Springer Old Growth Forests - Chapter 9 potx

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

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

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 belowabove-ground 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

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 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

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

ANOVA) Response

O2

O2

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

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 concentraacquisi-tions 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

produce poorer quality litter (e.g.Picea., Empetrum) begin to dominate; (2) pheno-typic plasticity within species, i.e a given plant species may produce poorer litter quality on a small island; (3) trees produce a greater proportion of poor quality twig litter relative to higher quality foliar litter; and (4) activity of the decomposer microflora declines As a consequence, some large islands store less than 5 kg

Because the belowground (rather than aboveground) component stores the majority

of carbon in these forests, there is net carbon sequestration over time, of around

indicates that long-term fire suppression significantly contributes to ecosystem carbon storage, and if the pattern identified in this system is representative of northern ecosystems in general, then current fire suppression practices in the boreal zone are likely to play an important role in the global carbon cycle In this light, a recent study of a long-term (over 2,300 years) chronosequence in the boreal zone of eastern Canada found belowground carbon accumulation rates to be significantly greater than that measured on the lake islands (Lecomte et al 2006)

The island study is also relevant for addressing the so-called ‘diversity-function’ issue, which relates to whether plant species diversity promotes key ecosystem processes such as production and decomposition [see Hooper et al (2005) for a review] As island size decreases, tree species diversity (Shannon-Weiner diversity index) increases sharply (Wardle et al 2008; Fig 9.1), as does total vascular plant species richness (Wardle et al 2008) However, small islands also have the lowest rates of key ecosystem processes such as decomposition, nutrient mineralisation and aboveground productivity The resulting negative correlation between plant diversity and process rates suggests that plant diversity is not a key driver of ecosystem processes across the island sequence, because of the overriding importance

of other factors that also vary across the sequence such as the traits of the dominant plant species In particular, the large islands are dominated by rapidly growing plant species that produce litter of high quality, and promote rapid ecosystem process rates However, these species are also highly competitive and appear to suppress subordinate species through competitive exclusion, reducing total plant diversity These competitive dominants cannot dominate on the less fertile small islands; this leads to a greater coexistence of species being possible, but also a greater incidence

of those plant species that are unproductive, produce litter of a poor quality, and slow ecosystem process rates down

While traits of dominant plant species may govern ecosystem functioning at the across-island (between ecosystem) spatial scale, biodiversity may have a role in influencing ecosystem processes at more local spatial scales To investigate this, an ongoing study was set up in 1996 on each of 30 islands and which involves 420 manipulative plots (first 7 years reported by Wardle and Zackrisson 2005); the study involves regularly maintained experimental manipulations of various plant species and functional groups with a particular focus on understorey vegetation Above-ground, removal of various components of the understorey layer often reduced total plant biomass in that layer Meanwhile, when belowground properties were considered,

Chronosequence stage

Fig 9.1 Changes in tree basal area, species richness, and Shannon Weiner (S.W.) diversity indices (mean of all plots for each stage) in response to ecosystem development (1 = youngest) for each of six long term chronosequences (see Table 9.2 for timescale of each sequence) For the species richness measures at each chronosequence stage, values represented by histogram bars have been corrected for varying total stem density using rarefraction analyses, while the values represented by crosses are the raw species richness values not adjusted using rarefraction Within

two dwarf shrub species (Vaccinium myrtillus and Vaccinium vitis-idaea ) emerged as major ecosystem drivers, but only on large islands Specifically, experimental removal of these species on large (but not on small) islands adversely affected plant litter decomposition rates respiration, soil microbial biomass, and plant-available forms of nitrogen This work points to the effects of biodiversity loss (either in terms of functional groups or species) at the within-island scale being context-dependent, and being of diminishing importance with increasing time since wildfire and as retrogression proceeds These results reveal that, although biodiver-sity is unlikely to be a major driver of ecosystem properties at the across-island scale, biodiversity loss may play a role at the within-island scale, but that this role may be important only in relative productive earlier successional ecosystems

It is apparent that as retrogression proceeds in this island system, a range of responses occur both above- and below-ground Several of these responses are driven in the first instance by the reduced availability of nutrients over time, and in the second instance by changes in the functional composition of the dominant vegetation Changes in the availability of other resources such as moisture cannot explain our results, because humus depth increases during retrogression, and this involves greater retention of soil moisture with increasing time since fire Other changes that may occur on these islands during retrogression involve shifts in the communities of microorganisms and above- and below-ground invertebrates, and investigations of the involvement of these organisms are in progress It is apparent

in the long-term absence of disturbance on these islands that high productivity and high biomass forests cannot be maintained beyond around 2,000 3,000 years and that, after this time, increasing nutrient limitation leads to reduced stature of the forest, slowdown of ecosystem process rates, and increasing storage of organic matter belowground rather than aboveground This type of retrogression resulting from the prolonged absence of wildfire may be a common phenomenon in boreal forests (Asselin et al 2006), and could ultimately lead to low productivity in forest tundra and taiga communities throughout many boreal forest habitats (see Payette 1992; Ho¨rnberg et al 1996)

9.3 Retrogressive Successions Elsewhere in the World

While the Swedish lake island system provides evidence of ecosystem

phenomenon is more widespread in nature Some other studies have also charac-terised long-term chronosequences that yield evidence of retrogression, and details

Fig 9.1 (Continued) each panel, histogram bars topped by the same letter do not differ signi ficantly at P = 0.05 according to the least significant difference test; this test has not been applied to panels for which chronosequence stage effects are not significant according to ANOVA ND Not determined, MSE mean standard error Stages 1 and 2 for the Glacier Bay chronosequence lack trees and are therefore not presented here (taken from Wardle et al 2008)

of six of these (the Swedish lake island system, and five others) are summarised in Table 9.2 These do not represent an exhaustive list of retrogressive chronose-quences , but rather a selection of sechronose-quences that have each been well characterised and well studied, and that have previously been used in a comparative study by Wardle et al (2004) to understand ecosystem decline These sequences are all very long term and span at least 6,000 (and up to 4.1 million) years Each chronose-quence represents a series of sites varying in age since surface formation or catastrophic disturbance, but with all other extrinsic driving factors being relatively constant Two of these sequences are in the Boreal zone, i.e the Arjeplog sequence

in northern Sweden (described above) and the Glacier Bay sequence of south-east Alaska (Noble et al 1984; Chapin et al 1994) Two are in the temperate zone, i.e the Franz Josef sequence of Westland, New Zealand (Walker and Syers 1976; Wardle and Ghani 1995; Richardson et al.2004) and the Waitutu sequence of southern New Zealand (Ward 1988; Coomes et al 2005) The remaining two are

in the sub-tropical zone, i.e the Hawaiian island sequence (Crews et al 1995; Vitousek and Farrington 1997; Vitousek 2004) and the Cooloola sequence of Queensland, Australia (Thompson 1981; Walker et al 2001) These sequences are formed on vastly different substrates and have been created by different agents

of disturbance (Table 9.2) In all six cases, ecosystem development in the long-term has occurred after a catastrophic disturbance event or an event that has substantially re-set the successional clock

Tree basal area (a surrogate of tree standing biomass) initially increases but eventually shows a sharp decline across each of the six chronosequences, in the order of 2,000 10,000 years following the disturbance that created the chronose-quence (Fig 9.1; Wardle et al 2004) This is accompanied by changes in forest structure and height for these sequences (Crews et al 1995; Richardson et al 2004; Wardle et al 2003, 2004) This decline in forest stature during retrogression has been shown to be accompanied by reductions in net primary productivity for the Arjeplog and Hawaii sequences (Wardle et al 2003; Vitousek 2004), and by shifts

in respiratory and photosynthetic characteristics of the dominant forest vegetation for the Franz Josef sequence (Turnbull et al 2005; Whitehead et al 2005) The declines in forest biomass and function are almost certainly driven by the aging of the soil and a decline in soil fertility Importantly, for all six chronosequences, there were general increases over time in the substrate nitrogen to phosphorus, notably in the uppermost layer of humus or, in the case of Cooloola (in which a humus layer is effectively lacking), mineral soil (Fig 9.2) In all six cases, signifi-cant increases in these ratios occurred at around the time that a decline in forest biomass was beginning to occur, indicative of ecosystem retrogression (Fig 9.1; Wardle et al 2004) Further, for each chronosequence, the nitrogen to phosphorus ratio during the retrogressive phases became higher than the ‘Redfield Ratio’ (Redfield 1958), i.e the ratio that has been previously postulated by aquatic ecologists as the ratio above which phosphorus becomes limiting relative to nitro-gen Consistent with this, there is evidence from several of these sequences for the litter or foliar nitrogen to phosphorus ratio to increase during retrogression (Vitousek 2004; Wardle et al 2004; Coomes et al 2005), indicative of increasing relative

temperature
(C)

temperature
(C)

precipitation sum

Parent material

chronosequence (years)

0
02

0N,

49

0E

boulders; moraine

N,

W

limestone, igneous intrusions

30

0S,

30

0E

25

0S,

10

0E

06

0S,

30

0E

N,

o W