We explore the use of active volcanoes to determine the short- and
long-term effects of elevated CO2 on tropical trees. Active
volcanoes continuously but variably emit CO2 through diffuse
emissions on their flanks, exposing the overlying ecosystems to elevated
levels of atmospheric CO2. We found tight correlations
(r2=0.86 and r2=0.74) between wood stable carbon isotopic
composition and co-located volcanogenic CO2 emissions for two of
three investigated species (Oreopanax xalapensis and
Buddleja nitida), which documents the long-term photosynthetic
incorporation of isotopically heavy volcanogenic carbon into wood biomass.
Measurements of leaf fluorescence and chlorophyll concentration suggest that
volcanic CO2 also has measurable short-term functional impacts on
select species of tropical trees. Our findings indicate significant potential
for future studies to utilize ecosystems located on active volcanoes as
natural experiments to examine the ecological impacts of elevated atmospheric
CO2 in the tropics and elsewhere. Results also point the way toward
a possible future utilization of ecosystems exposed to volcanically elevated
CO2 to detect changes in deep volcanic degassing by using selected
species of trees as sensors.
Introduction
Tropical forests represent about 40 % of terrestrial net primary
productivity (NPP) worldwide, store 25 % of biomass carbon, and may
contain 50 % of all species on Earth, but the projected future responses
of tropical plants to globally rising levels of CO2 are poorly
understood (Leigh et al., 2004; Townsend et al., 2011). The largest source of
uncertainty comes from a lack of understanding of long-term CO2
fertilization effects in the tropics (Cox et al., 2013). Reducing this
uncertainty would significantly improve Earth system models, advances which
would help better constrain projections in future climate models (Cox et al.,
2013; Friedlingstein et al., 2013). Ongoing debate surrounds the question of
how much more atmospheric CO2 tropical ecosystems can absorb; this
is known as the “CO2
fertilization effect” (Gregory et al., 2009; Kauwe et al., 2016; Keeling,
1973; Schimel et al., 2015).
Free Air CO2 Enrichment (FACE) experiments have been conducted to probe
this question, but none have been conducted in tropical ecosystems
(e.g., Ainsworth and Long, 2005; Norby et al., 2016). Some studies have used
CO2-emitting natural springs to study plant responses to elevated
CO2, but these have been limited in scope due to the small spatial
areas around springs that experience elevated CO2
(Hattenschwiler
et al., 1997; Körner and Miglietta, 1994; Paoletti et al., 2007; Saurer
et al., 2003). These studies have suffered from several confounding
influences, including other gas species that accompany CO2 emissions at
these springs, human disturbances, and difficulty with finding appropriate
control locations. Additionally, none have been conducted in the tropics
(Pinkard et al., 2010). A series of studies in Yellowstone
National Park (USA) used its widespread volcanic hydrothermal CO2
emissions for the same purpose, though it is not in the tropics
(Sharma and Williams, 2009; Tercek et al.,
2008). Yellowstone was particularly suitable for this type of study due to
its protected status as a national park and because the large areas of
CO2 emissions made control points more available
(Sharma and Williams, 2009; Tercek et al.,
2008). These studies reported changes in rubisco, an enzyme central to
CO2 fixation, and sugar production in leaves, similar to results from
FACE experiments, suggesting that volcanically influenced areas like
Yellowstone have untapped potential for studying the long-term effects of
elevated CO2 on plants.
Tropical ecosystems on the vegetated flanks of active volcanoes offer large
and diverse ecosystems that could make this type of study viable. Well over
200 active volcanoes are in the tropics (Global Volcanism Program, 2013), and
many of these volcanoes are heavily forested. However, fewer of these
tropical volcanic forests have sufficient legal protection for being a source of
long-term information, and the effects of diffuse volcanic flank gas
emissions on the overlying ecosystems remain largely unknown. Most previous
studies focused on extreme conditions, such as tree kill areas associated
with extraordinarily high CO2 emissions at Mammoth Mountain, CA
(USA; Biondi and Fessenden, 1999; Farrar et al., 1995; Sorey et al., 1998).
However, the non-lethal effects of cold volcanic CO2
emissions – away from the peak emission zones, but still in the theorized
fertilization window – have received little attention and could offer a new
approach for studying the effects of elevated CO2 on ecosystems
(Cawse-Nicholson et al., 2018; Vodnik et al., 2018). The broad flanks of
active volcanoes experience diffuse emissions of excess CO2 because
the underlying active magma bodies continuously release gas, dominated by
CO2 transported to the surface along fault lines (Chiodini et al.,
1998; Dietrich et al., 2016; Farrar et al., 1995). This process has
frequently been studied to understand the dynamics of active magma chambers
and to assess potential volcanic hazards (Chiodini et al., 1998; Sorey et
al., 1998). These emissions are released through faults and fractures on the
flanks of the volcano (Burton et al., 2013; Pérez et al., 2011;
Williams-Jones et al., 2000; see Supplement Fig. S1). Volcanic flanks
through which these gases emanate are broad, typically covering
50–200 km2, and often support well-developed, healthy ecosystems. Some
of these faults tap into shallow acid hydrothermal aquifers, but by the time
these gases reach the surface of most forested volcanoes, soluble and
reactive volcanic gas species (e.g., SO2, HF, HCl, and H2S)
have been scrubbed out in the deep subsurface, leading to a diffusely
emanated gas mix of predominantly CO2 with minor amounts of
hydrogen, helium, and water vapor reaching the surface (Symonds et al.,
2001).
Trees in these locations are continuously exposed to somewhat variably
elevated concentrations of CO2 (eCO2), although the
specific effects of this eCO2 on the trees are not well understood.
Volcanic CO2 has no 14C and a δ13C
signature typically ranging from around -7 ‰ to -1 ‰, which is
distinct from typical vegetation and noticeably enriched in 13C
compared to typical atmospheric values (Mason et al., 2017). If trees
incorporate volcanic CO2, then the stable carbon isotopic
composition of wood may document the long-term, possibly variable influence
of volcanic CO2 during the tree's growth. With this tracer
available, volcanic ecosystems could become a valuable natural laboratory for
studying the long-term effects of elevated CO2 on ecosystems,
especially in understudied regions like the tropics. Several studies have
found correlations between variations in volcanic CO2 flux and
plant 14C records at Mammoth Mountain, Yellowstone, and Naples,
which agreed well with previous observations at these well-studied sites
(Cook et al., 2001; Evans et al., 2010; Lefevre et al., 2017; Lewicki et al.,
2014). The Mammoth Mountain and Yellowstone studies linked seismic swarms and
accompanying increases in CO2 flux to decreases in 14C
content in tree rings in one or two trees, demonstrating the method's utility for
uncovering yearly scale variations in volcanic CO2 fluxes (Cook et
al., 2001; Evans et al., 2010; Lewicki et al., 2014). The Naples study
instead focused on using 14C in grasses as short-term (2 to
6 months) monitors of volcanic CO2 flux, which is useful for
volcanic monitoring due to the time-integrated signal they provide (Lefevre
et al., 2017). A study of plants growing at Furnas volcano found very strong
(r2>0.85) correlations between depletions in 14C
and enrichments in 13C from volcanic CO2 in three species
of plants, although this study also had a relatively limited (five samples per
species) dataset (Pasquier-Cardin et al., 1999). The previously mentioned
Naples study also found some correlation between 13C and
14C, although it was not as strong as the study in Furnas (Lefevre
et al., 2017; Pasquier-Cardin et al., 1999). Additionally, short-term effects
of eCO2 might be revealed by plant functional measurements at the
leaf scale, where the additional CO2 could increase carbon uptake
in photosynthesis. A series of studies at Mt. Etna in Italy and
Mt. Nyiragongo in the Democratic Republic of the Congo found linear anomalies
in the NDVI (normalized difference vegetation index), a measure of vegetation
greenness (Houlié et al., 2006). One to two years after the appearance of
the NDVI anomalies, flank eruptions occurred directly along the line of the
anomaly, indicating a plant response to the volcano's pre-eruptive state
which may be due to increased CO2 emissions in the buildup to the
eruption (Houlié et al., 2006). A follow-up study found that the trees on
Mt. Etna were relatively insensitive to changes in temperature and water
availability, strengthening the case that volcanic influence was indeed
responsible for the NDVI anomaly (Seiler et al., 2017).
Here we provide preliminary results on the short- and long-term non-lethal
impacts of diffuse volcanic CO2 emissions on three species of tropical
trees on the flanks of two active volcanoes in Costa Rica. We also explore
the viability in studying volcanically influenced ecosystems to better
understand potential future responses to elevated CO2 and suggest
adjustments to our approach that will benefit future, similarly motivated
studies.
Overview of measurement locations in two old-growth forests on the
upper flanks of two active volcanoes in Costa Rica, Turrialba and Irazú.
Distribution of mean soil CO2 flux across north flank of Irazú
(a) and south flank of Turrialba (b). Colors of dots
correspond to flux populations (see Fig. 3).
MethodsInvestigated locations and sampling strategy
Irazú and Turrialba are two active volcanoes located ∼25 and 35 km
east of San José, Costa Rica (Fig. 1). These two volcanoes are divided by
a large erosional basin. The forested portions of the two volcanoes cover
approximately 315 km2. The vast majority of the northern flanks of
Irazú and Turrialba are covered in legally protected dense old-growth
forest, while the southern flanks are dominated by pastureland and
agriculture. Turrialba rises 3300 m above its base and has been active for
at least 75 000 years, with mostly fumarolic activity since its last major
eruption in 1866 (Alvarado et al., 2006). It has experienced renewed activity
beginning in 2010, and its current activity is primarily characterized by a
near-constant volcanic degassing plume, episodic minor ash emissions, and
fumarolic discharges at two of the summit craters, as well as significant
diffuse and fumarolic gas emissions across its flanks, focused along fault
systems (Martini et al., 2010). Turrialba's CO2 emissions in areas
proximal to the crater were calculated at 113±46 tons d-1
(Epiard et al., 2017). The Falla Ariete (Ariete fault), a major regional
fault, runs northeast–southwest through the southern part of Turrialba's
central edifice and is one of the largest areas of diffuse CO2
emissions on Turrialba (Epiard et al., 2017; Rizzo et al., 2016). Atmospheric
CO2 has an average δ13C value of -9.2 ‰
at Turrialba, and the volcanic CO2 released at the Ariete fault has
significantly heavier δ13C values clustered around
-3.4 ‰ (Malowany et al., 2017).
Irazú has been active for at least 3000 years and had minor
phreatomagmatic eruptions in 1963 and a single hydrothermal eruption in 1994.
Currently, Irazú's activity primarily consists of shallow seismic swarms,
fumarolic crater gas emissions, small volcanic landslides, and minor gas
emissions on its northern forested flank (Alvarado et al., 2006; Barquero et
al., 1995). Diffuse cold flank emissions of volcanic CO2 represent
the vast majority of gas discharge from Irazú, as the main crater
releases 3.8 t d-1 of
CO2 and a small area on the north flank alone releases
15 t d-1 (Epiard et al., 2017). Between the two volcanoes, a major
erosional depression is partially occupied by extensive dairy farms and is
somewhat less forested than their flanks.
In this study, we focused on accessible areas between 2000 and 3300 m on
both volcanoes (Fig. 1). On Irazú, we sampled trees and CO2
fluxes from the summit area to the north, near the approximately north–south
striking Rio Sucio fault, crossing into the area dominated by dairy farms on
Irazú's lower northeastern slope. Of significant importance for this type
of study is that all active volcanoes on Earth continuously emit
CO2 diffusely through fractures and diffuse degassing structures on
their flanks, at distances hundreds to thousands of meters away from the
crater (Dietrich et al., 2016; Epiard et al., 2017), and this elevated
CO2 degassing persists continuously and consistently over decades
to centuries (Burton et al., 2013; Delmelle and Stix, 2000; Nicholson, 2017).
There is no inherent seasonal or meteorological variability in the source gas
pressure, and there is no dependence on shallow soil or vegetation chemistry
or biology (though increased soil moisture in the rainy season, wind, and
atmospheric pressure can modulate gas permeability of the shallow soil;
Camarda et al., 2006). The soil overlying deep-reaching fracture systems acts
as a diffuser through which the volcanic gas percolates and enters the
sub-canopy air. For our study sites, portions of the volcanoes with active
“cold” CO2 degassing have already been assessed and mapped
previously (Epiard et al., 2017; Malowany et al., 2017).
Our sampling locations on Irazú were located along a road from the summit
northward down into the low-lying area. On Turrialba, we focused on an area
of known strong emissions but intact forests on the SW slope, uphill of the
same erosional depression but cross-cut by the major NE–SW trending active
fracture system of the Falla Ariete. We sampled three main areas of the Falla
Ariete, each approximately perpendicularly transecting the degassing fault
along equal altitude, at the upper Ariete fault, the lower
Ariete fault, and a small basin directly east of the old Cerro Armado cinder
cone on Turrialba's southwestern flank. We took a total of 51 tree samples
(17 were excluded after stress screening) at irregular intervals depending on
the continued availability and specimen maturity of three species present
throughout the transect.
All transects are in areas experiencing measurable CO2 enhancements
from the Falla Ariete but that are not high enough in altitude to be in areas
generally downwind of the prevailing crater emissions plume (Epiard et al.,
2017). We avoided areas that experience ash fall, high volcanic SO2
concentrations, and local anthropogenic CO2 from farms or that were
likely to have heavily acidified soil. Excessively high soil CO2
concentrations can acidify soil, leading to negative impacts on ecosystems
growing there (McGee and Gerlach, 1998). Because such effects reflect
by-products of extreme soil CO2 concentrations rather than direct
consequences of elevated CO2 on plants, we avoided areas with
CO2 fluxes high enough to possibly cause noticeable
CO2-induced soil acidification. Light ash fall on some days likely
derived from atmospheric drift, as we were not sampling in areas downwind of
the crater. The ash fall did not, in any noticeably way, affect our samples, as
trees showing ash accumulation on their leaves or previous damage were the
exception and avoided. Altitude, the amount of sunlight during measurements, and
aspect had no consistent correlations with any of the parameters we measured.
Studied tree species
Our study focused on three tree species found commonly on Turrialba and
Irazú: Buddleja nitida, Alnus acuminata, and
Oreopanax xalapensis. B. nitida is a small tree with a
typical stem diameter (DBH) ranging from 5 to 40 cm that grows at elevations
of 2000–4000 m throughout most of Central America (Kappelle et al., 1996;
Norman, 2000). The DBH of the individuals we measured ranged from 11.5 to
51.3 cm, with an average of 29.85 cm. It averages 4–15 m in height and
grows primarily in early and late secondary forests (Kappelle et al., 1996;
Norman, 2000). A. acuminata is a nitrogen-fixing pioneer species
exotic to the tropics that can survive at elevations from 1500 to 3400 m,
although it is most commonly found between 2000 and 2800 m (Weng et al., 2004).
The trees we measured had DBH ranging from 14.3 to 112 cm, with an average of
57.14 cm. O. xalapensis thrives in early and late successional
forests, although it can survive in primary forests as well (Kappelle et al.,
1996; Quintana-Ascencio et al., 2004). It had the smallest average DBH of the
three species, ranging from 6.6 to 40.9 cm, with an average of 22.71 cm.
CO2 concentrations and soil diffuse flux measurements
Soil CO2 flux was measured with an accumulation chamber near the
base of the tree (generally within 5 m, terrain permitting) at three
different points and then averaged to provide a single CO2 flux
value to compare to the 13C measurement of the corresponding tree
sample. This technique is intended to provide a simple relative way to
compare the CO2 exposure of different trees, as a tree with high
CO2 flux near its base should experience consistently higher
CO2 concentrations than a tree with lower CO2 flux. We
also measured concentrations at ground level and 1.5–2.0 m above ground
level, though these were expectedly highly variable in time and location. We
analyzed CO2 fluxes, not concentrations, because the diffuse
emissions of excess volcanic CO2 through the soil, fed from a deep
magma source and dependent on the location of
constant deep geological permeability, are highly invariant in time compared
to under-canopy air concentrations. In contrast, instantaneous concentration
measurements in the sub-canopy air are modulated by many factors, including
meteorology, respiration of vegetation and animals, uptake by plants for
photosynthesis, and diurnal dynamic and slope effects. An approach of
instantaneous highly variable concentration measurements is thus not
representative of long-term exposure. The approach of measuring the largely
invariant soil-to-atmosphere volcanic CO2 fluxes is much more
representative of long-term exposure, varying mostly spatially, and the
site-to-site differences are therefore more representative of the lifetime of
exposure of the trees.
We used a custom-built soil flux chamber system which contained a LI-COR
840A non-dispersive infrared CO2 sensor (LI-COR Inc., Lincoln, NE, USA)
to measure soil CO2 flux. A custom-built cylindrical accumulation
chamber of defined volume was sealed to the ground and remained connected to
the LI-COR sensor. The air within the accumulation chamber was continuously
recirculated through the sensor, passing through a particle filter. The
sensor was calibrated before deployment and performed within specifications.
We recorded cell pressure and temperature; ambient pressure; air
temperature; GPS location; timestamps; location description; wind speed and
direction; relative humidity; and slope, aspect, and altitude as ancillary
data. In typical operation, each measurement site for flux measurements was
validated for leaks (visible in the live data stream display as spikes and
breaks in the CO2 concentration slope), and potential external
disturbances were avoided (such as vehicle traffic, generators, or breathing
animals and humans). Measurements were recorded in triplicate for at least 2 min per site. Data reduction was performed using recorded timestamps in
the dataset, with conservative time margins to account for sensor response
dead time, validated against consistent slope sections of increasing chamber
CO2. Fluxes were computed using ancillary pressure and temperature
measurements and the geometric chamber constant (chamber volume at inserted
depth, tubing volume, and sensor volume). Care was taken to not disturb the
soil and overlying litter inside and adjacent to the chamber.
Leaf function measurements
Chlorophyll fluorescence measurements were conducted on leaves of all three
species during the field campaign to obtain information on instantaneous
plant stress using an OS30p+ fluorometer (Opti-Sciences Inc., Hudson, NH,
USA). Five mature leaves from each individual tree were
adapted to the dark for at least 20 min to
ensure complete relaxation of the photosystems. After dark adaptation,
initial minimal fluorescence was recorded (Fo) under conditions
where we assume that the photosystem II (PSII) was fully reduced. Immediately
following the Fo measurement, a
6000 µmol m-2 s-1 saturation pulse was delivered from
an array of red LEDs at 660 nm to record maximal fluorescence emission
(Fm) when the reaction centers are assumed to be fully closed.
From this, the variable fluorescence was determined to be
Fv/Fm= (Fm-Fo)/Fm.
Fv/Fm is a widely used chlorophyll fluorescence
variable used to assess the efficiency of the PSII and, indirectly, plant
stress (Baker and Oxborough, 2004). The five Fv/Fm
measurements were averaged to provide a representative value for each
individual tree. Some trees had less than five measurements due to the dark
adaptation clips slipping off the leaf before measurements could be taken.
Ten trees had four measurements, and another six had three measurements.
The chlorophyll concentration index (CCI) was measured with a MC-100 Apogee
Instruments chlorophyll concentration meter (Apogee Instruments, Inc., Logan,
UT, USA). The CCI was converted to chlorophyll concentration
(µmol m-2) with the generic formula derived by Parry et al. (2014). Depending on availability, between three and six leaves were measured
for the CCI for each tree and then averaged to provide a single value for each
tree. If leaves were not within reach, a branch was pulled down or individual
leaves were shot down with a slingshot and collected. Photosynthetically
active radiation was measured at each tree with a handheld quantum meter
(Apogee Instruments, Inc., Logan, UT, USA; Supplement Table S2). Stomatal
conductance to water vapor, gs (mmol m-2 s-1), was
measured between 10:00–14:00 h using a steady-state porometer (SC-1,
Decagon Devices, Inc., Pullman, WA, USA), calibrated before use and read in
manual mode. This leaf porometer was rated for humidity < 90 %,
and humidity was sometimes above this limit during our field work.
Consequently, we have fewer stomatal conductance measurements than our other
data types.
Isotopic analysis
We collected wood cores from 31 individual trees at a 1.5 m height using a
5.15 mm diameter increment borer (JIM-GEM, Forestry Suppliers Inc., Jackson,
MS, USA). Since no definable tree rings were apparent, we created a fine
powder for isotope analysis by drilling holes into dried cores using a dry
ceramic drill bit (Dremel) along the outermost 5 cm of wood below the bark,
which was chosen to represent the most recent carbon signal for 13C
analyses. The fine powder (200 mesh, 0.2–5 mg) was then mixed, and a random
sample was used to extract 13C/12C ratios (to obtain
δ13C values against the VPDB standard), which we estimated to
be representative of at least the last 2–3 years, based on analogous
literature growth rate values: O. xalapensis and A. acuminata range from 0.25 to 2.5 and from 0.6 to 0.9 cm yr-1, respectively
(Kappelle et al., 1996; Ortega-Pieck et al, 2011). These rates result in a 5
cm range of at least 2 and 5.5 years, though the high rates were determined
for very young trees under very different conditions, and this is explicitly
unknown in our study. Since we only sample the most recent years, no isotopic
discrimination against atmospheric 13C due to preferential
diffusion and carboxylation of 12C was conducted. Rather, we
assume that δ13C values are representative of the relative
amount of volcanic CO2 vs. atmospheric CO2 sequestered by
the tree over the period of growth represented in the sample.
δ13C values were determined by continuous-flow dual-isotope
analysis using a CHNOS Elemental Analyzer and IsoPrime 100 mass spectrometer
at the University of California Berkeley Center for Stable Isotope
Biogeochemistry. External precision for C isotope determinations is ±0.10 ‰. Ten δ13C measurements did not have
corresponding soil CO2 flux measurements due to the flux
measurements being unavailable for the final 2 days of sampling, and
another five samples were from trees that showed signs of extreme stress, such
as browning leaves or anomalously low fluorescence measurements. Since the
purpose of our study was to explore the non-lethal effects of volcanic
CO2 on trees, during analysis we excluded all trees that were
observed in the field as showing visible signs of stress or being not fully
mature. After these exclusions, all remaining tree cores with co-located
CO2 flux measurements were from Turrialba.
Sulfur dioxide probability from satellite data
To assess the likelihood of trees having been significantly stressed in the
past by volcanic sulfur dioxide (SO2) from the central crater
vents, we took two approaches. First, we were guided by in situ measurements
taken in the same areas by Jenkins et al. (2012), who assessed the
physiological interactions of SO2 and CO2 on vegetation
on the upper slopes of Turrialba and demonstrated a rapid exponential decay
of SO2 away from the central vent. Second, for long-term exposure
we derived the likelihood of exposure per unit area using satellite data
sensitive to SO2 (Fig. 2). The Advanced Spaceborne Thermal Emission
and Reflection Radiometer (ASTER), launched in December 1999 on NASA's Terra
satellite, has bands sensitive to SO2 emission in the thermal
infrared (TIR), at ∼60 m × 60 m spatial resolution. We
initially used ASTER Surface Radiance TIR data (AST_09T), using all ASTER
observations of the target area over the entirety of the ASTER mission
(October 2000 until writing began in late 2017). The TIR bands were corrected for
downwelling sky irradiance and converted into units of
W m-2µm-1. For each observation, an absorption product
is calculated by subtracting SO2-insensitive from
SO2-sensitive bands:
St=b10+b12-2⋅b11,
where S is the SO2 index, t is an index representing the time
of acquisition, b10 is the radiance at band 10
(8.125–8.475 µm), b11 is the radiance at band 11
(8.475–8.825 µm), and b12 is the radiance at band 12
(8.925–9.275 µm). This is similar to the method of Campion et
al. (2010). The granules were then separated into day and night scenes,
projected onto a common grid, and then thresholded to
S>0.1 W m-2µm-1 and converted into a probability
(Abrams et al., 2015). The output is a spatial dataset that describes the
probability of an ASTER observation showing an absorption feature above a
0.1 W m-2µm-1 threshold across the entirety of the
ASTER observations for day or night separately. The number of scenes varies
per target, but they tend to be between 200 and 800 observations in total,
over the 17-year time period of satellite observations. However, certain
permanent features, such as salt pans, show absorption features in band 11
and therefore have high ratios for the algorithm used. We therefore used a
second method that seeks to map transient absorption features. For this
method, we subtract the median from each St, yielding a median deviation
stack. By plotting the maximum deviations across all observations, we then
get a map of transient absorption features; in our case, these are mostly
volcanic SO2 plumes, which map out the cumulative position of
different plume observations well. To speed up processing, some of the
retrieval runs were binned in order to increase the signal-to-noise ratio,
since the band difference can be rather noisy.
The influence of two potentially confounding gases on our study area
(right-hand white shape) in Costa Rica is low to non-existent:
anthropogenic CO2 from San José (blue to red color scale), and
volcanic SO2 (purple color scale). White shapes are drawn around locations of the
forested active volcanic edifices in Costa Rica. The red dashed line
indicates the rough border of the San José urban area. Prevailing winds
throughout the year consistently blow all anthropogenic CO2 away from
our study area and from all other white shapes.
Modeling the anthropogenic CO2 influence from inventory
data
We assessed the likelihood of anthropogenic CO2, enhancements of
air from San José, Costa Rica's capital and main industrial and
population center, influencing our measurements. We used a widely applied
FLEXible PARTicle dispersion model (Eckhardt et
al., 2017; Stohl et al., 1998, 2005; Stohl and Thomson, 1999) in a forward
mode (Stohl et al., 2005), FLEXPART, to simulate the downwind concentrations
of CO2 in the atmosphere (e.g., Belikov et al., 2016), due to
inventory-derived fossil fuel (FF) emissions in our study area for the year
2015 (Fig. 2). The National Centers for Environmental Prediction (NCEP) –
Climate Forecast System Reanalysis (CFSR) – 2.5∘ horizontal
resolution meteorology (Saha et al., 2010a, b) and 1 km Open-source Data
Inventory for Anthropogenic CO2 (ODIAC; Oda and Maksyutov, 2011)
emissions for 2015 were used to drive the FlEXPART model. The CO2
concentrations were generated at a 1 km spatial resolution within three
vertical levels of the atmosphere (0–100, 100–300, and 300–500 m) that
are possibly relevant to forest canopies in Costa Rica. However, to assess
the magnitude of enhancements we only used CO2 concentrations
observed within the lowest modeled level of the atmosphere, from 0 to 100 m.
Validation of the model with direct observations was not required because we
were only interested in ensuring that anthropogenic CO2 dispersed
upslope from San José was not having a significant effect on our study
area; we were not aiming to capture intra-canopy variability, typically
present at tens to hundreds of parts per million variable, which is not
relevant to the better mixed, distal single-digit-or-less parts per million signal from San José. The actual
concentration of CO2 and any biogenic influence in the modeled area
was irrelevant because the spatial distribution of anthropogenic
CO2 was the only factor relevant for this test. 2015 was used as a
representative year for simulating the seasonal cycle of CO2
concentrations that would be present in any particular year.
ResultsVolcanic CO2 emissions through the soil
We measured CO2 flux emitted through the soil at 66 points over
4 days (Fig. 1). The first eight points were on Irazú, and the rest
were located near the Ariete fault on Turrialba. Mean soil CO2 flux
values over the entire sampling area varied from 3 to
37 g m-2 d-1, with an average of 11.6 g m-2 d-1 and
a standard deviation of 6.6 g m-2 d-1. A 12-bin histogram of
mean CO2 flux shows a bimodal right-skewed distribution with a few
distinct outliers (Fig. 3). Fluxes were generally larger on Irazú than on
Turrialba. This result agrees with previous studies which showed that the
north flank of Irazú has areas of extremely high degassing, whereas most
of our sampling locations on Turrialba were in areas that had comparatively
lower diffuse emissions (Epiard et al., 2017; Stine and Banks, 1991). We used
a cumulative probability plot to identify different populations of
CO2 fluxes (Fig. 3; Cardellini et al., 2003; Sinclair, 1974).
Soil CO2 flux into the sub-canopy air of forests on the
Turrialba–Irazú volcanic complex is pervasively and significantly influenced by a deep volcanic gas source. At least four different overlapping populations of soil
CO2 flux were identified using a cumulative probability plot, where inflection points indicate population boundaries (Sinclair 1974).
69 % of sampling locations (45 total) are exposed to varying degrees of
volcanically derived elevated CO2. Populations are color-coded based
on the same color scale as Fig. 1.
We created an inventory-based model of anthropogenic CO2 emissions
from the San José urban area, parts of which are less than 15 km from
some of our sampling locations (Fig. 2). Our model shows that CO2
emitted from San José is blown west to southwest by prevailing winds. Our
study area is directly east of San José and as such is unaffected by
anthropogenic CO2 from San José, which is the only major urban
area near Turrialba and Irazú. Since the trees sampled are spatially
close to each other, they are exposed to the same regional background
CO2 variability. Additionally, we used ASTER data to map
probabilities of SO2 across Costa Rica as a possible confounding
factor. The active craters of both Turrialba and Irazú emit measurable
amounts of SO2, which is reflected by the high SO2
probabilities derived there (Fig. 2). Tropospheric SO2 quickly
converts to sulfate, a well-studied process intensified by the presence of
volcanic mineral ash, plume turbulence, and a humid tropical environment
(Oppenheimer et al., 1989; Eatough et al., 1994); furthermore, the bulk of
the SO2 emissions is carried aloft. Consequently, any remaining
SO2 causing acid damage effects on trees at Turrialba is limited to
a narrow band of a few 100 m around the mostly quietly steaming central
vent, which has been thoroughly ecologically evaluated for acid damage
(Jenkins et al., 2012). D'Arcy (2018) has assessed this narrow, heavily
SO2-affected area immediately surrounding the central crater vent
of Turrialba, which we avoided, and our sampling sites are mostly within
their control zone that is not considered majorly affected by SO2
but where diffuse CO2 degassing dominates the excess gas phase
(Epiard et al., 2017). Our study area is on the flanks of the volcano, where
ASTER-derived SO2 probability is minimal, and SO2
influence not detectable on the ground (Jenkins et al., 2012; Campion et al.,
2012). Most other volcanoes in Costa Rica emit little to no SO2 on
a decadal timescale, shown by the low or non-existent long-term SO2probabilities over the other volcanoes in Costa Rica (white shapes in
Fig. 2).
Bulk wood δ13C of trees on Costa Rica's Turrialba
volcano shows strong correlations with increasing volcanic CO2 flux
for two species, O. xalapensis and B. nitida, indicating
long-term photosynthetic incorporation of isotopically heavy volcanic
CO2. Stable carbon isotope ratio (δ13C) of wood cores
are plotted against soil CO2 flux measured immediately adjacent to
the tree that the core sample was taken from. Background and volcanic
influence labels apply to both axes – higher CO2 flux and heavier
(less negative) δ13C values are both characteristic of
volcanic CO2 emissions.
Tree core isotopes
Bulk wood δ13C measurements of all samples in this study,
independent of exposure, ranged from -24.03 ‰ to
-28.12 ‰, with most being clustered around -26 ‰
(Fig. 4). A five-bin histogram of all δ13C measurements shows
a slightly right-skewed unimodal normal distribution, with an average of
-26.37 ‰ and a standard deviation of 0.85 ‰. A. acuminata and O. xalapensis have nearly identical averages
(-26.14 ‰ and -25.97 ‰, respectively), while B. nitida has a noticeably lighter average of -27.02 ‰. Diffuse
excess CO2 emissions throughout the investigation areas reflect a
deep volcanic source which typically varies little in time (Epiard et al.,
2017), but such diffuse emissions spatially follow geological subsurface
structures (Giammanco et al., 1997). Their temporal variability therefore
reflects long-term low-amplitude modulation of the volcanic
heavy-δ13CO2 signal, and their spatial distribution is
mostly constant over tree lifetimes (Aiuppa et al., 2004; Peiffer et al.,
2018; Werner et al., 2014), providing a constant long-term spatial gradient
of CO2 exposure to the forest canopy. Our data show that in areas
where CO2 flux is higher, the wood cores contained progressively
higher amounts of 13C for two of the three species. Interestingly,
our tree core δ13C showed no relationship with instantaneous
stomatal conductance for any species, indicating that no stress threshold was
exceeded during measurement across the sample set.
Plant function (fluorescence, chlorophyll, stomatal
conductance)
Our measurements and literature data confirm that ecosystems growing in these
locations are consistently exposed to excess volcanic CO2, which
may impact chlorophyll fluorescence, chlorophyll concentrations, and stomatal
conductance of nearby trees. After excluding visibly damaged trees, leaf
fluorescence, expressed as Fv/Fm, was very high in most
samples. Fv/Fm ranged from 0.75 to 0.89, with most
measurements clustering between 0.8 and 0.85 (Fig. 5). The fluorescence data
have a left-skewed unimodal distribution. The leaf fluorescence
(Fv/Fm) values for A. acuminata had a strong
positive correlation with soil CO2 flux (r2=0.69, p<0.05), while the other two species showed no correlation. No confounding
factors measured were correlated with Fv/Fm for any
species. In general, B. nitida had the highest
Fv/Fm values, and A. acuminata and O. xalapensis had similar values except for a few O. xalapensis
outliers. Chlorophyll concentration measurements were highly variable,
ranging from 260 to 922 µmol m-2, with an average of
558 µmol m-2 and a standard deviation of
162 µmol m-2 (Fig. 6). Chlorophyll concentration had a
complicated right-skewed bimodal distribution, likely due to the noticeably
different averages for each species. A. acuminata and O. xalapensis both displayed weak correlations between chlorophyll
concentration and soil CO2 flux (r2=0.38 and r2=0.28,
respectively), but their trend lines were found to be almost perpendicular
(Fig. 6). As CO2 flux increased, A. acuminata showed a
slight increase in chlorophyll concentration, while O. xalapensis
had significant decreases in chlorophyll concentration. B. nitida
individuals growing on steeper slopes had significantly lower chlorophyll
concentration measurements (r2=0.42, p<0.05) than those on
gentler slopes, a trend not expressed by either of the other two species
(r2=0.01 for both), demonstrating no significant influence of slope
across the majority of samples. Stomatal conductance ranged from 83.5 to
361 mmol H2O m-2 s-1, with an average of 214 mmol
H2O m-2 s-1 and a standard deviation of 73.5 mmol
H2O m-2 s-1. Distribution was bimodal, with peaks
around 150 and 350 mmol H2O m-2 s-1. A. acuminata had a moderate positive correlation (r2=0.51) with soil
CO2 flux, but it was not statistically significant due to a lack of
data points (Fig. 7); however this is a result consistent with the observed
higher chlorophyll concentration (Fig. 6). The other two species displayed no
correlation with soil CO2 flux. B. nitida had a moderate
negative correlation (r2=0.61) with slope, similar to its correlation
between chlorophyll concentration and slope.
Photosynthetic activity of some tree species in old-growth forests
on the upper flanks of two active volcanoes in Costa Rica, Turrialba and
Irazú, may show short-term response to volcanically elevated CO2.
Leaf fluorescence (Fv/Fm) and soil CO2 flux
were strongly correlated for A. acuminata but not for other
species.
Some tree species in old-growth forests on the upper flanks of two
active volcanoes in Costa Rica, Turrialba and Irazú, may express their
short-term response to volcanically elevated CO2 by producing more
chlorophyll. A species that showed strong short-term response (A. Acuminata; Fig. 5) also shows a positive correlation between chlorophyll
concentration and mean soil CO2 flux.
Leaf stomatal conductance of a tree species that strongly responds
to volcanically elevated CO2 (Figs. 5, 6) has positive correlations
with volcanic CO2 flux, consistent with increased gas exchange.
DiscussionLong-term plant uptake in volcanic CO2
Turrialba and Irazú continuously emit CO2 through their
vegetated flanks, but prior to this study it was unknown if the trees growing
there were utilizing this additional isotopically heavy volcanic
CO2. All tree cores with corresponding CO2 flux
measurements were from areas proximal to the Ariete fault on Turrialba, where
atmospheric and volcanic δ13C have significantly different
values (-9.2 ‰ and -3.4 ‰, respectively; Malowany et al., 2017).
If the trees assimilate volcanic CO2 through their stomata, then we
would expect wood δ13C to trend towards heavier values as
diffuse volcanic CO2 flux increases. Studies at FACE sites have
found that altering the isotopic composition of the air by artificially
adding CO2 with a different carbon isotope composition than the
atmosphere leads to significant changes in the δ13C value of
plant matter and tree rings growing there, leading us to expect similar
effects from the naturally added volcanic CO2 (Körner, 2005).
It is worth noting that the FACE CO2
(δ13C is -29.7 ‰), is significantly depleted in
13C compared the atmosphere, whereas volcanic CO2 is
enriched (δ13C is -3.4 ‰ at Turrialba) compared
to atmosphere (Körner, 2005). After excluding damaged samples and
stressed trees, δ13C was strongly correlated with soil
CO2 flux for both B. nitida and O. xalapensis
(Fig. 4). A. acuminata did not have a statistically significant
correlation between soil CO2 flux and δ13C, likely
because it had the fewest data points and a minimal range of CO2
and δ13C values. The difference in regression slope between
B. nitida and O. xalapensis (Fig. 4) may be due to
physiological differences across traits or species, and/or due to differences
in exposure owing to canopy height differences. Resolving this question would
require a much larger multi-species sample size which could only be
sufficiently obtained using remote sensing methods. The strong positive
correlations between CO2 flux and increasingly heavy
δ13C values suggest that the trees have consistently
photosynthesized with isotopically heavy excess volcanic CO2 over
the last few years and are therefore growing in eCO2 conditions.
Assuming that most of the variations in δ13C are caused by
incorporation of heavy volcanic CO2, we can calculate the average
concentration of the mean volcanic excess CO2 in the air the plants
are exposed to with a mass balance equation (Eq. 2):
Cv=δb-δt(δa-δv)Ca,
where Cv is the mean volcanic excess component of the
CO2 concentration in air, Ca is the atmospheric
“background” (i.e., non-volcanic) CO2 concentration,
δa is atmospheric δ13C, δb
is the most negative δ13C measurement for the species being
studied, δt is the δ13C value for the tree
for which volcanic CO2 exposure is being calculated, and
δv is the δ13C value of the volcanic CO2.
Background wood δ13C is the value of the point for each
species with the lowest CO2 flux (Fig. 4), and the other wood
δ13C measurement is any other point from the same species.
Values for δv, δa, and Ca are
taken from Malowany et al. (2017). For the tree core with the highest measured
CO2 flux for O. xalapensis, this equation yields a mean
excess volcanic CO2 concentration of 115 ppm, bringing the
combined mean atmospheric (including volcanic) CO2 concentration
tree exposure to potentially around ∼520 ppm. For B. nitida
this equation yields 133 ppm of mean excess volcanic CO2 at the
highest flux location, for a combined total mean of potentially ∼538 ppm CO2. These numbers may be on the high side as the
calculation assumes that carbon isotope discrimination remains constant for
all trees within a given species, but they serve as an estimate of the
approximate magnitude of the average amount of CO2 that these trees
are exposed to. A 14C tree ring study at Mammoth Mountain found an
average yearly volcanic excess CO2 exposure of 20–70 ppm over a
15-year period (Lewicki et al., 2014). Turrialba is significantly more active
than Mammoth Mountain, so trees growing in high emission areas of Turrialba
may be exposed to similar or higher amounts of CO2 than the tree in
the Mammoth Mountain study. Additional measurements of tree core
δ13C and associated soil CO2 fluxes would help
corroborate our observations, which were based on a limited number of data
points. Though tree ring 14C content in volcanically active areas
has been linked to variations in volcanic CO2 emissions, and
comparing patterns of δ13C to 14C measurements for
the same wood samples could provide additional confirmation of this finding
(Evans et al., 2010; Lefevre et al., 2017; Lewicki et al., 2014), this
additional dimension was outside the scope of this exploratory study.
However, beyond such pattern confirmation, using 14C dating of
trees exposed to naturally isotopically distinct excess CO2 is, in
fact, unfortunately not a reliable method for these environments due to the
well-known δ14C deficiency in trees exposed to excess
volcanic CO2 which is isotopically “dead” with respect to
14C, creating spurious patterns that preclude dating by
14C (e.g., Lefevre et al., 2017; Lewicki et al., 2014).
Our data demonstrate that CO2 fluxes through the soil may be a
representative relative measure for eCO2 exposure of overlying tree
canopies. Forest canopy exposure to volcanic CO2 will vary over
time, as will volcanic eCO2; once emitted through the soil into the
sub-canopy atmosphere, the gas experiences highly variable thermal and wind
disturbances which significantly affect dispersion of CO2 on minute-to-minute, diurnal, and seasonal timescales (Staebler and Fitzjarrald, 2004;
Thomas, 2011). These processes cause in-canopy measurements of CO2
concentration to be highly variable, making instantaneous concentration
measurements in a single field campaign not representative of long-term
relative magnitudes of CO2 exposure. Soil CO2 fluxes are
less tied to atmospheric conditions and are primarily externally modulated
by rainfall which increases soil moisture and therefore lowers the soil's gas
permeability (Camarda et al., 2006; Viveiros et al., 2009). These fluxes can
also be affected by variations in barometric pressure, but both of these
factors are easily measurable and therefore can be factored in when
conducting field work (Viveiros et al., 2009). Assuming the avoidance of
significant rainfall and pressure spikes during sampling (measurements were
conducted in the dry season and no heavy rains or significant meteorological
variations in pressure occurred during field work), measuring the input of
CO2 into the sub-canopy atmosphere as soil CO2 fluxes is
therefore expected to better represent long-term input and exposure of tree
canopies to eCO2 than direct instantaneous measurements of
sub-canopy CO2 concentration. Previous studies at Turrialba have
shown that local volcanic CO2 flux is relatively constant on
monthly to yearly timescales (de Moor et al., 2016). Therefore, current soil
CO2 fluxes should give relatively accurate estimates of
CO2 exposure over time. This paper corroborates that expectation by
demonstrating strong spatial correlations between volcanically enhanced soil
CO2 emissions with co-located stable carbon isotope signals of
these emissions documented in the trees' xylem.
A study at the previously mentioned Mammoth Mountain tree kill area examined
the connection between δ13C and volcanic CO2 fluxes
but focused on the difference between trees killed by extreme CO2
conditions and those that were still alive (Biondi and Fessenden, 1999). They
concluded that the changes in δ13C that they observed were due
to extreme concentrations of CO2 (soil CO2 concentrations
of up to 100 %) impairing the functioning of root systems, leading to
closure of stomata and water stress (Biondi and Fessenden, 1999).
CO2 does not inherently harm trees, but the extreme CO2
concentrations (up to 100 % soil CO2) at the Mammoth Mountain
area caused major soil acidification, which led to the tree kill (McGee and
Gerlach, 1998). We have evidence that those acidification processes are not
affecting our δ13C measurements and that variations in our
δ13C measurements are more likely to be caused by the direct
photosynthetic incorporation of isotopically heavy volcanic CO2.
Our δ13C measurements have no statistically significant
correlation with stomatal conductance, which suggests that our heavier
δ13C measurements are not linked to stomatal closure. None of
the trees included in the analysis displayed obvious signs of stress, from
water or other factors, as indicated by their high fluorescence and
chlorophyll concentration values and the lack of visible indicators of
stress; specifically, our values of Fv/Fm∼0.8
indicate that the PSII was operating efficiently in most of the trees we
measured (Baker and Oxborough, 2004). The Mammoth Mountain tree kill areas
have higher CO2 fluxes by several orders of magnitude (well over
10 000 g m-2 d-1) than the areas we sampled (up to
38 g m-2 d-1), making it much more likely that stress from soil
acidification causes stomatal closure and affects wood δ13C
measurements at Mammoth Mountain (Biondi and Fessenden, 1999; McGee and
Gerlach, 1998; Werner et al., 2014). In contrast, most of the diffuse
degassing at Turrialba does not lead to soil acidification or pore space
saturation, as is evident in our own and others' field data (e.g., Epiard et
al., 2017). Thus, changes in our δ13C values are best
explained by direct photosynthetic incorporation of isotopically heavy
volcanic CO2. To the best of our knowledge, this is the first time
that a direct correlation between volcanic soil CO2 flux and wood
δ13C has been documented. Future studies should explore this
correlation further, as our findings are based on a limited sample size.
Short-term species response to eCO2
Short-term plant functional responses at the leaf level to elevated
CO2 were highly species-dependent. B. nitida had no
statistically significant functional responses to soil CO2 flux, and
O. xalapensis only had a weak negative correlation between soil
CO2 flux and chlorophyll concentration (Fig. 6). A. acuminata, a nitrogen-fixing species, was the only species with a consistent
and positive functional response to elevated CO2, displaying a
strong positive correlation with fluorescence and a weak positive correlation
with chlorophyll concentration and stomatal conductance (Figs. 5–7).
Previous studies which linked changes in the NDVI to pre-eruptive volcanic
activity on the flanks of Mt. Etna and Mt. Nyiragongo support our observation
of a correlation between plant function and volcanic CO2 flux
(Houlié et al., 2006; Seiler et al., 2017). This link raises the question
of why only one of three species displayed strong functional responses to
volcanic CO2. The lack of response in B. nitida and
O. xalapensis could be due to nitrogen limitation, a factor that
would not affect A. acuminata due to its nitrogen-fixing capability.
Previous studies have found that nitrogen availability strongly controls
plant responses to both naturally and artificially elevated CO2
concentrations in a variety of ecosystems, including grasslands and temperate
forests (Garten et al., 2011; Hebeisen et al., 1997; Lüscher et al.,
2000; Norby et al., 2010; Tognetti et al., 2000). Nitrogen limitation has
been posited to be an important factor in tropical montane cloud forests and
may be contributing to the lack of responses in B. nitida and
O. xalapensis (Tanner et al., 1998). Due to the exploratory nature
of our study, we do not have a large enough dataset to conclude that the
nitrogen-fixing capability of species like A. acuminata is the cause
for its positive response to volcanically elevated CO2
concentrations, as has been speculated before (Schwandner et al., 2004), but
it is a possible correlation that deserves further investigation.
Time constraints
To support these results, we further assessed the possibility of effects of
time constraints on growth rates and isotopic signals, despite the compelling
spatial variability in the independent variable (naturally isotopically
labeled excess volcanic CO2) in our study (Helle and Schleser,
2004; Verheyden et al., 2004). As tropical trees typically lack tree rings,
it is difficult to directly constrain the precise time period that the data
represent. However, since we sampled from the outside in, all the samples
appear to at least have the most recent growth period in common. To assess
how far back in time our samples could likely represent, we compared our
sampled core depths to reported growth rates for the same species in similar
environments. Reported growth rates for two of our species, O. xalapensis and A. acuminata, range from 0.25 to 2.5 and
0.6 to 0.9 cm yr-1, respectively (Kappelle et al., 1996; Ortega-Pieck et
al., 2011). Given that our samples are bulk measurements of the outer 5 cm
of wood, each sample would represent between 2 and 5.5 years, although the
conditions that these growth rates were measured in were different than in
our study. Clear time constraints would be necessary for higher resolution
analysis, but this need is somewhat mitigated by the continuous, long-term,
and, over multiple decades, mostly invariant nature of diffuse volcanic
CO2 emissions, which is completely independent of any non-volcanic
environmental influences on growth rates. By providing an upper and lower
bound in the expected growth span represented in our samples, we believe that
these samples represent similar time frames during the continuous exposure to
excess volcanic CO2 over the lifetimes of the trees sampled. Due to
the continuous nature of the volcanic CO2 enhancement, we are not
investigating and analyzing transient events, and our results instead
represent spatial variability in excess CO2 availability averaged
over similar time periods.
Although we do not believe that our samples represent a long enough time
period for long-term variations in δ13C (Suess
effect) to be relevant, if it does affect our
samples, it would be beneficial for detection of volcanic CO2, as
the Suess effect is gradually increasing the gap between atmospheric and
volcanic δ13C. Since our δ13C values likely
represent several years of growth, small-scale temporal variations in excess
volcanic CO2 release are unlikely to significantly impact the
results. Larger trees tend to grow slower than smaller trees, so the outer
5 cm of wood should represent a longer time period in larger trees. Thus, if
temporal variations had a significant effect on our δ13C
measurements, we would expect this to be represented by some correlation
between DBH and δ13C, which is not present for any species
studied. Three of the five B. nitida individuals measured were very
large (150–190 cm DBH), whereas the other two are much smaller (11.5 and
15.3 cm DBH). Although the age and growth rates of these two groups of trees
likely vary significantly, we found no correlation between DBH and
δ13C, though we did find a strong correlation between the
completely independent diffuse excess (volcanic) CO2 flux and wood
δ13C. Furthermore, the relationships presented are on a per
species basis to avoid complications resulting from different growth rates
across species. This is important because δ13C values provide
an integral value of assimilated carbon by the entire tree (not just
individual leaves). The depth of tree core sample was identical for each
species (the outermost part of the trunk), and we can safely assume that the
volcanic CO2 exposure has been consistent over the time period
under investigation.
Because individual time variability of growth rates can possibly affect these
signals as well, future studies that attempt to study tree ring isotopes in
this context at higher resolutions will likely require stricter and more
detailed time constraints and cell-level stress analysis to average out the
effects of long-term variations in δ13C (Suess effect),
seasonal cycles, potential short-term transient stress-induced growth rate
variations, effects of water use efficiency (WUE), and potential short-term
variations in CO2 flux, all of which may result in time-averaged
isotopic shifts over different growth periods (Helle and Schleser, 2004;
Verheyden et al., 2004). We include these notes as guidance in Sect. 4.4:
Lessons learned for future studies. Despite the additional difficulty of
conducting higher time resolution analysis, this type of study holds great
potential for attempting to reconstruct volcanic CO2 histories and
to study its potential fertilization effect, due to the completely
independent nature of the volcanic excess CO2 supply to the
sub-canopy air.
Lessons learned for future studies
This exploratory study reveals significant new potential for future studies
to utilize the volcanically enhanced CO2 emissions approach to
study tropical ecosystem responses to eCO2 – one of the largest
uncertainties in climate projections. Costa Rica's volcanoes are host to
large areas of relatively undisturbed rainforest, making them ideal study
areas for examining responses of ecosystems to eCO2. However, there
are several challenges that future studies should take into consideration if
attempting to expand upon this preliminary study. Given the enormous tropical
species diversity and the need to control for confounding factors, large
datasets will be needed to answer these questions conclusively. One open
question, for example, is how WUE in upper and lower canopy leaves of the same and
different individuals within a species may affect isotopic sequestration of
CO2. Since the excess volcanic CO2 is naturally
isotopically labeled, this could be assessed by a much more detailed
(by individual tree leaf, branch, and xylem) core study coupled with long-term
measurements of evapotranspiration, heat stress, and stomatal conductance,
the last of which in our study showed no significant correlation with the
δ13C signal in the wood cores across spatial gradients. Field
data can be difficult to acquire in these rugged and challenging
environments. A remote sensing approach using airborne measurements,
validated by targeted representative ground campaigns, could provide
sufficiently large datasets to represent species diversity and conditions
appropriately. Many of the data types that would be useful for this type of
study can be acquired from airborne platforms, and remote sensing instruments
can quickly produce the massive datasets required to provide more
comprehensive answers to these questions. A recent meta-analysis showed that
studies at natural CO2-producing springs and FACE experiments have
found similar results in a variety of plant traits, which significantly
strengthens the case that volcanoes are a potentially extremely valuable
resource for determining plant responses to elevated CO2
concentrations (Saban et al., 2019). While the spring studies have yielded
valuable results, volcanoes could offer several advantages over springs for
future studies. Active volcanoes are significantly larger systems than
non-volcanic springs and often feature several CO2-producing
springs and also several dry gas seeps; this offers more data, more control
points for comparison, greater species diversity, and greater potential for
comprehensive measurements of a statistically meaningful dataset from remote
sensing platforms. Due to their volcanic hazard potential, volcanoes are
also more likely to already have long-term volcanological monitoring programs
for CO2 fluxes and ecological disturbances, which may be utilized
to analyze the long-term effects of enhanced levels of CO2
emissions on these volcanically active tropical ecosystems.
Our results also offer significant new tools for the volcanology, where
reconstructing past volcano behavior through eruption histories is hampered
by severe preservation gaps in the stratigraphic record. A strong link
between δ13C and volcanic CO2 could be a
game changer by establishing long-term histories of volcanic CO2
emission variations. These proxy signals could be traced back in time using
living and preserved dead trees in order to fill gaps in the historical and
monitoring records – a boon for volcano researchers and observatories to
improve eruption prediction capabilities (Newhall et al., 2017; Pyle, 2017;
Sparks et al., 2012). While variations in tree ring 14C content
have been shown to correlate well with variations in volcanic CO2
flux (Evans et al., 2010; Lefevre et al., 2017; Lewicki and Hilley, 2014),
14C is relatively expensive to measure, limiting the spatial and
temporal coverage of data that can be acquired. 13C is an
inexpensive alternative to 14C and can be measured at more
laboratories, allowing for substantially more data to be acquired. Some
previously mentioned studies (Lefevre et al., 2017; Pasquier-Cardin et al.,
1999) have found correlations between 13C and 14C in
plants that have incorporated volcanic CO2, strengthening the
potential for using 13C in this type of study. Further development
of the 13C approach to tracking volcanic CO2 emissions
would prove beneficial to future studies attempting to use plants to study
large areas and timescales of volcanic degassing. Independent validation,
and calibration by wood core dendrochronology via 14C, tree rings,
or chemical event tracers like sulfur isotopes, could significantly advance
the concept of using wood carbon as an archive of past degassing activity.
Crucially, these tree ring archives could provide temporal records of
degassing at dangerous volcanoes which have previously been poorly monitored
or not monitored at all, significantly improving the accuracy of hazard
assessments. Furthermore, knowledge of the short-term real-time response of
leaves to diffusely emitted eCO2, which is more likely to represent
deeper processes inside volcanoes than crater-area degassing (Camarda et al.,
2012), may permit the use of trees as sensors of transient changes in
volcanic degassing indicative of volcanic reactivation and deep magma
movement possibly leading up to eruptions (Camarda et al., 2012; Houlié
et al., 2006; Pieri et al., 2016; Schwandner et al., 2017; Seiler et al.,
2017; Shinohara et al., 2008; Werner et al., 2013). To the best of our
knowledge, we are the first to propose utilizing the combination of
short-term leaf functional responses to volcanic CO2 with long-term
changes in δ13C values of wood for assessment of past and
present volcanic activity in a single study.
Conclusions
Multiple areas of dense tropical forest on two Costa Rican active volcanoes
are consistently and continuously exposed to volcanically elevated levels of
atmospheric CO2, diffusively cold emitted through soils into
overlying forests. These isotopically heavy volcanic CO2 emissions,
which are mostly invariant, not accompanied by acidic gases, and independent
of processes affecting growth rates, are well correlated with increases in
heavy carbon signatures in wood cores from two species of tropical trees,
possibly suggesting long-term incorporation of enhanced levels of
volcanically emitted CO2 into biomass. Each tree studied was
co-located with a soil CO2 flux measurement, and their soil
CO2 flux signals vary spatially around a continuous long-term local
natural excess volcanic CO2 source, which creates a local
CO2 gradient within which all the sampled trees are found. The
excess volcanic CO2 through local fault-bound gas seeps provides
continuous exposure to all sampled trees over timescales much greater than
the lifetimes of individual trees. Based on our limited exploratory
measurements, confounding factors that are known to influence
δ13C values in wood appear not to have significantly affected
our measurements, indicating that the heavier wood δ13C
values could be caused by photosynthetic incorporation of volcanic excess
CO2. One of the three species studied (A. acuminata) has
consistent positive correlations between instantaneous plant function
measurements and diffuse CO2 flux measurements, indicating that
short-term variations in elevated CO2 emissions may measurably
affect trees growing in areas of diffuse volcanic gas emissions. These
observations reveal significant potential for future studies to use these
areas of naturally elevated CO2 to study ecosystem responses to
elevated CO2 and to use trees as sensors of the changing degassing
behavior of volcanic flanks, which is indicative of deep magmatic processes.
Data availability
Data can be found in Tables S1 and S2 in the Supplement or
can be requested from Florian Schwandner (florian.schwandner@jpl.nasa.gov).
The supplement related to this article is available online at: https://doi.org/10.5194/bg-16-1343-2019-supplement.
Author contributions
FMS and JBF designed the study, and RRB, FMS, JBF, and ED conducted the
field work and collected all samples and data with some of the equipment
borrowed from GN, who helped interpret the results. TSM processed the samples
for analysis. JPL conducted the SO2 analysis, wrote the related
methods subsection, and helped interpret the results. VY modeled the
anthropogenic CO2 emissions, wrote the related methods subsection,
and helped interpret the results. CAF created the combined figure showing the
CO2 and SO2 results and assisted in writing the
paper. RRB wrote the publication, with contributions from all
co-authors.
Competing interests
The authors declare that they have no conflict of
interest.
Acknowledgements
We are grateful for LI-COR, Inc. (Lincoln, NE, USA) providing us a loaner
CO2 sensor for field work in Costa Rica. We thank
Rizalina Schwandner for engineering assistance during sensor integration,
OVSICORI (Observatorio Vulcanológico y Sismológico de Costa Rica –
the Costa Rican volcano monitoring authority) for logistical and permit
support, SINAC (Sistema Nacional de Áreas de Conservación – the
Costa Rican national parks service) for access to the Turrialba volcano, and
Marco Antonio Otárola Rojas (Universidad Nacional de Costa Rica –
ICOMVIS) for invaluable help in the field. We also thank three anonymous
reviewers, Akira Kagawa, and the handling editor for very helpful and
insightful suggestions that led us to improve the paper. Incidental funding
is acknowledged from the Sherman W. Hartman Memorial Fund at Occidental
College for funding Robert R. Bogue's field expenses as well as the Jet
Propulsion Laboratory's YIP (Year-Round Internship Program) and the Jet
Propulsion Laboratory Education Office for funding and support for
Robert R. Bogue. Florian M. Schwandner's UCLA contribution to this work was
supported by Jet Propulsion Laboratory subcontract 1570200. Part of the
research described in this paper was carried out at the Jet Propulsion
Laboratory at the California Institute of Technology under a contract with
the National Aeronautics and Space Administration.
Review statement
This paper was edited by David Gillikin and reviewed by
Akira Kagawa and three anonymous referees.
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