tmpDA91 TMP

Global Change Biology
Global Change Biology (2014) 20, 14811497, doi: 10.1111/gcb.12424
Replicated throughfall exclusion experiment in an

Indonesian perhumid rainforest: wood production, litter
fall and fine root growth under simulated drought
GERALD MOSER*, BERNHARD SCHULDT, DIETRICH HERTEL, VIVIANA HORNA,
H E I N Z C O N E R S , H E N R Y B A R U S and C H R I S T O P H L E U S C H N E R
*Plant Ecology, University of Giessen, Heinrich-Buff-Ring 26-29, 35392 Giessen, Germany, Plant Ecology and Ecosystems
Research, Albrecht von Haller Institute for Plant Sciences, University of Gottingen, Untere Karspule 2, 37073 Gottingen,
Germany, Agrotechnology, Faculty of Agricultural Sciences, Tadulako University, 94118 Palu, Sulawesi Tengah Indonesia
Abstract
Climate change scenarios predict increases in the frequency and duration of ENSO-related droughts for parts of
South-East Asia until the end of this century exposing the remaining rainforests to increasing drought risk. A
pan-tropical review of recorded drought-related tree mortalities in more than 100 monitoring plots before, during
and after drought events suggested a higher drought-vulnerability of trees in South-East Asian than in Amazonian
forests. Here, we present the results of a replicated (n = 3 plots) throughfall exclusion experiment in a perhumid
tropical rainforest in Sulawesi, Indonesia. In this first large-scale roof experiment outside semihumid eastern
Amazonia, 60% of the throughfall was displaced during the first 8 months and 80% during the subsequent
17 months, exposing the forest to severe soil desiccation for about 17 months. In the experiments second year, wood
production decreased on average by 40% with largely different responses of the tree families (ranging from 100 to
+100% change). Most sensitive were trees with high radial growth rates under moist conditions. In contrast, tree
height was only a secondary factor and wood specific gravity had no influence on growth sensitivity. Fine root
biomass was reduced by 35% after 25 months of soil desiccation while fine root necromass increased by 250%
indicating elevated fine root mortality. Cumulative aboveground litter production was not significantly reduced in
this period. The trees from this Indonesian perhumid rainforest revealed similar responses of wood and litter
production and root dynamics as those in two semihumid Amazonian forests subjected to experimental drought. We
conclude that trees from paleo- or neotropical forests growing in semihumid or perhumid climates may not differ
systematically in their growth sensitivity and vitality under sublethal drought stress. Drought vulnerability may
depend more on stem cambial activity in moist periods than on tree height or wood specific gravity.
Keywords: drought sensitivity of growth, fine root mortality, Paleotropis, perhumid climate, roof experiment, soil desiccation,
tree mortality
Received 20 June 2013 and accepted 28 August 2013
Introduction
Climate warming in the Tropics may lead to more
variable climates with larger extremes in the decades
and centuries to come (Dai, 2013). For most tropical
regions, a temperature increase by 24 K or more has
been predicted for the next hundred years (Christensen
et al., 2007). The effects of increasing temperatures may
be linked to an increasing evaporative demand of the
atmosphere, increases or decreases in precipitation,
changes of radiative forcing and regional wind systems.
The multitudes of factors that change in concert make
predictions about the response of natural and managed
tropical ecosystems difficult.
Correspondence: Christoph Leuschner, tel: +49 551 39 5718,
fax: +49 551 39 5701, e-mail: cleusch@gwdg.de
2013 John Wiley & Sons Ltd
For South-East Asia, a warming by about 2.5 K until

the end of the century has been predicted, which is
similar to the global mean (Christensen et al., 2007).
Since warmer oceans evaporate more water, most
model simulations assume increasing area means of
precipitation over this part of the Tropics with a
median rainfall increase of about 7% in all seasons
(Christensen et al., 2007). However, the projected
precipitation changes vary strongly within the region
ranging from substantial increases to decreases (Christensen et al., 2007; Mann, 2007; Sheffield & Wood,
2008). Moreover, rainfall and temperature extremes and
the frequency of drought events are ecologically more
important than changing means. Recent studies on the
most likely changes in the climate of South-East Asia,
based on scenarios with eight climate models, came to
the conclusion that the frequency, severity and duration
1481
1482 G . M O S E R et al.
of El Ni~
no-Southern Oscillation (ENSO) events should
continuously increase (Latif et al., 1998; Guilyardi, 2006;
Hansen et al., 2006; Merryfield, 2006; Philip & van
Oldenborgh, 2006; Christensen et al., 2007; Rosenzweig
et al., 2007; Paeth et al., 2008; Sheffield & Wood, 2008).
Interannual rainfall variation in South-East Asia is largely influenced by the ENSO system (Sheffield &
Wood, 2008) and severe droughts as in 1997/98 occur
most often in association with extreme ENSO events.
For example, on Mount Kinabalu (Borneo), monthly
rainfall was reduced in the 1998 drought to <60 and
<10 mm at two elevations with a rainless period lasting
for more than 90 d (Aiba & Kitayama, 2002). IPCC
scenarios predict for SE-Asia a drought of 46 months
to happen all 15 years and forcast a high probability of
a 12-month drought once in a century (Sheffield &
Wood, 2008). Drought may thus represent a major stressor for tropical forests not only in semihumid but also
in humid and per-humid climates.
During the last 10 years, the response of tropical
trees and forests to extended drought periods has
received increasing attention (Marengo et al., 2008;
Phillips et al., 2009, 2010; Anderson et al., 2010; Lewis
et al., 2011). Observational studies on drought effects
have been conducted in the tropical forests of the
Americas, Africa and South-East Asia (Aiba & Kitayama, 2002; Slik, 2004; van Nieuwstadt & Sheil, 2005;
Nishimura et al., 2007; Allen et al., 2010; Meir & Woodward, 2010; Phillips et al., 2010; Itoh et al., 2012). The
consequences of the severe ENSO drought of 1997/98
for tree mortality rate and the impact of subsequent forest fires have been intensively studied in particular in
Borneo and Sumatra (Siegert et al., 2001; van Nieuwstadt & Sheil, 2005; Fredriksson et al., 2007). One finding
is that trees of different size and position in the canopy
are differently susceptible to water shortage. For example, Aiba & Kitayama (2002) found increased mortality
of small- to medium-diameter trees together with
reductions in stem diameter increment of large trees
(DBH >100 cm) in stands at 700 m elevation on Mt. Kinabalu, Borneo, while others reported the highest mortality rates in large-diameter trees (Slik, 2004; van
Nieuwstadt & Sheil, 2005; Itoh et al., 2012). A pan-tropical survey indicated a particularly high droughtinduced mortality of large trees and, to a lesser extent,
of trees with low wood density (Phillips et al., 2010).
A mechanistic understanding of how drought may
affect tropical forests can only be achieved by rainfall
manipulation experiments with controlled water
supply. Wu et al. (2011) and Beier et al. (2012) provide
recent reviews of the results of precipitation
manipulation experiments, and Smith et al. (2009) offer
a conceptual framework for understanding the impacts
of altered resource supply on ecosystem dynamics.
Accordingly, a third of the 95 completed precipitation

manipulation experiments were conducted in forests
and most of them at middle latitudes. Only four studies
refer to subtropical and tropical ecosystems (mean
annual temperature >20 C) and five to systems with
annual precipitation totals >1500 mm, where manipulation is more difficult (Beier et al., 2012). However, some
of these warm and moist regions of the earth are
thought to be particularly sensitive to climate change
(Rosenzweig et al., 2007) and thus need special attention. In eastern Amazonia two large rainfall displacement experiments have been conducted in lowland
forests so far, one on sandy soil (Caxiuan~a National Forest) and the other on loamy soil (Tapaj
os National Forest) (Nepstad et al., 2002; Fisher et al., 2007). In both
regions, annual mean precipitation was about 2000 mm
with a regular 6-month-long dry season (monthly
precipitation <100 mm) in which air temperature and
vapour pressure deficit are elevated. In both experiments, throughfall was reduced by ca. 3550% in a one
hectare plot with subcanopy roof constructions that
covered about 7580% of the ground area with plastic
panels. At Caxiuan~a, the throughfall reduction was conducted permanently, at Tapaj
os only during the rainy
season (Brando et al., 2008; da Costa et al., 2010; Markewitz et al., 2010; Metcalfe et al., 2010). In these experiments, multi-annual throughfall exclusion reduced
stem wood production by 20 to 60% and increased tree
mortality after 34 years (Brando et al., 2008; da Costa
et al., 2010) indicating that a soil moisture threshold
value seems to exist beyond which certain tropical
forests would suffer catastrophic dieback.
Unfortunately, the results of these two experiments
may not be valid for large parts of the tropical moist
forest biome because the climate at the two sites in
eastern Amazonia is characterized by a distinct dry period up to 6 months, which differs from the perhumid
climate in, for example, parts of South-East Asia and
western Amazonia, where the trees are not exposed to
regular dry seasons. Desiccation experiments are
missing not only for tropical perhumid forests but also
for South-East Asia and the paleotropical realm in
general (Meir & Woodward, 2010). This is unsatisfactory because observations during natural droughts are
suggesting that the South-East Asian forests may be
particularly vulnerable to droughts (Rosenzweig et al.,
2007; Phillips et al., 2010) and thus deserve special
attention in the face of climate warming. The studies
surveyed by Phillips et al. (2010) (9 from Borneo and 25
from the Amazon) indicate a steeper increase of
mortality rate during and after drought with increasing
desiccation intensity in the Bornean than the Amazonian forests. However, the observed range and the
maximum intensity of drought events was much larger
2013 John Wiley & Sons Ltd, Global Change Biology, 20, 14811497
I N D O N E S I A N R A I N F O R E S T D R O U G H T E X P E R I M E N T 1483
in Borneo than in Amazonia, and differences in edaphic
factors, rooting depth and biogeography complicate
direct comparison.
To close this knowledge gap, we set up a replicated
throughfall exclusion experiment with three subcanopy
roofs of 1600 m2 area each in a perhumid, pre-montane
tropical rainforest in Sulawesi, Indonesia (Sulawesi
Throughfall Exclusion Experiment, STEE) for studying
drought responses at the tree and ecosystem levels in a
tropical forest, which is not exposed to longer regular
dry periods. The desiccation started in 2007 and was
maintained for 25 months until summer 2009. This
article presents results on the trees drought response
with a focus on aboveground (wood growth and litter
production) and belowground productivity and carbon
cycling (fine root production and mortality). We
wanted to answer three questions, first, how variable is
the drought response among the trees of a species-rich
tropical perhumid forest; second, what is the role of
species identity (or phylogeny) in comparison to tree
morphology (height and wood specific gravity) as a
determinant of drought sensitivity, and third, which
productivity component (production of wood, leaves or
fine roots) is the most drought-sensitive. We tested the
hypotheses (i) that the trees of this aseasonal perhumid
rainforest are on average more sensitive to drought
than the trees of the two existing Amazonian throughfall reduction experiments, where extended dry periods
are regularly occurring, and that (ii) the trees drought
sensitivity increases with tree size but decreases with
increasing wood specific gravity.
Material and methods
Study site
The Sulawesi Throughfall Exclusion Experiment was
established in 2006 in a natural pre-montane rainforest in
Pono Valley, about 3 km NE of the village of Toro in Lore Lindu National Park in Central Sulawesi, Indonesia (0129.6S,
12003.4E; see map in Fig. 1). Six study plots of 40 m 9 40 m
size on level terrain at 1050 m elevation were selected in close
proximity to each other in a forest section with no signs of
human disturbance (as evidenced by the absence of stumps
and charcoal in the soil, and the presence of rattan palms that
are extracted first). The plots were spread in a stratified
random design over an area of about 5 ha on a small plateau
in overall rugged terrain to guarantee comparability of site
conditions. The maximum distance between the first and the
last plot was ca. 250 m. The climate of the study area is perhumid with a long-term mean annual rainfall of 1894 mm and a
mean annual temperature of 21.3 C (WorldClim, 2006). During the study period, the mean annual rainfall was somewhat
higher with 2672 mm (3003 mm in the first and 2222 mm in
the second year) and a mean annual temperature of 20.8 C
measured on a 16 m high tower in a small forest gap close to

the plots (Fig. 2). According to a 20-year record of a local
weather station, regular dry periods longer than 2 weeks do
not occur in the region. In Toro village, six dry periods with
<5 mm rain within 2 weeks have been recorded from 2001 to
2007, while the monthly rainfall totals exceeded 50 mm
despite the occurrence of these dry periods (pers. comm. H.
Kreilein). The heavily weathered soils of this old-growth forest
(Nitisols according to the World Reference Base for Soil
Resources) are rich in clay and loam and developed on metamorphic rocks. The mineral soil to 250 cm depth consists of
2837% sand, 3153% silt and 1143% clay (van Straaten,
2010). The plots had average inclinations of 5 (maximum
slope angle: 20). The soils are moderately nutrient-rich with
pH(H2O) values of 4.4, a cation exchange capacity of ca. 600
lmolc g1, base saturation of ca. 22%, a total nitrogen concentration of 2 mg g1 and a C : N ratio of 13 in the upper 20 cm
of the mineral soil. The forest on the plateau is more or less
homogenous in aboveground structure (see biomass figures in
Table 1) and contains only minor gaps due to the fall of single
trees. The forest has a mean maximum height of ca. 45 m with
a few trees reaching up to 55 m. Average stem density is
456 ha1, basal area 43.4 m2 ha1 (>10 cm in diameter at
breast height DBH). Tree species diversity is high with about
130 species ha1 (Culmsee & Pitopang, 2009; Culmsee et al.,
2010).
Experimental design
Three of the six plots with an area of 0.16 ha were selected by
random (# 2, 3 and 6) and equipped with subcanopy roofs
(40 m 9 40 m) to cover the whole plot (total roof area:
0.48 ha; Fig. 1). Frames made of bamboo poles of
5 m 9 0.5 m size were placed at 1.23.0 m height above the
ground on a wooden roof construction and covered by
transparent and UV-insensitive polyethylene sheet to collect
the throughfall and channel it out of the plots with the help of
gutters (Fig. 1). The captured throughfall water percolated
into the soil at a distance of more than 3 m beyond the plot
boundary trenching in downslope direction. The efficiency of
the 40 cm deep trenching was controlled continuously by
weekly TDR measurements of soil moisture conducted with
high spatial resolution. Accordingly, the plot edges were not
moister than the interior (see Fig. S1 in the Appendix). Around
all six plots (roof and control), the 40 cm deep trenches were
covered by plastic foil for inhibiting root growth into the plots
and uptake of water from outside. According to excavations,
the soil profile to 40 cm contained ca. 80% of the fine root
biomass in the profile (Hertel et al., 2009). Gaps in the roofs
adjacent to tree stems were closed with smaller frames that fitted into the openings. Stem flow was not excluded from the
plots due to the large number of stems covered by the roofs
(in total more than 200 with DBH >10 cm); stemflow in a
nearby forest stand equalled <1% of gross precipitation and
thus contributed only marginally to soil infiltration (Dietz
et al., 2006). All measurements on trees and soil were conducted in a central core zone (30 m 9 30 m) of each plot surrounded by a 5 m wide buffer zone to exclude edge effects.
Fig. 1 Map of Indonesia with the island of Sulawesi, in detail the Toro and Pono Valleys, the relative position of the six study plots
(40 m 9 40 m) and the meteorological tower in a patch of the Pono Valley forest with surface relief of the terrain and photographs of
the roof construction. The three desiccation plots (#2, 3 and 6) carry a below-canopy roof construction for throughfall displacement.
Solar panels were mounted on the 16 m high meteorological tower in a natural forest gap.
The desiccation began on May 1, 2007, and lasted for about

25 months until June 13, 2009.
The efficiency of the roof was monitored with each six
throughfall collectors (4 m long and 0.2 m wide) per plot
above and six below the roof construction; they were sampled
twice a week. During the first 8 months of the desiccation
(MayJanuary 2008), about 60% of the throughfall water was
captured. In this period, soil infiltration was about 100 mm
per month. Subsequently, the density of the bamboo frames
was further increased resulting in a throughfall reduction by
ca. 80% in the remaining 17 months of the experiment
(February 2008 to June 2009). Thus, not more than
450 mm yr1 of rain (plus stem flow) entered the soil during
the main desiccation period. This moisture supply is well
below the agreed monthly rainfall threshold for characterizing
dry months (100 mm) and it might have reduced soil water
availability to a similar extent as the exceptional 12-month dry
periods predicted to occur once per century in future time
(Sheffield & Wood, 2008). We decided to extend the throughfall exclusion period to 17 months, that is, longer than
predicted by climate change scenarios, because we wished to
balance the mitigating effect of constantly high air humidity
during our experiment. Natural droughts are characterized by
the simultaneous occurrence of dry soil and dry air, a situation
that cannot be simulated in field experiments.
The fallen fine litter on the plastic-lined panels was
removed fortnightly and evenly spread out on the ground
below the roofs. We were not able to conduct a true pretreatment reference measuring phase prior to roof closure due to
the substantial logistic and technical problems (including a
169.1 23.0a
148.0 16.0
126.9 17.5a
76.5 10.3
67.1 7.1
4.8 0.3
325.4 43.7
4.8 0.2
13.4 0.4
13.9 4.2
870.8 20.4
866.7 46.4
4.7 0.2
4.5 0.2
20.9 3.8
20.9 0.3
0.12
1.13
5.9 0.1
5.8 0.1
6.6 0.2
6.3 0.3a
5.8 0.03
425
431.7 43.8a
396.0 23.3
456.5 9.3
435.0 5.6
0.09
6.6 0.2
0.1 0.02
0.13
5.8 0.1
0.29 0.41
0.11
5.8 0.1
6.1 2.9
413.8 23.6
Total
Mean SE
0.4 0.4
Control
Mean SE
1.1 0.6
Roof
Mean SE
1.8 1.1a
R
6
1.1
419
363
C
5
1.8
C
4
350
R
3
513
413
0
R
2
3.8
C
1
Trees/ha
0.14
height m
0.5 0.3a
m2/ha
Tree
m2/ha
Basal area
285.5 30.3
a
a
a
a
a
a
a
57.7 7.8a
245.6 33.1a
4.8 0.6a
14.3 1.0a
875.0 23.9a
4.3 0.4a
20.9 0.8a
477.3 43.8a
63.8
264.9
5.9
13.3 0.5
881
4.8
19.6 0.5
450
56.0
87.1
363.8
232.0
5.1
4.6
13.3 0.5
14.3 0.5
800
844
4.5
5.0
21.2 0.5
20.4 0.5
425
438
67.0
278.7
4.7
16.3 0.6
913
4.6
22.3 0.4
563
86.3
42.3
173.0
360.4
4.8
3.7
13.3 0.5
12.8 0.4
956
831
3.5
4.6
21.1 0.4
20.8 0.5
419
Mg/ha
m2/ha
Basal area
Tree height m
Trees/ha
m2/ha
Basal area
Tree height m
Trees/ha
444
Mg/ha
140.7
192.9
123.2
92.1
147.9
191.2
Mg/ha
Carbon pool
BGB
AGB
All Trees
Trees 10 cm DBH
Basal area
Roof/Control
#
An automatic weather station installed on a 16 m high tower

in a small forest gap 60 m distant to plot #6 (see Fig. 1)
recorded continuously relative air humidity and temperature
(CS 215, Campbell Scientific Inc., Logan, UT, USA), incident
global radiation (CS 300, Campbell Scientific Inc.) and rainfall
(ARG 100, Campbell Scientific Inc.) at 5-s intervals. The data
were stored as 30-min averages in a CR800 data logger
(Campbell Scientific Inc).
Volumetric soil water content was continuously measured
in one main and two additional soil pits per plot. In the main
soil pit, time domain reflectometry (TDR) probes (CS616,
Campbell Scientific Inc., Logan, UT, USA) were continuously
operated at 10, 20, 40, 75, 150 and 250 cm soil depth. The two
additional soil pits were equipped with further TDR probes in
10, 40 and 75 cm soil depth. The probes were inserted horizontally into the undisturbed soil at the end of a 30 cm long
hole dug into the soil pit wall. In total, 36 TDR probes were
operated per treatment and the data were logged hourly
(CR1000, Campbell Scientific Inc., Logan, UT, USA). The TDR
probes were calibrated for four soil depths only, following the
procedure described by Veldkamp & OBrien (2000) (only one
Trees 210 cm DBH
Climatic and soil moisture measurements
Stranglers
lightning strike) encountered at this remote site (about 4 km

walking distance to the next road).
Plot
Fig. 2 Climate diagram after Walter & Lieth (1967) with the
monthly means of air temperature (lower line) and precipitation
sums (upper line) for the period March 2007 to August 2009
recorded at a 16 m high tower in a forest gap close to the study
site. Hatched areas indicate humid periods, black areas perhumid conditions with monthly precipitation sums >100 mm
(compressed scale above 100 mm). Also given are elevation,
mean annual temperature and mean precipitation total, length
of observation period, and the coordinates of the station.
Table 1 Stand structure, above- (AGB) and belowground biomass (BGB) and total biomass carbon pool of the six forest plots in Pono Valley, Central Sulawesi, Indonesia
(means 1 SE for n = 3 plots each). AGB was estimated with allometric regressions and BGB derived from root : shoot ratios given in the literature (see Methods section). Tree
height is the mean of all trees in the respective DBH class, basal area of the plot total. Different letters indicate significant differences between control and roof plot means
(P < 0.05)
calibration was done for the 10-20 and 40-75 cm soil layers
due to very homogenous soil texture). The hydrological and
physiological measurements began on March 27, 2007, in the
roof plots and on May 31, 2007, in the control plots (the delay
was caused by a lightning strike in March 2007).
The soil moisture measurements were used to calculate the
relative amount of extractable water (REW) in the profile
using the equation given by Brda et al. (2006) and Granier
et al. (2007). REW is calculated from daily data on the fractional volumetric soil water content, the soil water content at
which all plant-available water is assumed to be extracted
(corresponding to a matric potential of 1.5 MPa in the considered soil depth), and the maximum water content recorded
during the study period in that depth. The volumetric soil
water content at 1.5 MPa was obtained from laboratoryderived soil water retention curves (van Genuchten, 1980)
established with a pressure plate apparatus (van Straaten
et al., 2011). REW varies between 1 (field capacity or highest
soil water content recorded) and 0 (at 1.5 MPa). According
to Granier et al. (2007), temperate trees typically experience
drought stress when REW drops below a threshold value of
0.4. The soil water retention curves were further used for
deriving soil matric potential values from the continuous soil
moisture measurements conducted in these soil depths. The
spatial heterogeneity of soil moisture was monitored with 100
TDR measurements per plot conducted at weekly intervals in
a regular grid (8.75 m grid net width with 2.5 m distance to
the plot edge) with a mobile TDR probe by inserting the metal
bars from the forest floor vertically 30 cm into the soil.
Aboveground stand structure, biomass and productivity

In August and September 2006, complete stand inventories
were carried out in the six study plots and all trees with diameter at breast height (DBH at 1.3 m) 10 cm were tagged, tree
height recorded using a Vertex III height metre (Hagl
of,
L
angsele, Sweden) and the DBH measured with a measuring
tape (Richter Measuring Tools, Speichersdorf, Germany). If
buttresses were present DBH was measured above them at
24 m height over ground according to the recommendations
given by Clark et al. (2001). Understory trees of 2 to 9.9 cm in
DBH were surveyed in a similar manner as the adults within
16 subplots (5 m 9 5 m) per plot that covered one-fourth of
the total plot area. Species identification and description were
conducted as described in Culmsee & Pitopang (2009); the
specimens were deposited at the herbaria in Leiden (L), G
ottingen (GOET), Palu (CEB) and London (K). Contact Culmsee &
Pitopang (2009) for the complete species list of the study site.
For converting the recorded tree structural data into aboveground biomass (AGB), we used several sources for obtaining
wood specific gravity q for the observed species/genera (Oey,
1990; Soerianegara & Lemmens, 1993; Lemmens et al., 1995;
Sosef et al., 1998). AGB was calculated with the allometric
equation of Chave et al. (2005) for tropical moist forests:
AGB exp2:557 0:940 lnq D2 H
where AGB is the estimated aboveground biomass (in kg per

tree, including stem and branch wood and leaf biomass), D is
trunk diameter (DBH in cm), H is total tree height (in m), and
q is wood specific gravity (in g cm3). The literature data on
wood density often refer to wood samples measured under
fresh weight conditions (i.e. at 12 or 15% moisture). For transforming these data to wood specific gravity on a dry weight
basis, we corrected the literature data for water content
following Chave et al. (2006). In cases where ranges of wood
density values were given, we used median values. In species
for which wood density data were not available, the average
across all species in that genus growing in the corresponding
habitat was used (see Baker et al., 2004; Slik, 2006). In the few
cases (n = 10) where a tree individual could not be identified
at least to the genus level or where a literature record was not
available, we used the plot average.
Two groups of tree species required a specific calculation
procedure for estimating AGB due to their specific growth
forms. (i) The abundant Fagaceae Castanopsis acuminatissima
Blume builds clusters of root suckers that sprout from a
common compact stem basis of up to 2 m height (Soepadmo, 1972). For each stem with a DBH 2 cm, we recorded
diameter and height separately above this common basis
and AGB was then calculated for every stem. (ii) Stranglers
of the genus Ficus L. (Moraceae) with a free-standing treelike structure are characterized by a large hole amidst of
the vertical axis that was originally filled by the trunk of
the host tree. The aboveground biomass of these stranglers
was estimated by calculating the AGB for both the strangler and the original host tree and subsequently subtracting
the latter from the former. These calculations were
conducted by Culmsee et al. (2010); contact this reference
for details.
Annual aboveground tree biomass production (ANPP; in
Mg dry mass ha1 yr1) was calculated from stem
increment data obtained from the repeated reading of
dendrometer tapes (UMS, Munich, Germany) that were
installed in December 2006 on 20 tree individuals per
study plot. The 20 trees in a plot were chosen by random
from all trees with a DBH >10 cm based within the core
zone of the plots; they belonged to different taxa and varied in DBH from 10 to 150 cm. The stem diameter increment recorded in the 120 trees in the first and second year
of the experiment (June 2007May 2008, and June 2008
May 2009 respectively) were extrapolated to all other tree
individuals of the covered families in the plots based on
DBH and by using family averages of increment. For the
24 (from 42) families not covered by the measurements,
such as Rubiaceae and most families with less than 1%
contribution to stand basal area, we calculated with increment rates that were proportional to their wood density in
the respective treatment, adopting a procedure described
in Hertel et al. (2009). The aboveground wood production
in the first and the second year of the experiment was
then calculated from basal area increment applying the
allometric regression equation used also for biomass estimation as described above. The mortality of trees in the
plot (for individuals with DBH 10 cm) was documented
in the 25-months period and mortality rates were calculated for every plot (see Sheil & May, 1996; Nepstad et al.,
2007; da Costa et al., 2010). Mortality was also taken into
account in the productivity calculation.
True LAI (LAItrue) values were derived from hemispherical photographs taken before roof closure in 1 m height at
30 points per plot located at regular grid positions. CanEye software (INRA, Avignon, France) was used for image
analysis and the effective LAI (LAIeff) was calculated for a
zenith angle of 57.5 after Bonhomme & Chartier (1972) as
follows:
LAItrue LAIeff =CI
with the clumping index (CI) being calculated for each photo
after Lang & Xiang (1986).
For estimating annual leaf mass production, 12 litter
traps (75 cm 9 75 cm aperture) were installed in every plot
in March 2007. The litter was collected every 2 weeks and
sorted into leaves and other fine litter components (mostly
flowers, fruits and small twigs); litter dry mass was
obtained by drying at 70 C for 48 h. We assumed that
annual leaf litter production was equal to annual leaf production in both the first and the second year of the experiment.
Analysis of vertical fine and coarse root distribution

For examining effects of soil desiccation on root mass and
root distribution, we collected soil samples for root analysis
before roof closure in each two soil pits per plot (1 m minimum distance to the next tree with DBH >10 cm) in January and February 2007. A second inventory was conducted
in June 2009 immediately after the end of the desiccation
by digging each two new soil pits in plot areas without
previous disturbance. Monoliths of 40 9 40 9 20 cm size
(b 9 w 9 d) were extracted at 20 cm depth intervals for
measuring fine root (diameter <2 mm), and large and
coarse root (diameter >2 to 250 mm) density in the soil
profile. The excavation was conducted to 3 m depth in January/February 2007 and to 1.2 m depth only in July 2009,
because root density was found to be very small at greater
depth. The soil was sieved quantitatively (mesh size:
2 mm) and all visible root fragments were transferred to
plastic bags and taken to the laboratory of Tadulako University in Palu, Central Sulawesi, were they were washed
and sorted into fine and coarse roots. The vast majority of
the fine roots (>95%) were alive at the time of sampling
according to microscopic inspection of selected fine root
samples (see criteria defined in Leuschner et al., 2001).
After drying at 70 C to constant mass, all samples were
weighed and the data were expressed as fine and coarse
root biomass total (g m2) of the profile.
The root stumps underneath the stem basis were not
excavated which results in underestimation of total
belowground biomass. For obtaining an estimate of total root
biomass, we used the root : shoot ratio average of tropical
moist forests (0.24) given by Mokany et al. (2006).
The carbon (C) concentration in root, stem wood and litter
samples was measured with a CN auto-analyser (Vario EL III,
Hanau, Germany) at the University of G
ottingen.
Estimation of fine root production

The fine root productivity in the roof and control plots was
studied in the first and the second desiccation phase with an
ingrowth core experiment in all six plots according to the
approach described in Powell & Day (1991) and Godbold
et al. (2003). Six soil cores (diameter: 67 mm, length: 200 mm)
were taken in February 2007 at random locations within each
plot. After carefully removing all visible fine root fragments
>10 mm from the soil, the root-free material was replaced
into the hole. Care was taken to conserve the soil structure
and density as much as possible. The ingrowth cores were
marked at the soil surface with PVC tubes and recollected
after 16 months to measure the regrowth of roots into this
soil volume. To cover the second desiccation phase, six additional ingrowth cores were installed in October 2008 and
extracted after 8 months, shortly before roof opening. In the
laboratory, the samples were washed and all fine root fragments >10 mm were extracted by hand, washed again and
dried (70 C, 48 h). Following Vogt et al. (1998), we assumed
that the fine root mass (living and dead) in the cores at harvest represented the fine root production in the time span
between the start of recolonization and harvest. Earlier studies in nearby forest plots had shown that the fine root recolonization of the cores started about 2 months after their
installation and that root mortality was low in these cores
(Leuschner et al., 2009). Consequently, we assumed that the
fine root biomass recorded in the first cores (16 months of
exposure) reflected a fine root growth period of 14 months
covering the first experimental year, and that the second
group of cores (8 months of exposure) covered the fine root
growth activity during the second year (assuming a 6-month
growth period). By relating the fine root growth into the cores
to the standing fine root biomass in the upper 20 cm of the
soil (inventory data), we calculated fine root productivity. In
order to estimate the annual fine root production in the soil
profile to 3.0 m depth, we conducted a simple extrapolation
of the growth rate in the 0-20 cm horizon to the root mass in
the lower horizons ignoring any vertical change in specific
root growth activity. The estimated fine root production in
the whole soil profile is given in Mg ha1 yr1. Since we have
no coarse and large root growth data, our root production
figures are underestimates.
Statistical analyses
The nonparametric U-test after Mann and Whitney was used
for detecting significant differences between roof and control
plots for the parameters above- and belowground biomass
and above- and belowground productivity. ANOVA was used to
test for significant treatment effects on leaf litter production
(log-transformed data). For identifying important factors
influencing the degree of radial growth reduction from the
first to the second year, we calculated linear mixed effects
models with six biomass or growth-related traits as fixed variables and plot and tree nested in plot as random factors. The
statistical analyses were done with the software package R
(R Development Core Team 2009, version 3.0.0).
Results
Comparability of study sites and temporal development of

soil desiccation
The detailed stand inventory in the six plots immediately before the start of the desiccation revealed that the
forest had a sufficiently homogenous structure in the
forest patch selected for the experiment. None of the
plots contained a larger canopy gap (> ca. 10 m) and
none of the investigated structural and biomass-related
variables showed a significant difference between the
each three roof and control plots (Table 1). However,
two of the control plots (#1 and 5) contained a larger
number of tall Ficus stranglers (cumulative strangler
basal area 3.8 and 1.8 m2 ha1) which showed a patchy
distribution in the Pono forest. These tall trees with
their specific stem architecture increased the estimated
aboveground tree biomass (AGB) in the plots #1 and 5
considerably (>360 Mg ha1), exceeding the AGB
figures of the other four plots with no or only small
strangler presence (173279 Mg ha1, Table 1). Despite
the strangler effect, the AGB means of the control and
roof plots (325 and 246 Mg ha1) were not significantly
different from each other. Neither leaf litter mass in the
first study year (control: 6.2 0.6 Mg ha1 yr1; roof:
5.9 0.2 Mg ha1 yr1), LAI (optical measurement;
control: 5.3 0.2; roof: 5.4 0.1) nor fine root biomass
(03 m,
control:
5.8 0.8 Mg ha1;
roof:
1
5.3 0.2 Mg ha ) differed significantly between the
roof and control plots prior to the experiments start.
On average, 74% (412 g m2) of the fine root biomass
total occurred in the 020 cm layer and >95%
(530 g m2) in the 0100 cm stratum. The vertical root
mass decrease was even more pronounced for the biomass of coarse and large roots (>2 mm) with > 90%
found in the 0-20 cm layer and no detectable coarse
root biomass below 80 cm depth. Since all soil pits were
more than 1 m distant to the next large stem, large-root
stocks are not covered by this survey. Microscopic
inspection of the fine root samples revealed that the
proportion of necromass in total fine root mass was
very small (<5%).
In the experiments first desiccation phase (June 2007
to January 2008, 8 months), about 60% of the throughfall water was displaced resulting in an infiltration of
about 1180 mm yr1, which caused only a moderate
reduction of the extractable soil water reserves (data
not shown; see Schuldt et al., 2011) and virtually no
decrease in soil matric potential (w) in 00.5 m and
0.53.0 m soil depth (data not shown; see Schuldt et al.,
2011). The more effective roof closure in the second desiccation phase (February 2008June 2009, 17 months)
displaced about 80% of the throughfall in the roof plots
and led to a progressive decrease in volumetric soil

water content (VWC; Fig. 3), soil matric potential and
REW from February 2008 to December 2008 despite
plenty of rainfall. During the pronounced dry spell in
January/February 2009, soil desiccation further proceeded in the roof plots until May 2009; this drought
reduced soil moisture for some weeks also in the control plots. In the upper soil (00.5 m), REW dropped
below the presumed critical threshold value of 0.4 in
February 2008 and kept this level for about 17 months.
Soil matric potential fell in the upper soil of the roof
plots below the 0.5 MPa value in July 2008 and
passed the conventional -1.5 MPa threshold in May
2009. In the lower soil (0.53.0 m), REW approached
the 0.4 threshold for several months in 2009 but was
not accompanied by a marked drop in soil matric
potential. The soil water status in the control plots
remained favourable throughout the 25 months of the
study period even in the moderately dry period in early
2008 and in the pronounced dry spell in early 2009
when about 50% of the extractable water was exhausted
in the upper soil (Fig. 3). The spatial variability of topsoil moisture in the roof plots was low demonstrating
the uniform throughfall displacement by the roofs (see
Figure S1). Temporal moisture variation was higher in
the control plots (topsoil and subsoil) than in the root
plots, in particular in the second desiccation phase
(Fig. 3).
Soil desiccation effects on ANPP

In the experiments first year (June 2007 to June 2008)
with only mild soil desiccation, the production of stem
wood, leaf litter and other fine litter components
(aboveground tree biomass production, ANPP) was not
significantly different between the roof and control
plots (Table 2). The annual growth of stem and branch
wood (control: 5.8 0.2 Mg ha1 yr1; roof: 5.4 0.5
Mg ha1 yr1) and leaf litter mass (control:
6.2 0.6 Mg ha1 yr1; roof: 5.9 0.2 Mg ha1 yr1)
were of similar size and not different between the two
treatments. Other fine litter fractions (mostly flowers,
fruits and epiphytes) amounted to 1.2 Mg ha1 yr1 in
the roof and control plots. For the experiments first
year, we calculated ANPP rates of 13.2 0.8 and
12.5 0.5 Mg ha1 yr1 in the control and roof plots
(stranglers not included).
In the experiments second year (June 2008June
2009) with marked soil desiccation, the ANPP in the
control plots (6.9, 5.8 and 1.8 Mg ha1 yr1 for stem
wood production, leaf litter mass and other fine litter
mass; ANPP: 14.5 Mg ha1 yr1) was not different
from previous years productivity. In the roof plots, in
contrast, stem and branch wood growth decreased by
(a)
(b)
(c)
(d)
(e)
Fig. 3 Daily rainfall amounts (a), relative air humidity (RH) and atmospheric vapour pressure deficit (VPD; measured at 16 m height
in a forest gap; b,c), and volumetric soil water content (VWC) expressed as volume fraction in 00.5 and 0.53.0 m soil depth (d,e). For
RH and VPD, daily means and the extremes are given. The first phase of the desiccation (8 months duration) with about 60% of
throughfall reduction and the second phase with ca. 80% throughfall reduction (17 months) are indicated.
Table 2 Annual net primary production (above- and belowground compartments) (in Mg dry mass ha1 yr1) during the first
and second year of the desiccation experiment in the control and roof plots (means 1 SE of n = 3 plots each). Different letters indicate significant differences between control and roof plots for the respective year (P < 0.05). The wood increment of the Ficus stranglers could not be determined
First year
Fraction
Control
Leaves
Other fine litter fractions
Stems and branches
Total aboveground
Fine roots
Stand total
6.19
1.19
5.84
13.21
1.76
14.97

Second year
Roof
0.63a
0.05a
0.22a
0.83a
0.28a
0.73a
5.93
1.17
5.41
12.50
1.96
14.46
Control

0.21a
0.18a
0.52a
0.52a
0.29a
0.43a
5.83
1.78
6.87
14.48
0.86
15.34

Roof
0.56A
0.05A
0.38A
0.45A
0.19A
0.35A
5.21
1.68
3.95
10.83
0.79
11.62

0.16A
0.15A
0.49B
0.24B
0.19A
0.41B
more than 40% compared to the control (4.0 vs.
6.9 Mg ha1 yr1, P < 0.05) and by about 27% relative
to the first year. Similar relative growth reductions
were found when the two most abundant tree families,
Fagaceae and Sapotaceae, were excluded. In contrast,
leaf litter mass and the remaining fine litter fraction
were not significantly reduced (Table 2). ANPP was by
25% lower in the roof than the control plots in the second year (P < 0.05).
The temporal fluctuation in leaf litter fall from May
2007 to January 2009 was similar in the roof and control
plots; significant treatment differences (positive or negative) occurred only in a minority of sampling intervals
with a higher significance in the second year and the
rewetting phase (Fig. 4). However, the annual amount
of leaf litter was not significantly reduced (P > 0.05;
Table 2).
The monitoring of stem diameter increment in the 60
trees of the three roof plots with variable species identity, tree height and DBH allowed searching for biometric, growth-related and phylogenetic factors that might
determine the drought sensitivity of radial stem
growth. We used the relative reduction in basal area
increment from the first (mild desiccation) to the second year (strong desiccation) as a measure of growth
sensitivity in the 60 investigated roof plot trees of 45
species. Contrary to expectation, wood specific gravity
and tree height had no significant influence on the magnitude of growth reduction in the experiments second
year (Table 3). The most influential factor was the relative basal area increment in the 1st year (P < 0.001),
followed by DBH (P = 0.017), that is, basal area increment per existing basal area (or specific cambial activity) and the size of the stem cambium (stem diameter)
determined the extent of growth reduction and not tree
height. Interestingly, only relative stem growth rate,
but not the absolute amount of wood production in the
first year (P = 0.131; Table 3), determined the desiccation sensitivity of radial growth.
The tree inventory before the start of the desiccation

recorded 123 tree species from 42 families with Fagaceae contributing by ca. 23% to stand AGB (averaged
over roof and control plots), Sapotaceae by 18%, Moraceae 13% (mostly occurring in control plots), Lauraceae
8%, Myrtaceae 4%, and Euphorbiaceae and Meliaceae
by 3% each (Fig. 5a). The two families with largest contribution to stand AGB (Fagaceae and Sapotaceae with
both >15%) were also most important in terms of ANPP
in the first desiccation year and showed the largest
absolute reduction in stem wood increment during the
second year (Fig. 5b) (Fagaceae: from >1.7 Mg ha1
yr1 in the first year to <0.5 Mg ha1 yr1; Sapotaceae:
from ca. 1.0 to ca. 0.6 Mg ha1 yr1). The families differed largely with respect to the growth reduction from
the 1st to the 2nd year, ranging from a reduction to the
half to a doubling of productivity upon soil desiccation.
The variability among the families responses appeared
to be largest in the rare families with highest productivity reduction in the Annonaceae, Rubiaceae, Clusiaceae
and Magnoliaceae, but increases in the dry second year
Table 3 Results of linear mixed-effects model runs examining the dependence of the relative change in basal area increment of individual trees from the first to the second year on
six biomass- or growth-related traits. Given are the difference
in the Akaike Information Criterion of the models (dAIC), the
likelihood ratio (L-ratio) and the P-value
Parameter
Wood density
Tree height
AG tree biomass*
AG wood production
1st year*
DBH
Relative basal area
increment in 1st year
Unit
dAIC
3
g cm
m
kg tree1
kg tree1
yr1
cm
%
L-ratio
1.748
0.519
0.097
0.276
0.252
2.519
1.903
2.277
0.615
0.113
0.168
0.131
3.741
28.431
5.741
30.431
0.017
<0.001
*log transformed.
Fig. 4 Time course of leaf litter fall during the desiccation experiment (June 2007May 2009) in the roof and control plots (means SE
of n = 3 plots). Significant differences between the treatments are marked with asterisks (P < 0.01*; P < 0.001**; P < 0.0001***).
(a)
(b)
Fig. 5 (a) Percental contribution of the 16 most abundant families to the stand total of aboveground biomass (AGB; calculated from
diameter at breast height, tree height and wood density for all trees per plot). Data from the 1st census before the start of the desiccation
(numbers in parentheses behind the families indicate the sample size for the mean of the six plots). (b) Absolute change in annual wood
production in the 16 most abundant families in the three roof plots from the first (60% throughfall displacement) to the second year of
the desiccation (80% displacement; calculated from AGB and repeated dendrometer tape readings; negative change = growth reduction, positive change = growth increase). Numbers in parentheses behind the families indicate the number of trees per family in the
three roof plots equipped with dendrometers. Only families with more than 1% contribution to AGB are considered*; aboveground
wood production of stranglers (Moraceae) was not determined. *Families with less than 1% contribution to stand basal area are given
with the total number of trees in all six plots (nall) and the number of dendrometer trees in the roof plots (nden-roof) as (nall/nden-roof):
Aceraceae (2/0), Apocynaceae (2/0), Araliaceae (1/0), Arecaceae (7/0), Chrysobalanaceae (1/0), Cyatheaceae (18/1), Dracaenaceae
(14/0), Escalloniaceae (16/0), Gesneriaceae (5/0), Himantadraceae (3/0), Juglandaceae (1/0), Leguminosae/Mimosoideae (17/0),
Magnoliaceae (5/0), Melastomataceae (2/0), Monimiaceae (18/0), Myrsinaceae (6/0), Oleaceae (4/0), Pandanaceae (13/0), Rhizophoraceae (1/0), Rutaceae (21/1), Sabiaceae (8/0), Sapindaceae (18/0), Staphyleaceae (9/0), Sterculiaceae (2/0), Theaceae (2/0), Verbenaceae
(1/0).
in the Rosaceae and Asteraceae on the other hand. The

two most abundant families in terms of biomass (Fagaceae and Sapotaceae) suffered productivity reductions
of about 40 and 75% and thus showed average sensitivities among the 42 families.
Tree mortality rate was not significantly different
between the roof and control plots during the entire
study period (May 2007 to June 2009: 2.6 1.3% and
2.1 0.4% yr1, respectively).
Soil desiccation effects on standing fine root biomass and

fine root growth
The fine root inventory in each two soil pits per plot
before the start of the desiccation and at the experiments end showed a significant reduction in fine root
density in 2040 cm soil depth (from 279 to 52 g m3,
P < 0.01) and a nonsignificant decrease in the 020 cm
layer (from 1404 to 1024 g m3, Fig. 6). The decrease in
live fine root mass was accompanied by an increase in
dead fine root mass which was about 6-times larger at
the end of the experiment in the topsoil (020 cm) of
the roof plots than the control plots. In lower horizons,
no fine root biomass reduction was detected (the resampling was restricted to the 0120 cm profile). The fine
root biomass profile total (0120 cm) decreased signifi 2013 John Wiley & Sons Ltd, Global Change Biology, 20, 14811497
cantly (by 56%; P < 0.01) in the roof plots and by 24% in
the control plots (P < 0.05). The ingrowth core
approach gave a fine root production estimate of ca.
1.76 Mg ha1 yr1 in the control and ca. 1.96 Mg ha1
yr1 in the roof plots in the experiments first year. In
the dry second year, the estimated productivity was
0.86 and 0.79 Mg ha1 yr1 in the control and roof
plots, respectively (difference between years significant
at P < 0.05, but no significant difference between the
treatments) (Table 2).
Discussion
Drought sensitivity of ANPP

The STEE experiment is the first drought simulation
experiment in a tropical forest outside eastern Amazonia and the first in a tropical perhumid climate where
drought stress is, in contrast to semihumid eastern
Amazonia, rare and unpredictable and mostly related
to strong ENSO events (Walsh & Newbery 1999). It has
been postulated that trees growing in an aseasonal wet
climate are lacking costly morphological and anatomical adaptations to cope with drought stress rendering
them more vulnerable to erratic droughts (Phillips
et al., 2010). In contrast to the two Amazonian experi-
Fig. 6 Comparing the vertical fine root biomass and necromass distribution to 120 cm soil depth before (February 2007) and immediately after the desiccation (June 2009). Given are means 1 SE, *** indicates a significant difference in fine root biomass between roof
and control for a distinct soil depth and sampling time.
ments at Tapaj
os and Caxiuan~
a, STEE was conducted
as a replicated experiment (n = 3 at the plot level)
enabling statistical testing of the roof effect and thereby
increasing the rigour of analysis. Working in a
perhumid environment with more than 2500 mm of
rain per year required a very effective rainfall displacement system that was able to reduce the throughfall by
ca. 80%. The operation of this construction at a remote
site was very labour-intensive and forced us to terminate the desiccation phase after 25 months, which was
long enough to produce a marked growth reduction
but did not lead to elevated tree mortality. The discussion of the results thus focuses on desiccation effects on
important above- and belowground productivity
components, fine root mortality and carbon allocation
shifts in a sublethal pre-dieback phase of the drought
response.
The tree mortality rates in the two treatments of STEE
(2.6 and 2.1% per year) were in the range of values
reported from other tropical moist forests without
excessive drought stress (e.g. Condit et al., 1995). Mortality did not increase in the roof plots in the 25-month
soil desiccation period indicating that our experiment
did not last long enough for driving sensitive trees
towards dieback. In support of this assumption, Brando
et al. (2008) observed a significantly higher tree mortality in the roof plot of the Tapaj
os experiment only in
the experiments third year with peak mortality rates as
high as 9.5% yr1; in the Caxiuan~
a experiment, significantly elevated dieback occurred only in the 5th year
(da Costa et al., 2010). While in natural droughts, most
mortality effects occurred within 9 months of the
drought (Phillips et al., 2010), a lag phase of 24 years
seems to be characteristic for throughfall displacement

experiments in tropical forests. This indicates that the
simulated droughts apparently were less severe than
natural ones in which the evaporative demand is much
higher.
With respect to aboveground productivity, the experimental desiccation of the Pono forest for 25 months
suggests that this perhumid forest may not be more
drought-sensitive than the two semihumid Amazonian
forests when exposed to comparable soil desiccation
(REW falling below the 0.4 threshold in the topsoil and
<0.8 in the subsoil) (Nepstad et al., 2007; Brando et al.,
2008; da Costa et al., 2010). First, our finding of an average wood production reduction by 40% during the
severe desiccation in the second year compares well
with the responses of the Tapaj
os forest (13% in the
1st year, up to 62% subsequently) and the Caxiuan~
a
forest (30%; Brando et al., 2008; da Costa et al., 2010).
Second, leaf litter fall was rather insensitive to soil drying in the Pono forest with no lasting deviation from
the control plots in the first 22 months of the experiment. Significantly reduced litter masses in the roof
plots were detected only on a few sampling dates, but
more frequently during the second study year and during the experiments rewetting phase. This matches
well with the desiccated Tapaj
os forest that responded
with litter fall reduction only from the third year
onwards (Nepstad et al., 2007). The absence of droughtinduced litter fall peaks in both the Pono and the Tapaj
os forests suggests that drought-affected tropical
moist forest trees may respond with stress-induced premature leaf shedding only after a lag phase that may be
longer than leaf lifespan.
Unexpected was the about 50% higher (nonleaf) fine
litter production in the experiments second year in
Pono. Since it was observed in both the roof and the
control plots, the increase likely is an expression of an
irregular mass flowering and fruiting event in this aseasonal forest, as it was observed in 2008 in particular in
the abundant Lithocarpus trees in the plots. The plus in
fruit production measured in the second year nearly
equalled the minus in fine root production in the roof
and control plots in that year pointing at a shift in allocation priorities that was independent from soil desiccation.
The principal comparability of the Pono forest and
the two Amazonian forests in terms of the ANPP
drought response astonishes, given the large differences in species composition and precipitation regimes.
While the reduction in REW was roughly comparable
in the three experiments, the Pono forest was exposed
to a shorter desiccation period and thus was lacking
certain tree reactions. It appears that the mean response
of tropical rainforest trees to sublethal drought stress is
not that different in the Neo- and Paleotropics, even
though large differences in the species response may
exist (see below). This leads us to the rejection of our
first hypothesis on the higher drought sensitivity of
trees in perhumid forests as compared to preadapted
species from semihumid forests (e.g. Phillips et al.,
2010). Clearly, this hypothesis was derived from field
observations on tree mortality during natural droughts
and did not consider growth responses of nondying
trees. Nevertheless, drought-induced growth sensitivity
and eventual dieback of a tree should be related
because the reasons for reductions in growth and overall tree vitality, for example, hydraulic failure, carbon
starvation or pathogen attack (McDowell et al., 2008)
should essentially be the same. Our results also do not
support the assumption that trees in South-East Asian
tropical forests should be more drought-sensitive than
Amazonian trees.
Extrapolating the results of throughfall manipulation experiments to the natural situation with regularly and irregularly occurring droughts must be
done with care. A main shortcoming of experiments
with subcanopy roofs is that only the soil is desiccated but not the atmosphere. This has the inevitable
consequence that the physiological effect of a natural
drought must be larger than that of a simulated
drought at equal rainfall reduction, because tree
water status and cambial growth is controlled not
only by soil moisture availability but also by the
atmospheric vapour pressure deficit and radiative
forcing (K
ocher et al., 2012). Furthermore, natural
drought periods are usually associated with higher
radiation loads than normal, which either can
stimulate photosynthesis when soil desiccation is

only mild, or may expose the canopy to heat stress.
This experimental shortcoming is well demonstrated
by the situation in Pono forest where the soil
remained clearly below the assumed critical threshold of 0.4 REW for about 17 months, while the daily
mean of relative air humidity in the canopy
remained at 88% and never dropped below 62% in
this period. Thus, we assume that the continuously
high air humidity during the experiment, in sharp
contrast with natural droughts, must have reduced
the drought stress exposure of the trees markedly
through transpiration reduction, increases in leaf and
stem water potential, and perhaps direct foliar water
uptake as it was observed in trees of subtropical climates (Yates & Hutley, 1995; Breshears et al., 2008;
Cassana & Dillenburg, 2013; Eller et al., 2013; Goldsmith et al., 2013). This would be one explanation
why the 25-month soil desiccation in STEE did not
result in elevated tree mortality rates while even
shorter ENSO-related droughts as in 1997/1998 did
(Aiba & Kitayama, 2002; van Nieuwstadt & Sheil,
2005). Such an experimental artefact must be particularly severe in humid and perhumid environments
where the simulated soil desiccation is not enhanced
by a naturally occurring dry season as in eastern
Amazonia. Even though we achieved a more effective soil desiccation (in the 2nd year ca. 80% of
throughfall exclusion and ca. 150 mm soil moisture
reduction in the 02 m profile) than in the Amazonian experiments [rainfall: minus 35 to 50%; soil
moisture: minus ca. 100 mm (Tapaj
os)], it is likely
that due to the permanently high air humidity, the
stress exposure in the first 2 years of STEE was not
greater than in the Amazonian experiments.
Drought effects on the fine root system and root/shoot

carbon partitioning
The repeated fine root inventory before and after the
desiccation revealed a reduction in standing fine root
biomass by 56% (from ca. 500 to <250 g m2 in the profile to 1.2 m) and a tripling of fine root necromass (0
1.2 m) in the 27-month period. The shift from live to
dead fine root mass was most pronounced in the upper
soil (040 cm) pointing to drought-induced fine root
mortality that significantly reduced the size of the fine
root system. Thus, fine root mortality appears to be
similarly sensitive to soil desiccation as is wood
production in the studied trees.
The results of the ingrowth core study gave no indication of a compensatory increase in fine root production as a response to soil desiccation in the roof plots. A
relative shift in the allocation of assimilates and
nutrients towards root growth under conditions of
water shortage is predicted by the functional balance
hypothesis (Thornley, 1972a,b; Bloom et al., 1985) but is
not supported by our root biomass and root production
data. Similarly, Metcalfe et al. (2010) found no indication of a greater relative investment of total NPP in root
growth in the Caxiuan~
a forest upon drought exposure.
Clearly, our root data cover only the uppermost 1.2 m
(or 3 m) of the profile and ignore the deeper subsoil.
However, we have no quantitative information on
deep-reaching sinker roots that were found to extend to
more than 8 m in the deeply weathered forest soils of
semihumid eastern Amazonia (Nepstad et al., 1994).
For the very deep soils of Tapaj
os National Forest, soil
hydrological modelling indicated that layers below
5.5 m depth had an increasing importance for water
uptake only in the second and third year of the desiccation adding up to 12% of total water uptake, but that
the overall contribution of these layers remained
remarkably small and declined to near zero in the following years (Markewitz et al., 2010). While at least the
dominant tall Fagaceae Castanopsis acuminatissima may
possess sinker roots, in the rugged mountainous terrain
of Central Sulawesi, it is unlikely that the weathering
front and maximum rooting depth are as deep-reaching
as in parts of the Amazonian lowlands.
From the Amazonian experiments, it was concluded that tree mortality increases when the water
resources in the deep soil are depleted. Due to
lacking data on root water absorption in STEE, some
hints on the role of deep roots for stand water
uptake may be obtained from subsoil moisture
dynamics. Apparently, significant amounts of water
were extracted from deeper soil layers (0.53.0 m)
only from February to April 2009 after a rainless
period in December 2008 and January 2009 when
the topsoil matric potential approached 1.5 MPa in
the roof plots and root water uptake shifted downwards in the profile. The high soil matric potential
(>0.1 MPa) at 0.53.0 m depth in this period suggests that deep-reaching roots should continuously
have had access to easily available moisture despite
severe topsoil desiccation. However, when considering that 80% of the fine root biomass is located in
the top 40 cm of the profile and this part of the root
system suffered dieback and may mostly have lost
its water uptake function in the dry soil, it is
astonishing how the trees survived with a greatly
reduced fine root surface area without shedding
leaves. Uptake studies with tracers have to show
whether deep roots can fully compensate such losses
in absorbing surface area and how nutrient supply
is affected by topsoil desiccation (e.g. Kreuzwieser &
Gessler, 2010).
Traits determining drought sensitivity in the trees

It has been hypothesized that wood specific gravity
(q) is a determinant of the drought sensitivity of trees
due to the typically negative relation between q and
vessel diameter in the stem xylem (Preston et al.,
2006; Fan et al., 2012; McCulloh et al., 2012). Phillips
et al. (2010) concluded that the risk of drought mortality in tropical trees is the higher the lower wood
specific gravity is, even though the relation was
found to be rather weak. In the Pono forest, however,
q had no influence on the drought sensitivity of wood
production in the 60 trees from 45 species monitored
in the roof plots. Possible explanations for the lacking
wood density influence are (i) that vessel diameter
and pit pore width may vary largely for a given
wood density (Zanne & Falster, 2010), (ii) the range
of wood specific gravities encountered in this study
(0.34 to 0.77 g cm3) may have been too small for a
significant effect, or (iii) other factors than q are more
important determinants of drought sensitivity in these
trees. Our analysis showed that tree size was a structural factor with negative influence on the rate of
wood production in the dry second year, but the
effect of stem diameter (P = 0.017) was much stronger
than that of tree height itself which was insignificant
(P = 0.113). This suggests that it is not the greater
canopy exposure to excessive light and higher atmospheric evaporative demand that led to the higher
drought sensitivity of wood production in the bigger
trees. Rather, a higher stem cambial activity (reflected
by a higher relative basal area increment) resulted in
stronger growth reductions with the trees with fastest
diameter growth under moist conditions suffering
most (see Table 3). The larger influence of DBH than
tree height on the sensitivity of wood production
becomes plausible when considering that trees with
higher radial growth rate should typically achieve
also larger diameters than slower growing trees,
while faster diameter growth leads often, but not
always to greater height. This suggests that the
growth reduction observed in our experiment was
more likely caused by direct effects of soil desiccation
on stem cambial activity than by mechanisms mediated indirectly through height-dependent effects, flow
path length or canopy exposure.
The observed large differences in the drought sensitivity of wood production among different plant families seem to indicate that the vulnerability is in part
determined by phylogeny and/or species identity. The
tall and abundant Fagaceae Castanopsis acuminatissima
was among the species with medium to large growth
reduction in the second year. One may speculate that
this is related to the particularly large vessel diameters
in the stem xylem in this species (Schuldt et al., 2013).
Investigations on the carbohydrate supply and hydraulic functioning of trees from tropical perhumid forests
that were exposed to soil desiccation have to reveal the
underlying mechanisms leading to the registered wood
growth reduction.
The Sulawesi Throughfall Exclusion Experiment
(STEE) is only the third experiment on the drought
response of tropical forests, the first in a perhumid
climate and also the first outside eastern Amazonia.
Even though the desiccation lasted only for
25 months, that is, shorter than in the Amazonian
experiments, and the climatic, edaphic and phylogenetic conditions were largely different, we found
remarkably similar growth and allocation responses
among the trees in Sulawesi and Amazonia pointing
at common elements in the drought response of neoand paleotropical trees. On the other hand, STEE
revealed marked phylogenetic differences in the
responsiveness at the community level as where
observed in the Amazonian experiments. Our results
point to a higher growth sensitivity of trees with fast
diameter growth when moisture is not limiting; however, sensitivity was not higher in trees with lighter
wood. The greater suppression of fast-growing species
should lead in the long run to a forest community
with dominance of slower growing species, either
through competitive exclusion in a drier climate with
altered competitive hierarchies, or through higher
drought-induced mortality. We are less optimistic than
earlier authors about the potential for identifying precise soil moisture or rainfall minimum thresholds
beyond which tropical forests should encounter catastrophic dieback. More than in the Amazonian experiments, STEE has revealed the limitations of
throughfall exclusion experiments where dry soil
meets a relatively moist atmosphere that cannot be
manipulated. Continuous soil desiccation for 2 years
(Sulawesi) to 67 years (Amazonia) is far from the
reality in natural droughts that typically develop faster
than in the experiment because the atmosphere is dry
and cloudless. Rapid stress development with relatively short duration (as in natural droughts) and
more gradual stress development with long duration
(experiments) require different plant responses.
Acknowledgements
This study was part of the German-Indonesian collaborative
research project SFB 552: Stability of Rain Forest Margins in
Indonesia funded by the German Research Foundation
(DFG). The financial support is gratefully acknowledged. We
thank the inhabitants of Toro village for their hospitality,
Thomas Kl
uter and Hilmar M
uller and their team of local
workers for the roof construction and its maintenance, our
local aides for their support during the fieldwork, S. Erasmi

for LAI data, H. Culmsee for tree species data, O. van
Straaten and M. K
ohler for data on soil chemistry and soil
water status and the Indonesian Research Foundation LIPI
and the authorities of the Lore Lindu National Park for the
research permission.
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Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Figure S1 Maps of the mean volumetric soil water content
in the six plots (uppermost 30 cm) according to weekly measurements with a mobile TDR system (each 100 measurements per plot and occasion). Given are the averages of the
experiments second phase (January 1, 2008 to May 7, 2009).

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Global Change Biology

Global Change Biology (2014) 20, 14811497, doi: 10.1111/gcb.12424

Replicated throughfall exclusion experiment in an

2013 John Wiley & Sons Ltd

For South-East Asia, a warming by about 2.5 K until

Accordingly, a third of the 95 completed precipitation

Material and methods

measured on a 16 m high tower in a small forest gap close to

The desiccation began on May 1, 2007, and lasted for about

An automatic weather station installed on a 16 m high tower

Trees 210 cm DBH

Climatic and soil moisture measurements

lightning strike) encountered at this remote site (about 4 km

Aboveground stand structure, biomass and productivity

where AGB is the estimated aboveground biomass (in kg per

Analysis of vertical fine and coarse root distribution

Estimation of fine root production

Comparability of study sites and temporal development of

and led to a progressive decrease in volumetric soil

Soil desiccation effects on ANPP

The tree inventory before the start of the desiccation

in the Rosaceae and Asteraceae on the other hand. The

Soil desiccation effects on standing fine root biomass and

Drought sensitivity of ANPP

seems to be characteristic for throughfall displacement

stimulate photosynthesis when soil desiccation is

Drought effects on the fine root system and root/shoot

Traits determining drought sensitivity in the trees

local aides for their support during the fieldwork, S. Erasmi

(Winteraceae). New Phytologist, 199, 151162.

Biology, 13, 118.

warming. Geophysical Research Letters, 33, 15.

terocarp forest. Biotropica, 44, 606617.

Leuschner C, Hertel D, Coners H , B

Schuldt B, Leuschner C, Brock N, Horna V (2013) Changes in wood density, wood

Amazon drought. Science, 331, 554.

Sheil D, May RM (1996) Mortality and recruitment rate evaluations in heterogeneous

Wu Z, Dijkstra P, Koch GW et al. (2011) Responses of terrestrial ecosystems to

tion. Global Change Biology, 17, 927942.

Veldkamp E, OBrien JJ (2000) Calibration of a frequency domain reflectometry sensor

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