Vol.2, No.4, 222-232 (2012) Open Journal of Ecology
http://dx.doi.org/10.4236/oje.2012.24026
Exploring the edge of a natural disaster
Michael W. Jenkins1*, Dan J. Krofcheck1, Rachel Teasdale2,3, James Houpis4,
James Pushnik3,5
1Department of Biology, University of New Mexico, Albuquerque, USA; *Corresponding Author:
2Center for Ecosyetem Research (CER), California State University, Chico, USA
3Department of Geological and Environmental Science, California State University, Chico, USA
4Department of Earth & Environmental Sciences and Office of Academic Affairs, California State University, East Bay Office of the
Academic Affairs, East Bay, USA
5Department of Biological Sciences, California State University, Chico, USA
Received 4 September 2012; revised 16 October 2012; accepted 24 October 2012
ABSTRACT
Natural geological, chronic and acute release of
volcanic gases can have a dramatic impact on
vegetative ecosystems and potential impact on
regional agriculture and human health. This re-
search incorporates a series of observations
using leaf level gas exchange, chlorophyll fluo-
rescence and remotely sensed reflectance mea-
surements of vegetation experiencing chronic
exposure to volcanic gas emissions; to develop
techniques for monitoring the relative health of
vegetation along the edge of an acute vegetative
kill zone of a natural disaster and potential pre-
eruption vegetation physiology. Experiments
were conducted along an elevation gradient that
corresponds to the SO2 gradient on vegetation
along the south flank of Volcán Turrialba, Costa
Rica. This study site is a natural environment
with high volcanic degassing activity with sig-
nificant SO2 emissions (n/d - 0.281 ppm). Cor-
responding to an SO2 gradient, a substantial in-
crease in CO2 concentration of (430 - 517 ppm)
was identified. We further show the physiologi-
cal interactions of SO2 and CO2 have on vegeta-
tion along the kill zone of this natural disaster
can be assessed by examining the SO2/CO2 ra-
tios. The physiological indices tested and rela-
tionships among measurements emphasized in
this research will add to the assessment of the
impact atmospheric volcanic gas emissions
have on the physiology of surrounding vegeta-
tion as well as advance the capability of remo-
tely sensed environmental stress in natural set-
tings.
Keywords: Carbon Dioxide; Chlorophyll
Fluorescence; Leaf Level Gas Exchange; Natural
Disaster; Remote Sensing; Sulphur Dioxide;
Volcanic Gas Emissions
1. INTRODUCTION
On January 4th, 2010 Volcán Turrialba entered a new
phase of activity, marked by an increased number of
volcanic low-frequency signal B type earthquakes and
large and high gas plumes [1]. On January 5th, two mi-
nor eruptive events occurred at 2:29 pm and 2:45 pm,
which emitted ash over local farming areas of La Central
and La Silvia, Capellades town, finer ash at Tierra
Blanca, Llano Grande and Tres Rios, and volcanic dust
in eastern San Jose [1]. Two new small craters opened,
which later joined and formed a fracture-like structure
where gases were expelled at temperatures greater than
350˚C [1]. Residents from nearby farms around the vol-
cano were evacuated. On January 8th the seismic activity
and ash emission decreased, but after almost 144 years of
inactivity, Volcán Turrialba had renewed its eruptive ac-
tivity.
It is well known that tropical forests across the globe
are disappearing [2-8]. It is widely recognized that tropi-
cal forest species are being adversely affected by exploit-
tation, land-use changes, climate change and natural
geological disturbances [7,9,10]. Along with the impor-
tance of tropical plants for their well recognized eco-
logical goods and services of habitat creation and global
carbon balance, these ecosystems have significant impli-
cations on water and soil quality in these regions. This
study is an initial examination of a natural gradient of
impact established by the recent volcanic gas releases on
native vegetation, but has added implications for the ag-
ricultural zone and food supply within the same vicinity
and potential impact on human health.
Sulphur dioxide (SO2) and carbon dioxide (CO2) are
among the atmospheric contaminants and phytotoxic
by-products emitted during recent volcanic activity at
Turrialba. This investigation attempts to characterize the
pre-symptomatic effects of these naturally emitted air
pollutants on the physiological performance of native
plants and their potential influence on the composition
and stability of the ecosystems in which the plants live.

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232 223
Leaf level gas exchange, chlorophyll fluorescence and
spectral reflectance are important tools for evaluating
stress and physiological impacts of air pollutants on
plants [11,12]. The scope of this initial work was to study
the effects of the recent volcanic emissions on photosyn-
thetic activity, chlorophyll fluorescence and reflectance
of plants under stress from chronic exposure to concen-
trations of elevated SO2 and CO2 under otherwise natural
conditions.
Stress is characterized as any disturbing influence that
results in physiological consequences [13]. However, by
the time plants display visible symptoms of stress, they
can already be adversely affected [14]. Photosynthetic
reduction, increase in chlorophyll fluorescence and shifts
in spectral reflectance in the absence of, or prior to, visi-
ble symptom expression could indicate suppression of
growth or reduced vigor in an otherwise apparently
healthy plant [15].
SO2 is a well known stress inducing agent which can
cause toxicity, reduced growth, cell death, plant organ
death and whole plant death; and on a larger scale can
influence biological systems, environments and whole
eco-regions [16]. Environmental conditions, concentra-
tions of SO2, duration of exposure, sulphur status of soil
and genetic attributes of plants determine the degree of
stress and physiological impact due to the phytotoxicity
of SO2 [17].
To investigate the interactive physiological effects of
elevated SO2 and CO2 under naturally occurring condi-
tions, experiments were conducted along an elevation
gradient between 1939 and 3280 meters along the south
flank of Volcán Turrialba, Costa Rica. Measurements
were conducted along an access road, which starts in
Pastora de Santa Cruz, and leads to the entrance to Par-
que Nacional Volcán Turrialba, and the peak of the edi-
fice of the volcano. Volcán Turrialba is a composite stra-
tovolcano located 25 kilometers north east of Cartago on
the eastern end of the Central Volcanic Range (Cordillera
Volcanica Central) and approximately 40 kilometers east
of San Jose, Costa Rica (Lat. 100 020 North, Long. 830
450 West) [18]. The peak of Volcán Turrialba is 3328
meters above sea level and is completely covered by
vegetation except in the caldera [19]. Volcán Turrialba is
the easternmost, and one of Costa Rica’s largest active
volcanoes.
This initial research had three main objectives: 1) to
establish relationships between leaf-level gas exchange
and elevated atmospheric concentrations of SO2 and CO2
related to increased volcanic emissions, 2) to identify
physiological correlations between leaf-level gas ex-
change and chlorophyll fluorescence measurements of
plants under long term stress induced by volcanically
emitted SO2, and 3) to provide evidence that remotely
sensed reflectance-derived fluorescence ratio indices can
be used to monitor plant stress and photosynthetic func-
tioning.
2. STUDY PLANT
Gunnera insignis, common name poor man’s umbrella or
sombrilla de pobre, was chosen as the experimental plant
for this experiment (Figure 1). G. i n si gn i s is located at
the peak of Volcán Turrialba and continuously at all ele-
vations, to approximately 500 meters. G. insignis is a
giant herb ranging throughout Panama, Costa Rica and
Nicaragua at elevations from 500 meters to 3400 meters
[20]. G. insign is inhabits moist, nutrient poor, acidic soils
and is capable of establishing a symbiotic relation with a
nitrogen fixing cyanbacterium (Nostoc sps.). The plant
has a solitary, thick, semi-erect stem, which holds a ter-
minal set of rounded extremely large (can reach greater
than 2 square meters) lobed leaves [20], providing a large
surface for gas exchange with prevailing atmospheric
conditions. Plants found at the lowest elevations at which
G. insignis was identified on the south flank of Turrialba
(1939 meters and 2454 meters), were designated as con-
trol plants, due to minimal levels of detectable atmos-
pheric SO2 concentration and used to run A-Ci, net CO2
assimilation rate, A, versus calculated substomatal CO2
concentration, Ci response curves and light response
curves.
Under natural conditions, multiple environmental stre-
ssors co-occur and can result in a wide range of physio-
logical effects. Analysis of the A/Ci curve and the light
response curve showed sample plants in this study were
neither light or CO2 stressed. The leaf temperature/air
temperature ratio shows that physiological shifts toward
increasing heat production, was limited, indicating mi-
nimal stress of control plants (Table 1).
3. GAS EXCHANGE
Simultaneous measurements of leaf level gas-ex-
change including CO2 assimilation rate (A), stomatal
conductance (gs), intercellular CO2 (Ci) and chlorophyll
fluorescence parameters of steady state fluorescence (F),
quantum yield of PSII calculated from
s

msm
F
FF
''
and maximum quantum yield of PSII calculated from


vm
F
F
''
as well as CO2 response and light response
curves were taken using infrared gas analyzers and a
Leaf Chamber Fluorometer (LCF) [21].
Leaf level gas exchange on G. insignis and atmos-
pheric SO2 and CO2 concentrations were measured at
elevations ranging between 1939 meters and 3280 meters
(Table 1 and Figure 1). A steady rise in atmospheric SO2
and CO2 concentrations with a corresponding rise in ele-
vation was detected during a 24-hour sampling period
(Table 1). A few anomalies were observed; at 2773 m,
SO2 measurements were lower than the previous lower

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232
224
9.97941 9.98941 9.99941 10.0094 10.0194 10.0294 10.0394
-83.79 -83.78 -83.77 -83.76 -83.75 -83.74
PREVAILING WIND
Figure 1. Map of Volcán Turrialba, access road (orange) with white arrows identifying sampling sites
with elevations A = 1939 m, B = 2454 m, C = 2594 m, D = 2673 m, E = 2789 m, F = 2950 m, and G =
3280 meters used for SO2, CO2 and physiological measurements. The highlighted area is the kill zone.
Image in bottom right is the study plant G. insignis.
valid comparisons. However, results may be seen as a
way to gain a better understanding of the interactive im-
pacts of naturally elevated SO2 and CO2 on the species
studied under these ecologically shifting conditions bor-
dering the edge of a natural disaster.
elevation, and at 2789 meters there was much lower SO2
measured. These anomalies are attributed to microcli-
matic variations in the data collection sites. G. insignis
measured at 2789 meters elevation displayed the maxi-
mum A of 16.7 μmol CO2 m–2 ·s–1 and the maximum gs of
0.329 mol CO2 m–2· s–1, the highest rates observed during
the study.
During this study period, volcanic gas concentrations
along an elevation gradient ranged from 0.2805 ppm to
non-detectable for SO2 and from 517 to 430 ppm for CO2.
SO2 concentrations of 4.872 ppm were identified at the
edifice of Volcán Turrialba at an elevation of 3280 meters
(Table 1). However, the measurements recorded at these
sites are not included in the experiments described below
The first objective of this research was to establish re-
lationships between leaf-level gas exchange and elevated
atmospheric concentrations of SO2 and CO2 due to geo-
logic emissions. Due to a limitation on the time available
to conduct this research it is difficult to make statistically
OPEN A CCESS

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232 225
Table 1. Gas exchange parameters measured on Gunnera insignis at different elevations with corresponding SO2 and CO2 concentra-
tions.
Elevation SO2 CO2 Photo (A) Ci Conductance (gs) LeafTemp/AirTemp
(meters) (ppm) (ppm)(μmol CO2 m–2·s–1) (μmol CO2 mol·air–1) (mol CO2 m–2·s–1) (˚C)
1939 n/d 430 14.9 278 0.275 1.03
2454 n/d 490 12.3 312 0.286 0.75
2594 0.053 - 10.75 306 0.236 0.74
2673 0.182 460 13.55 279.5 0.211 0.84
2773 0.137 440 12.65 303 0.258 0.68
2789 0.076 517 16.7 294 0.329 0.97
2950 0.281 430 15.17 247.7 0.184 0.99
due to extreme foliar damage and all related physiologi-
cal processes. A measurements reported in this study de-
monstrate a weak correlation with SO2 concentrations (r2
= 0.0575). Previous studies reveal that photosynthetic
response to SO2 exposure depends on pollutant dose and
genotype, and can either inhibit, stimulate or have no
effect on photosynthesis [16]. Overall, minimal variation
of carbon assimilation rates are observed among plants
tested along this SO2 gradient (Ta bl e 1 ). Moreover, car-
bon assimilation rates were not correlated with other
measurements in this study due to over saturating levels
of CO2 as identified by the A/Ci curve (not shown).
gs and SO2 concentrations are moderately correlated
(r2 = 0.552). Reports on effects of SO2 on gs are highly
variable, and depend strongly on environmental and ex-
posure conditions and SO2 concentrations [22]. Stomatal
conductance has been reported as increasing at low SO2
concentrations in some species, while partial stomatal
closure is induced due to high concentrations of SO2 [16].
In this study A measurements are weakly correlated with
gs (r2 = 0.073). Differences in SO2 uptake due to different
gs may partially explain the differences in SO2 sensitivity
[23], albeit not universally.
Intercellular carbon dioxide (Ci) and SO2 concentra-
tions are also moderately correlated (r2 = 0.514). A/Ci
curves developed from control plants, demonstrated as Ci
increases so does A. However, the correlation between A
and Ci along the study site transect is moderate (r2 =
0.331). In order to identify and quantify the effects of
SO2 on Ci, measurements of mesophyll conductance (gm)
should be included, but unfortunately these measure-
ments were not made. However, the potential impacts of
SO2 effects on mesophyll resistance should not be dis-
carded. SO2 effects on photosynthesis are more likely the
result of increases in mesophyll resistance (e.g. internal
cellular damage), as opposed to decreases in stomatal
conductance. This conclusion is consistent with results
from Barton et al. (1980) [24] and Karenlampi and Houpis,
(1986) [25].
4. CHLOROPHYLL FLUORESCENCE
The chlorophyll fluorescence parameters of steady-
state fluorescence


s
F
, quantum yield

msm
F
FF
''
and max quantum yield


vm
F
F
''
were measured on G.
insignis at elevations of 2673, 2773, 2789 and 2950 me-
ters (Ta b l e 2 ). Electron transport rate (ETR) was calcu-
lated, using the LI-COR algorithm, in simultaneous
measurements. Measurements of chlorophyll fluores-
cence parameters were utilized to evaluate the stress ef-
fects imposed on PSII photochemistry and the physio-
logical correlations between leaf-level gas exchange and
chlorophyll fluorescence of plants under stress from ele-
vated SO2 and CO2 concentrations, identified as the sec-
ond main objective of this study. Results reveal steady-
state-fluorescence


s
F
and interaction between SO2
and CO2 concentrations are moderately correlated and Fs
and A are weakly correlated with (r2 = 0.450, 0.113),
respectively.
The relationship between steady state chlorophyll
fluorescence, quantum yield and maximum quantum yield
and gas exchange measurements of A, gs and Ci is com-
plex and influenced by environmental factors, as well as
physiological adaptations. Dobrowski et al., (2005) [26]
emphasized that the relationship between Fs and A is
mediated through competing de-excitation pathways of
photochemical quenching and non-photochemical quen-
ching. This relationship shows a direct and inverse rela-
tionship depending on the intensity of the stress and the
status of the alternate de-excitation pathways.
Chlorophyll fluorescence parameters; msm
F
FF
''
and ETR are strongly correlated with atmospheric SO2
concentrations (r2 = 0.801 and 0.799), respectively. How-
ever, ETR and A, and msm
F
FF
''
and A show weak

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232
226
Table 2. Chlorophyll fluorescence parameters measured on Gunnera insignis at different elevations with corresponding SO2 concen-
trations.
Elevation SO2 Steady-State Fluores-
cence Quantum Yield Max Quantum Yield Electron Transport Rate
(meters) (ppm)


s
F


msm
F
FF
''


vm
F
F
''
(ETR)
2673 0.182 843.8 0.189 0.611 96.669
2773 0.137 1040.2 0.198 0.664 101.158
2789 0.076 1074.4 0.207 0.715 105.588
2950 0.281 927.7 0.189 0.741 96.38
correlations (r2 = 0.217 and r2 = 0.231), respectively, sug-
gesting the induction of a non-photosynthetically pro-
ductive metabolic pathway which could potentially pro-
vide a target mechanism for a remotely sensed measure
of overall plant health. Previous studies have identified
potentially large alternative electron sinks that contribute
to photo-protection which are particularly important in
plants growing for extended periods under of stressful
conditions [27-30]. Alternative-acceptor-dependent photo-
protection via O2, the water-water cycle, nitrate, sulphate,
light-stimulated synthesis of fatty acids, and oxaloacetate
reduction are among a list of suggested mechanisms which
may enable the progression of ETR under stress condi-
tions to maintain rates similar to those of non-stressed
leaves [30].
Zarco-Tejada et al., (2003) [31] state, “In general,
steady-state chlorophyll fluorescence is low when pho-
tosynthesis is high. However, chlorophyll fluorescence
can also decline when photosynthesis is low, because of
an intensified protective quenching action on chlorophyll
fluorescence production. Under increasing stress, plant
tissues shift toward increasing heat production to dissi-
pate excess energy, and this tends to have the effect of
reducing chlorophyll fluorescence production, at least in
the initial and intermediate stages of stress”. These ob-
servations suggest that under these environmental condi-
tions it is not possible to estimate A directly from Fs,
which is consistent with previous findings [26,32,33].
5. REMOTELY SENSED REFLECTANCE
A standard reflective index used in remote sensing
work is the normalized difference vegetation index
(NDVI), which is an index of chlorophyll content calcu-
lated from

To most accurately track subtle changes in Fs, the dou-
ble-peak optical index (DPi) was utilized, calculated
from


2
688 710697DDD[31]. Due to the complex-
ity of different study methods and field conditions, such
as instruments used, analytical methods, characteristics
of the species tested and changing environmental condi-
tions, no one method has been universally adopted as
satisfactory under all growth and environmental condi-
tions [38].
Leaf level reflectance data from sample plants were
gathered using a portable spectrometer (UniSpec, PP
systems, Haverhill, MA), 1 meter above vegetation. Re-
motely sensed spectra for intact leaves of G. insignis
were measured at elevations of 1939, 2594, 2673, 2789
and 2950 meters with SO2 concentrations of n/d, 0.053,
0.1823, 0.0755 and 0.2805 ppm, respectively (Table 3).
The third main objective of this research was to pro-
vide evidence that remotely sensed reflectance-derived
fluorescence ratio indices can be used to monitor plant
stress and photosynthetic functioning. Leaf reflectance of
SO2 stressed plants show that in at least some cases,
there were significant changes and shifts that could be
detected remotely. When comparing the shifts and changes
in reflectance across a wide range of wave-lengths there
are general trends, but a few inconsistencies. These in-
consistencies could have been caused by frequently
changing environmental conditions, such as changing light
conditions and precipitation causing differences in reflec-
tance.
Reflectance spectra for G. insignis measured at eleva-
tions 2673 and 2950 meters with SO2 concentrations of
0.1823 and 0.2805 ppm, respectively, show maximum
shifts in the Red-Edge region and maximum reflected
PAR (Figure 2). As expected and previously reported
[39-42] the maximum of the first derivative (the inflect-
tion point of the red-edge, IPP) shifted toward shorter
wavelengths, due to pigment degradation. Gates et al.,
1965 [43] provided observations that chlorosis caused by
the loss of chlorophyll induces an increase in reflectance
across the visible spectrum, which causes a blue shift of
the IPP. In addition, Rock et al., (1988) [41] displayed air
pollution results in a blue shift of the IPP due to loss of

750 - 675750675RRR[34]. A revised
version of the NDVI, which is based on a strong corre-
lation and sensitivity to a range of chlorophyll a con-
centrations and shifts in the Red-Edge is defined as chl
NDI or mNDVI
 
750 - 705750705RRR [12,35,
36]. The photochemical reflective index (PRI), which
is based on reflectance at 531 nm and calculated
as
 
531-570531570RR provides a strong esti-
mate of photosynthetic efficiency for most species [37]

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232 227
Table 3. Remotely sensed reflectance indices.
Elevation
(meters)
SO2
(ppm)
Red-Edge
mNDVI
Double Peak
Optical Index Dpi
Photochemical
Reflective Index
PRI
Normalized
Difference
Vegetation
Index NDVI
Modified
Red-Edge mNDI
Reflective
Water Index
WI
1939 n/d 0.585422 0.891596 0.015323 0.86752 0.654559 1.156297
2594 0.053 0.475426 0.953824 –0.00723 0.73413 0.568996 1.105463
2673 0.182 0.505334 1.093702 –0.01248 0.78142 0.595786 1.041003
2789 0.076 0.626071 0.95177 0.047125 0.85928 0.724589 1.130384
2950 0.281 0.433832 1.147461 0.016208 0.65548 0.58324 1.054046
Figure 2. Remotely sensed reflectance and derivative spectrum
on a single leaf of Gunnera insignis at different SO2 concentra-
tions, used to calculate Dpi index measured with Unispec-SC
portable spectrometer (UniSpec, PP Systems, Haverhill, MA)
in the 400 - 1000 and 640 - 820 nm spectral range, respectively.
chlorophyll b.
Reflectance spectra for G. insignis measured at eleva-
tions 1939, 2594 and 2789 meters with SO2 concentra-
tions of n/d, 0.053 and 0.0755 ppm, respectively, show
minimal shifts in the Red-Edge region and the least re-
flected PAR (Figure 2). These results generally corre-
spond to the highest values of CO2, the highest rates of
conductance and the highest A rates. The SO2 and CO2
relationship will be discussed in a following section, but
should be noted throughout these measurement results.
The most useful reflective index incorporated in this
study was that based on the double-peak (Dpi) feature in
the 700 - 715 nm spectral region, as reported and dem-
onstrated by Zarco-Tejada et al., 2003 [31]. Strong cor-
relations were calculated between Dpi and SO2,
msm
F
FF
''
, ETR and CO2 with r2 = 0.975, 0.945, 0.942
and 0.801, respectively. Moreover, Dpi is at least moder-
ately correlated with every physiological measurement in
this study.
It has been previously reported that the double-peak
indicator of fluorescence emission can be detected at
times of higher fluorescence emission can disappear
during times of lowest fluorescence emission [31], cor-
roborating results were found in this study (Figure 2).
However, Zarco-Tejada et al., 2003 [31] observed this
double-peak feature as diminishing with increasing stress
induction. Confounding results from this study are seen
in (Figure 2 and Ta b l e 3 ), which show the greatest Dpi
value of 1.148 and 1.094, corresponding to the highest
level of SO2 concentration of 0.2805 and 0.1823 ppm,
respectively. The Dpi index in this study was developed
as a modified optical index calculated using D702 ×
D715/(D708) 2. The above mentioned results suggest the
Dpi using D702 × D715/(D708)2 is capable of remotely
tracking SO2 induced stress under natural conditions.
In this study, ground based leaf-level reflectance
measurements allowed the evaluation of SO2 induced
stress and showed that shifts in the IPP toward shorter
wavelengths and greater maximum values corresponded
with SO2 stress. And thus the incorporated reflectance
indices appear to be a valid tool for remote tracking of
SO2 induced stress.
6. SULPHUR DIOXIDE AND CARBON
DIOXIDE RELATIONSHIP
Passive monitoring was conducted to determine at-
mospheric gas concentrations of SO2 using Ogawa Pas-

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232
228
sive Air Sampler’s [44]. Lab analyses of [SO2] were
conducted at Anatek Lab, in Moscow, Idaho. [CO2]
measurements were taken using a Vaisala CARBOCAP
Hand-Held Carbon Dioxide Meter GM70 with a GMP222
Carbon Dioxide Probe [45].
This study site is a natural environment with high gas
emission activity with significant SO2 emission. How-
ever, along with the increased SO2 emission a substantial
increase in CO2 concentration was identified (Ta ble 1).
Previous studies have reported an increase in A due to
CO2 enrichment, which has been attributed to an increase
in substrate availability for Rubisco [46]. The reduction
in gs due to high CO2 concentrations is a well known
phenomenon, however this reduction would be expected
to reduce the SO2 flux into the leaf interior, which would
reduce the effective dose of SO2 [47]. The role of CO2
enrichment in protecting plants against harmful airborne
pollutants has been reported in previous studies [48,49].
This SO2 and CO2 relationship is very apparent in the
measurements and observations collected around the
fault scarp at the 2789 meters sampling site (Table 1 and
Figure 1). The fault scarp likely facilitates CO2 accumu-
lation, either by virtue of CO2 emissions along the fault
plane and/or CO2 not being blown away from the low
area due to topography. Measurements collected within
the fault scarp seem to be influenced from the sharp drop
in SO2 from 0.1374 to 0.0755 ppm and back up to 0.2805
ppm (Ta ble 1) and a sharp rise in CO2 from 440 ppm to
517 ppm and back down to 430 ppm (Ta b l e 1). Gas ex-
change measurements of A and gs (Table 1), chlorophyll
fluorescence parameters of Fs, (F'm- Fs/F'm) and ETR
(Table 2) and remotely sensed reflectance indices of
mNDVI, PRI and mNDI were all highest at this sample
site (Table 3).
To emphasize the physiological interaction SO2 and
CO2 concentrations have on vegetation, the capability of
the interaction and induced effects to be remotely de-
tected using the Dpi index a ratio of SO2/CO2 concentra-
tions was developed and correlated with the Dpi index
results. The SO2/CO2 ratio and Dpi index are strongly
correlated (r2 = 0.927). Previous studies have shown that
physiological and physical measurements of plants ex-
posed to elevate CO2 and SO2 were similar to those ob-
served for CO2 enrichment only [47]. The findings of this
study lend further support to the observed relation of the
phytotoxic effect of SO2 is reduced by the positive phy-
siological responses plant undertake when exposed to
increase concentration of CO2 [47].
Limitation of plant growth and/or quantification of
SO2 induced stress cannot be assigned to a single
physiological process or measurement. The direction and
magnitude of the physiological alteration is not com-
pletely clear, and plants’ resistance to SO2 varies de-
pending on the plant species [50]. However, the results of
this study may be used to gain a better understanding of
the impacts of volcanically emitted SO2 on the species
studied, different species, the ecosystem and different
environments under elevated SO2 loading.
From a general analysis of the data collected along the
edge of this kill zone, it may be concluded that SO2 af-
fects G. insignis gas exchange, chlorophyll fluorescence
and reflectance in a variety of ways, which were in some
cases buffered by elevated CO2 concentration. The re-
sults of this study show that elevated CO2 mitigated the
damaging effects of SO2 in G. insignis. This study indi-
cates that G. insignis growing in the volcanically emitted
SO2 toxic region of Volcán Turrialba has developed a
physiological adaptive mechanism that enables the plant
to survive. One point to consider is the easily observable
chlorosis on mature leaves of G. insignis, as opposed to
the non-visible effects on younger leaves, which suggests
the plants resource partitioning mechanisms that allow
young leaves to remain relatively healthy despite high
SO2 levels, but eventually the adaptive adjustments break
down and leaves die. While adaptive responses may de-
velop in certain species and genotypes, most will eventu-
ally succumb to elevated SO2.
It should not be overlooked that results and physio-
logical responses of the study plants in this research
could have been confounded by the presence of other
volcanically emitted air pollutants and possibly a multi-
tude of non-measured environmental perturbations. How-
ever, environmental conditions such as light, moisture
and photoperiod remain fairly constant at these lati-
tudes. Most field experiments have not been able to sepa-
rate and distinguish between the physiological effects of
individual pollutants when they occur in mixtures.
Relationships identified between SO2 and the Dpi in-
dex developed using D702 × D715/(D708)2, Dpi and
quantum yield and Dpi and electron transport rate (r2 =
0.975, 0.945 and 0.942), respectively, along this SO2
gradient further demonstrate the validity to the already
well documented capability of the Dpi index to track
chlorophyll fluorescence. Results of this study add to the
increasing evidence that remote sensing and derivative
reflectance analysis is capable of identifying plant stress
under natural conditions. The capability and extent to
which this study’s findings can be extrapolated to larger
scale detection of SO2 induced stress using aerial and/or
satellite imaging should be further explored. Validation
of this study’s results via similar experiments on vegeta-
tion surrounding other volcanoes with similar gas emis-
sions would be of great value. With the above mentioned
recent increased volcanic activity of Volcán Turrialba and
the importance of the surrounding agricultural areas to
the locals, the region and the country; particular invested
research in both monitoring the volcanic activity and

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232 229
Table 4. NDVI values from Landsat 5 TM and Landsat 7 ETM+ images and ground measurements.
Elevation Dec.13 Dec.27 Jan.15 Apr.5 Ground Data
(m) 2000 2008 2010 2010 (May 2010)
1939 0.8157 0.809 0.7579 0.7654 0.8675
2594 0.8011 0.6445 0.696 0.7942 0.7341
2673 0.6789 0.7279 0.474 0.5524 0.7814
2789 0.7867 0.7692 0.7458 0.5958 0.8593
2950 0.7332 0.6895 0.5729 0.4377 0.6555
( a )
(a)
(b)
(b)
(b)
(c)
(c)
(c)
(d)
1:100000
2 0 0 4
Km
(d)
Figure 3. Landsat TM and ETM+ derived false color composites, near infra-red shown as red, red shown as green and green
shown as blue (4, 3, 2) time series of images used to calculate vegetation indices along the elevation gradient sampled on site
(Table 4). (a) Dec.13, 2000; (b) Dec. 27, 2008; (c) Jan. 15, 2010; and (d) April. 5, 2010. Horizontal white lines are due to the
scan line corrector error present in Landsat ETM+ data following its failure in 2003.
OPEN A CCESS

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232
230
Figure 4. NDVI extracted from available Landsat 5 TM scene
and three Landsat 7 ETM+ scenes over Costa Rica. Each point
represents the NDVI of a 30 meter pixel along an elevation
gradient following the edge of the natural disaster.
surrounding vegetative response is warranted.
7. PERSPECTIVE
This initial examination has highlighted potential phy-
siological measurements to describe effects of volcanic
emissions on G. insignis as an indicator species, but can
be used to emphasize and focus future experiments; from
direct leaf level physiological and reflective measure-
ments on single individuals to ecosystem scale remote
sensing with aerial and satellite imaging capabilities. As
proof of this concept, NDVI values were determined
from Landsat 5 TM and Landsat 7 ETM+ data using the
USGS GLOVIS tool, for temporal periods predating and
concurrent with the volcanic activity as well as a fourth
scene acquired close to the dates of the field campaign:
February 13, 2000, February 27, 2008, January 15, 2010
and April 5, 2010, respectively (Ta b le 4 and Figure 3).
The raw Digital Number (DN) values were converted to
top-of-atmosphere reflectance with dark object subtract-
tion (TOA-DOS) to account for atmospheric effects [51].
We then processed the imagery through a Matlab script
that calculated NDVI and queried pixels according to a
list of GPS coordinates relating elevation to sampling
location from the field campaign. Figure 4 shows the re-
sults of the ETM+ analysis.
When NDVI values are plotted along the elevational
gradient (Figure 4), a trend is easily identified. The first
data point (elevation = 1939 m) plotted in Figure 4
represents the control site with no detectable SO2, and
highest NDVI values. The second data point (elevation =
2594 m) represents minimal SO2 stress (SO2 = 0.053
ppm) with NDVI values dropping from the previous site
(Ta ble 4). The third data point (elevation = 2673) repre-
sents extreme SO2 induced stress (SO2 = 0.1823 ppm)
with moderate CO2 buffering (CO2 = 460 ppm) and dra-
matic drops in NDVI values. The next data point, we
have referred to as “fault scarp” (elevation = 2789 m);
this site displays the greatest CO2 buffering (CO2 = 517
ppm) from SO2 induced stress (SO2 = 0.0755 ppm),
which is clearly demonstrated in the satellite derived
NDVI values. The final data point in Figure 4, represents
the most extreme SO2 induced stress (SO2 = 0.2805 ppm)
and least CO2 buffering potential (CO2 = 430 ppm).
While the interactions between SO2 and CO2 are dif-
ficult to assess and whether the emissions are anthropo-
genic or natural, the ability to determine potential phyto-
toxic induced mortality can greatly limit the conse-
quences and extent of damage. For a more effective as-
sessment and possible control of the effects of atmos-
pheric pollutants on tropical plants and forests, human
health and the environment, it is necessary to further
develop strategies, test hypotheses and build models for
regional and ecosystem monitoring, that are economi-
cally viable, and can be used in remote areas.
REFERENCES
[1] National Seismological Network. (2010) Turrialba vol-
cano, costa rica current activity. Preliminary Report, Red
Sismolo’gica Nacional, 4-10 January 2010, pp. 1-6.
[2] Lanly, J.P. (1982) Tropical Forest Resources. FAO Fo r-
estry Paper 30, United Nations Food and Agricultural
Organization, Rome.
[3] Collins, N.M., Sayer, J.A. and Whitmore, T.C. (1991) The
conservation atlas of tropical forests Asia and the Pacific.
Simon and Schuster, New York.
[4] Food and Agricultural Organization (1993) Forest re-
sources assessment 1990: Tropical countries. FAO For-
estry Paper 112, United Nations Food and Agricultural
Organization, Rome.
[5] Primack, R.B. and Lovejoy, T.E. (1995) Ecology, con-
servation, and management of southeast Asian rainforests.
Yale University Press, New Haven.
[6] Laurance, W.F. and Bierregaard, R.O. (1997) Tropical
forest remnants: Ecology, management, and conservation
of fragmented communities. University of Chicago Press,
Chicago.
[7] Whitmore, T.C. (1997) Tropical forest disturbance, dis-
appearance, and species loss. In: Laurance, W.F. and
Bierregaard, R.O., Eds., Tropical Forest Remnants: Eco-
logy, Management, and Conservation of Frag mented Com-
munities, University of Chicago Press, Chicago, 3-12.
[8] Laurance, W.F. (1998) A crisis in the making: Responses
of Amazonian forests to land use and climate change.
Trends in Ecology and Evolution, 13, 411-415.
[9] Brooks, T.M., Pimm, S.L. and Oyugi, J.O. (1999) Time

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232 231
lag between deforestation and bird extinction in tropical
forest fragments. October, 13, 1140-1150.
[10] Laurance, W.F. (1999) Reflections on the tropical defor-
estation crisis. Biological Conservation, 91, 109-117.
doi:10.1016/S0006-3207(99)00088-9
[11] Panicucci, A., Nali, C. and Lorenzini, G. (1998) Differen-
tial photosynthetic response of two mediteranian species
(Arbutus unedo and Viburnum tinus) to sulphur dioxide.
Chemosphere, 36, 703-708.
doi:10.1016/S0045-6535(97)10111-4
[12] Gamon, J.A. and Surfus, J.S. (1999) Assessing leaf pig-
ment content and activity with a reflectometer. New Phy-
tologist, 143, 105-117.
doi:10.1046/j.1469-8137.1999.00424.x
[13] Rasmuson, M. (2002) Fluctuating asymmetry-indicator of
what. Hereditas, 136, 177-183.
doi:10.1034/j.1601-5223.2002.1360301.x
[14] Omasa, K. and Takayama, K. (2002) Image instrumenta-
tion of chlorophyll a fluorescence for diagnosing photo-
synthetic injury. In: Omasa, K., Saji, H., Youssefian, S.
and Kondo, N., Eds., Air Pollution and Plant Biotech-
nology, Springer-Verlag, Berlin, 287-308.
[15] Boyer, J.N., Houston, D.B. and Jensen, K.F. (1986) Im-
pacts of chronic SO2, O3, and SO2 + O3 exposures on
photosyn-thesis of Pinus strobes clones. European Jour-
nal of Plant Pathology, 16, 293-299.
doi:10.1111/j.1439-0329.1986.tb00194.x
[16] Darrall, N.M. (1989) The effect of air pollutants on
physiological processes in plants. Plant Cell and Envi-
ronment, 12, 1-30.
doi:10.1111/j.1365-3040.1989.tb01913.x
[17] De Kok, L.J. (1990) Sulphur metabolism in plants ex-
posed to atmospheric sulphur, sulphur nutrition and sul-
phur nutrition assimilation in higher plants, fundamental,
environmental and agricultural aspects. SPB Academic
Publishing, Hague, 125-138.
[18] Mooser, F., Meyer-Abich, H. and McBirney, A.R. (1958)
Catalogue of the active volcanoes of the world including
solfatra fields. International Volcanological Association,
Part VI Central America, 6, 144-145.
[19] Alvarado, G.E. and Soto, G.J. (2008) Volcanoes in the pre-
Columbian life, legend, and archaeology of Costa Rica
(Central America). Journal of Volcanology and Ge ot he rm al
Research, 176, 356-362.
doi:10.1016/j.jvolgeores.2008.01.032
[20] Palkovic, L. (1978) A hybrid of Gunnera from Costa Rica.
Systematic Botany, 3, 226-235. doi:10.2307/2418316
[21] LI-COR Bioscience, Inc. (2004) Using the LI-6400 port-
able photosynthesis system, Lincoln, NE, LI-COR Bio-
science, Inc.
[22] Black, V.J and Unsworth, M.H. (1980) Stomatal response
to sulphur dioxide and vapour pressure deficit. Journal of
Experimental Bo ta ny, 31, 667-677.
doi:10.1093/jxb/31.2.667
[23] Dodd, I.C. and Doley D. (1998) Growth responses of
cucumber seedlings to sulphur dioxide fumigation in a tro-
pical environment. Environmental and Experimental Bo-
tany, 39, 41-47. doi:10.1016/S0098-8472(97)00034-8
[24] Barton, J.R., McLaughlin, S.B. and McConathy, R.K.
(1980) The effects of SO2 on components of leaf resis-
tance to gas exchange. Environmental Pollution Series A,
Ecological and Biological, 21, 255-265.
doi:10.1016/0143-1471(80)90129-4
[25] Karenlampi, L. and Houpis, J.L.J. (1986) Structural con-
dition of mesophyll cells of Pinus-ponderosa-var-scopulo-
rum after sulfur dioxide fumigation. Canadian Journal of
Fore st Research, 16, 1381-1385. doi:10.1139/x86-246
[26] Dobrowski, S.Z., Pushnik, J.C., Zarco-Tejada, P.J. and
Ustin, S. (2005) Simple reflectance indices track heat and
water stress-induced changes in steady-state chlorophyll
fluorescence at the canopy scale. Remote Sensing of En-
vironment, 97, 403-414. doi:10.1016/j.rse.2005.05.006
[27] Cornic, G., Le Gouallec, J.L., Briantais, J.M. and Hodges,
M. (1989) Effect of dehydration and high light on photo-
synthesis of two C3 plants. Phaseolus vulgaris L. and
Elastostema repens. Planta, 177, 84-90.
doi:10.1007/BF00392157
[28] Renou, J.L., Gerbaud, A., Just, D. and Andre, M. (1990)
Different substomatal and chloroplastic CO2 concentra-
tion in water-stressed wheat. Planta, 182, 415-419.
doi:10.1007/BF02411393
[29] Noctor, G., Veljovic-Jovanovic, S., Driscoll, S., Novit-
skaya, L. and Foyer, C.H. (2002) Drought and oxidative
load in the leaves of CO3 plants: A predominant role for
photorespiration. Annals of Botany, 89, 841-850.
doi:10.1093/aob/mcf096
[30] Ort, D.R. and Baker, N.B. (2002) A photoprotective role
for O2 as an alternative electron sink in photosynthesis.
Current Opinion in Plant Biology, 5, 193-198.
doi:10.1016/S1369-5266(02)00259-5
[31] Zarco-Tejada, P.J., Pushnik, J.C., Dobrowski, S. and Us-
tin, S.L. (2003) Steady-state chlorophyll a fluorescence
detection from canopy derivative reflectance and double-
peak red-edge effects. Remote Sensing of Environment,
84, 283-294. doi:10.1016/S0034-4257(02)00113-X
[32] Flexas, J., Escalona, J.M., Evain, S., Gulias, J., Moya, I.,
Osmond, C. B. and Medrano, H. (2002a) Steady-state
chlorophyll fluorescence (Fs) measurements as a tool to
follow variations of net CO2 assimilation and stomatal
conductance during water-stress in C-3 plants. Physiolo-
gia Plantarum, 114, 231-240.
doi:10.1034/j.1399-3054.2002.1140209.x
[33] Flexas, J., Bota, J., Escalona, J. M., Sampol, B. and
Medrano, H. (2002) Effects of drought on photosynthesis
in grapevines under field conditions: An evaluation of
stomatal and mesophyll limitations. Functional Plant Bi-
ology, 29, 461-471. doi:10.1071/PP01119
[34] Gamon, J.A. and Qiu, H. (1999) Ecological applications
of remote sensing at multiple scales. In: Pugnaire, F.I. and
Valladares, F., Eds., Handbook of Functional Plant Eco-
logy, Marcel Dekker, Inc., New York, 805-846.
[35] Gitelson, A. and Merzlyak M.N. (1994) Spectral reflec-
tance changes associated with autmn senescence of aes-
culus hippocastanum L. and Acer platanoides L. leaves:
Spectral features and relation to chlorophyll estimation.
Journal of Plant Physiology, 143, 286-292.
doi:10.1016/S0176-1617(11)81633-0

M. W. Jenkins et al. / Open Journal of Ecology 2 (2012) 222-232
232
[36] Gamon, J.A., Field, C.B., Goulden, M.L., Griffin, K.L.,
Hartely, A.E., Peñuelas, J. and Valentini, R. (1995) Relation-
ship between NDVI, canopy structure and photosynthesis
in three Californian vegetation types. Ecological Applica-
tion, 5, 28-41. doi:10.2307/1942049
[37] Filella, I., Peñuelas, J., Llorens, L. and Estiarte, M. (2004)
Reflectance assessment of seasonal and annual changes in
biomass and CO2 uptake of a Mediterranean shrubland
submitted to experimental warming and drought. Remote
Sensing of Environment, 90, 308-318.
doi:10.1016/j.rse.2004.01.010
[38] Ustin, S., Gitelson, A., Jacquemoud, S., Schaepman, M.,
Asner, G., Gamon, J. and Zarco-Tejada, P. (2009) Retrieval
of foliar information about plant pigment systems from
high resolution spectroscopy. Remote Sensing of Envi-
ronment, 113, 567-577. doi:10.1016/j.rse.2008.10.019
[39] Horler, D.N.H., Barber, J. and Barringer, A.R. (1980) Ef-
fects of heavy metals on the absorbance and reflectance
spectra of plants. International Journal of Remote Sens-
ing, 1, 121-136.
[40] Horler, D.N.H., Dockray, M. and Barber, J. (1983) The
red edge of plant leaf reflectance. International Journal
of Remote Sensing, 4, 273-288.
doi:10.1080/01431168308948546
[41] Rock, B.N., Hoshizaki, T. and Miller, J.R. (1988) Com-
parison of in situ and airborne spectral measurements of
the blue shift associated with forest decline. Remote Sen-
sing of Environment, 24, 109-127.
doi:10.1016/0034-4257(88)90008-9
[42] Vogelmann, J.E., Rock, B.N. and Moss, D.M. (1993) Red
edge spectral measurements from sugar maple leaves. In-
ternational Journal of Remote Sensing, 14, 1563-1575.
doi:10.1080/01431169308953986
[43] Gates, D.M., Keegan, V.J., Schleter, C. and Weidner, V.R.
(1965) Spectral properties of plants. Applied Optics, 4, 11-
20. doi:10.1364/AO.4.000011
[44] Ogawa & Co. (1998) NO, NO2, and SO2 sampling proto-
col using the Ogawa sampler, Ogawa & Co., Pompano
Beach.
[45] Vaisala Oyj. (2008) User’s guide vaisala CARBOCAP
hand-held carbon dioxide meter GM70, Helsinki, Finland,
Vaisala Oyj, Helsinki.
[46] Bowes, G. (1993) Facing the inevitable: Plants and in-
creasing atmospheric CO2. Annual Review of Plant Phy-
siology and Plant Molecular Biology, 44, 309-332.
doi:10.1146/annurev.pp.44.060193.001521
[47] Verma, M. and Agrawal, M. (1996) Alleviation of injuri-
ous effects of SO2 on soybean by modifying NPK nutri-
ents. Agriculture, Ecosystems & Environment, 57, 49-55.
doi:10.1016/0167-8809(95)01000-9
[48] McKee, I.F., Eiblmeier, M. and Polle, A. (1997) Enhanced
ozone tolerance in wheat grown at an elevated CO2 con-
centration. New Phytologist, 137, 275-284.
doi:10.1046/j.1469-8137.1997.00801.x
[49] Miller, J.E., Heagle, A.S. and Pursley, W.A. (1998) Influ-
ence on soybean response to CO2 enrichment: II. biomass
and development. Crop Science, 38, 122-128.
doi:10.2135/cropsci1998.0011183X003800010021x
[50] Steubing, L. and Fangmeier, A. (1987) SO2 sensitivity of
plant communities in a beech forest. Environmental Pol-
lution, 44, 297-306. doi:10.1016/0269-7491(87)90205-3
[51] Chavez, P.S. Jr. (1989) Radiometric calibration of landsat
thematic mapper multispectral images. Photogrammetric
Engineering & Remote Sensing, 55, 1285-1294.