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Refining the interpretation of oxygen isotope variability in free-swimming organisms

Abstract

Serially sampled oxygen isotope ratios (δ18O) from fossil and modern cephalopods may provide new insight into the behavior and longevity of individuals. Interpretation of these data is generally more difficult than similar data from bivalves or brachiopods because the measured δ18O from shell combines both seasonal change and depth change over the life of an individual. In this paper, a simple null model is presented combining the three fundamental controls on a measured δ18O profile in a free-swimming organism: swimming behavior, seasonal water column change, and time averaging in sampling. Model results indicate that seasonal variability in δ18O in a free-swimming organism can be interpreted in locations with strong seasonality through most of the swimming range but is complicated by swimming velocity and is sometimes best expressed by changes in δ18O variance rather than simple sinusoidal patterns. In other locations with a stable thermocline or seasonal ranges in only a small portion of the water column, no variability caused by seasonality would be expected. Furthermore, large ranges of δ18O (~ 4‰) are possible within and between individuals in settings with persistent thermoclines like the tropics, depending on the swimming depth limits and behavior of individuals. These results suggest that future interpretation of serially sampled δ18O should consider seasonal water column variation from either modern or modeling sources in addition to comparison to co-occurring benthic and planktonic organisms. Additionally, this modeling casts doubt on the promise of isotope sclerochronology alone as a growth chronometer in ammonites and other free-swimming fossil organisms and highlights the need for other methods of quantitatively determining age.

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Data from (Locarnini et al. 2013)

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References

  1. Aitken, J. P. (2001). The bioenergetics of the giant Australian cuttlefish Sepia apama. PhD Thesis, MSc Thesis. (Dalhousie University: Halifax, Nova Scotia, Canada).

  2. Auclair, A.-C., Lecuyer, C., Bucher, H., & Sheppard, S. M. (2004). Carbon and oxygen isotope composition of Nautilus macromphalus: a record of thermocline waters off New Caledonia. Chemical Geology, 207, 91–100.

  3. Barbin, V. (2013). Application of cathodoluminescence microscopy to recent and past biological materials: a decade of progress. Mineralogy and Petrology, 107, 353–362.

  4. Bucher, H., Landman, N. H., Klofak, S. M., & Guex, J. (1996). Mode and rate of growth in ammonoids; p. In N. H. Landman, K. Tanabe, & R. A. Davis (Eds.), Ammonoid paleobiology (Vol. 13, pp. 407–461). Topics in Geobiology. New York: Plenum Press.

  5. Carlson, B., McKibben, J. N., & deGruy, M. V. (1984). Telemetric investigation of vertical migration of Nautilus belauensis in Palau. Pacific Science, 38, 183–188.

  6. Chamberlain, J. A., Jr. (1993). Locomotion in ancient seas: Constraint and opportunity in cephalopod adaptive design. Geobios, 26, 49–61.

  7. Chamberlain, J. A., Jr., & Westermann, G. E. G. (1976). Hydrodynamic properties of cephalopod shell ornament. Paleobiology, 2, 316–331.

  8. Clements, T., Colleary, C., De Baets, K., & Vinther, J. (2017). Buoyancy mechanisms limit preservation of coleoid cephalopod soft tissues in Mesozoic Lagerstätten. Palaeontology, 60, 1–14.

  9. R Core Team. (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  10. de Aguiar, D. C., Rossi-Wongtschowski, C. L. D. B., & Perez, J. A. A. (2012). Validation of daily growth increments of statoliths of Brazilian squid Doryteuthis plei and D. sanpaulensis (Cephalopoda: loliginidae). Bioikos, 26, 13–21.

  11. Dennis, K. J., Cochran, J. K., Landman, N. H., & Schrag, D. P. (2013). The climate of the Late Cretaceous: New insights from the application of the carbonate clumped isotope thermometer to Western Interior Seaway macrofossil. Earth and Planetary Science Letters, 362, 51–65.

  12. Doguzhaeva, L. (1982). Rhythms of ammonoid shell secretion. Lethaia, 15, 385–394.

  13. Dunstan, A. J., Ward, P. D., & Marshall, N. J. (2011). Vertical distribution and migration patterns of Nautilus pompilius. PLoS ONE, 6, e16311.

  14. Dutton, A., Huber, B. T., Lohmann, K. C., & Zinsmeister, W. J. (2007). High-resolution stable isotope profiles of a dimitobelid belemnite: Implications for paleodepth habitat and Late Maastrichtian climate seasonality. Palaios, 22, 642–650.

  15. Ellis, N. M., & Tobin, T. S. (2019). Evidence for seasonal variation in δ13C and δ18O profiles of Baculites and implications for growth rate. Palaeontology, 1–16.

  16. Fatherree, J. W., Harries, P. J., & Quinn, T. M. (1998). Oxygen and carbon isotopic “dissection” of Baculites compressus (Mollusca: Cephalopoda) from the Pierre Shale (upper Campanian) of South Dakota; implications for paleoenvironmental reconstructions. Palaios, 13, 376–385.

  17. Frank, M. G., Waldrop, R. H., Dumoulin, M., Aton, S., & Boal, J. G. (2012). A preliminary analysis of sleep-like states in the cuttlefish Sepia officinalis. PLoS One, 7, e38125.

  18. Gerringer, M. E., Andrews, A. H., Huss, G. R., Nagashima, K., Popp, B. N., Linley, T. D., et al. (2018). Life history of abyssal and hadal fishes from otolith growth zones and oxygen isotopic compositions. Deep Sea Research Part I: Oceanographic Research Papers, 132, 37–50.

  19. Grossman, E. L., & Ku, T.-L. (1986). Oxygen and carbon isotope fractionation in biogenic aragonite: Temperature effects. Chemical Geology: Isotope Geoscience Section, 59, 59–74.

  20. Hain, M. P., Sigman, D. M., & Haug, G. H. (2014). 8.18—The biological pump in the past; p. In H. D. Holland & K. K. Turekian (Eds.), Treatise on Geochemistry (Vol. 2, pp. 485–517). Oxford: Elsevier.

  21. Helser, T., Kastelle, C., Crowell, A., Ushikubo, T., Orland, I. J., Kozdon, R., et al. (2018). A 200-year archaeozoological record of Pacific cod (Gadus macrocephalus) life history as revealed through ion microprobe oxygen isotope ratios in otoliths. Journal of Archaeological Science: Reports, 21, 1236–1246.

  22. Hewitt, R. A. (2000). Geological interpretations from cephalopod habitat and implosion depth limits. Revue de Paléobiologie, Special, 8, 95–107.

  23. Huber, B. T., MacLeod, K. G., Watkins, D. K., & Coffin, M. F. (2018). The rise and fall of the Cretaceous Hot Greenhouse climate. Global and Planetary Change, 167, 1–23.

  24. Ivany, L. C. (2012). Reconstructing paleoseasonality from accretionary skeletal carbonates—Challenges and opportunities. In L. C. Ivany & B. T. Huber (Eds.) Earth’s Deep-Time Climate—The State of the Art in 2012. The Paleontological Society Papers (vol. 18, pp. 133–165). The Paleontological Society.

  25. Ivany, L. C., Patterson, W. P., & Lohmann, K. C. (2000). Cooler winters as a possible cause of mass extinctions at the Eocene/Oligocene boundary. Nature, 407, 887–890.

  26. Jacobs, D. K. (1992). Shape, drag, and power in ammonoid swimming. Paleobiology, 18, 203–220.

  27. Jacobs, D. K., & Chamberlain, J. A. (1996). Buoyancy and hydrodynamics in ammonoids; p. In N. H. Landman, K. Tanabe, & R. A. Davis (Eds.), Ammonoid paleobiology (Vol. 13, pp. 169–224). Topics in Geobiology. New York: Plenum Press.

  28. Jones, D. S. (1983). Sclerochronology: reading the record of the molluscan shell. American Scientist, 71, 384–391.

  29. Judd, E. J., Wilkinson, B. H., & Ivany, L. C. (2018). The life and time of clams: Derivation of intra-annual growth rates from high-resolution oxygen isotope profiles. Palaeogeography, Palaeoclimatology, Palaeoecology, 490, 70–83.

  30. Kim, S.-T., O’Neil, J. R., Hillaire-Marcel, C., & Mucci, A. (2007). Oxygen isotope fractionation between synthetic aragonite and water: influence of temperature and Mg2+ concentration. Geochimica et Cosmochimica Acta, 71, 4704–4715.

  31. Kump, L. R., & R. L. Slingerland. (1999). Circulation and stratification of the early Turonian Western Interior Seaway: Sensitivity to a variety of forcings. In E. Barrera & C. C. Johnson (Eds.) Evolution of the Cretaceous ocean–climate system (pp. 181–190). Geological Society of America Special Paper.

  32. Landman, N. H. (1983). Ammonoid growth rhythms. Lethaia, 16, 248–248.

  33. Landman, N. H., Cochran, J. K., Rye, D. M., Tanabe, K., & Arnold, J. M. (1994). Early life history of Nautilus: Evidence from isotopic analyses of aquarium-reared specimens. Paleobiology, 20, 40–51.

  34. Landman, N. H., Cochran, J. K., Slovacek, M., Larson, N. L., Garb, M. P., Brezina, J., et al. (2018a). Isotope sclerochronology of ammonites (Baculites compressus) from methane seep and non-seep sites in the Late Cretaceous Western Interior Seaway, USA: Implications for ammonite habitat and mode of life. American Journal of Science, 318, 603–639.

  35. Landman, N. H., Grier, J. W., Cochran, J. K., Grier, J. C., Petersen, J. G., & Towbin, W. H. (2018b). Nautilid nurseries: hatchlings and juveniles of Eutrephoceras dekayi from the lower Maastrichtian (Upper Cretaceous) Pierre Shale of east-central Montana. Lethaia, 51, 48–74.

  36. Landman, N. H., Rye, D. M., & Shelton, K. L. (1983). Early ontogeny of Eutrephoceras compared to recent Nautilus and Mesozoic ammonites: Evidence from shell morphology and light stable isotopes. Paleobiology, 9, 269–279.

  37. Lécuyer, C., & Bucher, H. (2006). Stable isotope compositions of a late Jurassic ammonite shell: a record of seasonal surface water temperatures in the southern hemisphere? eEarth Discussions, 1, 1–19.

  38. LeGrande, A. N., & Schmidt, G. A. (2006). Global gridded data set of the oxygen isotopic composition in seawater. Geophysical Research Letters, 33, L12604.

  39. Lemanis, R., Zachow, S., Fusseis, F., & Hoffmann, R. (2015). A new approach using high-resolution computed tomography to test the buoyant properties of chambered cephalopod shells. Paleobiology, 41, 313–329.

  40. Linzmeier, B. J., Kozdon, R., Peters, S. E., & Valley, J. W. (2016). Oxygen isotope variability within Nautilus shell growth bands. PLoS One, 11, e0153890.

  41. Linzmeier, B. J., Landman, N. H., Peters, S. E., Kozdon, R., Kitajima, K., & Valley, J. W. (2018). Ion microprobe–measured stable isotope evidence for ammonite habitat and life mode during early ontogeny. Paleobiology, 44, 684–708.

  42. Liu, B., Chen, X., Chen, Y., Lu, H., & Qian, W. (2011). Trace elements in the statoliths of jumbo flying squid off the Exclusive Economic Zones of Chile and Peru. Marine Ecology Progress Series, 429, 93–101.

  43. Locarnini, R. A., Mishonov, A. V., Antonov, J. I., Boyer, T. P., Garcia, H. E., Baranova, O. K., Zweng, M. M., Paver, C. R., Reagan, J. R., Johnson, D. R., Hamilton, M., & Seidov, D. (2013). World Ocean Atlas 2013, Volume 1: Temperature. In S. Levitus, A. Mishonov (Eds.), NOAA Atlas NESDIS 73 (p. 40).

  44. Lukeneder, A. (2015). Ammonoid habitats and life history; p. In C. Klug, D. Korn, K. D. Baets, I. Kruta, & R. H. Mapes (Eds.), Ammonoid paleobiology: From anatomy to ecology (Vol. 43, pp. 689–791). Topics in Geobiology, Dordrecht: Springer.

  45. Lukeneder, A., Harzhauser, M., Müllegger, S., & Piller, W. (2008). Stable isotopes (δ18O and δ13C) in Spirula spirula shells from three major oceans indicate developmental changes paralleling depth distributions. Marine Biology, 154, 175–182.

  46. Lukeneder, A., Harzhauser, M., Müllegger, S., & Piller, W. E. (2010). Ontogeny and habitat change in Mesozoic cephalopods revealed by stable isotopes (δ18O, δ13C). Earth and Planetary Science Letters, 296, 103–114.

  47. Martin, A. W., Catala-Stucki, I., & Ward, P. D. (1978). The growth rate and reproductive behavior of Nautilus macromphalus. Neues Jahrbuch Fur Geologie Und Palaontologie, 156, 207–225.

  48. McConnaughey, T. A., & Gillikin, D. P. (2008). Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters, 28, 287–299.

  49. Meyers, S. R. (2014). Astrochron: An R package for astrochronologyhttp://cran.r-project.org/package=astrochron

  50. Meyers, S. R., Sageman, B. B., & Hinnov, L. A. (2001). Integrated quantitative stratigraphy of the Cenomanian–Turonian bridge creek limestone member using evolutive harmonic analysis and stratigraphic modeling. Journal of Sedimentary Research, 71, 628–644.

  51. Moriya, K. (2015). Isotope signature of ammonoid shells; p. In C. Klug, D. Korn, K. De Baets, I. Kruta, & R. H. Mapes (Eds.), Ammonoid paleobiology: From anatomy to ecology (Vol. 43, pp. 793–836). Topics in Geobiology, Dordrecht: Springer.

  52. Moriya, K., Nishi, H., Kawahata, H., Tanabe, K., & Takayanagi, Y. (2003). Demersal habitat of Late Cretaceous ammonoids: Evidence from oxygen isotopes for the Campanian (Late Cretaceous) northwestern Pacific thermal structure. Geology, 31, 167–170.

  53. Moss, D. K., Ivany, L. C., Silver, R. B., Schue, J., & Artruc, E. G. (2017). High-latitude settings promote extreme longevity in fossil marine bivalves. Paleobiology, 43, 365–382.

  54. Naglik, C., Tajika, A., Chamberlain, J., Klug, C. (2015). Ammonoid locomotion. In C. Klug, D. Korn, K. De Baets, I. Kruta, & R. H. Mapes (Eds.), Ammonoid paleobiology: From anatomy to ecology (Vol. 43, pp. 649–688). Topics in Geobiology, Dordrecht: Springer

  55. Nakamura, Y. (1993). Vertical and horizontal movements of mature females of Ommastrephes bartramii observed by ultrasonic telemetry. In T. Okutani, R. K. O’Dor, & T. Kubodera (Eds.), Recent advances in cephalopod fisheries biology (pp. 331–336). Tokyo: Tokai University Press.

  56. O’Dor, R. (2002). Telemetered cephalopod energetics: Swimming, soaring, and blimping. Integrative and Comparative Biology, 42, 1065–1070.

  57. O’Dor, R. K., Adamo, S., Aitken, J. P., Andrade, Y., Finn, J., Hanlon, R. T., et al. (2002). Currents as environmental constraints on the behavior, energetics and distribution of squid and cuttlefish. Bulletin of Marine Science, 71, 601–617.

  58. O’Dor, R. K., Forsythe, J., Webber, D. M., Wells, J., & Wells, M. J. (1993). Activity levels of Nautilus in the wild. Nature, 362, 626–628.

  59. Oba, T., Kai, M., & Tanabe, K. (1992). Early life history and habitat of Nautilus pompilius inferred from oxygen isotope examinations. Marine Biology, 113, 211–217.

  60. Ohno, A., Miyaji, T., & Wani, R. (2015). Inconsistent oxygen isotopic values between contemporary secreted septa and outer shell walls in modern Nautilus. Lethaia, 48, 332–340.

  61. Passey, B. H., Robinson, T. F., Ayliffe, L. K., Cerling, T. E., Sponheimer, M., Dearing, M. D., et al. (2005). Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. Journal of Archaeological Science, 32, 1459–1470.

  62. Petersen, S. V., Tabor, C. R., Lohmann, K. C., Poulsen, C. J., Meyer, K. W., Carpenter, S. J., et al. (2016). Temperature and salinity of the Late Cretaceous Western Interior Seaway. Geology, 11, 903–906

  63. Rexfort, A., & Mutterlose, J. (2006). Stable isotope records from Sepia officinalis—A key to understanding the ecology of belemnites? Earth and Planetary Science Letters, 247, 212–221.

  64. Sakamoto, T., Komatsu, K., Shirai, K., Higuchi, T., Ishimura, T., Setou, T., Kamimura, Y., Watanabe, C., & Kawabata, A. (2018). Combining microvolume isotope analysis and numerical simulation to reproduce fish migration history. Methods in Ecology and Evolution , 10, 59–69.

  65. Schöne, B. R., Wanamaker, A. D., Jr., Fiebig, J., Thébault, J., & Kreutz, K. (2011). Annually resolved δ13C shell chronologies of long-lived bivalve mollusks (Arctica islandica) reveal oceanic carbon dynamics in the temperate North Atlantic during recent centuries. Palaeogeography, Palaeoclimatology, Palaeoecology, 302, 31–42.

  66. Scotese, C. R. (1991). Jurassic and Cretaceous plate tectonic reconstructions. Palaeogeography, Palaeoclimatology, Palaeoecology, 87, 493–501.

  67. Sessa, J. A., Larina, E., Knoll, K., Garb, M., Cochran, J. K., Huber, B. T., et al. (2015). Ammonite habitat revealed via isotopic composition and comparisons with co-occurring benthic and planktonic organisms. Proceedings of the National Academy of Sciences, 112, 15562–15567.

  68. Sobarzo, M., Bravo, L., Donoso, D., Garcés-Vargas, J., & Schneider, W. (2007). Coastal upwelling and seasonal cycles that influence the water column over the continental shelf off central Chile. Progress in Oceanography, 75, 363–382.

  69. Taylor, B. E., & Ward, P. D. (1983). Stable isotopic studies of Nautilus macromphalus Sowerby (New Caledonia) and Nautilus pompilius L. (Fiji). Palaeogeography, Palaeoclimatology, Palaeoecology, 41, 1–16.

  70. Tourtelot, H. A., & Rye, R. O. (1969). Distribution of oxygen and carbon isotopes in fossils of Late Cretaceous age, Western Interior region of North America. Geological Society of America Bulletin, 80, 1903–1922.

  71. van Leeuwen, S., Tett, P., Mills, D., & van der Molen, J. (2015). Stratified and nonstratified areas in the North Sea: Long-term variability and biological and policy implications. Journal of Geophysical Research: Oceans, 120, 4670–4686.

  72. Ward, P. D., Carlson, B., Weekly, M., & Brumbaugh, B. (1984). Remote telemetry of daily vertical and horizontal movement of Nautilus in Palau. Nature, 309, 248–250.

  73. Weidel, B. C., Ushikubo, T., Carpenter, S. R., Kita, N. T., Cole, J. J., Kitchell, J. F., et al. (2007). Diary of a bluegill (Lepomis macrochirus): daily 13C and 18O records in otoliths by ion microprobe. Canadian Journal of Fisheries and Aquatic Sciences, 64, 1641–1645.

  74. Westermann, G. E. G. (1996). Ammonoid life and habitat; p. In N. H. Landman, K. Tanabe, & R. A. Davis (Eds.), Ammonoid paleobiology (Vol. 13, pp. 607–707). Topics in Geobiology, New York: Plenum Press.

  75. Westermann, B., Beck-Schildwächter, I., Beuerlein, K., Kaleta, E. F., & Schipp, R. (2004). Shell growth and chamber formation of aquarium-reared Nautilus pompilius (Mollusca, Cephalopoda) by X-ray analysis. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 301A, 930–937.

  76. Wright, N., Zahirovic, S., Müller, R. D., & Seton, M. (2013). Towards community-driven paleogeographic reconstructions: Integrating open-access paleogeographic and paleobiology data with plate tectonics. Biogeosciences, 10, 1529–1541.

  77. Zakharov, Y. D., Shigeta, Y., Popov, A. M., Velivetskaya, T. A., & Afanasyeva, T. B. (2011). Cretaceous climatic oscillations in the Bering area (Alaska and Koryak Upland): Isotopic and palaeontological evidence. Sedimentary Geology, 235, 122–131.

  78. Zakharov, Y., Shigeta, Y., Smyshlyaeva, O., Popov, A., & Ignatiev, A. (2006). Relationship between δ13C and δ18O values of the Recent Nautilus and brachiopod shells in the wild and the problem of reconstruction of fossil cephalopod habitat. Geosciences Journal, 10, 331–345.

  79. Zakharov, Y. D., Smyshlyaeva, O. P., Tanabe, K., Shigeta, Y., Maeda, H., Ignatiev, A. V., et al. (2005). Seasonal temperature fluctuations in the high northern latitudes during the Cretaceous Period: isotopic evidence from Albian and Coniacian shallow-water invertebrates of the Talovka River Basin, Koryak Upland, Russian Far East. Cretaceous Research, 26, 113–132.

  80. Zumholz, K., Hansteen, T. H., Klügel, A., & Piatkowski, U. (2006). Food effects on statolith composition of the common cuttlefish (Sepia officinalis). Marine Biology, 150, 237–244.

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Acknowledgements

I would like to thank G.L. Wolfe, R. Hoffmann, S.E. Peters, J.L. Schnell, B.B. Sageman, and A.C. Denny for discussion of this project and the model. I am also indebted to Neil Landman and Alexander Lukeneder for their thoughtful reviews of this manuscript. This project was partially supported by the University of Wisconsin—Madison Department of Geoscience through teaching assistantships and by a postdoctoral fellowship through the Ubben fund at Northwestern University. The code for this model is available as a supplemental file.

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Linzmeier, B.J. Refining the interpretation of oxygen isotope variability in free-swimming organisms. Swiss J Palaeontol 138, 109–121 (2019). https://doi.org/10.1007/s13358-019-00187-3

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Keywords

  • Modeling
  • Stable isotopes
  • Sclerochronology
  • Seasonality
  • Growth rates