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Allometric projections of time-related growth

trajectories of two coexisting dipterocarp
canopy species in India

Article in Plant Ecology & Diversity December 2016

DOI: 10.1080/17550874.2016.1266403

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Plant Ecology & Diversity, 2016
http://dx.doi.org/10.1080/17550874.2016.1266403

Allometric projections of time-related growth trajectories of two coexisting dipterocarp canopy

species in India
a,b
Ccile Antin *, Jimmy Le Beca,b,c, Narayanan Ayyappanb, Bramasamdura Rangana Rameshb and Raphal Plissiera,b
a
IRD, UMR AMAP, Montpellier, France; bInstitut Franais de Pondichry, UMIFRE CNRS-MAE 21, Puducherry, India; cINRA, UMR
SYSTEM, Montpellier, France
(Received 2 February 2016; accepted 6 November 2016)

Background: The Western Ghats of India contain the westernmost dipterocarp forests of Asia. However, only a few dipterocarp
tree species actually coexist in the forest canopy among which Vateria indica and Dipterocarpus indicus are the most common.
The mechanisms contributing to the coexistence of these phylogenetically closely related species have not been identied.
Aims: We investigated the time-related growth trajectories in diameter, height and crown size of these two species in the
Uppangala Permanent Sample Plot to determine if trade-offs in their three-dimensional developmental strategies could
contribute to their long-term coexistence.
Methods: From annual diameter growth data of 692 trees >9.55 cm in diameter at breast height over a 21-year period, we
developed time-related diameter growth models for the two species, accounting for local density-dependent competition
effects and topography. Combining the diameter growth models with static stem and crown allometries, we projected time-
related tree growth trajectories in height and crown size.
Results: While both species can reach similar dimensions, V. indica grows much faster, or at least as fast as D. indicus in
diameter, height and crown size in all the observed situations. Both species respond similarly to topography, but V. indica
appears to be more responsive to local density-dependent competition than D. indicus. Finally, V. indica shows higher
mortality and recruitment rates and a greater basal area increase than D. indicus.
Conclusions: These results refute our hypothesis that D. indicus coexists with the outperformer V. indica by a growth
strategy allowing selected individuals in favourable conditions to reach the canopy more quickly than their competitors. The
current coexistence of the two dipterocarp species at Uppangala appears not to be at a static equilibrium; V. indica probably
being in a phase of canopy stand colonisation.
Keywords: density-dependent competition; Dipterocarpus indicus; stem and crown dimensions; terrain slope intensity;
terrain aspect; Vateria indica

Introduction 2005). This is why foresters have long-developed

Dipterocarps are an emblematic group of phylogenetically
closely related tree canopy-forming species that coexist in
sympatry in Asian tropical forests. Several mechanisms of
dipterocarp coexistence have been evidenced from niche
partitioning with respect to light gaps (e.g. Philipson et al.
2012) or soil conditions (e.g. Sukri et al. 2012), including
relationships with ectomycorrhizal fungi (Peay et al. 2010)
or to temporal phenological variations and masting (e.g.
Brearley et al. 2007; Kettle et al. 2011). Trade-offs in
resource allocation between rapid growth in light and
survival in the shade have also been investigated among
dipterocarp species but mainly at the seedling stage (e.g.
Dent and Burslem 2009). However, these trade-offs,
though possibly variable during ontogeny (Clark and
Clark 1992), are likely to persist at the adult stage (Reich
2014) and thus to contribute to resource partitioning
between coexisting canopy species.
Trees develop in a three-dimensional (3-D) space, and
the relationship between growth and its allocation among
different dimensions (e.g. stem diameter, tree height and
crown size) is strongly governed by allometric rules (King
approaches to characterise tree growth strategies based on
allometries, especially in temperate forests (e.g. Pretzsch
2006). Allometries vary among species, reecting the way
species allocate carbon to growth. For instance, a greater
allocation to height growth can allow canopy species to
rapidly reach a high-light environment, thus overtopping
and shading their neighbours (Poorter et al. 2005), while a
greater crown expansion can allow understory species to
increase their interception surface in low-light environments
(Kohyama 1987). Allometries can also vary with soil con-
ditions (Heineman et al. 2011) or with local competition
intensity, leading, for instance, to height growth being
enhanced in crowded conditions over lateral crown expan-
sion (Banin et al. 2012). Steep slopes also favour asym-
metric crown development (e.g. Lang et al. 2010), which
may result in additional biomechanical constraints on the
tree stem. This may induce feedback mechanisms requiring
greater resource allocation to radial growth and thus result-
ing in bulkier stems (Fournier et al. 2006).
The comparison among the species of allometric rela-
tionships between tree above-ground dimensions is com-
monly used to explore the inter-specic differences in

*Corresponding author. Email: cecile.madelaine-antin@cirad.fr

2016 Botanical Society of Scotland and Taylor & Francis

2 C. Antin et al.
terms of growth strategies (King and Clark 2011), includ-
ing plasticity of species growth responses with respect to
environmental variations (Lang et al. 2010; Harja et al.
2012). However, it is often overlooked that static allome-
tries are size-related relationships that do not properly
account for the temporal differences in exploration and
occupancy dynamics of the 3-D canopy space by coexist-
ing species. Understanding these dynamics requires inte-
grating allometric relationships with tree growth rates in
both the radial (stem diameter growth) and axial (exten-
sion growth) dimensions, the latter determining both total
tree height and crown width.
For obvious practical reasons, studies on adult tree
growth generally focus on stem diameter growth. In tropi-
cal trees, this has been demonstrated to vary between
species as an adaptation to resource acquisition, according
to life history strategies (fast-growing pioneers vs. slow-
growing shade tolerants; Valladares and Niinemets 2008)
or adult stature (e.g. maximum height; Hrault et al. 2011).
However, stem diameter growth also varies with indivi-
dual responses to the amount of resources available (plas-
ticity), either in the soil (water and nutrients, e.g. Russo
et al. 2005; Coomes et al. 2009) or above ground (crown
light exposure, e.g. Moravie et al. 1999). It may also vary
during ontogeny (Le Bec et al. 2015), a phenomenon that
is reinforced when large trees reach the canopy and access
greater light levels. While both extension growth and stem
diameter growth respond to soil fertility, extension growth
probably responds to competition for light more directly
(Poorter et al. 2005). As a consequence, projection of
time-related growth trajectories in various tree dimensions
could provide new insights into the mechanisms of com-
petition and resource partitioning among coexisting spe-
cies involved in the maintenance of canopy tree diversity
in tropical forests (Heineman et al. 2011).
In this article, we investigated the growth trajectories of
two coexisting dipterocarp canopy species, Dipterocarpus
indicus and Vateria indica, in order to determine whether
trade-offs in their growth strategies could contribute to their
long-term coexistence in a wet evergreen forest of the Western
Ghats of India. Indeed, though we have no evidence for
signicant differences in their regeneration niches, both spe-
cies are common large canopy trees. Previous studies also
showed that the stem diameter distribution of V. indica was
much closer to the expectation of a demographic equilibrium
(i.e. to a negative exponential function suggesting relatively
constant diameter growth and mortality rates with diameter;
Muller-Landau et al. 2006) than D. indicus. While V. indica
had a stem diameter growth rate twice as fast as D. indicus, the
latter reached the canopy with more slender stems and had a
narrower crown at the adult stage than V. indica (Pascal and
Plissier 1996; Moravie et al. 1997; Antin et al. 2013; Le Bec
et al. 2015). We therefore expected, from population structure
and static allometries, an opportunistic growth behaviour of D.
indicus, with individuals able to grow faster in height in
favourable conditions, becoming emergents. In contrast, we
expected that V. indica invested in a large crown to optimise
light capture in the crowded canopy layer, with potential
biomechanical feedbacks to stem growth allocation. Such a
hypothesis, which could contribute to explaining why the two
species can coexist in the forest canopy, is only testable,
however, if the growth trajectories of the two species in all
dimensions can be synchronised in time. As assessing tree age
of tropical tree species remains difcult (Nath et al. 2012),
projections of diameter growth from repeated measurements is
the most reliable way to obtain time-related growth trajectories
to make synchronised species comparisons. Even though dia-
meter growth is easily determined from eld measurements,
measuring extension growth is more challenging, especially in
crowded forest conditions, making direct time-related assess-
ment of height and crown extensions difcult.
We thus combined species-specic dynamic growth
models calibrated on a 21-year-long series of diameter mea-
surements with static stem and crown allometries to project
time-related height and crown size trajectories. Our models
also accounted for the main factors of growth variation at the
study site, i.e. tree size, local competition and topography.
We nally discuss the above hypothesis of a stable coexis-
tence of V. indica and D. indicus based on the time-related
growth trajectories owing to their 3-D growth strategies.
Material and methods
Study site and species
The study site was the Uppangala Permanent Sample Plot
(UPSP) in the Western Ghats of India at 12 32 15 N,
75 39 46 E (Pascal and Plissier 1996; Plissier et al.
2011). It was located at an altitude of 300600 m a.s.l. and
presented a marked relief dissected by streams running
downward from the crest of the Ghats: ridges with gentle
slopes separating watercourses alternate with deep valleys,
resulting in a major contrast between easterly and westerly
hillside aspects. Soil analyses in a nearby plot showed that
topography was the main local factor of environmental
variation and that it was a very good predictor of soil
water availability at Uppangala: while soils on the ridges
(gentle slopes) are several meters deep, soils on the (steep)
slopes are supercial and eroded (Ferry 1992). Local cli-
mate presents a strong seasonality with 90% of total rain-
fall (ca. 5000 mm year1) occurring during the monsoon
period (JuneOctober) and a mean daily temperature of ca.
2530 C all year round.
The stand belongs to an undisturbed, old-growth wet
evergreen forest in which eight sample plots (ve bands
and three rectangular plots overlapping the bands, see
Figure S1) covering a total of 5.07 ha were established
between 1990 and 1993 (Plissier et al. 2011). In these
plots, all the trees with girth at breast height exceeding
30 cm (i.e. a diameter at breast height of 9.55 cm) were
mapped within 10 m 10 m subplots, identied and
equipped with permanent dendrometer bands. All sub-
plots were georeferenced, and a digital elevation model
(DEM) was derived from slope measurements (angle
and direction) taken from each corner of the
10 m 10 m subplots. The stand, composed of 101

tree species, presents an average density of ca. 650 trees
ha1 and a basal area of ca. 40 m2 ha1, respectively.
Mortality and recruitment have also been regularly
recorded, and their rates have been calculated from
1993 (because of the progressive addition of new plots
between 1990 and 1993) to 2011.
The two dipterocarp species studied, D. indicus and V.
indica (species nomenclature refers to vouchers stored at
the herbarium of the French Institute of Pondicherry, HIFP),
are among the most abundant and dominant species in the
canopy at UPSP, accounting for 20.1% of the stand density
and 40.9% of the total basal area, respectively (Pascal and
Plissier 1996). Both are ectomycorrhizal canopy or emer-
gent tree species (Riviere et al. 2006) that exhibit irregular
phenological patterns and episodic mass fruiting (Elouard
et al. 1997). There is no evidence for any signicant differ-
ence between these two species with regard to their prefer-
ences in terms of gap-light environments for regeneration
(C. Antin, unpublished data).
Tree measurements
In the present article, we used a dataset of 122 D. indicus
and 570 V. indica individuals measured in UPSP from
1990 to 2011. Girth at breast height was recorded yearly
using permanent dendrometer bands and converted into
diameter at breast height (dbh, in cm), providing more
than 17,000 dbh measurements for the two species (see
Figure S2). Tree height (ht, in m) and crown base height
(cbht, in m) were measured for random subsamples of
these trees in 19901994 and 20072008. Total tree height
was measured for 585 trees in 19901994 using a Blume-
Leiss altimeter and for 348 trees in 20072008 using a
Haglf vertex clinometer. Crown base height was mea-
sured with the same instrumentation for 482 trees in
19901994 and for 338 trees in 20072008. Crown radii
were measured in the four cardinal directions from ground
projections of the crown edge to the stem centre (375 trees
in 19901994) and in four directions given by the largest
width of the crown projection and the perpendicular width
(343 trees in 20072008). Crown width (cw, in m) was
then calculated for both periods as twice the mean crown
radius. Only a small fraction of these trees were measured
twice for height and crown size (see Table S1 for more
details about the data set). We additionally attributed a
local slope angle (in %) and aspect (in degree) derived
from the DEM to each tree.
Stand demography
Tree mortality and recruitment rates were calculated as the total
number of dead or recruited trees (between 1993 and 2011)
divided by the initial abundance of the given species for V.
indica, D. indicus and all the other species grouped together.
Basal area was calculated from dbh. In case of missing dbh
measurements in 1993 or 2011, we used dbh measured in 1994
or 2010, considering the bias introduced as negligible given the
Allometric projections of time-related growth 3
very low annual dbh increment observed in UPSP. Finally, we
separated basal area uctuations due to tree growth and due to
recruitment and mortality (see Table 1).
Diameter growth models
We tted diameter growth using species-specic maxi-
mum likelihood mixed models. Following the general
design proposed in Le Bec et al. (2015), we introduced
in the model: (i) an individual tree random effect in order
to account for temporal autocorrelation of the growth data
over the 21-year period of observation (Kohyama et al.
2005), (ii) tree dbh and a local competition index (as well
as their log transformations) as time-varying covariates
and (iii) slope and aspect (as well as their sine and cosine
transformations) as time-invariant covariates. Variable
selection was made with a backward step-wise procedure
based on Akaike information criterion, which led to the
two following growth models:
V: indica ! dbhit a#dbhit b#logdbhit
c#logg15it
d#logdbhit #logg15it
e#logg15it #dbhit
f #sineaspecti i it
(1)
D: indicus ! dbhit a # logdbhit b
# logg15it i it (2)
In these equations dbhit is the annual diameter incre-
ment calculated for each individual tree i, as the difference
between its diameter at t and t1 divided by t in days to
account for the slightly variable census intervals (from 305
to 426 days). The term dbhit is the diameter of tree i at time
t. The term g15it is an index of local competition corre-
sponding to the total stand basal area of neighbours within a
15-m radius around tree i at time t, an index that was found
to better explain tree growth than others at the study site
(see Le Bec et al. 2015). The term aspecti is the local aspect
around tree i, with a sine transformation that emphasises
eastwest oppositions in slope orientation. The term i is the
individual random effect (on the intercept) for tree i, which
represents how much the growth trajectory of that tree
deviates consistently over time from its species growth
response. Finally, it is the residual growth for tree i at
time t (assumed independent and identically distributed).
Allometric relationships
To determine if topographical variation observed in UPSP
accounted for variation in allometric relationships, we rst
carried out an analysis of variance for assessing the effects
of slope, aspect and their interaction on ht:dbh, cbht:dbh
and cw:dbh ratios. The slope factor was as in Antin et al.
4 C. Antin et al.

Table 1. Demographic parameters over the period 19932011 for V. indica, D. indicus and for all other species grouped together in
UPSP, Western Ghats of India.

Initial Mortality Recruitment Initial basal Basal area increase Basal area increase Basal area
density rate (% rate (% area (m2 related to growth related to recruitment increase
Species (trees ha1) year1) year1) ha1) (%) and mortality (%) (%)

All species 647.6 0.88 0.86 41.8 21.6 13.8 7.8

V. indica 115.4 0.56 0.62 12 30.7 9.3 21.4
D. indicus 22.5 0.43 0.58 6.4 14.8 6.1 8.7
Other species 509.7 0.98 0.92 23.4 18.8 18.2 0.5
West gentle (0.72 ha) 720.5 0.80 0.86 52.6 17.1 12.8 4.3
V. indica 138 0.62 0.56 15.9 22.2 8.2 14
D. indicus 29.3 0.80 1.06 11.9 10.9 15.6 4.7
Other species 553.2 0.84 0.92 25.3 16.7 14.5 2.2
West steep (1.06 ha) 725.7 0.91 0.56 45.8 20.3 12.6 7.6
V. indica 128.3 0.66 0.49 14.8 26.5 7.7 18.7
D. indicus 17.9 0.29 0.29 5.3 11.7 0 11.7
Other species 579.4 0.98 0.58 25.6 18.4 18.1 0.3
East gentle (1.52 ha) 656.8 0.61 0.76 42.5 22.2 11 11.2
V. indica 144.5 0.33 0.43 9.6 44.9 9.6 35.4
D. indicus 26.9 0.13 0.40 9 13.1 0.6 12.6
Other species 485.4 0.72 0.97 23.9 16.4 15.5 0.9
East steep (1.10 ha) 618 1.25 1.25 37.1 26.7 21 5.7
V. indica 64.5 0.85 1.47 9.7 30.3 17.6 12.7
D. indicus 27.3 0.36 0.72 4.5 29.7 12.6 17.1
Other species 526.2 1.34 1.24 22.9 24.5 24.1 0.4
Variables were calculated according to slope (steep vs. gentle) and aspect (east vs. west) categories. Mortality and recruitment rates were assessed for the
whole period of observation (17 years). As new plots were progressively added between 1990 and 1993, we calculated demography from 1993 to 2011.

(2013), i.e. simplied in two classes (steep slopes 30
and gentle slopes < 30), while aspect was east (< 180
from north) and west ( 180 from north). Note that given
the 15-year interval between tree height and crown size
data that have been measured twice for some trees, we
considered them as independent observations for allome-
tries. Only the slope factor had a signicant effect for the
three ratios considered for D. indicus, whereas both slope
and aspect were signicant for V. indica (Table S2). We
thus chose to t separate allometric relationships for trees
on gentle and steep slopes for D. indicus, and for trees on
gentle or steep and east- or west-facing slopes for V.
indica.
As both species clearly present an asymptotic height, allo-
metric relationships between height and dbh were determined
by a Weibull-type function (Temesgen and Gadow 2004):
h hmax # 1 ! ea#dbh^b
where h is alternatively tree height (ht) or crown base height
(cbht). The parameters hmax, a and b were estimated with a
non-linear least square regression (Bates and Watts 1988).
The residuals of these models met the assumption of normal-
ity, whereas the use of a power function linearised by log
transformation would have led to an overestimation of the
predicted variable for smallest and largest trees (Figure S3).
Allometric relationship between crown width (cw) and
dbh was determined by a log-linear function:
The parameters a and b were estimated with a
linear least square regression. The residuals of these
models met the assumption of normality (not shown).
Projection of time-related growth trajectories
We then used the diameter growth model and allometric
relationships to integrate growth trajectories over time for
both species and accounting for the various topographic
situations. We started integration from dbht=0 = 10 cm and
calculated dbh predictions at a yearly time step t with:
dbht1 dbht dbhdbht (5)
where dbh(dbht) is estimated from parameters tted in
Equations 1 and 2, for V. indica and D. indicus, respectively.
We projected time-related trajectories of both species with a
(3) competition index (g15) xed to 40 m2 ha1 (mean observed
value of g15i at UPSP) and considered two situations for V.
indica with aspect alternatively xed to 90 (easterly aspect) or
270 (westerly aspect). We stopped trajectory projections at
120 cm dbh corresponding to the maximum observed diameter
in UPSP for both species.
We nally estimated ht, cbht and cw at the same
yearly time steps, by using the parameters estimated
while tting allometric relationships (Equations 3 and 4).
b
ht hmax # 1 ! ea#dbht^ (6)

logcw a b # logdbh (4) cwt a b # logdbht (7)


Finally, a 3-D representation of the development of a
hypothetical tree combining the predicted dbh, stem height
and crown dimensions was made by using the Allostand
model (Barbier et al. 2012) for both dipterocarp species in
various topographic situations. All the above analyses
were carried in the R environment, v. 3.0.2 (R
Development Core Team 2011).
Results
Stand and population demography
While the stand density and basal area varied with respect to
topography, V. indica and D. indicus populations were quite
homogeneously distributed except in steep east-facing
slopes, where V. indica was almost half as dense than in
other topographies (Table 1). Overall the observed popula-
tion dynamics were faster for V. indica (0.56% and 0.62%
year1 in terms of mortality and recruitment) than for D.
indicus (0.43% and 0.58% year1) except on gentle west-
facing slopes where it was the reverse (Table 1). Finally, total
stand basal area increased by more than 7.8% between 1993
and 2011 and was proportionally greater for V. indica
(21.4%) than for D. indicus (8.7%) or for the other species
(0.5%) (Table 1). The greatest increment in basal area
between 1993 and 2011 was observed on gentle east-facing
slopes for V. indica (35.4%) and on steep east-facing slopes
for D. indicus (17.1%), i.e. where V. indica is less dense and
shows the smallest increment in basal area (12.7%). The only
negative increment in basal area was recorded for D. indicus
in gentle west-facing slopes (4.7%), i.e. where its turnover
was the fastest (Table 1). These gures suggest that the
growth and demography of the two dipterocarp species
vary in a non-consistent manner according to slope and
aspect at UPSP. Furthermore, both species showed contrasted
dbh distributions: V. indica showed a density function
decreasing exponentially with tree size (and thus relatively
close to the expectation of a demographic equilibrium),
whereas D. indicus showed an atypical density function
with a greater proportion of large trees (Figure S4).
Moreover, the relative frequency of small tree size classes
decreased over time for V. indica, whereas the relative fre-
quency of large tree size classes decreased for D. indicus.
Variation in growth and allometries
The diameter growth models tted to the 21-year series of dbh
increments showed that V. indica grew faster than D. indicus.
Mean tree growth increased with tree dbh, with larger varia-
tion for V. indica, and decreased with competition, more
notably for small trees of V. indica; D. indicus was less
responsive to increased competition (Figure 1 and Table S3).
In terms of allometries, D. indicus and V. indica
showed contrasting responses to environmental factors:
htdbh allometry showed an asymptotic height signi-
cantly higher for D. indicus than for V. indica and an
asymptotic height signicantly higher on gentle slopes
than on steep slopes for both species (Figure S5 and
Allometric projections of time-related growth 5
Table S4). As a consequence, large trees of D. indicus
were more slender at a given diameter than those of V.
indica. The cbhtdbh allometry showed, for a given dbh, a
higher cbht for D. indicus than for V. indica and a higher
cbht on gentle slopes than on steep slopes, except for V.
indica on westerly aspects for which no difference was
observed between gentle and steep slopes (Figure S5 and
Table S4). The cwdbh allometry showed that large trees
had wider crowns on steep slopes and that, for a given
dbh, crowns of V. indica were wider than crowns of D.
indicus, except on steep east-facing slopes where V. indica
had the narrowest crowns (Figure S5 and Table S4).
Time-related growth trajectories
Projection of time-related trajectories showed a general
trend towards more rapid growth for V. indica than D.
indicus whatever the topographic situation. At
t = 200 years (>10 cm dbh), D. indicus reached a dbh of
37.9 cm, whereas V. indica reached a dbh of 50.5 cm on
westerly aspects and 87.7 cm on easterly aspects
(Figure 2). V. indica reached the maximum observed dbh
(120 cm) at t = 249 years on easterly aspects, at
t = 328 years on westerly aspects; whereas D. indicus
reached the same maximum dbh at t = 505 years. Both
species showed a continuous increase in growth rate over
time (see Figure 2). V. indica also showed a more rapid
and early height growth on easterly aspects than on wes-
terly aspects, and than D. indicus, regardless of the slope
(Figure 3). However, D. indicus always reached a higher
maximum height than V. indica (see also Figure S5).
Overall, both species showed a shift of growth allocation
in the stem from height growth to stem diameter growth
during ontogeny (Figure 4), with a predicted decrease in
the slenderness ratio, slower for D. indicus than for V.
indica. The predicted decrease in the slenderness ratio
was also slower on gentle slopes than on steep slopes for
both species and slower on westerly aspects than on east-
erly aspects for V. indica. It is noticeable that V. indica
reached a low slenderness ratio much earlier on gentle
east-facing slopes than in other topographic situations or
than D. indicus in all topographic situations.
Growth in crown width (cw) was also more rapid for V.
indica than for D. indicus (Figure 4). At t = 200 years and on
gentle slopes, D. indicus reached a cw of ca. 7 m, and V.
indica reached ca. 10 m on westerly aspects and ca. 16 m on
easterly aspects, whereas on steep slopes, D. indicus reached
a cw of ca. 8 m and V. indica reached ca. 9 m on westerly
aspects and ca. 14 m on easterly aspects.
Both species showed a decreasing crown depth
crown width ratio with time, indicating a shift from
crowns deeper than wide to crowns wider than deep.
But while D. indicus showed a lower initial ratio than V.
indica (at t = 0, i.e. dbh = 10 cm), the shift occurred
later than for V. indica (Figure 4). We note that D.
indicus maintained an equilibrium between crown
dimensions from t = 200 to t = 400 years on gentle
6 C. Antin et al.

Figure 1. Predicted dbh growth according to initial dbh with g15 (local basal area within a 15 m radius around tree) xed at 40 m2 ha1 (left
insert) and predicted dbh growth according to the competition index g15 with dbh alternatively xed to 10, 50 and 80 cm (right insert) for D.
indicus and V. indica in UPSP, Western Ghats, India. All other covariates are invariant and have been xed to their average values.

Figure 2. Time-related growth trajectories in dbh (left) and dbh growth (right) as predicted by species-specic growth models for D.
indicus and V. indica according to slope (steep vs. gentle) and aspect (east vs. west) categories in UPSP, Western Ghats, India.

slopes, whereas the shift from vertical extension to
horizontal extension occurred faster on steep slopes.
Projections of the time-related growth trajectories of V.
indica and D. indicus in stem diameter, tree height and
crown dimensions in different topographic situations are
summarised in Figure 5.
Discussion
Whereas the comparison of static allometric relationships
between these species has already been investigated (e.g.
Pascal and Plissier 1996; Antin et al. 2013), here we
advance by introducing the temporal dimension within
the projected time-related growth trajectories. Our results
bring new insights into the way the growth trajectories
vary between the two species and according to terrain
aspect and slope intensity. However, these differences do
not yet indicate trade-offs in the growth strategies of the
two species that could explain their long-term stable coex-
istence in the forest canopy as we expected. We further
discuss an alternative speculative hypothesis of a transient
coexistence after an undocumented large-scale disturbance
event.
V. indica is more responsive to light environment than D.
indicus
We showed that, unlike D. indicus, V. indica has a greater stem
diameter growth on easterly exposed hillsides (receiving sun-
light in the morning) than westerly exposed hillsides. It may be
due to some combination of less cloud cover in the morning
and/or inhibition of photosynthesis by greater water stress in
the afternoon. Moravie et al. (1999) showed that diameter
growth of V. indica was mainly driven by the light environment
at UPSP, as has been shown for other species in tropical forests
(King et al. 2005). On the other hand, V. indica exhibits a
greater crown volume on east-facing slopes than on west-
facing ones, which may also explain its greater growth rates
by increasing the total amount of light interception surface
(Kohyama 1987).
We also found that the growth response to competition
was more than twice as strong for V. indica as compared to

Figure 3. Time-related growth trajectories in tree height (top) and tree height growth (bottom) as predicted from species-specic
diameter growth models and heightdiameter allometries for D. indicus and V. indica according to slope (steep vs. gentle) and aspect (east
vs. west) categories in UPSP, Western Ghats, India.
that for D. indicus. The competition index selected in the
diameter growth model considers all the neighbouring trees
in a radius of 15 m around each tree and so partly includes
the effects of above-ground and below-ground competition.
These results suggest that V. indica is more sensitive to
the light environment and other growing conditions than D.
indicus. In other words, V. indica appears more plastic than
D. indicus in terms of stem diameter growth. Nevertheless,
D. indicus exhibits a basal area increase similar to that in V.
indica (29.7% and 30.3%, respectively) on steep east-facing
slopes, where initial density and basal area were the lowest
(618 trees ha1 and 37.1 m2 ha1, respectively). This basal
area increase is more than twice than the increase for D.
indicus in other topographic situations where initial density
and basal area were greater (657726 trees ha1 and 42.5
52.6 m2 ha1, respectively). This suggests that D. indicus
may be sensitive to competition in these conditions, but we
were not able to detect this with the growth model we tted.
Both species respond similarly to topography
For both species, we showed that projected height growth is
faster on gentle slopes. In contrast, no effect of slope was
detected on stem diameter growth. As a result, we observed
that total heights are taller for a given stem diameter on gentle
slopes, so that trees are slenderer there than elsewhere. Robert
and Moravie (2003) proposed that this reduced slenderness on
Allometric projections of time-related growth 7
steep slopes in UPSP could be the result of increased strati-
cation of tree crowns on the slope thus reducing competition
for light and consequently reducing investment in height
growth as compared to gentle slopes. We observed that the
slenderness ratio decreased more rapidly on steep slopes for
both species. This shows that the allocation pattern between
height growth and stem diameter growth is affected by local
environmental conditions for both species (Sumida et al. 1997;
Rozendaal et al. 2015). The shift from prevailing allocation to
height growth towards prevailing allocation to stem diameter
growth not only depends on age or size (Silveira et al. 2012)
but is also inuenced by environmental conditions.
Crown width growth and crown base increase are also
faster on gentle slopes than on steep slopes for both species.
While D. indicus shows a lower initial crown depth:crown
width ratio than V. indica (at t = 0, i.e. dbh = 10 cm) in all
topographic situations, we noticed that V. indica reached a
lower ratio much earlier on gentle east-facing slopes than in
other topographic situations and lower than D. indicus in all
topographic situations. This suggests that V. indica established
earlier and at a lower height in the canopy than D. indicus.
V. indica grows faster than D. indicus
V. indica exhibits a faster growth rate than D. indicus for
most of the tree dimensions and in most of the situations
observed at UPSP. The faster stem diameter growth of V.
8 C. Antin et al.

Figure 4. Time-related trajectories of slenderness ratio (h:dbh), crown width and crown shape (crown depth:crown width) as predicted
from species-specic diameter growth models and height-stem diameter allometries for D. indicus and V. indica according to slope (steep
vs. gentle) and aspect (east vs. west) categories in UPSP, Western Ghats, India.

indica could be partly attributed to its less dense wood
than that of D. indicus (0.48 and 0.59 g cm3, respectively;
see Bhat et al. 1990; Devagiri et al. 2013), as it has been
showed that stem growth is negatively correlated with
wood density (King et al. 2005). As both species show
very close scaling relationships between crown width and
stem diameter although V. indica tends to have wider
crowns than D. indicus V. indica exhibits a faster growth
in crown width. More surprisingly, while D. indicus has a
slenderer stem than V. indica, the latter also exhibits a
faster height growth than D. indicus on easterly aspects,
and both species show a similar height growth on westerly
aspects.
While we observed a general good concordance between
extension growth patterns inferred from time-related growth
trajectories on the one hand and from direct estimations on
the other hand, this is not the case for crown width trajec-
tories of V. indica and height growth trajectories for small
trees in the range 1580 cm dbh for D. indicus (see
Figure S6). This emphasises a potential limit to our method
of time-related reconstruction, which cannot account for
possible changes in allocation patterns that could have
occurred before 1990 because of different conditions and
forest dynamics. In particular, D. indicus individuals as old
as 300500 years according to our estimations may not
represent the actual conditions of competition that partly
determine the resource allocation patterns between stem,
height and crown extension. While stand density remained
almost constant over the study period (0.02% trees ha1
year1), stand basal area increased by 7.8% (up to 11.2% on
gentle east-facing slopes) indicating a progressive canopy
closure and therefore a more competitive environment. This
kind of change might both slow down the individual crown
width extension of V. indica (by lack of space) and promote a
faster height growth for some individuals of D. indicus (by
selection).
V. indica seems to do better than D. indicus at establish-
ing into the canopy, and this result might contribute to

Figure 5. Representation of the 3-D development of a hypothe-
tical tree combining the predicted dbh, stem height and crown
dimensions at 10, 50, 100, 150 and 250 years (above 10 cm dbh)
for V. indica and, additionally, at 350 and 500 years for D.
indicus in various topographic situations in UPSP, Western
Ghats, India. dbh is represented by a doubling size in order to
emphasise the visual differences between species and topo-
graphic situations (slope and aspect).
explaining its high density (17.8% of the stand density) and
basal area (28.7 % of the stand basal area) in the stand.
Moravie et al. (1997) developed a canopy regeneration
model for UPSP, which showed that, in the absence of
major disturbances, a dominant tree can be replaced when
it dies by suppressed trees that survived in its crown periph-
ery. With such a mechanism, V. indica would outperform D.
indicus by rapidly overshadowing trees of the same size, as
its growth in height and crown width is faster. We also
observed that V. indica showed the greatest increase in den-
sity and basal area on gentle east-facing slopes, where the
mortality rate is the lowest, indicating low disturbance.
A hypothesis of a temporal shift in species dominance of
V. indica and D. indicus in the forest canopy
Comparing two canopy and emergent dipterocarp species,
we found no evidence of existing trade-offs between
height growth and stem diameter growth as we
Allometric projections of time-related growth 9
hypothesised originally. It seems instead that V. indica
simply grows faster than D. indicus in all dimensions
and in most topographic situations. This is the main reason
for the more than doubling in basal area of V. indica over
the 21 years as compared to that of D. indicus. Such an
increase in basal area shows that the current dynamics
have not reached equilibrium, at least not a static equili-
brium. Le Bec (2014) showed, from simulations, that the
current dynamics observed in UPSP could be the result of
an undocumented large past disturbance (ca. 50% mortal-
ity, over 100 years ago). Our present study tends to con-
rm this hypothesis and that the stand could currently
being colonised by V. indica. We also observed that D.
indicus had a greater increase in basal area than the mean
increase for all other species, suggesting that it is not likely
to be excluded from the stand by V. indica in the near
future.
Limitations of the study
We are aware that our time-related projections of growth
trajectories based on repeated stem diameter growth data
may not exactly represent the growth trajectory of an
average individual (Zuidema et al. 2009). The high
temporal autocorrelation of tree growth (Kohyama
et al. 2005) and the increased frailty of slow growing
individuals (Rger et al. 2011) mean that large trees are
likely to be represented mostly by fast growing indivi-
duals, while juvenile trees exhibit a more heterogeneous
composition a selection effect, well known in popu-
lation demography (Cam et al. 2002). However, we
believe that our approach offers a relevant tool to com-
pare how growth is distributed among diameter classes
and to compare the growth patterns of the two dipter-
ocarp species. As a matter of fact, when we compared
the growth patterns in height and crown size inferred
from combining diameter growth models and static allo-
metries with direct estimations for the few trees that
have been measured twice in height and crown size
(once in 19901994 and again in 20072008), we
found a good concordance between the two approaches
except for a slight overestimation of the predicted crown
width increment for V. indica and a slight underestima-
tion of the predicted height growth in the range
1580 cm dbh for D. indicus (see Figure S6). These
slight discordances do not invalidate our general nd-
ings and conclusions. An alternative to improve the
prediction of growth trajectories would be to rely on
long-term growth series through direct dendrochronolo-
gical studies. However, comparison between direct and
indirect methods for deriving growth trajectories for
tropical species in the Western Ghats of India demon-
strated that both methods are only consistent when
annual growth rings can be assessed properly (Nath
et al. 2012). As many trees of evergreen tropical forests
do not form distinct annual growth rings, indirect esti-
mations remain for the time being the most reliable
approach.
10 C. Antin et al.
Conclusion
In this study, we proposed an original approach for inves-
tigating the contribution of trade-offs in growth strategies
to the long-term coexistence of D. indicus and V. indica in
a wet evergreen forest of the Western Ghats of India. As
we assumed that comparing static allometries was not
sufcient for investigating the role of growth strategies
in species coexistence, we projected time-related growth
trajectories in stem diameter, stem height and crown size
of these two species by integrating allometric relationships
with tree growth models.
Our results highlighted the importance of synchronis-
ing in time the growth trajectories of the two species in all
dimensions in order to compare their growth strategies.
Whereas the comparison of static allometric relationships
between these species leads to the hypothesis that D.
indicus coexists with the faster growing V. indica by a
growth strategy allowing selected individuals in favour-
able conditions to reach the canopy more quickly than
their competitors (Pascal and Plissier 1996; Moravie
et al. 1997; Antin et al. 2013), we conclude from our
results that there is no trade-off in the growth strategies
of the two species that could explain their long-term stable
coexistence. While D. indicus and V. indica show contrast-
ing responses to environmental factors in terms of allome-
tries, V. indica grows much faster, or at least as fast as D.
indicus in diameter, height and crown size in all the
observed situations. Combined with the observation that
the growth and demography of the two dipterocarp species
vary in a non-consistent manner according to slope and
aspect at UPSP, we offer an alternative hypothesis of a
transient coexistence after a possible undocumented large-
scale disturbance event, V. indica probably being in a
phase of canopy stand colonisation. A stand dynamic
simulation model could allow deeper investigation of the
dynamic coexistence of both dipterocarp populations in
Uppangala.
Acknowledgements
UPSP is a joint research station of the Karnataka Forest
Department, Bangalore, and the French Institute of
Pondicherry. We are very grateful to the many eld workers,
technicians, engineers and researchers who contributed to its
long-term monitoring. We thank Francis Brearley and three
anonymous reviewers for their thoughtful and constructive
comments and Philippe Verley for assistance in realisation of
Figure 5.
Funding
This work was supported by the French Academy of Agriculture
through a Dufrenoy grant to CA; French Academy of Agriculture
[Grant Dufrenoy 2007].
Disclosure statement
No potential conict of interest was reported by the authors.
Supplemental data
Supplemental data for this article can be accessed here.
ORCID
Ccile Antin http://orcid.org/0000-0002-0385-5886
Notes on contributors
Ccile Antin is a researcher in forest and agroforest ecology. Her
interests include forest dynamics and rules governing biomass
allocation in trees in undisturbed forests as well as in agroforests.
Jimmy Le Bec is a researcher in forest and agroforest ecology.
His interests include forest and agroforest dynamics, tree demo-
graphy and individual tree variability.
Narayanan Ayyappan is a researcher in tropical forest ecology in
charge of the management of the Uppangala Permanent Sample
Plot. His interests include plant systematics, diversity, structure
and dynamics of disturbed and undisturbed forests.
Bramasamdura Rangana Ramesh is a researcher in tropical forest
ecology. His interests include phytogeography, tropical forest tree
dynamics and forest landscape ecology.
Raphal Plissier is a senior researcher in tropical forest ecology,
with a special interest in the spatial organisation of tree species
diversity, and in 3-D forest stand structure and dynamics.
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