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Climate-mediated changes in predator–prey interactions in the fossil record: a case study using shell-drilling gastropods from the Pleistocene Japan Sea

Published online by Cambridge University Press:  09 February 2016

Tomoki Chiba  and
Shin’ichi Sato
Tomoki Chiba
Affiliation:
Institute of Geology and Paleontology, Graduate School of Science, Tohoku University, Aoba 6-3, Aramaki, Aoba-ku, Sendai 980-8578, Japan.
Shin’ichi Sato
Affiliation:
The Tohoku University Museum, Aoba 6-3, Aramaki, Aoba-ku, Sendai 980-8578, Japan.
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Abstract

Paleoecological studies enhance our understanding of biotic responses to climate change because they consider long timescales not accessible through observational and experimental studies. Using predatory drillholes produced on fossil bivalve shells by carnivorous gastropods, we provide an example of how climate change affected predator–prey interactions. We quantitatively examine temporal changes in fossil molluscan assemblages and predation patterns from the Pleistocene Japan Sea, which experienced drastic environmental changes in relation to glacial–interglacial climate cycles. We found significant changes in predation patterns associated with a decline in the abundance of warm-water molluscan species. Climate-mediated fluctuations in the eustatic sea level and resultant weakening of the Tsushima Warm Current caused a decline in a warm-water shell-drilling predator, which moderated the predation pressure and size relationship between the predators and the bivalve prey. Our results indicate that climate-mediated range shifts of species in present-day and future marine ecosystems can likewise increase altered predator–prey interactions.

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Articles
Information
Paleobiology , Volume 42 , Issue 2 , May 2016 , pp. 257 - 268
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

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References

Literature Cited

Alexander, R. R., and Dietl, G. P.. 2001. Latitudinal trends in naticid predation on Anadara ovalis (Bruguière, 1789) and Divalinga quadrisulcata (Orbigny, 1842) from New Jersey to the Florida Keys. American Malacological Bulletin 16:179–194.Google Scholar
Amano, K. 2006. Temporal pattern of naticid predation on Glycymeris yessoensis (Sowerby) during the late Cenozoic in Japan. Palaios 21:369–375.CrossRefGoogle Scholar
Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46.Google Scholar
Ansell, A. D., and Morton, B.. 1987. Alternative predation tactics of a tropical naticid gastropod. Journal of Experimental Marine Biology and Ecology 111:109–119.Google Scholar
Barry, J. P., Baxter, C. H., Sagarin, R. D., and Gilman, S. E.. 1995. Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672–675.Google Scholar
Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C., and Finnegan, S.. 2013. Climate change and the past, present, and future of biotic interactions. Science 341:499–504.CrossRefGoogle ScholarPubMed
Bookstein, F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge.Google Scholar
Borcard, D, Gillet, F., and Legendre, P.. 2011. Numerical ecology with R. Springer.Google Scholar
Casey, M. M., and Chattopadhyay, D.. 2008. Clumping behavior as a strategy against drilling predation: implications for the fossil record. Journal of Experimental Marine Biology and Ecology 367:174–179.CrossRefGoogle Scholar
Chiba, T., and Sato, S.. 2012. Size-selective predation and drillhole-site selectivity in Euspira fortunei (Gastropoda: Naticidae): implications for ecological and palaeoecological studies. Journal of Molluscan Studies 78:205–212.Google Scholar
Chiba, T., and Sato, S.. 2013. Invasion of Laguncula pulchella (Gastropoda: Naticidae) and predator–prey interactions with bivalves on the Tona Coast, Miyagi Prefecture, northern Japan. Biological Invasions 15:587–598.CrossRefGoogle Scholar
Chiba, T., and Sato, S.. 2014. Invasion of a naticid predator and associated changes in death assemblages of bivalve prey in northern Japan: implications for palaeoecological studies. Lethaia 47:4–14.Google Scholar
Chiba, T., Shirai, M., and Sato, S.. 2014. Recognizing cryptic environmental changes by using paleoecology and taphonomy of Pleistocene bivalve assemblages in the Oga Peninsula, northern Japan. Quaternary Research 81:21–34.Google Scholar
Chiba, T., Sato, S., and Yamada, T.. 2015. Fossilized intestine casts located within closed bivalve shells: implications for palaeoecological and sedimentological studies. Lethaia 48:341–352.Google Scholar
Daley, G. M., Ostrowski, S., and Geary, D. H.. 2007. Paleoenvironmentally correlated differences in a classic predator–prey system: the bivalve Chione elevata and its gastropod predators. Palaios 22:166–173.CrossRefGoogle Scholar
Dietl, G. P., and Alexander, R. R.. 1997. Predator-prey interactions between the naticids Euspira heros Say and Neverita duplicata Say and the Atlantic surfclam Spisula solidissima Dillwyn from Long Island to Delaware. Journal of Shellfish Research 16:413–422.Google Scholar
Dietl, G. P., and Herbert, G. S.. 2005. Influence of alternative shell-drilling behaviours on attack duration of the predatory snail, Chicoreus dilectus. Journal of Zoology 265:201–206.Google Scholar
Dietl, G. P., Herbert, G. S., and Vermeij, G. J.. 2004. Reduced competition and altered feeding behavior among marine snails after a mass extinction. Science 306:2229–2231.Google Scholar
Dudley, E. C., and Vermeij, G. J.. 1978. Predation in time and space: drilling in the gastropod Turritella. Paleobiology 4:436–441.Google Scholar
Gamo, T., Nakayama, N., Takahata, N., Sano, Y., Zhang, J., Yamazaki, E., Taniyasu, S., and Yamashita, N.. 2014. The Sea of Japan and its unique chemistry revealed by time-series observations over the last 30 years. Monographs on Environment, Earth and Planets 2:1–22.Google Scholar
Goddard, J. H. R., Gosliner, T. M., and Pearse, J. S.. 2011. Impacts associated with the recent range shift of the aeolid nudibranch Phidiana hiltoni (Mollusca, Opisthobranchia) in California. Marine Biology 158:1095–1109.Google Scholar
Grey, M., Boulding, E. G., and Brookfield, M. E.. 2006. Estimating multivariate selection gradients in the fossil record: a naticid gastropod case study. Paleobiology 32:100–108.Google Scholar
Habe, T. 1961. Colored illustrations of the shells of Japan, volume II. Hoikusha Publishing, Osaka [In Japanese.].Google Scholar
Habe, T., and Ito, K.. 1965. Shells of the world in color, volume I: the northern Pacific. Hoikusha Publishing, Osaka [In Japanese.].Google Scholar
Hansen, T. A., and Kelley, P. H.. 1995. Spatial variation of naticid gastropod predation in the Eocene of North America. Palaios 10:268–278.Google Scholar
Hellberg, M. E., Balch, D. P., and Roy, K.. 2001. Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1710.Google Scholar
Hoffmeister, A. P., and Kowalewski, M.. 2001. Spatial and environmental variation in the fossil record of drilling predation: a case study from the Miocene of Central Europe. Palaios 16:566–579.Google Scholar
Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6:65–70.Google Scholar
Horikoshi, M. 1962. Warm temperate region and coastal-water area in the marine biogeography of the shallow sea system around the Japanese islands. Quaternary Research (Daiyonki-Kenkyu) 2:117–124. [in Japanese with English abstract.].CrossRefGoogle Scholar
Hunt, G., Wicaksono, S. A., Brown, J. E., and MacLeod, K. G.. 2010. Climate-driven body-size trends in the ostracod fauna of the deep Indian Ocean. Palaeontology 53:1255–1268.Google Scholar
Huntley, J. W., Fürsich, F. T., Alberti, M., Hethke, M., and Liu, C.. 2014. A complete Holocene record of trematode–bivalve infection and implications for the response of parasitism to climate change. Proceedings of the National Academy of Sciences USA 111:18150–18155.CrossRefGoogle ScholarPubMed
Hutchings, J. A., and Herbert, G. S.. 2013. No honor among snails: conspecific competition leads to incomplete drill holes by a naticid gastropod. Palaeogeography, Palaeoclimatology, Palaeoecology 379–380:32–38.Google Scholar
Kabat, A. R. 1990. Predatory ecology of naticid gastropods with a review of shell boring predation. Malacologia 32:155–193.Google Scholar
Kanazawa, K. 1990. Early Pleistocene glacio-eustatic sea-level fluctuations as deduced from periodic changes in cold- and warm-water molluscan associations in the Shimokita Peninsula, Northeast Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 79:263–273.CrossRefGoogle Scholar
Kano, K., Ohguchi, T., Yanagisawa, Y., Awata, Y., Kobayashi, N., Sato, Y., Hayashi, S., Kitazato, H., Ogasawara, K., and Komazawa, M.. 2011. Geology of the Toga and Funakawa district, quadrangle series, 1:50,000. Geological Survey of Japan, AIST, Tsukuba. [In Japanese with English abstract.].Google Scholar
Kelley, P. H., and Hansen, T. A.. 2003. The fossil record of drilling predation on bivalves and gastropods. Pp. 113–139. in P. H. Kelley, M. Kowalewski, and T. A. Hansen, eds. Predator–prey interactions in the fossil record. Kluwer Academic/Plenum Publishers, New York.Google Scholar
Kelley, P. H., and Hansen, T. A.. 2007. Latitudinal patterns in naticid gastropod predation along the East Coast of the United States: a modern baseline for interpreting temporal patterns in the fossil record. In Bromley, R. G., L. A. Buatois, M. G. Mángano, J. F. Genise, and R. N. Melchor, eds. Sediment-organism interactions: a multifaceted ichnology. SEPM Special Publication 88:287–299.Google Scholar
Kido, Y., Minami, I., Tada, R., Fujine, K., Irino, T., Ikehara, K., and Chun, J.-H.. 2007. Orbital-scale stratigraphy and high-resolution analysis of biogenic components and deep-water oxygenation conditions in the Japan Sea during the last 640 kyr. Palaeogeography, Palaeoclimatology, Palaeoecology 247:32–49.Google Scholar
Kitamura, A, Omote, H., and Oda, M.. 2000. Molluscan response to early Pleistocene rapid warming in the Sea of Japan. Geology 28:723–726.Google Scholar
Kitchell, J. A., Boggs, C. H., Kitchell, J. F., and Rice, J. A.. 1981. Prey selection by naticid gastropods: experimental tests and application to the fossil record. Paleobiology 7:533–552.Google Scholar
Kondo, Y. 1987. Burrowing depth of infaunal bivalves – observation of living species and its relation to shell morphology. Transactions and Proceedings of the Palaeontological Society of Japan, New Series 148:306–323.Google Scholar
Kosuge, S. 1967. Boring habits of Neverita didyma (Röding) and Cryptonatica janthostomoides (Kuroda and Habe). Chiribotan 4:123–124. [In Japanese.].Google Scholar
Kowalewski, M. 2002. The fossil record of predation: an overview of analytical methods. Paleontological Society Papers 8:3–42.Google Scholar
Lützen, J., Faasse, M., Gittenberger, A., Glenner, H., and Hoffmann, E.. 2012. The Japanese oyster drill Ocinebrellus inornatus (Récluz, 1851) (Mollusca, Gastropoda, Muricidae), introduced to the Limfjord, Denmark. Aquatic Invasions 7:181–191.Google Scholar
Mondal, S., Hutchings, J. A., and Herbert, G. S.. 2014. A note on edge drilling predation by naticid gastropods. Journal of Molluscan Studies 80:206–212.CrossRefGoogle Scholar
Nojo, A., and Suzuki, A.. 1999. Taphonomy of shell concentrations: reconstruction of depositional processes by combined analyses of mollusc and foraminifer. Memoirs of the Geological Society of Japan 54:35–54. [In Japanese with English abstract.].Google Scholar
Oba, T., Kato, M., Kitazato, H., Koizumi, I., Omura, A., Sakai, T., and Takayama, T.. 1991. Paleoenvironmental changes in the Japan Sea during the last 85,000 years. Paleoceanography 6:499–518.Google Scholar
Ogasawara, K., Masuda, K., and Matoba, Y.. 1986. Neogene and Quaternary molluscs from the Akita oil-field, Japan. Commemorative Association of Professor Taisuke Takayasu’s Retirement and Supporters’ Fundation of Mineral Industry Museum, Mining College, Akita University, Akita. [In Japanese.].Google Scholar
Oksanen, J, Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H.. 2015. Vegan: community ecology package. http://CRAN.R-project.org/package=vegan.Google Scholar
Okutani, T. 2000. Marine mollusks in Japan. Tokai University Press, Tokyo.Google Scholar
Rasband, W. S. 2015. ImageJ. http://rsb.info.nih.gov/ij/.Google Scholar
R Core Team. 2014. R: a language and environment for statistical computing. http://www.R-project.org/.Google Scholar
Rodrigues, C. L., Nojima, S., and Kikuchi, T.. 1987. Mechanics of prey size preference in the gastropod Neverita didyma preying on the bivalve Ruditapes philippinarum. Marine Ecology Progress Series 40:87–93.Google Scholar
Roopnarine, P. D., and Beussink, A.. 1999. Extinction and naticid predation of the bivalve Chione von Mühlfeld in the late Neogene of Florida. Palaeontologia Electronica 2:24 pp.Google Scholar
Roy, K., Jablonski, D., and Valentine, J. W.. 1995. Thermally anomalous assemblages revisited: patterns in the extraprovincial latitudinal range shifts of Pleistocene marine mollusks. Geology 23:1071–1074.Google Scholar
Sanford, E. 1999. Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097.Google Scholar
Sanford, E. 2002. Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integrative and Comparative Biology 42:881–891.Google Scholar
Sarkar, D. 2008. Lattice: multivariate data visualization with R. Springer.Google Scholar
Sato, S. 1999. Temporal change of life-history traits in fossil bivalves: an example of Phacosoma japonicum from the Pleistocene of Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 154:313–323.Google Scholar
Sawyer, J. A., and Zuschin, M.. 2010. Intensities of drilling predation of molluscan assemblages along a transect through the northern Gulf of Trieste (Adriatic Sea). Palaeogeography, Palaeoclimatology, Palaeoecology 285:152–173.CrossRefGoogle Scholar
Schemske, D. W., Mittelbach, G. G., Cornell, H. V., Sobel, J. M., and Roy, K.. 2009. Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics 40:245–269.Google Scholar
Schiffbauer, J. D., Yanes, Y., Tyler, C., Kowalewski, M., and Leighton, L. R.. 2008. The microstructural record of predation: a new approach for identifying predatory drill holes. Palaios 23:810–820.Google Scholar
Shirai, M., and Tada, R.. 2000. Sedimentary successions formed by fifth-order glacio-eustatic cycles in the middle to upper Quaternary formations of the Oga Peninsula, Northeast Japan. Journal of Sedimentary Research 70:839–849.Google Scholar
Shirai, M., and Tada, R.. 2002. High-resolution reconstruction of Quaternary crustal movement based on sedimentary facies analysis: an example from the Oga Peninsula, Northern Japan. Journal of Sedimentary Research 72:386–392.Google Scholar
Tada, R., Irino, T., and Koizumi, I.. 1999. Land-ocean linkages over orbital and millennial timescales recorded in late Quaternary sediments of the Japan Sea. Paleoceanography 14:236–247.Google Scholar
Tian, Y., Kidokoro, H., Watanabe, T., and Iguchi, N.. 2008. The late 1980s regime shift in the ecosystem of Tsushima warm current in the Japan/East Sea: evidence from historical data and possible mechanisms. Progress in Oceanography 77:127–145.Google Scholar
Tian, Y., Kidokoro, H., Watanabe, T., Igeta, Y., Sakaji, H., and Ino, S.. 2012. Response of yellowtail, Seriola quinqueradiata, a key large predatory fish in the Japan Sea, to sea water temperature over the last century and potential effects of global warming. Journal of Marine Systems 91:1–10.CrossRefGoogle Scholar
Tsuchida, E., and Hayashi, I.. 1994. Characteristics of lower-sublittoral and bathyal molluscs in the western area of the Sea of Japan. Bulletin of the Japan Sea National Fisheries Research Institute 44:81–129. [In Japanese with English abstract.].Google Scholar
Vermeij, G. J. 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia 19:329–334.Google Scholar