Seasonal photosynthetic gas exchange and leaf ... - Tree Physiology

Tree Physiology 28, 1037–1048 

© 2008 Heron Publishing—Victoria, Canada 

Seasonal photosynthetic gas exchange and leaf reflectance 

characteristics of male and female cottonwoods in a riparian woodland 

MATTHEW G. LETTS, 1,2 COLLEEN A. PHELAN, 3 DAVIN R. E. JOHNSON 1 and STEWART 

B. ROOD 3 

1 

Department of Geography, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada 

2 

Corresponding author (matthew.letts@uleth.ca) 

3 

Department of Biological Sciences, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada 

Received September 16, 2007; accepted January 10, 2008; published online May 1, 2008 

Summary Cottonwoods (Populus spp.) are dioecious phreatophytes 

of hydrological and ecological importance in riparian 

woodlands throughout the Northern Hemisphere. In 

streamside zones of southern Alberta, groundwater and soil 

water typically decline between May and September. To understand 

how narrowleaf cottonwoods (Populus angustifolia 

James) are adapted to this seasonal decrease in water availability, 

we measured photosynthetic gas exchange, leaf reflectance, 

chlorophyll fluorescence and stable carbon isotope composition 

(δ 13 C) in trees growing in the Oldman River valley of 

southern Alberta during the 2006 growth season. Accompanying 

the seasonal recession in river flow, groundwater table 

depth (Zgw) declined by 1.6 m, but neither mean daily light-saturated 

net photosynthetic rate (Amax) nor stomatal conductance 

(gs) was correlated with this change. Both Amax and gs followed 

a parabolic seasonal pattern, with July 24 maxima of 15.8 µmol 

m –2 s –1 and 559 mmol m –2 s –1 , respectively. The early summer 

rise in Amax was related to an increase in the chlorophyll pool 

during leaf development. Peak Amax coincided with the maximum 

quantum efficiency of Photosystem II (Fv/Fm), chlorophyll 

index (CI) and scaled photochemical reflectance index 

(sPRI), but occurred one month after maximum volumetric soil 

water (θv) and minimum Zgw. In late summer, Amax decreased by 

30–40% from maximum values, in weak correlation with θv 

(r 2 = 0.50). Groundwater availability limited late-season water 

stress, so that there was little variation in mean daily transpiration 

(E ). Decreasing leaf nitrogen (% dry mass), CI, Fv/Fm and 

normalized difference vegetation index (NDVI) were also consistent 

with leaf aging effects. There was a strong correlation 

between Amax and gs (r 2 = 0.89), so that photosynthetic water-use 

efficiency (WUE; Amax/E) decreased logarithmically 

with increasing vapor pressure deficit in both males (r 2 = 0.75) 

and females (r 2 = 0.95). The male:female ratio was unequal 

(2:1, χ 2 = 16.5, P < 0.001) at the study site, but we found no significant 

between-sex differences in photosynthetic gas exchange, 

leaf reflectance or chlorophyll fluorescence that might 

explain the unequal ratio. Females tended to display lower 

NDVI than males (P = 0.07), but mean WUE did not differ significantly 

between males and females (2.1 ± 0.2 versus 2.5 ± 

0.2 mmol mol –1 ), and δ 13 C remained in the –28.8 to –29.3‰ 

range throughout the growth season, in both sexes. These results 

demonstrate changes in photosynthetic and water-use 

characteristics that collectively enable vigorous growth 

throughout the season, despite seasonal changes in water supply 

and demand. 

Keywords: chlorophyll fluorescence, photochemical reflectance 

index, Populus angustifolia, sexual dimorphism, stable 

carbon isotope. 

Introduction 

Cottonwood trees (Populus spp.) are found in riparian zones 

throughout continental North America and Eurasia (Naiman 

and Décamps 1997, Rood et al. 2003). As obligate phreatophytes, 

they typically obtain more than 80% of the water required 

for growth, development and reproduction from alluvial 

groundwater sources (Gazal et al. 2006). In arid and 

semi-arid regions of western North America, where streamdependent 

groundwater is the only persistent water source, 

cottonwoods are the dominant tree species (Patten 1998). 

They are of great hydrological importance because of the contribution 

of cottonwood transpiration to riparian water flux 

(Goodrich et al. 2000), and they are of great ecological importance 

through the provision of habitat for a variety of plant and 

animal species (Fierke and Kauffman 2006), the resistance of 

bank erosion (Perucca et al. 2007), the interception of nutrients 

and pollutants from surface and groundwater (Patten 

1998, Kelly et al. 2007), and the contribution of photosynthate 

to food-webs of riparian and aquatic ecosystems (Naiman et 

al. 2005). 

Effects of water stress on riparian cottonwoods 

Woody riparian plants are thought to be less physiologically 

adapted to drought than non-phreatophytes in otherwise arid 

environments (Smith et al. 1991, 1998). Cottonwoods exhibit 

high stomatal conductance (gs) and transpiration rates (E)under 

moist conditions (Chen et al. 2006), and low foliar stable 

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1038 LETTS, PHELAN, JOHNSON AND ROOD 

carbon isotope composition (δ 13 C), between –31 and –28‰. 

This suggests that persistent groundwater availability lowers 

photosynthetic water-use efficiency (WUE; Leffler and Evans 

2001). Transpiration is enhanced by the high atmospheric vapor 

pressure deficits (D) in arid regions (Schaeffer et al. 2000, 

Gazal et al. 2006), but the negative effect of high E on soil water 

availability is mitigated by groundwater replenishment 

from the adjacent losing streams. Nevertheless, a variety of 

physiological changes are observed in cottonwoods in response 

to increasing groundwater table depth (Zgw). At the leaf 

scale, the primary physiological response to water deficit is 

stomatal closure, which results in lower E (Smith et al. 1991, 

Braatne et al. 1992, Mahoney and Rood 1992, Loewenstein 

and Pallardy 1998, Amlin and Rood 2002, Cooper et al. 2003), 

lower light-saturated net photosynthetic rate (Amax; Horton et 

al. 2001a, 2001b, 2001c), higher WUE (Amax/E or Amax/gs) and 

a lower ratio between internal and atmospheric CO2 concentrations 

(ci/ca). Lower ci/ca leads to less negative stable carbon 

isotope ratios (δ 13 C) in plant tissues, including leaves 

(Ehleringer 1993). 

Leaf pigment concentration and composition are also influenced 

by plant water status. Water deficit tends to result in 

lower reflectance indices, including the normalized difference 

vegetation index (NDVI), chlorophyll index (CI), water band 

index (WBI) and photochemical reflectance index (PRI; 

Gamon et al. 1990). Chlorophyll fluorescence is also affected 

by plant water status. Dark-adapted values of the optimum 

quantum yield of Photosystem II (Fv/Fm) provide an indicator 

of photosynthetic capacity. Under optimal conditions, Fv/Fm is 

about 0.83 in most species (Björkman and Demmig 1987), but 

water stress and photoinhibition cause Fv/Fm to decrease. Photochemical 

efficiency of Photosystem II (ΦPSII) also responds 

negatively to water stress, with ΦPSII being a measure 

of the proportion of photosynthetic photon flux (PPF) absorbed 

by chlorophyll that is utilized in photochemistry. 

Sexual dimorphism in physiological traits 

Photosynthetic gas exchange characteristics and their response 

to drought often differ between male and female genotypes 

of dioecious plants (Dawson and Bliss 1989, Dawson 

and Ehleringer 1993, Leigh and Nicotra 2003). Females tend 

to exhibit decreased growth rates and survivorship compared 

with males in low resource environments, possibly because of 

higher allocation of resources to reproductive processes (Darwin 

1877, Putwain and Harper 1972, Dawson et al. 1990, 

Gehring and Linhart 1993, Gehring and Monson 1994, 

Braatne et al. 2007, Hultine et al. 2007). Sexual dimorphism in 

physiological responses to water stress varies among species. 

Water stress induces lower female gs in Salix arctica Pall. 

(Dawson and Bliss 1989), Pistacia lentiscus L. (Correia and 

Diaz Barradas 2000) and Populus deltoides Batr. ex Marsh. 

var. wislizenii, the Rio Grande cottonwood (Rowland 2001). 

This response may have evolved because of greater selection 

pressure favoring water conservation during the fruit maturation 

period (Gehring and Monson 1994). However, in other 

species, such as Acer negundo L. var. interior, males respond 

to water stress with lower gs than females (Dawson and 

Ehleringer 1993). Similarly, higher gs results in lower female 

leaf water potential (Ψl)inSalix glauca L. (Dudley and Galen 

2007) and in lower female WUE in Maireana pyramidata 

(Benth.) Paul G. Wilson (Leigh and Nicotra 2003). 

Skewed sex ratios are often observed in cottonwood groves 

of western North America (Gom and Rood 1999, Braatne et al. 

2007). In Rio Grande cottonwood groves of New Mexico, the 

highest male:female ratios are found in the driest riparian environments 

(Rowland and Johnson 2001). In a common garden 

study of the same species, gs varied significantly with reproductive 

status and sex (Rowland 2001). Non-reproductive 

specimens had the highest gs, followed by males and then females, 

but no significant differences were observed in Amax. 

Given the relevance of dioecy to both carbon and water cycling 

in riparian ecosystems (Hultine et al. 2007), it is important to 

categorize dioecious species on the basis of sex when evaluating 

the effects of environmental stress on photosynthetic productivity 

and water-use efficiency. 

We measured photosynthetic gas exchange, leaf reflectance, 

chlorophyll fluorescence and δ 13 C ratio during the growth period 

of 2006, in male and female genotypes of Populus 

angustifolia James, the narrowleaf cottonwood. We tested 

three hypotheses related to plant water use: (1) seasonal 

groundwater and soil water depletion result in higher WUE 

(Amax/gs), lower reflectance indices (PRI, NDVI, CI and WBI) 

and less negative δ 13 C; (2) E, gs and Amax increase in response 

to irrigation of soils with low water content in the vadose zone; 

and (3) females exhibit less negative δ 13 C, lower gs and higher 

WUE than males in response to water stress. 

Materials and methods 

TREE PHYSIOLOGY VOLUME 28, 2008 

Site description 

The study was carried out at Pearce Corner Cottonwood Grove 

(PCCG; 49°51′03″ N, 113°15′18″ W), a 3-ha woodland, east 

of Fort MacLeod, AB, Canada. The PCCG floodplain is located 

on the south side of the Oldman River, along a constrained, 

200–250-m-wide reach. Within the 430 × 70 m 

woodland, located 50 to 120 m inland from the riverbank, 

stand density is 205 stems ha –1 (Willms et al. 2006). Trees in 

the grove rely on groundwater that is largely supplied by the 

Oldman River. Stream flow at PCCG is reduced upstream by 

diversion at the Lethbridge Northern Irrigation District 

(LNID) weir, which was installed in 1925. The Oldman River 

Dam, completed in 1993, traps water from high spring flows 

for release in summer, to restore natural seasonal flow patterns 

(Rood et al. 2005). Mean August and September stream flow 

was reduced from 25.2 to 12.7 m 3 s –1 following construction 

of the LNID weir, but has been restored to a mean of 23.2 m 3 

s –1 since 1993. In addition to cottonwoods, willows (Salix 

spp.), especially the sandbar willow (Salix exigua Nutt.), occur 

at the site, and grow in highest density near the edge of the 

river, where soil water content is higher and flooding is most 

frequent. The cottonwood understory consists of a diverse set 

of tall C3 grasses and herbaceous dicotyledons. Mean annual 



PHOTOSYNTHETIC GAS EXCHANGE IN NARROWLEAF COTTONWOODS 1039 

precipitation is 425 mm, with 61% typically occurring during 

the May to September period covered by this study. Mean annual 

temperature is 5.7 °C at Fort Macleod, with mean 

monthly temperature peaking at 18.0 °C in July (Environment 

Canada 2005). 

Monitoring of environmental conditions 

Environmental variables were measured from day of year 

(DOY) 120 to 270 with a Dynamet weather station 

(Dynamax, Houston, TX) located in a clear area, 60 m to the 

WNW of the trees. Air temperature (Tair) and relative humidity 

(RH) at a height of 1.2 m were measured with a CS500 temperature 

and relative humidity probe (Campbell Scientific, Logan, 

UT). Precipitation was measured with a tipping bucket 

rain gauge (TE525, Campbell Scientific). Volumetric soil water 

(θv) was measured at 0.2-, 0.5- and 0.8-m depths with 

ThetaProbe ML2x sensors and recorded with a THLog-4 data 

logger (Dynamax). A silicon radiation sensor (LI-200SZ, 

Li-Cor, Lincoln, NE) was used to measure solar insolation 

(K ). Measurements were taken at hourly intervals, except for 

θv, which was determined at a 4-h interval. Depth to the saturated 

water table within the cluster of eight study trees was determined 

at two open wells consisting of steel pipes attached to 

stainless steel well points with mesh screens (Model 615N, 

Solinst Canada), driven 3.8 m into the riparian substrate. Water 

table depths were determined at weekly intervals with an electric 

water level meter (Model 101, Solinst Canada). 

Photosynthetic gas exchange measurements 

Eight Populus angustifolia trees, four male and four female, 

were selected for study within a 250 m 2 area of the floodplain 

60 to 80 m inland from the riverbank, to ensure the study trees 

were growing under similar hydrological conditions. The trees 

were selected on the basis of species analysis, apparent health 

and proximity to soil water sensors as well as for similarity in 

depth to water table, age, height and tree architecture. Species 

analysis was performed by measuring leaf blade and petiole 

shape (Rood et al. 1986), to avoid selecting trees strongly hybridized 

with P. balsamifera L. ssp. trichocarpa. Reproductive 

bud flush stage was recorded from DOY 130 to 135, to ensure 

that clones were not chosen as study trees. 

Photosynthetic gas exchange was measured on DOY 136, 

172, 191, 205, 220, 237 and 247 with a portable TPS-1 Photosynthesis 

System equipped with a 25 × 18 mm PLC6 automatic 

universal leaf cuvette (PP Systems, Amesbury, MA), 

calibrated by the manufacturer in April 2006. Gas exchange 

characteristics were determined in full sun (photosynthetic 

photon flux exceeding 1000 µmol m –2 s –1 ) on three sun-exposed 

leaves of the lower canopy (2–5 m above ground) of 

each tree, between 1100 and 1600 h. The three leaves chosen 

from each tree were each from a branch of different aspect (N, 

SE or SW). Ten gas exchange measurements were made to obtain 

a mean value for each leaf, and the three leaf values were 

averaged to obtain the mean for each tree. For each measurement 

date, mean values for each sex were derived from the 

four tree means. The mean (± standard error) chamber CO2 

concentration for the ten measurement dates was 386.7 ± 

1.8 ppm, with no seasonal trend. Time of day effects were minimized 

by switching between male and female trees at least 

once for every six leaves sampled. Cloudiness occasionally reduced 

the number of leaves sampled on certain trees, and the 

number of trees was reduced from 8 to 4 on DOY 237, because 

measurements were taken on both green and precociously senescent 

leaves. For the seven measurement dates, the total 

numbers of male and female leaves (measurements) were 

75 (801) and 68 (712), respectively. Following leaf collection, 

leaf area was determined with a Li-Cor LI-3100C leaf area 

meter. Leaves were then dried for 48 h at 70 °C and weighed. 

Specific leaf area (SLA) was calculated by dividing projected 

leaf area by leaf dry mass. 

Leaf reflectance 

Adaxial leaf reflectance was measured on three leaves (SW, 

SE and N aspect) of each study tree on six dates (DOY 172, 

191, 205, 220, 237 and 247), with a field spectroradiometer 

(Unispec-SC Spectral Analysis System, PP Systems), 

equipped with a bifurcated fiber optic cable (UNI400) and leaf 

clip (UNI500). The spectral range was 400 to 1000 nm and the 

resolution was 10 nm. To account for instrument noise effects, 

dark scans preceded all measurements. Leaf reflectance was 

calculated by dividing leaf radiance by the irradiance of a 

99%-reflective polytetrafluoroethylene (PTFE) calibration 

disk (UNI420). Reflectance from this disk was measured before 

each measurement, as a white reference. The mean of ten 

scans was used to obtain the spectral response curve for each 

leaf. Based on 1-nm bandwidths interpolated from the 

spectroradiometer data, PRI (Gamon et al. 1997), NDVI 

(Tucker 1979), CI (Gitelson and Merzlyak 1994) and WBI 

(Peñuelas et al. 1997) were determined as: 

R − R 

PRI = 

R + R 

531 570 

531 570 

R − R 

NDVI = 

R + R 

R − R 

CI = 

R + R 

WBI = R 

R 

800 670 

800 670 

750 705 

750 705 

900 

970 

where R is reflectance and subscripts refer to wavelengths in 

nm. To avoid negative values of PRI, we report the scaled 

value of PRI (sPRI): 

PRI +1 

sPRI = 

2 

TREE PHYSIOLOGY ONLINE at http://heronpublishing.com 

Chlorophyll fluorescence 

On DOY 172, 191, 205, 220 and 237, chlorophyll fluorescence 

(1) 

(2) 

(3) 

(4) 

(5) 




measurements (Fv/Fm and ΦPSII) were made on the same 

leaves sampled for leaf reflectance, with an FMS2 pulse modulated 

chlorophyll fluorimeter (Hansatech Instruments, U.K.). 

Before Fv/Fm was determined, all leaves were dark adapted for 

a minimum of 30 min, using the leaf clip. About 30 s after 

measuring Fv/Fm, ΦPSII was determined on the same leaf tissue 

in full natural sunlight, rather than with the actinic light 

source. 

Stable carbon isotope composition 

A selection of dried leaves gathered on DOY 172, 205 and 237 

were chosen for N and δ 13 C analyses. Individual leaf samples 

were immersed in liquid nitrogen and crushed with a mortar 

and pestle. To determine stable carbon isotope composition 

and total N concentration (%), tissue samples (about 5 mg) 

were weighed into tin cups, and combusted in an elemental analyzer 

(NC2100, CE Instruments, ThermoQuest Italia, Milan, 

Italy), coupled to a gas isotope ratio mass spectrometer (Optima,VG 

Isotech, Cheshire, U.K.) operating in continuous 

flow mode. The δ 13 C was determined from the ratio, R 

( 13 CO2/ 12 CO2): 

δ 13 

C(‰) = ⎛ R 

⎜ 

⎝ R 

sample 

std 

⎞ 

⎟ 1000 

⎠ 

where Rstd refers to the molar ratio of the international Pee Dee 

Belemnite standard. 

Photosynthetic water-use efficiency 

Photosynthetic water-use efficiency was calculated from both 

gas exchange measurements and from the δ 13 C composition of 

plant tissue. The former is an instantaneous measure of WUE, 

and was determined as: 

⎛ ci 

⎞ 

ca 

⎜1 

− ⎟ 

A ⎝ ca 

⎠ 

WUE = = 

E 16 . v 

where 1.6 is the ratio of the diffusion coefficients of H2O and 

CO2 and v is related to the difference between intracellular and 

atmospheric H2O vapor concentrations (ei – ea; kPa) and atmospheric 

pressure, P (kPa) as: 

e − e 

v = 

P 

i a 

The stable carbon isotope composition of leaf tissue, δ 13 Cp, 

can be used to determine an integrated measure of WUE. The 

stable carbon isotope composition of leaf material is related to 

that of the source atmospheric CO2 (δ 13 Ca) and to ci/ca 

(Farquhar et al. 1982, 1989): 

(6) 

(7) 

(8) 

13 13 

δ C δ C a b a ci 

p = a − −( − ) (9) 

c 

a 

where δ 13 Ca is assumed to be –8‰, a is the discrimination during 

diffusion of CO2 in air (4.4‰), b is net discrimination during 

carboxylation (27.0‰) and ca is 380 µmol mol –1 , the mean 

CO2 concentration in July 2006 at Mauna Loa, Hawaii (Tans 

2007). We derived WUE from Equations 7 and 9 as (Ponton et 

al. 2006): 

13 13 ⎛ δ Cp − δ Ca + a⎞ 

ca − ca⎜ 

⎟ 

A ⎝ a − b ⎠ 

WUE = = 

E 

16 . v 

(10) 

Irrigation treatment 

To examine the effect of soil water availability on photosynthetic 

gas exchange characteristics of male and female cottonwoods, 

45,000 l of water was pumped from the Oldman 

River to the base of two female and two male trees on DOY 

241. When irrigation was complete, the four trees were surrounded 

by standing water extending at least 4 m from the base 

of the trunk. On DOY 247, photosynthetic gas exchange and 

leaf reflectance measurements were taken on three leaves of 

each of the four irrigated and four non-irrigated trees. 

Statistical analysis of physiological data 

Between-sex differences in leaf photosynthetic gas exchange, 

reflectance and fluorescence characteristics were assessed by 

mixed model repeated measures analysis of variance 

(ANOVA), with DOY as the repeated measure, sex as a fixed 

effect, tree identity as a random effect, sex × DOY interaction 

and post hoc evaluation by Tukey’s HSD test. Repeated measures 

ANOVA was also used to assess seasonal differences in 

photosynthetic gas exchange, foliar δ 13 C composition and Ψl 

(Phelan 2007). One-tailed Student’s t-tests were used to test 

two hypotheses: (1) females have significantly more conservative 

water use indicators than males, based on stable carbon 

isotope composition (higher δ 13 C and WUE, but lower ci/ca); 

and (2) irrigated trees have higher gas exchange rates and 

lower WUE (Amax/E and Amax/gs) than non-irrigated trees. 

Results 

Environmental conditions 


Total precipitation at PCCG was 178.8 mm during DOY 121– 

247 (Table 1), with 76% occurring between DOY 146 and 171, 

and 48% occurring in a single event on DOY 165–166. Thereafter, 

rainfall was light, with all daily rainfall totals below 

8 mm. In response to this rainfall pattern and variation in water 

table depth, θv at 0.8-m depth was high in late June and early 

July, but decreased continuously from a peak of 0.40 m 3 m –3 

on DOY 170 through the months of July and August. Groundwater 

depth fell from –0.73 to –2.34 m from DOY 170 to 247. 

Total rainfall at PCCG was 23.5% below the 30-year mean for 

Fort Macleod during the study period (Table 1; Environment 

Canada 2005). 

Daily maximum air temperature and vapor pressure deficit 

were higher in July, August and early September than in May 



and June (Table 1). Mean Tmax was 25.1 °C at PCCG, which is 

3.1 °C higher than the 30-year mean at Fort Macleod. Elevated 

temperature may, in part, be caused by the sheltered microclimate 

of the cottonwood grove and the Oldman River valley, 

but Tmax was also above average regionally. At Lethbridge Airport, 

55 km to the southeast, Tmax was 1.6 °C higher than the 

1971–2000 mean from May to August 2006 (Environment 

Canada 2005). 

Structural traits of P. angustifolia trees at PCCG 

Mean age of the study trees was 36.3 ± 1.7 years. Mean tree 

height and trunk diameter at breast height (DBH) were 11.1 ± 

0.7 m and 24.8 ± 1.5 cm, respectively. No gross structural differences 

were observed between the male and female cottonwoods 

sampled (Table 2), but the sex structure of cottonwoods 

at PCCG was imbalanced, with a male:female ratio of 2:1 that 

was significantly different from the expected 1:1 ratio (n = 

140, χ 2 = 16.5, P < 0.001). Specific leaf area (SLA) decreased 

from 141.2 ± 3.9 cm 2 g –1 on DOY 136 to 95.61 ± 3.2 cm 2 g –1 

on DOY 205. Thereafter, in fully developed leaves, SLA decreased 

more slowly, reaching 79.7 ± 3.0 cm 2 g –1 by DOY 247. 

Seasonal patterns of photosynthetic gas exchange 

characteristics 


Table 1. Mean daily maximum air temperature (Tmax), maximum vapor pressure deficit (Dmax), maximum irradiance (K↓max), soil water at a depth 

of 0.8 m (θv), groundwater table depth (Zgw) and total precipitation at the Pearce Corner Cottonwood Grove, during and preceding the study period 

(day of year (DOY) 121–247). Values of Tmax, Dmax and K↓max were calculated from peak hourly values for each day. Errors shown are standard 

deviations. Abbreviation: ND = no data. 

Month (DOY) Tmax (°C) Dmax (kPa) K↓max(W m –2 ) θv (m 3 m –3 ) Zgw (cm) Precipitation (mm) 

May (121–151) 21.1 ± 7.0 2.0 ± 1.1 810 ± 154 ND –121.5 25.4 

June (152–181) 23.3 ± 4.5 1.8 ± 0.9 783 ± 233 0.24 –108.9 113.8 

July (182–212) 30.2 ± 3.1 3.0 ± 0.8 864 ± 102 0.22 –203.1 4.3 

August (213–243) 28.5 ± 3.8 3.0 ± 0.9 770 ± 109 0.15 –228.1 35.3 

September (244–247) 26.6 ± 6.9 2.9 ± 1.4 765 ± 26 0.12 –233.1 0.0 

Mean daily light-saturated photosynthetic rate increased during 

the late spring and early summer to a maximum near 

15.8 µmol m –2 s –1 on DOY 205 (Figure 1). For the remainder 

of the season, mean Amax ranged from 10.0 to 10.3 µmol m –2 

s –1 . With data from males and females pooled, Amax exhibited a 

Table 2. Characteristics of the trees and leaves studied, including age, 

height, diameter at breast height (DBH), peak season specific leaf 

area (SLA; day of year (DOY) 205) and area-based leaf nitrogen content 

(DOY 205). Errors shown are standard errors. Sample sizes are 

shown in parentheses. 

Characteristic Male Female 

Tree age (year) 38.0 ± 2.1 (4) 34.5 ± 4.2 (4) 

Plant height (m) 10.7 ± 1.4 (4) 11.5 ± 1.4 (4) 

DBH (cm) 23.7 ± 1.3 (4) 25.9 ± 4.1 (4) 

SLA (cm 2 g –1 ) 82.9 ± 1.6 (18) 90.0 ± 2.7 (18) 

Leaf N (g m –2 ) 2.40 ± 0.11 (10) 2.35 ± 0.10 (10) 


positive correlation with mean daily gs (logarithmic, 

r 2 = 0.89). Stomatal conductance reached a peak of 559 mmol 

m –2 s –1 on DOY 205, but fell to 246 mmol m –2 s –1 by DOY 

237. As θv declined, stomatal closure caused only a slight decrease 

in ci/ca, from a maximum of 0.79 at peak season to a 

minimum of 0.73 by DOY 237. Mean daily E remained within 

the 5.0 to 6.1 mmol m –2 s –1 range, except on DOY 237, when it 

fell to 3.3 mmol m –2 s –1 . This was the only date characterized 

by both low θv and low D. Water-use efficiency (Amax/E) 

ranged from 1.6 to 3.7 mmol mol –1 in response to variable atmospheric 

conditions, whereas WUE (Amax/gs) ranged from 

0.32 to 0.46 mmol mol –1 , with the lowest values occurring 

near mid-season (DOY 172–205). 

All photosynthetic gas exchange variables showed significant 

variation with DOY (P < 0.001), but no clear seasonal 

trend was observed in foliar δ 13 C composition, which ranged 

from –29.3 to –28.8‰ between DOY 172 and 237 (P = 0.93; 

Table 3). Using δ 13 C and D to determine ci/ca, no significant 

seasonal variation was observed, with values ranging from 

0.75 to 0.78. Values of WUE (A/E from δ 13 C) varied from 

2.1 to 2.8 mmol mol –1 , with significantly lower values observed 

on DOY 205 (P = 0.001; Table 3), because of a combi- 

Table 3. Water-use indicators of leaves of male and female narrowleaf 

cottonwoods at PCCG. The ratio of internal to atmospheric CO2 concentrations 

(ci/ca) and water-use efficiency (WUE; mmol CO2 mol –1 

H2O) were calculated from Equations 9 and 10. The total numbers of 

trees (leaves) analyzed for stable carbon isotope ratio (δ 13 C, ‰) were 

6(15), 8(20) and 4(12) on day of the year (DOY) 172, 205 and 237, 

respectively. Mean values shown were calculated as the average of 

tree means. Abbreviation: SE = standard error. 

DOY Water-use Mean ± SE t P 

indicator 

Male Female 

172 δ 13 C –28.91 ± 0.74 –28.96 ± 0.54 0.05 0.48 

ci/ca 0.76 ± 0.03 0.76 ± 0.03 0.05 0.48 

WUE 2.60 ± 0.32 2.70 ± 0.24 0.23 0.41 

205 δ 13 C –29.17 ± 0.28 –28.97 ± 0.21 0.58 0.29 

ci/ca 0.77 ± 0.01 0.75 ± 0.01 0.58 0.29 

WUE 2.17 ± 0.10 2.36 ± 0.08 0.84 0.22 

237 δ 13 C –29.09 ± 0.48 –29.33 ± 0.10 – – 

ci/ca 0.77 ± 0.02 0.78 ± 0.00 – – 

WUE 2.64 ± 0.22 2.74 ± 0.05 – – 




nation of higher D and slightly more negative δ 13 C. No significant 

differences were found between males and females in 

δ 13 C, ci/ca or WUE (Table 3). 

Mean daily Amax and gs were both positively correlated with 

θv, but negatively correlated with D (Figure 2). The relationship 

between gs and D was much stronger with the DOY 237 

data removed (r 2 = 0.81). The Zgw was poorly correlated with 

Amax (r 2 = 0.00), gs (r 2 = 0.03) and E (r 2 = 0.00; not shown). 

Transpiration rate was poorly correlated with θv (r 2 = 0.08) and 

D (r 2 = 0.09). Because of the strong relationship between Amax 

and gs, and the relative invariability of E, mean daily WUE 

(Amax/E) was negatively and logarithmically correlated with D 

(Figure 2), but poorly correlated with θv (linear, r 2 = 0.12). By 

contrast, WUE (Amax/gs) was correlated with θv (Figure 2), but 

not with D (r 2 = 0.14). 

Chlorophyll fluorescence and leaf reflectance 

Mean Fv/Fm followed a parabolic seasonal pattern, with a 

maximum of 0.85 on DOY 191 and 205 (Figure 3). Mean 


Figure 1. Photosynthetic gas exchange characteristics 

as a function of day of year (DOY) in 

leaves of male (�) and female (�) narrowleaf 

cottonwoods. Error bars denote the standard 

error of the mean. Definitions: Tleaf, leaf temperature; 

Amax, light-saturated net photosynthetic 

rate; Amax/gs and Amax/E, water-use 

efficiencies; gs, stomatal conductance; D, vapor 

pressure deficit; ci/ca, ratio between internal 

and atmospheric CO2 concentrations. 

ΦPSII peaked near 0.66 on DOY 191, and then decreased to 

0.30 by DOY 237. The NDVI exhibited a slight downward 

trend with DOY (Figure 3) in both males (r 2 = 0.63) and females 

(r 2 = 0.89), with mean daily NDVI falling from 0.874 on 

DOY 172 to 0.849 by DOY 237. The decline in NDVI was coincident 

with decreases in leaf N concentration, which fell 

from 2.20 ± 0.19% to 1.68 ± 0.19% on a mass basis and from 

2.20 ± 0.18 g m –2 to 2.13 ± 0.25 g m –2 on an area basis from 

DOY 172 to 237. Both CI and sPRI decreased after reaching 

maxima on DOY 191 and 205, respectively. The late-summer 

decrease in CI was proportionally larger than the decrease in 

NDVI. 

When photosynthesis and reflectance measurements were 

taken on the same leaf tissue (DOY 237), CI was weakly correlated 

with Amax (Figure 4). Net light-saturated photosynthetic 

rates increased exponentially with sPRI, and the correlation 

was similar in males (r 2 = 0.54) and females (r 2 = 0.48). Values 

of Amax were highly variable for NDVI above 0.79, but were 

near zero below this threshold. 




Response of water-stressed cottonwoods to irrigation 

On DOY 247, six days after irrigation of four of the eight cottonwoods, 

Amax, gs, E and ci/ca did not differ significantly between 

the irrigated and non-irrigated trees (P > 0.10; Table 4). 

However, large increases in gs and E were observed in individual 

trees, and these increases were consistent with higher sap 

flow rates following the irrigation treatment (Phelan 2007). 

Water-use efficiency measures (Amax/E and Amax/gs) were not 

significantly affected by the irrigation treatment. The irrigation 

treatment had no significant effects on the leaf reflectance 

indices NDVI, CI, sPRI and WBI (Table 4). 

Water-use efficiency of male and female cottonwoods 

With the exception of NDVI, which was lower in females than 

in males (Table 5), no significant differences were observed 

between the photosynthetic gas exchange, leaf reflectance, 

chlorophyll fluorescence or stable carbon isotope characteristics 

of male and female cottonwoods. No interaction was observed 

between sex and DOY, with the exception of sPRI, 

which reached a higher mid-season peak in males than in females. 

Discussion 


Figure 2. Effects of volumetric soil water 

content (θv) and vapor pressure deficit (D) 

on light-saturated net photosynthetic rate 

(Amax), stomatal conductance (gs) and water-use 

efficiencies (Amax/gs and Amax/E) in 

male (�) and female (�) narrowleaf cottonwoods. 

Values are daily means for all 

dates for which both photosynthetic gas 

exchange and θv at 0.8-m depth were 

available. 

Controls on photosynthetic gas exchange in cottonwoods 

Net photosynthetic rates of male and female cottonwoods followed 

a parabolic seasonal pattern, with strongly positive Amax 

values (above 10 µmol m –2 s –1 ) maintained throughout the late 

summer drought (Figure 1). During spring, increasing Amax 

was the result of a gradual increase in photosynthetic capacity. 

The rapid decline in SLA indicates that leaves thickened considerably 

during leaf expansion and development, and the increase 

in CI shows that the chlorophyll pool reached a maximum 

near DOY 191–205. Peak values of Fv/Fm, ΦPSII, sPRI 

and WBI also occurred at this time (Figure 3), indicating that 

leaves were not experiencing water stress, despite a substantial 

drop in θv from its peak near DOY 170. These results are consistent 

with those of Noormets et al. (2001), who reported substantial 

increases in the Rubisco content of Populus 

tremuloides Michx. (trembling aspen) leaves during leaf development 

and of Niinemets et al. (2004), who reported rapid 

increases in the capacity for photosynthetic electron transport 

(Jmax) during the first 30 days following bud burst in 




Populus tremula L. Following a period of high productivity in 

July, Amax fell by 30–40%, in a tight, logarithmic relationship 

with gs. Although Amax was unrelated to Zgw, it was weakly correlated 

with θv (r 2 = 0.50; Figure 2). 


Figure 3. Chlorophyll fluorescence and leaf 

reflectance characteristics as a function of day 

of year (DOY) in leaves of male (�) and female 

(�) narrowleaf cottonwoods. Abbreviations: 

quantum yield of Photosystem II, Fv/Fm; 

photochemical efficiency, ΦPSII; scaled value 

of the photochemical reflectance index, sPRI; 

water band index, WBI; chlorophyll index, CI; 

and normalized difference vegetation index, 

NDVI. 

Several observations suggest that only moderate drought 

occurred in 2006. First, Amax and E remained strongly positive 

throughout the late-summer drought with only a slight reduction 

in ci/ca in August. Second, Phelan (2007) observed only 

Table 4. Results of a one-tailed t-test (df = 6), comparing mean light-saturated photosynthetic gas exchange and leaf reflectance characteristics of 

four non-irrigated (2 male and 2 female) and four irrigated (2 male and 2 female) narrowleaf cottonwood trees, on day of year (DOY) 247. The 

mean value for each tree was derived from measurements of three green leaves. Standard errors are shown. Abbreviations: light-saturated 

photosynthetic rate, Amax; stomatal conductance, gs; transpiration, E; internal/atmospheric CO2 concentration ratio, ci/ca; water use efficiency, 

WUE; normalized difference vegetation index, NDVI; chlorophyll index, CI; scaled value of photochemical reflectance index, sPRI; and water 

band index, WBI. 

Variable Non-irrigated Irrigated F Ratio t p 

10.0 ± 0.9 10.8 ± 2.0 5.51 0.34 0.37 

242 ± 40 366 ± 112 7.70 1.04 0.17 

E, mmol m –2 s –1 

5.9 ± 0.6 6.8 ± 1.0 2.49 0.77 0.24 

ci/ca 0.73 ± 0.02 0.77 ± 0.03 1.92 1.08 0.16 

WUE (Amax/E), mmol mol –1 

1.7 ± 0.1 1.6 ± 0.2 2.94 –0.58 0.29 

WUE (Amax/gs), mmol mol –1 

0.045 ± 0.005 0.037 ± 0.007 2.33 –0.91 0.20 

NDVI 0.849 ± 0.015 0.859 ± 0.008 0.29 0.58 0.29 

CI 0.430 ± 0.023 0.439 ± 0.037 2.43 0.21 0.42 

sPRI 0.483 ± 0.008 0.481 ± 0.007 0.78 –0.18 0.43 

WBI 1.017 ± 0.003 1.018 ± 0.006 3.31 0.09 0.46 

Amax, µmol m –2 s –1 

gs, mmol m –2 s –1 




small seasonal reductions in predawn leaf water potential (Ψl) 

during the 2006 field season. In the six study trees for which 

measurements were obtained in all months, predawn Ψl decreased 

significantly from –0.21 MPa in June to –0.33 MPa in 

July and –0.43 MPa in August (P < 0.0001). However, mean 

daily minimum Ψl did not decrease seasonally in the study 

trees, with mean values of –1.94, –2.03 and –2.01 MPa in June, 

July and August, respectively (P = 0.09). Roots of cottonwood 

trees often extend well below 3 m (Williams and Cooper 

2005), so it is likely that the cottonwoods had continuous access 

to the capillary fringe, the zone above the saturated water 

table that is recharged with water from the adjacent river (Scott 

et al. 1999, Horton et al. 2001c). This could also explain the 

modest response to irrigation on DOY 247, when θv was low at 

0.8-m depth. Relatively constant E was observed, despite large 

variations in leaf temperature (Tleaf) and D. Thus, it is evident 

that regulation of gs occurred not only in response to water 

availability, but also in response to atmospheric demand (Figure 

2), as would be expected in plants experiencing little water 

stress. Finally, δ 13 C, an integrator of plant water stress, was indicative 

of low WUE (Table 3) and values did not become less 

negative as the drought progressed (Table 3). 

The weak relationships between θv and water use indicators 

do not preclude the possibility that soil water availability had 

longer term effects on photosynthetic capacity during the dry 

period, thereby explaining part of the reduction in Amax. Leaf N 

(%), NDVI and CI each decreased in association with θv, but 

leaf N and chlorophyll concentrations have been shown to decrease 

with leaf age in Populus spp, even in the absence of severe 

drought (Niinemets et al. 2004). The lack of evidence of 

severe water stress also indicates that the late-season decline in 

sPRI is most likely attributable to a seasonal increase in the ratio 

of the xanthophyll to chlorophyll pool size in mature 

leaves. Values of Fv/Fm and ΦPSII decreased substantially 

(Figure 3), indicating that photochemical capacity decreased 

as a result of leaf N depletion, and possibly soil drying (Figure 

3). The small but considerable late-season decrease in Amax 

was likely the result of synergistic interaction between leaf aging 

effects and soil water depletion, with additional variability 

caused by changing atmospheric demand. Similar processes 

have been observed at the canopy scale in both temperate deciduous 

forests (Wilson et al. 2000) and boreal forests dominated 

by P. tremuloides (Barr et al. 2007). 

Water-use efficiency of riparian cottonwoods at Pearce 

Corner 

Cottonwood leaves exhibited strongly negative δ 13 C, near 

–29‰, and low WUE (Amax/E), ranging from 1.6 to 3.7 mmol 

mol –1 . This is within or below the 1.8–5.0 mmol mol –1 range 

previously observed in Populus spp. (Chen et al. 2006, Liu et 

al. 2006). The lack of a clear seasonal trend in WUE (Amax/E), 

as soil water decreased, can be attributed to reliable groundwater 

availability. During a drought in July and August, WUE 

(Amax/E) maintained its strong negative correlation with D 

(Figure 2). In the absence of severe water stress, isohydric water 

use was observed, with gs regulated in response to D, so that 

E was maintained within a narrow range, with little effect on 

midday leaf water potential. 


Figure 4. Light-saturated net photosynthesis rate (Amax) as a function 

of leaf reflectance indices in leaves of male (�) and female (�) 

narrowleaf cottonwoods on day of year 237. Abbreviations: scaled 

value of the photochemical reflectance index (sPRI); normalized difference 

vegetation index (NDVI); and chlorophyll index (CI). 

Relationship between vegetation indices and cottonwood 

photosynthesis 

By late summer (DOY 237), individual leaves began to 

senesce, but most remained green. Precocious senescence and 




Table 5. Summary of repeated measures analysis of variance (tree identification as random effect) on photosynthetic gas exchange, leaf reflectance 

and chlorophyll fluorescence variables, for day of the year (DOY) 144–247, including (1) between-sex differences and (2) sex × DOY interaction. 

Abbreviations: least squares mean, LSM; standard error, SE; specific leaf area, SLA; light-saturated photosynthetic rate, Amax; photochemical efficiency 

of Photosystem II, ΦPSII; quantum yield of Photosystem II, Fv/Fm; stable carbon isotope ratio, δ 13 C; stomatal conductance, gs; transpiration, 

E; internal/atmospheric CO2 concentration ratio, ci/ca; water-use efficiency, WUE; scaled value of the photochemical reflectance index, 

sPRI; water band index, WBI; chlorophyll index, CI; and normalized difference vegetation index, NDVI. Significant differences at P = 0.10 are 

denoted by an asterisk (*). 

Variable Between-sex differences Sex × DOY interaction 

branch sacrifice are drought indicators in cottonwoods, and 

may alleviate water stress by reducing whole-plant leaf area 

(Rood et al. 2000). Certain leaf reflectance indices, measured 

in both green and yellowing leaves, were correlated with Amax. 

The greenness indices, CI and NDVI, differed in their relationship 

with Amax. Whereas CI was positively and exponentially 

related to Amax, NDVI served to provide a threshold of 0.79, below 

which net photosynthetic activity was near zero on DOY 

237. The sPRI, which decreases with increasing water stress or 

with increases in the ratio of the xanthophyll to chlorophyll 

pigment pools (Gamon et al. 1997, Stylinski et al. 2002, 

Thenot et al. 2002), was exponentially related to Amax. 

Sex-based differences in cottonwood water-use efficiency 

The lack of significant differences between male and female 

WUE (P > 0.05) is not consistent with the hypothesis that female 

cottonwoods experience greater stress in response to soil 

water deficit. The failure to detect significantly higher WUE in 

females than in males may be related to (1) the timing of soil 

drying in southern Alberta, (2) high among-leaf variability in 

photosynthetic gas exchange characteristics, (3) low reproductive 

costs in cottonwoods, or (4) the absence of severe drought 

during the 2006 field campaign. Sexual dimorphism of physiological 

traits in dioecious plants occurs primarily during periods 

of drought (Dawson and Ehleringer 1993) and fruit maturation 

(Gehring and Monson 1994). Soil water availability 

usually peaks during the fruit maturation season of May and 

June in Alberta, which limits the impact of reproduction on 

plant water status. This contrasts with cottonwood groves of 

Male (LSM and SE) Female (LSM and SE) F ratio P df F ratio P 

SLA, cm 2 g –1 

94.2 ± 2.2 96.7 ± 2.0 0.72 0.42 6 0.73 0.62 

Leaf N, g m –2 

2.08 ± 0.2 2.26 ± 0.2 0.62 0.46 2 0.43 0.65 

Amax, µmol m –2 s –1 

11.1 ± 0.7 11.5 ± 0.6 0.20 0.66 6 1.33 0.25 

Amax nmol g s –1 

102 ± 5 107 ± 5 0.69 0.43 6 1.73 0.12 

PSII 0.452 ± 0.033 0.461 ± 0.032 0.04 0.84 4 1.73 0.15 

Fv/Fm 0.816 ± 0.009 0.814 ± 0.009 0.04 0.83 4 0.37 0.83 

δ 13 C, ‰ –29.33 ± 0.35 –29.08 ± 0.31 0.27 0.62 2 0.74 0.49 

gs, mmol m –2 s –1 

346 ± 43 336 ± 40 0.03 0.86 6 0.46 0.84 

E, mmol m –2 s –1 

5.5 ± 0.4 5.0 ± 0.3 0.81 0.40 6 0.37 0.89 

ci/ca 0.765 ± 0.010 0.752 ± 0.010 0.87 0.38 6 0.78 0.59 

ci/ca from δ 13 C 0.778 ± 0.016 0.766 ± 0.015 0.27 0.62 2 0.74 0.49 

WUE (Amax/gs), mmol mol –1 

0.039 ± 0.002 0.042 ± 0.002 0.80 0.40 6 0.54 0.78 

WUE (Amax/E), mmol mol –1 

2.07 ± 0.19 2.47 ± 0.18 2.39 0.16 6 1.51 0.18 

WUE (A/E; from δ 13 C) 2.36 ± 0.15 2.57 ± 0.13 1.12 0.33 2 1.51 0.23 

sPRI 0.496 ± 0.002 0.495 ± 0.002 0.20 0.66 5 2.03 0.08 * 

WBI 1.029 ± 0.002 1.026 ± 0.002 0.77 0.41 5 1.43 0.22 

CI 0.471 ± 0.011 0.461 ± 0.011 0.38 0.56 5 1.69 0.14 

NDVI 0.871 ± 0.006 0.852 ± 0.006 4.82 0.07 * 

5 2.21 0.06 * 


southwestern USA, where drought often occurs before the August 

monsoon season (Gazal et al. 2006). Reproductive costs 

may also be low in relation to total biomass, because of the 

small size of cottonwood fruit and the limited food and water 

reserves in seeds. Photosynthetic activity of maturing fruits 

may partially offset these reproductive costs (Bazzaz et al. 

1979, Reekie and Bazzaz 1987, Cipollini and Levey 1991). 

The 2:1 sex ratio also suggests that some drought-sensitive females 

may have been eliminated from this subpopulation during 

the seven-decade interval of groundwater restriction, resulting 

from upstream water diversion for agricultural irrigation 

(Willms et al. 2005). 

Despite a major seasonal decline in Zgw, continuous groundwater 

availability associated with the phreatic zone prevented 

severe drought-induced water stress in streamside cottonwoods 

of the Oldman River valley. The seasonal pattern of 

Amax was parabolic, with an early season rise related to increasing 

photochemical capacity and a late-season decrease caused 

by a combination of leaf aging and declining soil water in the 

vadose zone. No major differences were observed between 

photosynthetic gas exchange, leaf reflectance, chlorophyll fluorescence 

or δ 13 C composition of male and female cottonwoods. 

These collective results demonstrate that groundwater 

availability remained sufficient to enable narrowleaf cottonwoods 

to use stomatal regulation to mitigate the effects of a 

late-summer drought on photosynthetic productivity. 

Acknowledgments 

This study was funded by the National Sciences and Engineering Re- 



search Council of Canada Discovery Grants (MGL and SBR) and by 

the Alberta Ingenuity Centre for Water Research (grants to Derek 

R. Peddle, Craig A. Coburn, MGL and SBR). K. Eric Van Gaalen and 

Yuan Yuan assisted with field measurements at PCCG. David 

W. Pearce provided insightful comments on the manuscript. We thank 

Liz Saunders and T. Andrew Hurly for site access. 

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