Introduction
The measurement of Mg and Sr concentrations in biogenic calcite as records of
past environmental conditions and geochemical cycles has a long tradition
(e.g. Odum, 1951; Turekian, 1955, Lowenstam, 1961). Palaeotemperature
estimates from element concentrations in fossil calcite in particular have
been intensively studied (e.g. Pilkey and Hower, 1960; Nürnberg et al.,
1996; Elderfield and Ganssen, 2000; McArthur et al., 2007).
A number of empirical studies have documented positive co-variation of
Mg / Ca ratios and/or Sr / Ca ratios with temperature in biogenic
calcite from belemnites (Rosales et al., 2004; McArthur et al., 2007; Li et
al., 2012), bivalves (Klein et al., 1996; Freitas et al., 2006; Wanamaker
et al., 2008; Tynan et al.,
2017), brachiopods (Brand et al., 2013; Butler et
al., 2015), coccoliths (Stoll et al., 2001), echinoderms (Pilkey and Hower,
1960), foraminifers (Lea et al., 1999; Elderfield and Ganssen, 2000; Lear et
al., 2002; de Nooijer et al., 2014) and ostracods (Chivas et al., 1986; De Dekker et al.,
1999). Inorganic precipitation experiments also show a significant
temperature control on the incorporation of Mg and Sr into calcite (Kinsman
and Holland, 1969; Katz, 1973; Oomori et al., 1987). While a positive
co-variation of Mg / Ca ratios with ambient temperature in biogenic
calcite agrees with experimental data from inorganic calcite precipitation
experiments, Sr / Ca ratios in shell calcite that are positively linked
with temperature (e.g. Lea et al., 1999; Stoll et al., 2002; Ullmann et al.,
2013a) contradict an expected negative correlation of these two parameters
(Kinsman and Holland, 1969; Rimstidt et al., 1998).
It is evident that a multitude of parameters besides temperature can affect
element concentrations in biogenic calcite, e.g. pH (Lea et al., 1999),
pCO2 (Dissard et al., 2010; Müller et al., 2014), salinity (Klein et
al., 1996; Lea et al., 1999; Wanamaker et al., 2008; Hönisch et al.,
2013) and notably calcite secretion rate (e.g. Klein et al., 1996; Lorrain et
al., 2005; Ullmann et al., 2015). Disentangling the effect of temperature on
shell geochemistry from the effects of physiological responses triggered by
temperature change, and constraining the relative contributions of these
parameters on shell chemistry, is difficult in growth experiments (Wanamaker
et al., 2008). For micro-organisms analyses need to be performed at high
spatial resolution and inter-specimen offsets become a concern (e.g.
de Nooijer et al., 2014). Most shell-building
macro-organisms for which growth rates can be readily established (e.g.
Mouchi et al., 2013; Nedoncelle et al., 2013; Pérez-Huerta et al., 2014)
form growth increments that do not show consistent, significant, lateral
differences in secretion rate.
Belemnites, Mesozoic predators whose fossil calcite is of major importance
for the reconstruction of palaeoenvironmental conditions during the Jurassic
and Cretaceous (e.g. Podlaha et al., 1998; McArthur et al., 2000; Ullmann et
al., 2014; Sørensen et al., 2015), constitute an exception to this. Their
rostra are typically large (a few to tens of centimetres long and a few
millimetres to centimetres in diameter) and are structured by a concentric
arrangement of growth bands around the apical line, which itself traces the
long axis of the fossil (Sælen, 1989; Ullmann et al., 2015). These growth
bands show systematic lateral changes in thickness and can be sampled by
milling, permitting high-precision analyses of element concentrations via
ICP-OES or ICP-MS. In the rostra it is possible to differentiate between
effects of crystal morphology, secretion rate and other physiological or
environmental controls (Ullmann et al., 2015). A significant contribution of
calcite secretion rate to Mg / Ca and Sr / Ca patterns in belemnite
calcite has been noted (Ullmann et al., 2015). The observed negative
correlation of Sr / Ca with secretion rate and a positive correlation of
Mg / Ca with secretion rate in the calcite of a rostrum of the belemnite
Passaloteuthis bisulcata agrees with published experimental studies
(Lorens, 1981; Tesoriero and Pankow, 1996; Gabitov and Watson, 2006; Tang et
al., 2008; Gabitov et al., 2014) and theoretical studies (DePaolo, 2011;
Gabitov et al., 2014). The magnitude of secretion rate-induced changes in
Mg / Ca and Sr / Ca ratios, however, has so far remained unquantified
in belemnite calcite.
Studied geochemical profiles and their relative secretion rates.
(a) Schematic representation of
the rostrum of P. bisulcata with approximate positions of the
transects. (b) Cross plot of the distance of selected luminescent
bands (a–f and white dots from Fig. 2) from the margin of the rostrum in
profiles 1 to 4 with respect to its position in profile 1. Stippled lines
indicate selected relative secretion rates with respect to profile 1. Letters
and circles are positioned as in Fig. 2. (c) Relative secretion rate
in geochemical transects computed from exponential relationships documented
in Ullmann et al. (2015).
Here, a quantitative appraisal of the available data is presented, backed up
by additional qualitative data, and the importance of calcite secretion rate
for the interpretation of Mg / Ca and Sr / Ca ratios in biogenic
calcite is discussed.
Materials and methods
The studied, nearly complete rostrum of Passoleuthis bisulcata
(Blainville, 1827) was collected from the Early Toarcian (Early Jurassic)
Grey Shale Member at Hawsker Bottoms, Yorkshire, UK (67 cm above the base of
the Dactylioceras tenuicostatum ammonite subzone,
D. tenuicostatum zone; Hesselbo and Jenkyns, 1995). A detailed
methodology for geochemical analyses and documentation of cathodoluminescence
patterns is described in Ullmann et al. (2015). In brief, the specimen was
cut perpendicular to the long axis into four slabs which were glued onto
glass slides, ground down to a thickness of ca. 3.5 mm and polished. Samples
for element / Ca analysis were prepared by incremental drilling of
samples (ca. 110 µm increments; ca. 2 mm drill depth; ca. 0.8 mm
drill bit diameter) through the slabs using a hand-held drill. Analyses were
performed using an Optima 7000 DV ICP-OES. After grinding down the
sampled slabs to ca. 0.5 mm and polishing, cathodoluminescence maps were
made using a microscope equipped with a Citl Mk-3a electron source (Fig. 2).
Element / Ca ratios were screened for diagenesis using Mn / Ca ratios
and only data from well-preserved samples are further considered.
Cathodoluminescence pattern for sections through the rostrum
adjacent to geochemical transects 1 to 4. Letters “a” to “f” correlated
with the profiles with white lines and white dots indicate arbitrarily chosen
marker bands for illustration of differences in shell secretion rate (see
also Fig. 1). Note the increasing distance of marker bands from profiles 1 to
4.
Data from the specimen of Passaloteuthis bisulcata analysed at high
resolution are supplemented by geochemical results of an additional transect
through another specimen of Passaloteuthis sp. from the Grey Shale
Member at Hawsker Bottoms (1 cm above the base of the Dactylioceras tenuicostatum ammonite subzone, D. tenuicostatum zone; Hesselbo and
Jenkyns, 1995; Table S1 in the Supplement). A
section of the specimen close to the phragmocone (comparable to profile 1 in
Fig. 1) was prepared as described above and sampled along a traverse with
300 µm spacing and drill depth of 500 µm using a
MicroMill with a 0.6 mm diameter drill bit. The resulting powders were
dissolved in weak HCl and diluted to a nominal Ca concentration of
10 µg g-1 with 2 % HNO3
and analysed for Mg / Ca, Sr / Ca and Mn / Ca ratios using a
Perkin Elmer Elan Quadrupole ICP-MS at the University of Oxford.
Quantification of concentrations was performed using a set of matrix-matched,
synthetic calibration solutions mixed from single element solutions. Accuracy
and precision were assessed by multiple analyses of the international
reference material JLs-1 and internal carbonate standards, and long-term
reproducibility over a period of 3 years is found to be ca. 6 %
(2 SD, n= 14) for all element ratios.
Assessment of sample preservation was performed analogously to Ullmann et
al. (2015).
Aggregated geochemical data for the four profiles plotted against
distance from the central apical line of the rostrum (zero) to the margin
(one) with profile 1 as a reference. The bin size is 2.5 % of the profile
length. (a) Mg / Ca ratios. (b) Sr / Ca ratios.
Results
Cathodoluminescence microscopy reveals a multitude of characteristic
luminescent bands in the rostrum that constitute time stamps which can be
correlated through the entire rostrum (Fig. 2). Differences in the distance
of these luminescent bands from the apical line in the four profiles can be
used to trace the relative secretion rate changes in belemnite rostra
(Fig. 2). Due to the position of the different profiles within the rostrum
(Fig. 1a), the relative secretion rate becomes greater from profiles 1 to 4
and the central growth bands in profile 1 are progressively lost (Figs.
1a, b, 2). Profile 4 yields only the outer ∼ 30 % of the growth
bands present in profile 1, but these growth bands have thicknesses (relative
secretion rates) 2.3 to > 3 times greater than the correlative
bands in profile 1 (Fig. 1c). Using exponential functions to express the
differences in secretion rate (Fig. 1c, Ullmann et al., 2015), Mg / Ca
and Sr / Ca ratios of the four geochemical profiles can be integrated
into a common ontogenetic profile (Fig. 3). These overlays show common
patterns but significant offsets between the profiles. All profiles are
characterized by a steady decrease in
Mg / Ca ratios and Sr / Ca ratios from the innermost growth bands,
reaching a minimum at ∼ 60 % distance from the centre of the
rostrum in the reference profile 1 (Fig. 3). Both ratios then increase until
about 75 % distance on the reference profile and towards the rim show a
minor decrease with subordinate peaks and lows which are specific to Mg and
Sr. In addition to this general pattern, progressively lower Mg / Ca and
higher Sr / Ca ratios are observed at the margin of the rostrum with
increasing profile number. Differences in element / Ca ratios with
respect to the reference profile 1 as a function of changes in calcite
secretion rate are plotted in Fig. 4. For these plots, only geochemical data
from the outer 2.0 mm (profile 2) to 2.6 mm (profile 4) were taken into
account, where differences between the profiles are thought to be dominated
by secretion rate effects (Ullmann et al., 2015). Deviations in Mg / Ca
and Sr / Ca from the reference profile co-vary strongly, and the
resulting enrichment factors show strong co-variation with relative secretion
rate (Fig. 4a–c). The best fits for these relations are
ΔMgCa=0.994±0.007-0.081±0.009×Δsecretion rate,ΔSrCa=1.006±0.006+0.059±0.007×Δsecretion rate,ΔMgCa=2.37±0.04-1.37±0.04×ΔSrCa,
where Δ(Mg / Ca) and Δ(Sr / Ca) are the enrichment
factors for the element / Ca ratios and Δsecretion rate
is the deviation in secretion rate from profile 1 (0 = 0 %;
1 = 100 %). A secretion rate increase of 100 % thus results in a
(8.1 ± 0.9) % depletion in Mg and a (5.9 ± 0.7) %
enrichment in Sr.
Changes in Mg / Ca and Sr / Ca ratios as a function of
precipitation rate. (a) Mg enrichment factor as a function of change
in precipitation rate expressed as a relative deviation from the
reference
precipitation rate of profile 1. Vertical lines denote 2 standard error
uncertainties for each binned interval of profiles 2 to 4 and circles show
average values with 2 standard error uncertainties. The trend line from
ordinary least square regression of the mean values is shown with a 95 %
uncertainty envelope. (b) Sr enrichment factor as a function of
calcite precipitation rate. Symbols as in (a).
(c) Correlation of Mg depletion with Sr enrichment.
Geochemical data for the transect through an additional specimen of
Passaloteuthis sp. (Figs. 5 and 6, Table S1 in the Supplement)
confirm the trends observed here and by Ullmann et al. (2015) qualitatively:
diagenesis traced by enrichments in Mn is confined to the apical zone and the
dorsal margin and absolute values of Mg / Ca and Sr / Ca ratios vary
independently of each other. Enrichments of Mg and Sr towards the apical zone
as well as a combination of higher Sr / Ca and lower Mg / Ca ratios
in the faster growing, thicker dorsal part as compared to the ventral part of
the transect are observed (Fig. 6).
Section through an additional specimen of
Passaloteuthis sp. with sample positions for geochemical analyses.
Discussion
Shell secretion of belemnite rostra and its utility to test growth rate
effects
In order to function as a biological experiment tracing the effects of shell
secretion rate on Mg and Sr concentrations, the calcite must have been formed
incrementally by the belemnite and the secretion rate signal must be large
enough not to be masked by other controls. Many aspects of belemnite
biomineralization remain obscure and there is still some ongoing debate about
the original mineralogy (aragonite or calcite) and biomineral architecture of
belemnite rostra (e.g. Dauphin et al., 2007; Hoffmann et al., 2016;
Immenhauser et al., 2016).
Original shell mineralogy and possible porosity
An originally aragonitic rostrum of Passaloteuthis analogous to
suggestions of Dauphin et al. (2007) for the Late Cretaceous
Goniocamax can confidently be excluded, because the originally
aragonitic phragmocones of Passaloteuthis are often found to be
replaced by minerals other than calcite at Hawsker Bottoms (e.g. pyrite or
barite), whereas these phases have never been observed to replace growth
bands in the rostra. Also, a 50–90 % original porosity of the bulk of
the rostrum which was cemented without direct control of the belemnite as
envisioned by Hoffmann et al. (2016) is unlikely for Passaloteuthis.
A restricted zone of original porosity in the apical zone of this genus
(Fig. 1a) has been proposed (Ullmann et al., 2015), because here geochemical
data fall on a mixing trend with early diagenetic cements of the phragmocone,
a signal that is not observed elsewhere in the rostrum apart from its contact
with the surrounding sediment matrix. Passaloteuthis rostra from
Hawsker Bottoms still preserve their original intra-crystalline organic
matrix, as evidenced by their translucent brown colour and pleochroic
behaviour when observed under polarized light (Ullmann et al., 2014). Growth
increments can be traced at a resolution of < 10 µm
throughout the entire rostrum using cathodoluminescence microscopy. The
relative positions of the luminescent bands faithfully define the outline of
the rostrum at a given ontogenetic stage and their luminescence intensities
are the same in the four profiles without any indication of the typical
bright luminescence indicative of early diagenetic cements at Hawsker Bottoms
(Ullmann et al., 2015, Fig. 2). Isotope and element patterns can be
consistently correlated using only growth band positions (Ullmann et al.,
2015), which would not be possible if the larger part of the calcite was
formed without the clear temporal transgression defined by the growth bands.
δ13C values in the studied profiles reach a maximum of
+3.3 ‰ V-PDB and δ18O values a minimum of
-2.2 ‰ V-PDB (Ullmann et al., 2015), in good agreement with other
shelly fossils in the area (Korte and Hesselbo, 2011). If these values were
to represent a mixture of less than 50 % original signal with a greater
part of calcite representative of bottom water conditions (lighter
δ13C values and δ18O of -0.4 ‰ or heavier,
Ullmann et al., 2014, 2015), recalculated values for the original calcite
would become incompatible with other coeval calcite archives. The sum of
these observations suggests that – apart from a small zone around the apical
line – the rostrum of Passaloteuthis was formed in growth
increments of calcite with very little original porosity.
Geochemical data for an additional specimen of
Passaloteuthis sp. (Mg / Ca green; Sr / Ca violet;
Mn / Ca brown). Samples excluded from interpretation due to
post-depositional alteration (Ullmann et al., 2015) are shaded in grey.
Significant differences in average Sr / Ca and Mg / Ca between the
ventral (slow growing) and dorsal (fast growing) parts of the section (light
straight lines) are evident and are compatible with the findings from the
multi-profile dataset.
Variability of Mg / Ca and Sr / Ca ratios in belemnite
calcite. Intra-specimen variability accounts for a residual range of values
in P. bisulcata after accounting for crystallographic forcing and
shell secretion rate (Ullmann et al., 2015). Intra-species variability of
Passaloteuthis (Ullmann et al., 2014) and the range of values
observed in Toarcian belemnites (Bailey et al., 2003; Rosales et al., 2004;
Ullmann et al., 2014) do not exclude samples potentially affected by
crystallographic forcing and are thus likely overestimated. The range of
reconstructed seawater Sr / Ca ratios is from Ullmann et al. (2013b). The
lengths of arrows for crystallographic forcing and secretion rate indicate
the maximum observed effect in P. bisulcata.
Utility of Passaloteuthis to test growth rate effects on Mg and Sr
Biological controls on element incorporation into shell carbonate are strong
and lead to partly significant intra-species differences (e.g. Gillikin et
al., 2005; Ullmann et al., 2013a, 2015; Sørensen et al., 2015; Fig. 7).
This biological regulation of element partition coefficients (e.g. Gillikin
et al., 2005) is also evident in belemnites, which have high Sr
concentrations when compared to other coeval calcite fossils (see the
discussion in Ullmann et al., 2013b). This problem makes constraining the
controls on absolute levels of element / Ca ratios in shell carbonate
challenging, but is cancelled out when comparing coeval growth increments
within a single fossil. While metabolic controls lead to systematic
ontogenetic changes in Mg / Ca and Sr / Ca in Passaloteuthis
(Figs. 3 and 6), at a given ontogenetic stage these metabolic controls are
expressed in the same way at the sites of mineralization at each of the
studied profiles. The only anticipated difference is the rate of shell
secretion, which can thus be isolated as a geochemical forcing and is
systematically faster the closer to the rostrum's apex the profile is laid
(Fig. 1).
Controls on element uptake and expected growth rate effects
Calcite precipitation experiments have established that Sr concentration
should increase and Mg concentrations decrease with increasing precipitation
rate (Lorens, 1981; Tesoriero and Pankow, 1996; Gabitov and Watson, 2006;
Tang et al., 2008; Gabitov et al., 2014). The same signature is expected to
be imposed by decreasing temperature (Rimstidt et al., 1998), necessitating
the measurement of a reliable temperature proxy alongside the element
concentrations or when comparing coeval growth increments. The latter
approach is adopted here, which rules out that temperature can have a
significant effect on the observed trends. Metabolic effects on element
incorporation and/or changes in the composition of the mineralizing fluid
throughout ontogeny are clearly evident (Figs. 3 and 6) but are not
manifested as a strong co-variation of Mg and Sr. These effects can thus be
accounted for by normalizing element / Ca data to element / Ca ratios
of profile 1, i.e. by computing element enrichment factors. Furthermore,
changes in relative growth rate (within a factor of 4) and likely also
absolute growth rate in the rostrum are not very large, so that the observed
effects are comparable throughout the studied part of the profiles. They
therefore image a linear segment of a relationship, which over a wider range
of secretion rates is expected to follow a more complex, curved function
(e.g. Tang et al., 2008; DePaolo, 2011; Gabitov et
al., 2014).
The observed sensitivities of Sr / Ca ratios and Mg / Ca ratios to
changing secretion rate (5.9 % increase and 8.1 % decrease per
100 % shell secretion rate increase) can be compared with experimental
results supported by theoretical considerations. The growth entrapment model
(Watson and Liang, 1995) predicts that elements present in the surface layer
of a growing crystal will become more efficiently trapped the faster the
crystal forms. Results of precipitation experiments at 20–25 ∘C
approximated with this model Gabitov et al. (2014) predict a Sr / Ca
sensitivity observed in P. bisulcata for calcite growth rates of
ca. 0.05 nm s-1 and ca. 40 nm s-1, whereas measured Mg / Ca
sensitivity is matched at ca. 0.3 and ca. 20 nm s-1. It is conceivable
that at slightly different temperatures a better match between these two
elements could be obtained, because the response of Sr changes significantly
with temperature (Tang et al., 2008). No equivalent experiments for Mg are
available, however, so this hypothesis cannot be quantitatively explored.
Nevertheless, conditions can be found in experimentally constrained
relationships under which the proposed sensitivities of Mg and Sr to shell
secretion rate change recorded in P. bisulcata are met, further
suggesting that relative secretion rate is the ultimate control of the
observed signal in Fig. 4.
Significance of shell secretion rate effects for fossil Mg / Ca and Sr / Ca
data
In order to use Mg / Ca and Sr / Ca data of fossil carbonates to
study aspects of palaeoenvironments, it is imperative that the dominant
controls of the signal are constrained. After excluding data that are
affected by crystallographic forcing near the centre of the rostrum (Ullmann
et al., 2015, Fig. 6) and samples showing clear secretion rate effects, the
residual range between the measured extreme values in the studied rostrum is
still ±25 % for Mg / Ca ratios and ±12 % for Sr / Ca
ratios (Fig. 7). The reported variability within the genus
Passaloteuthis and all Toarcian (Early Jurassic, ca. 183–174 Ma)
belemnite rostra (Bailey et al., 2003; Rosales et al., 2004; Ullmann et al.,
2014) is considerably larger (Fig. 7). Some of this variability is likely
related to crystallographic controls on Mg and Sr incorporation (Fig. 7,
Ullmann et al., 2015). In practice, there are only a few samples affected by
this factor in published datasets: crystallographic controls leading to such Sr and Mg
enrichments are most prevalent near the apical line of the rostrum (Ullmann
et al., 2015), an area where sampling is avoided (if possible) because of a
high probability of diagenetic overprint (e.g. Podlaha et al., 1998; McArthur
et al., 2000; Ullmann and Korte, 2015). For Passaloteuthis, the
observed range of Mg / Ca and Sr / Ca values in the genus (Ullmann et
al., 2014) is reduced by a third, when the highest 5 % of the
element / Ca ratios are excluded.
Significant changes in average Sr / Ca and Mg / Ca ratios have been
observed for whole belemnite specimens throughout the Toarcian (McArthur et
al., 2000; Bailey et al., 2003; Rosales et al., 2004). These changes are
considerably larger than observed intra-specimen variability (Fig. 7) and
show a large increase in both Sr / Ca and Mg / Ca ratios around the
Early Jurassic Toarcian Oceanic Anoxic Event (ca. 183 Ma, McArthur et al.,
2000; Bailey et al., 2003; Rosales et al., 2004). On an even longer timescale
of the Early and Middle Jurassic – some 38 million years – Sr / Ca
ratios in belemnite rostra averaged per ammonite biozone drift between 1.2
and 2.3 mmol mol-1, probably tracing secular changes in seawater
composition (Ullmann et al., 2013b).
While effects of secretion rate on Sr / Ca and Mg / Ca ratios in
belemnite rostra are significant (Fig. 4 and 6), all the above-described
ranges of data are considerably larger than the maximum observed effect of
calcite secretion rate in P. bisulcata (Fig. 7), suggesting that
growth rate is of minor importance for controlling element / Ca ratios in
this species. This likely also holds for other belemnites, as seen by
Sr / Ca ratios in transects through multiple specimens yielding
comparable results in Bellemnellocamax mammillatus (Sørensen et
al., 2015), even though the generalization remains to be tested rigorously.
When sampling belemnite rostra for palaeoenvironmental studies, avoiding the
apical zone and targeting profiles as far away from the apex as possible
(i.e. profile 1 rather than profiles 3 or 4) ensures the least possible bias
exerted by crystallographic forcing and internal growth rate effects.
Deriving information about past seawater composition then depends mostly on
other potential controls on shell chemistry like metabolic, kinetic, and
temperature effects (e.g. Rosales et al., 2004; McArthur et al., 2007; Li et
al., 2012) and the generation of large datasets which enable one to constrain
average values precisely.