Chapter 9
Aboveground and Belowground Consequences
of Long-Term Forest Retrogression in the
Timeframe of Millennia and Beyond
David A. Wardle
9.1 Introduction
Following the occurrence of a substantial disturbance and creation of a new surface,
primary succession occurs. This involves colonisation by new plant species, and
their associated aboveground and belowground biota. During this period, substan-
tial ecosystem development occurs (Odum 1969), and this involves the buildup of
ecosystem carbon through photosynthesis and nitrogen through biological nitrogen
fixation. The initial colonising plant species are short-lived and often herbaceous,
but these are replaced over time by those that are larger, woody, more conservative
at retaining nutrients, and produce organic matter of poorer quality (Grime 1979;
Walker and Chapin 1987). Disturbances that are not sufficiently severe to result in
new surfaces being formed can reverse the successional trajectory, resulting in a
secondary succession that often operates in a broadly similar way to primary
succession though from a later starting point (White and Jentsch 2001; Walker
and Del Moral 2001).
Following the initial development of forest during succession, and as trees age,
there may be a notable reduction in net biomass productivity. The generality of this
phenomenon is under debate (see Chap. 21, by Wirth, this volume), but where it
occurs, the decline is usually apparent in the order of decades to centuries following
forest stand development (Gower et al. 1996). The mechanistic basis for this decline
is unclear, but there are likely to be multiple factors involved (see detailed discus-
sion in Chap. 7 by Kutsch et al., this volume). Some proposed explanations have a
plant-physiological basis, such as increasing hydraulic limitation as trees grow
taller, shifts in the balance between photosynthesis and respiration, and increasing
stomatal limitation as trees age. However, the evidence for or against each of these
mechanisms is mixed and no universal explanation emerges (see, e.g. Gower et al.
1996; Magnani et al. 2000; Weiner and Thomas 2001; Ryan et al. 2004, 2006).
Other explanations relate to belowground properties and nutrient supply from the
soil. For example, as forest stands develop and succession progresses, the rate of
mineralisation of nutrients from the soil declines (Brais et al. 1995; De Luca et al.
C. Wirth et al. (eds.), Old‐Growth Forests, Ecological Studies 207, 193
DOI: 10.1007/978‐3‐540‐92706‐8 9, #Springer‐Verlag Berlin Heidelberg 2009
2002). This is at least partly as a result of a greater proportion of nutrients being
immobilised in plant tissue and because of the declining quality of plant litter
(Ha
¨ttenschwiler and Vitousek 2000; Nilsson and Wardle 2005). This reduced soil
activity is consistent with changes in the composition of the soil community that
have sometimes been observed during succession (e.g. Scheu 1990; Ohtonen et al.
1999). Often the reduction of nutrient availability is driven in part by changes in
the forest understorey composition, such as increased densities of dwarf shrubs
(Nilsson and Wardle 2005) and mosses (Zackrisson et al. 1997; Bond-Lamberty
et al. 2004), which may lock up nutrients or produce litter of poor quality. Regard-
less of the precise mechanisms involved, it is apparent that at least part of the
reduction in forest stand productivity in the order of decades to centuries is
frequently associated with the reduced rate of supply of nutrients from the soil,
and probably involves changes in the composition of the soil biota as well as the
vegetation.
In the prolonged absence of major disturbance, i.e. in the order of millennia and
beyond, the decline in forest productivity can be followed by significant declines in
forest stand biomass. This decline is often associated with declines in the availabil-
ity of soil nutrients that occur during pedogenesis (Walker and Syers 1976;
Richardson et al. 2004; Vitousek 2004; Wardle et al. 2004; Coomes et al. 2005).
We refer to this situation of long-term decline in forest biomass caused by reduction
in available nutrients as ‘ecosystem retrogression’ (Walker et al. 2001; Walker and
Reddell 2007). This phenomenon is distinct from the shorter term decline in forest
productivity that frequently occurs in the order of decades to centuries and that may
have a variety of causes (Gower et al. 1996). Significantly, as ecosystems age in the
order of thousands of years without major disturbance, phosphorus availability
may become a major factor limiting forest biomass. In a classical investigation of
long-term chronosequences on sand dunes and moraines in New Zealand (spanning
several millennia), Walker and Syers (1976) showed that as soils age the total
amounts of phosphorus declines significantly (presumably through leaching and
runoff), and that the remaining phosphorus becomes converted to forms that are
increasingly physically occluded or bound in relatively recalcitrant organic com-
pounds, and that are relatively unavailable to plants. This type of pattern has
subsequently been shown in other locations and for other ecosystems, e.g. in eastern
Australia (Walker et al. 1981) and the Hawaiian islands (Crews et al. 1995;
Vitousek 2004). In the long term, greatly reduced availability of nitrogen may
also occur, partly because of increased immobilisation, partly because of retention
of nitrogen in recalcitrant polyphenolic complexes that are less easily decomposed
(Northup et al. 1995, 1998; Wardle et al. 1997), and partly because of leaching
losses as dissolved organic nitrogen (see Chap. 16 by Armesto et al., this volume).
These changes in availability of key nutrients during retrogression appear to be
linked to both changes in soil biota (Williamson et al. 2005; Doblas-Miranda et al.
2008) and forest vegetation composition (Wardle et al. 1997; Nilsson and
Wardle 2005).
It is apparent that in forested ecosystems subjected to the absence of disturbance
in the order of thousands of years, the initial build-up phase is followed by a decline
194 D.A. Wardle
in net productivity, and, given sufficient time, by a decline in standing biomass
(Richardson et al. 2004; Vitousek 2004; Wardle et al. 2004; Coomes et al. 2005). At
least part of this decline is linked to reduced nutrient availability . In this chapter, I
will explore the changes that occur in forested ecosystems that have been absent
from disturbances for sufficient time for declines in standing tree biomass to occur,
i.e. in the order of millennia and beyond. In doing so, I will firstly describe an
ongoing study on forested lake islands in northern Sweden where these ideas are
being explicitly explored. I will then assess the generalities of these concepts by
considering other long-term forested chronosequences around the world. In doing
so, I will attempt to determine whether there are general trends that occur above-
ground and belowground with regard to how communities and ecosystems respond
to long-term ecosystem retrogression.
9.2 Lake Islands in Northern Sweden
The study system consists of an archipelago of forested lake islands in two adjacent
lake systems (Lakes Uddjaure and Hornavan), in the boreal zone of northern
Sweden (6655066090N; 1743017550E). Within this system are over 400
islands that vary in size from a few square metres to over 80 ha. For our studies,
we have selected several forested islands in each of three size classes, i.e. ‘small’
islands (<0.1 ha), ‘medium’ islands (0.1 1.0 ha) and ‘large’ islands (1.0 ha). Study
islands were been chosen such that their areas are distributed lognormally, and very
large islands with obvious signs of human activity were excluded. The selected
islands are all of approximately the same age, having been formed by the retreat of
land ice 9,000 years ago, and have been subjected to minimal human interference.
Islands are ideal systems for studying the effects of historical fire regimes on
large numbers of spatially independent ecosystems (Bergeron 1991). The main
extrinsic driver that varies across the islands in our study system is wildfire
disturbance through lightning strike; large islands get struck by lightning more
often than do smaller ones, and therefore burn more frequently (Wardle et al. 1997,
2003). This is apparent both from analyses of fire scars on trees, and from dating of
14
C of the most recent charcoal present in humus profiles (Table 9.1). Island size
therefore serves as a surrogate for time since fire and fire frequency. Some large
islands have burned in the past century, while others have not burned for the past
5,000 years (Wardle et al. 2003), making the system ideal for investigating the
effects of variation of a major agent of disturbance across essentially independent
discrete ecosystems. Some large islands have historical fire regimes that are proba-
bly comparable to those of Scandinavian boreal forests on the mainland (Zackrisson
1977; Niklasson and Granstro
¨m 2000), while most small islands have regimes that
are consistent with long-term fire suppression or absence.
Fire history is an important long-term determinant of vegetation composition in
boreal forests (Payette 1992; Le
´gare
´et al. 2005) and, consistent with this, the
variation in fire regime across islands has been found to exert important effects
9 Aboveground and Belowground Consequences of Long Term Forest 195
Table 9.1 Changes in selected aboveground and belowground properties (mean values with standard errors in brackets) across an island size gradient in
northern Sweden, in which decreasing island size is reflective of increasing ecosystem retrogression. Data from Wardle et al. (1997, 2003, 2004) and Wardle
and Zackrisson (2005). Within each row numbers followed by the same letter are not statistically significant at P= 0.05 (Tukey’s test following one-way
ANOVA).
Response variable Large island (>1 ha) Medium island (0.1–1.0 ha) Small island (<0.1 ha)
Disturbance regime
Time since last major fire (
14
C data) (years) 585 (233) c 2180 (385) b 3250 (439) a
Number of fire scars caused in past 250 years 0.667 (0.256) a 0.208 (0.085) b 0.143 (0.016) b
Aboveground properties
Tree biomass (kg m
–2
) 7.39 (0.83) a 5.38 (0.47) a 3.98 (0.62) b
Tree litterfall (g C m
–2
year
–1
) 37.3 (5.2) a 43.7 (4.0) a 32.3 (4.5) b
Tree productivity (g C m
–2
year
–1
) 148.1 (15.5) a 152.8 (12.9) a 78.4 (14.7) b
Dwarf shrub biomass (kg m
–2
) 0.365 (0.014) a 0.383 (0.015) a 0.288 (0.019) b
Dwarf shrub productivity (g C m
–2
year
–1
) 76.8 (3.9) a 72.7 (3.5) a 51.6 (4.8) b
Dominant tree species Pinus sylvestris Betula pubescens Picea abies
Dominant dwarf shrub species Vaccinium myrtillus Vaccinium vitis-idaea Empetrum hermaphroditum
Belowground properties
Soil polyphenols (mgg
–1
) 175 (6) b 204 (6) a 225 (8) a
Soil respiration (mgCO
2
-C g
–1
h
–1
) 4.23 (0.30) a 2.97 (0.28) b 1.81 (0.30) c
Substrate-induced respiration (mgCO
2
-C g
–1
h
–1
) 22.9 (1.43) a 14.5 (1.35) b 11.5 (2.13) b
Litter decomposition rate (% loss in 2 years) 45.9 (1.1) a 44.2 (1.0) b 41.5 (1.0) b
Total humus carbon mass (kg m
–2
) 6.4 (1.1) c 16.2 (2.5) b 27.3 (2.5) a
Humus C to N ratio 40.4 (1.18) a 36.0 (1.17) ab 32.9 (0.79) b
Humus C to P ratio 623 (20) b 687 (36) ab 759 (30) a
Humus N to P ratio 15.4 (0.5) c 19.1 (0.9) b 23.3 (1.1) a
196 D.A. Wardle
on vegetation composition (Wardle et al. 1997; Table 9.1). The largest and most
regularly burned islands are dominated by relatively fast-growing early-successional
species such as Pinus sylvestris and Vaccinium myrtillus, and the middle-sized
islands are dominated by Betula pubescens and Vaccinium vitis-idaea . Meanwhile,
the small islands are dominated by slow-growing late-successional species such as
Picea abies and Empetrum hermaphroditum . Those species that dominate on large
islands tend to allocate carbon to growth while those dominating on smaller islands
tend to allocate carbon to the production of secondary compounds such as poly-
phenolics (Nilsson 1994; Gallet and Lebreton 1995; Nilsson and Wardle 2005).
Consistent with this, humus on small islands has a significantly higher concentra-
tion of polyphenolics than that on the larger islands (Table 9.1).
Responses of the plant community to island size have important consequences
for the belowground subsystem. The poorer quality of litter returned to the soil on
small islands, and the higher concentrations of polyphenolics in the humus, leads to
significant impairment of soil microbial biomass and activity (Table 9.1). This in
turn results in reduced decomposition rates of plant litter in the soil, and lower rates
of supply of nutrients from the soil for subsequent plant growth. The concentration
of nitrogen in the humus of the small islands is slightly greater than that of the large
islands (Wardle et al. 1997), and biological nitrogen fixation by cyanobacteria
associated with feather mosses (the main biological form of nitrogen input to the
islands) is greatest on the small islands (Lagerstro
¨m et al. 2007). However, the
small islands appear to be more nitrogen limited: test litter placed on the small
islands releases nitrogen more slowly than when placed on large islands and the
concentrations of plant available forms of nitrogen are lower in soils of small
islands (Wardle and Zackrisson 2005). This appears to influence nitrogen acquisi-
tion by microbes and plants; the nitrogen concentrations of the microbial biomass
and green leaves of at least some plant species are lower on the small than the large
islands (Wardle et al. 1997). Despite there being more soil nitrogen (and nitrogen
input) on the small islands, it is likely that much of the soil nitrogen on the small
islands is not biologically available because it is bound tightly in polyphenolic
complexes (Wardle et al. 1997). Concomitant with this reduced availability of
nitrogen is reduced availability of phosphorus on the small islands (Wardle et al.
2004), which is a characteristic of retrogressive chronosequences that span
thousands of years (Walker and Syers 1976). As a consequence of reduced nutrient
availability and plant uptake following the prolonged absence of wildfire, small
islands show lower rates of tree and understorey productivity, less litterfall, and
lower vascular plant standing biomass (Wardle et al. 1997, 2003; Table 9.1).
The island system provides evidence that reductions in fire frequency, and the
ecosystem retrogression that follows, greatly affects ecosystem carbon sequestra-
tion. As island size decreases and time since fire increases, the amount of carbon
stored aboveground declines. However, because litter decomposition rates are also
impaired on the small islands, the amount of carbon stored belowground in the
humus increases (note that the mineral soil layer, and hence the amount of carbon
stored in it, is negligible). Reduction of decomposition on small islands emerges for
at least four reasons (Wardle et al. 2003, Dearden et al. 2006): (1) plant species that
9 Aboveground and Belowground Consequences of Long Term Forest 197