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Early Jurassic (late Pliensbachian) CO 2 concentrations based on stomatal analysis of fossil conifer leaves from eastern Australia ☆


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The stomatal index (a measure of stomatal density) of an extinct Australian Early Jurassic araucariacean conifer species, Allocladus helgei Jansson, is used to reconstruct the atmospheric carbon dioxide concentration (pCO2) in the Early Jurassic. The fossil leaves are preserved in a single bed, palynologically dated to late Pliensbachian (~185–183 Mya). Atmospheric pCO2 is estimated from the ratios between the stomatal index of A. helgei and the stomatal indices of three modern analogs (nearest living equivalent plants). CO2 concentration in the range of ~750–975 ppm was calibrated from the fossil material, with a best-estimated mean of ~900 ppm. The new average pCO2 determined for the late Pliensbachian is thus similar to, although ~10% lower, than previously inferred minimum concentrations of ~1000, based on data from the Northern Hemisphere, but may help constrain pCO2 during this period. Our results are the first pCO2 estimates produced using Jurassic leaves from the Southern Hemisphere and showthat i) paleo-atmospheric pCO2 estimates are consistent at a global scale, though more investigations of Southern Hemisphere material are required, and ii) the stomatal proxy method can now be used without the context of relative change in pCO2 when applying the correct methodology.
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Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of
fossil conifer leaves from eastern Australia
M. Steinthorsdottir
, V. Vajda
Department of Geological Sciences, Bolin Centre for Climate Research, Stockholm University, SE 109 61 Stockholm, Sweden
Department of Geology, Lund University, SE 223 62 Lund, Sweden
abstractarticle info
Article history:
Received 19 April 2013
Received in revised form 18 August 2013
Accepted 31 August 2013
Available online xxxx
Stomatal proxy method
Early Jurassic CO
Southern Hemisphere conifers
The stomatal index (a measure of stomatal density) of an extinct Australian Early Jurassic araucariacean conifer
species, Allocladus helgei Jansson, is used to reconstruct the atmospheric carbon dioxide concentration (pCO
the Early Jurassic. The fossil leaves are preserved in a single bed, palynologically dated to late Pliensbachian
(~185183 Mya). Atmospheric pCO
is estimated from the ratios between the stomatal index of A. helgei and
the stomatal indices of three modern analogs (nearest living equivalent plants). CO
concentration in the
range of ~750975 ppm was calibrated from the fossil material, with a best-estimated mean of ~900 ppm. The
new average pCO
determined for the late Pliensbachian is thus similar to, although ~10% lower, than previously
inferred minimum concentrations of ~1000, based on data from the Northern Hemisphere, but may help con-
strain pCO
during this period. Our results are the rst pCO
estimates produced using Jurassic leaves from the
Southern Hemisphere and show that i) paleo-atmospheric pCO
estimates are consistent at a global scale, though
more investigations of Southern Hemisphere material are required, and ii) the stomatal proxy method can now
be used without the context of relative change in pCO
when applying the correct methodology.
© 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
1. Introduction
Stomata are pores on plant leaf surfaces, through which gas ex-
change takes place, i.e. carbon is acquired for photosynthesis from
carbon dioxide (CO
) and water vapor and oxygen are lost by diffusion.
The inverse relationship between stomatal density (often recorded as
the percentage of stomata relative to stomata plus epidermal cells on
the leaf surface and referred to as stomatal index or SI) and pCO
been repeatedly demonstrated for a wide range of plant taxa from dif-
ferent geological and ecological settings from the Paleozoic until present
and this relationship has thus been established as a strong proxy
for paleo-pCO
(e.g. Woodward, 1987; Beerling and Chaloner, 1993;
McElwain and Chaloner, 1995; Kürschner et al., 1996; Beerling et al.,
1998; McElwain et al., 1998; Retallack, 2001; Royer, 2001; Rundgren
and Björck, 2003; Roth-Nebelsick, 2005; McElwain and Haworth,
2009; Barclay et al., 2010; Steinthorsdottir et al., 2011, 2013). Stomatal
density can also be used to test atmospheric models based on other
proxy data (McElwain and Chaloner, 1995; Chen et al., 2001; Beerling
and Royer, 2002; McElwain et al., 2002; Garcia-Amorena et al., 2006;
Haworth et al., 2013). Although the plant gene HIC signaling pathway,
which encodes a negative regulator of stomatal development that re-
sponds to pCO
concentrations, has been mapped (Gray et al., 2000;
Lake et al., 2002) and a large majority of (in particular gymnosperm)
woody pla nts has been shown to react to elevated pCO
2001; Haworth et al., 2013), some plant taxa do not respond by low-
ering their stomatal densities with elevated pCO
(e.g. Haworth et al.,
2011b). To obtain optimal res ults, we propose that only proven re-
sponders among modern analog taxa should be used in paleo-pCO
Stomatal proxy-based paleo-pCO
records have been obtained al-
most exclusively from the Northern Hemisphere and, so far, no studies
have been carried out on Southern Hemisphere Jurassic leaf fossils. To
our knowledge, the only previously published stomatal proxy-based
estimates from the Mesozoic of the Southern Hemisphere are for
the Triassic and the Cretaceous (Retallack, 2002; Passalia, 2009). This
is particularly striking since the Southern Hemisphere ora arguably
hosts the best nearest living equivalents (NLEs) to Mesozoic counter-
parts. Consequently, it would be ideal to test the applicability of using
fossil leaves and extant taxa from the same families within the same
hemisphere to reconstruct pCO
. Several relict conifers possess a high
ceiling of response, a concept that refers to the diminution of stomatal
response to pCO
after a certain level is reached (Kouwenberg et al.,
2003; Haworth et al., 2010, 2011a). This level is usually fairly low for
angiosperm trees that have evolved and adapted to the Cenozoic
icehouse conditions and pCO
of b 300 ppm (Beerling and Chaloner,
1993; Kouwenberg et al., 2003). Conversely, the araucariacean conifers
used as modern analogs here, clearly demonstrate that they retain
the stomatal responses developed in the Mesozoic greenhouse world,
in which pCO
reached N 600 ppm (Berner, 2006). This conserved re-
sponse makes these relict conifers ideal to employ as nearest living
Gondwana Research xxx (2013) xxxxxx
This article belongs to the Special Issue on Gondwanan Mesozoic biotas and bioevents.
Corresponding author.
E-mail address: (M. Steinthorsdottir).
GR-01141; No of Pages 8
1342-937X/$ see front matter © 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
Gondwana Research
journal homepage:
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
equivalents or modern analogs when reconstructing pCO for the Me-
sozoic , in addi tion to other plant groups with Mesozoic records, such
as Ginkgoales (Beerling et al., 1998; Chen et al., 2001; Kouwenberg
et al., 2003; Royer et al., 2003; Haworth et al., 2011a; Steinthorsdottir
et al., 2011).
For this study, we selected exceptionally well-preserved leaves of
the araucariacean conifer Allocladus helgei (Jansson in Jansson et al.,
2008a) from the Early Jurassic (Pliensbachian) of eastern Australia,
and used the stomatal proxy method to reconstruct paleo-pCO
study aims to constrain pCO
for the Early Jurassic based on Southern
Hemisphere fossil plants, and to test the reliability of the stomatal
method in the reconstructions of deep time pCO
using proven relict
Southern Hemisphere conifer responders.
2. Geological setting
The broad intracratonic ClarenceMoreton Basin, located largely
onshore in northeastern New South Wales and southern Queensland
(Fig. 1), was developed at a time of widespread subsidence in eastern
Australia and incorporates entirely non-marine sediments of latest
Triassic to Early Cretaceous age. The ClarenceMoreton sedimentary
succession is divided into three subgroups, in turn divided into several
formations. The fossil material in this study derived from strata is later-
ally equivalent to the Gatton Sandstone within the Marburg Subgroup
comprising of sandstones, mudstones and shale deposited in a braided
alluvial environment (Jansson et al., 2008b). The succession exposed
at Inverleigh quarry represents the lower part of the Marburg Subgroup
and is represented by ~15 m of organic-rich mudstones, siltstones and
shale intercalated with massive to planar and cross-laminated sand-
stone units deposited in a oodbasin setting. The ~10 cm thick siltstone
bed hosting the plant material of this study occurs about 4.1 m above the
quarry oor (see g. 3 of Jansson et al., 2008a; g. 4 of Jansson et al.,
2008b; McLoughlin et al., in press).
Based on palynostratigraphy, the sediments exposed in the quarry
were initially dated as encompassing the Pliensbachian early Toarcian
(Jansson et al., 2008a,b) but subsequent palynological studies have re-
vealed that the succession is constrained to the Pliensbachian. The age
determination was based on comparisons with several Australian
Jurassic palynological zonation schemes (see Helby et al., 1987 and
references therein), and the Pliensbachian age was based mainly
on th e large portion of Classopollis pollen in combination with t he
scarce representation of the gymnosperm pollen Callialasporites
spp. Representatives of the latter g enus reached much higher rela-
tive abundance within lower Toarcian palynological assemblages
(Helby et al., 1987).
3. Material and methods
3.1. Fossil leaf database
Ten exceptionally well-preserved leaves and leaf fragments of
A. helgei were obtained by macerating siltstones collected from
Inverleigh quarry in 2006 (Jansson et al., 2008a). A. helgei has a unique
combination of cuticular and macromorphological characters that
place it within Araucariaceae (Jansson et al., 2008a). The leaves are spi-
rally arranged on the shoots (Fig. 2A), generally ~89mmlongand
~5 mm wide, triangular to narrowly ovate, uni-veined with a short acu-
minate tip and denticulate leaf margins (Fig. 2B). Stomata occur on one
leaf surface only, interpreted to be the adaxial (upper) surface (Jansson
et al., 2008a). Stomata are arranged in two rows, separated and anked
by zones of rectangular epidermal cells (Fig. 2CD). Stomatal aperture
orientation relative to the long axis of leaves is variable. Each stoma is
circular to oval, surrounded by a narrow band of 46 subsidiary cells
in a cyclocytic arrangement sensu
Prabhakar (2004).OnA. helgei leaf
cuticle surfaces, most stomata occur as circular open holes, since
guard cells are generally not preserved (Jansson et al., 2008a). The
leaves studied here include whole leaves and leaf fragments, easily
identiable to species based on macromorphology (Fig. 2AB). The
cuticle morphology is well-preserved and identical in all specimens
(Fig. 2CD). Based on previous analyses of pollen, plant assemblages
and sediments from the Inverleigh quarry, the A. helgei-dominated
ora grew on waterlogged oodplains in a warm humid paleoclimate
(Jansson et al., 2008a,b). Illustrated macrofossils (prexed LO) are reg-
istered in the fossil collections of the Geology Department at Lund
3.2. Laboratory methods
The siltstone samples were carefully treated with dilute hydrouoric
acid (35%), and subsequently sieved through a 63 μm mesh before
A. helgei leaves and leaf fragments were handpicked under stereomi-
croscope and dried. No further treatment was necessa ry in order to
study the leaf surfaces. The f ossil leaves were dry-mounted, adaxial
side (stomatal surface) up, on glass slides and studied using an
epiuorescence microscope (Olympus BX51TF-5). The surface of
each leaf was photographed at several sites at ×200 magnication,
using a mounted microscope camera (INFINI TY2 -1C) and associated
software (Analyze 6.0). The images were evenly distributed across
the mi d-leaf areas, away from edge s, midrib and veins to minim ize
variation and provide optimal results, according to the methods of
Poole and Kürschner (1999). The images were annotated using the
software ImageJ (1.39u, NIH, USA) by engraving 0.1 mm
grids on each
image (~316 × 316 μm); all stomata and epidermal cells (including
subsidiary cells) within these grids were then counted and recorded.
Data was entered into Microsoft Excel spreadsheets. Following the
methodology of Poole and Kürschner (1999),eightimageswere
counted for each leaf fragment and the me an was obtained for sto-
matal indices. The means were conrmed by cumulative mean sta-
tis tical analysis.
3.3. Stomatal analysis and pCO
For calibration of late Pliensbachian pCO
based on mid-leaf stomatal
index, we use the NLE approach, incorporating the stomatal ratio (SR)
method of McElwain and Chaloner (McElwain and Chaloner, 1995,
1996), which compares the ratio between stomatal indices of fossil
plants and their nearest living relatives or equivalents (NLR or NLE) in
100 km
30 S
150 E
Fig. 1. Regional setting of the ClarenceMoreton sedimentary basin in eastern Australia.
The material studied here was derived from the Inverleigh quarry.
2 M. Steinthorsdottir, V. Vajda / Gondwana Research xxx (2013) xxxxxx
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
relation to the ratio between known pCO
and paleo-pCO
od was established using a range of NLE and modern SI values for current
matched against equivalent values for ancient pCO
inferred from
Berner's (1994) GEOCARB II model (McElwain et al., 1998). The pCO
data derived using the SR method showed a close t to independently es-
timated pCO
values and also to pCO
records constructed using experi-
mental data (Beerling et al., 1998). Based on analyses of best ttothe
curve, a Carboniferous standardization and a Modern
standardization were established for calibrating paleo-pCO
and McElwain, 1997; McElwain et al., 1998). The Carboniferous stan-
dardization is used for calibrations involving Mesozoic and Paleozoic
fossil plants: the ratio of past pCO
) to the pre-industrial pCO
~300 ppm was inferred to be ~2:1 (2RCO
)(Chaloner and McElwain,
1997). Stomatal indices, reecting changes in pCO
, also display this
ratio of approximately 2:1 for the Paleozoic and Mesozoic relative to
pre-industrial levels (McElwain and Chaloner, 1996; McElwain et al.,
1998). The concentr atio n of paleo- CO
is thus calibrated based on this
¼ SI
An alternative approach, the tra nsfer function method, is often
used to reconstruct paleo-pCO
. Using this method, inverse regres-
sion analyses are applie d to quantify paleo-p CO
from SI response
datasets derived from herbarium and/or CO
fumigation experiments.
This method relies on the assumption that the NLE should behave in
the same way as its fossil counterpart, but provides a more quantitative
approach to reconstructing paleo-pCO
. However, there are several ca-
veats to consider. Firstly, it is only possible to infer equivalent responses
between fossil and modern plants when working with the same species,
or at least closely related species, which are very seldom available. Even
when working with the same species, transfer functions may give widely
differing results for separate localities across the same time interval,
whereas the more simplied NLE approach gives similar results between
localities (see Steinthorsdottir et al., 2013). The SI of fossil plants com-
monly falls outside the response slope for modern plants and falls
instead on the at part of the curve. Therefore, even when using this
quantitative approach, the response curve typically needs to be extended
beyond the dataset, bringing its own set of uncertainties. In addition, the
transfer function method often producesvaluesthatareunrealistic
(commonly too low) and inconsistent with other proxies and other
transfer function based results. The NLE approach appears to give more
consistent results with both other NLE stomatal proxy results, with alter-
native proxy data, and with modeling estimates (see Steinthorsdottir
et al., 2011). Therefore, we employ the simpler, more qualitative NLE
NLRs (same species or genus) are generally not available further
back in time than the Neogene, so a NLE for the Pliensbachian leaves
studied here must be established before pCO
calibr ations can be
per formed. Following the protocol of Steinthorsdottir et al. (2011),
we limit the choice of NLEs to proven responders of pCO
that these will mor e accurately ree ct the physiological responses of
the fossil equivalent plants. Araucariacean c onifers are probably the
most appropriate NLEs for A. helgei (Jansson et al., 2008a). Based on
the elevated pCO
experiments of Haworth et al. (2010, 2011a),two
araucariacean species were selected: Wollemia nobilis and Agathis
australis, together with one cupressacean conifer bearing broadly simi-
lar scale-leaves to A. helgei: Athrotaxis cupressoides. The NLE's stomatal
indices under control or ambient conditions (pCO
12.3%, 14.4% and 11.2% respectively. The two araucariacean NLEs were
Fig. 2. Morphology of Allocladus helgei. A and B are respectively a photo and SEM image showing the leaf macro-morphology of A. helgei (from Jansson et al., 2008a).BandCshow
adaxial A. helgei leaf c uticle micro-morphology, i ncluding stomata and epidermal cell shape and orie ntation, under epiuoresence at ×100 and ×200 magnication respectively
(photo: M. Steinthorsdottir).
3M. Steinthorsdottir, V. Vajda / Gondwana Research xxx (2013) xxxxxx
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
selected based on the ir close phylogenetic rel ationship and analo-
gous cuticle morphology to the fossi l conifer s tudied here, whereas
the cupressacean NLE was chosen based on its simi lar leaf macro-
morphology to A. helgei. Perhaps other araucariacean conif er species
would be better NLEs to A. helgei,suchasAraucaria heterophylla,
closely matching in both morphology and ecology, but we consider it
essential that NLEs are proven CO
responders and, therefore, chose to
focus on taxa that have been used in elevated CO
experiments. See
Section 3.4 below for a brief description of each NLE.
The chosen NLEs are Southern Hemisphere scale- and broad-leafed
conifers th at possess high ceilings of response to pCO
(respo nse begins at N 500 ppm: Haworth et al., 2010, 2011a). The
high response ceilings indicate adaptation to higher pCO
for these
conifers than for modern angiosperm trees (Beerling and Chaloner,
1993; Kouwenberg et al., 2003), probably illustrating the more con-
served responses of conifers, reecting their evolutionary origin in the
world of the Mesozoic (Haworth et al., 2010, 2011a). Due
to the fact that the conifers have seemingly retained the Mesozoic
ceiling of response, they are regarded as reliable proxies for stomatal
ratio-based pCO
reconstructions (Haworth et al., 2011a). The three
NLEs have similar SI under ambient conditions, suggesting convergent
stomatal adaptations and gas exchange relationships. Using the mean
SI values derived from the use of multiple similar NLEs is a superior
approach to selecting just one NLE, since species-specic variability in
SI may be minimized and a more accurate SI signal of paleo-pCO
emerge. Each chosen NLE, its morphology, ecological preference and
taxonomic afnity, is listed briey below.
3.4. Nearest living equivalents
The fossil conifer species studied here, A. helgei,haspreviously
been placed within the Araucariaceae, based on macro- and micro-
morphology (Jansson et al., 2008b). The relative abundance of
Araucariaceae fossils in the geological record has provided an ex-
tensive understanding of the family's past distribution and evolution
(Stockey, 1982, 1994; Pole, 1995; Chambers et al., 1998; Kunzmann,
2007; Pole, 2008; Pole and Vajda, 2009). Araucariaceans are today
predominantly found in the Southern Hemisphere, but were globally
distributed during the Mesozoic (Kershaw and Wagstaff, 2001; Vajda
and Wigforss-Lange, 2006, 2009; Panti et al., 2012). Three NLEs were
selected for A. helgei, based on taxonomy, morphology, ecological
preferences, and the proven ability to respond to CO
species, two belong to Araucariaceae: W. nobilis and A. australis, while
the third: A. cupressoides, belongs to Cupressaceae.
3.4.1. W. nobilis
W. nobilis (Wollemi pine) was discovered in 1994 in a national park
not far from Sydney, Australia (Jones et al., 1995; McLoughlin and Vajda,
2005). Phylogenetic analyses indicate that Wollemia is a sister group to
Agathis (Gilmore and Hill, 1997; Stefanovíc et al., 1998; Liu et al., 2009).
W. nobilis is an evergreen tall tree, reaching a maximum height of
~40 m. The leaves are variable in shape, but mainly long and narrow,
~39 cm long and 26 mm broad, and spirally inserted (although typi-
cally basally twisted to form plagiotropic juvenile leaf arrangements or
orthotropic four-ranked adult leaf arrangements), with stomata occur-
ring in rows (Jones et al., 1995). Stomata are arranged in uni-seriate dis-
continuous rows of ~56 stomata, with their long axis predominantly
parallel to the long axis of the leaf (in adult foliage), separated within
each row by squarish epidermal cells. Stomatal rows are separated by
regions of elongate epidermal cells. The morphology of the stomatal
complexes sees each stomatal opening surrounded by 46 subsidiary
cells, and with the epidermal cells immediately surrounding these
modied in shape to form a second cycle around the subsidiary cells
(Chambers et al., 1998).
3.4.2. A. australis
Agathis ranges from southeast Asia, through northeastern Australia
to northern New Zealand, New Caledonia and Fiji (Pole, 2008). New
Caledonia is a center of diversity for the genus with ve species.
A. australis (New Zealand kauri) is a tall tree (up to 50 m), with a
straight cylindrical trunk (14 m thick) and an extensive crown; the
lowermost retained branches on mature trees are commonly at least
15 mfromtheground(Sando, 1936). Leaves are thick, elliptical to lance-
olate, about 37 cm long, 1 cm broad, and multiveined. Stomata occur in
rows; the stomatal openings are circular to rectangular, surrounded by
four subsidiary cells (Haworth et al., 2011a). Macrofossils condently
attributed to Agathis have only been recorded from Cenozoic strata
(Carpenter and Pole, 1995; Hill et al., 2008; Pole, 2008). Macrofossils as-
cribed to this genus from o lder strata (e.g., White, 1981; Daniel, 1989;
Cantrill, 1992)lackdenite characters for this genus and likely belong
to the large diversity of Mesozoic representatives of the family that has
been lost to extinction.
3.4.3. A. cupressoides
A. cupressoides (pencil pine) is a Southern Hemisphere evergreen
cupressacean conifer endemic to Tasmania. The conifer's leaf morphol-
ogy is scale-like, rhombic, ~45 mm long and 12 mm wide. Stomata
are irregularly arranged across the abaxial leaf surface, most abundant
distally (Haworth et al., 2010). Stomatal complexes are oval, with
the stomatal pore circular to rectangular and surrounded by 57sub-
sidiary cells. Epidermal cells are elongate and irregularly rectangula r.
A. cupressoides is endemic to Tasmania, Australia, whe re it grows at
7001300 m altitude, with an ecological preference for cool, moist
conditions (Cullen and Kirkpatrick, 1988; van der Ham et al., 2001;
Haworth et al., 2010). We include A. cupressoides here due to the su-
percial similarity of leaf macro-morphology and preference for wet
environments, but we consider it as the least ap propriate of the three
selected NLE species.
Table 1
Table of average stomatal index (SI), with standard error, of Allocladus helgei relative to each leaf analyzed (leaf 110: columns 1 and 2), and calculated average pCO
was calibrated using
each of the nearest living equivalents (Athrotaxis cupressoides, Wollemia nobilis, Agathis australis)relativetoeachleaf(columns34). Column 5 shows the average of all pCO
per leaf. The bottom line of the table shows the mean SI and pCO
for all leaves analyzed (with standard error).
Leaf nr. Mean SI pCO
A. cupressoides
W. nobilis
A. australis
Mean pCO
per leaf
(+/ 0.69)
707.4 776.8 909.5 797.9
(+/ 0.58)
752.5 826.4 967.5 848.8
(+/ 0.42)
801.9 880.7 1031.0 904.5
(+/ 1.03)
720.3 791.0 926.0 812.4
(+/ 0.80)
771.5 847.3 992.0 870.3
(+/ 0.53)
750.0 823.7 964.3 846.0
(+/ 0.39)
763.6 838.6 981.8 861.4
(+/ 0.69)
779.6 856.1 1002.3 879.4
(+/ 0.66)
833.7 915.6 1072.0 940.4
10 9.52
(+/ 0.67)
705.9 775.2 907.6 796.2
Mean 8.88
(+/ 0.48)
(+/ 45.0)
4 M. Steinthorsdottir, V. Vajda / Gondwana Research xxx (2013) xxxxxx
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
4. Results
The mean st omatal index based on ten leaves of A. helgei is
8.88% + / standard deviation of 0.4 8% (Table 1). Pliensbachian
calibrated using this mean SI, using the stomatal proxy method
with Carboniferous standardization and the three chosen NLEs, was
found to have a mean value of 855.7 ppm (Fig. 3 and Table 1). The
lowest pCO
value, using the NLE A. cupressoides is 758.6 ppm, whereas
W. nobilis and A. australis yield pCO
of 833.2 ppm and 975.4 ppm re-
spectively (Fig. 3). We speculate that since W. nobilis and A. australis
maybemorecloselyrelatedtoA. helgei than A. cupressoides, the former
are more appropriate NLEs to A. helgei. Focussing on the pCO
obtained using only the araucariacean conifers raises the calibrated
Pliensbachian pCO
to a mean of 904.3 ppm ( 900 ppm, see Fig. 3).
5. Discussion and conclusions
The ability to predict the effects of currently unfolding climate
change req uires detailed knowledge about the link between atmo-
spheri c CO
and climate through geologica l t ime. Although it may
be impossible to reconstruct pCO
based on stomatal density at
high resolution since the rise of vas cular plants, throughout the last
400 Ma of the Phanerozoic, every opportunity to add to our knowledge
about past pCO
should be seized. We suggest that the stomatal proxy
method, using ancient conifers with appropriate NLEs, is sufciently
well-established to reconstruct pCO
at any point in the geological time-
scale, including intervals of relatively stable pCO
ground of relative change.
5.1. Comparison with previous Early Jurassic pCO
While major events, pre- and postdating the Early Jurassic, such as
the mass extinction events outlined below, have been studied intensely
using multiple-proxy data and carbon cycle modeling, the intervening
non-event time periods, i.e. the Sinemurian and Pliensbachian, have
not received the same attention. During the Early Jurassic, greenhouse
conditions prevailed with generally very high atmospheric pCO
inferred (Cerling, 1991; Yapp and Poths, 1996; Ekart et al., 1999;
McElwain et al., 1999; Retallack, 2001; Beerling and Royer, 2002;
Berner, 2006; Retallack, 2009). However, t his has commonly been
based on background values close to stage boundaries characterized
by signicant global change (see Fig. 4).
Previous stomatal-based pCO
estimates from the Jurassic have been
carried out on Northern Hemisphere oras from intervals immediately
preceding and/or following major extinctions or turnovers in the geo-
logical record. Results from stomatal-proxy based pCO
estimates across
the TriassicJurassic (TrJ) boundary interval in Germany, Greenland
and the UK, based on conifer, ginkgoalean, bennettitalean and seed
fern leaves, reveal pCO
at ~20002500 ppm during the boundary inter-
val, whereas Late Triassic (Rhaetian) and Early Jurassic (Hettangian)
levels were signicantly lower, at ~10001500 ppm (McElwain et al.,
1999; Bonis et al., 2010a; Steinthorsdottir et al., 2011). The TrJbound-
ary is characterized by global extinctions of species both in the marine
and terrestrial realms followed by ecosystem collapse dened by signif-
icant carbon cycle perturbations traced in the carbon stable isotope
record (Raup and Sepkoski, 1982; Palfy et al., 2001; Hesselbo et al.,
2002; Kiessling et al., 2007; Lucas and Tanner, 2007; McElwain et al.,
2007, 2009; Aikikuni et al., 2010). Signals of elevated temperatures, in-
creased runoff and marine anoxia (indicated by black shale formation)
are evident at this time (Bonis e t al., 2010b; Richoz et al., 2010;
Steinthorsdottir et al., 2012). A narrowing consensus on the causal
mechanism of this disru ption of the ecos ystem centers on global
warming, driven by the relatively rapid increase of pCO
from eruptions within the Cent ral Atlantic Magmatic Province
(CAMP), is probably aggravated by the enhanced release of methane
and/or volcanic pollutants into the atmosphere (McElwain et al., 1999;
Hesselbo et al., 2002; McElwain et al., 2007; van d e Schootbrugge et al.,
2009; Ruhl et al., 2011; Lindström et al., 2012; Vajda et al., 2013). Al-
though past studies have concentrated on TrJ boundary events, they
also establish background conditions for the ensuing Early Jurassic
at ~10001500 ppm.
A subsequent mostly marine mass extinction took place in the earli-
est Toarcian (183 Ma; Hallam, 1987; Palfy and Smith, 2000; Gomez and
Goy, 2011; Cúneo et al., 2013), during the so-called Toarcian Ocean An-
oxic Event (T-OAE). Severe environmental perturbations occurred at
this time resulting in extinctions of biota and preservation of organic-
rich sediments in the marine realm (Aberhan and Baumiller, 2003;
McElwain et al., 2005; Dera et al., 2010; Gill et al., 2011). Further, the
T-OAE is characterized in the carbon isotope record by a distinct nega-
tive excursion and the formation of black shale, indicating anoxia
(Jiménez et al., 1996; Hesselbo et al., 2000; Beerling et al., 2002). This
event is most likely related to CO
out gas sing by the Ka rooFerrar
eruptions (Hesselbo et al., 2000; Palfy and Smith, 2000; Beerling
and Brentnall, 2007). The concentration of atmospheric CO
A. cupressoides W. nobilis A. australis
Mean pCO
Fig. 3. Calibrated stomatal proxy-based CO
) concentrations for the late Pliensbachian,
using the stomatal ratio method on fossil leaves of A. helgei, with the ne arest living
equivalent taxa Athrotaxis cupressoides, Wollemia nobilis and Agathis australi s.The
calibrated Pliensbachian pCO
values range from ~760 ppm to ~975 pmm, with a mean
of ~860 ppm.
Million years
from present
500 400
Fig. 4. The best Pliensbachian stomatal proxy-based CO
estimate of ~900ppm, using
Australian fossil conifer leaves, is shown (red box) relative to the Phanerozoic pCO
tained by the GEOCARB models (GEOCARB II of Berner (1994) as adjusted in GEOCARB
III of Berner and Kothavala (2001) (blue line with gray error envelope) and various addi-
tional proxies (green line). There is no direct proxy evidence from the Pliensbachian, but
rather pCO
is based on interpolation between data points. The pCO
values obtained in
this study are consistent with the lower estimates of previously published pCO
adapted from Berner and Kothavala (2001)). (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this article.)
5M. Steinthorsdottir, V. Vajda / Gondwana Research xxx (2013) xxxxxx
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
the T-OAE appears to have doubled, from ~1000 ppm to ~2000 ppm
(Beerling and Royer, 2002; McElwain et al., 2005; Berner, 2006;
Retallack, 2009). Early Jurassic background pCO
is thus conrmed
at around 1000 ppm.
Our calibrated pCO
values of ~900 ppm, based on Pliensbachian
araucariacean conifer leaf fossils from southeastern Australia are consis-
tent with high pCO
values relative to the present, but slightly less
than the Early Jurassic pCO
estimates of approximately 1000 ppm as
out lined above, based on different plant groups for the Nort hern
Hemisphere. The Pliensbachian pCO
constructed here falls close to
the med ian range (and well with in the error envelope) of pCO
reconstructed using the GEOCARB II and III models (Berner, 1994;
Berner and Kothavala, 2001; Fig. 4). Based on t he pCO
here using the stomatal method coupled with previous calculations
of Early Jurassic background pCO
values as detailed above, we sug-
gest that Early Jurassic pCO
(Hettangian to Pliensbachian) was approx-
imately 900 ppm (Fig. 4).
5.2. The importance of multiple locality, global pCO
Although CO
is the primary driver of climate change on geological
timescales (Royer et al., 2004), and has been shown to be well-mixed
in the global atmosphere (Keeling et al., 1989), some climate change
episodes have been attributed to internal dynamics, i.e. changes in
heat distribution via insolation, ocean currents or wind systems, typical-
ly because paleo-pCO
records commonly show little change and/or
contradictory results. Examples in the geological record include the
EoceneOligocene boundary event (~34 Mya) and the Younger Dryas
climate change (~12 800 cal years BP), when oxygen isotopes and
other proxies indicate large changes in temperatures, but changes in
records are small or enigmatic (Monnin et al., 2001; Zachos
et al., 2001; Broecker, 2006; Coxall and Pearson, 2007). However, the re-
sults of more recent paleo-pCO
studies are changing this view in unex-
pected ways. For instance, it seems that both the above-mentioned
cooling events may have been preceded by fairly abrupt but transient
rises in pCO
(Pagani et al., 2011; Steinthorsdottir et al., 2013), which
may then have forced a chain of feedbacks to unfold, leading eventually
to colder climates and associated CO
drawdown. Recent records show
dynamic behavior of pCO
across these climate change transitions, and
demonstrate that there is clearly still much to learn regarding the
coupling of pCO
and climate on short and long timescales. It is, there-
fore, important to obtain pCO
data preferably from multiple localities
and both hemispheres, when reconstructing paleoclimate, in order to
discriminate conditions that were global from those that were of re-
gional or local extent. Identical stomatal indices from multiple sources
on separate continents will strongly indicate a global climatic signature
and help explain mechanisms of climate change.
The results presented here are the rst pCO
estimates to derive
from Southern Hemisphere Jurassic plant material, but a few previously
published Southern Hemisphere stomatal proxy-based estimates do
exist. Passalia (2009) employed late Aptian (mid-Cretaceous) conifer
and Ginkgo leaf cuticles from Argentina, revealing that mid-Cretaceous
estimates range from 700 to 1400 ppm, which is also consistent
with Northern Hemisph ere results for Aptian pCO
levels. Retallack
(2002) collated, mostly from previously published taxonomical studies,
stomatal indices from several genera and multiple localities in both
hemispheres and c alibrated atmospheric pCO
for the Triassic
based on this data. Several Southern Hemisphere datasets were in-
cluded based on Lepidopteris leaves from Early Trias sic of Anta rctica
and Australia (McLoughlin et al., 1997), Middle Triassic of Australia
(To wnrow, 1966) and Late Triassic of Australia (Townrow, 1965),
Argentina (Baldoni, 1972) and South Africa (Townrow, 1956, 1960;
Anderson and Anderson, 1989). Results from these datasets conrmed
the Northern Hemisphere results of overall highly elevated Triassic
5.3. The potential of Australian fossil conifers in paleo-pCO
With time, the relatively new stomatal proxy method is becoming
increasingly well-established in paleo-pCO
reconstructions, after
most caveats h ave been ad dressed a nd early criticism rebuked
(McElwain and Haworth, 2009; Haworth et al., 2013). In particular,
the method is considered to provide the most accurate results when
using reliable NLEs such as araucariacean conifers (Haworth et al.,
2011a), and it now seems possible to accurately determine long-term
patterns using fossil leaves, even in the absence of supporting
The stomatal ratio method is continually being rened and strength-
ened by e.g. establishing specic criteria for the NLE plants that are used
in calibrations and by accumulating independent supporting evidence
of the stomata-based pCO
values. We suggest that the best practice in
Mesozoic pCO
reconstructions should include not only selecting NLEs
that are the closest equivalents in terms of phylogeny and ecology (as
per Chaloner and McElwain (1997)), but also applying multiple species
of proven CO
responders with closely matching stomatal indices. This
should maximize the probability that the NLEs are expressing real
physiological responses to pCO
, which evolved in the Mesozoic and
thus reect the same responses in fossil Mesozoic plants.
The relative abundance of Araucariaceae in the fossil record has
assisted paleobotanists to unravel much of this family's past evolution
and geographical distribution. Even though Araucariaceae primarily
ourishes in the Southern Hemisphere today, it is evident that this
distribution is a remnant of its past geographically widespread range,
which includes most parts of the Northern Hemisphere back to at least
the Jurassic (Stockey, 1982, 1994; Vajda, 2001; Kunzmann, 2007).
While this family's taxonomy has been documented in many studies,
analyses of stomata as a tool for interpreting climatic signals through
estimates have not been performed on Southern Hemisphere
araucariacean fossil conifers. We contend that the Southern Hemisphere
Araucariaceae leaf assemblages constitute a true geological treasure, es-
pecially as the close modern relatives to these middle and late Mesozoic
taxa presently ourishing in this region. The Australian record is particu-
larly signicant in this regard, with key macrofossil assemblages charac-
terized by organic preservation represented through the Early Jurassic
(Cattamarra Coal Measures: McLoughlin and Pott, 2009), Middle Jurassic
(Walloon Coal Measures: Gould, 1980), Late Jurassic (Talbragar Fossil
Fish Beds: White, 1981), Early Cretaceous (Otway and Strzelecki groups:
Douglas, 1969; McLoughlin et al., 2002; Nagalingum et al., 2005), mid-
Cretaceous (Otway Group and Winton Formation: Cantrill, 1991, 1992;
Pole, 2000) and Late Cretaceous (Waarre Formation: Douglas, 1965).
5.4. Concluding remarks
Based on the stomatal method, using fossil leaves from the Australian
araucariacean conifer A. helgei, we reconstructed pCO
for the late
Pliensbachian at ~900 ppm. This atmospheric CO
concentration is
slightly lower but broadly consistent with the results from stomatal-
based pCO
reconstructions for adjacent geological time periods based
on equivalent methodologies in the Northern Hemisphere, and also
with the lower ranges of GEOCARB II and GEOCARB III (Berner, 1994;
Berner and Kothavala, 2001)modeledpCO
(Fig. 4).
Constraining the uncertainty associated with predictions of the
likely impacts of future climate change is a topical eld of scientic
research. Records of biotic turnover coupled with well-constrained at-
mospheric models provide important insights into how past ecosystems
responded to climate change. Amassing an extensive database of past
interpretations will provide improved reconstructions of the
scale and rate of atmospheric pCO
changes and permit improved
predictions of biotic responses to future climate change. Australian coni-
fers are emerging as an ideal group to be utilized in stomatal-based
reconstructions, due to their long evolutionary lineages, and prov-
en retained responses to high levels of pCO
. With the recent advances
6 M. Steinthorsdottir, V. Vajda / Gondwana Research xxx (2013) xxxxxx
Please cite this article as: Steinthorsdottir, M., Vajda, V., Early Jurassic (late Pliensbachian) CO
concentrations based on stomatal analysis of fossil
conifer leaves from eastern Australia, Gondwana Research (2013),
in stomatal proxy research, it is now highly feasible to utilize fossil coni-
fers with the appropriate NLEs to reconstruct pCO
, enabling a more ex-
tensive range of fossil leaf material to be employed in paleo-pCO
M.S. acknowledges funding by the Swedish Research Council
(VR grant nr: 623-2011-1048). This research was further supported by
the Swedish Research Council LUCCI grant (Lund University Carbon
Cycle Centre) to V.V. L. Santasalo (Lund University) analyzed the fossil
leaves in a preliminary study to select the most well preserved speci-
mens. I.-M. Jansson and S. McLoughlin (Swedish Museum of Natural
History) helped collect material during eldwork in the Inverleigh
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