Aust. J. Bot.

, 1977, 25, 655-73

The History of Ilex (Aquifoliaceae)

with Special Reference to Australia:
Evidence from Pollen

Helene A. Martin
School of Botany, University of New South Wales,
P.O. Box 1, Kensington, N.S.W. 2033.

Abstvact
Ilex is cosmopolitan excluding the arid and arctic areas and consists of some 400 species. Australia
has one species, Ilex amhemensis, which is restricted to the north.
The pollen of Ilex is very distinctive and fossil specimens can be related to it with certainty.
There is an undescribed fossil species in the Turonian (earliest Upper Cretaceous) of south-eastern
Australia, where Ilex predates the first appearance of Nothofagus. Ilexpollenites spp. are usually
present from Maastrichtian (latest Upper Cretaceous) to late Miocene. Elsewhere in the world
there are three other Cretaceous records and abundant Tertiary occurrences from every geographic
region. Ilex was cosmopolitan throughout the Tertiary and it may have been world wide in the
Upper Cretaceous also.
Ilex grows as a tree or shrub and requires a relatively wet and equable climate (with perhaps a
few exceptions). The seeds are dispersed by birds and the embryo undergoes continuous development
until germination which may take from 2 to 8 years. Such strategies must be an asset for a wide
distribution.
Previous works on modern distributions and morphology have implicated south-eastern Asia
as the place of origin of Ilex. The fossil record does not support this hypothesis although it is not
sufficient to pinpoint its origin. At the time when Ilex evolved, more equable climates extended much
further towards the poles than they do today. The south-east Asian region has had one of the most
stable climates and is a refuge for ancient angiosperms, regardless of place of origin. No doubt the
development of aridity in Australia has restricted Ilex to the north.

Introduction
The genus Ilex (Aquifoliaceae) consists of over 400 species and has a world-wide
distribution except for arid and arctic areas. Dallimore (1908) describes South
America as the headquarters of the genus, with 60 species in Brazil alone. Asia is
another important centre of distribution, with 112 species described from China,
33 from Japan, 37 from Indochina, 15 from Burma, 17 from the Malay Peninsula,
21 from the Philippines, and 45 in the Sumatra-Borneo-New Guinea region (Hu 1949,
1950). Australia has one species in the north. There are about 13 species in New
Guinea (J. S. Womersley, personal communication) and one in New Caledonia
(Guillaumin 1948).
In both ancient and modern times there has been great interest in Ilex and some
species are of considerable economic importance.
Species of Ilex figure in the folklore and legends of many countries (Dengler 1970)
and such records are additional geographic information from remote areas. Ilex spp.
and hybrids are important horticulturally and commercial holly orchards, which
supply Christmas decorations, are worth millions of dollars in the United States
 Helene A. Martin

(Roberts and Ticknor 1970). Leaves of some 60 species are used for making beverages
in South and North America, South Africa and the Chinese-Tibetan border area
(Dengler 1970). Ilex paraguaviensis St. Hil. is cultivated extensively for tea in Brazil
and Paraguay (MacMillan 1952). Because of the economic importance of Ilex,
aspects of embryology, dormancy and germination have been investigated and are
relevant here.
In contrast with many other countries with a rich floristic and cultural heritage of
Ilex, Australia is poor indeed with one little-known species restricted to the north.
This has not always been the case. Ilex has distinctive pollen that is found in fossil
microfloral assemblages from many parts of Australia. Indeed, this country has one
of the very earliest records in the world. This paper traces the history of Ilex in
Australia and elsewhere. It examines the probable origin of Ilex, its migrations and
the likely cause of the present poor representation in Australia. The fossil history has
an important bearing on phytogeography, and interpretations of origin and migrations
from fossil distributions do not concur with those based on present-day distributions.

Taxonomy
The only comprehensive systematic treatment of the genus Ilex is that proposed
by Loesener (1942), and it is generally accepted that his subdivisions of the genus
reflect natural groupings and his arrangement of the infrageneric taxa reflect natural
affinities (Baas 1973). He divided the family Aquifoliaceae into two tribes, Iliceae
and Phellineae. In the tribe Iliceae he recognizes two genera, Ilex and Nemopanthus,
and in the tribe Phellineae one genus, Phelline. The close affinities of Ilex and
Nemopanthus are beyond doubt (Baas 1975), and Clark (1974) states that '. . . there
is sentiment amongst North American workers towards abandoning Nemopanthus as
a segregate of generic status'. On the basis of pollen morphology, Erdtman (1952)
concludes that Phelline has not been placed correctly. Airy Shaw (1966) suggests
that Phelline may belong in the Araliaceae, and Takhtajan (1969) places it in a new
family, Phellineaceae. Baas (1975), from an extensive study of vegetative anatomy,
and Lobreau-Callan (1975), from studies of pollen, both support the view that
Phelline should be placed in a family of its own.
At various times, different authors have included several other genera in the
Aquifoliaceae, but it is generally accepted that they belong elsewhere, e.g. Onocotheca
(Loesener 1942; Baas 1975). The most relevant to the Australian region is Spheno-
stemon Baill. (= Phlebocalymna Griff. ex Miers, see Smith 1957). This genus has
had a confused taxonomic history and has been referred to various families by different
authors (e.g. Burbidge 1963; Airy Shaw 1966). Baas (1975) presents substantial
evidence from vegetative anatomy which indicates that Sphenostemon should be placed
in a new family, the Sphenostemonaceae.
Although the family Aquifoliaceae has been placed in different orders by various
authors, most of the evidence favours its inclusion in the Celastrales, a position
accepted by most recent authors.

Pollen Morphology
Modern Pollen
The following specimens have been examined:
Ilex acuteolata Nakai, Yi Chang District, China, W. T. Tsang 23668.
History of Ilex

I. apoensis Elm., Island of Mindanao, Philippines, D. E. Elmer 11449.

I. aquiJoliumL., cultivated, Mt. Wilson, N.S.W. (native to Europe), J. H. Maiden 10-99.
I. arnhemensis (F. Muell.) Loess., west Arnhemland, N.T., BalgooylByrnes 1367.
I. beadlei Ashe, North Carolina, U.S.A., Biltmore Herbarium No. 5831d.
I. cassine L., cultivated, Sydney Botanic Gardens (native to Florida, U.S.A.), October 1898.
I. ciliospinosa Loess., cultivated, US. National Arboretum, P. Mazzeo, 21 April 1960.
I. cymosa Bl., Bucas Grande Island, Philippines, J. Pascasio, June 1919.
I , geniculata Maxim., cultivated, U S . National Arboretum (native to Japan), F. G. Meyer,
7 April 1964.
I. mitis (L.) Radlk., Umtali District, Southern Rhodesia, N. C. Chase 3084.
I. paraguariensis St. Hil., cultivated, Brazil, B. Rambo 43968.
I. sebertii Planch. et Seb., New Caledonia, at 600 m alt., R. Schlechtev 15436.
Nemopanthus fasciculavis Rafin., West Janius, New York, K. M. Wiegand 1896.
Phelline erubescens Baill., New Caledonia, at 900 m alt., R. Schlechter 15469.
P. lucida Vieill. ex Planch. et Seb., New Caledonia, at 1200 m alt., R. Schlechter 15340.
Sphenostemon papuanum (Laut.) Steen. & Erdtman, New Guinea, J. Flenley 2657.
Sphenostemon (Phlebocalymna) Iobospora ( F . Muell.) L. S. Smith, Queensland, Atherton Forestry
Herbarium Coll. R.99.
Tournefortia hirsurissima L., La Paz, Nicaragua, C. F. Baker, January 1931.

Table 1. Dimensions (pm) of Ilex spp.

Means (in parenthesis) obtained from 20 measurements
~ -~

Polar view Equatorial view Exine only Exine plus Diam, of ornaments
Polar axis Equ. axis ornaments Max. Min.

I. acuteolata
I , apoensis
I. aquifolium
I. avnhemensis
I. beadlei
1. cassine
I. cifliospinosa
I. cymosa
I. geniculata
I. mitis
I. paraguariensis
I. sebertii
Nemopanthus fan
-

* For data on collectors, locality, etc., see text.

The pollen of Ilex is tricolporate with poorly defined pores. The pores may appear
as a constriction in the middle of the colpus (Fig. 4) or form conspicuous bulges on
fully expanded grains (Fig. 11). The shape of the grain is prolate to oblate, depending
on the degree of expansion-contraction. The grains of any one species are mainly
all prolate (or all oblate), although a few of the alternative shape can sometimes be
found. The grains are ornamented with conspicuous gemmae and clavae of variable
size, and a single grain usually has an admixture of these sculptural elements. The
largest elements are usually found over the poles or in the intercolpium (Figs. 3, 6),
and occasionally several adjacent elements are fused. The size of the elements
decreases towards the colpus, which is usually lined with a regular row of slender
clavae (Figs. 1, 6). Although the width of the elements is variable the height is fairly
uniform, so that the slender clavae are almost as tall as the large gemmae. The exine
between the ornaments may have scattered granules. Of the species examined,
Ilex aquifolium had the largest ornaments and I, geniculata the smallest (cf. Figs. 1
and 9). Table 1 presents statistics on the size of the species examined. It can be
seen that the Australian Ilex avnhemensis (Figs. 4-8) is one of the smaller species,
 Helene A. Martin

The pollen of Nemopanthus (Figs. 12, 13) is exactly like tkat of Ilex and has been
included in Table 1.
Phelline also has tricolporate pollen, but the ornamentatim is quite different from
that found in Ilex. P. erubescens has tiny, sparse spinules and P. lucida has a thick,
psilate exine (Figs. 14-18). Lobreau-Callan (1975) indicates that the exine of Phelline
is tectate, tectate-perforate, or tectate-regulate, whereas the exine of Ilex is intectate
except for some of the smaller-sized grains which may have some of the clavae united
at their heads.
Of the other genera at some time placed in Aquifoliaceae, not one has pollen like
Ilex. Sphenostemon (Phlebocalymna) lobospora is either triporate or tricolporate with
poorly defined colpi and a reticulum with sinuous muri (F'gs. 21, 22). S. papuanum
is triporate with a fine reticulate ornamentation (Figs. 19, 20).
There are no other known pollen types which could be confused with Ilex. The
closest to Ilex is Nertera depressa Banks & Sol. (Rubiaeae), which has gemmate
sculpture very like Ilex but the colpi are short, more or less confined to the transverse
colpi which are bordered by costae (Heusser 1971), and these features readily
distinguish it from Ilex. The Australian species Nertera reptans (F. Muell.) F. Muell.
ex. Benth. is psilate and totally unlike Ilex. In the Palmae, Oncosperma and Iriatrea
have clavae somewhat similar to Ilex but they are monosuloate, or rarely trichomato-
sulcate in Oncosperma (Thanikaimoni 1970; Bartlett and aarghoorn 1973). Tourne-
fortia hirsutissima L. (Boraginaceae) (Figs. 23, 24) ha; large rounded gemmae
somewhat like those of Ilex but their distribution is more irregular and the grain is
triporate. (See Nowicke and Skvarla (1974) for pollen morphology of the genus
Tourn,gfortia.) Some species of Bauhinia (Caesalpiniaceae), e g. B. emarginata Mill.,
have gemmate pollen (Bartlett and Barghoorn 1973) but this is a much larger grain
(110 pm compared with 18-38 pm for Ilex) and the apertures are uncertain. Any
pollen with a similar ornamentation can easily be separated from Ilex by other
pollen morphological characters.

Fossil Pollen
The fossil specimens studied come from bores in vestern New South Wales.
These bores penetrate sediments of the eastern part of *-heMurray Basin. Martin
(1977) has correlated the pollen assemblages from thes: sediments with the spore
pollen zones described by Stover and Partridge (1973) in the Gippsland Basin of

Figs. 1-15. Specimens of modern pollen, magnifed 1000 times.

Figs. 1-3. Ilex ayuifolium. Fig. 1 shows large gemmae and small :lavae and granules interspersed,
and the colpus margin. Fig. 2 shows the optical section of the exine and gemmae. Fig. 3, in
pclar view, shows the colpus membrane.
Figs. 4 8 . Ilex arnhemensis. Fig. 4 shows the pore region. In Fig. 5, the optical section, larger
gemmae are seen at the poles. Fig. 6 shows the alignment of clavae and granules along the
colpus margin. Figs. 7 and 8 show mixed gemmae and clavae.
Figs. 9, 10. Ilex geniculata with the smallest and most widely spaced clavae observed in this study.
Fig. 11. Ilex paraguaviensis with expanded colpi membranes and bulging pores.
Figs. 12, 13. Nemopanthus fascicularis, indistinguishable from Zlex spp.
Figs. 14, 15. Phelline evubescens with small spines.
History of Ilex
 Helene A. Martin

Victoria. Table 2 lists the bores, locations of bores, depths at which fossil specimens
have been found and the age of the sediments. The approximate locations of the
bores are shown in Fig. 33.
All the fossil grains studied are tricolporate with a weak pore (Fig. 25). Most are
prolate and are usually seen in equatorial view, although an occasional specimen in
polar view is encountered (Figs. 31, 32). The ornamentation consists of an admixture
of gemmae and clavae which are of variable size on any one grain, the largest being
Table 2. Source of fossil Ilex pollen
Depth of Age of sediments
Bore Location samples (m) (Martin 1977)

Woodside Oil Bundy 65 km SSW. of Hay 277 Early Oligocene

No. 1 Well
N.S.W. Oil and Gas 48 km S. of Hay 140-329 Mid-late Oligocene-
N. L. Stratigraphic mid EoceneB
Test Bore, Hay No. 1
W.R.C.* 3602512 27 km ENE. of Hay 137 Oligocene-early Miocene
W.R.C. 30443 1-2 km S. of
Carrathool 118-207 Oligocene-early Miocene
W.R.C. 30383 35 km SSW. of 112 Oligocene-early Miocene
Carrathool
W.R.C. 30435 25 km S. of Hay 198 Oligocene-early Miocene
W.R.C. 36078 10 km NW. of Wakool 126-348 Oligocene-Miocene-late Eocene
W.R.C. 25394 Southern edge of 115-161 Oligocene-early Miocene-
Narranderra township late Eocene
W.R.C. 36040 74 km SW. of Narranderra 137-237 Oligocene-early Miocene-
late Eocene
W.R.C. 30323 25 km N. of Jerilderie 135-239 Oligocene-early Miocene
W.R.C. 36096 16 km WNW. of Conargo 121 Oligocene-early Miocene
A Water Resources Commission of New South Wales.
The two ages refer to the upper and lower depths respectively.

1-2 ym in diameter (Fig. 27). The exine is 0.5-1 pm tkick. Dimemi~ns~f grain:
polar axis 22(28)36 pm and equatorial axis 14(20)29 pm (average of 27 spkcimens).
All the fossil specimens studied can be identified with Ilexpollenites anguloclavatus
McIntyre 1968 and I. clifdenensis McIntyre 1968, both described from New Zealand
Tertiary deposits. The two species differ in the outline of the ornament: angular on
the former and rounded to subangular on the latter. Both species, and intermediate
forms, are found amongst the fossil specimens from western New South Wales.

Figs. 16-24. Specimens of modern pollen. Figs. 25-32. Specimens of fossil pollen. All figures
magnified 1000 times.
Fig. 16. Phelline erubesceus, polar view.
Figs. 17, 18. Phelline lucida with a psilate exine.
Figs. 19, 20. Sphenostemon papuanum, triporate with a fine reticulum.
Figs. 21, 22. Sphenostemon lobospora, either tricolporate or triporate with a sinuous reticulum.
Figs. 23, 24. Tournefortia hirsutissima, triporate, with large, irregularly distributed gemmae.
Figs. 25-32. Ilexpollenites spp. Fig. 25 shows a contracted pore. Fig. 26, optical section of
average-sized gemmae. Figs. 27, 28, a specimen with some of the largest gemmae found.
Figs. 29, 30, the smallest gemmae and clavae seen in this study. Figs. 31, 32, polar view of
contracted and expanded specimens respectively.
~ i s t o r ~ : oZlex
f 661
 Helene A. Martin

The morphology of these fossil specimens falls entirely within the range of modern
Ilex spp. reported here. The size range of the fossil is greater than that of I. arnhemensis
but the mean polar axis measurements are almost the same. The ornaments on the
fossil are only slightly smaller than those of I. arnhemensis, but there is wide variation
(cf. Figs. 28 and 30).

Distributions
Present-day Distributions and Ecology
If Ilex and Nernopunthus are considered together, they have a world-wide distri-
bution excluding the arid and arctic regions. Some species grow to large trees but
others are shrubs. Many tropical species of llex are trees (Muller, personal communi-
cation). Amongst the Chinese species, the habit generally changes from a tree to a

Fig. 33. The distribution of Ilex. Localities for Ilex arnhernensis in Western
Australia and the Northern Territory are from herbarium specimens. See
text for discussion of I. amhemensis in Queensland. Mr J. S. Womersley
kindly supplied the data for the distribution of Ilex spp, in New Guinea
(see Table 2 for the species). Fossil localities : 1, Martin, this paper; 2, Stover
and Partridge (1973); 3, Harris (1970) and personal communication;
4, Hekel (1972); 5, Hos, personal communication.

shrub with increasing altitude and there are three species which are prostrate or
creeping in the subalpine flora of Yunnan (Hu 1949). At least one species from the
Philippines is a climber (Baas 1973).
It is probably imprudent to generalize about the ecological requirements of such a
large and widely distributed genus, but Ilex does seem to require an adequate humidity.
History of Ilex

Ilex usually occurs in forests or damp woodlands and surprisingly many species are
associated with wet places such as swamps, bogs, along stream margins and the
edges of ponds. For example, Correll and Johnston (1970) lists 10 species of Ilex
from Texas, six of which are found in wet habitats though not necessarily restricted
to these places. Van Steenis (1965), in describing the lowland swamp forests of Java,
includes I. cymosa as one of the dominants. The European I, aqufolium is thought
to require an oceanic climate (Peterken and Lloyd 1967). In the vegetation of
Veracruz, Mexico, Ilex spp, occur in the deciduous forests restricted to the temperate
and more humid regions where fogs are frequent. Ilex is also found in several kinds
of 'selvas' (rain-forests), including mossy forest; it does not occur in any of the drier
vegetation types (G6mez-Pompa 1973). The only report of Ilex being found in any
sort of dry environment is that of I.jenmanii in the savannah vegetation of Surinam
which has a pronounced dry season (Muller, personal communication).

Table 3. The New Guinea species of IIex

Data kindly supplied by Mr J. S. Womersley

Name No. of Altitude Habitat

collections (m)

I. avchboldiana Alpine shrubbery. High montane cloud forest.

Montane forest and forest understorey. Upper
mid-mountain rain-forest. Grassland border of
moss forest. Ridge crest and ridge forest
I. avnhemensis Swampy savannah. Edge of sago swamp.
Peat swamp. Swampy lake. Swamp
I. aff, brassii Valley swamp forest. Mid-mountain rain-forest.
Rising ground.
I. cymosa Rain-forest on gentle slope. Spur, dense forest.
Ridge forest
I, forbesii Rain-forest on gentle slope
I. glomevata Savannah
i. iedevmanii Ridge and ridgt: top
I. scabvidula Mossy forest
I. spicata Ridge
I, vevsteeghii Valley forest. Montane and lower montane
rainforest. Impoverished montane forest.
Deforested slopes and disturbed forest.
Mossy forest. Mixed riverine forest
I. vitiensis Santa Cruz group only. Ridge forest.
Spur, dense forest

The Australian Ilex avnhemensis is a tree up to 21 m in height and found in

riverine or swampy lowland forests (Blake 1954). In the Northern Territory it has
been seen growing in shallow running water, and all the records are from perennially
wet rain-forest, as distinct from the seasonally dry monsoonal forest (C. Dunlop,
personal communication). In Queensland it is not found south of Rockingham Bay
at lat. IS0 10's. (Blake 1954). In the Atherton region it occurs up to an elevation of
680 m (B. Hyland, personal communication). It is also found in northern Western
Australia (Blake 1954). The recorded distribution is shown in Fig. 33, but not being
 Helene A. Martin

a well-known, common or conspicuous species it is likely to have a wider distribution

in northern Australia (C. Dunlop, B. Hyland, personal communication). There may
be a second undescribed species of Ilex, but it does not occur outside the range of
I. arnhemensis (B. Hyland, personal communication).
There are about 11 species of Ilex recorded in New Guinea and the nearby island
group to the east, and I am indebted to Mr J. S. Womersley for the following infor-
mation. Table 3 lists the species, their altitudinal range and habitats, as recorded on
the herbarium sheets. Some species have a restricted altitudinal range but the genus
as a whole has very wide limits. In New Guinea Ilex spp. are usually found as small
trees in the understorey and are often associated with deforested areas, e.g. alpine
shrubbery, and the borders of forest with grasslands or swamps. In the exceptional
cases when Ilex is cited as being present in dense forest, it is usually found on the
ridge tops. Table 3 shows that I, amhemensis, the Australian species, is the lowland
swamp species in New Guinea.

Distribution of Fossil Ilex

In western New South Wales, fossil Ilex, as Ilexpollenites anguloclavatus and
I, clifdenensis, is found in sediments that are middle-late Eocene (the oldest in this
part of the Murray Basin) to Oligocene-early Miocene. The assemblages in which
it is found are floristically rich and contain at least 70-80 different pollen species.
Nothofagus is the most abundant pollen type, and although Ilexpollenites rarely
accounts for more than 2-3 % of the total count it is frequently present. Modern Ilex
is a low pollen producer: it is insect-pollinated and very little pollen is found in the
atmosphere (Hyde 1961). With pollen behaviour such as this, a consistent presence
in the fossil assemblages would indicate that it was a relatively important member of
the ancient flora, although its pollen is only found in low frequencies. These assem-
blages are found in lignites and carbonaceous clays, and there is abundant evidence
that these deposits formed in swampy conditions in a very humid climate. Ilex-
pollenites has not been found in any of the middle Miocene or younger assemblages
that were deposited after lignite fc~rmationhzd ce~sed. These ycmge: assembiages
contain much less Nothofagus (or none at all), and all the evidence indicates that the
climate had become less humid (Martin 1977).
Elsewhere in Australia Ilexpollenites anguloclavatus is found in the Gippsland
Basin of Victoria from the Tvicolpites longus zone of Maastrichtian age (Stover and
Partridge 1973; Partridge 1976) into late Miocene strata (Partridge 1971 and
personal communication). Tetracolporites verrucosus Stover (Stover and Partridge
1973), a Maastrichtian to middle Paleocene species, has ornamentation very like Ilex,
but differs in that it is tetracolporate. There is an undescribed and unpublished
species of Ilexpollenites in the Clavifera triplex zone (Turonian or earliest Upper
Cretaceous) in sediments of south-eastern Australia. I am indebted to Mr A. D.
Partridge for showing me some of these specimens. They are tricolpate, possibly
with weak pores, although it is not possible to detect them on some specimens, and
the ornamentation is distinctively that of Ilex. There is a mixture of different-sized
gemmae, with the larger ones over the poles, and a few adjacent gemmae and clavae
are fused at the top.
In South Australia Ilexpollenites is ubiquitous throughout all the basins which
have middle Eocene to early Tertiary assemblages. These include the Eucla, Eyre
History of Ilex

Peninsula, St. Vincent, Pirie Torrens, Great Artesian, Murray and Otway Basins
(Harris, personal communication). In Western Australia IlexpolIenites angulocIavatus
is rare in middle to upper Eocene assemblages at Albany, Nornalup, Lake Lefroy
and Fitzgerald River (Hos, personal communication). In Queensland Ilexpollenites
sp. has been reported from undifferentiated Lower Tertiary and Oligocene deposits
(Hekel 1972). These localities are also shown in Fig. 33.
Fossil Ilex pollen has been recorded from many parts of the world. Pollen
identifications recorded in the literature should be treated with caution, but Ilex
pollen is so distinctive that it is easily checked from descriptions and photographs.
When dexcribed under form-generic names, most authors assign it to either Ilex or
Aquifoliaceae, so that identification is made by the original author. Extra-Australian
occurrences are listed below.
NEW ZEALAND: McIntyre (1968) described three species of Ilexpollenites in deposits of middle
Eocene to Miocene age. Ilex is not present in New Zealand today and the nearest occurrence is in
New Caledonia (Guillaumin 1948).
AFRICA: There is a report of a probable Pliocene occurrence of Ilex at Burundi (Sah 1967; from
Muller, personal communication).
BORPIEO: A pollen form found in Senonian (late Cretaceous) and early Tertiary deposits has been
described as Genmatricolpites pergemmatus (Muller 1968). It has smaller and less well-developed
clavae than most modern species of Ilex but is regarded as a possible forerunner of Ilex (Muller
1968). In a comparison of a Holocene peat and a Miocene coal deposit from NW. Borneo the
similarity is remarkable, and Ilex pollen occurs in both. Three species of Ilex were found growing
in the swamps of the region (Anderson and Muller 1975).
INDIA: Ilex pollen has been found in a Tertiary brown coal at Neyveli, 237 km SSW. of Madras
(Thiergart and Franz 1963).
MAINLAND CHINA: Ilex is prevalent in older Tertiary deposits, especially Oligocene, but it is
lacking from the younger Tertiary (Kung Zhao-Chen, personal communication).
JAPAN: Ilex spp. are found in Eocene to Oligocene strata in the Hokkaido region (Tokunaga
1964) and in a lower Oligocene coalfield in North Kyushu (Takahashi, in Krenlp 1964). They are
not recorded in Upper Cretaceous assemblages of the Hokkaido region (Takahashi 1964). Pliocene
lignites from the Sendai and Shinjo districts have also yielded Zlex pollen (Shimada 1951; Shimada
atld Takahashi 1952). Leaves are fonnd in macrofossil asrcmblages of Upper Eocene through to
the end of the Pliocene age (Tanai 1972). Species of Ilex are found in practically every floral province
in Japan today, from the warm temperate evergreen forests in the south to the Sphagnum peat bogs
in the north (Hara and Kani 1959).
U.S.S.R.: Ilex uvalensis has been described from the Cenomanian of the south Urals (Bolchovitina
1953). There are many occurrences of Zlex in the Tertiary sediments of the U.S.S.R. that have been
reviewed by Andreeva et a / . (translated by Neves and Downie 1970). llex is found in Paleocene
and early-mid Eocene deposits which are limited to Europe, the Urals and Western Siberia. These
assemblages are all of the European type. One Eocene assemblage from the South Maritime province
of the Far East contains Ilex. Miocene and Oligocene sediments are more common and are found
in the East European, Urals, Siberian, Kazakhstanian and Far Eastern Provinces. Ilex is usually
present in these assemblages. There are a few Pliocene assemblages which contain Ilex.
EUROPE: There are many reports of Zlex-type pollen, most of it in the brown coals of Germany,
Denmark and Poland. Ages range from one probable Paleocene-Eocene occurrence (Thompson
and Pflug 1953) to many Eocene-Pliocene records (Potonie 1960; Thompson and Pflug 1953;
Meyer 1956; Macko 1957). Most authors describe more than one form-species in the material under
study. Ilex leaves have been found in a Miocene flora of Western Germany (Ferguson 1971).
ICELAND: Fossil wood of Ilex from the Pliocene of Iceland has been described (Schonfeld 1956).
NORTH AMERICA: In Alaska, leaves and pollen of Ilex are found in Oligocene and early Miocene
sediments (Wolfe 1972). Two form-species of Ilex have been found in the latest Miocene or early
 Helene A. Martin

Pliocene of the Queen Charlotte Islands, north-west Canada (Martin and Rouse 1966). Ilex occurs in
the Oligocene to Pliocene deposits of Oregon and in the Miocene of northern California, Washington
and Idaho (Gray 1964). It is also present in the Eocene of the Rocky Mountains (Leopold and
MacGinitie 1972), Tennessee (Elsik and Dilcher 1974), Alabama (Gray 1960), in a mid-Tertiary
(possibly Oligocene) lignite of Vermont (Traverse 1955) and in the Miocene of Maryland (Leopold
1969). In deposits of the Gulf coast of Texas, Ilex-type pollen is present in the Paleocene, and it
increases in relative abundance in the upper Eocene (Elsik 1968). Chmura (1973) reports Ilex-
pollenites from the Campanian through Maastrichtian (Upper Cretaceous) of the San Joaquin Valley,
California.
SOUTH AMERICA: Probable Ilex pollen has been reported from lower and middle Eocene deposits
in Colombia. Such types are frequent in the Tertiary of Venezuela (Muller, personal communication).
Ilex has been found in Oligocene deposits of Puerto Rico (Graham and Jarzen 1969).
This review of the fossil record of Ilex throughout the world is almost certainly
incomplete, but it is sufficient to show that Ilex was cosmopolitan through most of
the Tertiary and had evolved by the beginning of the Upper Cretaceous.

Origin and Migration

The Origin o f Ilex
Many workers have tried to solve by a variety of methods the irresistible problem
of what is the exact place of origin of a taxon. The origin of Ilex is examined from
two angles: the fossil evidence and morphological studies of modern species.
As listed in the preceding section, there are four records of Ilex in the Cretaceous:
U.S.S.R., south-eastern Australia, north-west Borneo and California. Unfortunately,
Cretaceous stratigraphy and dating is not sufficiently precise to allow correlation on
a world-wide basis simply on the reported ages of these four occurrences. These
Cretaceous records simply indicate that Ilex is one of the older angiosperms and that
it was probably world wide in the Cretaceous. No doubt Ilex will be found in
Cretaceous sediments in other parts of the world. It is possible, however, to place Ilex
in the Australian record of the evolution of the angiosperms. The oldest angiosperms
in Australia are middle Albian (Dettmann 1973). The first record of Ilex is Turonian.
X ~ t h ~ f i i g -does
~ i ~ i i O i appear until the iv'odzofagidites senectus zone of Santonian age
(Stover and Partridge 1973; Partridge 1976 and personal communication). Hence
Ilex predates Nothofagus.
Many evolutionary postulates have been based on studies of extant taxa arranged
according to a series, from simple to complex, which is usually interpreted as primitive
to advanced. Ilex has been treated in this fashion. Lobreau-Callan (1975) found
that there is an increase in size of pollen grains through the series when arranged
according to Loesener's (1942) classification, which is accepted as a natural arrange-
ment (see Taxonomy). In general, the species at the beginning of Loesener's series
have smaller grains than those at the end of the series. When the geographical location
of these species is considered, several gradients in the size of pollen grains can be
discerned. The species with small grains are far more numerous in the south-east
Asian region, with a trend to larger grains across the Pacific, the largest of all occurring
in North America. There is also a latitudinal gradient; species near the equator
have smaller grains, and grain size increases with latitude. Apparently this same
gradient in size of pollen grains is evident with altitude. The species a t lower altitudes
have smaller grains than those at higher altitudes. On this evidence, Lobreau-Callan
postulates that south-east Asia, and probably the area from Malaysia to New Guinea,
History of Ilex

was the place of origin of Ilex. This hypothesis does not take into account climatic
factors. The south-east Asian area has been one of the most stable climatically, and
this region can be considered to be a relic of a humid type of climate that seems to
have been world wide in the late Cretaceous and early Tertiary (climate is discussed
in a later section). For this reason the more ancient forms may have been able to
persist unchanged in the stable south-east Asian region, whereas climatic changes in
the higher latitudes have forced evolutionary changes, including a change in pollen
size. While the Cretaceous records of Ilex do not disprove Lobreau-Callan's
hypothesis, they do not support it either. The latitude of the Turonian south-eastern
Australian Ilex was 60-65"s. on Cretaceous paleogeography, and a long way from
south-east Asia.
Latitudinal gradients have been demonstrated in the wood anatomy of Ilex
(Baas 1973). For example, the vessel members are longer in tropical lowlands and
shorter in temperate regions. Where scalariform perforations are present, the highest
number of bars are found in tropical lowlands and the numbers decrease with altitude
and latitude. These gradients are often interpreted as phylogenetic, the more primitive
features being found in the tropical lowlands. Baas, however, is inclined to attribute
these gradients to some adaptive significance as they parallel the climatic gradient,
and the same anatomical gradients have been found in the wood anatomy of several
other taxa. Moreover, when the species are arranged in a series according to their
wood anatomy, this series does not closely parallel the classification proposed by
Loesener (Baas 1973). Unlike Lobreau-Callan, Baas is not inclined to use his
latitudinal gradient as evidence of the place of origin of Ilex.

Seed Dispersal: the Basis of Migration

Plants can migrate only through the dispersal of seeds (or other propagules) and
the establishment of seedlings. How this is achieved will have a great influence on
the rate and direction of migration.
There is abundant evidence that Ilex is dispersed by birds (Ridley 1930; Pijl 1972).
The hard seeds are embedded in a pulpy berry that is usually red, pink, yellow or
v l a ~ k . Red is lij: fzr the moat common co!=ur: c. 95 "/, ef the Chinese species have
Ll--

red berries (Hu 1949). There are numerous eyewitness accounts of birds eating
berries, and the depredations of birds is one of the problems of holly orchardists
(Roberts and Ticknor 1970).
The seeds of Ilex pass through the gut of the bird unharmed and then germinate
sooner than if they had not been eaten (Hyde 1961). Horticultural experience shows
that seeds of many species of Ilex take a long time to germinate. For example,
I. aquifolium requires 2 or 3 years and Dallimore (1908) advises mixing the seed with
sand and leaving the mixture exposed to the weather for 12 months. The seeds are
then planted out and after another 12 months the seedlings appear. Ives (1923)
found that the embryo is immature when the berry falls off the tree and undergoes
continuous development until the time of germination. The development of the
embryo can be hastened by the presence of a sugar, especially glucose, at about
5 % concentration. Germination is aided by the decay or removal of the hard seed
coat, which the young hypocotyl is incapable of penetrating (Ives 1923). Hartline
(1970) points out that it is time or aging, rather than any cold treatment, which aids
germination. Neal and Dye (1964) describe a method for studying dormancies of
holly seeds, which require 8 years to germinate! However, not all species are slow
 Helene A. Martin

to germinate: according to Hartline (1970) the seeds of some species sprout after a
short time if handled correctly, but the 'correct' handling is not specified.
Throughout its Tertiary history in Australia Ilex is found associated with Notho-
fagus. The mechanisms of dispersal and speed of germination of the seed of these
two genera are in complete contrast. Nothofagus produces small nuts equipped with
little wings, but dispersal rarely exceeds 200 m under field conditions (Wardle 1970).
Birds are not imporant as dispersal agents. Finches eat the seeds, but the kernels
are digested. Some water transport downstream from the seed source may occur,
judging from riparian stands. Seeds are shed in autumn and some may germinate
then, but seeds which survive the winter germinate en masse the following spring.
Once the seeds dry out they will not germinate, and if storage is necessary the seeds
must be stored damp at about 6 % moisture content. Seeds rarely remain viable for
more than 1 year under field conditions (Wardle 1967, 1970; Howard 1973).
Dispersal of seeds by birds and longevity of seed must allow a much wider distri-
bution than could be achieved by taxa lacking these attributes. This topic will not be
pursued other than to suggest that different methods of seed dispersal and germination
will produce different migration abilities and can result in very different patterns of
distribution; in this case, a cosmopolitan Ilex and a restricted 'Gondwanan' Notho-
fagus (Couper 1960; Cranwell 1964). In using this hypothesis I have assumed that
behaviour with respect to seed dispersal and germination has remained much the
same throughout the history of these genera, a period of some 90 million years.
The available evidence does not contradict this assumption for these two genera.

Climatic Change in Australia: the Cause of Present Distribution Patterns

The most striking feature of the distribution in Australia of the fossil Ilex is its
disappearance from the south-east in the Miocene. Unfortunately there are no data
concerning the distribution of Ilex in Australia from late Miocene time to the present.
Zlex is not the only taxon to show this kind of distribution. The mid-late Miocene
was a time of profound change, when Nothofagus and many other taxa disappeared
from the fossil record in south-eastern Australia (Martin 1973, 1977; Stover and
Partridge 1973). Thereis every indicaiioii ijiiS tiiiie of was
with a marked decrease in humidity. From mid Eocene to early Miocene there was
extensive deposition of lignites and carbonaceous clays that must have been deposited
under a very wet climate. To judge from the present requirements of Nothofagus
(Martin 1969), the annual rainfall was at least 180 cm, and could have been very much
more. After the change, Myrtaceae and Casuarina dominate the pollen assemblages
and herbaceous taxa are present though not abundant. These assemblages probably
represent a drier kind of forest with a rainfall of c. 150-180 cm fairly uniformly
distributed through the year. In the late Pliocene, restricted numbers of the lower
Tertiary taxa, including two of the three pollen types of Nothofagus, reappear in
western New South Wales. It is thought that the remnants of the lower Tertiary
flora existed in small refuge areas in the eastern highlands and migrated westward
when the climate became wetter for a relatively brief interval in the late Pliocene.
Ilex, however, has not been found in the late Pliocene assemblages (Martin 1969,
1973, 1977).
There is every indication that aridity increased subsequent to Pliocene time.
In western New South Wales grasslands developed about Pleistocene time, and the
climate became more seasonal, with a well-marked dry period (Martin 1969). From
History of IIex 669

the reconstructions of Nix and Kalma (1972), aridity was intensified during the glacial
events of the Quaternary and closed-forest would have been eliminated from all but
locally favourable sites in north-eastern Australia at the time of the last maximum
lowering of the sea level. Closed-forest remained dominant over the major part of
New Guinea, which was then joined to the Australian mainland. As a result of these
periods of intensified aridity, Ilex could have been eliminated from the Australian
mainland or else restricted to very local favourable sites. Its present distribution
results from either expansion of these local sites or migration from New Guinea (or
perhaps a combination of both). It appears that the Australian stock of Ilex was
unable to cope with even moderate aridity, as evidenced by the present restriction of
llex amhemensis to permanently wet sites.

Discussion
This study of the history of Ilex shows clearly that present distributions are no
indication of past migrations. Taxa such as Ilex, with a distribution restricted to
northern Australia, are often thought to have migrated into Australia via Malaysia
and Indonesia, especially if the taxa under consideration are more abundant and/or
diverse in these islands. However, the taxa of the Malaysia-Indonesia-New Guinea
region require a humid tropical climate, and as the only parts of Australia with this
climate are in the north and along the north-east coast these taxa are restricted by
the climate and not by migrations. The fossil record shows conclusively that Ilex
was present in Australia in the earliest part of the Upper Cretaceous, long before the
interconnecting island chain was established with south-east Asia (about mid-Tertiary
time).
Earlier workers have proposed the south-east Asian area as the likely place of
origin of Ilex. The fossil evidence does not disprove this hypothesis but neither does
it substantiate it. Two of the earliest Cretaceous records are from high latitudes (on
Cretaceous palaeogeography), viz. south-eastern Australia and the U.S.S.R. Its origin
in south-east Asia is based on the high concentration of 'primitive' species there, but
Ilex is an ancient taxon and could be restricted to the type of climate under which
it e-dved, regardless. ~f place ~f erigir,.
There is abundant evidence of climatic change on a global scale during the Tertiary.
Tropical and subtropical climates extended much further towards the poles than they
do today. The climatic deterioration started about Upper Eocene time, and changes
have been greatest in the high latitudes (Frakes and Kemp 1973). Much of the early
angiosperm evolution occurred under a more equable climate, whether it took place
in the high or low latitudes. The taxa which were intolerant of climatic change were
forced to migrate or be exterminated. The south-east Asian area has probably had
one of the most stable climatic histories and can be considered a relic of a more
widespread climate, so it is not surprising that the ancient forms of llex (and other
angiosperms) are concentrated there. In Australia the development of aridity has
rendered most of the continent unsuitable for Ilex, especially during the glacial
periods of the Pleistocene when aridity was intensified.
In the past, plant geographers have deduced origins and migrations largely from
present distributions. Thus Good (1964) regards the Aquifoliaceae as a tropical
family, of which one species, Ilex aquifolium, reaches north-west Europe because of
the ameliorating influence of the Gulf Stream. AubrCville (1976) considers the same
distribution patterns, but with the benefit of the European Tertiary fossil record.
 Helene A. Martin

He thinks that Ilex is a Laurasian element which has migrated into the tropics,
'fleeing' the cooling climate. Croizat (1952) depicts very complex migrations of Ilex.
In discussing the 'knottiest problem', how Ilex reached the New World, he concludes
that '. . . Ilex was invading the New World full blast in remote ages, so doing from
three directions simultaneously, (a) the modern Atlantic . . . directly from the African
gate, meaning. . . the ancient continent of Gondwana; (b) the modern Northern
Pacific. . .; (c) the modern Southern Pacific . . .'.
While there are elements of truth in each of these phytogeographic interpretations,
this study shows that it is impossible to place the origin of Ilex from present-day
distributions. Unfortunately the fossil record is not sufficient to pinpoint the origin
and migrations of Ilex either, but Croizat's concept of a very ancient taxon and
complex migrations is probably nearest the mark, and AubrCville recognizes the
importance of changing climate. Burbidge (1960), in her study of the phytogeography
of the Australian region, recognizes a relic element which had a wider distribution
in the past but which is now restricted to northern Australia and north-east Queensland.
Ilex fits this concept of a relic.
Bird dispersal of the seeds and the slow germination of Ilex probably account for
its cosmopolitan distribution and may well be the solution to Croizat's (1952)
'knottiest problem'. It is not clear why Ilex should be unable to tolerate even mild
aridity (with perhaps the exception of a few species) unless the embryo, which
undergoes continuous development until the time of germination, is intolerant of
desiccation during this period. In contrast, the restricted 'Gondwanan' distribution
of Nothofagus probably results from seeds which remain viable for less than 1 year
and which are digested if eaten by birds. The seeds of Nothofagus do not germinate
if they dry out, and this behaviour undoubtedly restricts it to the wetter climates.
In conclusion, Ilex is a very ancient taxon which first appears about the beginning
of the Upper Cretaceous in geographically distant parts of the world. One of the
very earliest occurrences is in south-eastern Australia, and Ilex predates Nothofagus
here. It has had a cosmopolitan distribution throughout its long history. Changing
climate has restricted its distribution for it appears to be intolerant of aridity, with
perhaps a few eiiceptioiis. Tire deveioprnenr of aridity in Australia is thought to have
resulted in the restriction of Ilex to the north. The mechanisms of seed dispersal
and seedling establishment may account for observed migrations and distributions.

Acknowledgments
I wish to thank Mr J. S. Womersley, formerly of the Division of Botany, Depart-
ment of Forests, Territory of Papua and New Guinea, Mr C. R. Dunlop of the
Department of the Northern Territory, and Mr B. P. M. Hyland of the Queensland
Research Station, Forestry and Timber Bureau, who have provided invaluable
information from their personal experience. Professor R. S. Clark, of Erskine College,
South Carolina, U.S.A., and Dr J. Muller of the Rijksherbarium, the Netherlands,
have provided invaluable comment and information. I am indebted to Messrs A. D.
Partridge and Esso Australia Ltd., and W. K. Harris and D. Hos of the Department
of Mines, South Australia, who have kindly allowed me to quote some of their
unpublished work. The staff of the National Herbarium, Sydney, have been most
helpful with reference pollen. The Australian Research Grants Committee has
provided some financial assistance.
History of Zlex

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Manuscript received 3 June 1977