Habit and Ecology of the Petriellales, an Unusual Group of... Gondwana Author(s): Benjamin Bomfleur, Anne-Laure Decombeix, Andrew B. Schwendemann, Ignacio H.

Habit and Ecology of the Petriellales, an Unusual Group of... Gondwana Author(s): Benjamin Bomfleur, Anne-Laure Decombeix, Andrew B. Schwendemann, Ignacio H.
Habit and Ecology of the Petriellales, an Unusual Group of Seed Plants from the Triassic of
Gondwana
Author(s): Benjamin Bomfleur, Anne-Laure Decombeix, Andrew B. Schwendemann, Ignacio H.
Escapa, Edith L. Taylor, Thomas N. Taylor, Stephen McLoughlin
Source: International Journal of Plant Sciences, Vol. 175, No. 9 (November/December 2014),
pp. 1062-1075
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/10.1086/678087 .
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Int. J. Plant Sci. 175(9):1062–1075. 2014.
q 2014 by The University of Chicago. All rights reserved.
1058-5893/2014/17509-0008$15.00 DOI:10.1086/678087
HABIT AND ECOLOGY OF THE PETRIELLALES, AN UNUSUAL GROUP
OF SEED PLANTS FROM THE TRIASSIC OF GONDWANA
Benjamin Bomfleur,1,*,† Anne-Laure Decombeix,‡ Andrew B. Schwendemann,§ Ignacio H. Escapa,∥
Edith L. Taylor,† Thomas N. Taylor,† and Stephen McLoughlin*
*Department of Palaeobiology, Swedish Museum of Natural History, PO Box 50007, SE-104 05 Stockholm, Sweden; †Department of Ecology
and Evolutionary Biology and Biodiversity Institute, University of Kansas, Haworth Hall, 1200 Sunnyside Avenue, Lawrence, Kansas 66045,
USA; ‡Université Montpellier 2 and Centre National de la Recherche Scientifique, Unité Mixte de Recherche Botanique
et Bioinformatique de l’Architecture des Plantes, Montpellier F-34000, France; §Department of Biology,
Lander University, 320 Stanley Avenue, Greenwood, South Carolina 29649, USA; ∥Consejo
Nacional de Investigaciones Científicas y Técnicas–Museo Paleontológico
Egidio Feruglio, Trelew, Chubut 9100, Argentina
Editor: Michael T. Dunn
Premise of research. Well-preserved Triassic plant fossils from Antarctica yield insights into the physiology of plant growth under the seasonal light regimes of warm polar forests, a type of ecosystem without any
modern analogue. Among the many well-known Triassic plants from Antarctica is the enigmatic Petriellaea
triangulata, a dispersed seedpod structure that is considered a possible homologue of the angiosperm carpel.
However, the morphology and physiology of the plants that produced these seedpods have so far remained
largely elusive.
Methodology. Here, we describe petriellalean stems and leaves in compression and anatomical preservation that enable a detailed interpretation of the physiology and ecology of these plants.
Pivotal results. Our results indicate that the Petriellales were diminutive, evergreen, shade-adapted perennial shrubs that colonized the understory of the deciduous forest biome of polar Gondwana. This life form
is very unlike that of any other known seed-plant group of that time. By contrast, it fits remarkably well into
the “dark and disturbed” niche that some authors considered to have sheltered the rise of the flowering plants
some 100 Myr later.
Conclusions. The hitherto enigmatic Petriellales are now among the most comprehensively reconstructed
groups of extinct seed plants and emerge as promising candidates for elucidating the mysterious origin of the
angiosperms.
Keywords: Petriellales, gymnosperms, Triassic, paleoecology, polar forests, Antarctica.
Introduction
today exposed in the Transantarctic Mountains; these successions have yielded abundant compression-fossil assemblages as well as silicified peat deposits that contain plant
remains in exquisite anatomical detail. The rich and wellpreserved plant-fossil record from the Triassic of Antarctica
provides insights into the physiology of plant growth under
the strongly seasonal light regimes of a warm polar forest
biome—a type of ecosystem without any modern analogue
(Taylor and Taylor 1990; Escapa et al. 2011; Cantrill and
Poole 2012).
Among the numerous and, in many cases, well-studied
Triassic plants from Antarctica are the Petriellales—an order
of enigmatic seed plants that was established with the description of a peculiar type of dispersed seedpod structure in
the famous silicified peat deposit from Fremouw Peak, East
Antarctica (Taylor and Taylor 1987; Taylor et al. 1994).
Anatomical details led some authors to consider Petriellaea
triangulata a possible homologue of the angiosperm carpel
Since plant life conquered land in the early Paleozoic,
global climates have been generally much warmer than today,
enabling the terrestrial vegetation to spread far into polar
latitudes (Seward 1914; Spicer and Chapman 1990; Taylor
and Taylor 1990; Cantrill and Poole 2012). In the Triassic
greenhouse world, lush temperate forests covered large parts
of the high-latitude regions of the Gondwanan supercontinent
(Taylor and Taylor 1990; Escapa et al. 2011; Cantrill and
Poole 2012). Sedimentary successions of an extensive fluvial
drainage system that transected this polar forest biome are
1
Author for correspondence; e-mail: benjamin.bomfl[email protected]
Manuscript received April 2014; revised manuscript received July 2014;
electronically published October 28, 2014.
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BOMFLEUR ET AL.—HABIT AND ECOLOGY OF THE PETRIELLALES
(see Frohlich 2003; Frohlich and Chase 2007; Doyle 2008).
Compression fossils of similar cupulate structures (Kannaskoppia) and of associated pollen organs (Kannaskoppianthus)
were later found in organic connection to small stems with
attached leaves in Triassic deposits from South Africa (Anderson and Anderson 2003) and Australia (Holmes and Anderson 2005). The leaves (Rochipteris, Kannaskoppifolia) are
apetiolate, arise helically, and have a wedge-shaped, spreading, variably dissected lamina and distinctive anastomosing
venation (Anderson and Anderson 2003; Barone-Nugent
et al. 2003; Holmes and Anderson 2005). Anderson and Anderson (2003, p. 288) reconstructed the South African fossils
as the remains of small, erect plants that they tentatively interpreted as herbaceous pioneering shrublets or climbers (Anderson and Anderson 2003, p. 294).
Here, we present the first discoveries of petriellalean compression fossils from Antarctica. Information about the distinctive morphology of petriellalean stems and leaves enabled
us to identify the corresponding anatomically preserved parts
of these plants in the silicified peat deposit. Detailed analysis
of morphological, anatomical, and taphonomic features of
these new Antarctic fossils reveals that the Petriellales had
indeed established a habit and life strategy that are unique
among all known seed-plant groups of the time and much
more reminiscent of early angiosperms.
Material and Methods
In the Paleobotanical Collections of the Department of Ecology and Evolutionary History and Biodiversity Institute at the
University of Kansas, Lawrence (KUPB), petriellalean fossils
occur in three plant-fossil assemblages from different sites in
the Transantarctic Mountains (fig. 1). More or less complete
remains of more than 20 leaves plus abundant leaf fragments
occur on 10 hand specimens (KUPB T-234, 256, 257, 577,
581, 584, 585, 634, 661, 663) in a compression assemblage
from plant level 2 (in E. L. Taylor et al. 1990; Boucher et al.
1995; AH08 of Gabites 1985) near the base of member C of
the Lashly Formation, exposed at the Feather Bay section in
the northeastern arm of the Allan Hills, southern Victoria
Land (fig. 1). Palynological data indicate a Carnian (early Late
Triassic) age for this deposit (Kyle 1977). The second plantcompression assemblage, containing isolated leaf fragments on
11 hand specimens (KUPB T-1010, 1130, 1250, 1262, 1273,
1311, 1315, 1424, 1429; 5632, 5635), is the level 2 assemblage from a section of the upper Fremouw or the lower Falla
Formation exposed on an unnamed ridge near Schroeder Hill
in the Cumulus Hills in the Shackleton Glacier area; the locality is informally referred to as Alfie’s Elbow (Taylor et al.
1998). In the KUPB collection, specimens collected during the
1996 field season are labeled with “level 1 base” or “level 1b,”
whereas those collected during the 2003 field season are labeled “level 2,” according to the revised and published stratigraphic column (Taylor et al. 1998; Axsmith et al. 2000). A
preliminary palynological analysis (sample AE-12 of Askin and
Cully 1998) also indicates a Carnian age for these deposits.
Anatomically preserved petriellalean stems, leaves, cupulate
organs, and seeds occur in several blocks (including KUPB
specimens 10,023 [holotype material of Petriellaea triangulata], 10,852 [paratype material of P. triangulata], 17,082,
1063
and CB545) of the famous permineralized peat deposit from
the uppermost Fremouw Formation exposed at a col on the
north side of Fremouw Peak in the Beardmore Glacier area
of the central Transantarctic Mountains (fig. 1). The exact
age of this deposit remains uncertain. Following a palynological analysis by Farabee et al. (1990), the permineralized
peat deposit has conventionally been assigned to the Anisian
(early Middle Triassic). This dating was based on the assumption that the occurrence of Aratrisporites parvispinosus and an undetermined species of Protohaploxypinus (i.e.,
Protohaploxypinus cf. microcorpus) in a palynological sample from the permineralized peat would indicate an age no
younger than Anisian (early Middle Triassic). However, A.
parvispinosus and Protohaploxypinus species also occur in
younger deposits (e.g., Helby et al. 1987). By contrast, other
palynological studies (Fasola 1974; Kyle and Schopf 1982)
place the uppermost part of the Fremouw Formation, which
includes the silicified peat deposits, into subzone C of the
informal Alisporites zone (Kyle 1977), indicating a late Ladinian (latest Middle Triassic) or possibly Carnian (early Late
Triassic) age. We consider this latter assignment to be more
likely.
All material is housed in the Paleobotanical Collections of
the University of Kansas in Lawrence. Permineralized peat
blocks were prepared, analyzed, and photographed following
standard paleobotanical procedures (see, e.g., Galtier and
Phillips 1999).
Systematic Description
Order—Petriellales Taylor et al. 1994
Family—Petriellaceae Taylor et al. 1994
Genus—Rochipteris Herbst et al. 2001, emend. nov.
Type species. Rochipteris lacerata (Arber) Herbst et al.
2001.
Synonym. Kannaskoppifolia Anderson et Anderson 2003.
Emended diagnosis. Apetiolate leaves, obovate to wedgeshaped in outline; distal margin entire, undulate, or variably
incising to deeply dividing the leaf into narrow, wedge-shaped
to linear segments; lateral margins entire; venation spreading
from base, without midvein, generally subparallel to leaf or
segment margins, with acute-angled dichotomies and anastomoses forming a loose network of elongate, rhombic to
polygonal areoles.
Remarks. The original diagnosis of Rochipteris is restricted to isolated leaves only and further contained the
statement “Fructifications unknown” (Herbst et al. 2001,
pp. 261–262). Approximately at the same time that Rochipteris was erected, however, Anderson and Anderson (2003)
introduced the name Kannaskoppifolia for essentially similar
leaves that were found attached to stems (Anderson and Anderson 2003); the authors added a brief comment during the
final preparation of their monograph, indicating that Kannaskoppifolia should likely be considered a junior synonym of
Rochipteris (Anderson and Anderson 2003, p. 294). Holmes
and Anderson (2005) later proposed to use the name Kannaskoppifolia for attached leaves and Rochipteris for isolated
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1064
INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 1 Geographic and stratigraphic occurrences of the fossils. A, Feather Bay, Allan Hills. B, Fremouw Peak. C, Alfie’s Elbow. A and C
modified from Bomfleur et al. (2014a); B modified from Taylor et al. (1998).
leaves. This practice would make it necessary to assign different genus names to the attached and detached leaves of
the single individual plant from Allan Hills (fig. 2A). We thus
object to this proposal, consider Kannaskoppifolia a junior
synonym of Rochipteris, and modify the emended diagnosis
to allow inclusion of attached leaves also. Furthermore, in
light of the strong similarities between compressed and structurally preserved organs, we propose treating the family name
Kannaskoppiaceae Anderson et Anderson (originally based
on compression fossils) as a junior synonym of the family
Petriellaceae (Taylor et al. 1994).
Species—Rochipteris alexandriana Herbst et al. 2001
Description. The most complete compression specimen
consists of a 6-cm-long, up to 1.5-mm-wide, slender, curving
stem that is divided into smooth, ∼10–15-mm-long internodal
regions and ∼5–10-mm-long nodal regions with loose clusters
of helically arranged leaves (fig. 2A), each arising at an acute
angle from a short (∼1-mm-long), apically inclined, coneshaped, cushion-like protrusion of the cortex (fig. 2B, 2C). Individual leaves are apetiolate, wedge-shaped, up to 8 cm long,
and up to 3 cm wide; they are basally divided into three main
segments by two closely spaced dichotomies at a distance of
∼15 mm from the base, each segment being further dissected
by 2–3 successive acute-angled dichotomies (figs. 2A–2C, 3A,
3B); the resulting lamina segments are only 0.5–2 mm wide,
linear to narrowly wedge shaped, with entire, slightly recurved margins (i.e., adaxially convex surface; fig. 3A). The
apices of ultimate segments are truncate. The venation is fine,
spreading, generally straight and parallel to lamina margins,
and dichotomizing sporadically at acute angles when approaching lamina dichotomies (fig. 2B). Characteristic reticulate patterns occur sparsely in distal leaf portions; these
consist of a group of either a single or two parallel vein dichotomies (g forms), followed by a l-type or x-type anastomosis (see Melville 1976; fig. 3A–C). The vein number per
lamina segment ranges from up to six in basal leaf portions to
two or one in ultimate segments. The abaxial epidermal surface bears sparse dome-shaped protrusions of ∼50–150 mm
in diameter (fig. 3C). Additional specimens from Allan Hills
consist of isolated leaf fragments; some of these have conspicuously recurved margins, similar to petriellalean leaves
from South Africa (Anderson and Anderson 2003) and Australia (Holmes and Anderson 2005).
Remarks. The specimens correspond very well with the
diagnosis of R. alexandriana from the Triassic of Chile
(Herbst et al. 2001).
Species—Rochipteris sp. cf. R. lacerata (Arber)
Herbst et al. 2001
Description. The material consists of up to 4-cm-long
and 1.5-cm-wide fragments of spreading, presumably wedge-
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Fig. 2 Petriellalean stem with attached Rochipteris alexandriana leaves from the Upper Triassic part of the Fremouw Formation at Allan
Hills, south Victoria Land, Antarctica; KUPB specimen T11-661. A, Overview of the specimen. B, Detail showing cortical cushions (arrows). C,
Drawing of specimen with attached leaves illustrated on A. Scale bars p 1 cm in A; 5 mm in B.
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Fig. 3 Petriellalean compression fossils from the Triassic of Antarctica. A–C, Details of Rochipteris alexandriana leaves from the Upper
Triassic of the Allan Hills showing two vein dichotomies (g forms) followed by a x-type anastomosis (A), two vein dichotomies (g forms)
followed by a l-type anastomosis (B), and dome-shaped protrusions on the epidermal surface (C). All details from KUPB specimen T11-661b.
D–F, Fragments of Rochipteris sp. cf. R. lacerata from the Falla Formation of the central Transantarctic Mountains, showing abundant epidermal glands and characteristic anastomosing venation, including x-type and z-type anastomoses; D, T1424; E, T1273; F, T1262. Scale bars p
500 mm in A, C; 250 mm in B; 5 mm in D; 2 mm in E, F.
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BOMFLEUR ET AL.—HABIT AND ECOLOGY OF THE PETRIELLALES
shaped leaves, incised to varying depths up to at least two
times (fig. 3E, 3F). Veins are fine, spreading more or less
parallel to the leaf or segment margins, and have acute-angled
dichotomies (g forms), common x-type anastomoses, and
sparse z-type anastomoses (fig. 3D–3F); the vein density is
∼15–20 per 10 mm. The lamina appears membranous (i.e.,
conspicuously brownish and lighter-colored than other cooccurring gymnosperm foliage fossils), and intercostal fields
bear densely distributed dark spots ∼100–200 mm in diameter
(fig. 3E).
Remarks. In leaf dimensions, degree of leaf dissection,
and venation details, the specimens are most similar to the
type species R. lacerata (see Herbst et al. 2001). Due to the
rather strong fragmentation of the material, however, we refrain from attempting a formal identification.
Genus—Rudixylon gen. nov.
Generic diagnosis. Stems small, perennial, cylindrical, eustelic, pycnoxylic; pith large, parenchymatous; primary xylem
with helical to scalariform wall thickenings, not arranged in
distinct sympodia; secondary xylem cylinder with uniseriate
rays. Leaves helically arranged; leaf trace with a single, wide,
flattened, adaxially concave vascular bundle passing through
a prominent cortical cushion.
Etymology. The genus name refers to the small size and
slender habit of the stems (lat. rūdis p small stick; gr. xylon p
wood).
Type Species—Rudixylon serbetianum sp. nov.
Diagnosis. Stems small, up to ∼3 mm in diameter, perennial, erect, cylindrical, eustelic, pycnoxylic; pith large in
relation to entire stem diameter, up to ∼1.5 mm in diameter,
parenchymatous, overall homogeneous, in some cases containing cuboidal storage cells distributed at regular vertical
intervals; secondary xylem cylinder with uniseriate, parenchymatous rays up to at least 25 cells high; radial pitting of
secondary xylem tracheids, with one or two rows of circularbordered pits. Leaves helically arranged, persistent. Adventitious roots containing a thin aerenchyma cylinder.
Holotype (hic designatus). Stem with attached leaf base,
cross-sectioned on master peel Ctop, and prepared on slides
Ctop#01–03 of peat-block specimen 10,852, housed in the
Paleobotanical Collections of the Department of Ecology and
Evolutionary History and Biodiversity Institute at the University of Kansas, Lawrence.
Etymology. The specific epithet is chosen in honor of
Rudolph “Rudy” Serbet, collections manager at the University of Kansas Paleobotanical Collections, who first recognized and prepared many of the structurally preserved plants
described from the Antarctic silicified peat deposits over the
past decade.
Type locality. Unnamed col on the north side of Fremouw
Peak, Beardmore Glacier area, central Transantarctic Mountains.
Type stratum. Blocks of silicified peat in the uppermost
part of member C of the Fremouw Formation, Beacon Supergroup.
Age. Middle or early Late Triassic.
1067
Description. Stems and leaves occur in great abundance
together with isolated cupules and seeds in certain peat blocks,
including those that contain the type material of Petriellaea
triangulata). Stems are diminutive and measure only 1–3 mm
in diameter (fig. 4); they have a ∼0.5–1.5-mm-wide parenchymatous pith (fig. 4A, 4B, 4F, 4J) and a small amount of
pycnoxylic secondary xylem with up to at least four more
or less conspicuous growth rings (fig. 4A, 4F). Stems with
preserved bark tissues show a thin parenchymatous cortex
(fig. 4C, 4J). Secondary phloem consists of a few poorly preserved cell layers. The pith parenchyma is overall homogeneous but contains small, cuboidal cells with dark contents
that occur at regular vertical intervals (fig. 4D). The primary
xylem does not form distinct sympodia (fig. 4B, 4J). Primary
xylem tracheids have spiral to scalariform wall thickenings.
The secondary xylem consists of tracheids and parenchymatous rays that are uniseriate and up to at least 25 cells in
height (fig. 4E). Radial pitting of the tracheid walls consists
of one or two rows of circular bordered pits (fig. 4G). Leaf
vascular traces arise steeply in the form of a single, flattened,
crescentic xylem bundle that passes through a prominent cortical cushion and extends into the leaf base (fig. 4J).
Basal leaf cross sections are crescentic and contain a single,
flattened, adaxially concave dorsiventral xylem bundle essentially similar to the leaf traces in the cortical cushions
of the foliated stem portions (fig. 4K). A series of sections
through a basal leaf portion show that this bundle then flattens and becomes dissected several times to form an even set
of more or less parallel leaf veins (fig. 4M). In addition, we
found one basal portion of a leaf segment in which a pair of
veins forms a x-type anastomosis (fig. 5). Distal leaf portions
are extremely thin, some being only four cell layers high and
less than 150 mm thick (fig. 4N); their mesophyll is loosely
arranged, contains large intercellular air spaces, and lacks
palisade parenchyma. In all leaf portions, the lower epidermis
bears prominent glands that produce raised, dome-shaped
storage bodies ∼50–100 mm in diameter (fig. 4L).
Comparison and remarks. In addition to the distinctive
vascularization and anatomy of affiliated leaves, the anatomically preserved stems of the Petriellales can be readily
distinguished from those of the two co-occurring gymnosperm stem taxa with pycnoxylic wood, i.e., the corystosperm Kykloxylon and the conifer Notophytum. The most
distinctive characters for petriellalean stems are (1) the absence of the lacunae and sclerotic nests that are present in
the pith and cortex of all Kykloxylon axes, including shoot
apices (Meyer-Berthaud et al. 1993) and (2) the lack of the
distinctive primary xylem sympodia seen in Notophytum
(Meyer-Berthaud and Taylor 1991). In addition, even 4-yrold petriellalean stems have an exceptionally small diameter
of less than 3 mm, whereas the smallest stems known for
Notophytum and Kykloxylon (i.e., apices of 1-yr-old shoots)
measure 5 and 4 mm in diameter, respectively (Meyer-Berthaud
and Taylor 1991; Meyer-Berthaud et al. 1993). In those
young shoots of Kykloxylon and Notophytum, leaf traces
are crowded, with a very short internode, and several leaf
traces can be observed on a single transverse section (MeyerBerthaud and Taylor 1991; Meyer-Berthaud et al. 1993). This
is not the case in the petriellalean stems, which have a higher
internode length.
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Fig. 4 Anatomically preserved petriellalean stems (Rudixylon serbetianum, gen. et sp. nov.) and leaves from Triassic permineralized peat
from Antarctica. A, Cross section through large stem showing prominent parenchymatous pith and three indistinct growth rings; KUPB slide
17,082 Ctop#30. B, Cross section through young stem with particularly large pith; KUPB slide CB545A (B1-d). C, Cross section of small branch
with well-preserved cortex; KUPB slide 17,082 Dtop#20. D, Radial section through stem showing cuboidal storage cells in pith parenchyma;
KUPB slide 19,392. E, Detail of tangential section through stem showing high, uniseriate rays; KUPB slide 19,342. F, Cross section through a
large stem with multiple branching; KUPB peel 17,082 Atop. G, Detail of radial section through stem showing one or two rows of circularbordered pits; KUPB slide 17,082 Aside#4. H, I, Stem cross section showing emerging adventitious root with aerenchyma cylinder; KUPB peel
17,082 Dbot#1 (H) and KUPB slide 17,082 Dbot#26 (I). J, Holotype specimen showing stem cross section just below a leaf base, with prominent
cortical cushion containing crescentic leaf-trace bundle; KUPB 10,852 Ctop#02. K, Cross section through adaxially concave basal leaf portion
containing crescentic dorsiventral bundle similar to the leaf-trace bundle of the holotype specimen (see A); KUPB slide 10,023 A#109. L, Detail
of leaf cross section showing gland in lower epidermis; KUPB slide 10,023 Aa#14. M, Leaf cross section showing evenly distributed veins; KUPB
slide 10,023 A#77. N, Cross section through thin distal leaf portion; KUPB slide 19,351. Scale bars p 500 mm in A; 250 mm in B–D, I–K, M;
25 mm in E, G; 1 mm in F, H; 50 mm in L; 100 mm in N.
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BOMFLEUR ET AL.—HABIT AND ECOLOGY OF THE PETRIELLALES
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Habit Reconstruction
Fig. 5 Successive cross sections through a basal portion of a permineralized petriellalean leaf segment showing x-type anastomosis
of vascular bundles (in C); KUPB slides 10,023 A#119 (A), 10,023
A#109 (B), 10,023 A#077 (C), and 10,023 A#58 (D). Scale bars p
200 mm.
A critical character in the diagnoses is the small size of the
stems. It might be argued that all petriellalean fossils found
so far represent young individuals of tall, arborescent plants
similar to other gymnosperm taxa and that upright-buried
fossils are saplings. However, this can be ruled out for the
following reasons: first, given the amount of material available, one would expect to find larger petriellalean stems as
well, especially given that the plants apparently grew within
the depositional environment; second, one would then expect
to also find young plants of other local arborescent taxa (e.g.,
the much more common Dicroidium and Telemachus trees),
which is not the case; and finally, petriellalean fossils are
commonly found together with copious amounts of either
male or female reproductive organs from presumably the
same individuals (see, e.g., Anderson and Anderson 2003),
indicating that the fossils represent mature plants.
Discussion
The morphology, anatomy, and taphonomic context of
the new Antarctic petriellalean fossils provide comprehensive
information on the physiology and ecology of these peculiar
plants that inhabited the middle to high latitudes of the
Gondwana supercontinent (fig. 6).
The stems are consistently diminutive (!3 mm thick; fig. 4);
based on stem diameter-to-height relationships among extant
woody plants (Niklas 1993), the Antarctic petriellalean plants
must have been less than a meter tall. Yet, the largest stems
contain up to four growth rings (fig. 4A, 4F), demonstrating
that they were perennial and persisted over several growth
seasons. Upright (orthotropic) growth of the axes is reflected
in the combination of apetiolate, steeply inclined, simple foliage being radially arranged around the stem.
The anatomy of petriellalean foliage shows classic features
of shade-adapted leaves with low photosynthetic capacities,
including (1) an extremely thin lamina, (2) undifferentiated
mesophyll (i.e., lacking a palisade layer), and (3) large intercellular air spaces (see Givnish 1988; Smith et al. 1997).
Compared to co-occurring foliage taxa, these features are
much more similar to those of understory osmundaceous
ferns (see Rothwell et al. 2002) than to those of canopyforming gymnosperms, i.e., Corystospermales (Dicroidium)
and voltzialean conifers (Notophytum). The latter two leaf
types are considerably thicker and contain differentiated mesophyll with a palisade layer and a more or less densely packed
spongy layer (Pigg 1990; Axsmith et al. 1998). The lower
epidermis of petriellalean leaves also bears abundant glands
that produce raised, dome-shaped storage bodies (figs. 3E,
4L). This leaf character is usually interpreted to enhance leaf
durability (see, e.g., Feild and Arens 2007) and is notably
absent in the deciduous foliage of the co-occurring arborescent gymnosperm taxa mentioned above (Pigg 1990; Axsmith
et al. 1998; Bomfleur and Kerp 2010). Furthermore, cross
sections show that the margins of petriellalean leaves attenuate into winglike extensions (fig. 4M) and are commonly
enrolled or folded; similarly, many leaf compression fossils
have incurved margins or appear shriveled (see, e.g., Holmes
and Anderson 2005, figs. 21b, 22, 27b). We suggest that this
may reflect that the Petriellales were able to acclimate to unfavorable conditions by temporarily enrolling and shriveling
the leaf laminae. Altogether, this complement of features indicates a long leaf life span (see Smith et al. 1997; Givnish
2002; Feild and Arens 2007) and––in consequence––an evergreen phenology (Givnish 2002). This is supported by the
growth-ring anatomy, which is characterized by a much more
gradual transition from large-celled early wood to small-celled
late wood than seen in the co-occurring wood of deciduous
trees (Taylor and Taylor 1993; Taylor and Ryberg 2007).
Further evidence for diminutive growth and evergreen habit
comes from unusual taphonomic features of the petriellalean
compression fossils we studied (table 1). Remarkably, petriellalean foliage seems to be commonly preserved in organic
connection to stems not only in the KUPB Antarctic collections (fig. 2A) but also in other assemblages from South Africa (Anderson and Anderson 2003) and Australia (Holmes
and Anderson 2005). This kind of preservation is exceedingly
rare or unknown in all of the co-occurring gymnosperm foliage types (table 1). In addition, we found that detached
petriellalean foliage in the Antarctic collections is always
strongly fragmented and have never observed complete and
isolated leaves, which, by contrast, is the common mode of
leaf preservation of the co-occurring gymnosperms (Bomfleur
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Fig. 6 Paleogeographic occurrences of petriellalean fossils. Base map for the Late Triassic after Lawver et al. (1998); fossil occurrences
compiled from Anderson and Anderson (2003), Barone-Nugent et al. (2003), Holmes and Anderson (2005), Artabe et al. (2007), Morel et al.
(2011), and this study.
et al. 2011, 2013a; Escapa et al. 2011). Furthermore, petriellalean compression fossils are overall notably rare, occurring in only 2 of 49 or more plant-fossil assemblages
surveyed. They are absent in the typical “leaf-litter assemblages”—which accumulated during quiescent conditions
through the physiological loss of leaves and reproductive organs of seasonally deciduous gymnosperm trees (table 1;
Bomfleur et al. 2011, 2013a)—and are preserved only in
rather unusual plant-fossil assemblages; plant level 2 from
the Allan Hills, for example, contains redeposited, complete
fern rhizomes with attached fronds and croziers (T. N. Taylor et al. 1990; Phipps et al. 1998), subterranean organs of
sphenophytes (Bomfleur et al. 2013b), and abundant debris
of leafy and thallose bryophytes (Bomfleur et al. 2014a). At
the Alfie’s Elbow site, petriellalean remains occur only in the
level 2 bed, which also yielded (1) the only known occurrence
of corystosperm reproductive organs attached to short shoots
(Taylor et al. 1998; Axsmith et al. 2000, 2007), (2) one of
only three known occurrences worldwide of attached Dicroidium leaves (Axsmith et al. 2000), and (3) the only known
record of dipterid ferns in the Antarctic Triassic (Escapa et al.
2011). We interpret this rich assortment of otherwise rare
plant taxa and organs and the extraordinary proportion of
attached organs to reflect high-energy depositional events
(e.g., catastrophic river flooding or riverbank collapse after
heavy rainstorms) that caused traumatic removal of living
plants and plant parts, especially cryptogamic ground cover
(Bomfleur et al. 2014a). Of further significance is the unusual
preservation mode of petriellalean plants in the Nymboida
Coal Measures of Australia, where they are commonly preserved in the form of a succession of pseudowhorls of complete, attached leaves that spread from an upright-buried stem
(Holmes and Anderson 2005, figs. 18–20)—a distinctive form
of in situ burial that is uncommon among gymnosperms (but
see Anderson and Holmes 2008) and much more typical of
sphenophytes (see, e.g., Oplustil et al. 2007, fig. 2; Libertín
et al. 2009, pl. VI, 3, fig. 10; Thomas 2014, fig. 13).
Altogether, the complement of morphological, anatomical,
and taphonomic evidence demonstrates that the Petriellales
were low-growing, shade-adapted, perennial evergreens. The
vast number and small size of their seeds—borne in dehiscent
seedpods—is typical of pioneers and colonizers that litter
large quantities of seeds through ballistic dispersal (Howe and
Smallwood 1982).
Ecology and Paleoenvironment
This reconstruction gains particular significance in light of
the unusual paleogeographic and paleoenvironmental setting
of the Antarctic Petriellales in the Triassic polar forest biome
of Gondwana (fig. 6). Canopy and subcanopy trees in these
forests are composed of a diverse array of seed plants dominated by corystosperm seed ferns and voltzialean conifers
(fig. 7). Studies of anatomically preserved material in the
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Preservation
of attached
leaves
Isolated
leaves
Inferred
mode
of leaf loss
Inferred leaf
habit
Attachment
on . . .
Mesophyll
Leaf base
Relative
abundance
Predominant
occurrence
Usually complete
Physiological
(programmed
abscission)
Seasonally
deciduous
Fragmented
Traumatic
Evergreen
Very rare
(!1 in 1000)
Usually
complete
Physiological
(programmed
abscission)
Seasonally
deciduous
With palisade
parenchyma
and densely
packed
spongy layer
Very rare
(!1 in 1000)
With prominent
palisade
parenchyma
Common
(11 in 10)
Apetiolate,
base swollen
Short shoot
Leaf-litter
assemblages,
leaf mats
Dominant
Heidiphyllum
(Voltziales)
Petiolate, base
swollen
Short shoot
Leaf-litter
assemblages,
leaf mats
High-energy
event deposits
Apetiolate, base
not swollen
Cortical cushion
on stem
Undifferentiated,
loosely packed
Dominant
Dicroidium
(Corystospermales)
Rare
Rochipteris
(Petriellales)
Usually
complete
Physiological
(programmed
abscission)
Seasonally
deciduous
Usually
complete
Physiological
(programmed
abscission)
Seasonally
deciduous
Unknown
?
?
Unknown
Petiolate, base
swollen
?Short shoot
Leaf-litter
assemblages,
leaf mats
Uncommon
Dejerseya
(Peltaspermales)
Petiolate, base
swollen
?Short shoot
Leaf-litter
assemblages
Common
Sphenobaiera
(Ginkgoales)
Usually
complete
Physiological
(programmed
abscission)
(?Seasonally)
deciduous
Unknown
?
Petiolate, base
swollen
Unknown
Leaf-litter
assemblages
Uncommon
Linguifolium
(?Peltaspermales)
Complete or
fragmented
Physiological
(programmed
abscission)
(?Seasonally)
deciduous
Unknown
?
Unknown
Leaf-litter
assemblages,
high-energy
event deposits
Unknown
Uncommon
Taeniopteris
(Cycadophyta)
Selected Taphonomic, Morphological, Anatomical, and Inferred Physiological Features of Antarctic Petriellalean Foliage Compared to Those of
Co-occurring Gymnosperm Leaf Taxa in the Collection of the University of Kansas Natural History Museum, Division of Paleobotany
Table 1
Complete or
fragmented
Physiological
(programmed
abscission)
(?Seasonally)
deciduous
Unknown
?
Petiolate, base
swollen
Unknown
Leaf-litter
assemblages
Rare
Ginkgoites
(Ginkgoales)
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 7 Comparison of morphology and inferred life mode (Raunkiær classification) of selected well-known plants from the Triassic polar
forest biome of present-day Antarctica.
Triassic silicified peat deposits have enabled very detailed reconstructions of these plants (e.g., Taylor and Taylor 1990;
Hermsen et al. 2009; Bomfleur et al. 2013a; see Escapa et al.
2011; Cantrill and Poole 2012). Other gymnosperm groups
are more or less well documented by leaf compressions, including Dejerseya and Lepidopteris (Peltaspermales), Sphenobaiera and Ginkgoites (Ginkgoales), Taeniopteris (cycadophytes), and Rissikia (Podocarpaceae; Bomfleur et al. 2011;
Escapa et al. 2011; Cantrill and Poole 2012). Although anatomical details are not yet known for these plants, all are
considered to represent seasonally deciduous trees or tall
shrubs, based on their usual preservation in the form of accumulations of abscised, complete leaves (Bomfleur et al.
2011, 2013a; Escapa et al. 2011) or foliar spurs (Rissikia;
Townrow 1967). A peculiar exception is Antarcticycas, a diminutive cycad whose small (!10-cm-tall) stem was probably subterranean (Hermsen et al. 2009). Whether its leaves
were actively shed or shriveled on the plant remains uncertain; it is noteworthy, however, that none of the several dozens of stems found so far bears attached leaves, although the
stems are commonly covered in cataphylls (R. Serbet, personal communication, 2013) and seem to be preserved in situ
in the peat matrix, together indicating a probable deciduous
habit.
The most common understory plants in the Triassic polar
forests of Antarctica were apparently osmundaceous ferns,
judging from the widespread occurrences of their foliage
(Cladophlebis, “fossil Osmunda”) and rhizomes (Ashicaulis;
T. N. Taylor et al. 1990; Escapa et al. 2011; Cantrill and
Poole 2012). By analogy with their very similar extant relatives (Phipps et al. 1998; Rothwell et al. 2002; Bomfleur et al.
2014b), there is good evidence to suggest that the Triassic
Osmundaceae were herbaceous perennials. Other fern groups
are much rarer in the Triassic of Antarctica and belong to
Marattiaceae, Matoniaceae, Gleicheniaceae, and Dipteridaceae (Escapa et al. 2011; Cantrill and Poole 2012). Extant
representatives of these fern families are evergreen terrestrial
plants in (sub)tropical regions. At present, it is impossible
to ascertain whether the Triassic high-latitude representatives
of these groups were herbaceous perennials similar to the cooccurring Osmundaceae—as the prevalent strongly seasonal
climate might suggest. The Equisetum-like sphenophyte Spaciinodum was also a common herbaceous perennial in the
Triassic polar vegetation, producing seasonal dormant buds
to endure winter (Ryberg et al. 2008).
By and large, at the end of each growth season, the entire
forest canopy must have shed its leaves and—together with
the herbaceous understory plants—entered dormancy to endure the prolonged period of winter darkness. The Petriellales
apparently established a very different mode of life in this
environment: they formed low-growing understory vegetation that colonized the forest floor and remained evergreen
during winter, immersed alone in the dark for up to several
months in a quiescent forest (figs. 7, 8). Some understory
plants in deciduous forests today are known to assimilate the
highest carbon amounts over an entire year during the short
periods of increased exposure before canopy closure in early
spring and after canopy fall in late autumn (Fridley 2012).
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Fig. 8 Suggested reconstruction of a group of small evergreen petriellalean plants on the floor of a polar forest of Dicroidium and Telemachus trees at the onset of winter, some 230 Myr ago in what is now East Antarctica. Artwork by F. Spindler (Freiberg, Germany; http://
www.frederik-spindler.de).
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
In the warm polar forests of the Triassic, then, the evergreen
habit and the prominent adaptations to low-light photosynthesis can be expected to have extended the effective growing season of the Petriellales significantly beyond that of the
deciduous canopy trees, enabling these plants to exploit the
autumn niche (see Fridley 2012) and, perhaps, to continue assimilation even during the transitional phases of prolonged
twilight.
Many authors have noted the similarity of petriellalean cupules to those of the Caytoniales, a group of gymnosperms
that continues to figure prominently in theories about the
mysterious origin of flowering plants (e.g., Thomas 1925;
Crane 1985; Doyle 2006; Taylor and Taylor 2009). Recent
hypotheses propose that the earliest angiosperms may have
been small, woody shrubs that colonized disturbed sites in
the damp understory of humid forests (Feild et al. 2004; Feild
and Arens 2005, 2007; see Coiffard et al. 2012). The reconstructed physiology and ecology of the Petriellales matches
this life form to such detail that we suggest these unusual
gymnosperms may represent convergent ecological analogues
of early flowering plants.
Our knowledge of the Petriellales is still incomplete, as our
search for anatomically preserved pollen organs and rooting
structures has so far been unfruitful. However, the already
comprehensive information about their morphology, anatomy, and physiology places the Petriellales at once among
the most completely reconstructed groups of extinct gymnosperms. We anticipate that the evident question—whether
beyond the mere ecological similarity there may be phylogenetic relationships linking Petriellales to angiosperms—will be
answered once more detailed information about their reproductive biology becomes available.
Acknowledgments
We thank H. M. Anderson (Johannesburg), Mike Dunn
(Lawton, OK), and R. Spicer (Milton Keynes) for helpful
discussion; R. Serbet (Lawrence, KS) for technical assistance
and discussion; F. Spindler (Freiberg, Germany) for the reconstruction drawing; and six anonymous reviewers for comments on early versions of the manuscript. Financial support was provided by the Alexander von Humboldt-Stiftung
(Feodor Lynen fellowship to B. Bomfleur), the Agencia Nacional de Promoción Científica y Tecnológica (PICT-20102322 to I. H. Escapa), the National Science Foundation (ANT0943934 to E. L. Taylor and T. N. Taylor), and the Swedish
Research Council (VR grant to S. McLoughlin). AMAP (Botany and Computational Plant Architecture; http://amap.cirad
.fr) is a joint research unit with associates CIRAD (UMR51),
CNRS (UMR5120), INRA (UMR931), IRD (R123), and
Montpellier 2 University (UM2).
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