By recreating a range of geologically relevant concentrations of dissolved
inorganic carbon (DIC) in the laboratory, we demonstrate that the magnitude
of the vital effects in both carbon and oxygen isotopes of coccolith calcite
of multiple species relates to ambient DIC concentration. Under high DIC
levels, all the examined coccoliths exhibit significantly reduced isotopic
offsets from inorganic calcite compared to the substantial vital effects
expressed at low (preindustrial and present-day) DIC concentrations. The
supply of carbon to the cell exerts a primary control on biological
fractionation in coccolith calcite via the modulation of coccolithophore
growth rate, cell size and carbon utilisation by photosynthesis and
calcification, altogether accounting for the observed interspecific
differences between coccolith species. These laboratory observations support
the recent hypothesis from field observations that the appearance of
interspecific vital effect in coccolithophores coincides with the long-term
Neogene decline of atmospheric CO
The quest to generate reliable and accurate palaeoenvironmental reconstructions is hindered by uncertainties in our current proxies from the sedimentary archive. One prominent caveat comes from the biological origin of sedimentary calcareous particles in marine and oceanic realms. As a consequence of the biological controls on chemical signals in algae, most biominerals do not precipitate in equilibrium conditions and the compositional departure between biocarbonates and an inorganic reference is commonly referred to as the vital effect. Therefore, geochemical data from ancient biomineralising organisms must be corrected in order to derive the primary signals from palaeoseawater. In the case of the foraminifera, corals and coccoliths, the foremost carbonate producers in the marine realm, there has been a considerable number of studies during which living organisms were cultured in strictly controlled environmental conditions and their biominerals measured for a range of isotopic systems to generate empirical proxy calibrations (Erez and Luz, 1982; Dudley et al., 1986; Spero et al., 1997; Bemis et al., 1998; Ziveri et al., 2003; Tripati et al., 2010; Rickaby et al., 2010; Rollion-Bard et al., 2011; Grauel et al., 2013; Hermoso et al., 2014; Minoletti et al., 2014; Hermoso, 2015).
Another important aim in palaeoceanography is to determine whether the physiology-induced fractionation for a given taxon was constant through time from an evolutionary perspective, and over shorter time intervals comprising large climatic fluctuations, in turn inducing an environmentally driven modulation of the vital effect (Hermoso, 2014). In the absence of more reliable information, the Uniformitarianism principle – by which, the processes that were operating in the geological past still exist today, and vice versa – is commonly applied for elucidating vital effects and reconstructing primary oceanographic signals.
Although coccoliths are relatively challenging to extract at the
species-specific level from sediments compared to foraminifera,
coccolith-based studies represent a growing field since the pioneering work
by Anderson and Steinmetz (1981). To better interpret coccolith isotope
signals and generate more reliable palaeoenvironmental estimates from these
cosmopolitan organisms, we need to gain a broader picture of their vital
effects, and more specifically determine how environmental parameters govern
their magnitude. Several studies have specifically measured coccolith
These biogeochemical proxies raise questions regarding what vital effect
coefficients should be applied to ancient coccolith species extracted from
Meso-Cenozoic sediments as temperature and
The species
The large and relatively ancient taxon
Numerical data set.
A raw batch of natural seawater collected from the English Channel (station
L4; 50
During the acclimation and culture phases, cells were maintained at
15
The evolution of culture growth was determined by cell enumeration made every
2 days, approximately 3 h after the onset of the illuminated phase using a
Beckman Coulter Counter Series Z2 apparatus fitted with a 100
Carbon and oxygen isotope compositions of coccolith calcite and the oxygen
isotopic ratios from water media were measured as described in Hermoso et
al. (2014). In brief, coccolith calcites from rinsed and oxidised culture
residues were measured using a VG Isogas Prism II mass spectrometer with an
on-line VG Isocarb at Oxford University. Results (
The
The magnitude of the vital effects for the oxygen and carbon isotope systems
is expressed as the isotopic offset of coccolith calcite from inorganic
calcite (
Changes in algae specific growth rates
Changes in coccolith
Cell division rates at pre-industrial DIC levels (
The interspecies range in coccolith
The
Contrasting responses among examined species are observed in the evolution of
specific growth rates and coccosphere volume with increased ambient DIC
level, and as a result, in the carbon resource around the cells (Fig. 1a, b).
The relatively fast-growing
With increased DIC concentration in the culture medium, species that
exhibited high
The typology of a heavy and light isotopic group for the oxygen isotope
system still exists with increased ambient DIC concentration, but the
magnitude of the vital effect is considerably reduced with coccolith
In biological systems, an increase in the DIC concentration of the ambient
medium may not be linearly related to that of the mineralising fluid due to
the effects of physiology (vital effect). The observation of such contrasting
interspecific responses in
Theoretical work and experiments seeking to identify the control of inorganic
calcite isotopes have provided useful reference points that are valuable to
understand biogeochemical signals and the magnitude of the vital effect. For
the carbon isotope system, calcite
The present data set is not sufficient to tackle whether coccolithophore
calcite isotopically derives from a CO
In photosynthetic, or photosynthetic-associated biomineralisers such as the
foraminifera, corals and coccolithophores, a
The species
In species characterised by low PIC
Species originally with very high
It has been hypothesised that the isotopic heavy group is an isotopic relic
of a partial CO
Under low ambient DIC levels and consecutive carbon-limited conditions, there
may be a fast turnover of the internal carbon pool (Nimer et al., 1992),
which allows less time between CO
In the present study, in all species except
For
With this biogeochemical control of oxygen isotope fractionation in
coccolith calcite in mind, it remains difficult to explain the lower
magnitude of the
Scatter plot of carbon and oxygen isotopic offsets with increased
DIC concentration. Superimposed on the linear regression lines, the wider
side of the red triangles denotes a higher DIC level. With increased DIC and
aqueous CO
Using geological evidence in the Neogene, it was reported that large
coccoliths exhibit
Using our empirical calibration between the magnitude of the vital effect
with DIC concentration or with equivalent
Exploiting interspecies signals, such as the large–small coccolith isotopic
offset proposed by Bolton et al. (2012), has the notable advantage of
circumventing uncertainties that complicate palaeoceanographic
reconstructions (salinity, temperature, seawater
The hypothesis by Bolton and Stoll (2013) about a possible “Late Miocene
threshold” at about 375–575 ppm of atmospheric of CO
This work provides new constraints on the “
Since the pioneering studies on coccolith geochemistry in the 1980s (Anderson
and Steinmetz, 1981; Steinmetz and Anderson, 1984; Dudley et al., 1986), a
growing body of literature highlights the potential for application to
palaeoceanography. Recent work shows major steps towards a complete
understanding of the vital effect imprinting isotopes of coccolith calcite
based on biogeochemistry and physiology, which may “rival” our quantitative
understanding of foraminiferal proxies. These studies and the present work
point towards the possibility of generating coccolith-derived long-term SST
reconstruction and/or
The laboratory work presented in this paper was mostly undertaken by I. Z. X. Chan, as part of his Master's research project in 2013 under the main supervision and guidance of M. Hermoso. We thank C. Day for help with the isotopic analyses in Oxford and Phil Renforth for seawater alkalinity measurements. We are also grateful to J. Rolfe at Cambridge University for his diligence in running carbon isotope analyses of the seawater batches. The authors thank J. Bijma for editorial handling, and L.-M. Holtz and two other anonymous referees for comments on the discussion paper that have substantially improved the final version of the manuscript. This work was supported by the European Research Council (grant SP2-GA-2008-200915) to R. E. M. Rickaby and by the Natural Environment Research Council (grant NE/H015523/1) to M. Hermoso. The article processing charges of this paper have been covered by the OpenAIRE programme. Edited by: J. Bijma