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DIPTEROCARP BIOLOGY AS A
WINDOW TO THE
UNDERSTANDING OF TROPICAL
FOREST STRUCTURE
Peter

S.

Ashton

Professor of Dendrology, Department of Organismic and Evolutionary Biology,

vard University Cambridge, Massachusetts

Har

02138

INTRODUCTION
My aim is to show, by one example, why systematics must provide a
foundation equal to that of ecology if the structure of tropical forests, and

particularly their floristic structure and often extraordinary species richness, is

to be understood. Species composition accounts for much of the geographical
variation in structure that occurs among forests in different regions sharing the
same habitat. Our knowledge of rain forest structure has advanced from the
description of whole plant communities, or often their tree component alone,
to a contemporary interest in the demography and genetics of species pop
ulations, and to the physiological ecology of individuals. Always, though,
systematic as well as ecological relationships must be understood if this
knowledge is to contribute to understanding of the structure of the whole
forest.
The biological attributes shared among the individuals of species, and
which decide their success in interspecific competition, determine both the
ecological guild to which they belong and, in part, their systematic rela
tionships. Systematics aims to classify species into a hierarchy of categories
of increasing rank. The hierarchy is aimed to reflect evolutionary rela
tionships, and it thereby provides inferential evidence for the origin of the
major species groups constituting tropical rain forest communities.
that an

understanding

I argue

of the floristic structure of tropical forests, and more

347

0066-4162/88/1120-0347$02.00

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348

ASHTON

specifically of the way species invade and survive in mixture in these com
munities, of the way the communities vary in species composition and of
why, in particular, these forests vary in species richness-all these can be
achieved only by understanding how the hierarchies of systematic and ecolog
ical relationships are intermeshed.
My vehicle for analysis is the Dipterocarpoideae, the species-rich Asian
subfamily of a pantropical family that, because its trees dominate both
international hardwood markets and also the emergent canopy of most low
land rain forests in Asia, has been the subject of more-and a broader range
of-research than any other rain forest taxon of comparable size. It will soon
become obvious though that dipterocarps are unique in many important
ecological and systematic respects, and it is only partially possible to general
ize from them. This underlines how important it is to apply the same approach
to other groups.
This review is structured by systematic categories, starting with the sub
family itself and terminating with a more elaborate discussion of the species.
It serves to show how fragmentary our knowledge still is and where research
must now be directed.
The Dipterocarpoideae

Ashton (10) has elsewhere reviewed the systematic and ecological literature
on the group. Dipterocarps are trees; their simple penninerved leaves have
articulated stalks. Their bisexual and star-shaped nodding flowers have five
-merous perianths in which the sepals and petals, respectively, overlap. The
sepals enlarge and become winglike in fruit. Petals and fruit sepals are
generally twisted. The single ovary has three cells, each of which generally
contains two ovules; it generally ripens a single seed in a dry indehiscent nut.
The pollen grains are ellipsoid, slightly sticky, with smooth thin walls.
Dipterocarps are insect pollinated. Fruit dispersal, if it occurs at all, is by
wind or more often by gyration alone. Rats commonly scatter-hoard the nuts
but are thought not to carry them far (L. Curran, personal communication).
Asian dipterocarps are distinguished from others by their resin canals, which
are abundant in many tissues, and by details of wood anatomy, pollen, and
stamens. Two tribes are recognized, and these differ in details of the fruit
calyx and wood anatomy, and in basic chromosome number; any ecological
implications of these differences are unknown.
Though there are only 12 dipterocarp genera in Asia, some 470 species
with at least 100 infraspecific entities are recognized. This makes them
particularly suited for this review. Though species diversity is now centered in
Borneo and surrounding regions, systematic analysis suggests that the sub
family originally invaded Asia by way of the Indian fragment of Gondwana
(10). Total species diversity is markedly influenced by historical biogeogra-

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DIPTEROCARP BIOLOGY

349

phy, there being only 26 species east of Wallace's line, and 287 in Borneo as
against 7 in Sulawesi, which is only 80 km east of it at the same equatorial
latitude.
The absence of a towering emergent canopy dominated by dipterocarps in
New Guinea gives the structure of lowland forests there an aspect quite
different from those of Asia, and similar in many respects to that of neotropi
cal forests. Many other families fill the gap and are more abundant in the
canopy there, though tall emergents are either more scattered than in diptero
carp forests or absent. The southwest of Sri Lanka, in an area some 180 km
square, possesses 45-55 dipterocarp species, all but one endemic. The re
latively low number in this case must have an island biogeographic explana
tion (17). These regional differences in species diversity indicate major
differences in forest floristic structure. It is clear from the start, then, that
historic accident has been a major influence on the role of dipterocarps in
Asian forests.
Dipterocarps are exclusively components of the forest mature phase, only
gradually invading successional forests after a closed canopy is fully es
tablished. Most are confined to wet climates, with a dry season not exceeding
four months. All but a handful are evergreen. Dipterocarp species (but not
individuals) are dramatically more abundant in aseasonal than seasonal cli
mates. Thus, of the 155 occurring in peninsular Malaysia, only 27 occur also
in seasonal Indo-Burma, whose total dipterocarp flora is only 58 species (53).
In the Far East, the majority are confined to the lowlands, with a few species
endemic to higher altitudes. Curiously, this is not so in Sri Lanka, where a
majority of the large endemic genus Stemonoporus occur in hill or sub
mountane forest, and the family is best represented in moist premontane [in
the sense of Holdridge (37)] forests at 500-800 m (8). The overall species
richness of forest tree communities seems to reach a maximum at this altitude
in Sri Lanka (33), although elsewhere in the Asian tropics the maxima are in
the lowlands. This could reflect periods of aridity in the geological past, when
the South Asian I mixed rain forests might have been restricted to an area
immediately beneath and within the cloud belt on the mountain slopes, as they
are today in central peninsular India.
In seasonal climates, dipterocarps are confined to relatively infertile soils.
Thus, in India Shorea robusta forests are concentrated on granite and schists,
and are replaced by deciduous teak forest on basalts and other calcareous
rocks. In Indo-Burma the Dry Dipterocarp forests are confined to podsolic
sands and laterites, and mixed deciduous forests replace them on mesic sites
(23).
In the aseasonal humid tropics of the Far East, abundance of reproductively
'Peninsular India and the island of Ceylon (Sri Lanka)

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350

ASHTON

mature dipterocarps is greatest on yellow and red lowland soils (5). Not only
is the family as a whole generally dominant in the emergent stratum, there
comprising 80-100% of all individuals on yellow-red soils (e. g. 21, 5), but
single species dominance may be approached both on highly fertile (10, 15)
and highly infertile sites (1, 58). Dipterocarp species populations are general
ly aggregated into loose clusters of reproductive individuals, with juveniles
concentrated around them (6).
The ecological characteristics of the major tree families of Far Eastern rain
forests differ to a greater or lesser extent. Species richness in Myrtaceae varies
in ways similar to Dipterocarpaceae relative to soil for instance, but there are
few emergent species and clustering is less evident. Myrtaceae seeds are
mostly animal dispersed. Meliaceae and, to a lesser extent, Rubiaceae and
Euphorbiaceae broadly increase in species richness with increasing soil nutri
ent status (5). Dipterocarp ecology, however, remarkably recalls that of
Fagaceae.
Fagaceae reach their limits of species diversity in the submontane forests of
eastern Himalaya, Indo-Burma, southern China and western Malesia. 2 They
are represented, though more poorly in species and abundance, in the lowland
forests of the Far East. Like dipterocarps, few Fagaceae appear east of
Wallace's line. Fagaceae are absent from peninsular India and Sri Lanka,
presumably for historical biogeographical reasons. The altitudinal distribution
of the two families is suggestive of interfamilial competitive exclusion.
Asian Dipterocarpaceae and Fagaceae are both unusual among rain forest
tree families in being apparently obligately ectotrophic mycorrhizal (52; 54,
55). Trees of both families possess abundant mats of superficial fine roots.
These are best developed on less fertile soils. Smits (55) has evidence that
many basidiomycete mycorrhizal species are symbiot,ic with dipterocarps.
Dipterocarps, like many other tropical trees (19), experience high mortality
between anthesis and fruit set. Mortality is extended throughout this period.
Many fruit with fully extended winglike sepals apparently ripen, but the
carpels of most are empty. Dipterocarps (including saplings) flush in
termittently once or twice a year. In most species inflorescences are both
terminal and axillary, and they arise from the same positions from which leafy
shoots would otherwise originate. Ashton (12) has therefore suggested that
the retention of sterile fruits until full sepal extension may serve to increase
photosynthetic area at a time when energy demand is high but when the tree
lacks its usual leaf complement. It would be interesting to observe whether
fruit survivorship is the same among species with winglike fruit sepals as
among those many species in which all the sepals remain short. Whether
dipterocarp sepals function in the way suggested or not, it seems that
2Malaysia, the Philippines and Indonesia west of Sulawesi and Bali.

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DIPTEROCARP BIOLOGY

351

reproduction imposes severe stress on the trees. Primack & Chai (47) showed
that dipterocarps experience dramatic arrestment of growth in fruiting years.
Dipterocarps and tropical Fagaceae also share reproductive characteristics.
Both have poorly dispersed, one-seeded fruits. Both have seeds of high fat
content, lacking dormancy but nevertheless scatter-hoarded by rodents. In
both, the seeds are chemically defended by phenolic compounds and are
enclosed in a woody pericarp, though the dipterocarp pericarp is also richly
furnished with resin-canals. In both, the seeds are predated by beetles before
maturation and by vertebrates afterwards. Both are notorious for mast fruit
ing, though this does not seem to occur in the same years in the two families.
This lack of fruiting synchrony between the families appears largely to
explain the celebrated migrations of hordes of wild boars (Sus barbatus) in
Borneo, and formerly presumably elsewhere in Western Malesia (22). Janzen
(40) suggested that mast fruiting of the whole family is an adaptation to avoid
predation, among poorly defended seeds, by means of predator satiation.
Ashton et al (13) have provided further strong inferential evidence for this
hypothesis. Dipterocarps flower annually in the seasonal, and at intervals of
about five years in the aseasonal, tropics. They found a correlation between
dipterocarp flowering years and EI Nino climatic events, during which pro
longed depression of minimum night temperature is correlated with onset of
inflorescence development. Unusually heavy fruiting occurs at similar in
tervals in the seasonal tropics also, and intensity of seed predation is very high
there except in these years. Ashton et al (13), elaborating on Janzen (40),
nevertheless suggest that the seed predator satiation achieved by intensifica
tion of the mast fruiting event is occasioned in the aseasonal tropics by the
absence of an annual climatic cue to flowering. This may partially explain
how the Dipterocarps, as putative invaders, have become so successful
there.
The period between germination and establishment is critical for diptero
carps. The invasion of mycorrhiza has never been studied. Ashton (0)
speculated that the rarity of fruiting among tropical forest basidiomycetes may
be associated with poor spore dispersal and low spore dormancy in the
windless moist and equable rain forest understory. If this is so, and fungal
host specificity is variable but high in some cases (e. g. , see 36), fungal spread
may be principally through the soil, and this could partially explain why
dipterocarps are clustered in forests at both species, genus, and also family
level (Figure I; see also 6, 10).
Dipterocarp seedlings once established are generally able to survive in
shade, and many persist in the absence of canopy gaps between mast fruiting
years (28). This capacity appears to be limited by water stress (20). In
seasonal evergreen dipterocarp forests, few seedlings of dipterocarps or of
other mature-phase tree species survive beyond a year on this account (see
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SHORE" MACROPTERA
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Distribution of individuals exceeding 60 cm

girth, of species of Shorea section Mutica in Semengoh

Forest, Sarawak, East Malaysia

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DIPTEROCARP BIOLOGY

353

references in Ashton-12). This indicates a fundamental difference in the

dynamics of rain forests under seasonal and aseasonal climates. In the
aseasonal rain forest, gap regeneration is dominated by established regenera
tion except where the soil is disturbed, whereas pioneers play a more promi
nent role in seasonal forests. There, dipterocarps establish through later
invasion, following a mast year and the establishment of a pioneer canopy.
Predation on Dipterocarp seedlings is surprisingly low in comparison with
that on the seeds, though fungal pathogens may be an important source of
mortality (20). Low seedling and sapling predation may be associated with the
presence, possibly ubiquitous, of sugar-secreting glands on the upper, and
sometimes lower, leaf surface and stipules (29). These may attract ants that
may defend the seedling against predators, though this has not been observed.
With the exception of Dry Dipterocarp forest species, dipterocarp trees are
remarkable for their poor capacity for reiteration (12, 35), a character shared
by many gymnosperms. As seedlings, they have high capacity for shoot
reiteration, often through formation of accessory buds (45). By maturity,
however, the capacity to form new branches by reiteration becomes limited or
lost. Also, whereas seedlings and saplings respond to increased light with
increased growth, this capacity apparently declines as the plant matures (48).
Thus, the need for self-repair apparently declines as maturity is approached,
and selection may thus decline and even cease once the tree reaches full
height. Some evidence (e.g. 46) suggests that dipterocarps are not unique
among trees of the mature phase in these respects, which, in view of their
implications for understanding the floristic and dynamic structure of the forest
and the relationship between ontogenesis and changing selection pressures,
merit more study.
In summary, Dipterocarpoideae are seen to be as ecologically distinct a
group in Asian tropical lowland evergreen forests as they are systematically.
Their usually dominant presence distinguishes these forests from those else
where. Their success as a family there is apparently due to their ability to
maintain abundant seedling populations through satiation of seed predators,
possibly through offering rewards to predators of seedling herbivores, and
through their ability to enhance nutrition on leached infertile soils by sym
biosis with ectotrophic mycorrhizae. Dipterocarps appear to trade abundant
photosynthate from their often emergent crowns for cheap defense and superi
or nutrient acquisition in a limiting environment. Analysis of the cladistic
relationships of Dipterocarpaceae with other families has not been attempted
but would be valuable. Ashton (10) argues for including them in Malvales.
Though many Malvales are emergent forest trees with the same architecture as
emergent dipterocarp taxa (which is unusual and perhaps unique; this is
discussed below), none share the family dominance and gregarious habits of
dipterocarpoids. None have seed and seed dispersal characteristics of dip-

354

ASHTON

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terocarpoids, though some have small winged seeds. Some, such as many
Durio (Bombacaceae), may fruit supraannually in the wild, but fecundity is
low in these large-seeded trees. Rather, it is the Fagaceae, a quite unrelated
family within the angiosperms and one with a quite separate biogeographic
history (49, 43, 10), with which dipterocarpoids have most in common
ecologically and with whom, it seems, they survive at a familial level through
competitive exclusion. Here, then, is evidence that taxa of familial rank may
manifest niche specificity within the teaming forests of the humid tropics.

Genera and Sections

Though only 13 genera exist among Dipterocarpoideae, the large genera
Shorea and Hopea are divisible into 14 sections and 4 subsections, respective
ly, and Anisoptera is divisible into 2. These sections approach the status of
genera on structural grounds in some cases, but others distinguished on the
same set of character-states are less distinct. This is the reason for their
infrageneric status (4). All these taxa represent natural groups within the
family. Each contains an average of 16 species, though there is much variabil
ity in size, and 5 are monotypic.
These entities, which for simplicity I shall term quasigenera, possess
distinct geographical distributions. In some, such as Vateria, Vateriopsis,
Stemonoporus and Shorea section Doona, which are endemic to southern
India and some Indian ocean islands, their distribution may be explained by
historical biogeography alone. The ranges of one section (and of another but
for three species) of Hopea, of Cotylelobium, and of Shorea sections Riche
tioides, Ovales, Brachypterae and Mutica co-terminate at the sharp boundary
between aseasonal and seasonal climates at the Isthmus of Kra in southern
peninsular Thailand (See 58). All are confined everywhere to aseasonal
climates. Upuna and three further sections of Shorea are confined to aseason
al regions in the Far East west of Wallace's line. In all, this concentration of
quasigenera greatly enhances dipterocarp species richness in this zone. The
reasons for these coincident distributions within a continental area must be
ecological but remain entirely unknown.
Quasigenera differ consistently in one or more characters, including wood
and often bark anatomy, leaf venation, and in certain aspects of morphology
for which there are not obvious adaptive explanations. Each quasigenus has a
distinct architectural form, after the models of Halle & Oldeman (34,35), and
these models in some measure predicate the size at maturity of its members.
Thus Vatica, and apparently also Cotylelobium, early become sympodial
through terminal flowering of the plagiotropic branches and orthotropic lead
er. Both nevertheless continue to extend through apposition. Both genera
apparently conform to Kwan-Koriba's model. Most Vatica are understorey
trees, whereas Cotylelobium occupies the main canopy at reproductive matu-

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DIPTEROCARP BIOLOGY

355

rity. In Stemonoporus, many species conform to the model of Troll, whereby

the leader is initially vertical with spirally arranged leaves but eventually
bends over, apparently under its own weight, when the leaves become
distichous. Height is further extended through axillary shoots, which arise
from the upper side of the leaning or horizontal stem and these successively
repeat the process. Stemonoporus species rarely exceed 15 m in height.
Most emergent dipterocarpoid quasigenera have a distinctive growth pat
tern that appears to be shared by other emergent Malvalian trees including, in
Asia, Sterculia, Pterygota (Sterculiaceae), Pentace (Tiliaceae), and
Durioneae (Bombacaceae). Apical dominance is maintained in juveniles,
when the leader bears spiral leaves while branches are plagiotropic with
distichous leaves. At this stage, the branches may be arranged in pseudo
w90rls corresponding with each extension of the leader (Massart's model), or
-they may be arranged in an irregular spiral (R oux model). These forms
permit leaf surfaces to be spread diffusely in a horizontal plane, which will
maximize capture of sunflecks, but in such a manner that height increment
and the mechanical strength of the eventual tree are not compromised. When
the stem apex emerges above the canopy, the subsequent branches of all but a
few species are orthotropic, with ascending trajectory and spiral leaves, and
they are thus equivalent to the leader itself (33a). At that time, flowering
commences from terminal as well as axillary inflorescences so that branching
becomes partially sympodial. Surprisingly, neither Vatica, Stemonoporus,
Vateria or Vateriopsis, (regarded as the most primitive genera in the sub
family) nor African and South American dipterocarps have this malvalian
characteristic.
Quasigenera frequently possess distinct embryology. Shorea section
Doona, for instance, differs consistently from others in possessing one fleshy
cotyledon that remains hidden in the pericarp and is a food store, and one
minute, bract-like photosynthesizing cotyledon that emerges with the plu
mule. But there is much variability in the morphology of the mature embryo
within some quasigenera, particularly in Vatica and Stemonoporus (44), some
of which may be adaptive at the species level and none of which has so far
been shown to correlate with other, independent, characters of the tree.
Similarly, the presence or absence of extended wing-like sepals has for long
been given supraspecific taxonomic recognition, but it is uncorre1ated with
variation in independent character states and is therefore generally only of
value in species delimitation (4, 10).
There is some, still far too limited, evidence that quasigenera may con
sistently differ in some of the complex secondary hydrocarbons with which
dipterocarp exudates are richly endowed [for references see Hegnauer in (10),
pp. 273-74]. If correct, some herbivores and seed predators may be host
specific at a quasigeneric level. Evidence for this latter has recently been
'

356

ASHTON

found in some genera, such as Dipterocarpus, but not in most sections of

Shorea (R. Toy, personal communication, L. Curran, in preparation). Some
specificity at this level may occur between dipterocarp species and mycorrhi
za, which may invade in response to the specific cue of chemical root
exudations

(36). Both interdependencies, if they do exist, could help explain

how related quasigenera can co-occur in rain forest communities, through

density-dependent effects on the one hand
allocation

(40, 27) and through resource

(56, 57) on the other.

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Much is known of pollination biology and the functional morphology of the

H. T. Chan (2, 3, 24--26) and

c. v. S. and I. A. U. N. Gunatilleke (personal communication, in prepara
flower, thanks to the work of S. Appanah and

tion). One major group of dipterocarpoid quasigenera shares floral characters

that include large elongate yellow anthers with short appendages, a columnar
style that protrudes beyond them, and white petals that open widely at

Dryobalanops, Vateria, Neobalanocarpus, Shorea

Doona, Stemonoporus, Parashorea, Cotylelobium, and Vateriopsis.

anthesis. These include

section

This is not a monophyletic group; the members are equally represented in both
tribes of the subfamily. The flowers as well as other parts differ in other,
taxonomically important, characters. The flowers in this group are diurnal and
last one day. The first four are known to be principally visited by honey bees.
The pattern of visitation each morning is ostensibly the same in all cases (S.

V. S. and I. A. U. N. Gunatilleke, in
dorsata, and smaller A. indica var. cerrana
visiting first and then meloponid bees and various other insects. I have seen
Stemonoporus being visited by Trigona bees (Meliponidae), while no visitors
Appanah, personal communication; C.

preparation), with the large Apis

have been observed on flowers of the others. With the exception of Ceylon
quasigenera

Shorea section Doona and Stemonoporus, species in these taxa

contain few species. With the exception of species in section Doona, two or
more congeners rarely co-occur in the same community type. These taxa also
often flower more frequently between mast fruiting seasons than do other
dipterocarps.

Dipterocarpus has large flowers whose large yellow anthers with long
appendages and columnar style are enclosed in large pink and white petals.
The pollinators remain unknown. All other quasigenera possess small cream
colored anthers in flowers in which the petals, which are white, pink, or
yellow, remain strongly contorted at the base, thereby concealing the an
droecium and gynoecium. These flowers differ at a quasigeneric level in the
shape of the stamens and of the connectival appendage, in the length of the
style, and in the presence or absence of a stylopodium.
Appanah & Chan (24, 26, 3) made a thorough study of six species in
Shorea section Mutica. One tree can produce four million flowers over two
weeks. They found that the flowers open at night and last less than a day. The

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DIPTEROCARP BIOLOGY

357

corollas fall with stamens attached. Thrips lay their eggs between the petals in
the young bud. The juveniles feed on the petals. Up to five hundred adult
thrips can thereby originate from one female over three generations, or four
thousand juveniles over four, by which time anthesis begins. The thrips get
trapped during anthesis by the phalanx of connectival appendages, which
bend back against the corolla so that the anthers open inside a chamber
thereby created. There, the adults feed on pollen grains. Many escape though,
carrying one or a few of the sticky grains. Many others, including juveniles,
remain with the connate corolla and stamens, which together gyrate to the
forest floor at termination of anthesis. Juveniles can survive on the fallen
corollas for up to five days, and pollen can remain viable for this period.
Adults, some bearing pollen, fly up to the canopy each evening.
Trees in this section are outbreeders (25). Thrips can be transported on
convectional wind eddies, but they land directionally. No other floral visitors
have been observed during exhaustive studies in this section. Shorea section
Mutica, whose abundant individuals produce millions of flowers briefly and
at long intervals, achieve pollination through attraction of a fecund short-lived
pollinator which rapidly builds up numbers by feeding on the buds of the trees
that they will pollinate. Thrips are almost ubiquitous in dipterocarpoid flow
ers. Among other pale anthered quasigenera, Appanah (in Ashton et aI, 13)
found bugs (Hemiptera: Miridae: Decomia) to visit flowers of Shorea pauci
flora (section Brachypterae) and plant hoppers (Homoptera: Cicadellidae:
Varicopsella) to visit S. seminis (section, subsection Shorea). Neither of these
quasigenera is abundantly represented, by individuals or species, in individual
forest community types. In particular, studies of pollination are needed in
Shorea section Richetioides (which, after section Mutica, can occur in the
largest co-occurring species series) and in Dipterocarpus.
It does seem likely that competition for the services of pollinators is
avoided at a quasigeneric level. Pollinator specialization cannot, however,
provide a density controlling factor for the population of these taxa, and
cannot thereby explain their co-existence let alone the co-existence of the
multitude of other genera in the mixed rain forests. In the search for equilibri
um explanations for these coexistences we likely need to know more about
patterns of predator and herbivore specificity at this taxonomic level, and the
role of specific secondary metabolites.
The Species
With 12 genera and 470 species, Asian dipterocarps serve as an example of
those several families with large genera, the ecological range of whose
members is the principal determinant of variation in the species richness of
tropical evergreen forest (15). We have seen that the species of Dipterocarp
oideae are naturally grouped into some 30 generic and infrageneric

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ASHTON

taxa. Many of these species, as will be explained, are subdivided into distinct
geographical or edaphic subspecies.
Within quasigenera, habit is relatively unifonn, though maximum stature
can vary between and within species, according to site conditions, and in
particular according to soil depth (e.g. 5). Stemonoporus and Vatica can vary
substantially in habit, even among taxa closely related on the evidence of
other characters. In Hopea several species in two, and most species in a third,
of the four infrageneric groups are understorey trees. They differ from canopy
members in coming into flower while still in the monopodial juvenile habit,
which they maintain throughout life. Flowers in these neotenous species are
borne solely on the plagiotropic lateral branches. In Stemonoporus and Vatica
the difference in habit between understorey and canopy species is less extreme
owing to the sympodial habit of the understorey species, but distichous leaf
arrangements do not give way to whorled in the understorey species. In these
two genera neoteny can even differentiate infraspecific taxa. Vatica oblongi
folia Hook. f. , for instance, consists of four ecotypically differentiated sub
species, two of which first flower only after reaching the canopy while two
are understorey taxa. Stemonoporus canaliculatus Thw. occurs as two distinct
subspecies, sometimes recognized as species; one is a canopy tree of high
ridges, the other an understorey shrub of lowland yellow podsolic soils. In
Shorea too, subtle differences of habit can occur among subspecies. For
example, S. macroptera Dyer has one subspecies macropterifolia that is an
emergent tree while its other three subspecies do not emerge above the main
forest canopy.
In some quasigenera, notably Shorea section Richetioides and Vatica, a
correlation between habit and fruit characters occurs (6, 10). In these and
most other groups a significant minority of species lack winglike fruit sepals.
This wingless character has evolved many times, at least within the more
advanced quasigenera, and pairs of taxa differing only in this respect are
frequent. In Shorea section Richetioides most emergent species have winged
fruit, while all main canopy species have wingless (6). This implies that
winglike sepals actually reduce survivorship in species that drop their fruit
directly into the windless subcanopy. This is quite likely, as the wings can
entangle fruits among the boughs as they fall. Often, wingless fruited species
possess larger than average seed size, and the largest dipterocarp seeds are all
wingless. These characters, also sometimes correlated with distinct characters
of the embryo (44), may be adaptive, enhancing successful regeneration in
shady habitats. Wingless fruit also occur among riparian, water dispersed
species.
The overwhelming source of differences among species, however, is in leaf
morphology, principally in leaf shape, size, and number of veins, and in
presence or absence, length, and color of indumentum. Among canopy and

DIPTEROCARP BIOLOGY

359

emergent species these differences become most manifest at maturity, though

enough are possessed by the seedling for all ontogenetic stages to be generally
identifiable. Seedlings of related taxa are, however, generally more similar
than are reproductively mature individuals; this implies that selection for these
characters may continue up to maturity and that it may shift during ontogeny
from mainly intra- to mainly interspecific (6). These leaf characters may be
expected to influence water relations, but comparative studies of the physiolo
gy of closely related species which differ in these respects are still awaited.

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Large-leafed species generally also possess large buds, flowers and fruit,
and stout twigs. Frequently, taxa differ in leaf and twig size, and occasionally
number of nerves, but share distinctive leaf and twig shape, indumentum, and
other characters in common; these are almost always allopatric and are
recognized as subspecies (10). Occasionally, as in Shorea macroptera (6)
subspecies may co-occur. In this example, no morphologically intermediate
individuals occur in the mixed stands, suggesting that even when distinctions
are reduced to this level of subtlety the taxa may function as biological
species.
A remarkable feature of most dipterocarp taxa, therefore, is their morpho
logical constancy. This enables clear and consistent differentiation between
entities that may differ only, for instance, in leaf size and twig diameter, but
which are generally also geographically or ecologically allopatric. Notable
exceptions are those few species confined to the savanna woodlands, called
Dry Dipterocarp forests, of continental Asia, and to a lesser extent also some
species of Seasonal Evergreen Dipterocarp forests. Here variation, particular
ly in the presence, distribution, and density of indumentum, is common both
within and between populations (10). Populations in the driest habitats are
generally the most tomentose.
In Shorea section Pachycarpa, with ten species all endemic to the con
tinental island of Borneo, populations morphologically intermediate between
two species occur in at least one locality in every species, though all co-occur
with others throughout much of their range without this evidence of hybridiza
tion. The high uniformity within these hybrid populations is curious. An
experiment, not completed, suggested that hybridization is possible (24).
Evidence for interspecific hybridization is otherwise scanty among diptero
carps (see review and reference in 10). It is most abundant between related
species occurring in different, adjacent habitats. Most examples are between
species of Seasonal Evergreen and Dry Dipterocarp forests, suggesting recent
differentiation. However, these taxa are usually strikingly different in habit:
those of the latter forest type are short trees frequently with larger, more
coriaceous leaves, more diffusely arranged in the crown; they also have thick,
fissured bark. Occasionally, species of the Mixed Dipterocarp forests of the
aseasonal Far East occupying different edaphic ranges may hybridize in

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ASHTON

the ecotone between. The best known case is that of Shorea leprosula Miq. of
clay lowland soils and Shorea curtisii Dyer ex Brandis of xeric ridges, both in
section Mutica. Groups of individuals morphologically intermediate between
these species are known from several localities in peninsular Malaysia. In one
stand the inference of hybrid origin was supported by isozymal evidence; one
fruiting hybrid individual there failed to set viable seed (30). Jong (in 10)
provided evidence for hybrid origin of the tetraploid apomict S. ovalis
(Korth.) BI., a species monotypic to its section yet occurring as three geogra
phic subspecies. All evidence presently available to us, which is morpholo
gical and isozymal, suggests that speciation among dipterocarps is as a rule
geographically or at least ecologically allopatric (6, 7, 10, 11, 12a).
Biogeographical and paleontological evidence implies that dipterocarps
have been invading the Far East from the west since the late Eocene. Several
species endemic to the aseasonal southwest of Sri Lanka appear most closely
allied to taxa in the Far East. Curiously, the Far Eastern taxon in nearly every
case occurs entirely or principally in Seasonal Evergreen forest. It is no longer
possible, on biogeographic grounds to determine whether dipterocarps origi
nally arrived in Asia, which they almost certainly did by way of the Deccan
plate (l0, 17), principally or entirely as denizens of the mixed forests of the
aseasonal zone, although the three archaic genera endemic to the Deccan plate
and Seychelles are thus restricted. Many taxa of the aseasonal Far East also
have seasonal evergreen forest vicariants. If dipterocarps invaded from the
west, the original Asian dipterocarps may have been aseasonal mixed rain
forest species. They likely speciated into Seasonal Evergreen forests and
spread eastwards. Some of these further speciated into the aseasonal mixed
forests of the Far East, forming the progenitors of the rich modem flora there
(7). Independent evidence for a seasonal origin for the dipterocarp flora of the
aseasonal Far East is provided by the climatic cue for flowering which appears
to be a drop in minimum night temperature. This occurs annually in the
seasonal tropics, but at several year intervals in the aseasonal tropics (13).
The Dry Dipterocarp forest species all seem to be of recent origin, however,
as already implied by the evidence of hybridization.
Wallace's Line, and the Torres Straits, have been formidable barriers to
dipterocarp spread. Only one species is shared between Borneo and Sulawesi,
and that is a riparian species with water-dispersed fruit. Dipterocarps are
unknown in Australia and the Bismark Archipelago. A striking exception to
these restricted patterns is provided by Vatica odorata (Griff.) Sym. ssp
mindanensis (Foxw.) Ashton of the Philippines and northern Borneo, which
also occurs in Hainan and Kwangsi; and by Shorea falciferoides Foxw. of the
Philippines which is closely allied to a species so far known only from the
Quilon peninsula of coastal central Vietnam, S. falcata Vidal. The most
parsimonious explanation for such distributions, in the absence of a common
continental shelf between the two regions is typhoon dispersal, westward.

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361

Within the aseasonal Far East, west of Wallace's Line, dipterocarps mani
fest three patterns of distribution: (a) widespread, which includes several that
also occur in the Seasonal Evergreen Dipterocarp forests of Indo-Burma; (b)
island-wide endemics; and (c) local endemics and disjuncts (7). The third
category includes most taxa with wingless fruits, whereas only one wing
less fruited species, Shorea multiflora (Buck) Sym. falls into the first cate
gory.
Local endemism is unusual among dipterocarps in the forests of the Far
East. Hopea contains a number of local endemic and disjunct, apparently
relict distributions in the Seasonal Evergreen forest isolates of Indo-China and
southern India. In Sri Lanka, Stemonoporus is unique in the subfamily in the
absence of any widespread taxa. All species are more or less local endemics,
sometimes apparently vicarious on the main mountain masses but sometimes
also geographically, though not apparently ecologically, sympatric (17). To
this we return, but I now wish to address a more general fact-that the vast
majority of dipterocarps within the aseasonal zones are restricted in their
distribution by their edaphic and altitudinal ranges.
Dipterocarp species, particularly in the aseasonal tropics, almost invariably
occupy narrow ranges of soil fertility. Distribution is correlated with a number
of soil factors, but primarily with magnesium and then phosphorus (18, 14).
Widespread species are confined to widespread soils, endemics and disjuncts
to soils (and rock substrates) themselves of local and disjunct distribution
(10). No dipterocarps are endemic to limestone or to ultramaphic rocks,
though morphologically distinct forms occur, particularly on the latter (10).
Within a landscape on uniform rock, soil fertility is often correlated with
physiography, and congcneric and consectional species may occupy distinct
but overlapping ranges along the catena (5). Ashton et al (15) have shown that
dipterocarp species richness within individual habitats increases linearly with
total mineral soil magnesium concentration up to a threshold of about 1300
ppm Mg, above which close correlation is lost and there is a sudden drop in
species richness. In Borneo this represents a range of between 9 and 57
dipterocarp species in samples of 1000 trees. Species richness of Mixed
Dipterocarp forest is also, and independently, correlated with within-sample
variation in soil fertility up to but not above the same total magnesium
threshold, a point to which I return. Above the fertility threshold, dipterocarp
species richness continues to fall erratically as soil Mg and P values increase,
but the abundance of the commonest species markedly increases. The soil
specificity and center of edaphic distribution of dipterocarps is compatible
with their apparently obligate association with ectotrophic mycorrhiza, and
with the possibility that some of these symbionts may be host specific (54, 55,
personal communication). This implies that some secondary, species-specific
'metabolites may act as cues to mycorrhizal infestation. The pattern of tree
species-richness overall in Mixed Dipterocarp forests is similar to that of

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ASHTON

the dipterocarps themselves, even though some large individual families

including Meliaceae, Rubiaceae, and Euphorbiaceae are most species-rich on
the most mesic fertile sites (5).
Up to 11 consectional Shorea species are known to co-occur in a single
forest (Figure 1). An understanding of how these populations of closely
related taxa are maintained in mixture is central to our understanding of the
maintenance of species richness in rain forests, while their cladistic rela
tionships may throw light on the evolution of species richness (51 and in
press). Cladistic and genetic analyses of interspecific relations between clades
are still awaited. Ecological and biogeographic patterns among smaller groups
of species, closely related on morphological and isozymal evidence, and
among interspecific taxa suggest that speciation is generally but perhaps not
always geographically or ecologically allopatric (6, 11, 31).
Host specific mycorrhiza could allow differential exploitation of soil nutri
ent resources among consectional species. The ecological distribution of the
ten species of Shorea section Doona in Sri Lanka can be distinguished along
gradients of altitude, soil fertility (and the catena), and light response (Figure
2). Shorea trapezijolia (Thw. ) Ashton and S. congestiflora (Thw. ) Ashton in
section Doona, Shorea leprosula (section Mutica) and Dryobalanops lan-

Figure 2

Schematic ecological range, in the wet zone forests of Sri Lanka, of the species of

Shorea, section Doona. Key:

affinis

e.

gestiflora

S. trapezijolia

a.

b. S. gardneri c. S. zeylanica d. S.
g. S. disticha h. S. worthingtonii i. S. con

Shorea cordijolia

f. S. megistophylla

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DIPTEROCARP BIOLOGY

363

ceolata Burck differ from other members of their groups in their exceptional
maximal growth rates (16; P.M.S. Ashton, in preparation). Differences in
shade tolerances among members of quasigenera are well known to foresters.
All dipterocarps appear, remarkably, to have low compensation points, and
the differences appear to be principally attributable to differences in max
imum rates of photosynthesis (A. Moad, in preparation) and to rates of dark
respiration (R. A. Sunderland, unpublished).
The species with highest maximum growth rates overall are confined to
fertile soils. Dryobalanops lanceolata and also Parashorea malaanonan
(Bleo) Merrill are unusual in combining high maximum growth rates with
high shade tolerance as juveniles (A. Moad, personal communication). P.
Hall (personal communication) has found evidence from Borneo that seedling
survivorship of D. lanceolata is greater in the deep shade of Mixed Diptero
carp forest on basalt-derived soil than is that of D. beccarii in the relatively
open light conditions within forests on infertile leached yellow sands. The
ratios of adults to saplings to seedlings, estimated in the same year, were
1:5.2:87.6 in D. lanceolata. 1:1.5:46.3 in D. beccarii. High juvenile
survivorship in shade has also been noticed among some Shorea species on
volcanic soils in the Philippines (21). It is possible, where available soil
nitrogen is high, that species can maintain high enough photosynthetic rates in
shade to compensate for night respiration rates (F. A. Bazzaz, personal
communication). This may explain why D. lanceolata is among the dominant
species on fertile soils and, conversely, why species dominance is un
correlated with species richness throughout most of the range of less fertile
soils.
In most quasigenera, floral morphology is ostensibly identical among
closely related species. Chan & Appanah (26) have shown that six co
occurring members of Shorea section Mutica in Pasoh forest, peninsular
Malaysia, flower in overlapping sequence. Casual observations suggest that
this happens in other dipterocarp groups where several species co-occur (6).
Chan & Appanah found that flowering is very highly synchronized within
populations, but that the individuals of each succeeding species flower over
successively longer periods. Interestingly, the two-and one-half month period
over which all six species flowered is no longer than the flowering period of
Shorea robusta Roxb. , a single species dominant of Dry Dipterocarp forests
in northeast India in which individuals are more loosely synchronized. Ashton
et al (13) demonstrated that this sequential flowering is significantly nonran
dom. Dipterocarps, including the species in question, are outbreeders (25; C.
V. S. and I. A. U. N . Guantilleke in preparation). Sequential flowering has
presumably arisen as a consequence of lower fruit set during times of flower
ing overlap among species sharing a common pollinator. Co-occurrence of
such species series is only possible where barriers to hybridization are strong.
Extrapolating back on the basis of the length and time of the flowering

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ASHTON

periods of the six species, Ashton et al identified the time when inflorescence
development probably began. They discovered that over a 20-year period, a
2 C depression of minimum night temperature occurred for several days at
this same interval before each general flowering, and at no other time. They
further found a broad correlation between mass flowering seasons in east
facing lowlands and the EI Nino climatic event over the Pacific, when the
aseasonal region of the Far East may experience prolonged periods of clear
skies and relatively low humidity, hence lower than average night tempera
tures. This can explain why dipterocarps flower annually in the seasonal
tropics, and why mast fruiting has not been observed in the Mixed Diptero
carp forests of Sri Lanka, outside the main zone of EI Nino influence. The
evidence of Ashton et al also implies that dipterocarps were preadapted by
their flowering physiology to become mast fruiters when they invaded the
aseasonal lowlands of the Far East. It is remarkable that the fruiting of the six
species that flowered in close sequence coincide with one another and with the
other species in the family. This lends further strong support to Janzen's (40)
hypothesis and suggests that new species immigrants to a forest community
become entrained through selective predation to fruit synchronously with
those already established (13).
In Semengoh forest, Sarawak, East Malaysia, 11 species of Shorea section
Mutica co-occur (Table 1). Some of the most abundant species are common to
both Semengoh and Pasoh, which is 1000 km to the west across the South
China Sea. S. acuminata Dyer and S. quadrinervis Sioot. are vicariants.
Others such as S. dasyphylla Foxw. and S. parvifolia Dyer change their rank
order. We believe this is due to edaphic differences between the two sites,
because the most abundant species are remarkably constant on the same soil in
different localities in northwest Borneo (15). The difference in number of
consectional species at the two localities is attributable entirely to the different
number of species of low population density in each, and this has also been
found to explain differences in forest species richness overall (15). Un
derstanding how species of low population density (which comprise the vast
majority in species rich forests) are maintained is crucial to understanding
how species richness is maintained overall.
Some of the rare species in the Semengoh example, such as S. slootenii
Wood ex Ashton, S. rugosa Heim and S. hemsleyana Brandis seem always to
be rare, occurring as scattered individuals or clumps. Others clearly are not. A
comparison of the populations of Shorea dasyphyUa in Pasoh and Semengoh
forests provides one example (Table 1). Some species such as Dipterocarpus
gracilis Bl. and Anisoptera costata (Korth) Bl. are abundant in the seasonal
parts of their range but generally occur as far scattered individuals in aseason
al Borneo. Low population density may reduce fecundity in outbreeding trees,
and Chan (3) found evidence of this in the low density population of S.

DIPTEROCARP BIOLOGY
Table 1

365

Relative densities of reproductive individuals Shorea, sec

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tion Mutica, species in two low land mixed Dipterocarp forests

Pasoh Research Forest

Semengoh Forest

Peninsular M alaysia

Sarawak

Shorea acuminata

3 . 0/ha

Shorea quadrinervis

4 . 7/ha

Shorea parvifolia

2 . 8/ha

Shorea scabrida

4.7/ha

Shorea leprosula

2 . 7/ha

Shorea macroptera

4 . 6/ha

Shorea macroptera

2.4/ha

Shorea dasyphylla

3 . 5/ha

Shorea lepidota

1 . 6/ha

Shorea slootenii

1 . 1/ha

Shorea dasyphylla

O . 3/ha

Shorea ovata

I . O/ha

Shorea parvifolia

O.9/ha

Shorea Jeprosula

O . 2/ha

Shorea rubra

O . l Iha

Shorea rugosa

O . lIha

Shorea hemsleyana

O.07/ha

dasyphylla and in isolated individuals of S. leprosula. Chan (24, 1 1) found S.

dasyphylla to be the only species, among the 6 members of Shorea section
Mutica whose flowering phenology he studied, whose flowering period en
tirely overlapped with those of other species. It strains the imagination to
believe that all 11 species at Semengoh possess distinct flowering times. The
phenology and reproductive biology of the rarer species there would repay
study.
It is curious that dipterocarps of the seasonal tropics tend to have higher
pollen/ovule ratios than do those of the aseasonal tropics (9). In those few
quasigenera where staminal number varies, such as Shorea sections Shorea
and Anthoshorea, and most particularly in some understory Hopea and Stemo
noporus, a broad albeit inconsistent tendency exists for local endemics to
have reduced number of stamens. In Stemonoporus this is accompanied also
by a reduction of the number of ovules to four. It is unknown whether this
trend is accompanied by increases in self-compatibility.
These patterns would appear to be consistent with the presence-to a still
largely unknown extent but on inferential evidence probable in many
genera--of apomixis through pseudogamous agamospermy (4 1 , 42). Aga
mospermy has been confirmed in one species of Hopea and two of Shorea and
inferred, on the presence of polyembryony or triploidy, in some 10 of 70
species examined cytologically to date. Apomixis has been found or inferred
in abundant and widespread species such as S. ovalis and S. macroptera, but
also in one local endemic of specialized habitat (Hopea subalata Sym.), in
one gregarious species of river banks (H. odorata Roxb.), and another of Dry

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ASHTON

Dipterocarp forest (Dipterocarpus tuberculatus Roxb. ). S. macroptera is the

first of its section to come into flower. Pollinator numbers may not yet be at
full strength then, and it may be supposed that S. macroptera experiences the
greatest vicissitudes in securing successful cross-pollination. Certainly,
adventive embryony provides a means of maintaining fecundity without
reduction of heterozygosity, but a cost is paid in reduced genetic variability at
population level.
The proportion of seeds with multiple and perhaps apomictic embryos
varies between species, and in some cases between individuals within pop
ulations (24, 13) . Isozymal analysis of population samples of reproductive
individuals of Shorea species indicates that genetic variability can be remark
ably high (31, 32, D. Buckley in preparation). In a population sample of
almost mature individuals of S. trapezijlora, variation conformed with Hardy
Weinberg expectations. Whether this is due to outcrossing patterns or to
differential mortality between the progeny of selfed and cross-pollinated
flowers is so far unknown (D. Buckley in preparation). Gan (30) and Chan
(25) had evidence that isozymal and leaf morphological variation within
population samples of S. leprosula increases with distances between trees up
to 200 m, and within-population genetic variability can exceed variability
between populations 100 km distant. On the other hand Gan (30) found
sibling seedlings to be isozymally uniform in the apomictic S. ovalis, though
this result could have been an artifact of tetraploidy.
CONCLUSION

I argue that too much emphasis has been put on the species as an independent
unit to test for niche specificity in species-rich terrestrial plant communities
such as tropical rain forests. I have endeavored to show that dipterocarp taxa
in all levels in the systematic hierarchy possess character traits upon which

selection may be expected to act uniformly in nature. Families, I suggest, are

in competition with one another. The Dipterocarpoideae seem to com
petitively exclude other families under certain conditions, and not necessarily
those in which dipterocarp species richness is maximal more than under other
conditions. Selection acts on different character traits at different taxonomic
levels. Hubbell & Foster's (39) search for significant positive or negative
association between the spatial and temporal patterns of different species
populations, and between them and habitat variation, as a test of the equilibri
um hypothesis of community species composition, should be extended to taxa
of higher rank (11). Association can be expected to be manifest also between
taxa of differing rank. So far though, the relationship between phylogeny and
ecology is largely unknown above the species level of the taxonomic
hierarchy.

DIPTEROCARP BIOLOGY

367

Patterns of species richness of Dipterocarpaceae among different forest

types sharing a common climate conform extraordinarily closely with Til
man ' s (56, 57) equilibrium model for the relationship between species rich
ness and resource availability. The data currently available, though in
ferential, do suggest that the ecological range and performance of dipterocarp
taxa are influenced by a wide array of climatic and edaphic variables (see e.g.

18). In combination, it could easily be argued that every species in the mixed
rain forest may possess unique ecological requirements. But to further sug

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gest, in the case of sessile organisms of large size like trees, that their
ecological differences have evolved as a consequence of direct interspecific
competition is patently absurd. The high local genetic variability, yet regional
uniformity, of morphological and genetic variation that seems to characterize
some of the more abundant dipterocarps, such as Shorea leprosula and S.

trapezifolia, suggests that they are panmictic species in which (curiously, in

view of the biological heterogeneity of their habitats) selection acts uniformly
throughout their geographical ranges. W. Smits (personal communication)
has suggested that poor seed dispersal in combination with stringent require
ments for maintaining species-specific mycorrhizal symbionts could result in
the pattern of variation observed, and these might also explain the sharp
though subtle discontinuities in variation that differentiate taxa, and the
apparent rarity of hybridization. Some of the scant population genetic data
available and the existence of adventive embryony do cast doubt on natural
selection, that is, equilibrium phenomena, as the sole mediator of floristic
composition and species richness ( 1 5). Apomixis may serve to sustain fecund
ity in populations of low density and may also allow survival of taxa occupy
ing habitat fragments of limited area, where space precludes the full species
complement of a community type and therefore where species composition
and abundances will be unpredictable and substantially determ!ned by
stochastic processes of immigration and extinction. Selective processes
appear to determine maximum population density, but extinction in these
species-rich communities, stable over time, may essentially be a stochastic
process if fecundity can be maintained (13). The key to understanding the role
of selection in determining species composition will be the knowledge of
patterns of change in gene frequency which take place as sibling cohorts
develop to reproductive mat. "ity.
I believe that the principles that govern the role of dipterocarps in the
structure of tropical rain forests are general to all terrestrial rainforest plants
and perhaps also to epiphytes. Obviously, differences of detail exist between
taxa and guilds. Tree families known to be mycorrhizal, such as Myrtaceae,
show patterns similar to those of dipterocarps (5). Agamospermy is known
among many of these also (12). Others such as Meliaceae and Sapindaceae
differ in both species distribution and breeding systems (11 , 13). The role of

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ASHTON

non-equilibrium, island biogeographic processes may be expected to be larger

among epiphytes than terrestrial organisms. In every case, a fuller un
derstanding can only be reached by combining systematic with ecological
approaches.

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