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Volume 33 Issue 6
Dec 2022
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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
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

Stable Adult Growth but Reduced Asexual Fecundity in Marginopora vertebralis, under Global Climate Change Scenarios

doi: 10.1007/s12583-022-1657-6
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  • Corresponding author: Claire E. Reymond, claire.reymond@gmail.com
  • Received Date: 11 Aug 2021
  • Accepted Date: 16 Mar 2022
  • Issue Publish Date: 30 Dec 2022
  • 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 Marginopora vertebralis has a low threshold compared to several diatom-bearing and low-magnesium calcite species. In this multi-year mesocosm experiment, we tested three RPC 8.5 climate change scenarios (i) present day, (ii) the year 2050, and (iii) 2100. To enable a realistic epiphytic association, these experiments were uniquely conducted using natural carbonate substrate, living calcifying alga, and seagrass. In contrast to previous studies, we detected no reduction in surface-area growth under future climate conditions compared with present day conditions. In terms of calcification, M. vertebralis' epiphytic association to primary producers (i.e., calcifying algae and seagrasses) potentially ameliorates the effects of OA by buffering against declines in boundary layer pH during periods of photosynthesis (i.e., CO2 removal). Importantly for population maintenance, we observed a strong reduction in asexual fecundity under the 2100 scenario. We propose the additional energy needed to maintain growth might be one reason for drastically reduced asexual reproduction. An alternative explanation could be that the 2 ℃ temperature increase interfered with the environmental synchronization that triggered asexual multiple fission. We conclude that the low levels of reproduction will reduce populations in a high CO2 environment and reduce a valuable source of CaCO3 sediment production.

     

  • Electronic Supplementary Materials: Supplementary mate-rials (Tables S1 and S2) are available in the online version of this article at https://doi.org/10.1007/s12583-022-1657-6.
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  • 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
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