Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-27T20:51:05.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Exploring photosymbiotic ecology of planktic foraminifers from chamber-by-chamber isotopic history of individual foraminifers

Published online by Cambridge University Press:  10 March 2015

Haruka Takagi ,
Kazuyoshi Moriya ,
Toyoho Ishimura ,
Atsushi Suzuki ,
Hodaka Kawahata  and
Hiromichi Hirano
Haruka Takagi
Affiliation:
Graduate School of Creative Science and Engineering, Waseda University, 1-6-1 Nishiwaseda, Shinjuku, Tokyo 169-8050, Japan. E-mail: [email protected]
Kazuyoshi Moriya
Affiliation:
Department of Earth Sciences, School of Education, Waseda University, 1-6-1 Nishiwaseda, Shinjuku, Tokyo 169-8050, Japan
Toyoho Ishimura
Affiliation:
Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan
Atsushi Suzuki
Affiliation:
Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan
Hodaka Kawahata
Affiliation:
Atmospheric Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Hiromichi Hirano
Affiliation:
Department of Earth Sciences, School of Education, Waseda University, 1-6-1 Nishiwaseda, Shinjuku, Tokyo 169-8050, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

Evolution of photosymbiotic ecology is an important adaptation for planktic foraminifers that enhances the ecological advantage of living in oligotrophic oceans. Therefore, detecting photosymbiotic ecology in fossil species is one of the keys to understanding the paleobiodiversity dynamics of planktic foraminifers. Because foraminiferal tests record the ontogenetic history of ecological information in geochemical signatures, analyzing individual geochemical profiles with growth can reveal a species’ ecology. This study examined chamber-by-chamber stable isotopes (δ13C and δ18O) of foraminiferal individuals to identify photosymbiotic signals. We observed an ontogenetic δ13C increase of up to 2.4‰, accompanied by relatively stable, negative δ18O, in the symbiotic species Globigerinoides conglobatus and Globigerinoides sacculifer. In contrast, δ13C and δ18O showed significant positive correlation during ontogeny in the asymbiotic species Globorotalia truncatulinoides. These two ecological groups produce contrasting isotopic profiles, thereby allowing us to use our ontogenetic isotopic analyses of individual specimens to identify algal photosymbiosis in fossil foraminifers. The chamber-by-chamber isotope analyses with individual ontogeny have great advantages in analyzing rare species because only one individual is required to describe ontogenetic isotopic history. In addition to photosymbiotic identification, our methods hold great potential to provide new insight into species paleoecological studies such as the ontogenetic history of calcification depth.

Type
Articles
Information
Paleobiology , Volume 41 , Issue 1 , January 2015 , pp. 108 - 121
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved. 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Aze, T., Ezard, T. H. G., Purvis, A., Coxall, H. K., Stewart, D. R. M., Wade, B. S., and Pearson, P. N.. 2011. A phylogeny of Cenozoic macroperforate planktic foraminifera from fossil data. Biological Reviews 86:900–927.Google Scholar
Bé, A. W. H. 1980. Gametogenic calcification in a spinose planktonic foraminifer, Globigerinoides sacculifer (Brady). Marine Micropaleontology 5:283–310.CrossRefGoogle Scholar
Bé, A. W. H., Hemleben, C., Anderson, O. R., Spindler, M., Hacunda, J., and Tuntivate-Choy, S.. 1977. Laboratory and field observations of living planktonic foraminifera. Micropaleontology 23:155–179.Google Scholar
Berger, W. H., Killingley, J. S., and Vincent, E.. 1978. Stable isotopes in deep-sea carbonates: box core ERDC-92, west Equatorial Pacific. Oceanologica Acta 1:203–216.Google Scholar
Birch, H. S., Coxall, H. K., and Pearson, P. N.. 2012. Evolutionary ecology of Early Paleocene planktonic foraminifera: size, depth habitat and symbiosis. Paleobiology 38:374–390.CrossRefGoogle Scholar
Bornemann, A., and Norris, R. D.. 2007. Size-related stable isotope changes in Late Cretaceous planktic foraminifera: implications for paleoecology and photosymbiosis. Marine Micropaleontology 65:32–42.Google Scholar
Coxall, H. K., D’Hondt, S., and Zachos, J. C.. 2006. Pelagic evolution and environmental recovery after the Cretaceous-Paleogene mass extinction. Geology 34:297–300.Google Scholar
D’Hondt, S., and Zachos, J. C.. 1993. On stable isotopic variation and earliest Paleocene planktic foraminifera. Paleoceanography 8:527–547.Google Scholar
D’Hondt, S., Zachos, J. C., and Schultz, G.. 1994. Stable isotopic signals and photosymbiosis in Late Paleocene planktic foraminifera. Paleobiology 20:391–406.Google Scholar
Ezard, T. H. G., Aze, T., Pearson, P. N., and Purvis, A.. 2011. Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science 332:349–351.CrossRefGoogle ScholarPubMed
Faber, W. W. Jr., Anderson, O. R., Lindsey, J. L., and Caron, D. A.. 1988. Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis. I. Occurrence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. Journal of Foraminiferal Research 18:334–343.CrossRefGoogle Scholar
Gastrich, M. D. 1987. Ultrastructure of a new intracellular symbiotic alga found within planktonic foraminifera. Journal of Phycology 23:623–632.Google Scholar
Hart, M. B., Hylton, M. D., Oxford, M. J., Price, G. D., Hudson, W., and Swart, C. W.. 2003. The search for the origin of the planktic foraminifera. Journal of Geological Society, London 160:341–343.CrossRefGoogle Scholar
Hemleben, C., Spindler, M., Breitinger, I., and Deuser, W. G.. 1985. Field and laboratory studies on the ontogeny and ecology of some globorotaliid species from the Sargasso Sea off Bermuda. Journal of Foraminiferal Research 15:254–272.Google Scholar
Hemleben, C., Spindler, M., and Anderson, O. R.. 1989. Modern planktonic foraminifera. Springer, New York.Google Scholar
Houston, R. M., and Huber, B. T.. 1998. Evidence of photosymbiosis in fossil taxa? Ontogenetic stable isotope trends in some Late Cretaceous planktic foraminifera. Marine Micropaleontology 34:29–46.Google Scholar
Ishimura, T., Tsunogai, U., and Gamo, T.. 2004. Stable carbon and oxygen isotopic determination of sub-microgram quantities of CaCO3 to analyze individual foraminiferal shells. Rapid Communications in Mass Spectrometry 18:2883–2888.Google Scholar
Ishimura, T., Tsunogai, U., and Nakagawa, F.. 2008. Grain-scale heterogeneities in the stable carbon and oxygen isotopic compositions of the international standard calcite materials (NBS 19, NBS 18, IAEA-CO-1, and IAEA-CO-8). Rapid Communications in Mass Spectrometry 22:1925–1932.Google Scholar
Ishimura, T., Tsunogai, U., Hasegawa, S., Nakagawa, F., Oi, T., Kitazato, H., Suga, H., and Toyofuku, T.. 2012. Variation in stable carbon and oxygen isotopes of individual benthic foraminifera: tracers for quantifying the magnitude of isotopic disequilibrium. Biogeosciences 9:4353–4367.Google Scholar
Kennett, J. P., and Srinivasan, M. S.. 1983. Neogene planktonic foraminifera: a phylogenetic atlas. Hutchinson Ross, New York.Google Scholar
Kimoto, K., Ishimura, T., Tsunogai, U., Itaki, T., and Ujiié, Y.. 2009. The living triserial planktic foraminifer Gallitellia vivans (Cushman): distribution, stable isotopes, and paleoecological implications. Marine Micropaleontology 71:71–79.Google Scholar
Koppers, A. A. P., Yamazaki, T., Geldmacher, J., and the Expedition 330 Scientists. 2012. Proceedings of the Integrated Ocean Drilling Program, 330. Integrated Ocean Drilling Program Management International, Inc., Tokyo.Google Scholar
Kroopnick, P. M. 1985. The distribution of 13C of ΣCO2 in the world oceans. Deep-Sea Research 32:57–84.Google Scholar
Leckie, R. M. 1989. A paleoceanographic model for the early evolutionary history of planktonic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 73:107–138.Google Scholar
Lohmann, G. P. 1995. A model for variation in the chemistry of planktic foraminifera due to secondary calcification and selective dissolution. Paleoceanography 10:445–457.Google Scholar
Lohmann, G. P., and Schweitzer, P. N.. 1990. Growth and chemistry of Globorotalia truncatulinoides as probes of the past thermocline, Part I. Shell size. Paleoceanography 5:55–75.Google Scholar
McConnaughey, T. 1989a. 13C and 18O isotopic disequilibrium in biological carbonates. I. Patterns. Geochimica et Cosmochimica Acta 53:151–162.CrossRefGoogle Scholar
McConnaughey, T. 1989b. 13C and 18O isotopic disequilibrium in biological carbonates. II. In vitro simulation of kinetic isotope effects. Geochimica et Cosmochimica Acta 53:163–171.Google Scholar
Mulitza, S., Dürkoop, A., Hale, W., Wefer, G., and Nieber, H. S.. 1997. Planktonic foraminifera as recorders of past surface-water stratification. Geology 25:335–338.Google Scholar
Norris, R. D. 1991. Biased extinction and evolutionary trends. Paleobiology 17:388–399.Google Scholar
Norris, R. D. 1996. Symbiosis as an evolutionary innovation in the radiation of Paleocene planktic foraminifera. Paleobiology 22:461–480.Google Scholar
Ortiz, J. D., Mix, A. C., Rugh, W., Watkins, J. M., and Collier, R. W.. 1996. Deep-dwelling planktonic foraminifera of the northeastern Pacific Ocean reveal environmental control of oxygen and carbon isotopic disequilibria. Geochimica et Cosmochimica Acta 60:4509–4523.Google Scholar
Pearson, P. N., McMillan, I. K., Wade, B. S., Jones, T. D., Coxall, H. K., Bown, P. R., and Lear, C. H.. 2008. Extinction and environmental change across the Eocene-Oligocene boundary in Tanzania. Geology 36:179–182.Google Scholar
Pelejero, C., Calvo, E., and Hoegh-Guldberg, O.. 2010. Paleo-perspective on ocean acidification. Trends in Ecology and Evolution 25:332–344.Google Scholar
Ridgwell, A., and Zeebe, R. E.. 2005. The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth and Planetary Science Letters 234:299–315.Google Scholar
Saito, T., Thompson, P. R., and Breger, D.. 1981. Systematic index of Recent and Pleistocene planktic foraminifera. University of Tokyo Press, Tokyo.Google Scholar
Schiebel, R. 2002. Planktic foraminiferal sedimentation and the marine calcite budget. Global Biogeochemical Cycles 16. doi: 10.1029/2001GB001459.Google Scholar
Schiebel, R., and Hemleben, C.. 2005. Modern planktic foraminifera. Paläontologische Zeitschrift 79:135–148.Google Scholar
Shaked, Y., and de Vargas, C.. 2006. Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Marine Ecology Progress Series 325:59–71.Google Scholar
Siano, R., Montresor, M., Probert, I., Not, F., and de Vargas, C.. 2010. Pelagodinium gen. nov. and P. béii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385–399.Google Scholar
Simmons, M. D., BouDagher-Fadel, M. K., Banner, F. T., and Whittaker, J. E.. 1997. The Jurassic Favusellacea, the earliest Globigerinina. Pp. 17–52in M. K. BouDagher-Fadel, F. T. Banner, and J. E. Whittaker, eds. The early evolutionary history of planktonic foraminifera. Chapman and Hall, London.Google Scholar
Spero, H. J., and DeNiro, M. J.. 1987. The influence of symbiont photosynthesis on the δ18O and δ13C values of planktic foraminiferal shell calcite. Symbiosis 4:213–228.Google Scholar
Spero, H. J., and Lea, D. W.. 1993. Intraspecific stable isotope variability in the planktic foraminifera Globigerinoides sacculifer: results from laboratory experiments. Marine Micropaleontology 22:221–234.Google Scholar
Spero, H. J., and Lea, D. W.. 1996. Experimental determination of stable isotope variability in Globigerina bulloides: implications for paleoceanographic reconstructions. Marine Micropaleontology 28:231–246.Google Scholar
Spero, H. J., and Parker, S. L.. 1985. Photosynthesis in the symbiotic planktonic foraminifera Orbulina universa, and its potential contribution to oceanic primary productivity. Journal of Foraminiferal Research 15:273–281.Google Scholar
Spero, H. J., and Williams, D. F.. 1988. Extracting environmental information from planktic foraminiferal δ13C data. Nature 335:717–719.Google Scholar
Spero, H. J., Bijma, J., Lea, D. W., and Bemis, B. E.. 1997. Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390:497–500.Google Scholar
Wade, B. S., Al-Sabouni, N., Hemleben, C., and Kroon, D.. 2008. Symbiont bleaching in fossil planktic foraminifera. Evolutionary Ecology 22:253–265.CrossRefGoogle Scholar
Wessel, P., and Smith, W. H. F.. 1998. New, improved version of Generic Mapping Tools released. Eos, Transactions, American Geophysical Union79. doi: 10.1029/98EO00426.Google Scholar
Wolf-Gladrow, D. A., Bijma, J., and Zeebe, R. E.. 1999. Model simulation of the carbonate chemistry in the microenvironment of symbiont bearing foraminifera. Marine Chemistry 64:181–198.Google Scholar
Zeebe, R. E., and Westbroek, P.. 2003. A simple model for the CaCO3 saturation state of the ocean: the “Strangelove,” the “Neritan,” and the “Cretan” Ocean. Geochemistry Geophysics Geosystems 4:1104. doi:10.1029/2003GC000538.Google Scholar