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Volume 33 Issue 6
Dec 2022
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Alexander F. Humphreys, Sam J. Purkis, Chuyan Wan, Matthew Aldrich, Sarah Nichols, Jazmin Garza. A New Foraminiferal Bioindicator for Long-Term Heat Stress on Coral Reefs. Journal of Earth Science, 2022, 33(6): 1451-1459. doi: 10.1007/s12583-021-1543-7
Citation: Alexander F. Humphreys, Sam J. Purkis, Chuyan Wan, Matthew Aldrich, Sarah Nichols, Jazmin Garza. A New Foraminiferal Bioindicator for Long-Term Heat Stress on Coral Reefs. Journal of Earth Science, 2022, 33(6): 1451-1459. doi: 10.1007/s12583-021-1543-7

A New Foraminiferal Bioindicator for Long-Term Heat Stress on Coral Reefs

doi: 10.1007/s12583-021-1543-7
  • Received Date: 03 Aug 2021
  • Accepted Date: 08 Sep 2021
  • Issue Publish Date: 30 Dec 2022
  • Coral reefs are in terminal decline. For conservation to be effective, naturally depauperate reefs must be distinguished from those recently degraded by humans. Traditional reef monitoring is time consuming and lacks the longevity to make this distinction. Success in using foraminifera as bioindicators for reef health has hitherto levered their response to nutrients. Because ocean heat waves are the dominant driver of coral bleaching and death, there is compelling motivation to develop new foraminiferal bioindicators that inform on temperature stress over meaningful timescales. This study focuses on identifying which foraminifera respond systematically to the temperature stress that kills corals. Statistical models were used to compare endosymbiont-bearing foraminiferal families, collected along a heat-stress gradient spanning the Solomon Islands and New Caledonia, to live coral cover at the same sites. Results indicate that Amphisteginidae foraminifera and coral cover show a significant decline in abundance as heat stress increases along the transect sites. Furthermore, ocean productivity and salinity, both recognized environmental influences on foraminifera, are shown to be subordinate to temperature in their sway of this ecological patterning. These findings indicate the potential for using foraminifera to develop new indices capable of quantifying long-term thermal impacts on reefs.

     

  • Electronic Supplementary Materials: Supplementary mate-rials (Tables S1–S2) are available in the online version of this article at https://doi.org/10.1007/s12583-021-1543-7.
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  • Aronson, R., Precht, W., Toscano, M., et al., 2002. The 1998 Bleaching Event and Its Aftermath on a Coral Reef in Belize. Marine Biology, 141(3): 435–447. https://doi.org/10.1007/s00227-002-0842-5
    Barbosa, C. F., de Freitas Prazeres, M., Ferreira, B. P., et al., 2009. Foraminiferal Assemblage and Reef Check Census in Coral Reef Health Monitoring of East Brazilian Margin. Marine Micropaleontology, 73(1/2): 62–69. https://doi.org/10.1016/j.marmicro.2009.07.002
    Barbosa, C. F., Ferreira, B. P., Seoane, J. C. S., et al., 2012. Foraminifer-Based Coral Reef Health Assessment for Southwestern Atlantic Offshore Archipelagos, Brazil. The Journal of Foraminiferal Research, 42(2): 169–183. https://doi.org/10.2113/gsjfr.42.2.169
    Beccari, V., Spezzaferri, S., Stainbank, S., et al., 2020. Responses of Reef Bioindicators to Recent Temperature Anomalies in Distinct Areas of the North Ari and Rasdhoo Atolls (Maldives). Ecological Indicators, 112: 106128. https://doi.org/10.1016/j.ecolind.2020.106128
    Bellwood, D. R., Hughes, T. P., Folke, C., et al., 2004. Confronting the Coral Reef Crisis. Nature, 429(6994): 827–833. https://doi.org/10.1038/nature02691
    Borcard, D., Gillet, F., Legendre, P., 2011. Numerical Ecology with R. Springer, New York. https://doi.org/10.1007/978-1-4419-7976-6
    DeCarlo, T. M., Gajdzik, L., Ellis, J., et al., 2020. Nutrient-Supplying Ocean Currents Modulate Coral Bleaching Susceptibility. Science Advances, 6(34): eabc5493. https://doi.org/10.1126/sciadv.abc5493
    Fabricius, K. E., Cooper, T. F., Humphrey, C., et al., 2012. A Bioindicator System for Water Quality on Inshore Coral Reefs of the Great Barrier Reef. Marine Pollution Bulletin, 65(4/5/6/7/8/9): 320–332. https://doi.org/10.1016/j.marpolbul.2011.09.004
    Fajemila, O. T., Langer, M. R., Lipps, J. H., 2015. Spatial Patterns in the Distribution, Diversity and Abundance of Benthic Foraminifera around Moorea (Society Archipelago, French Polynesia). PLoS One, 10(12): e0145752. https://doi.org/10.1371/journal.pone.0145752
    Fujita, K., 2004. A Field Colonization Experiment on Small-Scale Distributions of Algal Symbiont-Bearing Larger Foraminifera on Reef Rubble. The Journal of Foraminiferal Research, 34(3): 169–179. https://doi.org/10.2113/34.3.169
    Gardner, T. A., Côté, I. M., Gill, J. A., et al., 2003. Long-Term Region-Wide Declines in Caribbean Corals. Science, 301(5635): 958–960. https://doi.org/10.1126/science.1086050
    Glynn, P. W., 1984. Widespread Coral Mortality and the 1982-83 El Niño Warming Event. Environmental Conservation, 11(2): 133–146. https://doi.org/10.1017/s0376892900013825
    Glynn, P. W., Wellington, G. M., Birkeland, C., 1979. Coral Reef Growth in the Galapagos: Limitation by Sea Urchins. Science, 203(4375): 47–49. https://doi.org/10.1126/science.203.4375.47
    Goreau, T. J. F., Hayes, R. L., 2021. Global Warming Triggers Coral Reef Bleaching Tipping Point. Ambio, 50(6): 1137–1140. https://doi.org/10.1007/s13280-021-01512-2
    Hallock, P., 2000. Symbiont-Bearing Foraminifera: Harbingers of Global Change? Micropaleontology, 46(1): 95–104
    Hallock, P., 2012. The FoRAM Index Revisited: Uses, Challenges, and Limitations. In: Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia. 9–13
    Hallock, P., Lidz, B. H., Cockey-Burkhard, E. M., et al., 2003. Foraminifera as Bioindicators in Coral Reef Assessment and Monitoring: The FoRAM Index. Environmental Monitoring and Assessment, 81(1/2/3): 221–238. https://doi.org/10.1023/a:1021337310386
    Hallock, P., Talge, H. K., 1995. Symbiont Loss ("Bleaching") in the Reef-Dwelling Benthic Foraminifer Amphistegina Gibbosa in the Florida Keys in 1991-92. Oceanographic Literature Review, 42(8): 977. https://digitalcommons.usf.edu/msc_facpub/977
    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-UFRJ, 29(1): 108–128. https://doi.org/10.11137/2006_1_108-128
    Humphreys, A. F., Halfar, J., Ingle, J. C., et al., 2018. Effect of Seawater Temperature, pH, and Nutrients on the Distribution and Character of Low Abundance Shallow Water Benthic Foraminifera in the Galápagos. PLoS One, 13(9): e0202746. https://doi.org/10.1371/journal.pone.0202746
    Humphreys, A. F., Halfar, J., Ingle, J. C., et al., 2019. Shallow-Water Benthic Foraminifera of the Galápagos Archipelago: Ecologically Sensitive Carbonate Producers in an Atypical Tropical Oceanographic Setting. Journal of Foraminiferal Research, 49(1): 48–65
    Humphreys, A. F., Halfar, J., Rivera, F., et al., 2016. Variable El Niño-Southern Oscillation Influence on Biofacies Dynamics of Eastern Pacific Shallow-Water Carbonate Systems. Geology, 44(7): 571–574. https://doi.org/10.1130/g37745.1
    Jackson, J. B. C., Kirby, M. X., Berger, W. H., et al., 2001. Historical Overfishing and the Recent Collapse of Coastal Ecosystems. Science, 293(5530): 629–637. https://doi.org/10.1126/science.1059199
    Kayanne, H., 2017. Validation of Degree Heating Weeks as a Coral Bleaching Index in the Northwestern Pacific. Coral Reefs, 36(1): 63–70. https://doi.org/10.1007/s00338-016-1524-y
    Kelmo, F., Hallock, P., 2013. Responses of Foraminiferal Assemblages to ENSO Climate Patterns on Bank Reefs of Northern Bahia, Brazil: A 17-Year Record. Ecological Indicators, 30: 148–157. https://doi.org/10.1016/j.ecolind.2013.02.009
    Kleypas, J. A., McManus, J. W., Menez, L. A., 1999. Environmental Limits to Coral Reef Development: Where do We Draw the Line? American Zoologist, 39(1): 146–159. https://doi.org/10.1093/icb/39.1.146
    Kumagai, N. H., Yamano, H., Sango-Map-Project, C., 2018. High-Resolution Modeling of Thermal Thresholds and Environmental Influences on Coral Bleaching for Local and Regional Reef Management. PeerJ, 6: e4382. https://doi.org/10.7717/peerj.4382
    Legendre, P., Gallagher, E. D., 2001. Ecologically Meaningful Transformations for Ordination of Species Data. Oecologia, 129(2): 271–280. https://doi.org/10.1007/s004420100716
    Legendre, P., Legendre, L. F., 1998. Numerical Ecology, 2nd Edition. Elsevier
    Liu, G., Strong, A. E., Skirving, W., 2003. Remote Sensing of Sea Surface Temperatures during 2002 Barrier Reef Coral Bleaching. Eos, Transactions American Geophysical Union, 84(15): 137–141. https://doi.org/10.1029/2003eo150001
    Martinez-Colón, M., Hallock, P., Green-Ruiz, C., 2009. Strategies for Using Shallow-Water Benthic Foraminifers as Bioindicators of Potentially Toxic Elements: A Review. The Journal of Foraminiferal Research, 39(4): 278–299. https://doi.org/10.2113/gsjfr.39.4.278
    McClenachan, L., O'Connor, G., Neal, B. P., et al., 2017. Ghost Reefs: Nautical Charts Document Large Spatial Scale of Coral Reef Loss over 240 Years. Science Advances, 3(9): e1603155. https://doi.org/10.1126/sciadv.1603155
    Narayan, Y. R., Pandolfi, J. M., 2010. Benthic Foraminiferal Assemblages from Moreton Bay, South-East Queensland, Australia: Applications in Monitoring Water and Substrate Quality in Subtropical Estuarine Environments. Marine Pollution Bulletin, 60(11): 2062–2078. https://doi.org/10.1016/j.marpolbul.2010.07.012
    Narayan, Y. R., Lybolt, M., Zhao, J. X., et al., 2015. Holocene Benthic Foraminiferal Assemblages Indicate Long-Term Marginality of Reef Habitats from Moreton Bay, Australia. Palaeogeography, Palaeoclimatology, Palaeoecology, 420: 49–64. https://doi.org/10.1016/j.palaeo.2014.12.010
    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
    Pandolfi, J. M., Bradbury, R. H., Sala, E., et al., 2003. Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems. Science, 301(5635): 955–958. https://doi.org/10.1126/science.1085706
    Perry, C. T., 2003. Coral Reefs in a High-Latitude, Siliciclastic Barrier Island Setting: Reef Framework and Sediment Production at Inhaca Island, Southern Mozambique. Coral Reefs, 22(4): 485–497. https://doi.org/10.1007/s00338-003-0339-9
    Pisapia, C., Kateb, A. E., Hallock, P., et al., 2017. Assessing Coral Reef Health in the North Ari Atoll (Maldives) Using the FoRAM Index. Marine Micropaleontology, 133: 50–57. https://doi.org/10.1016/j.marmicro. 2017.06.001 doi: 10.1016/j.marmicro.2017.06.001
    Prazeres, M., 2018. Bleaching-Associated Changes in the Microbiome of Large Benthic Foraminifera of the Great Barrier Reef, Australia. Frontiers in Microbiology, 9: 2404. https://doi.org/10.3389/fmicb. 2018.02404 doi: 10.3389/fmicb.2018.02404
    Prazeres, M., Roberts, T. E., Pandolfi, J. M., 2017a. Variation in Sensitivity of Large Benthic Foraminifera to the Combined Effects of Ocean Warming and Local Impacts. Scientific Reports, 7: 45227. https://doi.org/10.1038/srep45227
    Prazeres, M., Ainsworth, T., Roberts, T. E., et al., 2017b. Symbiosis and Microbiome Flexibility in Calcifying Benthic Foraminifera of the Great Barrier Reef. Microbiome, 5(1): 38. https://doi.org/10.1186/s40168-017-0257-7
    Prazeres, M., Martínez-Colón, M., Hallock, P., 2020. Foraminifera as Bioindicators of Water Quality: The FoRAM Index Revisited. Environmental Pollution, 257: 113612. https://doi.org/10.1016/j.envpol.2019.113612
    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. Scientific Reports, 6: 21936. https://doi.org/10.1038/srep21936
    Purkis, S. J., Riegl, B., 2005. Spatial and Temporal Dynamics of Arabian Gulf Coral Assemblages Quantified from Remote-Sensing and in situ Monitoring Data. Marine Ecology Progress Series, 287: 99–113. https://doi.org/10.3354/meps287099
    Purkis, S. J., Gleason, A. C. R., Purkis, C. R., et al., 2019. High-Resolution Habitat and Bathymetry Maps for 65, 000 sq. km of Earth's Remotest Coral Reefs. Coral Reefs, 38(3): 467–488. https://doi.org/10.1007/s00338-019-01802-y
    Purkis, S. J., Renegar, D. A., Riegl, B. M., 2011. The Most Temperature-Adapted Corals have an Achilles' Heel. Marine Pollution Bulletin, 62(2): 246–250. https://doi.org/10.1016/j.marpolbul.2010.11.005
    Renema, W., 2008. Habitat Selective Factors Influencing the Distribution of Larger Benthic Foraminiferal Assemblages over the Kepulauan Seribu. Marine Micropaleontology, 68(3/4): 286–298. https://doi.org/10.1016/j.marmicro.2008.06.002
    Renema, W., 2010. Is Increased Calcarinid (Foraminifera) Abundance Indicating a Larger Role for Macro-Algae in Indonesian Plio-Pleistocene Coral Reefs? Coral Reefs, 29(1): 165–173. https://doi.org/10.1007/s00338-009-0568-7
    Reymond, C. E., Uthicke, S., Pandolfi, J. M., 2012. Tropical Foraminifera as Indicators of Water Quality and Temperature. In: Proceedings of the 12th International Coral Reef Symposium, July 9–13, 2012, Cairns, Australia
    Riegl, B., 2003. Climate Change and Coral Reefs: Different Effects in Two High-Latitude Areas (Arabian Gulf, South Africa). Coral Reefs, 22(4): 433–446. https://doi.org/10.1007/s00338-003-0335-0
    Riegl, B., Piller, W. E., 2000. Biostromal Coral Facies: A Miocene Example from the Leitha Limestone (Austria) and Its Actualistic Interpretation. PALAIOS, 15(5): 399–413. https://doi.org/10.2307/3515512
    Riegl, B., Piller, W. E., 2003. Possible Refugia for Reefs in Times of Environmental Stress. International Journal of Earth Sciences, 92(4): 520–531. https://doi.org/10.1007/s00531-003-0328-9
    Riegl, B., Glynn, P. W., Wieters, E., et al., 2015. Water Column Productivity and Temperature Predict Coral Reef Regeneration across the Indo-Pacific. Scientific Reports, 5: 8273. https://doi.org/10.1038/srep08273
    Riegl, B. M., Purkis, S. J., Al-Cibahy, A. S., et al., 2012. Coral Bleaching and Mortality Thresholds in the SE Gulf: Highest in the World. In: Riegl, B., Purkis, S., eds., Coral Reefs of the Gulf. Coral Reefs of the World, vol. 3. Springer, Dordrecht. 95–105. https://doi.org/10.1007/978-94-007-3008-3_6
    Schafer, C. T., 2000. Monitoring Nearshore Marine Environments Using Benthic Foraminifera: Some Protocols and Pitfalls. Micropaleontology, 46: 161–169
    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
    Schönfeld, J., Alve, E., Geslin, E., et al., 2012. The FOBIMO (Foraminiferal Bio-Monitoring) Initiative—Towards a Standardised Protocol for Soft-Bottom Benthic Foraminiferal Monitoring Studies. Marine Micropaleontology, 94/95: 1–13. https://doi.org/10.1016/j.marmicro.2012.06.001
    Schueth, J. D., Frank, T. D., 2008. Reef Foraminifera as Bioindicators of Coral Reef Health: Low Isles Reef, Northern Great Barrier Reef, Australia. The Journal of Foraminiferal Research, 38(1): 11–22. https://doi.org/10.2113/gsjfr.38.1.11
    Spezzaferri, S., El Kateb, A., Pisapia, C., et al., 2018. In situ Observations of Foraminiferal Bleaching in the Maldives, Indian Ocean. Journal of Foraminiferal Research, 48(1): 75–84.https://doi.org/10.2113/gsjfr. 48.1.75 doi: 10.2113/gsjfr.48.1.75
    Sreenivasulu, G., Praseetha, B. S., Daud, N. R., et al., 2019. Benthic Foraminifera as Potential Ecological Proxies for Environmental Monitoring in Coastal Regions: A Study on the Beypore Estuary, Southwest Coast of India. Marine Pollution Bulletin, 138: 341–351. https://doi.org/10.1016/j.marpolbul.2018.11.058
    Stainbank, S., Spezzaferri, S., Beccari, V., et al., 2020. Photic Stress on Coral Reefs in the Maldives: The Amphistegina Bleaching Index. Ecological Indicators, 113: 106257. https://doi.org/10.1016/j.ecolind.2020.106257
    Stuhr, M., Reymond, C. E., Rieder, V., et al., 2017. Reef Calcifiers are Adapted to Episodic Heat Stress but Vulnerable to Sustained Warming. PLoS One, 12(7): e0179753. https://doi.org/10.1371/journal.pone.0179753
    Talge, H. K., Hallock, P., 2003. Ultrastructural Responses in Field-Bleached and Experimentally Stressed Amphistegina Gibbosa (Class Foramini-fera). Journal of Eukaryotic Microbiology, 50(5): 324–333. https://doi.org/10.1111/j.1550-7408.2003.tb00143.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., Nobes, K., 2008. Benthic Foraminifera as Ecological Indicators for Water Quality on the Great Barrier Reef. Estuarine, Coastal and Shelf Science, 78(4): 763–773. https://doi.org/10.1016/j.ecss.2008.02.014
    Uthicke, S., Patel, F., Ditchburn, R., 2012. Elevated Land Runoff after European Settlement Perturbs Persistent Foraminiferal Assemblages on the Great Barrier Reef. Ecology, 93(1): 111–121. https://doi.org/10.1890/11-0665.1
    van Hooidonk, R., Huber, M., 2009. Quantifying the Quality of Coral Bleaching Predictions. Coral Reefs, 28(3): 579–587. https://doi.org/10.1007/s00338-009-0502-z
    Webster, N. S., Negri, A. P., Botté, E. S., et al., 2016. Host-Associated Coral Reef Microbes Respond to the Cumulative Pressures of Ocean Warming and Ocean Acidification. Scientific Reports, 6: 19324. https://doi.org/10.1038/srep19324
    Webster, N. S., Negri, A. P., Flores, F., et al., 2013. Near-Future Ocean Acidification Causes Differences in Microbial Associations within Diverse Coral Reef Taxa. Environmental Microbiology Reports, 5(2): 243–251. https://doi.org/10.1111/1758-2229.12006
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