J Atmos Chem (2012) 69:215–230
DOI 10.1007/s10874-012-9238-1
Seasonal changes in the daily emission rates of terpenes
by Quercus ilex and the atmospheric concentrations
of terpenes in the natural park of Montseny, NE Spain
Joan Llusia & Josep Peñuelas & Roger Seco &
Iolanda Filella
Received: 14 December 2011 / Accepted: 25 June 2012 /
Published online: 15 July 2012
# Springer Science+Business Media B.V. 2012
Abstract We studied the daily patterns in the rates of terpene emissions by the
montane holm oak, Quercus ilex, in three typical days of winter and three typical days
of summer in Montseny, a natural park near Barcelona, and related them to the air
concentrations of terpenes, ozone and NO2. Terpene emission rates were about 10 times
higher in summer than in winter. Emissions virtually stopped in the dark. In both
seasons, rates of terpene emissions were well correlated with light, air temperature and
relative humidity. Rates of emissions were also correlated with stomatal conductance
and the rates of transpiration and photosynthesis. Almost all the individual terpenes
identified followed the same pattern as total terpenes. The most abundant terpene was
α-pinene, followed by sabinene + β-pinene, limonene, myrcene, camphene and αphellandrene. Atmospheric terpene concentrations were also about 10 times higher in
summer than in winter. A significant diurnal pattern with maxima at midday was
observed, especially in summer. The increase by one order of magnitude in the
concentrations of these volatile isoprenoids highlights the importance of local biogenic
summer emissions in these Mediterranean forested areas which also receive polluted air masses
from nearby or distant anthropic sources. Atmospheric concentrations of O3 and NO2 were also
significantly higher in summer and at midday hours. In both seasons, concentrations of O3 were
significantly correlated with concentrations of terpenes and NO2 in the air and with rates of
terpene emission.
Keywords Terpene emission rates . Terpene air concentrations . VOC . Seasonality .
Quercus ilex . Montseny
J. Llusia (*) : J. Peñuelas : R. Seco : I. Filella
Global Ecology Unit CREAF-CEAB-CSIC Center for Ecological Research and Forestry Applications,
Edifici C, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain
e-mail: [email protected]
Present Address:
R. Seco
Atmospheric Chemistry Division, National Center for Atmospheric Research, Boulder, CO 80301, USA
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1 Introduction
Most of the volatile organic compounds (VOCs) in the atmosphere come from plants (Ross
and Sombrero 1991; BEMA 1997; Peñuelas and Staudt 2010). VOCs are also present in the
atmosphere as a result of human activities linked to transport and land use (Hester and
Harrison 1995). VOCs have an important role in atmospheric chemistry (Peñuelas and
Llusia 2003; Peñuelas and Staudt 2010), particularly in the development of aerosols
(Andreae and Crutzen 1997) and in the physiological and ecological relationships between
plants and other organisms (Langenheim 1994; Peñuelas et al. 1995; Peñuelas and Staudt
2010; Seco et al. 2011a). In some plants, a kind of VOCs called isoprenoids, accumulate in
specialized organs in leaves and stems and can be released as deterrents against pathogens
and herbivores or as aids in wound sealing after damage (Pichersky and Gershenzon 2002).
In other plants, volatile isoprenoids are not stored but are emitted after production. They may
serve to attract pollinators and herbivore predators, to communicate with other plants and
organisms (Peñuelas et al. 1995; Llusia and Peñuelas 2001) and to confer some protection
against high temperatures and oxidative stress to the plant (Singsaas 2000; Peñuelas and
Llusia 2002; Peñuelas et al. 2005; Copolovici et al. 2005) or even to the ecosystem (Peñuelas
and Llusia 2003).
The production and rates of emission of terpenes are modulated by abiotic and biotic
factors (Langenheim 1994; Takabayashi et al. 1994; Peñuelas and Llusia 2001; Paris et al.
2010). Among the abiotic factors, irradiance and temperature (Sharkey and Loreto 1993;
Staudt and Bertin 1998; Peñuelas and Llusia 1999a; Filella et al. 2007; Porcar-Castell et al.
2009; Peñuelas and Staudt 2010) and water availability (Ebel et al. 1995; Bertin and Staudt
1996; Llusia et al. 2008) are important. These abiotic factors have strong effects, especially
under Mediterranean conditions that are characterized by long, dry summers coinciding with
high irradiance and temperatures (Di Castri 1973; Llusia et al. 2008). On the other hand,
seasonality (Llusia and Peñuelas 1998, 2000) and daily cycle (Peñuelas and Llusia 1999a)
also determine the production and emission of terpenes.
Light and temperature are known to affect the short-term (Staudt and Seufert 1995;
Peñuelas and Llusia 1999a, b) and seasonal control of emissions by the montane holm
oak, Quercus ilex L (Llusia and Peñuelas 2000). The emission appears to be mainly
influenced by temperature and light, probably through its dependence on the metabolites
of photosynthetic processes (Loreto et al. 1996a; Ciccioli et al. 1997; Peñuelas and Llusia
1999a). Irradiance and related physiological processes may thus influence the emission of
monoterpenes on a short timescale of minutes and hours, especially in species such as the
Mediterranean Q. ilex that do not store monoterpenes (Staudt and Seufert 1995; Peñuelas
and Llusia 1999b). The dependence of emission on light in these species has been ascribed
to the need of photosynthetic products for terpene biosynthesis. This dependence on light
has been confirmed by field observations (Kesselmeier et al. 1996; Bertin et al. 1997; Llusia
and Peñuelas 1999; Peñuelas and Llusia 1999b) and labelling experiments (Loreto et al.
1996a). On the other hand, higher temperatures exponentially increase the production and
rates of emission of most terpenes to a maximum by enhancing the enzymatic activity of
synthase, raising the vapour pressure of terpene and decreasing the resistance of emission
pathways (Tingey et al. 1991; Loreto et al. 1996b; Peñuelas and Llusia 2001).
Terpenes are one of the main groups of VOCs that favor the formation of O3 in the
troposphere (Calogirou et al. 1996; Emeis et al. 1997; Georgopoulos et al. 1997; Kleinman
et al. 1997). Tropospheric ozone, a very reactive oxidizing agent, is a by-product of the
photochemical processes associated with air pollution. This secondary pollutant forms from
chemical reactions involving oxides of nitrogen (NOx) and VOCs in the presence of sunlight
J Atmos Chem (2012) 69:215–230
217
(Simpson et al. 1995). In the steady state, a photochemical equilibrium exists among NO,
NO2 and O3. The presence of hydroxyl radicals and VOCs of anthropogenic or natural origin
causes a shift in the equilibrium towards higher concentrations of ozone (Jenkin and Hayman
1999). The production of ozone, and thus the concentrations reached, depends upon the input
concentrations and ratios of NO, NO2 and VOCs. While NOx are mainly emitted from vehicle
exhausts and industrial processes, both natural vegetation and industry are responsible for VOC
emissions. Some compounds, mainly terpenoids, are significant sources of ozone formation
and influence the oxidative characteristics of the atmosphere (Singh and Zimmerman 1992;
Lerdau and Peñuelas 1993; Peñuelas and Staudt 2010). In the Mediterranean region,
concentrations of ozone at ground level are high, and several toxic effects have been
described in crops and vegetation under experimental or field conditions (Gimeno et al.
1993; Peñuelas et al. 1995; Heiden et al. 1997; Ribas et al. 1998; Diaz-de-Quijano et al.
2009, 2012). As with other stressor effects, ozone could even favour VOC emission in
response to the stress and injury it produces, which would lead to a positive feedback in
the formation of tropospheric ozone (Peñuelas et al. 1999).
Q. ilex is a species of great interest in the Mediterranean area for its widespread and
abundant distribution (Castroviejo et al. 1996) and because it emits large amounts of
terpenes into the atmosphere (Peñuelas and Llusia 1999a; Llusia and Peñuelas 2000; Llusia
et al. 2011). The emission of terpenes by Q. ilex has been studied in relation to photosynthetic photon flux density (PPFD), temperature, water stress and rates of photosynthesis and
transpiration (Kesselmeier et al. 1996; Loreto et al. 1996a; BEMA 1997; Blanch et al. 2009;
Peñuelas et al. 2009; Llusia et al. 2011).
However, seasonal simultaneous measurements of daily terpene emissions and atmospheric concentrations are rare. In this work, we studied the daily patterns of the rates
of terpene emission in Q. ilex and related them first to net photosynthetic rates, stomatal
conductance (gs), PPFD and temperature, and thereafter to air concentrations of terpenes
and ozone in Montseny, a natural park near Barcelona. The study was conducted over
3 days typical of winter and three typical days of summer. These two seasons present
environmental conditions more limiting for photosynthesis than spring or autumn, and it
is during these winter and summer seasons that most errors in emission models have
been made (Bertin et al. 1997). The aim of this work was to study the effects of
terpene emissions by the dominant species on the terpene atmospheric concentration
and, additionally, to characterize the relationships between physiological and abiotic
factors under field conditions for the improvement of emission inventories in Mediterranean ecosystems that have been mostly based on emission algorithms developed from
growth-chamber studies.
2 Material and methods
2.1 Study site
The site of study was located within a densely forested natural park, Montseny, located about
60 km NNE of Barcelona (Catalonia, in the NE part of the Iberian Peninsula) and 25 km
from the Mediterranean coast (41°46′45.63″N, 02°21′28.92″E, 720 m above sea level;
Fig. 1). The site is highly representative of the montane holm oak (Q. ilex) forests in the
Mediterranean regions of France, Italy, Greece and eastern Spain (Terradas 1999). At
Montseny, the forests are dense and of resprout origin, having evolved from coppicing until
the 1950s to selection thinning afterwards (Avila and Rodrigo 2004).
218
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1600
PPFD (μmol m-2 s-1)
1400
Winter
Summer
1200
1000
800
600
400
**
200
Cuvette air temperature (0C)
0
40
***
30
***
20
10
***
***
***
***
0
Relative humidity (%)
100
80
60
40
***
20
0
5
8
11
14
17
20
Solar time (h)
Fig. 1 Daily time course of PPFD, cuvette air temperature and relative humidity during the sampling dates.
Asterisks indicate significant differences between seasons (ANOVAs, **, P<0.001; ***, P<0.0001)
2.2 Measurements of rates of gas exchange and sampling for leaf terpene emissions
Measurements were carried out in 3 days in the winter of 2009 (11 February 11 March and
25 March) and in 3 days in the summer of 2009 (15 July 28 July and 7 August). The same 3
or 4 Q. ilex trees were sampled each day. In each tree a twig with fully expanded sunlit
leaves was sampled. The trees were sampled six times daily for each sampling date.
Measurements were initiated between 6 h and 21 h. Measurements of net photosynthetic
rates, stomatal conductance and terpene levels were conducted using a gas-exchange system
J Atmos Chem (2012) 69:215–230
219
(CI-340 Hand-Held Photosynthesis System, CID, Inc., Camas, WA 98607 USA). Three to
five leaves were enclosed in a 35 cm2 clip-on gas-exchange cuvette. Air from the cuvette
was pumped through a glass cartridge (8 cm long and 0.3 cm internal diameter) manually
filled with terpene adsorbents Carbopack B, Carboxen 1003, and Carbopack Y (Supelco,
Bellefonte, Pennsylvania) separated by plugs of quartz wool. Samples were taken using a
Qmax air sampling pump (Supelco, Bellefonte, Pennsylvania). The hydrophobic properties
of activated carbon minimized sample displacement by water. In these tubes, terpenes did
not undergo chemical transformations as checked against trapped standards (α-pinene, βpinene, camphene, myrcene, p-cymene, limonene, sabinene, camphor, α-humulene and
dodecane). Prior to use for terpene sampling, these tubes were conditioned for 15 min at
350 °C with a stream of purified helium. The sampling time was 10 min, and the flow varied
between 470 and 500 mL/min depending on the glass tube adsorbent and quartz wool
packing. The efficiency of cartridge adsorption and desorption of volatilized liquid standards, such as α-pinene and d-limonene, was approximately 99 %. The adsorption efficiency
of the volatiles were estimated with the difference obtained from the standard amount of
volatilized and introduced into the tubes and thereby obtaining the desorption once made.
Blank air sampling on tubes was conducted for 10 min immediately before and after each
measurement without the plants in the cuvettes. The glass tubes were stored in a portable
fridge at 4 °C and taken to the laboratory. There, glass tubes were stored at −28 °C until the
analysis. In calculations of the terpene emission rates, terpene contents in the blank samples
measured without the plants were subtracted from the samples measured with the plants.
2.3 Air sampling for terpenes
Atmospheric terpenes were sampled for 20 min each hour at 0.5 Lmin−1. The samplings
were conducted between 6 h and 21 h at a height of 6 m from the soil. The type of cartridges
was the same as used for sampling terpene emissions. The samples were collected using a
Qmax air-sampling pump and were processed as explained above for emission rate analyses.
2.4 Meteorology and measurements of O3 and NO2
During both periods, meteorological data for temperature, relative humidity, wind direction
and speed, precipitation and solar radiation were gathered from a meteorological tower
meteorological tower at a height of 10 m was located at 100 m from the sampled trees and to
the atmospheric sampling site (Seco et al. 2011b).
Real-time measurements of concentrations of O3 and NO2 were provided by conventional
gas-phase air-pollution monitors maintained by the Department of the Environment of the
Catalan Government (Generalitat de Catalunya) at the same site.
2.5 Terpene analyses
Terpene analyses were performed by a GC-MS system (Hewlett Packard HP59822B, Palo
Alto, CA, USA). The monoterpenes trapped in the tubes were processed with an automatic
sample processor (Combi PAL, FOCUS-ATAS GL International BV 5500 AA Veldhoven,
The Netherlands) and desorbed using an OPTIC3 injector (ATAS GL International BV 5500
AA Veldhoven, The Netherlands) into a 30 m×0.25 mm×0.25 μm film thickness capillary
column (HP-5, Crosslinked 5 % pH Me Silicone; Supelco Inc.). The injector temperature
(60 °C) was increased at 16 °C s−1 to 300 °C. The injected sample was cryofocused at −20 °C
for 2 min after which the cryotrap was heated rapidly to 250 °C. Helium flow was
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0.7 ml min−1. Total run time was 23 min, and the solvent delay was 4 min. After injection of the
sample, the initial temperature (40 °C) was increased at 30 °C min−1 to 60 °C and
then at 10 °C min−1 to 150 °C. This temperature was maintained for 1 min and then increased at
70 °C min−1 to 250 °C and maintained for another 5 min.
The identification of monoterpenes was conducted by comparing the retention times with
standards from Fluka (Buchs, Switzerland), and the fractionation mass spectra with standards, literature spectra, and GCD Chemstation G1074A HP and the mass spectra library
wiley7n. Terpene concentrations were determined from calibration curves. The calibration
curves for common monoterpenes, α-pinene, Δ3-carene, β-pinene, β-myrcene, p-cymene,
limonene and sabinene, and common sesquiterpenes such as α-humulene were determined
once every five analyses using four different terpene concentrations. The liquid standards
were diluted in pentane and volatilized to be adsorbed in the tubes and then desorbed in the
same way than the samples. The calibration curves were always highly significant (r2 >0.99
for the relationships between the signal and terpene concentration). The other monoterpenes
and sesquiterpenes were calibrated using these calibration curves of the most common mono
and sesquiterpenes. The most abundant terpenes had very similar sensitivity with differences
less than 5 % among the calibration factors. The quantification of the peaks was conducted
using the fractionation product with mass 93.
2.6 Statistical analyses
To analyze the differences between seasons and among daily times in the variables studied,
we performed ANOVAs using STATISTICA v.6.0 for Windows (StatSoft, Inc. Tulsa,
Oklahoma). Statistical differences were also analyzed with post-hoc Fisher’s LSD tests.
Differences were considered significant at a probability level of P<0.05.
To test for the differences between terpene emissions and terpene air concentrations and
to accommodate random effects and interaction terms better, we also conducted PERMANOVAs (Anderson et al. 2008) using the Bray Curtis similarity, with time of day and season
(winter and summer) as fixed factors and individuals as random factors.
3 Results and discussion
3.1 PFD and temperature
PPFD and relative humidity, measured with the CI-340 cuvette sensors, were similar in
winter and summer except for differences due to the increase in diurnal hours in summer.
Summer temperatures were 10–20 °C warmer, depending on the time of day (Fig. 1).
3.2 Photosynthetic rates and stomatal conductances
Net photosynthetic rates (A) were higher in winter than in summer (P<0.0001, ANOVA,
Fig. 2). Maximum A values were measured in winter around noon (4.68±0.14 vs. 2.32±
0.34 μmol m−2 s−1 in summer). Values varied throughout the day following changes in
PPFD and temperature in both winter and summer. The maximum A was measured at 9 h. In
winter, the A values were constant between 9 h and 15 h, whereas in summer they tended to
decrease after 9 h, with a slight depression at midday (Fig. 2). The A values were correlated
with air temperature, but the correlation was higher in winter (r00.65, P<0.05) than in
summer (r00.28, P<0.05).
Photosynthetic rates (mol m-2 s-1)
160
-2
-1
7
Stomatal conductance (mmol m s )
J Atmos Chem (2012) 69:215–230
221
Winter
Summer
6
5
Season: P < 0.00001
Hour: P < 0.00001
S x H: P < 0.00001
4
***
3
***
***
2
1
0
Season: P < 0.00001
Hour: P < 0.00001
S x H: P < 0.02
140
120
100
*
80
**
60
**
40
*
20
0
5
8
11
14
17
20
Solar time (h)
Fig. 2 Daily time course of photosynthetic rates and stomatal conductances of Q. ilex leaves during the
sampling dates. Asterisks indicate significant differences between seasons (ANOVAs *, P<0.01; **, P<0.001;
***, P<0.0001)
Stomatal conductances (gs) were from twice to almost four times higher in winter than in
summer (P<0.0001, ANOVA). The maximum gs occurred at 9 h both winter (113±
23 mmol m−2 s−1) and summer (63±24 mmol m−2 s−1). The minimum gs values were
recorded at night in winter (27.7±2 mmol m−2 s−1) and summer (3.7±0.0 mmol m−2 s−1). No
significant correlations were found between gs and air temperature in either of the two
seasons. PPFD had a significant relationship with gs only in winter (r00.29, n051, P<0.05).
In general, and for any season, no correlations were found between gs and relative humidity.
The activity of gas exchange thus varied significantly between winter and summer
(Fig. 2). The holm oaks were less active in summer than in winter (Fig. 2).
3.3 Terpene emissions and tropospheric concentrations
Rates of terpene emission were about 10 times higher in summer than in winter (P<0.0001).
Emissions nearly stopped in the dark (Fig. 3a). The maximum rates of emission were recorded
at 18 h in summer (54.34±14.35 μg g−1 dry matter h−1) and at 12 h in winter (8.3±5.53 μg g−1
d.m. h−1). The minimum rates were recorded at 21 h in both summer (0.35±0.08 μg g−1 d.m. h−1)
and winter (0.07±0.03 μg g−1 d.m. h−1) (Fig. 3a).
222
J Atmos Chem (2012) 69:215–230
70.00
-1
-1
Terpene emission rates (g g d.m. h )
60.00
a)
50.00
Season: P < 0.00001
Hour: P < 0.00001
S x H: P < 0.00001
Winter
Summer
40.00
30.00
20.00
***
*
10.00
***
***
0.45
0.40
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
5
8
11
14
17
20
Individual compounds
-1
-1
emission rates (g g d.m. h )
Solar time (h)
20.00
18.00
16.00
14.00
12.00
10.00
8.00
6.00
4.00
2.00
0.12
b)
Winter
Summer
***
***
**
**
*
***
**
***
***
*
0.10
0.08
0.06
0.04
0.02
***
*
α
-P
he
lla
nd
re
ne
α
-P
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en
C
e
Sa
am
bi
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ne
en
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e
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en
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ar
M
en
yr
α
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-T
or
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m
on
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α
-T
er
Lpi
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α
at
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(β
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le
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0.00
Fig. 3 a Daily time course of rates of emission of total terpenes and b average rates of emission of individual
terpenes by Q. ilex leaves during the sampling dates. Asterisks indicate significant differences between seasons
(*, P<0.01; ***, P<0.0001). Measurements were conducted in winter 2009 (February 11, March 11 and
March 25) and in summer 2009 (July 15, July 28 and August 7)
J Atmos Chem (2012) 69:215–230
223
Almost all the individual terpenes identified followed the same pattern of emission as
total terpenes (Fig. 3b). The most emitted terpene was α-pinene (daily average of 2.37±
0.84 μg g−1 d.m. h−1 in winter, and 15.74±2.77 μg g−1 d.m. h−1 in summer, P<0.0001)
followed by sabinene + β-pinene (daily average of 1.59±0.56 μg g−1 d.m. h−1 in winter, and
6.56±1.85 μg g−1 d.m. h−1 in summer, P<0.001), limonene (daily average of 0.61±
0.22 μg g−1 d.m. h−1 in winter, and 4.03±0.78 μg g−1 d.m. h−1 in summer, P<0.0001), myrcene
(daily average of 0.61±0.06 μg g−1 d.m. h−1 in winter, and 3.25±0.48 μg g−1 d.m. h−1 in
summer), camphene (daily average of 0.07±0.03 μg g−1 d.m. h−1 in winter, and 3.97±
0.16 μg g−1 d.m. h−1 in summer, P<0.05) and α-phellandrene (daily average of 0.1±
0.04 μg g−1 d.m. h−1 in winter, and 0.9±0.16 μg g−1 d.m. h−1 in summer, P<0.001).
Since Q. ilex, the dominant plant species in the study area (Peñuelas and Boada 2003;
Bolòs 1983; Bolòs and Vigo 1990), is a strong emitter of terpenes, especially in warm
summer conditions (Llusia and Peñuelas 2000; Llusia et al. 2011), it strongly influenced the
atmospheric terpene concentrations of the natural park of Montseny.
As with the emission rates, the concentrations of total terpenes detected in the air (which
included monoterpenes and sesquiterpenes) were significantly different between seasons
(P<0.0001). They were about 10 times higher in summer than in winter (Fig. 4a). Seco et al.
(2011b) also reported one order of magnitude higher terpene air concentrations in summer
than in winter in their PTR-MS analyses. The maximum concentrations were recorded in
summer between 7 h and 10 h (approx. 1.65±0.10 nmol mol−1), and the minimum concentrations in winter were recorded between 18 h and 21 h (approx. 0.01±0.001 nmol mol−1).
The individual monoterpenes found and their concentrations in the air were very similar to
the emission profile of Quercus ilex (Fig. 4b), the dominant species in this forest. However,
there were particular daily patterns like the pattern of α-phellandrene that was present only
in summer and then it was greatly depleted in the morning and in the evening (Fig. 4b)
Concentrations of terpenes in the air in summer followed a diurnal cycle and correlated
well with light (r00.31, n054, P<0.05), air temperature (r00.39, n054, P<0.05), relative
humidity (r0−0.3, n054, P<0.05), photosynthetic rates (r00.68, n054, P<0.05) and
stomatal conductance (r00.66, n054, P<0.05). While the foliar rates of emission increased
with temperature and therefore reached maximum values at 17 h in summer and midday in
winter, the concentrations of terpenes in the air varied in parallel (Figs. 3 and 4) in winter
(r0−0.31, P<0.02) and in summer (r00.39, P<0.004). The higher terpene emission rates of
summer translated in higher tropospheric terpene concentrations (Figs. 3 and 4), thus
following the increase of temperature.
The daily variation of VOC concentrations was mainly governed by the wind regime
of the mountain, as the majority of the VOC species analyzed followed a very similar
diel cycle (Seco et al. 2011b). Mountain and sea breezes that develop after sunrise
advect polluted air masses to the mountain. These polluted air masses had previously
passed over the urban and industrial areas surrounding the Barcelona metropolitan area,
where they were enriched in nitrogen oxides and in VOCs of biotic and abiotic origin.
Moreover, these polluted air masses received additional biogenic VOCs emitted in the
local valley by the local vegetation dominated by the Quercus ilex forest, thus enhancing ozone formation in this forested site. The only VOC species that showed a
somewhat different daily pattern were monoterpenes because of their local biogenic
emission. Isoprene also followed in part the daily pattern of monoterpenes, but only in
summer when its biotic sources were stronger. The increase by one order of magnitude
in the concentrations of these volatile isoprenoids highlights the importance of local
biogenic summer emissions in these Mediterranean forested areas which also receive
polluted air masses from nearby or distant anthropic sources (Seco et al. 2011b).
224
J Atmos Chem (2012) 69:215–230
2.00
a)
Season: P < 0.00001
Hour: P < 0.00001
S x H: P < 0.00001
Tropospheric total terpene
concentrations (ppbv)
1.50
Winter
Summer
1.00
0.50
**
0.04
***
0.03
***
*
*
0.02
***
0.01
0.00
5
8
11
14
17
20
Solar time (h)
rt8.2
rt8.3
α-Phellandrene
α-Pinene
Camphene
Sabinene + -Pinene
β-Myrcene
3
Δ -Carene
rt10
rt10.1
rt10.2
Limonene
Tropospheric individual monoterpene
concentrations (ppbv)
2.00
b)
Winter
1.50
Summer
1.00
0.50
0.04
0.03
0.02
0.01
0.00
5
8
11
14
17
20
Solar time (h)
Fig. 4 a Daily time course of the total terpene concentrations in the air in winter and summer. Asterisks
indicate significant differences between seasons (ANOVAs, *, P<0.01; **, P<0.001, ***, P<0.0001). b
Daily time course of the individual monoterpene concentrations in the air. The rtx acronym stands for retention
time of unidentified compounds
Monoterpenes (α-Phellandrene, α-pinene, camphene, sabinene + β-pinene, β-myrcene,
limonene, γ-terpinene, α-terpinolene, α-terpineol), and sesquiterpenes (α-longipinene,
longicyclene, isolongifolene, α-caryophyllene, β-cariophyllene) were the main emitted
compounds. In general, the monoterpenes that were emitted were also detected in the air
(Fig. 6). This indicates the biotic origin of at least part of VOCs in the air. However, given
the entry of regional masses of contaminated air in this site (Seco et al. 2011a, b), the
contribution of other sources of VOCs analyzed is not ruled out.
Tropospheric NO2 concentrations
(ppmv)
J Atmos Chem (2012) 69:215–230
10
225
a)
Winter
Summer
8
6
4
***
***
2
**
0
Tropospheric O3 concentrations
(ppbv)
80
Season: P < 0.00001
Hour: P < 0.0001
b)
60
*
***
40
***
**
17
20
20
0
5
8
11
14
Solar time (h)
Fig. 5 Daily time course of the air a) NO2 and b) O3 concentrations in winter and summer (white and black
filled symbol respectively). Asterisks indicate significant differences between seasons (ANOVAs, *, P<0.01;
**, P<0.001, ***, P<0.0001)
The sesquiterpenes instead were not detected in the air (Fig. 6) which indicates that they
quickly reacted as expected from their high reactivity (Jardine et al. 2011). Other authors
have reported low relative concentrations of sesquiterpenes in the air (in winter maximum
of 6 pptv at 18 h in summer 65 pptv at 3 h, Bonn et al. 2007). Emissions and air
concentrations proportions were similar for all compounds in summer diurnal hours. In
winter, during daylight hours α-pinene concentrations represented a higher percentage of
total BVOC air concentrations than in total BVOC emissions (Fig. 6). Pre-dawn and night
samples presented different emission patterns, but the concentration patterns remained
similar to those of diurnal hours (Fig. 6) probably because the temperature of nocturnal
sampling times were greater than those in the early hours before sunrise (2 °C and 1 °C
difference in winter and summer respectively), and for the diurnal rhythmicity of emission
rates (Dement et al. 1975; Arey et al. 1995). The results of many studies based on
inclusion in chambers indicate that the temporal variations of the emissions of sesquiterpenes appear to be mainly dominated by the ambient temperature, although other contributing factors (for example, seasonal variations) may also be involved. This implies that
sesquiterpenes emissions are increasingly important at certain times of year, especially late
spring to midsummer (Duhl et al. 2008).
226
J Atmos Chem (2012) 69:215–230
Winter
100
E
C
E
C
E
C
E
C
E
C
E
C
α-Phellandrene
α-Pinene
Camphene
Sabinene+β-Pinene
β -Myrcene
Limonene
β-Terpinene
α-Terpinolene
α-Terpineol
α-Longipinene
Longicyclene
Isolongifolene
α-Caryophyllene
β -Caryophyllene
80
60
40
Percentage
20
0
5
8
11
14
17
20
Summer
E
C
E
C
E
C
E
C
E
C
E
C
100
80
60
40
20
0
5
8
11
14
17
20
Solar time (h)
Fig. 6 Daily time course of the individual percentage of the terpenes emitted (E) by Q. ilex and of the terpene
concentrations in the air (C) for winter and summer sampling days
3.4 Tropospheric concentrations of O3 and NO2
The tropospheric concentrations of O3 and NO2 were also significantly higher in summer
(P<0.0001) than in winter as reported in the nearby areas (Ribas and Peñuelas 2006). The
maximum concentrations of O3 in summer were registered at 12 h (72.55±3.57 ppmv) and
the minimum at 6 h (43.6±1.4 ppmv). In winter, the concentrations did not vary significantly
during the day, but the peak was registered between 9 h and 12 h (approx. 44±3.5 ppmv).
J Atmos Chem (2012) 69:215–230
227
The maximum concentrations of NO2 were registered in summer at 12 h and 15 h (approx.
3.25±1 ppmv) and the minimum at 6 h and 21 h (approx. 1.1±0.1 ppmv). In winter, the
concentrations during the day increased from 15 h (approx. 0.6±0.1 ppmv) to a maximum at
18 h (2.13±0.62 ppmv).
The higher terpene emission rates and tropospheric concentrations in summer also
translated into higher tropospheric ozone concentrations (Figs. 3, 4, 5 and 6). Terpene air
concentrations were significantly correlated with ozone concentrations when considering the
whole data set (r00.57, P<0.0001, N035). There was a positive correlation between
emissions of monoterpenes and ozone concentrations in both summer and winter (r00.49,
P<0.01, N018 and r00.77, P<0.0001, N017, respectively). However, there was a negative
correlation between concentrations of monoterpenes and concentrations of ozone in winter
(r0−0.64, P<0.01, N017). In summer the high concentrations of terpenes and NO2 together
with the high temperatures and radiation favored the formation of ozone and consequently,
due to its high reactivity, the destruction of the sesquiterpenes in air (Jardine et al. 2011).
4 Conclusions
So in summary, in the present study we studied the evolution of the gas exchange and the
VOC emission rates of Quercus ilex in Montseny in parallel with the measured terpene
concentrations and NO2 and O3 in the air. The main results indicate that there are great
differences in gas exchange of Quercus ilex between winter and summer seasons, with
higher photosynthetic rates in winter, and higher emission rates in summer, highlighting the
importance of the temperature as abiotic factor in the terpene emission rates and the
uncoupling between photosynthetic rates and terpene emission rates. The highest terpene
emission rates were accompanied by the highest tropospheric terpene and O3 concentrations
highlighting the significant local influence on atmospheric chemistry complementing the
long distance arrival of air masses.
Acknowledgments This study was supported by the Spanish Government grants CGL2006-04025/BOS,
CGL2010-17172, Consolider-Ingenio Montes CSD2008-00040 and Acción Complementaria DAURE
CGL2007-30502-E/CLI, and the Catalan Government grant SGR 2009-00 458. Roger Seco was partially
supported by an FPI fellowship (BES-2005-6989) from the Spanish Government and by a postdoctoral grant
from Fundación Ramón Areces. The National Center for Atmospheric Research is sponsored by the National
Science Foundation.
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