Ammonite habitat revealed via isotopic composition planktonic organisms

Ammonite habitat revealed via isotopic composition
and comparisons with co-occurring benthic and
planktonic organisms
Jocelyn Anne Sessaa,1, Ekaterina Larinaa,b,c, Katja Knolla,b, Matthew Garbb, J. Kirk Cochrand, Brian T. Hubere,
Kenneth G. MacLeodf, and Neil H. Landmana
a
Division of Paleontology, American Museum of Natural History, New York, NY 10024; bDepartment of Earth and Environmental Sciences, Brooklyn College,
Brooklyn, NY 11210; cDepartment of Earth Sciences, University of Southern California, Los Angeles, CA 90018; dSchool of Marine and Atmospheric
Sciences, Stony Brook University, Stony Brook, NY 11794; eDepartment of Paleobiology, National Museum of Natural History, Washington, DC 20013; and
f
Department of Geological Sciences, University of Missouri, Columbia, MO 65211
|
paleoecology mollusk
habitat reconstruction
mass extinction (8), died out, whereas their relatives the nautiloids
survived (9), have been used to understand the selectivity of marine
microfossil groups across the K–Pg event (10), highlighting the
importance of ammonites in understanding extinction mechanisms.
Despite the utility of ammonites to many disciplines, their ecology remains poorly known. A challenge in reconstructing their
habitat(s) is establishing if ammonites lived at the site from which
they are recovered. Ammonite tissues could drop out after death,
and the shell might float to the surface buoyed by relict air contained within the phragmocone (11). Empty shells of Nautilus are
found on beaches at remote distances from their actual habitat,
documenting the potential for postmortem drift of positively
buoyant shells (12). Similarly, Tanabe (13) mapped the distribution
of Turonian ammonites along an onshore–offshore transect, and
noted that their postmortem distribution was broader than the
settings they inhabited during life. Uncertainty in ammonites’ preferred habitat is especially concerning for temperature reconstructions based on their occurrence or isotopes because temperature
varies both with depth and with distance to the shoreline.
A variety of studies have attempted to determine the ecology
of ammonites based on analogies with living relatives, shell
morphology, facies distribution, faunal associations, and isotopic
composition. However, these studies have had limited success for
| Late Maastrichtian | ammonite |
Significance
Because ammonites are one of the most diverse, abundant, and
well-preserved clades in the history of life, they are a mainstay in
macroevolutionary and biodiversity studies; however, their ecologies are poorly understood, and it is unknown whether taxa
lived near the sea surface or seafloor. This uncertainty undermines their use in paleoecological and paleoenvironmental reconstructions, which depend on knowledge of organisms’ depth
preferences. Here, we use a rare co-occurrence of exquisitely wellpreserved ammonites and planktonic and benthic organisms to
constrain depth preferences of three common ammonite families
by comparing the oxygen and carbon isotopic signatures of these
taxa. The ammonites fall into two distinct depth habitats, enhancing the utility of these families for highly refined paleoecological and paleoclimatic studies.
A
mmonites have constituted a primary data source for the
fields of evolution, paleoceanography, biostratigraphy, and
paleoecology for more than a century; their ubiquity, diversity,
occurrence in a wide variety of marine environments, and readily
preservable shell account for their utility in both paleontological
and geological studies. Ammonites have been used extensively in
studies of heterochrony because their shells preserve distinct ontogenetic changes that can be tracked in evolving lineages (1, 2);
they are valued in paleoceanographic research because, like most
mollusks, they are inferred to have precipitated their aragonitic
shells in isotopic equilibrium with the surrounding seawater (3, 4).
Thus, shell chemistry may record temperature, via oxygen isotopes
(δ18O) (5), and water mass properties, such as strontium isotopes
(87Sr/86Sr), which are used to estimate numerical age (6). Ammonites are also a textbook example of an index fossil; besides
being abundant and widespread, they evolved rapidly, making them
the dominant Mesozoic tool for relative dating and correlation of
shallow water strata. For example, the 35-My-long stratigraphic
record of Upper Cretaceous deposits in the US Western Interior
Seaway (WIS) has been partitioned into 66 ammonite zones (7).
Finally, ammonites underwent a spectacular extinction at the close
of the Mesozoic. Explanations for why the ammonites, which were
flourishing immediately before the Cretaceous–Paleogene (K–Pg)
www.pnas.org/cgi/doi/10.1073/pnas.1507554112
Author contributions: J.A.S., E.L., and N.H.L. designed research; J.A.S., E.L., K.K., M.G., B.T.H.,
K.G.M., and N.H.L. performed research; J.A.S., K.K., J.K.C., B.T.H., K.G.M., and N.H.L. analyzed
data; and J.A.S., J.K.C., B.T.H., K.G.M., and N.H.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. R.M.L. is a guest editor invited by the Editorial
Board.
Freely available online through the PNAS open access option.
1
To whom correspondence should be addressed. Email: [email protected].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1507554112/-/DCSupplemental.
PNAS Early Edition | 1 of 6
ECOLOGY
Ammonites are among the best-known fossils of the Phanerozoic, yet
their habitat is poorly understood. Three common ammonite families
(Baculitidae, Scaphitidae, and Sphenodiscidae) co-occur with wellpreserved planktonic and benthic organisms at the type locality of
the upper Maastrichtian Owl Creek Formation, offering an excellent
opportunity to constrain their depth habitats through isotopic
comparisons among taxa. Based on sedimentary evidence and the
micro- and macrofauna at this site, we infer that the 9-m-thick
sequence was deposited at a paleodepth of 70–150 m. Taxa present
throughout the sequence include a diverse assemblage of ammonites, bivalves, and gastropods, abundant benthic foraminifera, and
rare planktonic foraminifera. No stratigraphic trends are observed
in the isotopic data of any taxon, and thus all of the data from each
taxon are considered as replicates. Oxygen isotope-based temperature estimates from the baculites and scaphites overlap with those of
the benthos and are distinct from those of the plankton. In contrast,
sphenodiscid temperature estimates span a range that includes estimates of the planktonic foraminifera and of the warmer half of the
benthic values. These results suggest baculites and scaphites lived
close to the seafloor, whereas sphenodiscids sometimes inhabited
the upper water column and/or lived closer to shore. In fact, the rarity
and poorer preservation of the sphenodiscids relative to the baculites
and scaphites suggests that the sphenodiscid shells may have only
reached the Owl Creek locality by drifting seaward after death.
EARTH, ATMOSPHERIC,
AND PLANETARY SCIENCES
Edited by R. Mark Leckie, University of Massachusetts, Amherst, MA, and accepted by the Editorial Board October 9, 2015 (received for review April 23, 2015)
both biological and geological reasons. Ammonites are extinct, and
their closest living relatives, the octopods, squids, cuttlefish, and
Nautilus, are all in different orders/subclasses (14). Even among
living cephalopods, a variety of behaviors are observed, including
vertical and lateral migrations (15). Other studies have sought to
reconstruct ammonite habitat by comparing the isotopes recorded
in their shells to those of co-occurring, or nearly co-occurring, taxa
of known depth habitats. A powerful approach in theory, these
studies have been limited in practice because ammonites are only
rarely recovered with the planktonic and benthic organisms needed
to establish a temperature-depth profile. Further, many studies
were undertaken in the WIS, where the water mass properties are
poorly understood and controversial (16, 17). We expand upon
previous isotopic studies by using exceptionally well-preserved
ammonites from the Owl Creek Formation (fm.) type locality in
northern Mississippi (Fig. S1). Ammonites are abundant at this
site and co-occur with bivalves, gastropods, and planktonic and
benthic foraminifera (Fig. 1 and Fig. S2), thus providing an
excellent opportunity to reconstruct a water column profile and
establish where the ammonites fall within it.
Results and Discussion
A total of 553 mollusk specimens were scored for taphonomic
features (SI Methods); of these, 405 specimens were evaluated
for isotopic analysis: 196 were found to be well preserved, and
subsequent analyses resulted in 234 isotopic measurements
(Table 1; SI Methods). Well-preserved foraminifera (116 planktonic and 72 benthic foraminifera) were picked and resulted in
isotopic measurements for 11 planktonic and 14 benthic separates
(Table 1); an additional 398 planktonic and 953 benthic foraminifera were counted to constrain depth estimates (Table S1).
Determining Whether Ammonites Experienced Postmortem Drift. Whole
specimens of baculites, scaphites, bivalves, and gastropods are
common and display low degrees of fragmentation, implying that
these groups experienced similar taphonomic histories (SI Methods).
The sphenodiscids, however, are highly fragmented; only 1 of the
11 collected specimens was more than 50% complete. Epizoans are
rare, occurring on less than 3% of specimens in each mollusk group
except for the sphenodiscids, where 27% (3 of 11 specimens) bear
serpulid worm tubes or encrusting bryozoans. In both baculites and
scaphites, delicate features, such as tubercles and the apertural margin, are frequently observed (Fig. 1). Tubercles on some sphenodiscid
shells are worn, and the apertural margin is always missing.
Adult scaphites can be differentiated from juveniles by shell shape
and size, and adult males and females can be identified (18) (Fig. 1).
For specimens where sex can be determined, 44% are males, 52%
are females, and 4% are juveniles. These proportions are representative of a living community (19) and not of an egg-laying habitat
transiently occupied by females (20). Predation indicators, such as
Fig. 1. Representative mollusks from the Owl Creek fm. (A) Left lateral and ventral views of a Discoscaphites iris macroconch AMNH 91329; (B) right lateral
and ventral views of a D. iris microconch AMNH 91335; (C) right lateral view of D. iris, showing a healed injury AMNH 77461; (D) ventral and right lateral views
of Eubaculites latecarinatus AMNH 91330; (E) ventral and right lateral views of Eubaculites carinatus AMNH 91334; (F) left lateral view of Sphenodiscus
pleurisepta; sutures are visible because most of the shell is missing AMNH 91520; (G) Gyrodes crenata AMNH 91333; (H) Nucula percrassa AMNH 91331.
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Sessa et al.
Table 1. Total number of well-preserved specimens of each taxon, number of measurements made from these specimens, average
carbon and oxygen isotopic composition and temperature, and temperature range
Baculites
Total
no. specimens
Total
no. measurements
Mean δ13C
Mean δ18O
Mean
temperature, °C
Mean
temperature, °C
Range in
temperature, °C
Scaphites
Sphenos
Infaunal
bivalves
Gastros
Epifaunal
oysters
Benthic foraminifera
Lingulogav. sp.
Gavelinella sp.
Planktonic foraminifera
P. globulosa
R. rugosa
65
67
7
22
32
3
33
39
84
32
89
78
8
22
33
4
5
9
6
4
−1.4
−0.6
18.1
0.4
−0.7
18.4
−3.9
−1.6
22.1
1.6
−1.0
19.5
1.7
−0.8
18.8
1.8
−1.7
18.9
0.8
−1.9
19.8
0.9
−1.8
19.8
1.6
−3.2
26
1.8
−3.3
26.4
18.1
18.4
22.1
Benthos
19.1
Plankton
26.2
8.4
6
9
4.4
—
For the mollusks, multiple measurements were made on some specimens. For the foraminifera, individual specimens were combined to achieve the weight
needed for isotopic analysis. Temperatures are calculated using the equations given in SI Methods. The range in temperature is calculated as the difference
between the means of the 10% warmest and 10% coolest values of each taxon, except for Sphenodiscus, where the maximum and minimum values were used
because of the small number of measurements. Benthos includes infaunal bivalves, gastropods, epifaunal oysters, and benthic foraminifera. Sphenos,
Sphenodiscus; Gastros, Gastropods; Lingulogav., Lingulogavelinella; P. globulosa, Planoheterohelix globulosa; R. rugosa, Rugoglobigerina rugosa.
healed injuries, are present on 5% of scaphite specimens (Fig. 1); a
similar incidence of predation as observed in other scaphite accumulations interpreted as in situ (21). Although it is more challenging
to determine sex in baculites than in scaphites, for those baculite
specimens where this assignment could be made, the proportion of
males and females is equal. In contrast, little can be inferred about
the sphenodiscid’s population structure; only adults were recovered,
and none could be assigned a sex because they were too incomplete.
Sphendosicids are also an outlier in terms of abundance. Although we did not count specimens from bulk samples, the number
of specimens in Table 1 reflects the general ammonite abundance.
Baculites and scaphites occur at roughly equal frequency, and
sphenodiscids are rare. Note that the relatively low numbers of bivalves and gastropods in Table 1 reflects our bias toward collecting
ammonites. In a synthesis of ammonites from the Owl Creek fm.,
Kennedy and Cobban (22) report relative abundances that are
consistent with our findings. The authors (22) studied four specimens of Sphenodiscus pleurisepta, noting that all were crushed to
varying degrees, one of which exhibits abraded tubercles (SI Methods), 80 Eubaculites carinatus specimens, and 140 Discoscaphites iris
specimens. In summary, preservational features and population
characteristics suggest that, like the bivalves and gastropods, the
baculites and scaphites experienced little postmortem transport;
they were living at or very near the studied site at the time of death.
In stark contrast, the rarity, poor preservation, and recovery of only
adult sphenodiscids indicate that these specimens could have experienced postmortem drift.
Environmental Reconstruction. In a study of modern foraminifera
along the North American Atlantic coastal margin, Gibson (23)
found that the ratio of planktonic to benthic foraminifera is strongly
correlated with depth, and this study has formed the basis for an
extensive body of work estimating depth in modern and ancient
settings via these proportions. The proportion of benthic foraminifera in the Owl Creek fm. ranges between 61% and 77% (Table
S1). In the Gibson (23) dataset, the minimum recorded depth for
assemblages with <80% benthics is 70 m, and for those with <50%
benthics is 100 m. Assemblages with these proportions were largely
found between 100 and 200 m, but some were recovered as deep as
1,000 m (23). An Owl Creek paleodepth of greater than 200 m is
Sessa et al.
highly unlikely. The Owl Creek fm. is composed of dark gray
glauconitic micaceous clayey silts to very fine quartz sands, interpreted to represent a fully marine prodelta shelf (24, 25) that
interfingers with shallow water chalks and sands (26). The absence
of sedimentary structures, with the exception of two beds with
centimeter-scale parallel laminations (at 5.2–5.4 m and 6–7 m),
suggest extensive bioturbation (SI Methods).
Comparison with the upper Maastrichtian deposits from Brazos
River (Rv.), TX, suggests that the Owl Creek section was shallower. Benthics comprise between 10% and 25% of the Brazos
Rv. foraminiferal assemblage (27), which translates to estimates
∼150–250 m in the Gibson (23) dataset. Ashckenazi-Polivoda
et al. (28), using the same taxa (Gavelinella sp., Globoheterohelix
globulosa, and Rugoglobigerina rugosa) as in our study, report
benthic foraminifera temperatures that are ∼2.5 °C cooler, and a
difference between planktonic and benthic values that is ∼2 °C
greater, at Brazos Rv. than at the Owl Creek site. If these faunal
and geochemical differences reflect changes in depth, then the
Owl Creek site was shallower than Brazos Rv. The macrofauna at
these sites corroborates this depth relationship. Sessa et al. (29)
categorized late Mesozoic Gulf Coastal Plain benthic mollusk
faunas as shallow subtidal or offshore. The Owl Creek taxa and
their abundance are transitional between these two settings,
with components of both shallow subtidal assemblages (naticids,
veneroids, crassatellids, and turritellids) and those of the offshore (ostreoids and pectinoids), whereas the Brazos Rv. fauna
comprises most of the offshore samples in Sessa et al. (29). Considered as a whole, a conservative estimate of the paleodepth
of the Owl Creek fm. is 70–150 m, with 100 m being likely.
The δ13C data are consistent with this conclusion, as discussed below.
Interpreting Oxygen Isotopes and Paleotemperatures. No stratigraphic
trends are observed in the isotopic data for any taxonomic group
(Fig. 2), and, therefore, all of the data from each taxon are considered as replicate samples. The analyzed planktonic foraminifera
species, Planoheterohelix globulosa and Rugoglobigerina rugosa,
display similar oxygen isotopic values (Table 1), yielding similar
temperature estimates (∼26 °C; Fig. 2). These taxa have been
interpreted as surface-to-subsurface mixed layer and/or near shore
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EARTH, ATMOSPHERIC,
AND PLANETARY SCIENCES
Ammonites
Calcitic taxa
ECOLOGY
Aragonitic taxa
A
30
Planktonic Foraminifera (c)
Benthic Foraminifera (c)
Gastropods
Sphenodiscidae
Epifaunal Bivalves (c)
Infaunal Bivalves
Baculitidae
Scaphitidae
Temp (°C)
25
20
15
10
B
4
3
2
δ13 C
1
0
-1
-2
-3
-4
-5
-6
0
8 0
8 0
8 0
meters
80
8
Fig. 2. (A) Temperature estimates and (B) carbon isotopic composition for all
taxa arranged by meter level. “(c)” indicates those taxa that secrete a calcitic shell
or test; all other taxa secrete aragonitic shells. The stratigraphic scale is plotted
along the horizontal axis (0–8 m) and is repeated for each taxonomic group. No
stratigraphic trends are apparent for any taxon; the horizontal axis of the
sphenodiscids is therefore compressed for visual ease. The baculites and scaphites
have similar temperatures as the benthic taxa, whereas the sphenodiscids encompass both planktonic temperatures and the warmer portion of the benthic
temperature distribution. The δ13C values of the planktonic foraminifera and of
the benthic foraminifera are consistent with the variation in δ13CDIC expected
with depth. The δ13C values of the ammonites likely reflect physiological processes, and the consistent offset among the baculites, scaphites, and sphenodiscids suggests differences in diet and/or lateral and depth differences in habitat.
dwellers, and, though they can exhibit distinct isotopic signatures
in open ocean settings, the variability in the inferred ecology of
P. globulosa is considerable (28, 30). For the Owl Creek specimens,
isotopic overlap likely results from the relatively shallow setting,
with both taxa living in a well-mixed portion of the upper
water column.
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Both benthic foraminifera, Lingulogavelinella sp. and Gavelinella
sp., yield temperature estimates of ∼20 °C (Fig. 2). Based on
analogy with modern gavelinellid taxa, these taxa probably lived at
the sediment-water interface or within the first few centimeters of
the sediment in well-oxygenated environments (31, 32). The calcitic
oysters were also epifaunal, and display δ18O values that are
comparable to those of the benthic foraminifera (Table 1 and Fig.
2). The gastropods and infaunal bivalves have aragonitic shells,
and their δ18O values are similar to one another (Table 1).
Temperature estimates from all benthic taxa are grouped around
19 °C (Fig. 2); they display a normal distribution (skew of −0.0004),
suggesting that these data accurately capture seasonal temperature
fluctuations at the seafloor. The 7 °C temperature difference
between the planktonic foraminifera (26 °C) and the benthic
taxa (19 °C) may represent a seasonal maximum of the surface-tobottom temperature gradient. Because modern planktonic foraminifera usually have spring or summer peaks in abundance (33),
the paleotemperature values reconstructed here may represent
surficial water temperatures of warmer seasons, and the gradient
could have been reduced during winter months. Because the
benthic data are never as warm as planktonic values, however,
finding ammonites with warm temperatures would provide strong
evidence that they inhabited surface waters.
Mean temperature estimates from the baculites and scaphites
are statistically indistinguishable (Kolmogorov–Smirnov test, P =
0.3936), align with benthic estimates, and never approach planktonic estimates (Fig. 2). Baculites and scaphites also display larger
variances than that of the benthos (Fligner–Killeen test of homogeneity of variances P = 0.00004 for baculites vs. benthos; P value
of 0.003 for scaphites vs. benthos) and have asymmetric distributions skewed toward cooler values (baculite skew, −0.4; scaphite
skew, −0.3; Fig. 2 and Table 1). The wider distribution may have
resulted from several interrelated causes; living above the seafloor,
the ammonites may have experienced wider temperature fluctuations than the benthic taxa, and/or they may have had higher
metabolic rates than the benthic taxa, resulting in faster growth
rates and thus recording a less time-averaged temperature signal
than that of the sedentary benthic taxa. The skew toward cool
values may result from preferential shell growth during the winter
months, or from migration to/from deeper (and cooler) water
seasonally or through ontogeny. However, investigations of the
morphology (muscle scars, shell shape) and distribution of Late
Cretaceous scaphites indicate that these animals were limited in
their mobility and may have remained at a single site for an extended period, subject to current activity (34, 35, and references
therein). These possibilities could be explored in future work by
serially sampling the baculites and scaphites throughout ontogeny.
Regardless of the relative importance of these alternatives, the
consistently high δ18O values among baculites and scaphites suggest
that they lived much closer to the seafloor than the sea surface.
Temperature estimates from the sphenodiscids encompass a
broad range (9 °C). The warmest estimates for the sphenodiscids
overlap with planktonic foraminiferal estimates, and their coolest values span the warmer half of the benthic (and baculite and
scaphite) estimates (Fig. 2 and Table 1). Though the small
number of measurements made from their shells prohibits statistical comparisons, it seems apparent that the sphenodiscids
spent at least some portion of their lives in waters warmer than
those where baculites and scaphites lived.
Interpreting Carbon Isotopes. Calcitic foraminifera generally secrete
their tests close to isotopic equilibrium with the dissolved inorganic
carbon (DIC) reservoir (32). The δ13C values of the planktonic
(1.7 ‰) and benthic (0.9‰) foraminifera (Table 1) are consistent
with expected δ13CDIC depth gradients due to photosynthetic
fractionation in the upper water column and remineralization of
sinking organic matter at depth. A 0.8‰ δ13CDIC depth variation
is found in modern settings of ∼100 m depth (36).
Sessa et al.
Sessa et al.
Methods
Geologic Setting and Age. The study section consists of the upper 9 m of the
Owl Creek fm. and 2 m of the overlying Danian Clayton fm. (SI Methods). The
region is tectonically undeformed and was never deeply buried, resulting in
unlithified sediments containing fossils that were not thermally altered (25).
The Owl Creek fm. was assigned to calcareous nannofossil zone CC26b (45),
which provides a conservative estimate that deposition occurred within the
last 1.3 My of the Cretaceous (46).
Specimen Collection. Fossils were collected throughout the lower 8 m of the
Owl Creek fm. (Table 1; SI Methods). Five bulk samples for microfossil study
were collected between 0.5 and 7.5 m above the base of the outcrop (Table
1). From these samples, foraminifera were isolated and concentrated using
standard techniques (SI Methods), counted to determine planktonic:benthic
ratios, and picked for isotopic analyses.
Taphonomy. We tabulated the degree of completeness of each ammonite
specimen, noting delicate, easily broken features such as the phragmocone
and tubercles, the presence of epizoans, the proportion of macroconchs to
microconchs (presumed to be females and males, respectively) (18), the size
and ontogenetic stage of specimens, and any features suggestive of predation (SI Methods). Parallel observations were made for bivalve and gastropod specimens, which do not experience postmortem drift.
Preservation, Isotopic Analysis, and Paleotemperature Determination. Preservation of foraminifera and mollusk shell microstructure was evaluated before
isotopic analysis (Figs. S2 and S3 and SI Methods). Isotopic results are
reported in standard δ-notation and on the Vienna-PDB (VPDB) scale. Fiftyone mollusk specimens (59 measurements; some specimens were sampled
multiple times) were analyzed at the University of South Florida (USF) on a
Delta V Isotope Ratio Mass Spectrometer coupled to a Gasbench II automatic preparation system using standard techniques (SI Methods). Additional analyses of mollusks (155 specimens with 175 measurements,
including 10 specimens also analyzed by USF), and all 25 foraminiferal
analyses were made at the University of Missouri using a Kiel III carbonate
device attached to a Finnigan DeltaPlus Isotope Ratio Mass Spectrometer
(IRMS) using standard techniques (SI Methods). Because some taxa analyzed are calcitic, whereas others are aragonitic, and calcite and aragonite
have different fractionation factors, δ18O values were converted to temperature using well-established formulas for each respective organism (SI Methods). Converting to temperature allows all taxa to be compared on the
same scale.
ACKNOWLEDGMENTS. We thank J. Slattery for a sphenodiscid specimen;
G. Phillips and R. Rovelli for field assistance; property owners A. Carroll and
B. Carroll; American Museum of Natural History (AMNH) Master of Arts in
Teaching 2013 graduates J. DeCosta, L. Hlinka, K. Lapenta, S. McFadden, and
A. Nesheim for data collection; S. Haynes, M. Hill, S. Mahmood, and H. Tobin
for laboratory assistance; Z. Atlas for isotopic analyses; M. Foote, M. Hopkins,
L. Petruny, and M. Tessler for helpful suggestions; E. Thomas for informative discussion; and editor R. Mark Leckie and two anonymous reviewers for constructive comments. Support for this work was provided by a Katherine Davis
Postdoctoral Fellowship at the AMNH and National Science Foundation (NSF)
Grant NSF-DR K-12:1119444; a Lerner–Gray Scholarship (AMNH), a Richard K.
Bambach Scholarship from the Paleontological Society, a James Welsch Scholarship from the Association of Applied Paleontological Sciences, and NSF-GRFP
Grant 2013171808 (to E.L.); and the AMNH Norman Newell Fund.
PNAS Early Edition | 5 of 6
EARTH, ATMOSPHERIC,
AND PLANETARY SCIENCES
Depth Habitats of Adult Baculites, Scaphites, and Sphenodiscids. The
Owl Creek fm. results match previous studies of baculites, scaphites, and sphenodiscids well. Tsujita and Westermann (41)
inferred a lower to middle water habitat for WIS baculites.
Similarly, Henderson and Price (42) interpreted the baculite
Sciponoceras as demersal because its δ18O values aligned with
those from benthic mollusks of the same formation. Tanabe (13)
suggested that scaphites did not occupy nearshore or offshore
settings, but rather lived in an intermediate depth zone, as we infer
for the Owl Creek fm. Landman et al. (8) compiled the global
geographic and facies distributions of Maastrichtian ammonites;
they noted that sphenodiscids were restricted to nearshore facies
(see also ref. 43), which strengthens our hypothesis that the Owl
Creek fm. sphenodiscids lived in a more landward setting and
floated out to the site after death. Moriya et al. (44) compared
the isotopic composition of ammonites with that of bivalves,
gastropods, and planktonic and benthic foraminifera from both
mudstones (the microfossils) and calcareous concretions (the
macrofossils) from throughout the 30-m-thick Yezo Group. A
demersal habitat was suggested for the Ancyloceratina, the
suborder that contains the baculites and scaphites, because
their isotopic values were similar to those of the benthos.
Our comparison of the occurrence, preservation, and stable
isotopic composition of ammonites with that of coexisting benthic and planktonic organisms shows vertical and lateral habitat
separation between the Sphenodiscidae, and the Baculitidae and
Scaphitidae. The baculites and scaphites had similar taphonomic
histories as the bivalves and gastropods, which did not experience postmortem drift, indicating that these ammonites likely
inhabited the study site. Further, δ18O-based temperature estimates for the baculites and scaphites completely overlap with
those of the benthos, but are distinct from those of the plankton,
indicating that they were demersal. The sphenodiscids, however,
are rare and have poorer preservation relative to all of the other
mollusks, implying that the sphenodiscids were transported to
the study site after death. These features, combined with often
low δ18O values (that is, warm, surface water-like temperatures), broad range in δ18O values, and low δ13C values support
the interpretation that these sphenodiscids sometimes lived in
nearshore, perhaps even brackish, waters for some portion of
their life.
This refined model of ammonite habitat sets the stage for highly
detailed coastal-water reconstruction, whereby the sphenodiscids’
isotopic compositions likely reflect nearshore waters, and that of
the baculites and scaphites represents near bottom, marine conditions of the areas in which they are preserved. Combining this improved ecological information with data from planktonic and benthic
foraminifera could be a powerful tool for paleoceanographic and
climate modeling studies. Related is the possibility that the greater
range of temperatures recorded in the baculites and scaphites
compared with the benthic mollusks is due to the ammonites preserving a less time-averaged record, again highlighting the strength of
using ammonite shells as an archive of temperature variation. For
example, in contrast to the well-resolved deep marine climate records from middle to high paleolatitudes near the K–Pg boundary,
temperature reconstructions from shallow marine settings at lower
paleolatitudes are rare. Using ammonites from shelf sections like the
Owl Creek fm. site would enhance our understanding of meridional
climatic conditions just before this event.
ECOLOGY
The δ13C of modern mollusk shells can reflect both the DIC
reservoir and metabolic pathways. Thus, environmental signals
are often overprinted by physiological processes that can change
seasonally and through ontogeny (37). Consistent with this possibility, the scaphites, baculites, and benthic mollusks display
offsets in their δ13C values relative to the δ13CDIC inferred from
analyses of benthic foraminifera. On average, the gastropods and
bivalves have δ13C values that are ∼1‰ higher than the inferred
δ13CDIC (Table 1), as has been found in some modern taxa (38).
The ammonites have δ13C values lower than the other taxa, with
the baculites intermediate between the scaphites and sphenodiscids, suggesting differences in diet and/or position within the
water column. Tobin and Ward (39) also documented lower
average δ13C values in Late Cretaceous ammonites relative to
benthic mollusks; however, these differences may be due to
methane-derived carbon incorporated into the shells (40). The
warm temperature recorded by the sphenodiscids, combined with
low δ13C, supports the notion that these organisms generally lived
close to shore; if they lived in the surface waters of the study site,
they would have been exposed to a higher δ13CDIC, as indicated by
the planktonic foraminifera δ13C. Thus, the marked δ13C differences between sphenodiscids and planktonic foraminifera reinforce
the conclusion of offshore postmortem transport of sphenodiscids
based on taphonomic observations.
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Sessa et al.
COMMENTARY
Evolution of habitat depth in the Jurassic–
Cretaceous ammonoids
Kazuyoshi Moriya1
Department of Earth Sciences, Faculty of Education and Integrated Arts and Sciences,
Waseda University, Shinjuku-ku, Tokyo 169-8050, Japan
Berriasian
Hettangian
Eoderoceratoidea
Sinemurian
Psiloceratoidea
Toarcian
Pliensbachian
Lytoceratoidea
Jurassic
175
Kimmeridgian
Oxfordian
Callovian
Bathonian
Bajocian
Aalenian
Phylloceratoidea
Tithonian
150
(9)
(8)
Turrilitoidea
Deshayesitoidea
(8)
Ancyloderatoidea
Barremian
Hauterivian
Valanginian
Desmoceratoidea
Aptian
Stephanoceratoidea
Albian
Perisphinctoidea
Cenomanian
(5)
Douvilleiceratoidea
(5)
(1) (1)
Scaphitoidea
(5)
Hoplitoidea
(5)
Haploceratoidea
125
Santonian
Coniacian
Turonian
Hildoceratoidea
Spiroceratoidea
Cretaceous
Campanian
Acanthoceratoidea
Phylogeny and evolution of mode of life
of the Jurassic–Cretaceous ammonoids
Stage
Maastrichtian
70
75
100
body fossils and close modern relatives. For
example, although one may usually imagine that
ammonoids were planktic or nektic organisms
within a water column, like the Nautilus, which
is the sole surviving cephalopod bearing an
external chambered shell, there is very little
direct evidence showing the habitat depth of
ammonoids within an ancient water column.
Sessa et al. (1) shed new light on the habitat
depth of the Cretaceous ammonoids using geochemical proxy records. When calcium carbonate, which composes the shell material of many
marine invertebrates, is secreted within the
ocean, the stable oxygen isotopic composition
of the carbonate is predominantly determined
by the ambient ocean temperature. Therefore,
Tetragonitoidea
Ma
Period
Ammonoids, a group of cephalopods with
external chambered shells, arose in the early
Devonian and went extinct at the Cretaceous/
Paleogene (K/Pg) boundary. During their 340million-y history, ammonoids suffered three
major diversity crises at the end of the Devonian,
Permian, and Triassic Periods, and the terminal
extinction event at the K/Pg boundary. Because
of their rapid morphological evolution and rich
fossil record, ammonoids have been used to
determine the relative age of marine strata and
correlation since the dawn of stratigraphy.
Although the morphological analyses of shell
materials have provided some insights into
ontogeny and evolution, their biological nature
is poorly understood because of the lack of soft
(6)
(4)
Planktic or nektic
Demersal
(Bottom dwelling)
Fig. 1. Phylogeny and evolution of mode of life of the Jurassic–Cretaceous ammonoids. Age of each stage boundary
is from Gradstein et al. (16). Phylogeny of ammonoids is cited from Yacobucci (17). Open white circles represent
isotopic results indicating demersal (bottom dwelling) habitat at the age plotted on each lineage. Gray filled circles
indicate planktic or nektic habitat. Numbers at left bottom of each circle represent references for each data. Pink bar,
Phylloceratina (5); orange bar, Lytoceratina (5); yellow bar, Ammonitina; pale green bar, Haploceratina; pale blue,
Perisphinctina (4–6, 8, 9); purple bar, Ancyloceratina (1, 5, 8).
15540–15541 | PNAS | December 22, 2015 | vol. 112 | no. 51
oxygen isotopic analyses of shell materials of
ammonoids reveal the temperature at which
the shell was secreted. This technique, called
oxygen isotopic thermometry, has been widely
used in paleoclimatological and paleobiological research. It was also applied to ammonoid
fossils more than 40 y ago (2, 3). Many scientists, however, assumed that ammonoids were
planktic or nektic organisms, so their discussion focused mainly on growth rates inferred
by identifying sinusoidal patterns, hence seasonality, in the temperature data. Among
those previous workers, Anderson et al. (4)
analyzed oxygen isotopic composition of the
middle Jurassic ammonoids and compared
the results with those of co-occurring benthic
and planktic organisms. The isotopic temperatures of Kosmoceras (Stephanoceratoidea) were
significantly warmer than those of benthic
bivalves and slightly cooler than those of surface-dwelling organisms, indicating a planktic
or nektic mode of life of Kosmoceras (i.e., a
position high in the water column) (Fig. 1).
In contrast, when Moriya et al. (5) analyzed
isotopic temperatures of the late Cretaceous
ammonoids and co-occurring planktic and benthic organisms, isotopic temperatures of all
ammonoids analyzed, regardless of their taxonomic and morphological relationships, were
essentially identical to those of benthic foraminifers and bivalves, and significantly cooler
than those of planktic foraminifers, indicating
a demersal (bottom dwelling) habitat of these
ammonoid species (Fig. 1). Because paleontologists working on ammonoids expected that
the morphological features of the external
shells must, at least partly, represent their ecology, these results raised many arguments
on ammonoid ecology. Since the works of
Anderson et al. (4) and Moriya et al. (5), the use
of isotopic thermometry on ammonoid fossils
for identifying their ecology has becomes more
widespread (6–8) (Fig. 1). However, because of
technical difficulties in identifying thermal
structure of the water column with analyzing
apparent planktic and benthic organisms, a full
set of data for planktic and benthic organisms
Author contributions: K.M. wrote the paper.
The author declares no conflict of interest.
See companion article on page 15562.
1
Email: [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1520961112
Moriya
expected that marine planktic ecosystem of
microorganisms was severely damaged at
the K/Pg boundary (11), Kruta et al. (10)
proposed that the collapse of the marine planktic food web was the trigger of
the ammonoid extinction event. However,
Tanabe (12) argued that other groups of
ammonoids with a jaw apparatus similar to
modern nautiloids (e.g., phylloceratids and
gaudryceratids), which are assumed to prey
on macroorganisms, also became extinct at
the boundary, indicating that feeding habits
at submature and mature growth stages were
also not related to loss of ammonoids in the
K/Pg terminal extinction event. Alternatively,
habitat of hatchling and juvenile ammonoids
is the other candidate for the fatal ecology for
the latest Cretaceous ammonoids. On the
basis of their small embryonic shell size (0.5–
1.8 mm in diameter) and the occurrence of
massive accumulation of embryonic shells,
eggs and hatchlings are thought to have been
planktic, feeding during early development
on planktic microorganisms (12–14). If this
were the case, the abrupt demise of planktic
ecosystems at the K/Pg boundary would have
had a great impact on the survival of newly
hatched ammonoids, but not on the directdeveloping nautiloids. However, Landman
et al. (15) pointed out the differences in
the timing of extinction between cosmopolitan and endemic ammonoids. Although
both cosmopolitans and endemics share the
similar embryonic shell size, only endemics
went extinct at the K/Pg boundary, and few
cosmopolitans survived into the earliest Paleocene, indicating embryonic shell size; hence,
embryonic ecology may not have been the
key to survival. However, the termination of
all ammonoids—including cosmopolitans—
at the earliest Paleocene ad extremum, and
the survival of the nautiloid cephalopods,
indicate that the fatal ecology for ammonoids has yet to be identified. The hypotheses mentioned above can be tested further
with developments of new analytical techniques and using exceptionally well-preserved
materials.
1 Sessa JA, et al. (2015) Ammonite habitat revealed via isotopic
composition and comparisons with co-occurring benthic and
planktonic organisms. Proc Natl Acad Sci USA 112:15562–15567.
2 Stahl W, Jordan R (1969) General considerations on isotopic
paleotemperature determinations and analyses of Jurassic
ammonites. Earth Planet Sci Lett 6(3):173–178.
3 Jordan R, Stahl W (1970) Isotopische Paläotemperatur
Bestimmungen an jurassischen Ammoniten and grundsätzliche
Voraussetzungen für diese Methode. Geol Jahrb 89:33–62.
4 Anderson TF, Popp BN, Williams AC, Ho L-Z, Hudson JD (1994) The
stable isotopic record of fossils from the Peterborough Member,
Oxford Clay Formation (Jurassic), UK: Palaeoenvironmental
implications. J Geol Soc London 151(1):125–138.
5 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(2):167–170.
6 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 1:1–7.
7 Henderson RA, Price GD (2012) Paleoenvironment and
paleoecology inferred from oxygen and carbon isotopes of
subtropical mollusks from the Late Cretaceous (Cenomanian) of
Bathurst Island, Australia. Palaios 27(9-10):618–627.
8 Stevens K, Mutterlose J, Wiedenroth K (2015) Stable isotope data
(δ18O, δ13C) of the ammonite genus Simbirskites—Implications for
habitat reconstructions of extinct cephalopods. Palaeogeogr
Palaeoclimatol Palaeoecol 417:164–175.
9 Landman NH, Garb MP, Rovelli R, Ebel DS, Edwards LE (2012)
Short-term survival of ammonites in New Jersey after the EndCretaceous Bolide impact. Acta Palaeontol Pol 57(4):703–715.
10 Kruta I, Landman NH, Rouget I, Cecca F, Tafforeau P (2011) The
role of ammonites in the Mesozoic marine food web revealed by jaw
preservation. Science 331(6013):70–72.
11 Huber BT, MacLeod KG, Norris RD (2002) Abrupt extinction and
subsequent reworking of Cretaceous planktonic foraminifera across
the Cretaceous-Tertiary boundary: Evidence from the subtropical
North Atlantic. Catastrophic Events and Mass Extinction: Impacts
and Beyond, eds Koeberl C, MacLeod KG (Geological Society of
America, Boulder, CO), pp 277–289.
12 Tanabe K (2011) Paleontology. The feeding habits of ammonites.
Science 331(6013):37–38.
13 Landman NH, Tanabe K, Shigeta Y (1996) Ammonoid embryonic
development. Ammonoid Paleobiology, eds Landman NH, Tanabe K,
David RA (Plenum, New York), pp 343–405.
14 De Baets K, et al. (2015) Ammonoid embryonic development.
Ammonoid Paleobiology: From Anatomy to Ecology, eds Klug C,
Korn D, de Baets K, Kruta I, Mapes RH (Springer, The Netherlands), pp
113–205.
15 Landman NH, et al. (2014) Ammonite extinction and nautilid
survival at the end of the Cretaceous. Geology 42(8):707–710.
16 Gradstein FM, Ogg JG, Schmitz MD, Ogg GM (2012) The
Geologic Time Scale 2012 (Elsevier, Boston).
17 Yacobucci MM (2015) Macroevolution and paleobiology of
Jurassic–Cretaceous ammonoids. Ammonoid Paleobiology: From
Macroevolution to Paleogeography, eds Klug C, Korn D, de Baets K,
Kruta I, Mapes RH (Elsevier, The Netherlands), pp 189–228.
tion, and other ecological factors must
have been critical for ammonoids at the
K/Pg boundary. One potential hypothesis
is the food habit. Kruta et al. (10) presented
that the late Cretaceous baculites preyed
upon planktic microorganisms. Because it is
The report by Sessa
et al. is the first paper to
describe the habitat of
ammonoids in the latest
Cretaceous Western Interior Seaway of North
America with a full set
of concrete evidence
from oxygen isotopic
thermometry.
PNAS | December 22, 2015 | vol. 112 | no. 51 | 15541
COMMENTARY
co-occurring with ammonoids have rarely been
described since Moriya et al. (5). An additional
unanswered question is how habitat depth preferences evolved in ammonoids, especially in the
latest Cretaceous time just before the terminal
extinction event. For discussing mechanisms
and dynamics of paleobiodiversity, paleoecosystem, and extinction events, a fundamental
knowledge about habitat depth of ammonoids
is crucial.
The report by Sessa et al. (1) is the first
paper to describe the habitat of ammonoids
in the latest Cretaceous Western Interior Seaway
of North America with a full set of concrete
evidence from oxygen isotopic thermometry.
Isotopic temperatures calculated from planktic
foraminifers inhabiting the mixed layer of the
water column and benthic organisms on the sea
floor show temperatures of ∼26 °C and ∼19 °C,
respectively, indicating ∼7 °C differences
between surface and bottom waters. The
mean isotopic temperatures of the latest Cretaceous ammonoids, Eubaculites carinatus
and Eubaculites latecarinatus (Turrilitoidea),
and Discoscaphites iris (Scaphitoidea) are estimated as ∼18 °C, comparable to those of
benthic organisms (1). In addition to isotopic
results, careful examination of the preservation
of shell materials excludes potential postmortem drift, often a concern in organisms with
potentially buoyant shells. These lines of evidence clearly indicate that these ammonoid
species were demersal (bottom dwelling) organisms, providing the first direct evidence of
habitat depths for the latest Cretaceous lineages
that became extinct at or just above the K/Pg
boundary (9),
Although data are still sparse, an overview of
evolutional history of habitats of the Jurassic–
Cretaceous ammonoids indicates a very interesting view (Fig. 1). Although many previous
workers expected that ammonoids were
predominantly planktic or nektic organisms,
isotopic data suggest that bottom-dwelling habitat seems to be more frequent among the ammonoids after the Triassic/Jurassic diversity
crisis. Additionally, in Perisphinctoidea, habitat
depth reverted back from demersal to planktic/
nektic even within a lineage. As Sessa et al. (1)
show, many groups of ammonoids (Phylloceratoidea, Tetragonitoidea, Desmoceratoidea,
Scaphitoidea, and Turrilitoidea), which possessed
a demersal habitat, went extinct at the K/Pg
boundary (Fig. 1). However, the planktic/
nektic group (Acanthoceratoidea) also went extinct at the same time. These facts suggest that
the habitat depth of submature and mature
individuals was not the determinant of extinc-