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Bidirectional ammonia exchange above a mixed coniferous forest

J. Neirynck a,*, R. Ceulemans b

a Research Institute for Nature and Forest, Gaverstraat 4, B-9500 Geraardsbergen, Belgiumb Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Antwerp, Belgium

Received 2 January 2007; received in revised form 21 November 2007; accepted 21 November 2007

Both stomatal emissions as well as ammonia evaporation from saturated leavescontributed to the canopy emissions from a nitrogen-saturated forest.

Abstract

Two canopy compensation point models were used to study the bidirectional exchange of ammonia over a mixed coniferous forest subjectedto high nitrogen deposition. The models were tested for 16 time series, average fluxes of which ranged between �270 and þ1 ng m�2 s�1. Thestatic model consisted of a bidirectional stomatal flux and a unidirectional cuticular flux component. The dynamic model also allowed for de-sorption of ammonia from the leaf surface and took into account ammonia fluxes from precedent periods. The apoplastic ammonium/hydrogenion ratio (G), which was derived to estimate the stomatal compensation point (cs), amounted to 3300 in spring and 1375 during the summer/autumn. Empirical descriptions for cuticular resistances (Rw) in the static model, developed as a function of micrometeorological conditionsand codeposition effects, failed to reproduce the measured fluxes. A better match with measurements was obtained using the dynamic model,which succeeded in simulating net-emission during the daytime.� 2007 Elsevier Ltd. All rights reserved.

Keywords: Ammonia; Bidirectional exchange; Compensation point; Cuticular flux; Stomatal flux

1. Introduction

Ammonia is the main contributor to nitrogen fluxes in coun-tries with intensive livestock production. Due to its high spatialvariability in emission and the multitude of variables mediatingits exchange with vegetation (Asman, 1998), modelling of am-monia deposition is still a challenge for the modelling commu-nity. There is need for long-term studies of ammonia exchangeover agricultural and semi-natural vegetations to incorporateparameters in soilevegetationeatmosphere transfer (SVAT)models and chemistry transport models. These models linkemissions with deposition fields and are used to estimate actualecosystem exposures, and hence propose abatement strategies(Erisman et al., 2005).

Physiological processes regulating stomatal conductanceand physico-chemical processes influencing uptake at theleaf surface drive ammonia exchange (Flechard et al., 1999).However, many physiological and environmental parametersare involved in the season- and species-dependent stomatal ex-change (Schjoerring et al., 1998). Concerning exchange withthe external leaf surface, interactions with other gases and pro-cesses over the leaf surface need to be considered (Erismanet al., 2005). Consequently, detailed information from the re-ceptor sites and the chemical climate are required to estimatedeposition within an acceptable degree of uncertainty.

Exchange of ammonia over agricultural crops differs drasti-cally from that over semi-natural vegetation. Fertilized (high ni-trogen) agricultural ecosystems are known to emit ammoniarather than absorbing it (Sutton et al., 1993a). Forests and moor-lands are considered as perfect sinks of ammonia (Duyzer et al.,1992; Sutton et al., 1993b) although increasingly more evidenceis present that ammonia uptake over semi-natural vegetationmight be limited (Fowler et al., 1998; Wyers and Erisman,

* Corresponding author. Tel.: þ32 (0) 54 437119; fax: þ32 (0) 54 436161.

E-mail address: johan.neirynck@inbo.be (J. Neirynck).

0269-7491/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2007.11.030

Available online at www.sciencedirect.com

Environmental Pollution 154 (2008) 424e438www.elsevier.com/locate/envpol

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1998). Forests or moorlands can occasionally emit ammonia asa consequence of raised stomatal compensation points due tohistorical nitrogen pollution (Sutton et al., 1993a, 1994,1995). In addition, ammonia, previously deposited on a wettedleaf surface, can also be volatilized in the atmosphere when wa-ter films are evaporating (Wyers and Erisman, 1998).

Our study site is a mixed coniferous, suburban forest,nearby Antwerp, subjected to local NOx emissions from trafficand NH3 bearing air masses originating from livestock facili-ties located 5e10 km to the northeast. Throughfall depositionsat the site, mainly consisting of ammonium, still exceed30 kg ha�1 yr�1 and excessive nitrate leaching and NO emis-sion are symptomatic for the nitrogen saturation of the site(Neirynck et al., 2007). Measurements of net ammonia fluxesindicate the presence of a substantial canopy resistance imped-ing turbulent deposition of ammonia on the canopy (Neiryncket al., 2005). Also net-emission occurs, but its origin (stomata,cuticle) remained speculative until now. In fact only the net-effect of different deposition and emission fluxes from or to-wards stomata and cuticle is measured. Internal cycles ofgaseous fluxes between these ammonia sinks or sources mayexist which never reach the atmosphere.

This study aims to understand the mechanisms behind thecanopy exchange process of ammonia above this nitrogen-saturated forest by applying bidirectional models. The netflux is subdivided into a stomatal and a cuticular componentafter scrutinizing the physiological control over the stomatalgas exchange and specifying the impact of physico-chemicalproperties on the cuticular sink. The relative contribution ofboth flux pathways to the total flux is examined under differentmeteorological conditions.

2. Material and methods

2.1. Site description

The measurement site is located in a 2 ha Scots pine (Pinus sylvestris L.)

stand (planting date¼ 1929) with a mean height of 21.5 m belonging to

a mixed coniferous, suburban forest located in the Campine region of Flanders

(Belgium, 51�180N, 4�310E). The forest encompasses over 300 ha and is het-

erogeneous but of even height. Other Scots pine stands surround (ca. 150e300 m) the measurement site, with patches of deciduous trees found further

away. It is bordered to the north and west by residential areas of the town

of Brasschaat at a distance of ca. 500 m (Fig. 1), and to the south and east

the forest extends over 2 km before turning into rural, partially forested terrain.

A footprint analysis, carried out by Gockede et al. (2005) based upon source

weight functions for all stratification regimes, revealed that the forestland use

type contributed on average about 80% to each eddy covariance flux measure-

ment at 41 m height. Potential perturbation effects due to limited fetch might

arise in NW direction.

Ammonia emission e from cattle stables and manure spreading e origi-

nates from rural areas located approximately 10 km north and east. The grid

cells containing these point sources have an emission flux density ranging be-

tween 4 and 11 ton N km�2 yr�1. Southwesterly winds correspond to SO2 and

NOx polluted air masses.

2.2. Meteorological and ammonia measurements

Half-hourly measurements of NH3 gradients were made with wet rotating

annular denuders (Wyers et al., 1993) using online conductivity analysis

(AMANDA, ECN, Petten, The Netherlands) at two platforms (23 and 39 m)

on the measuring tower above the canopy. Gaseous ammonia was absorbed

in acid solution (3.6 mM NaHSO4). The solution was transported to a common

detection cell at the 23 m level platform. Every 2 min one of the two flows was

fed to the detector and the flow rate was measured. In the detector, NaOH was

added to the sample, to form gaseous ammonia. After passing a semi-

permeable PTFE membrane, NH3 was dissolved into a counter flow of

double-demineralized water and was converted into NH4þ. After a 90-s stabi-

lization time, the temperature-corrected conductivity was measured for 30 s

to determine [NH4þ]. Given the differences in travelling time between the

two denuders, weekly measurements were checked and corrected for possible

lags in the readings.

Standard meteorological parameters (Neirynck et al., 2005) were sampled

at 0.1 Hz, averaged for output at 0.5-h intervals and stored electronically with

a CRT10 (Campbell Scientific Ltd., Shepshed, UK) data logger. A leaf wetness

sensor (237F, Campbell, Shepshed, UK) was mounted on a boom at 19 m.

Eddy flux measurements with a 3D sonic anemometer (model SOLENT

1012R2, Gill Instruments, UK) were taken at 20.8 Hz (Carrara et al., 2003).

2.3. Flux measurements

Fluxes (F ) were calculated from half-hourly mean values from the

BusingereDyer fluxeprofile relationships (Dyer and Hicks, 1970; Businger

et al., 1971):

F¼�Kv½NH3�

vzð1Þ

where F is defined positive-upward and K is the turbulent diffusivity, calcu-

lated as:

K ¼ kðz� dÞu�f

ð2Þ

In this formula k (the von Karman constant) is 0.4, z is the geometric mean

of the measurement heights (27.9 m), d is the displacement height (¼19.2 m)

inferred from wind profile measurements, and u* is the friction velocity deter-

mined as the (negative) square root of the kinematic momentum flux measured

by eddy covariance. In order to account for stability effects, the universal

fluxeprofile relationships for heat transfer (fh) were applied (Dyer and Hicks,

1970). Because the concentration measurements were made in the roughness

sublayer, turbulent diffusivities estimated by Eq. (2) were corrected by a factor

(a) to allow for wake turbulence generated above the canopy (Bosveld, 1991):

fh ¼(

L� 0.a�

1� 16 ðz�dÞL

��ð1=2Þ

L> 0.aþ 5 ðz�dÞL

ð3Þ

where L is the MonineObukhov length and (z� d )/L is the dimensionless sta-

bility parameter.

Lacking information on temperature gradients, the factor a was determined

empirically from measurements of wind profiles, momentum fluxes and

(z� d )/L (analogous to Eq. (3), but for momentum). Rejection criteria, which

were applied to meet the requirements of the constant flux layer, are detailed in

Neirynck et al. (2005).

2.4. Applied bidirectional models

In the classically used resistance model the affinity of the canopy surface

for the pollutant is approximated through the canopy resistance (Rc). The latter

is usually calculated as the inverse of the deposition velocity (yd) minus the

atmospheric resistances, Ra and Rb, which we calculated according to Hicks

et al. (1987) and Garland (1978), respectively:

Rc ¼1

ydðz� dÞ �Raðz� dÞ �Rb ð4Þ

This formulation can, however, only be applied when no emission fluxes

are measured and no surface concentration exists. Because the classical can-

opy resistance model cannot cope with emission events, bidirectional models

are used in which the role of the canopy is mediated through a canopy com-

pensation point (cc), which expresses the net potential of ammonia emission

425J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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from the canopy. The net flux Ft above the canopy can be calculated from cc

(in mg m�3):

Ft ¼�cðz� dÞ � cc

Raðz� dÞ þRb

ð5Þ

Emission above the canopy occurs through physiological and/or physico-

chemical processes when the ambient concentration c(z�d )< cc.

Two bidirectional models were applied to the data set:

(i) Static canopy compensation pointecuticular resistance (cceRw)

model

In this model (Sutton and Fowler, 1993), the net flux above the canopy (Ft)

is divided into a bidirectional flux through stomatal resistance (Fs) and a uni-

directional flux towards the leaf surface (Fw):

Ft ¼ Fs þFw ð6Þ

with

Fs ¼ðcs � ccÞ

Rs

ð7Þ

and

Fw ¼�cc

Rw

ð8Þ

The stomatal exchange flux (Fs) is determined by the difference between

the canopy concentration (cc) and the stomatal compensation point (cs), the

gas concentration in the substomatal cavity. The latter is linked to the dis-

solved [NH4þ] and pH in the apoplast via the temperature response of the com-

bined Henry and solubility equilibria (Nemitz et al., 2000):

cs ¼161 500

ðTþ 273Þ exp�� 10 380ðTþ 273Þ�1��NHþ4

��Hþ� ð9Þ

where T is the surface temperature in �C, all concentrations are expressed in

mol l�1. Stomatal emission occurs when cs> cc. The stomatal resistance

(Rs) is calculated from the measured water vapour flux. The apoplastic

[NH4þ]/[Hþ] ion ratio also termed as G is independent on meteorological

parameters.

The irreversible downward flux to the cuticle (Fw) depends on the cuticular

resistance (Rw), which is dependent on relative humidity and leaf surface

chemistry.

The canopy compensation point (cc) is the result of the two competing

pathways and represents the net-result of the exchange with all sites of the can-

opy. It depends on the ambient concentration c(z�d ) and includes cuticular

physico-chemical processes as well as physiological aspects. It is calculated

as (Sutton et al., 1995):

cc ¼½cðz� dÞ=ðRaðz� dÞ þRbÞ þ cs=Rs��ðRaðz� dÞ þRbÞ�1þR�1

s þR�1w

� ð10Þ

(ii) Dynamic canopy compensation pointecuticular capacitance (cceCd)

model

This model is extended with a bidirectional flux for leaf surface exchange

and takes into account the presence of formerly deposited fluxes onto the cu-

ticle surfaces. Ammonia can be either adsorbed by or desorbed from the cuti-

cle, depending on humidity, wetness and acidity of the water film (Sutton

et al., 1998). The epicuticular water film is described through a capacitance

(Cd) and the flux (Fd) entering or leaving the adsorption capacitor then

becomes:

Fd ¼ðcd � ccÞ

Rd

ð11Þ

with

cd ¼Qd

Cd

ð12Þ

where Qd and cd are, respectively, the adsorption charge (mg m�2) and concen-

tration (mg m�3) associated with the capacitor while Rd is the charging resis-

tance of the capacitor. An estimate of Cd is found using solubility equilibria

provided by Sutton et al. (1993a) and an equivalent canopy area water film

thickness (McH2O):

Cd ¼McH2O

� �Hþ�

10ð1:6035�ð4207:6=TÞÞ þ 10ðð1477:7=TÞ�1:6937Þ

ð13Þ

where Cd and McH2O are given in meter and T in Kelvin.

Fig. 1. Location of the measurement tower in the experimental forest site (grey: forest; black: residential areas; waves: water pools, horizontal bands: low veg-

etation types such as meadows, clearcuts or moorlands).

426 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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The canopy compensation point concentration is calculated as:

cc ¼½cðz� dÞ=ðRaðz� dÞ þRbÞ þ cs=Rs þ cd=Rd��

ðRaðz� dÞ þRbÞ�1þR�1s þR�1

d

� ð14Þ

In order to run the dynamic model an initial value of Qd{i} must be chosen.

The new charge density after t seconds is then:

Qdfiþtg ¼ Qdfig �Fdt ð15ÞThe dynamic model also accounts for net removal of NH3 by leaf surfaces

by adding a leaf uptake ‘‘Qd{i}Kr’’ term to Eq. (15) where Kr is a reaction rate

constant (s�1). In this way, Qd may decrease not only because of desorption,

but also because of net removal from the leaf surface into the leaf (rather

than wash-off and deposition to the ground).

2.5. Parameterisations

The stomatal resistance (Rs) was calculated from stomatal resistances for

water vapour Rs(H2O), which were estimated according to Thom (1975):

RsðNH3Þ ¼DH2O

DNH3

RsðH2OÞ ¼ DH2O

DNH3

r3�esat

�T�z0o�� ew

�z0o���

PEð16Þ

where DH2O and DNH3are the respective diffusivities of H2O and NH3

(DH2O=DNH3is equal to 0.97), r represents air density (g m�3), 3 is the ratio

of molecular weight of water to that of dry air (equal to 0.622), P is the atmo-

spheric pressure (kPa), T is the temperature (�C) at the mean canopy height

(z0o), E (kPa m s�1) is the water vapour flux, esat is the saturation pressure at

Tðz0oÞ and ew is the water vapour pressure (kPa). To provide stomatal resis-

tances for NH3 under conditions when the vegetation was wet with rain, a sim-

ple model of stomatal resistance was applied using photosynthetic photon flux

density (PPFD) while accounting for effects of vapour pressure deficit (vpd),

water potential (j) and temperature (T ) (Hicks et al., 1987). It was fitted to

bulk stomatal resistance values for dry conditions.

The resistance for leaf surface uptake (Rw) was parameterized using se-

lected measured ammonia canopy resistances Rc (Eq. (4)) after discarding up-

ward fluxes. Canopy resistances at night (global radiation< 5 W m�2) were

assumed to equate with Rw (assuming closed stomata). Canopy resistances

were related to relative humidity (RH) for every half-hourly time-step using

the following equation (Sutton and Fowler, 1993):

Rw ¼ Rw;min exp

1�RH

a

�ð17Þ

The coefficients Rw,min (minimal cuticular resistance) and a were fitted by

least-square optimization for different canopy wetness categories which were

further subdivided into different NH3/SO2 ratio and temperature sub-categories

(see Neirynck et al., 2005). With regard to canopy wetness, four different

wetness categories were differentiated based upon rainfall and leaf wetness

measurements. Data were first subdivided into rainy (rainfall measured by

pluviometer) and non-rainy events (no rainfall recorded by pluviometer). The

non-rainy events were further differentiated when the canopy was dry (plate

wetness of leaf wetness (LW) sensor¼ 0), wet (0< LW< 1) or water-saturated

(LW¼ 1). Median temperature was used to subdivide the canopy wetness cate-

gories into low and high temperature events. For the codeposition effects of NH3

and SO2 three classes were differentiated: (i) molar ratio< 1: excess of SO2 over

NH3, (ii) molar ratio between 1 and 5: near-equivalent ratios (close to 2 mol

NH3:1 mol SO2 to form (NH4)2SO4), and (iii) molar ratio> 5: excess of ammo-

nia over SO2.

For the calculation of the Rw during the daytime (global radi-

ation> 5 W m�2), similar parameterisations between Rw and RH were derived

from daytime values for which leaf wetness> 0.75. In these conditions it was

assumed that open stomata were covered by a water film and stomatal flux was

inhibited given lower radiation.

The G factor, necessary as input for calculating Fs in both models, was de-

termined by selecting ammonia air concentration and corresponding T from

the whole set of daytime events at which the flux changed sign for a dry can-

opy (LW¼ 0) and a RH below 55% (large Rw). In these conditions of assumed

absence of cuticle/atmosphere flux, a switch from deposition to emission or

vice versa was interpreted as an equality between measured air concentration

and stomatal compensation point concentration (Flechard et al., 1999). The re-

tained ammonia concentrations were plotted against temperature (leaf temper-

ature was approximated by the temperature measured at 24 m) and fitted to Eq.

(9). Selected data were also grouped according to season or year in order to

ascertain possible seasonal differences in G factor.

The canopy area water film thickness McH2O (dynamic model) was obtained

by multiplying the footprint related leaf area index (LAI) by the film thickness

on a leaf area basis MH2O:

McH2O ¼ LAIMH2O ð18Þ

MH2O (in mm) was approximated by (personal communication J. Burkhardt):

MH2O ¼ 0:0031 expð3:5061LWÞ ð19ÞUsing a scaled-up footprint LAI ranging between 1.5 and 3 (obtained from

up scaling of LI-COR LAI 2000 measurements using vegetation mapping data

(see Gond et al., 1999)), canopy area water film thickness McH2O values ranging

between 0.005 and 0.3 mm were obtained.

The charging resistance (Rd), calculated as Rd¼ 5000/Cd, was adopted

from Sutton et al. (1998). Parameterisations of the reaction rate Kr and the

acidity of the surface layer were obtained by optimizing the model results

to minimize bias and maximize the R2 between observed and modelled fluxes.

3. Results

3.1. Selected time series

Between June 1999 and November 2001, 8800 half-hourlyfluxes were obtained after removing biased data and applyingrejection criteria (Neirynck et al., 2005). An average netammonia flux of �90 ng m�2 s�1 was measured with corre-sponding average concentration c(z�d ) and deposition veloc-ity yd of 4.1 mg m�3 (st. dev.¼ 6.5 mg m�3) and 3.0 cm s�1 (st.dev.¼ 4.6 cm s�1), respectively. Of the net fluxes, 14% repre-sented emission fluxes, which occurred mainly during daytime.From these data, a selection of 16 complete series was made,across different years, seasons and weather conditions, repre-senting about 40% of the complete data set (Table 1). Time se-ries with abundant rainfall were avoided given the highermeasuring errors (gradient, sonic data), missing parameterisa-tions and unsuccessful re-initialisations of the model runs afterheavy rainfall, where Cd could not be linked to pH.

Average fluxes for the individual model runs ranged be-tween �270 and 1 ng m�2 s�1 (Table 2). In some runs(1999: June and July; 2000: February, May, July and August;2001: May and October) the daily flux pattern typically con-sisted of low nighttime fluxes and high daytime fluxes (com-piled in Fig. 2A). These high daytime fluxes could beattributed to high daytime turbulence combined with a high af-finity for canopy uptake (low Rc). At noon, however, a drop inthe deposition occurred as a consequence of stomatal emissionor reduced uptake. An opposite diurnal pattern was found forNovember (1999, 2000 and 2001), April (2001), August (2001and partly 2000) and September (2001B) with low daytimefluxes due to emission events during the day (compiled inFig. 2B). Ammonia levels were lower compared to Fig. 2Aas there was a distinct drop in the morning ammonia levels be-cause of the initiation of atmospheric mixing in the morning.As a consequence, nighttime deposition fluxes turned intoemission at noon. Fig. 2A and B have in common that thereare two local peaks in fluxes towards the direction of emission;

427J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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a small peak in the morning (9 and 10 a.m., respectively) anda larger peak at noon (12 a.m. and 2 p.m.).

3.2. Model results

3.2.1. Static cceRw modelEstimation of the stomatal compensation point according to

Eq. (9) yielded a different value for the spring and summer/au-tumn periods. During the spring a G factor of 3300 (R2¼ 0.59,se¼ 320, n¼ 37) was derived while G decreased to 1375(R2¼ 0.50, se¼ 205, n¼ 20) during the summer/autumn

period (Fig. 3). During winter no suitable emission recordswere found to make a winter estimate of G. The G factor of3300 (spring) was only applicable to the time series of April2001 and May (2000; 2001). For the other time series themodels were run using the lower value. Corresponding stoma-tal compensation points ranged between 3.0 and 25.1 mg m�3

(T: 8.3e25.9 �C) during spring and between 1.5 and18.9 mg m�3 (T: 9.5e31.2 �C) during summer/autumn.

Median daytime values of Rw (12 s m�1) were found to belower than nighttime values of Rw with values of 59 (dry can-opy) and 28 s m�1 (wet and water-saturated canopy). For

Table 1

Overview of measurement conditions for leaf wetness (LW), relative humidity (RH), rainfall (R), temperature (T ), NH3 level and molar NH3/SO2 ratio during the

selected time series from the measurement campaign (n¼ number of valid flux measurements)

Start date End date n LW (%) RH (%) R (mm) T (�C) NH3

(mg m�3)

NH3/SO2

(mol/mol)

1999Jun99 24/06/1999 1/07/1999 310 32 74 11.1 15.8 4 4.6

Jul99 8/07/1999 11/07/1999 104 37 69 0 19.3 11.3 14.8

Nov99 6/11/1999 15/11/1999 340 67 91 3.1 6.5 5.5 6.1

2000

Feb00 4/02/2000 16/02/2000 415 31 57 35 6.7 1.0 0.8

May00 30/04/2000 4/05/2000 178 56 87 0.4 11.8 7.3 19.5

Jul00 28/07/2000 30/07/2000 107 24 82 19 16.9 1.6 2.1

Aug00 17/08/2000 20/08/2000 102 45 76 28.2 17.8 1.5 1.7

Nov00 3/11/2000 7/11/2000 221 59 91 13.2 6.7 0.5 2.9

2001Apr01 20/04/2001 23/04/2001 109 22 62 0.2 7.2 6.2 42.5

May01 10/05/2001 14/05/2001 169 61 56 0 19.4 9.3 8.2

Aug01 17/08/2001 26/08/2001 253 37 72 13.4 21.7 0.7 1.2

Sep01A 18/09/2001 24/09/2001 224 57 87 29.5 12 3.3 6

Sep01B 27/09/2001 1/10/2001 191 53 85 14.3 15.4 1 0.74

Oct01 04/10/2001 12/10/2001 369 38 79 23.2 14.2 1.7 1.61

Nov01A 16/11/2001 19/11/2001 116 59 85 0.1 6.5 5.8 6.5

Nov01B 22/11/2001 28/11/2001 245 61 91 20 7.0 0.7 2.9

Table 2

Measured versus modelleda fluxes of ammonia divided into day and nighttime (in ng m�2 s�1) (modelled fluxes in bold indicate bias with measured flux> 25%)

and overall correlationb between measured and modelled fluxes (R2)

Measured flux Static model Dynamic model

Day Night All Day Night All R2 all Day Night All R2 all

Jun99 �232 �96 �186 �73 �42 �63 0.80 �211 �120 �181 0.89

Jul99 �341 �142 �269 �248 �67 �182 0.67 �318 �232 �286 0.58

Nov99 �26 �58 �47 �91 �55 �68 0.03 �22 �71 �55 0.23

Feb00 �41 �28 �33 �17 �9 �12 0.29 �45 �35 �38 0.28

May00 �211 �152 �187 �193 �73 �144 0.37 �239 �151 �204 0.12

Jul00 �69 �26 �58 �23 �15 �21 0.52 �70 �32 �60 0.68

Aug00 �73 �9 �54 �12 �10 �12 0.85 �67 �19 �53 0.94

Nov00 0 �6 �4 �9 �6 �7 0.01 �1 �6 �4 0.22

Apr01 �37 �91 �57 �86 �49 �72 0.15 �36 �90 �56 0.31

May01 �108 �60 �90 �108 �35 �81 0.43 �61 �217 �118 0.30

Aug01 2 �3 1 16 �3 11 0.19 2 �15 �3 0.33

Sep01A �42 �40 �41 �43 �49 �40 0.30 �46 �88 �68 0.11

Sep01B 7 �13 �3 �14 �11 �12 0.01 10 �16 �3 0.57

Oct01 �153 �90 �117 �27 �24 �25 0.52 �130 �84 �105 0.89

Nov01A �2 �127 �70 �68 �59 �63 0.07 �15 �114 �69 0.51

Nov01B �15 �16 �15 �13 �8 �9 0.37 �16 �13 �14 0.53

a Two model approaches were used; i.e., a static and a dynamic model.b Significance of correlation coefficient at P¼ 0.05 is denoted in bold.

428 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

Author's personal copy

several molar ratio/temperature sub-categories a statistical sig-nificant relationship between Rw and RH could be derived fornighttime Rw (Fig. 4) and daytime Rw (Fig. 5). When a statis-tically significant relationship (significant parameters Rw,min

and a) was missing, which was especially the case for wetand rainy events, a constant value for Rw was used. Explainedvariability of the significant nonlinear relationships was some-times low and corresponding standard errors of regressedparameters were large (Table 3). Lowest nocturnal values ofRw were typically found during events when NH3 and SO2

were present in near-equivalent concentrations (molar ratiosbetween 1 and 5) during warmer weather conditions (T>median¼ 11 �C for nighttime) (Fig. 4). The appearance ofa RH dependence for water-saturated canopies might be dueto desiccation effects triggered by dropping RH (decreasingwater pool) or incomplete inhibition of stomatal exchange.For daytime conditions (Fig. 5), excess of NH3 over SO2 (molarratio> 5) during warm conditions (>15 �C) seemed to be con-ducive to enhance cuticular uptake. Results should, however, beinterpreted with caution as standard errors are large.

Modelled fluxes of NH3 deviated significantly from themeasured net NH3 fluxes (Table 2). Only one time series

0

1

2

3

4

5

1 3 5 7 9 11 13 15 17 19 21 23

X(z-d

) (µ

g m

-3)

-240

-200

-160

-120

-80

-40

0

Net N

H3 flu

x (n

g m

-2 s

-1)

X(z-d)Fmeas

X(z-d)Fmeashour

A

0

1

2

3

4

5

1 3 5 7 9 11 13 15 17 19 21 23

X(z-d

) (µ

g m

-3)

-80

-40

0

40 Net N

H3 flu

x (n

g m

-2 s

-1)

hour

B

Fig. 2. Averaged diurnal pattern of ambient ammonia concentration (c(z�d ),

in mg m�3) and measured flux (Fmeas, ng m�2 s�1) compiled for time series

from Table 2 with high daytime fluxes and low nighttime fluxes (A) and

time series featuring daytime emission (B).

0

5

10

15

20

25

30

35

40

9 13 17 21 25T (°C)

Xs spring

Xs summer/autumn

Xs spring Г = 3300

Xs summer/autumn Г = 1375

RH < 55 %LW = 0

Xs

= 161500(T + 273)

exp(-10380 (T + 273)–1)[NH4

+]

[H+]

χs

(µ

g m

-3)

Fig. 3. Plot of stomatal compensation point cs against temperature (T ) and

fitted equations for spring (G¼ 3300) and summer/autumn (G¼ 1375).

0

100

200

300

400

55% 65% 75% 85% 95%RH (%)

Rw

(s m

-1)

NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5

A

0

50

100

150

200

250

65% 70% 75% 80% 85% 90% 95% 100%RH (%)

Rw

(s m

-1)

NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5

B

0

50

100

150

200

75% 80% 85% 90% 95% 100%RH (%)

Rw

(s m

-1)

NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5

C

Fig. 4. Relationships between nighttime cuticular resistance (Rw) and relative

humidity (RH) for dry (A); wet (B) and water-saturated (C) canopy across dif-

ferent molar NH3/SO2 ratios (<1; 1e5; >5) and temperature classes

(T> 11 �C, full line; T< 11 �C, dotted line).

429J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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(September 2001A) was modelled within a 25% deviationfrom the measured values (R2¼ 0.30; n¼ 224). With respectto the time series of May 2000 and 2001, the daily averageand daytime flux matched the corresponding modelled fluxbut nighttime depositions were underestimated. The model re-produced the daily variation of time series featuring highnighttime and low daytime fluxes (pattern type Fig. 2A) butmeasured fluxes were generally underestimated. Further dis-crepancies were encountered when simulating the opposite di-urnal pattern with low daytime fluxes due to emission events(pattern type Fig. 2B). Only for August 2001 this diurnal pat-tern was reproduced but average Ft and daytime emissionswere too high. Although stomatal emission (cs> cc) was gen-erally occurring during the daytime, canopy compensationpoints cc were mostly not large enough (cc< c(z�d )) to al-low any stomatal emission to leave the canopy into the atmo-sphere due to high counterbalancing cuticular fluxes Fw (lowvalues of Rw). The ammonia evolved from the stomata could

seldom reach the atmosphere since it was simulated to be re-captured by the leaf cuticle.

3.2.2. Dynamic cceCd modelThe dynamic model mostly outperformed the static model

given the smaller bias and the higher explained variability (Ta-ble 2). Too large bias was found for May 2001 and September2001A especially for nighttime fluxes. Time series of May2000 showed good agreement with modelled daytime, night-time and overall flux, but R2 was reduced to 0.12 (comparedto 0.37 for the static model).

Stomatal fluxes Fs during the growing season were generallyupward (cs> cc; positive Fs; Eq. (7)) with daytime averages upto 40 ng m�2 s�1 (Table 4). Stomatal uptake (cs< cc) occurredwhen cc was raised as a consequence of the high ambient con-centration c(z�d ) (Eq. (14)) and/or when cs decreased due tolow temperatures. This resulted in negative average Fs (April2001, November 1999 and 2001A) or fewer stomatal emissionevents during the runs (July 1999, May 2000) (see Table 4). Sto-matal fluxes were unimportant in magnitude outside the grow-ing season and during rainfall or dew events (high Rs).

Average cuticular fluxes Fd, which could be both modelledupward (cd> cc) as well as downward (cd< cc), were gener-ally downward except for September 2001B (Table 4) forwhich run Kr was set to zero. Generally cd was close to cc

(Table 4) indicating that the canopy emission potential wasclosely related to the cuticular emission potential. Adsorptioncharge Qd averaged 4300e4700 mg m�2 although highervalues over 10 000 mg m�2 were modelled. Chosen pH valueswere kept constant during every run and ranged between 3.7and 5.6. Within the considered NH3/SO2 range, pH valueswere about one unit lower (10 times more acid) compared tothe pH of throughfall water sampled within the same period(Fig. 6). Throughfall pH tended to rise with increasing NH3/SO2 ratio. There were too few data to examine this relation-ship for chosen surface water pH and average NH3/SO2,

0

50

100

65% 75% 85% 95%RH (%)

NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5NH3/SO2< 1 NH3/SO2 = 1-5 NH3/SO2 >5

Fig. 5. Relationships between daytime cuticular resistance (Rw) and relative

humidity (RH) for canopy wetness> 0.75 across different molar NH3/SO2

ratios (<1; 1e5; >5) and temperature classes (T> 15 �C, full line;

T< 15 �C, dotted line).

Table 3

Overview of statistical parameters and explained variability for significant empirical relationships (nonlinear regression in Eq. (17)) between Rw and RH for

different canopy wetness categories and temperature/molar NH3/SO2 sub-categories

Canopy wetness T class (�C) NH3/SO2 n Rw,min� se a� sea R2

Nighttime

Dry canopy <11 <1 477 49.6� 16.8 0.51� 0.21 0.05

<11 1e5 186 56.3� 17.7 0.34� 0.09 0.08

<11 >5 118 37.9� 7.8 0.30� 0.06 0.19

>11 <1 148 30.2� 13.8 0.31� 0.15 0.05

>11 1e5 220 6.3� 3.2 0.14� 0.02 0.14

>11 >5 145 53.9� 28.0 0.22� 0.06 0.11

Wet canopy <11 1e5 29 57.5� 28.5 0.25� 0.10 0.10

Water-saturated canopy <11 <1 475 69.5� 13.5 0.26� 0.04 0.09

>11 <1 319 59.5� 15.3 0.32� 0.15 0.05

>11 1e5 213 12.7� 5.1 0.09� 0.01 0.43

>11 >5 88 70.5� 24.8 0.29� 0.08 0.12

Daytime

LW> 0.75 <15 <1 515 34.0� 6.4 0.36� 0.07 0.06

>15 1e5 154 15.7� 7.0 0.41� 0.20 0.04

>15 >5 142 3.3� 2.1 0.20� 0.07 0.32

a Significance of parameter values Rw,min and a from Eq. (17) were tested using t-test.

430 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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encountered during the 16 individual runs. Especially for therange of higher ratios more data are necessary to elucidatethis relationship. Values of Kr chosen for the different modelruns ranged between 0 (no removal from the leaf surface intothe leaf) and 0.07 (7% of previous adsorption charge is ab-sorbed by the leaf; continuous sink).

According to the magnitude and sign of Fd and Fs the fol-lowing situations could be identified:

(i) No observed canopy emission: stomatal emission out-weighed by cuticular deposition

Stomatal emission episodes were mostly compensated bylarger downward Fd (June 1999, July 1999 and 2000, May2000, October 2001 and February 2000) (Table 4). The adsorp-tion concentration (cd) was continuously lower compared to cc

and fluxes evolved from the capacitor could therefore be pre-cluded. Canopy compensation points cc seldom exceededc(z�d ), preventing that any stomatal emission reached the

Table 4

Daily variability of main component fluxes and model parameters from the dynamic canopy compensation model for daytime and nighttime conditions (see text for

description of model parameters)

Fd (mg m�2 s�1) Fs (mg m�2 s�1) cd (mg m�3) cs (mg m�3) cc (mg m�3) c(z�d ) (mg m�3) Qd (mg m�2)

Daytime

Jun99 �0.227 0.016 0.8 3.7 0.9 4.6 6650

Jul99 �0.321 0.004 4.1 6.2 5.2 10.7 7290

Nov99 �0.017 �0.005 4.3 1.3 3.6 4.5 6130

Feb00 �0.045 0.001 0.5 1.2 0.5 1.2 5160

May00 �0.243 0.004 3.1 5.3 3.5 8.2 9590

Jul00 �0.098 0.028 0.5 4.2 0.6 1.8 3280

Aug00 �0.095 0.028 1.0 5.0 1.1 1.7 4610

Nov00 �0.003 0.002 0.6 1.1 0.5 0.6 630

Apr01 �0.031 �0.006 4.0 3.4 4.0 5.9 1450

May01 �0.084 0.023 7.3 16.4 6.3 8.6 5820

Aug01 �0.038 0.040 0.6 8.6 0.7 0.8 1990

Sep01A �0.050 0.004 1.4 2.3 1.3 2.4 1500

Sep01B 0.002 0.008 1.9 3.6 1.5 1.3 1150

Oct01 �0.146 0.016 0.2 3.4 0.2 1.9 3020

Nov01A �0.005 �0.010 3.9 1.1 3.6 4.7 11 300

Nov01B �0.018 0.002 0.3 1.2 0.3 0.9 5270

Average �0.089 0.010 2.2 4.3 2.1 3.7 4680

Nighttime

Jun99 �0.122 0.002 0.3 2.9 0.4 4.9 5320

Jul99 �0.234 0.002 0.6 4.1 0.7 12.3 4570

Nov99 �0.070 �0.001 2.7 1.1 2.6 6.0 5640

Feb00 �0.035 0.000 0.4 1.1 0.4 0.9 4830

May00 �0.151 0.000 2.7 4.3 2.8 6.9 10 350

Jul00 �0.033 0.001 0.3 3.0 0.3 1.7 2950

Aug00 �0.023 0.005 0.5 3.6 0.6 1.9 5350

Nov00 �0.006 0.000 0.3 1.0 0.3 0.4 580

Apr01 �0.090 0.000 0.9 1.9 1.3 6.0 1070

May01 �0.222 0.004 0.2 8.3 0.2 11.2 5690

Aug01 �0.021 0.006 0.2 5.2 0.2 1.2 2080

Sep01A �0.088 0.000 0.7 1.9 0.9 3.8 1630

Sep01B �0.019 0.003 0.3 2.9 0.4 0.8 1070

Oct01 �0.087 0.002 0.1 2.5 0.2 1.6 2620

Nov01A �0.114 0.000 1.0 0.9 1.0 7.0 10 500

Nov01B �0.014 0.001 0.1 1.1 0.1 0.4 4830

Average �0.083 0.002 0.7 2.9 0.8 4.2 4320

3

4

5

6

7

0 5 10 15 20 25 30 35 40 45Molar NH

3/SO

2

pH

pH throughfallpH water film

Fig. 6. pH of water film (chosen for 16 time series) and pH of throughfall sam-

ples collected during 2e3 weeks sampling exposure intervals versus corre-

sponding molar NH3/SO2 ratio of ambient air.

431J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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atmosphere. Fig. 7 illustrates this for a week in June 1999 withhigh ammonia morning fluxes over�800 ng m�2 s�1 occurringat the start, later decreasing to fluxes of �200 ng m�2 s�1

(Fig. 7A) Generally stomatal emission occurred because cs al-ways exceeded cc. The latter varied between 0 and 5 mg m�3

which was still much lower than c(z�d ), which achievedpeak values exceeding 20 mg m�3 (Fig. 7B). High fluxes inthe beginning of the week were caused by the large diffusion

gradient c(z�d ) [ cc (Eq. (5)), which guaranteed a strong cu-ticular flux, which recaptured any stomatal emission.

(ii) Observed canopy emission: stomatal emission partlyoutweighed by cuticular deposition

In some cases sustained stomatal emission events due toelevated stomatal compensation points cs (high temperatures),

-1

-0.8

-0.6

-0.4

-0.2

0 24-06-99 16:30

25-06-99 16:30

26-06-99 16:30

27-06-99 16:30

28-06-99 16:30

29-06-99 16:30

30-06-99 16:30

1-07-99 16:30

Flu

x (µ

g m

-2 s

-1)

A

0

5

10

15

20

25

X (µ

g m

-3)

B

0

5

10

15

20

25

30

24/0

6/19

99 1

6:30

25/0

6/19

99 1

6:30

26/0

6/19

99 1

6:30

27/0

6/19

99 1

6:30

28/0

6/19

99 1

6:30

29/0

6/19

99 1

6:30

30/0

6/19

99 1

6:30

1/07

/199

9 16

:30

T (°C

) ; R

(m

m)

0

10

20

30

40

50

60

70

80

90

100

LW

; R

H (%

)

RTRHLW

C

FmeasFt = Fd + FsFdFs

X(z-d)

Xd

XcXs

Fig. 7. Measured (Fmeas) and modelled ammonia fluxes (Ft) divided in adsorption (Fd) and stomatal fluxes (Fs) (A) in relation to ambient concentrations (c(z�d )),

stomatal concentration (cs), adsorption concentration (cd) and canopy compensation point (cc) (B) for June 1999. Course of environmental variables temperature

(T ), leaf wetness (LW), relative humidity (RH) and rainfall (R) (C) for June 1999.

432 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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low ambient ammonia concentrations c(z�d ) and low daytimeRs prevailed (August 2000 and 2001). This daytime emissioncould not fully be re-absorbed through Fd as in previous cases.An example is given for August 2001 during which averagedaytime temperatures steadily rose towards 27 �C (Fig. 8C)followed by a temperature dependent increase of cs to

12 mg m�3 (Fig. 8B). This led to high ammonia losses throughthe stomata (>60 ng m�2 s�1) since cs was by far exceedingcc, which enlarged Fs (Eq. (7), Fig. 8A and B). Cuticularadsorption was not strong enough in magnitude (low ambientammonia levels c(z�d )< 1 mg m�3; dry non-acidic surface)to counteract the stomatal emission which led to a net daytime

-0.08

-0.04

0.00

0.04

0.08

17/08/2001 18:00

18/08/2001 6:00

18/08/2001 18:00

19/08/2001 6:00

19/08/2001 18:00

20/08/2001 6:00

20/08/2001 18:00

21/08/2001 6:00

21/08/2001 18:00

22/08/2001 6:00

23/08/2001 6:00

23/08/2001 18:00

Flu

x (µ

g m

-2 s

-1)

A

0

4

8

12

X (µ

g m

-3)

X(z-d)B

0

5

10

15

20

25

30

17-0

8-01

18:

00

18-0

8-01

6:0

0

18-0

8-01

18:

00

19-0

8-01

6:0

0

19-0

8-01

18:

00

20-0

8-01

6:0

0

20-0

8-01

18:

00

21-0

8-01

6:0

0

21-0

8-01

18:

00

22-0

8-01

6:0

0

22-0

8-01

18:

00

23-0

8-01

6:0

0

23-0

8-01

18:

00

T (°C

) ; R

(m

m)

0

10

20

30

40

50

60

70

80

90

100

LW

; R

H (%

)

RTRHLW

C

22/08/2001 18:00

Xd

XcXs

FmeasFt = Fd + FsFdFs

Fig. 8. Measured (Fmeas) and modelled ammonia fluxes (Ft) divided in adsorption (Fd) and stomatal fluxes (Fs) (A) in relation to ambient concentrations (c(z�d )),

stomatal concentration (cs), adsorption concentration (cd) and canopy compensation point (cc) (B) for August 2001. Course of environmental variables temper-

ature (T ), leaf wetness (LW), relative humidity (RH) and rainfall (R) (C) for August 2001.

433J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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canopy loss of ammonia (cc> c(z�d ); Ft> 0) on at least sixconsecutive days.

(iii) Observed canopy emission: desorption from the cuticlelayer

Desorption often occurred when ammonia trapped in waterfilms was volatilized from evaporating water films. During the

observations made in April 2001, November 1999, 2000 and2001, volatilization of previously accumulated ammonia duringdew formation occurred when ambient concentrations weredropping (due to increased mixing) and water film evaporatedleading to higher cd compared to cc. Observations made inNovember 2001 (Fig. 9) illustrated how modelled flux Ft

(almost coinciding with Fd since Fs was small and negative)yielded three brief emission episodes (Fig. 9A). Rise of the cd

-0.5

-0.25

0

0.25

0.5

16-11-01 13:30

17-11-01 1:30

17-11-01 13:30

18-11-01 1:30

18-11-01 13:30

19-11-01 1:30

19-11-01 13:30

Flu

x (µ

g m

-2 s

-1)

FmeasFt = Fd + FsFdFs

A

0

4

8

12

16

X (µ

g m

-3)

X(z-d)XdXcXs

B

0123456789

10

16-1

1-01

13:

30

17-1

1-01

1:3

0

17-1

1-01

13:

30

18-1

1-01

1:3

0

18-1

1-01

13:

30

19-1

1-01

1:3

0

19-1

1-01

13:

30

T (°C

) ; R

(m

m)

0102030405060708090100

LW

; R

H (%

)

TRHLW

C

Fig. 9. Ammonia measured (Fmeas) and modelled fluxes (Ft) divided in adsorption (Fd) and stomatal fluxes (Fs) (A) in relation to ambient concentrations (c(z�d )),

stomatal concentration (cs), adsorption concentration (cd) and canopy compensation point (cc) (B) for November 2001. Course of environmental variables tem-

perature (T ), leaf wetness (LW) and relative humidity (RH) (C) for November 2001.

434 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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(which in turn resulted in higher cc) on 17, 18 and 19/11 follow-ing the onset of the desiccation of the cuticular surface (at 9 h30 min, 11 h and 11 h 30 min, respectively) (Fig. 9B and C)continued until the declining ambient concentration c(z�d )was exceeded (at 10 h, 13 h and 12 h 30 min, respectively)from which point the cuticular desorption of ammonia couldtake off (cd> cc> c(z�d )). The release of previously dis-solved [NH4

þ] led to a decrease of cd (which is in equilibriumwith the dissolved ammonia/ammonium in the water films)and adsorption charge Qd until the cd had dropped to the levelof c(z�d ) again (18 h, 17 h and 16 h, respectively). From thispoint onwards, cuticular adsorption resumed and the capacitorcould start to accumulate ammonia again (cd< cc< c(z�d ),Qd rising again). This pattern was also observed for the othertime series. During dry events, cuticular desorption could alsoenhance stomatal emissions as observed for September 2001Band May 2001 (Table 4). Due to the presence of stomatal emis-sion, canopy emission was sustained longer than in case onlycuticular desorption would be involved.

4. Discussion

The bidirectional exchange of ammonia at a nitrogen-saturated forest was studied using a static and a dynamiccompensation point model. These bidirectional models wereapplied to 16 selected time series of different flux magnitude,which could be characterized by a contrasting diurnal coursein flux. On the one hand, there was a deposition pattern, illus-trated in Fig. 2A, with higher deposition during the daytimecompared to nighttime. On the other hand, a bidirectionalexchange pattern emerged with a marked daytime emission(shown in Fig. 2B).

Although parameterisations carried out for the static modelattempted to consider both the impact of micro and macro-scopic wetness as well as codeposition effects, the static com-pensation point model was found inept to model most of theselected time series. Measured fluxes from series resemblingthe diurnal pattern from Fig. 2A were greatly underestimated(cuticular fluxes too low). The static model followed, however,its diurnal deposition variation, which could be attributed tothe fact that our Rw parameterisation to RH resulted in lowerRw during the daytime. This was supported by our measure-ments; median daytime Rw (12 s m�1) was lower than night-time Rw which attained median values up to 60 (dry canopy)and 28 s m�1 (wet and water-saturated canopy). The latterwas also found by Wyers and Erisman (1998) for a Douglasfir forest in The Netherlands, which the authors attributed toincreased humidity around transpiring stomata, favouring day-time uptake. The static model completely failed to simulatethe daytime emission fluxes (type Fig. 2B) as canopy compen-sation points (cc) were too low compared to ambient levelsc(z�d ) to allow any stomatal emission to reach the atmosphere.All stomatal emission fluxes were recaptured within thecuticular deposition flux. This finding was in contrast withmodel results for semi-natural grasslands (Horvath et al.,2005; Spindler et al., 2001) and moorlands (Flechard et al.,1999; Nemitz et al., 2004), which indicated that cceRw

models were also able to predict bidirectional fluxes over un-fertilized vegetation. The poor performance of the static modelat our site could be largely explained by the lack of robust re-lationships found between Rw and RH. Although regressionparameters listed in Table 3 were statistically significant, therewas a lot of scatter in Rc, which is obtained as a residual valuefrom Eq. (4), which terms (deposition velocity and turbulentresistances) suffer considerable scatter. The applicability ofthe latter equation under conditions where a substantial can-opy compensation point is encountered could also be ques-tioned. The presence of a surface concentration will lead toa clear dependence of Rc on ammonia levels, which shouldbe included in the estimation of Rc. Another reason for theweak relationship between Rc and RH might be the assumptionthat nighttime Rc equates with Rw. During the measuring cam-paign, there was abundant rainfall (900e1000 mm yr�1) andnighttime stomatal opening due to the absence of water stresscould have occurred during the growing season.

The dynamic model was found to be more adequate in re-producing the measured fluxes. It was especially successful inreproducing the daytime emission originating from stomata orevaporating surfaces. The complex model also simulated bet-ter the cuticular flux because it included a capacitance witha dynamic behaviour of cuticular ad/de-sorption dependingon previous accumulated ammonia fluxes and chemical influ-ences (Sutton et al., 1998). It was not possible to allow fordesorption or deposition history when making use of the staticmodel whose Rw parameterisations depended on instantaneousconditions; therefore, they were too simplistic to simulate thedynamic exchange mechanism.

The cuticular flux was found to be the dominating compo-nent of the net flux. Adsorption charge averaged 4300e4700 mg m�2 although higher values up to 10 000 mg m�2

were modelled. Wyers and Erisman (1998) calculated a yearlyaverage accumulated ammonia flux of 14 and 5 mg m�2 overa Douglas fir forest during two successive measuring years.The efficient leaf surface deposition is the driving force for av-erage net fluxes up to �0.1 mg m�2 s�1 at forests situated inammonia-polluted regions like Speulderbos (Wyers et al.,1995) or Brasschaat (Neirynck et al., 2005). Several studieson semi-natural vegetation confirmed the finding of leaf sur-face deposition short-circuiting the stomatal compensationpoint (Flechard et al., 1999; Nemitz et al., 2004; Suttonet al., 1993b). The larger part of ammonia evolved from thestomata was found to be redeposited to the leaf surfaces.

Stomatal emission was found to be sustained almost contin-uously across the growing season. Stomatal emissions weremostly recaptured by (wetted) leaf cuticles, which provided ef-ficient sinks (Nemitz et al., 2004). Only when cuticular fluxeswere low, stomatal emissions could effectively reach the atmo-sphere (August 2000 and 2001). To achieve this, conditionswith low ammonia levels and warm, dry conditions were re-quired (dry canopy surfaces with low cuticular fluxes, highstomatal compensation points with low Rs). Stomatal emissionfluxes could exceed 60 ng m�2 s�1 on warm days and weremodelled using G factors of 3300 and 1375 in spring and sum-mer/autumn, respectively (Fig. 3). The seasonal differences in

435J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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the G factor might be related to changes in assimilation or bio-chemical processes (related to retranslocation of nutrients, pol-lination, formation of cones and new foliage.) across theyear. Our values were high compared to those found forsemi-natural vegetation (Flechard et al., 1999; Milford et al.,2001) although Wyers and Erisman (1998) used a G factorof 8500 (apoplastic pH of 7 and apoplastic [NH4

þ] of850 mM) to simulate stomatal emissions for a Douglas firforest subjected to ammonia bearing air masses in TheNetherlands. Our corresponding stomatal compensation pointconcentrations ranged between 3.0 and 25.1 mg m�3 (T range:8.3e25.9 �C) during spring and between 1.5 and 18.9 mg m�3

(T range: 9.5e31.2 �C) during summer/autumn. Gravenhorstand Breiding (1990) determined cs of 0.3e2.2 mg m�3 (Trange: 10e27 �C; G¼ 310) for conifers during a chamber ex-periment while Langford and Fehsenfeld (1992) found a cs of0.6 mg m�3 at 20 �C (G¼ 155) for a montaneesubalpine forestin the Colorado mountains (USA). In healthy leaves there isa balance between NH4 production and consumption regulat-ing ammonium in the apoplast. When nitrogen is depositedin excess and ammonium cannot longer be assimilated, a largercs is obtained (Schjoerring et al., 1998). This was especiallythe case for our forest site where nitrogen concentrations’levels in the half-year’s pine needles amounted to 2.5% andsymptoms of nitrogen saturation (nitrate leaching, NO emis-sion) were obvious (Neirynck et al., 2002, 2007).

Besides the occurrence of prolonged net-emission eventsdue to stomatal emissions, there were also events of brief cu-ticular desorptions, which were initiated by evaporative effectsafter dew formation. Evaporating leaf water layers in themorning led to an increase of ammonia gas adsorption concen-tration (cd) in equilibrium with the dissolved [NH4

þ] in the wa-ter layers. When cd (wcc) exceeded the dropping ambientconcentrations c(z�d ) due to starting morning turbulence,desorption of ammonia was triggered which led, in turn, toa drop of cd above the evaporating water film. When c(z�d )and cd were back again in equilibrium, leaf surface depositioncould resume. Emission episodes occurring in April orNovember originated solely from cuticular release given thelower stomatal activity or the presence of stomatal uptakedue to low cs (low temperatures). The nature of the cuticularemissions contrasted with those originating from stomata(Sutton et al., 1998). Whereas cuticular desorptions were con-fined to sudden peaks related to short periods of water layerevaporation mainly in the morning (Sutton et al., 1995),stomatal emissions could be sustained during extended dryperiods (Nemitz et al., 2004; Sutton et al., 1998). The daily se-quence of emission peaks originating from the two differentammonia sources probably occurred separated in time, whichcould be clearly observed from the daily variability in fluxes,shown in Fig. 2A and B. The first local peak (9e10 a.m.) co-incided with ammonia desorptions from the surface (evapora-tion of water films), while the larger local flux peak at noon,early afternoon (12 a.m., 2 p.m.), was mainly related to emis-sion from the apoplast through the stomata.

The occurrence of cuticular desorption was recognized asa possible cause of canopy emission in semi-natural

vegetation. It was often associated with high ammonia concen-trations and transition from a wet to dry canopy (Andersenet al., 1999; Nemitz et al., 2004; Wyers and Erisman, 1998).High ammonia levels and fluxes led to accumulation of ammo-nia/ammonium on water layers of the leaf surface, forminga net potential for ammonia when evaporation started. Suttonet al. (1995), however, suggested from measurements over ex-tremely clean upland moorland that cuticular desorption ofammonia was also possible at low concentrations.

The pH of the surface water film from our 16 individualmodel runs was empirically found to range between 3.7 and5.6. This was roughly 10 times more acid than the aciditymeasured in biweekly throughfall samples taken during thesame measuring campaign. For throughfall a distinct relation-ship between NH3/SO2 ratio and pH existed (Fig. 6). It was,however, premature to establish such a relationship for thederived pH of surface water and the molar ratio. It is also con-ceivable that other compounds (base cations, HNO3, acidicaerosols.) contribute to the acidity of the surface water. Tosimulate Cd, an arbitrary value of cuticular pH of 4.5 basedon dew sample analysis was taken by Sutton et al. (1998).Flechard et al. (1999) numerically calculated pH values usingmodelled aqueous chemistry. Median leaf surface pH of alltheir model runs was 3.57 and remained at all levels below5 units.

5. Conclusions

Leaf surface deposition at our site has been demonstrated tobe the driving factor for net deposition. To achieve high leafsurface deposition, ideal conditions regarding wetness, acidityand ambient ammonia concentrations have to be met. Wet can-opies allow the fast deposition of large ammonia amounts ontothe canopy surface and at the same time they inhibit stomatalemissions given the cooler and lower radiation conditions in-herent to wet canopies (Nemitz et al., 2004). In our conditions,the cuticular flux could be best approached using a dynamicalcanopy compensation point model developed by Sutton et al.(1998). It took into account previously deposited ammoniafluxes, which determined the potential for forthcoming fluxesto accumulate on the leaf surface. The static model, on thecontrary, did not work out because Rw parameterisationswere not robust enough and were unsuitable to cope withthe ammonia dependent leaf surface dynamics. The dynamicmodel could additionally explain the mechanism behind cutic-ular desorption found at our site. Cuticular emission could oc-cur when non-acidic surface water or dew layers, saturatedwith ammonia, started to evaporate. These conditions couldrather be found during the growing season (April till Novem-ber). During the winter period, water layers are expected to bemore acidic (just like throughfall water) and canopies oftenmore saturated with water. In order to improve the modellingefforts of the bidirectional cuticular flux, reliable estimates ofcanopy area water film thickness and its containing aciditywith respect to changing meteorological conditions are there-fore required. Measurements of surface water acidity and can-opy wetness conducted by well-calibrated instrumentation

436 J. Neirynck, R. Ceulemans / Environmental Pollution 154 (2008) 424e438

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should be extended along the (sub-)canopy surface. In thisstudy pH of surface water layers was inferred during optimiza-tion but acidity should be preferably determined on dew sam-ples during future measurements.

In drier and warmer conditions combined with lower ambi-ent ammonia levels, stomatal emissions during daytime mayoutweigh the cuticular flux and finally reach the atmosphere.These stomatal emissions resulted from raised G due tolong-term atmospheric N deposition at our site. Uptake of am-monia through stomata hardly occurred during the growing pe-riod. As such, stomatal uptake was effectively inhibited asa feedback response to the high N loadings over the past de-cades. Evidence was found that the emission potential fromthe stomata might vary across the season (different G valuesfor spring compared to summer/autumn). Future measure-ments must further examine possible variations in physiologi-cal control on stomatal exchange. Bioassays of apoplasticsolutions (Husted et al., 2000) developed for tree species couldbe helpful in elucidating this. They should be conducted ona temporal scale with a sufficient precision to cover and ex-plain the seasonal and diurnal variations in the molar ammo-nium/hydrogen ion ratio.

Acknowledgements

Financial support for the purchase of the AMANDA monitorand for the employment of Yves Buidin was provided by theVLINA (Flemish Impulse Program on Nature Development).We also thank Fred Kockelbergh (UA) for logistic support atthe site. This project was performed under the authority ofthe Flemish minister of the Environment and was instigatedby Jos Van Slycken, Peter Roskams and Stijn Overloop.

This paper results from the ESF-FWF Conference onReduced Nitrogen in Ecology and the Environment, organizedin the Universitatszentrum Obergurgl, Austria on October14e18 2006 (http://www.esf.org/conferences/lc06203). Thisconference was organised by the European Science Foundation(ESF) in partnership with the Fonds zur Forderung der wissen-schaftlichen Forschung in Osterreich (FWF) and the Leopold-Franzens-Universitat Innsbruck (LFUI). We also acknowledgethe support of the COST Action 729, and the ESF programNitrogen in Europe (NinE).

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