Effects of stand age and tree species on canopy ... pdf/ewers... · Lamb. (jack pine), and Picea...

Plant, Cell and Environment

(2005)

28

, 660–678

660

© 2005 Blackwell Publishing Ltd

Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2005? 2005

28?660678Original Article

Transpiration and canopy average stomatal conductanceB. E. Ewers

et al.

Correspondence: B. E. Ewers. Fax:

+

1 307 766 2851; e-mail:[email protected]

Effects of stand age and tree species on canopy transpiration and average stomatal conductance of boreal forests

B. E. EWERS

1

*, S. T. GOWER

2

, B. BOND-LAMBERTY

2

& C. K. WANG

3

1

Department of Botany, University of Wyoming, Laramie, WY 82071 USA,

2

Department of Forest Ecology and Management, University of Wisconsin, Madison, WI 53706 USA and

3

Ecology Program, NorthEast Forestry University, Harbin 150040, China

ABSTRACT

We quantified the effect of stand age and tree species com-position on canopy transpiration (

E

C

) by analysing transpi-ration per unit leaf area (

E

L

) and canopy stomatalconductance (

G

S

) for boreal trees comprising a five standwildfire chronosequence. A total of 196 sap flux sensorswere used on 90 trees consisting of

Betula papyrifera

Marsh (paper birch; present in the youngest stand),

Popu-lus tremuloides

Michx (quaking aspen),

Pinus banksiana

Lamb. (jack pine), and

Picea mariana

(Mill.) (blackspruce). While fine roots were positively correlated withstand

E

C

; leaf area index, basal area, and sapwood areawere not. Stands less than 70 years old were dominated by

Populus tremuloides

and

Pinus banksiana

and standsgreater than 70 years old were composed almost entirely of

Picea mariana.

As

Populus tremuloides

and

Pinus bank-siana

increased in size and age, they displayed an increasingsapwood to leaf area ratio (

A

S

:

A

L

), a constant minimumleaf water potential (YYYY

L

), and a constant proportionalitybetween

G

S

at low vapour pressure deficit (

DjG

Sref

) and thesensitivity of

G

S

to

D

(–dddd

). In contrast,

A

S

:

A

L

, minimumYYYY

L

, and the proportionally between –dddd

and

G

Sref

decreasedwith height and age in

Picea mariana

. A

G

S

model thatincluded the effects of

D

,

A

S

:

A

L

, tree height, and for

Piceamariana

an increasing soil to leaf water potential gradientwith stand age, was able to capture the effects of contrast-ing hydraulic properties of

Picea mariana

,

Populus trem-uloides

and

Pinus banksiana

during stand developmentafter wildfire.

Key-words

: chronosequence; fire; hydraulic conductance;leaf water potential; sapwood-to-leaf area ratio; tree height.

INTRODUCTION

Water loss from a stand of plants is ultimately a function ofplant water stress which can occur in multiple form, includ-ing atmospheric, soil, and plant internal water balance and

at multiple time scales ranging from seconds to years. As aresult of atmospheric dryness and/or high photosyntheticrates, woody plants experience water stress at high transpi-ration rates due to hydraulic limitations to water transportfrom the roots to the leaves (Tyree & Sperry 1988; Sperry

et al

. 1998). As the vapour pressure deficit (

D

) increases,stomata close in response to dropping leaf water potentials(

Y

L

) in a cue that is linked to transpiration rather than

D

(Mott & Parkhurst 1991). While the mechanism of the sig-nal transduction and the identity of the cells receiving thesignal and are not known (Salleo

et al

. 2001; Franks 2004),available evidence suggests plants regulate transpirationvia changes in

Y

L

or leaf relative water content that resultfrom whole plant water status (Meinzer & Grantz 1991;Saliendra, Sperry, & Comstock 1995; Cochard, Breda &Granier 1996; Nardini, Lo Gullo & Trancanelli 1996; Salleo

et al

. 2000; Franks 2004).Such results argue for an analysis of stomatal responses

to

D

from the stand point of the regulation of transpiration(Monteith 1995) and

Y

L

(Oren

et al

. 1999a) to avoid poten-tially fatal cavitation of xylem (Tyree & Sperry 1989; Sperry

et al

. 1998). Regulation of

Y

L

occurs to maintain a homeo-stasis of water in the leaves for optimal carbon uptake as aresult of equilibrium between maximum carbon uptake andmaximum water supply of the soil (Katul, Leuning & Oren2003). The water supply side of this equilibrium can bedescribed by the following model (Whitehead & Jarvis1981; Whitehead, Edwards & Jarvis 1984; Sperry 1995;Oren

et al

. 1999a):

(1)

where

G

S

is canopy average stomatal conductance(mmol m

-

2

s

-

1

),

K

S

is the whole tree hydraulic conductanceper unit sapwood area (mmol m

-

2

s

-

1

MPa

-

1

),

A

S

:

A

L

is sap-wood-to-leaf area ratio (m

2

m

-

2

),

D

is vapour pressure def-icit (mmol mmol

-

1

),

Y

S

is soil water potential (MPa),

Y

L

isleaf water potential (MPa), and

h

r

W

g

is the gravitationalpull (

g

) on the water column of density

r

W

and height

h

.The response of

G

S

to environmental variables can bequantified using the following series of multiplicative func-tions formulated by Jarvis (1976)

G KAA D

h gS SS

LS L w= ◊ ◊ ◊ - -( )1

Y Y r

Transpiration and canopy average stomatal conductance

661

© 2005 Blackwell Publishing Ltd,

Plant, Cell and Environment,

28,

660–678

(2)

where

G

Smax

is maximum

G

S

,

Q

o

is photosynthetic photonflux density, and

T

A

is air temperature. By carefullyselecting subsets of data in a given range of

Q

o

,

T

A

, andsoil moisture conditions to remove correlations betweendriving variables (Rayment, Loustau & Jarvis 2000), theresponse of

G

S

to

D

can be isolated and analysed withEqn 1.

G

Smax

can be more precisely defined using itsproxy

G

Sref

which is

G

S

at

D

=

1 kPa (Ewers

et al

. 2001a).When defined in this manner, the relationship between

G

Sref

and

D

can be described by the following (Oren

et al

.1999a):

(3)

where –

d

is the sensitivity of the

G

S

response to ln

D

or theslope of

G

S

versus ln

D

(–d

G

S

/dln

D). GSref convenientlyoccurs within the D range of most species and –d is constantover the entire range of D of species or individuals unlike–dGS/dD. Across a large range of species, and even envi-ronmental conditions within species, –d is 0.6 GSref (Orenet al. 1999a, b, 2001; Ewers et al. 2001b; Gunderson et al.2002; Addington et al. 2004). The 0.6 proportionalitybetween –d and GSref results from the regulation of mini-mum YL to prevent excessive xylem cavitation as describedby Eqn 1. Species or individuals with high GSref have thedisadvantage of having a proportionally high –d and greaterabsolute reduction in GS with increasing D whereas specieswith low GSref have the advantage of having a low –d andsmaller absolute reduction in GS with increasing D. Impor-tant deviations from the 0.6 proportionality occur when: (1)a species allows the minimum YL to drop with increasingD; (2) the range of D increases; or (3) the ratio of boundarylayer conductance to stomatal conductance is low (Orenet al. 1999a). The first two conditions result in a ratio of –dto GSref that is less than 0.6 as a result of plants that haveless strict regulation of YL such as drought-tolerant desertspecies (Oren et al. 1999a; Ogle & Reynolds 2002). Thethird condition results in a ratio of –d to GSref that is greaterthan 0.6 (Oren et al. 1999a)

The hypothesis that hydraulics limit tree height growthand carbon uptake (Gower, Mcmurtrie & Murty 1996;Ryan & Yoder 1997) is currently debated (Becker, Meinzer& Wullschleger 2000; Bond & Ryan 2000). Experimentalevidence suggests that hydraulic limitations can be over-come through increases in AS : AL (Schafer, Oren & Ten-hunen 2000; McDowell et al. 2002a), sapwood specificconductivity (Pothier, Margolis & Waring 1989; Pothieret al. 1989), increased difference between the soil and leafwater potential (Hacke et al. 2000; McDowell et al. 2002b),increased root surface area (Sperry et al. 1998; Magnani,Mencuccini & Grace 2000), and increased water storage(Phillips et al. 2002). A recent literature survey demon-strated that across many conifers AS : AL increases inresponse to tree height while AS : AL decreases with heightin conifers with a low AS : AL and long leaf longevity(McDowell et al. 2002a). Such a response in low AS : AL

species (Picea spp. and Abies spp.) may be explained by a

G G f Q f D f T fS S O A L= ( ) ( ) ( ) ( )max Y

G G DS Sref= - ◊d ln

longer period of juvenile wood, which may have increasedconductivity in comparison with mature wood (Magnani etal. 2000). In addition, decreasing AS : AL would providemore leaf area and perhaps convey a competitive advan-tage over other trees that increase AS : AL with tree size.However, even with large shifts in AS : AL in Picea abies dueto changes in water and nutrient supplies there was nodeviation from the predicted 0.6 ratio (Eqn 2) between –dand GSref (Ewers et al. 2001b).

To our knowledge, the impact of tree age and height ontranspiration per unit leaf area (EL) and GS has only beeninvestigated in stands of single species or only on thedominant species within stands (Ryan & Yoder 1997;Magnani et al. 2000; Ryan et al. 2000; Schafer et al. 2000;McDowell et al. 2002b; Phillips et al. 2002). Such studiesare not suited to making inferences concerning the impactof stand age on stand canopy transpiration (EC) especiallywhen such stands include multiple species. Mixed standsof species, composed of deciduous trees which enhancenutrient cycling and coniferous trees which limit cycling,may have fundamentally different stand productivities(Légaré, Paré & Begeron 2004). Mixed forests can conse-quently be expected to have varying EC with changingspecies composition; especially in boreal forests wherenutrient cycling is limited by cold climatic conditions(Légaré et al. 2004).

In light of these expected differences in mixed versusmonospecific stands, the overall objective of this study wasto quantify and explain changes in EC across a 150-yearwildfire chronosequence in central Manitoba that has achanging tree size and species composition as a result ofecological succession (Bond-Lamberty et al. 2002b; Wang,Bond-Lamberty & Gower 2003; Table 1). We specificallyinvestigated the effects of forest stand age, tree species,and tree hydraulic architecture and their interaction on GS

and EL as drivers of EC in a boreal climate where treeheight is ultimately limited by cold environments (Gutsell& Johnson 2002). In five stands ranging in age from 12 to151 years, we quantified EC, EL and GS in four differentspecies Populus tremuloides Michx. (trembling aspen),Betula papyrifera March (paper birch), Picea mariana(Mill.) (black spruce), and Pinus banksiana (Lamb.) (jackpine). The specific objectives of this study were: (1) todetermine the interactive effects of tree species and standage on EC, EL and GS; and (2) evaluate a GS sensitivity toD model across the four species and five stand ages as ameans of explaining the findings of objective 1. Wehypothesized that: (1) early successional species (Populustremuloides and Pinus banksiana) would have a higher EL

than late successional species (Picea mariana) and earlysuccessional species’ EL would decline more with age thanlate successional species; (2) AS : AL would be positivelycorrelated to height in Populus tremuloides and Pinusbanksiana, but would decrease in Picea mariana; and (3)within a given species, minimum YL would be maintainedand all of the tree sizes and species would maintain a 0.6proportion between –d and GSref across the range of standages.

662 B. E. Ewers et al.

© 2005 Blackwell Publishing Ltd, Plant, Cell and Environment, 28, 660–678

MATERIALS AND METHODS

Site description

The study was conducted near Thompson, Manitoba fromJune to September, 2001 and includes the BOREAS North-ern Study Area (Sellers et al. 1995; 55∞53¢ N, 98∞20¢ W). Allstands originated from stand-killing wildfires in the years1989, 1981, 1964, 1930 and 1850. The two oldest stands, withages 71 and 151 years, were dominated by a Picea marianaoverstorey and the three younger stands, with stand ages of12, 20, and 37 years, were a mix of Picea mariana, Pinusbanksiana and Populus tremuloides; Betula papyrifera waspresent in the youngest stand (Table 1). Soils of these siteswere sedimentary materials deposited by glacial LakeAgassiz. The sites were on upland, moderately drained claysoils, although the 1930 and 1964 stands were consideredwell-drained sites derived from morainal deposits of sandand gravel (Bond-Lamberty et al. 2002b). Mean annual airtemperature was 0.8 ∞C with mean January and July airtemperatures of -19.7 and 16.5 ∞C, respectively. Meanannual precipitation was 439 mm.

Calculation of AS and AL

The sapwood area (AS), leaf biomass, and diameter atbreast height (d.b.h) data were obtained from Gower et al.(1997) and Bond-Lamberty, Wang & Gower (2002a). Leafbiomass was converted to leaf area (AL) using site- andspecies-specific leaf area (Bond-Lamberty et al. 2002b;Bond-Lamberty, Wang & Gower 2003). Tree height wasmeasured using a distance tape and clinometer. Sapwoodarea in the small Betula papyrifera (Table 1) was calculatedusing a bark thickness of 1 mm (B.E. Ewers, personalobservation).

JS measurements and calculation of EL

We measured sap flux per unit conducting xylem area (JS)in stem xylem using two types of sap flux sensors, Granier-

type (Granier 1987) in trees >4.0 cm diameter at 1.3 mabove ground and Kucera-type (Ewers et al. 2002) in trees<2.0 cm in diameter at 1.3 m above ground. The number ofsampled trees of each type is shown in Table 1. The inven-tory data of Bond-Lamberty et al. (2002b) and Wang et al.(2003) were used to either select 12 trees (when only asingle species was present) or eight trees (when multiplespecies were present) for Granier-type sap flux measure-ment that represent the entire diameter range (> 4 cm) ofthe five stands or to select six to seven trees <4 cm forKucera-type sap flow measurements. To accommodate thissampling scheme, circular plot radii varied with the differ-ent aged stands (7, 6, 15, 13 and 6 m for the 12, 20, 37, 70and 150-year-old stands, respectively).

Many recent studies have established the need for radialand circumferential measures of JS from Granier-type sen-sors for appropriate tree and stand scaling (Phillips, Oren& Zimmerman 1996; Oren et al. 1998; Lu, Miller & Chacko2000; Ewers & Oren 2000; Lundblad, Lagergren & Lin-droth 2001; Ewers et al. 2002; James et al. 2002). Across theentire chronosequence, we measured JS at three stem loca-tions: the outer 20 mm of the xylem on the north side(JSnorth), 21–40 mm depth of the xylem (JSin) to examineradial patterns in all trees > 4.0 cm, and the outer 20 mm ofxylem on the south side (JSsouth) of all trees measured withGranier-type sensors to account for circumferential trends.When the depth of sapwood was less than 20 mm for JSnorth

or JSsouth, or less than 40 mm for JSin we used the correctionsdescribed by Clearwater et al. (1999) to determine theappropriate JS. JSnorth was measured continuously but wealternated between measurements of JSin or JSsouth every twoweeks in order to preserve power supplied by solar panels.

We calculated a stem mean JS (Oren et al. 1998; Ewers &Oren 2000; Ewers et al. 2002) using the following equation

(4)JW J

W

i ii

ii

S

S=

3

=

3=Â

Â1

1

Table 1. Stand age, species, density of non-seedling trees, diameter at breast height (d.b.h), basal area (AB), leaf area index (L), height (Ht), and sap flux sample size (n) for the five chronosequence stands in 2001

Stand age(years) Species

Density(No. ha-1)

d.b.h.(cm)

AB

(m2 ha-1)L(m2 m-2)

Ht(m) n

12 Populus tremuloides 6800 1.2 2.4 0.2 2.7 0/0/7Betula papyrifera 6200 1.0 2.2 0.2 2.5 0/0/5

20 Populus tremuloides 3500 3.5 3.4 0.3 5.0 6/0/6Pinus banksiana 6000 5.7 5.9 0.9 4.9 12/6/0Picea mariana 4250 1.9 1.1 0.2 2.5 0/0/6

37 Populus tremuloides 4200 7.7 8.2 0.3 9.4 8/8/0Pinus banksiana 5000 7.2 7.5 0.9 5.7 8/8/0Picea mariana 3820 6.1 5.4 0.8 6.5 8/8/0

71 Picea mariana 4150 9.2 45.3 7.5 8.8 12/8/0151 Picea mariana 3500 10.5 49.9 6.1 9.8 12/8/0

The three numbers in the n column represent the number of sampled trees for JSnorth, JSin, and Kucera-type sap flux, respectively. All treesamples for JSnorth were also sampled for JSsouth. Ninety trees were sampled with 196 sap flux sensors.

Transpiration and canopy average stomatal conductance 663


where i equals each of the JS (g m-2 s-1) stem measure-ment (i.e. JSnorth, JSsouth and JSin) and Wi is the weight ofeach JSi stem measurement position. Wi is calculated usingthe proportion that each measurement position repre-sents of the total xylem area. In the simplest instancewhen there is no inner xylem, then Wi of JSnorth is 0.5 andJSsouth is 0.5. Equation 4 assumes that JSin represents theflux inside of 40 mm from the cambium. Equation 4 alsoassumes that the Wi among JSnorth, JSin, and JSsouth are con-stant throughout the entire JSnorth measurement period(Ewers et al. 2002).

All the trees in the 12-year-old stand, and the Populustremuloides and Picea mariana in the 20-year-old stand,were too small for Granier-type sensors (< 4 cm d.b.h), sowe used Kucera-type sensors (baby sap flow sensors; EMS,Brno, CZ; Ewers & Oren 2000; Ewers et al. 2002) on ran-domly selected trees within the appropriate stem diameterrange. Kucera-type sap flux sensors quantify sap flux bymaintaining a constant 4 ∞C difference between heatedand unheated sections of the stem. The amount of heatrequired to maintain the temperature difference is propor-tional to the sap flow. The Kucera-type sensors measurethe entire sap flow of the stem (for diameters between 12and 18 mm) and do not need additional scaling measure-ments to determine whole tree sap flux. To avoid thermalgradients from direct radiation, all sensors were shieldedwith mylar.

Analyses of daily water use for both Granier and Kucera-type sensors were performed on 24 h sums of JS from 0500 hof one day to 0430 h the next day, which corresponds to thetime of zero flow, and therefore includes night-timerecharge (Phillips & Oren 1998). To calculate EL (mmolm-2 (leaf area) s-1), JS (mmol m-2 (sapwood area) s-1) iscombined with AS : AL (m2 m-2) as follows (Oren et al. 1998;Pataki et al. 1998)

(5)

YYYYL and hydraulic conductance estimation

Leaf water potential (YL) from shaded, mid-canopy leaveswas sampled from three trees of each species measured forsap flux in each stand. Leaf water potential measurementswere made using a Scholander-type pressure chamber(Model 610; PMS Instruments, Corvallis, OR, USA). Leafwater potential was also measured in three Picea marianain the 12-year-old stand even though the trees were not yetlarge enough for sap flux measurements. Shoots were eithercollected with a pruning pole or with a shotgun, and imme-diately placed in plastic bags with a wet paper towel. Leafwater potential measurements were made within 5 min ofsampling. Leaf water potential was measured on 23 June,10 July and 1 August for the 12-, 37- and 71-year-old standsand on 2 July, 16 July and 2 August for the 20- and 151-year-old stands. Preliminary sap flux data from the first severalweeks of the measurements were used to determine zeroflux (predawn) and the point of maximum flux (mid-day).Thus, predawn YL was taken between hours 0200 and

E JAA

L SS

L

= ◊

0400 h and mid-day YL were taken between 1100 and1300 h.

Whole tree hydraulic conductance was calculated perunit leaf area (KL) from the following equation (Pataki,Oren & Phillips 1998)

(6)

where YS is soil water potential (MPa), YL is the leafwater potential taken at mid-day (MPa) and EL is molm-2 s-1. We assumed that predawn YL was equal to YS.Whole tree hydraulic conductance per unit sapwood area(KS) was calculated in the same manner as KL except JS wasused instead of EL in Eqn 6.

Environmental measurements

Vapour pressure deficit was calculated from relative humid-ity (RH) and air temperature (TA) measurements based onequations adapted from Goff & Gratch (1946). We usedexisting weather stations in each of the five stands to mea-sure RH and TA within the tree canopies (Vaisala HMP 35C;Campbell Scientific, Logan, UT, USA). Photosyntheticphoton flux density (Qo) above the canopy was monitoredwith a quantum sensor (LI-190s; Li-Cor, Lincoln, NEUSA). Soil volumetric water content (q) was monitoredwith volumetric soil water content probes (CS 615; Camp-bell Scientific) at 0–15 and 15–30 cm, with two replicates inall stands. Daily average daytime D (DZ) was normalizedby the number of light hours to account for seasonal differ-ences in day length (Oren, Zimmerman & Terborgh 1996).Sap flux and all environmental sensors were sampled every30 s (CR10X; Campbell Scientific) and 30-min means wererecorded.

Canopy stomatal conductance calculations

The mean canopy stomatal conductance to water vapour(m s-1), was calculated from EL and D using following(Monteith & Unsworth 1990):

(7)

where KG is the conductance coefficient (115.8 + 0.4236T;kPa m3 kg-1), which accounts for temperature effects onthe psychometric constant, latent heat of vaporization,specific heat of air at constant pressure, and the density ofair (Phillips & Oren 1998). GS values were converted fromm s-1 to mmol m-2 s-1 using Pearcy et al. (1989). Equation 7requires the following conditions (Ewers & Oren 2000):(1) D is close to the leaf-to-air vapour pressure deficit,namely boundary layer conductance is high; (2) there is novertical gradient in D through the canopy; and (3) there isnegligible water stored above the JS measurement posi-tion. In addition, to keep the measurement errors in GS

(both micrometeorological and sapflux) below 10%, GS

was only calculated when D ≥ 0.6 kPa (Ewers & Oren2000).

KE

LL

S L

=-( )Y Y

GK T E

DS

G L=( ) ◊



Statistical analyses

Statistical analyses were performed in SAS (version 8.0;SAS Institute, Cary, NC, USA). Because sap flux measure-ments are collected in a serial fashion, they often violatethe assumption of independent errors. Thus, we used theMIXED procedure to account for the effect of time seriesdata on ANOVA calculations. The effect of species on dailysums of EL was analysed using repeated measures. Wedetermined the appropriate number of parameters andvariance structure in repeated measures analysis that min-imized the Akaike’s Information Criterion (AIC) andBayesian Information Criterion (BIC; Littel et al.; 1996;Ewers et al. 2002). Both of these criteria are log likelihoodvalues penalized for the number of parameters used. Anal-yses of YL and KL measurements were also conducted usingrepeated measures analysis. Separation of species meanswas determined through the LSMEANS statement with theTukey criteria in SAS. Analyses of time lags and correlationwere done using Proc ARIMA and AUTOREG proceduresin SAS. Non-linear fits were performed using theNLMIXED procedure in SAS and SIGMAPLOT (version6.0; SPSS Inc., Chicago IL, USA).

One approach to data reduction is to distil data to param-eters that contain the information stored in the entire dataset. Variation in diurnal GS can often be explained mostlywith D and focusing analyses on D both removes correla-tion among variables and allows analysis of Eqns 1 and 2.By partitioning the data into categories of soil moisture,light and temperature, and performing a boundary lineanalysis on GS versus D within each category, the data canbe reduced to the parameters describing the relationshipbetween GS and D (Chambers et al. 1985; Pezeshki &Hinckley 1988; Schafer et al. 2000; Ewers et al. 2001b). Theboundary line was derived by: (1) partitioning the GS

response to D into at least five different levels of D; (2)calculating the mean and standard deviation of the GS datawithin each level of D; (3) removing outliers (P < 0.05Dixon’s test, Sokal & Rohlf 1995); and (4) selecting dataabove the mean and standard deviation of GS (Schafer etal. 2000; Ewers et al. 2001b). These parameters can then berelated to the categorizing variable (D). When a boundaryanalysis is made on the entire data set of each tree or apopulation, it allows analysis of the best physiologicalresponse (in this case highest GS) under the measured con-ditions (Martin et al. 1997). The resulting boundary lineprovides the best estimate of hydraulic limitation to waterflux in trees because the boundary line occurs during con-ditions that lead to the highest GS at any given D. Theseare the most appropriate conditions in which to analyse fortree species and tree age effects on the ratio of –d to GSref

(Eqn 3).

RESULTS

Relationship between AS : AL and tree height

The relationship between AS : AL and height varied amongthe species and between stand ages in Picea mariana

(Fig. 1; regression equations in caption). AS : AL wasinversely correlated with height in Picea mariana (Fig. 1a).There was a greater decrease in AS : AL with increasingheight in the 71- and 151-year-old Picea mariana stands incomparison with the 20- and 37-year-old Picea mariana

Figure 1. Relationship between height and sapwood-to-leaf area ratio (AS : AL) for Picea mariana (a), Pinus banksiana (b), and Populus tremuloides (c) across the five stand ages. Regression equations were y = -0.15x + 1.8 for 20- and 37-year-old Picea mariana; y = -0.41x + 6.1 for 71- and 151-year-old Picea mariana; y = 0.36x + 0.8 for all Pinus banksiana; and y = 0.61x + 0.4 for all Populus tremuloides. All slopes were significant at P < 0.001 and all intercepts were significant at P < 0.05.



stands (P < 0.0001 for slope comparison) There was noeffect of stand age on the slopes or the intercepts of thepositive relationship between tree height and AS : AL foreither Pinus banksiana or Populus tremuloides (Fig. 1b &c; P > 0.25 for all comparisons). Betula papyrifera data wasnot shown because there was very little variation in height(1.9–2.7 m); the species had a mean AS : AL of3.9 ± 0.7 cm2 m-2 with n = 5.

Daily environmental variables and EL

Neither daily sums of Qo or DZ differed significantly amongthe five stands (Fig. 2a, c, e, g & I; P > 0.7 for both) and bothQo and DZ declined during the growing season. Soil volu-metric water content was similar in all the stands except the12-year-old stand (Fig. 2a) when a rain event on day 210 ofyear (28 mm at the 12-year-old stand, < 3.0 mm at otherstands) caused a large increase in q relative to the otherfour stands.

In all species and stand ages, daily sums of EL followeddaily Qo and DZ (Figs 2 & 3). Peak values of EL for Piceamariana, Pinus banksiana, and Populus tremuloides (1.3,3.5 and 2.5 mm d-1, respectively) occurred in the 37-year-old stand (Fig. 2f). In the two stands where Pinus banksianaoccurred, it had the highest EL rates. Betula papyrifera waspresent only in the 12-year-old stand but despite its similarAS : AL to Populus tremuloides, it had a significantly(P < 0.01) higher EL rate. Because Betula papyrifera onlyappeared in the 12-year-old stand, we restrict any analysesof stand age and tree size effects to Populus tremuloides,Pinus banksiana, and Picea mariana.

Using a stepwise multiple regression analysis, daily Qo

and DZ explained most of the variability in daily EL acrossall species and stand ages (P < 0.01 for both variables;Fig. 3). Soil moisture explained a significant (P < 0.05)although lesser amount (less than 10% across all speciesand stand ages) of variation in daily EL. In all species andstand ages, EL was positively correlated to Qo (P < 0.01).The highest amount of variability in the relationship wasfound in Pinus banksiana and Populus tremuloides in the37-year-old stand, which also had the highest EL values(Fig. 3). The only relationship between DZ and EL with asatisfactory set of residuals was an exponential saturation(Fig. 3 and Table 2) in Populus tremuloides, Betula papy-rifera, Pinus banksiana, and Picea mariana <71 years old;all regressions were significant (P < 0.01). Similar to therelationship with Qo, the relationship between EL and DZ

in Pinus banksiana and Populus tremuloides in the 37-year-old stand showed the highest variability. In contrast to theother species, Picea mariana EL was linearly correlated todaily DZ (Fig. 3) in the 71- and 151-year-old stands (Fig. 3and Table 2).

Stand level EL and EC

Table 3 depicts the relationship between stand age, dailyEL, growing season EC, and fine roots. Stand age, fine rootbiomass, leaf area index and root-to-leaf area ratio did not

explain any of the variation in daily EL at the stand level(P > 0.4 for all; Tables 1 & 3). Stand age was positivelycorrelated with growing season EC through age 71(P < 0.01, R2 = 0.94) but age 151 stand EC was much lowerthan ages 37 and 71 (Table 3). This pattern could not beexplained by stand leaf area index, basal area, and root-to-leaf area ratio (P > 0.2 for all). In contrast, growing seasonEC was positively correlated with stand level fine root bio-mass (P < 0.01 R2 = 0.70).

Half-hourly EL

In order to decipher the potential impacts of changingspecies composition as the stands increased in age, webegan by analysing half hourly EL response to environ-mental conditions in anticipation of ultimately calculatinghalf-hourly GS for analysis with Eqns 1 and 3. Half-hourlyaverage EL across the species and stand ages displayedvarying degrees of lag with Qo and D (Table 3). In all spe-cies, there was either no lag between D and EL or EL wasbest correlated to D occurring in the next time step;Pinus banksiana had the best correlation with D at 1 h inthe ‘future’ (negative lag values in Table 4). Such negativelags are the result of the best statistical correlation but donot suggest that EL was ‘anticipating’ the environmentaldrivers. The lag between half-hourly Qo and EL variedbetween 1 and 2.5 h (Fig. 4). The widths of the hysteresisloops were greater between EL and Qo than between EL

and D across all species (Fig. 4), as also indicated by thelarger absolute values of lag in Table 4. The hysteresisloops with respect to D were smallest in Picea mariana.The direction of the D to EL hysteresis loops were clock-wise with the highest values of EL occurring in the firsthalf of the solar day. In contrast, the hysteresis loopsbetween Qo and EL were counterclockwise (Fig. 4). Nei-ther the volume of sapwood per tree, volume of sapwoodper unit leaf area (Table 4), or any other metric of treesize (Table 1) explained any of the lags (P > 0.3 for allanalyses). Using either zero lag or the lags reported inTable 4 made no difference in the subsequent analysesreported below.

Tree hydraulic properties

There was no effect of sampling date on predawn ormid-day YL (P > 0.30). However, species (P < 0.01) standage (P < 0.01) and the interaction between stand age andspecies (P < 0.01) all significantly affected predawn YL.There was no change in predawn YL across stand age inPopulus tremuloides and Pinus banksiana (P > 0.40 forboth), whereas Picea mariana had a significantly lowerYL in the 12-year-old stand (P < 0.01). For mid-day YL

there was no effect of stand age on Populus tremuloidesand Pinus banksiana (P > 0.30). Picea mariana showed adeclining (P < 0.01) mid-day YL with increasing stand age(Fig. 5).

There was no significant effect of age on KS within spe-cies (Fig. 5c) and Pinus banksianna had more than four



Figure 2. Comparisons of the seasonal patterns of daily average soil moisture (q), daily average vapour pressure deficit normalized by daylight hours (DZ), daily sums of photosynthetically active radiation (Qo) and daily sums of transpiration per unit leaf area (EL) across the fire chronosequence for the 12 (a, b), 20 (c, d), 37 (e, f), 71 (g, h), and 151 (i, j) year old stands.



times the KS of the other species. Similarly, KL was up tosix times greater for Pinus banksiana than for Picea mari-ana and Populus tremuloides (Fig. 5d). The differences inthe patterns between KS and KL reflected the changingAS : AL with increasing height (Fig. 1). KL was significantlylower in 37 compared with 20-year-old Pinus banksiana.Despite these changes in Pinus banksiana (albeit with onlytwo ages); there was no evidence of declining KS or KL withincreasing tree size and age in the other species (P > 0.2;Fig. 5c); in fact there was an increase in both KL and KS ofPopulus tremuloides and Picea mariana from the 20- to the37-year-old stands.

GS responses to D

Two general relationships were observed between GS andD; representative data is shown in Fig. 6. In Fig. 6a and c,all of the GS data for D-values greater than 0.6 kPa wereincluded from two representative trees of Picea marianaand Populus tremuloides. In order to isolate the responseof GS to D, a series of filters was used. First, data wereselected when Qo was greater than 1.0 mmol m-2 s-1 and qwas greater than 0.1 m3 m-3. Second, the resulting data weresubjected to a boundary line analysis such that the highestvalues of GS were selected within each 0.2 kPa grouping of

Figure 3. Relationships between daily sums of transpiration per unit leaf area (EL) and daily average vapour pressure deficit normalized by daylight hours (DZ; a, c, e, g) and photosynthetically active radiation (Qo; b, d, f, h) for the 12 (a, b), 20 (c, d), 37 (e, f), and 71 (g) and 151 (h) year-old stands. The legends for (e) and (f) are the same as (c) and (d). See Table 2 for equations and parameters used to fit all data.



D-values. In both species, GS declined with increasing D,but the rate of decline in GS was lower in Picea marianathan Populus tremuloides.

To quantify the changes in the rate of GS decline with Dwe determined the relationship between –d and GSref (Eqn3; Fig. 7) for all trees using the filtering and boundary lineanalysis depicted in Fig. 6. Across all species and stand ages,there was a significant, linear relationship between –d andGSref (P < 0.01) with no intercept (P > 0.40). There was nosignificant difference between the hypothesized 0.6 propor-tion between –d and GSref (shown as the dotted line; Fig. 7)and the slopes of Betula papyrifera, Pinus banksiana, Pop-

ulus tremuloides, and 20- and 37-year-old Picea mariana(P > 0.30). Picea mariana in the 71- and 151-year-old standshad a significantly lower (0.41 and 0.28, respectively;P < 0.01 for both) slope for the relationship between –d andGSref (Fig. 7).

Modelling GS based on leaf water potential regulation

Using the assumption that mid-day YL was regulated by GS

from D = 0.6–3.8 kPa (the range of D used to calculate GS;see methods), Eqn 1 was able to reproduce the ratios

Table 2. Environmental variables, stand age, species, equation type and parameters used in Fig. 3

Environmental variable Age Species Eqn a b

DZ 12 Populus tremuloides A 1.24 (0.04) a 2.28 (0.19) aBetula papyrifera A 0.58 (0.01) b 2.79 (0.19) b

20 Picea mariana A 0.18 (0.01) c 8.19 (2.0) cPinus banksiana A 0.96 (0.46) ab 2.23 (0.26) aPopulus tremuloides A 0.31 (0.01) d 2.73 (0.30) b

37 Picea mariana A 0.83 (0.06) b 2.64 (0.47) abPinus banksiana A 2.29 (0.16) e 2.67 (0.48) abPopulus tremuloides A 1.71 (0.13) f 2.31 (0.40) ab

71 Picea mariana B – 0.34 (0.22) i151 Picea mariana B – 0.31 (0.21) i

Qo 12 Populus tremuloides B 0.13 (0.004) a 0.008 (0.001) aBetula papyrifera B 0.18 (0.001) b 0.019 (0.001) b

20 Picea mariana B 0.12 (0.001) a 0.001 (0.001) cPinus banksiana B 0.20 (0.050) b 0.013 (0.001) dPopulus tremuloides B 0.08 (0.001) c 0.004 (0.001) e

37 Picea mariana B 0.18 (0.002) b 0.012 (0.003) dPinus banksiana B 0.53 (0.037) d 0.032 (0.006) fPopulus tremuloides B 0.31 (0.024) e 0.025 (0.004) g

71 Picea mariana B 0.031 (0.002) f 0.006 (0.001) e151 Picea mariana B 0.042 (0.003) f 0.005 (0.001) e

Parameters a and b are from either equation (Eqn) A (EL = a(1 - e–b var) or B (EL = a + b var) where var is either daily average vapourpressure deficit (DZ) or daily sum of photosynthetically active radiation (Qo). Values in parentheses are 1 SE of the mean (see Table 1 forn) and letters indicate significant differences at a = 0.05.

Table 3. Stand age, species daily transpiration per unit leaf area (EL), growing season canopy transpiration (EC), and fine root biomass (from Wang et al. 2003)

Stand age(years) Species

Daily EL

(mm d-1)Growing season EC

(mm)Fine roots(tons ha-1)

12 Populus tremuloides 0.36 (0.16) a 8Betula papyrifera 0.79 (0.19) b 16Total 0.9 24 0.37

20 Picea mariana 0.13 (0.18) a 3Pinus banksiana 0.7 (0.13) b 86Populus tremuloides 0.18 (0.18) a 8Total 1.0 97 1.59

37 Picea mariana 0.63 (0.16) ab 55Pinus banksiana 1.6 (0.16) b 110Populus tremuloides 1.1 (0.16) b 37Total 2.3 224 1.61

71 Picea mariana 0.28 (0.12) a 332 2.46151 Picea mariana 0.24 (0.13) a 183 1.02

Sample sizes for EL are given in Table 1 with letters representing significant difference at a = 0.05.



between –d and GSref (Eqn 2; see dotted lines and regressionslopes in Fig. 7) for all the species and ages except 71- and151-year-old Picea mariana. The values of YL were pooledbetween difference ages of Populus tremuloides and Pinusbanksiana because there were no significant impacts of ageon YL (Fig. 5). Pre-dawn YL values were used to estimateYS in Eqn 1 and values were pooled for Populus tremu-loides and Pinus banksiana because there were no signifi-cant impacts of age on predawn YL.

The unmodified model (Eqns 1 and 3) could notexplain the significantly lower ratio between –d and GSref

in 71- and 151-year-old Picea mariana trees (Fig. 7), so wemodified Eqn 1 using the assumption made by Oren et al.(1999a) to explain the lower ratio between –d and GSref insome desert shrub species. These shrubs appear to allowYL to decline as D increases violating the premise of Eqn1 that minimum YL is regulated by plants to preventexcessive cavitation. The modified model (Eqn 1) startedwith a mid-day YL of 0.8 MPa (Fig. 5) as the startingwater potential when D = 0.6 kPa because the unmodifiedmodel was able to reproduce the measured ratio between–d and GSref in the 20- and 37-year-old Picea mariana(Fig. 7). Next we modified the model such that YL

declined linearly to the measured mid-day YL values of1.35 and 1.50 MPa for 71- and 151-year-old Picea mari-ana, respectively (Fig. 5b). We used a linear decline basedon the finding of Dang et al. (1997) that stomatal conduc-tance of excised branches of Picea mariana decline lin-early with decreasing water potential. These modifications

resulted in modelled ratios of 0.43 and 0.32 for 71- and151-year-old Picea mariana, respectively, between –d andGSref which were not significantly different from the mea-sured ratios of the 71- and 151-year-old Picea mariana(Fig. 8; P > 0.3). Contrary to our expectations from previ-ous studies, we found no correlation between tree heightor basal area and GSref (P > 0.5 for both). We did not anal-yse for correlations between KS or KL and GSref becauseall three quantities are calculated from the same sap fluxmeasurements. Only the soil-to-leaf water potential gradi-ent was independent and could explain the changingratios between –d and GSref (Fig. 8).

In order to test whether boundary layer conductancemay have played a role in the lower ratio between –d andGSref of 71- and 151-year-old Picea mariana, we calculatedboundary layer conductances based on standard method-ology using wind speed and characteristic dimension offoliage (Jones 1992). We divided the measured windspeeds in half to approximate canopy interactions. Wetested two possible leaf characteristic dimensions: (1) indi-vidual Picea mariana needles at the site approximately0.002 mm; and (2) a clumped distribution approximately0.05 m. The resulting five-fold difference in boundary layerconductance only changed the ratio between –d and GSref

from 0.32 to 0.34 and from 0.43 to 0.45 for 71- and 151-year-old Picea mariana, respectively. Thus, boundary layerconductance could not have been responsible for the lowratios between –d and GSref in 71- and 151-year-old Piceamariana.

Table 4. Stand age, species, lag between half-hourly averages of transpiration per unit leaf area (EL) and vapour pressure deficit (D), correlation coefficient (R2) between D and EL, lag between photosynthetically active radiation (Qo) and EL, R2 between Qo and EL, volume of sapwood area per tree (VS), and volume of sapwood area divided by leaf area per tree (VSL)

Stand age(year) Species

D lag(h)

D R2

Qo lag(h)

Qo R2

VS

(m3 tree-1)VSL (m3 tree-1)

12 Populus tremuloides -0.5 0.74 1.0 0.81 1.0 ¥ 10-4 1.8 ¥ 10-4

(0.5) a (0.6) a (5.5 ¥ 10-5) a (9.6 ¥ 10-5) aBetula papyrifera –0.5 0.75 1.0 0.82 1.1 ¥ 10-4 1.7 ¥ 10-4

(0.5) a (0.7) a (5.3 ¥ 10-5) a (9.3 ¥ 10-5) a20 Populus tremuloides 0.0 0.76 2.0 0.79 7.6 ¥ 10-3 1.9 ¥ 10-3

(0.3) a (0.7) a (8.6 ¥ 10-3) b (2.2 ¥ 10-3) bPinus banksiana 0 0.78 2.0 0.82 4.7 ¥ 10-3 6.3 ¥ 10-4

(0.2) a (0.8) a (2.5 ¥ 10-3) b (3.3 ¥ 10-4) aPicea mariana 0.0 0.65 1.5 0.63 7.7 ¥ 10-5 1.3 ¥ 10-4

(0.4) a (0.9) a (6.1 ¥ 10-5) c (1.0 ¥ 10-4) a37 Populus tremuloides -0.5 0.73 1.5 0.76 2.0 ¥ 10-2 3.6 ¥ 10-3

(0.4) a (0.4) a (2.3 ¥ 10-2) d (4.1 ¥ 10-3) bPinus banksiana –1.0b 0.71 1.5 0.76 9.5 ¥ 10-3 8.7 ¥ 10-4

(0.4) (0.6) a (6.3 ¥ 10-3) b (5.8 ¥ 10-4) aPicea mariana 0.0 a 0.75 2.0 0.79 6.3 ¥ 10-3 4.1 ¥ 10-4

(0.3) (0.8) a (5.1 ¥ 10-3) b (3.3 ¥ 10-4) a71 Picea mariana 0.0 0.68 2.0 a 0.72 9.4 ¥ 10-3 6.5 ¥ 10-4

(0.4) a (0.5) (8.4 ¥ 10-3) b (5.9 ¥ 10-4) a151 Picea mariana 0.5 0.82 2.5 0.82 1.2 ¥ 10-2 6.4 ¥ 10-4

(0.4) a (0.4) a (9.4 ¥ 10-3) d (5.0 ¥ 10-4) a

A negative lag indicates EL is best correlated with D or Qo when EL is moved in front of the environmental variable. Values inparentheses are 1 SE of the mean (n = number of trees sampled for sapflux; Table 1) and letters indicate significant differences at thea = 0.05 level.



DISCUSSION

The effect of stand age on transpiration from boreal forestsdepends on species-specific responses to intrinsic water lim-itations when the atmosphere is relatively dry. While max-imizing carbon gain, most trees attempt to maintain ahomeostasis of leaf water status with changes in wateruptake and losses by regulating leaf water potential to pre-

vent runaway cavitation. This homeostasis is maintained onshort time scales by regulating water loss through declinesin stomatal conductance and over longer times scales byadjusting tree hydraulic architecture. We failed to reject ourfirst and second hypothesis, that Populus tremuloides andPinus banksiana would have a higher EL than Picea mari-ana, and that AS : AL would increase with height in Populustremuloides and Pinus banksiana but will decrease in Picea

Figure 4. Hysteresis curves between half hourly averages of transpiration per unit leaf area (EL) and vapour pressure deficit (D) and photosynthetically active radiation (Qo) for the 12 (a, b), 20 (c, d), 37 (e, f), 71 (g) and 151 (h) year-old stands. The legends for (e) and (f) are the same as (c) and (d). Each point represents the bin-average of all the half-hours at a given D or Qo and the corresponding EL. Arrows indicate the direction of the hysteresis.



Figure 5. Pre-dawn leaf water potential (YL; a), mid-day minimum YL (b), hydraulic conductance per unit sapwood area (KS; c) and hydraulic conductance per unit leaf area (KL; d) for Populus tremuloides, Pinus banksiana and Picea mariana across the five stand ages. Bars indicate 1 SE of the mean with n = 3 trees; letters indicate significant differences at a = 0.05.

Figure 6. Representative relationships between canopy average stomatal conductance (GS) and vapour pressure deficit on a half hourly basis for high and low GS Populus tremuloides (a). The relationship between D and GS after applying filters and boundary line analysis as described in the text is shown in (b). The same relationships are shown for Picea mariana in (c) and (d).



mariana. However, we rejected our third hypothesisbecause Picea mariana did not maintain minimum leafwater potential with increasing tree size.

Response of water relations to tree age and size

In Populus tremuloides and Pinus banksiana, we found thatwith increasing tree size AS : AL increased (Fig. 1), the min-imum YL was maintained (Fig. 5), and the proportionalitybetween –d and GSref was not different from 0.6 (Fig. 7). Allof these effects were as hypothesized, based on the ideathat trees attempt to maintain homeostasis of water statuswhile maximizing carbon gain. In contrast, Picea marianaexhibited a decreasing AS : AL with increasing tree size(Fig. 1), allowed minimum YL to decrease (Fig. 5), and theproportion between –d and GSref declined in the two oldeststands (Fig. 7). In Picea mariana, the decline in AS : AL wasas hypothesized for low AS : AL tree species whereas thedecline in YL was unexpected as was the lack of clear trendsin KS or KL (Fig. 4). We found no evidence of increasing KS

with height (Fig. 5c) as was found by Coyea & Margolis(1992) for Abies balsamea which, like Picea mariana alsohad declining AS : AL with increasing height. McDowellet al. (2002a) hypothesized that trees with declining AS : AL

with increasing height must either increase the soil-to-leafwater potential gradient through declines in mid-day leafwater potential or increase root area.

Our data suggest that a combination of both phenomenamay be occurring. Our simulated ratios between –d andGSref in the 71- and 151-year-old Picea mariana that incor-

Figure 7. Relationship between sensitivity of canopy average stomatal conductance to vapour pressure deficit (dGS/d lnD; –d) and canopy average stomatal conductance at vapour pressure deficit =1 kPa (GSref) for Picea mariana (a), Populus tremuloides and Betula papyrifera (b), and Pinus banksiana (c). The theoretical proportionality (Eqn 2) is shown by a dotted line in each figure. Figure 8. Comparison of the measured ratio of –d/GSref (Fig. 7)

and the modelled ratio of –d/GSref. The dotted line is unity, the solid line is the least squares regression, and the dashed curves are 95% confidence intervals.



porated a linear decline in YL with increasing D (Fig. 8)closely matched the observed ratios (Fig. 7). The likelyincrease in the fine root biomass of Picea mariana (fineroots were not separated by species; Table 3) in the 71- and151-year-old stands would also compensate for the declin-ing AS : AL found in Picea mariana. However, based on theanalysis of Oren et al. (1999a) changes in hydraulic proper-ties of the plant would merely cause the individual trees tomove up and down the line with zero intercept and slopeof 0.6 between –d and GSref and would not explain thedeclining ratio found in Picea mariana (Fig. 8). Unfortu-nately, our limited resources did not allow us to measurediurnal leaf water potentials and so we were unable todetermine whether the observed trend (Fig. 5c) is due todeclining mid-day water potentials or merely that Piceamariana in our chronosequence has not reached its thresh-old for minimum YL to prevent runaway caviation as sug-gested by Dang et al. (1997). Indeed, why some speciesappear capable of tight control of transpiration whereasothers do not is currently unexplained (Franks 2004).Future measurements at this site will quantify root hydrau-lic conductance and its vulnerability to cavitation andshould shed light on whether root vulnerability to cavita-tion may be the limiting resistance to soil-to-leaf waterpotential gradients (Sperry et al. 1998) and ultimately theratio between –d and GSref.

Other studies have also found that Pinus banksiana andPopulus tremuloides regulate YL at a critical value, but thereported thresholds were higher or lower than the valuesreported here (Dang et al. 1997; Hogg et al. 2000) mostlikely due to changes in site environmental conditions. Thevalue of minimum YL has been known to be a function ofsite conditions for some time (Whitehead & Jarvis 1981)and recent evidence suggests that minimum YL can accli-mate to edaphic conditions as was found in Pinus taedatrees growing on different soil types (Hacke et al. 2000).Wang et al. (2003) discussed how the increasing bryophytebiomass with age across our chronosequence could resultin a much colder root environment. Since the viscosity ofwater and the permeability of membranes decreases at lowtemperatures (Kramer & Boyer 1995) and root systems ofPicea mariana are much less developed than Pinus banksi-ana (Lieffers & Rothwell 1986, 1987), it is not surprisingthat predawn YL is changing across the chronosequenceand between species (Fig. 5a). Indeed, Picea marianashowed a constant decline in stomatal conductance withdecreasing water potential (Dang et al. 1997) in the samestand of trees as our 151-year-old stand which supports thelower ratio we found between –d and GSref (Figs 7 & 8).Thus, our future work will also test whether temperatureand soil organic matter change root hydraulic properties inthe oldest boreal forests.

It is clear that AS : AL alone does not explain the declinein the –d to GSref proportion, because the 20- and 37-year-old Picea mariana trees had similar AS : AL to the shorter71- and 151-year-old trees (Fig. 1). The root-to-leaf arearatio in the 71- and 151-year-old stands was approximatelyhalf that of the three younger stands (Wang et al. 2003).

Our results (Fig. 7) present the hypothesis that changes inroot vulnerability to cavitation acting in concert with shiftsin AS : AL may explain the behaviour of Picea mariana.Most studies of tree size effects on conifer GS have focusedon higher AS : AL species such as Pinus sylvestris (Magnaniet al. 2000) Pseudotsuga menziesii (McDowell et al. 2002b),and Pinus ponderosa (Ryan & Yoder 1997), and more stud-ies are needed on the relationship between root vulnerabil-ity to caviation and AS : AL in low AS : AL conifers todetermine if the behaviour shown by Picea mariana in thisstudy is due to the cold boreal climate or if it can begeneralized.

This study adds to an increasing body of evidence thatpoints to whole tree adjustments in hydraulic architecture(Magnani et al. 2000; Schafer et al. 2000; McDowell et al.2002a,b; Phillips et al. 2002). However, our study was notable to show the elegant relationship between tree hydrau-lic adjustment and height as was found in the aforemen-tioned studies. It is likely that the differences between thosestudies and this one are due to the fact that the maximumheights of 15 m (Fig. 1), which are not uncommon forboreal forests (Gutsell & Johnson 2002), are at the mini-mum heights of the aforementioned studies. A recentreview showed that in many conifers, AS : AL increased lin-early with increasing height except for high AS : AL speciessuch as Abies lasiocarpa and Picea abies in which it declined(McDowell et al. 2002a). What might set these low AS : AL

species apart from other species? A hypothesis put forwardby Magnani et al. (2000) suggests that low AS : AL speciesmay produce juvenile wood to a much later age; compare70 years in Abies balsamea (Coyea & Margolis 1992) with15 years in Pinus sylvestris (Mencuccini, Grace &Fioravanti 1997).

Juvenile wood properties contribute to an increase intracheid dimensions, thinner tracheid walls and increasedsapwood conductivity until the maturation of the xylem(Magnani et al. 2000). Recent work has suggested thatdecreased thickness of tracheid walls may contribute toincreased vulnerability to cavitation (Hacke et al. 2001);thus, juvenile wood may be more vulnerable to caviationthan mature wood. In 63-year-old Picea abies, another lowAS : AL tree species and congeneric to Picea mariana, acrossa two-fold change in AS : AL from 2.6 to 5.0 cm2 m-2 therewas no deviation in the proportionality of –d to GSref from0.6 (Ewers et al. 2001b). The discrepancy between this studyand the former may be because AS : AL of Picea abies wasnever as low as the Picea mariana in this study (Fig. 1), orthat 63-year-old Picea abies was not yet producing maturewood. Such differences in development rates are thusimportant considerations when explaining large changes inEC across successional patterns (Table 3) such as this study.The slower developmental pattern of Picea mariana com-pared with the other species suggest that stand age andspecies composition must be considered when determiningthe mechanisms that influence stand transpiration alongchronosequences.

Desert species Ephedra nevadensis and Larrea tridentataare the only other species thus far besides Picea mariana



reported to show a significantly lower proportion than 0.6between –d and GSref (0.41–0.46; Oren et al. 1999a; Ogle &Reynolds 2002). These species also allow minimum YL todecline with increasing D which results in the observedproportion <0.6 between –d and GSref as predicted by Eqn1. All three of these species may have convergent evolutionof their xylem morphology to withstand lower water poten-tials under high atmospheric demand without excessive andcatastrophic cavitation; such an adaptation would allowthese species to continue to take up carbon when otherspecies had to decrease GS to prevent excessive cavitation.However, in order to have a lower vulnerability to cavita-tion, maximum hydraulic conductance must also bereduced (Ewers, Oren & Sperry 2000; Hacke & Sperry2001). The lower ratios between –d and GSref would conferan advantage to the older Picea mariana because theywould not have as much of a decline in GS, at a given GSref,with increasing D as their competitors Pinus banksiana andPopulus tremuloides. Indeed, since Pinus banksiana andPopulus tremuloides must increase AS : AL with increasingheight (and thus carry less leaf area) as well as maintain thehypothesized ratio between –d and GSref, they have a muchreduced carbon uptake in the older stands. When maximumhydraulic conductance is reduced, GS and EL follow withthe possibility of reduced carbon uptake (Hubbard, Bond,& Ryan 1999; Katul et al. 2003). Such connections are sug-gested by the fact that NPP was highest in the 37-year-oldstand (Bond-Lamberty, Wang, & Gower 2004) which hadthe highest daily EL (Table 2). Thus, further study is war-ranted to determine if the lower proportion between –d andGSref, which confers an advantage to the Picea mariana inthe oldest stands, could explain the NPP declines observedin the two oldest stands.

Daily EL

The daily EL data (Fig. 4) suggest two different responsesto intrinsic water limitations that follow the two differentspecies’ ratios of –d and GSref (Fig. 8). In forest canopieswhere stomata close to regulate minimum water potential,transpiration shows either a plateau with increasing D(Meinzer et al. 1993; Goulden & Field 1994; Martin et al.1997; Ewers et al. 2001b, 2002) or even a decline at high D(Pataki, Oren & Smith 2000). Populus tremuloides, Betulapapyrifera, Pinus banksiana, and Picea mariana less than 71years old all show the expected response (Fig. 4) similar toother studies of boreal Populus tremuloides (Hogg & Hur-dle 1997; Hogg et al. 1997). The GS responses to D of thesespecies found in this study are consistent with branch levelgas exchange data, where there was little GS sensitivity toD in older Picea mariana, but normal sensitivity in Populustremuloides and Pinus banksiana (Dang et al. 1997). Thelinear increase in EL with increasing DZ in Picea marianagreater than 70 years old (Fig. 4) and the reduced ratiobetween –d and GSref (Fig. 8) further suggests that Piceamariana stomatal conductance does not regulate waterpotential as closely as Populus tremuloides and Pinusbanksiana.

Stand age and EC

The impact of stand age on EC is ultimately mitigated byspecies effects across this boreal wildfire chronosequence.While the maximum EC and L coincided in the 71-year-oldstand (Tables 1 & 3), L could not explain stand age effectsin the other stand ages. In the three stands less than71 years old, species changes in EL largely explain differ-ences in stand EC, whereas changes in Picea marianaexplain the differences in EC in the 71- and 151-year-oldstands. Picea mariana, Pinus banksiana, and Populus trem-uloides all had their highest EL values in the 37-year-oldstand. This stand age probably represents the optimal con-ditions for stand water loss and carbon uptake becauseweak competitors have been removed from each speciesdue to self- and competitive-thinning but the trees are notyet large enough for full exclusion of Pinus banksiana andPopulus tremuliodes by Picea mariana (Bond-Lambery,Wang & Gower 2004; Légaré et al. 2004). Once Pinus bank-siana and Populus tremuloides are excluded by the lowerEL Picea mariana, the daily stand EL declines drastically(Table 3). In the 71- and 151-year-old stands dominated byPicea mariana, their lower EL values are largely explainedby the changes in GS occurring as a result of physiologicalshifts in whole tree hydraulics (Figs 1, 7 & 8) that result inless total water use but continued, linear increases in wateruse with increasing DZ (Fig. 3 and Table 2). Such behaviourby Picea mariana further supports our contention that it isa superior competitor in the older stands as evidenced byits complete dominance.

The correlation between stand EC and fine roots presentsa challenge to our ability to explain stand level EC witheasy-to-obtain above-ground information alone. Althoughrecent studies have focused on the impact of AS:AL as aproxy for whole tree hydraulic changes in response to treesize (McDowell et al. 2002a; Schafer et al. 2000), it is clearthat roots must play a major role (Magnani et al. 2000). Ourcorrelation between stand EC and stand fine root biomassalso supports this idea. These data suggest that whileAS : AL (Fig. 1) and YL (Fig. 5) changes with stand age helpexplain the shifts in the relationship between GSref and –damong and between species, roots must ultimately beincluded in any final explanation. Because our root datawere not separated by species, we can not analyse for rooteffects on the relationship between GSref and –d among andbetween species (Figs 7 & 8). As root vulnerability to cav-itation is the ultimate driver of whole plant hydraulics(Sperry et al. 1998), it is not surprising that roots play acentral role in the total loss of water at the stand levelacross our chronosequence. Thus, our stand EC data furthersupports our call for future studies that focus on quantify-ing shifts in root hydraulic properties as a consequence ofboth physiological changes due to tree size and age and soilmicroclimatological changes in these boreal systems.

Potential methodological issues

Any use of sap flux measurements to calculate GS must becarefully considered due to methodological issues (Ewers



& Oren 2000). As expected from well-coupled stands (Mar-tin et al. 1997), there was less hysteresis between D and EL

than Qo and EL (Fig. 4). In addition, the reported lags(Table 4) had no impact on any of the analyses, suggestingthat internal water storage was not an important compo-nent of these forests. The largest hystereses between EL andD occurred in the 37-year-old stand; the lags were similarto 1 h lags reported for southern, tension zone boreal Pop-ulus tremuloides (Hogg et al. 1997) and Pinus banksianasites (Saugier et al. 1997). Whereas other studies havereported poor canopy coupling in conifers such as sub-alpine Picea engelmannii, Abies lasiocarpa, and Pinus con-torta (Smith & Carter 1988) and boreal Picea mariana(Rayment et al. 2000), the lack of canopy coupling wasinsufficient to significantly change the relationship between–d and GSref in this study. Picea mariana should have thetightest needle packing (Gower, Kucharik & Norman 1999)and display the least canopy coupling under a particular setof conditions, yet it had the least lag with D and greatestlag with Qo (Table 4). In addition, after dividing the dataset into high wind speed days (> 3 m s-1) and low windspeed days (< 3 m s-1), there was no significant effect on thereported ratios between –d and GSref as expected for well-coupled stands (Oren et al. 1999a)

Because studies of tree function across the life time of atree are nearly impossible to do in the life-time of aresearcher, the substitution of space for time is the mostwidely used method. The chronosequence method assumessufficient matching of climate, soil parent material, relief,and flora (Powers & Van Cleve 1991). However, spatialvariation in various environmental drivers (Fig. 2) canmake it hard to determine whether the resulting changeswere due to the variation in the environmental drivers overtime or to differences in time since disturbance (Yanai et al.2000). To test for these effects, Bond-Lamberty, Wang &Gower (2004) measured basal area, L, and tree net primaryproductivity in 14 chronosequence comparator stands, aged1–180 years, throughout the region of our study site. Theyfound that the chronosequence shown in this study was notdifferent from the comparator sites.

Potential impact of disturbance on ecosystem function and global cycles

The effects of species and tree sizes on the magnitude ofthe gas exchange response to D could have significantimplications for understanding the feed backs between theland surface and the atmosphere under different climatechange scenarios. In the same 151-year-old Picea marianastand as this study, Goulden et al. (1997) concluded fromeddy covariance measurements that high evaporativedemand would have little impact on photosynthesis andthat such aspects of climate change would not affect thegross production of boreal spruce forests. Our data agreewith that study since the GS of old stands of Picea marianawere less sensitive to D than the younger stands (Fig. 7).However, our results suggest that old stands of Picea mar-iana should not be taken as representative of Picea mariana

for the whole boreal forest. Any model of the impact ofdisturbance on boreal forests must incorporate species andstand age effects on the response of transpiration to envi-ronmental conditions.

CONCLUSIONS

We observed that canopy transpiration from a chronose-quence of boreal forests recovering from wildfire could notbe predicted from stand leaf area index or basal area alone.This observation was a direct consequence of changes inspecies composition across the chronosequence as a resultof ecological succession. Stands less than 70 years old hadmixtures of Populus tremuloides, Pinus banksiana, andPicea mariana whereas stands over 70 years old were nearlypure stands of Picea mariana. Populus tremuloides andPinus banksiana had higher transpiration rates per unit leafarea than Picea mariana which resulted in higher transpi-ration rates at the stand level at a given leaf area index inthe younger stands. Further differences in the speciesreflected the fact that Populus tremuloides, Pinus banksianaand the younger Picea mariana all had saturating dailytranspiration rates with increasing vapour pressure deficit,an indication of stomatal conductance control of minimumleaf water potentials. In contrast, Picea mariana that weremore than 70 years old had linear relationships betweendaily transpiration and vapour pressure deficit. These dif-ferences were further explained through the use of a mod-ified stomatal conductance model that was able toaccurately capture the response of canopy stomatal conduc-tance to vapour pressure deficit across all species and ages.Such contrasting behaviour by Picea mariana provides evi-dence for its ability to exclude competitors in the two oldeststands because its carbon uptake will not suffer as muchwith atmospheric drought as its competitors. Our resultsillustrate that process models should incorporate both spe-cies effects and stand age when predicting the response oftranspiration in boreal forests to disturbance. New researchshould focus on elucidating the mechanisms, most likely tobe found in roots, that allow the different species to accli-mate to changing demands on water supply as treesincrease in size and age in this cold, boreal climate.

ACKNOWLEDGMENTS

This research was supported by NSF Integrated ResearchChallenges in Environmental Biology (DEB-0077881) toS.T.G. We thank Myron Tanner for exceptional assistanceand morale boosts in the field and numerous undergradu-ates who assisted in field and laboratory work. We aregrateful to John Rigaux and Bruce Holmes of the ManitobaDepartment of Natural Resources for advice and the nec-essary permits, and to the Nisichawayasihk First Nation forpermission to work on tribal land.

REFERENCES

Addington R.N., Mitchell R.J., Oren R. & Donvan L.A. (2004)Stomatal sensitivity to vapor pressure deficit and its relationship



to hydraulic conductance in Pinus palustris. Tree Physiology 24,561–569.

Becker P., Meinzer F.C. & Wullschleger S.D. (2000) Hydrauliclimitation of tree height: a critique. Functional Ecology 14, 4–11.

Bond B.J. & Ryan M.G. (2000) Comment on ‘Hydraulic Limita-tion of Tree Height: a Critique’ by Becker, Meinzer &Wullschleger. Functional Ecology 14, 137–140.

Bond-Lamberty B., Wang C. & Gower S.T. (2002a) Abovegroundand belowground biomass and sapwood area equations for sixboreal tree species of northern Manitoba. Canadian Journal ofForest Research 32, 1441–1450.

Bond-Lamberty B., Wang C.K., Gower S.T. & Norman J. (2002)Leaf area dynamics of a boreal black spruce fire chronose-quence. Tree Physiology 22, 993–1001.

Bond-Lamberty B., Wang C.K. & Gower S.T. (2003) The use ofmultiple measurement techniques to refine estimates of coniferneedle geometry. Canadian Journal of Forest Research 33, 101–105.

Bond-Lamberty B., Wang C.K. & Gower S.T. (2004) Net primaryproduction and net ecosystem production of a boreal blackspruce wildfire chronosequence. Global Change Biology 10,473–487.

Chambers J.L., Hinckley T.M., Cox G.S., Metcalf C.L. & AslinR.G. (1985) Boundary-line analysis and models of leaf conduc-tance for 4 oak-hickory forest species. Forest Science 31, 437–450.

Clearwater M.J., Meinzer F.C., Andrade J.L., Goldstein G. &Holbrook N.M. (1999) Potential errors in measurement of non-uniform sap flow using heat dissipation probes. Tree Physiology19, 681–687.

Cochard Y., Bréda N. & Granier A. (1996) Whole tree hydraulicconductance and water loss regulation in Quercus duringdrought: evidence for stomatal control of embolism? AnnalesDes Sciences Forestieres 53, 197–206.

Coyea M.R. & Margolis H.A. (1992) Factors affecting the relation-ship between sapwood area and leaf area of balsam fir. CanadianJournal of Forest Research 22, 1684–1693.

Dang Q.L., Margolis H.A., Coyea M.R., Sy M. & Collatz G.J.(1997) Regulation of branch-level gas exchange of boreal trees:roles of shoot water potential and vapor pressure difference.Tree Physiology 17, 521–535.

Ewers B.E. & Oren R. (2000) Analyses of assumptions and errorsin the calculation of stomatal conductance from sap flux mea-surements. Tree Physiology 20, 579–589.

Ewers B.E., Mackay D.S., Gower S.T., Ahl D.E., Burrows S.N.& Samanta S.S. (2002) Tree species effects on stand transpira-tion in northern Wisconsin. Water Resources Research 38 (7),1–11.

Ewers B.E., Oren R., Johnsen K.H. & Landsberg J.J. (2001a)Estimating maximum mean canopy stomatal conductance foruse in models. Canadian Journal of Forest Research-Revue Cana-dienne de Recherche Forestiere 31, 198–207.

Ewers B.E., Oren R., Phillips N., Stromgren M. & Linder S.(2001b) Mean canopy stomatal conductance responses to waterand nutrient availabilities in Picea abies and Pinus taeda. TreePhysiology 21, 841–850.

Ewers B.E., Oren R. & Sperry J.S. (2000) Influence of nutrientversus water supply on hydraulic architecture and water balancein Pinus taeda. Plant Cell and Environment 23, 1055–1066.

Franks P.J. (2004) Stomatal control and hydraulic conductance,with special reference to tall trees. Tree Physiology 24, 865–878.

Goff J.A. & Gratch S. (1946) List 1947, Smithsonian Meteorolog-ical Tables. Transactions of the American Society of VentilationEngineering. 52, 95.

Goulden M.L. & Field C.B. (1994) 3 Methods for monitoring thegas-exchange of individual tree canopies – ventilated-chamber,

sap-flow and Penman–Monteith measurements on evergreenoaks. Functional Ecology 8, 125–135.

Goulden M.L., Daube B.C., Fan S.M., Sutton D.J., Bazzaz A.,Munger J.W. & Wofsy S.C. (1997) Physiological responses of ablack spruce forest to weather. Journal of Geophysical Research102, 28987–28996.

Gower S.T., Kucharik C.J. & Norman J.M. (1999) Direct andindirect estimation of leaf area index, fAPAR and net primaryproduction of terrestrial ecosystems. Remote Sensing of Envi-ronment 70, 29–51.

Gower S.T., Mcmurtrie R.E. & Murty D. (1996) Aboveground netprimary production decline with stand age: potential causes.Trends in Ecology and Evolution 11, 378–382.

Gower S.T., Vogel J.G., Norman J.M., Kucharik C.J., Steele S.J.& Stow T.K. (1997) Carbon distribution and aboveground netprimary production in aspen, jack pine, and black spruce standsin Saskatchewan and Manitoba, Canada. Journal of GeophysicalResearch-Atmospheres 24, 29029–29041.

Granier A. (1987) Sap flow measurements in Douglas-fir treetrunks by means of a new thermal method. Annales Des SciencesForestieres 44, 1–14.

Gunderson C.A., Sholtis J.D., Wullschleger S.D., Tissue D.T.,Hanson P.J. & Norby R.J. (2002) Environmental and stomatalcontrol of photosynthetic enhancement in the canopy of a sweet-gum (Liquidambar styraciflua L.) plantation during 3 years ofCO2 enrichment. Plant, Cell and Environment 25, 379–393.

Gutsell S.L. & Johnson E.A. (2002) Accurately ageing trees andexamining their height-growth rates: implications for interpret-ing forest dynamics. Journal of Ecology 90, 153–166.

Hacke U.G. & Sperry J.S. (2001) Functional and ecological xylemanatomy. Perspectives in Plant Ecology, Evolution and System-atics. 4, 97–115,.

Hacke U.G., Sperry J.S., Ewers B.E., Ellsworth D.S., SchaferK.V.R. & Oren R. (2000) Influence of soil porosity on water usein Pinus taeda. Oecologia 124, 495–505.

Hacke U.G., Sperry J.S., Pockman W.T., Davis S.D. & McCullohK.A. (2001) Trends in wood density and structure are linked toprevention of xylem implosion by negative pressure. Oecologia126, 457–461.

Hogg E.H. & Hurdle P.A. (1997) Sap flow in trembling aspen:implications for stomatal responses to vapor pressure deficit.Tree Physiology 17, 501–509.

Hogg E.H., Black T.A., Den Hartog G., Neumann H.H., Zimmer-mann R., Hurdle P.A., Blanken P.D., Nesic Z., Yang P.C., Stae-bler R.M., Mcdonald K.C. & Oren R. (1997) A Comparison ofsap flow and eddy fluxes of water vapor from a boreal deciduousforest. Journal of Geophysical Research-Atmospheres 102,28929–28937.

Hogg E.H., Saugier B., Pontailler J.Y., Black T.A., Chen W., Hur-dle P.A. & Wu A. (2000) Responses of trembling aspen andhazelnut to vapor pressure deficit in a boreal deciduous forest.Tree-Physiology. 20, 725–734.

Hubbard R.M., Bond B.J. & Ryan M.G. (1999) Evidence thathydraulic conductance limits photosynthesis in old Pinus pode-rosa trees. Tree Physiology 19, 165–172.

James S.A., Clearwater M.J., Meinzer F.C. & Goldstein G. (2002)Heat dissipation sensors of variable length for the measurementof sap flow in trees with deep sapwood. Tree Physiology 22, 277–283.

Jarvis P.G. (1976) The interpretation of the variation in leaf waterpotential and stomatal conductance found in canopies in thefield. Philosophical Transactions of the Royal Society of London.273, 593–610.

Jones H.G. (1992) Plants and Microclimate: a QuantitativeApproach to Environmental Plant Physiology, pp. 411. Cam-bridge University Press, New York, NY, USA.



Katul G., Leuning R. & Oren R. (2003) Relationship betweenplant hydraulic and biochemical properties derived from asteady-state coupled water and carbon transport model. Plant,Cell and Environment 26, 399–350.

Kramer P.J. & Boyer J.S. (1995) Water Relations of Plants andSoils pp. 495. Academic Press, San Diego, CA, USA.

Légaré S., Paré D. & Bergeron Y. (2004) The responses of blackspruce growth to an increased proportion of aspen in mixedstands. Canadian Journal of Forest Research I, 405–416.

Lieffers V.J. & Rothwell R.L. (1986) Effects of water table andsubstrate temperature on root and top growth of Picea marianaand Larix laricina seedlings. Canadian Journal of ForestResearch 16, 1201–1206.

Lieffers V.J. & Rothwell R.L. (1987) Rooting of peatland blackspruce and tamarack in relations to depth of water table. Cana-dian Journal of Forest Research. 65, 817–821.

Littel R.C., Milliken G.A., Stroup W.W. & Wolfinger R.D. (1996)SAS System for Mixed Models. SAS Institute, Cary, NC, USA.

Lu P., Muller W.J. & Chacko E.K. (2000) Spatial variations inxylem sap flux density in the trunk of orchard-grown, maturemango trees under changing soil water conditions. Tree Physiol-ogy 20, 683–692.

Lundblad M., Lagergren F. & Lindroth A. (2001) Evaluation ofheat balance and heat dissipation methods for sapflow measure-ments in pine and spruce. Annals of Forest Science 58, 625–638.

Magnani F., Mencuccini M. & Grace J. (2000) Age-related declinein stand productivity: the role of structural acclimation underhydraulic constraints. Plant, Cell and Environment 23, 251–263.

Martin T.A., Brown K.J., Cermak J., Ceulemans R., Kucera J.,Meinzer F.C., Rombold J.S., Sprugel D.G. & Hinckley T.M.(1997) Crown conductance and tree and stand transpiration ina second-growth Abies amabilis forest. Canadian Journal of For-est Research-Revue Canadienne de Recherche Forestiere 27, 797–808.

McDowell N., Barnard H., Bond B.J., et al. (2002a) The relation-ship between tree height and leaf area: sapwood area ratio.Oecologia 132, 12–20.

McDowell N.G., Phillips N., Lunch C., Bond B.J. & Ryan M.G.(2002b) An investigation of hydraulic limitation and compensa-tion in large, old Douglas-fir trees. Tree Physiology 22, 763–774.

Meinzer F.C. & Grantz D.A. (1991) Coordination of stomatal,hydraulic, and canopy boundary-layer properties – do stomatabalance conductances by measuring transpiration. PhysiologiaPlantarum 83, 324–329.

Meinzer F.C., Goldstein G., Holbrook N.M., Jackson P. & Cave-lier J. (1993) Stomatal and environmental-control of transpira-tion in a lowland tropical forest tree. Plant, Cell andEnvironment 16, 429–436.

Mencuccini M., Grace J. & Fioravanti M. (1997) Biomechanicaland hydraulic determinants of tree structure in scots pine: ana-tomical characteristics. Tree Physiology 17, 105–113.

Monteith J.L. (1995) A reinterpretation of stomatal responses tohumidity. Plant, Cell and Environment 18, 357–364.

Monteith J.L. & Unsworth M.H. (1990) Principles of Environmen-tal Physics. Edward Arnold, London., UK.

Mott K.A. & Parkhurst D.F. (1991) Stomatal response to humidityin air and helox. Plant, Cell and Environment 14, 509–515.

Nardini A., Lo Gullo M.A. & Tracanelli S. (1996) Influence of leafwater status on stomatal response to humidity, hydraulic con-ductance and soil drought in Betula occidentalis. Planta 196,357–366.

Ogle K. & Reynolds J.F. (2002) Desert dogma revisited: couplingof stomatal conductance and photosynthesis in the desert shrub,Larrea tridentata. Plant, Cell and Environment 25, 909–921.

Oren R., Phillips N., Ewers B.E., Pataki D.E. & Megonigal J.P.(1999b) Sap-flux-scaled transpiration responses to light, vapor

pressure deficit, and leaf area reduction in a flooded Taxodiumdistichum forest. Tree Physiology 19, 337–347.

Oren R., Phillips N., Katul G., Ewers B.E. & Pataki D.E. (1998)Scaling xylem sap flux and soil water balance and calculatingvariance: a method for partitioning water flux in forests. AnnalesDes Sciences Forestieres 55, 191–216.

Oren R., Sperry J.S., Ewers B.E., Pataki D.E., Phillips N. &Megonigal J.P. (2001) Sensitivity of mean canopy stomatal con-ductance to vapor pressure deficit in a flooded Taxodium disti-chum L. forest: hydraulic and non-hydraulic effects. Oecologia126, 21–29.

Oren R., Sperry J.S., Katul G.G., Pataki D.E., Ewers B.E., PhillipsN. & Schafer K.V.R. (1999a) Survey and synthesis of intra- andinterspecific variation in stomatal sensitivity to vapour pressuredeficit. Plant, Cell and Environment 22, 1515–1526.

Oren R., Zimmerman R. & Terborgh J. (1996) Transpiration inupper Amazonian floodplain and upland forests in response todrought breaking rains. Ecology 77, 968–973.

Pataki D.E., Oren R., Katul G. & Sigmon J. (1998) Canopy con-ductance of Pinus taeda, Liquidambar styraciflua and Quercusphellos under varying atmospheric and soil water conditions.Tree Physiology 18, 307–315.

Pataki D.E., Oren R. & Phillips N. (1998) Responses of sap fluxand stomatal conductance of Pinus taeda L. trees to stepwisereductions in leaf area. Journal of Experimental Botany 49, 871–878.

Pataki D.E., Oren R. & Smith W.K. (2000) Sap flux of co-occurringspecies in a western subalpine forest during seasonal soildrought. Ecology 81, 2557–2566.

Pearcy R.W., Ehleringer J., Mooney H.A. & Rundel P.W. (1989)Plant Physiological Ecology, pp. 434. Chapman & Hall, London,UK.

Pezeshki S.R. & Hinckley T.M. (1988) Water relations character-istics of Alnus rubra and Populus trichocarpa-response to fielddrought. Canadian Journal of Forest Research 18, 1159–1166.

Phillips N. & Oren R. (1998) A comparison of daily representa-tions of canopy conductance based on two conditional time-averaging methods and the dependence of daily conductance onenvironmental factors. Annales Des Sciences Forestieres 55, 217–235.

Phillips N., Bond B.J., McDowell N.G. & Ryan M.G. (2002) Can-opy and hydraulic conductance in young, mature and old dou-glas-fir trees. Tree Physiology 22, 205–211.

Phillips N., Oren R. & Zimmermann R. (1996) Radial patterns ofxylem sap flow in non-, diffuse- and ring-porous tree species.Plant, Cell and Environment 19, 983–990.

Pothier D., Margolis H.A., Poliquin J. & Waring R.H. (1989) Rela-tion between the permeability and the anatomy of jack pinesapwood with stand development. Canadian Journal of ForestResearch 19, 1564–1570.

Pothier D., Margolis H.A. & Waring R.H. (1989) Patterns ofchange of saturated sapwood permeability and sapwood con-ductance with stand development. Canadian Journal of ForestResearch 19, 432–439.

Powers R.F. & Van Cleve K. (1991) Long-term ecological researchin temperature and boreal forest ecosystems. Agronomy Journal83, 11–24.

Rayment M.B., Loustau D. & Jarvis P.G. (2000) Measuring andmodeling conductances of black spruce at three organizationalscales: shoot, branch and canopy. Tree Physiology 20, 713–723.

Ryan M.G. & Yoder B.J. (1997) Hydraulic limits to tree height andtree growth. Bioscience 47, 235–242.

Ryan M.G., Bond B.J., Law B.E., Hubbard R.M., Woodruff D.,Cienciala E. & Kucera J. (2000) Transpiration and whole-treeconductance in ponderosa pine trees of different heights. Oeco-logia 124, 553–560.



Saliendra N.Z., Sperry J.S. & Comstock J.P. (1995) Influence ofleaf water status on stomatal response to humidity, hydraulicconductance, and soil drought in Betula occidentalis. Planta 196,357–366.

Salleo S., Lo Gullo M.A., Raimondo F. & Nardini A. (2001) Vul-nerability to cavitation of leaf minor veins: any impact on leafgas exchange? Plant, Cell and Environment 24, 851–859.

Salleo S., Nardini A., Pitt F. & Lo Gullo M. (2000) Xylem Cavita-tion and hydraulic control of stomatal conductance in Laurel(Laurus noblis L.). Plant, Cell and Environment 23, 71–79.

Saugier B., Granier A., Pontailler J.Y., Dufrene E. & BaldocchiD.D. (1997) Transpiration of a boreal pine forest measured bybranch bag, sap flow and micrometeorological methods. TreePhysiology 17, 511–519.

Schafer K.V.R., Oren R. & Tenhunen J.D. (2000) The effect oftree height on crown level stomatal conductance. Plant Cell andEnvironment 23, 365–375.

Sellers P., Hall F., Margolis H., et al. (1995) The boreal ecosystem-atmosphere study (boreas) – an overview and early results fromthe 1994 field year. Bulletin of the American Meteorological Soci-ety 76, 1549–1577.

Smith W.K. & Carter G.A. (1988) Shoot structural effects onneedle temperatures and photosynthesis in conifers. AmericanJournal of Botany 75, 496–500.

Sokal R.R. & Rohlf F.J. (1995). Biometry. W.H. Freeman, NewYork, USA.

Sperry J.S. (1995) Limitations on stem water transport and theirconsequences. In Plant Stems: Physiology and Function Mor-phology (ed B.L. Gartner), pp. 105–224. Academic Press, SanDiego, CA, USA.

Sperry J.S., Adler F.R., Campbell G.S. & Comstock J.P. (1998)Limitation of plant water use by rhizosphere and xylem conduc-tance: results from a model. Plant, Cell and Environment 21,347–359.

Tyree M.T. & Sperry J.S. (1988) Do woody-plants operate near thepoint of catastrophic xylem dysfunction caused by dynamicwater-stress – answers from a model. Plant Physiology 88, 574–580.

Tyree M.T. & Sperry J.S. (1989) Vulnerability of xylem to cavita-tion and embolism. Annual Review of Plant Physiology andPlant Molecular Biology 40, 19–38.

Wang C.K., Bond-Lamberty B. & Gower S.T. (2003) Carbon dis-tribution of well- and poorly-drained black spruce fire chronose-quence. Global Change Biology 9, 1066–1079.

Whitehead D. & Jarvis P.G. (1981) Coniferous forests andplantations. In Water Deficits and Plant Growth, Vol. VI (ed.T.T. Kowlowski), pp. 49–152. Academic Press, New York,USA.

Whitehead D., Edwards W.R.N. & Jarvis P.G. (1984) Conductingsapwood area, foliage area, and permeability in mature trees ofPicea sitchensis and Pinus contorta. Canadian Journal of ForestResearch. 14, 940–947.

Yanai R.D., Arthur M.A., Siccama T.G. & Federer C.A. (2000)Challenges of measuring a forest floor organic matter dynamics:Repeated measures from a chronosequence. Forest Ecology andManagement 138, 273–283.

Received 8 September 2004; received in revised form 4 November2004; accepted for publication 19 November 2004

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