2014
research-articleResearch ArticleXXX10.1144/jgs2013-127E. L. Gulbranson et al.Leaf Habit of Glossopterid Forests
Journal of the Geological Society, London, Vol. 171, 2014, pp. 493­–507. http://dx.doi.org/10.1144/jgs2013-127
Published Online First on April 28, 2014
© 2014 The Authors
Leaf habit of Late Permian Glossopteris trees from high-palaeolatitude forests
Erik L. Gulbranson 1* , Patricia E. Ryberg 2 , Anne-Laure Decombeix 3 , Edith L.
Taylor 4 , Thomas N. Taylor 4 & John L. Isbell 1
1Department of Geosciences, University of Wisconsin–Milwaukee, Milwaukee, WI 53211, USA
2Department of Physical and Natural Sciences, Park University, Parkville, MO 64152, USA
3CNRS-UMR AMAP (Botanique et Bioinformatique de l’Architecture des Plantes), Montpellier, Cedex 5, France
4Department of Ecology and Evolutionary Biology, Natural History Museum and Biodiversity Institute, University of Kansas,
Lawrence, KS 66045, USA
*Corresponding author (e-mail: [email protected])
Abstract: The leaf longevity of trees, deciduous or evergreen, plays an important role in climate feedbacks
and plant ecology. In modern forests of the high latitudes, evergreen trees dominate; however, the fossil record indicates that deciduous vegetation dominated during some previous warm intervals. We show,
through an integration of palaeobotanical techniques and isotope geochemistry of trees in one of the earliest
polar forests (Late Permian, c. 260 Ma, Antarctica), that the arborescent glossopterid taxa were both deciduous and evergreen, with a greater abundance of evergreen trees occurring in the studied forests. These new
findings suggest the possibility that deciduousness was a plastic trait in ancient polar plants, and that deciduous plants, migrating poleward from lower latitudes, were probably better adapted to high-disturbance areas
in environments that were light-limited.
Supplementary material: Wood anatomy descriptions (supplemental file 1), stable carbon isotope data for
tree rings (supplemental files 2–4), and method and parameters for modelled ∆13C (supplemental file 5) are
available at www.geolsoc.org.uk/SUP18744.
Gold Open Access: this article is published under the terms of the CC-BY 3.0 license.
The discovery of fossil leaf mats implies that deciduous plants
occupied polar landmasses in Earth history and gave rise to the
hypothesis that deciduous leaf habits were favourable at high latitudes during times of global warmth (Wolfe 1980; Axelrod 1984;
Spicer & Chapman 1990). This hypothesis was based on the
assumption that leafless deciduous plants maintained a carbon balance edge over evergreen trees by losing less carbon through respiration during the extreme (c. 4 month) polar winter with 24 h of
continuous darkness. Thus, the positive carbon balance experienced by deciduous plants created a competitive edge that allowed
such plants to dominate warm ancient polar ecosystems. Growth
chamber experiments and numerical models, however, demonstrate
that there is no carbon balance advantage for deciduous trees over
evergreen trees grown under a simulated polar photoperiod
(Osborne & Beerling 2002; Royer et al. 2003, 2005), because
deciduous trees must annually regrow all leaf tissue, and the carbon
source for this new growth must be derived from photosynthate
fixed during previous growing seasons (Sauter 1967; Essiamah &
Eschrich 1985; Barbaroux & Breda 2002; Damesin & LeLarge
2003). Nevertheless, fossil evidence of trees such as Metasequoia,
Larix, Alnus and Betula provides support that deciduous trees dominated the Northern Hemisphere polar regions during the Cenozoic
(Wolfe 1980; Greenwood & Basinger 1993; Greenwood 1994; Williams et al. 2003, 2008; Ballantyne et al. 2010; Csank et al.
2011a,b) and the Cretaceous (Spicer & Parrish 1986; Spicer &
Chapman 1990), and they are interpreted to have dominated the
Southern Hemisphere polar regions during the Permian and Triassic (Fig. 1; Gould & Delevoryas 1977; Taylor et al. 1992; Francis
et al. 1993; McLoughlin 1994; McLoughlin et al. 1997; Cúneo
1996; McLoughlin et al. 2005). Evergreen trees belonging to Araucariaceae and Podocarpaceae, on the other hand, dominated the
Southern Hemisphere polar regions during the Cretaceous and
Jurassic (Cantrill 1991, 1992; Pole 1999; Falcon-Lang & Cantrill
2001). These deep-time examples of polar ecosystems suggest that
there may have been an adaptation of leaf longevity to high-latitude
ecosystems during greenhouse intervals; however, the mechanism
for determining the dominance of a particular type of leaf habit
remains poorly defined.
That leaf longevity varied with latitude in the past is an important
concept to understand because (1) leaf longevity affects a range of
processes (e.g. photosynthetic rate, drought tolerance) that allow
plants to respond to environmental stresses (Monk 1966; Mooney
1972; Reich et al. 1992), (2) leaf longevity of polar ecosystems is
modelled to have a strong influence on seasonal changes in albedo
and, therefore, has a strong impact on palaeoclimate (Otto-Bliesner
& Upchurch 1997; Ollinger et al. 2008; Horton et al. 2010), and (3)
extant forests display latitudinal variations in leaf habit that may be
dissimilar to those of the ancient forests, as evergreen trees currently
dominate northern high latitudes, whereas deciduous trees dominate
temperate forests (Fig. 1a; Chapin 1980; Chabot & Hicks 1982;
Givnish 2002). There is parity in inferences of leaf habit from lowlatitude fossil ecosystems and extant tropical ecosystems (DiMichele
et al. 2010; Falcon-Lang et al. 2011; Stull et al. 2012); however, the
disparity in the dominance of extant evergreen floras at modern high
latitudes and interpretations of dominantly deciduous floras at high
palaeolatitudes suggests that our understanding of plant migration
and the ecology of plants at high latitudes is poor. Thus, to better
understand plant–climate interactions in deep time it is important to
understand broad-scale patterns in leaf longevity. By understanding
this level of detail of plant ecology in deep time it is possible to
make more meaningful connections to contemporary global change
and the potential response of plants to this change.
This paper addresses the supposed dominance of deciduous vegetation in ancient forests at polar latitudes through reconstructions
493
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E. L. Gulbranson et al.
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of leaf longevity from Late Permian fossil trees (Fig. 1). We infer
leaf longevity from three in situ fossil forests (Fig. 2) using a multipronged approach where we (1) use traditional palaeobotanical
methods to assess the wood morphology and growth characteristics
by analysing the anatomy of fossil wood, determining each specimen’s morphogenus, and documenting tree ring growth patterns,
and (2) use carbon stable isotope geochemistry of fossil growth
rings to determine distinct patterns that we interpret as relating to
the disparate carbohydrate cycling strategies of evergreen versus
deciduous trees.
Background
Leaf habit of Glossopteris
Previous inferences of leaf longevity of Permian glossopterid trees
were based primarily on indirect evidence from sedimentological
observations that fossil Glossopteris leaves are found in dense
accumulations, so-called leaf mats, which were interpreted to be
the result of leaf abscission induced by seasonal light limitation
(Gould & Delevoryas 1977; Retallack 1980; Cúneo et al. 1993).
Direct evidence of leaf longevity can be determined by assessing
whether leaf traces found in wood terminate within a single growth
ring (deciduous) or transcend several annual increments of growth
(7
Fig. 1. Comparison of modern climate
and biomes with those reconstructed for
the latest Permian climate and biomes. (a)
Present-day distribution of climate regimes.
Some Köppen–Geiger climate zones are not
shown or are grouped together to make a
more direct comparison with latest Permian
climates (modified from Kottek et al.
2006). Boreal forests (Dfa–Dfb to Dfc) are
predominantly evergreen, whereas temperate
forests are dominated by deciduous trees
(Cfa to Dfa–Dfb). (b) Latest Permian
climate reconstruction (modified from
Rees et al. 2002; Kiehl & Shields 2006;
Horton & Poulsen 2009; Roscher et al.
2011). The Glossopteris flora occurs in
the Southern Hemisphere Dfa–Dfb to Dfc
zones and is interpreted to be deciduous.
The southernmost part of Gondwana was
interpreted to be a tundra ecosystem by
Rees et al. (2002), but modelled temperature
using a dynamic ocean–atmosphere model
produces conditions more favourable for
forest growth (Kiehl & Shields 2005;
Roscher et al. 2011).
(evergreen) (Eames & McDaniels 1947; Falcon-Lang & Cantrill
2001). Such palaeobotanical inferences of leaf longevity, however,
are limited in deep time, because of the low probability of preservation, taphonomy of the fossils and detection of such anatomy. As a
consequence, our concept of the Glossopteris plant is based on
indirect evidence that is interpreted to indicate that glossopterids
were deciduous plants (Plumstead 1958; Retallack 1980), and this
view holds for the glossopterids across Gondwana, throughout the
Permian (Gould & Delevoryas 1977). We will show here that this
concept is incomplete by using two independent methods to infer
leaf longevity (i.e. anatomical characteristics of tree rings and carbon isotope patterns within rings) from multiple trees at three fossil
forest localities, which will provide direct evidence for leaf longevity based on patterns imparted into tree rings owing to the physiological conditions of plant growth.
Geochemical inference of leaf habit
Stable isotope geochemistry has been applied to growth rings of
modern trees for over four decades to assess the environmental
controls on tree ring stable isotope composition (Lowden & Dyck
1974; Francey & Farquhar 1982; Leavitt & Long 1991; Loader
et al. 1995; Hemming et al. 2001; Barbour et al. 2002; Helle &
Schleser 2004; McCarroll & Loader 2004; Ogée et al. 2009;
Leaf Habit of Glossopterid Forests
495
Fig. 2. Study area in Antarctica and
reconstructions of the three fossil forests.
(a) Map of the study area in the central
Transantarctic Mountains showing the three
studied fossil forests at Graphite Peak, Wahl
Glacier, and Mt. Achernar. (b–d) Fossil
forest reconstructions (after Gulbranson
et al. 2012) showing tree positions and
average tree heights for Mt. Achernar and
Wahl Glacier, and tree height estimates for
each tree at the Graphite Peak fossil forest.
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δ13C (‰ VPDB)
Ohashi et al. 2009; Offermann et al. 2011; Roden & Farquhar
2012), and to complement dendrochronology-based dendroclimatology studies (Wilson & Grinstead 1977; Schleser et al. 1999;
Poussart et al. 2004; Treydte et al. 2006; Hafner et al. 2011; Au &
Tardif 2012). Only in the last decade, however, have high-resolution (more than three measurements per ring) isotope analyses
been completed on single growth rings in modern trees (e.g.
Barbour et al. 2002; Helle & Schleser 2004; Poussart et al. 2004;
Skomarkova et al. 2006; Ohashi et al. 2009; Schubert & Jahren
2011) and sub-fossil wood (Jahren & Sternberg 2003, 2008;
Schubert et al. 2012). The high-resolution sampling of growth
rings reveals changes in the δ13C value of wood throughout a
growing season that correspond to intra-ring patterns that are
reproducible from year to year and reproducible between different
species that share similar leaf longevity (Helle & Schleser 2004).
Moreover, these carbon isotope patterns within growth rings are
distinct between evergreen and deciduous trees (Fig. 3; Gulbranson
& Ryberg 2013). Therefore, high-resolution stable carbon isotope
analysis in tree rings is a new technique that can be used independent of, but in conjunction with, palaeobotanical techniques to infer
the leaf habit of fossil plants.
Evergreen trees produce a nearly symmetrical pattern in δ13C
values within their growth rings (Fig. 3a), with similar δ13C values at either end of a growth ring and a peak δ13C value near the
middle of a growth ring (Barbour et al. 2002; Schubert & Jahren
2011; fig. 1A of Gulbranson & Ryberg 2013). The symmetry is
probably related to a combination of factors including the following: (1) low rates of photosynthetic CO2 assimilation early in the
growing season (Francey & Farquhar 1982), resulting in relatively more negative δ13C values in the earlywood; (2) decreasing
atmospheric CO2 concentrations from bud burst to the time of
peak photosynthetic rate (Keeling 1960, 1961), which can produce increasingly more positive δ13C values, but with low magnitude near the middle of a ring; (3) increasing intercellular CO2
concentrations from the time period between peak photosynthetic
capacity and dormancy (Davis & McCree 1978; Rawson &
Constable 1980), which leads to successively more negative δ13C
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Fig. 3. Conceptual model of δ13C patterns in tree rings (modified from
Gulbranson & Ryberg 2013). (a) δ13C patterns of a ring in an evergreen
tree. (b) δ13C patterns of a ring in a deciduous tree; numbers correspond
to a three-phase model to explain the physiological basis for this
variation in δ13C values. Vertical dotted lines indicate ring boundaries;
continuous black lines indicate δ13C values of wood.
values into the latewood. The symmetry of δ13C patterns in a
given tree ring can be complicated by the response of a plant to
micrometeorological factors, which can produce slight asymmetry and multiple peaks and troughs of δ13C pattern (Walcroft et al.
1997; Barbour et al. 2002). Therefore, the δ13C value patterns of
evergreen tree rings can be modified by variations in meteorological conditions that affect the balance of photosynthetic assimilation and the loss of water via stomatal conductance during the
growing season (Livingston & Spittlehouse 1996; Walcroft et al.
1997; Barbour et al. 2002), which is consistent with the hypothesis developed by Francey & Farquhar (1982) to explain seasonal
δ13C variation in tree rings.
496
E. L. Gulbranson et al.
The model developed by Francey & Farquhar (1982), however,
does not take into account that leaf longevity may affect the δ13C
values of growth rings from deciduous trees. High-resolution sampling of tree rings of deciduous trees demonstrates a remarkably
different δ13C pattern than in evergreen trees, inconsistent with the
hypothesis that δ13C values of wood are controlled primarily by
photosynthetic isotope discrimination (Helle & Schleser 2004).
The complex trend of δ13C values in deciduous tree rings has been
broken down into three phases (Fig. 3b; Helle & Schleser 2004;
Offermann et al. 2011): (1) a δ13C peak in the earlywood corresponding to the use of stored carbohydrates prior to or concurrent
with bud burst and leaf expansion; (2) a progressive lowering of
δ13C values corresponding to a mixture of respiration and the use
of recently fixed photosynthate and stored carbohydrate for biomass production (Lowden & Dyck 1974; Damesin & LeLarge
2003; Kuptz et al. 2011), which potentially reaches a consistent
δ13C value after peak photosynthetic capacity has been reached
and just prior to renewed carbohydrate storage in preparation for
dormancy; (3) a slight increase in δ13C values in the latewood of a
tree ring corresponding to the preparation for winter dormancy
(Helle & Schleser 2004; Kagawa et al. 2006; Eglin et al. 2009).
These three components produce an asymmetric, sawtooth-like,
pattern in δ13C values that corresponds to storage of carbohydrates
and the use of stored carbohydrates as a carbon source (latewood
through a portion of earlywood), marked by an increase in δ13C
values, and autotrophy, marked by a subsequent decline in δ13C
values in the earlywood.
Stratigraphic and sedimentological setting
Fossil wood specimens studied herein were collected at Graphite
Peak (accession numbers 17,771; 17,772), Wahl Glacier (17,773;
17,774; 17,775; 17,776; Knepprath 2006), and Mt. Achernar
(17,169 A, B top and bottom, C; 11,617; 11,472) from the upper
Buckley Formation in the central Transantarctic Mountains (Fig.
2a; Beardmore Glacier region). The Buckley Formation contains
terrestrial sedimentary rocks that were deposited in a retroarc foreland
basin (Dalziel & Elliot 1982; Collinson 1990; Isbell et al. 1997;
Collinson et al. 2006). The Buckley Formation is informally
divided into two members: a lower member consisting of
quartzofeldspathic fluvial sandstones, and an upper member consisting of coal and volcaniclastic fluvial and lacustrine sandstones
(Barrett et al. 1986; Isbell 1990; Collinson et al. 1994).
Chronostratigraphy for the succession is based on palynomorphs,
whereas chemostratigraphic results suggest potentially higher-resolution correlation of stratigraphy and the preservation of the two
negative carbon isotope excursions associated with the end-Permian biotic crisis (Retallack et al. 2005, 2006). Palynological associations for the Buckley Formation include Dulhuntyispora
assemblages in the lower member and Protohaploxypinus and
Lunatisporites zones in the upper member (Farabee et al. 1990,
1991; Collinson et al. 2006). The microfloral zones of the upper
member correlate to the Australian APP5–APT1 biozones (Price
et al. 1985; Mantle et al. 2010) and indicate a Late Permian age
(260–251.2 Ma) for the fossil wood analysed here.
The fossil forests are found in the upper member of the Buckley
Formation in fine-grained, crudely laminated, volcaniclastic deposits. A sedimentological, stratigraphic, and palaeoforestry analysis
for the localities was presented by Gulbranson et al. (2012), but the
salient results are summarized here to provide a palaeoenvironmental context for the studied wood specimens. The three fossil forest
localities are found in channel proximal floodplain facies (Graphite
Peak and Wahl Glacier), and distal floodplain or marginal lacustrine facies (Mt. Achernar) (Taylor et al. 1992). Despite the absence
of higher-precision chronostratigraphic resolution, Gulbranson
et al. (2012) interpreted these three localities as approximately time
equivalent based on the stratigraphic position of the fossil forests
relative to the stratigraphically younger contact between the Upper
Permian Buckley and Triassic Fremouw formations. The fossil forests display variation in tree density, tree height, and wood basal
area that may correspond to variations in palaeoenvironments (Fig.
2b–d; Gulbranson et al. 2012), as well as differences in forest age
(Taylor et al. 1992). High-density juvenile forests (Mt. Achernar)
occur on distal floodplains or lake margins, whereas low-density
mature forests occur at Wahl Glacier and Graphite Peak, which
contain large-diameter trunks (30–60 cm) that correspond to tree
heights of 20–30 m (Knepprath 2006; Gulbranson et al. 2012).
We compare the documented plant macrofossils from the three
fossil forests with the well-preserved macrofossils from permineralized peat collected at Skaar Ridge (84.77°S, 163.28°E), which
is located on the Beardmore Glacier c. 42 km east and north of
Graphite Peak. Plants identified in the Skaar Ridge peat that
could probably be representatives of understorey vegetation
include a fern (Galtier & Taylor 1994), moss (Smoot & Taylor
1986), and a lycopsid (Ryberg et al. 2012). One of the few anatomical attachments of Glossopteris leaves to wood, G. skaarensis, has been recovered from the Skaar Ridge peat (Pigg & Taylor
1993). Given the proximity of Skaar Ridge to the studied fossil
forests, the abundance of macroflora and the specific plants preserved at Skaar Ridge have significant implications for our palaeoecological reconstruction. To date, understorey vegetation is
known from Mt. Achernar, where a herbaceous lycopsid is preserved in siltstone of the upper Buckley Formation (Schwendemann
et al. 2010), but understorey vegetation has not been recovered at
Graphite Peak or Wahl Glacier. It is unclear if the difference in
plant communities recovered from Skaar Ridge, Mt. Achernar,
Wahl Glacier, and Graphite Peak reflects a taphonomic bias (e.g.
DiMichele & Falcon-Lang 2011) in the stratigraphic record or a
variation in palaeoecology such as the occurrence of ferns in permineralized peat at the Skaar Ridge locality (Galtier & Taylor
1994) and absence of ferns and permineralized peat at the nearby
Mt. Achernar locality.
Methods
Thin sections were prepared from transverse, radial, and tangential
sections of fossil wood for wood taxonomic identification.
Observation and photography were conducted using Sony XCDU100CR digital cameras attached to an Olympus SZX12 stereomicroscope and an Olympus BX51 compound microscope. Images
were captured using Archimed software (Microvision Instruments)
and Figure 4 was composed using Adobe Photoshop CS5 version
12.0 (Adobe Systems Inc.). Transformations made to the images in
Photoshop include cropping, rotation, and adjustment of contrast.
Figure 4g is a composite of several photographs in different focus
planes created with the Multifocus option of Archimed.
Measurements for taxonomic identification were made using
ImageJ (Rasband 2013).
Leaf longevity was reconstructed using two independent methods, measurement of tracheid cells within growth rings known as
the cumulative sum of deviations from the mean (CSDM) (Creber
& Chaloner 1984) and stable carbon isotope patterns in tree rings.
For the CSDM approach, we used the method developed by
Falcon-Lang (2000) to determine leaf longevity in the fossil wood
specimens. Transverse thin sections were prepared from the
matching face of the specimen that was used for wood taxonomy.
Five adjacent rows of tracheid radial diameters were measured in
a single ring to determine the average change in cell formation
Leaf Habit of Glossopterid Forests
497
Fig. 4. Photomicrographs of fossil wood
specimens illustrating the anatomy and
affinities with Australoxylon. (a) General
aspect of the wood in transverse section;
slide WG-6 tr (specimen 17,775). (b, c)
Detail of growth ring anatomy in two
specimens showing the latewood of one
growth season (bottom), distinct ring
boundary, and earlywood of the next
growth season (top); slides WG-6 tr (b)
and MA-1 tr (c; specimen 17,169). (d, e)
Radial sections showing cross-field pitting
with numerous small crowded pits; slides
WG-6 ra (d) and WG-10 ra (e; specimen
17,776). (f, g) Tangential sections showing
uniseriate rays, with a partly biseriate ray
formed by the fusion of two uniseriate
rays (black arrow in (f)); slides WG-6 ta
(f) and MA-1 ta (g). (h, i) Mixed pitting
on the radial wall of tracheids; slide
WG-5 ra (specimen 17,774): uniseriate
pits with both spaced (s) and contiguous
(c) arrangement shown in (h); uniseriate
spaced (s) and multiseriate crowded (c)
pits in (i). (j) Grouped pits typical of
Australoxylon (arrows); slide WG-5 ra.
Scale bars represent 1 mm for (a); 100 µm
for (b), (c) and (f); 50 µm for (g); 25 µm for
(d), (e) and (h)–(j).
across a single season’s growth. Leaf longevity was determined by
graphing the CSDM curve.
Prior to stable carbon isotope analysis ring width measurements
were made with calipers (±0.001 mm), or via optical microscopy
for poorly preserved rings, to document growth characteristics of
wood specimens. To assess the acceptability of the data, duplicate
measurements of ring widths were made and differences between
the original and duplicate measurements were squared and summed,
where acceptable data have a summed square difference value <0.2
(Fritts 1976). We measured all preserved rings in the specimens
and the data are used to calculate two metrics used to assess growth
characteristics, annual sensitivity and mean sensitivity. Annual
sensitivity (AS) values,
AS = 2
Rw 1 − Rw 2
Rw 1 + Rw 2
, where Rw1 and Rw2 denote
ring widths for two successive tree rings, range from zero to two,
and are an indicator of the relative change in ring widths, where AS
values >0.3 indicate fluctuating growing conditions and low AS
values indicate complacent growth. Mean sensitivity (MS),
1
n −1
MS =
∑ ASn , is a measure of whether a plant is stressed
n − 1 n =1
(MS >0.3) or maintained all of the essential conditions for growth
(MS <0.3) (Fritts 1976). For leaf longevity analysis we hypothesize, based on the principle of limiting factors, that microsampling
increments of fluctuating growth may be more informative owing
to the potential to isolate a dominant climate control on plant
growth, whereas growth intervals with little variation in ring width
reflect equable growth and could be less sensitive to climate owing
to the competing effects of physiological and/or genetic factors.
Stable isotope ratios of carbon (13C/12C) in fossil wood specimens were measured in the Stable Isotope Facility at the University
of California–Davis. Samples of permineralized wood were ground
away from a pre-cut billet (small portion of rock trimmed with a
rock saw) by hand with a rotary tool equipped with a diamond bit
at the University of Wisconsin–Milwaukee. The sampled length (in
the growth direction) was measured with calipers, and the homogenized powders were transferred to tin capsules for analysis via
elemental analyser–continuous flow isotope ratio mass spectrometry (EA-CFIRMS). Sample sizes ranged from 23 to 56 mg and a
billet with a cross-sectional area of 6 cm2 was appropriate for sampling at <0.1 mm resolution. Billets were cut such that ring boundaries were approximately parallel, straight, and had minimal
distortion, to avoid mixing of different components of a growth
ring during grinding. The outermost growth rings were preferentially sampled to avoid physiological differences that can occur
during tree maturation (Francey & Farquhar 1982; Falcon-Lang
2005). X-ray diffraction analysis and petrography did not indicate
498
E. L. Gulbranson et al.
Table 1. Tree ring measurements for Late Permian wood
Specimen number
17,169
11,472A
11,617D
11,617B
17,773
17,774
17,775
17,776
17,771
17,772
Total rings
Maximum width (mm)
Minimum width (mm)
26
20
39
39
36
32
24
17
36
12
2.1
3.4
2.8
3.3
2.3
2.9
2.3
2.0
5.4
3.3
0.36
0.33
0.61
0.49
0.66
0.65
0.53
0.24
0.60
1.4
the presence of carbonate minerals, thus contamination from inorganic carbon sources is unlikely in these specimens. Results of isotope analysis are reported in the conventional delta notation (parts
per thousand) relative to the Vienna Pee Dee Belemnite (VPDB)
international reference.
Samples analysed at the UC Davis Stable Isotope Facility were
run with secondary reference materials (nylon, δ13C = –27.81‰;
bovine liver, δ13C = 21.69‰; peach leaves, δ13C = –26.12‰), each
calibrated against primary reference materials, to correct and normalize the data. These secondary reference materials have standard
deviations better than 0.1‰ (analysis period July 2011–June 2013);
however, the nylon reference material had a standard deviation of
0.2‰ for April 2012. A quality assurance standard was included in
the batches to assess the performance of the instrument in the long
term. This standard (USGS-41 Glutamic Acid, δ13C = +37.626‰)
had a standard deviation better than 0.3‰ over the course of the
experiment and a mean δ13C value of +37.62‰.
Specimens and slides are curated in the Paleobotanical
Collections (KUPB) of the Natural History Museum and
Biodiversity Institute, University of Kansas.
Results
Wood affinities
All specimens lack preserved primary vascular structures; therefore
they are classified only to wood morphogenera. They show distinct
growth rings (Fig. 4a–c). When compared with woods previously
reported from Antarctica, the new specimens can be distinguished
from Megaporoxylon, Protophyllocladoxylon, and Dadoxylon
(Maheshwari 1972). Both Megaporoxylon and Protophyllocladoxlyon
can be recognized by the presence of a single, large pit in most
cross-fields, and none of the specimens show this character (Fig. 4d
and e). Dadoxylon is easily recognized by the presence of biseriate
rays and none of the specimens show this characteristic either (Fig.
4f and g). The observed characters indicate that the specimens from
the three localities all have affinities with Australoxylon, a genus
close to Araucarioxylon (Philippe 2011). Australoxylon was created
by Marguerier (1973) for wood specimens from the Permian of
Gondwana and has the following characteristics: distinct growth
rings, square to rectangular tracheids in transverse section, three
types of radial pitting (araucarioid, abietinean, and conspicuous
arrangements of independent and spaced radial files of circular pits),
and groups of 2–3–4–5 pits distant from each other. Pits are small
(<15 µm). Australoxylon is recognized as a well-circumscribed
group of wood closely related to Araucarioxlyon and is associated
with Glossopteris flora across Gondwana (Merlotti & Kurzawe
2006; Philippe 2011). The main character distinguishing
Australoxylon from typical Araucarioxylon is the presence of
Mean width and SD (mm)
1.1 ± 0.4
1.1 ± 0.8
1.4 ± 0.6
1.4 ± 0.7
1.4 ± 0.4
1.4 ± 0.5
1.5 ± 0.4
0.93 ± 0.4
1.9 ± 0.9
2.3 ± 0.6
Mean sensitivity (MS)
0.46
0.78
0.40
0.39
0.35
0.42
0.25
0.37
0.43
0.31
mixed-type pitting on the tracheid radials, whereas Araucarioxylon
has only araucarian radial pitting (contiguous when uniseriate,
crowded and alternate when multiseriate). Vertebraria axes in the
Permian of Brazil, Skaar Ridge in Antarctica, and Prince Charles
Mountains in Antarctica have an Australoxylon wood type (Mussa
1978; Neish et al. 1993; Decombeix et al. 2009). Glossopteris skaarensis, one of three known taxa that has anatomical attachment of
Glossopteris leaves to wood (Pigg & Taylor 1993), has wood with
uni- to biseriate pits that are crowded to widely spaced and can be
compared with Australoxylon. All of the specimens in this study
show a mixed type of pitting, with both araucarioid and abietinean
pitting; in addition, pits arranged in radial groups are present in at
least four specimens (Fig. 4h–j). On this basis, all of the wood specimens studied herein can be classified as Australoxylon with a probable affinity to the glossopterids.
Anatomical ring analysis
Mean sensitivity for Mt. Achernar specimens ranges from 0.39 to
0.78 and average ring widths are between 1.1 and 1.4 mm (Table 1).
Annual sensitivity (AS) is highly variable within each specimen,
but in general, intervals of 2–4 rings have AS lower than 0.3, the
cutoff for tree rings that are considered ‘complacent’; that is, they
provide little record of climate variation (Fig. 5). These intervals
are punctuated by 3–6 ring intervals where AS is >0.3. Tree ring
intervals with high AS were preferentially selected for microsampling for carbon isotope analysis (Fig. 5), with the exception of
specimen 11,617B, which has better preservation of tree rings on
the outer portion of the specimen that facilitate microsampling. The
sampled interval of 11,617B, however, has AS values below 0.3.
Mean sensitivity for Wahl Glacier specimens ranges from 0.25 to
0.42 and average ring widths are between 0.93 and 1.5 mm (Table 1).
In contrast to Mt. Achernar, the Wahl Glacier specimens display
longer continuous intervals where AS is <0.3 (intervals of c. 14
rings), and shorter intervals, 2–5 rings, where AS is >0.3 (Fig. 5).
The two specimens from Graphite Peak have a mean sensitivity
of 0.43 for specimen 17,771 and 0.31 for 17,772. Specimen 17,771
has an average ring width of 1.9 mm, and 17,772 has an average
ring width of 2.3 mm. Both specimens display highly varied AS
values with intervals of 2–3 rings with AS > 0.3, and intervals of
3–5 rings with AS > 0.3 (Fig. 5).
Leaf longevity reconstructions based on the CSDM method
depend upon the position of the earlywood–latewood boundary
(EW–LW) relative to the median point of a ring. If the EW–LW
point on the graph is to the left (<10%) of the median point, then
the tree can be classified as deciduous. If the EW–LW point is to
the right (>10%) of the median point, then the tree can be classified
as evergreen. If the percentage skew is between −10% and +10%
of the median point, then the leaf habit is inconclusive, but may
Leaf Habit of Glossopterid Forests
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indicate relatively short-lived leaves. Measurement of tracheid cell
diameter was possible for seven specimens; poor preservation of
tracheid cells owing to compression and distortion did not permit
such measurements in all specimens. Two samples from Mt.
Achernar (17,169; 11,617) were measured (Fig. 6). Tangential tracheid diameters for sample 17,169 range from 11 to 31 µm (n = 19)
and radial tracheid diameters range from 11 to 50 µm (n = 22). The
per cent skew of 17,169 is 24.5%. In sample 11,617 the radial tracheid diameters range from 7 to 39 µm. The per cent skew of 11,617
is 15.1%. We interpret these CSDM results as indicating an evergreen habit for all of the studied specimens.
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Fig. 5. Ring width data for the studied
wood specimens. Annual sensitivities
(AS) >0.3 are interpreted to reflect
stressed conditions, and AS values < 0.3
are interpreted as growth intervals with
less environmental stress. Shaded areas in
(b), (d) and (f) correspond to the intervals
used for carbon isotope analysis. (a, c, e)
Histogram of annual sensitivity results for
each specimen from the study localities:
(a) Mt. Achernar; (c) Wahl Glacier; (e)
Graphite Peak. (b, d, f) Annual sensitivity
results plotted along the growth direction
for each specimen from the study localities:
(b) Mt. Achernar; (d) Wahl Glacier; (f)
Graphite Peak. Direction of growth is from
left to right.
Four specimens were analysed from Wahl Glacier. Specimen
17,776 has tracheid diameters in tangential section that range from
7 to 31 µm (n = 18) and tracheid diameters in radial section that
range from 6 to 25 µm (n = 15). Per cent skew of 17,776 is 31.2%.
Specimen 17,773 has tracheid diameters in tangential section that
range from 12 to 40 µm (n = 25) and tracheid diameters in radial
section that range from 12 to 42 µm (n = 23). Per cent skew for
17,773 is 23% (Fig. 6). Specimen 17,774 has tracheid diameters in
tangential section that range from 8 to 44 µm (n = 23) and tracheid
diameters in radial section that range from 12 to 38 µm (n = 23). Per
cent skew for 17,774 is 33.7%. Specimen 17,775 has tracheid
500
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rings were sampled per specimen. Differences in δ13C values
among the study localities are marked, and δ13C value patterns
expressed within tree rings vary between some specimens. Our
geochemical inferences of leaf habit are based on recognition of
δ13C value patterns within tree rings (Fig. 3). The criteria for the
recognition of these patterns are listed in Table 2.
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Fig. 6. Tracheid cell diameters versus cell number across single rings
from three representative specimens. Vertical lines indicate the apex
(dashed line) of the CSDM curve and centre (continuous line) of the
CSDM curve. The difference and location of the apex versus the centre
of the CSDM curve can be used as a proxy for leaf habit (Falcon-Lang
2000). (a) CSDM for specimen 17,771, (b) CSDM for specimen 17,169;
(c) CSDM for specimen 17,774.
diameters that range from 5 to 31 µm and a per cent skew of 24.8%.
The CSDM results suggest an evergreen leaf habit interpretation
for all of the Wahl Glacier specimens.
Only one specimen from Graphite Peak was analysed. Specimen
17,771 has tracheid diameters in tangential section that range from
5 to 37 µm with a per cent skew of 15% (Fig. 6). We interpret these
CSDM results as indicating that 17,771 had an evergreen habit.
Stable isotope geochemistry
Palaeoecology and leaf longevity in this study are partly based on
stable carbon isotope ratios measured from 339 microsamples of 39
growth rings from eight wood specimens. Microsamples were
taken from intervals of tree rings that display AS values higher than
0.3 (Fig. 5), fluctuating AS values or, in the case of specimen
11,617B, low AS values owing to the practical necessity of sampling rings with well-defined ring boundaries. Average δ13C values
for the wood specimens range from −25.5‰ to −22.1‰ (Table 2),
5–10 microsamples were collected per tree ring, and 3–8 growth
Mt. Achernar. Sample 17,169 has an average δ13C value of −22.2‰
(±0.1‰) and a mean δ13C value difference of 0.3‰ (±0.1‰, n = 4),
measured from the most negative and most positive δ13C value
within a tree ring averaged over n rings (Fig. 7). Sample 11,472A
has an average δ13C value of −22.1‰ (±0.3‰) and a mean δ13C
value difference of 0.7‰ (±0.3‰, n = 3). Sample 11,617B has an
average δ13C value of −23.2‰ (±0.3‰) and a mean δ13C value difference of 0.6‰ (±0.1‰, n = 4). The studied specimens from Mt.
Achernar display a predominantly symmetrical δ13C value pattern
with peak values near the middle of most tree rings (Table 2; Fig.
7). This symmetrical pattern with well-defined δ13C peak occurs for
nine out of 12 tree rings studied from the Mt Achernar specimens.
In contrast, one ring in specimen 17,169 displays a relatively uniform δ13C value with a single prominent negative excursion. The
third ring in 11,472A displays a progressive increase in δ13C value
throughout the ring in the direction of growth and a sharp decrease
in δ13C value at the ring boundary (Fig. 7b). The fourth ring in
11,617B displays no clear pattern.
Interpretation. The prominent peak in δ13C patterns near the middle of the rings in specimens 17,169 and 11,472A and roughly equivalent δ13C values at the ring boundaries lead us to interpret these
specimens as representing trees with an evergreen leaf habit (Fig. 7).
Specimen 11,617B displays highly varied δ13C values within each of
the studied growth rings, leading to a difficult interpretation of leaf
habit from this specimen (Fig. 7). This δ13C variation may be related
to the fact that the studied specimens have AS values <0.3 for the
sampled tree-ring interval, and therefore may represent a complacent
growth interval (Fig. 5), resulting in low sensitivity to the limiting
factors for growth (Fritts 1976; Phipps 1982; Orwig & Abrams 1997;
Abrams et al. 1998; Carrer & Urbinati 2006). In contrast, growth
rings from specimens 17,169 and 11,472A were sampled from intervals where growth was probably stressed, as interpreted by annual
sensitivity values >0.3 and large variations in annual sensitivity (Fig.
5). For rings with annual sensitivity >0.3 it is likely that the limiting
factors for growth exceeded the capacity for wood growth, resulting
in greater sensitivity to a given limiting factor (Fritts 1976), and in
such cases leaf habit and environmental effects on the δ13C values of
wood may be better expressed.
Wahl Glacier. Sample 17,773 has an average δ13C value of
−22.7‰ (±0.2‰) and a mean δ13C value difference of 0.6‰
(±0.3‰, n = 5). Sample 17,774 has an average δ13C value of
−22.9‰ (±0.2‰) and a mean δ13C value difference of 0.5‰
(±0.2‰, n = 4). Sample 17,775 has an average δ13C value of
−23.2‰ (±0.3‰) and a mean δ13C value difference of 0.6‰
(±0.4‰, n = 5). Specimen 17,776 is not represented by stable carbon isotope data owing to weight per cent carbon values <1%,
which do not permit accurate and precise isotope ratio measurements. Two of three specimens from Wahl Glacier (17,773;
17,774) display a predominantly symmetrical intra-ring δ13C pattern (Table 2; Fig. 8). In contrast, ring 1 from 17,773 displays a
sharp decrease in δ13C value at the beginning of the ring, a sharp
increase in δ13C value that remains uniform for 30% of the ring
thickness and a sharp decrease in δ13C value near the earlywood–
latewood boundary (Fig. 8a). Rings 3 and 4 from specimen 17,774
display a secondary peak that is 30–40% of the magnitude of the
prominent peak (Fig. 8b). The δ13C value pattern for growth rings
Leaf Habit of Glossopterid Forests
501
Table 2. Criteria for inferring leaf habit from tree ring δ13C values
Peak shape δ13C increase δ13C peak δ13C decrease, δ13C Peak near Similar δ13C Interpretation
through ring following ring or plateau into middle of ring? value at ring
boundary?
boundary?
latewood?
boundaries?
Specimen
17,169
Symmetrical
No
No
No
Yes
Yes
11,472A
Symmetrical
No
No
No
Yes
Yes
11,617B
Symmetrical
No
No
No
Yes
Yes
17,774
Symmetrical
No
No
No
Yes
Yes
17,775
Symmetrical
No
No
No
Yes
Yes
17,776
Asymmetrical
Yes
Yes
Yes
No
No
17,772
Symmetrical
No
No
No
Yes
Yes
17,771
Asymmetrical
Yes
Yes
Yes
No
No
in specimen 17,775 displays three distinct components (Table 2):
(1) a sharp increase in δ13C value across a ring boundary; (2) a
maximum δ13C value in the earlywood; (3) a gradual decline in
δ13C values into the latewood.
Interpretation. We interpret specimens 17,773 and 17,774 as
having an evergreen habit, because of the nearly symmetrical variations in δ13C within the tree rings (Fig. 8). Specimen 17,775 displays a three-component δ13C pattern in each of the four studied
rings, which we interpret as being consistent with a deciduous habit
(Table 2).
Graphite Peak. Specimen 17,771 has an average δ13C value of
−25.5‰ (±0.6‰) and a mean δ13C value difference of 1.7‰
(±1.2‰, n = 6). Sample 17,772 has an average δ13C value of
−24.5‰ (±0.7‰) and a mean δ13C value difference of 2.0‰
(±0.9‰, n = 5). Intra-ring patterns for Graphite Peak specimens
are summarized in Table 2. Ring 3 of 17,771 displays a pronounced decrease in δ13C values at the beginning of the ring followed by a sharp increase in δ13C value; the δ13C value pattern
continues for the remainder of this ring in a similar fashion to the
other rings (Fig. 9a). Patterns in δ13C values for growth rings in
specimen 17,772 display three components: (1) an increase in
δ13C value across ring boundaries; (2) a peak δ13C value in the
earlywood; (3) a decline in δ13C value into the latewood (Fig. 9b).
Interpretation. Specimen 17,771 displays a nearly symmetrical
δ13C pattern within the growth rings that we interpret as reflecting
an evergreen leaf habit. Ring 3 in 17,771 may have been affected by
enhanced precipitation early in the growing season (Fig. 9a),
because similar isotope excursions are observed in extant evergreen
gymnosperms in conjunction with high rainfall events (Livingston
& Spittlehouse 1996; Walcroft et al. 1997). In contrast, we interpret
a deciduous leaf habit for specimen 17,772 because of the wellexpressed asymmetric δ13C pattern in each of the three rings, and the
increase in δ13C values across each of the four ring boundaries.
Discussion
We use a multipronged approach to determine the leaf habit of
glossopterids and to assess the ecological significance of leaf
Notes
Evergreen Ring 4 displays sharp 0.3‰ decrease
in earlywood
Evergreen Ring 3 displays progressive δ13C
increase, but 0.3‰ decrease into
latewood
Evergreen Highly variable δ13C values within
each ring, but peak δ13C values occur
near middle of rings
Evergreen Progressive δ13C increase from ring
1 to ring 5
Evergreen Rings 3 and 4 display secondary δ13C
increase c. 30–40% of the initial δ13C
increase
Deciduous Ring 2 displays similar δ13C values
at ring boundaries, but other rings
do not
Evergreen Prominent negative δ13C excursion in
earlywood of ring 3
Deciduous δ13C plateau into latewood of ring 2
longevity in polar environments during the Late Permian. We
inferred leaf longevity from (1) skewedness of the EW–LW
boundary on the CSDM of cell widths within tree rings (Fig. 6;
Falcon-Lang 2000; Falcon-Lang & Cantrill 2001) and (2) the
stable carbon isotope signature within multiple tree rings from a
given specimen (Figs 7–9; Table 2). Growth characteristics of
the wood are inferred from ring width measurements (Fig. 5;
Table 1) and compared with the results of the stable isotope data
to assess whether the principle of limiting factors can affect geochemical interpretations of leaf longevity. To understand the
ecological significance of these results we examine the distribution of the leaf habit in the context of the forest structure on a
Late Permian palaeolandscape, and in the broader context of
Late Permian Glossopteris floras in Antarctica.
Interpretation of leaf habit
The results of CSDM analysis and δ13C pattern recognition agree
for six of the seven fossil wood specimens that had both methods
applied (Table 2), with an evergreen habit interpreted for all of the
Mt. Achernar specimens, two of the Wahl Glacier specimens, and
one Graphite Peak specimen. Stable isotope data suggest a deciduous habit for two specimens, one at Wahl Glacier and another at
Graphite Peak. Rings with relatively uniform δ13C trends, highly
varied δ13C values, and progressive increases in δ13C values are
uninformative for leaf habit determinations, and these patterns
occur in seven out of the 35 rings studied (Figs 7–9).
CSDM results and δ13C patterns suggest an evergreen habit for
two specimens from Wahl Glacier, 17,774 and 17,775 (Figs 6b and
8). In contrast, δ13C patterns for 17,776 suggest a deciduous habit,
whereas CSDM analysis for 17,776 resulted in a positive per cent
skew, which indicates an evergreen habit. The discrepancy between
the isotopic inference of leaf longevity and the CSDM approach
could be based on the following reasons: (1) inaccuracy of the
CSDM method based on overestimation of latewood and thus erroneous conclusions on leaf longevity; (2) microsampling of distorted or deformed wood growth increment; or (3) diagenetic
alteration of the sample material. The CSDM proxy relies heavily
on assuming a consistent growth pattern within studied tree rings,
502
E. L. Gulbranson et al.
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Fig. 7. Stable carbon isotope results for Mt. Achernar wood specimens: (a)
specimen 17,169; (b) specimen 11,617B; (c) specimen 11,472A (MA-3).
Data points reflect single microsamples collected along the direction of
growth; ring boundaries are indicated by vertical dotted lines.
thus only those rings that do not exhibit features such as ‘false
rings’ can be used. Wood growth, however, is non-linear and intraannual variations in environmental conditions and auxin synthesis
(e.g. drought, day length) can affect terminal elongation, which
will affect the diameters and wall thicknesses of tracheid cells
(Larson 1960). The day length effect is especially pronounced in
the experiments of Larson (1960), and this would be expected to be
a dominant signal in the studied specimens as rapid changes in day
length occur in the weeks-long transition from summer to winter at
polar latitudes (Llorens et al. 2009). As an example, tracheid cell
diameter gradually decreases throughout growth rings in similar
Late Permian wood specimens from Skaar Ridge as a result of
decreasing cell lumen diameter, as opposed to increasing cell wall
thickness (Taylor & Ryberg 2007). Thus, the nuances of the growth
characteristics of these fossil wood specimens are masked by the
CSDM approach, which considers only cell diameter, which would
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Fig. 8. Stable carbon isotope results for Wahl Glacier wood specimens:
(a) specimen 17,774; (b) specimen 17,775; (c) specimen 17,776. Data
points reflect single microsamples collected along the direction of
growth; ring boundaries are indicated by vertical dotted lines.
estimate more latewood (by a factor of about four) than is evident
from petrographic analysis and the formulae of Denne (1989).
Because CSDM was initially created to determine earlywood–latewood boundaries (Creber & Chaloner 1984), the potential for inaccuracy of this method in establishing fundamental plant
physiological traits would be expected to carry over in the use of
CSDM to provide leaf longevity determinations. Accurate results
of CSDM analysis applied to extant wood (Falcon-Lang & Cantrill
2001), however, suggest that there is probably a signal of leaf longevity expressed by this proxy, but the application of this proxy to
fossil specimens should be aided by the use of independent determinations of leaf longevity until more refinements are made to the
Leaf Habit of Glossopterid Forests
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Fig. 9. Stable carbon isotope results for Graphite Peak wood specimens:
(a) specimen 17,771; (b) specimen 17,772. Data points reflect single
microsamples collected along the direction of growth; ring boundaries
are indicated by vertical dotted lines.
CSDM approach that provide accurate determinations of earlywood–latewood boundaries. The microsamples used for stable isotope analysis reflect an average over c. 100–500 µm sample
thicknesses, which correspond to c. 10–50 tracheid cells, thus wood
distortion might be less well expressed in the isotopic data.
Therefore, with wood distortion it is likely that each microsample
contains a wood component from the previous microsampled interval in addition to a second component from the following microsampled interval. This interpretation is consistent with the intra-ring
δ13C pattern, which shows little scatter in δ13C values and a welldefined trend that is consistent with δ13C trends observed in extant
wood. Diagenetic alteration of the sample is not suspected for this
discrepancy because of (1) the lack of carbon-bearing secondary
minerals that are known to be produced through decarboxylation of
wood in a burial environment (e.g. calcite, goethite), (2) the repeating δ13C pattern that displays little scatter, and (3) δ13C values that
fall within the range of C3 vegetation.
Taylor & Ryberg (2007) applied the CSDM proxy to Late
Permian glossopterid fossil wood specimens from Antarctica and
found a predominance of positive per cent skew values for the studied samples, indicating that the majority of the specimens studied
26
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Fig. 10. Mean δ13C values for wood samples versus reconstruction of
the fossil forests. (a) Means and standard deviations for δ13C values for
wood specimens from Graphite Peak, Wahl Glacier, and Mt. Achernar
versus the log10 of tree density estimated for each fossil forest; n, number
of data points used. Despite the overlap, Mt. Achernar and Wahl Glacier
mean δ13C values are significantly different based on an F-statistic of
29.836 (P < 0.0001) with a DF of 218. (b) Basal area of wood (solid
line) and tree height (dotted line) versus log10 tree density for each fossil
forest.
were evergreen. This conclusion, however, was rejected on the basis
that the sedimentological evidence for deciduousness provided by
leaf mats (Plumstead 1958; Retallack 1980) was stronger than the
inferences from the CSDM proxy. The new carbon isotope technique for interpreting leaf habit of fossil plants presented here suggests that the general result of the CSDM analysis presented by
Taylor & Ryberg (2007), that evergreen trees dominated Late
Permian polar forests in Antarctica, was probably accurate to some
degree. Moreover, the specimens studied by Taylor & Ryberg (2007)
were collected from the Skaar Ridge locality, which has a similar
lacustrine or distal floodplain facies association to the fossil forest
site at Mt. Achernar (Fig. 2). Therefore, the application of two independent leaf habit proxies to fossil wood associated with the
Glossopteris flora indicates that this flora was composed of both
deciduous and evergreen varieties, as opposed to the long-held
assumption of a deciduous habit for this flora. Additionally, both
evergreen and deciduous trees occupied the same forests on some
landscapes in the palaeo-polar environment.
The potential for both leaf habit end-members to have existed
within glossopterids is valid for two reasons: (1) congeneric deciduous and evergreen habits occur in extant floras (e.g. Quercus); (2)
the Glossopteris plant is notoriously complex, covering a wide geographical and latitudinal range (Rigby 1972; Meyen 1987; Cúneo
504
E. L. Gulbranson et al.
1996; McLoughlin & Drinnan 1996; McLoughlin 2001; Pigg &
Nishida 2006; Nishida et al. 2007; Ryberg 2009; McLoughlin
2012) with numerous morphospecies among different organs (e.g.
leaves, megasporophylls) attributed to the glossopterids, yet only
three examples of anatomical attachment (plants bearing the leaf
types Glossopteris schopfii, G. skaarensis, and G. homevalensis).
Therefore, no single plant can be classified as the Glossopteris
plant, rather the organs assigned to the glossopterids probably originate from a multitude of different plants that bore leaves with a
similar type of venation and morphology.
Ecological variation on a palaeolandscape
We observe that δ13C values of the whole wood at each of the study
localities display important differences: (1) the mean δ13C values of
fossil wood are significantly different for each fossil forest site (Fig.
10; one-way ANOVA, P0.05 < 0.0001); (2) differences in the magnitudes of intra-ring δ13C variation are significant between the distal
floodplain and channel-proximal facies (Mt. Achernar, Graphite
Peak, P0.05 < 0.00066). In contrast, differences in the magnitude of
intra-ring change in δ13C are not significant between Mt. Achernar
and Wahl Glacier specimens, P0.05 < 0.672. Moreover, there is a
trend towards increasingly positive δ13C values in the fossil wood
from Graphite Peak to Wahl Glacier and from Wahl Glacier to Mt.
Achernar (Fig. 10a). These isotopic differences possibly reflect different ecological habitats of glossopterids on this Late Permian palaeolandscape or they may reflect different ages of the studied forests
(Taylor et al. 1992). Carbon isotope variations on modern landscapes exhibit trends towards increasingly smaller Δ13C values (the
difference between δ13C values of atmospheric CO2 and plant tissue) as plant water-use efficiency (WUE) increases (Ehleringer &
Cooper 1988), where plants with high WUE tend to occur in drier
sites (Ehleringer 1993a; Stewart et al. 1995). Low Δ13C values
occur in evergreen plants relative to low WUE deciduous plants
(Kloeppel et al. 1998), or in sites where competition is high
(Ehleringer 1993b). For the following discussion we model ∆13C for
these Late Permian fossil forests using the method of Lloyd &
Farquhar (1994). Where the δ13C value of atmospheric CO2 is estimated from equilibrium calculations against marine carbonate from
the surface ocean, temperature is inferred from palaeoclimate
simulations and a modern analogue site, seasonal change in Ci/Ca
(where Ci is the intercellular concentration of CO2 and Ca is the
atmospheric concentration of CO2) is referenced against modern
evergreen trees in cold or cool climates (Lloyd & Farquhar 1994),
and modern seasonal variations in CO2 over a 4 month growing season are incorporated to model ∆13C for the fossil wood.
The most positive ∆13C values observed for the fossil forests
occur at Graphite Peak and Wahl Glacier, and coincide with our
interpretation of the occurrence of deciduous trees in these forests.
These results conform with observations that deciduous trees in the
modern boreal forest have higher Ci/Ca ratios and more negative δ13C
values than evergreen-dominated forests (Lowden & Dyck 1974;
Lloyd & Farquhar 1994). Moreover, trees with different life forms
tend to adopt an isotope signature of the dominant ecosystem constituent, such that evergreen trees in a deciduous ecosystem have
larger ∆13C than evergreen trees in a predominantly evergreen ecosystem (Brooks et al. 1997), which may explain why the fossil we
interpret as evergreen at Graphite Peak has more negative δ13C values than the fossil trees at Mt. Achernar. In contrast, what we interpret to be a predominantly evergreen fossil forest at Mt. Achernar
displays the most positive mean δ13C values of wood and smallest
∆13C values. This isotopic difference suggests that leaf habit, forest
structure, and composition (e.g. pure evergreen stand v. mixed stand)
varied in this Late Permian polar ecosystem (Fig. 10a and b). In
extant high-latitude forests ∆13C displays a similar dependence on
leaf habit, where variations in ∆13C are significant only as leaf habit
or life form (e.g. tree, shrub) vary, but ∆13C variation is not significant at the southern or northern end of the boreal forest (Brooks et al.
1997; Flanagan et al. 1997). This means that the life form composition of ecosystems has an influence on carbon isotope discrimination
at the ecosystem scale that is stronger than latitudinal variation.
It is possible that the mean carbon isotope values and forest
structure indicate that the fossil forest at Mt. Achernar was a xeric
site, as evergreen trees, in general, tend to occupy drier sites and
have leaves with lower photosynthetic rate but high WUE (Reich
et al. 1992; Givnish 2002). All palaeosols of the Late Permian polar
forests at our three localities display similar morphologies, indicating poorly drained conditions (Gulbranson et al. 2012). If the fossil
forest at Mt. Achernar represents a distinctly different moisture
regime than the forest at the Graphite Peak locality, then a difference in soil morphology might be expected; however, this is not the
case. Forest structure, however, does display pronounced differences between the three sites. Stand density decreases from Mt.
Achernar to Wahl Glacier, to Graphite Peak, whereas canopy
height increases from Mt. Achernar to Wahl Glacier, to Graphite
Peak (Fig. 10b). Therefore, canopy effects may be more strongly
represented by the carbon isotope data for these fossil forests rather
than WUE based on intrinsic-WUE and soil moisture regime
because each of the fossil forests are found in the same type of
poorly drained palaeosol, indicating a similar soil moisture regime
for each site. Moreover, whole plant WUE in a simulated polar
photoperiod is enhanced under conditions of elevated atmospheric
CO2 (Llorens et al. 2009), such as are expected to exist for these
Late Permian polar forests; therefore interpreting WUE from these
measured δ13C values is probably an oversimplification.
If canopy effects are better reflected by our isotopic and palaeoecological data, then the processes that control biomass accumulation
should be important controls on the observed trends. Two principal
factors limit the accumulation of plant biomass: stress (lowers productivity) and disturbance (destroys biomass) (Grime 1977). The dominant stresses expected for these forests are seasonal variations in
temperature (Falcon-Lang & Cantrill 2001), which can control the
length and timing of the growth season and metabolic rates, and canopy-induced light limitation, which can affect the ability of an organism to compete for the same quanta of light or nutrients. We interpret
that erosion and fire were important disturbance processes. Erosive
processes in extant boreal forests produce trends in forest structure and
composition away from the margin of rivers and onto more stable
floodplain environments (Gregory et al. 1991; He & Duncan 2000).
Comparing the sites, Graphite Peak and Wahl Glacier are proximal to
the fluvial systems whereas Mt. Achernar preserves a distal floodplain
or lake-margin setting (Cúneo et al. 1993; Gulbranson et al. 2012),
thus erosion may have had an impact on the structure and composition
of these forests. Fire probably played a significant role in the highoxygen atmosphere of the late Palaeozoic (Glasspool 2000; Wildman
et al. 2004; Uhl et al. 2008); however, we lack information on these
forests that would allow us to understand how much of an impact fire
had on controlling ecosystem dynamics. Disturbance processes are
important for creating gaps in forest canopy cover, which can be
exploited by the establishment of new taxa, such as the poleward
migration of modern temperate forest trees into the boreal forests
(Leithead et al. 2010). Given that we find differences in leaf habit
between the three fossil forests based on our new data for stable carbon
isotope patterns in fossil wood and wood anatomy, and that the structure and composition of these forests varied as a function of landscape
position (Gulbranson et al. 2012), we conclude that the inferred trends
in leaf longevity and forest structure are related to disturbance and
stress. Thus, the prevalence of evergreen trees at Mt. Achernar could
Leaf Habit of Glossopterid Forests
be related to intraspecific competition on a stable landscape, whereas
mortality and exploitation of forest gaps produced through disturbance
allowed mixed stands to develop at Graphite Peak and Wahl Glacier.
The adaptation of leaf longevity as a function of climate change during
the Late Permian, however, is not known and may provide crucial
insights into the dynamics of plant–climate interactions.
Conclusions
We applied two independent proxies to infer leaf longevity from
multiple fossil wood specimens collected from three Late Permian
fossil forests in Antarctica. Our results show that all of the fossil
wood specimens belong to the same morphogenus of wood,
Australoxylon, which has an affinity to the Glossopteris flora. The
leaf longevity proxies converge on similar results for 83% of the
specimens and suggest mixed evergreen and deciduous Glossopteris
trees in the forests of the palaeo polar latitudes during the Late
Permian. This conclusion is in contrast to the long-held assumption
that the Glossopteris plant was strictly deciduous, an assumption
primarily based on the occurrence of leaf mats containing
Glossopteris leaf fossils. The congeneric occurrence of deciduous
and evergreen trees in forests of the palaeo polar latitudes further
demonstrates that deciduous trees may not have had a general competitive advantage at polar latitudes, rather we infer the dominance
of particular leaf habits in Late Permian polar forests to be a function of plant responses to environmental stress and disturbance.
Competition might give rise to evergreen-dominated forests in relatively stable Late Permian environments and mixed stands may
occur in areas of high disturbance, where mortality may have provided more avenues for the migration of deciduous trees.
This paper was improved by the comments of two anonymous reviewers.
The research was supported by NSF, ANT-1142749 to E.L.G. and ANT0943935 to J.L.I. at the University of Wisconsin–Milwaukee, and ANT0943934 to E.L.T. and T.N.T. at the University of Kansas. AMAP (Botany
and Computational Plant Architecture) is a joint research unit associated
with CIRAD (UMR51), CNRS (UMR5120), INRA (UMR931), IRD
(R123), and Montpellier 2 University (UM27) (http://amap.cirad.fr).
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Received 25 October 2013; revised typescript accepted 4 February 2014.
Scientific editing by Philip Donoghue.