*Corresponding author:
Environmental Science
EES-15, Mailstop J-495
Los Alamos National Laboratory
Los Alamos, NM 87545
USA
Direct measurement of LAI in large heterogeneous plant canopies, such as natural forests, is difficult (Baldocchi et al., 1984; Neumann et al., 1989; Daughtry, 1990; Martens et al., 1991). Destructive harvest of leaves is usually undesirable, if not impractical, so methods based on allometry have been developed (Whittaker and Woodwell, 1968; Marshall and Waring, 1986). Further refinements have yielded the sapwood area to leaf area estimate (Grier and Waring, 1974; Whitehead et al., 1984), which still requires much laborious fieldwork before its application at any particular site.
Gap fraction analysis is another indirect method of estimating LAI (Campbell and Norman, 1989; Norman and Campbell, 1989). It has been successfully applied to canopies of small plants and also to tree canopies. Recently, advances in instrumentation for measuring gap fraction in plant canopies and the development of gap fraction inversion models, from which canopy characteristics such as LAI and mean leaf inclination angle can be inferred, have increased the attractiveness of this method (Campbell, 1986).
The basic tenet of gap fraction analysis is that canopy leaf area (or more correctly the one-sided surface area of all canopy elements) can be inferred from measurements of canopy gap area. Gap area can be inferred from canopy photographs, measurement of sunfleck area on the ground, or by estimation of the fraction of the direct solar beam that penetrates the canopy. New optical instruments that can readily provide gap fraction data are the Decagon Ceptometer, the Li-Cor Line Quantum Sensor and the Li-Cor LAI-2000 Plant Canopy Analyzer (Welles, 1990). Additionally, the computerized digitization and analysis of hemispheric photographs for canopy gap fraction is readily available (Rich, 1989, 1990). Functionally, these four instruments are either linear (Ceptometer and Line Quantum Sensor) or hemispherical sensors (Plant Canopy Analyzer and hemispheric photographs ).
The robustness of LAI estimates, especially when various instruments,
analytical assumptions, and sampling schemes are used, needs careful evaluation.
Only a few combinations of instruments and analytical techniques have been
applied to tree canopies; for example, the Ceptometer was used with the
Beer-Lambert Law (Pierce and Running, 1988), and the Plant Canopy Analyzer
with a one-dimensional inversion model (Gower and Norman, 1991). We have
assessed the suitability and performance of four instruments in both broad-leaved
and needle-leaved tree canopies. We have also explored practical considerations
in field application and data analysis that are important to a typical
user of each instrument, and have included a comparison of instrument performance
using either of the two analytical methods. Finally, we have compared two
methods (Beer-Lambert Law and a one-dimensional inversion model) for analyzing
gap fraction data from each instrument.
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The one-dimensional inversion model (Campbell and Norman, 1989; Norman
and Campbell, 1989) has the same assumptions regarding canopy geometry
as the Beer-Lambert Law. However, it requires estimation of canopy gap
fraction at two or more zenith angles, from which it also yields the mean
leaf inclination angle (or mean tip angle). The estimation of gap fraction
as a function of zenith angle is relatively easy with hemispheric photographs
or the Plant Canopy Analyzer, as these instruments acquire data for a range
of zenith angles simultaneously. With the Ceptometer and the Line Quantum
Sensor, data at more than one zenith angle must be obtained by waiting
for the sun zenith angle to change and then re-measuring the gap fraction
at each sampling point.
The needle-leaved forest site was a mixed-conifer forest stand located
near Lava Butte in Sierra National Forest, CA (T13S R28E S25; 36.77°
N, 118.88° W). The forest was dominated by Pinus ponderosa Laws.
and Calocedrus decurrens (Torn ) Florin, but also included Abies
concolor (Gord. & Glend. ) Lindl. and Pinus lambertiana
Dougl. In the forest, 40 sample points were located at 20 m intervals along
two randomly placed 400 m line transects.
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Measurements of below-canopy incident PAR (Eb) were
made while holding the Ceptometer level (using a bubble level) at four
compass directions around each sample point. The average of the four values
was used for subsequent calculations. Diffuse PAR was measured by holding
a 3 cm by 1 m board approximately 20 cm above the instrument to block all
incident direct solar beam. In the orchard, below-canopy diffuse PAR (Ebd)
was measured at five points along a transect from directly below the center
of the canopy (along a row) to the aisle center. Ebd
along the transect was measured before and after measuring Eb
at the set of 40 sampling points. For each of the 40 sampling points, Ebd
was spatially and temporally interpolated from the transect data. We measured
Ea and Ead in an adjacent open field.
In the forest, Ebd was measured at each of the 40 sampling points, and
Ea and Ead were measured in a large
gap (about 30 m diameter) within the forest stand. At least two sets of
PAR measurements were made for each canopy type to yield gap fraction at
more than one solar zenith angle.
Mean LAI values were always lower (paired t-tests, P<0.0001-0.0074) when gap fraction was calculated by including diffuse PAR as compared with subtracting diffuse from total PAR. The decrease in LAI was about the same in forest and orchard canopies (19-29% reduction). The downward bias in LAI that results from including diffuse PAR is expected to increase as diffuse PAR becomes a greater proportion of total below-canopy PAR. Thus, this bias could be significant in many forests.
When diffuse PAR was subtracted to avoid this bias, the numerator of Eq. (3) occasionally became zero when the measured below-canopy diffuse PAR was equal, within the resolution of the instrument, to total below-canopy PAR. This resulted in a gap fraction of zero for which no LAI can be calculated, as the logarithm of zero is undefined. We examined two ways to solve this problem -- by discarding zero gap fraction data points, or by substituting a small number (which reflected the sensitivity of the instrument) for the zero numerator of Eq. (3) when calculating gap fraction.
The small value we chose to substitute was 0.5 m mol m-2 s-1 PAR flux because the Ceptometer PAR readout is in whole units. Hence, when the numerator of Eq. (3) was zero we substituted 0.5. (For comparison, standard PAR in full sunlight is approximately 2000, m mol m-2 s-1.) When gap fraction values of zero were excluded from the calculations (Table 1), the resulting mean LAI values were lower in all eight comparisons than when 0.5 m mol m-2 s-1 was substituted.
The sensitivity of calculated LAI to the substitution of a small value for zero gap fractions is shown for the forest data in Fig. 1. LAI results for two data sets, which differed in number of zero gap fraction values, are plotted. The Line Quantum Sensor data set had 14 zero gap fraction values (17.5% of data set ), and LAI (Campbell's or Beer-Lambert) was more sensitive to this substitution than in the Ceptometer data set, which had only three zero values (3.8% of data set). LAI calculated using the Beer-Lambert Law is more sensitive (steeper slope) than LAI from Campbell's inversion model for both tree canopy data sets. From the regression equations for these lines, we calculated that our substitution of 0.5 m mol m-2 s-1 PAR in the numerator of Eq. (3) is equivalent to substituting a value of about 10-3 for gap fraction.
The Beer-Lambert Law always yielded a higher LAI than Campbell's method (Table 1). The increase in LAI with the Beer-Lambert method ranged from 26 to 88%. Subtracting or including diffuse PAR had little effect on the magnitude of the increase. Line Quantum Sensor results showed a greater response (55-88%increase)than Ceptometer LAI results (26-43%increase).
LAI calculated from the Ceptometer and Line Quantum Sensor differed significantly for the forest regardless of analytical method or whether diffuse PAR was subtracted or included (paired t-tests, 0.0001<P<0.017). Ceptometer LAI was greater than Line Quantum Sensor LAI when Campbell's method was used but Ceptometer LAI was lower when the Beer-Lambert Law was used. For the orchard, the LAI calculated from the Ceptometer and Line Quantum Sensor with Campbell's method did not differ significantly (paired t-tests, P=0.80). However, LAI from these two instruments differed when the Beer-Lambert Law was used with diffuse PAR subtracted (P=0.03) but not when diffuse PAR was included (P=0.09).
Hemispherical photographs
Gap fraction analysis of hemispherical photographs revealed that occasionally
some segments (of the 160 segments per photograph) have gap fractions of
zero. Rather than discard these zero values (which leads to a downward
biased LAI estimate) or substitute a wholly arbitrary value we attempted
to use a value close to the resolution of the digitizing procedure. When
the unweighted openness of a segment was zero we assigned 0.5 pixel of
openness to that segment. Because of the hemispheric projection onto a
flat surface, the number of pixels per segment is lowest at the center
(near the zenith) and highest at the perimeter (near the zenith horizon).
Therefore the substituted gap fraction value (0.5 pixel/number of pixels
per segment) was highest for segments near the center and lowest for those
at the perimeter.
A sensitivity analysis of LAI to the gap fraction value substituted
for zero is presented in Fig. 2. LAI values
calculated by the Beer-Lambert Law are more sensitive than those calculated
from Campbell's inversion model, following the trend found for the Ceptometer
and Line Quantum Sensor data. The forest data set had 23.5% zeroes and
was slightly more sensitive than the orchard data set, which had 21.6%
zeroes. From the linear regression equations of this LAI sensitivity analysis,
we calculated that our 'half-pixel' substitution for zero was equivalent
to substituting a gap fraction of 5 x 10-9 for Campbell's inversion
method and 1.2 x 10-10 for the Beer-Lambert Law calculation.
Three instruments produced values which compared favorably with directly measured LAI for the orchard (Table 2). The Line Quantum Sensor (LAI=3.29) and Ceptometer (LAI=3.23), when used with Campbell's inversion method, or Plant Canopy Analyzer data analyzed with the Beer-Lambert method (LAI=3.25) were not significantly different from the direct measurement (LAI=3.29). Hemispheric photograph data used with Campbell's method (LAI=2.68) underestimated the direct LAI (3.29), but overestimated LAI when used with the Beer-Lambert method (LAI=6.56) .
Correlations among instruments for a given canopy type and analytical technique are given in Table 3. Correlations between instruments of the same type (line or hemispheric sensors) are generally significant (Bonferroni criterion, P<0.002). The highest correlations are between the Ceptometer and Line Quantum Sensor in the orchard (r=0.489-0.852). The correlations between the two hemispheric instruments (r=0.373-0.492) are less strong.
Correlations across instrument types are significant in only one instance.
An exceptionally high correlation (r=0.707) was obtained between
the hemispheric photographs and Ceptometer for the Beer-Lambert Law technique
in the forest. This Ceptometer data set was also correlated with the Plant
Canopy Analyzer LAI values (r=0.419, P< 0.01).
The exception to the extremely high correlation between the analytical
techniques is with the Ceptometer forest data set (r=0.675, P<0.0001;
Table 4). Even when three points that had
zero transmission values are eliminated, the correlation between Campbell
and Beer-Lambert techniques rises to only 0.736. The large intercept (2.16)
decreases to 1.07 when these three values are omitted.
The Plant Canopy Analyzer may underestimate LAI in heterogeneous canopies, and the use of view restrictors (which were not available for this study ) is recommended to overcome this problem (Li-Cor,1989). Lang et al. (1985) found that inverting transmission measurements in a sorghum canopy underestimated directly measured LAI. Separately averaging the logarithms of transmission (or averaging LAI ) for distinctly different regions in the canopy (e.g. large gaps between rows) yields more accurate results (Lang and Yuequin, l 986). The proper use of view restrictors on the Plant Canopy Analyzer has the same effect. Gower and Norman (1991) found that multiplying Plant Canopy Analyzer LAI values by the ratio of total projected needle area to shoot silhouette area (about 1.5) improved the accuracy of LAI estimates of four needle-leaved species. Their technique accounts for the underestimation of LAI caused by the clumping of needles along stems. The accurate results we obtained for orchard LAI using the Plant Canopy Analyzer with the Beer-Lambert Law might be due to offsetting errors: LAI is underestimated by the instrument but overestimated by the analytical technique. With respect to precision, the Plant Canopy Analyzer had the highest precision (lowest coefficient of variation) of any instrument (Table 2).
Hemispheric photographs did not yield an accurate orchard LAI. Inaccuracies in gap sizes may result from subjective thresholding of photographs (Becker et al., 1989). However, a post hoc investigation of our subjective thresholding method showed that mean differences between high and low cover estimates were less than 5%. This difference is too small to account for the inaccuracy of the hemispheric photograph orchard LAI estimates. Hemispheric photographs appear to yield data which are very sensitive to the analytical method used. Hemispheric photograph LAI values calculated with Campbell's method were generally lowest, and Beer-Lambert method were usually highest, among the four instruments. Each hemispheric photograph provides data for 20 zenith angles in eight azimuth directions, which is far more detail than provided by any other instrument. Perhaps the analytical methods, especially Campbell's inversion method, are sensitive to the number or range of zenith angles used for calculation of LAI.
In general, calculated LAI was notably influenced by canopy type and analytical technique, so that results among instruments varied in a complex manner. There was no simple, consistent ranking of LAI values among instruments across the combinations of canopy type and analytical technique (Table 2). This precludes a single cross-calibration among instruments for comparison of LAI among different canopies or analytical techniques.
The failure of a one-dimensional inversion model for canopies that grossly violate assumptions of the model is not surprising. A more complex, three-dimensional model (Norman and Welles, 1983) that considers canopies to be an arrangement of ellipsoids within which canopy elements are randomly distributed may yield better results. However, this model requires more information on the geometry of a canopy than is usually obtained, although some suitable data are available for tree canopies (e.g. Martens et al., 1991; Ustin et al., 1991).
Nevertheless, LAI estimates with these techniques may be improved in
some cases by using a sampling strategy that assumes a two-phase system
-- gap and non-gap (canopy) regions. This is especially suitable for row-structured
crops and forests before canopy closure. Our LAI results show greater coefficients
of variation in the orchard than in the forest perhaps because our one-phase
sampling was more appropriate for the randomly distributed trees in the
forest than for the row-structured orchard. When sampling a two-phase system,
optical measurements are concentrated in the canopy region and combined
with an estimate of the fraction of canopy region relative to the area
studied to yield an estimate of LAI for the entire area.
The two linear PAR sensors differ little in most respects, except that the Ceptometer is easier for one person to use under field conditions than the Line Quantum Sensor. Both sensors require sunny, cloudless sky conditions for use, and data must be collected at least twice at each point to obtain the gap fraction at two solar zenith angles. Data should be taken near solar noon, especially in dense canopies, because the fraction of direct beam transmitted at low sun angles approaches zero (numerator of Eq. (3 ) ) and requires assumption of an arbitrary value for direct beam PAR. With both instruments, data processing is relatively difficult because the resulting PAR values require much manipulation to obtain the gap fraction. Gap fractions must then be input to a user-supplied program to calculate LAI. Both line sensors are less expensive than either of the hemispheric types and each can be used as a PAR sensor for other applications.
The Plant Canopy Analyzer is relatively expensive and has limited use
other than for LAI measurements. When used in extensive tree canopies without
large gaps, it is necessary to have a second instrument to record simultaneously
above-canopy (or outside-of-canopy) reference readings. The Plant Canopy
Analyzer does not require the user to provide additional data processing
to obtain LAI (Campbell's Method) for each point. This is a significant
advantage over the other instruments because of savings in time and skilled
labor. Plant Canopy Analyzer measurements (and hemispheric photographs)
should be made with the sun at or below the horizon, or with a diffuse
sky, to avoid mistaking brightly sunlit leaves for gaps. This restricts
the time available for data collection to about
h near sunrise or sunset, and could increase the number of field days necessary
to acquire sufficient data. In contrast, use of the line sensors may be
restricted to a few hours near solar noon on sunny days, for reasons described
above.
Hemispheric photographs can be processed by hand, but are most efficiently processed using digitizing hardware and software (e.g. CANOPY program) in a personal computer (Rich, 1989 ). Because of the necessity for film processing, digitizing, and computer analysis, there is a relatively long lag time between data acquisition and LAI, and each step may introduce errors (Rich, 1990). Although the CANOPY program calculates unweighted openness from the digitized images, user-supplied software is still necessary to calculate LAI. However, the gap fraction is more readily obtained from the CANOPY program results than from the linear PAR sensing instruments. Hemispheric photography inherently provides a permanent photographic record of the canopy that may be valuable for other research purposes (e.g. calculating solar tracks and canopy structure).
The equipment necessary for the hemispheric photograph technique represents
a substantial investment (about equal to two Plant Canopy Analyzers). However,
some equipment may already be on hand (e.g. camera and computer) and a
computerized digitizing set-up has many applications other than LAI estimation.
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