BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-13-6385-2016Stable carbon isotope gradients in benthic foraminifera as proxy for organic
carbon fluxes in the Mediterranean SeaTheodorMarcmarc.theodor@uni-hamburg.deSchmiedlGerhardJorissenFransMackensenAndreashttps://orcid.org/0000-0002-5024-4455Center for Earth System Research and Sustainability, Institute of
Geology, University of Hamburg, Bundesstrasse 55, 20146 Hamburg, GermanyCNRS, UMR 6112, LPG–BIAF, Recent and Fossil Bio-Indicators,
Université d'Angers, 2 Boulevard Lavoisier, 49045 Angers CEDEX, FranceAlfred Wegener Institute, Helmholtz Centre for Polar and Marine
Research, Am Alten Hafen 26, 27568 Bremerhaven, GermanyMarc Theodor (marc.theodor@uni-hamburg.de)30November20161323638564046June20169June201626October20168November2016This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/13/6385/2016/bg-13-6385-2016.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/13/6385/2016/bg-13-6385-2016.pdf
We have determined stable carbon isotope ratios of epifaunal and shallow
infaunal benthic foraminifera in the Mediterranean Sea to relate the inferred
gradient of pore water δ13CDIC to varying trophic
conditions. This is a prerequisite for developing this difference into a
potential transfer function for organic matter flux rates. The data set is
based on samples retrieved from a well-defined bathymetric range
(400–1500 m water depth) of sub-basins in the western, central, and eastern
Mediterranean Sea. Regional contrasts in organic matter fluxes and associated
δ13CDIC of pore water are recorded by the δ13C difference (Δδ13CUmed-Epi) between the shallow
infaunal Uvigerina mediterranea and epifaunal species
(Planulina ariminensis, Cibicidoides pachydermus, Cibicides lobatulus). Within epifaunal taxa, the highest δ13C values are
recorded for P. ariminensis, providing the best indicator for bottom
water δ13CDIC. In contrast, C. pachydermus
reveals minor pore water effects at the more eutrophic sites. Because of
ontogenetic trends in the δ13C signal of U. mediterranea
of up to 1.04 ‰, only tests larger than 600 µm were used
for the development of the transfer function. The recorded differences in the
δ13C values of U. mediterranea and epifaunal taxa (Δδ13CUmed-Epi) range from -0.46 to -2.13 ‰,
with generally higher offsets at more eutrophic sites. The measured
δ13C differences are related to site-specific differences in
microhabitat, depth of the principal sedimentary redox boundary, and TOC
content of the ambient sediment. The Δδ13CUmed-Epi
values reveal a consistent relation to Corg fluxes estimated from
satellite-derived surface water primary production in open-marine settings of
the Alboran Sea, Mallorca Channel, Strait of Sicily, and southern Aegean Sea.
In contrast, Δδ13CUmed-Epi values in areas affected
by intense resuspension and riverine organic matter sources of the northern
to central Aegean Sea and the canyon systems of the Gulf of Lion suggest
higher Corg fluxes compared to the values based on recent primary
production. Taking regional biases and uncertainties into account, we
establish a first Δδ13CUmed-Epi-based transfer
function for Corg fluxes for the Mediterranean Sea.
Introduction
The stable isotope composition of benthic foraminifera is used in a wide
range of paleoceanographic applications. The δ18O signal of benthic
foraminifera provides information on bottom water temperature and salinity,
and has been applied to estimate global ice volume changes (e.g., Shackleton
and Opdyke, 1973; Adkins et al., 2002; Marchitto et al., 2014). The benthic
foraminiferal δ13C signal is mainly used for the reconstruction of
changes in deep-sea circulation, bottom water oxygen concentrations, and
organic carbon fluxes to the sea floor (Curry and Lohmann, 1982; Zahn et al.,
1986; McCorkle and Emerson, 1988; Mackensen and Bickert, 1999; Pahnke and
Zahn, 2005). Recently, more quantitative approaches have been applied to the
reconstruction of past changes in deep-water oxygenation (Stott et al., 2000;
Schmiedl and Mackensen, 2006; Hoogakker et al., 2015). There have also been
attempts to use multispecies δ13C records to reconstruct past
organic carbon fluxes (Zahn et al., 1986; Schilman et al., 2003; Kuhnt et
al., 2008). However, all of these studies lack a regional calibration based
on living specimens and modern organic carbon flux data.
The δ13C gradient of pore water dissolved inorganic carbon (DIC) in
the uppermost surface sediment is directly related to the flux and
decomposition rates of organic matter (McCorkle and Emerson, 1988; McCorkle
et al., 1990; Holsten et al., 2004). With increasing depth in the sediment,
more 13C depleted organic matter (δ13C around -18 to
-23 ‰, e.g., Mackensen, 2008) is remineralized by microbial
activity (McCorkle et al., 1985). This process results in δ13CDIC pore water depletions of up to -4 ‰ relative
to the bottom water signal (McCorkle and Emerson, 1988; McCorkle et al.,
1990; Holsten et al., 2004). The preferential release of 12C to the pore
water stops when no more organic matter (OM) is remineralized, which mostly coincides with the
total consumption of electron acceptors, of which oxygen, nitrate, and sulfate
are the most energy-efficient ones (McCorkle and Emerson, 1988; McCorkle et
al., 1990; Koho and Pina-Ochoa, 2012, Hoogakker et al., 2015).
The δ13CDIC pore water gradient is reflected in the
δ13C signal of benthic foraminifera from defined microhabitats on
and below the sediment–water interface (Grossman, 1984a, b; McCorkle et al.,
1990, 1997; Rathburn et al., 1996; Mackensen and Licari, 2004; Schmiedl et
al., 2004; Fontanier et al., 2006). Although benthic foraminifera can migrate
through the sediment (Linke and Lutze, 1993; Ohga and Kitazato, 1997) and
living individuals may occur across a relatively wide depth interval, the
δ13C of a species exhibits relatively little scatter, and all
specimens tend to reflect the same calcification depth (Mackensen and
Douglas, 1989; McCorkle et al., 1990, 1997; Mackensen et al., 2000; Schmiedl
et al., 2004). The study of McCorkle and Emerson (1988) has shown that the
difference between δ13CDIC of bottom water and
δ13CDIC of pore water at the depth in the sediment where
oxygen approaches zero is directly related to the oxygen content of the
bottom water mass. Based on this observation, the δ13C difference
of epifaunal (e.g., Cibicidoides) and deep infaunal
(Globobulimina) taxa was used as proxy for the quantification of
past changes in deep-water oxygenation (Schmiedl and Mackensen, 2006;
Hoogakker et al., 2015). In well-oxygenated bottom waters, enhanced organic
matter fluxes and decomposition rates result in steepening δ13CDIC gradients in the uppermost sediment, which is then
reflected by the δ13C difference between epifaunal and shallow
infaunal (e.g., Uvigerina) species (Zahn et al., 1986; Mackensen et
al., 2000; Brückner and Mackensen, 2008). A simple relation between
observed δ13C gradients and organic matter fluxes is obscured by
the ability of infaunal species to shift their microhabitat in response to
changing trophic conditions (Schmiedl and Mackensen, 2006; Theodor et al.,
2016). Interspecific differences in the δ13C composition of benthic
foraminifera are further influenced by species-specific “vital effects”,
which can be as large as 1 ‰ (Schmiedl et al., 2004; McCorkle et
al., 2008; Brückner and Mackensen, 2008) and are a reflection of
metabolic processes and test calcification rates (McConnaughey, 1989a, b). Of
minor impact, but still traceable, is the influence of carbonate ion
concentration and alkalinity gradients in pore waters (Bemis et al., 1998).
Finally, significant ontogenetic δ13C trends have been documented
for certain taxa, particularly for the genera Uvigerina and
Bolivina (Schmiedl et al., 2004; Schumacher et al., 2010; Theodor et
al., 2016).
Location of the study areas in the Mediterranean Sea and regional
bathymetric maps with locations of sample sites in the (a) Mallorca
Channel, (b) Alboran Sea, (c) Gulf of Lion and Spanish
slope off Barcelona, (d) Strait of Sicily, and (e) Aegean
Sea.
The complexity of factors influencing the stable isotope composition of
deep-sea benthic foraminifera and differences between species in different
depths in the sediment motivates isotopic studies on living foraminifera in
relation to their biology and microhabitat. In particular, combined
ecological and biogeochemical studies on a statistically relevant number of
sites and on live specimens from areas with well-defined environmental
gradients are required for the establishment of reference data sets and
transfer functions that could then be used for a more quantitative assessment
of organic matter fluxes. The Mediterranean Sea is particularly suitable for
such a study because the present deep-sea environments are characterized by
systematically high oxygen contents along a gradient of trophic differences.
In all basins, subsurface water masses are highly oxygenated with O2
concentrations of greater than 160 µmol kg-1 due to frequent
replenishment of intermediate water in the Levantine Sea and deep water in
the Gulf of Lion, Adriatic Sea, and Aegean Sea (Wüst, 1961; Lascaratos
et al., 1999; Pinardi and Masetti, 2000; Tanhua et al., 2013; Pinardi et al.,
2015). The inflow of nutrients with Atlantic surface waters causes an overall
west–east gradient in primary production, from values of about
225 g C m-2 yr-1 in the Alboran Sea to about
40 g C m-2 yr-1 in the extremely nutrient-depleted oligotrophic
Levantine Basin (Bosc et al., 2004; López-Sandoval et al., 2011; Puyo-Pay et
al., 2011; Huertas et al., 2012; Tanhua et al., 2013, Gogou et al., 2014). In
areas influenced by nutrient input of larger rivers and Black Sea outflow,
primary production can be locally enhanced, for example, leading to a trend of
decreasing primary production values along a north–south transect in the Aegean Sea
(Lykousis et al., 2002; Skliris et al., 2010). In addition, resuspension and
lateral transport of organic matter can lead to locally enhanced food
availability in submarine canyons and isolated basins (Puig and Palanques,
1998; Danovaro et al., 1999; Heussner et al., 2006; Canals et al., 2013).
In this study, we have compiled a data set on the stable carbon isotope
composition of living and dead individuals of three epifaunal species
(Cibicidoides pachydermus, Planulina ariminensis,
Cibicides lobatulus), and one shallow infaunal species
(Uvigerina mediterranea) from 19 Mediterranean sites. The sites are
located in a well-defined depth interval (between 400 and 1500 m) and
represent a wide range of trophic conditions. Adjusted for ontogenetic
effects, the Δδ13CUmed-Epi signal was compared to
the microhabitat of U. mediterranea, the depth of the main redox
boundary, TOC content, and organic carbon flux rates calculated from
satellite-derived primary production or (if available) flux measurements from
sediment trap studies. Major objective of this study is the development and
evaluation of a transfer function for organic matter fluxes applicable to the
quantification of past trophic changes in the Mediterranean Sea.
Material and methods
This study is based on a compilation of new and published isotope data of
multicorer samples retrieved from various Mediterranean sub-basins covering a
water depth range of 424 to 1466 m (Table 1). The study areas include the
Alboran Sea and the Mallorca Channel (R/V Meteor cruise M69/1 in
August 2006, Hübscher et al., 2010; data published in Theodor et al.,
2016); the Gulf of Lion, Spanish slope off Barcelona, and Strait of Sicily
(M40/4 in February 1998, Hieke et al., 1999; this study and data published in
Schmiedl et al., 2004); and the Aegean Sea (M51/3 in November 2001, Hemleben
et al., 2003; this study) (Fig. 1). For each station, the sediment color
change from yellowish brown to greenish gray was used as an indicator for the
change in redox potential from positive to negative values, which serves as
an approximation of oxygen consumption and penetration in the surface
sediment (Lyle, 1983; Schmiedl et al., 2000).
Position, water depth, median living depth (MLD) of Uvigerina mediterranea, geochemical,
primary production (PP), and Corg flux values of the investigated
multicorer sites. Annual PP values are averages for the year prior to
sampling after data from the GlobColour project. Corg fluxes were
calculated after Betzer et al. (1984) and the MLD after Theodor et al. (2016).
The upper 10 cm of the sediment were commonly sliced into 0.5 to 1 cm
intervals (in the Aegean Sea into coarser intervals below 3 cm) and all
samples were subsequently preserved in rose-bengal-stained alcohol (1.5 g rose
bengal per 1 L of 96 % ethanol) in order to stain cytoplasm of living or
recently living foraminifera (Walton, 1952; Bernhard, 2000). In the
laboratory, the sediment samples were wet sieved over a 63 µm sieve
and, after drying at 40 ∘C, dry sieved over a 150 µm
(Aegean Sea samples) or 125 µm (remaining samples) mesh,
respectively. From the coarse fraction of the different down-core intervals,
stained individuals of selected epifaunal and shallow infaunal taxa were
counted and the median living depths (MLDs; Theodor et al., 2016) were
calculated as references for the respective microhabitat preferences. Only
tests with at least three subsequent brightly red-colored chambers were
considered as living. The low number of stained individuals of epifaunal taxa
impeded analyses, except at Site 540B, where stained tests of C. pachydermus were available. Likewise, stained tests of U. mediterranea were absent at Sites 586 and 589.
(a) The δ13C of epifaunal species
(Cibicidoides pachydermus, Cibicides lobatulus,
Planulina ariminensis) for each investigated site. Each symbol
represents a single measurement. Red symbols mark relocated or fossil tests
that have not been used to calculate δ13CEpi. Green
circles show δ13CEpi values used as an approximation of the
δ13C of bottom water DIC. Details on the selection of tests and
procedure for the estimation of δ13CEpi values are
discussed in Sect. 4.1. (b) The δ13CEpi vs.
water depth shows a wider scattering for the Aegean Sea than for the western
Mediterranean Sea. Colored lines in the background indicate water mass end
members of the Mediterranean Sea after Pierre (1999).
For stable isotope measurements, stained tests (and unstained tests if no
stained tests were available) of three epifaunal species (C. pachydermus, P. ariminensis, C. lobatulus) and one shallow
infaunal species (U. mediterranea) were selected and each test was
measured using an optical micrometer with an accuracy of 10 µm. In
total, 2 stained and 63 unstained epifaunal tests as well as 155 stained and
197 unstained tests of U. mediterranea were measured. Individual
numbers of tests measured were 1–6 for C. pachydermus, 1–5 for
P. ariminensis, 1–5 for C. lobatulus, and 1–8 for
U. mediterranea. The stable carbon and oxygen isotope measurements
were performed at the Alfred Wegener Institute, Helmholtz Centre for Polar
and Marine Research at Bremerhaven with two Finnigan MAT 253 stable isotope
ratio mass spectrometers coupled to automatic carbonate preparation devices
(Kiel IV). The mass spectrometers were calibrated via international standard
NBS 19 to the PDB scale, with results given in δ notation vs.
VPDB. Based on an internal laboratory standard (Solnhofen limestone) measured
over a 1-year period together with samples, the precision of stable isotope
measurements was better than 0.06 and 0.08 ‰ for carbon and oxygen,
respectively. The δ13C difference between epifaunal and shallow infaunal
taxa was calculated as a proxy for the difference in δ13C in DIC of
bottom and shallow pore water. For U. mediterranea, this procedure
was restricted to measurements from the size fraction
greater than 600 µm in order to minimize ontogenetic effects
(Schmiedl et al., 2004; Theodor et al., 2016).
Total organic carbon (TOC) concentration in the surface sediment was measured
with a Carlo Erba 1500 CNS analyzer with a precision of 0.02 % on
weighted sample splits in tin capsules. Before measurement, CaCO3 was
removed from these weighted samples by adding 1N HCl. The TOC values of Sites
596, 601, and 602 were taken from Möbius et al. (2010a, b). Bottom water
oxygen concentrations are based on CTD measurements stored in the MedAtlas
data set. Primary productivity values in surface waters of the year preceding
the sampling at each site are based on satellite data of the GlobColour
project, and were calculated with the algorithms of Antoine and Morel (1996)
as well as Uitz et al. (2008). If available, these estimates were compared
with nearby direct primary productivity and export flux measurements. The
export fluxes down to the sea floor were estimated according to the function
of Betzer et al. (1984) adapted by Felix (2014).
Correlation between δ13CUmed and δ13CEpi difference (Δδ13CUmed-Epi)
and size classes of U. mediterranea. For better clarity and due to the large number of
measured data (Table 1), the linear regressions for each
site are given, showing clear ontogenetic trends in δ13CUmed due to size-independent δ13CEpi values.
The shown data are from live (rose-bengal-stained) and dead (unstained)
individuals of U. mediterranea as well as for the western Mediterranean Sea (left) and
Aegean Sea (right). Dashed lines represent already published data (Schmiedl
et al., 2004; Theodor et al., 2016).
Results
Benthic foraminiferal δ13C values of our samples cover a range of
more than 3 ‰, with higher average values of epifaunal species than
shallow infaunal Uvigerina mediterranea (Table 2). The epifaunal
species Cibicidoides pachydermus, Cibicides lobatulus, and
Planulina ariminensis show average values between 1.90 ‰ at
Site 586 (southern Aegean Sea) and -0.16 ‰ at Site 347 (Mallorca
Channel) (Table 2, Fig. 2). The highest average epifaunal δ13CEpi values are in the southern and central Aegean Sea (Sites 586,
595), while further to the north at Site 602 (northern Aegean Sea) the
average δ13CEpi value of 0.87 ‰ is among the
lowest measured. At Site 540B in the Gulf of Lion, the average δ13CEpi value of 1.01 ‰ is in good agreement with
1.00 ‰ measured by Schmiedl et al. (2004) at the same site.
Size-dependent measurements did not reveal any ontogenetic trend in the
δ13C signal of the epifaunal taxa (Table S1 in the Supplement).
Average stable carbon isotope composition of selected benthic
foraminifera with standard deviations. Bold values of epifaunal
species were applied to estimate δ13CEpi. Also given are
values for Uvigerina mediterranea tests larger than 600 µm and the difference of this
species compared to the average epifaunal stable carbon isotope ratios
(Δδ13CUmed-Epi).
For U. mediterranea, δ13CUmed values vary between
-1.41 and 0.85 ‰ for stained tests and between -1.52 and
1.77 ‰ for unstained tests (Table 1). The highest
average values are recorded in the southern Aegean Sea, with 0.58 and
1.11 ‰ for stained and unstained tests, respectively. The lowest
average values are recorded for the northern Aegean Sea, with -0.98 and
-1.13 ‰ for stained and unstained tests, respectively. The
variability at a single site reaches 1.38 ‰ in stained (Site 537)
and 2.21 ‰ in unstained tests (Site 586). The ontogenetic
δ13CUmed trends are generally comparable in the western
Mediterranean Sea and the Strait of Sicily, with
0.11 ± 0.03 ‰ 100 µm-1 for stained and
0.07 ± 0.03 ‰ 100 µm-1 for unstained tests,
except for Site 396 that shows an anomalous negative trend (Table 3, Fig. 3).
In the Aegean Sea, the ontogenetic δ13CUmed trends are
approximately 50 % steeper with an increase of
0.16 ± 0.04 ‰ 100 µm-1 for stained tests.
Unstained tests reveal a higher variability and a less steep slope of
0.10 ± 0.07 ‰ 100 µm-1 (Table 3, Fig. 3). In
order to avoid bias due to ontogenetic effects, only δ13C values of
U. mediterranea tests larger than 600 µm were used for
comparison with δ13CEpi values.
Linear regressions of ontogenetic trends of δ13CUmed. The measured number of stained and unstained tests as
well as the significance values are added.
The δ13C difference between live Uvigerina mediterranea and epifaunal taxa (Δδ13CUmed-Epi)
plotted against (a) MLD of U. mediterranea, (b) depth of redox boundary in the sediment, and
(c) TOC content of the sediment. The MLD
error bars for the canyon and slope sites in the Gulf of Lion reflect the
seasonal MLD contrasts of U. mediterranea between February and
August 1997 (Schmiedl et al., 2004).
The calculated Δδ13CUmed-Epi values for stained
tests range from -0.64 ‰ in the Gulf of Lion (slope site) and
-0.74 ‰ (Site 585) to -1.29 ‰ in the western
Mediterranean Sea (Sites 347 and 540A) to -1.85 ‰ in the northern
Aegean Sea (Site 602) (Table 2). Due to the wider scattering of the
δ13C values of unstained tests, Δδ13CUmed-Epi values range from -0.61 ‰ (Site 589) to
-2.0 ‰ (Site 602) in the Aegean Sea and from
-0.55 ‰ (Site 540B) to -1.06 ‰ (Site 339) in the western
Mediterranean Sea and the Strait of Sicily (Table 2). The magnitude of
Δδ13CUmed-Epi values exhibits a relation with
trophic conditions at each site, revealing higher values at more eutrophic
sites.
The median living depth of the shallow infaunal U. mediterranea
(MLDUmed) is used here to describe its microhabitat and generally
increases at sites with deep main redox boundaries, at least in the western
Mediterranean Sea. The deepest MLDUmed are 2.13 and 2.25 cm in the
southern Aegean Sea, while the shallowest depths of 0.27 and 0.38 cm are
recorded in the central and northern Aegean Sea, respectively (Table 1). In
the Gulf of Lion, the MLDUmed is between 0.43 and 0.49 cm in the
axis of the Lacaze–Duthiers Canyon and around 1.22 cm on the open slope
(Table 1, Fig. 4a). The depth of the sediment color change, which marks the
shift in redox potential and thus oxygen penetration, ranges from 2.25 cm in
the Gulf of Lion (Site 540A) to as much as 30 cm in the central Aegean Sea
(Site 596) (Table 1, Fig. 4b). The measured TOC contents of the surface
sediment range from 0.41 % (Site 586, southern Aegean Sea) and 0.58 %
(Site 537, Strait of Sicily) to a maximum of 0.82 % (Site 602, northern
Aegean Sea) (Table 1, Fig. 4c). The Δδ13CUmed-Epi
and the MLDUmed (Fig. 4a) as well as the main redox boundary depth
(Fig. 4b) show good correspondence, whereas the link to percentage of TOC is less
distinct (Fig. 4c).
The estimated values for annual primary production (PP) range from 106 to
294 g C m-2 a-1. Application of the different algorithms of
Antoine and Morel (1996) and Uitz et al. (2008) resulted in an average offset
of 54 g C m-2 a-1, with PP values consistently higher when
applying the algorithm of Antoine and Morel (1996). The highest PP values
occur in the Alboran Sea (274–294 vs. 192–207 g C m-2 a-1
according to Uitz et al., 2008) and the northern Aegean Sea (196–237 and
139–164 g C m-2 a-1, respectively), while the lowest PP values occur in the
southern and central Aegean Sea (151–161 and 106–116 g C m-2 a-1, respectively) (Table 1).
DiscussionStable carbon isotope signal of epifaunal foraminifera in relation to
surrounding water masses
The δ13C of Cibicidoides pachydermus, Cibicides lobatulus, and Planulina ariminensis seems to reflect the δ13CDIC of the ambient bottom water since these species prefer an
epifaunal microhabitat (Lutze and Thiel, 1989; Kitazato, 1994; Schmiedl et
al., 2000). Comparison with published water δ13CDIC
measurements confirms that δ13CEpi values are a possible
bottom water proxy for the Mediterranean Sea (Pierre, 1999; Schmiedl et al.,
2004; Theodor et al., 2016). Further, our new data corroborate previous
observations that ontogenetic effects in the δ13CEpi
signal of these taxa are lacking (Corliss et al., 2002; Franco-Fraguas et
al., 2011; Theodor et al., 2016) (Table S1).
Because of the lack of stained epifaunal tests at most sites, unstained tests
were integrated into the analysis. For empty tests, a shift to higher
δ13CEpi values due to potential dissolution effects should
be considered (Edgar et al., 2013). In addition, reworked or allochthonous
tests can bias the results as documented for the δ13CCpachy of Site 396 in the Mallorca Channel. At this site, fossil
tests have been admixed in the surface sediment as indicated by heavy
δ18O values of greater than 4.0 ‰ (Table S1). In the
Alboran Sea (Sites 339 and 347), we measured interspecific epifaunal
δ13C differences of up to 1.4 ‰. This variability is a
result of implausibly low δ13CClob values, probably due to
a relocation from shallower depths closer to the coast. These unrealistic
δ13CCpachy and δ13CClob values were
omitted for δ13CEpi estimation. In order to minimize these
biases, a large number of tests were measured, which was possible for
C. pachydermus and P. ariminensis, showing commonly
0.3–0.5 ‰ higher δ13C values for the latter species
(Table 2, Fig. 2a). Despite the aforementioned uncertainties, data of
C. lobatulus were used to estimate δ13CEpi at the
Mallorca Channel Sites 394 and 395, when no tests of other species were
available for analysis (Theodor et al., 2016). For proper δ13CEpi estimation of Sites 394 and 395, the difference between
δ13CPari and δ13CClob (Δδ13CPari-Clob= 0.30 ‰) at Site 396 was added to the
δ13CClob values (Table 2, Fig. 2a).
The δ13C offset between C. pachydermus and P. ariminensis is not constant and appears to increase at sites with deep main
redox boundaries. This suggests a connection with increasing organic matter
availability and the varying offsets can be attributed to slight differences
in their microhabitat (Table 2, Fig. 2a). While P. ariminensis is a
strictly epifaunal species, living attached on surfaces or above the sediment
(Lutze and Thiel, 1989), C. pachydermus commonly lives at or
slightly below the sediment–water interface (Rathburn and Corliss, 1994;
Schmiedl et al., 2000; Licari and Mackensen, 2005). A very shallow infaunal
microhabitat of C. pachydermus is corroborated by slightly lower
δ13C values relative to bottom water δ13CDIC
suggesting pore water influence (Schmiedl et al., 2004; Fontanier et al.,
2006). In order to compensate for potential pore water effects in the
δ13C signal of the epifaunal species, the highest δ13CEpi values, mostly of P. ariminensis, should be selected
for further comparison with shallow infaunal δ13CUmed
signals. This strategy could not always be realized, either due to the lack
of P. ariminensis (Sites 537, 601, canyon, and slope) or when lower
δ13C values were recorded for P. ariminensis relative to
C. pachydermus (Site 540C). In these cases, bottom water δ13CDIC measurements (canyon, slope; data from Schmiedl et al., 2004),
the addition of the Δδ13CPari-Cpachy value of the
nearby Site 602 (for correction of Site 601) or the δ13CCpachy
values (Sites 537, 540C) were used, accepting possible deviations of
δ13CEpi from bottom water δ13CDIC
(Table 2).
The applied δ13CEpi values are related to different
Mediterranean water masses (Fig. 2b). The δ13CEpi values
of the Gulf of Lion and the Spanish continental slope off Barcelona are
around 1.0 ‰ matching the δ13CDIC signature of
upper western Mediterranean deep water (WMDW) (Pierre, 1999). Likewise, the
slightly higher δ13CEpi values of 1.1 ‰ in the
Strait of Sicily fall in the range of δ13CDIC values of
intermediate waters from the eastern Mediterranean Sea and reflect the
transitional setting of this area. In contrast, the δ13CEpi values of the Mallorca Channel and the Alboran Sea are even
higher than those recorded for the eastern Mediterranean Sea (Fig. 2b). This
inconsistent isotope pattern likely reflects a shift in deep-water formation
in the eastern Mediterranean during the 1990s, the so-called Eastern
Mediterranean Transient (EMT; Roether et al., 2007). The EMT was accompanied
by an enhanced deep-water formation in the Aegean Sea and also fostered a
complete renewal of WMDW during the
mid-2000s (Schroeder et al., 2006, 2008). Unfortunately, the imprint of WMDW
change on δ13CDIC of the water mass was not documented,
but it should have affected the sites sampled after this transition, i.e.,
during Meteor cruise M69/1 in 2006.
The broad range of recorded δ13CEpi values of 0.87 to
1.95 ‰ in the Aegean Sea reflects the strong small-scale
oceanographic differences of this region, including presence of various small
isolated basins (Figs. 1, 2b). The comparatively high δ13CEpi
values of the shallower sites indicate intensified vertical
convection at sites of subsurface water formation, which recently resumed
after the stagnation phase of 1994–2000 (Androulidakis et al., 2012),
although the main deep-water formation area is restricted to the Cretan Sea
(Roether et al., 1996; Lascaratos et al., 1999). Reduced replenishment of
bottom waters at greater depth of isolated basins (Zervakis et al., 2003;
Velaoras and Lascaratos, 2005) is accompanied by relatively low δ13CDIC and accordingly low δ13CEpi values in these
environments.
Biological and environmental effects on the stable carbon isotope
signal of Uvigerina mediterranea
Size-dependent changes in the δ13C signal of Uvigerina mediterranea are attributed to ontogenetic effects. Small tests are depleted
in 13C, while larger tests are closer to δ13CDIC of
the ambient pore water (Fig. 3). Relatively low δ13CUmed values of small tests suggest stronger metabolic fractionation in
younger individuals (Schmiedl et al., 2004; McCorkle et al., 2008; Schumacher
et al., 2010; Theodor et al., 2016). A linear ontogenetic increase of
0.11 ‰ 100 µm-1 was observed at all sites of the
western Mediterranean Sea, while a steeper slope of 0.16 ‰
100 µm-1 was recorded in the Aegean Sea (Fig. 3). In addition,
the δ13CUmed values of small individuals from the Aegean
Sea were of order 1 ‰ lower compared to those from the western
Mediterranean Sea.
Differences in ontogenetic δ13C slopes of the related species
U. peregrina have been attributed to its highly opportunistic
response to regional contrasts in organic matter quantity and quality, and
seasonality of supply (Theodor et al., 2016). Obviously, similar effects are
also operational in ontogenetic δ13C trends of U. mediterranea. In the Aegean Sea, this species appears to respond to strong
seasonal contrasts in organic matter fluxes (Siokou-Frangou et al., 2002)
resulting in particularly high metabolic activity and low δ13CUmed
values in young individuals. A steepening of the δ13CUmed slopes
from the north to the south Aegean Sea probably occurs for the
same reasons as U. peregrina in the western Mediterranean Sea.
Because of the higher number of measured tests, this shift of the slope
angles is more obvious in unstained than stained tests (Fig. 3). Although the
number of sites was larger than in Theodor et al. (2016), a similar trend in
δ13CUmed is not recognizable for the western Mediterranean
Sea. This may express lower differences in the seasonal food supply between
the sites or the total higher input of organic matter compared to the
Aegean Sea.
The δ13CUmed of unstained individuals from 5 cm sediment
depth in the western Mediterranean Sea and Strait of Sicily are on average
0.1 to 0.2 ‰ lower than those of stained specimens in the topmost
centimeter. This adds to previous observations of Theodor et al. (2016)
suggesting the influence of the Suess effect (Keeling, 1979; Quay et al.,
1992) in living individuals while it is absent in some 100-year-old specimens. The
Suess effect reduces δ13C values in the atmosphere and oceans due
to the anthropogenic release of isotopically light CO2 out of fossil
fuels. A similar effect was not seen in the Aegean Sea since live and dead
individuals were selected from the same sediment depth and thus had only
minor age differences (Table 2, Fig. 3). The only exception is Site 595 in
the central Aegean Sea, where the deviation is even higher
(0.5–0.7 ‰) when compared to the western Mediterranean Sea. Since
this signal is restricted to only one site, it is probably due to relocation
of fossil tests by the effects of bioturbation or lateral sediment transport.
The δ13C difference between live and dead
Uvigerina mediterranea and epifaunal taxa (Δδ13CUmed-Epi) against organic carbon flux rates (Corg flux)
calculated from primary productivity in surface waters after Betzer et
al. (1984). As in Fig. 4, satellite-derived primary production values of
Antoine and Morel (1996) (top) and Uitz et al. (2008) (bottom) were used.
Under well-oxygenated conditions, the pore water δ13CDIC
gradient depends on the organic matter fluxes and associated decomposition
rates of organic matter in the surface sediment (McCorkle and Emerson, 1988;
McCorkle et al., 1985, 1990; Holsten et al., 2004). Organic matter fluxes
also control the depth of the oxygenated layer (Rutgers van der Loeff, 1990)
and thus the microhabitat range of infaunal foraminifera (Corliss, 1985;
Jorissen et al., 1995; Koho et al., 2008; Koho and Pina-Ochoa, 2012).
Subsurface waters in the Mediterranean Sea are well ventilated resulting in
bottom water oxygen concentrations above 4.1 mL L-1 at all sites in
our study (MedAtlas, 1997). The δ13C signal of U. mediterranea appears particularly suitable to monitor the pore water δ13CDIC signal in the near-surface sediment because it seems to
be less influenced by species-specific vital effects (McConnaughy, 1989a,
b) when compared to other shallow infaunal taxa (for example, U. peregrina) (Schmiedl et al., 2004; Theodor et al., 2016).
In this study, the deviation of δ13CUmed from bottom water
δ13CDIC (reflected as higher Δδ13CUmed-Epi values; Fig. 4) suggests exponential relations with the
MLD of U. mediterranea, the depth of the oxygenated layer, and
the TOC content of the surface sediment. At the more oligotrophic to
mesotrophic sites of the Mallorca Channel, the Gulf of Lion, the Spanish
slope off Barcelona, and the southern Aegean Sea, relatively low Δδ13CUmed-Epi values correspond to a relatively thick
oxygenated layer and low TOC contents. The rather deep position of the redox
boundary, exceeding 10 cm at some sites, enables U. mediterranea to
inhabit a relatively wide microhabitat range. In contrast, relatively high
Δδ13CUmed-Epi values at the more mesotrophic to
eutrophic sites of the Alboran Sea coincide with relatively thin oxygenated
layers and higher TOC contents. Here, the microhabitat range of U. mediterranea is compressed because of limited pore water oxygen (Fig. 4).
When comparing sites within the central and northern Aegean Sea, the
foraminiferal stable isotope difference and the biogeochemical and ecological
characteristics lack a consistent relation (Fig. 4). In these areas, strongly
negative Δδ13CUmed-Epi values do not systematically
correspond to maximum TOC contents and the shallowest redox boundary
(Fig. 4). The reasons for this absence of a clear relation between Δδ13CUmed-Epi and environmental parameters within this area
cannot be unraveled with our data. It may be related to the high variability
in oceanographic and biogeochemical conditions of the bottom water in the
isolated basins that are characterized by focusing of organic-rich
sedimentary material (Lykousis et al., 2002; Giresse et al., 2003; Poulos,
2009) and/or temporarily intermittent replenishment of deep waters on
seasonal to decadal timescales (Zervakis et al., 2003; Velaoras and
Lascaratos, 2005; Androulidakis et al., 2012). The first possibility can
increase the supply of refractory Corg, recorded by higher TOC
contents, and influence the foraminiferal microhabitat depths, but has minor
effects on the δ13CDIC pore water gradient. Latter
possibility refers to local ventilation events, which exchange aged bottom
water with comparatively low δ13CDIC signature by surface
waters enhanced in 13CDIC. This may also push the pore water
gradient towards stronger differences, explaining the more negative Δδ13CUmed-Epi values, compared to the remaining sites with
similar conditions (Fig. 4).
Development of a stable carbon-isotope-based transfer function for
organic carbon fluxes
Our results suggest a close relationship between the δ13C gradient
in pore waters of the surface sediment (expressed as Δδ13CUmed-Epi) and the OM fluxes to the sea floor, for
open-ocean settings of the western and central Mediterranean Sea and the
southern Aegean Sea (Fig. 5). Based on these observations, we tested the
potential for the development of a δ13C-based transfer function
for OM flux rates. In open-ocean settings, the main food source of deep-sea
environments is the exported OM from the surface layer, where photosynthetic
PP takes place (e.g., Boyd and Trull, 2007; Bishop,
2009). The majority of produced particulate organic carbon (POC) is recycled
within the photic zone. In the open Mediterranean Sea, around 4 % of the
POC is exported out of the photic zone, which is lower than for other open
oceans, caused by a specific nutrient distribution in the Mediterranean Sea
(Moutin and Raimbault, 2002; Gogou et al., 2014). The remineralization of
organic matter is intensified, which leads to reduced fluxes to the sea
floor.
During transfer from the surface ocean to the deep sea, the amount of
exported OM decreases exponentially reflecting microbial decay (Suess, 1980;
de la Rocha and Passow, 2007; Packard and Gomez, 2013). Various functions
have been developed for the estimation of OM fluxes during sinking of
particles through the water column integrating numerous observational data
(Suess, 1980; Betzer et al., 1984; Martin et al., 1987; Antia, et al., 2001).
The different functions reveal a high variability for the active surface
layer, while the results for deeper parts of the water column are within a
comparable range (Felix, 2014). In our study (Table 1, Fig. 5), we applied
the function of Betzer et al. (1984) for calculating the depth-dependent
Corg fluxes at the different Mediterranean sites using
satellite-derived PP data (Antoine and Morel, 1996; Uitz et al., 2008).
A comparison with direct PP and export flux measurements of sediment trap
studies revealed ambiguous results. The PP values calculated after Antoine
and Morel (1996) are in a comparable range to PP measurements in the western
Mediterranean (Moutin and Raimbault, 2002; Sanchez-Vidal et al., 2004, 2005;
Zúñiga et al., 2007, 2008). However, the estimated export fluxes are
too high in these areas compared to direct measurements of the referred
studies, probably due to the aforementioned high remineralization rate in the
Mediterranean Sea. However, the discrepancy in export fluxes is partly
compensated by the application of the 21–30 % lower PP values calculated
after Uitz et al. (2008). For the Aegean Sea, in contrast, distinctively
higher measured PP values have been reported than were estimated
(Siokou-Frangou et al., 2002). For the Gulf of Lion, measured OM export
fluxes exceed the predicted values (Heussner et al., 2006), which can be
explained by the additional lateral input of organic carbon channeled within
the local canyon systems (Schmiedl et al., 2000). In order to compensate for
these possible additional Corg fluxes in marginal basin areas, the
application of the function of Antoine and Morel (1996) is more promising;
hence, a potential overestimation of Corg fluxes in open-ocean areas
has to be considered.
For both approaches of PP calculation (Antoine and Morel, 1996; Uitz et al.,
2008), the relation between the estimated Corg fluxes and the
Δδ13CUmed-Epi exhibits a complex pattern and, at
first instance, lacks a simple and statistically significant correlation
(Fig. 5). Particularly, strongly negative Δδ13CUmed-Epi in the central and northern Aegean Sea suggest high
Corg fluxes, which however are not reflected in the estimated
PP-based values. The eventual underestimation of Corg fluxes in
these more marginal areas is likely caused by additional lateral OM input and
the focusing of organic matter in isolated small basins. In fact, the
northern and central Aegean Sea experiences high OM input from terrestrial
sources through outflow of north Aegean rivers and the Black Sea (Aksu et
al., 1999; Tsiaras et al., 2012). In contrast, the measured main redox
boundary depth and the TOC contents do not indicate a higher supply in
organic matter. However, sediment trap data from the northern Aegean Sea
(Lykousis et al., 2002) reveal Corg fluxes of
35–81 g C m-2 a-1, which are 3–10 times higher than
estimated values solely based on PP-based vertical fluxes. Although the high
measured values can be partly attributed to the short sampling interval of
2 months in late spring and thus to elevated vertical fluxes during the
spring bloom, elevated year-round lateral Corg fluxes can be
expected, but of a clearly lower dimension. The measured ratio of primary to
reworked OM in the sediment at this site is around 60–70 % (Lykousis et
al., 2002; Poulos, 2009), which leaves the PP as the main source of the
Corg fluxes to the deep sea. Similar results have been derived for
canyon systems of the Gulf of Lion where OM resuspension, shelf-to-slope
cascading, and channeling results in significantly higher observed than
PP-derived estimated Corg fluxes (Heussner et al., 2006; Pusceddu
et al., 2010, Pasqual et al., 2010). Even in open slope settings, resuspended
OM can significantly contribute to the total Corg flux (McCave et
al., 2001; Tesi et al., 2010; Stabholz et al., 2013).
Despite these biases, it appears reasonable to develop a Corg flux
transfer function at least for the more open marine settings of the western
and central Mediterranean Sea and the southern Aegean Sea (Fig. 6). Here,
vertical sinking of PP-derived OM appears to be the main source for
Corg fluxes (Pusceddu et al., 2010) explaining the good correlation
with the Δδ13CUmed-Epi values (Fig. 5). Elevated
Corg fluxes of the upwelling-affected Alboran Sea
(Hernandez-Almeida et al., 2011) are reflected in rather negative Δδ13CUmed-Epi values while the observed δ13C
differences in the more oligotrophic regions of the Mallorca Channel, the
Spanish slope off Barcelona, the Strait of Sicily, and the southern Aegean
Sea are lower. So, omitting the data from the northern and central Aegean
Sea, and considering sediment trap data from the Gulf of Lion (Heussner et
al., 2006) the derived function can be expressed as
Corgflux=-15.99×Δδ13CUmed-Epi+0.34,
with a coefficient of determination (R2) of 0.63 and a significance (p)
of 0.0021 (Fig. 6). The estimated Corg fluxes can be used to
recalculate marine PP, but should be handled carefully due to the highly
possible overestimation caused by lateral advection. Especially in more
marginal areas, this bias can lead to unreliable recalculated PP values.
Correlation of the δ13C difference between live
Uvigerina mediterranea and epifaunal taxa (Δδ13CUmed-Epi) and organic carbon flux rate (Corg flux)
calculated according to Antoine and Morel (1996) and Betzer et al. (1984).
Transparent data from the central and northern Aegean Sea and the Gulf of
Lion have been removed from the function since PP-based Corg flux
values are likely underestimated because of the additional influence of
lateral organic matter fluxes on the δ13CUmed values in
these areas.
The application of this function to unstained U. mediterranea tests
creates a higher range of uncertainty. The main reason for this inconsistency
seems to be the relocation of fossil tests at particular sites, leading to
significant contrasts between δ13CUmed values of stained
and unstained tests. For empty U. mediterranea tests, marked
negative δ13CUmed outliers appear at Sites 537 and 396,
which has already been mentioned in Theodor et al. (2016) for the latter
site. In the Alboran Sea (Sites 338 and 347) on the other hand,
δ13CUmed values of unstained tests are about
0.50 ‰ higher than those of stained tests. Less distinct
δ13CUmed differences between autochthonous and
allochthonous tests may not be detected so easily. These potential
uncertainties have to be considered in the application of the transfer
function to sediment cores, particularly to down-core records from sites
influenced by strong lateral transport such as canyon environments or the
northern and central Aegean Sea. Likewise, the application of the transfer
function to areas outside of the Mediterranean Sea may be biased by
contrasting remineralization rates due to the specific oceanographic
conditions, especially the higher temperatures in the Mediterranean Sea.
Further refinement of this function will require an interdisciplinary effort
including a larger number of direct Corg flux measurements in
sediment trap deployments, which can be directly related to the obtained
foraminiferal δ13C signals.
Conclusions
The δ13C signal of deep-sea benthic foraminifera from different
areas of the western, central, and eastern Mediterranean Sea reflects an
integration of various environmental and biological signals. The application
of epifaunal benthic foraminifera as an unbiased proxy for the δ13CDIC
of the surrounding water mass is ambiguous due to possible
allochthonous tests, but also due to a slight species-specific difference in the
microhabitat that can result in significant δ13CEpi
shifts. The δ13C signal of the strictly epifaunal Planulina ariminensis should be preferred, in contrast to the δ13C signal of
the less strictly epifaunal Cibicidoides pachydermus, which appears
to be influenced by pore water DIC and its δ13C value.
The δ13C signal of epifaunal taxa lacks ontogenetic effects
supporting results from previous studies (Dunbar and Wefer, 1984; Corliss et
al., 2002; Theodor et al., 2016). Significant ontogenetic effects were
recorded in the δ13C signal of Uvigerina mediterranea.
While the ontogenetic increase of δ13CUmed is more or
less comparable (0.11 ± 0.03 ‰ 100 µm-1) in the
western Mediterranean and the Strait of Sicily, a stronger increase and even
a regional south–north trend is documented for the Aegean Sea
(0.16 ± 0.04 ‰ 100 µm-1). In general, the
δ13C values of U. mediterranea from the Aegean Sea are
more negative when compared to those from the western and central
Mediterranean Sea. This regional contrast cannot be reconciled with different
vital and pore water effects but instead seems to be caused by enhanced
residence times of bottom waters in the partly isolated small basins within
the Aegean Sea. In cases of well-oxygenated conditions, the
δ13CUmed signal, compared to bottom water, is mainly
controlled by regional trophic contrasts and related remineralisation rates.
The Δδ13CUmed-Epi are clearly related to the median
microhabitat depth, the depth of the redox boundary (indicating the extent of
the oxygenated layer), and (to a lower extent) to the TOC of the surface
sediment. Based on satellite-derived primary production estimates
Corg fluxes were calculated and related to the recorded Δδ13CUmed-Epi values. Comparison with sediment trap data
reveals underestimation of satellite-derived Corg fluxes for the
marginal areas of the central and northern Aegean Sea and the canyon systems
of the Gulf of Lion. In these ecosystems, additional lateral transport of
resuspended and terrestrial OM contributes substantially to Corg
fluxes. Considering these biases, a first estimation for Corg fluxes
in open-ocean settings of the Mediterranean Sea could be established.
Data availability
The main data source (stable isotope data) of this work is within the appendix.
List of benthic foraminiferal taxa used in this study Cibicides lobatulus (Walker and Jakob)Nautilus lobatulus (Walker and Jacob, 1798, p. 642, pl. 14, Fig. 36)Cibicidoides pachydermus (Rzehak)Truncatulina pachyderma (Rzehak, 1886, p. 87, pl. 1, Fig. 5)Planulina ariminensis (d'Orbigny)Planulina ariminensis (d'Orbigny, 1826, p. 280, pl. 14, Figs. 1–3)Uvigerina mediterranea (Hofker)Uvigerina mediterranea (Hofker, 1932, pp. 118–121, Fig. 32)
The Supplement related to this article is available online at doi:10.5194/bg-13-6385-2016-supplement.
Acknowledgements
We would like to thank K.-C. Emeis and two anonymous referees for their
helpful remarks and suggestions. We thank the ship crews and scientists of
the R/V Meteor for good collaboration during cruises M40/4, M51/3, and M69/1. We give thanks
to Valerie Menke for foraminifera test size measurements and Mareike Paul
for selection of epifaunal specimens. We thank David Antoine for suggestions
on the GlobColour data set and Jürgen Möbius for support during
processing of the TOC samples. Lisa Schönborn and Günther Meyer are
thanked for technical support during stable isotope measurements. This study
was supported by the Deutsche Forschungsgemeinschaft, grants SCHM1180/16 and
MA1942/11.
Edited by: A. Shemesh
Reviewed by: three anonymous referees
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