Botanical Journal o f f h e Lmnean Socie!v of'London (1982) 85: 75-88. With 3 figures
The biogeography of Nothofagus and
Trigonobalanus and the origin of the Fagaceae
R. MELVILLE, F.L.S.
Royal Bolanic Gardens, K e w , Richmond, Surrey TW9 3DS
Jub 1981
ReceiLied .\lay 1981. accepted f o r pubhation
The suggestion that Trigonobalanu~excelsa reached Colombia by migration from south-east Asia via the
Bering land-bridge is criticized. The distribution of 'Trigonohalanw can be more simply explained hy the
disruption and drift of the former Pacific continent and the peninsula of West Gondwanaland. All but
the New Guinea species of.Vothofagusremain on the drifted fragments of the Gondwana peninsula, the
original home of the family. DriFt accounts for the present disjunct distribution of related .VothofaguJ
species in the Southern hemisphere, but topoclines in characters of the fructifications and of the leaves
linking New Zealand, New Caledonia and New Guinea indicate the overland migration route into the
Pacific continent, Diversification of the family occurred in Pacifica before that continent was disrupted
in the late Jurassic. With the formation of Eurasia, a topocline in leaf characten developed in Fagus
along the migration route from China to Western Europe. Absence of topidines involving the Bering
land-bridge indicate that this bridge played no significant part in the dispersal of the Fagaceae.
Shedding of the fruits of Glossopieris before the development of an embryo draws attention to the
primitive character of delay in fertilization found in .Vothofagus.
KEY WORDS :-Biogeography
.Vothofagu! Pacifica topocline
~
disjunct distribution
continental drift
Trigonobalanus.
Fagus
Fagaceae
~
CONTENTS
Introduction . .
Palaeogeography .
Origin of Fagaceae.
Acknowledgements .
References. . .
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75
76
78
87
87
INTRODUCTION
The discovery of a third species of Trigonobalanus in Colombia by Lozano-C.,
Hernandez-C. & Henao-S. ( 1979) was an event of considerable phytogeographical
interest, extending as it did the range of this relatively primitive genus of Fagaceae
across the Pacific into South America. I n a subsequent paper, Hernandez-C.,
Lozano-C. & Henao-S. (1980) have discussed the origin of Trigonobalanus and of
the Fagaceae in general. They follow a widely accepted opinion that the
angiosperms originated in south-east Asia (Thorne, 1963; Takhtajan, 1969;
Smith, 1973) and assume, that when the Bering land-bridge became available in
the Pliocene, as suggested by Raven & Axelrod (1974) Trigonobalanus migrated
northwards and passed into North America and then along the Panama isthmus
0024--4074/82/060075+ 14 $03.00/0
6
15
0 1982 The Linnean Society of London
76
R. XIELVILLE
into South America. Against this possibility is the lack of any evidence, litring or
fossil, for the presence of Trigonobalanus in North America. The conclusion reached
by Hernandez-C. et al. ( 1980) rests heavily on the views ofRaven & Axelrod ( 1974).
There is no fossil record for the Fagaceae in India or in Africa south of the Sahara.
A single pollen record for .Vothofagus on the Cape flats is best accounted for by
wind transport from South America, as suggested by Raven & Axelrod. They are
at a loss to account for the presence of .Vothofagus in the Southern hemisphere in
spite of the well-established occurrence of .VothoJagus pollen in Australia, New
Zealand and South America in the Cretaceous. Nevertheless, they hazard a guess
that there was a mid-Cretaceous migration of an ancestral group from southern
montane Eurasia into Austral regions via Africa or India. This concept must be
rejected, for i t is not supported by fossil evidence and it cannot be reconciled with
the known timing of continental drift in the regions involved. The present
distribution of the family, with a high concentration of both genera and species in
south-east Asia, indicates that this region was an important centre for adaptive
radiation. Qutrcus subgenus Quercus has a circum-boreal distribution with a high
concentration of species in China, which has served as a secondary centre of
diversification for the subgenus.
PALAEOGEOGRAPHY
Controversies of the kind outlined above were unavoidable so long as the
progenitors of the angiosperms remained unidentified. Not until the
Glossopteridae had been identified as the parent group was it possible to be certain
that the angiosperms first arose in the former super-continent of Gondwanaland.
Indications that this might be so came with the enunciation of the gonophyll
theory (Melville, 1962, 1963) and the realization that the fructifications of the
Glossopteridae were gonophylls. Many new kinds of glossopterid fructification
have been discovered during the last 30 years and some of these have been
recognized as similar to component units of angiosperm flowers. Confirmation
came from the discovery of a few angiosperms with leaf architecture differing little
from either Gangamopteris or Glossopteris and evidence that the leaves of at least 120
angiosperm families were derived from these fossil forms (Melville, 1970, 197 1 ) .
Then came the discovery of a petrifaction of a glossopterid fructification from the
late Permian of Queensland (Gould & Delevoryas, 1977) in which orthotropous,
unitegminous, crassinucellate ovules were enclosed in typical angiosperm fashion
by the enfolding of a leaf-like organ having the structure of a gonophyll. One of the
principal stumbling blocks to the recognition of this relationship had been the
carpel theory (Eames, 1961).AlthoughThomas (1958) had realized that theremains
of angiosperm ancestors may have been found but not recognized he failed to
recognize that Scutum and Ottokaria, then recently described by Plumstead (1956),
bore any relationship to angiosperms. Finally, the Ranunculaceae provided
anatomical and developmental evidence for the fallacy of the carpel theory
(Melville, in press).
It had long been known that many genera occurred in both eastern Asia and
North America and that numerous species pairs were distributed vicariously on
either side of the Pacific. Van Steenis (1962) had attempted to explain these
distributions on the basis of a series of land-bridges across the Pacific, but there is
no geological evidence for this and no mechanism is known that could account for
ORIGIN OF FAGACE.4E
77
their de\,elopment. hlost authors, assuming an origin in south-east Asia, have
postulated a northward migration followed by a crossing of the Bering Strait and a
southward migration in North America. Although the Bering Strait was closed
intermittently during the Tertiary, its importance as a plant migration route has
been grossly overrated (Hulten, 1928; Colinvaux, 1964). If this had been the
principal migration route there should be evidence for adaptation to colder
climates on the northward migration and then a readaptation to warmer
conditions on the southward migration in America. Clinal variation along the
proposed migration route should be evident on this basis, but is not observed.
Instead, trans-Pacific distribution of vicarious species pairs at the same level of
e\rolution is the dominant phenomenon and this is not consistent with the use of the
postulated migration route. A third possibility is continental drift.
With the acceptance of sea-floor spreading and continental drift it was evident
that the continental fragments would bear away representative portions of entire
floras and faunas. Species distributions would be cut in two and the separated
populations, in the course of time, would differentiate to the species level or above
and so gi\.e rise to vicarious pairs. Chance long-distance dispersal across the
breadth of the Pacific is incapable of explaining the many vicarious distributions
ohserired. Only continental drift can account for this. Evidence of sea-floor
spreading in recent years, combined with geological evidence from the continents,
enabled the reconstruction of the Pacific continent of the Mesozoic (Melville,
1981i . O n e conclusion of great biological significance arising from this
investigation was that the Greater Antilles had formed a part of Pacifica and that
in the Palaeocene they had made contact with South America forming a landbridge along which early marsupials and notoungulates passed into South
,lmerica. Continued drift broke this land-bridge and the present Panamanian
Isthmus was not brought into contact until the Pliocene, after a lapse of about
50 My.
The reconstruction of Pacifica did not at once explain how the Fagaceae and
other angiosperms had reached that continent. It was necessary to study the
reconstruction of Gondwanaland and the evidence for its disruption and drift.
Current reconstructions of Gondwanaland showed the southern tip of South
America overlapping on Antarctica and pointed to an error. This was corrected
when it was found that southern Chile with Patagonia-here called Magellaniawere not glaciated in the Permo-Carboniferous ice-age, when the ice cap extended
from Brazil southwards over Antarctica. Both Magellania and Peru are marked off
from the rest of South America by bands of marine Jurassic strata and must have
been somewhere to the west of their present position in the Permian. These two
regions and the West Antarctic Peninsula reached their present positions at about
the beginning of the Oligocene (38 My) and by this time Australia was in contact
with New Guinea. Australia and Antarctica separated early in the Eocene (50 My)
(Heirtzler et al., 1973). There never was a period when South America was in
direct contact with Antarctica and all claims for a migration route from South
America through Antarctica to Australia must be rejected. When allowance is
made for the eastward drift of Australia and Antarctica starting in the Upper
Jurassic (140 My) (Heirtzler et a/., 1973) and the rotation of Antarctica
subsequent to its separation from Australia (Blundell, 1962), it is concluded that in
the Permian, western Antarctica projected northwards a t about 170" W longitude
and formed a peninsula of West Gondwanaland together with New Zealand, New
78
R . MELVILLE
Caledonia and associated islands and Peru and Magellania. West Gondwanaland
was then situated directly to the south of Pacifica and separated by a relatively
narrow strait of the Tethys Sea. Towards the end of the Permian, uplift marking
the onset of the orogenesis closed the strait and provided a land-bridge across
which Glossopteris was able to migrate into New Guinea and Thailand as testified
by fossils (Asama, 1966). Land connection was broken when Australia and
Antarctica began to drift to the east (140 My), but by this time early angiosperms
were already established in what was to become south-east Asia and the rift valley
phase of the orogenesis was well advanced. The rift valley produced a greatly
diversified topography with rapidly changing, ecological conditions which
stimulated a rapid burst of evolution. When finally the rift valley opened and drift
began (150 My) (Larson & Pitman, 1972) many angiosperm families were wellestablished in both eastern and western halves of Pacifica.
ORIGIN OF FAGACEAE
The question of the origin of the Fagaceae can now be re-examined with the
background of the palaeogeography outlined above. No evidence has been found
for progenitors of the family in Africa or India, nor is there any evidence to support
the suggestion that Fagaceae from either region migrated into south-east Asia.
Trigonobalanus and .Nothofagus are the most archaic of the surviving genera and it is
now evident that their present distributions are linked to the former West
Gondwanaland Peninsula of the Permian, as defined here. T o avoid confusion, it
should be pointed out that Raven & Axelrod (1974) refer to Africa plus South
America as West Gondwanaland although it would be more rational to call this
central core of the old continent, Central Gondwanaland or East Gondwanaland.
When the extant species of Nothofagus are plotted on the reconstructed map of the
West Gondwanaland Peninsula (Fig. 1) they form a coherent population, which is
extended into the West Antarctic Peninsula by fossils (Cranwell, 1963). This is the
core of the genus, which following migration horthwards into New Guinea, gave
rise to the most advanced species. The Australian and Tasmanian species, or their
progenitors, probably reached their present stations not later than the Eocene,
before Australia and Antarctica separated. These conclusions are supported by the
interrelationships of the species (Melville, 1973) and the transoceanic separation of
related species.
The absence of Fagaceae from Africa is consistent with the early Triassic
separation of Australia and Antarctica from the rest of Gondwanaland and an
origin in the peninsula of West Gondwanaland some time in the Triassic.
Migration of Nothofagus into Australia from the peninsula would have been
possible up to 50 My ago (late Palaeocene), when Australia broke away from
Antarctica. By this time, .Nothofagus was well-established, as testified by Cretaceous
fossils from Australia, New Zealand, Chile and the West Antarctic Peninsula
(Cranwell, 1963). The migration of Nothofagus into New Guinea extended the
range of the genus beyond its old gondwanic homeland. This migration route was
opened in the late Permian when orogenic uplift connected the West
Gondwanaland Peninsula with the Pacific continent and would have been broken
when the two halves of Pacifica began to drift apart in the Jurassic about 150 My
ago (Melville, 1981). That it was an effective land-bridge is indicated by the
presence of Glossopteris fossils in western New Guinea and Thailand in the late
ORIGIN O F F.iGACE.4E
Figurr I . 'l'hr Pacific Ocean with the reconstructed Pacific continent and thr Ll'est Gondwanaland
and Fu,qu~.
Peninsula wperimposed to illustrate the tlistrihutional history of .Votho/u,quJ, Tr<~onobulunu~
Arrons indicate the direction of continent;il drift .ind migration routes on land. Key to syml)ols; 0 thr original distrihtioii of .tdhuJo,p.r arid its migration route t o New Guinea; V-fossil sites; Bp i - r s r n t distril)ution ; 0 7 i i g u ~ 0 6 a l a n u ~prrsent
.
distributions; .-presumrd
former distril)iition of
7.r x r r h Lomrio, Hrrnaiidcz CG, Heiiao;
Fagur. present distribution; .-fi)ssil
rrcords.
Permian, at the time when the Glossopteridae was beginning to exhibit
angiospermy. Early angiosperms and pro-angiosperms thus obtained a foothold in
the southern tip of Pacifica and would have made considerable evolutionary
progress during the period of approximately 80 My before the disruption of the
continent. Muchofthe early evolutionof.VothoJagusmust have been completed before
the fragmentation of the West Gondwanaland Peninsula divided and dispersed the
original coherent population into isolated colonies. The centre of origin and centre
for- the adaptive radiation of .Vothofagus and probably for the Fagaceae as a whole,
appears to have been in the southern part ofthe West Gondwanaland Peninsula. T h e
most primitive of the surviving species, %V.alessandrii Espinosa, now occurs in
southern Chile which had been part of the Magellanian sector of the former
peninsula. From this species, which has four-lobed cupules enclosing seven fruits, a
reduction series can be traced, which forms a topocline along the migration route
of the genus (Melville, 1973).
The majority of the species of .Vothofagus have four-lobed cupules containing a
dimerous fruit flanked by two triangular trimerous fruits. Among these are several
species pairs that have been separated by continental drift and are now vicariously
distributed between New Zealand and South America or Australia and South
America. Together, these form the nucleus of the genus. The topocline begins in
New Zealand where .N.solandri (Hooker fil.) Oerst. appears with the cupule lobes
reduced to three by the fusion of one pair and the fruits reduced to two by the loss
80
R. MELVILLE
of a lateral triangular one. In New Caledonia there are five species with two-lobed
cupules which enclose three dimerous fruits. In New Guinea there are four species
at the same level of evolution as those of New Caledonia, including .V. f i e r y ‘
Steenis and N. brussii Steenis. In the remaining New Guinea species the number of
fruits is reduced to one, forming .Nothofugus series UnijZorae. I n some of these the two
cupule lobes enclose the fruit, but in N . carrii Steenis and N . bernhardii Steenis the
cupule lobes are reduced in size and they are absent in N . resinosa Steenis and
.N. cornuta Steenis, leaving the fruits unprotected.
The reduction series in Nothofagus reaches its peak of evolution in .V. resinosa and
,V. cornutu in New Guinea. The cline in reproductive structures is clearly linked
with the migration route from New Zealand through New Caledonia to New
Guinea (Fig. 1 ) . O n account of the advanced stage of the New Guinea species,
suggestions that the surviving Australian species reached their present stations by
migration from New Guinea are untenable. After Australia contacted New Guinea
in the Oligocene, migration of advanced species into Australia would have been
possible. If this happened, the immigrants could be detected by leaf or
fructification characters, but not by pollen alone. The close relationship between
the surviving Australian species and their Chilean and New Zealand congeners
indicate migration through Antarctica before the separation of the two continents.
They must have reached Australia not later than the beginning of the Eocene 50
My ago.
T o account for the close relationship between the New Zealand and South
American species of Nothofagus, Fleming (1963) suggested that there had been
“more than three interchanges of stock across the Pacific”. Such long-distance
migration across the ocean must be rejected since the fruits sink in water and have
very short survival in sea water (Preest, 1963; van Steenis, 1971). There are no
known animal vectors capable of carrying these fruits across the distances involved.
In the face of the new evidence for the existence of the West Gondwanaland
Peninsula, there is no need to postulate long-distance trans-oceanic dispersal. The
dispersal and interchange took place overland and must have been completed by
the mid-Cretaceous before the disruption and drift of the Peninsula. Similarly, the
northern movement of the N . brussii group into New Guinea in Plio-Pleistocene
time suggested by Fleming (1963) cannot be entertained. It would not allow
sufficient time for the evolution of the reduction series and the migration must have
taken place before the disruption of the peninsula. More probably, early Nothofagus
or proto-Nothofagus had reached New Guinea by the mid-Jurassic, there to evolve
on its own when New Guinea became isolated about 120 My ago, during the
disruption of the Pacific continent. We are left with the conclusion that the present
distribution of Nothofagus and its fossil distribution in Antarctica are the direct
result of the disruption of the West Gondwanaland Peninsula followed by drift of
the fragments. Similar conclusions apply to many other angiosperms of
Australasian affinity that occur in Peru or in the Magellanian sector of South
America.
The distribution of Trigonobulanus is an extension of that of Nothofagus. The
present range in south-east Asia indicates that it, or its progenitors, took the
migration route from the centre in the West Gondwanaland Peninsula through
New Guinea into Malaya, Thailand, Bornea and Celebes, which had been
followed in the Permian by Glossopteris and early angiosperms. Before drift of the
Peninsula, Peru formed the major landmass of its northern extremity and it is likely
ORIGIN OF FAGACE.4E
XI
that Trigonobalanus originated there. With the break-up of the Peninsula,
Trigonobalanus was transported in the Peruvian enclave, with many other
angiosperms, to South America. Its present station in Colombia is probably the
result of migration from Peru, when the Miocene uplift of the Andes altered the
ecological conditions, causing its extinction in Peru and survival under more
favourable conditions in Colombia. Thus the presence of T. excelsa Lozano,
Hernandez 8.1 Henao in Colombia is accepted here as the direct result of rafting by
continental drift. It is a much more parsimonious interpretation of the data than
the suggestion ofnorthward migration in Asia, passage across the Bering Strait and
then south again until Colombia was reached. Trigonobalanus and .Vothofagus are
the two genera of Fagaceae that have retained the greatest number of archaic
characters. They may indicate the route whereby the family first made an entry
into the Pacific continent and hence into the northern hemisphere. Before the
disruption of Pacifica in the mid-Jurassic Fagaceae must have dispersed over most,
if not all, of the continent, although individual genera were probably not
uniformly distributed. O n the evidence of modern distributions Lithocarpus and
Castanopsis were almost Confined to the western half, the former being represented
by a single species in California and Oregon. C'hrysolepsis, with two species in
California, is a 'sister genus' to Castanopsis, the two now being separated by the full
breadth of the Pacific (Forman, 1966). Quercus and Castanea were more evenly
distributed and after drift have occupied both the Eurasian and North American
continents directly, without involvement of the Bering Strait. The migration route
followed by Quercus subgenus Quercus from China across Eurasia to western Europe
is the path probably followed by numerous other genera in many families that had
their origin, in whole or in part, in the West Gondwanaland Peninsula.
No evidence has been found to show that Trigonobalanus reached North America,
but fossils from Europe attributed to this genus by Mai (1970) range in age from
mid-Eocene to Miocene. These fossils consist of lobed cupules containing small
triangular fruits and in T. andreansgkyi Mai the cupule lobes bear transverse rows of
scales reminiscent of 7. verticillata Forman. Trigonobalanus succinea (Goeppert &
Menge) Mai, a small triangular fruit with capitate stigmas preserved in Baltic
amber, possibly of Eocene age, fits Trigonobalanus better than any other genus of
Fagaceae (Forman, 1964). Mai also illustrates a transverse section of the pericarp
of T. exucantha Mai, which shows a row of radially oriented, elliptic sclereids under
the epidermis and several rows of smaller angular sclereids internal to this. This
character excludes Nothofagus, which has a band of transversely elongated sclereids
in the centre of the pericarp, but it does not distinguish the fossil unequivocally
from other genera. Elongated subepidermal sclereids are radially arranged in
Quercus, Castanea, Castanopsis and Lithocarpus (Soepadmo, 1968) whereas in Fagus
and Trigonobalanus there are several layers of angular isodiametric sclereids. The
fossil is intermediate in these pericarp characters, which may indicate a more
generalized condition attributable to an earlier phase of evolution from which the
modern genera have diverged. The cupules are associated with leaves of the
Dryophyllum-type and D. furcinerue (Rossm.) Schmalh., illustrated by Mai (1970:
409, taf. IV), are pinnately veined, sharply serrate, with polygono-scalariform
ternary veins and a well-developed acroscopic vein below the tooth. These
characters occur together in Castanea, Castanopsis and some species of Quercus (e.g.
Q. castanefolia C.A.Mey.) as well as in the serrate leaves of T. verticillata. Some
uncertainty remains as to the attribution of the fossil leaves to a Trigonobalanus, but
x2
R. MELVILLE
the total evidence favours this genus rather than any other known member of the
Fagaceae.
If we accept the fossil evidence for the presence of Trigonobalanus in Europe in
the Eocene it follows that the modern range is a relict of a former, much more
extended distribution. From Thailand the genus must have migrated into China
and then followed the migration path across Asia into Europe utilized by
numerous other angiosperms, including Quercus, Fagus and Castenea. 'The
conclusion is reached that the latter three genera must have arisen in Pacifica from
primitive Fagaceae that had migrated north from the Gondwanaland Peninsula in
Permo-Triassic time. All three genera must have been widespread in Pacifica by
the mid-Jurassic, when that continent began to break up. The present pan-boreal
distribution of the genera is the result of migration made possible by the drifting
together of the European, Angara and Pacific sectors of Eurasia and of the western
and eastern sectors of North America. The severance of Pacifica into two
subcontinents and the rafting of the floras on the separated sectors by continental
drift accounts for the presence of Quercus, Fagus and Castanea in both Eurasia and
North America. It was responsible also for the separation of Chrysolepsis in
California from Castanopsis in south-east Asia and for the isolation of one species of
Lithocarpus in western North America from the rest of the genus in eastern Asia.
The separation of the island arcs ofJapan and of the Philippines from the Asiatic
mainland was the result of secondary drift movements during the Tertiary, after
the primary drift of Pacifica had been completed (Karig, 1971). The movements
did not have any marked effect on the general pattern of distribution, although
isolation of populations on islands favoured speciation. The continental mass of
Eurasia was the result of the drifting of the eastern half of the Atlantic continent
and the western half of the Pacific continent into contact with the Angara
continent, which now forms part of Siberia. By the end of the Cretaceous a
continuous land route across to Europe was available for the migration of
angiosperms from the western half of Pacifica. By the Eocene Quercus,
Trigonobalanus, a number of Lauraceae, Magnolia and many others had reached
western Europe (Mai, 1970). Fagus participated in this migration and the effect of
adaptation and selection along the route is reflected in the topocline in leaf margin
characters from China and Japan across to Europe (Melville, 1981 : fig. 3).
Cursory inspection of Quercus suggests that comparable morphoclines exist in this
genus and await systematic study. South of the equator a morphocline in cupule
and fruit characters exists in Xothofagus along the migration route from New
Zealand through New Caledonia to New Guinea (Melville, 1973).
Of all of the species of.Nothofagus, .V. alessandrii comes closest to Fagus, not only in
leaf margin characters but also in the size, texture and general appearances of the
leaves. The study of the leaf margin characters has now been extended to include
the ,Vothofagus complex. The phylogenetic scheme presented here (Fig. 3) is based
primarily on leaf characters, but cupule, fruit and stipule characters harmonize
with it. In his classification of the genus, van Steenis (1953) used leaf vernation as
one of the principal characters to separate Nothofagus subgenus Caluechinus with
plicate vernation from Nothofagus subgenus Calusparassus with flat or conduplicate
vernation. Following the recognition of the Glossopteridae as the progenitor of the
angiosperms (Melville, in press), these characters cab now be placed in their
correct evolutionary perspective. The leaf architecture in the majority of Fagaceae
is too far advanced to give an indication of the leaf structure of their progenitors.
ORIGIN OF FAGACEAE
83
Only in .VothoJhsuJ has any evidence survived that the leaf architecture of the
Fagaceae has been derived from leaves of the Gangamopteris-type. This takes the
form of a flabellate arrangement of the major veins at the base of the leaf observed
in .V-. anturctica (G. Forster) Oersted, .I$ dombeyi (Mirbel) Oersted, .N. betuloides
(Mirbel) Oersted and JV.nitidu Reiche. The leaf spectrum of long shoots of N .
nitidu shows an interesting gradation from suborbicular with five to seven flabellate
veins, through deltoid, ovate to ovate-lanceolate in which only the midrib is
prominent. Three to five veins may be present at the base of normal leaves of
.Ir.dombeyi, which also show another archaic character: the principal lateral veins
J
2 mm
Figure 2. .VothOf4pl~~
dmnbeyz A-Leaf from gall with archaic leaf venation. B,C-Details of minor
venation, zig-zag veins (zeta series) arrowed. D-Normal leaf, note veins terminate in teeth or at
sinuses or both, E,F-Details of minor venation of D, are more advanced than in B and C.
84
R . MELVILLE
may end in a marginal tooth, or at the base of a sinus, or they may fork with one
branch serving a tooth and the other the adjacent sinus (Fig. 2D). All of these
conditions may be found in a single leaf and indicate a relatively primitive state in
which the leaf architecture is indeterminate. The venation pattern is stabilized in
<4'. pumilio and -V. gunnii with the lateral veins running to the sinuses. In .N. fusca,
.Y. truncata and ,V. alessandrii, which have simple teeth, the veins always end in the
tooth apex and this feature is stabilized in Castanea and many species of Quercus.
The specimen of .V. dombeyi illustrated was collected by H.J. Elwes on the
Chile-Argentine border in 1902 (in Herb. Kew) and bears several leafy galls. The
Fagus
'm
Figure 3. Evolution of leaf margin characters in Nothofagus and Fagus. A, Theoretical proto-Fagus with
gangamopteroid venation. B-F, The topocline from New Zealand through New Caledonia to New
Guinea with simplification of the margin and specialization of the minor venation. B, .N. codonandra. C,
.N. solandri. D, .hr. balamae. E, .N. pullei. F, N . cornuta. G-J, Nothojagus, the main complex. G, ~hr.dombeyi.
H , .V. betuloides. I, N . nitida. 3, - N f s c a . , K, N . menziesii. L, .N. truncata (Col.) Ckn. M, N . cunninghamii.
N, JV.moorei. 0 ,N. antarctica. P, , obbqua. Q N. procera. R, N . pumilio. S, N . gunnii. T, N. alessandrii
Espinosa. U-X, Fagus. U , F. grandfolio Ehrh. V, F. lucida Rehd. & Wils. W , F. sieboldii Endl. X, F.
syluatica L.
ORIGIS OF F.\G.\CE.\E
85
gall lea\.es differ considerably from the normal foliage leaves (Fig. 2L2),in their
venation pattern, in the almost entire margin and in details of the venation, which
includes zig-zag vein junction series (Fig. 2C, arrowed), (Zeta series, Melville,
1976), which are characteristic of advanced species of Gangamople,is, but are absent
dombtyi. The gall leaves have, in fact, reirerted halfway
from normal lea\res of .I?.
back to Gangamopteris and support the indications of the evolutionary origin noted
in the normal lea\res. The application of teratological phenomena to phylogenetic
problems has been much questioned. In his discussion of this subject HeslopHarrison (1952) came to the conclusion that each case must be judged on its
merits. Sometimes the genetic control is so disrupted that the resultant phenotype
is uninterpretable, at others reversion to an ancestral phenotype may result.
Excluding , Iothofagu\ subgenus Culusparassus sections Bipartitae and Tripa,/itae,
the remaining species o f ,ZbthofaguJ all haire four-parted cupules enclosing three
fruits of which the median one is dimerous and the laterals trimerous. T h e one
exception to this generalization is ,I*.alessandiii which has an additional four
a/essandjii
.
has
dimerous h i t s external to the central dichasium. On this account .I.
been accepted as the most primiti\,e of the surviving species. Some further light is
shed on the primitive condition by a tree of .I-.
d o m b y i formerly in the arboretum
at Kew. In addition to normal cupules this tree always bore a proportion of
cupules with four lobes and one to three additional peripheral fruits all of which
were trimerous. One cupule was found with the central as well as the lateral fruits
trimerous, suggesting an ancestor with se\’en trigonous fruits arranged as in
TrigonobalanuJ (Mel\ille, 1973, fig. 6). Later evidence that T.excelsa may have up
to 27 fruits within a cupule (Lozano-C. et al., 1979) indicates the se\ren-fruit cupule
was only a stage in the reduction of an even more complex inflorescence.
Although the evidence for a derivation of the leaf architecture of the Fagaceae
from a leaf of the Gan‘gamopteris-typemay appear somewhat tenuous, confidence in
this interpretation is given by the extensive series of intermediates that connect
gangamopteroid leaves with more modern forms in such families as Compositae
and Ranunculaceae. Such evidence as has survived suggests that by the end of the
Permian ‘proto-Fagus’ had gangamopteroid leaves, which during the Triassic and
Jurassic diversified to produce the complex of leaf forms now observed in
Vothofagus. I hesitate to call this an adaptive radiation for it is difficult to attribute
any survival value to the variants of leaf margin patterns, which in .5bthofagus cover
a large part of the leafvariation within the family and are extended only slightly in
other genera. A phylogenetic scheme (Fig. 3) based on leaf margin patterns runs
closely parallel to the phylogeny indicated by cupule and fruit characters
(Melville, 1973). In the less advanced species, .I-.dombeyi and .Ie.
antarctira (Fig.
3G, 0 ) the
, lateral veins may run to either a tooth or a sinus. Related to .Y. dombeyi,
.Y. betuloides (Fig. 3H) has the veins running to the sinus and .V. nitida (Fig. 31) to
the teeth. Similarly, in the relatives of .V. antarctica, the veins run to the teeth in
, Y. obliqua (Mirbel) Oersted and .Y. procera (Poeppig & Endl.) Oersted (Fig. 3P, Q,
and to the sinuses in .Y. pumilio (Poeppig & Endl.) Krasser and .Y. gunnii (Hooker
fil.) Oersted (Fig. 3R, S). O f simply serrate types, .N. fusca (Hooker Fil.) Oersted
is related to .4*.menziesii (Hooker fil.) Oersted and these are the only species that
carry domatia, while .I;. truncata from New Zealand is related to .V. cunninghamii
(Hooker fil.) Oersted and N . moorei (F. Muell.) Krasser of Australia. T h e
curvipinnate venation of -Y. codonandra (Baillon) Steenis from New Caledonia
represents another relatively primitive form which may be antecedent to the
86
R . MELVILLE
pinnate forms of N . dombeyi and N . antarctica. It is readily formed by the gentle
arching-in towards the margin of the spreading longitudinal veins of the
gangamopteroid ancestor. The margin may continue entire as in N . codonandra,
many species of Lithocarpus and some of Quercus and Castanopsis, or it may become
serrate. Nothofagus balansae (Baillon) Steenis of New Caledonia has a shallowly
undulate dentate margin in which the lateral veins terminate in glands at the tips
of the undulations. This may result from a smoothing out of a formerly dentate
margin, an unusual process which is more obvious in the topocline in Fagus
(Fig. 3U-X). There is a strong tendency in curvipinnate leaves for branches of the
lateral veins to link up and form arches some distance below the margin, so giving
rise to the common co-arcuate pattern. A relatively early stage in this process
occurs in N . solandri (Hooker fil.) Oersted, where the tips of the curvipinnate veins
are still distinguishable, as well as somewhat angular arches connecting the laterals
(Fig. 3C). In more advanced species, such as N . balansae and N . pullei Steenis, the
arches are smooth (Fig. 3D, E), but in the most advanced members of the series
they tend to become indistinguishable from the fine mesh of small areoli which
forms the vascular system of the leaf. Among the more primitive forms, such as in
N . antarctica, veins of different orders are formed in sequence with a time gap
between the initiation of each grade. Thus the midrib (primary) is formed first,
followed by the laterals (secondaries) and so on. In the most advanced forms the
midrib is initiated first, but by the time the laterals begin to form, the whole of the
developing leaf has been converted into a plate meristem in which the fine
polygonal mesh is initiated simultaneously and the arching veins and other
ternaries merge into the mesh. It is unusual to find a genus in which such a wide
range of evolutionary processes is manifest. In passing along the sequence,
primitive features are eliminated one by one until, in the most advanced members,
all evidence of the ancestral condition has been suppressed
The evidence from Nothofagus sections Tripartitae and Bipartitae is confined to the
migration route : New Zealand-New Caledonia-New Guinea. Both leaf characters
and cupule and fruit characters indicate a progression in one direction with the
most advanced conditions in New Guinea. Van Steenis (1971) has accepted the
impossibility of trans-ocean dispersal in Nothofagus so that a continuous land
surface was essential along the migration route to account for these topoclines
(Fig. 1). Excluding these clines, the remaining species of Nothofagus form a
complex, related members of which are separated by wide stretches of ocean. Thus
N . pumilio is in South America and N . gunnii in Tasmania; N . truncata is in New
Zealand and the related N . cunninghamii and N . moorei in Australia. Continental
drift affords the only acceptable mechanism to account for these disjunct
distributions, which are a direct consequence of the separation of continental
fragments. In passing north up the Pacific the same kind ofpattern is repeated with
the two species of Trigonobalanus in south-east Asia and one in Colombia and with
Quercus, Castanea and Lithocarpus split on either side of the ocean. The genera
Castanopsis and Chrysocepsis take the disjunction to the generic level.
Van Steenis (197 1) claimed Nothofagus as a key genus for plant geography, a
conclusion that the present review endorses. This concept can be extended to the
family as a whole, for the distribution of the genera and species on either side of the
Pacific provides a classic example of the effect of continental drift on plant
distribution. Other conclusions of van Steenis must be rejected, notably the claim
that a Gondwanaland origin of the Fagaceae is taxonomically impossible.
ORIGIN OF FAGACEAE
87
.Vothofagus is the most primitive genus in the family and the only one in which any
primitive leaf characters survive. Except for the New Guinea species, which are the
most advanced in the genus on both leaf characters and fructifications, all of the
remaining species still occupy fragments of the old Gondwanaland continent and
retain a more archaic morphology. This is consistent with a gondwanic origin, as
all of the other genera are more advanced, including Trigonobalanus, in its leaf
morphology. Moreover, recent evidence that the Glossopteridae is the progenitor
of the angiosperms points inevitably to Gondwanaland as the place of origin. Also,
characters of the ovule and its development must be considered. Poole (1952)
found that the ovule of .Nothofigus has only a single integument although elsewhere
in the family (e.g. Fagus) there are two. Many authors have considered the
bitegmic ovule to be primitive in the angiosperms, but the ovules in the
petrification mentioned above (Gould & Delevoryas, 1977) were unitegmic,
suggesting that in fact the unitegmic condition was primitive. The fruits ofthe fossil
were shed before an embryo had developed, so presumably the embryo developed
while fruits were lying on the ground. Nothofagus is only one stage further advanced
over this Permian fossil, for Poole found that at pollination the ovule was only
beginning to form and fertilization did not occur until after a lapse of nine to ten
weeks. The fossil evidence indicates that the delay in fertilization and ovule
development are primitive characters which endorse the conclusions already
reached from leaf, cupule and fruit characters on the relative primitiveness of
.Nothofagus. In this context, the delay in the development of the acorns of many
speciesofQuercussubgenusEythrobalanusunti1thesecondseason (Elias, 1971) could be
regarded as the survival of a primitive character in a sub-genus or a family that is
otherwise advanced. A similar delay in fruit development occurs in Chysolepsis,which
has the most primitive form ofcupule in the family ( Forman, 1966).These are striking
examples of differential evolution (heterobathmy) .
The fact that the pollen of Nothofapus is easily recognizable has frequently
brought it into phytogeographical discussions. Although the Nothofagus-type pollen
first appears in the Upper Cretaceous, van Steenis (1971) considered that the
genus must have been in existence before this period, a n opinion that is supported
by other characters discussed above. In genera of Fagaceae pollen grains are either
tricolpate or tricolporate. The tricolpate grain, in which the number of colpi in the
equatorial plane is increased (zonacolpate grains) by a diffusion reaction
controlling their morphogenesis, could lead to the tricolporate grain by t h e
roundingoff of the colpi to form pores. In Nothofagus the tricolpate stage would not
be recognized as belonging to the genus. Therefore, the apparently sudden
appearance of Nothofagus in the Cretaceous, may mean only that this was the time
when zonaporate grains evolved in this genus. It appears that too much emphasis
has been placed on pollen character and a more balanced view of the evolution of
Nothofagus can only be reached by the correlation of the other characters discussed.
ACKNOWLEDGEMENTS
I am indebted to my colleague L. L. Forman for discussions on the evolution of
the Fagaceae and for reading a draft of this paper.
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