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NPK fertilization at planting of three hybrid poplar clones in the

boreal region of Alberta

Annie DesRochers a,*, R. van den Driessche b,c,1, Barb R. Thomas d,e

a Dep. Sciences Appliquees, Universite du Quebec en Abitibi-Temiscamingue, 341 rue Principale nord, Amos, Que. J9T 2L8, Canadab Biology Department, University of Victoria, P.O. Box 3020, Victoria, BC V8W 3N5, Canada

c New Dendrology Inc., 2361 Queenswood Drive, Victoria, BC V8N 1X4, Canadad Alberta-Pacific Forest Industries Inc., Box 8000, Boyle, Alta. T0A 0M0, Canada

e Genstat Consulting, Box 45086, Lansdowne Postal Outlet, Edmonton, Alta. T6H-5Y1, Canada

Received 9 February 2006; received in revised form 30 May 2006; accepted 4 June 2006

www.elsevier.com/locate/foreco

Forest Ecology and Management xxx (2006) xxx–xxx

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Abstract

EC

TED

PTrees from three hybrid poplar clones (one Populus balsamifera � P. simonii clone and two P. deltoides � P. � petrowskyana clones), were

grown for 3 years in an agricultural field and fertilized at planting with 27 combinations of nitrogen (N), phosphorus (P) and potassium (K)

fertilizers. Fertilizers used were granular ammonium nitrate (34.5–0–0) at three levels (0, 8 and 16 g/tree), triple-super-phosphate (0–45–0) at three

levels (0, 12.5 and 25 g/tree), and potassium sulfate (0–0–50) at three levels (0, 8 and 16 g /tree). Growth responses to N fertilization were negative

during the first growing season: N fertilization reduced growth, net assimilation rate (A), stomatal conductance (Gs), and increased the abundance

of 13C in the leaves. These results might be related to the soil pH at the site which ranged from 7.7 to 8.1, and to the dry conditions that prevailed

during the first growing season. Leaf N concentrations were unaffected by the fertilization level. Conversely, N fertilization decreased leaf P

concentrations, which were in turn positively correlated with growth and negatively correlated with carbon isotopic composition (d13C). There

were clonal differences in d13C that varied between the first and second growing seasons in relation to the relative growth rates of the clones.

Growth responses to fertilization at planting were nil or slightly positive during the second and third growing seasons. These results indicated that

ammonium nitrate was unsuitable for fertilizing these hybrid poplar clones at planting, and that further study is required to test fertilization at

planting with nitrate-N versus ammonium-N sources under these field conditions.

# 2006 Published by Elsevier B.V.

Keywords: Fertilization; Stable isotope; Hybrid poplar; Water-use efficiency; Ammonium nitrate; Mineral nutrition

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OR1. Introduction

There is increasing interest in utilizing wood fiber from fast-

growing high-yield plantations to reduce the exploitation

pressure on Canadian native forests (Gordon, 2001). Unlike

natural forests, plantations incur significant costs to establish

and maintain until the trees are ready to harvest. Fertilization is

typically one of the least expensive silvicultural treatments for

increasing yields. The establishment of new plantations can be

improved by fertilizing at the time of planting, to increase early

growth rates, allowing the trees to overtop competing

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* Corresponding author. Tel.: +1 819 732 8809x8327; fax: +1 819 732 8805.

E-mail addresses: annie.desrochers@uqat.ca (A. DesRochers),

robtvdd@telus.net (R. van den Driessche), thomasba@alpac.ca,

genstat@shaw.ca (B.R. Thomas).1 Tel.: +1 205 477 4134.

0378-1127/$ – see front matter # 2006 Published by Elsevier B.V.

doi:10.1016/j.foreco.2006.06.004

vegetation and form established stands sooner, ultimately

reducing the time period between planting and harvest (Miller,

1981). Moreover, placing fertilizer in small holes adjacent to

planted trees has been shown to increase growth by increasing

access to nutrients (van den Driessche, 1999). Fertilizer

placement also causes less promotion of competing vegetation

growth, which is often one of the major obstacles to the success

of fast-growing plantations (Rose and Ketchum, 2002),

especially on water-limited sites (Powers and Reynolds, 1999).

Fertilization of hybrid poplars (Populus spp.), one of the

most-utilized tree types in fast-growing plantations, is known to

be effective (van den Driessche, 1999; Brown and van den

Driessche, 2002). However, details of appropriate nutrients and

specific amounts vary according to regions and clones. Work

with aspen (Populus tremuloides Michx.) showed that

fertilizing a 12-year-old stand with a broadcast application

of 111 kg ha�1 each of nitrogen (N) and potassium (K), and

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55 kg ha�1 of phosphorus (P), increased height growth by 21%

and diameter growth by 37% after 5 years (van Cleve, 1973;

Coyne and van Cleve, 1977). In an older aspen stand with an

initial wood volume of 204 m3 ha�1, fertilization at 35 years

with 224 kg ha�1 of N, 112 kg ha�1 of P and 112 kg ha�1 of K

increased wood volumes by 145 m3 ha�1 over the unfertilized

control at 50 years (Yang, 1991).

Nitrogen fertilization may however increase the suscept-

ibility of hybrid poplars to drought-stress, although adding

phosphorus (P) may counteract this effect (Harvey and van den

Driessche, 1997). Given the recent drought history across the

boreal fringe of the Prairies (Environment Canada, 2004), this

is of concern for plantations being established in Western

Canada, because drought is often considered a limiting factor

for growth in these areas (Hogg, 1994; van den Driessche et al.,

2003). This is even more important for recently planted trees

and cuttings which usually have low root-to-shoot ratios

compared to naturally regenerated plants. Thus, fertilization

strategies should also be tested in conjunction with water-use

efficiency of the fertilized trees.

The objectives of this study were to examine the growth

responses of hybrid poplars to N, P and K fertilization applied at

the time of planting on a sandy loam soil in North Central

Alberta. The effects of treatment on growth were examined in

relation to foliar nutrient concentrations and water-use

efficiency.

2. Methods

The planting site is located in the Central Mixedwood

Subregion (Hosie, 1979) or Mid Boreal Mixedwood ecoregion of

Alberta (Strong and Leggat, 1992). The topography is flat to

undulating with an average elevation of 575 m. This subregion is

characterized by a continental boreal climate with long and cold

winters (mean temperature �10.5 8C) and short cool summers

(mean temperature 13.8 8C). The average total annual precipita-

tion is 380 mm with the majority falling in the summer months

(240 mm). Thesoils are classifiedasTolmansoil seriesdeveloped

on till materials and are characterized by loam to sandy loam

textures (Kjearsgaard, 1972). Aspen and balsam poplar (Populus

balsamifera L.) stands interspersed with pockets of white spruce

(Picea glauca Moench), in pure or mixed stands, make up the

surrounding forests. Most common understorey species are

bluejoint grass (Calamagrostis canadensis Michx.), wild

sarsparilla (Aralia nudicaulis L.), prickly rose (Rosa acicularis

Lindb.), fireweed (Epilobium angustifolium L.), bunchberry

(Cornus canadensis L.) and dewberry (Rubus pubescens Raf.).

The trees were planted in May 2002, in a previously cleared

agricultural field belonging to Alberta-Pacific Forest Industries

Inc. (548N, 1128W). The field was site-prepared with a plow

and cultivated with a farm tractor to remove weeds and to aerate

the soil. Three hybrid poplar clones were chosen for the

experiment: 33 (P. balsamifera � P. simonii cv. P38P38), 24 (P.

deltoides � P. � petrowskyana cv. Walker), 794 (P. deltoi-

des � P. � petrowskyana cv. Brooks6), based on material

availability, potential growth rates and operational use for

the area. The stock used was dormant 1-year-old container-

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grown rooted cuttings (6 cm � 15 cm plugs), obtained from a

commercial nursery. Trees were planted with regular planting

shovels. The different combinations of granular fertilizers were

placed approximately 10 cm from the stem of each tree, into a

slit made with the planting shovel to a depth of 10–15 cm.

The fertilizers were applied according to a 3N � 3P � 3K

factorial design, replicated three times as split plots within each

of the three poplar clones. The clones were randomized and

replicated into three blocks. The treatment unit was a two-tree

plot of one clone, planted at a 2 m � 2 m spacing (n = 486).

Fertilizers used were granular ammonium nitrate (34.5–0–0) at

three levels (0, 8 and 16 g N/tree), triple-super-phosphate (0–

45–0) at three levels (0, 12.5 and 25 g P/tree), and potassium

sulfate (0–0–50) at three levels (0, 8 and 16 g K/tree). These

doses correspond to 0, 20, and 40 kg ha�1 of N, 0, 31.25, and

62.5 kg ha�1 of P and 0, 20, 40 kg ha�1 of K.

Height and basal diameter were measured on all trees

immediately after planting and after each of the first three

growing seasons (October of each year). The plantation was kept

free of weeds throughout each growing season by mechanical

cross cultivation of the soil between and within each row of trees.

In mid-July of the first and second growing seasons,

measurements of net assimilation rate (A), transpiration (E),

and stomatal conductance (Gs) were made with an infrared gas

analyzer (IRGA, CIRAS I, PP Systems, Haverhill, MA).

Instantaneous water-use efficiency (WUE) was calculated as A/

E. Following the photosynthesis measurements, foliage was

collected for dry weight determination and chemical analysis.

Depending on leaf size, 5–10 mature leaves were collected

from each of the two trees in a treatment unit. Leaf samples

were pooled into two replicates for the first growing season

because of the small size of the trees. There were three

replicates of leaf samples for the second growing season. Leaf

area of the leaves sampled was measured at year 2 with a Licor

3100 leaf area meter, and weight was determined after drying at

80 8C to a constant value. Leaf samples were ground-up with a

Cyclone Sample Mill with a 1 mm mesh size (UDY Corp., Fort

Collins, CO) and chemical analyses of total N, P, K, Ca, Na,

Mg, S, Fe, Mn, Cu, Zn, Mo, and B were carried out (Norwest

Labs, Lethbridge, Alta.). Sub-samples of leaves were ground

more finely with a Brinkmann MM2 ball grinder and carbon

isotopic composition (d13C) was determined (Soil Biochem-

istry Laboratory, University of Alberta, Edmonton) using a

Carlo-Erba 1500 NCS directly interfaced to a V.G. Sira mass

spectrometer (Middlewich, Cheshire, UK) tuned for continuous

flow 13C IRMS measurements. The isotopic composition of the

samples was calculated from:

d13C ¼ ½ðRsample=RstandardÞ � 1� � 1000;

where Rsample and Rstandard are the ratios of 13C/12C in the

sample and standard, respectively. Spring wheat grain was used

as the working standard, with a carbon isotope composition of

�23.47% relative to Pee Dee Belemnite (PDB).

Prior to fertilization, a combined sample of four soil sub-

samples was taken from the 0 to 20 cm and 20–40 soil horizons

of each block. The soil samples were sent to the laboratory

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Table 1

Mean soil characteristics for both sampling depths

Depth

(cm)

Available P

(ppm)

Total N

(%)

K

(%)

pH Ca

(mequiv./100 g)

Mg

(mequiv./100 g)

Na

(mequiv./100 g)

C

(%)

CEC

(mequiv./100 g)

Base saturation

(%)

0–20 11.3 0.17 0.33 7.8 34.2 5 0.17 2.63 24 167

20–40 6.5 0.08 nda 7.9 26 5.5 0.1 1.18 21 153

a Non-detectable.

(Norwest Labs, Lethbridge, Alberta) and analyzed for total

Kjeldahl N, total C, available P (dilute acid fluoride method),

exchangeable K, Ca, Mg, total cation exchange capacity (CEC),

B and pH. Soil pH was quite high (7.8–7.9) and soil Ca was in

excess raising base saturation levels over 100% (Table 1).

Data was analyzed with the general linear model analysis of

variance (SAS Institute Inc., Cary, NC, version 8.2). Separate

analyses were conducted for each year. In order to test for yearly

growth variations, height and basal diameter were analyzed using

height and basal diameter at planting as covariates for the first

growing season, and using the previous year’s height and basal

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Fig. 1. Mean (a) height and (b) basal diameter growth of the three hybrid poplar clone

Bars with the same letters are not significantly different at p < 0.05.

Table 2

Analysis of covariance giving sources of variation, degrees of freedom and F valu

Source of variation d.f. Growth (year 1) Gr

Height Basal diameter He

Block 2 7.69 (0.04) 132.10 (<0.001) 12

Clone 2 83.07 (<0.001) 487.55 (<0.001) 0

Block � clone (error) 4 0.54 (0.71) 0.12 (0.97) 2

N 2 7.89 (<0.001) 4.68 (<0.01) 1

P 2 0.86 (0.43) 0.88 (0.42) 1

K 2 0.58 (0.56) 1.37 (0.25) 3

N � P 4 0.29 (0.89) 0.09 (0.99) 1

N � K 4 1.29 (0.27) 0.90 (0.46) 0

P � K 4 1.51 (0.20) 0.33 (0.86) 1

N � P � K 8 0.95 (0.47) 0.34 (0.95) 1

Clone � N 4 1.42 (0.23) 0.81 (0.52) 1

Clone � P 4 1.29 (0.27) 0.71 (0.59) 1

Clone � K 4 0.57 (0.68) 0.76 (0.55) 3

Clone � N � P 8 0.27 (0.97) 0.38 (0.93) 0

Clone � N � K 8 1.82 (0.07) 1.37 (0.21) 1

Clone � P � K 8 1.42 (0.19) 1.66 (0.11) 1

Clone � N � P � K 16 1.15 (0.31) 0.95 (0.51) 1

Height covariate 1 45.22 (<0.001) 4.29 (0.04) 6

Basal diameter covariate 1 7.32 (<0.01) 41.58 (<0.001) 63

Error 372

Probabilities for F tests are given in parentheses. The height and basal diameter c

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OFdiameter values for the second and third growing seasons. Least

square means were compared using Fisher’s protected LSD and a

significance level of p < 0.05 was chosen.

3. Results

Nitrogen (N) fertilization reduced height and basal

diameter growth of all clones by 6–10% (Fig. 1), while P

and K fertilization had no significant effect on growth during

the first growing season (Table 2). K fertilization at planting

increased height of clone 33 by 12% during the second

TED

P

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s for each N fertilization level after the first growing season. Error bars are S.E.s.

es for height and basal diameter growth of each growing season

owth (year 2) Growth (year 3)

ight Basal diameter Height Basal diameter

.63 (0.02) 14.97 (0.01) 1.56 (0.32) 0.69 (0.55)

.22 (0.22) 13.9 (0.02) 13.26 (0.02) 2.35 (0.21)

.88 (0.02) 2.58 (0.04) 4.09 (<0.01) 1.91 (0.11)

.62 (0.20) 3.05 (0.05) 2.59 (0.08) 2.35 (0.10)

.34 (0.26) 1.28 (0.28) 0.47 (0.62) 0.56 (0.57)

.38 (0.04) 1.89 (0.15) 0.35 (0.70) 0.19 (0.83)

.18 (0.32) 1.17 (0.33) 0.52 (0.72) 0.23 (0.92)

.76 (0.55) 1.07 (0.37) 0.43 (0.79) 1.19 (0.31)

.73 (0.14) 2.04 (0.09) 0.24 (0.92) 0.34 (0.85)

.42 (0.19) 1.37 (0.21) 0.72 (0.67) 1.93 (0.05)

.79 (0.13) 1.23 (0.30) 1.65 (0.16) 2.69 (0.03)

.98 (0.10) 0.87 (0.48) 0.50 (0.74) 0.36 (0.84)

.03 (0.02) 1.56 (0.18) 1.76 (0.14) 0.24 (0.92)

.93 (0.49) 1.50 (0.15) 0.65 (0.73) 0.68 (0.71)

.62 (0.12) 2.43 (0.01) 1.21 (0.29) 0.89 (0.53)

.31 (0.24) 1.37 (0.21) 0.65 (0.73) 0.63 (0.75)

.23 (0.24) 1.48 (0.10) 1.35 (0.17) 1.40 (0.14)

.06 (0.01) 0.20 (0.65) 225.34 (<0.001) 21.15 (<0.001)

.99 (<0.001) 100.74 (<0.001) 6.70 (0.01) 109.92 (<0.001)

ovariates correspond to tree sizes at the beginning of each growing season.

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Fig. 2. Mean height for each K fertilization level and clone combination after

the second growing season. Error bars are S.E.s. Bars with the same letters are

not significantly different at p < 0.05.

Table 3

Average height and basal diameter of trees at planting and at the end of each of

the three growing seasons

Clone

24 33 794

At planting

Height (m) 0.31 (0.01) a 0.30 (0.01) a 0.40 (0.01) b

Basal diameter (mm) 3.32 (0.08) a 3.15 (0.07) ab 3.00 (0.07) b

Year 1

Height (m) 0.64 (0.01) a 0.67 (0.01) a 0.49 (0.01) b

Basal diameter (mm) 7.88 (0.06) a 8.90 (0.05) b 5.99 (0.07) c

Year 2

Height (m) 1.31 (0.03) a 1.39 (0.02) a 1.35 (0.03) a

Basal diameter (mm) 20.80 (0.63) a 24.73 (0.59) b 24.58 (0.67) b

Year 3

Height (m) 3.01 (0.04) b 2.76 (0.03) a 2.81 (0.03) a

Basal diameter (mm) 48.80 (0.73) a 47.46 (0.65) a 46.61 (0.69) a

Note: standard errors are given in parentheses. Values in a line with the same

letter are not significantly different at p < 0.05.

Rgrowing season (Fig. 2), while there were no other effects of

fertilizers on height in the second and third years (Table 2).

Basal diameter growth after the third growing season

increased slightly for trees of clones 33 and 794 that had

received N at planting (Fig. 3). Average growth rank order of

clones was 794 < 24 < 33 during the first year (Table 3). At

the end of the third growing season, the trees on average had

reached nearly 3 m in height and 50 mm in basal diameter

(Table 3).

N fertilization at planting increased d13C, while it decreased

net assimilation rate (A) and stomatal conductance (Gs) (Fig. 4,

Table 4). Trees from clone 24 had higher d13C than those from

clones 33 and 794 (Fig. 5a) in the year of planting, while trees

from clone 794 had the highest d13C during the second growing

season (Fig. 5b). The addition of K increased d13C by an

average of 0.20% ( p = 0.04), while phosphorus fertilization

had no effect on d13C ( p = 0.29), the year of planting. There

were no significant interactions between the fertilizer treat-

ments and the clones for d13C during the first year, except for a

four-way interaction between N, P, K and clone ( p = 0.04),

which revealed a slightly higher increase of d13C for clone 24

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245Fig. 3. Mean basal diameter for each N fertilization level and clone combina-

tion after the third growing season. Error bars are S.E.s. Bars with the same

letters are not significantly different at p < 0.05.

CTE

D Punder the highest N level when no P was provided and K was

added (data not shown). Apart from the clonal differences noted

above, none of the treatments affected d13C or gas exchange

measurements during the second growing season. The

fertilizers had no significant effect on instantaneous water-

use efficiency (WUE) (Fig. 4d). In the year of planting,

instantaneous WUE was not correlated with d13C for each

individual clone, but was negatively correlated with d13C

(Pearson’s r = �0.17, p = 0.03) when data from all clones were

pooled. During the second growing season, the relationship

between WUE and d13C was only significant for clone 794

(r = �0.30; p = 0.04). The fertilizers applied at planting did not

influence gas exchange measurements during the second

growing season (Table 4); however, clone 794 had higher A

rates than the other clones (Fig. 6). There were positive

correlations between d13C and leaf P concentrations the year of

planting: Leaf P concentration explained 42%, 35% and 13% of

d13C variation for clones 24, 33, and 794, respectively

( p < 0.01).

Clone 33 had 33% smaller leaves (average leaf weight) than

the other clones during the first two growing seasons

( p < 0.01). The year of planting, N fertilization decreased

average leaf weight of clones 24 and 33 by 22% and 14%,

respectively, while it increased leaf weight of clone 794 by 17%

(Fig. 7a). Average leaf weight was greater during the second

growing season for all clones, and N applied at planting still had

a decreasing effect on average leaf weight (Fig. 7b) and leaf

area (not shown) of clone 24. Mean leaf weight and mean leaf

area (only measured in year 2) were well correlated (r2 = 0.94;

p < 0.001). Mean leaf weight of trees from clones 33 and 794

was positively correlated with d13C during the second growing

season (Table 5). Tree growth, on the other hand, was

negatively correlated with d13C, for clone 794 during the first

growing season and for clones 24 and 794 during the second

growing season (Table 5). Only height growth during the first

growing season of clone 33 was positively correlated with d13C

(Table 5).

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Fig. 4. Mean (a) carbon isotope ratio (b) net assimilation rate (c) stomatal conductance, and (d) instantaneous water-use efficiency of the three hybrid poplar clones

for each N fertilization level during the first growing season. Error bars are S.E.s. Bars with the same letters are not significantly different at p < 0.05.

RR

EDuring the first growing season, N fertilization decreased

leaf P ( p = 0.02) and leaf B ( p = 0.02) concentrations, and

increased leaf Ca ( p < 0.001) concentration (Fig. 8). However,

N fertilization had no significant effect on leaf N concentration

( p = 0.62; Fig. 8). Phosphorus fertilization had no effect on leaf

nutrient concentrations for either of the growing seasons

(Table 6). Potassium fertilization slightly increased leaf Ca

concentration from 1.73% to 1.84% ( p = 0.04) and leaf Mg

concentration from 0.50% to 0.53% ( p = 0.02), the year of

planting. During the second growing season, K fertilization

increased leaf N concentration by 0.11% ( p = 0.04), leaf K

concentration by 0.21% ( p < 0.001) and decreased leaf Mg

concentration by 0.04% ( p = 0.004). Nutrient concentrations

were similar between the clones during the first growing season,

however leaf B concentrations differed: 2.85 ppm for clone 24,

3.02 ppm for clone 33, and 3.20 ppm for clone 794 ( p = 0.004).

During the second growing season, clone 24 had higher leaf Ca

concentrations than the other clones ( p = 0.01), while clone

794 had lower leaf Mg concentrations than clones 24 and 33

( p = 0.02; Table 6). Eighteen percent and 46% of growth in the

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COTable 4

Mean net assimilation rate (A), stomatal conductance (Gs), water-use efficiency (WU

the three poplar clones

Plant measurement N level (g/tree)

0 8

First growing season

A (mmol m�2 s�1) 17.82 (0.44) a 16

Gs (mmol m�2 s�1) 459.00 (13.08) a 402

WUE (A/E) 4.08 (0.08) 4

d13C (%) �26.95 (0.07) a �26

Second growing season

A (mmol m�2 s�1) 17.67 (0.30) 18

Gs (mmol m�2 s�1) 396.99 (8.86) 409

WUE (A/E) 5.67 (0.11) 5

d13C (%) �28.37 (0.04) �28

Note: standard errors are given in parentheses. Values in a line with the same lette

TED

Pfirst year was explained by leaf B and P concentrations for

clones 33 and 794 ( p < 0.05), respectively, but leaf B and P

concentrations were not significantly correlated with height or

basal diameter growth of clone 24 ( p > 0.05). There were very

few interactions between the fertilizers and the clones for leaf

nutrient concentrations (Table 6), and those present did not

reveal any particular trend.

4. Discussion

Rather than enhancing plantation establishment and early

growth, N fertilization at planting reduced both height and basal

diameter, while P and K fertilization had no effect on growth,

the year of planting. Similar results were recently obtained for

an aspen (P. tremuloides Michx.) plantation receiving NH4NO3

in an N, P, K and B mixed fertilizer without irrigation (van den

Driessche et al., 2003). The lack of positive response to N

fertilization by aspen seedlings has also been demonstrated at

three different grassland sites (van den Driessche et al., in

press). Under greenhouse conditions, we showed that NH4NO3

FORECO 9905 1–10

E) and carbon isotope ratio (d13C) for each N level and treatment p values across

p-Value

16

.89 (0.44) a 15.54 (0.44) b <0.01

.85 (13.06) b 355.92 (12.99) c <0.001

.10 (0.08) 4.05 (0.08) 0.87

.65 (0.07) b �26.43 (0.07) c <0.001

.01 (0.30) 17.94 (0.30) 0.70

.43 (8.97) 403.91 (8.92) 0.61

.63 (0.12) 5.79 (0.11) 0.59

.37 (0.04) �28.33 (0.04) 0.70

r are not significantly different at p < 0.05.

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Fig. 5. Mean carbon isotope ratio for each hybrid poplar clone during (a) the

first and (b) second growing seasons. Error bars are S.E.s. Bars with the same

letters are not significantly different at p < 0.05.

Fig. 7. Mean leaf dry weight for each N level and hybrid poplar clone

combination during (a) the first and (b) second growing seasons. Error bars

are S.E.s. Bars with the same letters are not significantly different at p < 0.05.

CO

RR

fertilizer behaved like a NO3�-N source, although half of its N

is NH4� (DesRochers et al., 2003); Ammonium nitrate

produced similar physiological and growth responses as

calcium nitrate, when compared to other ammonium-sources

fertilizers. In this study, the soil pH was quite high (range 7.7–

8.1), and the trees were apparently unable to take up the N from

the fertilizer (Fig. 8a). Recent work by Lu et al. (2005) also

showed that NH4NO3 and NO3-N had similar effects on the

physiology of tobacco (Nicotiana tabacum) plants. These

results indicate that ammonium (NH4+) sources of N rather than

NO3-N or NH4NO3 fertilizers should be used for hybrid poplars

on soils with high pH levels (DesRochers et al., 2003; Choi

et al., 2005), to facilitate N uptake and promote growth of the

trees. This is further supported by evidence from hydroponic

cultures showing that uptake of NH4+ by aspen is faster than

uptake of NO3� (Min et al., 2000). Even if nitrification takes

place over a wide range of pH values, the optimum pH is 8.5

(Tisdale et al., 1999), suggesting that the NH4+ in this fertilizer

was rapidly changed into nitrate (NO3�). As the pH of the soil

solution increases, uptake of NO3� usually decreases because

the reduction of NO3� produces hydroxide (OH�) ions which

then have to be neutralized, normally by the production of

UN

Fig. 6. Mean (a) net assimilation rate and (b) stomatal conductance for each hybrid p

same letters are not significantly different at p < 0.05.

CTE

Dorganic acids by the plant. If the pH is high, the neutralization

process is more difficult and may disrupt the organic synthesis,

affecting in turn the overall uptake of NO3� (Huffaker and

Rains, 1978; Miller and Cramer, 2004).

Leaf Ca concentration increased, while leaf B and P

concentrations decreased with the increase of N fertilization

levels (Fig. 8), reflecting the effect of NH4NO3 in accentuating

the adverse effect of pH (Gupta and MacLoed, 1981). Most

studies place critical P concentrations of different hybrid poplar

varieties above or around 0.25% (Leech and Kim, 1981;

Hansen, 1994; McLennan, 1996). Leaf P concentrations of

unfertilized trees in this study were already below 0.20%, and

the high N level reduced P concentrations by about 0.195–

0.185% (Fig. 8b). Phosphorus is important for the establish-

ment phase of hybrid poplars (Brown and van den Driessche,

2005), and this is probably why growth of the N-fertilized trees

was reduced (Fig. 1). Together, leaf B and P concentrations

explained 18% and 46% of first-year growth of clones 33 and

794, respectively. At high soil pH, NH4NO3 negatively affected

absorption of P and B of aspen (DesRochers et al., 2003). In a

growth solution, Bengtsson et al. (1994) also found that high

concentrations of NO3� reduced P concentrations in beech

plants (Fagus sylvatica L.).

FORECO 9905 1–10

oplar clone during the second growing season. Error bars are S.E.s. Bars with the

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Table 5

Pearson’s correlation coefficients between d13C and height growth, basal diameter growth and mean leaf dry weight

First growing season Second growing season

Clone 24 Clone 33 Clone 794 Clone 24 Clone 33 Clone 794

Height growth �0.03 (0.82) 0.28 (0.05) �0.40 (0.003) �0.32 (0.003) �0.09 (0.37) �0.36 (0.008)

Basal diameter growth �0.17 (0.23) 0.15 (0.31) �0.52 (<0.001) �0.32 (0.002) 0.03 (0.74) �0.35 (0.01)

Mean leaf dry weight 0.01 (0.94) 0.13 (0.35) 0.17 (0.23) 0.10 (0.33) 0.42 (<0.001) 0.58 (<0.001)

p values are given in parentheses.

N fertilization did not significantly affect instantaneous

WUE (Fig. 4d), however, instantaneous WUE was negatively

correlated, though only slightly, with d13C. The high N level

increased d13C by 0.51% compared to the unfertilized trees

UN

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380Fig. 8. Mean leaf (a) N, (b) P, (c) Ca, and (d) B concentrations of the three hybrid

poplar clones for each N fertilization level after the first growing season. Error bars

are S.E.s. Bars with the same letters are not significantly different at p < 0.05.

TED

PR

OO

F(Fig. 4a). This effect of N fertilization was not caused by higher

leaf N concentrations (Ripullone et al., 2004) because they did

not vary with N fertilization levels (Fig. 8a). Somehow the

addition of NH4NO3 at planting stressed the trees during the

first growing season so that Gs was reduced. It is possible that

the decrease in Gs with N fertilization (Fig. 8) was caused by the

increase in leaf Ca concentration, which has been shown to

inhibit stomatal opening through a synergism with abscisic acid

in Commelina communis L. (De Silva et al., 1985). The increase

in d13C was likely a result of this lower Gs, which was reduced

by 20% in the high N level treatment, although A was only

reduced by 10% (Fig. 4b and c). This would limit the supply of

CO2 inside the leaf for photosynthesis and therefore induce

more 13CO2 fixation (Siegwolf et al., 2001). Yin and Raven

(1998) also found that NO3�-grown plants of Triticum

aestivum L. had lower WUE, with more water lost per gram

of dry weight gain, than NH4+-grown plants. The decrease in A

and Gs could also be due to the lower P concentrations of the N-

fertilized trees. Bruck et al. (2000) found a relationship between

P concentrations and 13CO2 discrimination in pearl millet

(Pennisetum glaucum (L.) R. Br.), where d13C increased by

0.36% when P supply was low. This is in accordance with our

results, where leaf P concentration explained 42%, 35% and

13% of the d13C variation for clones 24, 33, and 794,

respectively, the year of planting.

The carbon isotope composition of plant tissues has been

used to estimate long-term water-use efficiency (Farquhar et al.,

1989; Livingston and Spittlehouse, 1996; Livingston et al.,

1999). As plants become moisture stressed, leaf stomatal

apertures are reduced to limit water loss in comparison with the

rate of CO2 uptake, because the gradient for water loss is greater

than the gradient for CO2 uptake, leading to greater water-use

efficiency. The year 2002 was a relatively dry year, with

approximately 255 mm of rain (Environment Canada, 2004).

During this year, trees of clones 24 and 33 grew significantly

more than those of clone 794 (more than 25% in height and

basal diameter; Table 1). Interestingly, d13C of these two clones

was not negatively correlated with their height and basal

diameter growth, as were those from clone 794, during the first

growing season (Table 5). Faster-growing trees fix more CO2,

which can increase 13CO2 abundance when water is limited and

plants are water-stressed (Hogberg et al., 1993). This is

especially important the year of planting, since all trees were

grown in the same-sized containers prior to out-planting

(similar amounts of roots), implying that larger plants had

smaller root-to-shoot ratios. This could explain some of the

observed clonal differences in d13C during the first growing

season (Fig. 5a). It could also be argued that the lower d13C

FORECO 9905 1–10

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Table 6

Analysis of variance giving sources of variation, degrees of freedom and F values for leaf nutrient concentration during the first and second growing seasons

Source of variation d.f. First growing season Second growing season

N (%) P (%) K (%) Ca (%) Mg (%) B (ppm) N (%) P (%) K (%) Ca (%) Mg (%) B (ppm)

Block 2 2.07 (0.29) 5.48 (0.14) 19.64 (0.05) 1.72 (0.32) 72.68 (0.01) 860.05 (0.001) 3.49 (0.13) 1.07 (0.43) 4.68 (0.09) 1.14 (0.41) 6.02 (0.06) 0.54 (0.62)

Clone 2 6.25 (0.14) 15.34 (0.06) 16.36 (0.06) 11.87 (0.08) 12.68 (0.07) 254.19 (0.004) 3.99 (0.11) 1.90 (0.26) 1.94 (0.26) 15.99 (0.01) 12.74 (0.02) 1.19 (0.39)

Block � clone (error) 4 15.91 (<0.001) 1.75 (0.18) 0.65 (0.53) 6.98 (0.002) 0.21 (0.81) 0.01 (0.99) 4.41 (0.002) 5.83 (<0.001) 4.00 (0.004) 5.29 (<0.001) 1.25 (0.29) 2.17 (0.08)

N 2 0.49 (0.62) 4.11 (0.02) 1.06 (0.35) 18.37 (<0.001) 1.73 (0.19) 4.04 (0.02) 0.20 (0.82) 1.22 (0.30) 0.50 (0.61) 2.48 (0.09) 1.12 (0.33) 2.17 (0.12)

P 2 0.09 (0.91) 0.57 (0.57) 0.62 (0.54) 0.55 (0.58) 2.22 (0.12) 0.82 (0.45) 0.96 (0.39) 2.61 (0.08) 0.20 (0.82) 0.07 (0.93) 0.54 (0.58) 0.31 (0.73)

K 2 0.86 (0.43) 0.53 (0.59) 0.12 (0.89) 3.52 (0.04) 4.33 (0.02) 0.86 (0.43) 3.39 (0.04) 1.34 (0.26) 14.25 (<0.001) 1.70 (0.19) 5.67 (0.004) 2.88 (0.06)

N � P 4 0.24 (0.91) 1.00 (0.42) 0.35 (0.84) 1.50 (0.21) 0.34 (0.85) 0.42 (0.79) 0.67 (0.62) 1.55 (0.19) 1.19 (0.32) 2.20 (0.07) 1.71 (0.15) 1.48 (0.21)

N � K 4 2.08 (0.09) 0.50 (0.74) 0.39 (0.82) 0.50 (0.73) 0.38 (0.82) 2.06 (0.10) 0.34 (0.85) 0.05 (0.99) 0.14 (0.97) 0.47 (0.76) 0.24 (0.92) 0.35 (0.84)

P � K 4 1.01 (0.41) 0.26 (0.90) 0.46 (0.77) 2.85 (0.03) 2.27 (0.07) 0.88 (0.48) 1.13 (0.35) 2.17 (0.08) 1.31 (0.27) 0.21 (0.93) 0.15 (0.96) 0.34 (0.85)

N � P � K 8 0.88 (0.54) 1.18 (0.32) 0.55 (0.81) 1.41 (0.21) 0.77 (0.63) 0.68 (0.71) 0.28 (0.97) 0.78 (0.62) 0.45 (0.89) 0.98 (0.46) 1.88 (0.07) 0.73 (0.67)

Clone � N 4 0.30 (0.87) 0.61 (0.66) 0.87 (0.49) 1.00 (0.42) 1.08 (0.37) 2.40 (0.06) 0.21 (0.93) 0.58 (0.68) 0.12 (0.98) 2.34 (0.06) 1.57 (0.19) 0.79 (0.53)

Clone � P 4 2.47 (0.05) 0.26 (0.90) 1.30 (0.28) 3.07 (0.02) 0.39 (0.82) 1.90 (0.13) 1.67 (0.16) 4.19 (0.003) 3.28 (0.01) 2.04 (0.09) 0.90 (0.47) 0.73 (0.57)

Clone � K 4 0.89 (0.48) 0.21 (0.93) 0.50 (0.73) 0.35 (0.84) 0.13 (0.97) 0.61 (0.66) 1.51 (0.20) 0.65 (0.62) 0.98 (0.42) 0.18 (0.95) 1.25 (0.29) 0.50 (0.73)

Clone � N � P 8 0.40 (0.92) 0.38 (0.93) 0.39 (0.92) 0.97 (0.47) 1.07 (0.40) 0.54 (0.82) 0.39 (0.93) 0.38 (0.93) 0.58 (0.79) 0.74 (0.66) 0.95 (0.48) 0.72 (0.68)

Clone � N � K 8 2.05 (0.05) 1.06 (0.40) 1.72 (0.11) 2.20 (0.04) 1.06 (0.40) 1.40 (0.22) 0.52 (0.84) 1.07 (0.39) 1.58 (0.14) 0.48 (0.87) 0.33 (0.95) 0.66 (0.73)

Clone � P � K 8 1.03 (0.43) 0.63 (0.75) 0.60 (0.77) 1.34 (0.24) 0.35 (0.94) 1.65 (0.14) 0.20 (0.99) 2.03 (0.05) 1.81 (0.08) 1.04 (0.41) 1.03 (0.42) 0.40 (0.92)

Clone � N � P � K 16 1.58 (0.10) 1.09 (0.38) 1.26 (0.26) 0.48 (0.94) 0.60 (0.87) 0.85 (0.61) 0.60 (0.88) 0.85 (0.62) 0.88 (0.60) 0.75 (0.74) 0.68 (0.81) 0.46 (0.96)

Error 60

Probabilities for F tests are given in parentheses.

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values of trees from clone 33, despite their greater growth rates,

were due to the smaller average leaf size of this clone (Fig. 7).

Narrow leaves are usually better adapted to dry environments

compared to wider leaves (Ackerly, 2004). However, average

leaf dry weight was not correlated with d13C during the first

growing season, and it was positively correlated with d13C

during the second growing season, for clones 33 and 794

(Table 5). This indicates that trees from these two clones that

produced larger (or heavier) leaves during the second growing

season fixed less 13CO2 than trees with smaller leaves,

suggesting that their stomatal function was not restricted by

moisture, allowing the trees to discriminate more against13CO2. Moreover, we saw that N fertilization significantly

reduced average leaf size of clone 24 (Fig. 7). Reduction of leaf

size can be a result of drought stress (Fair and Breshears, 2005;

Otieno et al., 2005), suggesting that clone 24 is more drought-

sensitive than the other clones used in this study. Trees from

clone 24 also tended to have the lowest leaf P concentrations

( p = 0.06), which could indicate that hybrid poplar trees with

higher leaf P concentrations can better withstand drought stress,

as previously suggested by Harvey and van den Driessche

(1999). The plantation received 22% more rain during the

second growing season (Environment Canada, 2004), and this

was reflected in all clones having lower d13C values than in the

previous year (Fig. 5b). Trees from clone 794 had the highest

d13C values during the second growing season (Fig. 5b), which

could be related to their higher A rates during this period,

although their Gs remained similar to that of the other clones

(Fig. 6). This could constitute a physiological advantage for this

clone in dry environments such as the Canadian Prairies.

The effects of the fertilizers in the second and third growing

seasons were relatively small (Figs. 2 and 3). The negative

effect of N fertilization on growth of clones 33 and 794 had

ceased and their basal diameter growth in the second growing

season increased slightly for trees that had received N at

planting (Fig. 3). This suggests that some of the NH4NO3

fertilizer remained in the soil for the second growing season,

but that it did not cause the stomatal stress (Table 4) it had

caused during the first growing season. The amount of fertilizer

remaining in the soil during the second growing season was

most likely reduced, and the shift in its effect on the growth of

clones 33 and 794 could be due to the wetter conditions (van

den Driessche et al., 2003).

In conclusion, this study showed that NPK fertilization at

planting failed to increase first-year growth of three hybrid

poplar clones grown under field conditions with high soil pH.

Trees showed mainly negative responses to N fertilization

with NH4NO3 until year 3, when small diameter increases

were detected. During the first growing season, N fertiliza-

tion reduced net assimilation rate (A), stomatal conductance

(Gs) and leaf P concentrations, and increased the abundance

of 13C and Ca in the leaves. Differences in d13C suggest that

N fertilization has rendered the trees more sensitive to

drought, and that clone 24 was more sensitive than the

others. These clonal differences could be exploited in

afforestation strategies in the dry conditions of the

Canadian Prairies.

TED

PR

OO

F

Uncited reference

Gomez-Del-Campo et al. (2003).

Acknowledgements

This research was funded by Alberta-Pacific Forest

Industries Inc., in collaboration with Forest Resource Improve-

ment Association of Alberta, and the Natural Sciences and

Engineering Research Council of Canada through an Industrial

Research Fellowship to AD. We also thank the University of

Alberta, Canada Economic Development, Norwest Labs and

Line Blackburn and David Kamelchuk for field and lab work.

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