Ecological Indicators 58 (2015) 356364

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Ecological Indicators
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Short Communication

An indirect method of estimating leaf area index in a tropical

deciduous forest of India
Soumit K. Behera a,b, , M.D. Behera b , R. Tuli a,c
a
b
c

Plant Ecology and Environmental Sciences Division, CSIR National Botanical Research Institute, Rana Pratap Marg, Lucknow, India
Centre for Oceans, Rivers, Atmosphere and Land Sciences, Indian Institute of Technology, Kharagpur, India
National Agri-Food Biotechnology Institute, Mohali, India

a r t i c l e

i n f o

Article history:
Received 16 January 2015
Received in revised form 18 May 2015
Accepted 20 May 2015
Keywords:
Tropical forest
Moist deciduous forest
Leaf area index
Plant canopy analyzer
Aboveground biomass
Litter fall

a b s t r a c t
Rapid, reliable and meaningful estimates of leaf area index (LAI) are essential to functional characterization of forest ecosystems including biomass and primary productivity studies. Accurate LAI estimates of
tropical deciduous forest are required in studies of regional and global change modeling. Tropical deciduous forest due to higher species richness, multiple species association, varied phenophases, irregular
stem densities and basal cover, multistoried canopy architecture and different micro-climatic conditions offers dynamism to the understanding of the LAI dynamics of different PFTs in an ecosystem. This
investigation reports a new indirect method for measurement of leaf area index (LAI) in a topical moist
deciduous forest in Himalayan foothills using LAI-2000 Plant Canopy Analyzer. We measured the LAI in
two seasons (summer; leaf senescence stage and post-monsoon; full green stage) in three (dry miscellaneous, sal mixed and teak plantations) plant functional types (PFT) in Katerniaghat Wildlife Sanctuary,
India. Ground LAI values ranged between 2.41 and 6.89, 1.17 and 7.71, and 1.92 and 5.19 during postmonsoon season and 1.364.49, 0.673.1 and 0.371.83 during summer season in dry miscellaneous, sal
mixed and teak plantation, respectively. We observed strong correlation between LAI and community
structural parameters (tree density, basal cover and species richness), with maximum with annual litter
fall (R2 > 0.8) and aboveground biomass (AGB) (R2 > 0.75). We provided equations relating LAI with AGB,
which can be utilized in future studies for this region and can be reasonably extrapolated to other regions
with suitable statistical extrapolations. However, the relations between LAI and other parameters can be
further improved with incorporation of data from optimized and seasonal sampling. Our indirect method
of LAI estimation using litter fall as a proxy, offers repetitive potential for LAI estimate in other PFTs with
relatively time and cost-effective way, thereby generating quicker and reliable data for model run for
regional and global change studies.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
Rapid, reliable and meaningful estimates of leaf area index (LAI)
are essential to the functional characterization of forest ecosystems.
The leaf area is the exchange surface between the photosynthetically active component of the vegetation and the atmosphere
(Cohen et al., 2003; Chen et al., 1997; Chen and Cichlar, 1995),
which controls not only the radiation regime within the canopy,
but also the thermal and hydric conditions (Chen et al., 2009). LAI is
a key variable in driving the biological processes of the plants, thus

Corresponding author at: Plant Ecology and Environmental Sciences Division,

CSIR National Botanical Research Institute, Rana Pratap Marg, Lucknow, India.
Tel.: +91 522 2297860/2205847.
E-mail address: soumitkbehera@gmail.com (S.K. Behera).
http://dx.doi.org/10.1016/j.ecolind.2015.05.038
1470-160X/ 2015 Elsevier Ltd. All rights reserved.

is a necessary input variable in many ecological models studying

canopy structure and productivity (Norman and Campbell, 1989;
Welles and Norman, 1991; Chen et al., 2009). LAI is mostly directly
proportional to transpiration and net primary production (NPP),
and inversely proportional to canopy transmissivity (Whitehead
et al., 1984; Zhou et al., 2002; Asner et al., 2003). LAI is inuenced
by elevation (or temperature), water availability, soil fertility and
topography, and much of these studies are from temperate biomes
(Leuschner et al., 2007). However, comprehensive studies on LAI
from tropical complex forest ecosystems are less in number.
Leaf area index (LAI) is a dimensionless variable and is dened
as the total one-sided area of photosynthetic tissue per unit ground
surface area (Watson, 1947), and thus is strictly applicable for
broad-leaved trees with at leaves since both sides of a leaf have
the same surface area. However, if foliage elements are not at
(i.e., wrinkled, bent or rolled) or for coniferous trees wherein

S.K. Behera et al. / Ecological Indicators 58 (2015) 356364

needles may be cylindrical or hemi-cylindrical, the one-sided area

is not clearly dened (Chen and Black, 1992), a projected leaf area
is taken into account for the irregular form of needles and leaves
(Smith et al., 1991; Bolstad and Gower, 1990). LAI measurements
can be performed by two methods: direct and/or indirect. Direct
measurements through harvesting and litter traps are laborious
and impractical; though, they can be used to calibrate indirect
methods. Most eld campaigns utilize indirect measurements of
LAI through allometric and optical methods. Optical measurements
are performed with the LAI-2000 Plant Canopy Analyzer, Tracing
Radiation and Architecture of Canopies (TRAC) instrument, and
hemispherical sheye photographs. Even though direct destructive measurements of LAI are widely believed to be more accurate
than indirect optical estimates, the LAI-2000 system has proven
to provide LAI measurements closest to those obtained with leaf
harvest methods in tropical forests (Asner et al., 2003).
LAI can be estimated indirectly from the incident radiation
transmitted through the canopy at a given zenith angle using
a number of instruments (LAI-2000, DEMON, Ceptometer, hemispherical photography), known as gap fraction method (Chen
et al., 1997; Li-Cor, 1992). The problems with gap fraction method
are (i) branches and stems contribute to the intercepted light, and
(ii) LAI estimation assumes a random distribution of foliage elements, while in reality the spatial distribution of leaves depends
on the distribution of shoots, branches and tree crowns. However,
Optical measurements of LAI could also be biased because they (i)
do not account for clumping of vegetation elements (e.g., LAI-2000
measurements) or, (ii) do it in a semi-empirical way (TRAC measurements) (Welles and Cohen, 1996). Vegetation clumping and
saturation of the optical signal reduce the accuracy of LAI measurements in high LAI stands (mostly in broadleaf forests); and also
automated processing of optical LAI measurements does not distinguish between green leaves and hardwood material. The removal
of such effects is tedious with manual images processing and thus
or requires specic allometric relations to convert plant area index
to LAI. Since the clumping index varies with the zenith angle, the
gap fraction is easily measured at different zenith angles by LAI2000 PCA. In deciduous forests, the same gap fraction method that
is used for estimating LAI can be used for measuring the effective woody area index during the non-vegetative season, when the

357

leaves are shed. The size of the non-green elements of the trees
does not vary much within the season than between the growing
and non-growing season due to exposure of branches during leaf
fall.
Tropical deciduous forest due to higher species richness,
multiple species association, varied phenophases, irregular stem
densities and basal cover, multistoried canopy architecture and
different micro-climatic conditions, offers dynamism to the understanding of the LAI dynamics of different PFTs in an ecosystem
(Blackburn and Gaston, 1996; Behera et al., 2012). We aimed to
establish an indirect method for LAI estimation using LAI-2000 PCA.
We also tried to analyze the relation between LAI with community,
as well as structural and functional variables such as species richness, basal cover, stem density, litter fall and above-ground biomass
in three PFTs having distinct tree species compositions, different
carbon assimilation rates and micro-climate conditions in a tropical deciduous ecosystem along Himalayan foothills. Additionally,
we attempted to establish the relationship between in situ LAI and
the annual litter fall, and to predict aboveground biomass (AGB)
from ground measured LAI for each PFTs.
2. Methodology
2.1. Study area
The present study was undertaken at Katerniaghat Wildlife
Sanctuary (KWLS), a representative tropical deciduous forest in
the upper Gangetic plains adjoining Himalayan foothills in Uttar
Pradesh state, India (Fig. 1). The KWLS is situated between 27 41
and 27 56 N latitude; and 81 48 and 81 56 E longitude, with elevation ranges from 116 to 165 m along the southern border of
Nepal. It is a dense patch of 40 km long and 10 km wide with an
area of 440 km2 . The site experiences climatic variation, typical of
northern India with extremes of heat and cold; and winter nights
are very cold and foggy and heavy dew falls regularly. The nights
remain cool and dew falls until late in the spring, the hot weather
commencing in April and lasting until the rains break toward the
end of June. Heavy monsoon rain is experienced from June end to
September, and along with the winter rainfall an average annual
rainfall of about 1300 mm is experienced.

Fig. 1. Location map of Katerniaghat Wildlife Sanctuary, Uttar Pradesh, India.

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S.K. Behera et al. / Ecological Indicators 58 (2015) 356364

Fig. 2. Layout plan for sampling of 50 m 50 m plot of forest stand by LAI-2000 PCA. (a) The 50 m 50 m plot is divided into 25 sub-plots of 10 m 10 m each (numbered
as 125), (b) the position of series of 10 below canopy readings in one measurement cycle (numbered as 110 in layout). The 10 below-canopy measuring points in each
10 m 10 m plot were located along the boundary line of quadrat at 2 m apart from the successive measurement points, 5 measurements each along two perpendicularly
transecting boundaries.

2.2. Forest phytosociology analysis and aboveground biomass

estimation
KWLS forest was analyzed for plant community structure during 20092010. Phytosociological attributes of each tree species
were studied by laying 15 quadrats of 50 m 50 m (0.25 ha) size
each in all three PFTs randomly, for trees (5 cm diameter at breast
height (DBH)). Frequency, density and basal area were calculated
following Misra (1968). Importance value index (IVI) for individual
tree species in each forest community/PFT were calculated (Misra,
1968). The diameters at breast height (DBH) of all stems/trees having 5 cm were measured at 1.37 m within each random sampling
plot in all three PFT communities. Tree species richness (SR) in
each sampled stand was computed (Misra, 1968). We determined
the stand aboveground biomass (AGB) using DBH censuses of each
tree in each sampling random plots. These individual DBH measurements were subsequently converted into estimates of aboveground
biomass using allometric equations for moist deciduous forest
stands that relate tree diameter to biomass (Chave et al., 2005).
Per tree individual biomass was summed for each individual tree
species and all tree species biomass were estimated for each random sampling plots and per stand total AGB (Mg) was calculated.

2.3. LAI measurements

For above three PFTs, relatively homogeneous patches are
dened in order to sample the natural range of the vegetation.
Multiple LAI measurements along with GPS based location information were repeatedly recorded for minimal measurement errors.
Measurements are also performed at multiple spatially distributed
patches in each PFT to capture the wide range.

2.3.1. Indirect measurement of LAI

The LAI of the stands was measured with the LAI-2000 (LI-COR
Inc., Lincoln, NE, USA) plant canopy analyzer in the remote mode,
i.e., by simultaneous readings below canopy at 2 m height above
the forest oor, and in nearby open areas. All measurements were
conducted during periods of overcast sky between August 2011 and
May 2012. A 0.25 ha (50 m 50 m) plot was divided into 25 quadrants of 10 m 10 m each numbered in the measurement protocol
layout (Fig. 2a). A series of 10 below-canopy measurements were
made in each 10 m 10 m quadrant, along the two perpendicular
boundary lines during each LAI measurement cycle (Fig. 2b). On
each 50 m 50 m plot, a total of 25 LAI measurements cycles were
made. The 10 below-canopy measuring points in each 10 m 10 m
plot were located along the boundary line of quadrat at 2 m apart
from the successive measurement points; 5 measurements each
along two perpendicularly transecting boundaries (Fig. 2b). The
measurements in the open were conducted in larger gaps at a distance of not more than 4 km from the plots. We conducted one set of
LAI measurements during post-monsoon period (AugustOctober
2011) and another set of measurements during leaf senescence
stage of summer season (MarchMay 2012) to account for the seasonal variation of LAI in both full leaf stage and leaess stage in each
plot. LAI-2000 plant canopy analyzer measurements were acquired
either at sunset or on overcast days. All below canopy readings
were made at 270 view angle with the sensor at 2 m height from
the ground level, to include all the multistory canopy layers excluding the ground vegetation. Total 30, 40 and 25 numbers of plots of
50 m 50 m were sampled for in situ LAI measurements in each dry
miscellaneous, sal mixed and teak plantation PFTs for two seasons.
Measuring LAI at a height of 2 m ignores the vegetation closer to the
ground, which can constitute at least one foliage layer. Data from
15 sampling plots were used for correlation analysis.

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359

2.3.2. Estimating LAI through litter traps

The traps that collected the litters were installed at random locations within each forest stands and emptied at several occasions
during the fall season, every 45 weeks after the rst to last leaf
fall. The traps had a circular area with a diameter of about 50 cm
and were placed about 1 m above the ground. Branches and other
non-leafy material were removed, the leaves were dried at 70 C for
24 h and total dry weight of the leaves was obtained. Total annual
litter fall was then estimated for the year 2012 in each PFT. Owing
to extensive manual labor, it was decided to use only 10 random
traps in all the random quadrat plots of 50 m 50 m for collecting,
drying and weighing the litter.
2.4. Data analysis
Linear regression analyses were applied to identify signicant
relationships between LAI as an independent variable and density
of stems (dbh 5 cm), tree diversity (species richness), and stand
basal area as dependent variables. Scatter plot of community structural parameters like stand basal cover (m2 ha1 ), stem density/tree
density (stem/individual ha1 ), species richness (SR) values were
plotted against stand LAI values (post-monsoon). All the statistical analysis was done between the LAI of full canopy development
stage/full green stage (post-monsoon LAI value) and the variables
to establish the optimum relationship. All the statistical analysis
including two ways ANOVA were done by using GraphPad Prism
software (Prism Version 6).
3. Results and discussion
Ground LAI values ranged between 2.41 and 6.89, 1.17 and 7.71
and 1.92 and 5.19 with 270 view angles in dry miscellaneous,
sal mixed and teak plantation PFTs during post-monsoon season,
respectively (Fig. 3a). Sal mixed showed maximum range of LAI values forming fairly open to very dense canopy, whereas teak being
a managed ecosystems having row plantations showing moderate
range of LAI values. Dry miscellaneous, which comprises 3540% of
the sanctuary area is well represented with three storied canopy
architecture with full grown woody lianas, showed higher LAI (>5)
values in majority of stands (Fig. 3a). Ground LAI values ranged
between 1.36 and 4.49, 0.67 and 3.1 and 0.37 and 1.83 with 270
view angles in dry miscellaneous, sal mixed and teak plantation
PFTs during summer season, respectively (Fig. 3b). Nackaerts et al.
(2000) also observed best ground based LAI with 270 view caps, as
in the present study, which restricts the observer from coming in
the eld of view of the sensor, at the same time sensing the gap fractions under the canopy. Maximum LAI (LAImax ) in post-monsoon
seasons were observed in sal mixed PFT due to presence of full
grown continuous sal (Shorea robusta) and terminalia (Terminalia
alata) species at the top storey. In summer season, the top storey
canopy gets leaess and the LAI drops drastically in sal mixed PFT
due to poor representation of middle storey canopy. Teak plantation showed lowest LAI values in majority of plots due to lesser leaf
biomass, absence of other major tree associates at top storey layer
and absence of lianas. Dry miscellaneous PFT showed lower LAImax
values compared to sal PFT stands in post-monsoon stage due to
canopy gaps in the top storey layer. Although, dry miscellaneous
forest show high tree density, but the top storey does not form
a continuous canopy, rather have small openings at intervals. Dry
miscellaneous PFT top storey is being dominated by Shorea robusta,
Lannea coromandelica, Adina cordifolia, Madhuca indica, Diospyros
tomentosa, Schleichera oleosa, Streblus asper, Aegle marmelos, Mitragyna parvifolia, Ehretia laevis, Lagerstroemia parviora, which forms
relatively open canopy having sufcient gap fractions, allowing
solar radiation to penetrate down the understory layer allowing

Fig. 3. Box plot showing the (a) in situ LAI (post-monsoon season) (b) in situ LAI
(summer season) (c) annual litter fall trends among three plant functional types
(PFTs) at Katerniaghat Wildlife Sanctuary, Uttar Pradesh, India.

receipt of maximum amount of sun akes (Behera et al., 2012).

Morgan and Smith (1981) in another tropical ecosystem found that
broadleaved dry deciduous forests received more light at understory layer, leading to lower LAI values in comparison to sal mixed
forests.
Two way ANOVA analysis within and among PFTs showed significant difference (P < 0.0001) among LAI value for both the seasons
(post-monsoon and summer) (Table 2). This clearly indicates that
all 3 PFTs are having distinct LAI representations based on different tree species composition, stem density and different vertical
stratication and canopy structure. All three PFTs showed higher
LAI values in post-monsoon season as compared to summer season due to full green canopy development after rainy season in all
PFTs that restrict transmittance of incoming solar radiation to the
forest understory layer. Teak forest understory showed lowest LAI
values among three PFTs in both seasons due to open canopy architecture and least clumping of teak (Tectona grandis) broadleaves in
branches. Teak trees dominate completely in the teak plantation
having 256 IVI. Teak species has been introduced in the sanctuary during last 4045 years as large scale plantation in the clear
felled areas and subsequently as gap lling plantations in rows to
ll the gap due to tree mortality. So later on the teak plantation
has been established as a community with systematically arranged
canopy architecture. As teak plantation is being made in rows with
spacing, therefore sufcient gap exists in the top storey canopy

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S.K. Behera et al. / Ecological Indicators 58 (2015) 356364

leading to higher gap fractions resulting lower LAI in teak stands. Sal
PFT experienced least light transmittance to the understory layer
among the three (Behera et al., 2012). Sal forms a huge tree with
very dense canopy with highest leaf clumping in branches with
multi-storey leaf arrangements in different branches at different
heights. Dense canopy of sal species restricts incoming light transmittance to below canopy resulting highest LAI (LAImax , 7.71) in
post-monsoon season as also observed by Smith et al. (1993).
In summer season, although the top storey tree species like
Lannea coromandelica, Adina cordifolia, Madhuca indica, Diospyros
tomentosa, Aegle marmelos, Mitragyna parvifolia become leaess,
the middle storey and understory layers (specially dense understory layer of Mallotus spp.) which is fairly represented by 34
semi-evergreen species such as Mallotus philippensis, Syzygium
cumini, Schleichera oleosa remains green along with the high density green lianas contributing to comparatively higher LAI in dry
miscellaneous as compared to sal and teak PFTs. Chaturvedi et al.
(2011a,b) reviewed the functional traits (FTs) for four different
categories: leaf traits, stem and root traits, reproductive traits
and traits particular relevant to water availability with particular reference to tropical deciduous forests, recognized incomplete
knowledge about many FTs and highlighted the importance of
detailed characterization of different FTs including detail in situ
LAI measurement for tropical deciduous forest. There is no ground
LAI data available for Indian tropical deciduous forest, whereas
FT SLA (specic leaf area, i.e. the ratio of leaf area to dry mass,
mm2 mg1 ) has been measured (mean value ranging from 10.9 to
11.7) for few deciduous forests of India (Lal et al., 2001; Chaturvedi
et al., 2011a,b; Pandey et al., 2009). Satellite derived LAI (MODIS
8 day composites LAI product at 1-km spatial resolution) varies
from 0.1 to 6.9 among the different forest types of India (Chhabra
and Panigrahy, 2011). Maximum LAI (6.9) was observed in topical
evergreen forest in North-east India and Western Ghats, which is
equal with the maximum LAI (6.89) in dry miscellaneous and lower
than the LAI (7.71) in sal mixed PFTs in our study. MODIS LAI (2.5)
observed in tropical dry deciduous forest in central India is much
lower than the mean LAI value observed for all 3 PFTs in present
study (Chhabra and Panigrahy, 2011). Tropical rain forest stands in
Indonesian Borneo reported LAI value of 7.3 (Yamakura et al., 1986),
which is comparable to sal mixed PFT (LAI, 7.71). All the three PFTs
showed comparable LAI values (5.5 in seasonal forest at Colombia,
Folster et al., 1976; 7.4 in seasonal forest at Cambodia, Hozumi et al.,
1969), whereas lower LAI in comparison to various tropical evergreen forests (10.7 in rain forest at Thailand, Ogawa et al., 1965; 8.0
in tropical rain forest at Malaysia, Kato et al., 1978). However, our
LAI estimates are higher than the LAI reported for eastern Amazonia (lowland forest (5.10), secondary forest (3.46) and pasture
(1.56) in Tapajos region, Eastern Amazonia) (Aragao et al., 2005).
Sal mixed forest showed maximum range of LAI value, as sal tree
stands are ranging from open to very dense canopy, whereas teak
being a partially managed ecosystems showing lowest range of LAI
values among the stands within the PFT class. The variation among
the forest stands is also due to the different species composition
and stem population density.
Although, calibration of optical LAI estimates is labor intensive,
we recommend that our method can be used with cautions in other
dry deciduous and moist deciduous forests of India and south-Asian
countries. As this method takes into account a series of 10 below
canopy reading in one measurement cycle, below canopy readings at 2 m distance fairly estimate the gap fractions ranging from
very open monoculture stands or plantations to very dense moist
deciduous forest having dense lianas and 3 storied canopy architecture. Our method is having advantage over the method followed by
Nackaerts et al. (2000), where they used single below canopy reading at 10 m intervals in each measurement cycle. Present method
fairly sense the small canopy gap areas (<2 m area) (representing

the discontinuity of forest canopy) which is very prevalent in dry

deciduous and moist deciduous tropical forests, which will otherwise lead to overestimation of LAI, if below canopy readings are
taken at large distances under canopy.
3.1. Relationship between litter fall and LAI
Litter fall varied greatly with the forest stands and it was found
to be highest during summer season and lowest during winter season in all types, as expected in a tropical deciduous forest. Annual
litter fall (Mg ha1 ) ranged between 5.99 and 9.44, 5.13 and 8.45 and
3.87 and 7.32 among 15 random sampling plots each in dry miscellaneous, sal mixed and teak plantation PFTs, respectively (Fig. 3c).
Average annual litter fall was maximum in dry miscellaneous forest (7.95 Mg ha1 ) followed by sal mixed forest (7.1 Mg ha1 ) and
teak plantations (5.2 Mg ha1 ) (Table 1). Two way ANOVA analysis
within and among PFTs showed signicant difference (P < 0.0001)
for annual litter fall production (Table 2). The variation in litter fall
observed is expected because of differences in species composition,
successional stage and microclimate greatly affect litter fall patterns (Kalacska et al., 2005). Earlier reviews of litter fall have shown
a range from 2.44 to 9.4 Mg ha1 in different forests of the world
(Vitousek and Sanford, 1986). The litter fall estimates of the present
study fall within the range reported from another Indian tropical
forest by Dadhwal et al. (1997). Annual litter fall showed signicant positive correlation with stand LAI (post-monsoon) in all three
PFTs (R2 = 0.887, 0.816 and 0.794 in dry miscellaneous, sal mixed
and teak plantation, respectively: Fig. 4). Litter fall showed strong
positive correlations with LAI in dry miscellaneous stand, being
dominated mostly by deciduous tree species in the top-storey layer,
which gets leaess completely during February-March. Dufrene
and Breda (1995) also got closest estimate with indirect LAI measured from LAI-2000 compared against direct estimates of LAI from
litter collection.
3.2. Relationship of species richness with LAI
Tree species richness (SR) ranged between 5 and 27, 7 and 22
and 4 and 12 among 15 sampling plots of 50 m 50 m each in dry
miscellaneous, sal mixed and teak plantation PFTs respectively.
Average SR was maximum in dry miscellaneous forest (17) followed by sal mixed forest (14) and teak plantations (8) (Table 1).
Tree species richness showed signicant positive correlation with
stand LAI (post-monsoon) in dry miscellaneous and sal mixed
PFTs (R2 = 0.741 and 0.66 in dry miscellaneous and sal mixed
respectively) (Fig. 4). Tree species richness showed weak positive
correlation (R2 = 0.148) with stand LAI in teak PFT, may be explained
due to higher dominance of teak trees in stands (>90% canopy leaf
area) with minimal presence of other species. Therefore, the relationship between LAI and SR in teak plantation is not prominent
as in others, which may be attributed to the dominant effect. SR
showed strong positive correlations with LAI in dry miscellaneous
and sal mixed stands, which clearly indicates higher tree species
diversity in top storey and understory layer leads to more canopy
resulting less gap fractions leading to higher LAI.
3.3. Relationship of tree basal cover with LAI
Stand total tree basal cover (BC) (m2 ha1 ) ranged between
23.56 and 34.39, 26.22 and 35.53 and 13.07 and 26.55 in dry miscellaneous, sal mixed and teak plantations, respectively (Table 1).
Average stand BC (m2 ha1 ) was maximum in sal PFT (30.43)
followed by dry miscellaneous PFT (29.7) and teak PFT (20.08).
BC showed signicant positive correlation with stand LAI (postmonsoon) in all three PFT communities (R2 = 0.915, 0.813 and 0.828
in dry miscellaneous, sal mixed and teak plantation respectively)

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361

Table 1
Ranges of variation in structural and functional parameters (tree species richness, stem density, basal cover, litter fall and aboveground biomass) for three PFTs.
Plant functional type (PFT)

Variable

Dry miscellaneous

Sal mixed

5
27
17 (7.01)

Teak plantation

7
22
14 (4.56)

4
12
8 (2.12)

Tree species richness

(SR)

Minimum
Maximum
Mean ( SD)

Number of individuals
(stem ha1 )

Minimum
Maximum
Mean (SD)

475
650
566.66 (66.59)

350
550
458.33 (66.59)

325
475
398.33 (48.61)

Basal area (m2 ha1 )

Minimum
Maximum
Mean (SD)

23.56
34.39
29.70 (3.29)

26.22
35.53
30.43 (3.65)

13.07
26.55
20.08 (4.96)

Litter fall (Mg ha1 )

Minimum
Maximum
Mean (SD)

5.99
9.44
7.95 (1.18)

5.13
8.45
7.10 (1.10)

3.87
7.32
5.20 (1.07)

Above ground biomass

(AGB) (Mg ha1 )

Minimum
Maximum
Mean (SD)

387.89
457.28
418.41 (24.19)

266.39
329.22
309.95 (22.76)

347.22
451.22
406.19 (31.68)

(Fig. 4). Higher basal cover in all the three PFT communities supports higher stem cover supporting more branches and more leaf
areas leading to higher LAI. Therefore, we may conclude higher the
stem basal cover, higher will be the stand LAI.

big canopy development resulting to higher stand LAI values with

lesser number of stem density. Whereas in dry miscellaneous PFT,
multiple tree associates shared the community equally and having lower basal cover at the same time having higher stem density,
equally contributing in both top and understory layer. Therefore,
more diverse tree community in dry miscellaneous PFT with larger
stem density leads to higher a LAI, showing highest positive correlation between stem density and stand LAI (R2 = 0.827) among
three PFTs.

3.4. Relationship of stem density with LAI

Tree density/stem density (SD) (nos. stem ha1 ) ranged between
475 and 650, 350 and 550 and 325 and 475 among 15 random sampling plots each in dry miscellaneous, sal mixed and teak plantation
PFTs respectively (Table 1). Average stem density (m2 ha1 ) was
maximum in dry miscellaneous (566.66) followed by sal mixed
(458.33) and teak (398.33). Stem density showed strong positive correlation (R2 = 0.827) with stand LAI (post-monsoon) in dry
miscellaneous PFT (Fig. 4). Stem density showed lower positive correlation in sal mixed (R2 = 0.652) and teak plantation (R2 = 0.623)
PFTs (Fig. 4). Sal and teak dominate completely in the community
and showed higher basal cover with less number of stem density in sal mixed and teak plantation PFTs respectively, leading to

3.5. Relationship of above ground biomass with LAI

Total above ground biomass (AGB) (Mg ha1 ) ranged between
347.22 and 451.22, 387.89 and 457.28 and 266.39 and 329.22
among 15 random sampling plots each in dry miscellaneous, sal
and teak PFTs, respectively (Table 1). Average AGB (Mg ha1 ) was
maximum in sal mixed PFT (418.41) followed by dry miscellaneous
(406.19) and teak (309.95). Two way ANOVA analysis within and
among PFTs showed signicant difference (P < 0.0001) for AGB in

Table 2
Two-way ANNOVA test for LAI-2000 PCA indirect LAI (post-monsoon and summer season) and two functional parameters (litter fall and aboveground biomass) within and
among the three PFTs.
Ground LAI among 3 PFTs (post-monsoon season)

Ground LAI among 3 PFTs (summer season)

Source of variation

% of total variation

P value

P value summary

Signicant

% of total variation

P value

P value summary

Signicant

Within PFT class

Among PFT class

84.13
6.552

<0.0001
<0.0001

****
****

Yes
Yes

37.39
58.67

<0.0001
<0.0001

****
****

Yes
Yes

Ground LAI among 3 PFTs (post-monsoon season)

Ground LAI among 3 PFTs (summer season)

ANOVA table

SS

DF

MS

F (DFn, DFd)

P value

SS

DF

MS

F (DFn, DFd)

P value

Within PFT class

Among PFT class
Residual

223.7
17.42
24.77

29
2
58

7.712
8.709
0.4271

F (29, 58) = 18.06

F (2, 58) = 20.39

<0.0001
<0.0001

33.63
52.77
3.544

24
2
48

1.401
26.38
0.0738

F (24, 48) = 18.98

F (2, 48) = 357.4

<0.0001
<0.0001

Annual litter fall (Mg ha1 ) among 3 PFTs

Aboveground biomass (Mg ha1 ) among 3 PFTs

Source of variation

% of total variation

P value

P value summary

Signicant

% of total variation

P value

P value summary

Signicant

Within PFT class

Among PFT class

45.37
53.1

<0.0001
<0.0001

****
****

Yes
Yes

17.9
78.21

<0.0001
<0.0001

****
****

Yes
Yes

Annual litter fall (Mg ha1 ) among 3 PFTs

Aboveground biomass (Mg ha1 ) among 3 PFTs

ANOVA table

SS

DF

MS

F (DFn, DFd)

P value

SS

DF

Within PFT class

Among PFT class
Residual

50.88
59.55
1.719

14
2
28

3.634
29.78
0.0614

F (14, 28) = 59.20

F (2, 28) = 485.0

<0.0001
<0.0001

24,233
105,873
5257

14
2
28

MS
1731
52,937
187.7

F (DFn, DFd)

P value

F (14, 28) = 9.220

F (2, 28) = 282.0

<0.0001
<0.0001

362

S.K. Behera et al. / Ecological Indicators 58 (2015) 356364

Fig. 4. Scatter analysis between the LAI estimated indirectly with LAI-2000 (post-monsoon) (on X axis) against the Litter fall, species richness, tree basal cover, tree density
and aboveground biomass (AGB) among the three PFTs.

the year 2012 (Table 2). AGB showed strong positive correlation
with LAI (post-monsoon) in all three PFT communities (R2 = 0.796,
0.748 and 0.761 in dry miscellaneous, sal mixed and teak PFTs
respectively) (Fig. 4). Higher the LAI, higher is the net carbon
assimilation, higher gross primary productivity, resulting in higher
standing aboveground biomass. Therefore, we may conclude higher
the LAI, higher will be the AGB. Biomass and LAI are important variables in many ecological and environmental models. Chen et al.
(2009) also found similar positive correlation at the plant group
level to estimate plot total vascular aboveground biomass and LAI
(R2 = 0.910.95) in Arctic tundra ecosystems across Canada. The
present study showed strong agreement between stand AGB with
LAI, therefore AGB (Mg ha1 ) can be predicted from ground LAI with
the following equations for different moist deciduous forest PFT
class of India.
AGB = 18.63(LAI) + 311.3 for

drymiscellaneousPFT

(1)

AGB = 16.75(LAI) + 326.0 for

salmixedPFT

(2)

AGB = 27.90(LAI) + 186.6 for

teakPFT

(3)

These liner regression equations can be further improved with

optimized sampling and measurements from other tropical deciduous forests with varied biogeographical regions to account the
micro-climatic and edaphic variability. The present LAI vs AGB
relationships can be further improved by studying the functional
relationship of all three seasonal LAI dynamics on the seasonal
biomass accumulation patterns in all PFTs. The relationships may be
improved with incorporation of longer term spatial and temporal
LAI dynamics.
Among different forest classes, temperate evergreen broadleaf
and needleleaf biomes had the highest mean (SD) LAI values of
5.7 (2.4) and 5.5 (3.4), respectively (Asner et al., 2003). Asner
et al. (2003) reported higher LAI (maximum LAI of 8.9) in tropical

deciduous broadleaf forest, which is higher than the maximum LAI

in all three PFTs in present study. In the wet season, when foliage
is most abundant, LAI ranged widely from 3 to 8 m2 m2 in tropical
moist semideciduous forest on Barro Colorado Island, Republic of
Panama, which is similar with the observed range of LAI in dry miscellaneous (2.416.89) and sal mixed (1.177.71) and higher than
teak plantations (1.925.19) PFTs during post-monsoon in present
study (Wirth et al., 2001). LAI ranged from 2.7 to 8.2 having average
LAI of 5.8 m2 m2 in deciduous forests in western North Carolina,
which is comparable with the LAI range in post-monsoon in dry
miscellaneous and sal mixed PFTs in our study (Bolstad et al., 2001).
Our average LAI (LAIavg in Post-Monsoon) of 4.39 and 3.94 in dry
miscellaneous and sal mixed PFTs are somewhat similar with the
global means determined by Asner et al. (2003) for tropical evergreen forests (4.84.9) and tropical deciduous forests (3.9). Wirth
et al. (2001) also observed similar LAI (mean LAI of 5.41 0.82 in
wet season) in tropical moist semideciduous forest on Barro Colorado Island (BCI), Republic of Panama, which is higher than the
mean LAI in all three PFTs in present study. However, in general it
appears that LAI for tropical forests averages roughly 6.2 m2 m2
(SD = 1.5), suggesting that the mean LAI in post-monsoon for all the
three PFTs is within the lower range of values typically described
for tropical lowland forests (Leigh, 1999). The mean LAI (LAIavg
in Post-Monsoon) of 4.39 measured in dry miscellaneous PFT was
27% lower than the LAI of 6.0 reported by Clark et al. (2008) from
a lowland rainforest in Costa Rica. Our values from dry miscellaneous and sal mixed forests are also similar with the LAI-2000
measurements in three pre-montane to lower montane rainforests
in South Ecuador (5.1 at 1050 m, 4.6 at 1540 m and 3.9 at 1890 m
a.s.l., Moser et al., 2007) and in mountain forests in Sabah, Borneo (5.6 at 700 m, Kitayama and Aiba, 2002). The comparatively
low LAI values in the teak plantations may in part result from the
trees being shorter, being of comparatively young age and without

S.K. Behera et al. / Ecological Indicators 58 (2015) 356364

having middle storey tree layers and relatively poor soil organic carbon in that region (Mishra et al., 2013). Teak plantations showed
lowest LAI values due to lesser contribution of the poorly developed
understory layer to the stand total LAI (Montgomery, 2004). The
present study area represents a wide variation in relative humidity (Behera et al., 2012), shows a wide variation in phenophases
of different tree species associates in different PFTs, which further
needs to be studied in detail to understand the annual LAI dynamics among PFTs and to study the independent contribution of top
storey and understory layer to stand total LAI.

4. Conclusions
The LAI measurement method presented here evaluated the
utility of the LAI-2000 Plant Canopy Analyzer estimates in an Indian
tropical deciduous forest by comparison with annual litter fall estimation. The high R2 (R2 0.8) observed with the 270 azimuthal
viewing in the present method used to evaluate the stand LAI shows
great association between the indirect and direct methods (litter
fall estimation).
The possible inuence of community structural factors such as
species diversity, stem density and basal area on LAI was investigated rst time for Indian tropical deciduous forests. We found a
positive correlation of LAI with three structural parameters (tree
density, tree basal cover and species richness) in 3 PFTS of KWLS.
We found strong positive correlation between LAI and key functional parameter i.e., aboveground biomass (AGB) in all three forest
PFTs (R2 > 0.75). Higher basal cover and stem density in all the three
communities supports higher LAI. Therefore we may conclude that
(i) the community structural parameters (i.e. tree species diversity,
stem density and basal cover) are positively correlated with LAI
and (ii) LAI can be used for predicting the AGB in tropical deciduous forest ecosystems. By having ground LAI data, we could model
the stand AGB for the above 3 PFT classes within deciduous forest biome. The present method can be extrapolated to measure the
LAI in other dry deciduous, evergreen and semi-evergreen forests of
India and other tropical regions. The 10 series of below canopy reading at regular 2 m intervals very well considered the gap fractions
ranging from very less gap fractions having continuous canopies as
in evergreen forests, moderate gap fractions as in semi-evergreen
and moist deciduous forest and highest gap fractions in dry deciduous forests.
The in situ LAI sampling methodology have potential to address
three important aspects of C and water uxes modeling at ecosystem level: (a) optimize the LAI and litter fall information obtained
from eld measurements, which is an advance for models parameterization, compared to the usual random sampling; (b) generate
information for a subsequent scaling up of point eld measurements to landscape level up-scaling; and (c) build a useful basis
for validation of estimations, based on remote sensing data, like
MODIS LAI in the Himalayan foothills region. The wide variability
of LAI within the sanctuary area showed that LAI can be a source
of uncertainty for large-scale process modeling and may lead to
underestimation of net primary productivity (NPP), so therefore
needs to be parameterized carefully while given as input variable
in different regional and global vegetation dynamics models. The
study owes importance to biogeochemical models that require LAI
as an input (e.g., FOREST-BGC; Running and Coughlan, 1988), these
differences in in situ LAI value among different plant functional
types/forest communities highlight the importance of examining a
forest cover segregated by different plant functional types rather
than a single input variable, even though the dependency of these
models on accurate estimates of LAI decreases above a value of
3.0 (Waring and Running, 1998). Models like FOREST-BGC mostly
underestimate the NPP value at global scale particularly for Indian

363

deciduous forests, which is mostly modeled with a default LAI value

of 3, whereas the average LAI value for Indian moist deciduous forest is 4. Therefore present in situ LAI measurements in Indian
deciduous forest will help to parameterize the LAI input variable
for real time expression of NPP in BIOME-BGC. Moreover, present
LAI value can be used by the meteorologist to estimate the accurate forest evapo-transpiration in Indian moist deciduous forests,
because canopy conductance for water vapour is proportional to
LAI. Further more detailed study is required to segregate the wood
area index (WAI) from plant area index (PAI) for different PFTs
and to understand the contribution of WAI for LAI (Eriksson et al.,
2005). Additionally we need to establish the mathematical relationship of satellite derived LAI (MODIS LAI) with in situ LAI for moist
deciduous forests for further global carbon modeling.
Present higher LAI value of moist deciduous forest of Indian
tropics, clearly highlights further need of detail eco-physiological
study for understanding the net ecosystem exchange (NEE) at
regional and global scale. The present study highlighted the variability and diversity in LAI in Indian tropical moist deciduous forest
at PFT class level and therefore LAI needs to be carefully parameterized as input variable for dynamic global vegetation models
(DGVMs) and global carbon model for future NPP prediction and
climate change simulations. Additionally, moist deciduous forest is
one of the major tropical forest biome worldwide, so this in situ
LAI range will help the forest eco-physiology and agrometeorology
modeler to formulate new functional relationship for NPP. Therefore the present signicant LAI differences at PFT class level make
us to understand to parameterize the LAI input variables for global
climate and carbon dynamic model at PFT class level, not to deal at
broad forest class level, as dealt presently and to further develop
new coefcient for linking the Indian tropical deciduous forest NPP
at a global scale. Future scope of the study could be further detail
investigation for monthly LAI cycle for each PFT class and to understand its functional relationship with micro-climate at PFTs level.

Acknowledgements
The authors are grateful to Dr. C. S. Nautiyal, Director, National
Botanical Research Institute (CSIR), Lucknow, India for providing
necessary facilities and encouragement. Mr. Nayan Sahu (CSIRSRF), Mr. Ashish K. Mishra (PA) and Mr. Lav Singh (PA) (CSIR-NBRI
Project NWP-20 and BSC-109) are also acknowledged for their
assistance in the eld. Thanks are also due to Dr. Rupak De, PCCF
(Wildlife), Government of Uttar Pradesh, Lucknow and Sri. Sailesh
Prasad, CCF cum Field Director (Dudhwa National Park), Bahraich
for granting permission to carry out the research and facilities to
visit the area and all the Forest Range Ofcers of Katerniaghat
Wildlife Sanctuary for their valuable support. The funds to carry
out this work were received from CSIR, New Delhi under NWP-020.
The comments and recommendations of two anonymous reviewers
and Associate Editor Roland Achtziger are greatly acknowledged.

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