Two bio-indicators, the Photochemical Reflectance Index (PRI) and solar-induced red and far-red Chlorophyll Fluorescence (SIF), were derived from directional hyperspectral observations and studied in a cornfield on two contrasting days in the growing season. Both red and far-red SIF exhibited higher values on the day when the canopy in the early senescent stage, but only the far-red SIF showed sensitivity to viewing geometry. Consequently, the red/far-red SIF ratio varied greatly among azimuth positions while the largest values were obtained for the "hotspot" at both growth stages. This ratio was lower (approx.0.88 +/- 0.4) in early July than in August when the ratio approached equivalence (near approx.1). In concert, the PRI exhibited stronger responses to both zenith and azimuth angles and different values on the two growth stages. The potential of using these indices to monitor photosynthetic activities needs further investigatio

Campbell, Petya K. E.

Cheng, Yen-Ben

Corp, Lawrence A.

Huemmrich, K. Fred

Kustas, William P.

Middleton, Elizabeth M.

Zhang, Qingyuan

NASA Technical Reports Server

CANOPY LEVEL CHLOROPHYLL FLUORESCENCE AND THE PRI IN A CORNFIELD 
 
Elizabeth M. Middleton
a
*, Yen-Ben Cheng
b
, Lawrence A. Corp
c
, Petya K.E. Campbell
d
,  
K. Fred Huemmrich
d
,Qingyuan Zhang
e
, and William P. Kustas
f
 
 
a
 Biospheric Sciences Laboratory, NASA/ Goddard Space Flight Center (GSFC),  
Greenbelt, MD 20771, USA 
b
 Earth Resources Technology, Inc. (ERT), Laurel, MD 20707, USA 
c
 Sigma Space Corp, Lanham, MD 20706, USA 
d
 Joint Center for Earth Technology/Univ. Maryland Baltimore Co. (JCET/UMBC),  
Baltimore, MD 21228, USA 
e
 Universities Space Research Association (USRA), Columbia, MD 21044, USA 
f
 Hydrology and Remote Sensing Laboratory, USDA/ARS, Beltsville, MD 20705, USA 
*Corresponding author, email: Elizabeth.M.Middleton@nasa.gov 
 
ABSTRACT 
 
Two bio-indicators, the Photochemical Reflectance Index 
(PRI) and solar-induced red and far-red Chlorophyll 
Fluorescence (SIF), were derived from directional 
hyperspectral observations and studied in a cornfield on two 
contrasting days in the growing season. Both red and far-red 
SIF exhibited higher values on the day when the canopy in 
the early senescent stage, but only the far-red SIF showed 
sensitivity to viewing geometry.  Consequently, the red/far-
red SIF ratio varied greatly among azimuth positions while 
the largest values were obtained for the “hotspot” at both 
growth stages.  This ratio was lower (~0.88 ± 0.4) in early 
July than in August when the ratio approached equivalence 
(near ~1). In concert, the PRI exhibited stronger responses 
to both zenith and azimuth angles and different values on the 
two growth stages. The potential of using these indices to 
monitor photosynthetic activities needs further investigation. 
 
Index Terms— Ecosystems, agriculture, hyperspectral 
sensors, photosynthesis 
 
1. INTRODUCTION 
 
Determining the health and vigor of vegetation using high 
spectral resolution remote sensing techniques is a critical 
component in monitoring productivity from both natural and 
managed ecosystems and their feedbacks to climate [1].  
Two spectrally based indices now used in field studies to 
assess whether vegetation is performing near-optimally or 
exhibiting symptoms of environmental stress (e.g., drought 
or nutrient deficiency, non-optimal temperatures, etc.) are 
the Photochemical Reflectance Index (PRI) [2] and solar-
induced red and far-red Chlorophyll Fluorescence (SIF)[3-
5].  Both the PRI and SIF express the dynamics of 
photosynthetic function within green foliage:  the PRI is 
based on reflected radiation in the green spectrum associated 
with photoprotection via the xanthophyll cycle [2,6-9], 
whereas SIF [10] measures the absorbed photosynthetically 
active radiation discarded through emissions, rather than 
being utilized for photosynthesis.  Our previous research 
demonstrates that the PRI displays directional responses that 
are strongly expressed and which can be related to the sunlit 
and shaded canopy fractions [6-9, 11-13].  Here, we 
examine the directional characteristics of red and far-red SIF 
and their ratio (red/far-red SIF ratio), and compare with 
those simultaneously acquired for the PRI, in a cornfield at 
two growth stages in 2010. 
 
2. METHODS 
 
In a USDA-ARS experimental field site located in 
Beltsville, MD, USA, canopy optical and biophysical 
measurements were acquired for a corn crop throughout the 
2010 growing season, with the results from two growth 
stages are described here.  Canopy passive optical 
measurements were made at nadir and for directional 
observations with a USB4000 Miniature Fiber Optic 
Spectrometer (Ocean Optics Inc., Dunedin, Florida, USA) at 
several times of day, to enable retrieval of SIF and PRI as a 
function view zenith angle  (VZA, V) and relative azimuth 
angle (RAA, ) at different times of day. The PRI is a 
normalized difference index (computed as the difference 
divided the sum) for reflectance measured at 531 nm and 
570 nm [3].  SIF was determined from retrievals in the 
atmospheric oxygen absorption features centered at 688 and 
760 nm using a modified Fraunhofer Line Depth (FLD) 
method [5]. 
https://ntrs.nasa.gov/search.jsp?R=20120015312 2019-08-30T22:18:14+00:00Z
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r/
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)
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SIF@Red
SIF@Far-red
Red/Far-red
(a) (b)
(c)
RAA
VZA
(d)
Red SIF
Far-red SIF
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R
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Far-red SIF
 
Figure 1. The daily average values for the red and far-red SIF (a,b), their ratio (a,b,c,d), and the PRI (c,d) obtained at four 
view zenith angles (VZA= 0
o
, 30
o
, 45
o
, 60
o
) with eight relative azimuth angles (RAA = 0
o
, 45
o
, 90
o
, 135
o
, 180
o
, 225
o
, 270
o
, 
315
o
) on two field days in 2010 -- July 1(left)  and August 9 (right). Y axes are: F(W/m
2
/sr/nm) and PRI (left side) and SIF 
ratio(right side). 
 
3. RESULTS 
 
We examined the SIF measured in situ with various 
directional viewing configurations on two contrasting days 
during the 2010 growing season that represent early (July 1) 
vs. late (Aug. 9) vegetative canopy conditions for the 
cornfield.  The young canopy on July 1, comprised entirely 
of healthy, green foliage at ~1 m height, was actively 
growing and relatively unstressed.  One month later in 
August, the lower canopy had begun to senesce after the 
mature canopy had attained full height (~2 m) and entered 
the early senescent stage (R3).  Daily averages for canopy 
remote sensing observations [Fig. 1] acquired in complete 
360o azimuth sweeps at three VZAs ( V = 30
o
, 45
o
, 60
o
) 
differed significantly: (a) for the SIF at the two growth 
stages, and (b) for SIF vs. PRI at both growth stages.  For 
the young crop, SIF in the red band [Fig. 1a] was relatively 
constant at ~0.0055 ± 0.0025 W/m
2
/sr/nm at all viewing 
conditions (3 V, 8 ) whereas far-red SIF was slightly 
higher and increased for V 30
o→60o (0.0055-0.0067 
W/m
2
/sr/nm). 
   SIF in both bands was greater in the mature canopy 
[Fig. 1b] where average SIF decreased for V 30
o→60o.  
But, the red SIF at this stage remained relatively insensitive 
to RAA differences, declining only slightly at the oblique V 
= 60
o
 (~0.0061 to 0.0058 W/m
2
/sr/nm).  However, the 
average far-red SIF exhibited a significant decrease (from 
0.0065 to 0.006 W/m
2
/sr/nm) at oblique V, and significant 
variation with .  The highest far-red SIF in the mature 
canopy was obtained at smaller V (nadir, 30
o
) and near the 
“coldspot” associated with shaded foliage at each V.  These 
responses affected the red/far-red SIF ratios:  the largest 
ratio values were obtained for the “hotspot” (  = 0o) at both 
growth stages.  This ratio was lower (~0.88 ± 0.4) in early 
July, indicating relatively more red than far-red SIF was 
emitted from the canopy, than in August when the ratio 
approached equivalence (near ~1) [Fig. 1 a,b] but varied 
greatly among azimuth positions at each V (0.83 – 1.07) 
and, most important, was highest for any V at the hotspot.  
In concert, the PRI exhibited stronger directional responses 
than the SIF ratio, and showed consistent patterns with RAA 
variations, where for both growth stages the higher PRI 
values retrieved at any V were associated with the coldspot 
[Fig. 1 c,d].  The average PRI increased with V in the 
young “unstressed” crop, but was more influenced by 
azimuth position in the mature crop.  Clearly, the directional 
trends for the PRI and the SIF ratio exhibit inverse patterns 
[Fig. 1 c,d]. 
   The daily averages (X ± SE) are summarized for these 
results [Fig. 2] along the solar principal plane for the hotspot 
(RAA = 0
o
, orange bars) and the coldspot (RAA = 180
o
, 
purple bars); nadir values (green bars) are included for 
comparison.  For the young canopy, daily averaged red SIF 
was equal for hotspot vs. coldspot vs. nadir, at each V [Fig. 
2a].  A similar pattern in the mature canopy was obtained at 
the hotspot, coldspot, and nadir viewing positions for red 
SIF, but values were somewhat higher and more variable 
[Fig. 2b].  However, the SIF ratio exhibited higher values at 
the hotspot at both growth stages, a trend that continued and 
was more strongly expressed in the mature canopy where a 
significantly lower SIF ratio was obtained at nadir [Fig. 
2c,d].  In contrast to the SIF ratio, the PRI in the mature 
crop was significantly higher for the coldspot at each V, as 
compared to either the hotspot or nadir [Fig. 2f].  A similar 
but less well developed PRI pattern occurred in the young 
crop [Fig. 2e]. 
   A better understanding is gained by examining the 
morning vs. afternoon observations [Fig. 3]. Here, the bar 
chart provides the hotspots as orange (AM) or brown (PM), 
the coldspots as purple (AM) or navy (PM), and nadir as 
either light green (AM) or dark green (PM).   Clearly, lower 
red SIF was obtained in AM vs. PM in the young canopy 
[Fig. 3a].  By Aug. 9, the red SIF in the morning had 
increased and was more variable [Fig. 3b].  The SIF ratio 
was higher in the hotspots vs. coldspots during mornings 
(both dates, Fig. 3 c,d), a trend that was more pronounced in 
the mature stage when the nadir values (AM, PM) were 
lowest.  The PRI values in the mature crop were noticeably 
lower for any pair (e.g., hotspot at V = 30
o
) for morning vs. 
afternoon [Fig. 3f].  Moreover, higher PRI values in the 
coldspot than the hotspot were observed for all examples in 
the mature growth stage [Fig. 3f], a trend that was also 
apparent but not significant in the young crop [Fig. 3e]. 
 
4. SUMMARY 
 
Two spectral indices (PRI, SIF ratio) provided 
complementary information on the photosynthetic function 
of a corn canopy in 2010 at early vegetative and 
reproductive growth stages. More research is needed to 
understand the interrelationship of the PRI, SIF and 
photosynthetic function using remote sensing observations. 
 
5. REFERENCES 
 
[1] Beer, C., M. Reichstein, E. Tomelleri, P. Ciais, M. Jung, N. 
Carvalhais, C. Rodenbeck, M. A. Arain, D. Baaldocchi, G. B. 
Bonan, A. Bondeau, A. Cescatti, G. Lasslop, A. Lindroth, M. 
Lomas, S. Luyssaert, H. Margolis, K. W. Oleson, O. 
Roupsard, E. Veenendaal, N. Viovy, C. Williams, F. I. 
Woodward, and D. Papale, "Terrestrial gross carbon dioxide 
uptake: Global distribution and covariation with climate," 
Science, vol. 329, pp. 834-838, 2010. 
[2] Middleton, E.M., K. F. Huemmrich, Y.-B. Cheng, and H. A. 
Margolis, "Spectral bioindicators of photosynthetic efficiency 
and vegetation stress," in Hyperspectral Remote Sensing of 
Vegetation, P. S. Thenkabail, J. G. Lyon, and A. Huete, Eds., 
CRC Press, pp. 265-288, 2011. 
[3] Gamon, J.A, C.B. Field, W. Bilger, O. Björkman, A. L. 
Fredeen, and J. Peñuelas, "Remote sensing of the xanthophyll 
cycle and chlorophyll fluorescence in sunflower leaves and 
canopies," Oecologia, vol. 85, pp. 1-7, 1990. 
[4] Meroni, M., M. Rossini, L. Guanter, L. Alonso, U. Rascher, R. 
Colombo, and J. Moreno, "Remote sensing of solar-induced 
chlorophyll fluorescence: Review of methods and 
applications," Rem. Sensing of Environ., vol. 113, pp. 2037-
2051, 2009. 
[5]  Maier, S.W., K. P. Günther, and M. Stellmes, "Sun-induced 
fluorescence: A new tool for precision farming," in Digital 
imaging and spectral techniques: Applications to precision 
agriculture and crop physiology, T. Van Toai, D. Major, M. 
McDonald, J. Schepers, and L. Tarpley, Eds., American 
Society of Agronomy, pp. 209-222, 2003. 
[6] Middleton, E.M., Y.-B. Cheng, T. Hilker, T.A. Black, P. 
Krishnan, N.C. Coops, and K.F. Huemmrich (2009), “Linking 
foliage spectral responses to canopy level ecosystem 
photosynthetic light use efficiency at a Douglas-fir forest in 
Canada”, Canadian J. Rem. Sens., vol. 35, pp. 166-188, 2009. 
[7] Hilker, T., N. C. Coops, M. A. Wulder, T. A. Black, and R. D. 
Guy, "The use of remote sensing in light use efficiency based 
models of gross primary production: A review of current 
status and future requirements," Science of The Total 
Environment, vol. 404, pp. 411-423, 2008. 
[8] Hilker, T., N. C. Coops, F. G. Hall, C. J. Nichol, A. Lyapustin, 
T. A. Black, M. A. Wulder, R. Leuning, A. Barr, D. Y. 
Hollinger, B. Munger, and C. J. Tucker, "Inferring terrestrial 
photosynthetic light use efficiency of temperate ecosystems 
from space," J. Geophys. Res., vol. 116, p. G03014, 2011. 
[9] Cheng, Y.-B., Middleton, E.M., Hilker, T., Coops, N.C., 
Krishnan, P., & Black, T.A. “Dynamics of Spectral Bio-
indicators and Their Correlations with Light Use Efficiency 
Using Directional Observations at a Douglas-fir Forest”, 
Measurement Science and Technology, vol. 20, 15 pp., 2009. 
[10] Middleton, E.M., Y.-B. Cheng, L. Corp, K. F. Huemmrich, 
W. Kustas, and P. K. E. Campbell, "Diurnal and Directional 
Responses of Chlorophyll Fluorescence and the PRI in a 
Cornfield," the 4th International Workshop on Remote 
Sensing of Vegetation Fluorescence, Valencia, Spain, 15-17 
November, 2010. 
[11] Cheng, Y.-B., E. M. Middleton, Q. Zhang, L. A. Corp, A. L. 
Russ, J. Dandois, and W.P. Kustas, "Utilizing in situ 
Directional Hyperspectral Measurements to Validate Bio-
Indicators for a Corn Crop Canopy," Ecological Informatics, 
vol. 5, pp. 330-338, 2010. 
[12] Cheng, Y.-B., E.M. Middleton, K.F. Huemmrich, Q. Zhang, 
L.A. Corp, P. Campbell, and W. Kustas, “Spectral Bio-
indicator Simulations for Tracking Photosynthetic Activities 
in a Corn Field,” In, SPIE Optics and Photonics, San Diego, 
CA, USA, 2011. 
[13] Cheng, Y.-B., E.M. Middleton, Q. Zhang, L.A. Corp, A.L. 
Russ, J. Dandois, and W.P. Kustas, W. P., “The 
Photochemical reflectance index from directional cornfield 
reflectances: Observations and simulations”, submitted to 
Rem. Sensing of Environ., Nov. 2011. 
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Coldspot
VZA
(a) (b)
(d)(c)
(e) (f)
R
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d
 S
IF
 /
 F
ar
-r
e
d
 S
IF
 
R
ed
 S
IF
 (W
/m
2
/s
r/
n
m
)
 
Figure 2. The daily average values (mean ± SE) for the hotspot (RAA = 0
o
; orange bars), coldspot (RAA = 180
o
, purple 
bars), and nadir (RAA = 0
o
, green bars) along the solar principal plane were extracted from the full azimuth polar set, 
obtained at four VZAs (0
o
, 30
o
, 45
o
, 60
o
) on July 1 (a,c,e on left) and August 9 (b,d,f on right) in 2010. 
 
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I
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Coldspot
(a) (b)
(d)(c)
(e) (f)
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VZA
SI
F@
R
ed
/ 
SI
F@
Fa
r-
re
d
R
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IF
 (W
/m
2
/s
r/
n
m
)
R
ed
 S
IF
 /
 F
ar
-r
ed
 S
IF
 
 
Figure 3. The average morning (A ) and afternoon (PM) values for three variables are shown: red SIF, top row; SIF ratio, 
middle row; PRI, bottom row.  Results are for the hotspot (orange or brown bars; mean ± SE), coldspot (purple or navy 
bars), and nadir (light green or dark green bars) along the solar principal plane were extracted from the full azimuth polar 
set, obtained at four VZAs (0
o
, 30
o
, 45
o
, 60
o
) on July 1 (a,c,e on left) and August 9 (b,d,f on right) in 2010. 


Canopy Level Chlorophyll Fluorescence and the PRI in a Cornfield

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