Advances in Water Resources 26 (2003) 1267–1278

www.elsevier.com/locate/advwatres

Species differences in stomatal control of water loss at thecanopy scale in a mature bottomland deciduous forest

D.E. Pataki a,*, R. Oren b

a Department of Biology, University of Utah, 257 S 1400 E, Salt Lake City, UT 84112, USAb Nicholas School of the Environment, Duke University, Durham, NC 27708, USA

Abstract

In order to evaluate factors controlling transpiration of six common eastern deciduous species in North America, a model

describing responses of canopy stomatal conductance (GS) to net radiation (RN), vapor pressure deficit (D) and relative extractable

soil water (REW) was parameterized from sap flux data. Sap flux was measured in 24 mature trees consisting of the species Carya

tomentosa, Quercus alba, Q. rubra, Fraxinus americana, Liriodendron tulipifera, and Liquidambar styraciflua in a bottomland oak-

hickory forest in the Duke Forest, NC. Species differences in model coefficients were found during the 1997 growing season. All

species showed a reduction in GS with increasing D. RN influenced GS in the overstory shade intolerant L. styraciflua to a larger

extent than the other species measured. In addition, despite a severe drought during the study period, only L. tulipifera showed a

decline in GS with decreasing REW. The primary effect of the drought for the other species appeared to be early autumn leaf se-

nescence and abscission. As a result, despite the drought in this bottomland forest accustomed to ample water supply, maximum

daily transpiration (1.6 mm) and growing season transpiration (264 mm) were similar to a nearby upland forest measured during a

year of above average precipitation. These results may aid in assessing differences in water use and the ability of bottomland de-

ciduous species to tolerate alterations in the frequency or amount of precipitation. Results also suggest little variation in water use

among forests of similar composition and structure growing in different positions in the landscape and subjected to large interannual

variation in water supply.

� 2003 Elsevier Ltd. All rights reserved.

Keywords: Canopy stomatal conductance; Drought responses; Sap flux; Transpiration; Carya tomentosa; Fraxinus americana; Liquidambar

styraciflua; Liriodendron tulipifera; Quercus alba; Quercus rubra

1. Introduction

Species differences in patterns of water use and re-

sponses to soil drought are two areas of uncertainty in

determining the transpiration component of evapo-

transpiration in diverse ecosystems [1]. This uncertainty

is compounded in mature forests due to the difficulties of

directly measuring whole canopy transpiration andstomatal conductance in individual trees. To address

these issues, thermal methods of measuring sap flux

density in the stems of large trees have been developed

to estimate water use and canopy stomatal conductance

(GS, mean canopy stomatal conductance weighted by

*Corresponding author. Tel.: +1-801-581-3545; fax: +1-801-581-

4665.

E-mail addresses: pataki@biology.utah.edu (D.E. Pataki), ramo-

ren@duke.edu (R. Oren).

0309-1708/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/j.advwatres.2003.08.001

leaf area) for patches of tree crowns. Continuous mea-

surements of GS in response to changing atmospheric

and soil moisture conditions can be used to address the

role of water stress in influencing transpiration and

the importance of species composition in determining

ecosystem water use, water balance, and soil moisture

depletion.

In this study, GS was calculated from sap flux mea-surements in a southeastern oak-hickory forest in order

to assess responses to vapor pressure deficit (D), light,and soil moisture depletion in six co-occurring species.

Mixed species stands dominated by Quercus spp. (oak)

and Carya spp. (hickory) overstories are common

throughout the southeastern US in areas which have

been permitted to reach late successional stages of

development [2–4]. In addition to shade-tolerant, co-dominant Quercus and Carya spp., these stands may

contain more shade-intolerant but fast-growing pioneer

species in the overstory, such as Liriodendron tulipifera L.

Nomenclature

a, a0, b, b0, c empirical model coefficients

cp heat capacity of moist air (J kg�1 K�1)d diameter (cm)

dbh diameter at 1.4 m (cm)

gbl boundary layer conductance (mmolm�2 s�1)

gs stomatal conductance (mmolm�2 s�1)

Al leaf area (m)

Al=AS leaf to sapwood area ratio (m2 cm�2)

AS=AG sapwood to ground area ratio (m2 m�2)

D vapor pressure deficit (kPa)EC transpiration of canopy trees (mmd�1)

GS canopy stomatal conductance (mmolm�2 s�1)

GSmax canopy stomatal conductance under moist

conditions (mmolm�2 s�1)

IO overstory photosynthetically active radiation

(lmolm�2 s�1)JS sap flux density (gm�2 s�1)

LAI leaf area index (m2 m�2)

REW relative extractable soil water (unitless)

RN net radiation (Wm�2)

SLA specific leaf area (cm g�1)

k latent heat of vaporization (J kg�1)

h soil moisture content (cm3 cm�3)

hmax soil moisture content at saturation(cm3 cm�3)

hmin minimum recorded soil moisture content

(cm3 cm�3)

q density of moist air (kgm�3)

1268 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

(yellow poplar) and Liquidambar styraciflua L., (sweet-

gum) as well as moderately shade tolerant Fraxinus

americana L. (white ash) in moister, alluvial areas

[2,3,5].

Contrasting patterns of leaf-level stomatal conduc-

tance (gs) have been observed for these species in re-

sponse to drought. Quercus spp. and C. tomentosa have

been found to be relatively resistant to drought, withsustained gs and photosynthesis during water stress, i.e.

leaf water potentials less than )2.5 MPa [6], as well as

osmotic adjustment in response to soil water deficits [7].

In a comparative study of L. styraciflua and Q. falcata,

Pezeshki and Chambers [8] reported a larger decline in

gs of L. styraciflua following water stress treatment.

Conductance in L. tulipifera has also been found to be

sensitive to water stress, with midday stomatal closureoccurring during periods of drought [9]. Rapid stomatal

closure in response to drought has been reported for F.

americana [10,11], as well as slow stomatal re-opening

following drought-induced stomatal closure in compar-

ison to co-occurring species [11]. However, given the

difficulties in scaling leaf-level gas exchange to large

canopies, it is difficult to translate these results directly

into the implications for ecosystem water use and hy-drology [12].

From previous leaf-level studies, we expected crown-

scale conductance responses of species in our bottom-

land site to fall into two general categories. While

drought-avoidant stomatal closure and reduced water

use was hypothesized for L. tulipifera, L. styraciflua, and

F. americana during the summer of 1997, a season with

long periods without precipitation, we hypothesized thatC. tomentosa, Q. alba, and Q. rubra would show smaller

reductions in fluxes during the same period. We em-

ployed a simple set of models to assess the significance

of environmental variables in influencing GS, and to test

species differences in responses at the stand level. Al-

though the growing season of 1997 was similar overall

(626 mm) to previous years, the long dry periods be-

tween rain events coupled with the shallow rooting zone

and high rock content prevents this bottomland forest

soil from storing water during the infrequent and intense

storms that occurred in 1997, thus limiting water supply.

At the stand level we expected that the bottomland

forest would exhibit stand-level water stress in greatlyreduced transpiration when compared to an upland

forest of similar structure monitored during a period of

less restricting water supply [1].

2. Methods

2.1. Study site

The site was located in the Duke Forest, NC

(35�580N, 79�080W), situated in a transitional zone be-

tween the coastal plain and the Piedmont plateau at

approximately 130 m above sea level, with 15.5 �C mean

annual temperature and 1140 mm mean annual precip-

itation. A circular plot 25 m in radius was established

around a 45 m research tower in a bottomland decidu-

ous forest consisting primarily of Carya tomentosa

[Poir.] Nutt., C. glabra (Mill.) Sweet, Quercus alba L., Q.

rubra L., Q. michauxii Nutt., Q. prinus L., Liriodendron

tulipifera L. and Liquidambar styraciflua L. in the

overstory, and Cornus florida L., Fraxinus americana L.,

Ostraya virginiana (Mill.), and Ulmus rubra M€uuhl in the

understory. The soil type was an Iredell gravely loam

with a >4% slope.

2.2. Instrumentation

Twenty mm long sap flow sensors were constructed

after Granier [13]. The sensors were installed in the outer

Table 1

Sample size (n), diameter range at 1.4 m above the ground (d), specificleaf area (SLA)± 1 SE, and leaf area index (LAI) for each species in the

1050 m2 study plot

Species n d (cm) SLA (cm2 g�1) LAI (m2 m�2)

C. tomentosa 6 16.8–54.0 119.0± 7.3 1.35

Q. alba 3 18.2–33.9 108.7± 5.3 0.26

Q. rubra 2 33.2–45.7 94.1± 3.9 0.27

L. styraciflua 5 14.9–38.0 120.1± 7.1 0.44

L. tulipifera 5 17.8–57.4 106.2± 7.0 0.62

F. americana 3 11.8–14.6 209.7± 11.8a 0.07

aDue to the low density of this species in the stand, mean SLA of

the other primary understory species Cornus florida and Ostrya vir-

giniana.

D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278 1269

xylem and were utilized to calculate sap flux density (JS,g H2Om�2 s�1) as described in Pataki et al. [14]. Sample

sizes and plot characteristics are given in Table 1. A

probe for temperature and relative humidity measure-

ments (Vaisala HMP 35C, Campbell Scientific, Logan,UT, USA) was located at approximately two-thirds

canopy height (about 20 m) for estimating the vapor

pressure deficit (D, kPa). In addition, a net radiometer

(Q7, REBS, Bellevue, WA, USA) and a tipping bucket

rain gauge was placed on the top of the tower. Inci-

dent overstory photosynthetically active radiation (IO,lmolm�2 s�1) was periodically available atop a second

meteorological tower in an adjacent forest.The presence of surface bedrock throughout the

stand was indicative of a shallow soil depth. Augering at

this site indicated an average rooting depth of �40 cm.

Installation of soil sensors was inhibited by prevalence

of rocks and bedrock. We were able to measure volu-

metric soil water content (h, cm3 cm�3) with two theta-

probes (Delta-T Devices Ltd., Cambridge, UK) placed

at different locations at a depth of 5–10 cm where rockswere relatively sparse.

Sap flow, soil moisture, and atmospheric data were

recorded on a data logger (DL2, Delta-T devices) sam-

pling every 30 s and averaging every 30 min for the

duration of the study, May 28–October 31, 1997.

2.3. Leaf area measurements

To determine stand leaf area by species, five 1 m · 1 mlitter traps were distributed under the canopy. From

August–December, abscised leaves were collected twice

weekly while still moist, and were identified and sorted

by species. The projected area of a subsample of 5–10

leaves from each species was measured optically with a

digital leaf area meter (DIAS Digital Image AnalysisSystem, Decagon Devices, Inc., Pullman, WA, USA).

These sample leaves were dried for 48 h at 70 �C after

determination of leaf area, and dry weights were ob-

tained to calculate the specific leaf area (SLA, cm2 g�1)

of each species during each collection period. The re-

mainder of collected leaves was also dried and weighed.

The leaf area of each species (A1i) was then obtained by

multiplying SLA by the total dry weight for that species,

and averaging the values of the five litter traps. Sufficient

samples of F. americana foliage were not available in

collected litter due its low density in the stand. A meanSLA value for the understory species Cornus florida and

O. virginiana, for which leaves were available in greater

abundance, was substituted to determine the LAI of F.

americana. This approach will probably affect the ab-

solute values of GS in F. americana, which is expressed

on a leaf area basis, but not the responses of GS to en-

vironmental variables during the period of stable AL.

2.4. Stand transpiration

Transpiration of each species was then scaled to the

stand level as follows:

ECi ¼ JS � ASi=AG ð1Þ

where ECi is the transpiration of canopy species i, JS is

the species mean sap flux density, and ASi=AG is thesapwood to ground area ratio of species i.

ECi summed for all measured species is equal to the

canopy stand transpiration EC. As only overstory spe-

cies were measured in this study, this value does not

include transpiration of understory and herbaceous

species in the stand.

To estimate ASi, hydroactive xylem area was esti-

mated for each tree in the plot. A relationship betweendiameter and sapwood area was developed from cross-

sections of fallen trees uprooted by a hurricane in Sep-

tember, 1996 throughout the Duke Forest and the Eno

State Park, NC. Individuals used to generate relation-

ships covered a range in size and represented a variety of

topographical areas, from ridge tops and slope forests to

bottomland stands. For each individual, stem diameter

was first measured using a tape, and then bark thicknessand heartwood diameter were measured in four radial

directions using a caliper. Sapwood area was obtained

by the difference between total stem cross-sectional area

excluding bark and heartwood area. The relationships

between sapwood and diameter for each species were

used to estimate the sapwood area of all individuals in

the plot, which was then summed and divided by the

plot area to obtain ASi=AG.

2.5. Canopy stomatal conductance calculations

GS may be calculated from sap flux measurements

with a simplified form of the Penman–Monteith equa-tion when certain assumptions are met, namely: (1) JSmay be assumed to be radially uniform throughout the

hydroactive xylem area, (2) boundary layer conductance

(gbl) is sufficiently large, and (3) stem capacitance may be

neglected [15–17]. The first assumption was addressed

by Phillips et al. [18], who found uniform JS at varying

1270 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

depths of sapwood in Q. alba and L. styraciflua at a

separate stand in the Duke Forest. These results have

since been confirmed in the other species occurring at

this site, particularly C. tomentosa and L. tulipifera

which have deep sapwood (Oishi, unpublished data).The second assumption has been discussed by Oren et al.

[19], who point out that that large values of gbl may

reduce the sensitivity of GS to D; however, a 20 fold

increase in the ratio of gbl to stomatal conductance re-

duced the sensitivity of GS to D by only 20% in their

theoretical calculations.

With regard to the third assumption, lag times be-

tween JS and D of 0–5 h were evaluated for each speciesunder conditions of high and low soil moisture, as time

lags have been shown to increase with soil moisture

depletion [20]. The highest correlations (P < 0:05) werefound at a zero lag for all species except L. tulipifera

under dry conditions only. In other words, stem ca-

pacitance in these trees resulted in time lags between sap

flux at the base and transpiration at the canopy of less

than half an hour, with the exception of L. tulipifera.For the drought period, it was necessary to incorporate

a one-hour lag in half-hourly GS calculations for this

species, the time lag at which JS and D were most

strongly correlated (P < 0:05).GS was calculated with the following simplified form

of the Penman–Monteith equation after Whitehead and

Jarvis [15]:

GS ¼GCi

LAIi¼ ckECi

qcpDLAIið2Þ

where GCi is canopy conductance of species i, c is the

psychrometric constant (kPaK�1), k is the latent heat of

vaporization (J kg�1), q is the density of moist air

(kgm�3), and cp is the heat capacity of moist air

(J kg�1 K�1). As values are calculated from LAI, GS is

presented on a one-sided leaf area basis.Due to collinearity of the independent variables in

this analysis, the response of GS to radiation, D, and soil

moisture was described with a set of multiplicative non-

linear equations rather than multivariate regression

analysis, an approach described by Jarvis [21]. For each

species, the general decline of GS with decreasing soil

moisture availability, increase with increasing incident

radiation, and decrease with increasing D typically ob-served under most circumstances was described with

equations taken from Granier and Br�eeda [22]:

GS ¼ GSmax � ða0 þ b0 � log10 ðREWÞÞ ð3Þ

GSmax ¼ ðRN=ðRN þ aÞÞ � ðbþ c � lnðDÞÞ ð4Þ

REW ¼ ðh � hminÞ=ðhmax � hminÞ ð5Þ

where hmin and hmax are the minimum and maximum

values of h recorded during the entire study, b is a ref-

erence conductance at D ¼ 1 kPa, c describes stomatal

sensitivity to D, and a, a0 and b0 are species-dependent

empirical constants. While the analysis of Granier and

Br�eeda [22] utilizes global radiation, RN was available at

this site from concurrent measurements due to its ap-

plication in calculating energy balance. As total and netradiation are linearly related under a common range of

conditions, the choice of RN rather than total or pho-

tosynthetically active radiation should have little influ-

ence on the results.

Coefficients were obtained by a non-linear least

squares fitting procedure (Sigma Plot 5.0, SPSS Inc.,

Chicago, IL, USA). The resulting coefficients are largely

descriptive; however, the mechanistic basis for the ob-served variation in b and c for a range of species, in-

cluding those measured in this study, has been described

by Oren et al. [23]. Here, we utilized model coefficients

to evaluate differences in the behavior of each species

with regard to the dependent variables. In addition, an

analysis of residuals was employed to differentiate pe-

riods in which coefficients were unable to capture the

behavior of GS. In this manner, additional factors whichtemporally affect GS of each species could be evaluated,

e.g. changes in leaf phenology at the beginning or end of

the growing season.

3. Results

3.1. Environmental and sap flux data

Daily atmospheric and soil moisture data for the

duration of the study are shown in Fig. 1. Maximum

temperature reached 36.4 �C in August, while the min-

imum temperature was )0.2 �C in October. Tempera-ture, and therefore D, showed a seasonal trend, while no

pattern in humidity was apparent. Temporal variation

in h is high due to long, intermittent periods without

precipitation during July and August. Shallow soil

moisture declined from a maximum of about 38% water

content by volume in late June to values close to 10% in

July and August. The soil was re-saturated in late Au-

gust following a large precipitation event. Although thespatial variability in h was probably not adequately

captured, both sensors showed the same temporal pat-

terns throughout the season. Responses of JS to these

patterns, particularly variations in responses to D, areevident in the seasonal pattern of daily values shown by

species in Fig. 2. While relative day to day variability is

small in Quercus spp. and F. americana, large changes in

L. tulipifera are evident.Species differences in daily water use result from

variation in atmospheric conditions and/or soil mois-

ture. In Fig. 3, diurnal patterns of JS are shown for a day

of high and low IO and D. Volumetric soil moisture was

equal to 0.36 and 0.35 cm3 cm�3 on each day, respec-

tively. The difference in sap flux values on both days is

160 200 240 2800.0

0.1

0.2

0.3

0

0.0

0.5

1.0

1.5

20

40

60

80

1000

10

20

30

40

50

Day of year

θ 5-

10 c

m

(cm

3 cm

-3)

Mea

n da

ytim

e D

(kP

a)M

ean

dayt

ime

RH

(%

)T

A (

˚C)

Fig. 1. Maximum (), mean (�), and minimum (H) ambient tem-

perature (TA), mean daytime relative humidity (RH), mean daytime

vapor pressure deficit (D), and volumetric soil water content (h) areshown for the duration of the study.

160 200 240 2800

50

100

150

0

50

100

150

0

50

100

150

Q. rubra

C. tomentosa

Q. alba

Day

Dai

ly J

s (g

.cm

-2d-1

)

Duke Forest, NC

Fig. 2. Daily sap flux density (JS) for each species ±1 SE for the duration of t

equipment failure.

D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278 1271

lesser for Quercus spp. and C. tomentosa than for L.

tulipifera, L. styraciflua, and F. americana (ANOVA

with repeated measurements, P < 0:05), indicating

greater sensitivity to radiation or D in these latter spe-

cies. Despite being in the understory, F. americanashowed a similar diurnal pattern to L. styraciflua and L.

tulipifera.

L. tulipifera and L. styraciflua were highly responsive

to D, and showed a slight saturation in increases in daily

JS with D (Fig. 4). In contrast, increases in JS with Dwere small in the Quercus species, and saturation was

reached at low D values. Responses were similar at all

soil moisture levels for all species except L. tulipifera andto a lesser extent, L. styraciflua. In the first dry period

from July 5–28, JS of L. tulipifera was reduced at the

same D (t-test, P < 0:05), although there was no effect in

the other species. Following precipitation in early Au-

gust, soil moisture dropped again to similar levels from

August 10–19. During this period JS was further reducedin L. tulipifera (t-test, P < 0:05), and some effect is ap-

parent in L. styraciflua, although the difference wasmarginal (P ¼ 0:14). At, this time, leaf wilting and

senescence were apparent in L. tulipifera.

3.2. Canopy stomatal conductance

In calculating GS values were excluded when D was

<0.6 kPa or RN was <10 lmolm�2 s�1 to avoid errors in

estimating GS resulting from conditions of very low flux

[20,24]. In order to estimate ASi for Eq. (2), relation-

ships between diameter and ASi derived from stem

160 200 240 280

L. styraciflua

L. tulipifera

F. americana

of year

May 28 - Oct. 31, 1997

he study. Days of missing data appear as a result of lightening-induced

5 10 15 20 0 5 10 15 20 00

10

20

30

40

50

400

800

1200

1600

C. tomentosaF. americanaL. tulipiferaQ. rubraQ. albaL. styraciflua

June 16, 1997

0.0

4.0

8.0

1.2

1.6

D (kP

a)

Hour of day

J s (

g.m

-2s-1

)I o

(µm

ol. m

-2s-1

)

June 14, 1997

Duke Forest, NC

IoD

Fig. 3. Diurnal patterns of sap flux density (JS) for each species on days of different incident overstory radiation (IO) and vapor pressure deficit (D).Error bars represent 1 SE.

1272 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

cross-sections were applied from Table 2, which shows

good correlations for all species.

The model describing GS was used both before and

after the drought to evaluate the initiation of leaf se-nescence in early September, as reflected in changes in

coefficient estimates. The model was parameterized on

an individual tree basis, with resulting coefficients av-

eraged by species for species comparisons. Initially, GS

under non-limiting soil moisture conditions (GSmax) from

June 7–June 19 was parameterized according to Eq. (4).

(In this context, GSmax refers to values obtained for a

subset of soil moisture conditions but a range of atmo-spheric conditions, and is therefore non-constant.) In

Fig. 5, GSmax is shown in response to RN and D sepa-

rately. In response to RN alone, GSmax increased only in

L. tulipifera, L. styraciflua, and Quercus spp. (P < 0:05).However, because RN and D co-vary, Eq. (4) was used to

separate the effects of these variables on GSmax by eval-

uating the significance of the coefficients a, b, and c. Theresults showed that RN significantly explained variationsin GS in all species when variations in D were taken in

account; i.e. the coefficient a explained variations in GS

(P < 0:05) for all species in Eq. (4). In response to D,GSmax of all species showed the characteristic curvilinear

decrease (Fig. 5). The mean model coefficients for each

species are given in Table 3. As no difference in pa-

rameters was apparent for the two Quercus spp., which

had low sample sizes, values for the two Quercus spp.

are combined for statistical tests of parameters.

To assess the effects of h on GS of each species, themodel was used to calculate GSmax from June 20–July 15.

During this period h progressively decreased from about

0.36 to 0.15 (Fig. 1). The ratio of GS (Eq. (3)) to GSmax

(Eq. (4)) in response to REW (Eq. (5)) is shown in Fig.

6. Only L. tulipifera showed an increase of GS=GSmax

with increasing REW. Thus, the REW portion of the

model given in Eq. (3) was not included in descriptions

of GS of the other species. The REW model parametersfor L. tulipifera are shown in Table 3.

From the analyses of responses to RN, D, and REW

described above, the resulting model coefficients (Table

3) were used to estimate GS half-hourly for each species

during the entire growing season. Residuals of model-

estimated GS minus GS calculated from sap flux and Dfor the length study period for each species are shown

normalized by 1 SD in Fig. 7. The residuals plotsshowed that the model captured variations in GS satis-

factorily for much of the growing season, with 10 day

running averages of residuals captured within 1 SD.

Seasonally, trends in residuals were evident late in the

season after mid-September for Quercus spp., C. tom-

entosa, and L. tulipifera, when running averages of

Fig. 4. The response of daily sap flux density (JS) to vapor pressure

deficit (D) under conditions of varying volumetric soil moisture (h,cm3 cm�3). Two dry periods are shown from July 5–28 and from

August 10–19 during which h was <0.2 cm3 cm�3. Differences in JSresponses to D during the August drought are likely due to foliage loss

in L. tulipifera, and to a lesser extent L. styraciflua.

Table 2

Regression coefficients for predictions of cross-sectional sapwood area

(AS, cm2) from basal area (AB) at 1.4 m above the ground

(AS ¼ b0 þ b1 � AB, P < 0:01), with sample size (n) and the range of

diameters used in the analysis

Species n d (cm) b0 b1 r2 Al=AS

(m2 cm�2)

Carya spp. 10 16.1–47.5 90.5 0.50 0.85 0.22

Quercus spp.

(red)

10 21.1–47.5 )36.4 0.26 0.95 0.21

Quercus spp.

(white)

10 20.0–62.4 98.8 0.17 0.82 0.46

L. styraciflua 11 8.7–37.5 14.0 0.70 0.84 0.11

L. tulipifera 23 9.8–62.3 59.3 0.43 0.78 0.15

Tree diameter (d) at 1.4 m and leaf to sapwood area ratios (Al=AS,

m2 cm�2) generated from litterfall and sapwood area estimates are also

given.

D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278 1273

residuals began to exceed 1 SD and in some cases 2 SD

from the mean (Fig. 7).

3.3. Canopy transpiration

Daily EC was estimated from daily JS and ASi=AG

according to Eq. (1). This estimate of EC represents the

water uptake for overstory species only, which consti-tuted approximately 70% of the total LAI of woody

species in the stand (4.7 m2m�2) based on litter collec-

tion, the remaining LAI being attributable to sub-

canopy Cornus florida, Ostraya virginiana, and Ulmus

rubra. The maximum daily value of EC by canopy trees

(LAI ¼ 3.3) was 1.6 mmd�1, with a seasonal mean of

1.2 mmd�1.

4. Discussion

Characteristic decreases in GS with increasing D and

increases in GS with increasing RN were observed in allspecies. Liquidambar styraciflua showed the largest re-

sponses to RN (Table 3). However, contrary to hypoth-

esized responses of GS to soil moisture in L. styraciflua,

L. tulipifera, and F. americana, relative soil water ex-

traction affected GS only in L. tulipifera (Fig. 6). For the

other species, the primary effect of the drought appeared

to be unusually early leaf senescence and abscission

beginning in mid to late September (Fig. 8). Changes inmodel residuals indicated that the inclusion of canopy

leaf area as estimated from litterfall did not explain

variations in GS for all species in the fall. Additional

physiological changes, probably associated with leaf

senescence, affected GS in mid-September for C. tomen-

tosa, L. tulipifera, and Quercus spp. (Fig. 7).

Absolute values of GS were slightly lower than those

previously reported for these species, particularly forQuercus [8,25–28]; however, previous studies were con-

ducted at the single leaf scale, often on seedlings or

saplings. Sap flux-derived GS values in a previous study

of a mature, upland deciduous forest [1] were more

similar to the values reported here. In mature individ-

uals, shading effects as well as the need to preserve the

hydraulic integrity of xylem may limit the capacity for

GS, in the latter case due to increases in hydraulic pathlength, decreases in the permeability of mature wood,

and increased contribution of the gravitational compo-

nent of leaf water potential, reducing the force driving

water from soil to leaf [29,30]. While sap flux measure-

ments in large trees can underestimate actual canopy

transpiration by the amount of water transpired from

stem storage [16], this effect was found to be minimal in

the analysis of lag times between JS and D. Qualitatively,this is illustrated in the rapid decline in flux following

nightfall shown in Fig. 3.

In studies where natural shade effects were evaluated,

leaf-level gs values were more similar to GS reported

here, as for gs of C. tomentosa and F. americana given

by Abrams and Mostoller [27]. In that study, gs of

Table 3

Mean model parameters (±1 standard error) describing canopy stomatal conductance in relation to light, vapor pressure deficit, and soil moisture

(see Eqs. (3)–(5))

Species a b c a0 b0

C. tomentosa 39.8a ± 17.3 55.0ac ± 8.7 46.8a ± 11.1 NS NS

F. americana 43.1a ± 6.0 80.5ac ± 11.1 57.6a ± 10.6 NS NS

L. tulipifera 64.0a ± 15.2 104.2c ± 34.7 66.5a ± 25.4 1.1± 0.1 0.5± 0.2

Quercus spp. 44.6a ± 13.2 20.5a ± 6.1 16.1a ± 5.8 NS NS

L. styraciflua 231.7b ± 70.8 167.0b ± 28.8 89.0a ± 38.9 NS NS

NS indicates parameters are not significant at a ¼ 0:05. Superscripts indicate species differences by the least squared difference test (a ¼ 0:05).

0

50

100

150

0

50

100

150

0 200 400 600

RN (W.m-2)

L. styraciflua

L. tulipiferaF. americana

C. tomentosa

0.5 1 1.5 2

D (kPa)

Duke Forest, NC June 8 - June 19, 1997

GS

max

(m

mol

. m-2

s-1 )

Quercus spp.

Fig. 5. Upper panels––Canopy stomatal conductance under non-limiting soil moisture conditions (GSmax) is shown in relation to net radiation (RN)

and vapor pressure deficit (D). Lower panels––GSmax estimated from the relationship GSmax ¼ RN=ðRN þ aÞ in the left panel and GSmax ¼ bþ c � lnðDÞin right panel. Filled symbols indicate that this relationship was significant at a ¼ 0:05.

1274 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

C. tomentosa varied from approximately 100–800

mmolm�2 s�1 for sun leaves, compared with 30–300

mmolm�2 s�1 in the shade. For F. americana, gs variedfrom 150–600 mmolm�2 s�1 in the sun to 50–150

mmolm�2 s�1 in the shade. As an integration of gsfor the whole canopy, values on the order of 100

mmolm�2 s�1 commonly recorded in this study show the

effect of large proportions of shaded foliage on total GS.Species differences in sap flux density were similar

to previously reported patterns of high JS in C. tom-

entosa, and low JS in Quercus spp. that rapidly satu-

rates with increasing D [1]. Thus, these values appear

to reflect typical fluxes for southeastern forests. When

mid-season flux values were scaled to the stand-level to

obtain canopy transpiration, average EC fell well

within the range of values for this region at 1.2

mmd�1, with a maximum of 1.6 mmd�1. The standard

error of the EC estimate was 0.3 mmd�1, based on thetree-to-tree variability in sap flux. Therefore, EC in this

study was not distinguishable from the value of 1.3

0

0.4

0.8

1.2

1.6

2

0.4

0.8

1.2

1.6

2

0.2 0.4 0.6 0.8

Relative Extractable Soil Water

Jun.20-Jul.15, 1997

GS/G

Sm

ax

Fig. 6. Upper panel––Canopy stomatal conductance (GS) as a pro-

portion of model estimated maximum GS (GSmax) under non-limiting

soil moisture conditions is shown in relation to relative extractable

water (REW). GSmax was estimated from Eq. (4) in the text, and REW

from Eq. (5). As an increase of GS=GSmax with REW was found in L.

tulipifera (a ¼ 0:05), symbols for this species are filled. Lower panel––

GS=GSmax estimated from the data in the upper panel is shown for

L. tulipifera.

D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278 1275

mmd�1 previously measured in two similarly tall

stands in the Duke Forest, an upland deciduous forestand a flooded forest of the deciduous conifer Taxo-

dium distichum [1,31].

The study in the upland forest in 1993 encompassed

the complete growing season beginning in March, while

in the current study monitoring began in late May. In

1993, transpiration in March when leaves were only

beginning to develop was below average, while transpi-

ration in May with fully developed leaves and ample soilmoisture was above average [1]. Assuming that average

EC during March–May is similar to the average of the

rest of the season, growing season EC by trees in this

bottomland forest was 264 mm (42% of the 1997

growing season precipitation, Table 4). This is remark-

ably similar to EC of 278 mm (43%) estimated in the

upland forest which had a somewhat deeper soil and a

50% larger main canopy leaf area index [1], Table 4. Inthe upland forest, interception by the canopy was rela-

tively small, or 14% of growing season precipitation,

despite the large leaf area index. If this ratio can be

extrapolated to the lowland forest, then EC as a pro-

portion of throughfall, growing season precipitation and

potential evapotranspiration was very similar in the two

forests (Table 4). Mean daily EC during the 1993

growing season averaged 1.4 mmd�1 in two pine standsadjacent to the deciduous forest plot in this study, when

their LAI was �2.1 [32], for a growing season total of

297 mm. This seems to support Roberts’ hypothesis that

transpiration is a conservative value [33]. However, EC

may not be conserved across all forest types. By 1997,

LAI in these evergreen stands reached 3.2 during the

growing season, supporting a mean daily EC of 1.8

mmd�1, for a season sum of 404 mm. As these standsdeveloped and LAI increased to over 5, annual EC was

well over 500 mm [34]. Nevertheless, our results suggest

that mature deciduous forests with fully developed

canopies use similar amounts of water despite large

variations in available moisture caused by differences in

site characteristics and annual precipitation.

4.1. Effects of vapor pressure deficit

The mechanistic basis underlying the slope of the

relationship between b and c in Eq. (4) has been de-

scribed by Oren et al. [23], who applied a steady-statemodel of stomatal regulation of leaf water potential to

derive a theoretical slope of 0.59. The b and c coefficients

of all 24 individuals in this study, which represent a

reference conductance at D ¼ 1 kPa and the stomatal

sensitivity to D, respectively, were linearly related with a

slope of 0.7 ± 0.04 (P < 0:05, R2 ¼ 0:85) when the re-

gression was forced through the origin (the intercept was

non-significant, P > 0:1). Implicit in the theoreticalcalculation are the assumptions that leaf water potential

is perfectly regulated, gbl is twice the value of stomatal

conductance, and leaf-specific hydraulic conductance

decreases slightly with respect to changes in D (i.e. xylem

cavitation and changes in leaf mesophyll physiology at

high D are negligible). In addition, the D range over

which the analysis is performed has an effect on the

slope, which for example increases to 0.68 when therange decreases from 1–4 to 1–3 kPa. While less strict

regulation of leaf water potential tends to reduce the

theoretical slope, lower values of gbl=gs tends to increase

it [23]. This latter mechanism, and perhaps even more

the restricted D range at the site (Fig. 1), may explain the

observed value of 0.7.

240 260 280 300 320 3400.0

0.2

0.4

0.6

0.8

1.0

C. tomentosaF. americanaL. tulipiferaQ. rubraQ. albaL. styraciflua

Day of year

Nor

mal

ized

LA

I

Duke Forest, NC Aug. 26 - Dec. 14, 1997

Fig. 8. Leaf area index (LAI) normalized by the maximum value for

each species.

Fig. 7. Normalized residuals of the canopy stomatal conductance (GS) model for each species (except Quercus spp., which combines two oak species)

during the length of the study. A ten-day running average was used to highlight the major features in the residuals. Horizontal sections reflect missing

data (see Fig. 2).

Table 4

Water balance of the forest described in this study (lowland hardwood

forest) in comparison to an upland forest measured in 1993 as

described by Oren and Pataki [1]

Upland hardwood

1993a, LAI ¼ 5

Lowland hardwood

1997, LAI ¼ 3.3

Annual

Precipitation 1235 1036

Growing season

Precipitation 642 626

Interception 90 [88]

Throughfall 552 [538]

Canopy

transpiration (EC)

278 264

Potential

evapotranspiration

765 800

The values in brackets are estimated from the results of the upland

study. Annual precipitation and potential evapotranspiration are es-

timated from nearby weather stations in Orange County, NC.a From [1], correcting for the mixing of annual and growing season

values.

1276 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

4.2. Effects of net radiation

Light responses in the GS model followed known

patterns of succession and shade tolerance for the spe-

cies in this stand. Liquidambar styraciflua and L. tuli-

pifera are pioneer species which occur early in succession

[35]. Such species are generally shade intolerant [35],

such that variations in incident radiation may strongly

affect flux, as shown in the diurnal patterns in Fig. 3.Liquidambar styraciflua showed the greatest response to

RN in that the coefficient a in the RN model term was the

largest in this species (Table 3). In fact, this species ex-

hibits a greater degree of shade intolerance than L.

tulipifera, which regenerates beneath forest canopies to

larger extent [2,36]. In similar model parameterizationsof GS, effects of radiation have not always been found

[37]. Our current results suggest that radiation may be

important in describing the average stomatal behavior

of deciduous forests, similar to the findings of Oren and

Pataki [1].

4.3. Effects of soil moisture

The model was utilized to evaluate responses to the

protracted period of drought which occurred during the

1997 season (Fig. 1). During this period, corresponding

reductions in GS with decreasing extractable soil mois-

D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278 1277

ture were apparent only in L. tulipifera. Modeling GS for

this species necessitated the addition of a function de-

scribing the response to soil moisture (Eq. (3)). In an

adjacent stand, GS was also strongly affected by soil

moisture in Pinus taeda [38,39], another fast growing,shade intolerant species commonly found in this area.

For the other species studied here, as soil moisture in the

upper horizons declined, maximal conductance was

sustained for much of the summer (Figs. 2 and 6).

Although GS of L. styraciflua and F. americana did

not show responses to soil moisture during the mid-

season period, model residuals beginning in mid-

September indicated that effects of the July drought mayhave manifested at a later time (Fig. 7). By mid-

September, gas exchange measurements of intact leaves

of L. styraciflua individuals in Duke Forest showed a

lack of stomatal opening in response to light [40].

Changes in the sensitivity of gs to environmental factors

such as light and D have been reported to accompany

leaf aging [41].

A late-season over-estimation of modeled GS wasapparent for the Quercus spp. (Fig. 7). The reduction in

the calculated GS in these species may have been caused

by declines in transpiration accompanying photosyn-

thesis, but the calculated GS may have underestimated

due to the retention of non-functional leaves which

continues to some degree throughout the winter in

Quercus [42]. The litterfall data collected here show

greater abscission in Q. alba than Q. rubra late into theseason (Fig. 8). This may be partially due to leaf re-

tention in Q. rubra, a species noted for this behavior

[42]. During the leaf-fall period, the litterfall method

overestimates effective leaf area by including non-func-

tional but intact leaves still in the canopy, resulting in

underestimation of GS. The initiation of autumnal

physiological changes early in the season and sub-

sequent changes in model parameters indicates thatdrought-induced early senescence, unaccompanied by a

comparable decrease in leaf area, occurred in Quercus

spp.

The drought sensitivity of L. tulipifera illustrated here

is consistent with observation that this species is more

restricted in its distribution than the other species we

studied [35]. Thus, future changes in the occurrence or

duration of precipitation may affect the success of thisspecies to a greater extent than associated species, pro-

moting shifts in the composition and structure of de-

ciduous forests.

5. Conclusions

In evaluating the water use of mixed species stands,

incorporating species differences in canopy stomatal

behavior may improve the representation of transpira-

tion in response to dynamic environmental conditions

and spatial variability in species composition. In this

stand, vapor pressure deficit, radiation, and soil mois-

ture had varying influences on canopy-scale stomatal

control of water loss in six co-occurring species. Dstrongly influenced GS in all species. RN had a largerinfluence on GS in the shade intolerant species L. sty-

raciflua than other species studied, indicating that light

may be a useful parameter in modeling canopy con-

ductance and water use of this species. Declining soil

moisture during long periods without precipitation

caused mid-season declines in GS only in L. tulipifera.

For the other species in this bottomland forest infre-

quently subjected to drought, the primary drought effectwas early leaf senescence and abscission later in the

growing season. Through comparisons with other

stands composed of deciduous or evergreen species, the

results suggest that more frequent or lengthy periods

without precipitation may reduce the length of the

growing season in low-lying stands adapted to moist

conditions, with strong consequences for seasonal tree

water use and hydrology in bottomland deciduousforests.

Acknowledgements

We thank Ce Huang, Nathan Phillips, Brent Ewers,

and Shauna Uselman for their assistance with site

maintenance and data collection. This project was sup-ported by the US Department of Energy (DOE) through

the National Institute for Global Environmental Change

(NIGEC) Southeast Regional Center at the University

of Alabama, Tuscaloosa (DOE Cooperative Agreement

DE FC0390ER61010) and by the Environmental Pro-

tection Agency (EPA) under the co-operative agree-

ment 91-0074-94 (CR817766). This manuscript has not

been subject to agency review, and does not necessarilyreflect the view of the agency; therefore the contents

should be not be considered official endorsements by

the EPA.

References

[1] Oren R, Pataki DE. Transpiration in response to variation in

microclimate and soil moisture in southeastern deciduous forests.

Oecologia 2001;127(4):549–59.

[2] Oosting HJ. An ecological analysis of the plant communities of

the Piedmont, North Carolina. Am Midland Naturalist 1942;

28:1–126.

[3] Christensen NL. Changes in structure, pattern and diversity

associated with climax forest maturation in Piedmont, North

Carolina. Am Midland Naturalist 1977;97:176–88.

[4] Peet RK, Christensen NL. Succession: a population process.

Vegetatio 1980;43:131–40.

[5] Burns RM, Honkala BH. Silvics of North America. Agricultural

Handbook 654, vol. 2. Washington, DC: USDA Forest Service;

1990.

1278 D.E. Pataki, R. Oren / Advances in Water Resources 26 (2003) 1267–1278

[6] Ni B, Pallardy SG. Response of gas exchange to water stress in

seedlings of woody angiosperms. Tree Physiol 1991;8:1–9.

[7] Parker WC et al. Seasonal changes in tissue water relations of

three woody species of the Quercus-Carya forest type. Ecology

1982;63:1259–67.

[8] Pezeshki SR, Chambers JL. Stomatal and photosynthetic re-

sponse of drought-stressed cherrybark oak (Quercus falcata var.

pagodaefolia) and sweetgum (Liquidambar styraciflua). Can J

Forest Res 1986;16:841–6.

[9] Roberts SW, Knoerr KR, Strain BR. Comparative field water

relations of four co-occurring forest tree species. Can J Botany

1979;57:1876–82.

[10] Tobiessen PL, Kana TM. Drought stress avoidance in three

pioneer tree species. Ecology 1974;55:667–70.

[11] Davies WJ, Kozlowski TT. Variations among woody plants in

stomatal conductance and photosynthesis during and after

drought. Plant Soil 1977;46:435–44.

[12] Wullschleger SD et al. Sensitivity of stomatal and canopy

conductance to elevated CO2 concentration––interacting variables

and perspectives of scale. New Phytol 2002;153:485–96.

[13] Granier A. Evaluation of transpiration in a Douglas-fir stand by

means of sap flow measurements. Tree Physiol 1987;3:309–20.

[14] Pataki DE, Oren R, Phillips N. Responses of sap flux and

stomatal conductance of Pinus taeda L. trees to stepwise reduc-

tions in leaf area. J Exp Botany 1998;49(322):871–8.

[15] Whitehead D, Jarvis PG. Coniferous forests and plantations. In:

Kozlowski TT, editor. Water deficits and plant growth. New

York: Academic Press; 1981. p. 49–152.

[16] Phillips N et al. Time constant for water transport in loblolly pine

trees estimated from time series of evaporative demand and stem

sapflow. Trees 1997;11:412–9.

[17] Pataki DE et al. Canopy conductance of Pinus taeda, Liquidambar

styraciflua and Quercus phellos under varying atmospheric and soil

water conditions. Tree Physiol 1998;18:307–15.

[18] Phillips N, Oren R, Zimmerman R. Radial patterns of xylem sap

flow in non-, diffuse- and ring-porous tree species. Plant, Cell

Environ 1996;19:983–90.

[19] Oren R et al. Sensitivity of mean canopy stomatal conductance to

vapor pressure deficit in a flooded Taxodium distichum L. forest:

hydraulic and non-hydraulic effects. Oecologia 2001;126:21–9.

[20] Phillips N, Oren R. A comparison of two daily representations of

canopy conductance based on two conditional time-averaging

methods and the dependence of daily conductance on environ-

mental factors. Annales des Sciences Forestieres 1998;55:217–35.

[21] Jarvis PG. The interpretation of the variations in leaf water

potential and stomatal conductance found in canopies in the field.

Phil Trans Roy Soc Lond B 1976;273(927):593–610.

[22] Granier A, Br�eeda N. Modeling canopy conductance and stand

transpiration of an oak forest from sap flow measurements.

Annales des Sciences Forestieres 1996;53:537–46.

[23] Oren R et al. Survey and synthesis of intra- and interspecific

variation in stomatal sensitivity to vapour pressure deficit. Plant,

Cell Environ 1999;22:1515–26.

[24] Ewers BE, Oren R. Analyses of assumptions and erros in the

calculation of stomatal conductance from sap flux measurements.

Tree Physiol 2000;20:579–89.

[25] Bahari ZA, Pallardy SG, Parker WC. Photosynthesis, water

relations, and drought adaptation in six woody species of oak-

hickory forests in central Missouri. Forest Sci 1985;31:557–69.

[26] Hinckley TM et al. Leaf conductance and photosynthesis in four

species of the oak-hickory forest type. Forest Sci 1978;1:73–84.

[27] Abrams MD, Mostoller SA. Gas exchange, leaf structure and

nitrogen in contrasting successional tree species growing in open

and understory sites during a drought. Tree Physiol 1995;15:

361–70.

[28] Luxmoore RJ et al. Some measured and simulated plant water

relations of yellow-poplar. Forest Sci 1978;24:327–41.

[29] Ryan MG, Yoder BJ. Hydraulic limits to tree height and tree

growth. Bioscience 1997;47(4):235–42.

[30] Sch€aaffer KVR, Oren R, Tenhunen J. The effect of tree height on

crown-level stomatal conductance. Plant, Cell Environ 2000;

23:365–77.

[31] Oren R et al. Sap-flux-scaled transpiration responses to light,

vapor pressure deficit, and leaf area reduction in a flooded

Taxodium distichum forest. Tree Physiol 1999;19:337–47.

[32] Phillips N, Oren R. Intra- and inter-annual variation in transpi-

ration of a pine forest in relation to environmental variability and

canopy development. Ecol Appl 2001;11:385–96.

[33] Roberts J. Forest transpiration: a conservative hydrological

process? J Hydrol 1983;66:133–41.

[34] Sch€aafer KVR et al. Hydrological balance in an intact temperate

forest ecosystem under ambient and elevated atmospheric CO2

concentration. Global Change Biol 2002;8:895–911.

[35] Fowells HA. Silvics of forest trees of the United States. Agricul-

tural Handbook no. 271. Washington, DC: USDA Forest Service;

1965.

[36] Groninger JW et al. Growth and photosynthetic responses of four

Virginia Piedmont tree species to shade. Tree Physiol 1996;16:

773–8.

[37] Cienciala E et al. Assessment of transpiration estimates for Picea

abies during a growing season. Trees 1992;6:121–7.

[38] Oren R et al. Scaling xylem sap flux and soil water balance and

calculating variance: a method for partitioning water flux in

forests. Annales des Sciences Forestieres 1998;55:191–216.

[39] Oren R et al. Water balance delineates the soil layer in which

moisture affects canopy conductance. Ecol Appl 1998;8:990–

1002.

[40] Naumburg E, Ellsworth DS. Photosynthetic sunfleck utilization

potential of understory saplings growing under elevated CO2 in

FACE. Oecologia 2000;122:163–74.

[41] Field CB. Leaf-age effects of stomatal conductance. In: Zeiger

GD, Farquhar GD, Cowan IR, editors. Stomatal function.

Stanford: Stanford University Press; 1987.

[42] Addicott FT, Lyon JL. Physiological ecology of abscission. In:

Kozlowski TT, editor. Shedding of plant parts. New York:

Academic Press; 1973.