See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/320272890

Carbon stocks and cocoa yields in agroforestry systems of Central America

Article · January 2013

CITATIONS READS

48 178

13 authors, including:

Eduardo Jose Somarriba Rolando H. Cerda

CATIE - Centro Agronómico Tropical de Investigación y Enseñanza CATIE - Centro Agronómico Tropical de Investigación y Enseñanza
251 PUBLICATIONS   3,317 CITATIONS    45 PUBLICATIONS   489 CITATIONS   

SEE PROFILE SEE PROFILE

Luis Orozco-Aguilar Miguel Cifuentes

University of Melbourne CATIE - Centro Agronómico Tropical de Investigación y Enseñanza
68 PUBLICATIONS   166 CITATIONS    46 PUBLICATIONS   406 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

ethnobotanic View project

Cacao cultivation/management View project

All content following this page was uploaded by Henry Mavisoy Muchavisoy on 08 October 2017.

The user has requested enhancement of the downloaded file.

 Agriculture, Ecosystems and Environment 173 (2013) 46–57

Contents lists available at SciVerse ScienceDirect

Agriculture, Ecosystems and Environment

journal homepage: www.elsevier.com/locate/agee

Carbon stocks and cocoa yields in agroforestry systems of

Central America
Eduardo Somarriba a,∗ , Rolando Cerda a , Luis Orozco a , Miguel Cifuentes a , Héctor Dávila a ,
Tania Espin a , Henry Mavisoy a , Guadalupe Ávila a , Estefany Alvarado a , Verónica Poveda a ,
Carlos Astorga a , Eduardo Say a , Olivier Deheuvels b,c
a
CATIE, DID, 7170, Cartago, Turrialba 30501, Costa Rica
b
CIRAD, UMR System, F-34070 Montpellier, France
c
CATIE, PAAS, CR-7170 Turrialba, Costa Rica

a r t i c l e i n f o a b s t r a c t

Article history: The cocoa tree (Theobroma cacao L.) is cultivated typically in agroforestry systems in close association
Received 13 August 2012 with a rich list of tree species and other useful plants on the same plot. Cocoa based agroforestry systems
Received in revised form 3 April 2013 are credited for stocking significant amounts of carbon and hence have the potential to mitigate climate
Accepted 15 April 2013
change. Since cocoa yields decrease non-linearly with increasing shade, a need is to design optimal cocoa
Available online 16 May 2013
agroforestry systems with high yields and high carbon stocks. We estimated the carbon stocked in a
network of 229 permanent sample plots in cacao-based agroforestry systems and natural forests in five
Keywords:
Central American countries. Carbon stocks were fractioned by both system compartments (aboveground,
Biomass
Certification roots, soil, litter, dead wood – fine and coarse, and total) and tree use/form (cocoa, timber, fruit, bananas,
Climate change shade and ornamentals, and palms). Cocoa plantations were assigned to a five-class typology and tested
Timber for independence with growing region using contingency analysis. Most Central American cocoa plan-
Trade-off tations had mixed or productive shade canopies. Only 4% of cocoa plantations were full sun or rustic
Forest (cocoa under thinned natural forest). Cocoa tree density was low (548 ± 192 trees ha−1 ). Total carbon
(soil + biomass + dead biomass) was 117 ± 47 Mg ha−1 , with 51 Mg ha−1 in the soil and 49 Mg ha−1 (42%
of total carbon) in aboveground biomass (cocoa and canopy trees). Cocoa trees accumulated 9 Mg C ha−1
(18% of carbon in aboveground biomass). Timber and fruit trees stored 65% of aboveground carbon. The
annual rate of accumulation of carbon in aboveground biomass ranged between 1.3 and 2.6 Mg C ha−1 y−1 .
Trade-offs between carbon levels and yields were explored qualitatively using functional relationships
documented in the scientific and technical literature, and expert knowledge. We argue that it is possible
to design cocoa-based AFS with good yields (cocoa and shade canopy) and high carbon stock levels. The
botanical composition of the shade canopy provides a large set of morphological and functional traits
that can be used to optimize shade canopy design. Our results offer Central American cocoa producers a
rigorous estimate of carbon stocks in their cocoa plantations. This knowledge may help them to certify
and sell their cocoa, timber, fruits and other goods to niche markets with good prices. Our results will
also assist governments and the private sector in (i) designing better legal, institutional and policy frame-
works, local and national, promoting an agriculture with trees and (ii) contributing to the development
of the national monitoring, reporting and verification systems required by the international community
to access funding and payment for ecosystem services.
© 2013 Elsevier B.V. All rights reserved.

1. Introduction
The atmospheric concentration of CO2 and other green-
house gases increased by 70% between 1970 and 2004 (Solomon
et al., 2007). Carbon accumulates in the atmosphere at a rate
∗ Corresponding author. Tel.: +506 25 58 25 93; fax: +506 25 56 30 18.
E-mail addresses: eduardo.somarriba56@gmail.com, esomarri@catie.ac.cr
(E. Somarriba).
of 3.5 × 109 tons a year, due mostly to fossil fuel consumption
and the conversion of tropical forests into land for agriculture
and pasture (Paustian et al., 2000). Industry and energy sectors
(transport, industrial processes, electricity, and heat generation)
are responsible for approximately 65% of all emissions. Land
use change and agriculture are responsible for 18% and 14%,
respectively (WRI, 2005). There are incentives to emit less and
capture more greenhouse gases, such as the Joint Implementation
and Clean Development Mechanisms, REDD+ (Reduced Emissions
from Deforestation and Forest Degradation), and voluntary carbon

0167-8809/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.agee.2013.04.013
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57
Fig. 1. Name and location of the cocoa growing areas where our study was conducted in Central America.
markets (Miles and Kapos, 2008; FAO, 2010). Cocoa (Theobroma
cacao L.) is cultivated in agroforestry systems, i.e. together with a
rich list of tree species and other useful plants on the same plot.
Cocoa based agroforestry systems are credited for stocking
significant amounts of carbon and hence have the potential to
mitigate climate change. Carbon stocks in shaded agroforestry
systems with perennial crops—such as coffee (Coffea arabica L.),
rubber (Hevea brasiliensis (HBK) Muell.-Arg.), and cocoa—may vary
between 12 and 228 Mg ha−1 and could help to mitigate cli-
mate change (Winjum et al., 1992; Schroeder, 1994; Dixon, 1995;
Albrecht and Kandji, 2003; Montagnini and Nair, 2004; Nair et al.,
2009). In Central America, 24,000 ha of cocoa are grown without
inorganic inputs or pesticides, plantations are small (0.25–3.0 ha)
and yield only 250 kg dry cocoa ha−1 y−1 (Deheuvels et al., 2012;
Whelan et al., 2007; Somarriba et al., 2009). Central American
cocoa agroforestry systems have high plant species richness and
structural complexity (Deheuvels et al., 2012), product diversifi-
cation for self-consumption and sale (Dalquist et al., 2007), and
permanent soil cover and large amounts of organic matter. These
later conditions promote soil and water conservation (Adejumo,
2005; Verchot et al., 2007; Binternagel et al., 2010). Taxonomically
diverse shaded cocoa plantations share many features usually rec-
ommended to adapt farming to climate change (Smit and Skinner,
2002).
Cocoa yields decrease non-linearly with increasing shade
(Zuidema et al., 2005; Stephan-Dewenter et al., 2007; Wade et al.,
2010; Gockowski and Sonwa, 2011), and shade in turn increases –
albeit not deterministically – with carbon stock level. This raises
the question whether optimal cocoa agroforestry systems can be
designed that simultaneously produce high yields (cocoa and prod-
ucts from the shade canopy species) and retain high carbon stock
levels. We quantified carbon stocks in Central American cocoa
agroforestry systems and local forests patches, and qualitatively
explored the trade-offs of maintaining both high carbon levels and
high crop yields.
2. Materials and methods
2.1. Definitions, terms and concepts
We use the following definitions: A cocoa growing area is the
territory where farms having cocoa plantations are located. A farm
is the land unit (in a single block or not) managed by the family
47
or enterprise, which typically includes several cropping systems,
one of which may be cocoa. A cocoa plantation is a single block of
land, of variable size and form, dedicated to cultivating cocoa with
or without other associated plants. A plot is a 50 m × 20 m repre-
sentative sample area within the cocoa plantation. A plot may be
divided into sub-plots. A cocoa plantation has two components:
cocoa and shade canopy (or simply, the canopy). The cocoa compo-
nent includes all cocoa plants. The canopy component includes all
non-cocoa plants taller than cocoa trees. A cocoa plantation under
shade trees is a cocoa based agroforestry system (cocoa AFS). As
young cocoa trees grow in height and develop their crowns, upper
leaves shade those underneath, producing self-shading. The site is
the set of biophysical conditions (soil, climate, biology and local
culture) that determines growth and yield of cocoa and canopy
components.
2.2. Description of cocoa plantations and sample plots
We sampled 229 cocoa plantations in six cocoa growing areas
in five Central American countries (Fig. 1). In each cocoa growing
area, we established a network of permanent sample plots located
in 36–40 cocoa-based AFS and in 3–4 mature or secondary natural
forest patches, as control. The natural forest present in the area
at the time of sampling may be a degraded version of the original
native primary forest at the site. Cocoa-based AFS in each growing
area were selected in order to sample as much variability as
possible in terms of farm typology and biophysical conditions.
Further details of the criteria used to develop the research network
are given in Deheuvels et al. (2012) and Deheuvels (2011).
2.3. Field measurements and data analysis
Tree biomass was estimated using locally derived allometric
equations (Table 1).
The carbon content was 0.5 of dry biomass (IPCC, 2003b). Carbon
per plot was fractioned into: (i) system’s compartments [above-
ground, litter (leaves and fine branches ≤2 cm diameter), coarse
(>10 cm) and fine (>2 and <10 cm) dead wood, coarse (>2 mm in
diameter) and fine roots (<2 mm in diameter), soil, total] and (ii)
plant type: cocoa, timber trees, fruit and medicinal trees, other
shade and ornamental trees, bananas, and palm trees. We measured
carbon in soil organic matter, litter, soil bulk density, fine roots den-
sity, and fine dead wood in composite samples of 10 sub-samples
48 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57

Table 1
Allometric equations used to estimate carbon in aboveground biomass and coarse roots in Central American cocoa plantations.

Species or plant type Equation or formula Source

Theobroma cacao Log B = (−1.684 + 2.158 * Log(d30 ) + 0.892 * Log(alt)) CATIE (unpublished)
Cordia alliodora Log B = (−0.94 + 1.32 * Log(dbh) + 1.14 * Log(alt)) CATIE (unpublished)
Bactris gasipaes B = 0.74 * alt2 Szott et al. (1993)
Other timber trees B = (21.3–6.95 * (dbh) + 0.74 * (dbh2 )) Brown and Iverson (1992)
Other fruit trees Log B = (−1.11 + 2.64 * Log(dbh)) CATIE (unpublished)
Other palms B = 4.5 + 7.7 * alt Frangi and Lugo (1985)
Coarse roots B = exp[−1.0587 + 0.8836 * ln(AB)] Cairns et al. (1997)
Musacea 1.5 kg/m height Tanaka and Yamaguchi (1972)

B: biomass (kg); Log: logarithm base 10; dbh: trunk diameter (cm) at breast height (1.3 m); d30 : trunk diameter at 30 cm; alt: total height (m); AB: aboveground biomass.

per plot. Coarse dead wood was measured on two perpendicular
transects (50 and 20 m, respectively) traced on the sample plot (Van
Wagner, 1968; IPCC, 2003b). Carbon content in soil, fine roots, dead
wood and litter were determined by combustion (Thermoffinigan,
Flash EA 1112 series; MacDiken, 1997). The annual rate of accumu-
lation of aboveground carbon (cocoa and canopy) was estimated
both by using plantation age as indicated by farmers, and by re-
measuring ten sample plots in Waslala, Nicaragua.
A multivariate Principal Component Analysis (PCA) was per-
formed on our 229 cocoa plantations sample for biomass, carbon
content and accumulation rate for each plant type (cocoa, tim-
ber trees, fruit and medicinal trees, palm trees, other shade and
ornamental trees, and Musacea) and in each compartment (above-
ground: aerial, litter, coarse and fine dead wood; belowground:
coarse and fine roots, soil). This PCA was performed with the Info-
Stat software (Di Rienzo et al., 2012) to give a descriptive overview
of the global dataset and to identify correlations to be tested
between variables and between countries. Differences between
cocoa-growing areas in terms of carbon stocks were then tested
with ANOVA and LSD Fisher tests with a 95% confidence interval.
We calculated the gross monetary value of current carbon stocks
(total and aboveground) and accumulation rates using a price of
US$ 5 per ton of CO2 (CO2 = C * 3.67) in the voluntary markets
(Seeberg-Elverfeldt et al., 2009; Hamilton et al., 2010). Although
other authors propose US$ 1.2 per CO2 ton in voluntary markets
(Gockowski and Sonwa, 2011), average agroforestry credit prices
increased from US$ 5 to 10 between 2009 and 2010 (Peters-Stanley
et al., 2011).
Central American cocoa plantations were classified according
to a five-class, modified version of the typology proposed by Rice
and Greenberg (2000). Our cocoa plantation typology included:
(1) cocoa without shade; (2) cocoa with specialized shade (e.g.
shade from service legume trees such as various species of Gliri-
cidia, Inga, Leucaena, Erythrina, Albizia); (3) cocoa with productive
shade (e.g. cocoa with a mono-specific canopy of coconut, fruit,
banana, or timber species); (4) cocoa with mixed shade; and (5)
cocoa with rustic shade (cocoa planted under thinned natural for-
est), known as “cabrucas” in Brazil (Sambuichi, 2002). Because, in
general, shade levels increase with decreasing crop management
intensity, other authors have suggested using canopy cover as an
indicator of cocoa management intensity (Stephan-Dewenter et al.,
2007; Clough et al., 2011; Deheuvels, 2011). We tested the hypoth-
esis that cocoa farm typologies were similar in all cocoa growing
areas by contingency analysis (X2 5%).
3. Results
3.1. Soil and site characteristics of the sample
Cocoa plots were located in rainy (1700–4000 mm y−1 ), warm
areas (24–25 ◦ C), at <500 m altitude, in valleys (flat terrain) and hills
(hillsides), on inceptisol (valleys) and ultisol (hills) soils. On aver-
age, cocoa soils had medium to low fertility, pH between 5.0 and
6.5, carbon between 2 and 7%, little P and normal to low amounts of
Ca and K. Cocoa plantations were 1.6 ha (0.1–9.0) in size, used local

90
PANAMA
85
80
75
NICARAGUA
70
COSTA RICA
65
60 HONDURAS
Plant species richness

55
GUATEMALA
50
Costa Sur
45
40
GUATEMALA
35
Alta Verapaz
30
25
20
15
10
5
0
0,2 0,4 0,6 0,8 1,0 1,2 1,4 1,6 1,8 2,0 2,2 2,4 2,6 2,8 3,0 3,2 3,4 3,6 3,8 4,0

Sampled area (ha)

Fig. 2. Rarefaction curves for shade canopy plant species in 229 cocoa-based agroforestry systems in Central America.
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57 49

Fig. 3. Principal Component Analysis conducted on 229 cocoa-based agroforestry systems in Panama, Costa Rica, Nicaragua, Honduras and Guatemala. The quality of the
correlations for biomass, carbon content and accumulation rate in each plant type (cocoa, timber trees, fruit and medicinal trees, palm trees, other shade and ornamental trees,
and Musacea) and in each compartment (aboveground: aerial, litter, coarse and fine dead wood; belowground: coarse and fine roots, soil) is shown on the first 2 principal
components (58.2% of total variability); age: number of years since creation of the cocoa plantation; area: surface of the cocoa plantation; CCoarseRoots: carbon in coarse
roots; CCoarseWood: carbon in coarse dead wood; Ccocoa: carbon in cocoa trees; CFineRoots: carbon in fine roots; CFineWood: carbon in fine dead wood; CFruitMed: carbon
in fruit and medicinal trees; CLeafLitter: carbon in leaf litter; Cmusa: carbon in Musacea; Cothers: carbon in other only-shade trees; Cpalm: carbon in Palmacea; Csoil: carbon
in soil; CTimber: carbon in timer trees; CocoaDens: density of cocoa trees; FruitMedDens: density of fruit and medicinal trees; MusaDens: density of Musacea; OthersDens:
density of other only-shade trees; PalmDens: density of palm trees; TimberDens: density of timber trees; TotalCacuRate: total carbon accumulation rate; TotalBiomass: total
aerial biomass.

hybrid cocoa varieties, and were between 18 and 30 years old; a
few plantations were >40 years old.
3.2. Botanical composition of the sample
Rarefaction curves of canopy species, using 1000 m2 plots and
a total of 3.6 ha inventoried per cocoa growing region showed
that these cocoa plantations contained between 40 and 80 species,
with noticeable differences between cocoa growing areas (Fig. 2).
Canopy species were either spontaneous or planted, managed and
exploited for timber, fruit or firewood, and may include several tim-
ber species—such as Cordia alliodora (Ruiz and Pavón) Oken, Cedrela
odorata L., Terminalia oblonga Exell); palm species (Iriartea spp., in
particular), and several fruit tree species, such as Bactris gasipaes
Kunth, Cocos nucifera L., Nephelium lappaceum L., Mangifera indica
L., Pouteria sapota (Jacq.) H.E. Moore and Stearn, and Persea ameri-
cana Mill. The most commonly used legume species were Gliricidia
sepium (Jacq.) Kunth ex. Walp, Inga spp. and Leucaena leucocephala
(Lam.) de Wil (unpublished data).
3.4. Plant density and cocoa plantation typology
The average plant density in the plots was 866 plants ha−1 ,
including 545 cocoa trees ha−1 , 117 banana stems ha−1 ,
104 timber trees ha−1 , 52 fruit trees ha−1 , and 47 palms and other
trees ha−1 (Table 2). Bananas (90%) and plantains (10%) were fre-
quent in Nicaragua, Costa Rica and Panama (150–240 stems ha−1 ),
but rare in Guatemala and Honduras (2–40 stems ha−1 ). Central
American cocoa plantations have a total basal area of 23 m2 ha−1 ,
with cocoa contributing 11 m2 ha−1 , timber trees (6 m2 ha−1 ) and
the rest of plant types (palms, bananas, fruit trees, and other) an
additional 6 m2 ha−1 (Table 2).
Forty-six percent of Central American cocoa plantations had
mixed shade canopies; 37% had a productive shade cover. Only
3–4% of all cocoa plantations were cultivated either without shade
or under rustic shade (Table 3). Cocoa plantation typologies and
growing areas were not independent (p < 0.0001). For example, rus-
tic and full sun plantations were found only in Guatemala; cocoa
plantations with mixed shade were common in all Central Ameri-
can countries.

3.3. Overview of the correlations in the sample 3.5. Carbon stocks

The first two axes of the PCA contain 58.2% of the variation in the
sample (Fig. 3). Cocoa producing regions separated into three dis-
tinct groups: in group 1, cocoa plantations in Nicaragua, Guatemala
Alta Verapaz and Honduras are associated with steep slopes, high
cocoa planting density, high carbon stock in cocoa trees, low carbon
stock in shade canopy plants, low species richness, and low carbon
stock in soil and leaf litter.
In group 2, Panama and Costa Rica are associated with cocoa
plantations at low altitude, high plant species richness, high abun-
dance of bananas, palm, fruit and medicinal trees. Cocoa AFS in
these two countries tend to stock more carbon in banana, palm and
timber trees, and much less in cocoa trees.
The Guatemala Costa Sur region clearly differentiated as a dis-
tinct group 3, with old cocoa plantation, with high carbon stocks in
fruit, medicinal and shade-only trees, and in soil and leaf litter.
Central American cocoa-based AFS stocked, on average,
117 ± 47 Mg ha−1 of total carbon, with wide differences among
plots (46–333 Mg C ha−1 ). Carbon in aboveground biomass (cocoa
and canopy) was 49 ± 35 Mg C ha−1 (Table 4).
The frequency distributions of total and carbon in aboveground
biomass were slightly asymmetrically positive and moderately lep-
tokurtic, signaling that means are good indicators of the central
tendency of the data (Fig. 4).
Carbon stocks differed widely between growing areas. The
highest level of total carbon was found in Guatemala-Costa
Sur (155 Mg C ha−1 ), and the lowest in Nicaragua (93 Mg C ha−1 ).
Aboveground biomass contained 42% of total carbon (Table 4). The
annual rate of accumulation of carbon in aboveground biomass
varied with plantation age, with an average of 2.6 Mg C ha−1 y−1 ,
respectively (Table 4). The rate of carbon accumulation was high
50 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57

Table 2
Density and basal area for cocoa and shade canopy in Central American cocoa-based agroforestry systems, 2011.

Nicaragua Honduras Guatemala Alta Verapaz Costa Rica Panama Guatemala Costa Sur Average

Density (trees ha−1 )

Timber trees 42 ± 52a 91 ± 99b 170 ± 91d 119 ± 84bc 134 ± 77cd 88 ± 98b 104 ± 92
Fruit trees 60 ± 57bc 35 ± 65ab 14 ± 23a 84 ± 63c 64 ± 148bc 48 ± 49abc 52 ± 81
Other trees 24 ± 29ab 18 ± 28a 36 ± 43bc 42 ± 58c 15 ± 21a 20 ± 30ab 25 ± 37
Palms 8 ± 25ab 37 ± 83c 1.43 ± 5.5a 43 ± 48c 24 ± 34bc 22 ± 29bc 22 ± 45
Bananas 158 ± 152b 42 ± 74a 0.57 ± 2.0a 193 ± 261bc 240 ± 163c 31 ± 42a 117 ± 169
Cocoa 562 ± 98b 583 ± 205b 604 ± 128b 591 ± 218b 588 ± 215b 335 ± 148a 545 ± 192
Total 855 ± 190b 808 ± 295b 826 ± 156b 1071 ± 242c 1065 ± 323c 544 ± 199a 866 ± 296
Basal area (m2 ha−1 )
Timber trees 2.2 ± 2.9a 6.3 ± 5.9b 7.1 ± 3.5b 8.2 ± 5.6b 7.5 ± 5.1b 8.0 ± 7.8b 6.4 ± 5.8
Fruit trees 3.1 ± 3.5cd 1.4 ± 3.0ab 0.5 ± 1.0a 1.9 ± 1.7bc 1.2 ± 1.5ab 4.3 ± 4.1d 2.1 ± 3.0
Other trees 1.1 ± 1.6a 1.1 ± 3.1a 1.1 ± 1.5a 0.9 ± 2.2a 1.8 ± 3.6ab 3.0 ± 6.1b 1.5 ± 3.3
Palms 0.2 ± 0.6a 0.6 ± 1.6a 0.4 ± 1.6a 0.9 ± 1.2a 0.6 ± 0.9a 2.6 ± 3.5b 0.8 ± 1.9
Bananas 2.7 ± 2.7b 0.7 ± 1.3a 0.02 ± 0.1a 3.4 ± 4.6bc 4.3 ± 2.9c 0.5 ± 0.7a 2.1 ± 2.9
Cocoa 10.7 ± 5.3b 12.8 ± 5.9c 14.2 ± 4.7c 10.2 ± 4.3ab 8.2 ± 4.1a 8.6 ± 3.2a 10.7 ± 5.1
Total 19.9 ± 6.2a 22.9 ± 10.1ab 23.3 ± 7.2bc 25.5 ± 7.4bc 23.6 ± 6.2bc 27.5 ± 14.5c 23.6 ± 8.3

Different letters along rows indicate significant differences among countries (LSD Fisher, p < 0.05).

Table 3
Number cocoa-based agroforestry systems sampled in each of the five types typology and in each Central American country, 2011.

Country Without shade Specialized shade Productive shade Mixed Rustic Total

Nicaragua 0 2 25 22 0 49
Guatemala Alta Vera Paz 0 21 0 14 0 35
Honduras 0 1 18 14 0 33
Costa Rica 0 0 16 20 0 36
Panama 0 0 21 19 0 40
Guatemala Costa Sur 3 0 5 17 11 36

Total 3 24 85 106 11 229

Table 4
Carbon stored per compartment, plantation age and carbon storage rates in Central American cocoa-based agroforestry systems, 2011.

Carbon stored (Mg ha−1 ) in each Nicaragua Honduras Guatemala Alta Costa Rica Panama Guatemala Average
compartment Verapaz Costa Sur

Soil 48.3 ± 14.7b 33.3 ± 11.5a 52.8 ± 10.3bc 49.3 ± 8.5b 56.9 ± 13.2c 64.1 ± 13.4d 51.0 ± 15.2
Aboveground biomass 33.1 ± 19.5a 45.1 ± 29.0abc 39.4 ± 19.4ab 52.7 ± 21.7bc 56.7 ± 47.4c 74.4 ± 47.0d 49.2 ± 34.9
Coarse roots 6.9 ± 3.6ab 9.4 ± 5.4bc 6.6 ± 3.6a 9.3 ± 3.6bc 11.5 ± 8.3cd 13.4 ± 8.0d 9.4 ± 6.2
Fine roots 3.8 ± 2.5c 1.3 ± 0.8a 1.4 ± 1.1a 1.9 ± 0.9ab 2.1 ± 0.9b 1.6 ± 0.8ab 2.1 ± 1.7
Coarse dead wood 0.01 ± 0.06a 6.2 ± 4.8c 3.7 ± 5.1b 6.2 ± 5.1c 3.2 ± 4.9b 0.02 ± 0.07a 3.0 ± 4.7
Fine dead wood 0.3 ± 0.1b 0.1 ± 0.1a 1.2 ± 0.1d 1.2 ± 0.5d 0.7 ± 0.4c 0.3 ± 0.1b 0.6 ± 0.5
Litter 0.3 ± 0.1a 0.8 ± 0.4bc 0.4 ± 0.2ab 1.2 ± 0.4d 0.9 ± 0.3c 3.6 ± 1.8e 1.1 ± 1.3
Total 93 ± 30a 96 ± 37a 106 ± 25ab 122 ± 24bc 132 ± 60c 155 ± 58d 117 ± 47
Age (years) 20.3 ± 6.7ab 20.5 ± 6.5ab 18.1 ± 8.4a 24.9 ± 14.5bc 26.9 ± 6.1cd 30.8 ± 20.2d 23.5 ± 12
Total C rate (Mg ha−1 y−1 )a 5.4 ± 3.4a 5.6 ± 4.7a 7.9 ± 5.3b 6.9 ± 4.3ab 5.3 ± 3.3a 7.9 ± 6.2b 6.4 ± 4.6
Aboveground biomass C rate 1.9 ± 1.6a 2.6 ± 2.7ab 2.6 ± 1.9ab 3.0 ± 1.9bc 2.2 ± 1.8ab 3.7 ± 3.7c 2.6 ± 2.4
(Mg ha−1 y−1 )
a
Over-estimates the real carbon accumulation rate in the plot, because we do not know how much soil carbon was present at the establishment of the cocoa plantation.

in young plantations AFS (<10 years) and decreased with age

(Fig. 5).
Annual accumulation rate of aboveground carbon estimated
by re-measurement of plots in Nicaragua, was estimated at
1.3 Mg C ha−1 y−1 .
Timber and fruit trees stored 32 Mg C ha−1 , equivalent to 64% of
carbon in aboveground biomass. Cocoa trees stored 9 Mg C ha−1 ,
equal to 18% of carbon in aboveground biomass. In nearly all
countries, most aboveground biomass carbon was concentrated
in timber trees. Only in Nicaragua carbon aboveground biomass
was mainly stored in fruit trees (Persea americana, Pouteria sapota,
Mangifera indica, Inga spp., Citrus spp.). Bananas and palm trees
stored only 4% of carbon in aboveground biomass irrespective of
growing area (Table 5).
Some site and soil variables (area, apparent density, pH, K and N
content) correlated significantly with total and aboveground car-
Fig. 4. Frequency distributions, mean, asymmetry and kurtosis for aboveground
carbon in Central American cocoa plantations (n = 229).
bon levels, but correlation coefficients were less than 0.30.
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57 51

Table 5
Carbon found in aboveground biomass per plant type and per country in 229 Central American cocoa-based agroforestry systems, 2011.

Carbon C in aboveground Nicaragua Guatemala Alta Honduras Costa Rica Panama Guatemala Average
biomass (Mg ha−1 ) Verapaz Costa Sur

Timber 6.9 ± 12.8a 22.9 ± 12.9b 21.5 ± 19.3b 27.7 ± 17.3b 31.6 ± 34.7c 30.9 ± 33.3b 22.8 ± 24.8
Fruit trees 11.6 ± 17.1b 1.8 ± 4.3a 7.5 ± 17.0ab 8.1 ± 8.3ab 3.0 ± 4.0a 19.7 ± 25.1c 8.7 ± 16.0
Cocoa 9.8 ± 5.8b 9.6 ± 4.8b 10.5 ± 5.4b 8.6 ± 5.2ab 7.0 ± 4.0a 8.4 ± 4.4ab 9.0 ± 5.1
Others 4.3 ± 8.3ab 3.6 ± 5.4ab 4.2 ± 12.1ab 2.9 ± 8.9a 12.9 ± 33.6c 11.7 ± 24.5bc 6.6 ± 18.8
Palms 0.6 ± 1.7a 1.5 ± 6.4a 0.9 ± 2.3a 4.6 ± 7.7b 1.6 ± 2.4a 1.7 ± 2.1a 1.8 ± 4.5
Musacea 0.3 ± 0.1a 0.0 ± 0.0a 0.5 ± 1.1b 0.8 ± 1.1b 0.8 ± 0.5b 0.1 ± 0.3a 0.3 ± 0.7

Total 33.5 ± 20a 39.4 ± 19ab 45.1 ± 29abc 52.7 ± 22bc 56.9 ± 47c 72.5 ± 47d 49.2 ± 35

Different letters along rows indicate significant differences among countries (LSD Fisher, p < 0.05).

4. Discussion

4.1. Comparing the carbon stocks in Central American cocoa

plantations with other sites

Fig. 5. Accumulation rate of carbon in aboveground biomass in Central American
cocoa agroforestry systems: (A) total = cocoa + shade canopy and (B) in cocoa trees.
The monetary value of carbon stocked in Central American cocoa
plantations is modest. For example, 117 tons of total carbon are
worth 2152 US$ ha−1 . The monetary value of carbon in above-
ground biomass is only 920 US$ ha−1 . If only the accumulation rate
of aboveground carbon is valued, cocoa plantations would yield
49 US$ ha−1 y−1 (Table 6).
Forests are the main atmospheric CO2 sink on Earth. The car-
bon stock of the local climax forest depends on the ecological
conditions (rainfall, temperature, soil, local flora and fauna) that
determine tree growth. Most cacao trees in the world are grown
between 18◦ N and 18◦ S latitude (Schmitz and Shapiro, 2012), in
humid forest areas with rainfall between 1200 and 2800 mm yr−1 ,
mean annual temperature between 20 and 28 ◦ C, without frosts,
and on a variety of mid-textured, medium to high fertility soils
(Wood and Lass, 2001). Humid climax forests within the ecologi-
cal range of cocoa (such as natural climax forests in the Amazonia,
Central America, Mata Atlantica in Brazil, Indonesia, Malaysia and
Ghana) store on average 180 Mg C ha−1 , with variations between
75 and 275 Mg C ha−1 (Brown et al., 1991; Kotto-Same et al., 1997;
Clark and Clark, 2000; Woomer et al., 2000; Duguma et al., 2001;
Cummings et al., 2002; Chave et al., 2003; DeWalt and Chave, 2004;
Hoshizaki et al., 2004; Rolim et al., 2005; Smiley and Kroschel, 2008;
Alves Luciana et al., 2010; Chiti et al., 2010; Girardin et al., 2010;
Ibrahima et al., 2010; Lindner, 2010; Wade et al., 2010; Baraloto
et al., 2011; de Paula et al., 2011; Metzker et al., 2011; Morel et al.,
2011). Cocoa is also grown at a few dry forest locations, with rain-
fall between 800–1100 mm y−1 . Dry forests of Venezuela (Delaney
et al., 1997), Mexico (Jaramillo et al., 2003), South and Southeast
Asia (Brown et al., 1991), and Madagascar (Raherison and Grouzis,
2005), store between 27 and 63 Mg ha−1 of carbon in their above-
ground biomass.
The transformation of primary forests into cocoa plantations
entails a drastic reduction of forest carbon to give room and create
light and air circulation conditions adequate for cocoa production.
In Indonesia, the transformation of primary forests into cocoa AFS
decreased forest carbon by 75–88% (Stephan-Dewenter et al., 2007;
Smiley and Kroschel, 2008). In Central and West Africa, the conver-
sion of natural forests into cocoa plantations resulted in a 50% loss
of biomass (Duguma et al., 2001). In Cameroon, out of the original
forest’s 204 Mg C ha−1 stored in aboveground biomass, rustic cocoa
plantation retained 126 Mg C ha−1 , that is, 38% of the forest carbon

Table 6
Monetary value of carbon dioxide stored and accumulation rate per country in 229 Central American cocoa-based agroforestry systems, 2011.

CO2 rates and monetary values Nicaragua Guatemala Alta Verapaz Honduras Costa Rica Panama Guatemala Costa Sur Average

CO2 in aboveground biomass (Mg ha−1 ) 121 143 165 194 209 272 184
CO2 rate in aboveground biomass (Mg ha−1 year−1 ) 7 10 10 11 8 14 10
CO2 value in aboveground biomass (US$) 605 716 826 972 1046 1358 920
CO2 rate value in aboveground biomass (US$ year−1 ) 35 48 48 54 40 71 49

Mg CO2 = Mg C × 3.67; US$ = Mg CO2 × 5 us$ [Mg CO2 ]−1 .

52 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57
was lost (Kotto-Same et al., 1997). Other estimates from West Africa
establish forest carbon losses at 60–75% (Gockowski and Sonwa,
2011). In Ghana, carbon losses caused by clearing primary forests
to plant cocoa varied between 15 and 75%, depending on the typo-
logy of the cocoa plantation. Traditional cocoa plantations with
>25% shade cover retained 131 Mg C ha−1 of the 155 Mg ha−1 of
the local primary forest, while intensive cocoa plantations with
<25% shade retained 39 Mg ha−1 (Wade et al., 2010). The 32 Mg ha−1
of carbon retained by cocoa plantations with Erythrina fusca Lour
in Bahia, Brazil (Gama-Rodrigues et al., 2011) represent scarcely
18% of the carbon in primary forest of the “Mata Atlantica”, esti-
mated between 100 and 237 Mg ha−1 (Lindner, 2010). Central
American cocoa plantations retained only 49 Mg C ha−1 in above-
ground biomass, representing 27% of forest aboveground carbon
(180 Mg ha−1 ).
Total and aboveground carbon in Central American cocoa plan-
tations estimated in this study fall within ranges measured in other
parts of the world (Table 7).
The 49 Mg ha−1 of aboveground carbon in Central American
cocoa plantations are considerably lower than the average of
95 Mg C ha−1 reported by Albrecht and Kandji (2003), but com-
parable to cocoa plantations with specialized E. fusca shade in
Bahia, Brazil, which accumulated 32 Mg C ha−1 in aboveground
biomass (Gama-Rodrigues et al., 2011). Mixed-shade cocoa plan-
tations in the Peruvian Amazon, at 250–450 m altitude and
1000–1500 mm y−1 rainfall, stock 40–45 Mg ha−1 of aboveground
carbon (Concha et al., 2007). Hybrid cocoa plantations with mono-
specific Cordia alliodora shade stored 43–62 Mg ha−1 in 25 years
in Panama (Ortiz et al., 2008), 60 Mg ha−1 in Turrialba, Costa Rica
(Beer et al., 1990) and 49 Mg ha−1 in Caldas, Colombia (Aristizabal
and Guerra, 2002). Commercial rubber-cocoa mixed cropping in
Bahia (Brazil) stored 82 Mg ha−1 in aboveground carbon, includ-
ing 68 Mg ha−1 in rubber and 3.8 Mg ha−1 in cocoa (Cotta et al.,
2008). African cocoa plantations appear to store more aboveground
biomass carbon than their American counterparts. For example,
rustic shade (Kotto-Same et al., 1997) and mixed shade (Duguma
et al., 2001) cocoa plantations in Cameroon stored 125 Mg C ha−1 in
aboveground biomass. However, other estimates for West African
establish aboveground biomass at 89 Mg C ha−1 (Gockowski and
Sonwa, 2011). In Ghana, aboveground carbon varied between 39
and 131 Mg C ha−1 , depending on cocoa farm typology (Wade et al.,
2010).
Carbon in Central American cocoa-based AFS is stocked mainly
in the soil and in aboveground biomass (cocoa + shade canopy
trees). The amount of carbon in soil (51 Mg ha−1 ) was higher than
in 30 year-old, mixed shade cocoa plantations in Ghana, which
stocked 41 Mg C ha−1 (Dawoe et al., 2010). In Ghana, soil car-
bon content decreased with increased cocoa tree density (Ofori-
Frimpong et al., 2010). Unfortunately, most studies on soil carbon
in cocoa plantation soils are not directly comparable to our study
because they measured different soil profiles (Isaac et al., 2005; Rita
et al., 2011). There is evidence that soil carbon may be significantly
increased, especially during the first ten years of development of
the cocoa AFS (Beer et al., 1990; Albrecht and Kandji, 2003; Isaac
et al., 2005).
Carbon stored in cocoa tress under mixed shade canopies
in Central American plantations (9 Mg ha−1 ) compares well to
the 10.5 Mg C ha−1 stocked in an eight years old, full sun cocoa
plantations in Ghana (Isaac et al., 2007). Central American
cocoa plantations (rainfall of 2300–2600 mm y−1 ) maintain barely
1.1 Mg C ha−1 in the litter, while in Ghana (1300–1850 mm y−1 )
they store 2–3 Mg C ha−1 (Dawoe et al., 2010). In Bahia, Brazil, cocoa
plantations under E. fusca shade store 2.7 Mg C ha−1 in litter (Gama-
Rodrigues et al., 2011), while commercial associations of 6 year-old
grafted cocoa and 30 year-old rubber accumulated 1.67 Mg C ha−1
(Cotta et al., 2008).
Accumulation rates of aboveground carbon in Central Ameri-
can cocoa AFS (1.3–2.6 Mg C ha−1 ) are similar to the 1–2 Mg C ha−1
reported for several cocoa plantations worldwide (Table 7), but
lower than the 6 Mg C ha−1 reported for cocoa plantations with
mono-specific C. alliodora and Erythrina poeppigiana (Walp.) O.F.
Cook in Costa Rica (Beer et al., 1990), and rustic cocoa plantations
in Cameroon (Duguma et al., 2001).
4.2. Balancing carbon stocks and yields
In the search for cocoa agroforestry designs that optimally solve
the trade-offs between high yields and high carbon stocks a set
of key questions must be addressed: Can natural forests be mini-
mally degraded when converted into cocoa plantations? Are losses
of forest carbon, the allocation of carbon between soil and veg-
etation, and between cocoa and shade canopy trees determined
by the ecological conditions of the site, or vary depending on cli-
mate and soil? Can a maximum carbon stock compatible with
farmers’ objectives be reached for each cocoa plantation typo-
logy? To evaluate the effects of ecological conditions on these
trade-offs, a global study of the relevant literature combined with
expert knowledge and field work is needed. In what follows we
explore qualitatively the relationships, and alternatives for man-
aging the trade-offs, between carbon stocks and yields in cocoa
plantations.
Is it possible to design cocoa plantations with large stocks of car-
bon in both the cocoa (Ck) and canopy (Cc) compartments that also
produce high yields from both cocoa (Yk) and canopy (Yc) com-
partments? Current knowledge in crop management provides a
first glance at the interactions and functional relationships between
these four variables:
1. The effects of Ck on Yk has been the subject of research seeking
to determine the optimal cocoa tree density needed to achieve
maximum cocoa yield per hectare (Lockwood and Yina, 1996;
Dias et al., 2000). A detailed analysis of density–yield relation-
ship in cocoa is outside the scope of this paper, although we do
know that Yk increases with density—and Ck along with it—until
it peaks at the optimal density and then experiences a moderate
decrease at very high densities (Fig. 6a).
2. Carbon levels in cocoa (Ck) are not expected to have an effect
on canopy yields (Yc) (Fig. 6b). A as consequence, differences
in yields between cocoa plantations will depend on system’s
design, management, and other factors.
3. The relationship between Cc and Yk is well-known both in theory
(Zuidema et al., 2005; de Almeida and Valle, 2007) and practice
(Stephan-Dewenter et al., 2007; Wade et al., 2010; Gockowski
and Sonwa, 2011): cocoa yield (Yk) decreases in a non-linear
way with increased shade—and Cc along with it—(Fig. 6c).
4. It is expected that Yc increases asymptotically with increasing
Cc (Fig. 6d). However, if instead of total outputs from the canopy
(for both people and for nature) we look at useful output for
people, Yc may be expected to peak at an intermediate Cc level,
and then decrease slightly with increasing Cc.
After exploring the relationships between carbon levels and
yields, we now need to explore the relationships between Cc and
Ck in the five cocoa plantation typologies. In Fig. 7, we propose a
hypothetical preliminary distribution of Ck and Cc per typology,
based on the following arguments:
Although cocoa is planted at high densities in full sun cocoa
plantations (1600–2000 plants ha−1 ), Ck is not the maximum
attainable because the cocoa trees are regularly and heavily pruned
(Lockwood and Yina, 1996; Souza et al., 2009).
Maximum Ck is expected to occur in specialized-shade cocoa
plantations and decrease as Cc increases with the cocoa typology.
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57 53

Table 7
Carbon stocks in compartments of cocoa agroforestry systems in tropical regions around the world.

Region Temperature (◦ C) Rainfall (mm) Type of agroforestry system Age (years) Compartment Mg C ha−1 Source

Aboveground biomass 49.2 ± 34.9

Annual rate 2.6 ± 2.4
Central America 25 1700–4000 Mixed shade 24 This study
Cocoa biomass 9.0 ± 5.1
Annual cocoa rate 0.5 ± 0.4
Aboveground biomass 32
Cocoa/Erythrina fusca
Annual rate 1.1
26 1500 30 1
Aboveground biomass 33
Bahia, Brazil Cocoa cabruca
Annual rate 1.1
Cocoa/Hevea Aboveground biomass 82
25 1500 34 2
brasiliensis Annual rate 2.4
Aboveground biomass 30
20
Annual rate 1.5
Cocoa/timber/fruit Aboveground biomass 34
Amazonas, Peru 25 1500 12 3
trees Annual rate 2.8
Aboveground biomass 13
5
Annual rate 2.6
Caldas, Colombia 23 2250 Cocoa/musa/Cordia 13 Aboveground biomass 49 4
alliodora Annual rate 4.3
Bocas del Toro, Panama 27 3000 Cocoa/Cordia alliodora 25 Aboveground biomass 62 5
Annual rate 2.5
Turrialba, Costa Rica 24 2500–3000 Cocoa/Cordia alliodora 10 Aboveground biomass 60 6
Annual rate 6.0
Traditional cocoa Aboveground biomass 131
(>25% shade) Annual rate 2.6
East Ghana 24–29 1200–1600 50 7
Intensive cocoa (<25% Aboveground biomass 39
shade) Annual rate 0.8
Aboveground biomass 10
Shadeless cocoa
Annual rate 1.3
Aboveground biomass 18
Cocoa-Albizia
Annual rate 2.3
West Ghana 26 1100 8 8
Aboveground biomass 19
Cocoa/Milicia
Annual rate 2.3
Aboveground biomass 14
Cocoa/Newbouldia
Annual rate 1.8
Aboveground biomass 5
2
Annual rate 2.5
Aboveground biomass 54
Sefwi Wiawso, Ghana 26 1050 Multilayer cocoa 15 9
Annual rate 3.6
Aboveground biomass 81
25
Annual rate 3.2
Aboveground biomass 125
Cameroon sd sd Rustic cocoa 26 10
Annual rate 4.8
Aboveground biomass 89
Cocoa/timber
Annual rate 2.2
Southeast Cameroon 21 1550 40 11
Aboveground biomass 49
Shadeless cocoa
Annual rate 1.2
Aboveground biomass 31
Sulawesi, Indonesia 21 1550 Cocoa/Gliricidia sp. 15 12
Annual rate 2.1
Central America 25 1700–4000 Mixed shade 24 Soil (0–20 cm) 51 ± 15 This study
Southeast Cameroon 21 1550 Cocoa/timber Shadeless cocoa 40 Soil (0–20 cm) 43 11
Soil (0–15 cm) 25
Ghana sd 1500 Mixed shade 19 Soil (15–30 cm) 19 13
Soil (30–45 cm) 17
2 23
Sefwi Wiawso, Ghana 26 1050 Multilayer cocoa 15 Soil (0–15 cm) 18 9
25 18
Soil (0–10 cm) 40
Soil (10–30 cm) 38
Cocoa/Erythrina fusca 30
Soil (30–60 cm) 33
Soil (60–100 cm) 28
Bahia, Brazil 26 1500 1,15
Soil (0–10 cm) 58
Soil (10–30 cm) 50
Cocoa cabruca 30
Soil (30–60 cm) 37
Soil (60–100 cm) 27
Central America 25 1700–4000 Mixed shade 24 Litter 1.1 ± 1.3 This study
3 Litter 2
West Ghana 27 1300–1850 Mixed cocoa 15 3 14
30 3
26 1500 Cocoa/Erythrina fuscaCocoa cabruca 30 Litter 2.7 1
Bahia, Brazil
25 1500 Cocoa/Hevea brasiliensis 34 Litter 1.7 2

Source: 1: Gama-Rodrigues et al., 2011; 2: Cotta et al., 2008; 3: Concha et al., 2007; 4: Aristizabal and Guerra, 2002; 5: Ortiz et al., 2008; 6: Beer et al., 1990; 7: Wade et al.,
2010; 8: Isaac et al., 2007; 9: Isaac et al., 2005; 10: Duguma et al., 2001; 11: Gockowski and Sonwa, 2011; 12: Smiley and Kroschel, 2008; 13: Ofori-Frimpong et al., 2010; 14:
Dawoe et al., 2010; 15: Gama-Rodrigues et al., 2010.
Note: Carbon accumulation rates were calculated based on inventories and plantation age as reported by each author. The sources did not report soil and residual vegetation
carbon inventories at the moment of the cocoa-based AFS establishment.
54 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57

Fig. 6. Qualitative relationships between levels of aboveground C in cocoa (Ck) and in shade canopy trees (Cc), and yields of cocoa (Yk) and shade canopy (Yc).

This pattern is apparently confirmed by carbon distribution in

cocoa plantations with Gliricidia sepium in Indonesia (Smiley
and Kroschel, 2008) and cocoa plantations with E. fusca shade
in Bahia, Brazil (Gama-Rodrigues et al., 2011). Cocoa and canopy
carbon distribution data in the 229 cocoa plantations measured
by us in Central America (most of them under mixed canopies
and low cocoa plant density) seem to adjust to this hypothetical
distribution, as well.
Maximum Yk is expected to occur in full sun cocoa plantations,
and then decrease with increases in Cc in the cocoa typologies.
There is evidence for this. In Ghana, a cocoa intensification gradient
varied aboveground biomass carbon between 39 and 131 Mg ha−1
(Wade et al., 2010). Similar results were observed in an intensi-
fication gradient in Sulawesi, Indonesia (Stephan-Dewenter et al.,
2007).
Yc is nil in full sun cocoa, peaks in cocoa plantations with pro-
ductive (Cotta et al., 2008) and mixed shade, and decreases in
rustic ones (Gama-Rodrigues et al., 2011). Rustic canopies typi-
cally include a mix of valuable and non-commercial tree species
(Sambuichi, 2002).
The analysis above assumes that carbon level is a good pre-
dictors of yield, which may not always be the case. Two cocoa
plantations may have the same canopy carbon level, but in Plan-
tation 1 concentrated in a few, very tall trees, and in Plantation
2 distributed in many, small, short trees. Plantations 1 and 2
will have significant differences in the pattern of transmission of
solar radiation inside the cocoa plantation and may result in sig-
nificant differences in cocoa yield. In yet another example, two
plantations with the same canopy carbon level may have radically
different botanical compositions resulting again in very different
patterns of transmission of solar radiation into the plantation and
possibly in cocoa yields. Canopy species have an array of mor-
phological (e.g. leaf size and morphology, root systems, etc.) and
functional attributes (e.g. leaf fall patterns) that drastically influ-
Fig. 7. Carbon levels and expected yields for the cocoa and the canopy components
ence the transmission of solar radiation into the cocoa plantation,
and for each type of cocoa-based agroforestry systems.
thereby affecting the growth and yield of cocoa, and altering the
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57 55

Table 8
Standards for tandem-type certification, including considerations about amounts of stored carbon.

Standard Mechanism Elements Online source

VCM CDM C S B

The climate, community and Biodiversity Alliance (CCB) X X X X X http://www.climate-standards.org/index.html

Verified Carbon Standard (VCS) X X http://v-c-s.org/
The gold standard X X X X X http://www.cdmgoldstandard.org/
Social Carbon Standard X X X X http://www.socialcarbon.org/
Forest stewardship council (FSC) X X X X http://www.fsc.org/77.html
American Carbon Registry Standard (ACRS) X X X X X http://www.americancarbonregistry.org/
Carbco Platinum Carbon Standard X X X X http://www.cquestor.com/
Carbon Fix Standard (CFS) X X X X http://www.carbonfix.info/
EPA Climate Leaders Offset Guidance X X http://www.epa.gov/
Panda Standard X X X X http://www.pandastandard.org/
Plan Vivo X X X X http://www.planvivo.org/standard/
VER+ Standard X X X http://www.tuev-sued.de/
Chicago Climate Exchange (CCX) X X https://www.theice.com/ccx.jhtml
Green-e Climate X X http://www.green-e.org/
WRI/WBCSD GHG Protocol for Project Accounting X X X http://www.ghgprotocol.org/
Rain Forest Alliance X X X X X http://www.rainforest-alliance.org/

VCM: voluntary carbon markets; CDM: clean development mechanisms; C: carbon; S: social impacts; B: environmental impacts (biodiversity, land use, reforestation).

microclimate that is so determinant to the life cycles of pest and
diseases that reduce yields.
The manipulation of the morphological and functional traits of
canopy species has been used to optimize shade canopy design
in coffee (Bellow and Muschler, 1999; Linkimer et al., 2002) and
could be used in cocoa to both maintain high yields and car-
bon stocks. To stock high levels of carbon in the plot without
adversely affecting cocoa yields, one could select tree species with
(1) tall, cylindrical and thick stems—a tree form that may be called
Sequoia—like Terminalia ivorensis A. Chev. in West African cocoa
plantations. Large trees store most of forest aboveground biomass
(Lindner, 2010); tall trees cast a “lighter” shade than short trees;
(2) small canopies and light foliage (like Albizia spp.; (3) large,
deep, thick roots (Nair et al., 2009); and (4) rapid growth and
high-density timber; (5) inverted phenology which would be of
special interest (e.g. Faidherbia albida (Delile) A. Chev. in Africa,
which loses foliage during the rainy season and keeps it during the
dry season). This inverted phenology behavior has been observed
in Dalbergia glomerata Hemsley (a highly valuable timber) used
as shade over cacao in Honduras (Aroldo Dubón, FHIA, Honduras,
personal communication, 2011). It seems possible to design cocoa
plantations with high carbon stock levels and good cocoa yields.
Other authors have reached similar conclusions for cocoa plan-
tations in Indonesia and Ghana (Clough et al., 2011; Wade et al.,
2010).
The contribution of cocoa to sustainable production and the pro-
vision of ecosystem services (including carbon sequestration to
abate climate change) at the landscape level has been explored
(at least conceptually) in terms of the dichotomy between pro-
moting intensive cocoa production to free natural forest areas for
pure conservation (land-sparing strategy) and promoting mixed,
environmentally friendly cocoa agroforestry systems, which may
require a larger area due to smaller yields (wildlife-friendly farm-
ing strategy) but could reduce deforestation (Montagnini and Nair,
2004; Clough et al., 2011; Tscharntke et al., 2011; Wade et al.,
2010). To reduce deforestation and loss of natural forests, authors
have proposed to transform rustic cocoa into cocoa with produc-
tive shade (e.g. cocoa – timber systems), a controlled intensification
that would nonetheless reduce biodiversity and ecological com-
plexity (Stephan-Dewenter et al., 2007; Gockowski and Sonwa,
2011). In Bahia, Brazil, a large cocoa-growing territory encom-
passing more than 500,000 ha of rustic cocoa (a wildlife-friendly
landscape) and a few remnants of protected mature forest, inten-
sive production (land sparing strategy) is not attractive because
there is no more natural forest left to lose (Cotta et al., 2006).
In this region, the key question is how to increase rustic cocoa
yield without sacrificing its biodiversity and high total carbon stock
(Schroth et al., 2011). Central American cocoa plantations con-
form to a wildlife-friendly farming strategy, because 51% are using
mixed or rustic shade. Only 11% of Central American cocoa planta-
tions are intensively managed either at full sun or with specialized
shade.
Our results offer Central American cocoa producers a rigorous
estimate of carbon stocks in their cocoa plantations. Several stud-
ies show that, for these small producers (who must organize into
larger groups to accumulate a marketable amount of carbon certifi-
cates), voluntary markets seem to be the most appropriate (Miles
and Kapos, 2008; Somarriba et al., 2009; Hamilton et al., 2010; FAO,
2010). Large and small cocoa producers may choose among several
voluntary market-compatible standards (Table 8).
Tandem standards, which consider climate change, social
justice and ecological sustainability production aspects (organic or
low-input, biodiversity-friendly, etc.) seem appropriate for small
farmers (Somarriba et al., 2009). Additionally, tandem standards
point toward sustainable cocoa production, in line with the strate-
gies of the cocoa industry (http://www.worldcocoafoundation.
org/sustainability-principles-and-goals/; http://www.mars.com/
global/commitments/sustainability/cocoa-sustainability.aspx;
http://www.mars.com/global/principle-in-action/cocoa-
certification.aspx; Millard, 2011).
The results from our study will help cocoa farmers’ orga-
nizations to sell certified agroforestry products (cocoa, banana,
timber, fruit, carbon sequestration and other ecosystem ser-
vices) in market niches with better prices. Some possibilities
include (1) sustainable timber, Forest Stewardship Council pro-
tocol (www.fsc.org); (2) REDD+ offers access to payments for
carbon sequestration (Miles and Kapos, 2008); and (3) the Climate
Smart Agriculture program, supporting initiatives that enhance
food security, reduce vulnerability, mitigate and adapt to cli-
mate change (www.fao.org/climatechange/climatesmart/en/; FAO,
2010). The results and data gathered by our research could also
assist governments and the private sector in (1) designing bet-
ter legal, institutional and policy frameworks, local and national,
promoting an agriculture with trees (Albrecht and Kandji, 2003;
Seeberg-Elverfeldt et al., 2009; Wade et al., 2010; FAO, 2010;
Somarriba et al., 2012a,b); and (2) contributing to the development
of national monitoring, reporting and verification systems required
by the international community to access funding and payment for
ecosystem services (Angelsen et al., 2009; Intergovernmental Panel
on Climate Change, 2003a).
56 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57
5. Conclusion
It is possible to design cocoa-based AFS that provide both good
yields (cocoa and shade canopy) and high carbon densities. The
manipulation of morphological and functional traits of canopy
species may be used to optimize shade canopy design. To stock
high levels of carbon in the plot without adversely affecting cocoa
yields, one could select tree species with (1) tall, cylindrical and
thick stems (a “sequoia” type of tree); (2) small canopies and small,
light foliage; (3) large, deep, thick roots; (4) rapid growth and high-
density timber; and (5) inverted phenology.
Inventories and carbon storage rates in Central American cocoa
plantations are significant and similar to those in other cocoa-
growing regions around the world. The sale of carbon stored in
Central American cocoa can generate a modest income for cocoa
farmers. We expect that our results help governments, private firms
and producer organizations to formulate climate change adaptation
and abatement strategies, access payments for ecosystem services,
certify and obtain better prices for other products derived from
cocoa plantations (cocoa, fruits, timber, etc.), and to improve sus-
tainable cocoa production.
Acknowledgements
We would like to thank the support provided by field assis-
tants from COCABO (Cooperativa de Servicios Múltiples de Cacao
Bocatoreña, Panamá), ACOMUITA (Asociación de Mujeres Indíge-
nas de Talamanca, Costa Rica), CACAONICA (Cooperativa de Servicio
Agroforestal y de Comercialización de Cacao, Waslala, Nicaragua),
APROCACAHO (Asociación de productores de cacao de Honduras),
Instituto agroecológico bilingüe Fray Domingo de Vico, Cahabón,
Guatemala; ASECAN (Asociación de sembradores de cacao de la
cuenca del Nahualapa, Guatemala) and APROCA (Asociación de pro-
ductores de sur occidente de Guatemala). We would also like to
thank Ignacio Rodriguez Arias for is valuable help in the field in Tala-
manca (Costa Rica). Jenny Ordóñez, Bruno Rapidel, Goetz Schroth,
Antonio Carlos Gama-Rodríguez and anonymous reviewers pro-
vided valuable comments on the manuscript. Alejandra Villota and
David Calvache, from the University of Nariño, Colombia, helped
prepare tables, figures and bibliography. Research was funded by
CATIE/MAP/PCC.
References
Adejumo, T.O., 2005. Crop protection strategies for major diseases of cocoa, coffee
and cashew in Nigeria. Afr. J. Biotechnol. 4 (2), 143–150.
Albrecht, A., Kandji, S.T., 2003. Carbon sequestration in tropical agroforestry sys-
tems. Agric. Ecosyst. Environ. 99, 15–27.
Alves Luciana, F., Vieira Simone, A., Scaranello Marcos, A., 2010. Forest structure
and live aboveground biomass variation along an elevational gradient of tropical
Atlantic moist forest (Brazil). Forest Ecol. Manag. 260 (5), 679–691.
Angelsen, A., Brockhaus, M., Kanninen, M., Sills, E., Sunderlin, W.D., Wertz-
Kanounnikoff, S. (Eds.), 2009. Realising REDD+: National Strategy and Policy
Options. Cifor, Bogor.
Aristizabal, J., Guerra, A., 2002. Estimación de la tasa de fijación de C en el sistema
agroforestal Nogal Cafetero (Cordia alliodora) – Cacao (Theobroma cacao L.) –
Plátano (Musa paradisiaca). Univ. Distrital “Francisco José de Caldas” Fac. Med.
Amb. y Rec. Nat., Bogota.
Baraloto, C., Rabaud, D., Molto, Q., Blanc, L., Fortunel, C., Hérault, B., Dávila, N.,
Mesones, I., Ríos, M., Valderrama, E., Fine, P.V.A., 2011. Disentangling stand and
environmental correlates of aboveground biomass in Amazonian Forests. Glob.
Change Biol. 17 (8), 2677–2688.
Beer, J., Bonnemann, A., Chavez, W., Fassbender, H.W., Imbach, A.C., Martel, I., 1990.
Modelling agroforestry systems of cacao (Theobroma cacao) with laurel (Cordia
alliodora) or poro (Erythrina poeppigiana) in Costa Rica. V. Productivity indices,
organic material models and sustainability over ten years. Agrofor. Syst. 12,
229–249.
Bellow, J.G., Muschler, R.G., 1999. Screening for promising tree associates for cof-
fee in Central America. In: Jiménez, F., Beer, J. (Eds.), Multi-strata Agroforestry
Systems with Perennial Crops. CATIE, Turrialba, pp. 171–174.
Binternagel, N.B., Juhrbrandt, J., Koch, S., Purnomo, M., Schwarze, S., Barkmann, J.,
Faust, H., 2010. Adaptation to climate change in Indonesia – livelihood strategies
of rural households in the face of ENSO related droughts. Env. Sci. Eng. 2,
351–375.
Brown, S., Iverson, L.R., 1992. Biomass estimates for tropical forests. World Res. Rev.
4 (3), 366–383.
Brown, S., Gillespie, A.J.R., Lugo, A.E., 1991. Biomass of tropical forests of south and
southeast Asia. Can. J. For. Res. 21, 111–117.
Cairns, M.A., Brown, S., Helmer, E.H., Baungardner, G.A., 1997. Root biomass alloca-
tion in the world’s upland forests. Oecologia 111, 1–11.
Chave, J., Condit, R., Lao, S., Caspersen, J.P., Foster, R.M., Hubbell, S.P., 2003. Spatial
and temporal variation of biomass in a tropical forest: results from a large census
plot in Panama. J. Ecol. 91, 240–252.
Chiti, T., Certini, G., Grieco, E., Valentini, R., 2010. The role of soil in storing car-
bon in tropical rainforests: the case of Ankasa Park, Ghana. Plant Soil 331 (1),
453–461.
Clark, D.B., Clark, D.A., 2000. Landscape-scale variation in forest structure and
biomass in a tropical rainforest. Forest Ecol. Manag. 137, 185–198.
Clough, Y., Barkmann, J., Juhrbandt, J., Kessler, M., Wanger, T.C., Anshary, A., Buchori,
D., Cicuzza, D., Darras, K., Putra, D., Erasmi, S., Pitopang, R., Schmidt, C., Schulze,
C.H., Seidel, Steffan-Dewenter, I., Stenchly, K., Vidal, S., Weist, M., Wielgoss, A.C.,
Tscharntke, T., 2011. Combining high biodiversity with high yields in tropical
agroforests. PNAS 108, 8311–8316.
Concha, J., Alegre, J., Pocomucha, V., 2007. Determinación de las reservas de C
en la biomasa aérea de sistemas agroforestales de Theobroma cacao, L. en el
departamento de San Martín, Perú. Ecol. Appl. 6, 75–82.
Cotta, M., Goncalves, L., de Paiva, H.N., Soares, C.P.B., Virgens Filho, A. de C., Valverde,
S.R., 2008. Quantificacao de biomassa e geracao de certificados de emissoes
reduzidas no consorcio seringueira – cacau. Árvore 32 (6), 969–978.
Cotta, M., Gonçalves, L., Valverde, S., Nogueira, H., Virgens, A., Lopes, M., 2006.
Análise econômica do consorcio seringueira – cacau para geração de certificados
de emissões reduzidas. Árvore 30 (6), 969–979.
Cummings, D.L., Kauffman, J.B., Perry, D.A., Hughes, R.F., 2002. Aboveground biomass
and structure of rainforests in the southwestern Brazilian Amazon. Forest Ecol.
Manag. 163, 293–307.
Dalquist, R.M., Whelan, M.P., Winowiecki, L., Polidoro, B., Candela, S., Harvey, C.A.,
Wulfhorst, J.D., McDaniel, P.A., Bosque-Pérez, N.A., 2007. Incorporating liveli-
hoods in biodiversity conservation: a case study of cacao agroforestry systems
in Talamanca, Costa Rica. Biodivers. Conserv. 16, 2311–2333.
Dawoe, E.K., Isaac, M.E., Quashie-Sam, J., 2010. Litterfall and litter nutrient dynamics
under cocoa ecosystems in lowland humid Ghana. Plant Soil 330, 55–64.
de Almeida, A.A.F., Valle, R., 2007. Ecophysiology of the cacao tree. Braz. J. Plant.
Physiol. 19 (4), 425–448.
de Paula, M.D., Costa, C.P.A., Tabarelli, M., 2011. Carbon storage in fragmented land-
scape of Atlantic forest: the role played by edge-affected habitats and emergent
trees. Trop. Conserv. Sci. 4 (3), 349–358.
Deheuvels, O., 2011. Compromis entre productivité et biodiversité sur un gradi-
ent d’intensité de gestion de systèmes agroforestiers à base de cacaoyers de
Talamanca, Costa Rica. SupAgro, Montpellier.
Deheuvels, O., Avelino, J., Somarriba, E., Malezieux, E., 2012. Vegetation structure
and productivity in cocoa-based agroforestry systems in Talamanca, Costa Rica.
Agric. Ecosyst. Environ. 149, 181–188.
Delaney, M., Brown, S., Lugo, A.E., Torres-Lezama, A., Bello-Quintero, N., 1997. The
distribution of organic carbon in major components of forests located in five life
zones of Venezuela. J. Trop. Ecol. 13, 697–708.
DeWalt, S.J., Chave, J., 2004. Structure and biomass of four lowland neotropical
forest. Biotropica 36 (1), 7–19.
Dias, L.A.S., Santos, M.M., Santos, A.O.S., Almeida, C.M.V.C., Cruz, D.C., Carneiro, P.C.S.,
2000. Effect of planting density on yield and incidence of witches broom disease
in a Young plantation of hybrid cacao trees. Exp. Agric. 36, 501–508.
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W.,
InfoStat versión 2012. Grupo InfoStat, FCA, Universidad Nacional de Córdoba,
Argentina. URL: http://www.infostat.com.ar
Dixon, R.K., 1995. Agroforestry systems: sources or sinks of greenhouse gases?
Agrofor. Syst. 31, 99–116.
Duguma, B., Gockowski, J., Bakala, J., 2001. Smallholder cacao (Theobroma cacao,
Linn.) cultivation in agroforestry systems of West and Central Africa: challenges
and opportunities. Agrofor. Syst. 51, 177–188.
FAO, 2010. Climate-smart agriculture. In: Policies, Practices and Financing for Food
Security, Adaptation and Mitigation. FAO, Rome.
Frangi, J.L., Lugo, A.E., 1985. Ecosystem dynamics of a subtropical floodplain forest.
Ecol. Monogr. 55, 351–369.
Gama-Rodrigues, E.F., Gama-Rodrigues, A.C., Nair, P.K.R., 2011. Soil carbon seques-
tration in cacao Agroforestry Systems: a case study from Bahia, Brazil. In: Kumar,
B.M., Nair, P.K.R. (Eds.), Carbon Sequestration Potential of Agroforestry Systems:
Opportunities and Challenges. Advances in Agroforestry 8. Springer-Science,
New York, pp. 85–99.
Gama-Rodrigues, E., Nair, P.K.R., Nair, V.D., Gama-Rodrigues, A.C., Baligar, V.,
Machado, R.C.R., 2010. Carbon storage in soil size fractions under two cacao
agroforestry systems in Bahia, Brazil. J. Environ. Manag. 45, 274–283.
Girardin, C.A.J., Malhi, Y., Aragao, L.E.O.C., Mamani, M., Huaraca-Huasco, W., Durand,
L., Feeley, K.J., Rapp, J., Silva-Espejo, J.E., Silman, M., Salinas, N., Whittaker, R.J.,
2010. Net primary productivity allocation and cycling of carbon along a trop-
ical forest elevational transect in the Peruvian Andes. Glob. Change Biol. 16,
3176–3192.
Gockowski, J., Sonwa, D., 2011. Cocoa intensification scenarios and their predicted
impact on CO2 emissions, biodiversity conservation, and rural livelihoods in the
Guinea rain forest of West Africa. Environ. Manage. 48, 307–321.
 E. Somarriba et al. / Agriculture, Ecosystems and Environment 173 (2013) 46–57
Hamilton, K., Sjardin, M., Peters-Stanley, M., Marcello, T., 2010. Building bridges:
state of the voluntary carbon markets 2010. Ecosystems Marketplace and
Bloomberg New Energy Finance, USA.
Hoshizaki, K., Niiyama, K., Kimura, K., Yamashita, T., Bekku, Y., Okuda, T., Quah, E.S.,
Supardi, N., 2004. Temporal and spatial variation of forest biomass in relation
to stand dynamics in a mature, lowland tropical rainforest, Malaysia. Ecol. Res.
19, 357–363.
Ibrahima, A., Mvondoze, A., Ntonga, J.C., 2010. Aboveground biomass and nutrient
accumulation in the tropical rainforest of southern Cameroon: effects of logging.
Cameroon J. Exp. Biol. 6 (1), 49–62.
Intergovernmental Panel on Climate Change, 2003a. Climate change 2000: Synthesis
Report. IPCC Third Assessment Report, WMO UNEP, Geneva.
Intergovernmental Panel on Climate Change, 2003b. Good Practice Guidance for
Land Use, Land-Use Change and Forestry. IGES, Kanagawa.
Isaac, M.E., Gordon, A.M., Thevathasan, N., Oppong, S.K., Quashie-Sam, J., 2005.
Temporal changes in soil carbon and nitrogen in west African multistrata
agroforestry systems: a chronosequence of pools and fluxes. Agrofor. Syst. 65,
23–31.
Isaac, M.E., Timmer, V.R., Quashie-Sam, S.J., 2007. Shade tree effects in an 8-year old
cocoa agroforestry system: biomass and nutrient diagnosis of Theobroma cacao
by vector analysis. Nutr. Cycl. Agroecosyst. 78, 155–165.
Jaramillo, V.J., Kauffman, J.B., Rentería-Rodríguez, L., Cummings, D.L., Ellingson, L.J.,
2003. Biomass, carbon, and nitrogen pools in Mexican tropical dry forest land-
scapes. Ecosystem 6, 609–629.
Kotto-Same, J., Woomer, P.L., Mounkan, A., Zapfack, L., 1997. Carbon dynamics in
slash-and-bum agriculture and land use alternatives of the humid forest zone
in Cameroon. Agric. Ecosyst. Environ. 65, 245–256.
Lindner, A., 2010. Biomass storage and stand structure in a conservation unit in the
Atlantic Rainforest—the role of big trees. Ecol. Eng. 36, 1769–1773.
Linkimer, M., Muschler, R., Benjamin, T., Harvey, C., 2002. Árboles nativos para diver-
sificar cafetales en la zona Atlántica de Costa Rica. Agrofor. Amér. 9 (35–36),
37–43.
Lockwood, G., Yina, J.P.T., 1996. Yields of cocoa clones in response to planting density
in Malaysia. Exp. Agric. 32, 41–47.
MacDiken, K., 1997. A guide to monitoring carbon storage in forestry and agro-
forestry projects. Winrock International, Arlington.
Metzker, R., Spósito, T.C., Martins, M.T.F., Horta, M.B., García, Q.S., 2011. For-
est dynamics and carbon stocks in Rio Doce State Park, an Atlantic rainforest
hotspot. Curr. Sci. 100 (12), 1855–1862.
Miles, L., Kapos, V., 2008. Reducing greenhouse gas emissions from defor-
estation and forest degradation: global land-use implications. Science 320,
1454–1455.
Millard, E., 2011. Incorporating agroforestry approaches into commodity value
chains. Environ. Manage. 48, 365–377.
Montagnini, F., Nair, F.P.K.R., 2004. Carbon sequestration: an underex-
ploited environmental benefit of agroforestry systems. Agrofor. Syst. 61,
281–295.
Morel, A.C., Saatchi, S.S., Malhi, Y., Berry, N.J., Banin, L., Burslem, D., Nilus, R., Ong,
R.C., 2011. Estimating above ground biomass in forest and oil palm plantation
in Sabah, Malaysian Borneo, using ALOS PALSAR data. Forest Ecol. Manag. 262
(9), 1786–1798.
Nair, P.K.R., Kumar, B.M., Nair, V.D., 2009. Agroforestry as a strategy for carbon
sequestration. J. Plant Nutr. Soil Sci. 172, 10–23.
Ofori-Frimpong, K., Afrifa, A.A., Acquaye, A., 2010. Impact of shade and cocoa plant
densities on soil organic carbon sequestration rates in a cocoa growing soil of
Ghana. Afric. J. Environ. Sci. Technol. 4 (9), 621–624.
Ortiz, A., Riascos, L., Somarriba, E., 2008. Almacenamiento y tasas de fijación de
biomasa y C en sistemas agroforestales de cacao (Theobroma cacao) y laurel
(Cordia alliodora). Agrofor. Amér. 46, 26–30.
Paustian, K., Six, J., Elliott, E.T., Hunt, H.W., 2000. Management options for reducing
CO2 emissions from agricultural soils. Biogeochemistry 48, 147–163.
Peters-Stanley, M., Hamilton, K., Marcello, T., Sjardin, M., 2011. Back to the Future:
State of the Voluntary Carbon Markets 2011. Ecosystem Market Place Forest
Trends Association and Bloomberg New Energy Finance, USA.
Raherison, S.M., Grouzis, M., 2005. Plant biomass, nutrient concentration and nutri-
ent storage in a tropical dry forest in the south-west of Madagascar. Plant Ecol.
180, 33–45.
Rice, R., Greenberg, R., 2000. Cacao cultivation and the conservation of biological
diversity. Ambio 29, 167–173.
Rita, J.C.O., Gama-Rodrigues, E.F., Gama-Rodrigues, A.C., Polidoro, J.C., Machado,
R.C.R., Baligar, V.C., 2011. C and N content in density fractions of whole soil
and soil size fraction under cacao agroforestry systems and natural forest in
Bahia, Brazil. Environ. Manage. 48 (1), 134–141.
Rolim, S.G., Henrique, R.M.J., Nascimento, H.E.M., do Couto, H.T.Z., Chambers,
J.Q., 2005. Biomass changes in an Atlantic tropical moist forest. The ENSO
effect in permanent sample plots over a 22-year period. Oecologia 142,
238–246.
Sambuichi, R.H.S., 2002. Fitossociologia e diversidade de especies arbóreas em
cabruca (mata Atlantica raleada sobre plantaçao de cacau) na regiao sul da Bahía,
Brasil. Acta Bot. Brasil. 16 (1), 89–101.
View publication stats
57
Schmitz, H., Shapiro, H.Y., 2012. The future of chocolate. Sci. Am. 2012, 60–65.
Schroeder, P., 1994. Carbon storage benefits of agroforestry systems. Agrofor. Syst.
27, 89–97.
Schroth, G., Faria, D., Araujo, M., Bede, L., van Bael, S.A., Cassano, C.R., Oliveira, L.C.,
Delabie, J.H.C., 2011. Conservation in tropical landscape mosaics: the case of the
cacao landscape of southern Bahia, Brazil. Biodivers. Conserv. 20, 1635–1654.
Seeberg-Elverfeldt, C., Schwarze, S., Zeller, M., 2009. Payments for environmental
services – carbon finance options for smallholders’ agroforestry in Indonesia.
Int. J. Commons 3, 108–130.
Smiley, G.L., Kroschel, J., 2008. Temporal change in carbon stocks of cocoa – Gliricidia
agroforests in Central Sulawesi, Indonesia. Agrofor. Syst. 73, 219–231.
Smit, B., Skinner, M.W., 2002. Adaptation options in agriculture to climate change:
a typology. Mitig. Adapt. Strat. Glob. Change 7, 85–114.
Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M.,
Miller, H.L. (Eds.), 2007. Climate Change 2007: The physical science basis. Con-
tribution of IPCC Working Group I to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change, Cambridge Univ. Press, USA.
Somarriba, E., Andrade, H., Segura, M., Villalobos, M., 2008. ¿Cómo fijar C atmosférico,
fijarlo y venderlo para complementar los ingresos de productores indígenas de
Costa Rica? Agrofor. Amér. 46, 81–88.
Somarriba, E., Beer, J., Orihuela, J.A., Andrade, H., Cerda, R., DeClerck, F., Detlefsen, G.,
Escalante, M., Giraldo, L.A., Ibrahim, M.A., Krishnamurthy, L., Mena, V.E., Mora,
J.R., Orozco, L., Scheelje, M., Campos, J.J., 2012b. Mainstreaming agroforestry in
Latin AmericaA, Advances in Agroforestry. In: Nair, P.K.R., Garrity, D.P. (Eds.),
Agroforestry: the way forward. Springer, USA, 9: 429-453.
Somarriba, E., Villalobos, M., Orozco, L., 2009. Cocoa in Central America. GRO-Cocoa
Bull. 14 (November), 5–9.
Souza, C.A.S., dos Santos Dias, L.A., Aguilar, M.A.G., Sonegheti, S., Oliveira, J., Andrade
Costa, J.L., 2009. Cacao yield in different planting densities. Braz. Arch. Biol.
Technol. 52 (6), 1313–1320.
Stephan-Dewenter, I., Kesslerc, M., Barkmannc, J., Bosa, M., Buchorig, D., Erasmih,
S., Fausth, H., Geroldh, G., Glenke, K., Gradsteind, S.R., Guhardjai, E., Harteveldd,
M., Herteld, D., Höhna, P., Kappash, M., Köhlerh, S., Leuschnerd, C., Maertensj,
M., Marggrafe, R., Migge-Kleiank, S., Mogeai, J., Pitopangl, R., Schaeferk, M.,
Schwarzem, S., Spornd, S.G., Steingrebek, A., Tjitrosoedirdjoi, S.S., Tjitrosoemi-
toi, S., Tweleh, A., Weberh, R., Woltmannk, L., Zellerm, M.N., Tscharntkea, T.,
2007. Tradeoffs between income, biodiversity, and ecosystem functioning dur-
ing tropical rainforest conversion and agroforestry intensification. PNAS 104
(12), 4973–4978.
Szott, L.T., Arévalo-López, L.A., Pérez, J., 1993. Allometric relationships in Pijuayo
(Bactris gasipaes H.B.K.). In: Mora-Urpí, J., Szott, L.T., Murillo, M., Patiño, V.M.
(Eds.), Congreso Internacional sobre Biología, Agronomía e Industrialización del
Pijuayo. San José, pp. 91–114.
Tanaka, A., Yamaguchi, 1972. Producción de materia seca, componentes del
rendimiento y rendimiento del grano de maíz. Colegio de postgraduados,
Chapingo.
Tscharntke, T., Clough, Y., Bhagwat, S.A., Buchori, D., Faust, H., Hertel, D., lscher,
D.H., Juhrbandt, J., Kessler, M., Perfecto, I., Scherber, C., Schroth, G., Veldkamp,
E., Wanger, T.C., 2011. Multifunctional shade-tree management in tropical agro-
forestry landscapes. J. Appl. Ecol. 48, 619–629.
Van Wagner, C.E., 1968. The line intersect method in forest fuel sampling. Forest
Sci. 14, 20–26.
Verchot, L.V., Van Noordwijk, M., Kandji, S., Tomich, T., Ong, C., Albrecht, A.,
Mackensen, J., Bantilan, C., Anupama, K.V., Palm, C., 2007. Climate change: link-
ing adaptation and mitigation through agroforestry. Mitig. Adapt. Strat. Glob.
Change 12, 901–918.
Wade, A.S.I., Asase, A., Hadley, P., Mason, J., Ofori-Frimpong, K., Preece, D., Spring,
N., Norris, K., 2010. Management strategies for maximizing carbon storage and
tree species diversity in cocoa-growing landscapes. Agric. Ecosyst. Environ. 138,
324–334.
Whelan, M., Dahlquist, R., Winowiecki, L., Polidoro, B., Candela, S., Harvey, C.,
Wulfhorst, J., McDaniel, P., Bosque-Pérez, N., 2007. Incorporating livelihoods
approach for biodiversity conservation: a case study in cocoa agroforestry sys-
tems in Talamanca, Costa Rica. Biodivers. Conserv. 16, 2311–2333.
Winjum, J.K., Dixon, R.K., Schroeder, P.E., 1992. Estimating the global potential of
forest and agroforest management practices to sequester carbon. Water Air Soil
Pollut. 64, 213–223.
Wood, G.A.R., Lass, R.A., 2001. Cocoa, 4th ed. Blackwell Science, Oxford.
Woomer, P.L., Palm, C.A., Alegre, J., Castilla, C., Cordeiro, D.G., Hairiah, K., Kotto-Same,
J., Moukam, A., Riese, A., Rodrigues, V., van Noordwijk, M., 2000. Slash-and-burn
effects on carbon stocks in the humid tropics. In: Lal, R., Kimble, J.M., Stewart, B.A.
(Eds.), Global Climate Change and Tropical Ecosystems. CRC Press, Boca Raton,
pp. 99–115.
World Resources Institute, 2005. Climate Analysis Indicator Tool (CAIT), Navi-
gating the Numbers: Greenhouse Gas Data and International Climate Policy.
www.lowcarboneconomy.com/Resources/UserImages/06-prob wri-flowchart
009Original.jpg (accessed July 2012).
Zuidema, P.A., Leffelaar, P.A., Gerritsma, W., Mommer, L., Anten, N.P.R., 2005. A phys-
iological production model for cocoa (Theobroma cacao): model presentation,
validation and application. Agric. Syst. 84 (2), 195–225.