Chemical Geology 359 (2013) 23–31
Contents lists available at ScienceDirect
Chemical Geology
journal homepage: www.elsevier.com/locate/chemgeo
Oxygen isotopes and MgCO3 in brachiopod calcite and a new
paleotemperature equation
Uwe Brand a,⁎, K. Azmy b, M.A. Bitner c, A. Logan d, M. Zuschin e, R. Came f, E. Ruggiero g
a
Department of Earth Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canada
Department of Earth Sciences, Memorial University of Newfoundland, St. John's, Newfoundland and Labrador A1B 3X5, Canada
Institute of Paleobiology, Polish Academy of Sciences, ul. Twarda 51/55, 00-818 Warszawa, Poland
d
Centre for Coastal Studies, University of New Brunswick, Saint John, New Brunswick E2L 4L5, Canada
e
University of Vienna, Department of Paleontology, A-1090 Vienna, Austria
f
Department of Earth Sciences, The University of New Hampshire, Durham, NH 03824, USA
g
Dipartimento di Scienze della Terra, Universita di Napoli Federico II, 801380 Napoli, Italy
b
c
a r t i c l e
i n f o
Article history:
Received 25 February 2013
Received in revised form 20 September 2013
Accepted 24 September 2013
Available online 4 October 2013
Editor: David R. Hilton
Keywords:
Modern brachiopod calcite
δ18O equilibrium
Shell SrCO3 and MgCO3 contents
Paleotemperature equation
δ18OSW–salinity habitat relationship
a b s t r a c t
Modern brachiopods and their ambient seawater, compiled from 34 localities, covering shallow-waters from the
poles to the tropics were analyzed for their oxygen isotopic compositions, and SrCO3 and MgCO3 contents. If the
routine seawater δ18O composition and the ‘MgCO3 effect’ on oxygen isotopes are considered in calculations, calcification temperatures are concordant with measured ambient seawater temperatures. The SrCO3 contents of
modern brachiopods appear to be unrelated to ambient growth temperatures, while their MgCO3 contents exhibit some relationship with temperature and growth rate, controlled, in part, by ambient productivity or clearance
rates or local environment, and by taxonomic affinity such as presence or absence of caeca.
Linear least-squares regression analysis yields a new oxygen isotope paleotemperature equation for brachiopod
calcite, which makes adjustment for shell MgCO3 contents, and covers habitats with water temperatures ranging
from −2° to +32 °C:
T C ¼ 16:192–3:468ðδc –δSW –Mgc Þ
2
N ¼ 319; R ¼ 0:98 :
The Mg-effect adjustment is based on the change in shell-calcite δ18O by +0.17‰ per mol% MgCO3 (JiménezLópez et al., 2004). This adjustment is critical to the determination of calcification temperatures for modern
articulated brachiopods, especially the ones from cold and warm water habitats, and/or the ones with exceptionally low or high MgCO3 contents, which otherwise may be offset (lower or higher) by as much as 7 °C. Furthermore, this adjustment may be critical for fossil brachiopods and other marine calcitic invertebrates with variable
MgCO3 contents, and when using their δ18O and Δ47 for determining ancient seawater δ18O compositions and
temperatures.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
The pioneering studies of McCrea (1950), Epstein et al. (1951, 1953),
Urey et al. (1951), Compston (1960) and Lowenstam (1961) established
the field of carbonate isotope geochemistry with introduction of the oxygen isotope carbonate-water paleotemperature equation and its application to modern and fossil marine invertebrates. These studies ushered
in a time of deciphering sea surface (SSTs) and deep-sea temperatures
(DSTs) of modern and ancient environments from the poles to the
tropics using mollusks and an increasing array of other archives (e.g., foraminifera, brachiopods; e.g., Emiliani, 1955; Lowenstam, 1961; Savin,
1977). In 1961, Lowenstam examined the SrCO3, MgCO3 and δ18O
⁎ Corresponding author.
E-mail address: [email protected] (U. Brand).
0009-2541/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.chemgeo.2013.09.014
compositions of modern shallow-water (b140 m) brachiopods from
environments with salinities ranging from 30.0 to 38.4 and annual temperatures ranging from 6 to 26 °C. Since their elemental and isotopic
compositions are affected by the composition and temperature of the
ambient seawater, based on these observations Lowenstam (1961)
asserted that brachiopods incorporate oxygen isotopes into shell calcite
in equilibrium. For many years this assertion remained unverified, but
the question of isotope equilibrium incorporation into brachiopod
shell calcite has been raised and tested by a number of studies with different outcomes (e.g., Carpenter and Lohmann, 1995; Buening and
Spero, 1996; Auclair et al., 2003; Brand et al., 2003; Parkinson et al.,
2005; Yamamoto et al., 2010a). Despite the use of liberal test parameters for equilibrium incorporation of oxygen isotopes into shell calcite,
the uncertainty did not dissipate (e.g., Brand et al., 2003; Parkinson
et al., 2005). In addition, the incorporation of Sr and/or Mg into
24
U. Brand et al. / Chemical Geology 359 (2013) 23–31
brachiopod shell calcite as SST recorders and archives has received some
attention albeit with qualified success (e.g., Buening and Carlson, 1992;
Lee et al., 2004; England et al., 2007; Griesshaber et al., 2007; Cusack
et al., 2008; Pérez-Huerta et al., 2008).
The paleotemperature equation proposed by McCrea (1950) and
Epstein et al. (1951, 1953) was based on the oxygen isotopic compositions of synthetic calcite and on shell carbonate derived mostly from
mollusks of mixed, calcitic or aragonitic mineralogy, respectively. δ18O
results were calibrated using CO2 evolved from the Peedee belemnite
(PDB) carbonate. The original paleotemperature equation proposed
by Epstein et al. (1951) and later modified by Epstein and Mayeda
(1953) includes a correction for the isotopic composition of the ambient
seawater (Epstein et al., 1953). This practice continued until the mid
1960s when Craig (1961, 1965) suggested that SMOW would be a better
standard for seawater than PDB. Consequently results of climatology and
paleoclimatology studies, prior to this time, may have to be adjusted by
0.27‰ to obtain ambient seawater values (e.g., Hut, 1987; Coplen,
1988) if they used the Epstein et al. (1953) paleotemperature equation
and derivatives of the same (e.g., Lowenstam, 1961). In subsequent
decades, the oxygen isotope paleotemperature equation experienced
many modifications/upgrades/new experiments (e.g., Anderson and
Arthur, 1983; Kim and O'Neil, 1997; Leng and Marshall, 2004) with researchers targeting other carbonates (e.g., forams, synthetic carbonates).
Lowenstam (1961) noted a covariance of MgCO3 with δ18O, and subsequently a Mg impact on oxygen isotope partitioning into calcite was
first reported by Tarutani et al. (1969), which was followed by the recent
work of Jiménez-López et al. (2004). But, application of this Mg–18O adjustment to brachiopod shell calcite remained limited because of their
generally accepted, low-Mg calcite mineralogy (b 4 mol% MgCO3) and
its assumed minimal effect (cf. Carpenter and Lohmann, 1995). Interestingly, none of the paleotemperature equations in the literature are based
on brachiopod calcite, despite the fact that an overwhelming number of
δ18O and temperature determinations of deep-time studies are based on
brachiopod archives (e.g., Wenzel and Joachimski, 1996; Mii et al., 1999;
Veizer et al., 1999; van Geldern et al., 2006; Korte et al., 2008; Brand et al.,
2011, 2012a). Furthermore, the control of Mg incorporation into and distribution in brachiopod shell calcite is a subject of ongoing debate (cf.
Buening and Carlson, 1992; England et al., 2007; Pérez-Huerta et al.,
2008), and remains unresolved because of difficulties in deciphering
the exact mechanism(s) for the distribution of Mg in biogenic shell- or
synthetic-calcite (cf. Mucci, 1987).
Also, articulated and inarticulated brachiopods contain highly variable amounts of Mg, with large differences between their primary and
secondary/tertiary layers, and elevated Mg contents in the juvenile
stage but that decrease with increasing age (Buening and Carlson,
1992; England et al., 2007). Other parts/segments of brachiopod shells
such as umbo area, muscle scar areas, loops, teeth and sockets present
their own isotopic concerns (cf. Carpenter and Lohmann, 1995; Brand
et al., 2003; Parkinson et al., 2005; Griesshaber et al., 2007; PérezHuerta et al., 2008). The Mg content of brachiopod shells and layers
exhibits two patterns with ontogeny (Rosenberg and Hughes, 1989).
During the initial fast growth-stage, Mg content is high, and was labeled
the Primary Ontogenetic Pattern (POP) by Buening and Carlson (1992).
As brachiopods continue to grow and mature, their growth rate slows
significantly and concomitantly their Mg content decreases and levels
off in accreting shell material; this stage represents the Secondary Ontogenetic Pattern (SOP; Buening and Carlson, 1992). A ‘slow’ growth rate
of the mature SOP shell segment is well within the norm expected of the
low-energy and low-metabolism articulated brachiopods (e.g., James
et al., 1992; Peck, 1992, 1996; Thayer, 1992).
Articulated brachiopod shells generally consist of low-Mg calcite (cf.
Dodd, 1967; James et al., 1997; Brand et al., 2003), and the Mg effect on
their shell's δ18O was ignored based on the small, 0.06‰ per mol%
MgCO3 impact (cf. Tarutani et al., 1969). But, this is questioned by the
much higher value determined by experiments with synthetic magnesian calcites conducted by Jiménez-López et al. (2004). Indeed, they
determined an impact of MgCO3 on oxygen isotopes about 3 times
larger (+0.17‰/mol% MgCO3) than that proposed by Tarutani et al.
(1969), and the realization that modern articulated brachiopods may
contain as much as 10.64 mol% MgCO3 (Brand et al., 2003, 2011) has
re-ignited the debate. This ‘new’ impact will be a major consideration
in evaluating the oxygen isotopic compositions of our modern brachiopods with their ambient seawater δ18O and reconstruction of calcification temperatures.
There appears to be a concern with oxygen isotope equilibrium
for brachiopod shell calcite based on deviations of calculated isotopic
temperatures from actual calcification ones (cf. Table 1). This deviation
from measured water temperatures tends to be exacerbated in brachiopods from environments with high or low temperatures such as the
tropics (e.g., Palau and Jamaica), polar seas (Ross and Signy Islands,
Antarctica), or from intertidal zones (e.g., Puget Sound, Washington
State; cf. Table 2). In the documented examples, calculated ambient
temperatures (with consideration of seawater δ18O), using the four
major paleotemperature equations, are either higher or lower than
measured ambient water temperatures (Table 2), and, generally, carbonate oxygen isotopic disequilibrium is put forth to explain this
discrepancy (cf. Carpenter and Lohmann, 1995; Brand et al., 2003;
Parkinson et al., 2005). With this persistent uncertainty about oxygen
isotope equilibrium in brachiopod shell calcite, a study of ambient
water and biogenic parameters are important considerations, especially,
if we are to retain brachiopods as paleotemperature archives of climate
change.
Our study reconsiders the oxygen isotope fractionation of modern
brachiopods, by: 1) fully evaluating the oxygen isotope incorporation
process into brachiopod shell calcite, while considering their shell
SrCO3 and MgCO3 contents as well as seawater δ18O compositions,
by: 2) evaluating the potential of brachiopod shell calcite SrCO3 and
Table 1
List of modern brachiopod species with concerns of equilibrium incorporation of stable
isotopes (δ18O) into shell calcite from various sources. (a — Carpenter and Lohmann,
1995; b — Rao, 1996; c — Auclair et al., 2003; d — Brand et al., 2003; e — Parkinson et al.,
2005; f — Marshall et al., 1997; g — Zakharov et al., 2006).
Brachiopod species
Locality
a
Aerothyris macquariensis
Stethothyris* sp.a
Hemithiris psittaceaa
Magellina sp.a
Terebratella sanguineaa
Notosaria sp.a
Terebratulina sp.a
T. dorsataa
Thecidellina sp.a,d,e **
Terebratulina uniquiculab
Tichosina floridensisb
Hemithiris psittaceab
Terebratalia transversac
Anakinetica cumingid
Bouchardia rosead
Kraussina rubrad
K. mercatorid
Terebratella sanguinead
Magallania flavescensd
Megerlia truncatad
Dallina septigerad
Dallinid, new sp. and gen.d
Macandrevia tenerad
Hispanirhyncia corniad
Terebratulina septentrionalisd
Terebratulina retusad
Terebratalia transversad
Thecidellina blochmannid
Liothyrella uvae,f
Thecidellina barrettie
Dallinidaeg
South Pacific
Ross Island, Antarctica
Norway
Hokodate, Japan
South Island, New Zealand
South Island, New Zealand
South Island, New Zealand
Straits of Magellan
Palau & Curacao
Puget Sound
Dry Tortugas, Florida
Bering Sea & Puget Sound
Friday Harbor, intertidal zone
Australian Shelf
Brazil
Durban, South Africa
Cape Verde Islands
Stewart Island, New Zealand
Westerport Bay, Australia
Corsica
Canary Islands
Australian Shelf
Ireland
Canary Islands
Bay of Fundy, Canada
Kattegat
Queen Charlotte Islands
Europa Island
Signy Island, Antarctica
Rio Bueno, Jamaica
Balicasag Island, Philippines
Note: * name and identification may be questionable; ** may be in equilibrium if MgCO3
content is considered in temperature calculations.a
U. Brand et al. / Chemical Geology 359 (2013) 23–31
Buening and Spero, 1996; Rao, 1996; Marshall et al., 1997; Auclair
et al., 2003; Brand et al., 2003; Parkinson et al., 2005; Zakharov et al.,
2006; Yamamoto et al., 2010a,b).
Table 2
Seawater temperatures of select modern brachiopods from warm, temperate and coldwater environments (superscripted letters as in Table 1), determined with maximum and
minimum δ18O values (‰, PDB) of populations (and corrected with δ18OSW of corresponding studies) and various paleotemperature equations (1 — Epstein et al., 1953; 2 — Craig,
1965; 3 — Anderson and Arthur, 1983; 4 — Kim and O'Neil, 1997; Leng and Marshall, 2004).
18
Species
Locality
δ O
1
2
3
4
Thecidellina sp.a
Palau
(−0.1)
Jamaica
(+0.8)
Puget S.
(−1.8)
−2.62
−2.90
−0.93
−1.29
−0.35
−0.77
−0.37
−2.81
−0.34
−5.07
+3.25
+2.91
+3.68
+2.15
26.9
28.3
23.1
24.8
9.5
11.2
9.6
19.8
9.5
30.7
3.8
4.9
−1.9
2.8
28.3
29.7
24.6
26.3
11.1
12.7
11.2
21.3
11.1
32.0
5.3
6.5
−0.5
4.3
27.3
28.6
23.6
25.2
10.3
11.9
10.4
20.3
10.2
30.9
4.6
5.7
−1.1
3.6
25.9
27.3
22.0
23.7
7.3
9.2
7.4
18.5
7.3
29.6
0.6
2.0
−6.7
−0.7
Thecidellina barrettie
Terebratalia transversac
Stethothyris sp.a
Ross I.
(+0.2)
Signy I.
(−1.2)
Liothyrella uvae
25
2.1. Modern brachiopods
A total of 422 articulated brachiopods (including 43 specimens of
other authors) from 34 geographic locations were collected from 1 to
137 m depth, with one from a depth of about 575 m (Appendix 1),
with 319 examined for their Mg and δ18O compositions. An additional
five populations of inarticulated brachiopods (including two published
ones, N = 19) were studied representing one species (Appendix 1).
The articulated brachiopods represent 34 populations inhabiting
environments with water temperatures ranging from −2° to 32 °C, salinities ranging from 29 to 42, and the Orders Rhynchonellida,
Terebratulida, Thecideida, and Craniida.
2.2. Modern seawater
Note: Temperature values in normal font within expected range, values in bold are too
high, values in bold-italic are too low. Species names as per original source, and values
in () are δ18OSW of the local habitat (location).
MgCO3 contents as independent paleotemperature equations of carbonate formation, and by: 3) constructing a new isotope paleotemperature
equation for ambient temperatures considering the effect of seawater
δ18O and shell MgCO3 on brachiopod calcite δ18O compositions.
Seawater was collected at 23 geographic locations representing
38 brachiopod sample stations to record the seasonal, where possible,
ambient temperature, salinity, and chemical and isotopic compositions
(includes data of Lowenstam, 1961; adjusted to VSMOW, Coplen,
1988, and of other authors; Appendix 2). Bodies of water include:
Hudson Bay, North Atlantic Ocean, Caribbean Sea, North and South
Pacific Oceans, Indian Ocean, Southern Ocean, Mediterranean Sea, and
the Red Sea (Fig. 1).
2. Study material
2.3. Analytical methods
Our material consists of modern brachiopods and their ambient habitat seawater δ18O and temperatures, supplemented by samples from
studies that also provide these water quality chemistry and temperature parameters. This assures the best possible global coverage (Fig. 1;
cf. Lowenstam, 1961; Wefer, 1985; Carpenter and Lohmann, 1995;
Shells of brachiopods were cleaned of pedicles, organic tissue, loops,
teeth and sockets. The whole shell, prior to further processing, was
leached with 10% HCl to remove the outermost organic periostracum
as well as the primary layer (since the latter of these components is
deemed not to incorporate oxygen isotopes in equilibrium with
150°
120°
90°
60°
30°
0°
30°
60°
90°
120°
150°
180°
60°
1
2
1
1,3,4,5
Hudson
Bay
4
1,3
2,8
30°
1,9,4
1,2,6
2
Pacific
1,9,4
1,2
1
Atlantic
1,4
1
3
9
1
Pacific
1
1,3
2
Equator
1
Ocean
Indian
Ocean
Ocean
Ocean
30°
1
1,4
1,4,7
60°
Southern Ocean
1
Fig. 1. Localities of modern brachiopods examined in this study (#1, Appendix 1; supplemented by material from Rao, 1996; Brand et al., 2003) and of other authors (2 — Lowenstam, 1961;
3 — Carpenter and Lohmann, 1995; 4 — Parkinson et al., 2005; 5 — Auclair et al., 2003; 6 — Wefer, 1985; 7 — Marshall et al., 1997; 8 — Buening and Spero, 1996; 9 — Yamamoto et al., 2010a,b).
Seawater information and chemistry are presented in Appendix 2.
U. Brand et al. / Chemical Geology 359 (2013) 23–31
recorder because it should be independent of the ambient seawater
δ18O composition (e.g., Vinogradov, 1953; Odum, 1957). Results have
been encouraging in characterizing ambient environmental conditions
using MgCO3; for example, Lowenstam (1961) documented an increase
in MgCO3 with increasingly negative shell δ18O values (i.e. increasing
ambient water temperatures). Our results — which include previously
published data of Lowenstam (1961), Buening and Spero (1996) and
Pérez-Huerta et al. (2008) — show a reasonable logarithmic relationship
(R2 = 0.62 using ALL data) and an improved correlation (R2 = 0.80)
between shell-MgCO3 content and ambient water temperature with
few exceptions (Fig. 2). The following brachiopod populations from
Signy Island, Arthur Harbor, and the Terebratulina septentrionalis from
Bonne Bay will be considered separately, because their Mg contents
are above the Mg-content line described by all the other brachiopods
(Fig. 2).
The brachiopods from Signy Island, Arthur Harbor (both Antarctica),
and, in part, some from Bonne Bay, Newfoundland are enriched in shell
MgCO3 (Fig. 2). This suggests that some factors, other than calcification
temperature, such as growth rate, productivity and/or feeding pattern/
rate influences the MgCO3 content of brachiopod shells (cf., Buening
and Carlson, 1992). The Southern Ocean is an area of generally high productivity and thus considered a favorable environment for fast marine
invertebrate growth (e.g., Rose and Caron, 2007). This concept is
underscored by observations of extreme seasonal blooms in and near
coastal areas (cf. Clarke and Leakey, 1996). Thus, the distinct and significantly higher Mg contents of the brachiopods from Signy Island, Arthur
Harbor, and Bonne Bay would support the suggestion of faster shell
growth due to higher seawater productivity (Fig. 2).
At this stage, the MgCO3 content of brachiopods may be used for
determining ambient water temperatures provided they fall on the
‘global brachiopod-Mg’ line (GBMgL; Fig. 2). But, it raises the question,
how will this MgCO3 enrichment and potentially faster growth rate in
brachiopod shell calcite affect the oxygen isotopic composition, and
ultimately its potential as a reliable archive of ambient seawater
temperatures?
3.2. Oxygen isotopes and water temperature
The information presented in Tables 1 and 2 suggests that numerous
brachiopods may not incorporate oxygen isotopes into shell calcite in
x = 15.428log(y) + 14.386
3.1. Shell MgCO3 content
The MgCO3 content of brachiopods and other marine invertebrates
has received great attention for its potential as a paleotemperature
AH
L
GB
Mg
SOP(slow)
SI
1.0
POP
Lowenstam (1961) collected both modern brachiopods and ambient
seawater to test the equilibrium incorporation of elements and oxygen
isotopes into shell calcite. Similarly, instead of relying on isotope data
from global water tables, charts and databanks, we collected seawater
at brachiopod collection sites to characterize their ambient habitat (cf.
Marshall et al., 1997; Brand et al., 2003). Since it was not always possible
to collect ambient water during different times (seasons) of the year
(Appendix 2), results by necessity are extrapolated based on expected
and reasonable seasonal habitat water temperature variations. This
was extremely important, because our main objective was to investigate the impacts of SrCO3, MgCO3 and δ18O on the calculation of calcification seawater temperatures using brachiopod shell calcite. Evaluation
of our large database suggests that the SrCO3 content of modern brachiopod calcite is controlled by processes other than water temperature
and chemistry, and will not be discussed further in this study.
MgCO3mol%
3. Results and foundation
R 2 = 0.80 ( )
CA(bb)
10.0
faster
ambient seawater; cf. Carpenter and Lohmann, 1995; Parkinson et al.,
2005). Subsequently, whenever possible shells were sub-sampled to
capture their ontogenetic variation (cf. Lee et al., 2004).
Shell carbonate, powdered in an agate mortar and 5–20 mg weighed
to four decimals or 1–2 mg drilled from the shell, was digested with 10
or 2 mL of 2% (v/v) distilled HNO3 (cf. Brand et al., 2003). Most solutions
were analyzed for Ca, Mg, Sr, Na, Mn and Fe by atomic absorption spectrophotometer (Varian 400P AAS), and matrix modifiers (e.g., La and K
solutions) were added to all analytical solutions to counter chemical
interferences and problems of ionization. All elemental results were adjusted to a 100% carbonate basis (cf. Brand and Veizer, 1980). Comparison of AAS with ICP-MS results is discussed in the Supplementary
section. Reproducibility of elemental results is better than ± 5% (1σ)
compared to certified values for Ca, Mg, Sr, Na, Mn and Fe of NBS
(NIST) 633 (N = 75) standard rock material.
A subset of brachiopod material was analyzed for carbon and oxygen
isotope compositions at Memorial University. About 200 μg of powder
of each sample was reacted with ultrapure 100% orthophosphoric acid
at 70 °C in a Thermo-Finnigan Gasbench II, and gas was introduced
into a Thermo-Finnigan Delta V+ mass spectrometer for analysis.
Long-term reproducibility of NBS-19 standard values on this instrument
is better than 0.05‰ (1σ) VPDB for both δ13C and δ18O. All geochemical
results of modern brachiopods are reported in Appendix 1. For detailed
description of clumped isotope method and technique see Came et al.
(2007) and Brand et al. (2012b).
Seawater was collected at the locations by the authors or by colleagues using a Kemmerer sampler or by direct immersion of vials/bottles
at sample stations during dives. Aliquots of seawater were tested for salinity, trace elements, and δ18OSW (VSMOW). Water temperature was
measured with a Fish Hawk TD probe and before storage of the retrieved
sample batch with a NIST calibrated thermometer. Water was stored in
50 mL brown vials with solid septum and cap, and kept cold until shipment and processing in the lab.
Salinity was measured with a Hach SensIon5 meter calibrated to
35.0 ppt at Brock University. Trace elements were analyzed on a Varian
400P atomic absorption spectrophotometer, and results of standard solutions (Delta High Purity Standards) were within ±4.5% of certified values.
Seawater δ18O (VSMOW) was analyzed by the G.G. Hatch Isotope Lab,
Department of Earth Sciences, University of Ottawa, Ottawa, Canada.
Their standard, sample preparation and analytical procedures are listed
at: www.isotope.uottawa.ca/techniques/water.html. Reproducibility of
replicate analyses is better than 0.01‰ for δ18O (VSMOW). All geochemical results of seawater are reported in Appendix 2.
SOP-GR
26
0.1
-5
0
5
10
15
20
25
30
35
Temperature (°C)
Fig. 2. MgCO3 contents of modern brachiopods relative to their ambient water temperature (T°C). Mg contents of many brachiopod populations cluster about a logarithmic correlation line (R2 = 0.80). Some populations (SI = Signy Island; AH — Arthur Harbor;
CA(bb) — Bonne Bay, Canada) define outliers with higher MgCO3 contents than those considered in ‘equilibrium’ with their ambient temperatures (GBMgL — Global Brachiopod Mg
Line). These are specimens from environments with higher nutrient levels, greater productivity or faster growth rate (cf. Peck et al., 1987, 1997; Marshall et al., 1997; Brand
et al., 2003). The POP and SOP are Primary Ontogenetic Pattern and Secondary Ontogenetic Pattern, respectively (Buening and Carlson, 1992).
U. Brand et al. / Chemical Geology 359 (2013) 23–31
T C ¼ 16:192–3:468 δC −δSW −δMg
2
N ¼ 319; R ¼ 0:98; 95% CI
where δC represents δ18O of the shell carbonate, δSW represents δ18O of
the ambient seawater, and δMg represents adjustment for the MgCO3 effect. The latter effect is a shift in carbonate δ18O of +0.17‰ per mol%
MgCO3 (Jiménez-López et al., 2004). This result reveals that ‘differential’
MgCO3 contents and potentially growth rates of modern articulated
brachiopods do not complicate or scramble the temperature archive.
Indeed, the correlation between shell δ18O (adjusted for seawater δ18O
and shell-MgCO3) is high (R2 = 0.98, Fig. 4), but more importantly, the
proposed paleotemperature equation gives calculated water temperatures that are consistently in agreement with measured calcification
temperatures of the tested populations (Appendix 2; further statistical
details and discussion in the supplementary text).
y = -3.468x + 16.192
R 2 = 0.98 N=319
30
25
20
15
10
5
0
-5
-5
-4
-3
-2
-1
0
1
2
3
4
5
6
δ18O(SW+Mg)(‰,PDB)
Fig. 4. Brachiopod δ18O values (adjusted by seawater-18O and shell MgCO3-content) and
their ambient (habitat) seawater temperatures. Populations were placed according to measured mean ambient seawater temperatures (Appendix 2). Brachiopod δ18O values adjusted with the seawater-18O composition (dashed line) and re-plotted with adjustment for
seawater-18O and effect of MgCO3 content on isotopic compositions (solid line, N = 319,
R2 = 0.98, 95% CI). The MgCO3-effect adjustment is defined as 0.17‰ per mol% MgCO3
(cf. Jiménez-Lopéz et al., 2004). The MgCO3 content of our modern articulated brachiopods
ranges from 250 to 30,660 ppm (0.09 to 10.64 mol% MgCO3, Appendix 1; Brand et al.,
2003), and statistical analysis of the populations is presented in Table S2.
4. Applications
Our new δ18O paleotemperature equation proposed for brachiopod
calcite includes an adjustment for shell MgCO3 content and raises several
important questions: What controls the MgCO3 content and growth rate
of brachiopod shell calcite? Does the MgCO3 adjustment apply only to articulated brachiopods or may it also apply to their inarticulated calcitic
cousins, and possibly other marine invertebrates secreting carbonate
shells/tests? How will the proposed paleotemperature equation based
on brachiopod-calcite resolve the questionable temperatures obtained
for the specimens listed in Table 1? How will the new equation impact
on deep time brachiopod-based temperatures and thus the δ18O composition of ancient seawater? Some of these questions may require more
detailed studies, but we address some of them here.
4.1. Shell-MgCO3 Secondary Ontogenetic Pattern — growth rate
+3
( ) Atlantic, ( ) Pacific, Epstein & Mayeda, (1953).
( ) Pacific, Crowley & Taylor, (2000).
+2
Red Sea
+1
SW
L
(B
)
0
G
δ18OSW (‰, SMOW)
35
Temperature (°C)
equilibrium with their ambient water (cf. Carpenter and Lohmann,
1995; Auclair et al., 2003; Brand et al., 2003; Parkinson et al., 2005).
However, this assumption is based on the strict adherence to just a
seawater-18O adjustment for determining brachiopod habitat water
temperatures, and using one of the traditional δ18O paleotemperature
equations. In many instances, a or some seawater δ18O composition is
obtained from NOAA charts and tables or from salinity–seawater-18O
equations (cf. Carpenter and Lohmann, 1995; Brand et al., 2003;
Parkinson et al., 2005) that may or may not be directly related to the
δ18OSW of the brachiopod habitat. We avoided this situation by obtaining
seawater samples from the sample locations of the modern brachiopods
(Fig. 3, Appendix 2). Seawater collected from brachiopod habitats of
the Atlantic and Pacific Oceans defines a single salinity–seawater-δ18O
equation of δ18OSW (‰) = 0.419 salinity − 14.25 (Fig. 3), which is similar to the one proposed by Buening and Spero (1996). In contrast, seawater from environments such as the Red Sea (δ18OSW (‰) = 0.037
salinity − 3.648) and Borge Bay (Southern Ocean; δ18OSW (‰) =
0.417 salinity − 15.188) are quite distinct from the all encompassing
trend and equation of Atlantic and Pacific waters (Fig. 3).
Brachiopod calcite δ18O results, only adjusted for a seawater δ18O
contribution, define a slightly curving line-equation with greatest deviations at the temperature extremes (dashed line, Fig. 4). After adjustment of shell δ18O values by the seawater δ18O contribution and the
MgCO3 effect, the brachiopod database is defined by a linear leastsquares regression between δ18O shell-archive and ambient ‘habitat’
water temperature (Fig. 4), which is as follows:
27
-1
)
y = 0.419x - 14.250 R 2 = 0.917 (
y = 0.037x - 3.648 R 2 = 0.714 ( )
y = 0.417x - 15.188 R 2 = 0.981 ( )
Marshall et al., 1997.
Southern
Ocean
-2
28
30
32
34
36
38
40
42
44
Salinity (Psu)
Fig. 3. Salinity and seawater-18O compositions from brachiopod sampling localities in the
North Atlantic Ocean, Caribbean Sea, and Pacific Ocean represent the Global-Seawater
LineBrachiopod (GSWLB). The results from the Southern Ocean and Red Sea, of brachiopod
sampling stations, define distinctly different δ18O–salinity relationships from the GBSWL
(Appendix 2).
Some studies relate Mg contents of brachiopod shells to any specific
cause, and go on to state that during the juvenile stage Mg incorporation
is higher than in later stages (e.g., Buening and Carlson, 1992). Many of
our brachiopod populations have Mg contents that define a relationship
with ambient growth temperature by the ‘global brachiopod Mg line’
(Fig. 2). However, there are a several exceptions to the rule where the
populations defined by their MgCO3 contents fall above the ‘global brachiopod Mg-line’. It is postulated that those above the line grow faster
and thus incorporate more Mg into shell calcite. Fortunately, the brachiopod Liothyrella uva from Borge Bay (Signy Island, Antarctica) has
been studied in detail by Peck and co-workers, who determined that, although, it ‘gorges’ itself during the austral spring–summer bloom (Peck
and Holmes, 1989; Peck et al., 1997), it grows fastest during the leaner
austral winter months when chlorophyll levels are low (Clarke et al.,
1988). The water temperature in Borge Bay varies from −2 to about
+2 °C annually, and temperatures above 4.5 °C are considered lethal
to the local brachiopods (Peck, 1989). Interestingly growth rate, of the
secondary ontogenetic pattern (SOP), of L. uva specimens larger than
20 mm can be 13 times faster during the leaner winter months than
during the corresponding high-productivity summer ones. In addition
to this exception, the overall Mg content of L. uva is about 4 times higher
than that expected at prevailing growth temperatures (Fig. 2, Appendix
28
U. Brand et al. / Chemical Geology 359 (2013) 23–31
separately and serially, and ontogenetically they define two distinct
MgCO3 trends, with an average of 2.96 mol% MgCO3 for the larger
ventral (pedicle) valve and 0.99 mol% MgCO3 for the smaller dorsal
(brachial) one (Fig. 2, Appendix 1). The impunctate H. psittacea feeds
at higher nutrient concentrations and is not able to store food such as
the endopunctate T. septentrionalis with its lower clearance rate of nutrients (cf. Rhodes and Thompson, 1993). These examples suggest that
ability to store nutrients for later release is an important factor in the
growth rate of shells, and the correspondingly greater incorporation of
MgCO3 into brachiopod valves. Indeed, more detailed studies on growth
rates in brachiopods from natural settings and cultured in labs are required to resolve the relationship between calcification rate, Mg content
and oxygen isotope compositions.
2). Consequently, water temperature and food availability can be ruled
out as causes for the increased growth rate observed in L. uva during the
austral winter (cf. Peck et al., 1997). Instead it has been postulated that
caeca, sites of nutrient storage in shells, are used by brachiopods to
maintain metabolic activity during lean times (Owen and Williams,
1969; Curry, 1983). This supply of energy could help the organism
with reproduction and over-wintering during the chlorophyll-lean winter period by regulating release of nutrients, and thus facilitate its accelerated shell growth (Peck et al., 1987). Further evidence for this type of
action comes from observations on the brachiopod Terebratulina retusa
and its gonad development during the lean winter months in Scottish
lochs (Curry, 1982), and on other brachiopods from intertidal and
subtidal pools of New Zealand (Curry, 1983).
The MgCO3 content of another Antarctic brachiopod, Liothyrella sp.
from Arthur Harbor, is higher than that expected under ambient growth
temperatures (Fig. 2). In contrast, in two species of brachiopods, the
impunctate Hemithiris psittacea and the endopunctate T. septentrionalis
from Bonne Bay, Newfoundland, the MgCO3 content of the former falls
on the brachiopod Mg-line, whereas that of the latter is well above it
(Fig. 2). Furthermore, two valves of T. septentrionalis were analyzed
4.2. Shell carbonate-MgCO3 adjustment
In 1969, Tarutani et al. demonstrated a small effect of magnesium
substitution on oxygen isotope fractionation, which was the prevailing
consensus until 2004. The study by Jiménez-Lopéz et al. (2004) revealed
a much larger effect of MgCO3 content on carbonate δ18O values. This
Table 3
Seawater temperatures based on oxygen isotopes of modern brachiopods from warm (low-latitude), temperate (mid-latitude) and cold-water (high-latitude) environments (Appendix 1;
other sourcesL, C). Calculated temperatures determined with maximum and minimum δ18O values (‰, PDB) of populations adjusted with δ18OSW; (Appendix 2) and paleotemperature
Eq. (1) of Epstein et al. (1953) and 4 of Kim and O'Neil, 1997; Leng and Marshall (2004), and the new paleotemperature equation with (B) MgCO3 adjustment (Fig. 4), and the differences
in temperatures between #1, 4 and B (ΔT).
Species (depth m)
Locality
δ18OC
δ18OSW
Thecidellina congregata
(2)
T. congregata
(91)
Argyrotheca sp.
(91)
T. barretti
(94)
T. sp.
(13)
T. barretti
(8)
A. woodwardiana
(20)
Terebratulina cailleti
(137)
Ospreyella maldiviana
(34)
Terebratalia transversa
(75)
Terebratulina unguicula
(75)
Hemithiris psittacea
(75)
T. septentrionalis
(15)
Laqueus rubellus
(80)
Megerlina pisum
(1)
Liothyrella neozelanica
(18)
Calloria inconspicua
(18)
Notosaria nigricans
(18)
Terebratella sanguinea
(18)
Hemithiris psittacea
(20)
Liothyrella sp.
(15)
L. uva
(15)
Palau
−1.92
−2.79
−1.78
−1.88
−1.83
−0.1
−0.68
−1.02
−0.76
−1.02
−0.80
−0.86
−0.79
−0.89
+0.11
−0.88
−1.56
−1.98
+0.31
−0.72
+0.17
−0.38
+0.15
−0.88
+1.26
+0.54
+0.81
+0.48
+0.66
−0.51
+1.39
+1.10
+0.86
+0.60
+1.27
+1.07
+0.92
+0.22
−0.07
−1.11
+3.01
+1.1
MarshallL
MarshallL
Jamaica
C
Curacao
G. Cayman
G. Cayman
Barbados
Maldives
Friday H.
Friday H.
Friday H.
B. Fundy
Sagami B.
Kidds B.
Doubtful S.
Doubtful S.
Doubtful S.
Doubtful S.
Hudson B.
Arthur H.
Signy I.
+3.82
+3.43
+0.4
+0.4
+0.9
+1.1
+1.1
+1.3
+0.5a
−1.8
−1.8
−1.8
−1.3
+0.2
+0.6
+0.3
+0.3
+0.3
+0.3
−3.7
−1.5a
−1.2
1
4
B
ΔT
23.5
27.7
25.2
25.7
25.5
22.4
26.7
24.2
24.7
24.4
27.6
29.0
27.6
28.4
26.8
4.1; 5.2
1.3; 2.3
2.4; 3.4
2.7; 3.7
1.3; 2.4
23.3
24.9
22.8
24.0
23.9
24.2
23.8
24.3
20.6
25.2
24.7
26.7
7.1
11.0
7.6
9.6
7.6
11.6
5.5
8.1
12.8
14.2
15.1
20.2
10.9
12.1
13.0
14.1
11.4
12.2
12.8
15.7
1.9
5.4
−0.9
22.2
23.9
21.6
22.9
22.8
23.1
22.7
23.2
19.4
24.2
23.6
25.7
4.5
9.0
5.1
7.5
5.2
9.7
2.6
5.6
11.0
12.5
13.5
19.0
8.9
10.2
11.3
12.4
9.4
10.3
11.0
14.2
−1.8
2.5
−5.2
27.4
28.4
26.7
27.4
29.1
28.8
24.4
24.8
21.2
24.3
27.0
28.4
9.3
12.8
9.8
11.7
9.7
13.2
7.8
10.4
14.3
15.4
16.3
20.3
12.8
13.8
14.7
15.6
13.7
14.1
14.4
16.8
3.8
7.4
1.7
4.1; 5.2
3.5; 4.5
3.9; 5.1
3.4; 4.5
5.2; 6.3
4.6; 5.7
0.6; 1.7
0.5; 1.6
0.6; 1.8
0.9; 0.1
2.3; 3.4
1.7; 2.7
2.2; 4.8
1.8; 3.8
2.2; 4.7
2.1; 4.2
2.1; 4.5
1.6; 3.5
2.3; 5.2
2.3; 5.8
2.5; 3.3
1.2; 2.9
1.2; 2.8
0.1; 1.2
1.9; 3.9
1.7; 3.6
1.7; 3.4
1.5; 3.2
2.3; 4.3
1.9; 3.8
1.6; 3.4
1.1; 2.6
1.9; 5.6
2.0; 4.9
3.2; 6.9
−2.3
−1.2
−7.2
−5.7
−0.8
0.5
1.5; 6.6
1.7; 6.2
Note: Temperature values in normal font are within range of measured seawater temperatures, values in bold-italic are too low.
a
Determined with the brachiopod habitat seawater–18O salinity relationship (Fig. 3).
U. Brand et al. / Chemical Geology 359 (2013) 23–31
revelation coupled with the observation that the MgCO3 content of lowMg calcite (b 4 mol% MgCO3) articulated brachiopods actually varies
from 0.09 to 10.64 mol% (Brand et al., 2003), requires a rethinking of
calculated paleotemperatures using carbonate archives without compensating for this effect and information.
Paleotemperatures of a large suite of modern brachiopods (Table 2)
were re-examined using all available information. Brachiopods assembled from cold (polar) to warm (tropical) and from water depths of
less than 100 m are compiled in Table 3. Temperatures are calculated
using the latest δ18Oc values, the δ18O of ambient seawater (Appendices
1, 2), the equations of Epstein et al. (1953) and of (Leng and Marshall,
2004; modified from the relationship presented by Kim and O'Neil,
1997), and ours. Concurrence between calculated and measured ambient growth water temperatures is 10 and 20 out of 42 results using
the Epstein et al. and Leng and Marshall equations, respectively, and
42 out of 42 using our MgCO3-adjusted paleotemperature equation
(Table 3).
A detailed evaluation of paleotemperatures obtained for L. uva from
Borge Bay (Signy Island) analyzed in this study (#MB-552, Appendix 1)
suggests that ambient temperatures are not achieved with the Epstein
et al. (1953; −0.94 °C), Craig (1965; 0.54°T), Anderson and Arthur
(1983; −0.12°T), nor Kim and O'Neil, 1997; −5.34 °C) equations. An
actual calcification temperature of 0.81 °C is attained with a MgCO3 adjustment and the new equation above, and confirmed independently by
clumped isotope results giving a temperature of 1.1 °C (#MB-552a,
Appendix 1; cf. Came et al., 2007). The above discussion suggests that
articulated brachiopods are in equilibrium when position of sample on
the shell layer, shell MgCO3 chemistry, and habitat seawater δ18O are
considered in calcification temperature evaluations.
4.3. Paleotemperature equation comparison & application
The paleotemperature equation of Epstein et al. (1953) was a milestone in carbonate isotope geochemistry, and opened up among many
aspects, the determination of paleotemperatures of Paleozoic seas
using a multitude of proxies. Based on calculations of modern brachiopods, however, water temperatures may be off by as little as 0.1 °C or
as high as 6.9 °C (Table 3). If increases of such magnitude in temperature are not feasible for fossil counterparts (cf. Brand et al., 2012a,b),
35
2
y = 13.81 - 4.58x + 0.08x
y = 16.00 - 4.14x + 0.13x 2
y = 16.88 - 4.20x + 0.13x 2
y = 15.35 - 4.23x + 0.14x 2
30
Leng & Marshall, 2004
Anderson & Arthur, 1983
Craig, 1965
Epstein et al., 1953
This study
Temperature (°C)
25
20
15
10
5
29
Table 4
Seawater temperatures based on oxygen isotopes of inarticulated brachiopods from
several localities (Friday Harbor, Firth of Lorne, Sagres, Isca, and central Pacific;
Appendix 1, Ruggiero, 2001; Parkinson et al., 2005). Calculated temperatures
determined with minimum and maximum δ18O values (‰, PDB) of populations,
adjusted for seawater δ18O (Appendix 2), paleotemperature equation (4 — Kim and
O'Neil, 1997; Leng and Marshall, 2004), new oxygen-isotope paleotemperature equation
(B), and difference in temperature between #4 and B.
Species (depth, m)
a
Novocrania anomala
(24)
N. anomalaa
(150)
N. anomala
(20)
N. anomala
(4)
N. anomala
(6)
N. anomala
(208)
Locality
δ18OC
δ18OSW
4
B
ΔT
Friday Harbor
+0.54
+1.50
+0.93
+3.99
+1.49
+2.55
+1.19
+1.49
+2.31
+1.21
−0.58
−1.8
3.5
−0.4
10.0
−2.8
12.0
7.3
13.9
12.5
8.8
13.8
17.4
13.2
9.9
18.4
7.8
20.8
16.9
22.3
21.3
19.8
23.6
25.8
9.7
10.3
8.4
10.6
8.8
9.6
8.4
8.8
11.0
9.8
8.4
Firth of Lorne
Sagres, Portugal
Isca, Italy
Isca, Italy
Central Pacific
+0.1
+1.1
+1.2
+1.2
+0.2
Note: values in normal font are within range of measured water temperatures (values in
bold-italic are too low).
a
A Mg value was substituted for this indetermined parameter (Carpenter and
Lohmann, 1995; England et al., 2007).
then the isotopic composition of the seawater would be have to be adjusted accordingly, which raises concerns of another nature and within
its own constraints. The impact of the new paleotemperature equation
with adjustment for MgCO3 content may give temperatures offset by
as much as 6.2 °C, and which is further discussed in the supplementary
section.
Modifications of the Epstein et al. (1953) paleotemperature equation
presented in the literature were minor in nature, which is mirrored by
the similar slopes and trends of these equations with the exception of
the one by Leng and Marshall (Fig. 5 which in itself is a re-statement of
the Kim and O'Neil, 1997 relationship). Our new paleotemperature equation is an improvement because it utilizes samples 1) from a larger water
temperature range and 2) incorporates the MgCO3 effect on shell δ18O
values (Fig. 4). Many other marine invertebrates precipitate shells/tests
that have variable or are high in MgCO3, and thus may benefit from an
approach similar to that suggested for the articulated calcitic brachiopods. Carpenter and Lohmann (1995) suggested that the inarticulated
calcitic brachiopod from Friday Harbor (Crania anomala = Novocrania
anomala) by virtue of their elevated MgCO3 contents maybe in near equilibrium, but others suggested disequilibrium with ambient seawater
(cf. Brand et al., 2003; Parkinson et al., 2005). A re-evaluation of
N. anomala from several localities (Scotland, Portugal, Italy, and Pacific)
including those from Friday Harbor suggests that once their MgCO3
content is taken into consideration, these inarticulated brachiopods incorporate shell δ18O values that reflect ambient seawater temperatures
(Table 4). Therefore, inarticulated brachiopods (Middle Ordovician–
Recent), in addition to the articulated ones, are robust archives of ancient
seawater chemistry and temperatures. In light of these findings, it is
possible that other marine invertebrates with elevated/variable MgCO3
contents (e.g., benthic foraminifera) may require re-consideration of
the mineralogical effect, thus, potentially improving their efficacy as
paleotemperature archives.
0
5. Conclusions
-5
-4
-3
-2
-1
0
1
2
3
4
5
δ18O(‰,PDB)
Fig. 5. Comparison of trends of the major paleotemperature equations with the new one
incorporating both seawater-18O and shell-MgCO3 adjustments. The paleotemperature
equation of Epstein et al. (1953) has been adjusted for a seawater correction in SMOW instead of PDB. Lines defining the various equations were computed with a global seawater
composition of 0‰ (SMOW).
Our re-evaluation of isotopic and MgCO3 compositions of modern
shallow-water articulated brachiopods from the poles to the tropics
demonstrates their reliability as recorders of ambient water temperatures. The results suggest further:
1) that modern articulated brachiopods incorporate δ18O into shell carbonate in equilibrium with respect to seawater δ18O,
30
U. Brand et al. / Chemical Geology 359 (2013) 23–31
2) to obtain habitat-growth-temperatures, the MgCO3 effect of
+0.17‰/mol% MgCO3 on δ18O values must be considered, since
the MgCO3 content of articulated brachiopod shells may range up
to 10.64 mol%, otherwise offsets as high as 7 °C are possible,
3) that a new paleotemperature equation considering both seawater
δ18O and shell MgCO3 content gives enhanced calcification seawater
temperatures for articulated brachiopods, and reads as follows:
T C ¼ 16:192–3:468ðδC –δSW –Mgc Þ
4) that shell growth rate and MgCO3 content may be, in part, be controlled by food availability and time of utilization, and
5) that by adjusting paleotemperature calculations by MgCO3 contents,
calcitic inarticulated brachiopods, and other high-Mg calcite marine
invertebrates may be valuable archives of paleotemperature.
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.chemgeo.2013.09.014.
Acknowledgments
We thank E. Grossman and an anonymous reviewer for their incisive
comments that greatly improved the manuscript. Also, thanks to M.
Ouellette for technical assistance and M. Lozon for drafting services.
Thank you to: B. Durzi, T. Durzi and N. Buckles (Cayman Islands), G.
Maddock (Bermuda), S. Thomas (Barbados), M. Lamare and R. Major
(New Zealand), D. Duggins, D. Willows and W. Krieger (Friday Harbor),
G. Lundie, K. Layton, J. Batstone and C. Basler (Hudson Bay, and the Churchill Studies Centre for their hospitality), M. Ouellette (Jamaica), M.
Strong and M. Ines-Buzeta (Bay of Fundy), R. Donnel (OSC-MUN), and
A. Zaky (Egypt) for field assistance or sample collection. Special acknowledgement to L. Colin and P. Colin (Palau) for field sampling
(water and brachiopods) under license RE-12-23 issued by the Bureau
of Marine Resources, Republic of Palau. The Department of Fisheries
and Oceans (Canada) gave permission (under section 52) to collect brachiopods in the Bay of Fundy National Marine Park, and special thanks
to L. Peck (British Antarctic Survey) for a generous supply of brachiopods from Signy Island. This work was supported by a Brock University
Chancellor's Research Chair award and by a NSERC grant (7961) to UB.
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