Plant Biology ISSN 1435-8603

REVIEW ARTICLE

Why and how terrestrial plants exchange gases with air
S. Cieslik1, K. Omasa2 & E. Paoletti3
1 Joint Research Centre, via Enrico Fesmi 2749, Ispra, Italy
2 University of Tokyo, 1-1-1 Yayoi, Bunkyo-Ku, Tokyo, Japan
3 Istituto Protezione delle Piante, Centro Nazionale delle Ricerche, Sesto Fiorentino, Italy

Keywords
Air pollutants; carbon dioxide; photosynthesis;
stomatal physiology; volatile organic
compounds; water vapour.
Correspondence
Stanislaw Cieslik, Joint Research Centre – IES,
via E. Fermi 2749, Ispra VA 21027, Italy.
E-mail: stanislaw.cieslik@jrc.it

ABSTRACTThis work is intended as a review of gas exchange processes between theatmosphere and the terrestrial vegetation, which have been known for morethan two centuries since the discovery of photosynthesis. The physical andbiological mechanisms of exchange of carbon dioxide, water vapour, volatileorganic compounds emitted by plants and air pollutants taken up by them,is critically reviewed. The role of stomatal physiology is emphasised, as it
controls most of these processes. The techniques used for measurement ofgas exchange fluxes between the atmosphere and vegetation are outlined.

EditorM. Tausz
Conflicts of interest
The authors declare no conflicts of interest.
Received: 14 April 2009; Accepted: 21
July 2009
doi:10.1111/j.1438-8677.2009.00262.x

INTRODUCTION
The Earth’s atmosphere and the vegetation layer covering
its surface (the phytosphere) are not isolated from eachother. A number of physical and chemical processes occur
at the atmosphere ⁄ phytosphere (or more simply, air ⁄plant) interface, and these profoundly influence both airand plants. As a first example, the current atmosphericchemical composition has been completely modified inpast geological times due to the emergence of photosynthetic vegetation on the continents about three billion
years ago (Levine 1985). The primitive Earth’s atmosphere, the composition of which was mainly determinedby outgassing of the primitive Earth, was probably dominated by water vapour (H2O), carbon dioxide (CO2),
molecular nitrogen (N2), some methane (CH4) andammonia (NH3). Molecular oxygen (O2) was present only
as a trace gas, and was formed by photolysis of CO2 andH2O. When photosynthetic plants spread out over thecontinents, a massive release of O2 took place, favouring
the development of respiring animals. A steady state was24

then reached, with a mean O2 molar fraction of about
21%.
Photosynthesis is a biochemical process that has been
known for more than two centuries, and was first discovered in Priestley’s experiment (1771) and then studied by
Lavoisier. The Dutch physiologist Moleschott (1851)
rightly wrote: ‘‘The field on which wheat grows feeds us.
But when we cross a forest, we feed it with the CO2 weexhale.’’ This sentence summarizes in a concise way theenvironmental and biogeochemical equilibrium existing
between photosynthetic plants and respiring animals,
which continuously exchange O2 and CO2 with eachother through the atmosphere. So, it is not exaggerated to
say that plants, but also animals, profoundly influence thecomposition of the atmosphere. However, photosynthesis
and respiration are far from being the only gas exchange
processes between air and vegetation. Water vapour,which is an important atmospheric chemical, is continuously released to air by plants through evapotranspiration.
This process has been described by Penman (1948), Monteith (1981) and many others. The mass fractions of water

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

Cieslik, Omasa & Paoletti

vapour in the atmosphere are highly variable according toplace and time, ranging roughly between 0 and 0.04,
depending on a number of environmental and meteorological factors. The water vapour mass fraction (or specific humidity) has an essential influence on weather andclimate by participating in the hydrological cycle.
A number of other gaseous substances are exchanged
between air and plants in both directions: from plant toair (hereafter referred to as upward) and vice versa(downward). An array of volatile organic compounds(VOC), as byproducts of metabolism, are released to air
by plants in significant amounts, estimated at 1200 Tg ofcarbon per year (Guenther et al. 1995). Among these, isoprene (C5H8) is by far the most important, as its global
emission rate probably exceeds 500 TgÆyear)1 (Wiedinmyer et al. 2006), outweighing the sum of all VOCs emitted
through human activities around the world (ranging from
130 to 160 TgÆy)1; Butler et al. 2008).
Besides photosynthetic vegetation, other organisms soil
microorganisms or marine algae like emit substances likemethane (CH4), nitrous oxide (N2O) and dimethylsulfide(DMS, or CH3-S-CH3). Methane, first identified in air byMigeotte (1948), is mostly emitted from the soil in anaerobic conditions, as in rice paddies; it is also released
from faecal matter produced by livestock. Methane is a
powerful greenhouse gas. Since both worldwide rice production and world livestock are directly related to humanpopulation, the increase in CH4 concentration in air is
exponential (Khalil et al. 2007). DMS, first discovered inocean waters by Lovelock et al. (1972), is produced bymarine algae as a byproduct of their metabolism, andparticipates in the sulphur cycle, contributing to the formation of sulphate aerosols, which have consequences on
the atmospheric radiation balance and hence on climate.
The substances mentioned in this paragraph are notstrictly speaking emitted by photosynthetic terrestrial vegetation, and thus will not be treated in this review, butthey deserve to be mentioned because of their role in the
global climate system.
Chemical atmosphere ⁄ vegetation exchange can also
occur from air to plant, mainly consisting of the uptakeof CO2 (Jones 1992) and various air pollutants (Omasa
et al. 2002a) by plants. The main pollutants that can penetrate plant tissues are ozone (O3), nitrogen oxides(NOx), ammonia (NH3) and sulphur dioxide (SO2).
Deposition of aerosol particles can also play an indirectrole in air ⁄ plant gas exchange processes, especially when
hygroscopic salts are deposited on leaves and absorbed bydeliquescence water vapour evaporated from the stomata,thus modifying the stomatal aperture (Burkhardt et al.
2001a,b; Eichert & Burkhardt 2001). Only gaseous
exchange, however, is treated in this review.
From a more general perspective, both emission anduptake of chemical substances from and into vegetation
can be seen as a part of global environmental processes,
described as global environmental change (Graedel &Crutzen 1993). This includes not only climate change,
which involves physical variables such as temperature,

Gas exchange of terrestrial plants

wind, humidity, precipitation regime, etc., but also thechange in chemical composition of the atmosphere, nowadays often called ‘‘chemical climate’’. A synthesis of thischange at European scale can be found in Slanina (1997),
and at global scale in Brasseur et al. (2003). But see also
the IPCC reports (e.g. Climate Change 2007).
The exchange of gases between air and terrestrial vegetation is part of a vaster system known as global biogeochemical cycling, in which chemical substances areexchanged between the different reservoirs present on planet Earth: atmosphere, oceans, biosphere and lithosphere.
Molecular oxygen, water, CO2 and many other substances
are present in these reservoirs in variable quantities(expressed e.g. in mol) and are transferred from one toanother with characteristic times (days, years, millions ofyears) and fluxes (mol per unit time, the area being integrated over the whole Earth surface). Global cycling has
been extensively studied, both through modelling andobservations (Bolin & Cook 1983; Fung et al. 1991; Keeling et al. 1993; Siegenthaler & Sarmiento 1993; Bender
et al. 1998). In these processes, oxygen plays a crucial role,both in molecular form (as O2) and as an element entering
into the composition of many substances (water, CO2, O3,
oxygenated organics). The main scope of the present
review is not, however, a synthesis of global cycling, about
which abundant literature can be found (Wigley & Schimel
2000; Jorgensen & Fath 2008; Miller 2008). Gas exchange
between atmosphere and terrestrial plants, where this work
is focused on is a subsystem of global cycling.
THE ROLE OF STOMATA
Stomata are microscopic pores present on the surface ofleaves, constituting organs that permit gaseous substances
to penetrate or leave plant tissues. The stomatal apertureis physiologically regulated in such a way as to control
the quantity of gaseous matter transiting through them
(Meidner & Mansfield 1968; Jarvis & Mansfield 1981; Zeiger et al. 1987; Omasa et al. 2002a; Shimazaki et al.
2008). Environmental conditions such as light, temperature, humidity, soil water content, CO2 and air pollutant
concentrations influence stomatal regulation, directly or
indirectly. Since evaporation of liquid water uses heat, it
causes cooling. If stomata are more open, more water is
evaporated, resulting in lowering of the temperature.
Opening the stomata is thus used by the plant to reduce
foliar temperature to protect leaves from excessive heating
due to the absorption of sunlight. This constitutes thethermal regulation mechanism. When the intercellularconcentrations of CO2 are sufficient for optimal photosynthesis, stomata close in order to save water (hydrological regulation). Stomatal closure typically occurs indrought conditions. A conflict between the need toreduce foliar temperature by opening the stomata and theneed to reduce water use by closing them may appear inconditions of excessive drought and heat. In such cases,
stomata tend to close to save water, but thermal regulation is inhibited and the leaves become too hot. The plant

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

25Gas exchange of terrestrial plants

Cieslik, Omasa & Paolettithen becomes stressed and, if conditions worsen, this maylead to the death of leaves.
Air pollutants may take advantage of the stomatal aperture to enter leaves. The more stomata are open, thegreater are the quantities of air pollutants entering planttissues. The role of stomata is described in great detail in
Zeiger et al. (1987). The leaf-scale stomatal conductancefor water vapour (gsw) can be estimated using the multiplicative model developed by Jarvis (1976) and further
developed by Emberson et al. (2000):
gsw ¼ gmax  fage  flight  ftemp  fVPD  fSMD

ð1Þ

where the maximum stomatal conductance of a plant species (gmax) is modified as a function of plant development(fage), light availability (flight), air temperature (ftemp),
vapour pressure deficit (fVPD) and soil moisture deficit(fSMD). All f functions range between 0 and 1 (LRTAPConvention 2004). A microscopic picture of stomata isshown in Fig. 1.
PHOTOSYNTHESIS AND RESPIRATION
Photosynthesis and respiration provide an important
contribution to exchange processes between atmosphereand vegetation (Monteith & Unsworth 1990; Jones
1992). They involve three chemical species: O2, CO2
and H2O. These processes have been known for a longtime, as noted in the introduction, and play an essential role not only in plant physiology, as they ensure
the survival of plants, but as regulators of atmosphericcomposition. For example, if vegetal biomass dramatically decreased as a consequence of a badly managed
environment, the atmospheric concentration of O2
would decrease with unpredictable consequences for thereign of animals and mankind. Vegetation also absorbs
CO2 and tends to counteract the increase of this gas in
the atmosphere.
TRANSPIRATIONThe release of water vapour through stomata criticallydepends on stomatal aperture, which generally undergoesa daily cycle, opening after sunrise, decreasing in theafternoon, and having a tendency to remain closed during
the night. According to some recent work, however,stomata might remain open during the night in particular conditions (Dawson et al. 2007). This cycle is modulated by environmental conditions, like water supply,
intensity of sunlight and wind speed. When the latter isstrong, stomata close in reaction to the stress that has
appeared.
Extending the theory introduced by Penman (1948) to
describe evapotranspiration, Monteith (1981) used theresistance analogy to parameterise the role of surface elements that are responsible for this process by introducing
the surface resistance rs expressed in s m)1. When vegetation completely covers the surface, the surface resistanceis equal to the stomatal resistance, because the entire
water vapour flux uses the stomatal pathway. The quantity of water vapour evaporated to the atmosphere perunit area and time is then expressed by the Penman–
Monteith (PM) equation, where both water vapour flux
and stomatal resistance appear. The PM equation is
widely used in the field of agrometeorology. Inverting theequation permits the calculation of the stomatal resistancefor evaporation if all other parameters are known. The
PM equation contains parameters such as measured radiative and ground heat fluxes, temperature and humidity,
and other quantities appearing in the equation (aerodynamic and laminar resistances) are accessible throughparameterisations (Hicks et al. 1987; Garland et al. 1988;
Massman 1993).
As far as chemical exchange between air and vegetationis concerned, the PM approach is very useful as the stomatal resistance for water vapour can be used to deduce thestomatal resistances for other chemical substances penetrating or leaving the stomata. Subsequently the fluxes ofthese substances through the stomata can be obtained.
This can be done since stomatal resistances for different
gases, i.e. the resistances against the diffusive transfer ofthese gases through the stomatal cavity are proportional toeach other because the fluxes are laminar inside the stomatal cavity. Hence, the fluxes obey the laws of molecular
diffusion and are characterised by a diffusive coefficient,which is constant for a given gas, but its value depends on
the nature of the gas. The resistance against diffusivetransfer is defined by

Fig. 1. Microscope view of stomata (arrow)of Castanea sativa (left) and Pinus halepensis(right). White bar = 100 lm.

26

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

Cieslik, Omasa & Paoletti

Gas exchange of terrestrial plants

r

Zz2
z1

dz
;
Di

ð2Þ

where z is a spatial coordinate of the system where thediffusion process occurs, and Di is the molecular diffusion
coefficient for the gaseous i-labelled substance. Since Di isindependent from any space coordinate but depends on
the nature of the diffusing substance only, we can easily
integrate equation (2) over the spatial coordinate, assuming a spherical shape for the stomatal cavity. We thus
obtain a simple expression for the stomatal resistance forgaseous substance i
rs ¼

z2  z1;Dið3Þ

where we see that resistances are inversely proportional tomolecular diffusion coefficients. Thus, if we want to know
the stomatal resistance for a substance like O3, we canrelate it to the stomatal resistance for water vapour
through the proportion
rO2
DH2 O
¼
rH2 O
DO3

ð4Þ

We can see from the above developments that knowledgeof the stomatal resistance for water vapour, e.g. throughthe application of the PM approach, is essential for studying the transfer of any gaseous substance through the stomata.
EMISSION OF VOCs
Volatile organic compounds (VOCs) constitute animportant group of substances released by plants to theatmosphere. Emission of VOC species like essential oils
or leaf oils has been known for a long time (Guenther
1949; Simonsen 1953). Rasmussen (1970) establishedthat isoprene (C5H8), which is emitted by many plant
species worldwide, is produced in a biochemical process
and is not part of the composition of leaves. This compound plays an important role in atmospheric chemistry
as it participates in a number of reactions producing O3(Trainer et al. 1987; Jacob & Wofsy 1988). It reacts with
the OH radical, reducing the oxidising capacity of theatmosphere (Ehhalt et al. 1991) and increasing its‘‘cleaning’’ capacity for air pollutants. Other VOC
species are mono- and sesquiterpenes, such as a- andb-pinene, camphene, D-3 carene, sabinene, limonene,a- and b-phellandrene, thuyene and myrcene. Plants
also emit alkanes (n-hexane), alkenes (ethylene), arenes(toluene), aldehydes (formaldehyde, acetaldehyde, etc.),
ketones (acetone, camphor, 2-methyl-5-heptene-2-one,butanone), ethers (1,8-cineole), alcohols (methanol, linalool) and carboxylic acids (formic, acetic). Overviews ofworldwide VOC emissions from vegetation and their rolein the global atmospheric system can be found in

Brasseur et al. (2003), Wiedinmyer et al. (2004) and
Loreto et al. (2008).
Biogenically emitted VOCs are byproducts of physiological activity. Not all of their production and emission
mechanisms are fully explained, and they can differ considerably from each other. Some of these substances aresynthesised inside the chloroplasts and related to photosynthesis; while others are produced as defences against
stressors. Decaying and drying vegetation also produces
VOCs. Plant growth hormones and floral scents can also
be emitted (Hewitt 1999). The emission fluxes depend
only partly on stomatal aperture, but also on the rates ofsynthesis of the substance emitted, which, in turn, depend
on availability of the precursors.
Production of isoprene inside the leaves may play aprotective role against the damaging effect of drought(Sharkey & Loreto 1993), heat (Loreto & Sharkey 1990)
and O3 (Loreto & Velikova 2001).
Emission rates of isoprenoids (isoprene and monoterpenes) from leaves are functions of both sunlight intensity
and temperature, as shown e.g. by Guenther et al. (1991,
1993). These authors made use of systems called cuvettes
or enclosures in which portions (leaves or branches) ofplants were confined in order to directly measureamounts of emitted substances. These measurements led
to the development of parameterisations that were subsequently used in modelling (Thunis & Cuvelier 2000).
UPTAKE OF AIR POLLUTANTS
It has been known for more than 30 years that air pollutants can penetrate plant tissues and damage them(Omasa et al. 2002a). The mechanism of stomatal uptakeof air pollutants was first studied by O’Dell et al. (1977),
as a molecular diffusion process inside the stomatal cavity. Subsequent work (Omasa et al. 2000, 2002a,b) demonstrated that pollutant uptake is not simply controlled
by this diffusive process but also by leaf metabolism. Pollutant solubility in water does not seem to play an important role. Other authors, like Pasqualini et al. (2002),
Grulke et al. (2007) and Fares et al. (2008), also studied
stomatal uptake experimentally, as explained later.
Kerstiens & Lendzian (1989) and Van Hove et al.
(1999) showed that the penetration of most pollutants
through the cuticle can be considered as negligible since
the cuticle is covered by waxes that constitute a barrier
against stressors. Among air pollutants, O3 is now recognised as responsible for most of the damage to vegetation.
Damage by O3 to agricultural crops has been estimated inmany modelling studies (e.g. Legge et al. 1995; Krupa
et al. 1998; Simpson et al. 2007) and is very important at
global scale (Van Dingenen et al. 2009). The role of stomata in favouring O3 uptake by leaves is illustrated inFig. 2, showing a microscope view of cells subjected to O3
damage. This damage is visualised by a dye reacting withhydrogen peroxide (H2O2) molecules formed after theoxidation processes initiated by O3 (Faoro & Iriti 2009).
The damage is visible on cells surrounding the stomata.

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

27Gas exchange of terrestrial plants

Cieslik, Omasa & Paolettiand many others. The flux of NH3 is bidirectional, so thata compensation point exists. Plants have very different
responses to NH3, and the problem becomes more complicated by the very inhomogeneous distribution ofconcentrations of this species in air. Strong concentrations are observed in the case of presence of farms anduse of fertilisers (Mattsson et al. 2009). Phytotoxic concentrations of NOx and NH3 occur only very close to
their emission sources (Bytnerowicz et al. 1998).
FLUXES AND METHODS OF DETERMINATION

Fig. 2. Microscope view of ozone-damaged onion leaf cells near thestomata (S) (Faoro & Iriti 2009). The brownish colour of cells surrounding the stomata is due to precipitates formed by reaction
between the 3,30-diaminobenzidine (DAB) stain and the peroxidation
product H2O2. Bar = 100 lm.

Using 3D cell-level chlorophyll fluorescence imaging.
Endo & Omasa (2007) also showed that O3-induced inhibition occurs in cells immediately located under the epidermal cells.
The damaging effect of O3 to vegetation is related toits oxidising capacity and its high reactivity. After diffusion through stomatal cavities, O3 reaches the cell walls
and is rapidly decomposed. Other oxidants such ashydroxyl radicals (OH), more generally known as reactive
oxygen species (ROS), are formed and damage membranes, proteins and chorophylls (Haberer et al. 2007).
Plants have developed defence mechanisms consisting
mostly in producing antioxidant molecules, such as ascorbate, which serve as electron donors and reduce ROS.
Obviously, the efficiency of the defence mechanisms islimited by the availability of antioxidants and by thequantity of O3 reaching the cells.
Besides O3, the main air pollutants that have damaging
potential are mainly sulphur oxides, nitrogen oxides(NOx) and NH3. The damaging action of sulphur compounds on plants was studied by Thomas (1951) andsubsequently by many authors. The action of these pollutants is complex, as both adverse and beneficial effects
may arise, since sulphur can be used for plant growth(De Kok et al. 1998). A similar effect can be ascribed tothe uptake of NOx, which can be used by plants to synthesise amino acids when absorbed at low atmosphericconcentrations (Yoneyama et al. 2002). Nitrogen dioxide(NO2) is the most abundant NOx species. It dissolves inextracellular water and is converted into nitrite andnitrate ions, which participate in protein build up. At
higher atmospheric NO2 concentrations, however, damage
occurs. Exchange of NH3 between air and plants has beenstudied by Farquhar et al. (1980), Sutton et al. (1995)
28

Chemical exchange between air and vegetation is best
quantified by the flux of the chemical species exchanged.
This quantity can be expressed in units of quantity ofmatter (mol) or mass (kg) per unit area and time. Fluxes
can be positive (upward, emission) when directed to theatmosphere, or negative when directed to the plant(downward, uptake). Their determination is not straightforward but several methods exist, some are observationaland others computational. Flux measurement methods
are essentially divided into two categories: in situ (withenclosures or cuvettes) and micrometeorological (or aerodynamic).
Determining the flux of air pollutants through the stomata into leaves by in situ, leaf-level gas exchange measurements is the first step before upscaling to the tree,
stand and landscape level. The following discussion is
focused on O3 for clarity, as much work has been carriedout on this substance and since it is the most importantstressor for vegetation, but similar features characterise
other air pollutants, such as nitrogen and sulphur oxides.
Ozone is extremely reactive, and direct measurements of
its fluxes are thus challenging. Leaf-level O3 flux is usuallycalculated using a mass-balance approach from the difference between O3 concentration at the chamber inlet andoutlet, multiplied by air flow rate and subtracted fromthe chamber sink strength for O3 deposition (Omasa
et al. 1979a; Skärby et al. 1987; Havranek & Wieser 1994;
Matyssek et al. 1995; Wang et al. 1995; Pasqualini et al.
2002; Wieser 2002; Grulke et al. 2007). By this approach,stomatal uptake cannot be distinguished from other O3sink processes, unless measurements are also carried out
after stomatal closure (Grulke et al. 2007). Cuticulardeposition (adsorption and decomposition) of O3, however, is very small compared to that of open stomata(Omasa et al. 1979b; Pleijel et al. 2004; Grulke et al. 2007;
Fares et al. 2008). The water vapour surrogate method isthus being used to calculate stomatal O3 uptake on thebasis of direct measurements of stomatal conductance forwater vapour, the diffusion coefficient of water vapour
against that of O3, and difference among the mole fractions of O3 in air outside and inside the leaf (Wieser et al.
2008). This method assumes that the O3 flux through the
cuticle is negligible (Kerstiens & Lendzian 1989) and O3
concentrations inside the leaf approach zero (Laisk et al.
1989; Moldau et al. 1990), given the rapid decompositionof O3 into oxidative derivatives in the apoplast (Runec-

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

Cieslik, Omasa & Paoletti

Gas exchange of terrestrial plants

kles 1992). In general, stomatal O3 fluxes derived fromgas exchange measurement are in agreement with assessments based on the chamber inlet ⁄ outlet approach (Wieser et al. 2008). In addition, boundary layers aredestroyed by leaf-level gas exchange assessments, which
may strongly affect O3 uptake (Wieser et al. 2003). Sincetranspiration and O3 flux into the tree crown are coupledthrough stomatal regulation, sap flow measurement ofcrown transpiration has been suggested for assessing stomatal O3 flux at the tree level (Wieser et al. 2008). The
sap-flow assessment may then be combined with micrometeorological techniques.
The micrometeorological methods are based on theanalysis of turbulent motion of lower air layers in contact with vegetation. Air transports chemical substances
upward and downward by means of turbulent eddies.
Molecules of the transported substances are like passengers on a train (the air motions). The vertical flux Fi of
species i in a turbulent medium is governed by a Fick-like
diffusion law (Fick 1855), which can be written as
Fi ¼ KðzÞ

@Ci
@z

ð5Þ

where K(z) is the turbulent diffusion coefficient, Ci thelocal concentration of the species i and z is the height
above ground level (a.g.l.). Contrary to the molecular
diffusion coefficient, which is independent of space andtime but depends on the nature of the transported gas,
the turbulent diffusion coefficient depends on space andtime but not on the nature of the gas. Equation (5) is thebasis for a first method of measurement of vertical fluxes,
called the vertical gradient method. It consists in measuring concentrations of the gas at several heights a.g.l. inorder to calculate their vertical gradient. The turbulent
diffusion coefficient can be calculated since there are various parameterisations available in the literature (Dyer &Hicks 1970; Dyer 1974).
Another micrometeorological method is the so-callededdy covariance technique, based on calculation of thecovariance of the vertical component w of the windvector and of the concentration of the substance underconsideration, both measured at very high sampling frequency. This method was introduced by Scrase (1930) for
momentum, and later by Swinbank (1951) for water
vapour fluxes. It was then applied to various gaseous substances (Desjardins 1972; Delany et al. 1986; Baldocchi
et al. 1988; Hicks & Matt 1988; Foken et al. 1995). The
covariance is expressed by
Fi ¼ w0 Ci0ð6Þ

where the primed quantities represent fluctuations aroundthe time-averaged value of the corresponding variable,
and the overbar stands for the time-averaging process.
The eddy covariance technique is generally considered as
the most reliable micrometeorological flux determination
method as it does not suffer from artifacts or biases.
However, this method presents two main disadvantages:
its use is delicate and it requires fast-response chemicalsensors, which only exist for a few gases. Nevertheless,fluxes of CO2, O3 (Delany et al. 1986; Hicks et al. 1987;
Massman 1993; Lamaud et al. 1994; Gerosa et al. 2003;
Cieslik 1998, 2004, 2009; Affre et al. 2000 and many others), NOx (Wesely et al. 1989; Coe & Gallagher 1992;
Stocker et al. 1993), NH3 (Famulari et al. 2004), N2O andCH4 (Fowler et al. 1995; Di Marco et al. 2004), isoprene(Guenther & Hills 1998) and some others have beensuccessfully obtained by this method. An example ofresults obtained with the eddy covariance method isshown in Fig. 3, where O3 fluxes measured during 4 daysof May 2003 over an onion field in northern Italy (Gerosa
et al. 2007) are represented.
A third micrometeorological method, the eddy accumulation technique, sometimes quoted as ‘‘conditional
sampling’’, was mainly developed by Businger & Oncley(1990) for CO2 and CH4 and subsequently used for anumber of other gases (Baker et al. 1992; Darmais et al.
2000; Myles et al. 2007), is a kind of compromise between
the two previously described methods. It consists in accumulating air in two containers according to the direction(up- or downward) of the vertical wind during a certain

Fig. 3. Vertical total ozone fluxes recorded during a measuring campaign conducted over an onion field near Voghera (northern Italy) in May
2003.

Plant Biology 11 (Suppl. 1) (2009) 24–34 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands

29Gas exchange of terrestrial plants

Cieslik, Omasa & Paolettitime interval (generally 30 min); the content of the containers is subsequently analysed to obtain the concentrations of the gases for which the flux is measured. The
flux is then given by
F ¼ bwðCþ  C Þ

ð7Þ

where b is an empirical coefficient, w is the vertical wind;C+ and C) are the concentrations measured in the twocontainers. This technique is easier to use in the field
than the eddy covariance technique. It does not require
fast-response sensors and the measurement is made at
one single level, unlike the gradient technique, whichneeds measurement at different levels. It is thus especially
adapted for the measurement of fluxes of VOC species(see e.g. Graus et al. 2006).

REFERENCES

CONCLUDING REMARKSThe interactions between the chemical composition of theatmosphere and vegetation are an evident fact. The concentrations of major components of the atmosphere, likeO2, water vapour and CO2, are strictly related to the presence of vegetation at the surface of the Earth, and any
modification of the vegetal cover has consequences onthese concentrations. Conversely, changes in concentrations of these substances have consequences on the stateof vegetation and not only on climate. Besides these‘‘main’’ substances, a number of chemical species, often
called ‘‘minor atmospheric species’’, are exchanged
between plants and the atmosphere in both directions
and, in spite of their low atmospheric concentrations they
can have an important influence on both atmosphericchemistry and vegetation health. Many organic substances
are produced by vegetation, released in the air and influence air chemistry; air pollutants penetrate plant tissues
and cause deleterious effects on plant health. Due toincreasing emissions of various man-made substances, theatmospheric composition is changing. For example, ozone
concentrations are increasing around the world; thisreduces plant growth and consequently carbon sequestration. This process hinders policies aimed at fighting global warming (Sitch et al. 2007). Another important
example is the role of isoprene, emitted by plants, andinfluencing atmospheric photochemistry at global scale byinteracting with various air pollutants. The interactions
between air pollutants, climate change and vegetation areoften neglected by decision-makers. Air ⁄ vegetation interactions are bidirectional and their study is complex, being
highly nonlinear and causing feedbacks. These studies arethus important to preserve the quality of both air andbiosphere.
The quantities of gases exchanged between the atmosphere and terrestrial plants are enormous and most ofthese substances use the stomatal pathway. But at singlestoma level, the quantities exchanged are minute. This
causes technical difficulties for measurements, increasing
uncertainties in the assessment of exchanged quantities at

30

global level, and constitutes a major challenge for future
research in this field. Another difficulty is how to relatethese very different scales to each other and thus solve
the upscaling problem.
The gas exchange processes between terrestrial vegetation and the atmosphere are an essential component of
the global atmosphere ⁄ biosphere ⁄ lithosphere system andalso interact with the climate system. A considerable
amount of knowledge has been accumulated on thistheme since the discovery of photosynthesis. Remaining
unknowns are related to differences in spatial and temporal scales involved and technical problems in measurement. More interdisciplinarity is also needed to obtain a
global depiction of gas exchange, since the phenomena
are of a biological, chemical and physical nature.

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