Environ. Sci. Technol. 2006, 40, 6580-6586
Accumulation of Persistent Organic
Pollutants in Canopies of Different
Forest Types: Role of Species
Composition and
Altitudinal-Temperature Gradient
L U C A N I Z Z E T T O , †,§ K E V I N C . J O N E S , ‡
PAOLA GRAMATICA,† ESTER PAPA,†
BRUNO CERABOLINI,† AND
A N T O N I O D I G U A R D O * ,§
Department of Structural and Functional Biology, University
of Insubria, Via J. H. Dunant 3, 21100 Varese VA, Italy, Centre
for Chemicals Management and Environmental Science
Department, Lancaster Environment Centre, Lancaster
University, Lancaster, LA1 4YQ, UK, and Department of
Chemical and Environmental Sciences, University of Insubria,
Via Valleggio, 11, 22100 Como CO, Italy
Leaves from the dominant tree species in three different
alpine forests were sampled along an altitudinal gradient and
analyzed for HCB, R- and γ-HCH, and PCBs. The mean
canopy concentration was calculated, considering the relative
abundance of each species in the respective forest.
Compound fractionation occurred in the vegetation along
the altitudinal/temperature gradient. Results were compared
with air concentrations and in-field plant/air partition
coefficients (KPA) were calculated for each species; this
showed differences between broadleaves and needles. The
mean canopy/air partition coefficient (KCA) was also
calculated by averaging results from single species. The
variability of persistent organic pollutants distribution
in canopies is discussed considering two main factors,
the altitudinal/temperature gradient and the species
composition. The latter is responsible for most of the
concentration variability of the more volatile compounds.
A model to calculate dry gaseous deposition to different
forest canopies is presented.
Introduction
Important advances in our knowledge of the global distribution of organic pollutants have been made by studying
vegetation (1). Persistent organic pollutants (POPs) have been
measured in the vegetal biomass across latitudes and with
altitude, reflecting the accumulation of organic pollutants
from the atmosphere (2, 3) and supplying terrestrial food
webs (4, 5). Exposure of forest ecosystems to semivolatile
organic pollutants has also been investigated (6-10). Forest
canopies can influence air concentrations temporally (11,
12) and spatially (13). Given the proportion of the earth’s
surface covered by forests, their role in influencing pollutant
* Corresponding author phone: +39 031 2386480; fax: +39 031
2386449; e-mail: antonio.diguardo@uninsubria.it.
† Department of Structural and Functional Biology, University of
Insubria.
‡ Lancaster University.
§ Department of Chemical and Environmental Sciences, University
of Insubria.
6580
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 21, 2006
fate on a regional or global scale merits consideration (1417).
POPs were recently studied in vegetation in the Canadian
Rocky Mountains (18). Concentrations of some organochlorine pesticides increased along the altitudinal gradient. Alpine
systems provide the opportunity to compare different forest
types which change in specific composition with the increasing elevation over relatively small distances (compared
to latitudinal gradients) and where air concentrations may
be more uniform. Mountain environments were therefore
recently pinpointed as ideal sites to comparatively investigate
some of the transport phenomena (such as role of temperature or species composition) associated with the global
distribution of pollutants (19).
In this study, concentrations of PCBs, R- and γ-HCH, and
HCB were determined in leaves and needles from three
different forest sites in the Italian Alps. Previously, these
sampling sites were used to compare air concentrations
within and outside the forest (13, 20) and the deposition
fluxes to the canopies. The main aims of this investigation
were to evaluate the distribution of POPs in vegetation in
three different ecosystems and assess the contribution of
dominant species to the overall load of POPs in forest
canopies.
Experimental Section
Sampling Sites. Leaves were sampled from three sites in the
Lys Valley, Aosta, Italy, located at 1100, 1420, and 1790 m
above sea level (asl), respectively (Figure 1). Each site is
characterized by a different forest type, according to the
altitude, as described in Table 1.
Sampling. Leaf samples were collected from the dominant
tree species. Table 1 summarizes the species sampled and
their abundance at each site. Samples were collected in
October 2002, at the end of the growth season. For spruce
(Picea abies) new needles (year 0) were collected, to normalize
exposure time to deciduous species. Leaves were collected
from 21 transects using latex gloves at least 1.5 m from the
soil. At each location g3 trees of the same species were
sampled in an area of 400 m2 at least 100 m from the forest
edge. Samples therefore reflected the most abundant foliar
biomass in the inner canopy. Samples were kept in solventrinsed glass jars and frozen at -20 °C, until extraction.
Analysis. Samples were freeze-dried, homogenized, and
spiked with PCB 40 and PCB 128 as recovery standards.
Extraction (typically of 5 g) was performed in precleaned
cellulose thimbles (Schleicher & Schuell, Dassel, Germany)
using an all glass Soxtech-type automatic extractor (Velp
Scientifica, Usmate, Italy) with n-hexane/acetone 6:1 for 6
h. Solvents were pesticide residue grade from Sigma-Aldrich,
Seelze, Germany. Gel permeation cleanup was then performed in accordance with method USEPA 3640A (1998) (21),
using a 600 mm length, 26 mm i.d. glass column filled with
SX-3 beads (200-400 mesh, Bio-Rad, Hercules, CA) and
coupled to an Agilent 1100 series HPLC system (flow rate 3.5
mL/min, run time 72 min). Fractions were collected using
retention times of chemical markers according to the USEPA
procedure (21). Calibration standards were injected every 6
samples. Samples were subsequently fractionated in 15 cm
× 5 mm i.d. glass columns packed with activated Florisil for
residue analysis (60-100 mesh) purchased from Merck,
Darmstadt, Germany. Samples were eventually concentrated
to 50 µL and PCB 30 and PCB 141 were added as internal
standards. Analyses were performed using a Hewlett-Packard
5890 series 2 gas chromatograph (GC) equipped with dual
ECD. Injection was split via a Y connector into two parallel
10.1021/es0605523 CCC: $33.50
2006 American Chemical Society
Published on Web 09/28/2006
Calculation of Mean Canopy Concentration (MCC). The
MCC (expressed in pg g-1 dw) was calculated as follows,
n
MCC )
∑f Ci
(2)
i
i)1
where fi is the frequency of the species i and Ci is the mean
concentration of a certain chemical in that species.
Due to interspecific variability in accumulation behavior
(6, 23), the concentration distribution in samples of different
species collected in the same forest was not expected to be
normal. It was assumed that an estimation of the error
associated with the MCC calculation is the following,
x∑
n
EMCC )
fj(ci,j - MCC)2
i,j)1
(3)
xN
where EMCC is the error associated with MCC calculation, ci,j
is the concentration of the i observations of the j species and
N is the total number of observations.
FIGURE 1. Geographical location of sampling sites. 1100 m:
Broadleaf forest; 1400 m: Mixed broadleaf/conifer forest; 1800 m:
coniferous forest.
columns: a 60 m DB-5 (J&W Scientific, Folsom, CA, i.d. 0.25
mm, film thickness 0.25 µm) and a 60 m BP-50 (SGE
International, Melbourne, Australia, i.d. 0.25 mm, film
thickness 0.25 µm). This facilitated peak recognition when
compounds coeluted on one column. Carrier gas (He) flow
rate was 1 mL/min. The GC oven temperature program was
as follows: initially 90 °C hold for 1 min, 25 °C min-1 to 170
°C, 1 °C min-1 to 260 °C, then 15 °C min-1 to 300 °C, and hold
for 10 min. PCB congeners included (according to homologue
groups) the following: tri-PCB 28/31; tetra-PCB 52, 44, 49,
64, 74, 70; penta-PCB 104, 101, 99, 97, 87, 110, 118, 105; hexaPCB 136, 151, 149, 132/153, 138, 156; hepta-PCB 188, 187,
183, 174, 177, 180; octa-PCB 201, 203, 194. Single-compound
analytical standards were purchased from AccuStandard,
New Haven, CT. Purities were >98%.
QA/QC. Blanks were included as 1 in every 4 samples.
MDL was set as 3 times the blank values and varied from 7
to 25 pg/g dry weight (dw). No blank correction was
performed. Recoveries were 81 ( 11% for PCB 40 and 95 (
7% for PCB 128. All samples were corrected individually for
recovery. Analysis of standard reference material was performed using a certified sewage sludge.
Vegetation Survey and Temperature. Canopy composition was estimated in terms of species frequency (fj) in the
forest in a 2500 m2 plot. The parameter fj is calculated for
each species as follows,
fj )
Aj
(1)
n
∑A
j
j)1
where Aj is the surface of the canopy projection to the ground
of a given species (j) in a plot divided by the total canopy
projection for all the species of the same plot.
Specific leaf area (SLA) was measured according to ref 22.
Temperature was recorded hourly at each clearing and forest
site throughout the campaign using 6 Testo 174 data loggers
(Testo, Lenzkirch, Germany) equipped with a NTC-temperature sensor with resolution of 0.1 °C.
Results and Discussion
Levels of POPs in Vegetation and General Comments on
Trends. Table 2 summarizes the POPs concentrations
determined in each dominant species. HCB and R-HCH levels
were within the range reported for spruce and pine needles
collected in the Canadian Rocky Mountains (150-400 pg g1
dw) (18) at altitudes similar to those of the present study.
HCB concentrations in spruce needles were also consistent
with data from Austrian high-altitude sites (300-1100 pg g-1
dw) (24). Concentrations generally reflect remote and diffuse
contamination, rather than local sources, in agreement with
the air concentrations measured at the same sites (13). The
remote origin of the contamination is also confirmed by the
R-HCH/γ-HCH ratio that averaged 1.3 with the highest values
at the upper sites. These values are a factor of 6-7 times
higher than recent data from air measurements in the north
of Italy (25) where some of the most elevated concentrations
of γ-HCH in Europe have been detected. Davidson et al. (26)
measured concentrations of organochlorine pesticides along
an altitudinal-temperature gradient and showed that R- and
γ-HCH have opposite trends with decreasing temperature,
with the overall effect that the R/γ ratio increases with altitude.
Increasing R/γ ratios with altitude were also generally
observed elsewhere (24). These findings suggest that the
agricultural and urbanized areas in northern Italy do not
directly affect the concentrations recorded in the elevated
mountainous sites in the southern part of the Alps, probably
because of the lower contribution of local sources with height
as shown by the back trajectory analysis of air masses (13).
There are not many previous studies on PCB accumulation
by different tree species (30). Most of the available data relate
to conifers. PCB levels in spruce needles in the present study
exceed the values reported for Austrian mountains (24) by
a factor of 3-5. This could reflect the fact that the western
Alps tend to receive air masses coming from the highly
urbanized areas of the Po Valley and the northern and central
part of France (13). Unfortunately, no comparable measurements of atmospheric concentrations in these areas are
available. Nevertheless, the Austrian Alps appear to be
“protected” from the higher inputs from southern and
western sites (24). Recent data for pine needles collected in
the Central Pyrenean Mountains (27) also fall into the same
range as observed here.
PCB levels measured here also exceed the concentrations
reported by Ockenden et al. (6) for spruce collected in remote
VOL. 40, NO. 21, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
6581
TABLE 1. Sampling Sites and Dominant Speciesa
log KOA vs DF regression parameters**
a*
b*
species
SLA
(m2 kg-1)
relative
abundance
LAI*
(m2 m-2)
1100 m
chestnut: Castanea sativa
hazel tree: Corylus avellana
maple: Acer pseudoplatanus
0.013
0.020
0.012
0.33
0.33
0.33
3.9
-0.069
1.192
11.6
1400 m
beech: Fagus sylvatica
spruce: Picea abies (pn)
0.033
0.008
0.75
0.25
4.8
-0.079
1.312
8.5
1800 m
larch: Larix decidua (dn)
spruce: Picea abies (pn)
0.010
0.008
0.80
0.20
1.7
-0.032
0.969
7.6
site elevation
(m asl)
mean site
temp. (°C)
a SLA (specific leaf area) represents the foliar area corresponding to the unit of dry weight; LAI (leaf area index) represents the foliar surface
area corresponding to the corresponding ground unit. *From ref 13. **a and b can be used to calculate the respective forest specific depletion
factor as DF ) a log KOA + b. (pn): persistent needle species; (dn) deciduous needle species.
TABLE 2. Concentrations (Mean of Three Replicates ( Standard Errora) and Mean Canopy Concentrations (MCC) in pg g-1 of Dry
Weight
HCB
R-HCH
γ-HCH
PCB 28/31
PCB 52
PCB 101
PCB 118
PCB 138
PCB 153
PCB 180
a
chestnut
maple
hazel
beech
spruce
(1400 m)
spruce
(1800 m)
larch
MCC
(1100 m)
MCC
(1400 m)
MCC
(1800 m)
43 ( 6
69 ( 25
23 ( 8
117 ( 7
118 ( 9
370 ( 100
214 ( 35
97 ( 21
493 ( 72
162 ( 25
205 ( 92
129 ( 35
109 ( 42
244 ( 25
242 ( 39
492 ( 130
261 ( 8
400 ( 120
465 ( 27
151 ( 15
63 ( 2
76 ( 11
125 ( 22
187 ( 71
335 ( 114
264 ( 43
77 ( 11
311 ( 51
420 ( 21
163 ( 8
190 ( 77
156 ( 59
199 ( 77
160 ( 8
228 ( 11
388 ( 62
166 ( 7
149 ( 25
406 ( 28
156 ( 8
442 ( 109
198 ( 50
387 ( 150
336 ( 52
169 ( 34
280 ( 55
179 ( 6
184 ( 37
281 ( 21
81 ( 13
481 ( 263
266 ( 141
213 ( 118
241 ( 120
202 ( 117
287 ( 58
240 ( 34
162 ( 23
362 ( 110
93 ( 34
609 ( 53
152 ( 5
185 ( 70
284 ( 48
317 ( 37
409 ( 147
202 ( 93
213 ( 76
590 ( 257
174 ( 49
104 ( 37
91 ( 16
93 ( 21
183 ( 29
232 ( 47
375 ( 59
184 ( 30
269 ( 52
460 ( 25
159 ( 9
253 ( 40
166 ( 35
246 ( 47
204 ( 25
213 ( 11
361 ( 53
169 ( 35
158 ( 49
374 ( 53
137 ( 22
584 ( 54
175 ( 121
191 ( 118
275 ( 29
294 ( 29
385 ( 65
209 ( 54
203 ( 66
544 ( 105
158 ( 40
In the case of MCC the calculation of the error is performed as EMCC; see eq 3 for definition.
areas along the latitudinal transect in Norway by a factor of
3-5. This presumably reflects differences in the distance
from sources and the same factor difference in air concentrations (13, 28).
Forest Ecosystems and Altitudinal Distribution. Forest
ecosystem zonation with altitude is mainly driven by average
temperatures. Jaward et al. (13) showed that air concentrations within the forest canopy are strongly influenced by the
vegetation itself. Kylin et al. (29) measured different concentrations in needles within a planted pine forest and
attributed them to the effect of biomass density. Leaf
concentrations for a given species collected in different parts
of the transect or different forests will be influenced by many
factors (e.g., density and presence of other species). The MCC
was therefore calculated for the “forest canopy” compartment
as a whole. Data are presented in Table 2 and Figure 2, for
different compounds on the altitudinal gradient.
The HCB MCC significantly (P < 0.05) increased with
altitude, as did the air concentration (13). This is in agreement
with concentrations in needles collected in the Rockies (18)
where Davidson et al. related this to the orographic temperature gradient. In their study forest species composition
was quite constant with altitude. In the present study the
same trend occurs, but across varying canopy compositions.
The concentrations of other organochlorine pesticides and
total PCB did not vary significantly with altitude (Figure 2).
However, a trend of fractionation of PCB congeners in leaves
occurred with altitude (see Figure 3), even if not significant.
This was also reported in a recent study in pine canopies (27)
even if the authors suggested that the temperature dependence may have been a result of the combined seasonal and
altitudinal contributions. Previous studies have shown a
similar fractionation of PCBs with latitude in soil and air
(31-34).
It is interesting to note that (i) the altitudinal temperature
gradient and distance from sources are smaller than those
6582
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 21, 2006
FIGURE 2. Mean canopy concentration (MCC) of selected compounds
along the altitudinal gradient. Bars report EMCC (error in MCC, see
eq 3 for definition). ΣPCBs ) sum of PCB 28/31, 52, 101, 118, 138,
153, 180.
where latitudinal fractionation has been observed and (ii)
no fractionation of PCBs was observed in the air sampled on
this transect (13).
Fractionation was observed here in a medium (the overall
forest canopy) that changes composition along the altitudinal
gradient. The progressive replacement of broadleaf species
by conifer species with increasing altitude occurs in the Alps
(as well as along the latitudinal gradient from the tropics to
the sub-arctic region) could result in different accumulation
behaviors in different forest canopies. To evaluate the pattern
of accumulation in canopies, plant-air partition coefficients
(KPA) were calculated for each species.
FIGURE 3. Fractionation of PCBs congeners along the altitudinal gradient. Points represent single sample values. Bars report the weighted
average for each forest and the EMCC (error in MCC, see eq 3 for definition). Lines indicate the trend of means.
Plant-Air Partition Coefficients (KPA) Derived in the
Field for Different Species. To allow the contribution of
different species to the MCC to be compared, their concentrations (CP) were normalized by dividing them by the air
concentrations (CA). Air concentrations were derived from
passive sampler data reported by Jaward et al. (13) by
assuming an uptake rate of 3.5 m3 day-1 as directly measured
and suggested previously (13). Such normalization gave an
in-field derived KPA. The air concentrations measured within
the forest are influenced by the forest biomass itself, resulting
in lower concentrations than observed in clearings (13).
Therefore, the concept of an air concentration depletion
factor (DF) was introduced. This is a compound and canopy
specific parameter, defined as the ratio between the mean
atmospheric concentration measured within the forest
canopy and the one measured outside the forest (CA,in/CA,out)
(13) (Table 1).
Leaves were collected from the inner canopy for this
study, thereby being in contact with “depleted air”. The KPA
values (CP/CA) were therefore corrected by the depletion
factors DF. Thus, assuming CA ) CA,out where CA,out and CA,in
are the concentrations outside and inside the canopy,
respectively:
KPA ) CP/(CADF) ) CP/CA,in
(4)
KPA values derived for each species and chemical therefore
reflect the specific bioconcentration factor, assuming equilibrium conditions prevail. Previous studies reported different
times to reach plant-air equilibrium, depending on species,
experimental conditions, etc., ranging between a few days
and several months (35, 36). As far as we are aware, no BCF
data were reported for most of these species in the literature,
so it is unclear when such conditions prevail. Nevertheless,
in this study, mature leaves were sampled in autumn after
4-6 months of exposure (depending on altitude), at the end
of their life cycle (the canopies are mainly comprised of
deciduous leaves), so if equilibrium was not reached, it may
be assumed that this condition was approached as much as
temporally possible.
Data for log KPA are plotted against log KOA and corrected
for the average site temperature and linear regressions were
obtained:
log KPA ) n log KOA + c
VOL. 40, NO. 21, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
(5)
9
6583
Physical-chemical properties and regressions for PCBs and
HCB were taken from Li et al. (37) and Harner and Mackay
(38), respectively. Table S1 (Supporting Information) shows
the regression parameters for each sampled species. Good
linear correlations were found in all cases. Intercepts ranged
between -1.03 and -4.54, with the highest values for the
needle species. The slopes were lower for the needle species
(ranging between 0.38 and 0.43) than for the broadleaves
(0.53-0.74) and were highest for the chestnut (Castanea
sativa). This suggests that broadleaves better reflect the
accumulation characteristics of octanol since they have KPA
slopes which are closer to 1 when plotted against KOA. These
trends are similar to previous reports. Brorström-Lunden
and Löfgren (9) present data for spruce and air concentrations
which allow an intercept (-1.76) and slope (0.37) to be
calculated while Ockenden et al. (6) reported lowest slopes
for pine needles (0.51) compared to spruce and larch needles.
However, caution must be taken in comparing the accumulation behavior of different types of needles (e.g., pine
vs spruce) except where exposure conditions are similar. Di
Guardo et al. (39) compared DDT concentrations in pine
and spruce needles which were exposed to contaminated air
near a point source. They reported differences of a factor of
2-3 in the sequestered amounts in pine needles >2 years
old, while concentrations in spruce needle did not significantly vary with age. It was hypothesized that morphological
differences in the position of the resin channel within the
needle can result in a higher long-term accumulation capacity
for pine needles. Concerning broadleaves, few data are
available in the literature and most relate to monocotyledon
grass species that present very different structural and
physiological characteristics. Slopes varying between 0.16
and 0.52, with intercept ranging between -0.8 and -3.8,
were found in a field uptake experiment (35).
Figure S1 (Supporting Information) presents a comparison
of regression lines for all the species in the present study. It
appears that needles are more efficient at collecting the more
volatile compounds than broadleaves, generally when log
KOA < 9.5-10. If the temperature dependence of KPA and KOA
are known, it is possible to compare the accumulation
behavior of different plant species independently of temperature. Komp and McLachlan (40) showed that KPA
increased considerably at lower temperatures in ryegrasses.
They derived the enthalpy of phase transfer (∆HPA) experimentally. The application of such approaches to tree leaves
is not known. However, to a first approximation, KPA values
measured at different temperatures were normalized to the
temperature recorded at the 1400 m site using reported ∆HPA
(40) and plotted with the respective temperature-corrected
KOA. Results are reported in Figure S1b (Supporting Information). Comparing the trend reported in Figures S1a and S1b
(Supporting Information), it appears that the temperature
gradient does not account for a large part of the observed
variability. Figure S1b (Supporting Information) indicates
that the “cross point” of the regression model is shifted to
log KOA values of about 10-10.5.
Spruce and larch showed a net accumulation of more
volatile POPs during the exposure times at a rate approximately double that of the broadleaf species, while for
less volatile compounds KPA values were closer. The concentrations in each species (values taken from Table 2) can
be normalized by multiplying them by their relative abundance in the respective forests (data reported in Table 1).
This shows that, at the 1400 m site, spruce represents only
25% of the total foliar biomass but accounts for 40% of the
total load of HCB or PCB 28/31 in the canopy, yet only 14%
for PCB 180. Similarly, at the 1100 m site, the accumulation
of more volatile compounds is due primarily to the maple,
which captures about 60% of the total HCB in the canopy.
6584
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 21, 2006
These results show that the specific composition of the
forest and the relative abundance of species foliar biomass
are important in controlling the distribution and load of POPs
in the canopy, together with deposition velocities and the
forest ecological parameters such as density or volume. All
these parameters will influence the distribution and uptake
of POPs in forests (7-10, 15-17).
A Model for Dry Gaseous Deposition to the Forest
Canopy. The results presented above showed that in complex
forest systems, such as those occurring in temperate areas
and characterized by large biodiversity and high density,
forest structural parameters will be important for the
development of accumulation models. McLachlan and
Horstmann (10) have described the dry gaseous deposition
of organic chemicals as a diffusive process that can be treated
as a one-compartment model as follows:
[
(
kaV
∆t
CV ) KVACA 1 - exp KVA
)]
(6)
where CV and CA are the concentrations in the vegetation
and in air (mol m-3), respectively. The term KVA is the
vegetation-air partition coefficient and could be derived from
eq 1 as a function of KOA. k (m s-1) is the mass-transfer
coefficient describing transport from the air to the vegetation
and aV is the specific surface area of the vegetation AV/VV
(area of vegetation (m2)/volume of vegetation (m3)). In this
model, the canopy is a well-mixed monospecies compartment. In a multispecies forest, the accumulation behavior of
different species can affect both the pollutant uptake rate
and partitioning with the atmosphere, depending on the plant
species and their contribution to the forest canopy biomass,
as shown in the previous paragraphs. The KVA should therefore
refer to the canopy as a whole, and for the sake of clarity will
be called KCA, where
KCA )
MCCV
CADF
(7)
where MCCV (ng m-3) is the mean canopy concentration on
a volume basis, derived using the contribution of each species
leaf volume to the total canopy volume. Measures of DF and
its dependence on log KOA are reported elsewhere (13) for
three different forest types. Thus, eq 6 can be rewritten as
follows:
[
(
kaV
MCCV ) KCACADF 1 - exp ∆t
KCA
)]
(8)
Most of the problems of canopy parametrization arise in
estimating the volumetric concentrations, which requires
knowledge of the vegetation density F (kg m-3 based on dry
weight). Variability in this parameter can introduce a large
uncertainty in the predictive model. Specifically, estimating
values for the average leaf thickness (17) to represent the
overall canopy density (FC) is problematic. Intraspecies leaf
thickness variability of up to 40% depends on ecological
conditions, notably the total daily irradiance received by
leaves during their development (41). It is therefore useful
to obtain a F-independent model.
The parameter aV (specific surface area of vegetation) is
F-dependent and it can be expressed in terms of the specific
leaf area (SLA) (m2 kg-1), a parameter that expresses the
amount of leaf surface (of one face) of a certain species per
unit of dry weight, as follows,
aV ) FC2SLAC
(9)
where the subscript indicates that the SLA refers to its mean
value in the canopy. The SLA is commonly used in plant
ecology as an index of the photosynthetic efficiency. It can
be easily measured (22) and obtained from the literature.
Thus, to obtain a model independent of leaf density (F), eq
9 was introduced into eq 8 and both members were divided
by FC:
[
(
MCCV KCA
kFC2SLAC
)
CADF 1 - exp ∆t
FC
FC
KCA
)]
(10)
The ratio MCCV/FC and KCA/FC represent the MCC (mol kg-1)
and the canopy/air partition coefficient K/CA on a massvolume basis (m3 kg-1), respectively. Thus,
(
[
MCC ) K/CACADF 1 - exp -
k2SLAC
∆t
K/CA
)]
(11)
Equation 11 describes the dry gaseous deposition to the
canopy of a multispecies dense forest at a given time,
independent of F. It is easy now to describe the dry gaseous
deposition to the forest canopy per unit of ground surface
N (mol m-2 s-1), by introducing the leaf area index (LAI) (m2
m-2), a measure of the amount of vegetation surface per unit
of ground surface, as follows:
LAI
N ) MCC
)
SLAC
[
(
k2SLAC
LAI /
K C DF 1 - exp ∆t
SLAC CA A
K/
CA
)]
(12)
LAI/SLA (kg m-2) is a measure of the foliar biomass. As for
SLA, LAI values are commonly available in spatially and
monthly resolved forms (42). They can also be obtained using
remote sensing techniques for regional application.
As an example, the data reported in Table 2 and Table S1
(Supporting Information) can be used to calculate N for the
three forests of this study, assuming they have reached the
partitioning equilibrium with the atmosphere. In that case
eq 12 can be simplified as follows:
LAI
N ) MCC
SLAC
SLAC was obtained by averaging specific SLA values considering the relative abundance of each species. Results are
reported in Figure 4. Sites at 1100 and 1400 m appear to be
the most efficient in sequestering POPs. When a comparison
is performed by considering the same LAI value ) 1 to each
forest type (Figure 4b), the coniferous forest at 1800 m appears
much more efficient than the others. This normalization
makes it possible to assess the storage capacity of the canopy
due to density-independent factors. The enhanced efficiency
of the coniferous canopy in storing POPs is mainly due to
the high storage capacity of needles for accumulating gasphase POPs, even though their SLA is on average 50-70%
lower than that of the broadleaves. The SLA therefore does
not explain the differences in accumulation behavior, which
are presumably due to other structural/chemical features of
the leaves.
Considering the parameters expressed in eq 12, it appears
that the accumulation of gaseous POPs by canopies is a
process strongly influenced by the dynamics of canopy
growth and structure. Most of the parameters employed vary
with time and ecological conditions. In temperate deciduous
forests, for example, LAI can range from <1 to 4-5 (m2 m-2)
during the growing season, influencing the DF and the mass
balance of pollutant reaching the canopy. SLA is subject to
both inter- and intraspecific variability that can reach 50%
(43) depending on light availability. A similar variability of
SLA with time was also observed in a study of the carbon
FIGURE 4. (a) Pollutant load in forest canopy (ng m-2 of ground
surface). (b) Density-independent pollutant load in forest canopy
(LAI ) 1 m2 m-2 for each forest type).
cycle of a tropical forest (44). KPA and consequently KCA may
also be subject to variability, related to the life span of different
leaves, due to the structural and chemical changes occurring
in leaves during the growing period. An accurate evaluation
of the impact of forest biomass on the environmental fate
of POPs therefore needs to take account for the spatial and
temporal variability of forest structural parameters.
Acknowledgments
MIUR-COFIN 2001 is acknowledged for financial support.
We thank Mary Chiara (Mont Mars Regional Reserve, Valle
d’Aosta Region) for help with site selection, quality control
at the sampling sites, and general logistics.
Supporting Information Available
An additional table and figure illustrating regressions parameters for the log KPA equation and interspecific comparison of log KPA vs log KOA regression lines is reported. This
material is available free of charge via the Internet at http://
pubs.acs.org.
Literature Cited
(1) Calamari, D.; Bacci, E.; Focardi, S.; Gaggi, C.; Morosini, M.; Vighi,
M. Role of plant biomass in the global environmental partitioning of chlorinated hydrocarbons. Environ. Sci. Technol. 1994,
28, 429-434.
(2) Eriksson, G.; Jensen, S.; Kylin, H.; Strachan. W. The pine needles
as monitor of atmospheric pollution. Nature 1989, 341, 42-44.
(3) Gaggi, C.; Bacci, E.; Calamari, D.; Fanelli, R. Chlorinated
hydrocarbons in plant foliage: an indication of the troposheric
contamination level. Chemosphere 1985, 14, 1673-1686.
(4) McLachlan, M. S. Bioaccumulation of hydrophobic chemicals
in agricultural food chains. Environ. Sci. Technol. 1996, 30, 252259.
(5) McLachlan, M. S. A simple model to predict accumulation of
PCDD/Fs in an agricultural food chain. Chemosphere 1997, 34,
1263-1276.
(6) Ockenden, W. A.; Steinnes, E.; Parker, C.; Jones, K. C. Observations on persistent organic pollutants in plants: implications
for their use as passive air samplers and POP cycling. Environ.
Sci. Technol. 1998, 32, 2721-2726.
VOL. 40, NO. 21, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
6585
(7) Horstmann, M.; Bopp, U.; McLachlan, M. S. Comparison of the
bulk deposition of PCDD/F in a spruce forest and adjacent
clearing. Chemosphere 1997, 34, 1245-1254.
(8) Horstmann, M.; McLachlan, M. S.; Atmospheric deposition of
semivolatile organic compounds to two forest canopies. Atmos.
Environ. 1998, 32, 1799-1809.
(9) Brorström-Lundén, E.; Löfgren, C. Atmospheric fluxes of
persistent semivolatile organic pollutants to a forest ecological
system at the Swedish west coast and accumulation in spruce
needles. Environ. Pollut. 1998, 102, 139-149.
(10) McLachlan, M. S.; Horstmann, M. Forests as filters of airborne
organic pollutants: a model. Environ. Sci. Technol. 1998, 32,
413-420.
(11) Hornbuckle, K. C.; Eisenreich, S. J. Dynamics of gaseous
semivolatile organic compounds in a terrestrial ecosystem effects of diurnal and seasonal climate variations. Atmos.
Environ. 1996, 30, 3935-3945.
(12) Gouin, T.; Thomas, G. O.; Cousins, I.; Barber, J.; Mackay, D.;
Jones, K. C. Air-surface exchange of polybrominated diphenyl
ethers and polychlorinated biphenyls. Environ. Sci. Technol.
2002, 36, 1426-1434.
(13) Jaward, F. M.; Di Guardo, A.; Nizzetto, L.; Cassani, C.; Raffaele,
F.; Ferretti, R.; Jones, K. C. PCBs and selected organochlorine
compounds in Italian mountain air: the influence of altitude
and vegetation type. Environ. Sci. Technol. 2005, 39, 34553463.
(14) Simonich, S. L.; Hites, R. A. Importance of vegetation in removing
polycyclic aromatic hydrocarbons from the atmosphere. Nature
1994, 370, 49-51.
(15) Wania, F.; Mclachlan, M. S. Estimating the Influence of Forests
on the Overall Fate of Semivolatile Organic Compounds Using
a Multimedia Fate Model. Environ. Sci. Technol. 2001, 35, 582590.
(16) Wegmann, F.; Scheringer, M.; Möller, M.; Hungebühler, K.
Influence of vegetation on the environmental partitioning of
DDT in two global multimedia models. Environ. Sci. Technol.
2004, 38, 1505-1512.
(17) Yushan, S.; Wania, F. Does the Forest Filter Effect Prevent
Semivolatile Organic Compounds from Reaching the Arctic?
Environ. Sci. Technol. 2005, 39, 7185-7193.
(18) Davidson, D.; Wilkinson, A.; Blais, J. M. Orographic cold-trapping
of persistent organic pollutants by vegetation in mountains of
western Canada. Environ. Sci. Technol. 2003, 37, 209-215.
(19) Kallenborn, R. Persistent organic pollutant (POPs) as environmental risk factors in remote high-altitude ecosystems. Ecotox.
Environ. Safety 2006, 63, 108-112.
(20) Nizzetto, L.; Cassani, C.; Di Guardo, A. Deposition of PCBs in
mountains: The forest filter effect of different forest ecosystem
types. Ecotox. Environ. Safety 2006, 63, 75-83.
(21) SW-846, Test Methods for Evaluating Solid Waste, Physical/
Chemical Methods; U.S. Environmental Protection Agency, U.S.
Government Printing Office: Washington, DC, 1998; Vol. 1.
(22) Garnier, E.; Shipley, B.; Roumet, C.; Laurent, G. A standardized
protocol for determination of specific leaf area and leaf dry
matter content. Funct. Ecol. 2001, 15, 688-695.
(23) Böhme, F.; Welsch-Pausch, K.; McLachlan, M. S. Uptake of
semivolatile organic compounds in agricultural plants: field
measurements of interspecies variabilities. Environ. Sci. Technol.
1999, 33, 1805-1813.
(24) Weiss, P.; Lorbeer, G.; Scharf, S. Regional aspects and statistical
characterization of the load with semivolatile organic compounds at remote Austrian forest sites. Chemosphere 2000, 40,
1159-1171.
(25) Jaward, F. M.; Farrar, N. J.; Harner, T.; Sweetman, A. J.; Jones,
K. C. Passive air sampling of PCBs, PBDEs and organochlorine
pesticides across the Europe. Environ. Sci. Technol. 2004, 38,
34-41.
(26) Davidson, D. A.; Wilkinson, A. C.; Kimpe, L. E.; Blais, J. M.
Persistent organic pollutants in air and vegetation in Canadian
Rocky Mountains. Environ. Toxicol. Chem. 2004, 23, 540-549.
(27) Grimalt, J. O.; van Drooge, B. L. Polychlorinated biphenyls in
mountain pine (Pinus uncinata) needles from Central Pyrenean
6586
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 21, 2006
(28)
(29)
(30)
(31)
(32)
(33)
(34)
(35)
(36)
(37)
(38)
(39)
(40)
(41)
(42)
(43)
(44)
high mountains (Catalonia, Spain). Ecotox. Environ. Safety 2006,
63, 61-67.
Jaward, F. M.; Meijer, S. N.; Steinnes, E.; Thomas, G. O.; Jones,
K. C. Further study in the latitudinal and temporal trends of
persistent organic pollutant in Norwegian and U.K. background
air. Environ. Sci. Technol. 2004, 38, 2523-2530.
Kylin, H.; Hellstrom, A.; Nordstrand, E.; Zaid, A. Organochlorine
pollutants in scots pine needles - biological and site related
variation within a forest stand. Chemosphere 2003, 51, 669675.
Barber, L.; Thomas, G. O.; Parkman, S. A.; Jones, K. C. Variability
in the PCB concentrations of vegetation. Organohalogen Compd.
1999, 41, 379-382.
Agrell, C.; Okla, L.; Larsson, P.; Backe, C.; Wania, F. Evidence
of latitudinal fractionation of polychlorinated biphenyl congeners along the Baltic sea region. Environ. Sci. Technol. 1999,
33, 1149-1156.
Meijer, S. N.; Ockenden, W. A.; Steinnes, E.; Corrigan, B. P.;
Jones, K. C. Spatial and temporal trends of POPs in norwegian
and UK background air: implications for global cycling. Environ.
Sci. Technol. 2003, 37, 454-461.
Meijer, S. N.; Ockenden, W. A.; Sweetman, A.; Breivik, K.; Grimalt,
J. O.; Jones, K. C. Global distribution and budget of PCBs and
HCB in Background surface soils: implication for sources and
environmental processes. Environ. Sci. Technol. 2003, 37, 667672.
Ockenden, W. A.; Breivik, K.; Meijer, S. N.; Steinnes, E.;
Sweetman, A. J.; Jones, K. C. The global re-cycling of persistent
organic pollutants is strongly retarded by soils. Environ. Pollut.
2003, 121, 75-80.
Thomas, G. O.; Smith, K. E. C.; Sweetman, A. J.; Jones, K. C.
Further studies of the air-pasture transfer of polychlorinated
biphenyls. Environ. Pollut. 1998, 102, 119-128.
Barber, J. L.; Thomas, G. O.; Kerstiens, G.; Jones, K. C. Air-side
plant -side resistances influence the uptake of airborne PCBs
by evergreen plants. Environ. Sci. Technol. 2003, 36, 32243229.
Li, N.; Wania, F.; Ley, D.; Daly, G. A. Comprehensive and critical
compilation, evaluation, and selection of physical-chemical
property data for selected polychlorinated biphenyls. J. Phys.
Chem. Ref. Data 2003, 32, 1545-1590.
Harner, T.; Mackay, D. Measurement of octanol-air partition
coefficients for Chlorobenzenes, PCBs and DDT. Environ. Sci.
Technol. 1995, 29, 1599-1606.
Di Guardo, A.; Zaccara, S.; Cerabolini, B.; Acciari, M.; Terzaghi,
G.; Calamari, D. Conifer needles as passive biomonitors of the
spatial and temporal distribution of DDT from a point source.
Chemosphere 2003, 52, 789-797.
Komp, P.; McLachlan, M. S. Influence of temperature on the
plant/air partitioning of semivolatile organic compound. Environ. Sci. Technol. 1997, 31, 886-890.
Nobel, P. S. Internal leaf area and cellular CO2 resistance:
photosynthetic implications of variations with growth conditions
and plant species. Physiol. Plant. 1977, 40, 137-144.
Meeson, B. W.; Corprew, F. E.; McManus, J. M. P.; Myers, D. M.;
Closs, J. W.; Sun, J.-K.; Sunday, D. J.; Sellers, P. J. Global Data
Sets for Land-Atmosphere Models Available on CD and On-line;
LSLSCP Initiative 1: 1987-1988; American Geophysical
Union: March 1995; Vols. 1-5, http://www.agu.org/eos_elec/
95212e.html.
Gratani, L. Canopy structure, vertical radiation profile and
photosynthetic function in a Quercus ilex evergreen forest.
Photosynthetica 1997, 33, 139-149.
Nebel, G.; Dragsted, J.; Vega, A. S. Litter fall biomass and net
primary production in flood plain forests in the Peruvian
Amazon. For. Ecol. Manage. 2001, 150, 93-102.
Received for review March 8, 2006. Revised manuscript received August 8, 2006. Accepted August 23, 2006.
ES0605523