Professional Documents
Culture Documents
Abstract
Agroforestry systems may play a critical role in reducing the vulnerability of farmers
livelihood to droughts as tree-based systems provide several mechanisms that can mitigate
the impacts from extreme weather events. Here, we use a replicated throughfall reduction
experiment to study the drought response of a cacao/Gliricidia stand over a 13-month period.
Soil water content was successfully reduced down to a soil depth of at least 2.5 m. Contrary to
our expectations we measured only relatively small nonsignificant changes in cacao (11%)
and Gliricidia (12%) sap flux densities, cacao leaf litterfall ( 1 8%), Gliricidia leaf litterfall
(2%), soil carbon dioxide efflux (14%), and cacao yield (10%) during roof closure.
However, cacao bean yield in roof plots was substantially lower (45%) compared with
control plots during the main harvest following the period when soil water content was
lowest. This indicates that cacao bean yield was more sensitive to drought than other
ecosystem functions. We found evidence in this agroforest that there is complementary use
of soil water resources through vertical partitioning of water uptake between cacao and
Gliricidia. This, in combination with acclimation may have helped cacao trees to cope with the
induced drought. Cacao agroforests may thus play an important role as a drought-tolerant
land use in those (sub-) tropical regions where the frequency and severity of droughts is
projected to increase.
Keywords: cacao yield, CO2 efflux, fine root biomass, leaf litterfall, plant water uptake, sap flux, shade
trees, soil water, throughfall reduction
Introduction
Rain-fed agriculture is the main source of income in
many developing countries and is vulnerable to the
occurrence of droughts. If changes in precipitation and
temperature occur, this will directly affect the rural
population that depends on rain-fed agriculture (Slingo
et al., 2005). Some climate scenarios for the (sub-) tropics
predict that extreme weather events like drought
1515
1516 L . S C H W E N D E N M A N N et al.
episodes will become more frequent and severe, and
average precipitation may decrease (Sheffield & Wood,
2008). To reduce the impact of droughts on the rural
population it may be necessary to adapt land use
practices to address such future climatic conditions.
Recent publications suggest that diversified and sustainable production systems such as tree-based systems
(e.g. agroforestry) may be more resilient to extreme
climatic conditions than annual crops and tree crop
monocultures as they have several mechanisms to reduce the impact of droughts such as buffering of
humidity, and reduction of air and soil temperature
extremes (Verchot et al., 2007; Lin et al., 2008). Agroforestry systems may thus play a critical role in minimizing the vulnerability of farmers livelihoods to extreme
weather events.
Cacao (Theobroma cacao L.), a neotropical understory
rain forest species, is one of the most important perennial cash crops world wide, and cultivated in the
tropical areas of Central and South America, South-East
Asia and Africa. Millions of farmers, mostly smallholders, depend on cacao for their livelihoods. Traditional cultivation systems are established by planting
cacao under primary or older secondary forest with
minor modifications to the original forest canopy.
Nowadays, however, cacao cultivation takes place in a
range of management systems from shaded agroforests
(under remaining forest cover or planted shade trees) to
nonshaded monocultures (Rice & Greenberg, 2000).
Cacao stands are often established with fast-growing
nitrogen-fixing tree species such as Gliricidia spp. or
Erythrina spp. While recognizing the advantages that
intercropped shade trees provide young cacao plants,
farmers often remove these shade trees after cacao
begins to bear fruit as they fear that competition between cacao and shade trees for water and nutrients
may lower cacao yield (Purseglove, 1968; Alvim, 1977;
Belsky & Siebert, 2003). Although the combination of
crops with shade trees holds the risk of competition
both for aboveground (light) and belowground (water
and nutrients) resources, these risks may be reduced by
the choice of the shade tree species and/or appropriate
management practices (Beer, 1987). Belowground competition for water may for instance be minimized by
planting shade tree species which shed their leaves
during the drier season (Broadhead et al., 2003), or
which take up their water from different soil horizons
than crops (van Noordwijk et al., 1996).
Several studies indicate that water availability affects
key functions of the cacao plant. Results from a field
experiment by Rada et al. (2005) showed that severely
stressed 4-year-old cacao plants (25 days without water)
had the lowest leaf transpiration rates and considerably
lower stomatal conductance as compared with control
Study site
The experimental site was located in the vicinity of
the village of Marena in the Kulawi Valley, Central
Sulawesi, Indonesia (1.5521S, 120.0201E) at 560 m a.s.l.
Average annual precipitation in the region is 2092 mm
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
(measured at the Gimpu meteorological station between
20022006, about 5 km south of Marena at 417 m a.s.l.;
H. Kreilein, O. Panferov & G. Gravenhorst, unpublished
results) and shows a weak bimodal pattern. The mean
annual temperature is 25.5 1C.
We selected a site where we anticipated there would
be no influence of ground water. The water table at this
site was o4.5 m depth as estimated with piezometers.
The soil was classified as a Cambisol with a sandy loam
texture and a high stone content (30%) in the subsoil
(D. Leitner & B. Michalzik, unpublished results). The
main soil physical and chemical characteristics are
summarized in Table 1.
The cacao/Gliricidia agroforest stand was established
in December 2000 on former upland rice and maize
fields planting cacao saplings and Gliricidia sepium
1517
Table 1 Soil texture, bulk density, carbon and nitrogen concentration, effective cation exchange capacity (ECEC), and pH (H2O) at
the experimental site at different depths, Marena, Central Sulawesi
Soil texture
Depth (m)
Sand (%)
Silt (%)
0.00.05
0.050.1
0.10.2
0.20.4
0.40.75
0.751.5
1.52.5
60.2
55.0
55.7
53.9
57.9
68.7
70.3
27.0
29.7
28.2
26.5
22.8
19.4
22.8
3.4
2.1
0.9
4.8
2.3
5.3
7.1*
2.5
3.6
3.0
3.3
3.4
3.0
6.4*
Clay (%)
Bulk density
(g cm3)
12.8
15.3
16.1
18.6
19.3
11.9
6.9
1.25
1.28
1.31
1.32
1.37
1.52
1.60
2.2
2.4
3.5
2.9
3.3
4.4
2.3*
0.04
0.04
0.02
0.05
0.09
0.10
0.06
Carbon
(g kg1)
16.5
12.6
7.0
4.4
3.3
1.9
0.8
3.1
4.0
1.4
0.5
0.4
0.5
0.1w
Nitrogen
(g kg1)
1.51
1.13
0.64
0.43
0.37
0.29
0.21
0.22
0.31
0.10
0.03
0.04
0.03
0.02w
ECEC
(cmol kg1)
8.78
7.77
7.57
5.47
7.70
8.86
11.38
2.30
1.52
1.45
0.87
3.46
1.70
5.00w
Soil pH
(H2O)
5.9
6.0
6.1
5.9
5.9
5.9
6.1
0.4
0.4
0.4
0.2
0.3
0.2
0.7w
Table 2 Stem density, height and diameter, and leaf area index (LAI) of cacao, Gliricidia, and coconut in control and roof plots,
Marena, Central Sulawesi
Gliricidia
Cacao
Parameters
Units
Control
Stem density
Height
Diameter*
LAIw
Trees ha1
m
cm
m2 m2
1038
4.5
9.5
3.5
67
0.1
0.2
0.4
Roof
1022
4.6
9.5
4.1
Control
68
0.1
0.6
0.4
279
9.7
12.5
1.30z
15
1.6
1.0
0.1
Coconut
Roof
371
10.6
13.0
1.33z
46
1.1
0.5
0.1
Control
Roof
43 22
11.2 1.3
34.4 5.7
nd
48
8.3 2.3
21.8 9.7
nd
Measurements were conducted between August and December 2006. The values are means SD; n 5 3 per treatment.
*Stem diameter was measured at 0.8 m (cacao) and 1.3 m (Gliricidia).
wTrue LAI (LAItrue) values were derived from hemispherical photographs taken with a digital camera (Coolpix S3 with EC-F8
fisheye lens, Nikon Corp.) at 1 and 5 m height at 12 points located on a rectangular grid (10 m 12.5 m) in each plot. WinScanopy
(Regent Instruments Inc., Sainte-Foy, QC, Canada) was used for photograph analyses and the effective LAI (LAIeff) for a zenith angle
of 57.51 was calculated after Bonhomme & Chartier (1972); LAItrue was calculated as LAItrue 5 LAIeff/CI; the clumping index (CI)
was calculated for each photograph after Lang & Xiang (1986).
zGliricidia and coconut.
nd, no data.
r 2009 Blackwell Publishing Ltd, Global Change Biology, 16, 15151530
Samples were taken in December 2006 (pretreatment) and June 2008 (post-treatment). The values are means SD (n 5 3). No significant differences in fine root biomass were
found between control and roof plots in a given period and between sampling dates (ANOVA, Tukeys HSD, Po0.05).
Fine root biomass (diameter o2 mm) and vertical rooting pattern were investigated by excavating two soil pits per plot to 3 m depth. Minimum distance of the soil pit to the
closest stem was 1 m. In each soil pit monoliths of 0.5 m 0.5 m 0.2 m were taken at 0.2 m depth intervals. Roots were sorted in living and dead fine root fractions of cacao,
Gliricidia and coconut. The root biomass was expressed as g root biomass m2 per 0.2 m depth interval, which is equivalent to 0.2 g m3.
52.2 25.1
37
2.2
87.8 31.9
78
2.4
79.7 23.5
76
2.2
63.4 30.2
31
2.4
78.6 30.2
34
2.4
118.5 83.5
83
2.4
Roof
Control
Control
Control
Roof
Gliricidia
Cacao
Roof
Cacao
91.9 62.4
96
2.2
Biomass (g m2)
Proportion of fine roots at 00.4 m depth (%)
Maximum root depth (m)
Fine root biomass (diameter o2 mm) of cacao and Gliricidia in control and roof plots, Marena, Central Sulawesi
Table 3
Gliricidia
Experimental design
Control
Roof
61.8 17.3
35
2.4
1518 L . S C H W E N D E N M A N N et al.
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
1519
Fig. 1 Picture (a) above and (b) below roof, throughfall reduction experiment, Marena, Central Sulawesi, Indonesia.
SWSj SWSmin
;
SWSmax SWSmin
1520 L . S C H W E N D E N M A N N et al.
species were collected from control and roof plots during
the pretreatment period (February 2007). Suberized twigs
approximately 10 mm in diameter and 50 mm long were
cut from the canopy. Bark was removed to avoid contamination of xylem water with phloem water. Soil
samples were taken directly below the canopy of each
tree at the following intervals: 00.1, 0.10.3, 0.30.5, 0.5
0.7, and 0.71.0 m. Twigs and soil samples were placed
into 40 mL glass bottles, closed with a Teflon coated lid,
wrapped in Parafilm, and then kept frozen until water
extraction. Water was extracted from plant and soil
samples by cryogenic vacuum extraction (Ehleringer &
Osmond, 1989). Hydrogen isotopic composition was
measured by injecting the extracted water into a hightemperature elemental analyzer (TC/EA, Thermoelectron cooperation, Breman, Germany) coupled via a ConFlo III interface to a Delta V Plus isotope ratio mass
spectrometer (Thermo-Electron Cooperation) (Gehre
et al., 2004). Deuterium isotope ratios were expressed in
% relative to Vienna Standard Mean Ocean Water. Measurement precision was 2%. Analyses were carried out at
the Center for Stable Isotope Research and Analysis
(KOSI, Georg-August-University, Gottingen, Germany).
The isotopic composition of plant water was then compared with soil water at multiple depths in order to
identify the best match based on direct inference (Brunel et al., 1995).
Data analyses
We divided the observation time into three periods:
pretreatment (February 2007), treatment (March 1,
2007April 10, 2008), and post-treatment (April 11,
2008June 5, 2008). For all parameters, except
stand transpiration, mean values were calculated for
each plot and sampling date. Mean values of stand
transpiration were estimated based on the nine
trees measured on control and roof plots, respectively.
Mean values were then calculated for each plot-period
combination.
Before analyses, parameters were tested for normality
using ShapiroWilks normality test. The effects of the
treatment were analyzed for each period using one-way
analysis of variance followed by Tukeys HSD post hoc
test. Regression analyses were used to examine relationships between parameters. Effects were considered significant if Po0.05. All statistical analyses were carried
out using STATISTICA version 7 (StatSoft Inc., Tulsa, OK,
USA).
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
Results
1521
1522 L . S C H W E N D E N M A N N et al.
Fig. 2 Volumetric soil water content (m3 m3) in (a) 0.10 m, (b) 0.75 m, (c) in 1.50 m, (d) relative extractable water to 2 m depth, and (e)
rainfall in the control and roof plots, Marena, Central Sulawesi. (ac) Values are means SD (n 5 3). The treatment period (roof closure,
March 1, 2007April 10, 2008) is indicated by an arrow.
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
1523
Table 4 Soil water storage to 2 m depth, sap flux density of cacao and Gliricidia, stand transpiration, leaf litterfall of cacao and
Gliricidia, soil CO2 efflux, cacao yield, infection rates of black pod disease, cacao pod borer, and Helopeltis during the pretreatment
(February 2007), treatment (March 1, 2007April 10, 2008) and post-treatment (April 11, 2008June 5, 2008) period
Pretreatment
Parameters
Units
Control
mm
g cm2 day1
g cm2 day1
mm day1
g m2 2 week1
g m2 2 week1
mg C m2 h1
kg ha1 2 week1
n ha1 2 week1
n ha1 2 week1
n ha1 2 week1
495
151.8
143.8
1.4
4.7
11.9
113.1
n.d
nd
nd
nd
Treatment
Roof
27
20.3
16.6
1.5
2.8
13.7
470
151.5
154.9
1.4
4.0
15.2
130.5
n.d
nd
nd
nd
Control
24
25.3
43.6
2.0
5.4
28.0
494
166.9
151.7
1.5
9.9
14.1
131.1
26.4
58
281
206
Post-treatment
Roof
33
22.0
13.6
0.5
2.0
15.1
5.9
10
63
68
348
147.9
133.7
1.3
10.7
13.9
112.8
23.7
49
196
184
Control
26*
22.9
36.9
1.6
2.7
16.5
4.2
4
58
34
502
153.3
150.1
1.4
7.7
9.5
105.4
45.2
523
147
108
Roof
33
23.9
14.9
0.8
0.9
18.1
16.0
155
40
54
406
147.0
147.0
1.4
6.6
9.5
132.6
25.0
376
149
102
19*
34.0
46.2
0.3*
0.9
26.7
1.9*
177
61
6
Leaf litterfall
During the pretreatment period cacao leaf litterfall did
not differ significantly between roof and control plots
(Table 4). Cacao leaf shedding in roof plots exceeded
leaf loss in control plots by 22% between March and
July 2007 (P 5 0.12) (Fig. 3d). However, over the course
1524 L . S C H W E N D E N M A N N et al.
Fig. 3 (a) Soil water storage to 2 m depth, (b) sap flux density of cacao, (c) sap flux density of Gliricidia, (d) leaf litterfall of cacao, (e) leaf
litterfall of Gliricidia, and (f) soil CO2 efflux. Values are expressed as roof to control ratio (i.e. a value of 1.0 represents roof-control plot
parity, and dashed line). The lines represent the centered moving average over 30 days. The treatment period (roof closure, March 1,
2007April 10, 2008) is indicated by an arrow.
Cacao yield
During the main harvest (April to June 2008; post-treatment period) cacao yield in roof plots was reduced to
55% of that in the control plots (Table 4). Yields peaked in
May of both 2007 and 2008. Highest cacao yield (80 kg
oven-dry beans ha1 2 week1) occurred in control plots
in May 2007. Between July 2007 and March 2008 bean
yield was o20 kg oven-dry beans ha1 2 week1 in both
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
1525
Fig. 4 Gap fraction above cacao trees and sap flux density of
the same individuals in roof plots during November/December
2007. Factor 1 indicates highest gap fraction. An inverse parabolic function was used to fit the data (R2 5 0.87, R2adj. 5 0.85,
P 5 0.001). Gap fraction (here 101 from azimuth) was estimated
from hemispherical photographs using CANEYE 5.0 (INRA, 2007).
Photographs were taken with a digital camera (Coolpix S3 with
EC-F8 fisheye lens, Nikon Corp., Tokyo, Japan) above each of the
nine cacao trees.
Fig. 5 Values of dD (%) of plant water and soil water from the agroforest stand, Marena, Central Sulawesi: (a) cacao and (b) Gliricidia.
Values are means SD (n 5 5). Samples were taken during the pretreatment period (February 2007). The dashed lines indicate the depth
of water uptake of the respective species.
r 2009 Blackwell Publishing Ltd, Global Change Biology, 16, 15151530
1526 L . S C H W E N D E N M A N N et al.
Discussion
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
(2) Water uptake was partitioned vertically between cacao
and Gliricidia. An analysis of the dD in water extracted
from cacao and Gliricidia plant water and soil water at
different depths conducted during the pretreatment
period indicated that cacao obtained most of its water
from the upper horizon, while Gliricidia obtained more
of its water from deeper soil layers. This vertical partitioning in water uptake may limit competition between
cacao and Gliricidia for soil water resources. The reliance on deeper water sources may also explain why
Gliricidia sap flux densities recovered slower after roof
opening as it took some time to rewet lower soil
compartments.
(3) Cacao may have benefited from water input through
small openings in the roof. In our experiment approximately 20% of the throughfall (plus stemflow) reached
the soil surface. As storm events were frequent (Fig. 2e),
and cacao predominantly took up water from the
topsoil (Fig. 5a), it probably profited more from the
small amount of throughfall reaching the soil surface
(Fig. 2a) than the Gliricidia trees.
(4) Benchmark values such as permanent wilting point
(PWP) or relative extractable soil water (REW) are misleading. A REW value of about 0.4 is considered as a
physiological threshold at which soil water content
begins to limit transpiration rates due to stomatal
closure (Granier et al., 1999). Our data shows that sap
flux densities only declined considerably (roof to contol
ratio o0.75) when REW was o0.1 indicating that both
species are quite tolerant to low soil water availability.
(5) Acclimation to drought may have taken place in both
tree species. In cacao and Gliricidia leaves, d13C values
and intrinsic water use efficiencies (iWUE) increased
with decreasing water availability in the roof plots
(A. Camejo Diaz & L. Schwendenmann, unpublished
results) implying changes in stomatal control of transpirational water loss (Farquhar et al., 1989).
1527
1528 L . S C H W E N D E N M A N N et al.
differences in stem increment (G. Moser, unpublished
results) and leaf litterfall between roof and control plots,
this indicates that the reproduction was more sensitive
to drought than vegetative growth and fine litter production corroborated by Nepstad et al. (2002) who
found some preliminary evidence that fruiting phenology in a tropical rain forest was more sensitive to
drought than fine litter production.
The observed yield loss was higher than the reduction
obtained from a socioeconomic survey in Central Sulawesi (Keil et al., 2008) where farmers reported a decline
of up to 38% of average cacao yield levels after strong
ENSO-related droughts in 1997 and 2002. In January
2002 rainfall in the study region was as low as in January
2008. According to Keil et al. (2008) most of the droughtaffected farm households were forced to substantially
reduce expenditures for food and other basic necessities
to adapt to the reduction in agricultural income. In
addition, the level of preparedness for the case of
drought is low and risk management often includes
environmentally damaging and illegal activities such as
rattan extraction from protected forests (Keil et al., 2008).
The physiological modeling study by Zuidema et al.
(2005) suggested that droughts may induce yield reductions as high as 50% which is close to the result we
observed in our experiment. Yield reduction in our
experiment was closely linked to the two driest months
(January and February 2008) which was also found by
Zuidema et al. (2005).
Infection rates of cacao pods by pest insects and fungal
disease were high (485%) in both control and roof plots.
Bos et al. (2007) and Y. Clough (unpublished results) both
investigated cacao pests and pathogens in the vicinity of
our study site and also reported a high proportion of
damage caused by black pod, cacao pod borer, and
Helopeltis (see also Hebbar, 2007). Yield losses due to
black pod disease P. palmivora have increased in Sulawesi
in 2007 and 2008 due to increased rainfall (Y. Clough,
unpublished results). Our data suggests that low humidity due to low rainfall led to a significant decrease in
black pod occurrence between January and April 2008.
Herbivory caused by Helopeltis and cacao pod borer was
initially expected to be higher at the wet end of precipitation gradients (Connell, 1971), but recent evidence
suggests higher herbivory takes place at intermediate
precipitation levels (Marquis et al., 2002). In this study,
we did not find evidence of changes in occurrence of
insect damage caused by the induced drought.
E X P E R I M E N TA L D R O U G H T I N C A C A O A G R O F O R E S T R Y
critical role in minimizing the vulnerability of farmers
livelihood to extreme weather events such as droughts.
Acknowledgements
This study was conducted in the framework of the joint Indonesian-German research project Stability of Tropical Rainforest
Margins in Indonesia (STORMA) funded by the Deutsche Forschungsgemeinschaft, DFG (SFB 552). We thank Thomas Kluter
and his team for roof construction and maintenance; Pak Andi
Sofyan for his assistance with the field work; three anonymous
reviewers and Eric A. Davidson for constructive reviews and
suggestions; the German and Indonesian project coordination for
technical support, and LIPI, the Indonesian Research Institute,
for the research permit.
References
Alvim PT (1977) Cacao. In: Ecophysiology of Tropical Crops (eds Alvim PT,
Kozlowski TT), pp. 279313. Academic Press, London.
Alvim PT, Alvim R (1978) Relation of climate to growth periodicity in
tropical trees. In: Tropical Trees as Living Systems (eds Tomlinson PB,
Zimmermann MH), pp. 445464. Cambridge University Press, Cambridge, UK.
Alvim PT, Machado AD, Vello F (1974) Physiological responses of cacao to
environmental factors. Revista Theobroma, 4, 325.
Aranguren J, Escalante G, Herrera R (1982) Nitrogen cycle of tropical
perennial crops under shade trees. II. Cacao. Plant and Soil, 67, 259269.
Beer J (1988) Litter production and nutrient cycling in coffee (Coffea
arabica) or cacao (Theobroma cacao) plantations with shade trees. Agroforestry Systems, 7, 103114.
Beer JW (1987) Advantages, disadvantages and desirable characteristics
of shade trees for coffee, cacao and tea. Agroforestry Systems, 5, 313.
Belsky JM, Siebert SF (2003) Cultivating cacao: implications of sun-grown
cacao on local food security and environmental sustainability. Agriculture and Human Values, 20, 277285.
Bonhomme R, Chartier P (1972) The interpretation and automatic measurement of hemispherical photographs to obtain sunlit foliage. Israel
Journal of Agricultural Research, 22, 5361.
Bos MM, Steffan-Dewenter I, Tscharntke T (2007) Shade tree management
affects fruit abortion, insect pests and pathogens of cacao. Agriculture,
Ecosystems and Environment, 120, 201205.
Brando PM, Nepstad DC, Davidson EA, Trumbore SE, Ray D, Camargo P
(2008) Drought effects on litterfall, wood production, and belowground
carbon cycling in an Amazon forest: results of a throughfall reduction
experiment. Philosophical Transactions of the Royal Society B, 363, 1839
1848.
Broadhead JS, Black CR, Ong CK (2003) Tree leafing phenology and crop
productivity in semi-arid agroforestry systems in Kenya. Agroforestry
Systems, 58, 137148.
Brunel JP, Walker GR, Kenneth-Smith AK (1995) Field validation of
isotopic procedures for determining sources of water used by plants
in a semi-arid environment. Journal of Hydrology, 167, 351368.
Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson JR, Ni J,
Holland EA (2001) Net primary production in tropical forests: an
evaluation and synthesis of existing field data. Ecological Applications,
11, 371384.
Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and rain forest trees. In:
Dynamics of Populations (eds den Boer PJ, Gradwell GR), pp. 298312.
PUDOC, Wageningen.
1529
1530 L . S C H W E N D E N M A N N et al.
Lamersdorf NP, Beier C, Blanck K et al. (1998) Effect of drought experiments using roof installations on acidification/nitrification of soils.
Forest Ecology and Management, 101, 95109.
Lang ARG, Xiang YQ (1986) Estimation of leaf area index from transmission of direct sunlight in discontinuous canopies. Agricultural and Forest
Meteorology, 37, 229243.
Lin B, Perfecto I, Vandermeer J (2008) Synergies between agricultural
intensification and climate change could create surprising vulnerabilities for crops. BioScience, 58, 847954.
Ling AH (1986) Litter production and nutrient cycling in a mature cocoa
plantation on inland soils of Peninsular Malaysia. In: Proceedings of the
International Conference on Cocoa and Coconuts, Kuala Lumpur (eds
Pushparajah E, Chew PS), pp. 451465. Incorporated Society of Planters, Kuala Lumpur, Malaysia.
Marquis RJ, Morais HC, Diniz IR (2002) Interactions among cerrado
plants and their herbivores: unique or typical? In: The Cerrados of Brazil:
Ecology and Natural History of a Neotropical Savanna (eds Oliveira PS,
Marquis RJ), pp. 306328. Columbia University Press, New York.
Nepstad DC, Moutinho P, Dias-Filho MB et al. (2002) The effects of partial
throughfall exclusion on canopy processes, aboveground production,
and biogeochemistry of an Amazon forest. Journal of Geophysical
Research, 107, 53.153.18.
Purseglove J (1968) Tropical Crops: Dicotyledons. Longman, Harlow, UK.
Rada F, Jaimez RE, Garcia-Nunez C, Azocar A, Ramrez ME (2005) Water
relations and gas exchange in Theobroma cacao var. Guasare under
periods of water deficit. Revista de la Falcultad de Agronomia, 22, 112120.
Rice RA, Greenberg R (2000) Cacao cultivation and the conservation of
biological diversity. Ambio, 29, 167173.
Schwendenmann L, Veldkamp E, Brenes T, OBrien JJ, Mackensen J (2003)
Spatial and temporal variation in soil CO2 efflux in an old-growth
neotropical rain forest, La Selva, Costa Rica. Biogeochemistry, 64, 111128.
Sheffield J, Wood EF (2008) Projected changes in drought occurrence
under future global warming from multi-model, multi-scenario, IPCC
AR4 simulations. Climate Dynamics, 31, 79105.
Slingo JM, Challinor AJ, Hoskins BJ, Wheeler TR (2005) Introduction: food
crops in a changing climate. Philosophical Transactions of the Royal Society
B, 360, 19831989.
Sotta ED, Veldkamp E, Schwendenmann L et al. (2007) Effects of an
induced drought on the soil CO2 production and soil CO2 efflux in an
Eastern Amazonian Rainforest, Brazil. Global Change Biology, 13, 2218
2229.
Topp GC (1971) Soil water hysteresis in silt loam and clay loam soils.
Water Resources Research, 7, 914920.
van Noordwijk M, Lawson G, Soumare A, Groot JJR, Hairiah K (1996)
Root distribution of trees and crops: competition and/or complementarity. In: Tree-Crop Interactions (eds Ong CK, Huxley P), pp. 319364.
CAB International, Wallingford.
Veldkamp E, OBrien JJ (2000) Calibration of a frequency domain reflectometry sensor for humid tropical soils of volcanic origin. Soil Science
Society of America Journal, 64, 15491553.
Verchot LV, van Noordwijk M, Kandji S et al. (2007) Climate change:
linking adaptation and mitigation through agroforestry. Mitigation and
Adaptation Strategies for Global Change, 12, 901918.
Vincke C, Thiry Y (2008) Water table is a relevant source for water uptake
by a Scots pine (Pinus sylvestris L.) stand: Evidences from continuous
evapotranspiration and water table monitoring. Agricultural and Forest
Meteorology, 148, 14191432.
Vitousek PM (1984) Litterfall, nutrient cycling and nutrient limitation in
tropical forests. Ecology, 65, 285298.
Wright SJ, Cornejo FH (1990) Seasonal drought and leaf fall in a tropical
forest. Ecology, 71, 11651175.
Young AM (1994) The Chocolate Tree. A Natural History of Cacao. Smithsonian Institution Press, Washington, DC.
Zuidema PA, Leffelaar PA, Gerritsma W, Mommer L, Anten NPR (2005) A
physiological production model for cocoa (Theobroma cacao): model
presentation, validation and application. Agricultural Systems, 84, 195
225.