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Biol. J . Litin. SOC.,1, pp. 223-23 1. With 1 plate and 5 figures
April 1969
First thoughts on species evolution in Malayan Macaranga
(Studies in Macaranga 111)
T. C. WHITMORE, F.L.S.
Forest Research Institute, Kepong, Malaya
Macaranga (Euphorbiaceae) is a genus of tropical trees. Five aspects of species evolution in
Malaya are discussed. (1) Seventy per cent (20) of the species in Malaya have come to be common
as small trees in secondary forest. Their original habitat was small forest clearings mainly
along rivers, where they grow as bigtrees in small populations, fruitingall the year round. Their
biology has enabled them to become the most successful genus in the extensive 'secondary
forests that have resulted from forest clearing over the last 90 years. In so spreading they have
not hybridized or developed regional differences within the country. (2) There are however
marked differences from populations in northern Borneo, 800 km east over the shallow South
China Sea; this is thought to reflect morphological divergence since the lands were last separated
in the Pleistocene. (3) M. andamanica has a disjunct distribution coupled with polymorphism.
(4) M. Zaciniata which replaces M . heynei in north and east Malaya has trivial morphological
differences, thought to be genetically simple. ( 5 ) M. quadricornis, member of a close-knit
species group round M. t d o b a , grows in lowland swampy forest in south Malaya to 2'20"
and in the mountains of central and north Malaya from 3"20'N. It is a very conspicuous and
common species yet no intermediates have been found between these two groups. The simplest
explanation of the disjunction in habitat and distribution seems to be that it has evolved twice
from out of its complex.
CONTENTS
Introduction .
Observations on living Macarauga
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(1) The impact of Europeans .
(2) The Macarangas of Malaya and northern Borneo
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(3) Polymorphism in M. andamanica.
(4) Evolution within the M. jaoanica species group
(5) The M. triloba group, especially M . quadricornis
Acknowledgements .
References
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22s
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INTRODUCTION
Macaranga (Euphorbiaceae, tribe Acalypheae, subtribe Mercurialinae) is a genus of
about 280 species (Willis, 1966) distributed from west Africa to Fiji, and strongly centred in Malesia. Macarangas are small to medium trees, occasionally reaching 30 m tall.
Many of them are abundant in, and characteristic of, regrowth forest, where they grow
fast to form a continuous canopy early in the secondary succession; of the 28 species
in Malaya no fewer than 20 have this habitat.
Macaranga is thus a good subject for the study of speciation, a subject which has been
rather neglected in tropical trees. It is not yet known from observation whether the
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speciation mechanisms discovered from studies on temperate plants, mainly herbs,
are important, or indeed whether some of them, such as polyploidy, work at all, in
genera of tropical woody plants.
The speculations presented here are based on five years observation of living Macaranga, three of them in Malaya. I have also seen most of the herbarium collections ever
made from Malaya. The conclusions seem to me to give the most economical explanations of the facts as they are known. Of course they stand open to amendment if new
and conflicting observations should be made.
OBSERVATIONS ON LIVING MACARANGA
I shall mention five particular aspects.
(1) The impact of Europeans
Twenty species of Macaranga in Malaya grow in secondary forest, 18 of them
gregariously. They are small bushy-crowned trees commonly attaining only 7-10 m
height and often fruiting at less. They are to be be seen along the railways and roads
and the other places where the primary forest has been felled. Only two of them
( M . heynei I. M. Johnston, M . laciniata Airy Shaw & Whitmore, in prep.) grow in
very poor soils, such as the exposed subsoil of deep road-cuttings.
The size and extent of the secondary forest habitat has increased continuously and
increasingly rapidly in the 90 years or so since European penetration of the interior
of the peninsula began. Prior to that, these Macarangas were restricted to much smaller
and relatively isolated clearings made by the small Malay communities, and to their
original habitat, which was gaps in the high forest, especially landslips along valley
sides, where they may still be found throughout the country, in tiny separate populations.
Wide-scale destruction of primary forest has led to very big increases in population
size and to the coming together of previously separate populations.
In their original habitat several of these Macarangas are often found as quite large
trees, sometimes attaining 1.8 m girth and 24 m height with rather shallow terminal
crowns. In the man-made habitats they are small 6-9 m trees with deep bushy crowns,
and get no larger. Coupled with the move into man-made habitats there has been a
reduction in tree size, a reduction in the length of the reproductive cycle,* and a change
from small populations to large ones.
So far I have been unable to detect any changes in morphology which might have
arisen from these major changes in biology. I find no evidence of hybridization between
species,? and the po1ymorphism:which exists for example in M . puncticuZata Muell. Arg.
and M . triloba Muell. Arg. seems to have no basis in habitat or geographical range. There
is some evidence that Macaranga is cytologically uniform, the chromosome number of
eight Malayan species being always 2n = 22 (Whitmore, Soh & Jones, 1969).
* In cultivation at Kepong M . tanarius Muell. Arg. from Guadalcanal has flowered within two years
t Except possibly M . diepenhorstii Muell. Arg., M . hullettii King and M . quadricornis Ridley around
from germination.
The Gap (840 m altitude),one of the passes over the Main Range.
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Seventy per cent of Malayan Macarangas are found in secondary forest. No other
genus has such a high percentage of species in this habitat. I attribute the success of
Macaranga to its biology, which suited it ideally to move from small natural openings
in the rain forest. The trees fruit all round the year; the small leathery capsules are
eaten by birds (Ridley, 1930: 487, 502). T h e capsules ultimately dehisce but not
explosively. Most species have a thin red sarcotesta around the black seed, and I think
that small mammals also aid dispersal.
I n the course of moving habitat the species have changed from tall forest trees to
small bushy ones. But this is a morphological change that formal taxonomy cannot
record.
It is significant that seven of the remaining eight Macaranga species in Malaya not
found in secondary forest grow within the rain forest, not in natural clearings.* Five of
them belong to section Pseudorottlera, morphologically intermediate with the genus
Mallotus which is also a genus predominantly of the closed forest. Those few Mallotus
species common in secondary forest (principally M . cochinchinensis Lour., M . macrostachyus Muell. Arg.) are also to be found in natural clearings like the majority of
Macarangas.
O n Gunong Benom a logging operation in 1966 penetrated a colony of the very rare
newly-discovered species M . constricta Airy Shaw & Whitmore (ined.). By the time
this species was discovered in 1967 it had seeded into the extraction roads and was
behaving just like a secondary forest Macaranga: the species clearly had the potentiality
to become gregarious in secondary forest and the first opportunity was provided in
1966.
(2) The Macarangas of Malaya and nortlzern Borneo
T h e secondary forest Macarangas are constant throughout Malaya despite the
changes they must have undergone with the impact of Europeans on the country.
But to view the secondary forest in Sarawak or Sabah 800 km further east is like looking
through a distorting mirror. T h e species are nearly all present but they look slightly
different. To give one example, M . muinguyi Hk.f. differs from M . hosei King in possessing peltate leaves and in Malaya it is confined to swamp forest. In Sarawak both taxa
occur but their habitats are reversed. Thus although I have been unable to detect
differences from place to place within Malaya (admittedly without elaborate population
analyses) there undoubtedly are differences across the South China Sea. Malaya and
Borneo lie on a continental shelf. The sea between them is only c. 50 m deep and was
probably dry at the glacial maxima of the Pleistocene (van Bemmelen, 1949). Malayan
and Bornean Macarangas have presumably diverged since the two lands were separated.
(3) Polymorphism in M. andamanica
M , andamanica Kurz (recently annotated by Airy Shaw, 1965) is only known in
Malaya from Kedah Peak in the north-west, where it is common. It grows further
* The eighth, M . caludiifoliu Becc., is known in Malaya from very few collections. In Sarawak it
also is a non-gregarious primary forest species (J. A, R. Andcrson, pcrs. comm.).
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north along the Kra isthmus, in the Andamans, and through Indo-China to south
China. It isapparently uncommon and the distribution is rather disjunct. M . andamanica
has a wide range of variation and the characters are not correlated with each other.
The evidence suggests that disjunction has been followed by divergence of the population segments.
(4)Evolution within the M. javanica species group
fig. kzciniata Airy Shaw& Whitmore (ined.) is a newly-discovered species of north-east
Malaya, just crossing the border into Thailand (Fig. 1). It differs strikingly from M .
FIGURE
1. Mucarangu heynei ( 0 ) is replaced by closely related M . lachiiata
Malaya.
( 0 ) in
north-east
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heynei in that the bracteoles which subtend the flower clusters are laciniate rather than
toothed (Fig. 2). Also, the flower clusters are slightly closer (2-3 against 5 mm) and
the inflorescences stiffer and shorter (3-8 against 15 cm), but these are weak differences
because M. heynei has rather variable inflorescences.
These two species are allopatric (Fig. 1) and adjacent. The exact boundary between
them remains to be discovered. The difference between M. heynei and M . laciniata
A
B
FIGURE
2. Bracteoles of Mucurungu luciniutu (A)and M . heynei (B).
looks to me to be of a kind likely to be due to a very simple genetic difference, the
difference in bracteole toothing could even be due to a single gene. Clearly it will be
interesting to study what happens at the boundary of the two species (which is traversed
in several places by roads).
These two species are members of a group of five which differ from each other in
similar trivial characters. Thus M. jaaanica Hk. f., the first described, differs from M.
heynei only in having the bracteoles entire. On a broader species concept than currently
prevails the whole group would be reduced to one variable species. The genetic and
geographical relation of the component variants to each other remains a fascinating
field for investigation.
( 5 ) The M. triloba group, especially M. quadricornis
M . triloba (Plate 1) has already been mentioned as a wide-ranging, rather polymorphic, secondary-forest species. It is one of a group of species (section Pachystemon)
found through western Malesia comprising M. hullettii, M. kingii Hk.f. and M .
quadricornis in Malaya and M. depressa Muell. Arg., M . divergens Muell. Arg. and M.
tenuifolia Muell. Arg. plus several undescribed species elsewhere. Single chromosome
counts of M. hullettii, M. quadricornis and M . triloba were all 2n = 22 (Whitmore et al.,
1969).
The group is closely knit and undoubtedly natural. T o simplify slightly, the species
are all similar in the ornamentation of the lower leaf surface, the stipules, the bracteoles
of the inflorescence, the infructescence and fruits. Most of them have hollow antinhabited twigs (the ant is Crematogaster borneensis var. macarangae, Baker 1934).
They differ in whether the fruit is horned or not, in the degree and persistence of red
pigment in the leaves, and in the degree of lobing of the leaf, which varies from simple
to fully five-lobed (Fig. 3).
The species are all ‘variations upon a theme’. Their ranges are variously overlapping
(Fig. 4). M. triloba has the widest geographical range, and is common. M. depressa is
known from Lampong (Sumatra) and Borneo. M. hullettiiand M. tenuifolia are endemic
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to Malaya and Bangka respectively. M. diwergens is known only from a few scattered
localities in Bangka, Borneo and Philippines. M. kingii is found in southern Malaya
FIGUM
3. Leaves of Macaranga triloba and its allies (section Pachystemon).
(Johore) and western Sarawak (around Kuching) , a common distribution pattern
presumably dating from the Pleistocene sea minimum.
The most interesting species of this group is M. quadricmnis, endemic to Malaya.
This is one of the most beautiful and conspicuous wayside trees of the hill station at
Fraser’s Hill and has now been found through the main mountains of Malaya south to
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Gunong Nuang at 3'20'N (Fig. 5). Despite thorough searching it has not been found
lower than 890 m, nor has it been found on the isolated mountain ranges of south
Malaya. The habitat is hillsides.
In lowland swamps and seasonal swamps in Johore north to 2'20' an identical taxon
occurs. The only differences I have been able to detect are a slightly longer central lobe
to the leaf of juvenile trees, and an indefinable difference in the velvety texture of the
living leaves, which disappears on drying.
I 0'
0'
I OC
FIGURE
4. Species distributions of Mucurungu triloba and its allies. T==
M . triloba; H= M .
hullettii; K = M. kingii; DE and + =M . depressa; 0 = M. divergens; X = M . tenuifoliu; solid
black = M. quudricornis.
M . quadricornis has the leaves beetroot-red below and is common and conspicuous
along roadsides. It is very easy to spot. Thorough searching has failed to discover it in
the lowlands except in Johore. The species consists of two disjunct groups which are
widely separated in altitude, geographical range and habitat. T o explain the distribution
we either have to postulate widescale extinction between 2'20' and 3'20' north,
followed by or coupled with a massive altitudinal and habitat shift in one group or the
other, or alternatively the observations can more simply be explained by postulating that
M . quadricornis has evolved twice from out of the close-knit M. triloba complex. This
latter hypothesis satisfies Occam's razor as the simplest explanation to fit all the known
facts. It is to my knowledge the first record of bitopic evolution from out of a species
15,
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complex, and differs from previous known instances, which either involve polyploidy
(all the instances in Davis & Heywood, 1963;and Whitmore et al., 1969,show 2n = 22
in M . quadricomis, M. hullettii and M . triloba) ;or involve selection several times for a
FIGURE
5. Macaranga quadricomis (0)
has two, disjunct, groups in Malaya.
change in environment (all the other recorded instances, e.g. those in van Steenis,
1955,are all species evolved several times on different Malesian mountains from out
of a widespread lowland species). The discovery of a new type of polytopic evolution
amply bears out the original choice of Mmurunga as a potentially instructive genus
within which to study speciation phenomena.
Bio1.J. Linn.
Sac., 1 (1969)
T. C. WHITMORE
Plate 1
(Facing page 230)
STUDIJB
IN MACARANGA
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23 1
ACKNOWLEDGEMENTS
The drawings are by Yusoff bin Haji Mohd. Saman, artist at Kepong. Mr. H. K.
Airy Shaw has been of continual assistance during the course of these studies.
REFERENCES
AIRY SHAW,H. K., 1965. Notes on Malesian and other Asiatic Euphorbiaceae. LV. A preliminary
survey of IPIacaranga Sect. Pseudorottlera (Reichb.f. & Zoll.) Pax & K. Hoffm. Keu, Bull. 19: 315328.
BAKER,
J. A., 1934. Notes on the biology of Macaranga spp. Gdns’ Bull. Straits Settl. 8 : 63-68.
BEMMELEN,
R. W. VAN,1949. The Geology of Indonesia. The Hague: Government Printing Office.
DAVIS,P. H. & HEYWOOD,
V. H., 1963. Principles of Angiosperm Tuxonomy. Edinburgh: Oliver & Boyd.
RIDLEY,H. N., 1930. The Dispersal of Plants throughout the World. Ashford: Reeve.
STEENIS,
C. G. G. J. VAN, 1955. Flora Malesiana, I. chap. 3.
WHITMORE,
T. C., SOHKIM-GAI&JONES, B. M. G., 1969. Studies in Macaranga. 11. Some chroniosome counts. Gdns’ Bull. Singapore. (in press).
WILLIS,J. C., 1966. A Dictionary of the Flowering Plants and Ferns. 7th edition revised by H. K. Airy
Shaw. Cambridge University Press.
EXPLANATION OF PLATE
PLATE
1
Macaranga triloba. A, Roadside tree; B,fruiting twig; note the ant holes in the internodes.