005. Molecular Evidence for Host-Symbiont Specificity in Soritid Foraminifera. Protist, 156(4): 399–412. https://doi.org/10.1016/j.protis.2005.08.003 |
Goldstein, S. T., 1999. Foraminifera: A Biological Overview. In: Sen Gupta, B. K., ed., Modern Foraminifera. Springer, Dordrecht. 37–55 |
Glas, M. S., Langer, G., Keul, N., 2012. Calcification Acidifies the Microenvironment of a Benthic Foraminifer (Ammonia sp.). Journal of Experimental Marine Biology and Ecology, 424/425: 53–58. https://doi.org/10.1016/j.jembe.2012.05.006 |
Hallock, P., Williams, D. E., Fisher, E. M., et al., 2006. Bleaching in Foraminifera with Algal Symbionts: Implications for Reef Monitoring and Risk Asessment. Anuário do Instituto de Geociências, 29(1): 108–128. https://doi.org/10.11137/2006_1_108-128 |
Hayward, B. W., Le Coze, F., Vachard, D., et al., 2021. World Foraminifera Database. [2021-8-1]. http://www.marinespecies.org/foraminifera |
Hohenegger, J., Briguglio, A., 2014. Methods for Estimating Individual Growth of Foraminifera Based on Chamber Volumes. In: Kitazato, H., Bernhard, J. M., eds., Approaches to Study Living Foraminifera: Collection, Maintenance and Experimentation. Springer, Japan. 29–54 |
Hohenegger, J., Kinoshita, S., Briguglio, A., et al., 2019. Lunar Cycles and Rainy Seasons Drive Growth and Reproduction in Nummulitid Foraminifera, Important Producers of Carbonate Buildups. Scientific Reports, 9: 8286. https://doi.org/10.1038/s41598-019-44646-w |
Hohn, S., Reymond, C. E., 2019. Coral Calcification, Mucus, and the Origin of Skeletal Organic Molecules. Coral Reefs, 38(5): 973–984. https://doi.org/10.1007/s00338-019-01826-4 |
Hosono, T., Lopati, P., Makolo, F., et al., 2014. Mass Culturing of Living Sands (Baculogypsina Sphaerulata) to Protect Island Coasts Against Sea-Level Rise. Journal of Sea Research, 90: 121–126. https://doi.org/10.1016/j.seares.2014.03.007 |
Hothorn, T., Bretz, F., Westfall, P., 2008. Simultaneous Inference in General Parametric Models. Biometrical Journal, 50(3): 346–363. https://doi.org/10.1002/bimj.200810425 |
Kinoshita, S., Eder, W., Wöger, J., et al., 2017. Growth, Chamber Building Rate and Reproduction Time of Palaeonummulites venosus (Foraminifera) under Natural Conditions. Coral Reefs (Online), 36(4): 1097–1109. https://doi.org/10.1007/s00338-017-1601-x |
Kirkwood, T. B., Rose, M. R., 1991. Evolution of Senescence: Late Survival Sacrificed for Reproduction. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 332(1262): 15–24. https://doi.org/10.1098/rstb.1991.0028 |
Langer, M. R., Silk, M. T., Lipps, J. H., 1997. Global Ocean Carbonate and Carbon Dioxide Production; The Role of Reef Foraminifera. Journal of Foraminiferal Research, 27(4): 271–277. https://doi.org/10.2113/gsjfr.27.4.271 |
Lee, J. J., Hallock, P., 1987. Algal Symbiosis as the Driving Force in the Evolution of Larger Foraminifera. Annals of the New York Academy of Sciences, 503(1): 330–347. https://doi.org/10.1111/j.1749-6632.1987.tb40619.x |
Lee, J. J., Cevasco, M., Morales, J., et al., 2016. Variation among the Marginopora vertebralis Collected from the Great Barrier Reef, Australia. Journal of Foraminiferal Research, 46(2): 201–219. https://doi.org/10.2113/gsjfr.46.2.201 |
Mateu-Vicens, G., Khokhlova, A., Sebastian-Pastor, T., 2014. Epiphytic Foraminiferal Indices as Bioindicators in Mediterranean Seagrass Meadows. Journal of Foraminiferal Research, 44(3): 325–339. https://doi.org/10.2113/gsjfr.44.3.325 |
Meinshausen, M., Smith, S. J., Calvin, K., et al., 2011. The RCP Greenhouse Gas Concentrations and Their Extensions from 1765 to 2300. Climatic Change, 109(1/2): 213–241. https://doi.org/10.1007/s10584-011-0156-z |
Mirzaghaderi, G., Hörandl, E., 2016. The Evolution of Meiotic Sex and Its Alternatives. Proceedings of the Royal Society B: Biological Sciences, 283(1838): 20161221. https://doi.org/10.1098/rspb.2016.1221 |
Momigliano, P., Uthicke, S., 2013. Symbiosis in a Giant Protist (Marginopora vertebralis, Soritinae): Flexibility in Symbiotic Partnerships along a Natural Temperature Gradient. Marine Ecology Progress Series, 491: 33–46. https://doi.org/10.3354/meps10465 |
Naidu, R., Hallock, P., Erez, J., et al., 2017. Response of Marginopora vertebralis (Foraminifera) from Laucala Bay, Fiji, to Changing Ocean pH. In: Filho, W. L., ed., Climate Change Adaptation in Pacific Countries. Springer International Publishing, Cham. 137–150. https://doi.org/10.1007/978-3-319-50094-2_8 |
Narayan, G. R., Reymond, C. E., Stuhr, M., et al., 2022. Response of Large Benthic Foraminifera to Climate and Local Changes: Implications for Future Carbonate Production. Sedimentology, 69(1): 121–161. https://doi.org/10.1111/sed.12858 |
Nilsson, J. Å., Svensson, E., 1996. The Cost of Reproduction: A New Link between Current Reproductive Effort and Future Reproductive Success. Proceedings of the Royal Society of London Series B: Biological Sciences, 263(1371): 711–714. https://doi.org/10.1098/rspb.1996.0106 |
Pawlowski, J., Holzmann, M., 2008. Diversity and Geographic Distribution of Benthic Foraminifera: A Molecular Perspective. Biodiversity and Conser-vation, 17(2): 317–328. https://doi.org/10.1007/s10531-007-9253-8 |
Prazeres, M., Uthicke, S., Pandolfi, J. M., 2015. Ocean Acidification Induces Biochemical and Morphological Changes in the Calcification Process of Large Benthic Foraminifera. Proceedings of the Royal Society B: Biological Sciences, 282: 20142782. https://doi.org/10.1098/rspb.2014.2782 |
R Core Team, 2020. R: A Language and Environment for Statistical Computing (Vienna, Austria). R Foundation for Statistical Computing |
Renema, W., 2018. Morphological Diversity in the Foraminiferal Genus Marginopora. PLoS One, 13(12): e0208158. https://doi.org/10.1371/journal.pone.0208158 |
Reymond, C. E., Hohn, S., 2021. An Experimental Approach to Assessing the Roles of Magnesium, Calcium, and Carbonate Ratios in Marine Carbonates. Oceans, 2(1): 193–214. https://doi.org/10.3390/oceans2010012 |
Reymond, C. E., Uthicke, S., Pandolfi, J. M., 2012. Increased Temperatures and Eutrophication Inhibit Growth of Marginopora vertebralis. In: Yellowlees, D., Hughes, T. P., eds., Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia |
Reymond, C. E., Lloyd, A., Kline, D. I., et al., 2013. Decline in Growth of Foraminifer Marginopora rossi under Eutrophication and Ocean Acidification Scenarios. Global Change Biology, 19(1): 291–302. https://doi.org/10.1111/gcb.12035 |
Reymond, C. E., Uthicke, S., Pandolfi, J. M., 2011. Inhibited Growth in the Photosymbiont-Bearing Foraminifer Marginopora vertebralis from the Nearshore Great Barrier Reef, Australia. Marine Ecology Progress Series, 435: 97–109. https://doi.org/10.3354/meps09172 |
Ross, C. A., 1972. Biology and Ecology of Marginopora vertebralis (Foraminiferida), Great Barrier Reef. Journal of Protozoology, 19(1): 181–192. https://doi.org/10.1111/j.1550-7408.1972.tb03433.x |
Schmidt, C., Heinz, P., Kucera, M., et al., 2011. Temperature-Induced Stress Leads to Bleaching in Larger Benthic Foraminifera Hosting Endosymbiotic Diatoms. Limnology and Oceanography, 56(5): 1587–1602. https://doi.org/10.4319/lo.2011.56.5.1587 |
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(3): 805–818. https://doi.org/10.1007/s00338-014-1151-4 |
Shaw, E. C., McNeil, B. I., 2014. Seasonal Variability in Carbonate Chemistry and Air-Sea CO2 Fluxes in the Southern Great Barrier Reef. Marine Chemistry, 158: 49–58. https://doi.org/10.1016/j.marchem.2013.11.007 |
Sinutok, S., Hill, R., Doblin, M. A., et al., 2011. Warmer more Acidic Conditions Cause Decreased Productivity and Calcification in Subtrop-ical Coral Reef Sediment-Dwelling Calcifiers. Limnology and Oceano-graphy, 56(4): 1200–1212. https://doi.org/10.4319/lo.2011.56.4.1200 |
Sinutok, S., Hill, R., Kühl, M., et al., 2014. Ocean Acidification and Warming Alter Photosynthesis and Calcification of the Symbiont-Bearing Foraminifera Marginopora vertebralis. Marine Biology, 161(9): 2143–2154. https://doi.org/10.1007/s00227-014-2494-7 |
Stuhr, M., Cameron, L. P., Blank-Landeshammer, B., et al., 2021. Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios. Oceans, 2(2): 281–314. https://doi.org/10.3390/oceans2020017 |
Talge, H. K., Hallock, P., 2003. Ultrastructural Responses in Field-Bleached and Experimentally Stressed Amphistegina gibbosa (Class Foraminifera). Journal of Eukaryotic Microbiology, 50(5): 324–333. https://doi.org/10.1111/j.1550-7408.2003.tb00143.x |
ter Kuile, B., Erez, J., 1984. In situ Growth Rate Experiments on the Symbiont-Bearing Foraminifera Amphistegina lobifera and Amphisorus hemprichii. Journal of Foraminiferal Research, 14(4): 262–276. https://doi.org/10.2113/gsjfr.14.4.262 |
Uthicke, S., Patel, F., Karelitz, S., et al., 2020. Key Biological Responses over Two Generations of the Sea Urchin Echinometra sp. A under Future Ocean Conditions. Marine Ecology Progress Series, 637: 87–101. https://doi.org/10.3354/meps13236 |
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. Global Change Biology, 18(9): 2781–2791. https://doi.org/10.1111/j.1365-2486.2012.02715.x |
Uthicke, S., Momigliano, P., Fabricius, K. E., 2013. High Risk of Extinction of Benthic Foraminifera in this Century due to Ocean Acidification. Scientific Reports, 3: 1769. https://doi.org/10.1038/srep01769 |
Uthicke, S., Vogel, N., Doyle, J., et al., 2012. Interactive Effects of Climate Change and Eutrophication on the Dinoflagellate-Bearing Benthic Foraminifera in this Century Marginopora vertebralis. Coral Reefs, 31(2): 401–414. https://doi.org/10.1007/s00338-011-0851-2 |
van Dam, J. W. V., Negri, A. P., Mueller, J. F., et al., 2012. Additive Pressures of Elevated Sea Surface Temperatures and Herbicides on Symbiont-Bearing Foraminifera. PLoS One, 7(3): e33900. https://doi.org/10.1371/journal.pone.0033900 |
Vogel, N., Uthicke, S., 2012. Calcification and Photobiology in Symbiont-Bearing Benthic Foraminifera and Responses to a High CO2 Environment. Journal of Experimental Marine Biology and Ecology, 424/425: 15–24. https://doi.org/10.1016/j.jembe.2012.05.008 |
Weinkauf, M. F. G., Siccha, M., Weiner, A. K. M., 2020. Reproduction of a Marine Planktonic Protist: Individual Success versus Population Survival. bioRxiv. https://doi.org/10.1101/2020.11.04.368100 |