Springer Old Growth Forests - Chapter 4 ppt

Old and tall trees usually have a leaf-to-mass ratioLMR = leaf mass per total tree biomass of between 5% and 20%, with theremaining biomass in the stem, branches, and roots Bernoulli and

Ecophysiological Characteristics

of Mature Trees and Stands – Consequences for Old-Growth Forest Productivity

Werner L Kutsch, Christian Wirth, Jens Kattge, Stefanie Nollert,

Matthias Herbst, and Ludger Kappen

4.1 Introduction

Trees increase their relative fitness to competing trees or to other life forms bothdirectly and indirectly, by growing tall, as increased light interception increasesphotosynthesis (direct) and simultaneously making this resource unavailable tocompetitors (indirect) Consequently, trees that grow taller, larger, or havegreater shading power may dominate smaller trees with less shading power.However, as trees become older and grow taller they face constraints that differdrastically from those experienced by smaller species or early ontogeneticstages Falster and Westoby (2003), who used game-theoretic models to learnabout the evolutionary background of tree height, summarised thus: ‘heightincreases costs as past investment in stems for support, as continuing maintenancecosts for the stems and vasculature, as disadvantages in the transport of water toheight and as increased risk of breakage’ No wonder that trees do not growinfinitely high In general, absolute and relative growth rates tend to decreasewith age and height This decline in productivity observed at both the tree andstand level has been attributed to a range of processes, e.g., increasingrespiratory demand and limitation of photosynthesis on the tree level, and, onthe stand level, increasing sequestration of nutrients in slow-decomposing litterand ecophysiological differences between early-, mid- and late-successionalcanopies This chapter will review these current hypotheses, first on the treelevel, then the stand level, as well as in the context of successional changes ofcommunity composition

A widespread hypothesis about the decrease in growth with tree age is based on theidea that higher respiratory demand limits resources for wood growth Kira andShidei (1967) first developed this hypothesis from empirical data over 10 years It

C Wirth et al (eds.), Old ‐Growth Forests, Ecological Studies, 207 57 DOI: 10.1007/978 ‐3‐540‐92706‐8 4, # Springer‐Verlag Berlin Heidelberg 2009

became well accepted that forest production declines with age because woodyrespiration increases while gross primary productivity (GPP) remains constant oreven decreases slightly This idea was adopted by Odum (1969) in his well-knowntheory of ecosystem succession, which predicts that ecosystem respiration increaseswith community age and balances a slightly decreasing GPP until the differenceapproaches zero at steady state.

The net carbon yield of a tree depends on the ratio of assimilating organs tothat of respiring tissues Old and tall trees usually have a leaf-to-mass ratio(LMR = leaf mass per total tree biomass) of between 5% and 20%, with theremaining biomass in the stem, branches, and roots (Bernoulli and Ko¨rner 1999).The cost for maintaining these non-productive tissues may increase when treesgrow taller Especially for trees growing at high elevation, Wieser et al (2005) haveargued that, besides low temperatures and a short vegetation period, an imbalance

in carbon-accumulating foliage versus respiring tissues might upset the carbonbalance (see also Ha¨ttenschwiler et al 2002) However, even though integrativestudies have shown that the fraction of net photosynthetic production consumed

by autotrophic respiration can vary between 30% and 70% (Sprugel et al 1995;Luyssaert et al 2007), no significant age effects on this ratio were revealed Thereason for this might be a decrease in activity (biomass-specific respiration rate) ofaccumulated woody tissue Such observations oppose the traditional view that treeproduction decreases with age due to increasing respiratory demand Moreover,several more studies have shown that a decrease in net primary productivity inold-growth forests if it occurs is related more to decreasing photosynthesis inold and tall trees (as well as in old-growth forest canopies) than to increasingrespiratory demand (Ryan and Yoder 1997)

4.3 Limitations of Photosynthesis

The mechanisms that could lead to decreased photosynthetic income in high treesand old-growth forests are still unclear The widespread hypothesis of hydrauliclimitation will be discussed in the first part of this chapter This more source-relatedmechanism will then be compared to the more sink-related mechanisms that havebeen introduced recently At the end of the chapter we will return to the reduction ofphotosynthesis in the context of community composition, as late-successionalspecies may show an imperfect acclimatisation to full sunlight

4.3.1 Hydraulic Limitation

The basic assumption of the hydraulic limitation hypothesis (HLH) is that, astrees grow taller, gravitational potential, which increases by 0.01 MPa per metre ofheight (Fig 4.1), and increased path length decrease leaf water potential (Fig 4.2a)

Fig 4.1 The hydraulic

limitation hypothesis (HLH)

proposes decreased leaf

specific hydraulic

conductance as trees grow in

height The figure shows the

increase in gravitational

potential with tree height.

Trees have to overcome this

potential to transport water to

the leaves.

Fig 4.2 a Xylem pressure of small branches measured at predawn (upper group) and midday (lower group) of redwood trees at Humboldt Redwoods State Park, California during September and October 2000 b Foliar carbon isotope composition (d 13 C) of redwood trees at Humboldt Redwoods State Park, California increases with height within the crowns of 5 trees over 110 m tall, and among the tops (filled circles) of 16 trees from 85 to 113 m tall Different symbol types denote different trees and are consistent in a and b (from Koch et al 2004, with permission).

and, consequently, stomatal conductance Promoters of the HLH usually employ asimplified Ohm’s law analogy (Tyree and Ewers 1991) to provide a mathematicaldescription of differences in stomatal conductance with height:

GC¼KL DC

whereGC = canopy conductance for water vapour, KL = hydraulic conductancefrom soil to leaf, DC = soil-to-leaf water potential difference, andD = leaf to airsaturation deficit Since decreased stomatal conductance reduces photosyntheticuptake, Ryan and Yoder (1997) proposed the HLH as a mechanism to explain theslowing of height growth with tree size and the maximum limits to tree height.Barnard (2003) and Ryan et al (2004) refined the HLH and stated that fivenecessary components have to be fulfilled: ‘(1) stomata must close to maintain

CLEAFabove a minimum, critical threshold and this threshold must be the same forall tree heights; (2) stomata must close in response to decreased hydraulic conduc-tance; (3) hydraulic conductance must decrease with tree height; (4) stomatalclosure promoted by reduced hydraulic conductance must cause lower photosyn-thesis; and (5) reduction in photosynthesis in older, taller trees must be sufficient toaccount for reduced growth.’ The HLH has been widely discussed and has inspired

a huge number of studies on tall trees during the past decade

4.3.1.1 Empirical Evidence for the Hydraulic Limitation Hypothesis

4.3.1.1.1 Calculation of Hydraulic Conductance

The hydraulic conductance can be calculated either for a single leaf in a certainposition in a tree or for the whole tree In the first case, the hydraulic conductance isrelated to the insertion height of the leaf, in the second to the total height of the tree

In both cases the hydraulic conductance is related to the leaf area

For a single leaf, the specific hydraulic conductance can be calculated from thefollowing equation:

In order to compensate for the gravitational component, the leaf has to decrease itspotential by the value of rgh Gradients of leaf water potential with tree height wereindeed found in several studies (Waring and McDowell 2002; Koch et al 2004)

Predawn measurements of Cleafduring periods with high soil moisture reflectthe gravitational potential very well (Koch et al 2004), and therefore can be used topartition total water potential into ‘gravitational’ and ‘non-gravitational’ fractions(Waring and McDowell 2002; McDowell et al 2002a, 2002b, 2005; Delzon et al.2004) Correcting Cleaffor the gravitational component (Celeaf, according to Delzon

et al 2004) allows direct calculation of DC between soil and leaf and incombination with transpiration measurements of kl Whole tree hydraulic con-ductance (KL) is usually estimated by relating sap flow measurements to waterpotential (e.g Hubbard et al 1999) Delzon et al (2004) measured sap flow about 1 mbelow the live crown, and Cleafon leaves in the upper crown Several studies haveshown thatKLdecreases as trees grow taller and age (Hubbard et al 1999; Delzon

et al 2004)

4.3.1.1.2 Gas Exchange

Direct measurements of leaf gas exchange by means of infrared gas analysers withleaf-scale cuvettes may support the HLH if lower values of leaf net photosynthesis(A) and stomatal conductance (gs) are associated with lower values ofkl In mostcases, neither photosynthetic capacity (Amax) nor leaf or needle nitrogen wasreduced but increased stomatal closure caused a more sensitive response ofA toreduced air humidity at greater heights in at least some studies (Yoder et al 1994;Hubbard et al 1999; McDowell et al 2005) A decrease in stomatal conductance orincreased stomatal sensitivity with height, which was also observed by Delzon et al.(2004), is commonly interpreted as a result of reduced hydraulic conductance

4.3.1.1.3 Stable Isotopes

Another approach utilises the stable carbon isotope ratio (d13C) of foliage, which isclosely related to leaf gas exchange (Farquhar et al 1989; Ehleringer et al 2002).The discrimination against 13CO2by the CO2-fixing enzyme increases with theleaf-internal CO2concentration In conditions of low stomatal conductance theleaf-internal CO2concentration is reduced and, consequently, the d13C of assim-ilates is enhanced (Meinzer 1993; Flanagan and Ehleringer 1998) Accordingly, anincrease in foliage d13C with tree size for individuals of the same species grown insimilar environments (Fig 4.2b) can be related to hydraulic constraints to gasexchange, and has been observed in many studies (Yoder et al 1994; Hubbard

et al 1999; Waring and McDowell 2002; Phillips et al 2003; Koch et al 2004;McDowell et al 2005; Schoettle 1994)

Overall, the results from these approaches indicates that height, and the resultinggravimetrical and hydraulic strain can burden photosynthetic uptake and possiblyfurther growth of old and tall trees However, it remains unclear whether hydrauliclimitation is exclusively the reason for growth cessation in trees, in particular in treesthat remain shorter than the theoretically calculated maximum tree height of about 120

m (Koch et al 2004) Therefore, several reservations about the HLH have beenformulated

4.3.1.2 Reservations Against the Hydraulic Limitation Hypothesis

The most important argument against the HLH is the fact that trees can compensatefor increased path length by changes in xylem structure, such as the production ofxylem vessels with increased conductivity (Pothier et al 1989) Xylem architecturevaries between species and is very plastic within species or even within a singletree Weitz et al (2006) claimed that there is a general trend of tapering of conduitdimensions that might be regulated by a hormonal signal originating in the apices

of tree branches However, they described single vessel dimensions, whereasMencuccini and Grace (1996), who worked on whole trees, reported a proportionalincrease of branch over stem wood sapflow area with age in Scots Pine, which canalso be seen at least partially as hydraulic compensation The formal hydraulicmodel of Whitehead et al (1984) predicts compensation by a homeostatic balancebetween transport capacity and transpiration demand Consequently, it was argued

by Becker et al (2000), that‘any path-length effects on water transport could befully compensated if this was advantageous to the plant’

Another way of compensation is to decrease transpiring leaf area relative toxylem conductive area with height (Vanninen et al 1996) Cochard et al (1997)found forFraxinus excelsior L., that the xylem resistance of single branches wascorrelated to their leaf area, thus keeping the leaf-area-specific conductivity con-stant Several other studies showed adaptations in the leaf area to sapwood arearatio (AL:AS) in order to compensate for hydraulic or gravitational limitation(Waring and McDowell 2002; Delzon et al 2004; McDowell et al 2005) whichresults in a decrease in productivity, but on a whole plant or stand level

Furthermore, trees can compensate by increasing the fine-root:foliage ratio(Sperry et al 1998; Magnani et al 2000) or by decreasing the minimum leafwater potential and consequently increasing the water potential gradient betweensoil and leaf (Hacke et al 2000) In addition, a role in increased water storage in thestem for compensation is discussed (Phillips et al 2003) Nevertheless, all thesecompensating reactions of tall trees are not ‘for free’ but are paid for by increasedrespiration costs

4.3.2 Reduced Sink Strength

An alternative to the HLH and other theories that support source regulation, tion of photosynthesis may also be induced by product inhibition of photosynthates.This kind of sink regulation can be explained by at least two mechanisms:

reduc-(1) Phloem transport may be reduced in tall trees because the resistance betweensource and sink also increases with distance In-vivo whole-plant measurementshave demonstrated that carbon flow rates are dependent not only on the proper-ties of the sink, but also on the properties of the whole transport system (Gould

et al 2004; Minchin and Lacointe 2005)

(2) There is some evidence that old and tall trees cease later growth genetically.Given the fact that genetic programs were generated over thousands of genera-tions, the cessation of height growth in old trees may be explained by thedevelopment of several mechanisms inducing a high risk/advantage-ratiowhen trees grow taller The advantage is high-light supply for the highesttrees, whereas the risks comprise mechanical damage due to windthrow orsnowbreak, or climatic damage by frost or desiccation As soon as a tree hasgrown taller than its neighbours, these risks will exceed the advantages ofgrowing even taller Understanding the evolution of height growth of trees interms of risk (or cost)-to-advantage assessment in an uncooperative game(Falster and Westoby 2003), results in a high probability of genetic cessation

of height growth and resulting sink reduction

It is well known from leaf-level measurements that a reduction in sink strengthresults in an increase in starch and soluble sugars within the leaves followed bydown-regulation of photosynthetic capacity (Equiza et al 2006) Hoch et al (2003)and Ko¨rner et al (2005) showed that whole trees also exhibit high concentrations ofstorage carbohydrates, which suggests that growth is limited by the availability ofsinks but not carbon supply (Day et al 2001, 2002) Whether this lack of growthstimulus is related to an intrinsic genetic programme or progressive nutrientlimitation is not known The strong growth response of mature forests towardsatmospheric nitrogen deposition in Europe may indicate the latter (Schulze 2000;Mund et al 2002; Magnani et al 2007)

Irrespective of the underlying mechanism, old and tall trees eventually reach a pointwhere they become less efficient in assimilating carbon for growth per unit leafarea To what extent this physiological response translates into individual-levelgrowth performance, and eventually into stand-level decline in productivity, is stillsubject to debate (Gower et al 1996; Ryan et al 1997; Magnani et al 2000; Weinerand Thomas 2001; Binkley et al 2002) As pointed out in a seminal review by Ryan

et al (1997), stand-level net primary production could theoretically decline because

of (1) a decline in assimilation rate at a given leaf area, or (2) a decline in total leafarea at a given assimilation rate In the first case, the decline is driven purely byphysiological changes (see above); in the latter purely by structural changes of thecanopy, e.g resulting from leaf abrasion or tree mortality The 13 chronosequencespresented by Ryan et al (1997) clearly exhibited age-related decline of productivity

at the stand-level Stem growth peaked at the time of maximum leaf area, which, inthis case, was after 29 22 (SD) years It is important to note that this very earlyonset of observed growth reduction rules out the notion that a physiological reaction

to ‘majestic’ size or high age is the major driver of the stand-level decline inproductivity sensu Ryan et al (1997) In at least some chronosequences there was

a post-peak decline in growth efficiency (i.e stem-growth per unit leaf area), which

is why the authors argued that age-related decline results from both structural andphysiological changes However, the chosen chronosequences were by no meansrepresentative of the world’s forests; all were even-aged monocultures, most ofthem were managed, and there was a strong bias towards shade-intolerant conifer-ous pioneers These grow up quickly in a monolayer and respond strongly tocrowding by down-regulating the stand-level leaf area With productivity beingclosely related to leaf area index (LAI), the productivity peak may thus merelyreflect the ‘over-shooting’ leaf area prior to the onset of self-thinning.

Recently, a new global database of forest productivity that comprises data fromboth chronosequences and individual stands has become available (Luyssaert et al.2007) In addition to stand-level estimates of net primary productivity, the databasecontains details on the methodology, and a wide range of site descriptors that can beused as covariates or to filter and stratify the data We used the database to modelthe aboveground and total net primary productivity (abbreviated ANPP and totalNPP, respectively) as a linear function of LAI and stand age per se, thus separatingphysiological and structural effects Because productivity and age are oftenconfounded with site variables (stands become older on sites with more adversegrowing conditions), we included two climate variables, mean annual temperatureand annual precipitation, as additional predictors All predictor variables werestandardised to a mean of zero and a standard deviation of one With this transfor-mation, the intercept of the models is the productivity at the means of all predictors,and the absolute values of the coefficients reflect the explanatory strength of therespective predictors For model simplification, we applied backward selectionbased on the Akaike Information Criterion The best candidate models are pre-sented in Table 4.1 The analysis was done separately for coniferous and broad-leaved forests of the northern hemisphere Mixed stands and stands subject tofertilisation or irrigation were excluded

All four variables were significant predictors of ANPP in conifers ANPP at thecovariate means was 324 g C m 2year 1 Temperature had the strongest influence,followed by LAI (Fig 4.3a) and precipitation The negative effect of stand age,which was significant (at a = 0.05) but relatively weak, indicated a slightdecline in aboveground growth efficiency with age In original units, this translates

to 30 g C m 2year 1in 100 years In comparison with ANPP, the total NPP was 1.6times higher (intercepts 324 and 510 g C m 2year 1, respectively) and the fourvariables explained a higher fraction of the variance in total NPP (adjustedR2=0.50 and 0.74, respectively) The importance of predictors decreased in the sameorder (temperature> LAI > precipitation > age, Fig 4.3b again shows LAI as anindicator of ANPP) The similarity of the models for ANPP and NPP suggest thatshifts in allocation from above- to below-ground NPP are of little relevance Forbroadleaved forests, stand age was not a significant predictor of ANPP The overalllevel of ANPP as reflected by the intercept was 506 g C m 2year 1and thus higherthan in coniferous forests The ‘minimum model’ contained only LAI and precipi-tation as predictors; the latter was not significant The minimum model for totalNPP was structurally similar, but the influence of precipitation was significant andthe intercept was 1.35 times higher The lower ratio of total to aboveground NPP

illustrates that broadleaved forests allocate less carbon to belowground productivitythan coniferous forests, which dominate under harsher (drier, colder) growingconditions In summary, differences in ANPP and NPP when controlled forclimate were driven mostly by leaf area This result suggests that structuralchanges leading to reduced displays of leaf area are more important than a deterio-ration in photosynthetic performance.

on Age/Size-Productivity Relationships

Thus far we have been discussing the ecophysiological consequences of tree statureand age Besides these two aspects of being a tall tree, major drivers of productivity,such as light, nutrient and water availability, may change significantly and predict-ably throughout the development of a single tree Another aspect is that secondarysuccessions usually involve species turnover, which in turn introduces a shift in thespectrum of relevant ecophysiological and morphological traits In the following,

we discuss these two aspects in more detail

Table 4.1 Coefficients, significance level and indicators of model performance for the statistical analysis of aboveground and total net primary productivity (ANPP and NPP, respectively) Because all predictors were z transformed prior to analysis, the absolute magnitude of the coefficients is indicative of their relative importance df Degrees of freedom, Std.err standard error, p probability that coefficient equals zero, LAI leaf area index, P precipitation sum, T mean annual temperature, Age stand age

Parameter Std.err t Value p Parameter Std.err t Value p ANPP Coniferous forests Deciduous forests

Intercept 324.8 11.7 27.63 <0.001 506.8 21.2 23.9 <0.001 LAI 99.7 13.8 7.25 <0.001 93.1 21.6 4.3 <0.001

Fig 4.3 Relationship between aboveground primary productivity (ANPP; g C m2year1) and leaf area index (LAI; m2m2) for coniferous (a) and deciduous (b) forests of the temperate and boreal biome The symbols denote stand age classes: open circles 1 100 years, open triangles

101 200 years, filled circles 201 400 years, filled triangles >400 years The size of the symbols is proportional to the mean annual temperature (without scale)

4.5.1 Light, Water and Nutrient Availability

In the struggle for light, trees have developed different strategies Light-demandingpioneer species arrive early after stand-replacing disturbances, establish well, andgrow fast They dominate the early stages of succession, but are then graduallyovergrown by more shade-tolerant species Shade-tolerant species usually starttheir development in the understorey and reach the canopy after a long period ofsuppression Shade-avoiding gap-phase species take an intermediate position As arule of thumb, size and age at the population level are negatively correlated withlight availability in pioneers and positively correlated in shade-tolerant species Thesign of the correlation tends to aggravate size-/age-related decline in pioneers, butmitigates it in shade-tolerant species

Water availability may also change with size, and the sign of the response varieswith site conditions and root architecture in a predictable fashion A positivecorrelation between individual tree structure and water availability is expected toemerge when trees protrude through a dry topsoil into subsoil aquifers by means oflong tap roots (Irvine et al 2004) A negative correlation usually occurs duringstand development on shallow soils where root competition intensifies with standage and biomass, often inducing stagnation of growth (Oliver and Larson 1996).Post-fire regeneration on permafrost soils represents an extreme example where theavailable unfrozen soil volume, the active layer, even shrinks during the course

of stand development This usually induces a cessation of tree growth after about

60 years in boreal larch and black spruce stands irrespective of tree size (Abaimov

et al 1997; Abaimov and Sofronov 1996) There are often pronounced changes innutrient availability with succession Most disturbances leave behind soils that aretemporarily enriched in nutrients due to the decomposition of the newly availabledead plant material and also, in the case of fire, thermal mineralisation (Neary et al.1999) In secondary succession forest, re-growth progressively locks up nutrients(Vitousek and White 1981; see Chap 9 by Wardle, this volume) Furthermore, litterquality, and thus remobilisation of nutrients, decreases as the proportion of woodylitter increases over time This led Gower et al (1996) to hypothesise that the so-called ‘age-related’ decline in forest productivity can be explained by the temporaldynamics of nutrient availability (cf Sect 4.3.2 above) Wardle (Chap 9, thisvolume) discusses additional mechanisms evoking the phenomenon of reducednutrient availability in old versus young forests

4.5.2 Shifts in Ecophysiological Traits with Changes

in Community Composition

Secondary forest succession usually involves species turnover (see Chap 5 byWirth and Lichstein, this volume) In other words, tree species constituting old-growth stands are not likely to be the same as those that founded the community a