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Response of subtropical submarine-cave ecosystem to Holocene cave development and Asian monsoon variability

Published online by Cambridge University Press:  05 April 2017

Wing-Tung Ruby Chiu
Affiliation:
School of Biological Sciences, Swire Institute of Marine Science, University of Hong Kong, Kadoorie Biological Sciences Building, Pokfulam Road, Hong Kong SAR, China. E-mail: rubychiu@ymail.com, moriakiyasuhara@gmail.com, hokuto.iwatani@gmail.com
Moriaki Yasuhara
Affiliation:
School of Biological Sciences, Swire Institute of Marine Science, University of Hong Kong, Kadoorie Biological Sciences Building, Pokfulam Road, Hong Kong SAR, China. E-mail: rubychiu@ymail.com, moriakiyasuhara@gmail.com, hokuto.iwatani@gmail.com
Hokuto Iwatani
Affiliation:
School of Biological Sciences, Swire Institute of Marine Science, University of Hong Kong, Kadoorie Biological Sciences Building, Pokfulam Road, Hong Kong SAR, China. E-mail: rubychiu@ymail.com, moriakiyasuhara@gmail.com, hokuto.iwatani@gmail.com
Akihisa Kitamura
Affiliation:
Institute of Geosciences, Shizuoka University, Shizuoka, 422-8529, Japan
Kazuhiko Fujita
Affiliation:
Department of Physics and Earth Sciences, Faculty of Science and Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, 903-0213, Japan

Abstract

A submarine cave is a unique environment that is dark, food limited, semi-isolated from the outside, and sheltered from wave action. However, our knowledge of the long-term change in submarine-cave ecosystems remains limited. We document here the community-scale responses toward long-term change in a submarine cave, Daidokutsu in Okinawa in southern Japan. Using both metazoans (ostracods and bivalves) and protozoans (larger benthic foraminiferans) in two sediment cores obtained from the cave, we reconstruct the faunal and diversity changes of the past 7 Kyr. All taxonomic groups showed long-term, gradual linear change of faunal composition from predominantly open-water taxa to predominantly cave taxa, and ostracods showed short-term variability of species diversity. The long-term faunal trend probably reflects gradual isolation of the cave ecosystem due to coral reef development (i.e., development of the cave ceiling) during periods of the Holocene transgression and subsequent sea-level highstand. The short-term diversity changes show substantial similarity to centennial- to millennial-scale Holocene Asian monsoon variability. Ostracod species diversity peaks tend to correspond with periods of strong East Asian winter monsoons. The results indicate that limestone submarine-cave ecosystems, an important cryptic habitat, developed gradually during the Holocene and may be sensitive to rapid climate changes.

Type
Articles
Copyright
Copyright © 2017 The Paleontological Society. All rights reserved 

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References

Literature Cited

Chiu, W.-T. R., Yasuhara, M., Iwatani, H., Kitamura, A., and Fujita, K.. 2016. An enigmatic Holocene podocopid ostracod from a submarine cave, Okinawa, Japan: “living fossil” or adaptive morphotype. Journal of Systematic Palaeontology 14:643652.Google Scholar
Garrett, P., Smith, D. L., Wilson, A. O., and Patriquin, D.. 1971. Physiography, ecology, and sediments of two Bermuda patch reefs. Journal of Geology 79:647668.Google Scholar
Ginsburg, R. N. 1983. Geological and biological roles of cavities in coral reefs. Pp. 148153 in D. J. Barnes, ed. Perspectives on coral reefs. Australian Institute of Marine Science, Queensland.Google Scholar
Hayami, I., and Kase, T.. 1992. A new cryptic species of Pycnodonte from Ryukyu Islands: a living fossil oyster. Transactions and Proceedings of the Palaeontological Society of Japan, new series 165:10701089.Google Scholar
Hou, Y., and Gou, Y.. 2007. Fossil Ostracoda of China, Vol. 2: Cytheracea and Cytherellidae. Beijing: Science Publishing House. [In Chinese.]Google Scholar
Jackson, J. B. C., Goreau, T. F., and Hartman, W. D.. 1971. Recent brachiopod-coralline sponge communities and their paleoecological significance. Science 173:623625.Google Scholar
Kano, Y., and Kase, T.. 2008. Diversity and distributions of the submarine-cave Neritiliidae in the Indo-Pacific (Gastropoda: Neritimorpha). Organisms Diversity and Evolution 8:2243.Google Scholar
Kase, T., and Hayami, I.. 1992. Unique submarine cave mollusc fauna: composition, origin and adaptation. Journal of Molluscan Studies 58:446449.Google Scholar
Kidwell, S. M. 2015. Biology in the Anthropocene: challenges and insights from young fossil records. Proceedings of the National Academy of Sciences USA 112:4922–4929.Google Scholar
Kitamura, A., Hiramoto, M., Kase, T., Yamamoto, N., Amemiya, M., and Ohashi, S.. 2007a. Changes in cavernicolous bivalve assemblages and environments within a submarine cave in the Okinawa Islands during the last 5,000 years. Paleontological Research 11:163182.Google Scholar
Kitamura, A., Kobayashi, K., Tamaki, C., Yamamoto, N., Irino, T., Miyairi, Y., and Yokoyama, Y.. 2013. Evidence of recent warming in the Okinawa region, subtropical northwestern Pacific, from an oxygen isotope record of a cave-dwelling marine micro-bivalve. Paleontological Research 17:5868.Google Scholar
Kitamura, A., Yamamoto, N., Kase, T., Ohashi, S.-i., Hiramoto, M., Fukusawa, H., Watanabe, T., Irino, T., Kojitani, H., Shimamura, M., and Kawakami, I.. 2007b. Potential of submarine-cave sediments and oxygen isotope composition of cavernicolous micro-bivalve as a late Holocene paleoenvironmental record. Global and Planetary Change 55:301316.Google Scholar
Logan, A., Mathers, S. M., and Thomas, M. L. H.. 1984. Sessile invertebrate coelobite communities from reefs of Bermuda: species composition and distribution. Coral Reefs 2:205213.Google Scholar
Maddocks, R. F. 1969. Recent ostracodes of the family Pontocyprididae chiefly from the Indian Ocean. Smithsonian Contributions to Zoology 7:156.Google Scholar
Maddocks, R. F., and Iliffe, T. M.. 1986. Podocopid ostracoda of Bermudian caves. Stygologia 2:2676.Google Scholar
Moffitt, S. E., Hill, T. M., Roopnarine, P. D., and Kennett, J. P.. 2015. Response of seafloor ecosystems to abrupt global climate change. Proceedings of the National Academy of Sciences USA 112:4684–4689.Google Scholar
Murray, J. W. 2000. When does environmental variability become environmental change. Pp. 737 in R. E. Martin, ed. Environmental micropaleontology: the application of microfossils to environmental geology. Springer, Boston, Mass.Google Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H.. 2016. vegan: community ecology package. https://CRAN.R-project.org/package=vegan.Google Scholar
Omori, A., Kitamura, A., Fujita, K., Honda, K., and Yamamoto, N.. 2010. Reconstruction of light conditions within a submarine cave during the past 7000 years based on the temporal and spatial distribution of algal symbiont-bearing large benthic foraminifers. Palaeogeography, Palaeoclimatology, Palaeoecology 292:443452.Google Scholar
R Development Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rogers, A. D. 2015. Environmental change in the deep ocean. Annual Review of Environment and Resources 40:138.Google Scholar
Ruan, P., and Hao, Y.. 1988. Systematic description of microfossils, 2. Ostracoda. Quaternary Microbiotas in the Okinawa Trough and Their Geological Significance Pp. 227395. Geological Publishing House, Beijing. [In Chinese.]Google Scholar
Sagawa, T., Kuwae, M., Tsuruoka, K., Nakamura, Y., Ikehara, M., and Murayama, M.. 2014. Solar forcing of centennial-scale East Asian winter monsoon variability in the mid- to late Holocene. Earth and Planetary Science Letters 395:124135.Google Scholar
Tabuki, R., and Hanai, T.. 1994. A “living fossil ostracod” in submarine caves—a new saipanettid genus. Fossils 57:1620 [In Japanese.]Google Scholar
——.Tabuki, R. 1999. A new sigillid ostracod from submarine caves of the Ryukyu Islands, Japan. Palaeontology 42:569593.Google Scholar
Tabuki, R., and Nohara, T.. 1990. The Ostracoda of the Sekisei-sho area, Ryukyu Islands, Japan: a preliminary report on ostracods from coral reefs in the Ryukyu Islands. Pp. 365377 in R. C. Whatley and C. Maybury, eds. Ostracoda and global events. Chapman and Hall, London.Google Scholar
Tabuki, R., Nakano, T., and Nohara, T.. 1987. Preliminary report on ostracode fauna from Sekisei–sho area, Yaeyama Islands. Bulletin of College of Education, University of the Ryukyus 31:323335. [In Japanese.]Google Scholar
Taylor, P. D., and Palmer, T. J.. 1994. Submarine caves in a Jurassic reef (La Rochelle, France) and the evolution of cave biotas. Naturwissenschaften 81:357360.Google Scholar
Ubukata, T., Kitamura, A., Hiramoto, M., and Kase, T.. 2009. A 5000-year fossil record of larval shell morphology of submarine cave microshells. Evolution 63:295300.Google Scholar
van Hengstum, P. J., and Scott, D. B.. 2012. Sea-level rise and coastal circulation controlled Holocene groundwater development in Bermuda and caused a meteoric lens to collapse 1600 years ago. Marine Micropaleontology 90–91:2943.Google Scholar
van Hengstum, P. J., Scott, D. B., Gröcke, D. R., and Charette, M. A.. 2011. Sea level controls sedimentation and environments in coastal caves and sinkholes. Marine Geology 286:3550.Google Scholar
Yamamoto, N., Kitamura, A., Ohmori, A., Morishima, Y., Toyofuku, T., and Ohashi, S.. 2009a. Long-term changes in sediment type and cavernicolous bivalve assemblages in Daidokutsu submarine cave, Okinawa Islands: evidence from a new core extending over the past 7,000 years. Coral Reefs 28:967976.Google Scholar
Yamamoto, N., Sakai, S., and Kitamura, A.. 2009b. Evaluation of the δ18O value of the submarine cavernicolous micro-bivalve Carditella iejimensis as a proxy for palaeotemperature. Paleontological Research 13:279284.Google Scholar
Yasuhara, M., and Cronin, T. M.. 2008. Climatic influences on deep-sea ostracode (Crustacea) diversity for the last three million years. Ecology 89:S53S65.Google Scholar
Yasuhara, M., and Danovaro, R.. 2016. Temperature impacts on deep-sea biodiversity. Biological Reviews 91:275287.Google Scholar
Yasuhara, M., Cronin, T. M., deMenocal, P. B., Okahashi, H., and Linsley, B. K.. 2008. Abrupt climate change and collapse of deep-sea ecosystems. Proceedings of the National Academy of Sciences USA 105:1556–1560.Google Scholar
Yasuhara, M., Hunt, G., Breitburg, D., Tsujimoto, A., and Katsuki, K.. 2012a. Human-induced marine ecological degradation: micropaleontological perspectives. Ecology and Evolution 2:32423268.Google Scholar
Yasuhara, M., Hunt, G., Cronin, T. M., Hokanishi, N., Kawahata, H., Tsujimoto, A., and Ishitake, M.. 2012b. Climatic forcing of quaternary deep-sea benthic communities in the North Pacific Ocean. Paleobiology 38:162179.Google Scholar
Yasuhara, M., Okahashi, H., Cronin, T. M., Rasmussen, T. L., and Hunt, G.. 2014. Response of deep-sea biodiversity to abrupt deglacial and Holocene climate changes in the North Atlantic Ocean. Global Ecology and Biogeography 23:957967.Google Scholar
Yasuhara, M., Tittensor, D. P., Hillebrand, H., and Worm, B.. 2017. Combining marine macroecology and palaeoecology in understanding biodiversity: microfossils as a model. Biological Reviews 92:199–215.Google Scholar