Demersal habitat of Late Cretaceous ammonoids: Evidence from oxygen isotopes for the Campanian (Late Cretaceous) northwestern Pacific thermal structure Kazuyoshi Moriya Department of Earth and Planetary Science, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
Hiroshi Nishi Department of Earth Science, Graduate School of Social and Cultural Studies, Kyushu University, 4-2-1 Ropponmatsu, Chuo-ku, Fukuoka 810-8560, Japan
Hodaka Kawahata National Institute of Advanced Industrial Science and Technology, 1-1-1 Higashi, Tsukuba, Ibaraki 3058567, Japan, and Department of Geoenvironmental Science, Graduate School of Science, Tohoku University, Sendai 980-8578, Japan Kazushige Tanabe Department of Earth and Planetary Science, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Yokichi Takayanagi Department of Geoenvironmental Science, Graduate School of Science, Tohoku University, Sendai 9808578, Japan ABSTRACT Comparison of oxygen isotope data for exceptionally well preserved cooccurring plankton and benthos from the Campanian of Hokkaido, Japan, with nine species of ammonoids clearly indicates the demersal (nektobenthic) habitat of ammonoids; unlike Nautilus, the ammonoids studied did not engage in significant short-term vertical migrations in the water column. The new foraminiferal isotopic data suggest that sea-surface and sea-bottom temperatures were ;26 and 18 8C, respectively, at 408N in the Campanian northwestern Pacific. The temperatures were significantly warmer than those in the modern northwest Pacific. This finding provides the first reliable evidence for the warm Late Cretaceous mid-latitude North Pacific. Isotopic analyses of ammonoids show that the average calcification temperature of all ammonoid shells analyzed was ;19 8C, comparable to those of cooccurring benthos. None of these ammonoids display calcification temperatures equivalent to those of planktonic foraminifers. Keywords: Campanian (Cretaceous), foraminifers, mollusks, stable isotopes, paleotemperatures, ammonoid habitats. INTRODUCTION Since their first appearance in the middle Paleozoic, ammonoids, a group of cephalopod mollusks with an external chambered shell, became an extraordinarily diverse group of marine mollusks. During their long evolutionary history, they underwent three major extinction events and faunal turnovers, in the end Devonian, the end Permian, and the end Triassic, and the terminal extinction event in the end Cretaceous (House, 1988). Moreover, their diversity changes through geologic time are well correlated with Earth’s environmental changes, such as diversity increasing with high sea-level periods and decreasing with oceanic anoxic events (Hallam, 1987; Wiedman and Kullumann, 1996). In order to analyze a relationship between paleoenvironment and evolution of ammonoids, it is very important to clarify the habitats and mode of life of various genera. Analyses of body density (Jacobs and Chamberlain, 1996) and theoretical morphological considerations of shell growth (Okamoto, 1996) show that ammonoids were able to maintain neutral buoyancy. However, despite a vast amount of published data, their exact habitat, especially vertical distribution within a water column, is still under debate (Ebel, 1983; Kase et al., 1994; Westermann, 1996). Here we employ stable isotopic analysis to provide direct and quantitative evidence for Cretaceous ammonoid habitats. We establish a vertical temperature scale for the Campanian epicontinental sea in
the northwestern Pacific by evaluation of the surface- and bottom-water temperatures on the basis of oxygen isotope measurements of skeletal remains of planktonic foraminifers and benthic organisms (foraminifers, bivalves, and gastropods), respectively. Then, the water temperatures estimated from oxygen isotope compositions of ammonoid shells are compared with this temperature scale to evaluate the ammonoid depth habitat. Those ammonoid habitats are tested by analogy of isotope records of modern Nautilus shell. Our results are consistent with a demersal habitat of ammonoids, a finding that has important implications for Paleozoic and Mesozoic paleoceanography. MATERIALS AND METHODS The Cretaceous Yezo Group, a sequence of fully marine strata, is widely distributed in the Haboro area of northwestern Hokkaido, Japan (458N, 1428E). The Campanian strata of the group are composed of impermeable mudstone, and yield extraordinarily well preserved microfossils and megafossils. Benthic foraminiferal assemblages and lithofacies indicate that the depositional environment of these strata corresponds to the outer shelf or upper slope (300–350 m depth; Kaiho et al., 1993). The sedimentation rate of these strata was 36 cm/k.y. Microfossil and megafossil samples analyzed in this study were extracted from impermeable mudstone and calcareous concretions, respectively. For oxygen isotope analysis, the ammonoid, benthic bivalve, and gastropod samples (each of which was usually ,100 mg) were prepared by powdering under a binocular microscope using a dental drill 0.3 mm in diameter. Samples of different growth stages were milled only from the nacreous layer along the growth direction (Fig. 1A). The sampling intervals were ;2–5 mm. We picked only specimens of a certain size; the range from sieved fractions for each planktonic foraminifers is as follows: Archaeoglobigerina blowi (33 individuals; 125– 200 mm maximum linear dimension), A. cretacea (36; 125–200 mm), Globotruncana arca (26; 125–200 mm), and G. linneiana (17; 400– 600 mm). Analyses for benthic foraminiferal samples were carried out by using samples containing 2–11 individuals. Oxygen isotope analyses were performed by a mass spectrometer (Optima) with an automated carbonate device at the Institute for Marine Resources and Environment, National Institute of Advanced Industrial Science and Technology, Japan. The instrumental precision was 0.05‰ and 0.08‰ for d13C and d18O, respectively, based on standard deviations over five replicate analyses. Paleotemperatures were calculated by using the equations of Erez and Luz (1983) and Grossman and Ku (1986) for calcite and aragonite, respectively. Ocean water is
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microfossils and megafossils. Scanning electron microscopy (SEM) demonstrated that the nacreous layers of all aragonitic mollusks showed no sign of dissolution of shell material or overgrowths (Fig. 1C). The aragonite content of these specimens was .96 wt% on the basis of semiquantitative X-ray diffraction (XRD) analysis (Fig. DR11), which suggests that the original d18O values should be well preserved (cf. Anderson et al., 1994). Likewise, SEM and electron-microprobe analysis showed that benthic and planktonic foraminifera used in this analysis were well preserved (Fig. 1D; Fig. DR2 [see footnote 1]). Foraminifera were glassy in appearance (Fig. 1B) with empty chambers and primary calcite shell structure (Fig. 1D). Thus, isotope data are produced from exceptionally well preserved metastable substrate (aragonite) and glassy foraminiferers from the same sediments.
Figure 1. Textural and visual preservation of microfossils and megafossils. A: Photograph of Gaudryceras tenuiliratum (Gt6) analyzed in this study. Dotted lines show sampling positions. Scale bar represents 2 cm. B: Reflected optical micrograph of ‘‘glassy’’ preserved Globotruncana linneiana. Scale bar represents 100 mm. C: Scanning electron micrograph (SEM) of nacreous layer of Eupachydiscus sp. (ammonoid). Scale bar represents 2 mm. D: SEM of shell fragment of Archaeoglobigerina blowi (planktonic foraminifera). Scale bar represents 10 mm.
assumed to be 21.0‰ (relative to SMOW [standard mean ocean water]) for a nonglacial world (Shackleton and Kennett, 1975). RESULTS AND DISCUSSION Preservation of Calcitic Microfossils and Aragonitic Megafossils To eliminate significant bias due to diagenetic alteration in stable isotopic analyses, we carefully selected unaltered samples of all the
Vertical Thermal Structure of the Campanian Northwestern Pacific Considering paleobiogeographic distribution of globular and keeled morphotypes of planktonic foraminifers (Leckie, 1987) and the average d18O and d13C ranking among the assemblages analyzed (Table DR1 [see footnote 1]; Huber et al., 1995), it is inferred that Archaeoglobigerina inhabited surface waters, and Globotruncana dwelt deeper than Archaeoglobigerina. The calculated sea-surface temperature (SST) from A. blowi and A. cretacea was 26 8C, whereas cooccurring planktonic G. linneiana and G. arca yielded slightly cooler paleotemperatures of 25 8C (Fig. 2). Analyses of benthic foraminifers from the same samples suggest that temperatures at ;350 m water depth were ;18 8C, comparable to the average temperatures of 17 and 21 8C calculated from analyses of associated bivalve and gastropod mollusks, respec1GSA Data Repository item 2003015, Table DR1, Taxonomic positions, oxygen isotope compositions, and calculated (paleo)temperatures, Table DR2, Summary of data used in Figure 3, Figure DR1, Calibration curve for estimation of aragonite content showing weight percent aragonite, and Figure DR2, FeO and MnO contents of the foraminiferal shell wall and fibrous calcite filling in the chambers, is available from Documents Secretary, GSA, P.O. Box 9140, Boulder, CO 80301-9140,
[email protected], or at www.geosociety.org/ pubs/ft2003.htm.
Figure 2. Calculated temperatures of analyzed specimens compared with original oxygen isotopes. Each linked point in A and B represents data obtained from individual specimen along growth direction, whereas isolated points in A for specimen 1 of Acila hokkaidoensis represent data from bulk sample analyses within single specimens. Left side of series of linked points represents later ontogenetic stage in each plot. VPDB—Vienna Peedee belemnite. A: Planktonic foraminifers and benthic organisms (bivalves, gastropods, and foraminifers). B: Ammonoids. Abbreviations: Ah—A. hokkaidoensis; Msp— Margarites sp.; Gsp—Gyroidinoides sp.; Lspp— Lenticulina spp.; Na— Nodogenerina alexanderi; Ab—Archaeoglobigerina blowi; Ac—A. cretacea; Ga—Globotruncana arca; Gl—G. linneiana; Hs— Hypophylloceras subramosum; Pe—Phyllopachyceras ezoense; Tg—Tetragonites glabrus; Gt—Gaudryceras tenuiliratum; Dd—Damesites damesi; Ha—Hauericeras angustum; Yi—Yokoyamaoceras ishikawai; Esp—Eupachydiscus sp.; Pp—Polyptychoceras pseudogaultinum. 168
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Figure 3. Reconstruction of latitudinal thermal gradients for early Campanian based on averaged oxygen isotope records of planktonic and benthic organisms. Southern Hemisphere: Ocean Drilling Program and Deep Sea Drilling Project sites. Northern Hemisphere: this study. Solid symbols: original calculated paleotemperatures. Open symbols: paleotemperatures adjusted for present-day latitudinal changes in surface salinity by using correction of Zachos et al. (1994). If meridional salinity gradient of sea-surface water (Zachos et al., 1994) is taken into consideration, calculated sea-surface temperature in Haboro area (northwestern Hokkaido, Japan) should be increased by ~1.7 8C. Original data are from Douglas and Savin (1973) for Site 305, from Douglas and Savin (1975) for Site 167, and from Huber et al. (1995) for Site 511. (For summary of data, see footnote 1 in text.)
tively. The seasonal temperature range of bottom water estimated from the ontogenetically sequential d18O range of samples Ah3 and Msp3 (for sample abbreviations, see Fig. 2), both of which were recovered from a single concretion, was 6 8C. On the basis of geological evi-
dence, the Haboro area was an open outer neritic sea in the Campanian, and there has been no evidence for enhanced local evaporation and/or strong river input. Therefore, the obtained stable isotopic results are probably not biased by local changes in the d18O of seawater compared to the nearby open ocean. Although the paleolatitude of Hokkaido was ;408N (cf. Kodama et al., 2000), our estimated temperatures correspond with those off modern Taiwan (258N). Because water temperatures at the outer shelf environment in the modern present northwestern mid-latitude Pacific are gradually decreasing from the sea surface to sea bottom without a thermocline, it is supposed that water temperatures in the Haboro area also showed a gentle gradient. Our results are distinctly higher than those reported previously from the Ocean Drilling Program (ODP) and Deep Sea Drilling Project (DSDP) samples of early Campanian age (Fig. 3). We attribute the difference between our results and those of previous studies in the tropics to the excellent fossil preservation in our material, whereas Pearson et al. (2001) showed that samples from an open-ocean site may contain subtle alteration. Our interpretation is supported by the paleo-SST estimate of 30–31 8C from ‘‘glassy’’ preserved planktonic foraminifers obtained in the Atlantic (Norris and Wilson, 1998). These results provide the first reliable evidence for a warm Late Cretaceous mid-latitude North Pacific. Mode of Life and Habitat of Late Cretaceous Ammonoids versus Holocene Nautilus Strikingly, the calculated temperatures of all the ammonoids analyzed, with different shell morphologies, showed no marked difference (Fig. 2) and are broadly similar to those of contemporaneous benthic organisms (Fig. 4A). There is a large range in calculated temperatures within a given specimen (3–5 8C), and even in the same species, the median values of different specimens do not coincide, as typically seen in samples Hs1 and Hs2, or Pp1 and Pp2 (Fig. 4A). However, ammonoid specimens extracted from a single concretion show almost the same temperatures regardless of their taxonomic relationship, such as Hs2 and Esp2, or Tg, Yi1, and Esp1, whereas specimens collected from different concretions show different temperatures. Because each concretion was embedded at a slightly different strati-
Figure 4. Plots showing calcification temperature distributions of analyzed specimens. A: Planktonic foraminifers, benthic organisms (bivalves, gastropods, and foraminifers) and ammonoids. For ammonoids, calculated temperatures of each specimen are individually plotted, whereas those of all specimens are grouped for bivalves, gastropods, and foraminifers (Acila hokkaidoensis, Margarites sp., and BF—benthic and PF—planktonic foraminifers). Refer to Figure 2 for other abbreviations. B: Modern Nautilus pompilius from Tan˜on Straits, Philippines. Calcification temperatures are calculated based on Oba et al. (1992). Depth distribution vs. water temperatures is from Hayasaka et al. (1982). GEOLOGY, February 2003
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graphic positions within a 30 m stratigraphic interval, this variation in median values may represent temperature fluctuations of ocean water during thousands of years rather than ecological or environmental factors. The similarity of shell microstructure between modern Nautilus and Cretaceous ammonoids suggests that the outer shell of ammonoids might have grown continuously, as seen in modern Nautilus. Temperatures estimated from the septal d18O values of modern N. pompilius that we have analyzed were almost constant throughout the posthatching ontogeny and averaged 20 8C, corresponding to 140 m depth (Fig. 4B; Hayasaka et al., 1982). Because it takes ;70 days to complete a single septum during the submature stage (Ward, 1987), and lowoxygen stagnant water prevents N. pompilius from inhabiting levels deeper than 150 m depth in the Tan˜on Straits (Hayasaka et al., 1982), the constant temperatures estimated from the septal d18O values in the posthatching stage of N. pompilius may represent the temperature of their optimum habitat depth. In contrast, the temperatures calculated from the outer shell wall of N. pompilius, based on a sampling procedure almost identical to that adopted for ammonoids, fluctuate between 21 and 26 8C, corresponding to the temperatures at 140 and 60 m depths, respectively (Fig. 4B; Hayasaka et al., 1982). Because the sampling width on the N. pompilius shell, ,500 mm, corresponds to a growth increment of less than 2 days (Landman and Cochran, 1987), these temperature fluctuations may represent a short-term vertical migration of the individual, as has been evidenced by remote telemetry analysis of living animals (Ward et al., 1984). The general similarity between the paleotemperature estimates for all the ammonoids in our study and coexisting benthic mollusks and foraminifers suggests that these ammonoid species lived near the seafloor. There is no evidence that the ammonoids underwent a large vertical migration into the surface ocean, because none of them display any isotopic evidence for temperatures close to the SSTs recorded by cooccurring planktonic foraminifers. Indeed, we assume from the analogy of oxygen isotope records of N. pompilius that the sampling width and intervals of ammonoid shells adopted in this study are fine enough to detect whether the ammonoid animals did a short-term vertical migration. However, temperature fluctuations within a given specimen seem to reflect seasonal changes in temperature at ;350 m water depth, because the range, ,5 8C, almost corresponds to those of other benthic mollusks (bivalves and gastropods), 6 8C, and never beyond the total range of benthos. However, another possibility is that these ammonoids undertook near-bottom migration from offshore to onshore habitats, as seen in modern codfish. CONCLUDING REMARKS In previous studies on Cretaceous paleoceanography, ammonoids have been assumed to be planktonic or nektonic organisms (Pirrie and Marshall, 1990; Price et al., 1996). However, as shown in this study, we need to carefully establish the ecology of ancient organisms based not only on uniformitarian considerations and functional morphology, but also on physicochemical properties. The demersal mode of life may not necessarily be shared by all ammonoids with different evolutionary histories. For example, oxygen isotope analysis suggests that Late Jurassic stephanoceratoid ammonites, which became extinct in the end Jurassic, seem to have had a planktonic or nektonic mode of life (Anderson et al., 1994). Therefore, it could be hypothesized that a faunal turnover of ammonoids such as extinction and subsequent diversification was achieved not only by evolution of physiological tolerance of ambient conditions, but also by loss of habitat followed by acquisition of a new habitat and/or a new mode of life.
was partly supported by the Sasakawa Scientific Research Grant from the Japan Science Society.
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ACKNOWLEDGMENTS
Manuscript received 19 July 2002 Revised manuscript received 17 October 2002 Manuscript accepted 21 October 2002
We thank R.D. Norris and K. Endo for critical reading of the manuscript. N.H. Landman and P.A. Wilson reviewed the manuscript and gave fruitful comments. This study
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