REVIEWS

The populationgenetic consequencesof

habitat fragmentationfor plants
Andrew Young, .Tim Boyle and Tony Brown
Habitat fragmentation reduces the size
Population genetic variation
abitat fragmentation-the
and increases the spatial isolation
Population genetic variation
reduction of continuous
of plant populations. Initial predictions
consists of the sum of all genhabitat into several smaller
have been that such changes will be
etic variation among individuals
spatially isolated remaccompanied by an erosion of genetic
nants -is a significant threat to the
within a population and is measvariation and increased interpopulation
maintenance of biodiversity in
ured by parameters such as allelic
genetic divergence due to increased
richness (A) and gene diversity
many terrestrial ecosystems. It
random genetic drift, elevated inbreeding
disturbs biological and physical
(H,), which is commonly referred
and reduced gene flow. Results of
ecosystem processesl-3. So far,
to as expected heterozygosity.
recent empirical studies suggest that
research into the biological effects
Theoretically, habitat fragmentawhile genetic variation may decrease
of habitat fragmentation has been
tion can cause a loss of population
with reduced remnant population size,
primarily of an ecological nature,
genetic variation in two main
concentrating on changes in spenot all fragmentation events lead to
ways. First, reductions in popucies richness and composition as
genetic losses and different types of
lation size at the time of fragmengenetic variation (e.g. allozyme and
well as population dynamic&s.
tation create genetic bottlenecks
quantitative varlation) may respond
Recently however, attention has
because remaining individuals
differently. In some circumstances,
contain only a small sample of
passed to the population genetic
fragmentation actually appears to
the original gene pool (Box 1).
consequences of fragmentation
increase gene flow among remnant
Subsequent to this initial loss of
and their implications for species
populations, breaking down local
variation, remnant populations
conservation6~7.
genetlc structure.
Initial predictions about the
that remain small and isolated for
genetic consequences of habitat
several generations continue to
fragmentation focus on the relose alleles due to random genetic
Andrew Young and Tony Brown are at the Centre for
duced size and increased spatial
drift16J7. In the absence of immiPlant Biodiversity Research, Division of Plant
gration and selection, the mean
isolation of populations occupying
Industry, Commonwealth Scientific and Industrial
habitat remnantsQ. Theoretically,
expected change in allele freResearch Organization, Canberra, Australia;
quency (A@due to one generation
such population changes lead
Tim Boyle is at the Centre for International Forestry
of drift is:
to an erosion of genetic variResearch, Bogor, Indonesia.
ation and increased interpopuA9= ~(1- 9)/2Ne
lation genetic divergence through:
where N, is the variance effective
(1) increased random genetic
drift, (2) elevated inbreeding, (3) reduced interpopupopulation size*s. The probability of fixation for a particular
allele is equal to its initial frequency.
lation gene flow, and (4) increased probability of local
extinction of demes within a metapopulationlOJ*. Such
Empirical data generally confirm that reductions in geneffects have serious implications for species persistence.
etic variation accompany reductions in plant population size
In the short term, a loss of heterozygosity can reduce
associated with habitat fragmentation. Studies of the herbaindividual fitness and lower remnant population viability.
ceous perennials Saluia pratensis, Scabiosa columbaria8 and
In the longer term, reduced allelic richness may limit
Gentiana pneumonanthe
and the tree Eucalyptus albenslg
have all identified significant positive logarithmic relationa species ability to respond to changing selection
ships between remnant population size and both polymorpressures*.
phism and allelic richness (A) at allozyme loci (Fig. 1).
For plants, the genetic effects of habitat fragmentation
are likely to be complicated by their sessile habit, interGenerally, population size had less effect on gene diversity
specific differences in longevity, generation time and presuggesting that, as expected, alleles lost are mainly those
fragmentation abundance, their wide variety of sexual and
initially present at low frequencies.
asexual reproductive systems, the possibility of gene flow
Intriguingly, Prober and Browns also observed some effects of population isolation on genetic variation. Small remby both pollen and seed, the storage of genetic material as
seed, and their interactions with animal pollination and disnant populations (~500 reproductive individuals) of E. a&ens
persal vectors, which may themselves be affected by frag- that were less than 250 m from a larger population exhibited
mentation events.
no obvious reductions in allelic richness, while moreGenetic studies have now been conducted on several
isolated remnants of a similar size were genetically depauplant species occupying fragmented grassland, heathland,
perate (Fig. lc). This is an important result as it points to
woodland and forest habitats. These studies provide em- the possible existence of fragmentation thresholds, in this
pirical insights into the population genetic consequences
case an isolation threshold, up to which effects on genetic
of habitat fragmentation. This article reviews the results of variation are not encountered, but beyond which variation
these studies regarding the effects of fragmentation on
is lost.
(1) population genetic variation, (2) heterozygosity, inbreedGiven that the effect of genetic drift depends on the numing and fitness, and (3) gene flow and interpopulation gen- ber of generations for which a population remains small,
etic divergence.
then species with short generation times, such as herbs,

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should show a greater loss of variation than species with
long generation times, for example, trees. However, this
simple prediction is complicated by the fact that overlap of
generations may reduce effective population sizes in longlived species*O.The similarity in response of the three herb
species and E. dens therefore suggests that losses of
genetic variation are primarily due to the creation of genetic
bottlenecks, rather than to the subsequent action of genetic
drift. Indeed, given the population sizes involved, the effects
of drift are expected to be minor over the few generations
(probably ~5) that these four species have been subject to
fragmentation.
In a recent test of the effects of genetic drift in remnant
populations that controlled for genetic bottleneck effects,
Young et al.9compared the levels of allozyme variation between eight remnant populations OfACerSQCChQnUn
and eight
similarly sized samples from large intact populations. Remnant populations as small as 96 trees showed no signs of reduced genetic variation, suggesting that there has been little
effect of increased genetic drift in the 150-200 years (2-3 generations) since they were created by forest fragmentation.
The previous studies address the effects of fragmentation on single-locus allozyme variation. However, much of
the adaptively significant phenotypic variation in plant populations is under polygenic control. Changes in population
size and structure can also erode this quantitative genetic
variation (Box 2). Such effects are difficult to detect, requiring estimation of the genetic components of phenotypic
variance (Box 2).
Ouberg et ~1.31found positive correlations between remnant reproductive population size and phenotypic variances
for adaptive traits related to growth rate in Scabiosa columbaria and Salvia pratensis plants that were grown in a common environment. hi contrast, Oostermeijer et Q/.~*found
very few relationships between population size and variance for phenotypic and growth traits among remnant populations of Gentiana pneumonanthe. Those that did exist were
mainly negative, with small populations exhibiting higher
coefficients of variation than large populations. These results are less conclusive than allozyme studies of the same
species that we discussed previously. One reason for this is
that the results are based on phenotypic variation, which
includes confounding effects of environment as well as effects of non-additive components of genetic variance. In a
more recent study, Widen and Andersson33 derived additive
genetic variances for several quantitative traits in one large
and one small population of Senecio integrifofius. On average, these were higher in the small, disturbed population
than in the large, undisturbed one.
Increases in quantitative genetic variation associated
with small population size, such as those apparently ob
served for Gentiana pneumonanthe and Senecio integrifolius,
have been observed previously in experimental studies of
plants34.Several explanations are plausible. increased pheno
typic variances could result from segregation and recombination under increased selfing in small populations. Increased
additive genetic variances may reflect a conversion of
non-additive genetic variance to additive variance in small
populations (Box 2). Finally, if reduced population size is
related to reduced heterozygosity, as is the case for G.
pneumonanthe, increased quantitative variation could also
be due to lower developmental homeostasis of homozygous
individualsszJ5.
Heterozygosity, inbreeding and fitness
Genetic variation at the level of the individual is measured in terms of heterozygosity (H). The number and fre414

Box I. Theoretical relationship between remnant

population size and allelic richness
Assuming that, before fragmentation, alleles are randomly distributed
among and within panmictic populations, the number of alleles
retained in remnant populations will depend on their size and the initial
distribution of allele frequencies, with rarer alleles being at greatest risk
of loss. The allelic richness (A)retained in a random sample of individuals (in this case, a remnant population) has an approximately logarithmic relationship13 to the sample size of S gametes (S/2 diploid
individuals) when 10 < S < N, (where N, is the variance effective
population size) and can be estimated from:
A = elo&[(S+

6)/6] t 0.6

where 0.1~ 0 = 4N,p, and p is the mutation rate.

This formula is based on the equilibrium distribution of allele fre
quencies generated by Kimura and Crows14 model of an infinite number of neutral alleles.
Assuming that N, - 0.5N (where N is population size) and a mutation rate of 1 x10-s, a reduction in population size from 10 000 to
250 individuals will result in a loss of allelic richness of about 22%.
Reduction in population size of this order of magnitude resulting from
habitat fragmentation appears to be relatively common (see fig. 1). If
there is spatial genetic structure, with clumping of genetically similar
individuals, then the expected loss of alleles is increasedIs.

quency of alleles at a locus, the amount of inbreeding, and

the type and intensity of naturalselection, all determine the
level of heterozygosity within a population. Habitat fragmentation can decrease heterozygosity in two ways. First, it is
lost directly as a function of reduced gene diversity in remnant populations. However, this effect is likely to be small,
as the loss of gene diversity is an inverse function of population sizei2.
Second, and of greater significance, heterozygosity erodes
when inbreeding accompanies fragmentation. Such inbreeding arises from increased self-pollination, or when the remaining mates are related through recent common ancestry
in small populations. Changes to the pollination system,
such as in the composition of pollinator guilds, or effects on
the behaviour of individual pollinator species, can also mediate changes to the mating system. Much evidence now
exists showing effects of habitat fragmentation on pollinator
speciessJ6.37.Since such changes immediately affect mating
system parameters, heterozygosity is expected to respond
more rapidly to fragmentation than allelic richness or gene
diversity.
Allozyme studies in two species, Eucdyptus albenslg and
Gentiana pneumonanthell, have examined the effect of remnant population size on heterozygosity. Both of the studies
showed positive logarithmic relationships between remnant
population size and heterozygosity at allozyme loci (Fig. 2)
suggesting that decreases in heterozygosity accompany reductions in population size. This loss of variation is greater
than expected due to bottlenecks and genetic drift alone,
where the change in gene diversity is predicted to be:
AH, = -H, 1.9

where S is the number of gamete@.

Presumably this extra loss of heterozygosity is due to
increased inbreeding, but this is difficult to assess, as direct
estimates of mating system parameters are not available
for the species examined. Fixation indices for Eucalyptus
&ens
showed no obvious relationship to population
size, though negative effects of density were detected suggesting that reduced density may increase inbreeding in
population remnantsig. In two other studies, comparisons
of outcrossing rates between large and small remnant
populations of Salvia pratensis38 and Scabiosa coiumbriQ3g
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showed no evidence of increased inbreeding in small
dispersal or pollination, increased interpopulation distances
populations.
can reduce gene flow directly. While for animal-pollinated
The primary concern with decline in heterozygosity in
or animal-dispersed plants, this can be indirect, owing to
remnant populations is the possibility of negative fitness
effects on the associated species. Powell and Powell36found
effects due to inbreeding depression (Box 3) and associthat a 100m wide clearing formed an effective barrier to the
ated reductions in population viability. However, studies
movement of four euglossine bee species between remthat explicitly link habitat fragmentation with reduced
nants of Amazonian tropical forest.
heterozygosity and lowered
fitness are rare. In one such
study, Oostermeijer et al.35
has demonstrated a posi(a) Salvia pratensis
tive relationship between
1.60
0.60 .
heterozygosity and fitness
for Gentiana pneumonanthe,
0.45
a species that has lower
heterozygosity in small rem0.30 I
.A
>
t
nant populations.
r = 0.62
r = 0.54
.
An important issue reP< 0.05
-.15
0.15 P c 0.01
garding the effect of inI I I11111,
I I I,,,,,, I I,_ 1.0
breeding depression on rem , a 11 a 11 8 hJ(U
0
1
10
102
103
104
1
10
10
103
104
nant population viability is
whether intense inbreeding
in small populations, coupled
(b) Scabiosa columbaria
with selection against less
fit homozygotes, might eliminate deleterious alleles and
restore fitness. This is known
as purging genetic load and
is currently the subject of
considerable research and
debate411@44
(Box 3).
So far, comparative studies of genetic load in large
10
102
103
104
105
and small remnant populations of three species -Suluia

??

::I

o.60
7

(c) Eucalyptus albens

pratensis45, Scabiosa columbaria46 and Senecio integrifolius47 - have found no evi-

dence of reduced genetic

load in small populations.
They tested for increased
fitness of inbred progeny
or lower numbers of lethal
equivalents. This apparent
lack of purging may be because the observed
inbreeding depression was due
primarily to many genes of
small effect, in which case
purging of load is difficul?,
or because substantial differences in genetic load take
time to evolve, and small differences are difficult to
detect experimentally.
Gene flow and
interpopulation divergence
It is generally assumed
that the loss of populations
associated with habitat fragmentation, and the changes
in the intervening land use
between those that remain,
reduce interpopulation gene
flow6J79.For species that rely
on gravity or wind for seed
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p
3.2

.
0.60

c
10

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104

, , , , ,,(

, , , , ,,,

102

103

10

3.0

P < 0.05

aa

2.4

I,# 2.2
104

(d) Gentiana pneumonanthe

0.35 -

0.20,i
0.15
0.10

??
*

.
.

??*

11111
j 111111
8llld
10

10

103

- 1.25

-1.15
-1.10
_,,05

I I ,,,,,,,, I ,,,,,,,, ,,,,,,,, ,,- 1 .oo

11111
8c104

r= 0.33
PcO.11

r = 0.49
P c 0.05

1.30

105

Population

10

102

103

104

105

size

Fig. 1. Relationships between reproductive population size (log scale) and population genetic variation at allozyme loci for
remnant populations of: (a) Salvia pratensis*, (b) Scabiosa columbaria*, (c) Eucalyptus alben@ (open circles are small
populations isolated by ~250 m), and (d) Gentiana pneumonanthell. Polymorphism is the proportion of loci at which the
frequency of the most common allele is cO.99. Allelic richness (A) is the average number of alleles per locus (G. pneume
nanthe values are for effective number of alleles). r is the correlation coefficient. P is probability.

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Given a stable population structure, and assuming an
Island Model of gene flow, interpopulation genetic divergence will increase due to random genetic drift, particularly
when population sizes and gene flow are such that N,m < 1
(where m is the fraction of migrants per generation)@. Conversely, only a very small amount of gene flow (approximately 1 individual per generation) is required to reduce the
loss of alleles due to genetic drift.
If population structure is unstable, and species persist
as metapopulation9, habitat fragmentation may also affect
genetic divergence among remnant populations through
changes in the frequency of colonization and extinction
events, or in the number of sources of colonists23,*5,26.
Extinction and colonization rates of more than twice the migration
rate will substantially reduce genetic variance among
subpopulations within a metapopulationz3. Reducing the
number of subpopulations from which colonists are
drawn increases differentiation26. Temporal and spatial variation in migration rates and effective subpopulation sizes
will also affect variances among subpopulations, with spatial heterogeneity having more influence than temporal
differences25.
So far, only two studies have examined whether habitat
fragmentation leads to increased genetic divergence among
remnant plant populations. In both cases, the species studied
has been Acersaccharum, which is both wind and insect pollinated and has wind dispersed seed. ForC et al.Qcompared
interpopulation genetic divergence at eight allozyme loci
between pre-fragmentation and post-fragmentation cohorts
of 15A. saccharum remnant populations in Ohio, USA.They
found that genetic divergence among post-fragmentation
cohorts was less than half that among pre-fragmentation cohorts, indicating a reduction in genetic differentiation since
fragmentation, and suggesting increased interpopulation
gene flow. However, this result may also simply reflect
greater variances for gene frequency estimates for prefragmentation cohorts. These were based on much smaller
sample sizes than were post-fragmentation estimates. Sub
sequently, more exhaustive intercohort comparisons on a
subset of the same populations revealed the presence
of allozyme alleles in remnant population embryo cohorts
that did not occur in their respective parental cohort@.
This provides clear evidence of gene flow into remnant
populations.
In the second comparison, the average genetic distance
between eight remnant Acersucchuvum populations was similar to that for eight population samples taken over the same
spatial scale from intact populationsg. A marginal increase in
the spread of allozyme alleles among remnant populations,
combined with their higher mean polymorphism, again
pointed to increased interpopulation gene flow as a consequence of fragmentation for this tree species.
The hypothesis that habitat fragmentation can lead to
increased rather than decreased interpopulation gene flow
and possibly higher population genetic variation is an interesting one. High genetic variation is desirable for maximizing
population viability and evolutionary potential. Mixing of
remnant population gene pools may also mean that further
population losses will have less impact on species-level genetic variation than the original fragmentation eventl5. However, if interpopulation genetic structure was originally
strong, such a redistribution of genetic variation may have
at least one negative consequence, and that is outbreeding
depression due to the break-up of locally adaptive gene
complexes. Whether outbreeding depression is a major or
persisting consequence of habitat fragmentation is an open
questionlzJ6.
416

Box 2. Effects of habitat fragmentation

on quantitative genetic variances

Partitioning quantitative genetic variances

The total variance for a phenotypic trait VP (phenotypic variance) consists of three components: additive genetic variance(V,), non-additive
genetic variance (V,,), and environmental variance (V,). Accurate estimation of V, from common environment experiments requires either
knowledge of mating system parameters, or the use of clonal material
to estimate V, (Ref. 18). The narrow-sense heritability (h2) is equal to
V,/V,, and measures how much of the observed phenotypic variance
is due to underlying additive genetic variance. Inbreeding reduces
heritability according to the formula:
h:= [hz(l-F,)]/(l-h*F,)
where F,,is the inbreeding coefficient at time t (Ref. 18).
Quantitatlve genetic variances in remnant populations
Impact ofgenetic drift on a sing/e population
For a single isolated remnant population, additive genetic variance for
neutral traits is lost due to genetic drift at a rate per generation of:
AV,= -V,I2N,t

V,

where V, is the input of genetic variance by mutation and N, is the variance effective population size*l.
Interaction of genetic drift and migration in subdivided populations
Remnant populations often exist as mosaics of partially isolated pop&
lations. Changes in quantitative genetic variances in such subdivided
populations depend on the balance between genetic drift and migration*2-26. In the absence of diversifying selection, the total genetic variance maintained within a subdivided population with a stable structure
is equal to the total expected in a panmictic population of equal sizeZ3.
The variance among subpopulations increases with their number and
is inversely proportional to the migration rate. If population structure is
not stable, with extinction and recolonization of subpopulations occurring within a metapopulatiorP,
the genetic variance maintained within
subpopulations is reduced owing to decreased local effective population sizes as a result of founder effect+.
Non-additive genetic variance
Increased heritabilities and additive genetic variances have been
observed following severe reductions in population size28. During such
population bottlenecks non-additive variance can be converted into additive variance. This is because increasing fixation at some loci reduces
the multilocus diversity, and hence the number of genetic environments
in which a polymorphism is expressed2g. Traits related to fitness often
have high non-additive genetic variances, so founder events could pr@
mote Increased variation in fitness owing to this conversion of nonadditive to additive variance29.30.

Conclusions
Current empirical results clearly show that habitat fragmentation has population genetic consequences for plants.
However, these would appear to be more varied than predicted from simple population genetics models.
For the species examined so far, reductions in remnant
population size usually erode genetic variation; both as population allelic richness and individual heterozygosity. These
losses are more likely due to the formation of genetic bottlenecks at the time of fragmentation and to subsequent inbreeding in small populations (though there is no direct evidence for increased inbreeding), than to effects of continuing
random genetic drift. Given this, remnant populations should
not be viewed as being in mutation-drift balance, and current levels of genetic variation may provide little indication
of a populations ability to retain variation in the long term.
However, it is also already obvious that not all fragmentation events lead to reduced genetic variation for plants.
The data from Eucalyptus &ens point to the possible existence of fragmentation thresholds up to which genetic variation is not lostlg. These results suggest that remnant
populations can play a significant role in maintaining the
genetic diversity of a species.
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Box 3. Inbreeding depression and purging of genetic load

(a) Eucalyptusalbens
0.33
0.31

Models of inbreeding depression

Inbreeding depression is the reduction in fitness of progeny resulting from selfing
or mating among relatives. Two models have been proposed to account for inbreecC
ing depression. Under the partial or complete dominance model, reduced fitness
arises from homozygosity for recessive deleterious alleles. Under the overdominance model, heterozygous genotypes have greater fitness than homozygotes, and
it is the erosion of heterozygosity per se that reduces fitness. Current empirical
data favour the partial or complete dominance model40.

.
1

g.:-l;:--::i
102

10

103

104

s.

.Ti

ic

!$

(b) Gentiana pneumonanthe

4
0.16

r = u.Su
P< 0.10

0.06
0.04
1

10

10

103

Population

size

104

Fig. 2. Relationships between reproductive population size (log scale)

and heterozygosity (H) at allozyme loci for remnant populations of:
(a) Eucalyptus albenslg and (b) Gentiana pneumonanthell.
Heterozygosity is the proportion of loci at which an individual carries more than
one allele. r is the correlation coefficient. P is probability.

Another important observation has been that allozyme

and quantitative variation can respond differently to changes
in population size associated with fragmentationllJ2. So far,
however, the effect of fragmentation on the genetic components of quantitative variation has received limited study.
Given the adaptive significance of quantitative genetic variation, and the theoretical framework that exists regarding
effects of genetic drift and gene flow on both additive and
non-additive genetic variances, this is an important and
potentially fruitful area for further research.
Erosion of genetic variation due to habitat fragmentation
may have significant long-term evolutionary consequences
and is also of immediate concern if genetic changes directly
affect individual fitness and the short-term viability of remnant populations. Oostermeijer et ds35 work on Gentiuna
pneumonanthe shows that such links do exist. Further research to examine interactions between genetic and demographic processes in remnant populations should be a
priority. Questions to be addressed include: (1) Does inbreeding depression significantly influence remnant population
viability? (2) Under what conditions can remnant populations purge genetic load effectively? Such investigations
will require the integrated use of genetic markers, longterm demographic monitoring, and population modelling
approaches.
Perhaps the most surprising results have been the apparent increases in interpopulation gene flow observed for
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Purging of genetic load

Purging of genetic load is the reduction in frequency of deleterious alleles respon
sible for inbreeding depression. This reduction is brought about by inbreeding
followed by selection. If the inbreeding depression is due to symmetric overdominance, where homozygotes are equally unfit, purging cannot take place41. However,
if inbreeding depression is due to partial or complete dominance, or if overdominance is asymmetric, then inbreeding, followed by selection against less fit homozygotes, reduces the frequency of deleterious alleles and increases mean individual
fitness, despite an overall reduction in heterozygosity. To what degree purging
is effective depends on: (1) the rate of selfing, (2) the strength of selection
against deleterious homozygotes, (3) whether genetic load is due to many
genes of small effect or a few lethals, and (4) the stage of the life cycle at which
inbreeding depression occurs 42,43. Box 2 noted that population bottlenecks can
convert non-additive to additive genetic variance. If this is additive variation for
fitness, it becomes amenable to selection and leads to another mode of purging
genetic load.

Acer sacchavum populations that have been subject to frag-

mentationgJ9. These findings are counterintuitive and raise

new conservation and evolutionary questions about the effects of a breakdown of local population genetic structure
due to habitat fragmentation. Such findings highlight the
value of empirical studies of real populations and ecosystems when examining the response to disturbance of complex processes such as gene flow.
Overall, the studies have provided some interesting initial insights into the genetic effects of habitat fragmentation.
They highlight that population genetics needs to be considered when assessing the conservation value of remnant
plant populations. However, it is clear that there is a good
deal more to learn. For example, habitat fragmentation often
alters environmental conditions (e.g. temperature, soil moisture and light)51within habitat remnants but, so far, the genetic impacts of these potential changes in selection regimes
have not been investigated.
Of more general concern is that the species studied so far
have all been temperate, perennial, insect-pollinated angiosperms that occur naturally in large populations. It is crucial
that future research examines the effects of fragmentation
on species with a broader range of ecological and reproductive traits. Given current rates of habitat fragmentation
and degradation in tropical ecosystems, and their immense
species diversity, investigations into the effects of fragmentation on tropical species, which are often animaldispersed and occur at low densities, are a much needed
next step.
Acknowledgements
We thank Spencer Barrett, Jeremy Burdon and three
anonymous reviewers for their comments on earlier
drafts of this manuscript.

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TREE vol.

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no.

IO October

1996