Content uploaded by G.W. Rothwell
Author content
All content in this area was uploaded by G.W. Rothwell on Feb 04, 2020
Content may be subject to copyright.
Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
www.elsevier.nl/locate/palaeo
An herbaceous fossil conifer: Gymnospermous ruderals in
the evolution of Mesozoic vegetation
Gar W. Rothwell a, *,Le
´a Grauvogel-Stamm b, Gene Mapes a
aDepartment of Environmental and Plant Biology, Ohio University, Athens, OH 45701, USA
bEOST-Ge
´ologie, Universite
´Louis Pasteur and CNRS (UMR 5554), 67084 Strasbourg Cedex, France
Received 6 May 1999; received in revised form 17 August 1999; accepted for publication 30 August 1999
Abstract
Fast growing conifers have been recognized in disturbed habitats of the transitional Lower Middle Triassic Gre
`s
a
`Voltzia delta from the Buntsandstein in eastern France. These herbaceous conifer fossils reveal that some Mesozoic
seed plants were capable of opportunistic growth and rapid prolific reproduction long before the origin of flowering
plants. Such ruderals indicate that certain gymnosperms came to characterize river terrace floras by the evolution of
reduced size and enhanced reproductive allocation, while others dispersed to dominate more arid expanses of the
Mesozoic landscape before the rise of flowering plants. The widespread occurrence and quantitative distribution
patterns of pollen similar to that of Aethophyllum in the Middle Triassic suggests that Aethophyllum and related
conifers may have played an important role in the evolution of distinctive Mesozoic wetland communities. © 2000
Elsevier Science B.V. All rights reserved.
Keywords: delta habitat; evolutionary ecology; herbaceous conifer; ruderal; Triassic
1. Introduction contrast to herbaceous angiosperms, all living gym-
nosperms (i.e. cycads, Ginkgo, conifers, and gneto-
phytes) are long lived woody plants that do not
Among living seed plants, angiosperms are the
begin sexual reproduction until after an extended
only clade that includes herbaceous species that
period of juvenile growth (Gifford and Foster,
are capable of opportunistic growth and rapid
1989). Such a life history pattern has also been
reproduction in unstable habitats (Stebbins, 1981;
presumed to characterize all fossil gymnosperms,
Bond, 1989). This ruderal life history pattern
including conifers (Bond, 1989). However, in her
appears to have played an important role in angio-
characterization of Aethophyllum stipulare,
sperms becoming the most diverse clade to ever
Grauvogel-Stamm (1978) described seedlings and
dominate the land surface (Retallack and Dilcher,
entire fertile plants that she interpreted to be
1981; Crane, 1987; Doyle and Donoghue, 1993; herbaceous conifers. Re-examination of the struc-
Crane et al., 1995; Taylor and Hickey, 1996). In ture, depositional regime, and biotic associations
of A. stipulare adds strong support for this inter-
pretation, and reveals that some fossil gymno-
* Corresponding author. Tel.: +1-614-593-1118;
sperms could have had a much wider range of life
Fax: +1-614-593-1130.
E-mail address: rothwell@ohiou.edu (G.W. Rothwell )
history patterns than previously realized.
0031-0182/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved.
PII: S0031-0182( 99) 00136-4
140 G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
2. Methods this paper, the reader is referred to Grauvogel-
Stamm (1978).
Growth patterns and ecological settings for
fossil plants are extremely difficult to observe
directly. Nevertheless, developmentally diagnostic 3. Results and discussion
structural features can be preserved in specimens
of extinct species. Moreover, habitats of growth 3.1. Structural indicators of growth and life history
patterncan be inferred both from analyses of sediments
in which the plants are deposited and by the
organismal associations with which the plants are A. stipulare is a relatively small conifer with
stems that branch only two or three times, andpreserved (e.g. Gall and Grauvogel-Stamm, 1993).
If a species of fossil plants displays a suite of that produce terminal pollen cones on some shoots
and terminal ovulate cones on others ( Fig. 1;characters characteristic of a particular life history
pattern among living plants, then the extinct Grauvogel-Stamm, 1978). Leaves are strap shaped
(Plate IPLA1, 1, 2 ) with several parallel veinsspecies can be hypothesized as conforming to a
similar life history pattern. Likewise, if a distinctive (Grauvogel-Stamm, 1978 ), which is similar to
some species of living podocarpaceous and arau-combination of features is produced by the
deposition of sediments in a particular modern cariaceous conifers ( Kramer and Green, 1990 ). As
is typical of conifers, ovulate cones of A. stipulareenvironment, then a similar combination of sedi-
mentological features can be interpreted as repre- are compound shoots, consisting of an axis that
bears helically arranged bracts and axillary ovuli-senting a similar environment in the past. These
inferences are further strengthened if the life his- ferous shoots (Grauvogel-Stamm, 1978 ). The latter
are usually termed ovuliferous scales in moderntory patterns for the biotic associations within the
sediments are also characteristic of comparable species. Seeds are small (approximately 2 mm
long), ellipsoidal and unwinged, and the pollen ismodern environments and associated taxa.
The Triassic fossil conifer A. stipulare saccate (Grauvogel-Stamm, 1978 ).
The largest Aethophyllum plants are 1.5 to 2.0 mBrongniart is a prominent element of a low diver-
sity biota inhabiting fluvial flood plains of the tall with stems that reach 2 cm or less in diameter
at the base. All of the branches terminate in cones,early Mesozoic Gre
`sa
`Voltzia delta in north-
eastern France (Grauvogel-Stamm, 1978 ). We re- with ovulate cones positioned toward the apex of
the plant and pollen cones clustered lower on theexamined A. stipulare and associated organisms in
the extensive Grauvogel and Gall collections that shoot ( Fig. 1 ). As a result, none of the branches
is capable of additional apical growth. Whereasare housed in Ringendorf and at the Universite
´
Louis Pasteur Institut de Ge
´ologie, Strasbourg, to these plants could have continued to grow by
branching from lateral axillary buds at a laterrecord features of both external morphology and
internal anatomy that are diagnostic of growth stage than is represented by any of the available
specimens, the absence of larger stems from theforms, growth rates and ontogeny in living plants.
Specimens that provide data to formulate hypothe- extensive collections of this species suggests a
determinant growth pattern for A. stipulare shoots.ses of growth, phenology and life history pattern
for A. stipulare include intact seedlings, juvenile Stems have an endarch eustele with tiny cauline
bundles and a broad pith that consists of large airplants, and essentially whole fertile plants. The
resulting hypotheses of growth and life history spaces and interspersed parenchyma cells ( Plate I,
2). Wood is produced by both roots and shootspattern were tested by comparing them to sedimen-
tological and biotic associational data from the (Grauvogel-Stamm, 1978). However, there are
only about six rows of secondary tracheids thatGre
`sa
`Voltzia delta to determine if these indepen-
dent interpretations are concordant. For documen- accompany the primary xylem of cauline bundles
in the stem, and there is no interfascicular second-tation and further details of the A. stipulare
characters that are interpreted and evaluated in ary xylem at all (Plate I, 2). Because some of the
141G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
A. stipulare produced such a small increment of
secondary tissue that it was essentially an herba-
ceous plant.
There is excellent cellular preservation of the
pith parenchyma in A. stipulare (Plate I, 2). This
demonstrates that the large air spaces that make
up most of the volume of the pith are an anatomi-
cal feature of the plant, rather than having origi-
nated by decomposition of thin walled pith cells.
By correlation to living plants that display a broad
pith and have a large percentage of plant volume
that consists of air space (e.g. bamboo, Equisetum,
and the inflorescence axes of Agave), Aethophyllum
can be interpreted to have had extremely rapid
primary growth and maturation of the shoot
systems.
Several immature A. stipulare specimens consist
of intact plants. The smallest seedlings are only
about 4 cm tall. Seedlings display a hypocotyl and
primary root system, two two-veined cotyledons,
and a short stem with helically arranged four-
veined leaves (Plate I, 3 ). Leaves on more mature
plants typically have six veins. The occurrence of
these complete seedlings interspersed among well-
preserved, articulated remains of larger plants in
the sediments implies that the fossils were buried
close to their site of growth, and further suggests
that they grew in developmentally heterogeneous
stands of continuously reproducing individuals.
The smallest fertile plant of A. stipulare is only
about 30 cm tall ( Plate I, 1). It consists of a
primary root and two shoots, one of which is
terminated by an ovulate cone ( Plate I, 1;
Grauvogel-Stamm, 1978). In the Ohio University
greenhouse, germinating seeds of the wetland coni-
Fig. 1. Largest adult plant of A. stipulare in the Grauvogel and
fer Taxodium distichum grow to plants of this same
Gall collections showing relatively large, strap shaped leaves,
two orders of branches from the stem, and all of the branches
size in about 15 weeks ( personal observations,
terminating in cones. Elongated cones in the apical region are
GWR, 1998), suggesting that fertile A. stipulare
ovulate, and pollen cones are ellipsoidal. Reproduced from
fossils could have been as little as three or four
Grauvogel-Stamm (1978 ) (scale bar=1M).
months old when they began sexual reproduction.
3.2. Sedimentological data and biotic associationsstem sections that show these characters were made
from branches immediately below mature cones
(Grauvogel-Stamm, 1978 ), it is clear that this Sedimentological data suggest high disturbance
rates characterized the terrestrial ecology of thespecies became fertile at about the same time as
the onset of secondary growth, and that only a Gre
`sa
`Voltzia delta, with a progressively westward
intertonguing of fluvial and marine influences.tiny amount of secondary xylem was produced
before cone senescence. Therefore, the shoots of Intermittent flood currents and shifting sand bars
142 G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
produced a mosaic of soils, temperatures, sediment senting three main facies. The youngest facies
represents incursions of the sea. It occurs as intra-stability, and unreliable water availability in a
dynamic continental environment that was eventu- formational breccias, and sometimes autochtho-
nous banks of calcareous to dolomitic sandstoneally fully inundated by the Muschelkalk marine
transgression (Gall and Grauvogel-Stamm, 1993). that contain a sparse marine fauna of foraminifers,
pelecypods and gastropods and essentially no ter-Plant and animal remains in the delta are pre-
served in sandstone, shale and clay horizons repre- restrial plant remains.
In the more proximal or easternmost facies, large
unlaminated channel deposits form thick sandstone
PLATE I lenses. In these areas, a few randomly oriented 1 to
2 m logs and numerous fragmentary iron stained
plant impressions occur, along with scattered stego-
cephalian bones. The generally coarse sandstone
lenses represent high energy flood erosion of chan-
nel banks and levees, which resulted in deposition
of point bars and barrier bars in strongly sinuous
channels throughout the flood plain (Gall and
Grauvogel-Stamm, 1993). Although low diversity,
poorly preserved and often transported short dis-
tances, remains of the delta vegetation can some-
times be identified in these sandstones.
By contrast, the silty clay facies contains a
remarkably well-preserved biota of terrestrial
plants and euryhaline aquatic invertebrates.
Sediment lenses are up to several decimeters thick
with vertically graded millimeter thick laminae. In
places, the lenses show subaquatic slumping, boron
enrichment of the clays, mudcracks and rare salt
pseudomorphs (Gall, 1971, 1983 ). These sediments
contain the most complete specimens of A. stipu-
lare and associated plants, including several speci-
mens with in situ roots and rhizomes. The
associated plants include well-preserved remains
PLATE I
A. stipulare.
1. Smallest fertile plant in the Grauvogel and Gall collec-
tions, with two stems extending from the root, and termi-
nal ovulate cone (OC ) on one branch (scale bar=10 cm).
2. Cross-section of stem in the Grauvogel and Gall collec-
tions showing cauline bundles with scanty wood (at left,
top and right) surrounding large pith with large, aeren-
chymatous lacunae and interspersed pith parenchyma
cells. Vascular cambium, phloem, and more peripheral
tissues are not preserved (scale bar=200 mm).
3. Seedling in the Grauvogel and Gall collections showing
primary root (R ), cotyledons (C ) and stem (S ) with api-
cally borne leaves (scale bar=10 cm).
143G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
of the fern Anomopteris and the equisetophytes therefore, the in situ plants could potentially be
either stress tolerant or ruderal species. However,Equisetites and Schizoneura (Grauvogel-Stamm,
1978). Similar ferns and equisetophytes also char- the species of stress tolerant communities differ in
many structural and sedimentological featuresacterize unstable habitats in certain Triassic flood
plain environments in North America ( Wing and from species of ruderals.
Stress tolerant plants are typically slow growingSues, 1992).
In addition to preserving the delta vegetation, and long lived, with persistent organs, leathery or
needle like leaves, slow intermittent reproduction,this combination of rapid sedimentation and
anaerobic microbial activity has preserved many and small numbers of large seeds. Stress tolerant
seed plants are further characterized by a largedevelopmental stages of insect larvae, fish eggs,
small conchostracan crustaceans, jellyfish, worms, volume of wood in the stems. By contrast, ruderals
tend to be fast growing, short lived plants withand small, thin shelled lingulid brachiopods in life
position (Gall, 1971, 1983, 1990 ). The silty clay mesomorphic leaves, precocious reproductive
maturity, and large quantities of small seedsshale horizons are interpreted as ephemeral pools
with fluctuating salinities. The lenses vary in lateral (Grime, 1979).
The very small size of some fertile plantsextent and thickness, but all represent shallow
stagnant water bodies located between the chan- (Plate I, 1 ) and the paucity of wood in
Aethophyllum stems ( Plate I, 2) indicates that fastnels and levees of the overbank plain.
Both the plants and animals of the Gre
`sa
`growth characterized this plant. The mesomorphic
leaves of A. stipulare further support the interpreta-Voltzia delta are abundant in numbers, but low in
species diversity. The herbaceous conifer and three tion of this species as a ruderal. As emphasized
above, a large aerenchymatous pith like that in A.pteridophyte species apparently grew on the banks
and islands of the fluviatile watercourses. stipulare is diagnostic of plants with extremely
rapid growth. The occurrence of cones at the tipAbundant pollen, disarticulated seed cones, and
leaf litter in individual clay layers indicate that the of every branch on the largest Aethophyllum plants
(Fig. 1) suggests a determinant growth pattern,rapid burial in some clay laminae may represent
only a few weeks, or the spring and autumn of a and demonstrates the potential for prolific pro-
duction of small seeds ( 2 mm). All of these charac-single year (Gall, 1983). These sedimentologic and
biotic data are concordant with disturbed habitats ters are consistent with A. stipulare having made
the disproportionately large investment in sexualthat favor rapidly growing, opportunistic ruderals
such as A. stipulare. reproduction that is characteristic of fast growing
ruderals.
3.3. Life history pattern of A. stipulare
3.4. Paleovegetational consequences
Plants that live in different environments display
distinct suites of diagnostic structural features that The recognition of fast growing fossil conifers
in disturbed habitats of the Triassic providesreveal the life history pattern for which they are
adapted. The most detailed characterization of unequivocal evidence that certain seed plants were
capable of weedy growth and prolific reproductionthese life history patterns has been developed by
Grime, who recognized three primary patterns: before the diversification of flowering plants. This
demonstrates that some fossil gymnosperms hadcompetitive, stress tolerant and ruderal (Grime,
1979). Whereas competitive species typically grow life history patterns like the living flowering plants
that rapidly colonize disturbed habitats in whichin high diversity communities and show a wide
range of growth form, stress tolerant and ruderal plant speciation is thought to be most prevalent
(DiMichele et al., 1987; DiMichele and Aronson,species tend to occur in low diversity communities
and be relatively small in stature. The latter fea- 1992 ).
There is an extensive palynological record oftures characterize the flora of the Gre
`sa
`Voltzia
delta (Grauvogel-Stamm, 1978; Gall, 1983) and, Illinites chitonoides Klaus, the palynospecies to
144 G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
which pollen of A. stipulare conforms, in Middle Publication ISEM No. 99-070, UMR 5554 CNRS,
Montpellier, France.Triassic deltaic sediments of western, central and
southern Europe, and possibly also Russia,
Northern Africa and China (H. Visscher, personal
communication, June 1999; Grauvogel-Stamm, References
1978; Gall et al., 1998). Application of quantitative
distribution patterns for I. chitonoides in paleo-
Bond, W.J., 1989. The tortoise and the hare: ecology of angio-
sperm dominance and gymnosperm persistence. Biol.
environmental analyses strongly supports the
J. Linnean Soc. 36, 227–249.
hypothesis that A. stipulare was a highly successful
Brugman, W.A., Van Bergen, P.F., Kerp, J.H.F., 1994. A quan-
herbaceous conifer occupying wetland environ-
titative approach to Triassic palynology: the Lettenkeuper
ments in a wide geographic area during the Middle
of the Germanic Basin as an example. In: Traverse, A. ( Ed.),
Triassic (Grauvogel-Stamm, 1978; Brugman et al.,
Sedimentation of Organic Particles. Cambridge University
Press, Cambridge, pp. 409–429.
1994). This indicates a much more important
Crane, P.R., 1987. Vegetational consequences of the angiosperm
ecological role for Aethophyllum and similar gym-
diversification. In: Friis, E.M., Chaloner, W.G., Crane, P.R.
nospermous ruderals than can be interpreted from
(Eds.), The Origins of Angiosperms and their Biological
the megafossil record alone, possibly contributing
Consequences. Cambridge University Press, Cambridge,
significantly to the evolution of distinctive
pp. 107–144.
Crane, P.R., Friis, E.M., Pederson, K.R., 1995. The origin and
Mesozoic wetland communities.
early diversification of angiosperms. Nature 374, 27–33.
Although our understanding of the role of
DiMichele, W.A., Aronson, R.B., 1992. The Pennsylva-
evolutionary ecology in changing vegetational pat-
nian–Permian vegetational transition: a terrestrial analogue
terns remains incomplete, several general patterns
to the onshore–offshore hypothesis. Evolution 46, 807– 824.
are emerging. The initial diversification of angio-
DiMichele, W.A., Phillips, T.L., Olmstead, R.G., 1987. Oppor-
tunistic evolution: Abiotic environmental stress and the
sperms in the Upper Cretaceous is strongly corre-
fossil record of plants. Rev. Palaeobot. Palynol. 50,
lated, for some species, with the ruderal life history
151–178.
pattern and with flowering plants sequentially
Doyle, J.A., Donoghue, M.J., 1993. Phylogenies and angio-
invading and displacing other groups in a wide
sperm diversification. Paleobiology 19, 141–167.
variety of habitats into the Tertiary (Midgley and
Gall, J.C., 1971. Faunes et paysages du Gre
`sa
`Voltzia du Nord
des Vosges. Essai pale
´oe
´cologique sur le Buntsandstein
Bond, 1991; Crane, 1987; Wing et al., 1993; Crane
supe
´rieur. Me
´m. Serv. Carte ge
´ol. d’Alsace et de Lorraine,
et al., 1995; Hickey, 1996). By contrast, conifers
Universite
´Louis Pasteur de Strasbourg 34, 1–318.
initially diversified in much drier habitats that
Gall, J.C., 1983. Ancient Sedimentary Environments and the
favor long lived, woody perennials ( Rothwell et al.,
Habitats of Living Organisms. Introduction to Palaeo-
1996), and only a small number of specialized
ecology. Springer-Verlag, Berlin. 219 pp.
Gall, J.C., 1990. Les voiles microbiens. Leur contribution a
`la
species appear to have been associated with unsta-
fossilisation des organisms au corps mou. Lethaia 23, 21 –28.
ble wetland habitats before the Tertiary. A. stipu-
Gall, J.C., Grauvogel-Stamm, L., 1993. Paleoecology of ter-
lare provides the best evidence to date that some
restrial ecosystems from the Buntsandstein ( Lower Triassic)
early Mesozoic conifers were ruderals, and that
of eastern France. In: Lucas, S.G., Morales, M. ( Eds.), The
such species played a significant role in the evolu-
Nonmarine Triassic. New Mexico Museum of Natural His-
tory and Science, 3, Albuquerque, NM, pp. 141–145.
tionary turnover leading to the establishment of
Gall, J.C., Grauvogel-Stamm, L., Papier, F., 1998. La Crise
Mesozoic wetland plant communities.
biologique du Permian et la renaissance triasique (The Per-
mian mass-extinction and the Triassic recovery. C.R. Acad.
Sci. Paris). Sciences de la terre et des plane
ˆtes (Earth and
Acknowledgements
Planetary Sciences) 326, 1–12.
Gifford, E.M., Foster, A.S., 1989. Morphology and Evolution
of Vascular Plants. 3rd edn., Freeman, New York. 625 pp.
This study was supported in part by the
Grauvogel-Stamm, L., 1978. La flore du Gre
`sa
`Voltzia (Bunt-
National Science Foundation (DEB-9527920 to
sandstein Supe
´rieur) des Vosges du Nord (France). Mor-
G.W.R. and G.M.). We are indebted to H.
phologie, Anatomie, interpre
´tations phyloge
´nique et
Visscher and W.A. DiMichele for their con-
pale
´oge
´ographique. Me
´m. Sci. Ge
´ol., Universite
´Louis
Pasteur de Strasbourg Inst. Ge
´ol. 50, 1–225.
structive reviews and helpful suggestions.
145G.W. Rothwell et al. /Palaeogeography, Palaeoclimatology, Palaeoecology 156 (2000) 139–145
Grime, J.P., 1979. Plant Strategies and Vegetation Processes. Rothwell, G.W., Mapes, G., Mapes, R.H., 1996. Paleozoic coni-
fers of North America, structure, diversity and occurrences.Wiley, New York. 222 pp.
Hickey, L.J., 1996. The ancestral habit of the flowering plants. Rev. Palaeobot. Palynol. 95, 95–113.
Stebbins, G.L., 1981. Why are there so many species of flower-In: Akhmetiev, M.A., Doludenko, M.P. ( Eds.), Abstracts
and Proceedings of the Memorial Conference Dedicated to ing plants? BioScience 31, 573–577.
Taylor, D.W., Hickey, L.J., 1996. Evidence for and implicationsVsevolod Andreevich Vakhrameev. Geological Institute,
Russian Academy of Sciences, Moscow, pp. 70–72. of an herbaceous origin for angiosperms. In: Taylor, D.W.,
Hickey, L.J. (Eds.), Flowering Plant Origin, Evolution andKramer, K.U., Green, P.S., 1990. The Families and Genera of
Vascular Plants I: Pteridophytes and Gymnosperms. Phylogeny. Chapman and Hall, New York, pp. 341–403.
Wing, S.L., Sues, H.-D., 1992. Mesozoic and early CenozoicSpringer-Verlag, Berlin. 404 pp.
Midgley, J.J., Bond, W.J., 1991. Ecological aspects of the rise terrestrial ecosystems. In: Behrensmeyer, A.K., Damuth,
J.D., DiMichele, W.A., Potts, R., Sues, S.D., Wing, S.L.of angiosperms: a challenge to the reproductive superiority
hypothesis. Biol. J. Linnean Soc. 44, 81–92. (Eds.), Terrestrial Ecosystems Through Time. The Univer-
sity of Chicago Press, Chicago, pp. 337– 416.Retallack, G.J., Dilcher, D.L., 1981. A coastal hypothesis for
the dispersal and rise to dominance of flowering plants. In: Wing, S.L., Hickey, L.J., Swisher, C.C., 1993. Implications of
an exceptional fossil flora for Late Cretaceous vegetation.Niklas, J.K. ( Ed.), Paleobotany, Paleoecology and Evolu-
tion Vol. 2. Praeger, New York, pp. 27–77. Nature 36, 342–344.
