BohicalJournal ofthe Linnean Socieo (1999), 129: 177-186. With 4 figures
Article I D bojl. 1998.0222, available online at http://www.idealibrary.com on
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Latest Albian-earliest Cenomanian
monocotyledonous leaves from Australia
MIKE POLE
Department of Botany, Universip of Queemland, Brisbane, QIB 4072, Australia
Received February 1998; accepted for publication September 1998
Two forms of monocotyledon macrofossil are documented from latest Albian-earliest Cenomanian sediments of the Eromanga Basin, central Queensland, Australia. One form is
preserved as strap-shaped leaves with cross-linked parallel venation and epidermal features
characteristic of monocots. Its affinities are suggested to be with the AreciRorae and it
dominated a community lying between a coastal coal swamp and open marine conditions.
A second form is found only as thin, dispersed cuticle, with poor detail, but is most likely
also a monocot. It dominated a more inland community. These appear to be the currently
known, oldest, organically preserved monocotyledonous macrofossils.
0 1999 The Linnean Society of London
ADDITIONAL KEY WORDS:-Cretaceous - cuticle - evolution - palaeobotany - stomata.
CONTENTS
Introduction . . .
Methods . . . .
Results . . . .
Monocot-1 . .
Monocot-2 . .
Discussion . . .
Acknowledgements
References . . .
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INTRODUCTION
Information from fossils is steadily increasing our knowledge of early angiosperm
evolution. The oldest angiosperms are probably represented by inaperturate late
Valanginian to Hauterivian pollen from Israel (Brenner, 1996) while the earliest
flowers are from the Aptian of Australia (Taylor & Hickey, 1990). The more precise
relationships of these fossils are unclear. Cladistic analyses show the monocotyledons
are a monophyletic clade rooted within the basal angiosperms, although fossil
evidence of early monocots is sparse. The oldest pollen is from the late Hauterivian
(Brenner, 1996) while a recent review of the fossil history of the monocotyledons
(Herendeen & Crane, 1995)cited Acaciaephyllum Doyle (1973)as the earliest monocot
00244074/99/030177
+ 10 $30.00/0
177
0 1999 The Linnean Society of London
178
M. POLE
leaves known. These come from the Aptian of the Potomac Group of North America
and are impressions. Younger monocot records are almost entirely Campanian or
later, the exceptions being possible Araceae fruits or seeds from the Albian, and
palm pollen from the Santonian/Coniacian. Prior to the present study, the oldest
organically preserved monocot leaves were probably those of Nemejc & Kvacek
(1975) from the early Senonian of Bohemia, followed by those of Upchurch (1995)
from the Maastrichtian of New Mexico. Organic preservation adds the evidence of
stomatal morphology to support identification as a monocot.
From the Jurassic into the Cretaceous the Eromanga Basin was the location of
Australia’s great inland sea. The sea regressed in the mid Cretaceous and fluvial
sediments prograded far into the basin. The lithostratigraphy of the upper part of
the Eromanga Basin records a change from marine sedimentation of the Mackunda
Formation to the non-marine and dominantly fluvial sedimentation of the Winton
Formation (Vine & Day, 1965; Exon & Senior, 1976).
Dettman & Playford (1 969) placed all of the Mackunda Formation as well as the
Winton Formation within their Coptospora paradoxa Zone. A more recent revision
(Helby, Morgan & Partridge, 1987) treats the Coptospora paradoxa Oppel Zone as
extending from the Early Albian (c. 110 Ma) to the early Late Albian (c. 102 Ma). In
this scheme two succeeding zones also occur in the Winton Formation; the entirely
Late Albanian Phimopollenites pannosus Oppel Zone, followed by the almost entirely
Cenomanian Appendickporites distocarinatus Oppel Zone. Palynologicalwork in progress
(M. Dettmann, pers. comm., 1998) suggests the age of all the samples studied here,
from both the Mackunda and Winton Formations, lies close to the AlbianCenomanian boundary, but precision is not yet adequate to place the boundary
exactly.
Although surface exposures of Eromanga Basin sediments have produced plant
remains which are either silicified (Peters & Christophel, 1978) or deeply weathered
(McLoughlin, Drinnan & Rozefelds, 1995), the bore core material recovered by an
extensive drilling programme has proved to be rich in organically preserved plant
fossils. The broader study (Pole, unpublished data) has found that almost all
samples are dominated by coniferous remains, with prominent bennettitaleans and
ginkgoaleans. Dicotyledonous angiosperms are patchy and of minor importance.
The aim of this paper is to describe early monocotyledonous macrofossil remains
from Australia which are organically preserved.
METHODS
Seven drill cores were selected from the Eromanga Basin in central Queensland
(Fig. 1); G S Q Eromanga-1, G S Q Maneroo-1, and G S Q Thargominda-3 were
sampled in September 1995, and GSQBlackall- 1, GSQQuilpie-1, GSQMachattie1, and GSQTickalara-1 in June 1997 (these cores are stored in a Geological Survey
of Queensland (GSQ warehouse at Zillmere, Brisbane). Each of these cores
penetrates fluvial sediment of the Winton Formation and underlying marine sediment
of the Mackunda Formation. O n present information it is not possible to place the
Winton-Mackunda Formation boundary precisely. Marine molluscs are taken as
clear evidence of the Mackunda Formation. In Thargomindah-3 and Maneroo- 1
they are abundant, then disappear abruptly upsection. There is then a gap of nearly
MONOCOTYLEDON FOSSILS FROM AUSTRALIA
17%
Figure 1. Above: Location map of all seven drill cores sampled for this study. The two cores which
contain monocot fossils are italicized, the prefix 'GSQ' has been omitted. Below: The position of
samples from Thargomindah-3 and Maneroo- 1 which contain monocot fossils. The scales show depths
below the present surface. For each sample these are: THA-39 (284.3 m), MAN-9 (29.8 m), MAN-I0
(29.9 m), MAN-I 1 (29.95 m), MAN-17 (36.0 m), MAN-I9 (39.15 m), MAN-24 (42.5 m), MAN-36
(208.6 m). The upper dotted l i e indicates a possible correlation of the only prominent coal beds in
each core. These coals and all sediment above is considered as the Winton Formation. The lower
dotted l i e indicates the highest occurrence of marine mollusc fossils. This is considered as the
maximum depth of the upper boundary of the Mackunda Formation. The predominant lithology has
been indicated by stipple (sand) and horizontal lines (mud). For detailed lithological logs see Gunther
& Dixon (1988) and Hoffmann, McKellar & Carmichael(l991).
100 m before a prominent coal bed (about 1 m thick) in both cores. In this region
the only clear subaerial evidence is a rootlet horizon 30m below the coal. The
Mackunda-Winton Formation boundary lies somewhere in this 100 m zone.
In total, 235 samples of approximately 5 cm3 each were selected for macrofossil
180
M. POLE
investigation. Carbonaceous muds were preferred, sands were avoided unless they
contained prominent carbonaceous horizons, and lignites were also generally avoided
(previous experience and some tests indicated these usually do not preserve cuticle).
For ease of reference the samples were prefixed with the first three letters of the
core name and numbered consecutively from the top of each core.
Most of the sample was processed for cuticle, leaving a small amount as a voucher
specimen. Samples usually broke down into a sludge with the addition of warm
water, but sometimes addition of a little hydrogen peroxide was needed. Sludge was
washed through 500 and 125 J..lm mesh sieves, with most workable cuticle being
retained on the 500 J..lm. Further clearing of cuticle involved increasing concentrations
of warm peroxide, or sometimes aqueous chromium trioxide acid for particularly
recalcitrant remains. Any adhering silicates were removed with HF and the cuticle
was stained with crystal violet.
With the exception of one sample (MAN-1) in which monocot leaf fragments
were visible on the bedding surface of a core sample, samples at this stage consisted
of small (3-4 mm or less) dispersed fragments of cuticle in water. These samples
were scanned under a binocular microscope and fragments removed with tweezers
for transmitted light microscopy (TLM) or scanning electron microscopy (SEM).
Macrofossils are catalogued with the prefix 'SL' and are stored in the Department
of Botany, University of Queensland. Specimens mounted on electron microscope
stubs are catalogued with the prefix'S'. Specimens for TLM viewing were mounted
on microscope slides with glycerine jelly, and those for SEM viewing on stubs with
magnetic tape and coated with gold.
RESULTS
Monocot-1
(Figs 2, 3)
Riference specimen. SL769 (MAN-10).
Riferred specimens (sample number, depth, specimen number). MAN 9 (29.8 m) SL0724;
MAN 10 (29.9 m) SL0725, SL0769; MAN 11 (29.95 m) SL0726; MAN-17 (36.0 m)
SL989; MAN 19 (39.15m) SL0727; MAN 24 (42.5m) SL0728; MAN 25 (42.6m)
SL0729, SL0770; MAN 36 (208.6 m) SL0730.
Description. Two samples from GSQ Maneroo-1 within the Winton Formation
produced fragments of strap-shaped leaves with parallel venation and mostly oblique
cross-linking veins. The total1eaflength is unknown, but would be several centimetres
at least, the width is approximately 15 mm, the margins entire and parallel. Venation
is longitudinal, of 2-3 orders, parallel, and cross-linked by fine, mostly oblique veins.
Vein order is generally ACBCBCACB (A=thickest vein order, C =thinnest). There
is no indication of a mid rib on the available fragments.
The cuticle is well preserved with stomata and epidermal cells clearly visible.
Stomata are longitudinally orientated, widely scattered, not forming obvious rows
or located in zones, and occur on both leaf surfaces. The guard cells are surficial,
with a prominent thickening forming an outer stomatal ledge positioned over each.
Other than these, there is no other differentiation by cuticle thickening over the
hlONOC~OTY1,EI~ON
FOSSI1.S FROM AUSTRALIA
181
Figure 2. Monocot-I; A, TLM of leaf fragment including margin, SL770. Scale bar = I mrn; B, TLM
of leaf showing thrce orders of longitudinal venation and oblique, connecting \reins. Dark spots are
probably due to degradation process, SL770. Scale bar = 1 rnm; C, TLM of leaf showing three orders
of longitudinal venation, oblique connecting veins and margin, SL770. Scale bar = I rnm; D, TLM of
single stornate, SL769. Scale bar = 23 pm; E, SEM of outer surfacc of singlc stomate, S757. Scnlc
bar = 10 pm; F, SEM of outer surface of single stornate, S757. Scale bar = 20 pm.
stomata or other epidermal cells. The stomata are essentially paratetracytic but
show a lack of consistency in subsidiary cell pattern, grading from monocyclic to
dicyclic. Figure 3 illustrates six stomatal complexes both as photographs and as
schematic interpretations of the subsidiary cell pattern for each. The stomatal
complexes are characterized by the products of oblique cell division. They include
Tomlinson’s ( 1974) ‘non-intersecting’ type which results in typically ‘trapezoid’ cells
h l . 1’OI.E
Figure 3. Stoinatal patterns of Alonocot-1 . l’hotographs of six srparate stomata1 complexrs are shown
with a schematic linc intcqmwtion to the right; A, non-iniersrcting sulxidiary ccll walls forming nvo
‘trapezoid’ sihsitliary cells; H, a Kirimit o f t h r above where only (me of thr walls leading IO a ’trapezoid’
cell h a s Ibrnicd; C . one irapczoicl cell h a s divided longitudinally giving rise to the Arrcalcan type: 11,
both trapezoid cells have divided loiigitudin;illy; E, intersecting subsidiary cell walls on one sirlc of the
stoma; F, mirror iimgc of above.
latcrally adjacent to the guard cells (Fig. 3A). Variation occurs when only one of
the oblique divisionr nccdcd to form a trapezoid crll occurs (Fig. 3B) or when the
trapczoid cell may itsrlf divide longitudinally (Fig. 3C, D). Intersecting oblique
MONOCOTYLEDON FOSSILS FROM AUSTRALIA
I83
divisions are also present (Fig. 3E, F). A large variety of patterns results as each side
of the stoma may exhibit any one of the basic forms. There are no trichomes or
papillae. A further six samples from Maneroo-1 produced fragments of this type of
cuticle, but without venation details.
Discussion. The differentiation of longitidunal venation into more than one order
( s m u Hickey, 1973) and the cross-linking of longitudinal veins by finer cross-veins
are two of the three criteria considered diagnostic of monocotyledon leaves by Doyle
(1973). The third criterion, the convergence and successive fusion of the longitudinal
veins towards the apex, was not noted on this material as no apices were recovered.
The epidermal morphology indicates stomata with distinct outer stomatal ledges,
and stomatal poles which are level with the stomatal pore. These are general
characters which distinguish it from other taxa which sometimes have longitudinally
aligned stomates (for instance conifers and the gnetalean Welwitschiu),which, in the
absence of venation details, may be confused. These taxa usually also have deeply
sunken guard cells.
The subsidiary cell pattern is characteristic of many monocots. Tomlinson (1974)
presented a scheme of monocot stomatal development starting‘with three files of
initial cells. This is distinct from Welwitschiu but similar to conifers (Florin, 1931,
1934). In Tomlinson’s scheme an initial cell in the central file divides lengthwise
giving rise to the guard cells while adjacent cells in this file and the flanking file
may further divide to form subsidiary cells. Subsidiary cells may then be distinguished
by a difference in size and shape from normal epidermal cells, although subsequent
growth and cell rearrangement may obscure the original pattern. Tomlinson divided
monocot stomatal development into two basic groups-those with oblique cell
division and those without-but stressed that stomatal complex type should be used
cautiously in monocot taxonomy. He noted that a range of types could occur, even
within a single individual, but that nevertheless, they had broad taxonomic value.
Some natural groups, for instance Poaceae and Arecaceae, had consistent, distinct
stomatal types. Dahlgren & Clifford (1982) demonstrated the taxonomic importance
of other stomatal characters amongst monocots, including whether stomata were
largely absent, and the number (or absence) of subsidiary cells. Combining the
results of both Tomlinson (1974) and Dahlgren & Clifford (1982), on the basis of
the paratetracytic stomates and oblique cell divisions the affinities of Monocot- 1
may lie with the Areciflorae.
It would be misleading to search for a close relative amongst the extant Areciflorae.
Although Tomlinson noted that a variety of stomatal form could occur in single
extant taxa, among the extant Areciflorae at least, stomatal form seems much more
regular than the fossil. For instance, among the extant Arecales the pattern of
trapezoid cells divided longitudinally, is “constant and characteristic” (Tomlinson,
1974: 1 18; pers. obs.), whereas in the Pandanaceae this happens “rarely” (Tomlinson,
1965: 43). This pattern is not rare in Monocot-I, but is certainly not characteristic.
The proportion of types may vary considerably; in one fragment (SL871) the
unmodified, non-intersecting type forms over 75% of stomata, in another (SL725),
the figure is reversed, over 40% are of the intersecting type and over 30% of the
modified, non-intersecting (Arecalean) type. This may be the same phenomenon
which Upchurch (1984) noted for early dicots where stomatal development appeared
to be loosely controlled, resulting in a broader representation of stomatal types
within single individuals than seen today. Stomatal development appears to have
184
M. POLE
Figure 4. Monocot-2; A, TLM showing stomatal zone, SL768. Scale bar= 200 J.Lm; B, TLM detail of
stomates, SL768. Scale bar= 23 J.Lm; C, SEM of inner stomatal surface, S 751. Scale bar= 50 J.Lm; D,
SEM of outer surface of single stomatc, S751. Scale bar= 20 J.Lm.
'channellized' since and mid Cretaceous so that a specific stomatal type is now more
rigidly adhered to within a species. The absence of any definitively monocot pollen
in the Winton Formation (M. Dettmann, pers. comm. 1998) suggests the absence
of any extant group (it does not rule out the presence of monocots producing
pollen indistinguishable, at present, from non-monocots). Monocot-1 is perhaps best
considered as an early representative or relative of the Areciflorae.
Monocot-2
(Fig. 4)
Riference specimen. SL635 (THA 39).
Riferred specimens. SL634, SL635 (THA 39).
Description. Sample THA-39 within the Winton Formation of GSQ Thargomindah3 was dominated by cuticle fragments where stomata are longitudinally orientated
and almost evenly spaced, although they are mostly in recognizable rows. The
interpretation of the stomatal complex is difficult. Under TLM the anticlinal walls
are not clear-the thickest cuticle surrounds the guard cells and cells at the polar
ends of the guard cells. The form of these polar cells is difficult to interpret and
may be confused foldings of the cuticle. SEM indicates that the guard cells arc
MONOCOTYLEDON FOSSILS FROM AUSTRALIA
185
sunken, covered with granular cuticle, and are slightly overarched by surrounding
cells. Ordinary epidermal cells have sinuous or slightly buttressed anticlinal walls
and are covered with smooth cuticle.
Discussion. The over-all appearance of this cuticle suggests it is most likely a monocot,
however the lack of detail precludes any more precise comparison.
DISCUSSION
All the monocot-bearing samples documented here are close to the base of the
Winton, or in the case of MAN-36, well within the Mackunda Formation. As these
date from around the Albian-Cenomanian boundary, the monocot leaves described
here are certainly among the oldest, and perhaps the oldest known with cuticular
detail.
The age and possible relationships of Monocot- 1 are consistent with the cladogram
of monocot relationships presented by Herendeen & Crane (1995). They showed
Arecales as basal to one of the two major clades of monocots and the Pandaniflorae
and Cyclanthiflorae are sister taxa, and at a possibly more basal position.
Monocot- 1 dominated four of the samples it was found in (Man-9, 10, 1 1, 25)
almost to the exclusion of all other taxa. In the other samples it featured prominently.
Monocot-2 dominated the only sample it was found in (THA-39). This suggests
they may have grown in extensive communities which were often broad enough to
exclude input of litter from the surrounding conifer forest. The location of all the
Monocot-1 bearing samples below the major, basal coal of GSQManeroo- 1 suggests
an environment between a near-coastal coal-swamp and open marine conditions.
A possible modern analogue would be the herbaceous (the growth habit of Monocot1 is not known) marshes growing in the lowest, most distal portions of the MobileTensaw River delta of Alabama (Gastaldo, 1989).
These fossils confirm the presence of monocots as early as the Albian-Cenomanian
boundary. Moreover, they suggest that one of the major extant clades, the Arecales,
had differentiated. The possible growth of these plants in extensive, monospecific
marshes within what were otherwise coniferous forests, might provide an avenue
for future research on what triggered the initial evolution of the monocots and their
continuing dominance of particular habitats.
ACKNOWLEDGEMENTS
I am most grateful to the Geological Survey of Queensland, particularly Kinta
Hoffmann, and the staff at the Zillmere core store for providing access to the drill
cores. Assistance from the staff of the Centre for Microscopy and Microanalysis,
University of Queensland, was greatly appreciated. This research was completed
with funding from an ARC grant to M.E. Dettmann and G. Stewart.
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