Botanical Journal of the Linnean Socie!Y (1988), 97: 205-227. With 44 figures
Tertiary leaves of the tribe Banksieae
(Proteaceae) from south-eastern Australia
ROBERT S. HILL, F.L.S.
Department qf Plant Science, University qf Tasmania, G.P.O. Box 252C, Hobart,
Tasmania, Australia 7001
AND
DAVID C. CHRISTOPHEL
Botany Department, University qf Adelaide, G.P.O. Box 498, Adelaide, South Australia,
Australia 5001
Received March 1987, accepted for publication December 1987
HILL, R. S. & CHRISTOPHEL, D. C., 1988. Tertiary leaves of the tribe Bauksieae
(Proteaceae) from south-eastern Australia. Leaves from the tribe Banksieae of the Proteaceae
are well represented in Tertiary deposits in south-eastern Australia. Four new species of
Banksieaephyllum are erected, taking the total to II, and two species are described in a new genus,
with leaves with architectural similarities to the tribe Banksieae but without organic preservation.
The fossil species demonstrate that the tribe was diverse by the end of the Eocene, but it is difficult
to determine the ancestral type from the fossil evidence at present. The vegetation associated with
some of the fossil species suggests that the tribe may have had its origins in rainforest, and became
adapted to the typically dry, nutrient-poor conditions of sclerophyllous vegetation during the course
of the Tertiary.
ADDITIONAL KEY WORDS:-Banksia- Dryandra- Eocene- leaf architecture - Macrofossils.
CONTENTS
Introduction .
Materials and methods.
Fossil localities
Fossil and extant specimens
Taxonomic descriptions
Definition of Banksieaephyllum
Taxonomic descriptions of new Banksieaephyllum species
Definition of Banksieaiformis
Taxonomic descriptions of new Banksieaiformis species
Architectural relationships of extant Banksia and Dryandra species
Leaf architecture in Banksia
Leaf architecture in Dryandra .
Comparison of fossil and living species
Discussion .
Acknowledgements
References.
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1988 The Linnean Society of London
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R. S. HILL AND D. C. CHRISTOPHEL
INTRODUCTION
Banksia and Dryandra constitute the subtribe Banksiinae of Johnson & Briggs
(1975), which, together with Austromuellera and Musgravea (subtribe
Musgravinae) form the tribe Banksieae of the Proteaceae. Johnson & Briggs·
considered that the Banksieae must have evolved by the Late Cretaceous,
although the earliest fossil record is pollen from the Palaeocene (Martin, 1978).
George ( 1981) revised Banksia, and suggested that the genus originated under
tropical or subtropical conditions in Australia during the Tertiary. He believed
that the genus was widespread across Australia before the onset of aridity in the
Tertiary and the emergence of the Nullarbor Plain, since the two sections of the
major subgenus, Banksia, occur on both sides of the Nullarbor Plain.
The macrofossil record of the tribe Banksieae consists of leaves and fruits. The
genus Banksieaephyllum was proposed by Cookson & Duigan ( 1950) to encompass
fossil leaves having affinities with the extant genera Banksia and Dryandra.
According to Cookson & Duigan, no combination of leaf characters can
consistently separate these closely related genera in the Proteaceae. They also
reviewed the status of 20 fossil Australian species, but transferred only one to
Banksieaephyllum, the others being omitted on the grounds of inadequate
comparative work in the original descriptions. Similarly, they discounted all
extra-Australian fossil species.
There are currently seven species of Banksieaphyllum: six from the Oligocene
Yallourn brown coal in Victoria (Cookson & Duigan, 1950), and the other from
the Middle Eocene Maslin Bay mudstone in South Australia (Blackburn, 1981).
Banksia fruits have been described from the Yallourn brown coal (Pike, 1953)
and from the Middle or Late Eocene Merlinleigh Sandstone in Western
Australia (McNamara & Scott, 1983). The aim of this study is to describe six
new fossil species in the tribe Banksieae, and to consider the implications of these
species for the evolution of the tribe.
MATERIAL AND METHODS
Fossil localities
The fossil species described in this paper were collected from eight Tertiary
deposits in south-eastern Australia (Fig. l). Details of the age of the deposits are:
(1) Dean's Marsh (38°36'S, 143°54'E). W. K. Harris (personal
communication) has placed the microflora in the Malvacipollis diversus zone of
Stover & Partridge (1973), which spans the Early Eocene.
(2) Anglesea (38°25'S, 144° 11'E). Christophel ( 1984) assigned an Early
Eocene age to the flora based on an analysis of the microflora.
(3) Maslin Bay (35°l4'S, 138°28'E). Alley ( 1987) assigned a Middle Eocene
age to the flora based on an analysis of the microflora.
(4) Golden Grove (34°45'S, 138°40'E). Alley (1987) assigned a Middle
Eocene age to the flora based on an analysis of the microflora, and considered
that the sand deposit at Golden Grove (which contains the fossiliferous material)
is a correlative of the North Maslin sands (which contains the Maslin Bay
fossiliferous rna terial).
(5) Cethana (41°29'S, 146°09'E). Carpenter & Hill (in press) assigned a Late
Eocene-Oligocene age to the flora based on an analysis of the microflora.
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
207
Figure I. Map of south-eastern Australia showing the fossil localities. I = Maslin Bay; 2 = Golden
Grove; 3 =Deane's Marsh; 4 =Anglesea; 5 =Loy Yang; 6 = Cethana; 7 =Pioneer; 8 =Loch
Aber.
(6) Loch Aber (4l 0 02'S, 144°ll'E). M. K. Macphail (personal communication) considered that the microftora can be assigned stratigraphically to
the Lower Nothofagidites asperus Zone of Stover & Partridge ( 1973), which spans
the Middle and Late Eocene.
(7) Pioneer (4l 0 05'S, 14T56'E). Hill & Macphail (1983) assigned an
Oligocene age to the flora based on an analysis of the microflora.
(8) Loy Yang (38°ll'S, 146°37'E). A. D. Partridge (personal communication)
assigned the fossil-bearing coal to the Proteacidites tuberculatus zone of Stover &
Partridge ( 1973) based on an analysis of the microflora. This gives an age range
of Oligocene (probably Late) to Early Miocene.
Fossil and extant specimens
Specimens from Maslin Bay and Cethana consist of impressions, and cuticular
detail could not be recorded. All other specimens were compressions, from
which both venation detail and cuticular characteristics were recorded.
Fossils were photographed using either transmitted, reflected or low angle
reflected light, depending on which best highlighted the venation pattern.
Cuticles were prepared using the technique described by Hill (1983).
Banksia has recently been the subject of a detailed revision by George ( 1981).
The current taxonomic treatment is given in Table 1, including an indication of
the species available for this study. Dryandra has not been revised since 1870, and
the current revision will appear in Volume 17 of the Flora of Australia according
to George ( 1984). Table 2 contains the list of species presented by Griffin ( 1985)
and George (1984), and indicates the species available for this study.
208
R. S. HILL AND D. C. CHRISTOPHEL
Leaves of all except the needle-leaved Banksia species were cleared using the
method of Blackburn ( 1978), and photographed using transmitted light.
Cuticles were prepared from all species using the method described by Hill
( 1983). Terminology follows Hickey ( 1979) for leaf architecture and Dilcher
(1974) for cuticular morphology.
An attempt was made to cluster the fossil and extant species using a
numerical taxonomic approach. This was only moderately successful, probably
due to the difficulty in compiling a useful character set for such a
morphologically diverse set of leaves, and the results are not presented here.
TAXONOMIC DESCRIPTIONS
Dfjinition ofBanksieaephyllum
Banksieaephyllum was described by Cookson & Duigan ( 1950) to accommodate
six species from the Y allourn brown coal. Blackburn ( 1981 ) emended the
diagnosis to incorporate the species from Maslin Bay. His emended diagnosis is:
Leaves simple with entire, serrate, or lobed margins, or pinnate; bilateral.
Stomates superficial, or in pits, or in grooves, each with pair of subsidiary
cells placed parallel to pore. Cells of stomatiferous epidermis with thick or
thin, pitted, straight or curved lateral walls, some with bicellular hairs.
Basal cells of hairs either thick or thin walled, sometimes with beaded
thickening, of even diameter throughout or expanded distally or
proximally. Cylindrical hair bases present on some or all cells of the nonstomatiferous epidermis. Cuticular papillae sometimes present.
The diagnosis contains information on both leaf architecture and cuticular
structure, and in all species so far described cuticular morphology was observed.
Cookson & Duigan ( 1950) believed that fossil leaves could not be confidently
assigned to the tribe Banksieae without information on cuticular morphology.
Given the importance of cuticular morphology in determining the affinity of
these fossil leaves, it is clear that leaves without cuticular preservation should
not be placed in Banksieaephyllum.
Taxonomic descriptions of new Banksieaephyllum species
Family: Proteaceae
Subfamily: Grevilleoideae
Tribe: Banksieae
Banksieaephyllum Cookson & Duigan, Australian Journal of Scientific Research Series
B, 3: 133-165 (1950).
Banksieaephyllum cuneatum Hill & Christophel, sp. nova
Leaves bilateral, pinnately lobed, lobes acute and apically directed. Apical side
of lobe usually concave, basal side convex, sinuses acute. Leaf base cuneate,
apex unknown. Leaf length at least 12 em, width up to 4 em. Secondary
venation craspedodromous, usually four veins per lobe. Stomata brachyparacytic, individually sunken below general epidermal surface or level with the
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
Figures 2-7. Banksieuplayllum cuneatxm sp. nova. Scale bars = I em in all figures. Fig. 2.
Holotype of Banksieaephyllum cuneatum (AM 4331, compression specimen). Fig. 3. Impression of
B. cuneatum (AM 10051) showing the major venation pattern. Fig. 4. Impression of B. cuneatum
(AM 10052) showing detail of the higher order venation. Fig. 5. Mummified leaf of B. cuneatum
(AM 10053) showing the cuneate base. Fig. 6. Compression specimen of B. cuneatum from Deane's
Marsh (DM 001). Fig. 7. Mummified leaf of B. cuneatum from Golden Grove (GG 051).
209
210
R. S. HILL AND D. C. CHRISTOPHEL
surface. Small trichome bases associated with one or two epidermal cells
abundant on stomatiferous surface, basal trichome cell thickly cutinized,
cylindrical, apical cell(s) not preserved. Large trichome bases associated with
one to five epidermal cells common on non-stomatiferous surface. Trichomes not
preserved. Epidermal cells on non-stomatiferous surface striated.
LOCATION: Anglesea, Deane's Marsh, Golden Grove.
HOLOTYPE: AM-4331, stored in the South Australian State Herbarium (AD)
(Fig. 2).
ETYMOLOGY: Named for the very characteristic cuneate leaf base (Figs 5-7).
DiscussiON: The single specimen from Deane's Marsh (Fig. 6) and the specimens
from Anglesea (Figs 2-5) and Golden Grove (Fig. 7) are similar in all but one
respect. The stomates on the Anglesea specimens are below the general
epidermal surface (Fig. 8), whereas on the Dt:ane's Marsh and Golden Grove
specimens they are superficiaf-(Figs 9, 10). This character was not deemed
sufficiep.t to warrant separate specific status. The cuticle from the upper
epidermis exhibits characteristic multi-celled proteaceous trichome bases and an
obviously striated surface (Figs 11-13). Banksieaephyllum cuneatum differs from
B. incisum (Blackburn, 1981) in the shape of the lobes, but it is closely allied to
that species in both leaf architecture and cuticular morphology.
Banksieaephyllv.m attenuatv.m Hill & Christophel, sp. nova
Leaves bilateral, serrate. Serrations small, with rounded apex and sinus. Leaf
base cuneate, apex attenuate. Leaf length at least 6 em, width up to 1.5 em.
Secondary venation craspedodromous, one secondary vein per serration.
lntersecondary veins prominent, common. Stomata brachyparacytic,
superficial. Trichome bases associated with two to six epidermal cells common
on stomatiferous epidermis. Trichomes bicellular, basal trichome cell thickly
cutinized, cylindrical, apical trichome cell thinly cutinized, tapering. Trichome
bases not observed on non-stomatiferous epidermis.
LOCATION: Loch Aber.
HOLOTYPE: LA-005, stored m the Department of Plant Science, University of
Tasmania (Fig. 14).
ETYMOLOGY: Named for the unusual attenuate apex of the leaves.
DiscussiON: Several specimens of this species have been recovered, and although
none is complete, the whole leaf can be reconstructed. Both the apex (Fig. 15)
and the base (Fig. 16) gradually narrow, and in the case of the apex, this is
unknown among extant species. The venation pattern is very distinct, with
secondary veins terminating in small serrations separated by intersecondary
veins (Fig. 14). The cuticular pattern of the specimens (Figs 17, 18) exhibit the
stomatal arrangement and trichome bases typical of the genus.
Banksieaephyllv.m regv.laris Hill & Christophel, sp. nova
Leaves bilateral, serrate, serrations acute. Apical side of serrations straight, basal
side convex, sinuses acute. Leaf base obtuse, apex probably acute. Leaf length
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
211
Figures 8-10. Cuticle from the stomatiferous surface of Bankaieaeplayllum cuneatxm •P· nova.
All figures to same scale as Fig. 8: scale bar = 50 J.lm. Fig. 8. Anglesea; note the stomate (arrowed)
which is sunken just below the general cuticular surface. Fig. 9. Deane's Marsh; the stomata are on
the same level as the numerous trichome bases. Fig. 10. Golden Grove; the stomata are on the same
level as the numerous trichome bases.
Figures 11-13. Cuticle from the non-stomatiferous surface of Banksieaephyllum cuneatum. Note the
multicellular trichome bases and striated surface ornamentation. Fig. II. Anglesea. Fig. 12. Deane's
Marsh. Fig. 13. Golden Grove.
approximately 4 em, width approximately 0.8 em. Secondary venation pattern
semicraspedodromous, usually two veins per serration. Stomata brachyparacytic, superficial. Trichome bases on stomatiferous epidermis small,
irregular, sunken between epidermal cells, common over veins. Trichome basal
cell thinly cutinized, apical cell(s) not preserved. Similar trichome bases rare on
non-stomatiferous epidermis.
LOCATION:
Pioneer.
212
R. S. HILL AND D. C. CHRISTOPHEL
.,,._,.m
sp. aova. Fig. 14. Holotype of Banksieaephyllum
Figures 14-18. Baalc.UupltyUam
altenualum (LA-005, compression); scale bar = I em. Fig. 15. Compression of B. atlenuatum (LA004) showing the attenuate apex; scale bar = 1 em. Fig. 16. Compression of B . attenuatum (LA-051)
showing the cuneate base; scale bar = I em. Fig. 17. Cuticle from the stomatiferous surface of
B. allenualum, showing the superficial stomata and trichome bases; scale bar = 50 11m. Fig. 18.
Cuticle from the non-stomatiferous surface of B. attenuatum; scale bar = 50 11m.
HOLOTYPE: P-428, stored in the Department of Plant Science, University of
Tasmania (Fig. 19).
ETYMOLOGY: Named for the regular alternation of secondary and intersecondary
vems.
DiscussiON: The leaves of this species are relatively small (Fig. 19), and have a
regular venation pattern with secondary veins terminating in serrations and
intersecondary veins terminating in the serration sinuses (Figs 19, 20). The
cuticular pattern exhibits the stomatal arrangement and trichome bases typical
of the genus (Figs 21-23).
Banksieaephyllum elongatus Hill & Christophel, sp. nova
Leaves bilateral, pinnately lobed, lobes acute and apically directed. Apical side
oflobe usually straight or slightly concave, basal side convex. Apical side of lobe
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
213
19
Figures 19-23. BanksieiUiphyllum replari• sp. nova. Fig. 19. Holotype of B. regularis (P-428,
mummified leaf); scale bar = I em. Fig. 20. Part of a mummified leaf of B. regularis (P-1055), ·
showing details of the venation pattern; scale bar= 2 mm. Figs 21, 22. Cuticle from the
stomatiferous surface of B. regularis showing the superficial stomata and the trichome bases; scale
bars = 50 J.lm. Fig. 23. Cuticle from the non-stomatiferous surface of B. regularis; scale bar =
50J.tm.
much shorter than basal side. Leaf base cuneate, apex unknown. Leaf length at
least 6 em, width up to I em. Secondary venation pattern craspedodromous,
with a variable number of secondary veins per lobe. Stomata brachyparacytic,
superficial. Trichome bases of two types abundant on stomatiferous epidermis.
Large trichome bases associated with usually one but sometimes two or three
epidermal cells, trichome small, unicellular. Small trichome bases associated
with one epidermal cell, trichome basal cell thickly cutinized, cylindrical, apical
cell(s) not preserved. Trichome bases absent from non-stomatiferous epidermis.
LOCATION:
Loy Yang.
LY-022, stored m the Department of Plant Science, University of
Tasmania (Fig. 24).
HOLOTYPE:
ETYMOLOGY:
Named for the elongate serrations at the leaf margin.
Deane ( 1925) described Dryandra urniformis from a single leaf
fragment from the brown coal deposit at Yallourn North. The specimen is
similar to B. elongatus, but the lobes are consistently of a different shape and
proportion (Figs 24, 25). The leaf base is rarely preserved, but it can be seen
that it is cuneate (Fig. 26) with a very gradual taper of the lamina to the
petiole. The cuticular pattern (Figs 27-29) confirms the affinities of the fossil
DiscussiON:
214
R. S. HILL AND D. C. CHRISTOPHEL
Figures 24-29. Banbieaeplayllum ~thmg•hu sp. Dova. Fig. 24. Holotype of B. elongatus (LY022, compression). Note the regular dentations extending in to the midvein; scale bar = I em.
Fig. 25. Compression of B. elongatus (LY-007 ), showing a slightly different dentation shape from the
holotype; scale bar = I em. Fig. 26. Compression of B. elongalus (LY-001 ), showing the extended
cuneate base (arrowed); scale bar = I em. Figs 27, 28. Cuticle from the stomatiferous surface of
B. elongatus, showing the superficial stomata, trichome bases and basal trichome cells at two focal
planes; scale bar = 50 jlm. Fig. 29. Cuticle from the non-stomatiferous surface of B . elongalus,
showing a single-celled trichome base; scale bar = 50 jlm.
with Bansieaphyllum. It is considered therefore that the specimens from Loy
Yang constitute a distinct and new species.
Definition
of Banksieaeformis
Some specimens have been recovered which exhibit great architectural
similarity with extant Banksia and Dryandra species, but which have no organic
remains. These specimens cannot be placed in the genus Banksieaephyllum due to
the lack of cuticular preservation. We propose the genus Banksieaejormis for
specimens which have the architecture of Banksia, Dryandra or Banksieaephyllum,
but which have no organic preservation.
Family: Proteaceae
Subfamily: Grevilleoideae
Tribe: Banksieae
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
215
Figures 30, 31. Banksieaiformis decurrens gen. et sp. nova; scale bars = I em. Fig. 30. Holotype of
B. decurrens gen. et sp. nova (S-1497, impression). Fig. 31. Close-up of a section of the holotype of
B. decurrens in Fig. 30 showing details of the venation pattern.
Figures 32, 33. Banksieaiformis dentatus gen. et sp. nova; scale bars = I em. Fig. 32. Holotype of
B. dentatus (C-251, impression). Fig. 33. Close-up of a section of the holotype of B. dentatus, showing
details of the venation pattern.
Banksieaeformis Hill & Christophel genus novuJD
Leaves simple with entire, serrate or lobed margins, or pinnate; bilateral,
architecturally similar to Banksia, Dryandra or Banksieaephyllum species.
TYPE SPECIEs: Banksieaeformis decurrens Hill & Christophel (Fig. 30).
Taxonomic descriptions if new Banksieaeformis species
Banksieaeformis decurrens Hill & Christophel, sp. nova
Leaf entire in basal half, pinnately lobed in apical half. Lobes acute, apically
directed. Apical side of lobe straight, basal side convex, sinuses acute. Leaf
base decurrent, apex unknown. Leaf length approximately 7 em, width
approximately I em. Secondary venation pattern brochidodromous in the basal
half, craspedodromous in the apical half.
LOCATION: Maslin Bay.
HOLOTYPE: S-1497, stored m the South Australian State Herbarium (AD)
(Fig. 30).
ETYMOLOGY: Named for the decurrent leaf base.
DISCUSSION: Only one specimen of this species has been recovered (Figs 30, 31).
The leaf has a very long decurrent base, but in the apical half the leaf form is
very similar to Banksieaephyllum cuneatum (Figs 2-7) and B. incisum (Blackburn,
1981), although it is much smaller.
216
R. S. HILL AND D. C. CHRISTOPHEL
Banksieaeformis dentatus Hill & Christophel, sp. nova
Leaf serrate, serrations acute. Apical and basal side of serrations convex, sinuses
acute. Leaf base cuneate, apex unknown. Leaf length approximately 6 em,
width approximately 1 em. Secondary venation pattern craspedodromous, one
vein per serration. Intersecondary veins prominent, common.
LOCATION: Cethana.
HOLOTYPE: C-251, stored m the Department of Plant Science, University of
Tasmania (Fig. 32).
ETYMOLOGY: Named for the dentate appearance of the leaf margin.
DiscussiON: Several specimens of this species have been recovered from Cethana,
but only one represents a complete leaf (Figs 32, 33). The venation pattern is
clear on this specimen, but as with much of the Cethana flora, no cuticular
preservation is present.
ARCHITECTURAL RELATIONSHIPS OF EXTANT BANKS/A AND DRYANDRA SPECIES
In comparing the fossil species to living species of Banksia and Dryandra it was
clear that the cuticular and architectural patterns gave conflicting results. This
was mainly because the older fossils usually had superficial stomates, whereas
many of the architecturally similar living species had the stomates sunk deep in
pits. It is probable that this difference is the result of evolution in response to
drier conditions and consequently towards reduced transpiration. Unlike many
other sclerophyllous plants, Banksia and Dryandra appear to have often
maintained a large leaf form while developing other xeromorphic
characteristics. Therefore in determining the affinities of the fossil leaves, the leaf
architecture should be a far more reliable guide than cuticular characteristics
which have clearly altered dramatically, at least in some cases, and bear little
resemblance to the fossils. In order to compare the species of Banksieaephyllum
and Banksieaeformis with extant species of Banksia and Dryandra it is first
necessary to examine trends in leaf architecture among the extant species.
A number of trends can be seen among the extant Banksia and Dryandra
species, and in order to illustrate and describe them adequately it is necessary to
select a starting point. The leaf form which was chosen for this purpose in both
genera was that which most closely resembled the oldest Banksieaephyllum species
described to date. These species were Banksia grandis Willd. (Figs 34, 36) and
Dryandra drummondii Meisn. (Figs 35, 37), respectively. For simplicity, the two
genera will be considered separately.
Leaf archtitecture in Banksia
The most notable feature of Banksia leaf architecture is that the morphological
extremes of leaves with serrations which reach the mid-vein (pinnately lobed,
e.g. B. grandis, Figs 34, 36) and leaves with entire margins (e.g.
B. integrifolia var. integrifolia L. Fil., Fig. 34) are separted by a continuum of
forms with varying degrees of serrations (Fig. 34). Clearly then, if B. grandis is
chosen as the starting point, the major trend in Banksia is towards entiremargined leaves through the gradual reduction of serrations. However, there
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Subgenus Banksia
Section Banksia
Series Salicinae
*B. dentata L. Fil. (N)
B. integrifolia L. Fil.
*var. integrifolia L. Fil. (E)
*var. compar (R. Br.) Bailey (E)
*var. auqilonia A. S. George (E)
B. conferta A. S. George
*var. conferta A. S. George (E)
*var. penicillata A. S. George (E)
*B. marginata Cav. (E+T)
*B. caneij. H. Willis (SE)
*B. saxicola A. S. George (SE)
*B. plagiocarpa A. S. George (E)
*B. oblongifolia Cav. (E)
*B. robur Cav. (E)
*B. paludosa R. Br. (E)
Series Grandes
*B. grandis Willd. (SW)
*B. solandri R. Br. (SW)
Series Q.uercinae
B. quercifolia R. Br. (SW)
*B. oreophila A. S. George (SW)
*B. baueri R. Br. (SW)
Series Orthosrylis
*B. smata L. Fil. (E+T)
*B. aemula R. Br. (E)
*B. ornata F. Muell ex Meissner (SE)
*B. menz;iesii R. Br. (SW)
*B. speciosa R. Br. (SW)
*B. baxteri R. Br. (SW)
*B. candolleana Meissner (SW)
*B. sceptrum Meissner (SW)
Section Oncosrylis
Series Spicigerae
B. spinulosa Smith
*var. spinulosa Smith (E)
var. collina (R. Br.) A. S. George (E)
*var. cunninghamii (Sieber ex Reichb.)
A. S. George (E)
*B. ericifolia L. Fil.
var. ericifolia L. Fil. (E)
var. macrantha A. S. George (E)
*B. brownii Baxter ex R. Br. (SW)
*B. occidentalis R. Br. (SW)
B. littoralis R. Br.
*var. littoralis R. Br. (SW)
*var. seminuda A. S. George (SW)
*B. verticillata R. Br. (SW)
B. tricuspis Meissner (SW)
Series Dryandroideae
*B. dryandroides Baxter ex Sweet (SW)
Series Abeitinae
B. sphaerocarpa R. Br.
var. sphaerocarpa R. Br. (SW)
var. caesia A. S. George (SW)
var. dolichostyla A. S. George (SW)
B. micrantha A. S. George (SW)
B. grossa A. S. George (SW)
B. leptophylla A. S. George (SW)
*B. lanata A. S. George (SW)
B. scabrella A. S. George (SW)
B. telmatiaea A. S. George (SW)
*B. laricina C. Gardner (SW)
B. incana A. S. George (SW)
B. violacea C. Gardner (SW)
TABLE I. List of extant Banksia species according to George ( 1981). An asterisk denotes species which were
included for comparison in this study. The distribution of the species- is given in brackets; E = eastern
Australia, N =northern Australia, SE =south eastern Australia, SW =south western Australia,
T =Tasmania
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Series Crocinae
*B. prionotes Lindley (SW)
*B. victoriae Meissner (SW)
*B. hookerana Meissner (SW)
*B. burdettii E. G. Baker (SW)
Series Cyrtosrylis
*B. media R. Br. (SW)
*B. praemorsa Andrews (SW)
*B. pilosrylis C. Gardner (SW)
*B. attenuata R. Br. (SW)
*B. lindleyana Meissner (SW)
*B. ashbyi E. G. Baker (W)
*B. benthamiana C. Gardner (SW)
*B. audax C. Gardner (SW)
*B. laevigata Meissner
ssp. laevigata C. Gardner (SW)
ssp.fuscolutea A. S. George (SW)
*B. lulljitzii C. Gardner (SW)
*B. elderana F. Muell. & Tate (W)
*B. elegans Meissner (SW)
Series Prostratae
*B. goodii R. Br. (SW)
B. gardneri A. S. George
*var. gardneri A. S. George (SW)
*var. brevidentata A. S. George (SW)
var. hiemalis A. S. George (SW)
*B. chamaephyton A. S. George (SW)
*B. repens La bill. (SW)
*B. blechnifolia F. Muell. (SW)
*B. petiolaris F. Muell. (SW)
Series Tetragonae
*B. lemanniana Meissner (SW)
*B. caleyi R. Br. (SW)
*B. aculeata A. S. George (SW)
Series Coccineae
*B. coccinea R. Br. (SW)
Subgenus lsosrylis
*B. ilicifolia R. Br. (SW)
B. cuneata A. S. George (SW)
B. meisneri Lehm.
var. meisneri Lehm. (SW)
var. ascendens A. S. George (SW)
B. pulchella R. Br. (SW)
B. nutans R. Br.
var. nutans R. Br. (SW)
var. cemuella A. S. George (SW)
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220
R. S. HILL AND D. C. CHRISTOPHEL
appear to be at least two major pathways by which serrations have been
reduced.
In the first pathway, there is a reduction in the number of intersecondary
veins. Initially, in B. grandis, there is one major secondary vein per serration,
which terminates in the apex of the serration, and a number of minor secondary
veins (intersecondary veins) on each side of this vein which terminate before the
leaf margin. As the serrations become smaller, the secondary vein continues to
terminate in the apex, but the number of intersecondary veins between each
secondary vein reduces, eventually to one (e.g. B. speciosa R. Br. -+ B. gardneri
var. gardneri A. S. George in Fig. 34). This branching intersecondary vein alters
its course until eventually the two branches loop apically and basally to merge
with the apical and basal secondary veins (B. gardneri var. gardneri -+ B. dentata
L. Fil. in Fig. 34). From this point onwards the serrations become smaller, and
are eventually lost, although apparently in a random manner. When the
serrations are lost, the secondary vein becomes indistinguishable from the
intersecondary veins, and all would be classified as secondary veins (B. dentata
-+ B. integrifolia var. integrifolia in Fig. 34).
In the second pathway, the number of intersecondary veins do not decrease,
but remain at a minimum of two. These intersecondary veins gradually change
direction and loop into each other and into adjacent secondary veins
(B. pilostylis C. Gardner -+ B. audax C. Gardner in Fig. 34). The number of
serrations then decreases, and the number ofintersecondary veins between them
increases (B. audax -+ B. benthamiana C. Gardner in Fig. 34). From this point
there may be a link with the B. canei J. H. Willis type of architecture. It can be
seen (Fig. 34) that these two pathways are not clearly separate and could
contain the same species at the beginning and end.
Leaf architecture in Dryandra
In contrast to Banksia, there are no entire-margined Dryandra species.
However, in many ways the Dryandra species are similar in architecture to the
Banksia species. Two lines can be seen developing from the starting point of
D. drummondii.
In the first pathway, the serrations retain the approximate symmetry
exhibited by D. drummondii, but they become smaller, the number of
intersecondary veins decreases to one between each pair of secondary veins, and
. the intersecondary veins begin to loop into the apical and basal secondary veins
(D. drummondii-+ D. cuneata R. Br. and D. quercifolia Meisn. in Fig. 35). This is
similar to part of the first pathway outlined for Banksia (Fig. 34).
All other pathways in Dryandra are typified by an increasing asymmetry in the
serration. For example, from D. drummondii to D. preissii Meisn. it can be seen
that one of the major differences is the extension of the basal side of the serration
in the latter species. This extension is more highly developed in other species,
leading to a pronounced serration, with a short apical side, and a long, tapering
basal side (D. preissii -+ D. senecifolia R. Br. in Fig. 35). In some cases the basal
side of the serration expands, giving a venation pattern similar to some Banksia
species (D. concinna R. Br. in Fig. 35 compared with B. benthamiana in Fig. 34).
Finally, in some species the asymmetry of the serrations appears to be
secondarily lost, while at the same time there is a marked reduction in the leaf
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
221
2. List of extant Dryandra species according to George ( 1984) and Griffin
( 1985). An asterisk denotes species which were included for comparison in this
study
TABLE
*D. arborea C. A. Gardner
*D. arctotidis R. Br.
*D. armata R. Br.
*D. ashbyi B. L. Burtt
*D. baxteri R. Br.
*D. bipinnatifida R. Br.
*D. calophylla R. Br.
*D. carduacea Lindley
D. carlinoides Meisn.
*D. cirsioides Meisn.
D. comosa Meisn.
*D. concinna R. Br.
*D. conferta Benth.
*D. cuneata R. Br.
D. cynaroides C. A. Gardner
*D. drummondii Meisn.
D. erythrocephala C. A. Gardner
*D.falcata R. Br.
*D.ferruginea Kipp. ex Meisn.
*D.folio/ata R. Br.
"D. foliosissima C. A. Gardner
"D. formosa R. Br.
*D.fraseri R. Br.
*D. hewardiana Meisn.
D. horrida Meisn.
*D. kippistiana Meisn.
*D. longifolia R. Br.
"D. mucronulata R. Br.
*D. nana Meisn.
*D. nivea (Labill.) R. Br.
*D. nobilis Lindley
*D. obtusa R. Br.
D. patens Benth.
D. plumosa R. Br.
*D. polycephala Ben th.
*D. praemorsa Meisn.
*D. preissii Meisn.
*D. proteoides Lindley
D. pteridifo/ia R. Br.
D. pulchel/a Meisn.
*D. quercifo/ia Meisn.
D. sclerophylla Meisn.
"D. seneciifolia R. Br.
*D. serra R. Br.
*D. serratuloides Meisn.
*D. sessilis (Knight) Domin
*D. shuttleworthiana Meisn.
*D. speciosa Meisn.
*D. squarrosa R. Br.
*D. stuposa Lindley
D. subpinnatifida C. A. Gardner
D. subulata C. A. Gardner
*D. tenuifolia R. Br.
D. tortifolia Kipp. ex Meisn.
*D. tridentata Meisn.
D. vestita Kipp. ex Meisn.
area, g1vmg rise to leaves with many small, deep, more or less symmetrical
serrations (D. preissii --+ D. shuttleworthiana Meisn. and D. obtusa R. Br. m
Fig. 35).
Some species of Banksia and Dryandra exhibit remarkable similarity m
architecture (e.g. B. benthamiana with D. concinna; Figs 34, 35). However,
attempts to combine Banksia and Dryandra species in a single system becomes
very complicated, which is to be expected since they are distinct genera, even if
they have evolved under similar conditions in Western Australia. Although the
starting points chosen (B. grandis and D. drummondii) represent leaf forms which
are very similar and which are similar to the oldest known Banksieaephyllum
species, it is not suggested that this is the only possible point of divergence
between the genera. Without a leaf fossil record for the tribe Banksieae in
Western Australia, the history of Dryandra remains conjectural.
Many of the extant species of Banksia and Dryandra fall within morphological
series, at least as far as leaf architecture is concerned. In terms of evolution
within the genera, it is important to consider whether these series may represent
evolutionary pathways. That is, are some extant species more primitive (at least
in leaf architecture) than some others? While this can only be answered
conclusively by studying the fossil record, it should be noted that in other genera
(e.g. Nothofagus Hill (1983)), it has been suggested that ancestral and derived
leaf forms currently co-exist.
222
R. S. HILL AND D. C. CHRISTOPHEL
D. hewordiono
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D. corduoceo
D.nobilis
!
-
D.bipinnotifido
D.preissli
D. drummondti
~F-J-f
D.formoso
D.shutfleworfhiono
D.nive~ ~
F-~
D. mucronu/ofo
D. orctotidis
D.obtuso
D.cuneofo
D.quercifolio
Figure 35. Diagram showing the proposed inter-relationships among selected extant Dryandra
species based on details of the leaf margin and venation pattern. D. drummondii has been selected as
a starting point.
COMPARISON OF FOSSIL AND LIVING SPECIES
There are currently 11 species of Banksieaphyllum and two species of
Banksieaiformis. Only one species, Banksieaephyllum incisum Blackburn, has been
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
223
Figures 36-38. Fig. 36. Portion of a cleared leaf of Banksia grandis. Fig. 37. Portion of a cleared leaf
of Dryandra drummondii. Fig. 38. Portion of a cleared leaf of Banksia haxteri. Scale bars = I em.
critically compared with living species (Blackburn, 1981), and even in that
instance the comparison was not comprehensive.
Among the fossil species, it is clear that there is strong similarity between
Banksieaephyllum incisum, Banksieaephyllum cuneatum and Banksieaiformis decurrens
(Figs 2-7, 30, 31). Banksieaephyllum cuneatum and B. decurrens are unlike any
extant species in having an elongate base which changes abruptly into pinnate
lobes. The leaf base of B. incisum is unknown. However, apart from the unusual
leaf base, these fossil species are very similar to a group of extant species with
pinnately lobed leaves. These species include members of Banksia (e.g. B. grandis
and B. baxteri R. Br.; Figs 36, 38) and Dryandra (e.g. D. drummondii; Fig. 37).
Banksieaephyllum attenuatum (Figs 14-16) and B.Jastigatum (Cookson & Duigan,
1950) are closely related. Both have secondary veins which terminate in small
serrations, and a single intersecondary vein between each pair of secondary
veins which branches weakly just before the margin. They also share a cuneate
base and an attenuate apex, a feature which is absent from extant species. There
are a number of differences in leaf shape and size, serration morphology and
cuticular pattern which justify their separate specific status. The stomates of
B. attenuatum are superficial, whereas those of B. fastigatum are found in slight
depressions (Cookson & Duigan, 1950), suggesting evolution in response to a
drier climate. Banksieaephyllum attenuatum may have been the precursor of
B. Jastigatum, with the former being a rainforest species and the latter occurring
in more open conditions. The venation pattern exhibited by these species is not
found in extant Dryandra species (Fig. 35), and it is probable that their affinities
lie more closely with Banksia. A number of species of Banksia from both western
and eastern Australia have a similar venation pattern to these fossil species (e.g.
B. sceptrum, B. serrata, B. burdettii; Figs 39-41 ).
Banksieaiformis dentatus (Figs 32, 33) has a similar venation pattern to
224
R. S. HILL AND D. C. CHRISTOPHEL
41
Figures 39-41. Fig. 39. Portion of a cleared leaf of Banksia sceptrum. Fig. 40. Portion of a cleared leaf
of Banksia serrata. Fig. 41. Cleared leaf of Banksia burdettii. Scale bars = I em.
Banksieaephyllum attenuatum (Figs 14-16) and B. fastigatum but the serration
morphology is quite distinct from those species and the apex is truncate.
Banksieaiformis dentata is architecturally similar to several Banksia species across
the present geographical range (e.g. Banksia serrata (Fig. 40) and Banksia burdettii
(Fig. 41)).
Banksieaephyllum regularis has well developed serrations, and has a relatively
small leaf in comparison with the species already discussed (Figs 19, 20). It
bears some resemblance to both Banksia and Dryandra species in Western
Australia, but differs in some aspects from all extant species.
Banksieaephyllum angustum from the Latrobe Valley (Cookson & Duigan, 1950)
(Fig. 42) has extremely long, narrow leaves and in this as well as serration
morphology it resembles some Banksia and Dryandra species in Western Australia
(e.g. B. candolleana Meissner (Fig. 43) and D.jormosa R. Br. (Fig. 44)). However,
no extant species has particularly close affinities with the fossil. Banksieaephyllum
acuminatum, also from the Latrobe Valley, has very unusual leaves. They are
long, narrow and tapering, with a strongly recurved margin. Few extant species
have leaves with recurved margins, and it is never seen to the extent of
B. acuminatum in an entire margined leaf. The remaining species from the
Latrobe Valley, B. elongatus, B. laeve and B. pinnatum are known only from leaf
fragments, and it is difficult to make reliable comparisons with extant species.
B. pinnatum has the pinnately lobed leaves which are now restricted to species of
Banksia and Dryandra in Western Australia, although they are of a type unknown
among extant species.
DISCUSSION
The macrofossils assigned to Banksieaephyllum and Banksieaeformis illustrate
some interesting trends in the evolution of the tribe Banksieae. The oldest fossil
TERTIARY BANKSIEAE LEAVES FROM AUSTRALIA
225
42
Figures 42-44. Fig. 42. Portion of a leaf of Banksieaeplryllum angustum. Scale bar = I em; Figs 43 and
44 are to same scale. Fig. 43. Portion of a cleared leaf of Banksia candolleana. Fig. 44. Portion of a
cleared leaf of Dryandra formosa.
species, Banksieaephyllum incisum, B. cuneatum and Banksieaeformis decurrens exhibit
most similarity with a group of pinnately lobed Banksia and Dryandra species
(e.g. B. grandis, B. baxteri, D. drummondii). This leaf form may therefore be the
most primitive and may indicate the form of the ancestral taxon from which
Banksia and Dryandra arose. An interesting feature of the fossils is that they are
widespread across south-eastern Australia and yet the extant species which they
resemble are restricted to the south-western corner of Western Australia. This
form may have been widespread prior to the formation of the Nullarbor Plain,
but at some time in the past has become extinct in the eastern half of Australia.
Many of the species found in the Latrobe Valley coal are pinnately lobed, which
demonstrates that this condition persisted at least until the Miocene in eastern
Australia.
A feature of the oldest fossil species which has no modern counterpart is an
extended entire-margined base below a pinnately lobed leaf. This occurs in
B. cuneatum, but is best developed in Banksieaeformis decurrens (the base of
Banksieaephyllum incisum is unknown). This feature could have led to the
evolution of entire margined leaves by continued loss of pinnae from the base to
the apex. However, there is no evidence among extant species for this. It is also
possible that these species represent evolutionary dead-ends, and although they
may have had a common ancestor with the extant deeply serrate species, they
are not directly related to them. Until reproductive structures are found in
organic connection with these fossils this problem is insoluble. The presence of
Banksia fruits in the Eocene of Western Australia (McNamara & Scott, 1983)
shows that the genus was extant at that time.
However, other Banksieaephyllum and Banksieaeformis fossils are only slightly
serrate, and are more similar to extant eastern Australian species. Some of these
specimens are almost as old as the pinnately lobed species mentioned above, and
226
R. S. HILL AND D. C. CHRISTOPHEL
this suggests that if all these species had a common ancestor then it must have
been well before the time of any of the fossils described here, or that evolution in
leaf form in this group was very rapid. The Tasmanian Banksieaephyllum and
Banksieaiformis fossils are quite distinct from those of a similar age on mainland
Australia. In general they are considerably smaller and less deeply toothed. This
is in keeping with the more temperate nature of Eocene/Oligocene vegetation in
Tasmania compared with mainland Australia, and the generally smaller leaf
size of angiosperms there (Hill & Read, 1987). It is therefore likely that
considerable evolution of leaf form in Banksia had taken place by the end of the
Eocene, possibly in response to a combination of climatic and edaphic effects. If
this is the case then it cannot be said with any certainty that the pinnate leaves
represent the ancestral form. It may simply be that this leaf form was common
under the conditions prevailing at the sites where the oldest fossils of this type
have been found (Deane's Marsh, Anglesea, Golden Grove, Maslin Bay).
The relationships among living species (Figs 34, 35) suggests a gradual
change in leaf form, but more fossil species from a wider geographic range and
older deposits are required to determine the ancestral form and the direction of
evolution in the group. It is clear that the subtribe Banksiinae was extent by the
start of the Eocene, and was diverse by the Oligocene. Banksia has been present
since the Middle Eocene at least, but the origins and past extent of Dryandra are
unknown. Many of the fossil species are associated with rainforest vegetation,
e.g. Banksieaephyllum regularis (Hill & Macphail, 1983), Banksieaephyllum incisum
and Banksieaiformis decurrens (Christophel & Blackburn, 1978) and Banksieaiformis
dentatus (Hill, 1984). This suggests that the modern sclerophyllous genera,
Banksia and Dryandra, may have had their origins in rainforest. This hypothesis
was first advanced by Beadle (1966), and has been reiterated by many authors
smce.
ACKNOWLEDGEMENTS
This study was supported by the Australian Research Grants Scheme. Our
thanks to Dr R. K. Crowden and Dr J. Read for collecting some of the extant
species for comparison with the fossils, and to Mr A. D. Partridge and Drs
M. K. Macphail and W. K. Harris for stratigraphic determinations.
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