Impact of severe dry season on net ecosystem exchangein the Neotropical rainforest of French Guiana

D A M I E N B O N A L *, A L E X A N D R E B O S C w , S T E P H A N E P O N T O N z, J E A N - Y V E S G O R E T *,

B E N O I T B U R B A N *, PA T R I C K G R O S S z, J E A N - M A R C B O N N E F O N D w , J A N E L B E R S § ,

B E R N A R D L O N G D O Z z, D A N I E L E P R O N } , J E A N - M A R C G U E H L z and A N D R E G R A N I E R z*INRA, UMR Ecologie des Forets de Guyane, BP 709, 97387 Kourou Cedex, French Guiana, wINRA, UR Ecologie Fonctionnelle

et Physique de l’Environnement, Domaine de la Grande Ferrade, 71 avenue Edouard Bourlaux – BP 81, 33883 Villenave-d’Ornon

Cedex, France, zINRA, UMR Ecologie et Ecophysiologie Forestieres, 54280 Champenoux, France, §Alterra – Green World Research,

PO Box 47, 6700 AA Wageningen, The Netherlands, }UMR Ecologie et Ecophysiologie forestieres, Faculte des Sciences, Universite

Henri Poincare-Nancy 1, BP 239, 54506 Vandoeuvre, France

Abstract

The lack of information on the ways seasonal drought modifies the CO2 exchange

between Neotropical rainforest ecosystems and the atmosphere and the resulting carbon

balance hinders our ability to precisely predict how these ecosystems will respond as

global environmental changes force them to face increasingly contrasting conditions in

the future. To address this issue, seasonal variations in daily net ecosystem productivity

(NEPd) and two main components of this productivity, daily total ecosystem respiration

(REd) and daily gross ecosystem productivity (GEPd), were estimated over 2 years at a flux

tower site in French Guiana, South America (511605400N, 5215404400W). We compared

seasonal variations between wet and dry periods and between dry periods of contrasting

levels of intensity (i.e. mild vs. severe) during equivalent 93-day periods. During the wet

periods, the ecosystem was almost in balance with the atmosphere (storage of

9.0 g C m�2). Seasonal dry periods, regardless of their severity, are associated with higher

incident radiation and lower REd combined with reduced soil respiration associated with

low soil water availability. During the mild dry period, as is normally the case in this

region, the amount of carbon stored in the ecosystem was 32.7 g C m�2. Severe drought

conditions resulted in even lower REd, whereas the photosynthetic activity was only

moderately reduced and no change in canopy structure was observed. Thus, the severe

dry period was characterized by greater carbon storage (64.6 g C m�2), emphasizing that

environmental conditions, such as during a severe drought, modify the CO2 exchange

between Neotropical rainforest ecosystems and the atmosphere and potentially the

resulting carbon balance.

Nomenclature:

Amax 5 Maximum photosynthetic rate (calculated coefficient)

c0 5 Fluctuations in CO2 concentration

ENSO 5 El Nino Southern Oscillation

Fc 5 CO2 eddy flux (Fco0 denotes ecosystem uptake)

GEE 5 Gross ecosystem exchange (30-min)

GEP 5 Gross ecosystem productivity

GEPd 5 Daily gross ecosystem productivity

h 5 Height above the ground surfaceITCZ 5 Inter-Tropical Convergence Zone

k 5 Initial slope of the photosynthetic curve (calculated coefficient)

NEE 5 Net ecosystem CO2 exchange (30 min) (NEEo0 denotes ecosystem

uptake)

Correspondence: Damien Bonal, tel. 1 (594) 594 32 92 87,

fax 1 (594) 594 32 43 02, e-mail: damien.bonal@kourou.cirad.fr

Global Change Biology (2008) 14, 1917–1933, doi: 10.1111/j.1365-2486.2008.01610.x

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd 1917

NEP 5 Net ecosystem productivity (NEPo0 denotes ecosystem uptake)

NEPd 5 Daily net ecosystem productivity (NEPdo0 denotes ecosystem uptake)

PAI 5 Plant area index

PPFD 5 Photosynthetic photon flux density

PPFDd 5 Daily photosynthetic photon flux density

RE 5 Total ecosystem respirationREd 5 Daily total ecosystem respiration

Sc 5 Rate of change in canopy storage (Sc40 denotes storage in ecosystem)

SR 5 Soil respiration

SRd 5 Daily soil respiration

SWC 5 Volumetric soil water content

SWCd 5 Daily volumetric soil water content

SWCnz 5 Soil water content measurements for tube n at depth zu* 5 Friction velocity

VPD 5 Vapour pressure deficit

VPDd 5 Daytime vapour pressure deficit

w0 5 Fluctuations in vertical wind velocity

wSWCd 5 Daily weighted soil water content

wzn 5 Weighting coefficient for tube n at the depth zz 5 Depth in soil

Keywords: dry season, ecosystem respiration, eddy covariance, gross ecosystem productivity, Neotro-

pical rainforest, net ecosystem productivity, soil drought, solar radiation

Received 19 June 2007; revised version received 5 December 2007 and accepted 28 December 2007

Introduction

The role undisturbed Neotropical rainforest ecosystems

play in the amount of carbon exchanged between the

atmosphere and the biosphere has been a subject of

great debate for more than a decade. The first analyses

conducted in the 1990s on direct CO2 flux measure-

ments (Grace et al., 1995a, b, 1996; Malhi et al., 1998,

1999) using the eddy covariance technique (Aubinet

et al., 2000; Baldocchi, 2003) suggested that these eco-

systems were major carbon sinks. However, recent

measurements (e.g. Saleska et al., 2003) or the re-analy-

sis of already-existing flux data (Kruijt et al., 2004; Sierra

et al., 2007) now lead us to believe that the assessment of

these forest ecosystems as large carbon sinks is not so

clear-cut. Other approaches based on either inventory

plots (e.g. Clark, 2002; Baker et al., 2004), modelling of

the functioning of ecosystems (Tian et al., 1998) or the

inverse modelling of atmospheric CO2 fluxes (Ciais

et al., 2005) reinforced this uncertainty.

At the heart of this issue is the fact that variations in

climatic conditions are now being taken into considera-

tion in these analyses. These variations include inter-

annual environmental changes, particularly the El Nino

Southern Oscillation (ENSO) event, and the alternating

dry/rainy seasons (whose intensities might also de-

pend on ENSO events). Such climatic variations affect

the canopy structure and the flux in total ecosystem

respiration (RE) and gross ecosystem productivity

(GEP), the two components of the net ecosystem pro-

ductivity (NEP), leading to contrasting seasonal varia-

tions in the carbon balance in these regions (Grace et al.,

1995a, b, 1996; Malhi et al., 1998; Williams et al., 1998;

Araujo et al., 2002; Carswell et al., 2002; Loescher et al.,

2003; Saleska et al., 2003; Goulden et al., 2004; Meir &

Grace, 2005; Hutyra et al., 2007). A decrease in RE

during dry periods (months with o100 mm precipita-

tion) related to decreases in both heterotrophic soil

respiration (SR) and litter decomposition has been

described as having a mainly positive effect on NEP

(greater negative values) (Tian et al., 2000; Vourlitis et al.,

2001, 2004; Araujo et al., 2002; Goulden et al., 2004;

Hutyra et al., 2007). In contrast, a decrease in GEP

associated with hydraulic limitations to water transfer

in soil, roots, stems and leaves (Malhi et al., 1998;

Vourlitis et al., 2001, 2004; Goulden et al., 2004; Meir &

Grace, 2005) or a decrease in total ecosystem leaf area

(Vourlitis et al., 2001, 2004; Carswell et al., 2002; Goulden

et al., 2004; Meir & Grace, 2005; Hutyra et al., 2007) have

a negative impact on NEP (lesser negative values)

during dry periods. It has been suggested that the

environmental conditions that best explain differences

in NEP between wet and dry periods are the amount of

precipitation during the dry period (Tian et al., 2000),

the variation in cloud cover that leads to a variation in

total solar radiation (Nemani et al., 2003; Goulden et al.,

1918 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

2004; Ichii et al., 2005) and differences in vapour pres-

sure deficit (VPD) (Williams et al., 1998). In contrast, the

lack of seasonal variations in NEP was usually inter-

preted as evidence that tree roots attain deep soil layers

where soil water content remains high even during the

driest months (Da Rocha et al., 2004; Goulden et al.,

2004; Hutyra et al., 2007) or points to the potential

hydraulic redistribution at night by deep root systems

(Lee et al., 2005).

The problem today, however, is that most of the flux

measurements and carbon balance estimations that

have been made to date, with the exception of a study

undertaken in Mato Grosso, Brazil (Vourlitis et al., 2001,

2004; Priante-Filho et al., 2004), have been conducted in

regions where the dry season remains mild (i.e. less

than 2–3 months with o50 mm precipitation), whereas

most climate change scenarios predict an intensification

in the seasons (Trenberth & Hoar, 1997; Cox et al., 2000;

Neelin et al., 2006). In these Neotropical rainforest

ecosystems, the dry seasons will then become drier

and the rainy seasons wetter. Thus, as suggested by

Goulden et al. (2004), studying forest ecosystems that

are subjected today to contrasting amounts of soil water

content throughout the year might help to give us some

indication of the future response of Neotropical rain-

forest ecosystems to climatic changes and the resulting

carbon balance.

To that end, in 2003 a monitoring site, known as the

‘Guyaflux’ experimental site, was set up in an undis-

turbed tropical rainforest in French Guiana to examine

seasonal variations in the climate and their influence on

the carbon balance in these ecosystems. The Guyaflux

site is located in an area where annual rainfall is high

(3041 mm on the average over the past decade) and

severe seasonal dry periods (at least 4 consecutive

months with o50 mm precipitation) occur every 2–3

years, in association or not with ENSO events (Meteo

France, personal communication). These periods result

in a sharp decrease in the amount of soil water available

in the upper soil layers and could induce a water-

related stress to the trees (Guehl, 1984). Based on data

collected during a mild dry period in 2004 vs. those

collected during a severely dry season in 2005, we

sought to answer the following questions:

� Are there seasonal variations in daily NEP (NEPd) in

the Neotropical rainforest in French Guiana?

� Does the intensity of the seasonal dry periods (mild

vs. severe) influence daily NEPd and its carbon

balance over these periods?

� Are the main components of NEPd (i.e. daily total

ecosystem, REd, and daily gross ecosystem produc-

tivity, GEPd) affected by seasonal variations in cli-

matic conditions and their intensity?

� Which environmental parameters explain these

variations?

Materials and methods

Study site

This study was conducted in French Guiana, South

America (511605400N, 5215404400W; Fig. 1) where the

climate is tropical wet, mainly driven by the north/

south movement of the Inter-Tropical Convergence

Zone (ITCZ). This zone brings heavy rains when it is

above French Guiana (December–February and April–

July); it leads to a short, dry period (March) when

located south of French Guiana and a long, dry period

(August–November) when located to the north (Fig. 2).

The severity of this long, dry period is highly variable

from year to year. Some long, dry periods remain mild

(e.g. in 2004), with 50–100 mm precipitation each

month, whereas some dry periods are severe (e.g.

in 2005), with 4 months with o50 mm precipitation

(Fig. 2).

Over the past decade, the average annual rainfall at

the study site (Paracou field station, Gourlet-Fleury

70° 60°80° 50° 40°

10°

0°

10°

20°

30°

W

Fig. 1 Location of the Guyaflux experimental unit, French

Guiana (511605400N, 5215404400W; white triangle). The shaded area

corresponds to the Neotropical rainforest region. The black

triangles represent the main tropical rainforest sites with flux

tower measurements published so far. The grey triangle corre-

sponds to a transitional tropical forest site (Mato Grosso, Brazil)

subjected to strong seasonal dry periods (Vourlitis et al., 2001,

2004; Priante-Filho et al., 2004).

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1919

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

et al., 2004) was 3041 mm and the air temperature was

25.7 1C. The site is located in the northernmost part of a

region on the Guiana Plateau characterized by a succes-

sion of small, elliptical hills rising to 10–40 m a.s.l.,

sometimes associated with plateaus of similar altitude.

The soils are mostly nutrient-poor acrisol (FAO-ISRIC-

ISSS, 1998) with pockets of sandy ultisols developed

over a Precambrian metamorphic formation called the

‘Bonidoro series’ and composed of schist and sand-

stone, sporadically traversed by veins of pegmatite,

aplite and quartz. Given the latitude of the study site,

there is only a 30 min difference (greatest in May) in day

length between solstices, and extraterrestrial radiation

changes by 15% throughout the year. Unlike similar

data previously published on Amazonian sites (Fig. 1),

this flux tower site is located in the northern hemi-

sphere. Incident extraterrestrial radiation is at its high-

est in March and in September (i.e. at the early

beginning of the dry season, and decreases during the

long, dry period).

The Guyaflux experimental unit covers more than

400 ha of undisturbed forest. In 2003, a 55 m high self-

supporting metallic tower was built in the westernmost

part of the Guyaflux area in an existing, natural 100 m2

gap, and, thus, with a minimum of disturbance to the

upper canopy. This location enabled us to cover a range

of more than 1 km of undisturbed forest in the direction

of the prevailing winds. The top of the tower is about

20 m higher than the overall canopy and meteorological

and eddy flux sensors were mounted 3 m above the

tower. The ecosystem is considered to be pristine,

tropical wet forest. Tree density averages 620 trees ha�1

(diameter at breast height 40.1 m) and tree species

richness is about 140 species ha�1. Mean tree height is

35 m, with emergent trees exceeding 40 m. The fetch of

the flux-tower mainly covers a relief of large hills over

schist rock, a bottomland (50–100 m wide) with a small

(1 m wide) creek, and a transition zone between the hills

and a sandy plateau over migmatite rock. Drainage

characteristics of these soils are given in Epron et al.

(2006). Clay and sand content in the 1 m deep horizon

are 43.2% and 47.8% on top of the hills and 25.8% and

64.6% on the sandy plateau. To characterize the forest

structure and composition in the different zones, 10

0.49 ha inventory plots were set up in 2003.

Meteorological and flux data

Microclimate and eddy covariance data have been

recorded continuously since December 2003 using the

Euroflux methodology described in Aubinet et al.

(2000). We present here data from the years 2004 and

2005. Air temperature and humidity (HMP45, Vaisala,

Helsinki, Finland), bulk rainfall (ARG100, EM lmt,

Sunderland, UK), wind direction and speed (A05103-

5, Young, Traverse City, MI, USA), global and infrared

incident and reflected radiations (CNR1, Kipp & Zonen,

Bohemia, NY, USA), and incident and reflected photo-

synthetic photon flux density (PPFD; mmolphoton m�2 s�1)

(SKP 215; Skye Instruments Limited, Powys, UK) were

measured above the canopy. Atmospheric pressure

(144-SC-0811; SensorTechnics, Kaufbeuren, Germany)

was monitored in the cabin at the base of the tower.

Additionally, soil temperature (107; Campbell Scientific

Inc., Logan, UT, USA) and volumetric soil water content

(SWC; m3 m�3) using a frequency domain sensor

(CS615; Campbell Scientific Inc.) at 0.05 m depth were

recorded. All meteorological data were collected at

1 min intervals and compiled as 30 min averages or

sums with a CR23X datalogger (Campbell Scientific

Inc.). VPD (kPa) was calculated based on air tempera-

ture and humidity.

A 3-D sonic anemometer (R3-50; Gill Instruments,

Lymington, UK) was used to measure wind velocities

at each polar coordinate and sonic temperature. CO2

and H2O concentrations were monitored using an open-

path infrared gas analyser (Li7500, LI-COR Inc., Lin-

coln, NE, USA). The head of the gas analyser was

mounted 0.3 m from the head of the anemometer. As

the open-path gas analyser proved to be very sensitive

to rain, generating gaps in the data under rainy condi-

tions, a closed-path analyser (Li7000, LI-COR Inc.) was

added to the system in June 2005. Air near the head of

the 3-D anemometer was pumped at about 3.4 L min�1

into an 8 m long tube (diameter 4 mm, Teflon) and then

down into the gas analyser installed on a 52 m high

platform on the tower. The resulting time-lag was

typically 1.5 s. Eddy covariance data were sampled at

20 Hz frequency and downloaded using EDDYLOGP soft-

ware (Alterra, Wageningen, the Netherlands) on 256 MB

0

100

200

300

400

500

600

700

800

J F M A M J J A S O

2004200510-year average

Rai

nfal

l (m

m)

MonthsN D

Fig. 2 Average monthly rainfall in the years 2004 and 2005, and

for the past decade (11 SE).

1920 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

memory cards inserted into a HP200LX laptop (Hewlett

Packard, Palo Alto, CA, USA). Data were recorded

weekly and the proper functioning and cleanliness of

the instruments was ensured. The CO2 and H2O analy-

sers were recalibrated using N2 and CO2 reference gases

and a chilled mirror hygrometer (MTS-1; Walz, Effel-

trich, Germany) according to the manufacturers’ in-

structions, typically three to four times a year.

Because turbulent transfer is not always seen within

the ecosystem at night (e.g. calm nights), a CO2 profile

system was used to estimate the 30 min storage or

release of CO2 from the soil level to eddy flux instru-

ment (Aubinet et al., 2000). Atmospheric CO2 concen-

tration was analysed at six different heights (0.5, 6, 13,

23, 32 and 58 m) using a 0.8 L min�1 pump connected to

a six-line solenoid valve and an infrared gas analyser

(Li820, LI-COR Inc.). The system is operated by a

CR10X datalogger (Campbell Scientific Inc.) that re-

cords CO2 concentration data every 15 min.

Soil respiration was measured using a flowthrough,

non-steady-state chamber system multiplexing four

chambers set up in the vicinity of the tower

(i.e. � 100 m). The system started to record continuous

half-hourly measurements from May 3, 2005 with three

chambers only. A fourth chamber was added on June

22. The chambers are fully described in Jassal et al.

(2005). A CR10X datalogger (Campbell Scientific Inc.)

recorded the sequential operation of the chambers and

programmed to sample each chamber for 3.75 min every

half hour (consequently, the lid was kept open 87% of the

time for each chamber). The system measured the in-

crease in CO2 concentration in the headspace by circulat-

ing the air through Synflex 1300 tubing to a closed-path

CO2 infrared gas analyser (Li840; LI-COR Inc.). The flow

rate in the tubing was 2.5–3.0 L min�1 except in the gas

analyser loop where the diverted air circulated at

0.35 L min�1. The gas analyser was calibrated monthly

by sequentially using CO2-free nitrogen gas for the offset

calibration and a gas of known CO2 concentration (ca.

501mmol mol�1) for the gain calibration. Soil CO2 flux

was calculated by a linear regression of the 10 s time

average of the CO2 concentration starting after the first

40 s of measurement. Records characterized by coeffi-

cients of determination of the regression o0.99 were

discarded (i.e. o0.3% of the records).

Flux data processing and gap-filling

The net ecosystem CO2 exchange (NEE) for each 30 min

period was calculated based on the mass exchange

between the ecosystem and the atmosphere following

standard methodologies (Aubinet et al., 2000). NEE was

computed as the sum of CO2 eddy fluxes (Fc 5 covar-

iance between vertical wind velocity fluctuations,

w0, and fluctuations in CO2 concentration, c0) and the

rate of change in canopy storage (second term, Sc) every

30 min:

NEE ¼ w0c0 þ @

@t

Z58

0

cðhÞdh;

where t is the time and h is the height above the ground

surface. Because the vertical coordinate for wind velo-

cities is positive upward, positive values for fluxes

denote CO2 emission to the atmosphere by the ecosys-

tem and negative values denote uptake. Data were

processed with ALTEDDY V2.1 software (Alterra) using

the Euroflux methodology (Aubinet et al., 2000), includ-

ing standard data quality checks (Foken et al., 2004) and

corrections. We also applied the procedure detailed by

Reichstein et al. (2005) to determine the threshold of

friction velocity (u*) below which night-time NEE was

correlated with u*. Thirty-minute data were sorted

according to 0.05 m s�1 classes in u*. This threshold

was calculated as 0.15 m s�1 (Fig. 3) and night-time data

below this threshold were eliminated. This represented

54% of the available night-time data. Eliminated data

were distributed randomly over the night and then did

not induce any bias in night-time C flux estimations.

After all data quality checks were performed, the clean

raw data over the 2 studied years represented 78% and

36% of the 30 min values during daytime and night-

time, respectively. These percentages were 94% and 38%

when considering only the long, dry periods.

Assuming that daytime variations in total ecosystem

respiration are low (low diurnal air temperature ampli-

tude) and that diurnal ecosystem respiration equals

nocturnal respiration [see discussion in Reichstein

FcSc

−2

0

2

4

6

8

10

12

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7

NEEFcSc

Flu

x (µ

mol

CO

2 m

−2 s

−1)

Friction velocity (m s−1)

Fig. 3 The relationship between the CO2 eddy flux (Fc, * ), the rate

of change in canopy storage (Sc, �) or the net ecosystem exchange

(NEE, �) and friction velocity (u*) at night. The vertical dotted line

represents the threshold of u* (0.15 m s�1) below which night-time

NEE was correlated with u*, as determined following Reichstein

et al. (2005).

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1921

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

et al. (2005)], gross ecosystem exchange (GEE) for

each 30 min period was calculated as the difference

between the running mean of RE over 7 days obtained

from NEE values at night and NEE values for each

30 min period.

NEP was computed as the algebraic sum of NEE

values over a given period, mainly 24 h (then becoming

NEPd) or a season. To calculate NEP, missing data were

gap-filled using the following three procedures. (i)

Under dry air conditions, the correlations between

open- and closed-path analysers for CO2 and H2O

fluxes were high (typically with R240.92) and were

used to gap-fill the data from the open-path analyser

from June to December 2005 lost due to wet conditions

(typically rainy half-hours and the following hour). (ii)

Night-time data: air or soil temperature variations at

night are low and no significant empirical model could

be found to relate night-time NEE values with any other

environmental parameter. As such, commonly used

empirical models or look-up tables for data gap-filling

(Falge et al., 2001) could not be used here. Missing

night-time data were then gap-filled using the following

procedure, adapted from Van Dick & Dolman (2004).

For gaps smaller than 2 h in duration, half-hourly

values were estimated as the mean of the flux over

the 2 preceding and that over the 2 following hours for

the considered day and the days before and after. For

larger gaps, the flux was estimated as the mean of the

flux for this time of the night and for the 2 preceding

and 2 following hours over the 3 preceding and that

over the 3 following days, respectively. If the procedure

failed to produce an estimate, we consecutively used

the preceding and following 15, 30 and 60 days instead.

(iii) Daytime data: missing NEE data were gap-filled

using nonlinear multiple regression models that esti-

mated 30 min data as a function of 30 min averages of

PPFD and VPD for each homogeneous climatic period

(adapted from Falge et al., 2001). Meteorological data

covered the full 2004–2005 period, except for 2 days in

2005 (March 18–19) because of a datalogger breakdown.

These data were gap-filled using regressions obtained

with 30 min data from an automatic weather station

(Enerco 407, Cimel Electronique, Paris, France) installed

in grassland 10 km away from the tower. Errors asso-

ciated with these procedures might clearly affect the

absolute magnitude of the fluxes, but fluxes in different

seasons and years should be affected similarly and still

allow pertinent comparisons.

Missing SR values represented o5% of the 30 min

data. The following gap-filling procedure was applied

to each chamber individually. Short gaps (o6 h) were

filled by using a 6 h running mean. For longer gaps,

linear multiple regression models were used to gap-fill a

single chamber dataset from the three others (R2 ranged

from 0.61 to 0.79). No gaps were filled when missing

values concerned more than one chamber at a time.

Weighted soil water content

In July 2003, we set up twenty 3 m long Tecanats tubes

(SDEC France, Reignac, France; external diameter: 42 mm)

along a 1 km long transect that crosses the Guyaflux site

from the tower. The tubes were inserted into holes bored

using a 40 mm wide auger. They were sealed at the base

and could be opened at the top to insert a probe. In the

bottomland, the tubes could not be inserted deeper than

1.3 m because of the presence of the permanent water

table. Soil water content measurements (SWCnz) were

made every 0.2 m in each tube using a time domain

reflectometry probe (TRIME FM3; Imko, Ettlingen,

Germany) at a frequency of about 3 weeks.

To examine the possible impact of soil drought on the

functioning of the ecosystem, we characterized the

weighted soil water content (wSWC, m), which is

representative of the soil water content from the surface

to 2.4 m depth and covers the different soil types in the

Guyaflux area. For a given sampling date, wSWC was

calculated as follows:

wSWC ¼ 0:2�X

z

Xn

ðSWCzn � wznÞ" #

;

where 0.2 is the distance between two consecutive

measurements in each tube, SWCzn is the soil water

content (m3 m�3) recorded on this date for tube n at

depth z and wzn is a weighting coefficient for tube n at

the depth z. wzn takes into account the estimated area

represented by each soil type in the Guyaflux site

(putative average footprint of the eddy fluxes from

the tower) and the number of tubes in each soil type.

In order to estimate the daily wSWC (wSWCd), we used

an empirical regression between wSWC and the aver-

age of SWC measured at 0.05 m depth over the 5 days

before wSWC was measured. No SWCnz measurements

were made between May 27 and October 8, 2004

because of a breakdown in the probe.

Plant area index (PAI) and litter production

Plant area index in the 10 inventory plots was estimated

using two LAI2000 (LI-COR Inc.) during both the wet

and dry periods in 2005, the reference sensor placed on

top of the flux tower. Within each inventory plot, 35–45

randomly distributed measurements were made in the

morning before direct sunlight could reach the sensors.

To reduce the influence of standing trunks in the PAI

calculations, a 381 solid angle was chosen.

1922 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

Estimated litter production (Mg carbon ha�1 yr�1) in

the footprint of the flux tower was calculated based on

40 litter traps (0.67 m� 0.67 m 5 0.45 m2) placed 1.5 m

high above the ground at each corner of the 10 inven-

tory plots. Trap contents were collected on the same day

twice a month and oven-dried at 60 1C for 3 days before

being weighed to the nearest 0.1 g.

Data analysis

Based on daily rainfall and variations in wSWCd, we

defined two different periods (wet vs. long, dry period)

in each year with the same length (93 consecutive days).

We selected ‘Day of the Year’ (DOY) 90–182 for the wet

period and DOY 243–335 for the long, dry period.

The response of GEE to variations in PPFD during

different climatic periods was assessed using nonlinear,

least-square regressions from the SAS program (SAS

Institute, Cary, NC, USA) expressed as follows:

GEE ¼ Amax �PPFD

kþ PPFD;

where Amax and k are coefficients calculated using raw

GEE and PPFD data. Following this expression, Amax is

the maximum photosynthetic rate (mmolCO2 m�2 s�1)

and k is the initial slope of the photosynthetic curve

(mmolphoton m�2 s�1). Each parameter was associated

with a 95% confidence interval and the intercomparison

of the parameter estimates of a given period with the

intervals of the other periods allowed us to discuss

whether the fitted curves differed between the 2005

wet, and the 2004 and 2005 long, dry periods.

We calculated daily sums or averages of ecosystem

and environmental parameters (denoted by the sub-

script suffix ‘d’). Negative NEPd values denote CO2

uptake by the ecosystem from the atmosphere and

positive values carbon emission. GEPd and REd are both

positive. To compare variations in NEPd, GEPd and REd

over time during the long, dry periods, we calculated a

2-week running mean of the daily values (6 consecutive

days before and after the given date). To test the

influence of PPFDd on seasonal variations in GEPd or

REd, linear or nonlinear regression models (Vourlitis

et al., 2001; Granier et al., 2007) were fitted to our data.

Both the linear or nonlinear correlations between the

residuals from these functions and other environmental

variables (i.e. air temperature, wind speed or direction,

VPDd, wSWCd) were tested. We also tested the correla-

tion between NEPd and REd, and between the residuals

of this function and environmental variables, and be-

tween REd and SRd. All these tests were performed

either over the 2-year study period or over the above-

mentioned seasonal periods using SAS software (SAS

Institute).

Results

Seasonal variations in climatic conditions and standcharacteristics

Climatic conditions were characterized by the succes-

sion of wet and dry periods, associated with large

variations in mean daily air temperatures (22.9–

27.2 1C), daytime VPD (0.1–1.4 kPa) and total, daily

global radiation (0.9–26.5 MJ m�2 day�1) (Fig. 4). At

the end of the long, dry period, SWCd at the surface

was lower in 2005 than in 2004 (0.12 and 0:17 m3H2O m�3

soil)

(Fig. 5). The same pattern was observed at 2.4 m depth

(0.17 and 0:23 m3H2O m�3

soil). The decrease in wSWCd

during the 2005 long, dry period was sharper and fell

lower (0.38) than during the 2004 dry period (0.49).

Furthermore, wSWCd in 2005 was lower over a 45-day

period than the minimum values reached in 2004. In

2004, several sporadic rain events during the dry season

induced a succession of increases (and subsequent

decreases) in wSWCd that were not observed in 2005

(Fig. 5).

Daily average air temperature, VPDd and PPFDd

during the long, dry periods were higher than during

the wet season (Table 1), whereas atmospheric pressure,

wind direction, wind speed and soil temperature were

not different. The 2005 long, dry period was character-

ized by a strong deficit in cumulated precipitation as

compared with values averaged over the past 10 years

at this site (Fig. 2), whereas cumulated values during

the 2004 dry period were close to average (i.e. 2.5 times

more than in 2005), except in November. Except for

PPFDd (slightly higher in 2004 than in 2005), there were

no other significant differences in climatic parameters

between the long 2004 and 2005 dry periods.

Average litter production was 4.3 and 4.6 MgC ha�1 yr�1

in 2004 and 2005. The highest values occurred at the

beginning of the long, dry season in 2004 and in the

middle of the long, dry season in 2005 (Fig. 6). PAI did

not differ between the 2005 wet and long, dry periods

(7.0 � 0.2 and 6.9 � 0.3 m2 m�2, respectively) (Fig. 6).

Seasonal variations in CO2 fluxes

There were large seasonal variations in NEPd, GEPd and

REd in 2004 and 2005 (Fig. 7). Whatever the season,

NEPd values were both negative and positive, with

average values of �0.43 and �0.39 g C m�2 day�1 in

2004 and 2005, respectively. The lowest values were

found during the short, dry period in March

(� �4.20 g C m�2 day�1) and the highest during the

wet season (� 6.12 g C m�2 day�1). NEPd was positive

over 41.3% of the days during the 2005 wet period and

over 38.7% and 25.8% of the days during the 2004 and

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1923

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

2005 long, dry periods, respectively. When periods with

the same duration were compared, cumulated NEPd led

to higher carbon storage (more negative values) in the

ecosystem during the long, dry periods than during the

wet ones (Table 1).

In both years, there was a seasonal trend towards

higher REd and GEPd values during the transition

between the wet and the long, dry period and decreas-

ing values during the long, dry periods (Fig. 7).

The seasonal pattern of SRd paralleled REd, with wet

season values (� 3.5 g C m�2 day�1) intermediate be-

tween the highest fluxes of the transitional periods

(� 4.5 g C m�2 day�1) and the lowest fluxes of the long,

dry season (� 2.5 g C m�2 day�1) (Fig. 8). The observed

increase in SRd during the transitional period (Novem-

ber 26–December 16) was not transferred to REd.

0.0

0.1

0.2

0.3

0.4

j-04 a-04 a-04 d-04 a-05 a-05 d-050.0

0.2

0.4

0.6

0.8

1.0

−0.2 m −2.4 m wSWCdSW

Cd(m

3 H O

m3 so

l−1)

Date

wS

WC

d(m

)

Fig. 5 Seasonal variations in daily average soil water content

(SWCd, m3 m�3) at 0.20 m (�) and 2.40 m (�) depth and weighed

soil water content (wSWCd, m) (grey line). The wSWCd is

representative of the SWC from the soil surface to 2.4 m depth

and covers the spatial variations in soil types in the footprint of

the eddy fluxes in the Guyaflux experimental area (see ‘Materials

and methods’ for details on the calculations). The horizontal

black lines illustrate the periods (93 consecutive days in 2004 and

2005) considered in this study as the long, dry periods.

0

40

80

120

160

200R

ainf

all (

mm

day

−1)

0

5

10

15

20

25

30

Glo

bal r

adat

ion

(MJ

m−2

day−1

)

22

23

24

25

26

27

28

Air

tem

pera

ture

(°C

)(a)

(b)

(c)

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

j-04 m-04 m-04 j-04 s-04 n-04 j-05 m-05 m-05 j-05 s-05 n-05

Date

Vap

our

pres

sure

def

ict (

KP

a) (d)

Fig. 4 Seasonal variations (2004–2005) in daily (a) rainfall, (b)

global radiation, (c) air temperature and (d) daytime air vapour

pressure deficit at the Guyaflux experimental unit, French Guiana.

Each dot represents 1 day. The lines represent the running mean

(6 days before and 6 days after) of the parameters. The horizontal

black lines illustrate the periods (93 consecutive days in 2004 and

2005) considered in this study as the long, dry periods.

Table 1 Average values or sums of climatic parameters, litter

production, daily net ecosystem productivity (NEPd), daily

total ecosystem respiration (REd) and daily gross ecosystem

productivity (GEPd) during 93 consecutive days in the 2005

wet period [days of the year (DOY) 90–182] and in the 2004

and 2005 (DOY 243–335) long, dry periods

2004 2005 2005

Long, dry

period

Wet

period

Long, dry

period

Air temperature ( 1C) 26.4 25.7 26.6

Soil temperature ( 1C) 25.6 25.3 25.7

Wind direction (1) 116.7 116.1 108.1

Wind speed (m s�1) 2.8 2.6 2.9

Atmospheric pressure

(mbar)

1005.5 1006.3 1006.0

Rainfall (mm) 156.4 1473.4 66.8

VPDd (kPa) 1.10 0.65 1.11

PPFDd (molphoton m�2) 3888.6 2756.3 3677.1

Litter production

(MgC ha�1)

1.15 0.99 1.37

NEPd (g C m�2) �32.7 �9.0 �64.6

REd (g C m�2) 975.6 876.2 888.6

GEPd (g C m�2) 1008.4 885.2 953.2

1924 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

Contrasting patterns between mild and severe dry periods

During the long, dry periods, NEPd was highly variable

(Fig. 9a), mainly displaying negative values. In 2004,

NEPd remained stable until the middle of the dry

period (October 13), when it started to decrease. It

reached its minimum (more negative) values around

November 8 and sharply increased thereafter to reach

positive values by November 24. On the contrary, NEPd

decreased early during the 2005 long, dry period and

then increased until October 22. Another sharp decrease

occurred until November 8 when NEPd reached its

minimum values. After this date, NEPd increased,

nearly reaching positive values on December 1.

The REd was lower under severe (vs. mild) drought

conditions, except in the middle of the dry period when

values between the years were similar (Fig. 9b). At the

end of the long, dry period, the ratio of REd under

severe vs. mild drought conditions was 0.80. Mean-

while, lower GEPd values during severe drought con-

ditions were found only over the last third of the period

(from November 1) (Fig. 9c). At the end of the long, dry

periods, the ratio of GEPd under severe vs. mild

drought conditions was 0.82.

Seasonal, environmental monitoring of GEPd, REd

and NEPd

Daily photosynthetic photon flux density accounted

for 46% and 8% of the seasonal variation in GEPd

(Fig. 10) and REd (data not shown), respectively.

Residuals from this function with GEPd were not

correlated with any other variable (P 5 0.12), whereas

residuals from this function with REd were slightly

correlated with wSWCd and VPDd (R2 5 0.02,

P 5 0.003).

When only considering the long, dry periods, varia-

tions in GEPd in 2004 could not be explained by any

environmental variable (all P-values 40.10). Variations

in REd were only correlated with wSWCd (R2 5 0.09,

0

2

4

6

8

10

Litte

r pr

oduc

tion

(Mg

ha−1

yr−1

) P

lant

are

a in

dex

(m2

m−2

)

Date

Fig. 6 Seasonal variations (�1 SE) in average litter production

(�) calculated from 40 litter traps distributed over the 10 in-

ventory plots in the footprint of the flux tower at the Guyaflux

experimental unit, French Guiana. Additionally, the average

plant area index (PAI, m2 m�2, ^) during the 2005 wet (May

16–18) and long, dry (November 16–18) seasons was estimated

based on � 40 measurements within each inventory plot using

LAI2000 sensors. The horizontal black lines illustrate the periods

(93 consecutive days in 2004 and 2005) considered in this study

as the long, dry periods.

−6

−4

−2

0

2

4

6

8

Date

NE

Pd

(gC

m−2

day

−1)

(a)

0

2

4

6

8

10

12

14

16

RE

d (g

C m

−2 d

ay−1

)

Date

(b)

0

2

4

6

8

10

12

14

16

Date

GE

Pd

(gC

m−2

day

−1) (c)

Fig. 7 Seasonal variations (2004–2005) in (a) daily net ecosys-

tem productivity (NEPd, g C m�2 day�1), (b) daily total ecosys-

tem respiration (REd, g C m�2 day�1) and (c) daily gross

ecosystem productivity (GEPd, g C m�2 day�1) at the Guyaflux

experimental unit, French Guiana. For NEPd, negative values

denote carbon storage in the ecosystem. Each dot represents

1 day. The lines represent the running mean (6 days before and

6 days after). The horizontal black lines illustrate the periods

(93 consecutive days in 2004 and 2005) considered in this study

as the long, dry periods.

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1925

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

Po0.01). During the 2005 long, dry period, variations in

GEPd were only correlated with wSWCd (R2 5 0.09,

Po0.001) and variations in REd were correlated with

wSWCd and VPDd (R2 5 0.22, Po0.001).

NEPd was slightly linearly correlated with REd

(R2 5 0.07, Po0.001) (Fig. 11a). When only considering

the long, dry periods, this correlation was stronger

(R2 5 0.22 and 0.19 in 2004 and 2005, respectively;

Po0.001) (Fig. 11b). There was a weak linear relation-

ship between REd and SRd (R2 5 0.02, P 5 0.027)

(data not shown). This correlation was stronger

(R2 5 0.19, Po0.001) when considering only the data

from the long, dry season and the days before Novem-

ber 13 when SRd increased without any increase

in REd.

There were significant differences between periods in

the parameters (Amax and k) of the model between GEE

and PPFD (Fig. 12). Amax was lower during both long,

dry periods as compared to the wet period, but it did

not differ between long, dry periods. k was lower in the

2005 long, dry period as compared with the wet and the

2004 long, dry periods.

0

1

2

3

4

5

6

j-05 m-05 m-05 j-05 s-05 n-05

SR

d (g

C m

−2 d

ay−1

)

Date

Fig. 8 Estimated seasonal variations in daily soil respiration

(SRd, g C m�2 day�1) at the Guyaflux experimental unit, French

Guiana, from automatic chambers installed in May 2005. Each

dot represents 1 day. The lines represent the running mean

(6 days before and 6 days after). The horizontal black lines

illustrate the periods (93 consecutive days) considered in this

study as the long, dry periods.

NE

P d (g

C m

−2 d

ay−1

)

−1.6

−1.2

−0.8

−0.4

0.0

0.4

0.8(a)

RE

d (g

C m

−2 d

ay−1

)

8

9

10

11

12

13

14(b)

GE

P d (g

C m

−2 d

ay−1

)

8

9

10

11

12

13

14

a o nDate

(c)

s

wS

WC

d (m

)

0.3

0.4

0.5

0.6

0.7(d)

PP

FD

d (m

olph

oton

m−2

day

−1)

25

30

35

40

45

50

a o nDate

(e)

s

Fig. 9 Left: Running mean (6 days before and 6 days after) of (a) daily net ecosystem productivity (NEPd, g C m�2 day�1), (b) daily total

ecosystem respiration (REd, g C m�2 day�1) and (c) daily gross ecosystem productivity (GEPd, g C m�2 day�1) during the 2004 (black line)

and 2005 (grey line) long, dry periods (93 consecutive days, days of the year 243–335) at the Guyaflux experimental unit, French Guiana.

For NEPd, negative values denote carbon storage in the ecosystem. Right: Running mean (6 days before and 6 days after) of (d) daily

average weighted soil water content (wSWCd, m) and (e) daily sum of photosynthetic photon flux density (PPFDd, molphoton m�2 day�1)

during the 2004 (black line) and 2005 (grey line) long, dry periods (93 consecutive days).

1926 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

Discussion

Seasonal variations in NEPd

Our results were consistent with the strong seasonal

patterns in NEPd observed so far for Neotropical rain-

forests. The studied ecosystem successively acted as a

sink or a source of CO2 on a daily scale during both wet

and dry periods (Fig. 7a), but NEPd patterns varied

between seasons. The frequency and amplitude of these

variations were higher during wet periods, underlying

the fast response of CO2 fluxes to the highly variable

climatic conditions encountered during wet periods

(Fig. 4). Cumulated NEPd values over periods of the

same duration led to higher carbon storage in the

ecosystem during long, dry periods as compared with

wet ones (Table 1). The magnitude of the difference was

2.7 and 5.4 in 2004 and 2005, respectively. Our results

are then consistent with the higher carbon storage

observed during dry periods in Neotropical rainforest

ecosystems located in Central Amazonia (Nepstad et al.,

2002; Goulden et al., 2004; Hutyra et al., 2007).

Contrasting environmental conditions during mild vs.severe dry periods

Both studied years were characterized by a long, dry

period (August–November), but the decrease in preci-

pitation was much higher in 2005, with four months

with o50 mm precipitation (Fig. 2). Although the entire

Neotropical region experienced a severe deficit in rain

during the last quarter of 2005, in French Guiana the

deficit was similar to that observed during years with

ENSO events (i.e. 1997, 2003; M. France, personal com-

munication). There were no major differences in cli-

matic variables other than rainfall between the mild

(2004) and severe (2005) long, dry periods (Table 1). As

expected, the rainfall deficit during the severe dry

period led to lower wSWCd, greatly reducing the

amount of water extractable by the trees in these types

of soil (Guehl, 1984). We conclude that potential differ-

ences in the functioning of the ecosystem between these

two dry periods would mainly be related to different

SWC in the upper layers. Generally, lower SWC is likely

to induce a restriction in tree growth and transpiration

through stomatal closure (e.g. Bonal et al., 2000b; Bonal

& Guehl, 2001) or xylem embolism (e.g. Tyree et al.,

1998), as well as a decrease in autotrophic respiration

(Epron et al., 2004; Salimon et al., 2004; Sotta et al.,

2004, 2006) and/or heterotrophic respiration through

0

2

4

6

8

10

12

14

16

0 10 30 5020

GE

P d (g

C m

−2 d

ay−1

)

PPFDd (molphoton m−2 day−2)

40

Fig. 10 Relationship between daily gross ecosystem productiv-

ity (GEPd, g C m�2 day�1) and daily sum of photosynthetic

photon flux density (PPFDd, molphoton m�2 day�1) in 2004 and

2005. The model that best explained this relationship was

GEPd ¼ 14:41� PPFDd=ð12:85þ PPFDdÞ (R2 5 0.46; Po0.001).

Each dot represents one day.

12 16

−6

−4

−2

0

2

4

6

8

0 2 4 6 8 14

NE

P d (g

C m

−2 d

ay−1

)

(a)

10

REd (gC m−2 day−1)

1

−4

−3

−2

−1

0

1

2

3

1

(b)

REd (gC m−2 day−1)

NE

P d (g

C m

−2 d

ay−1

)

12 160 2 4 6 8 1410

Fig. 11 (a) Relationship between daily net ecosystem produc-

tivity (NEPd, g C m�2 day�1) and daily total ecosystem respira-

tion (REd, g C m�2 day�1) in 2004 and 2005 (R2 5 0.07, Po0.01).

(b) Relationship between daily net ecosystem productivity

(NEPd, g C m�2 day�1) and daily total ecosystem respiration

(REd, g C m�2 day�1) during the 2004 ( * ) and 2005 (�) long, dry

periods (R2 5 0.22 and 0.19 in 2004 and 2005, respectively;

Po0.001). Each dot represents 1 day.

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1927

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

decreased microbial activity in the soil (Meir et al., 1996;

Li et al., 2006).

The influence of severe drought on NEPd

When comparing mild vs. severe long, dry periods we

expected that different environmental conditions would

result in different NEPd and levels of carbon storage.

Both long, dry periods were characterized by highly

variable NEPd values (succession of positive and nega-

tive values with an amplitude of 4.80 g C m�2 day�1)

(Fig. 9a), associated with variable climatic conditions

encountered during these periods, even though rain

events were infrequent (Fig. 4). Severe drought condi-

tions induced lower NEPd values over the first half of

the dry period, but similar values thereafter.

Both dry periods were characterized by net carbon

storage in the ecosystem (Table 1), but one of the major

conclusions of our study is that environmental condi-

tions such as that during extremely severe drought

double the amount of total carbon stored in the ecosys-

tem (Table 1). The influence of such severe drought

conditions on carbon storage in Neotropical forest eco-

systems has not been reported earlier. Nevertheless, a

throughfall exclusion experiment undertaken in east-

ern-central Amazonia (The ‘Tapajo’ site), Brazil, to

simulate extremely severe dry periods confirmed that

this ecosystem was sensitive to a reduction in rainfall

during dry periods and demonstrated a decline in

annual aboveground net primary productivity under

dry-down conditions (Nepstad et al., 2002; Asner et al.,

2004). Even though we did not estimate intra-annual

aboveground net primary productivity during this

study, Goulden et al. (2004) showed that carbon storage

in the aboveground biomass is not necessarily corre-

lated with that of the entire ecosystem, particularly

during dry periods. Carbon storage depends mainly

on fast turnover pools, such as leaves and litter, rather

than slow turnover pools, such as woody biomass. We

then conclude that a significant reduction in rainfall

during severe seasonal dry periods and the resulting

decrease in available soil water do induce higher carbon

storage in this ecosystem. Accumulated carbon might

not necessarily be stored in woody pools. Further

measurements of wood increments over a fine time

scale will soon be conducted at this site to confirm this

hypothesis.

Seasonal variations in REd and GEPd

We observed strong seasonal variations in both REd and

GEPd (Table 1, Fig. 7b and c). REd varied in a threefold

manner, from 4.7 to 14.9 g C m�2 day�1, with average

values of 10.1 and 9.5 g C m�2 day�1 in 2004 and 2005,

respectively (Fig. 7b). GEPd was also highly variable

(1.9–16.8 g C m�2 day�1), with average values of 10.6

and 10.0 g C m�2 day�1 in 2004 and 2005, respectively

(Fig. 7c). The annual average of 9.84 for REd and

10.22 g C m�2 day�1 for GEPd were in the upper range

of values found at Neotropical rainforest sites (5.6–

9.3 g C m�2 day�1 for REd, 4.2–9.3 g C m�2 day�1 for

GEPd).

Both years were characterized by higher REd values

during the transitional period between wet and dry

conditions and a decrease thereafter. This peak was

associated with the more highly positive NEPd values

found over the year. Furthermore, seasonal variations in

REd were significantly correlated with those of NEPd

(Fig. 11). Then, as previously generalized for temperate

forest ecosystems (Valentini et al., 2000) and discussed

for another Neotropical ecosystem (Goulden et al., 2004;

Hutyra et al., 2007), variations in REd were a main

determinant of seasonal variations in NEPd. The ampli-

tude of REd was in the higher range of other Neotropical

ecosystems (Malhi et al., 1998; Araujo et al., 2002;

Goulden et al., 2004; Hutyra et al., 2007), but was

proportionally lower than in a transitional tropical

forest subjected to long seasonal dry periods (average

seasonal variations: 3.1–6.0 g C m�2 day�1; Vourlitis

et al., 2004). Seasonal variations in REd were then inter-

mediate between previously published data on Neotro-

pical rainforests and a transitional tropical forest,

probably in association with the intermediate level of

drought conditions found here.

Whereas REd was almost constantly lower under

severe (vs. mild) drought conditions, lower GEPd va-

lues were found only over the last third of the dry

0

5

10

15

20

25

30

35

0 500 1000 1500 2000PPFD (µmolphoton m−2 s−1)

549.3315.8

33.930.6

2004-dry506.640.7

kAmax

2005-dry

40.72005-wet

GE

E (

µmol

CO

2 m

−2 s

−1)

Fig. 12 Modelled relationship between 30 min gross ecosystem

exchange (GEE, mmolCO2 m�2s�1) and the photosynthetic photon

flux density (PPFD, mmolphoton m�2 s�1) during the 2005 wet

period (* ) and the 2004 (�) and 2005 (�) long, dry periods. The

model used was GEE ¼ Amax � PPFD=ðkþ PPFDÞ:

1928 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

period (from November 1; Fig. 9c). Consequently, the

impact of a severe reduction in water availability ap-

pears to be stronger on REd than on GEPd and the

consequences of these different variations over time

were higher levels of carbon storage in the ecosystem

during severe dry periods (Table 1).

Which environmental parameters best explain theseseasonal variations?

REd is the sum of various respiration components in the

ecosystem (roots, litter decomposition, soil micro-

organisms and aboveground biomass). The functioning

of these components depends on processes that are

differently influenced by environmental conditions

and whose response to environmental changes might

be asynchronous, and thus probably displaying differ-

ent seasonal patterns. In contrast to most temperate

forest ecosystems (e.g. Valentini et al., 2000; Reichstein

et al., 2002), seasonal variations in REd could not be

clearly explained by any climatic variables. Soil tem-

perature in the upper layers and atmospheric air tem-

perature have been found to control REd in various

forested ecosystems (e.g. Reichstein et al., 2002). In our

study, like in those conducted in other Neotropical

forests (Grace et al., 1996; Malhi et al., 1998; Araujo

et al., 2002; Loescher et al., 2003), no night-time response

of instantaneous NEE to atmospheric air temperature

was found. During the day, the 5–7 1C range of atmo-

spheric air temperature might indeed induce a slight

temperature response in instantaneous NEE. Neverthe-

less, seasonal variations in mean daily atmospheric

temperature were not correlated with seasonal varia-

tions in REd. Because of the dense forest cover

(PAI � 7.0 m2 m�2), very low amounts of energy

reached the ground and variations in soil temperature

at 0.05 m depth did not exceed 1.7 1C throughout the

year. Variations in soil temperature were then neither

sufficient enough to induce any significant seasonal

change in REd.

Differences in REd between mild and severe dry

periods clearly arose from different levels of SWC.

Several authors have previously examined the influence

of SWC on REd in tropical forest ecosystems. Under dry

soil conditions, the decomposition of organic matter on

the forest floor (Meir et al., 1996; Davidson et al., 2000,

2004), autotrophic respiration in the ground (Epron

et al., 2004; Salimon et al., 2004; Sotta et al., 2004, 2006),

coarse woody debris decomposition (Chambers et al.,

2001) and, to a lesser extent, leaf or wood respiration

(Nepstad et al., 2002; Cavaleri et al., 2006) are greatly

reduced. Among these processes, we measured seaso-

nal variations in SR throughout 2005 and observed a

clear reduction in SRd during the dry period. The

seasonal pattern of SRd is likely driven by the dynamics

in fine root systems (Lee et al., 2004; Misson et al., 2006).

The increase in soil efflux at both the beginning and the

end of the long, dry season might be associated with

periods of fine root growth (Trumbore et al., 2006).

Alternatively, they might also correspond to a period

where inputs of fresh labile carbon were high, for

instance after a period when the rate of fine root

mortality was also high and environmental conditions

were favourable to microbial activities. Variations in

REd did not parallel SRd patterns during the dry–wet

transition (November/December), contrary to the wet–

dry transition (July/August). We hypothesized that

while SR was stimulated by the return of water soil

conditions leading to both renewed root growth and a

burst in the microbial decomposition of accumulated

organic matter, the drop in air temperature (from

26.8 1C in October to 24.5 1C in December) induced a

decrease in aboveground respiration (Damesin et al.,

2002), offsetting the trend in belowground respiration.

Further measurements are needed to confirm this

hypothesis.

Available incident radiation was clearly the key factor

that influenced seasonal variations in GEPd, as pre-

viously found for other Neotropical forest ecosystems

(Malhi et al., 1998; Malhi & Grace, 2000; Loescher et al.,

2003; Goulden et al., 2004, Huete et al., 2006; Hutyra

et al., 2007). It was responsible here for about half of

these variations. Seasonal variations in PPFDd are asso-

ciated with annual variations in incident extraterrestrial

radiation (15% throughout the year) and with the cloud

cover related to the oscillation of the ITCZ. The effect of

PPFDd on GEPd was clearly observable when wet and

long, dry periods were compared. Furthermore, this

effect was also observable when comparing mild dry

and severe dry periods. Indeed, there was a good match

between the lower PPFDd values found at the end of the

long, dry season in 2005 when compared with 2004

(� 18%, Fig. 9e) and the lower GEPd values between the

two periods (19%, Fig. 9c).

In our study, the maximum photosynthetic activity

(Amax) for a given instantaneous PPFD was slightly

lower under drought conditions when compared with

wet ones, but rather similar under mild and severe

drought conditions (Fig. 12). This suggests that drier

conditions induced the alteration of photosynthetic

processes, even though this regulation process did not

significantly increase under more severe conditions.

The absence of major photosynthetic regulation under

drier soil conditions has been previously debated (Cars-

well et al., 2002; Goulden et al., 2004; Huete et al., 2006).

It has been suggested to be mainly associated with the

deep rooting system developed by most tropical rain-

forest tree species (Nepstad et al., 1994), which allows

H I G H E R N E P U N D E R S E V E R E D R O U G H T 1929

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

them to extract water from the deep soil layers that are

less affected by seasonal drought conditions (Bonal

et al., 2000a; Nepstad et al., 2002). Using a remote

sensing approach, Ichii et al. (2007) confirmed that the

depth of the rooting system is a key factor likely to

control seasonal variations in modelled GEP. Our re-

sults suggest that the mean rooting depth in this eco-

system extends below the soil layers investigated here,

(i.e. to 2.4 m depth). This is consistent with the average

maximum rooting depth observed in Neotropical rain-

forests [i.e. 8.0 m (Nepstad et al., 1994)], and with a

study conducted at a nearby site in French Guiana

showing deep water extraction by some tropical tree

species during the dry season (Bonal et al., 2000a).

The similarities in air characteristics (air temperature

and VPD) between mild and severe dry periods (Table

1) precluded the hypothesis that lower GEPd values

during severe dry periods might also be related to the

influence of VPD on stomatal closure during the day,

which could eventually reduce photosynthesis. It has

also been suggested that the lack of certain nutrients,

particularly nitrogen, might be a potential factor reg-

ulating the function of ecosystems experiencing severe

drought conditions. This question was not studied here,

but Williams et al. (1998) concluded that such effect was

minor in another Neotropical forest site.

Other causes for the absence of a significant reduction

in photosynthetic activity in those ecosystems experien-

cing severe drought could be related to the large differ-

ences between tropical rainforest tree species in their

sensitivity to soil water availability. Under similar en-

vironmental conditions, the threshold of soil water

availability that induces a reduction in photosynthetic

activity greatly differs between species (e.g. Bonal et al.,

2000b; Bonal & Guehl, 2001; Engelbrecht & Kursar,

2003); however, this information was obtained for seed-

lings and young trees growing in plantations. To the

best of our knowledge, no such data yet exist on adult

canopy trees; nevertheless, it is reasonable to believe

that independent of the architecture and depth of the

rooting system, contrasting levels of sensibility to soil

drought do exist among mature individuals. Reduced

GEPd under severe drought conditions, while not sig-

nificantly lower, might then also have occurred because

more trees and species during the 2005 long, dry period

reached the SWC threshold at which an alteration in

photosynthetic processes is induced.

Modifications in canopy properties in response to soil

drought have also been described to explain seasonal

variations in GEPd (Vourlitis et al., 2001, 2004; Carswell

et al., 2002; Goulden et al., 2004; Meir & Grace, 2005).

Variations in litter production over the 2-year study

period (Fig. 6) were consistent with the higher cumu-

lated litter production found during dry periods in

other Neotropical forest ecosystems (Malhi et al., 1998;

Williams et al., 1998; Goulden et al., 2004). However, the

increase in litter production occurred at the onset and

not towards the end of the dry period and did not

induce major changes in canopy properties during long,

dry periods (Fig. 6), in contrast to other Neotropical

forests that displayed a lower leaf area index during

seasonal dry periods (Carswell et al., 2002; Saleska et al.,

2003). Large floristic gradients do exist within the

Neotropical rainforests associated with the different

relative ratios of deciduous vs. evergreen species (Ter

Steege et al., 2000). Whether these gradients could

locally lead to different seasonal patterns in canopy

properties is a worthy question. A clear seasonal cycle

in leaf area throughout Amazonia was recently detected

using satellite data (Myneni et al., 2007); unfortunately,

this study did not cover French Guiana and, thus,

comparisons with our data are impossible. A more

thorough and frequent study of seasonal variations in

canopy leaf dynamics will help confirm the punctual

observations made so far.

Conclusions

These results emphasize that environmental conditions

such as during a severe drought, as expected with

global environmental changes, will modify the CO2

exchange between Neotropical rainforest ecosystems

and the atmosphere and the resulting carbon balance.

The main determinants of these changes seem to be the

amount of available incident radiation and the regula-

tion of ecosystem respiration components given low soil

water availability. A change in canopy structure and the

regulation of photosynthetic activity will play a minor

role, if any, in the seasonal variations in NEPd, probably

in relation to the deep rooting system developed by the

trees in these ecosystems.

We focused on the contrast between mild and severe

long, dry periods to underline the potential effects of

climatic changes on NEP, but the carbon balance of this

ecosystem over the long term also greatly depends on

its functioning during transitional periods during

which climatic conditions and soil water availability

change quickly. Further analyses covering longer time

periods (typically 4–5 years) and including these transi-

tional periods will then be necessary to predict the

future CO2 exchange between this ecosystem and the

atmosphere. Our approach did not take into account

possible, rapid changes in the floristic composition in

these ecosystems that could result from environmental

changes. Additional studies on the response of both

young and adult tropical rainforest tree species to long-

er and more severe dry periods are necessary to predict

1930 D . B O N A L et al.

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 1917–1933

the future floristic compositions of these ecosystems

and their potential role in atmospheric CO2 storage.

Acknowledgements

We wish to thank the Centre Spatial Guyanais (CSG), the CentreNational des Etudes Spatiales (CNES) and the Centre Interna-tional de Recherche en Agronomie et developpement (CIRAD) forallowing us to install the Guyaflux site on their land property. Theinstallation of this site was made possible thanks to funding fromthe Institut National de la Recherche Agronomique (INRA), theFrench Ministry of Research and the European Community in theframework of the 12th CPER Guyane (Research and Environmentprogrammes) in which the GIS-Silvolab, the French GuiananRegion and Prefecture and the DIREN were involved. Thisresearch was supported by a FNS programme (ACI PNBC) fromthe French Ministry of Research. We thank M. Fournier, E. Dreyerand D. Girou for their help in preparing the initial project, J. Chavefor his help to set up the litter traps, V. Freycon for the soilanalyses, N. Breda for lending LAI2000 sensors, E. Marcon and T.Almeras for their help in data analysis, A. Dejean for her greathelp in revising this manuscript and two anonymous reviewers.

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