Carbon sequestration in boreal jack pine stands followingharvesting

T I A N S H A N Z H A *, A L A N G . B A R R *, T . A N D Y B L A C K w , J . H A R R Y M C C A U G H E Y z,J . B H A T T I § , I . H AW T H O R N E w , P R AV E E N A K R I S H N A N w , J . K I D S T O N w , N . S A I G U S A } ,

A . S H A S H K O V k and Z . N E S I C w*Climate Research Division, Environment Canada, 11 Innovation Blvd, Saskatoon, SK, Canada S7N 3H5, wFaculty of Land and

Food Systems, University of British Columbia, Vancouver, BC, Canada V6T 1Z4, zDepartment of Geography, Queen’s University,

Kingston, ON, Canada K7L 3N6, §Northern Forestry Centre, Canadian Forest Service, Edmonton, AB, Canada T6H 3S5,

}Air Quality Research Division, Environment Canada, Toronto, ON, Canada M3H 5T4, kNational Institute of Advanced Industrial

Science and Technology (AIST), Tsukuba 305-8569, Japan

Abstract

A large area of boreal jack pine (Pinus banksiana Lamb.) forest in Canada is recovering

from clear-cut harvesting, and the carbon (C) balance of these regenerating forests

remains uncertain. Net ecosystem CO2 exchange was measured using the eddy-

covariance technique at four jack pine sites representing different stages of stand

development: three postharvest sites (HJP02, HJP94, and HJP75) and one preharvest site

(OJP). The four sites, located in the southern Canadian boreal forest, Saskatchewan,

Canada, are typical of low productivity jack pine stands and were 2, 10, 29, and 90 years

old in 2004, respectively. Mean annual net ecosystem production (NEP) for 2004 and 2005

was �137� 11, 19� 16, 73� 28, and 22� 30 g C m�2 yr�1 at HJP02, HJP94, HJP75 and OJP,

respectively, showing the postharvest jack pine stands to be moderate C sources

immediately after harvesting, weak sinks at 10 years, moderate C sinks at 30 years, then

weak C sinks at 90 years. Mean annual gross ecosystem photosynthesis (GEP) for the

2 years was 96� 10, 347� 20, 576� 34, and 583� 35 g C m�2 yr�1 at HJP02, HJP94, HJP75,

and OJP, respectively. The ratio of annual ecosystem respiration (R) to annual GEP was

2.51� 0.15, 0.95� 0.04, 0.87� 0.03, and 0.96� 0.03. Seasonally, NEP peaked in May or

June at all four sites but GEP and R were highest in July. R at a reference soil temperature

of 10 1C, ecosystem quantum yield and photosynthetic capacity were lowest for the

2-year-old stand. R was most sensitive to soil temperature for the 90-year-old stand.

The primary source of variability in NEP over the course of succession of the jack pine

ecosystem following harvesting was stand age due to the changes in leaf area index.

Intersite variability in GEP and R was an order of magnitude greater than interannual

variability at OJP. For both young and old stands, GEP had greater interannual variability

than R and played a more important role than R in interannual variation in NEP. Based

on year-round flux measurements from 2000 to 2005, the 10-year stand had larger

interannual variability in GEP and R than the 90-year stand. Interannual variability in

NEP was driven primarily by early-growing-season temperature and growing-season

length. Photosynthesis played a dominant role in the rapid rise in NEP early in stand

development. Late in stand development, however, the subtle decrease in NEP resulted

primarily from increasing respiration.

Keywords: carbon balance, eddy covariance, harvesting, jack pine, net ecosystem production, photo-

synthesis, photosynthetic capacity, Pinus banksiana, quantum yield, respiration

Received 16 June 2008 and accepted 08 September 2008

Correspondence: Tianshan Zha, fax: 1 1 306 975 6516, e-mail:

tianshan.zha@ec.gc.ca

Global Change Biology (2009) 15, 1475–1487, doi: 10.1111/j.1365-2486.2008.01817.x

r 2009 The AuthorsJournal compilation r 2009 Blackwell Publishing Ltd 1475

Introduction

The carbon (C) balance of a forest varies dramatically

during stand development (e.g. Odum, 1969; Sprugel,

1985; Law et al., 2003; Clark et al., 2004; Howard et al.,

2004; Kolari et al., 2004; Martin et al., 2005; Humphreys

et al., 2006; Grant et al., 2007). As a result, the C balance

at the landscape scale is strongly influenced by forest

age-class structure (Kurz & Apps, 1995), which in turn

is the legacy of stand-replacing disturbances. Clear-

cutting, a common practice in forest management,

removes the commercial stem wood and leaves residues

of foliage, twigs, branches, stumps, and roots. It elim-

inates canopy photosynthesis and affects autotrophic

and heterotrophic respiration both directly and indir-

ectly. As a result, the postharvest stand is expected to be

a source of C for several years after disturbance

(Schulze et al., 1999; Kowalski et al., 2003, 2004; Kolari

et al., 2004). Middle-aged stands are usually C sinks

(Valentini et al., 2000). As stands mature, the sink

strength declines. Old stands often become moderate

to small C sinks or even C sources (Hollinger et al., 1994;

Goulden et al., 1998; Malhi et al., 1999; Griffis et al., 2003;

Knohl et al., 2003; Law et al., 2003; Desai et al., 2005).

Jack pine is the most widely distributed tree species

in the boreal forest (Farrar, 1995). However, the C

balances of such regenerating forests are not well char-

acterized. In Canada, 1 million hectare of 247 million

hectares of commercial forestland are harvested an-

nually. On average, another 2–3 million hectares of

forest are lost to fire, while 1–4 million hectares are

killed by insect damage annually (Kurz & Apps, 1999).

Postharvest forests represent a significant fraction of the

land cover. Intensive stand-replacing disturbance re-

sults in an extensive mosaic containing patches of

even-aged forest stands at various stages of secondary

succession. Understanding the terrestrial C cycle of such

a landscape requires an assessment of the C dynamics

at various stages of stand development (Desai et al.,

2008).

Several recent studies have characterized forest C

storage and net primary production (NPP) following

stand-replacing harvesting (Striegl & Wickland, 1998;

Law et al., 2001, 2003; Howard et al., 2004; Martin et al.,

2005; Grant et al., 2007). The postharvest chronose-

quence of net ecosystem production (NEP) following

disturbance has been estimated from independent mea-

surements of NPP and heterotrophic respiration (e.g.

Howard et al., 2004; Pregitzer & Euskirchen, 2004).

However, biometric estimates of NEP have methodolo-

gical and sampling limitations, including uncertainty in

the partitioning of R into heterotrophic and autotrophic

components (Gough et al., 2008). A more detailed and

direct examination of C dynamics following distur-

bance can be achieved by continuous, long-term flux

measurements. The eddy-covariance (EC) technique

provides a direct method to investigate the ecosys-

tem–atmosphere C exchange of whole forest ecosystems

(Baldocchi, 2003; Goulden et al., 2006) and is widely

used in C balance studies following harvesting (Clark

et al., 2004; Kolari et al., 2004; Kowalski et al., 2004;

Humphreys et al., 2006).

This study examines the C cycle using the EC tech-

nique across a postharvest age sequence of jack pine

stands. The primary objectives are (1) to determine the

carbon balance at different stages of stand development

following harvesting, (2) to understand the effect of

climatic factors on the C dynamics in the different

stages of stand development, and (3) to examine the

interannual variability in NEP.

Materials and methods

Site description

The study sites are located in the southern Canadian

boreal forest, about 100 km northeast of Prince Albert,

Saskatchewan, Canada. Four jack pine stands were

selected, which represent four critical stages of stand

development following harvesting: stand initiation,

young, intermediate and mature. Table 1 summarizes

the stand and site characteristics. Two sites, HJP75 and

OJP, were established in 1994 as part of the Boreal

Ecosystem Atmosphere Study (BOREAS; Sellers et al.,

1997). HJP94 was established in 2000 as part of the

Boreal Ecosystem Research and Monitoring Sites pro-

gram (BERMS; http://berms.ccrp.ec.gc.ca). HJP02 was

established in 2003 as part of the Fluxnet-Canada Re-

search Network (FCRN). The understories were mix-

tures of reindeer lichen (Cladina spp.), which dominated

the old stands, bearberry [Arctostaphylos uvaursi (L.)

Spreng], which dominated the younger stands, and

infrequent, scattered clumps of green alder [Alnus vir-

idis spp. crispa (Ait.) Turrill] co-occurring with feath-

ermoss (Pleurozium spp.).

The three younger stands regenerated following

clear-cut harvesting in 1975 (HJP75), 1994 (HJP94),

and 2002 (HJP02), and the older stand (OJP) originated

after wildfire in 1914. Before harvest, all sites had

mature jack pine stands that originated after wildfire.

The four stands are within 5 km of each other. All stands

are located in flat portions of a glacial outwash plain.

The soil is sandy (Table 1), well drained, and nutrient-

poor. Because of their similar soil parent material,

mineral soil texture and water-holding capacity, miner-

al soil C and N content, and environmental conditions

and stand histories (Table 1), the four stands constitute a

uniform postharvest chronosequence. Although the two

1476 T . Z H A et al.

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older sites, HJP75 and OJP, have a developed surface

organic horizon (LFH), which is virtually absent at

HJP02 and HJP94, and have more soil organic matter

in the A and B horizons, these attributes vary character-

istically with stand age and so do not reflect hetero-

geneity in stand development.

Mean annual air temperature (2000–2005, 28 m above

the ground, OJP) was 1.3 1C. Mean annual precipitation

was 454 mm (2000–2005, OJP). Monthly mean tempera-

ture was lowest in January (�16.9 1C) and highest in

July (17.9 1C).

Measurements

CO2 fluxes were measured continuously throughout

year by the EC technique at each site. The EC systems

consisted of a sonic anemometer (model CSAT3, Camp-

bell Scientific Inc., Logan, UT, USA, at HJP02 and OJP;

model SAT-550, Kaijo Co., Tokyo, Japan, at HJP94;

model Gill R3-50, Gill Instruments Ltd, Lymington,

UK, at HJP75), and a closed-path infrared gas analyzer

(model LI-6262, LI-COR Inc., Lincoln, NE, USA, at

HJP02, HJP94, and OJP; model LI-7000, LI-COR Inc.,

at HJP75). The instruments were mounted on scaffold

towers 5, 6, 16, and 29 m tall at HJP02, HJP94, HJP75,

and OJP, respectively. The IRGAs were in temperature-

controlled housings and had heated air-sampling tubes

3–4 m long, through which air was drawn at 10 L min�1.

The IRGAs were calibrated daily by sequentially using

CO2-free nitrogen gas (zero offset calibration) and a gas

of known CO2 concentration (close to 370 mmol mol�1)

in dry air from gas cylinders calibrated against a

standard from Environment Canada’s Greenhouse Gas

Measurement Laboratory in Downsview, ON, Canada.

Continuous high-frequency (10 Hz for HJP94, 20 Hz for

other sites) data were archived and postprocessed to

calculate the eddy fluxes at half-hour intervals. Mea-

surements started from 2003, 2001, 2004, and 2000 for

HJP02, HJP94, HJP75, and OJP, respectively. The analy-

sis of intersite variability focused on 2004 and 2005,

when measurements were made at all sites. The analy-

sis of interannual variability and its climatic controls

focused on OJP, which had 6 years of data, and HJP94,

which had 5 years of data.

Net ecosystem CO2 exchange (NEE) was calculated

as the sum of the measured eddy flux (Fc) and storage

flux (Sc).

NEE ¼ Fc þ Sc; ð1Þ

Table 1 Site and stand characteristics

HJP02 HJP94 HJP75 OJP

Stand inception date (year) 2002 1994 1975 1914

Age (years, 2004) 2 10 29 90

Latitude (decimal1) 53.941N 53.911N 53.881N 53.921N

Longitude (decimal1) 104.651W 104.661W 104.651W 104.691W

LAI (m2 m�2, 2004) 0.18* 0.8 3.1 2.0

Stem density (stem ha�1, 2002) 0 12 500 (2458) 7000 (816) 1900 (397)

Height (m, 2002) 0 1.7 (0.5) 7.6 (1.8) 16.7 (3.3)

Basal area (m2 ha�1, 2002) 0 1.01 (0.4) 69.8 (2.8) 110 (19.5)

Dead above ground (t C ha�1) 8.8 (1.3) 5.6 (1.1) 3.6 (0.9) 6.2 (1.3)

Fine woody debris (t C ha�1) 0.14 (0.04) 0.20 (0.04) 0.03 (0.01) 0.08 (0.03)

LFH

C(t C ha�1) 0.96 (0.7) 0.98 (0.3) 8.8 (1.5) 5.3 (0.5)

N(t C ha�1) 0.01 0.03 0.20 0.12

C/N 44 44

Sand/silt/clay in BC horizon (%) 92/6/2 92/5/3 86/10/4 87/8/5

Mineral soil C to 50 cm (t C ha�1) 17.5 (3.3) 14.0 (2.7) 18.4 (2.2) 15.8 (1.2)

Mineral soil N to 50 cm (t N/ha) 0.81 1.07 0.77 0.89

WHC* (%) 0–30 cm 6.8 6.7 9.6 (6.7) 9.3 (9.1)

Annual air temperature ( 1C) 1.3 (0.6) 1.4 (1.1) 1.2 (1.1) 0.9 (1.1)

April–May air temperature ( 1C) 5.4 (2.6) 6.1 (2.1) 6.7 (2.1) 6.5 (1.9)

Annual precipitation (mm) 417 (109) 413 (87) 414 (70) 401 (80)

Age and LAI (hemisurface) are from 2004, other measurements are from 2002. Climatic data are the mean of the time period from

respective stand initiation to 2005, based on the records from the nearby Prince Albert Airport. The value in the parenthesis is the

standard error. Data were measured according to the Fluxnet-Canada protocols (http://www.fluxnet-canada.ca/).

Note:

*LAI estimated using the relationship between LAI and NDVI developed using 2006 data. WHC is water-holding capacity.

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where

Sc ¼Z zec

0

ra

dsc

dtdz; ð2Þ

where zec is height above ground level of the EC

measurement, ra is the molar density of dry air, and sc

is the CO2 molar mixing ratio. Fc was calculated using

Fc ¼ raw0s0c, where w0s0c is the covariance between sc and

the vertical velocity (w). A coordinate rotation was

applied to make the mean vertical and lateral compo-

nents of wind velocity equal to zero (Tanner & Thurtell,

1969). The overbar and prime denote half-hour average

and fluctuation from the average, respectively. NEP was

then estimated as NEE.

Meteorological variables were measured at each site.

Incident photosynthetically active radiation (Q) was

measured using ML-020P (Eko Co. Ltd, Tokyo, Japan)

at HJP94 and LI-190 SA (LI-COR Inc.) at the other sites.

Air temperature was measured using HMP45C tem-

perature/humidity probes (Vaisala Oyj, Helsinki, Fin-

land) at 2, 4, 15, and 28 m above the ground at HJP02,

HJP94, HJP75, and OJP, respectively. Precipitation was

measured with a weighing gauge (Belfort Instruments,

Baltimore, MD, USA) at OJP. The gauge was located in a

clearing in the forest where the solid angle above the

gauge always exceeded 901. Soil water content at

0–15 cm depth was measured using CS615 soil water

reflectometers (Campbell Scientific Inc. ). Soil tempera-

ture was measured at a depth of 2 cm using copper-

constantan thermocouples at four locations at each site.

The average of the four locations was used in the

analysis.

Data processing

Quality control of NEE included the elimination of

spikes in the high frequency data and bad half-hour data

caused by instrument failure, power failure, pump fail-

ure, and depletion of the zero gas. Night-time NEE data

were excluded below a friction velocity u*

threshold

(Fig. 1; Griffis et al., 2003; Iwashita et al., 2005), determined

from the data to be 0.10, 0.10, 0.25, and 0.25 m s�1 for

HJP02, HJP94, HJP75, and OJP, respectively. On average,

about 16%, 11%, 26%, and 21% data were excluded by the

u*

threshold for the four sites, respectively. After screen-

ing, data were available for 58%, 45%, 54%, and 66% of

the periods for the four sites, respectively.

Gaps in NEP were filled using the standard method

of the FCRN method (Barr et al., 2004; Amiro et al.,

2006). The gap-filling procedure used two simple em-

pirical equations: a three-parameter logistic equation

relating ecosystem respiration R to shallow soil tem-

perature and the Michaelis–Menten equation relating

gross ecosystem photosynthesis (GEP) to Q above the

canopy. Some model parameters (e.g. a – the ecosystem

quantum yield) were evaluated annually whereas

others [e.g. Amax – the photosynthetic capacity (GEP at

light saturation)] were allowed to vary in time, fit to a

moving window of 100 measured NEE data points.

Parameter estimation and statistical analysis

Two ecosystem respiration parameters, the respiration

at a reference soil temperature of 10 1C (R10) and the

temperature coefficient of respiration (Q10) were esti-

mated annually, by first fitting the night-time respira-

tion data (from EC) to a logistic model:

R ¼ r1

1þ exp½r2ðr3 � TsÞ�; ð3Þ

where Ts is the soil temperature at 2 cm depth and r1 to r3

are empirical constants, and then estimating R10 and Q10

from Eqn (3) as the value at 10 1C (R10) and ratio of the

values at 15 and 5 1C (Q10). Two photosynthetic para-

meters (the ecosystem quantum yield a and the photo-

synthetic capacity Amax) were estimated annually from

the nonrectangular hyperbolic NEP light response curve:

NEP ¼aQþ Amax �

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiðaQþ AmaxÞ2 � 4ayAmaxQ

q2y

R;

ð4Þ

Fig. 1 Normalized night-time ecosystem respiration (R) as a function of friction velocity (u*) over a period of 2004–2005. Normalized R

is the ratio of observed values to modeled ones using a logistic model. The vertical line represents the u*

threshold of 0.1, 0.1, 0.25, and

0.25 m s�1 for HJP02, HJP94, HJP75, and OJP, respectively.

1478 T . Z H A et al.

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where y was fixed at 0.98 on the basis of curve fitting at

all sites.

Growing-season length (GSL) was defined based on

the daily mean GEP time series. The GSL was defined as

the time period between first and last occurrence of

3 consecutive days when daily mean GEP, estimated for

daytime periods only, exceeded 5% of summertime

maximum GEP, determined as the 90% percentile of

May–September daily mean GEP.

Regression analysis was used to examine the relation-

ship between variables. The coefficient of variation (CV)

was used to characterize variability. Regression signifi-

cance was evaluated using the F statistic at a signifi-

cance level of 0.05. The uncertainty for annual fluxes

was estimated using the Monte Carlo bootstrapping

approach (Hagen et al., 2006; Dragoni et al., 2007), with

the Monte Carlo process (random sampling with repla-

cement, applied to half-hour data) repeated 2000 times.

The uncertainty was expressed as a 95% confidence

interval. A one-way analysis of variance (ANOVA) was

performed to compare differences in GEP and R among

stands and years (data used were daily means). All

statistical analyses were done using MATLAB (Version

7.5.0, The MathWorks, Natick, MA, USA).

Results

Photosynthetic and respiratory parameters across thechronosequence

The respiratory parameters R10 and Q10 derived from

Eqn (3) represented ecosystem respiration R at 10 1C

and the ratio of the R values at 15 and 5 1C, respectively.

Before fitting the model parameters, the R and Ts values

were averaged in time using blocks of 20 good data

points, representing periods of 1–10 days depending on

the number of missing data. Because the 20 points were

typically from several diurnal cycles, the resulting Q10

values represent seasonal rather than diurnal tempera-

ture sensitivity. R as measured directly by EC at night

was closely related to Ts at the 2 cm depth and fit Eqn (3)

well (r240.7, Po0.05; Fig. 2). R10 increased with in-

creasing stand age, being lowest for the HJP02 site (41%

of the OJP value, Table 2). Q10 was largest for OJP,

indicating that the mature stand had the highest sensi-

tivity of R to the seasonal cycle of soil temperature.

For the growing season (May–October), daytime NEP

fit Eqn (4) well for HJP94, HJP75, and OJP (r240.9,

Po0.05; Fig. 3). At HJP02, however, the relationship

was weak (r2 5 0.38, Po0.05). Among sites, HJP02 had

the lowest ecosystem quantum yield a (Table 2), 10% of

the OJP value in 2005. For the three forested stands, aranged from 0.006 to 0.009 mol mol�1. Amax was lowest

at HJP02 (6% of that at OJP), moderate at HJP94 (61% of

that at OJP), and highest for HJP75. The results showed

a rapid initial rise in Amax as the forest recovered

following harvesting. As the forest further developed,

Amax reached a maximum by 30 years and then declined

slightly by 90 years.

Seasonal variation in NEP

All sites were weak C sources in the cold season (Fig. 4).

The three forested sites (HJP94, HJP75, and OJP) were C

Fig. 2 Night-time ecosystem respiration (R) for a period of 2004–2005 as a function of soil temperature at 2 cm depth (Ts) for three

postharvest jack pine sites (HJP02, HJP94, HJP75) and one preharvest site (OJP). Data were binned into percentile classes, with a

minimum of 20 points per bin. Curves are fitted lines by Eqn (3). Closed circles are data points with low volumetric water content (VWC).

The solid line is fitted line with all data and the dotted line is one with the exclusion of low VWC data points.

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sinks in the early growing season (April–June), with C

uptake peaking in May (2005) or June (2004). All three

became near C neutral in July, August, and September.

In the growing season, HJP02 was the strongest C

source while HJP75 was the strongest C sink.

Unlike monthly NEP, which peaked in May or June,

monthly GEP and R were highest in July or August

when temperature was highest (Figs 4 and 5). The

spring months were characterized by long days, high

soil volumetric water content (VWC) and moderate air

temperature, which promoted GEP, and relatively low

Ts, which suppressed R (Fig. 5). Therefore, the R/GEP

ratio for forested sites was relatively small in early

spring and increased in late summer (Fig. 4). All four

sites showed a characteristic summer depression in

NEP, associated with warmer soils and increased soil

respiration.

C balance and its variation across stand age classes

Figure 6 shows annual C fluxes as a function of stand

age. In 2004 and 2005, HJP02 was a C source (NEP 5

�152 � 11 and �123 � 10 g C m�2, respectively), HJP94

a weak C sink (NEP 5 4 � 14 and 34 � 17 g C m�2,

Table 2 Ecosystem respiration at reference temperature of 10 1C (R10), temperature coefficient of ecosystem respiration (Q10),

ecosystem quantum yield (a), and photosynthetic capacity (Amax) for three postharvest (HJP02, HJP94, HJP75) and one preharvest

jack pine sites (OJP) over 2004–2005

HJP02 HJP94 HJP75 OJP

a (mol mol�1) Photosynthesis parameters from Eqn (4) 0.001 0.006 0.009 0.009

(0.000) (0.004) (0.004) (0.005)

Amax (mmol m�2 s�1) 0.39 3.69 6.62 6.07

(0.09) (0.12) (0.15) (0.17)

r2 0.39 0.98 0.99 0.98

R10 (mmol m�2 s�1) Using all data 1.16 1.71 2.23 2.79

Q10 2.84 2.99 3.04 3.38

r2 0.72 0.78 0.88 0.85

R10 (mmol m�2 s�1) After excluding data at low VWC (below the

10th percentile)

1.19 1.74 2.3 2.71

Q10 3.03 3.74 3.16 4.11

r2 0.73 0.83 0.87 0.86

r2 Relationship between respiration residual and VWC 0.01 0.15 0.09 0.11

P value 0.20 0.0002 0.0024 0.0000

r2 Relationship between respiration residual and VWC

after excluding low-VWC data

0.01 0.04 0.03 0.08

P value 0.29 0.07 0.08 0.0007

The coefficient of determination of the regression is signified by r2. P value is based on 5% significance level. VWC, volumetric water

content.

Fig. 3 Daytime net ecosystem production (NEP) during the growing season (from April to October) over a period of 2004–2005 as a

function of photosynthetically active radiation (Q) for three postharvest jack pine sites (HJP02, HJP94, HJP75) and one preharvest site

(OJP). Data were binned into percentile classes, with a minimum of 50 points per bin. Curves are fitted lines by Eqn (4).

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respectively), HJP75 a moderate C sink (NEP 5 67 � 27

and 79 � 29 g C m�2, respectively), and OJP a weak C

sink (NEP 5 7 � 28 g C m�2 and 36 � 30 g C m�2, re-

spectively). On the basis of 5 years of consecutive EC

measurements, the 10-year-old stand is C neutral or a

weak C sink (Fig. 6). The C compensation point (where

NEP recovers to C neutrality) occurs at about 10 years

following harvesting based both on the fitted line

(r2 5 0.91, Po0.05; Fig. 6) and the data themselves.

A clear contrast was observed in GEP and R during

stand development following harvesting (Fig. 6).

Although the youngest stand (HJP02) had the lowest

GEP and R, the postharvest reduction was far greater

for GEP than R. The three young stands had greater

differences in GEP (e.g. 14%, 52%, and 98% of the OJP

value for HJP02, HJP94, and HJP75 in 2004) than R (e.g.

41%, 52%, and 88% of the 2004 OJP value). The aver-

aged GEP for HJP75 was close to that for OJP, whereas

R was � 10% greater at OJP. The ratio of R to GEP was,

on average for 2004 and 2005, highest for HJP02 (2.51),

followed by HJP94 (0.95), OJP (0.96), and HJP75 (0.87).

Interannual variability

Annual NEP was larger in 2005 than in 2004 for all sites,

the result of a more sensitive response of GEP than R to

the longer growing season in 2005 (Fig. 6). Annual GEP

was 47%, 36%, 6%, and 4% higher in 2005 than 2004 for

HJP02, HJP94, HJP75, and OJP, respectively. In contrast,

annual R was 3%, 26%, and 4% higher in 2005 than 2004

for HJP02, HJP94, and HJP75, respectively, but 1% lower

for OJP.

There was significant interstand and interannual

variability in GEP and R (Po0.05, ANOVA). Mean annual

NEP from 2000 to 2005 ranged from �146 g C m�2 yr�1

at HJP02 to 28 g C m�2 yr�1 at OJP, whereas GEP ranged

from 89 g C m�2 yr�1 at HJP02 to 589 g C m�2 yr�1 at OJP

(Fig. 6). Table 3 compares interannual and intersite

variability in annual GEP, annual R, R10, Q10, Amax,

and a using the CV and the range, with the interannual

statistics derived for the two longest running sites

(HJP94 and OJP). For all variables, the range and CV

among sites were larger than those among years. Inter-

stand variability in GEP and R was almost an order of

magnitude greater than interannual variablity at OJP in

terms of CV. Both interstand and interannual variability

were larger for GEP than R (Table 3). The interannual

variability of all variables at OJP and HJP94 was greater

at the young site HJP94 than the mature site OJP,

reflecting the dramatic effects of leaf area recovery for

the young stand.

Fig. 4 Annual cycles of monthly net ecosystem productivity

(NEP), gross ecosystem photosynthesis (GEP), ecosystem re-

spiration (R), and ratio of R to GEP (R/GEP) for three post-

harvest jack pine sites (HJP02, HJP94, HJP75) and one preharvest

site (OJP) in years 2004–2005.

Fig. 5 Annual cycles of mean monthly photosynthetically ac-

tive radiation (Q), mean monthly soil temperature (Ts) at the 2 cm

depth, and mean soil volumetric water content (VWC) at 0–15 cm

depth, for three postharvest jack pine sites (HJP02, HJP94,

HJP75) and one preharvest site (OJP) in years 2004–2005.

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Uncertainty estimated using the bootstrapping meth-

od at the OJP site (2000–2005) ranged from 28 to

31 g C m�2 yr�1 for NEP, 33 to 38 g C m�2 yr�1 for GEP,

and 17 to 20 g C m�2 yr�1 for R. Among the four sites

in 2005, uncertainty ranged from 10 to 30 g C m�2 yr�1

for NEP, 10 to 36 g C m�2 yr�1 for GEP, and 9 to

17 g C m�2 yr�1 for R. Both intersite and interannual

variability in annual flux were larger than the corre-

sponding uncertainty ranges, indicating that there was

significant interstand and interannual variability in

NEP, GEP, and R.

Factors affecting interannual variation in NEP

Annual NEP increased with GSL at the two longest

running sites, but the relationship was not statistically

significant at the 5% level (Fig. 7). Annual NEP in-

creased by � 1 g C m�2 (OJP) and 2 g C m�2 (HJP94)

for each additional day in the growing season. GSL

explained � 22% and 95% of interannual variation in

NEP at OJP and HJP94, respectively. GSL varied among

years by 50 days at HJP94 and 39 days at OJP, but for

any given year, was similar among stands (the max-

imum difference was 11 days; Table 4). Interannual

variation in GSL was influenced more by the GEP onset

date, which varied from day 97 (2005) to day 130 (2002)

at HJP94, than the ending date, which varied from day

288 (2002) to day 305 (2005). Interannual variation in

GEP was more sensitive to GSL for the young stand

than the old stand (Fig. 7). The interannual variability of

the onset date may have contributed to the positive

effects of GSL on NEP, because of the high NEP values

Fig. 6 Annual net ecosystem production (NEP), gross ecosys-

tem photosynthesis (GEP), ecosystem respiration (R), and the R/

GEP ratio for three postharvest jack pine sites (HJP02, HJP94,

HJP75) and one preharvest site (OJP) for all measurement years,

as functions of stand age. The fitted curve is described by

y 5�192.536�0.00199x2.5 1 81.17 ln(x), r2 5 0.91, Po0.05. The

R/GEP ratio is plotted logarithmically. The last data point of

each site represents the value for 2005. The error bars represent

the 95% confidence interval obtained using a Monte Carlo boot-

strapping approach with 2000 sampling repetitions. The asterisk

symbols are the annual NEP values from Howard et al. (2004).

Table 3 Coefficient of variation (CV) and range in gross

ecosystem photosynthesis (GEP) (g C m�2 yr�1), ecosystem

respiration (R) (g C m�2 yr�1), ecosystem respiration at a re-

ference temperature of 10 1C R10 (mmol m�2 s�1), temperature

coefficient of ecosystem respiration Q10, ecosystem quantum

yield a (mol mol�1), and photosynthetic capacity Amax

(mmol m�2 s�1) among four stands (HJP02, HJP94, HJP75,

and OJP) for years 2004 and 2005, and among years for

HJP94 and OJP

Interstand variation

Interannual variation

(2004–2005)

2004–2005 2004 2005

HJP94

(2001–2005)

OJP

(2000–2005)

Range CV CV Range CV Range CV

GEP 486 0.54 0.46 165 0.19 118 0.06

R 327 0.35 0.30 99 0.11 62 0.04

R10 1.54 0.34 0.24 0.97 0.25 0.87 0.10

Q10 1.09 0.14 0.20 1.63 0.18 1.09 0.10

a 0.008 0.58 0.48 0.004 0.54 0.002 0.07

Amax 6.25 0.64 0.53 2.55 0.28 0.97 0.06

Range is the difference between maximum and minimum.

Fig. 7 Annual net ecosystem production (NEP) as a function of

growing-season length (GSL). The lines are fitted line from

regression equations for HJP94 (y 5�389 1 2.0x, r2 5 0.95,

P 5 0.005) and OJP (y 5�172 1 1.1x, r2 5 0.22, P 5 0.347).

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in spring. Large variations were observed in annual

mean temperature (Ta) and total precipitation (Table 4).

Annual NEP was higher in warm years than in cold

years. No significant interannual variation was ob-

served for monthly mean Q (P 5 0.33, ANOVA).

The effect of temperature on interannual variability

was analyzed by linear regression of monthly NEP, GEP

and R against monthly mean soil temperature Ts over 6

years for the OJP site (Fig. 8). The relationships were

strongest in spring and were often significant at the 5%

level, despite the limited number of data points. Both

GEP and R were linearly and positively related to Ts

early in the growing season (April–May; r240.70,

Po0.05). However, warm soil temperatures in April

and May caused GEP to increase more than R, with

larger slope for GEP than for R, leading to a positive

relationship between NEP and Ts. As Ts warmed to

above 10 1C, GEP tended to plateau whereas R contin-

ued to increase (Fig. 8), resulting in a negative summer

response of NEP to Ts. In June, the relationship between

monthly Ts and R was significant (r2 5 0.83, P 5 0.012),

but the relationships between monthly Ts and GEP and

monthly Ts and NEP were not (r2o0.5, P40.05). During

and after June, the data showed a negative response of

NEP to Ts although the monthly relationships were not

significant at the 5% level. No significant relationships

were found between monthly mean VWC and either

monthly GEP or R for any month (P40.05). The key

factor controlling interannual variability in NEP thus

appears to be early growing-season temperature via the

differential impacts on R and GEP.

Discussion

Effect of low VWC on respiratory parameters

We evaluated the effect of low VWC on R10 and Q10 by

excluding low-VWC data (closed circles in Fig. 2) from

the model fitting (dotted lines in Fig. 2). The VWC

exclusion threshold was delineated by: (1) fitting the R

models to all data (solid lines in Fig. 2), (2) plotting the

model residuals against VWC (solid lines in Fig. 2), (3)

identifying a VWC threshold from (2) (the 10th VWC

percentile), (4) excluding data below the VWC thresh-

old and refitting the R models (dotted line in Fig. 2).

Without this exclusion, Q10 was biased low by the

confounding influence of the soil VWC (Fig. 2), which

is negatively correlated with Ts. The effectiveness of this

procedure was confirmed by the consistent, significant

positive relationships (Po0.05) between R residues and

VWC from step 2 at all sites but HJP02 where R was

independent of VWC, and by the insignificance (or

increased P value for OJP, Table 2) of these relationships

after the low-VWC data were excluded. The low-VWC

Table 4 Annual net ecosystem production (NEP), onset of growing season (GS), and growing-season length (GSL) for HJP94 and

OJP, and mean air temperature (Ta, 28 m above the ground), total photosynthetically active radiation (Q) and annual precipitation (P)

at OJP, 2000–2005

NEP

(g C m�2 yr�1)

Onset of GS

(day of the year) GSL (days)

Q (OJP)

(kmol m�2 yr�1)

Ta(OJP) ( 1C)

HJP94 OJP HJP94 OJP HJP94 OJP yr�1

April–

May

P (OJP)

(mm)

2000 68 108 189 8.27 1.3 2.8 379

2001 �32 43 114 108 179 184 8.92 3.1 3.8 307

2002 �67 �15 130 118 158 169 8.58 0.4 0.7 429

2003 �16 28 110 109 191 193 8.44 1.2 2.9 262

2004 4 8 117 96 188 193 8.02 �0.2 1.5 721

2005 34 36 97 97 208 208 8.11 1.8 2.5 624

Fig. 8 Interannual variation in the relationship between mean

monthly soil temperature (Ts) and mean monthly NEP, GEP, and

R for OJP from 2000 to 2005 (March–September). Lines are fitted

line with significant relationship (Po0.05).

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data exclusion had little ( 1 2–3%) effect on R10 but

increased Q10 by 7% at HJP02, 25% at HJP94, 4% at

HJP75 and 22% at OJP (Table 2). Low VWC occurred

almost exclusively in late summer at high Ts (see closed

circles in Fig. 2). Thus, R was suppressed by summer

drought. However, this suppression was minor, as seen

in the small r2 values (o0.2; Table 2) for the relationship

between the R residual and VWC for all sites. Tempera-

ture was the dominant factor controlling respiration,

explaining over 70% variations in R, as shown in Fig. 2

and Table 2. The logistic model [Eqn (3)], as used in the

FCRN gap-filling method, fit the data set well at these

sites (r240.7). The minor effects of seasonal variations

in VWC on NEP, GEP and R were well captured by the

FCRN moving-window gap-filling method (Barr et al.,

2004; Amiro et al., 2006), so that the dependence of these

fluxes on VWC are fully accounted for in the gap-filled

estimates of monthly and annual NEP, GEP and R. In a

comparison analysis of 15 current gap-filling techniques,

Moffat et al. (2007) showed that the FCRN method was

among the techniques with good overall performance.

Seasonal variation in NEP

The seasonal pattern in NEP reflected the combined

effect of PAR, Ta, Ts, VWC and shoot emergence on GEP

and R. In the spring, GEP was more sensitive to the

initial warming to above freezing temperatures than

R, causing a decrease in R/GEP and an increase in NEP.

The response of NEP to early growing-season Ts re-

sulted from the � 6-week lag between the annual Q

and Ts cycles (Fig. 5). The beginning and end of the

growing season (GS) had similar air temperatures but Q

was twice as high at the beginning than the end.

Consequently, GEP was higher early in the growing-

season whereas R had similar values early and late in

the GS, so that days added to the GS in spring had a

greater impact on NEP than days added in fall.

All four sites showed a characteristic summer suppres-

sion in NEP, associated with warm soils and low soil

moisture (Figs 4 and 5). The low NEP values in July 2004

and July–August 2005 may reflect the greater sensitivity

of R than GEP to soil warming, the greater sensitivity of

GEP than R to soil water stress, or both. Grant et al. (2007)

reported similar results as simulated by the ecosystem

model ecosys (Grant, 2001). The decrease in NEP during

summer (primarily in August) is characteristic of boreal

coniferous forests (Zha et al., 2004; Black et al., 2005;

Dunn et al., 2007; Barr et al., 2007; Bergeron et al., 2007).

C balance and its variation across stand age classes

The annual NEP vs. stand age pattern from this study

(Fig. 6) is very similar to the previous biometric esti-

mates of Howard et al. (2004), measured at three of the

study sites (HJP94, HJP75, and OJP) and two additional

sites, harvested in 1998 and 1989. The Howard et al.

(2004) estimates for NEP were derived by combining

biometric measurements with estimated heterotrophic

respiration. The Howard et al. (2004) estimates were

�190 � 70 (1-year stand), �40 � 60 (HJP94 at 5 years),

40 � 90 (10-year stand), 40 � 100 (HJP75 at 24 years),

and �20 � 70 g C m�2 yr�1 (OJP at 84 years) (shown as

asterisks in Fig. 6). However, the EC NEP estimates

have much lower uncertainty (e.g. 10–30 g C m�2 yr�1 in

2005; Fig. 6), increasing our confidence in the C balance

trajectory with stand age following harvesting. The NEP

pattern shown here is consistent with the NPP pattern

observed across similar jack pine stands, where NPP

increased linearly for approximately the first 15 years

then peaked and leveled off approximately 30 years

following disturbance (Howard et al., 2004). The similar-

ity between the postharvest NEP and NPP trajectories

indicates that the effect of stand age on NEP was domi-

nated by photosynthesis and autotrophic respiration.

The C compensation point of � 10 years in this study

is comparable with that of other boreal coniferous

stands: 12 years for a Scots pine chronosequence follow-

ing harvesting (Kolari et al., 2004), 11–19 years for a

black spruce chronosequence following wildfire (Litvak

et al., 2002; Bond-Lamberty et al., 2004), and 10–20 years

for ponderosa pine stands after clear-cutting (Law et al.,

2001). It is earlier than the C compensation point of

� 20 years for postharvest temperate coastal Douglas-

fir stands (Humphreys et al., 2006). The range of annual

NEP along this chronosequence ( � 250 g C m�2 yr�1) is

smaller than the range reported for ponderosa pine

(� 400 g C m�2 yr�1; Law et al., 2003) and Douglas fir

(� 1000 g C m�2 yr�1; Humphreys et al., 2006), but si-

milar to that simulated for boreal black spruce

(� 300 g C m�2 yr�1; Bond-Lamberty et al., 2006) and

boreal jack pine (� 250–300 g C m�2 yr�1; Grant et al.,

2007). The relatively small range along the boreal jack

pine chronosequence is associated with low site pro-

ductivity. The chronosequence in this study does not

include an intermediate-aged stand of � 50 years be-

cause intensive harvesting in this area is limited to the

recent past. However, the data in Fig. 6 may suggest that

NEP for jack pine stands following harvesting peaks at

an intermediate age of � 50 years (Fig. 6), although we

need additional data to support this. We recommend

that the measurement gap at intermediate stand ages be

filled in future jack pine chronosequence research.

The variation in NEP at the four stages of stand

development reflects the impacts of clear-cut harvesting

on GEP and R. Harvesting removed the forest overstory

and much of the understory, resulting in low posthar-

vest GEP at the HJP02 site. As the stand developed from

newly harvested to intermediate age, GEP recovered

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rapidly, driven by the recovery of leaf area index, from

0.18 at HJP02 to 0.8 at HJP94 to 3.1 at HJP75 (Table 1).

Like GEP, R increased as the stand regenerated, but at a

slower rate. Therefore, GEP dominated the changes in

NEP with stand age before canopy closure. The subtle

decrease in NEP in the late stage of stand development

was due to increasing R. The sharp decrease in the R/

GEP ratio during the early successional stage (Fig. 6)

and the slight increase during later stand development

further indicates that GEP played a dominant role in

NEP change among the stands in the early stage of

stand development following harvesting, whereas the

changes in NEP in the late stage resulted primarily from

increasing R. This pattern is also supported by the

relative changes in Amax and R10 for different stages of

stand development (Tables 2 and 3). We conclude that

the trajectory of NEP during stand development follow-

ing harvesting was dominated by increasing GEP during

forest regeneration and increasing R during maturation.

The concurrent increase in R with stand age may have

been mainly driven by increasing autotrophic respira-

tion (Ra) via root system development and increasing

above ground biomass (Howard et al., 2004; Litton et al.,

2007). To determine how heterotrophic respiration (Rh)

likely varied with stand age, Ra and Rh at each site were

estimated assuming a constant NPP/GEP ratio of

� 0.45 (Waring et al., 1998; Law et al., 2001). The

resulting Rh values showed only small variation with

stand age, from 181 g C m�2 yr�1 at HJP02 to 137, 186,

and 240 g C m�2 yr�1 at HJP94, HJP75 and OJP, respec-

tively. At all sites, the Rh values in the 2 measurement

years were similar. The overall CV for annual Rh among

sites and years was 16%. In contrast, the estimates of Ra

showed a sixfold increase across the different stand

stages, from 52 g C m�2 yr�1 at HJP02 to 320 g C m�2 yr�1

at OJP. The Ra/R ratio increased from 22% for HJP02 to

58% and 63% for HJP94 and HJP75, respectively, and

then decreased to 57% for OJP. The larger variation in

Ra than Rh across stand development is consistent

with estimates of Rh and Ra from equation: Rr0.5 5

�7.97 1 0.93Rs0.5 of Bond-Lamberty et al. (2004), where

Rr and Rs denotes root and soil surface respiration,

r2 5 0.87, Po0.001, based on Rs from Howard et al.

(2004). The resulting estimates for the four respective

sites are 198, 250, 367, and 245 g C m�2 yr�1 for Rh and

37, 115, 144, and 312 g C m�2 yr�1 for Ra.

Interstand and interannual variability in GEP and R

Interstand variability in GEP and R was greater than

interannual variability, indicating that the C balance at

the landscape scale was dominated by disturbance

history and the resulting stand age-class distribution

(Kurz & Apps, 1995; Kowalski et al., 2004). Both inter-

stand and interannual variability were greater for GEP

than R, confirming that GEP was the main determinant

of variability in NEP. This result was further supported

by the contrast in the strong annual NEP vs. GEP

relationship at OJP (r2 5 0.71, P 5 0.04) vis-a-vis the very

weak NEP vs. R relationship (r2 5 0.07, P 5 0.62). Similar

results were reported for a deciduous boreal forest (Barr

et al., 2002), but not for European forests or an Ontario

peatland (Valentini et al., 2000; Bubier et al., 2003).

The interannual range and CV of all variables in Table

3 was larger for HJP94 than OJP, showing that inter-

annual variability was larger for the young stand than

the mature stand. This difference resulted from the

significant annual increases in leaf area with stand

development in the young stand, which likely led to a

greater interannual variation in photosynthesis and

autotrophic respiration. This inference is supported by

the rapid decline in the R/GEP ratio observed at HJP94

(Fig. 6), where photosynthesis was increasing more

rapidly than respiration.

The result that interannual variation in GEP and R

was positively and significantly affected by the varia-

tion in early spring temperature (Po0.05; Fig. 8) sug-

gests that interannual variation in early spring

temperature controls NEP. The importance of early

spring temperature in interannual variation in NEP

was reported previously (Black et al., 2000; Saigusa

et al., 2002). The finding that annual NEP increased

with GSL is consistent with published results (Hum-

phreys et al., 2006). Conversely, no correlation between

longer growing seasons and net uptake was found in a

boreal black spruce forest (Dunn et al., 2007), possibly

because of offsetting increases in ecosystem respiration.

There was an obvious trend of NEP increasing with

increasing GSL, although the regression relationship in

the present study was not statistically significant at the

0.05 significance level for OJP due to only 6 years of data.

Studies of the C dynamics following harvesting that

use sites of different ages have been criticized for a lack

of replication at each stand age. In this study, the biases

that arise from the lack of replication were minimized

by carefully selecting the sites to be uniform in their

nonvegetation characteristics and to represent the typi-

cal stages of development following harvesting (Table

1). We believe that the measurements accurately reflect

the C balance at different stages following harvesting.

Summary

1. Following clear-cutting, a boreal jack pine forest in

central Canada changed from a C source at 2 years

after harvesting (HJP02) to a weak C sink or neutral

at � 10 years (HJP94), a C sink at 30 years (HJP75),

and a weak C sink or C-neutral at 90 years.

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2. The rapid recovery of NEP with stand age following

harvesting was caused by a rapid rise in LAI and

GEP (up to 30 years). As the stand further matured, a

slight decrease in NEP resulted from increasing R.

3. Seasonally, NEP was highest in late spring (May and

June), while ecosystem photosynthesis (GEP) and eco-

system respiration (R) peaked in midsummer (July).

4. The trajectories of GEP and R with stand age follow-

ing harvesting were related to changes in R10, Amax,

and a. Photosynthetic capacity (Amax) was lowest in

the youngest stand, increased through stand ages of

10–29 years, and then declined somewhat at an age

of 90 years.

5. The 10-year-old stand had larger interannual varia-

bility than the 90-year-old stand in GEP and R. At

both stands, interannual variation in NEP was influ-

enced more strongly by GEP than R. The interannual

variation in NEP of these stands was driven mainly

by early growing season temperature.

6. For postharvest jack pine ecosystems, disturbance

history and the resulting stand age-class distribution

is a more important determinant of current NEP than

interannual variability.

Acknowledgements

We thank Dell Bayne, Charmaine Hrynkiw, Erin Thompson, JoeEley, Bruce Cole, Steve Enns, and Alison Theede, who oversawthe meteorological measurements and data management; An-drew Sauter, Rick Ketler, Don Zuiker, Sheila McQueen, DanFinch, and Werner Bauer, who provided laboratory, field anddata management support for the flux measurements; ThierryVarem-Sanders, who measured the site characteristics; and BarryGoodison and Bob Stewart, who championed the BERMS pro-gram. Financial support was provided by the Climate ResearchDivision of Environment Canada, the Canadian Forest Service,Parks Canada, the Action Plan 2000 on Climate Change, theProgram of Energy Research and Development, the ClimateChange Action Fund, the Natural Sciences and EngineeringResearch Council of Canada, the Canadian Foundation forClimate and Atmospheric Sciences, BIOCAP Canada, and theNational Aeronautics and Space Administration.

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