Chapter 7
Biosphere–Atmosphere Exchange
of Old-Growth Forests: Processes and Pattern
Alexander Knohl, Ernst-Detlef Schulze, and Christian Wirth
7.1 Introduction
Forests are important agents of the global climate system in that they absorb and
reflect solar radiation, photosynthesise and respire carbon dioxide and transpire
water vapour to the atmosphere (Jones 1992). Through these functions, forests act
as substantial sinks for carbon dioxide from the atmosphere (Wofsy et al. 1993;
Janssens et al. 2003) and sources of water vapour to the global climate system
(Shukla and Mintz 1982). Since old-growth forests differ in age, structure and
composition from younger or managed forests (see Chap. 2 by Wirth et al., this
volume) the question arises whether these characteristics also result in differences
in the biosphere atmosphere exchange of carbon, water, and energy of old-growth
forests.
This chapter reviews studies using two contrasting experimental approaches:
the eddy covariance technique, and paired catchment studies. The eddy covari-
ance technique is a micrometeorological standard method to directly quantify the
exchange of trace gasses between forest ecosystems and the atmosphere by mea-
suring up- and down-drafts of air parcels above the forest (Baldocchi 2003). Fluxes
of scalars such as carbon dioxide, water vapour as well as sensible heat can be
inferred from the covariance between scalar and vertical wind speed (Aubinet et al.
2000). The advantages of this approach are that no disturbances or harvests are
needed to assess fluxes and that the eddy flux tower typically integrates over a flux
source area of approximately 1 km
2
. This approach, however, assumes that the
underlying surface, i.e. the forest, is horizontally homogeneous, which is typically
the case over managed, even-aged forests. Old-growth forests, however, are often
characterised by a dense and structured canopy including canopy gaps and a diverse
range of tree heights (see Chap. 2 by Wirth et al., this volume; Parker et al. 2004).
Additionally, in many parts of the world, old-growth forests occur mainly in
complex often sloped terrain of mountain ranges, which are less favourable or
accessible for anthropogenic land use [see Chaps. 15 (Schulze et al.) and 19 (Frank
et al.), this volume]. This raises the question of how these characteristics of old-
growth forests affect the direct measurement of biosphere atmosphere exchange of
C. Wirth et al. (eds.), Old‐Growth Forests, Ecological Studies 207, 141
DOI: 10.1007/978‐3‐540‐92706‐8 7, #Springer‐Verlag Berlin Heidelberg 2009
carbon, water, and energy. With the second approach, i.e. paired catchment studies,
only water exchange is quantified. This is done by comparing the streamflow of
two catchments that are similar with respect to soil, topography and climate but
differ in land use or vegetation cover (Andre
´assian 2004). The method is suited to
the study of differences in evapotranspiration and water yield between contrasting
land-use types, forest developmental stages, and management strategies. Topo-
graphic complexity per se does not pose a problem. However, this comes at the
expense of a lower temporal resolution and the need for multi-year calibration
periods.
In this chapter, we summarise results from studies in old-growth forests across
the globe in order to (1) describe structural characteristics of old-growth forests
relevant for biosphere atmosphere exchange (Sect. 7.2); (2) show how these
characteristics influence net ecosystem carbon fluxes (Sect. 7.3); (3) investigate
the interplay between canopy structure, water, and energy fluxes (Sect. 7.4); and
(4) study the absorption of radiation, particularly of diffuse radiation in old-growth
forests (Sect. 7.5).
7.2 Characteristics of Old-Growth Forests Relevant
for Biosphere–Atmosphere Exchange
When forest ecosystems advance in age they typically undergo changes in their
structural properties (see Chap. 2 by Wirth et al., this volume). Old and large trees
are more at risk to external forces such as disturbance by wind or by rotting of the
heartwood due to fungal attack (Dho
ˆte 2005; Pontailler et al. 1997). As a conse-
quence, individual trees, or parts of trees, sporadically die resulting in small scale
canopy gaps (Spies et al. 1990). These gaps then supply light to lower parts of the
canopy that were previously in shade. With this light supply, individuals previously
limited by light are able to enhance their growth and finally close the canopy gap. In
old-growth forests gaps are typically very dynamic, leading to ongoing changes in
canopy structure, light environment, and hence species composition (see Chap. 6 by
Messier et al., this volume). The spatial extent of canopy gaps and speed of canopy
closure is likely to depend on species, site conditions and disturbance intensity, and
varies greatly among biomes. For old-growth forests in the Pacific Northwest of the
United States canopy gaps were reported to remain open for decades (Spies et al.
1990). Even in cases where canopy gaps in old-growth deciduous forests caused by,
e.g., storms were closed within a few years, the light quantity and quality reaching
understorey vegetation may remain dynamic for decades or even longer (see Chap.
6 by Messier et al., this volume). As a consequence of these gap-phase dynamics,
old-growth forests typically form a canopy consisting of diverse age classes and
also varying heights of individual trees and canopy parts. Older and tall trees may
act as shelter for younger trees. The 450-year-old Douglas fir/Western hemlock
forest at the Wind River Canopy Crane Research Facility (WRCCRF) consists of
142 A. Knohl et al.
an extremely complex outer canopy surface due to high and narrow crowns and
numerous larger and smaller gaps (Parker et al. 2004). As a result, the surface area
of the canopy reaches more than 12 times that of the ground area. The outer shape of
the canopy strongly influences the permeability to solar radiation and the coupling
of environmental conditions such as air temperature and humidity with the atmo-
sphere. Since the top canopy consists of narrow crowns, a large part of leaf area is
distributed to lower parts of the canopy, hence allowing solar radiation to penetrate
deeply into the canopy resulting in a high efficiency in trapping light and hence low
surface reflectance (Weiss 2000).
Along with processes leading to canopy gaps, coarse woody detritus, either
standing or lying on the ground, accumulates and may account for a substantial
fraction of the carbon pool within in an ecosystem. The amount and decay rates of
coarse woody debris vary among biomes and environmental conditions (see Chap. 8 by
Harmon et al., this volume.). At the WRCCRF forest about 25% of aboveground
biomass is dead, resulting in large carbon pools contributing to heterotrophic
respiration (Harmon et al. 2004). Also, old-growth forests often contain large
aboveground biomass stocks (see Chap. 15 by Schulze, this volume) for temperate
and boreal biomes. Pregitzer and Euskirchen (2004) show a consistent increase in
biomass carbon pools with age for boreal, temperate and tropical ecosystems.
Similarly, soil carbon pools are also often large due to carbon accumulation during
stand development since the last disturbance (Harmon et al. 2004; Pregitzer and
Euskirchen 2004).
All these structural features typical of old-growth forests are expected to influ-
ence biosphere atmosphere exchange of such forests. In this chapter we will focus
on structural features of old-growth, i.e. the fact that old-growth forests tend to be
uneven-aged, horizontally and vertically structured forests, which at high age show
gap dynamics and contain large amounts of woody detritus. In general, we concen-
trate on forests located in the temperate zone, but also include some examples from
the boreal and tropical zones.
7.3 Exchange of Carbon Dioxide
Old-growth forests are often considered to be insignificant as carbon sinks since it is
assumed that they are in a state of dynamic equilibrium (Odum 1969; Salati and
Vose 1984) where assimilation is balanced by respiration as a forest stand reaches
an old stage of development (Jarvis 1989; Melillo et al. 1996). This hypothesis is
based on studies showing a decline with stand age in net primary productivity at stand
level (Yoder et al. 1994; Gower et al. 1996; Ryan et al. 1997) and in photosynthesis
at tree level (Hubbard et al. 1999; and see Chap. 4 by Kutsch et al., this volume)
and the general idea that ecosystem respiration increases with stand age (Odum
1969). Potential mechanisms such as increasing respiration costs and nutrient or
hydraulic limitation are critically discussed by Kutsch et al. (Chap. 4, this volume)
and Ryan et al. (2004). Recent studies find carbon uptake rates in old-growth
7 Biosphere Atmosphere Exchange of Old Growth Forests: Processes and Pattern 143
forests indicating a small-to-moderate carbon sink (Phillips et al. 1998; Carey et al.
2001), sometimes even comparable to younger forests in the same region (Anthoni
et al. 2004). Data for coniferous forests show that, even when old, some forests can
retain their capacity to absorb carbon from the atmosphere, as shown for a 450-year
old Douglas fir/Western hemlock site in Washington (Paw et al. 2004), a 250-
yearold ponderosa pine site in Oregon (Law et al. 2001), a 300-year old Nothofagus
site in New Zealand (Hollinger et al. 1994), and 200- to 250-year old boreal
forests (Roser et al. 2002). This is supported by results from studies in mixed and
deciduous forests that remained significant carbon sinks even when at high
age, such as a 250-year old uneven-aged mixed beech forest in Germany (Knohl
et al. 2003), a 200-year old mixed forest in China (Guan et al. 2006; Zhang et al.
2006), and a 350-year old uneven-aged mixed forest in the United States
(Desai et al. 2005).
In this book, Kutsch et al. (Chap. 4) and Schulze et al. (Chap. 15; and see
Luyssaert et al. 2008) argue that structure not age determines the capacity of forest
ecosystems to absorb carbon from the atmosphere, and hence old forests may
remain carbon sinks even at high age. The argumentation is based on a global
dataset of net primary productivity, biomass, stand density and net ecosystem
exchange measurements (Luyssaert et al. 2007) showing that a decline in
productivity is more strongly related to leaf area index than to stand age, and
that it only occurs when stand density drops below 330 trees ha
–1
in temperate
forest and 690 trees ha
–1
in boreal forest, independent of tree age. This finding is
supported by recent grafting studies showing that leaf level decline in photosynthe-
sis is also related not to age, but to tree structure (Mencuccini et al. 2007;
Vanderklein et al. 2007). Moreover, we also find that even 211-year old Pinus
sylvestris trees have the ability to maintain high growth rates, as seen by an increase
in radial growth by factor of five immediately after thinning. This indicates that
these trees have been limited not by an age-related effect but by competition for
resources (Fig. 7.1). Once resources became more abundant again due to exclusion
of competitors, even old trees increase their growth. Individuals with previously
high growth rates responded more strongly to thinning than individuals with smaller
growth rates. These findings are supported by a study in the temperate zone. Tall
140-year old Norway spruce trees in southern Germany showed an increase of
about 50% in annual stem volume increment after stand thinning via harvest (Mund
et al. 2002).
A global compilation of net ecosystem exchange data from eddy covariance
(Luyssaert et al. 2007) reveals that there are several old-growth forests (older than
200 years) that are net carbon sinks (Fig. 7.2). It is important to note that the global
coverage of eddy covariance flux measurements is strongly biased towards younger
and managed forests. Only very few flux towers are located in old-growth forests.
Additionally, some of these old-growth forests are ecosystems where factors
other than just age play an important role. A chronosequence of boreal forests in
Canada shows following classical theory a decrease in net ecosystem produc-
tivity with age, with the oldest forests (aged around 160 years) being close to
carbon neutral (Amiro et al. 2006). However, a more detailed study from the same
144 A. Knohl et al.
old-growth forest reveals that the low net ecosystem productivity at this site is
determined mainly by a combination of low stand density and large heterotrophic
respiration due to peat decomposition depending on changes in water table depth
(Dunn et al. 2007). Midday carbon uptake rates of this old-growth forest, however,
are not lower than at other much younger ecosystems (Goulden et al. 2006).
Similarly, a recent study of eddy covariance measurements across five chronose-
quences in Europe showed a strong age-related pattern of net ecosystem
exchange, where young forests are carbon sources, intermediate forests carbon
sinks and the only older forests in this study was close to carbon neutral (Magnani
et al. 2007). However, when looking more closely at the oldest forest in that study, a
boreal coniferous forest in Sweden, it seems likely that factors other than just
age are important such as horizontal advection of CO
2
(A. Lindroth, personal
communication).
There has been a recent controversial discussion over whether the eddy covari-
ance technique can be used to accurately measure the exchange of carbon between
forest and atmosphere in terrain typical of old-growth forests, i.e. mountainous
regions or tall and dense canopies (Kutsch et al. 2008). Advection, i.e. a non-
turbulent transport of scalars such as CO
2
, has been observed at several sites across
the globe, often in dense forests, even at sites with only a minor slope (Staebler and
Fitzjarrald 2004; Aubinet et al. 2003, 2005; Feigenwinter et al. 2008; Kutsch et al.
2008). Measuring advection directly is technically challenging since it requires
Fig. 7.1 Radial stem increment of 211 year old Pinus sylvestris trees (n= 9) in Central Siberia.
The stand was thinned via harvest in 1983 resulting in a strong increase in radial growth. Error
bars Standard error
7 Biosphere Atmosphere Exchange of Old Growth Forests: Processes and Pattern 145