Biogeosciences, 16, 1343–1360, 2019 https://doi.org/10.5194/bg-16-1343-2019 © Author(s) 2019. This work is distributed under the Creative Commons Attribution 4.0 License.

Plant responses to volcanically elevated CO2 in two Costa Rican forests

Robert R. Bogue1,2,3, Florian M. Schwandner1,4, Joshua B. Fisher1, Ryan Pavlick1, Troy S. Magney1, Caroline A. Famiglietti1,5, Kerry Cawse-Nicholson1, Vineet Yadav1, Justin P. Linick1, Gretchen B. North6, and Eliecer Duarte7 1Jet Propulsion Laboratory, California Institute of Technology, 4800 Oak Grove Drive, Pasadena, CA 91109, USA 2Geology Department, Occidental College, 1600 Campus Road, Los Angeles, CA 90041, USA 3Department of Earth and Planetary Sciences, McGill University, 845 Sherbrooke Street, Montréal, QC H3A 0G4, Canada 4Joint Institute for Regional Earth System Science and Engineering, University of California Los Angeles, Los Angeles, CA 90095, USA 5Department of Earth System Science, Stanford University, 450 Serra Mall, Stanford, CA 94305, USA 6Biology Department, Occidental College, 1600 Campus Road, Los Angeles, CA 90041, USA 7Observatory of Volcanology and Seismology (OVSICORI), Universidad Nacional de Costa Rica, 2386-3000 Heredia, Costa Rica

Correspondence: Florian M. Schwandner (fl[email protected])

Received: 21 February 2018 – Discussion started: 5 March 2018 Revised: 17 February 2019 – Accepted: 21 February 2019 – Published: 1 April 2019

Abstract. We explore the use of active volcanoes to deter- 1 Introduction mine the short- and long-term effects of elevated CO2 on tropical trees. Active volcanoes continuously but variably Tropical forests represent about 40 % of terrestrial net pri- emit CO2 through diffuse emissions on their flanks, exposing mary productivity (NPP) worldwide, store 25 % of biomass the overlying ecosystems to elevated levels of atmospheric carbon, and may contain 50 % of all species on Earth, but the 2 2 CO2. We found tight correlations (r = 0.86 and r = 0.74) projected future responses of tropical plants to globally ris- between wood stable carbon isotopic composition and co- ing levels of CO2 are poorly understood (Leigh et al., 2004; located volcanogenic CO2 emissions for two of three investi- Townsend et al., 2011). The largest source of uncertainty gated species (Oreopanax xalapensis and Buddleja nitida), comes from a lack of understanding of long-term CO2 fertil- which documents the long-term photosynthetic incorpora- ization effects in the tropics (Cox et al., 2013). Reducing this tion of isotopically heavy volcanogenic carbon into wood uncertainty would significantly improve Earth system mod- biomass. Measurements of leaf fluorescence and chlorophyll els, advances which would help better constrain projections concentration suggest that volcanic CO2 also has measur- in future climate models (Cox et al., 2013; Friedlingstein et able short-term functional impacts on select species of trop- al., 2013). Ongoing debate surrounds the question of how ical trees. Our findings indicate significant potential for fu- much more atmospheric CO2 tropical ecosystems can ab- ture studies to utilize ecosystems located on active volcanoes sorb; this is known as the “CO2 fertilization effect” (Gregory as natural experiments to examine the ecological impacts of et al., 2009; Kauwe et al., 2016; Keeling, 1973; Schimel et elevated atmospheric CO2 in the tropics and elsewhere. Re- al., 2015). sults also point the way toward a possible future utilization Free Air CO2 Enrichment (FACE) experiments have been of ecosystems exposed to volcanically elevated CO2 to detect conducted to probe this question, but none have been con- changes in deep volcanic degassing by using selected species ducted in tropical ecosystems (e.g., Ainsworth and Long, of trees as sensors. 2005; Norby et al., 2016). Some studies have used CO2- emitting natural springs to study plant responses to ele-

Published by Copernicus Publications on behalf of the European Geosciences Union. 1344 R. R. Bogue et al.: Plant responses to volcanically elevated CO2 vated CO2, but these have been limited in scope due to time these gases reach the surface of most forested volca- the small spatial areas around springs that experience ele- noes, soluble and reactive volcanic gas species (e.g., SO2, vated CO2 (Hattenschwiler et al., 1997; Körner and Migli- HF, HCl, and H2S) have been scrubbed out in the deep sub- etta, 1994; Paoletti et al., 2007; Saurer et al., 2003). These surface, leading to a diffusely emanated gas mix of predom- studies have suffered from several confounding influences, inantly CO2 with minor amounts of hydrogen, helium, and including other gas species that accompany CO2 emissions at water vapor reaching the surface (Symonds et al., 2001). these springs, human disturbances, and difficulty with find- Trees in these locations are continuously exposed to some- ing appropriate control locations. Additionally, none have what variably elevated concentrations of CO2 (eCO2), al- been conducted in the tropics (Pinkard et al., 2010). A se- though the specific effects of this eCO2 on the trees are not 14 13 ries of studies in Yellowstone National Park (USA) used its well understood. Volcanic CO2 has no C and a δ C sig- widespread volcanic hydrothermal CO2 emissions for the nature typically ranging from around −7 ‰ to −1 ‰, which same purpose, though it is not in the tropics (Sharma and is distinct from typical vegetation and noticeably enriched in Williams, 2009; Tercek et al., 2008). Yellowstone was par- 13C compared to typical atmospheric values (Mason et al., ticularly suitable for this type of study due to its protected 2017). If trees incorporate volcanic CO2, then the stable car- status as a national park and because the large areas of CO2 bon isotopic composition of wood may document the long- emissions made control points more available (Sharma and term, possibly variable influence of volcanic CO2 during the Williams, 2009; Tercek et al., 2008). These studies reported tree’s growth. With this tracer available, volcanic ecosystems changes in rubisco, an enzyme central to CO2 fixation, and could become a valuable natural laboratory for studying the sugar production in leaves, similar to results from FACE ex- long-term effects of elevated CO2 on ecosystems, especially periments, suggesting that volcanically influenced areas like in understudied regions like the tropics. Several studies have Yellowstone have untapped potential for studying the long- found correlations between variations in volcanic CO2 flux 14 term effects of elevated CO2 on plants. and plant C records at Mammoth Mountain, Yellowstone, Tropical ecosystems on the vegetated flanks of active vol- and Naples, which agreed well with previous observations at canoes offer large and diverse ecosystems that could make these well-studied sites (Cook et al., 2001; Evans et al., 2010; this type of study viable. Well over 200 active volcanoes are Lefevre et al., 2017; Lewicki et al., 2014). The Mammoth in the tropics (Global Volcanism Program, 2013), and many Mountain and Yellowstone studies linked seismic swarms 14 of these volcanoes are heavily forested. However, fewer of and accompanying increases in CO2 flux to decreases in C these tropical volcanic forests have sufficient legal protec- content in tree rings in one or two trees, demonstrating the tion for being a source of long-term information, and the ef- method’s utility for uncovering yearly scale variations in vol- fects of diffuse volcanic flank gas emissions on the overlying canic CO2 fluxes (Cook et al., 2001; Evans et al., 2010; ecosystems remain largely unknown. Most previous studies Lewicki et al., 2014). The Naples study instead focused on focused on extreme conditions, such as tree kill areas as- using 14C in grasses as short-term (2 to 6 months) monitors sociated with extraordinarily high CO2 emissions at Mam- of volcanic CO2 flux, which is useful for volcanic monitor- moth Mountain, CA (USA; Biondi and Fessenden, 1999; ing due to the time-integrated signal they provide (Lefevre et Farrar et al., 1995; Sorey et al., 1998). However, the non- al., 2017). A study of plants growing at Furnas volcano found 2 14 lethal effects of cold volcanic CO2 emissions – away from very strong (r >0.85) correlations between depletions in C 13 the peak emission zones, but still in the theorized fertil- and enrichments in C from volcanic CO2 in three species of ization window – have received little attention and could plants, although this study also had a relatively limited (five offer a new approach for studying the effects of elevated samples per species) dataset (Pasquier-Cardin et al., 1999). CO2 on ecosystems (Cawse-Nicholson et al., 2018; Vodnik The previously mentioned Naples study also found some cor- et al., 2018). The broad flanks of active volcanoes experi- relation between 13C and 14C, although it was not as strong as ence diffuse emissions of excess CO2 because the under- the study in Furnas (Lefevre et al., 2017; Pasquier-Cardin et lying active magma bodies continuously release gas, dom- al., 1999). Additionally, short-term effects of eCO2 might be inated by CO2 transported to the surface along fault lines revealed by plant functional measurements at the leaf scale, (Chiodini et al., 1998; Dietrich et al., 2016; Farrar et al., where the additional CO2 could increase carbon uptake in 1995). This process has frequently been studied to under- photosynthesis. A series of studies at Mt. Etna in Italy and stand the dynamics of active magma chambers and to assess Mt. Nyiragongo in the Democratic Republic of the Congo potential volcanic hazards (Chiodini et al., 1998; Sorey et found linear anomalies in the NDVI (normalized difference al., 1998). These emissions are released through faults and vegetation index), a measure of vegetation greenness (Houlié fractures on the flanks of the volcano (Burton et al., 2013; et al., 2006). One to two years after the appearance of the Pérez et al., 2011; Williams-Jones et al., 2000; see Supple- NDVI anomalies, flank eruptions occurred directly along the ment Fig. S1). Volcanic flanks through which these gases line of the anomaly, indicating a plant response to the vol- 2 emanate are broad, typically covering 50–200 km , and often cano’s pre-eruptive state which may be due to increased CO2 support well-developed, healthy ecosystems. Some of these emissions in the buildup to the eruption (Houlié et al., 2006). faults tap into shallow acid hydrothermal aquifers, but by the A follow-up study found that the trees on Mt. Etna were rel-

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1345 atively insensitive to changes in temperature and water avail- sion is partially occupied by extensive dairy farms and is ability, strengthening the case that volcanic influence was in- somewhat less forested than their flanks. deed responsible for the NDVI anomaly (Seiler et al., 2017). In this study, we focused on accessible areas between 2000 Here we provide preliminary results on the short- and and 3300 m on both volcanoes (Fig. 1). On Irazú, we sam- long-term non-lethal impacts of diffuse volcanic CO2 emis- pled trees and CO2 fluxes from the summit area to the north, sions on three species of tropical trees on the flanks of two near the approximately north–south striking Rio Sucio fault, active volcanoes in Costa Rica. We also explore the viabil- crossing into the area dominated by dairy farms on Irazú’s ity in studying volcanically influenced ecosystems to better lower northeastern slope. Of significant importance for this understand potential future responses to elevated CO2 and type of study is that all active volcanoes on Earth continu- suggest adjustments to our approach that will benefit future, ously emit CO2 diffusely through fractures and diffuse de- similarly motivated studies. gassing 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 cen- 2 Methods turies (Burton et al., 2013; Delmelle and Stix, 2000; Nichol- son, 2017). There is no inherent seasonal or meteorologi- 2.1 Investigated locations and sampling strategy cal variability in the source gas pressure, and there is no dependence on shallow soil or vegetation chemistry or bi- Irazú and Turrialba are two active volcanoes located ∼ 25 ology (though increased soil moisture in the rainy season, and 35 km east of San José, Costa Rica (Fig. 1). These two wind, and atmospheric pressure can modulate gas permeabil- volcanoes are divided by a large erosional basin. The forested ity of the shallow soil; Camarda et al., 2006). The soil overly- portions of the two volcanoes cover approximately 315 km2. ing deep-reaching fracture systems acts as a diffuser through The vast majority of the northern flanks of Irazú and Turri- which the volcanic gas percolates and enters the sub-canopy alba are covered in legally protected dense old-growth for- air. For our study sites, portions of the volcanoes with ac- est, while the southern flanks are dominated by pastureland tive “cold” CO2 degassing have already been assessed and and agriculture. Turrialba rises 3300 m above its base and has mapped previously (Epiard et al., 2017; Malowany et al., been active for at least 75 000 years, with mostly fumarolic 2017). activity since its last major eruption in 1866 (Alvarado et Our sampling locations on Irazú were located along a road al., 2006). It has experienced renewed activity beginning from the summit northward down into the low-lying area. On in 2010, and its current activity is primarily characterized Turrialba, we focused on an area of known strong emissions by a near-constant volcanic degassing plume, episodic minor but intact forests on the SW slope, uphill of the same ero- ash emissions, and fumarolic discharges at two of the summit sional depression but cross-cut by the major NE–SW trend- craters, as well as significant diffuse and fumarolic gas emis- ing active fracture system of the Falla Ariete. We sampled sions across its flanks, focused along fault systems (Martini three main areas of the Falla Ariete, each approximately per- et al., 2010). Turrialba’s CO2 emissions in areas proximal to pendicularly transecting the degassing fault along equal alti- the crater were calculated at 113 ± 46 tons d−1 (Epiard et al., tude, at the upper Ariete fault, the lower Ariete fault, and a 2017). The Falla Ariete (Ariete fault), a major regional fault, small basin directly east of the old Cerro Armado cinder cone runs northeast–southwest through the southern part of Turri- on Turrialba’s southwestern flank. We took a total of 51 tree alba’s central edifice and is one of the largest areas of diffuse samples (17 were excluded after stress screening) at irregular CO2 emissions on Turrialba (Epiard et al., 2017; Rizzo et intervals depending on the continued availability and speci- 13 al., 2016). Atmospheric CO2 has an average δ C value of men maturity of three species present throughout the tran- −9.2 ‰ at Turrialba, and the volcanic CO2 released at the sect. 13 Ariete fault has significantly heavier δ C values clustered All transects are in areas experiencing measurable CO2 around −3.4 ‰ (Malowany et al., 2017). enhancements from the Falla Ariete but that are not high Irazú has been active for at least 3000 years and had minor enough in altitude to be in areas generally downwind of the phreatomagmatic eruptions in 1963 and a single hydrother- prevailing crater emissions plume (Epiard et al., 2017). We mal eruption in 1994. Currently, Irazú’s activity primarily avoided areas that experience ash fall, high volcanic SO2 consists of shallow seismic swarms, fumarolic crater gas concentrations, and local anthropogenic CO2 from farms or emissions, small volcanic landslides, and minor gas emis- that were likely to have heavily acidified soil. Excessively sions on its northern forested flank (Alvarado et al., 2006; high soil CO2 concentrations can acidify soil, leading to Barquero et al., 1995). Diffuse cold flank emissions of vol- negative impacts on ecosystems growing there (McGee and canic CO2 represent the vast majority of gas discharge from Gerlach, 1998). Because such effects reflect by-products of −1 Irazú, as the main crater releases 3.8 t d of CO2 and a small extreme soil CO2 concentrations rather than direct conse- −1 area on the north flank alone releases 15 t d (Epiard et al., quences of elevated CO2 on plants, we avoided areas with 2017). Between the two volcanoes, a major erosional depres- CO2 fluxes high enough to possibly cause noticeable CO2- www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1346 R. R. Bogue et al.: Plant responses to volcanically elevated CO2

Figure 1. 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). induced soil acidification. Light ash fall on some days likely can survive in primary forests as well (Kappelle et al., 1996; derived from atmospheric drift, as we were not sampling in Quintana-Ascencio et al., 2004). It had the smallest average areas downwind of the crater. The ash fall did not, in any DBH of the three species, ranging from 6.6 to 40.9 cm, with noticeably way, affect our samples, as trees showing ash ac- an average of 22.71 cm. cumulation on their leaves or previous damage were the ex- ception and avoided. Altitude, the amount of sunlight dur- 2.3 CO2 concentrations and soil diffuse flux ing measurements, and aspect had no consistent correlations measurements with any of the parameters we measured.

Soil CO2 flux was measured with an accumulation chamber 2.2 Studied tree species near the base of the tree (generally within 5 m, terrain per- mitting) at three different points and then averaged to pro- 13 Our study focused on three tree species found commonly vide a single CO2 flux value to compare to the C mea- on Turrialba and Irazú: Buddleja nitida, Alnus acuminata, surement of the corresponding tree sample. This technique and Oreopanax xalapensis. B. nitida is a small tree with a is intended to provide a simple relative way to compare the typical stem diameter (DBH) ranging from 5 to 40 cm that CO2 exposure of different trees, as a tree with high CO2 flux grows at elevations of 2000–4000 m throughout most of Cen- near its base should experience consistently higher CO2 con- tral America (Kappelle et al., 1996; Norman, 2000). The centrations than a tree with lower CO2 flux. We also mea- DBH of the individuals we measured ranged from 11.5 to sured concentrations at ground level and 1.5–2.0 m above 51.3 cm, with an average of 29.85 cm. It averages 4–15 m ground level, though these were expectedly highly variable in height and grows primarily in early and late secondary in time and location. We analyzed CO2 fluxes, not concentra- forests (Kappelle et al., 1996; Norman, 2000). A. acuminata tions, because the diffuse emissions of excess volcanic CO2 is a nitrogen-fixing pioneer species exotic to the tropics that through the soil, fed from a deep magma source and depen- can survive at elevations from 1500 to 3400 m, although it dent on the location of constant deep geological permeabil- is most commonly found between 2000 and 2800 m (Weng ity, are highly invariant in time compared to under-canopy et al., 2004). The trees we measured had DBH ranging from air concentrations. In contrast, instantaneous concentration 14.3 to 112 cm, with an average of 57.14 cm. O. xalapen- measurements in the sub-canopy air are modulated by many sis thrives in early and late successional forests, although it factors, including meteorology, respiration of vegetation and

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1347 animals, uptake by plants for photosynthesis, and diurnal dy- and, indirectly, plant stress (Baker and Oxborough, 2004). namic and slope effects. An approach of instantaneous highly The five Fv/Fm measurements were averaged to provide a variable concentration measurements is thus not representa- representative value for each individual tree. Some trees had tive of long-term exposure. The approach of measuring the less than five measurements due to the dark adaptation clips largely invariant soil-to-atmosphere volcanic CO2 fluxes is slipping off the leaf before measurements could be taken. Ten much more representative of long-term exposure, varying trees had four measurements, and another six had three mea- mostly spatially, and the site-to-site differences are therefore surements. more representative of the lifetime of exposure of the trees. The chlorophyll concentration index (CCI) was measured We used a custom-built soil flux chamber system which with a MC-100 Apogee Instruments chlorophyll concentra- contained a LI-COR 840A non-dispersive infrared CO2 sen- tion meter (Apogee Instruments, Inc., Logan, UT, USA). The −2 sor (LI-COR Inc., Lincoln, NE, USA) to measure soil CO2 CCI was converted to chlorophyll concentration (µmol m ) flux. A custom-built cylindrical accumulation chamber of de- with the generic formula derived by Parry et al. (2014). De- fined volume was sealed to the ground and remained con- pending on availability, between three and six leaves were nected to the LI-COR sensor. The air within the accumulation measured for the CCI for each tree and then averaged to pro- chamber was continuously recirculated through the sensor, vide a single value for each tree. If leaves were not within passing through a particle filter. The sensor was calibrated reach, a branch was pulled down or individual leaves were before deployment and performed within specifications. We shot down with a slingshot and collected. Photosyntheti- recorded cell pressure and temperature; ambient pressure; air cally active radiation was measured at each tree with a hand- temperature; GPS location; timestamps; location description; held quantum meter (Apogee Instruments, Inc., Logan, UT, wind speed and direction; relative humidity; and slope, as- USA; Supplement Table S2). Stomatal conductance to wa- −2 −1 pect, and altitude as ancillary data. In typical operation, each ter vapor, gs (mmol m s ), was measured between 10:00– measurement site for flux measurements was validated for 14:00 h using a steady-state porometer (SC-1, Decagon De- leaks (visible in the live data stream display as spikes and vices, Inc., Pullman, WA, USA), calibrated before use and breaks in the CO2 concentration slope), and potential exter- read in manual mode. This leaf porometer was rated for hu- nal disturbances were avoided (such as vehicle traffic, gen- midity < 90 %, and humidity was sometimes above this limit erators, or breathing animals and humans). Measurements during our field work. Consequently, we have fewer stomatal were recorded in triplicate for at least 2 min per site. Data conductance measurements than our other data types. reduction was performed using recorded timestamps in the dataset, with conservative time margins to account for sen- 2.5 Isotopic analysis sor response dead time, validated against consistent slope sections of increasing chamber CO2. Fluxes were computed We collected wood cores from 31 individual trees at a 1.5 m using ancillary pressure and temperature measurements and height using a 5.15 mm diameter increment borer (JIM- the geometric chamber constant (chamber volume at inserted GEM, Forestry Suppliers Inc., Jackson, MS, USA). Since no depth, tubing volume, and sensor volume). Care was taken to definable tree rings were apparent, we created a fine powder not disturb the soil and overlying litter inside and adjacent to for isotope analysis by drilling holes into dried cores using the chamber. a dry ceramic drill bit (Dremel) along the outermost 5 cm of wood below the bark, which was chosen to represent the 2.4 Leaf function measurements most recent carbon signal for 13C analyses. The fine powder (200 mesh, 0.2–5 mg) was then mixed, and a random sam- Chlorophyll fluorescence measurements were conducted on ple was used to extract 13C/12C ratios (to obtain δ13C values leaves of all three species during the field campaign to obtain against the VPDB standard), which we estimated to be rep- information on instantaneous plant stress using an OS30p+ resentative of at least the last 2–3 years, based on analogous fluorometer (Opti-Sciences Inc., Hudson, NH, USA). Five literature growth rate values: O. xalapensis and A. acuminata mature leaves from each individual tree were adapted to the range from 0.25 to 2.5 and from 0.6 to 0.9 cm yr−1, respec- dark for at least 20 min to ensure complete relaxation of the tively (Kappelle et al., 1996; Ortega-Pieck et al, 2011). These photosystems. After dark adaptation, initial minimal fluores- rates result in a 5 cm range of at least 2 and 5.5 years, though cence was recorded (Fo) under conditions where we assume the high rates were determined for very young trees under that the photosystem II (PSII) was fully reduced. Immedi- very different conditions, and this is explicitly unknown in −2 −1 ately following the Fo measurement, a 6000 µmol m s our study. Since we only sample the most recent years, no saturation pulse was delivered from an array of red LEDs isotopic discrimination against atmospheric 13C due to pref- 12 at 660 nm to record maximal fluorescence emission (Fm) erential diffusion and carboxylation of C was conducted. when the reaction centers are assumed to be fully closed. Rather, we assume that δ13C values are representative of the From this, the variable fluorescence was determined to be relative amount of volcanic CO2 vs. atmospheric CO2 se- Fv/Fm = (Fm−Fo)/Fm. Fv/Fm is a widely used chlorophyll questered by the tree over the period of growth represented in fluorescence variable used to assess the efficiency of the PSII the sample. δ13C values were determined by continuous-flow www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1348 R. R. Bogue et al.: Plant responses to volcanically elevated CO2 dual-isotope analysis using a CHNOS Elemental Analyzer to be between 200 and 800 observations in total, over the 17- and IsoPrime 100 mass spectrometer at the University of Cal- year time period of satellite observations. However, certain ifornia Berkeley Center for Stable Isotope Biogeochemistry. permanent features, such as salt pans, show absorption fea- External precision for C isotope determinations is ±0.10 ‰. tures in band 11 and therefore have high ratios for the algo- 13 Ten δ C measurements did not have corresponding soil CO2 rithm used. We therefore used a second method that seeks to flux measurements due to the flux measurements being un- map transient absorption features. For this method, we sub- available for the final 2 days of sampling, and another five tract the median from each St , yielding a median deviation samples were from trees that showed signs of extreme stress, stack. By plotting the maximum deviations across all obser- such as browning leaves or anomalously low fluorescence vations, we then get a map of transient absorption features; in measurements. Since the purpose of our study was to explore our case, these are mostly volcanic SO2 plumes, which map the non-lethal effects of volcanic CO2 on trees, during anal- out the cumulative position of different plume observations ysis we excluded all trees that were observed in the field as well. To speed up processing, some of the retrieval runs were showing visible signs of stress or being not fully mature. Af- binned in order to increase the signal-to-noise ratio, since the ter these exclusions, all remaining tree cores with co-located band difference can be rather noisy. CO2 flux measurements were from Turrialba. 2.7 Modeling the anthropogenic CO2 influence from 2.6 Sulfur dioxide probability from satellite data inventory data

To assess the likelihood of trees having been significantly We assessed the likelihood of anthropogenic CO2, enhance- stressed in the past by volcanic sulfur dioxide (SO2) from ments of air from San José, Costa Rica’s capital and main the central crater vents, we took two approaches. First, we industrial and population center, influencing our measure- were guided by in situ measurements taken in the same ar- ments. We used a widely applied FLEXible PARTicle dis- eas by Jenkins et al. (2012), who assessed the physiologi- persion model (Eckhardt et al., 2017; Stohl et al., 1998, cal interactions of SO2 and CO2 on vegetation on the up- 2005; Stohl and Thomson, 1999) in a forward mode (Stohl per slopes of Turrialba and demonstrated a rapid exponen- et al., 2005), FLEXPART, to simulate the downwind con- tial decay of SO2 away from the central vent. Second, for centrations of CO2 in the atmosphere (e.g., Belikov et al., long-term exposure we derived the likelihood of exposure 2016), due to inventory-derived fossil fuel (FF) emissions in per unit area using satellite data sensitive to SO2 (Fig. 2). our study area for the year 2015 (Fig. 2). The National Cen- The Advanced Spaceborne Thermal Emission and Reflec- ters for Environmental Prediction (NCEP) – Climate Fore- tion Radiometer (ASTER), launched in December 1999 on cast System Reanalysis (CFSR) – 2.5◦ horizontal resolution NASA’s Terra satellite, has bands sensitive to SO2 emission meteorology (Saha et al., 2010a, b) and 1 km Open-source in the thermal infrared (TIR), at ∼ 60 m × 60 m spatial reso- Data Inventory for Anthropogenic CO2 (ODIAC; Oda and lution. We initially used ASTER Surface Radiance TIR data Maksyutov, 2011) emissions for 2015 were used to drive the (AST_09T), using all ASTER observations of the target area FlEXPART model. The CO2 concentrations were generated over the entirety of the ASTER mission (October 2000 until at a 1 km spatial resolution within three vertical levels of the writing began in late 2017). The TIR bands were corrected atmosphere (0–100, 100–300, and 300–500 m) that are possi- for downwelling sky irradiance and converted into units of bly relevant to forest canopies in Costa Rica. However, to as- −2 −1 W m µm . For each observation, an absorption product is sess the magnitude of enhancements we only used CO2 con- calculated by subtracting SO2-insensitive from SO2-sensitive centrations observed within the lowest modeled level of the bands: atmosphere, from 0 to 100 m. Validation of the model with t direct observations was not required because we were only S = (b10 + b12) − 2 · b11, (1) interested in ensuring that anthropogenic CO2 dispersed up- slope from San José was not having a significant effect on where S is the SO2 index, t is an index representing the our study area; we were not aiming to capture intra-canopy time of acquisition, b10 is the radiance at band 10 (8.125– variability, typically present at tens to hundreds of parts per 8.475 µm), b11 is the radiance at band 11 (8.475–8.825 µm), million variable, which is not relevant to the better mixed, 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 gran- distal single-digit-or-less parts per million signal from San ules were then separated into day and night scenes, pro- José. The actual concentration of CO2 and any biogenic in- jected onto a common grid, and then thresholded to S > fluence in the modeled area was irrelevant because the spa- 0.1 W m−2 µm−1 and converted into a probability (Abrams tial distribution of anthropogenic CO2 was the only factor et al., 2015). The output is a spatial dataset that describes relevant for this test. 2015 was used as a representative year the probability of an ASTER observation showing an ab- for simulating the seasonal cycle of CO2 concentrations that sorption feature above a 0.1 W m−2 µm−1 threshold across would be present in any particular year. the entirety of the ASTER observations for day or night sep- arately. The number of scenes varies per target, but they tend

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1349

Figure 2. 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.

3 Results

3.1 Volcanic 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 his- togram of mean CO2 flux shows a bimodal right-skewed dis- tribution 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; Figure 3. Soil CO2 flux into the sub-canopy air of forests on the Cardellini et al., 2003; Sinclair, 1974). Turrialba–Irazú volcanic complex is pervasively and significantly We created an inventory-based model of anthropogenic influenced by a deep volcanic gas source. At least four different CO emissions from the San José urban area, parts of which 2 overlapping populations of soil CO2 flux were identified using a are less than 15 km from some of our sampling locations cumulative probability plot, where inflection points indicate popula- (Fig. 2). Our model shows that CO2 emitted from San José tion boundaries (Sinclair 1974). 69 % of sampling locations (45 to- is blown west to southwest by prevailing winds. Our study tal) are exposed to varying degrees of volcanically derived elevated area is directly east of San José and as such is unaffected CO2. Populations are color-coded based on the same color scale as by anthropogenic CO2 from San José, which is the only ma- Fig. 1. jor urban area near Turrialba and Irazú. Since the trees sam- pled are spatially close to each other, they are exposed to the same regional background CO2 variability. Additionally, we sulfate, a well-studied process intensified by the presence of used ASTER data to map probabilities of SO2 across Costa volcanic mineral ash, plume turbulence, and a humid tropi- Rica as a possible confounding factor. The active craters cal environment (Oppenheimer et al., 1989; Eatough et al., of both Turrialba and Irazú emit measurable amounts of 1994); furthermore, the bulk of the SO2 emissions is car- SO2, which is reflected by the high SO2 probabilities de- ried aloft. Consequently, any remaining SO2 causing acid rived there (Fig. 2). Tropospheric SO2 quickly converts to damage effects on trees at Turrialba is limited to a narrow www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1350 R. R. Bogue et al.: Plant responses to volcanically elevated CO2

cal averages (−26.14 ‰ and −25.97 ‰, respectively), while B. nitida has a noticeably lighter average of −27.02 ‰. Dif- fuse 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 spa- tially follow geological subsurface structures (Giammanco et al., 1997). Their temporal variability therefore reflects long-term low-amplitude modulation of the volcanic heavy- 13 δ CO2 signal, and their spatial distribution is mostly con- stant 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.

Figure 4. Bulk wood δ13C of trees on Costa Rica’s Turrialba vol- 3.3 Plant function (fluorescence, chlorophyll, stomatal cano shows strong correlations with increasing volcanic CO2 flux conductance) for two species, O. xalapensis and B. nitida, indicating long-term photosynthetic incorporation of isotopically heavy volcanic CO2. 13 Our measurements and literature data confirm that ecosys- Stable carbon isotope ratio (δ C) of wood cores are plotted against tems growing in these locations are consistently exposed to soil CO flux measured immediately adjacent to the tree that the 2 excess volcanic CO , which may impact chlorophyll fluo- core sample was taken from. Background and volcanic influence la- 2 rescence, chlorophyll concentrations, and stomatal conduc- bels apply to both axes – higher CO2 flux and heavier (less negative) 13 tance of nearby trees. After excluding visibly damaged trees, δ C values are both characteristic of volcanic CO2 emissions. leaf fluorescence, expressed as Fv/Fm, was very high in most samples. Fv/Fm ranged from 0.75 to 0.89, with most band of a few 100 m around the mostly quietly steaming measurements clustering between 0.8 and 0.85 (Fig. 5). The central vent, which has been thoroughly ecologically eval- fluorescence data have a left-skewed unimodal distribution. uated for acid damage (Jenkins et al., 2012). D’Arcy (2018) The leaf fluorescence (Fv/Fm) values for A. acuminata had 2 = has assessed this narrow, heavily SO2-affected area immedi- a strong positive correlation with soil CO2 flux (r 0.69, ately surrounding the central crater vent of Turrialba, which p<0.05), while the other two species showed no corre- we avoided, and our sampling sites are mostly within their lation. No confounding factors measured were correlated B. nitida control zone that is not considered majorly affected by SO2 with Fv/Fm for any species. In general, had the A. acuminata O. xalapensis but where diffuse CO2 degassing dominates the excess gas highest Fv/Fm values, and and phase (Epiard et al., 2017). Our study area is on the flanks of had similar values except for a few O. xalapensis outliers. the volcano, where ASTER-derived SO2 probability is min- Chlorophyll concentration measurements were highly vari- −2 imal, and SO2 influence not detectable on the ground (Jenk- able, ranging from 260 to 922 µmol m , with an average −2 −2 ins et al., 2012; Campion et al., 2012). Most other volcanoes of 558 µmol m and a standard deviation of 162 µmol m in Costa Rica emit little to no SO2 on a decadal timescale, (Fig. 6). Chlorophyll concentration had a complicated right- shown by the low or non-existent long-term SO2 probabilities skewed bimodal distribution, likely due to the noticeably over the other volcanoes in Costa Rica (white shapes in different averages for each species. A. acuminata and O. Fig. 2). xalapensis both displayed weak correlations between chloro- 2 2 phyll concentration and soil CO2 flux (r = 0.38 and r = 3.2 Tree core isotopes 0.28, respectively), but their trend lines were found to be almost perpendicular (Fig. 6). As CO2 flux increased, A. Bulk wood δ13C measurements of all samples in this acuminata showed a slight increase in chlorophyll concen- study, independent of exposure, ranged from −24.03 ‰ tration, while O. xalapensis had significant decreases in to −28.12 ‰, with most being clustered around −26 ‰ chlorophyll concentration. B. nitida individuals growing on (Fig. 4). A five-bin histogram of all δ13C measurements steeper slopes had significantly lower chlorophyll concentra- shows a slightly right-skewed unimodal normal distribution, tion measurements (r2 = 0.42, p<0.05) than those on gen- with an average of −26.37 ‰ and a standard deviation of tler slopes, a trend not expressed by either of the other two 0.85 ‰. A. acuminata and O. xalapensis have nearly identi- species (r2 = 0.01 for both), demonstrating no significant in-

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1351

Figure 5. Photosynthetic activity of some tree species in old-growth Figure 6. Some tree species in old-growth forests on the upper forests on the upper flanks of two active volcanoes in Costa Rica, flanks of two active volcanoes in Costa Rica, Turrialba and Irazú, Turrialba and Irazú, may show short-term response to volcanically may express their short-term response to volcanically elevated CO2 elevated CO2. Leaf fluorescence (Fv/Fm) and soil CO2 flux were by producing more chlorophyll. A species that showed strong short- strongly correlated for A. acuminata but not for other species. term response (A. Acuminata; Fig. 5) also shows a positive correla- tion between chlorophyll concentration and mean soil CO2 flux.

fluence of slope across the majority of samples. Stomatal −2 −1 conductance ranged from 83.5 to 361 mmol H2O m s , −2 −1 with an average of 214 mmol H2O m s and a standard −2 −1 deviation of 73.5 mmol H2O m s . Distribution was bi- −2 −1 modal, with peaks around 150 and 350 mmol H2O m s . 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 concentra- tion (Fig. 6). The other two species displayed no correlation with soil CO2 flux. B. nitida had a moderate negative correla- tion (r2 = 0.61) with slope, similar to its correlation between chlorophyll concentration and slope.

4 Discussion

4.1 Long-term plant uptake in volcanic CO2

Turrialba and Irazú continuously emit CO2 through their veg- etated flanks, but prior to this study it was unknown if the Figure 7. Leaf stomatal conductance of a tree species that strongly trees growing there were utilizing this additional isotopi- responds to volcanically elevated CO2 (Figs. 5, 6) has positive cor- cally heavy volcanic CO2. All tree cores with correspond- relations with volcanic CO2 flux, consistent with increased gas ex- ing CO2 flux measurements were from areas proximal to change. the Ariete fault on Turrialba, where atmospheric and vol- canic δ13C have significantly different values (−9.2 ‰ and −3.4 ‰, respectively; Malowany et al., 2017). If the trees as- found that altering the isotopic composition of the air by ar- similate volcanic CO2 through their stomata, then we would tificially adding CO2 with a different carbon isotope com- expect wood δ13C to trend towards heavier values as dif- position than the atmosphere leads to significant changes 13 fuse volcanic CO2 flux increases. Studies at FACE sites have in the δ C value of plant matter and tree rings growing www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1352 R. R. Bogue et al.: Plant responses to volcanically elevated CO2 there, leading us to expect similar effects from the natu- active than Mammoth Mountain, so trees growing in high rally added volcanic CO2 (Körner, 2005). It is worth not- emission areas of Turrialba may be exposed to similar or 13 ing that the FACE CO2 (δ C is −29.7 ‰), is significantly higher amounts of CO2 than the tree in the Mammoth Moun- depleted in 13C compared the atmosphere, whereas volcanic tain study. Additional measurements of tree core δ13C and 13 CO2 is enriched (δ C is −3.4 ‰ at Turrialba) compared to associated soil CO2 fluxes would help corroborate our ob- atmosphere (Körner, 2005). After excluding damaged sam- servations, which were based on a limited number of data ples and stressed trees, δ13C was strongly correlated with points. Though tree ring 14C content in volcanically active soil CO2 flux for both B. nitida and O. xalapensis (Fig. 4). areas has been linked to variations in volcanic CO2 emis- A. acuminata did not have a statistically significant correla- sions, and comparing patterns of δ13C to 14C measurements 13 tion between soil CO2 flux and δ C, likely because it had for the same wood samples could provide additional con- 13 the fewest data points and a minimal range of CO2 and δ C firmation of this finding (Evans et al., 2010; Lefevre et al., values. The difference in regression slope between B. nitida 2017; Lewicki et al., 2014), this additional dimension was and O. xalapensis (Fig. 4) may be due to physiological dif- outside the scope of this exploratory study. However, beyond ferences across traits or species, and/or due to differences such pattern confirmation, using 14C dating of trees exposed in exposure owing to canopy height differences. Resolving to naturally isotopically distinct excess CO2 is, in fact, un- this question would require a much larger multi-species sam- fortunately not a reliable method for these environments due ple size which could only be sufficiently obtained using re- to the well-known δ14C deficiency in trees exposed to excess mote sensing methods. The strong positive correlations be- volcanic CO2 which is isotopically “dead” with respect to 13 14 14 tween CO2 flux and increasingly heavy δ C values suggest C, creating spurious patterns that preclude dating by C that the trees have consistently photosynthesized with iso- (e.g., Lefevre et al., 2017; Lewicki et al., 2014). topically heavy excess volcanic CO2 over the last few years Our data demonstrate that CO2 fluxes through the soil and are therefore growing in eCO2 conditions. Assuming that may be a representative relative measure for eCO2 exposure most of the variations in δ13C are caused by incorporation of of overlying tree canopies. Forest canopy exposure to vol- heavy volcanic CO2, we can calculate the average concentra- canic CO2 will vary over time, as will volcanic eCO2; once tion of the mean volcanic excess CO2 in the air the plants are emitted through the soil into the sub-canopy atmosphere, exposed to with a mass balance equation (Eq. 2): the gas experiences highly variable thermal and wind dis- turbances which significantly affect dispersion of CO on (δ − δ ) 2 C = b t C , (2) minute-to-minute, diurnal, and seasonal timescales (Staebler v − a (δa δv) and Fitzjarrald, 2004; Thomas, 2011). These processes cause where Cv is the mean volcanic excess component of the CO2 in-canopy measurements of CO2 concentration to be highly concentration in air, Ca is the atmospheric “background” variable, making instantaneous concentration measurements (i.e., non-volcanic) CO2 concentration, δa is atmospheric in a single field campaign not representative of long-term 13 13 δ C, δb is the most negative δ C measurement for the relative magnitudes of CO2 exposure. Soil CO2 fluxes are 13 species being studied, δt is the δ C value for the tree for less tied to atmospheric conditions and are primarily exter- which volcanic CO2 exposure is being calculated, and δv is nally modulated by rainfall which increases soil moisture 13 13 the δ C value of the volcanic CO2. Background wood δ C and therefore lowers the soil’s gas permeability (Camarda is the value of the point for each species with the lowest et al., 2006; Viveiros et al., 2009). These fluxes can also 13 CO2 flux (Fig. 4), and the other wood δ C measurement be affected by variations in barometric pressure, but both of is any other point from the same species. Values for δv, δa, these factors are easily measurable and therefore can be fac- and Ca are taken from Malowany et al. (2017). For the tree tored in when conducting field work (Viveiros et al., 2009). core with the highest measured CO2 flux for O. xalapensis, Assuming the avoidance of significant rainfall and pressure this equation yields a mean excess volcanic CO2 concentra- spikes during sampling (measurements were conducted in tion of 115 ppm, bringing the combined mean atmospheric the dry season and no heavy rains or significant meteoro- (including volcanic) CO2 concentration tree exposure to po- logical variations in pressure occurred during field work), tentially around ∼ 520 ppm. For B. nitida this equation yields measuring the input of CO2 into the sub-canopy atmosphere 133 ppm of mean excess volcanic CO2 at the highest flux lo- as soil CO2 fluxes is therefore expected to better represent cation, for a combined total mean of potentially ∼ 538 ppm long-term input and exposure of tree canopies to eCO2 than CO2. These numbers may be on the high side as the cal- direct instantaneous measurements of sub-canopy CO2 con- culation assumes that carbon isotope discrimination remains centration. Previous studies at Turrialba have shown that lo- constant for all trees within a given species, but they serve cal volcanic CO2 flux is relatively constant on monthly to as an estimate of the approximate magnitude of the average yearly timescales (de Moor et al., 2016). Therefore, current 14 amount of CO2 that these trees are exposed to. A C tree soil CO2 fluxes should give relatively accurate estimates of ring study at Mammoth Mountain found an average yearly CO2 exposure over time. This paper corroborates that expec- volcanic excess CO2 exposure of 20–70 ppm over a 15-year tation by demonstrating strong spatial correlations between period (Lewicki et al., 2014). Turrialba is significantly more volcanically enhanced soil CO2 emissions with co-located

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1353 stable carbon isotope signals of these emissions documented CO2, displaying a strong positive correlation with fluores- in the trees’ xylem. cence and a weak positive correlation with chlorophyll con- A study at the previously mentioned Mammoth Moun- centration and stomatal conductance (Figs. 5–7). Previous tain tree kill area examined the connection between δ13C studies which linked changes in the NDVI to pre-eruptive and volcanic CO2 fluxes but focused on the difference be- volcanic activity on the flanks of Mt. Etna and Mt. Nyi- tween trees killed by extreme CO2 conditions and those that ragongo support our observation of a correlation between were still alive (Biondi and Fessenden, 1999). They con- plant function and volcanic CO2 flux (Houlié et al., 2006; cluded that the changes in δ13C that they observed were due Seiler et al., 2017). This link raises the question of why only to extreme concentrations of CO2 (soil CO2 concentrations one of three species displayed strong functional responses of up to 100 %) impairing the functioning of root systems, to volcanic CO2. The lack of response in B. nitida and O. leading to closure of stomata and water stress (Biondi and xalapensis could be due to nitrogen limitation, a factor that Fessenden, 1999). CO2 does not inherently harm trees, but would not affect A. acuminata due to its nitrogen-fixing capa- the extreme CO2 concentrations (up to 100 % soil CO2) at bility. Previous studies have found that nitrogen availability the Mammoth Mountain area caused major soil acidification, strongly controls plant responses to both naturally and arti- which led to the tree kill (McGee and Gerlach, 1998). We ficially elevated CO2 concentrations in a variety of ecosys- have evidence that those acidification processes are not af- tems, including grasslands and temperate forests (Garten et fecting our δ13C measurements and that variations in our al., 2011; Hebeisen et al., 1997; Lüscher et al., 2000; Norby δ13C measurements are more likely to be caused by the direct et al., 2010; Tognetti et al., 2000). Nitrogen limitation has photosynthetic incorporation of isotopically heavy volcanic been posited to be an important factor in tropical montane 13 CO2. Our δ C measurements have no statistically signifi- cloud forests and may be contributing to the lack of responses cant correlation with stomatal conductance, which suggests in B. nitida and O. xalapensis (Tanner et al., 1998). Due to that our heavier δ13C measurements are not linked to stom- the exploratory nature of our study, we do not have a large atal closure. None of the trees included in the analysis dis- enough dataset to conclude that the nitrogen-fixing capabil- played obvious signs of stress, from water or other factors, ity of species like A. acuminata is the cause for its positive as indicated by their high fluorescence and chlorophyll con- response to volcanically elevated CO2 concentrations, as has centration values and the lack of visible indicators of stress; been speculated before (Schwandner et al., 2004), but it is a specifically, our values of Fv/Fm ∼ 0.8 indicate that the PSII possible correlation that deserves further investigation. was operating efficiently in most of the trees we measured (Baker and Oxborough, 2004). The Mammoth Mountain tree 4.3 Time constraints kill areas have higher CO2 fluxes by several orders of magni- tude (well over 10 000 g m−2 d−1) than the areas we sampled To support these results, we further assessed the possibility (up to 38 g m−2 d−1), making it much more likely that stress of effects of time constraints on growth rates and isotopic from soil acidification causes stomatal closure and affects signals, despite the compelling spatial variability in the inde- wood δ13C measurements at Mammoth Mountain (Biondi pendent variable (naturally isotopically labeled excess vol- and Fessenden, 1999; McGee and Gerlach, 1998; Werner et canic CO2) in our study (Helle and Schleser, 2004; Verhey- al., 2014). In contrast, most of the diffuse degassing at Tur- den et al., 2004). As tropical trees typically lack tree rings, rialba does not lead to soil acidification or pore space satu- it is difficult to directly constrain the precise time period that ration, as is evident in our own and others’ field data (e.g., the data represent. However, since we sampled from the out- Epiard et al., 2017). Thus, changes in our δ13C values are side in, all the samples appear to at least have the most re- best explained by direct photosynthetic incorporation of iso- cent growth period in common. To assess how far back in topically heavy volcanic CO2. To the best of our knowledge, time our samples could likely represent, we compared our this is the first time that a direct correlation between volcanic sampled core depths to reported growth rates for the same 13 soil CO2 flux and wood δ C has been documented. Future species in similar environments. Reported growth rates for studies should explore this correlation further, as our findings two of our species, O. xalapensis and A. acuminata, range are based on a limited sample size. from 0.25 to 2.5 and 0.6 to 0.9 cm yr−1, respectively (Kap- pelle et al., 1996; Ortega-Pieck et al., 2011). Given that our 4.2 Short-term species response to eCO2 samples are bulk measurements of the outer 5 cm of wood, each sample would represent between 2 and 5.5 years, al- Short-term plant functional responses at the leaf level to el- though the conditions that these growth rates were measured evated CO2 were highly species-dependent. B. nitida had no in were different than in our study. Clear time constraints statistically significant functional responses to soil CO2 flux, would be necessary for higher resolution analysis, but this and O. xalapensis only had a weak negative correlation be- need is somewhat mitigated by the continuous, long-term, tween soil CO2 flux and chlorophyll concentration (Fig. 6). and, over multiple decades, mostly invariant nature of dif- A. acuminata, a nitrogen-fixing species, was the only species fuse volcanic CO2 emissions, which is completely indepen- with a consistent and positive functional response to elevated dent of any non-volcanic environmental influences on growth www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1354 R. R. Bogue et al.: Plant responses to volcanically elevated CO2 rates. By providing an upper and lower bound in the expected due to the completely independent nature of the volcanic ex- growth span represented in our samples, we believe that these cess CO2 supply to the sub-canopy air. samples represent similar time frames during the continuous exposure to excess volcanic CO over the lifetimes of the 2 4.4 Lessons learned for future studies 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 vari- This exploratory study reveals significant new potential for ability in excess CO2 availability averaged over similar time future studies to utilize the volcanically enhanced CO2 emis- periods. sions approach to study tropical ecosystem responses to Although we do not believe that our samples represent a eCO2 – one of the largest uncertainties in climate projec- long enough time period for long-term variations in δ13C tions. Costa Rica’s volcanoes are host to large areas of rel- (Suess effect) to be relevant, if it does affect our samples, atively undisturbed rainforest, making them ideal study ar- it would be beneficial for detection of volcanic CO2, as the eas for examining responses of ecosystems to eCO2. How- Suess effect is gradually increasing the gap between atmo- ever, there are several challenges that future studies should spheric and volcanic δ13C. Since our δ13C values likely rep- take into consideration if attempting to expand upon this pre- resent several years of growth, small-scale temporal varia- liminary study. Given the enormous tropical species diver- tions in excess volcanic CO2 release are unlikely to signif- sity and the need to control for confounding factors, large icantly impact the results. Larger trees tend to grow slower datasets will be needed to answer these questions conclu- than smaller trees, so the outer 5 cm of wood should repre- sively. One open question, for example, is how WUE in sent a longer time period in larger trees. Thus, if temporal upper and lower canopy leaves of the same and different variations had a significant effect on our δ13C measurements, individuals within a species may affect isotopic sequestra- we would expect this to be represented by some correlation tion of CO2. Since the excess volcanic CO2 is naturally iso- between DBH and δ13C, which is not present for any species topically labeled, this could be assessed by a much more studied. Three of the five B. nitida individuals measured were detailed (by individual tree leaf, branch, and xylem) core very large (150–190 cm DBH), whereas the other two are study coupled with long-term measurements of evapotran- much smaller (11.5 and 15.3 cm DBH). Although the age spiration, heat stress, and stomatal conductance, the last of and growth rates of these two groups of trees likely vary sig- which in our study showed no significant correlation with nificantly, we found no correlation between DBH and δ13C, the δ13C signal in the wood cores across spatial gradients. though we did find a strong correlation between the com- Field data can be difficult to acquire in these rugged and pletely independent diffuse excess (volcanic) CO2 flux and challenging environments. A remote sensing approach using wood δ13C. Furthermore, the relationships presented are on airborne measurements, validated by targeted representative a per species basis to avoid complications resulting from dif- ground campaigns, could provide sufficiently large datasets ferent growth rates across species. This is important because to represent species diversity and conditions appropriately. δ13C values provide an integral value of assimilated carbon Many of the data types that would be useful for this type by the entire tree (not just individual leaves). The depth of of study can be acquired from airborne platforms, and re- tree core sample was identical for each species (the outer- mote sensing instruments can quickly produce the massive most part of the trunk), and we can safely assume that the datasets required to provide more comprehensive answers to volcanic CO2 exposure has been consistent over the time pe- these questions. A recent meta-analysis showed that stud- riod under investigation. ies at natural CO2-producing springs and FACE experiments Because individual time variability of growth rates can have found similar results in a variety of plant traits, which possibly affect these signals as well, future studies that at- significantly strengthens the case that volcanoes are a poten- tempt to study tree ring isotopes in this context at higher res- tially extremely valuable resource for determining plant re- olutions will likely require stricter and more detailed time sponses to elevated CO2 concentrations (Saban et al., 2019). constraints and cell-level stress analysis to average out the ef- While the spring studies have yielded valuable results, vol- fects of long-term variations in δ13C (Suess effect), seasonal canoes could offer several advantages over springs for fu- cycles, potential short-term transient stress-induced growth ture studies. Active volcanoes are significantly larger systems rate variations, effects of water use efficiency (WUE), and than non-volcanic springs and often feature several CO2- potential short-term variations in CO2 flux, all of which may producing springs and also several dry gas seeps; this of- result in time-averaged isotopic shifts over different growth fers more data, more control points for comparison, greater periods (Helle and Schleser, 2004; Verheyden et al., 2004). species diversity, and greater potential for comprehensive We include these notes as guidance in Sect. 4.4: Lessons measurements of a statistically meaningful dataset from re- learned for future studies. Despite the additional difficulty of mote sensing platforms. Due to their volcanic hazard poten- conducting higher time resolution analysis, this type of study tial, volcanoes are also more likely to already have long-term holds great potential for attempting to reconstruct volcanic volcanological monitoring programs for CO2 fluxes and eco- CO2 histories and to study its potential fertilization effect, logical disturbances, which may be utilized to analyze the

Biogeosciences, 16, 1343–1360, 2019 www.biogeosciences.net/16/1343/2019/ R. R. Bogue et al.: Plant responses to volcanically elevated CO2 1355 long-term effects of enhanced levels of CO2 emissions on 5 Conclusions these volcanically active tropical ecosystems. Our results also offer significant new tools for the Multiple areas of dense tropical forest on two Costa Rican ac- volcanology, where reconstructing past volcano behavior tive volcanoes are consistently and continuously exposed to through eruption histories is hampered by severe preserva- volcanically elevated levels of atmospheric CO2, diffusively tion gaps in the stratigraphic record. A strong link between cold emitted through soils into overlying forests. These iso- δ13C and volcanic CO could be a game changer by estab- 2 topically heavy volcanic CO2 emissions, which are mostly lishing long-term histories of volcanic CO2 emission varia- invariant, not accompanied by acidic gases, and independent tions. These proxy signals could be traced back in time using of processes affecting growth rates, are well correlated with living and preserved dead trees in order to fill gaps in the increases in heavy carbon signatures in wood cores from two historical and monitoring records – a boon for volcano re- species of tropical trees, possibly suggesting long-term in- searchers and observatories to improve eruption prediction corporation of enhanced levels of volcanically emitted CO2 capabilities (Newhall et al., 2017; Pyle, 2017; Sparks et al., into biomass. Each tree studied was co-located with a soil 2012). While variations in tree ring 14C content have been CO2 flux measurement, and their soil CO2 flux signals vary shown to correlate well with variations in volcanic CO2 flux spatially around a continuous long-term local natural excess (Evans et al., 2010; Lefevre et al., 2017; Lewicki and Hilley, volcanic CO2 source, which creates a local CO2 gradient 14 2014), C is relatively expensive to measure, limiting the within which all the sampled trees are found. The excess vol- spatial and temporal coverage of data that can be acquired. canic CO2 through local fault-bound gas seeps provides con- 13 14 C is an inexpensive alternative to C and can be measured tinuous exposure to all sampled trees over timescales much at more laboratories, allowing for substantially more data to greater than the lifetimes of individual trees. Based on our be acquired. Some previously mentioned studies (Lefevre et limited exploratory measurements, confounding factors that al., 2017; Pasquier-Cardin et al., 1999) have found correla- are known to influence δ13C values in wood appear not to 13 14 tions between C and C in plants that have incorporated have significantly affected our measurements, indicating that 13 volcanic CO2, strengthening the potential for using C in the heavier wood δ13C values could be caused by photosyn- this type of study. Further development of the 13C approach thetic incorporation of volcanic excess CO2. One of the three to tracking volcanic CO2 emissions would prove beneficial species studied (A. acuminata) has consistent positive corre- to future studies attempting to use plants to study large ar- lations between instantaneous plant function measurements eas and timescales of volcanic degassing. Independent vali- and diffuse CO2 flux measurements, indicating that short- dation, and calibration by wood core dendrochronology via term variations in elevated CO2 emissions may measurably 14 C, tree rings, or chemical event tracers like sulfur iso- affect trees growing in areas of diffuse volcanic gas emis- topes, could significantly advance the concept of using wood sions. These observations reveal significant potential for fu- carbon as an archive of past degassing activity. Crucially, ture studies to use these areas of naturally elevated CO2 to these tree ring archives could provide temporal records of de- study ecosystem responses to elevated CO2 and to use trees gassing at dangerous volcanoes which have previously been as sensors of the changing degassing behavior of volcanic poorly monitored or not monitored at all, significantly im- flanks, which is indicative of deep magmatic processes. proving 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 Data availability. Data can be found in Tables S1 and S2 in the deeper processes inside volcanoes than crater-area degassing Supplement or can be requested from Florian Schwandner (flo- (Camarda et al., 2012), may permit the use of trees as sen- [email protected]). sors 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., Supplement. The supplement related to this article is available 2006; Pieri et al., 2016; Schwandner et al., 2017; Seiler et online at: https://doi.org/10.5194/bg-16-1343-2019-supplement. al., 2017; Shinohara et al., 2008; Werner et al., 2013). To the best of our knowledge, we are the first to propose utiliz- ing the combination of short-term leaf functional responses Author contributions. FMS and JBF designed the study, and RRB, 13 FMS, JBF, and ED conducted the field work and collected all sam- to volcanic CO2 with long-term changes in δ C values of wood for assessment of past and present volcanic activity in ples and data with some of the equipment borrowed from GN, who helped interpret the results. TSM processed the samples for anal- a single study. ysis. JPL conducted the SO2 analysis, wrote the related methods subsection, and helped interpret the results. VY modeled the an- thropogenic 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. www.biogeosciences.net/16/1343/2019/ Biogeosciences, 16, 1343–1360, 2019 1356 R. R. Bogue et al.: Plant responses to volcanically elevated CO2

Competing interests. The authors declare that they have no conflict Barquero, R., Lesage, P., Metaxian, J. P., Creusot, A., and of interest. Fernández, M.: La crisis sísmica en el volcán Irazú en 1991 (Costa Rica), Rev. Geológica América Cent., 18, 5–18, https://doi.org/10.15517/rgac.v0i18.13494, 1995. Acknowledgements. We are grateful for LI-COR, Inc. (Lincoln, Belikov, D. A., Maksyutov, S., Yaremchuk, A., Ganshin, A., NE, USA) providing us a loaner CO2 sensor for field work in Costa Kaminski, T., Blessing, S., Sasakawa, M., Gomez-Pelaez, A. J., Rica. We thank Rizalina Schwandner for engineering assistance and Starchenko, A.: Adjoint of the global Eulerian–Lagrangian during sensor integration, OVSICORI (Observatorio Vulcanológico coupled atmospheric transport model (A-GELCA v1.0): de- y Sismológico de Costa Rica – the Costa Rican volcano monitoring velopment and validation, Geosci. Model Dev., 9, 749–764, authority) for logistical and permit support, SINAC (Sistema Na- https://doi.org/10.5194/gmd-9-749-2016, 2016. cional de Áreas de Conservación – the Costa Rican national parks Biondi, F. and Fessenden, J. E.: Response of lodgepole pine growth service) for access to the Turrialba volcano, and Marco Antonio to CO2 degassing at Mammoth Mountain, California, Ecol. Otárola Rojas (Universidad Nacional de Costa Rica – ICOMVIS) Brooklyn, 80, 2420–2426, 1999. for invaluable help in the field. We also thank three anonymous re- Burton, M. R., Sawyer, G. M., and Granieri, D.: Deep Carbon Emis- viewers, Akira Kagawa, and the handling editor for very helpful and sions from Volcanoes, Rev. Mineral. Geochem., 75, 323–354, insightful suggestions that led us to improve the paper. Incidental https://doi.org/10.2138/rmg.2013.75.11, 2013. funding is acknowledged from the Sherman W. Hartman Memo- Camarda, M., Gurrieri, S., and Valenza, M.: CO2 flux measure- rial Fund at Occidental College for funding Robert R. Bogue’s field ments in volcanic areas using the dynamic concentration method: expenses as well as the Jet Propulsion Laboratory’s YIP (Year- Influence of soil permeability, J. Geophys. Res.-Sol. Ea., 111, Round Internship Program) and the Jet Propulsion Laboratory Ed- B05202, https://doi.org/10.1029/2005JB003898, 2006. ucation Office for funding and support for Robert R. Bogue. Flo- Camarda, M., De Gregorio, S., and Gurrieri, S.: Magma-ascent pro- rian M. Schwandner’s UCLA contribution to this work was sup- cesses during 2005–2009 at Mt Etna inferred by soil CO2 emis- ported by Jet Propulsion Laboratory subcontract 1570200. Part of sions in peripheral areas of the volcano, Chem. 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