Cacao Cultivation and the Conservation of Biological Diversity

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Article
Robert A. Rice and Russell Greenberg
Cacao
Cultivation
Biological
Diversity
and
the
Cacao (Theobromacacao) is a crop of the humidlowland
tropics produced largely by small-scale producers and
often on farms with a canopy of shade trees. Where a
diverse shaded canopy is used, cacao farms support
higherlevels of biologicaldiversitythan most othertropical
crops. A host of viral and fungal diseases, loss of soil
fertility,and numerous socioeconomic problems facing
producers,often makes cacao productionlocallyunsustainable. Continuedclearingof new lands threatens biodiversity.Moreover,new frontiersforcacao expansionare rapidly
disappearing. Such problems can be addressed by increasingthe long-termproductivityof existingcacao farms
and restoringabandoned lands. Improvedshade management offers guidance along this path. Institutionsinvolved
with cocoa should establish collaborations with groups
concerned with development, environmentalprotection,
and most importantlyproducers themselves to pursue a
program of research, extension and policy initiatives
focused on the ecologically and economicallysustainable
cacao productionon farms witha diverse shade canopy.
Conservation of
est species-to commercialshade where other tree crops are interspersed among planted shade trees and the cacao, to
monocultural,specialized shade, where the shade is dominated
by one or a few tree species or genus (genera).Some indigenous
shade systems are truly diverse agroforests.However, in most
plantedsystems where a multitudeof shade species is found (up
to 30-40 in some planted systems), one or a few species generally comprise the "backbone"shade component in which other
fruitingand timberspecies are inserted.Such backbonespecies,
usuallyfast-growing,nitrogen-fixinglegumes, includeErythrina
spp., Gliricidiasepium, Cassia, and Inga spp. In some areas,cacao is grownunder,or intercroppedprimarilywith, fruitandfast-
Figure1. Cacao shade managementsystems,
showing shade gradientand canopy heights.
Rustic cacao
planted beneath thinned
primary or old secondary
forest
1 {; a
INTRODUCTION
As the world faces alarmingrates of tropical forest loss, some
agricultural systems offer a glimmer of hope. In particular,
agroforestry,wherecrops are cultivatedin associationwith trees,
provides some of the ecological benefits of naturalforest while
allowing farmersto make a living off theirland (1-3). However,
only in agroforestrysystems that involve the productionof globally tradedand economically importantcommodities, such as
cocoa (Theobroma cacao), can we realistically expect that
enough land and people will be affected to make a difference.
The environmentalbenefits thatcacao farmsmay confer depend
upon the managementsystem. On one hand, we find a low-input and generally low-yield system that requires few, if any,
agrochemicals. These farms often incorporateremnant forest
shadeinto the farmmanagementsystem. In contrast,are the systems characterizedby high-input,high-yield farms, often with
little or no shade. These are extremes of a continuumand between them we find managedagroforestrysystems with planted
shade trees and moderatelevels of chemical inputs.
We will develop the argument that systems using diverse
shade offer the greatest potential for long-term production,
biodiversityconservation,and environmentalprotection.We begin our discussion of how different shade cacao systems influence tropicalbiological diversity, then provide a brief overview
of patternsof production,and finally explore ways in which the
patternof productionmight be changed to optimize biological
diversity, cacao production,and the livelihood of the millions
of small farmerswho grow the crop.
1 3 . .. i .......
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.......
, ......
.r........ f
~~~~~~~.
8
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16
Shade
~~~~~~Planted
ranges from traditional
polyculturethrough
commercialto a specialized,
single-species shade
8
0
meters
SHADESYSTEMS
Shade managementsystems in cacao form a gradient(Fig. 1),
analogousto thatseen in coffee (3, 4). Rusticcacao management,
widespreadin the humid portion of West Africa and local in
Latin America, is characterizedby the planting of cacao under
thinnedprimaryor older secondaryforest (5). Plantedshade systems vary widely, from traditionalpolyculturalsystems-multiple species of plantedshadetrees with occasional remnantforAmbio Vol. 29 No. 3, May 2000
8
Technified Cacao
no shade component
o
meters
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167
growing timbertrees. Zero-shadecacao (6) cultivation,without
shade, is common in Malaysia and becoming more widespread
in parts of Colombia and Peru. These three basic systems contributevery differentlyto the conservationof biological conservation.
DIVERSITYIN CACAOFARMS
BIOLOGICAL
Three fundamental questions concerning the relationship between the cultivationof shade-growncacao and biodiversityare:
i) How much of the original tropical forest diversity is maintained on cacao farms? ii) How does this compare with other
agriculturalsystems?iii) Whatis the role of differentcacao managementsystems in the maintenanceof tropicaldiversity?
Rustic Cacao
A limitedbody of work upholdsthe notionthatcacao farmswith
a diverse shade canopy supportgreaterbiological diversity,particularlyof forest-dependentorganisms,thanothercash crop systems in the lowland tropics (7-15).
However, even the most diverse rustic shade farmsare highly
modified comparedto naturalforest-combining forest generalist and early successional species (7, 16, 17); tropicalforest specialists are often missing. For example, one study found only
two out of seven forestAnolis lizard species in rusticplantations
in Costa Rica (18). In Brazil's cabruca system, large-bodiedterrestrial mammals and larger primates were among the groups
underrepresentedin the cacao. Rustic cacao bird assemblages
lackedmany of the specializedunderstoryspecies, and supported
low abundancesof foliage-gleaning insectivorousbirds, understory frugivores, and relatively high abundances of canopy
frugivoresand omnivores (19). Rustic cacao farms form highly
modified tropical forest systems. The change to the understory
is obvious, and the canopy is also dramaticallyaltered.For example,in the cabrucamanagementsystem of Bahia,Brazil,trees
and shrubsare thinned to 10% of their original abundanceand
most lianas removed (19), which substantiallyreduces plant diversity. More importantly,canopy regenerationis eliminatedor
the ecological conditionsfor regenerationare not met, and eventually the naturallyoccurringtrees are replacedby plantedtrees
often nitrogen-fixing legumes, trees that provide optimal
shade,or plantsthatproduceuseful fruits,wood, and otherproducts. Management that removes or modifies specific microhabitats(mistletoe, epiphytes, etc.) may cause critical changes
in overall diversity.The importanceof specific microhabitats
to ants and otherinvertebrateshas been underscoredin the re-
search of Room (8, 20) and Young, (21, and ref. therein). At
the landscape scale, cacao farms suffer from fragmentationand
isolation, representingone land-use type within a mixed mosaic
of uses. This alone leads to the loss of the original forest species and the increase in habitatgeneralists-organisms usually
associatedwith disturbedor recoveringhabitats.
Zero and Planted Shade Systems
Althoughlittle researchhas examinedbiodiversityin zero-shade
cacao systems, ongoing studies of bird communities in the PeruvianAndes have shown that zero-shadecacao supportsa few
early successional species (Greenberg,unpubl.data);further,it
is reasonable to assume from work in coffee that cacao farms
using few or no shade tree species supportlower levels of biological diversity and relatively few forest-dependentorganisms.
Some work suggests that planted shade systems are less diverse than rustic systems (2). Room (17) speculated that the
abovegroundant diversityof Ghanaiancacao farmswas substantially greaterthanthatof New Guineaat least partlybecause the
former are small rustic plantationsand the latter largerplanted
shadefarms.From studies of the ant-mosaics,thereis some suggestion thatin plantationsof structurallysimple shade,fewer ants
are able to dominatethe habitatmore thoroughly(22).
Greenberget al. (23) found that the bird diversity of cacao
plantationsin the Gulf Lowlandsof Tabasco,Mexico, supported
only a modest abundanceand diversity of birds, even compared
with other agriculturaland disturbedhabitats.These farms supported almost no resident forest birds, although migratoryforest species were quite common. They speculated that the lack
of bird diversity may, in part, be a result of the lack of small
bird-dispersedfruitin the cacao understoryand the shadecanopy.
However, the Tabasco cacao region has little forest and the lack
of nearby naturalforest may have played an importantrole as
well.
It is likely that a numberof forest organismscan occur in cacao, but requireforest for partof theirlife cycle. A small amount
of data (9-13, 19) sustain the concept that rustic cacao systems
close to naturalforest-particularly large tractsof forest-support substantiallygreaterdiversity of forest birds and mammals
than those systems isolated from naturalhabitats. Young (21)
has made a similar argumentfor invertebrates,including some
of the pollinatorsfor cacao. In fact, some noteworthyendemic
vertebratesfound in rusticcacao farms,i.e., the recentlydiscovered Pink-legged Graveteiro,Acrobatornisfonsecai and the endangeredGolden-headedLion Tamarin,Leontopithecuschrysomelis, seem also to require forest
patches and use cacao as a secondary habitat(19, 24).
The implicationsof this proximity effect are unclear.Cacao farms
may be populationsinks, unableto
supportpopulationsof many forest
organismsin the long run,but benefiting from periodic emigration
from source forest habitats.On the
positive side, mobile forest organisms may requireresourcesnot present in a protectedforest patch on
a seasonalbasis. This is particularly
true for altitudinally migrating
birds and insects where forest remains only at higher elevations.
Moreover, cacao farms may provide a suboptimal buffer habitat
thatwould promotepopulationstability in the optimal forest habitat.
Finally, cacao farmsmight provide
corridorsor stepping stones of ac-
Figure 2. Majorcacao producing countries, hectares harvested.
Thousandsof
hectares
*1200
*
0
168
600
120
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Ambio Vol. 29 No. 3, May 2000
forest lands, 1.3% of all forest converted to agriculturallands,
and 0.5% of all lands convertedfrom primaryforest to agriculture or secondaryand degradedforests (27). Cacao's contribution to deforestationvaries considerablybetween regions (Table 3). In particular,13.4% of the original forestlandsof Cote
d'Ivoire are now in cacao plantations.Almost one-sixth of the
cleared lands is in cacao farms.
Cacao historiansgenerally concur that the expansion of "cacao frontiers"has often occurredat the expense of forestlands.
During recent decades, when cacao area expanded upwardsof
2.1 mill. ha worldwide, COted'Ivoire in West Africa, and Malaysia and Indonesiain SoutheastAsia, accountedfor some 82%
of thatgrowth.Duringthe 1970s and 1980s, approximately90%
of the cacao expansionin Cote d'Ivoire took place in forestlands
(Ruf, pers. comm.). In Malaysia, the advanceof the cacao frontier into forested areas characterized60% of the new production zones overall;however, whereasin Sabahand Sarawak8090% of the expansion occurredin forests, in peninsularMalaysia, where producersopted to place cacao beneath extant coconut groves, only about20% of the growth took place in forested
lands. In Indonesia, and especially in Sulawesi, the 1980s and
1990s saw about 50% of the cacao area appearingin formerly
forestedareas(Ruf, pers.comm.). The directconnectionbetween
cacao and deforestation,however,must be viewed within the dynamic of other agriculturalactivities and logging interests. For
instance, the alluvial soils of the Indonesian coastal cacao region were previously planted to other crops. In this particular
CACAOPRODUCTIONAND DEFORESTATION
instance, cacao displaced those crops due to the rich soil and
Cacao productionshows rapid expansion in recent decades. In favorablerainfallpatterns.Moreover, cacao often moved in af1970, the global cacao harvestwas only 1.5 mill. tonnes on 4.1 ter logging activity in Indonesia. Thus, approximately50% of
mill. ha. By 1995, 3.0 mill. tonnes of beans (25) was harvested the cacao expansiontook place at the expense of forest,with only
from 6.57 mill. ha. This representsa doubling of cacao produc- half of that (25%) being the direct result of small producersadtion and a 50% increasein areacultivatedin only 25 years. Cur- vancing into forested zones (Ruf, pers. comm.).
rent productionis concentratedin African, and to a lesser degree Asian countries(Fig. 2; Table 1), particularlyCOted'Ivoire
and Ghana, each with more than a mill. ha harvested in 1996 SMALL-SCALEPRODUCERS
With a few regional exceptions, such as Brazil and Malaysia,
(26).
How has this increaseimpactedthe scarce remaininglowland small-scale producersform the backbone of the industry.Even
humid tropical forests? On a worldwide scale, cacao accounts when the average size of holdings is large, such as in Brazil,
for only (and very approximately)0.3% of the original tropical those farms at the small end of the size spectrumgreatly outnumber larger plantations.Cameroon and Ghana have typical
distributions for farm size, with a predominance of holdings
ranging in size from less than 1 ha to 5 or 10 ha (see Table 2).
Table1. Cacaoarea harvestedand percentof
In Nigeria, the averagefarm size is 1.7 ha, in Ecuadorit reaches
globalarea represented,by country,1996.
4.5 ha, and in Cote d'Ivoire, farms average 2.8 ha (Ng, pers.
Source: FAO,1996 (26).
comm.). Brazil, by contrast,has farms larger than 1000 ha and
%Global
Area
farmsaverageabout28 ha. Yet, for nearlyall countries,the small
Cacao Area
(000s ha)
Country
end of the farm-size spectrumdominatesthe cacao landscape.
32.7
2150
C6te d'lvoire
In general, small- to medium-sized farms are both more pro18.25
1200
Ghana
ductive (pods per ha) and more efficient (pods per dollar input)
688
10.47
Brazil
6.54
430
Nigeria
than largercorporateholdings (28). Moreover, small producers
360
5.48
Cameroon
accomplishthis despitegovernmentpolicies favoringlargerplan5.32
350
Ecuador
332
5.05
Indonesia
tationsdatingback to colonial times in Asian and Africancoun3.12
205
Malaysia
2.08
137
DominicanRepublic
tries (29). Governmentsin Java and East Sumatra,for instance,
124
1.89
Colombia
delivered the tripodof production-land, labor, and capital-to
91
1.38
Mexico
88
1.34
PapuaNew Guinea
large producersin efforts to keep estate productioncosts com65.
0.99
Venezuela
petitive. Exportregulationsin Cameroonfavoredlarge holdings.
60
0.91
Guinea
Equatorial
0.55
36
Peru
And in the Dutch East Indies, state authoritiesaccused small0.38
25
Togo
holdersof spreadingdreadedpests into estateproperties,a charge
0.37
24
Sao Tome
0.3
20
Costa Rica
thatresultedin the uprootingof small producers'tree stock. Suit0.25
16.6
Philippines
0.16
10.5
able cacao lands were monopolized by largerholdings in EcuaUganda
0.07
4.6
Guatemala
dor in the late 19th century. Even so, small producersaround
0.06
4
Panama
0.03
2.1
Honduras
the worldhave remainedcompetitivedespite the institutionalob0.02
1.5
Nicaragua
stacles placed before them. Large-scale plantersgenerally paid
0.01
0.4
El Salvador
2.27
149.2
Others
more for their land, used more expensive labor, and had higher
fixed and working capital costs comparedto their smallholder
Note :Totalworldarea harvestedin 1996 was 6574000 ha; not all
producingcountriesshown in chart.
brethren(29).
The tendency to favor plantationproductionover smallhold-
ceptable habitat for animals dispersing between small forest
patches.Shade cacao is being promotedas a corridorforest and
buffer zone crop in the Talamancanmountainregion in Costa
Rica (13). Other areas have been identified where cacao could
be used in restorationefforts, as well, in particularas part of a
reforestationaims in Vietnam.
In summary,a greaterdiversity of tropical forest organisms
occurs in shaded cacao plantationsthan in most other lowland
tropical agriculturalsystems. Rustic plantations incorporating
naturalforest shade trees are probably the best in this regard.
However, to the degree that these rustic systems are not stable,
they may not provide habitatin the long term. Cacao grown under plantedshade may provide the best long-termprotectionfor
some tropicalforestbiodiversity.Systems thatincorporatea high
diversityof trees with animaldispersedand pollinatedfruitsand
flowers, along with retainingepiphytes, lianas, and mistletoes,
will supportthe greatest diversity. Research on the ecological
and agronomiccharacteristicsof trees, as well as an evaluation
of theireconomicvalue, may help establisharraysof species that,
when used, will optimize the economic value of farms and
biodiversityconservation.Cacao grown closer to forest supports
a greaterbiodiversity-perhaps forminga bufferhabitatfor mobile organisms.Cacao farms could be concentratedin the buffer
zone of existingreservesor used to form corridorsbetween small
forest reserves.
Ambio Vol. 29 No. 3, May 2000
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169
ings, as well as Europeanplantersover local residents, derives
largely from unquestionedbelief by people in governmentagricultural institutions in western "scientific" growing practices
(29). Part of this belief system has held-even until the 1980s
in the case of Malaysia-that advantages from economies of
scale could be obtained with larger productionunits. Malaysia
provides a textbook case of plantationproduction.With at least
85% of its productioncoming from holdings larger than 40 ha
(30) upon which high levels of costly agrochemicalsare applied,
we should expect some ecological and social consequencesnow
commonly attributedto monoculturalsystems (31-33).
The Malaysianproblemsinvolve high productioncosts (labor,
agrochemicals,etc.), the aging of the tree stock, and shortages
of labor(34, 35). Regularlyscheduledsprayings,whetherneeded
or not, increase production costs. The
cost of labor has also climbed as the
work force opts for higher industrial
Table2. Structureof the cacao sector InCameroon,Ghana,and Brazil,showing numberof
farmsand hectareaccordingto size category of holding.
wages. Furthermore, prices have
dropped in the 1990s and other crops
Cameroon
Ghana
Brazil
have
shown better relative returns;esSize category
Farms
ha
Farms
ha
Farms
Hectares
pecially oil palm.
<0.1
14 200
600
In general, small producers tend to
0.1-0.5
92 300
22 100
have lower per unit production costs.
0.6-1.0
57 700
43 700
<1.0
(164 200)?
(66 400)?
119 850
98 963
Peasantsdepend upon and benefit from
1.1-2.0
65 500
95 000
87 529
159 258
family laborworkinglong hoursand re2.1-3.0
24 100
57 800
2.1-4.0
84 535
276 532
ceiving scant pay. But there are other
3.1-5.0
14 400
54 900
reasons for the greater efficiency of
4.1-8.0
40 330
258 694
<5.0
401
1350
small growers. Smaller farmersare po>5.1
8200
75 700
5.0-10.0
1031
5674
sitioned to have an intimateknowledge
8.1-20.0
13 323
182 398
of theirplots. This knowledge and care10.0-20.0
2475
19 998
20.0-30.0
2386
25 261
ful tendingis ideal for a crop like cacao,
20.1-40.0
37 382
1175
a crop often characterizedby small plots
30.0-40.0
27 512
1848
40.1-100.0*
258
190 062
5030
129 711
of
1000 to 3000 cacao trees. As one
100.1-200.0
2043
107 979
200.1-400.0
Malaysian cacao research manager
962
81 777
400.1-1000.0
482
62 020
stated, "Cocoa is like horticulture:the
>1000.1
122
23 738
planter must almost know each tree"
Total
276 400
349 800
347 000
1 203 280
16780
485 380
(30). This small-scale approachcan reNotes: ? Thissize categoryforCameroonis the sum of all smallerones; this intermediatesum has of
in incrediblyhigh yields. For examsult
course not been added to the total.* this size categoryis ">40"forGhana;also size categoryrelatesto
ple, smallholdersin Sulawesi obtain up
totalfarmarea whereas "hectares"for Brazilreferonlyto cacao area cultivated.
Source: RecensementAgricole 1984 Republicdu CamerounMinisterede L'Agriculture
Volume1
to 2000 kg ha-' of marketable beans;
(Cameroon);Cocoa Services Division unpubi.data obtainedfromDr.BeatricePadi (Ghana);CEPLAC
figures rarely achieved by commercial
data providedby Dr.KeithAlger(Brazil).
estates (28).
Individual pioneering farmers have
often been responsible for the new expansions of much of the world's cacao area. Whenever prices
Table 3. The geography of the global cacao cycle.
increase,and sometimeseven when they do not, pioneeringpeasCountry
Stage in
Comments
ant producersturnto cacao as a survivalstrategy.With low barcacao cycle
riers to entry and the crop's ability to produce something with
C6te d'lvoire middle*
littlelandavailableforexpansion;about
relativelylittle strenuouslabor,it has been classified as an "easy
20%of tree stock >30 yrs old;labor
crop" (28). In forested areas, producersbenefit from untapped
difficultiesfewer, now thatworkersare
comingin fromneighboringcountries;
soil fertility-augmented by the burning of aboveground
low incidenceof pest and disease; 66%
of cacao unshaded
biomass-and the lack of weeds. From the standpointof a small
Ghana
some landavailablein southwest;neariy
late*
grower, it is more attractiveand profitableto go into a forested
halfof tree stock >30 yrs old;labor
limitedbutfunctional;considerable
area,clear the forest for new planting,and producethereinthan
losses fromdisease and pests; most of
to replantareasalreadydevoted to cacao. The fundamentalforce
the cacao area is managedwithshade
behind this attractionresides in differentialyields and labordeNigeria
late
littlelandforexpansion;60%of tree
mands. A newly cleared forested area produces, at least for the
stock >30 yrs old;no laborshortage;
severe problemswithBlackPod, which
first few years, 15%to 25% higher yields than a replantedarea
reduces productionup to 70%
Cameroon
late
average landarea availablefor
(Matlick, pers. comm.). Moreover, the labor involved in clearexpansion;neariyhalfof tree stock >30
ing
primary forest for cacao versus replanting is nearly half.
yrs old;acute laborshortages except in
newest productionareas; high incidence
Ruf (36) found in Cote d'Ivoire that forest clearing and prepaof disease and pests
rationrequired86 days ha-' of labor, comparedto 168 days unMalaysia
middleto late littleto no landleftforexpansion;tree
stock quiteyoung;laborshortageon
der a replantingregime.
peninsula
Indonesia
Brazil
early
late
considerablelandavailablefor
expansion;veryyoungtree stock;plenty
of labor,except on Sulawesi,where
access to workershas become difficult;
potentialfutureproblemswithCacao
Pod Borer
virtuallyno landavailableforexpansion;
50%of tree stock >30 yrs old;labor
supplygood now, but mobileand able to
seek higherwages in othersectorspossible long-termshortages;severe
disease problemswithWitches'Broom
Sources: Ruf,(3);Taylor,(35);John Lunde,pers.comm.
pendingliberalization
schemes aimedat reducing/eliminating
govemment
pricecontrolscould bringhigherpricesto growers,thus reinvigorating
the
cacao sector forsome period.
170
CACAOCYCLES
As in any agriculturalcommodity, cocoa suffers periodically
from the crisis of overproduction.These wavelike variationslead
to global price fluctuations.Cyclical fluctuationsin the international price translate,in turn,into boom/bustcycles at the level
of production.When prices are high, one or more production
zones boom onto the global scene. As supply creeps up, prices
fall. Simply stated, prices follow a supply and demand model,
whether real or perceived. However, as with other major commodity pricing,the variablesfeaturedin the complex price equation all relatein some way to futuresupply, and include weather
?DRoyal Swedish Academy of Sciences 2000
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Ambio Vol. 29 No. 3, May 2000
and yield forecasts, changing consumptionhabits, social conditions in producingcountries,disease and pest problems,and institutionalinterventions.Historical data on cocoa show a pricing cycle of about 25 years (36). The development of genetic
stock that can toleratemarginalconditions, in conjunctionwith
policies that have allowed for their disseminationwith human
migration,are also factors favoring boom/bust cycles in cacao
(6).
Focusing on the behaviorof small cacao producers,Ruf and
Zadi (6) present a profile of the regional progressionof cacao
systems. Placementwithin the model depends not merely upon
how long cacao has been associatedwith a region, but also upon
the managementtechnology used, available labor, and exploitable forest regions (Table 3).
Regions newly opened to cacao show boom periods, during
which the harvestedarea,the numberof producers,and exports,
all increase as prices remain relatively high. Over a period of
15 to 20 years or more, the aging process of the cacao holdings
proceeds, characterizedby falling yields that can be linked to
increasingdisease and pest problems,and decreasingsoil fertility. Ecological changes are accompaniedby shifts in humandemography:migrationof landless people slows; emigrationmay
begin; the farmpopulationages (36).
Establishinga cacao farm involves the use of shade trees to
help form an erect habit and provide a windbreakfor young cacao trees (5). As the cacao matures,shade is often removed or
reduced; shade reduction leads to increased short-termyields,
but yields may decline dramaticallyunless chemical fertilizers
are applied (37). The "zero-shade"system is a recurrenttemptation, capturingthe imagination and hopes of small growers,
extension agents, and policymakers.The final stage of the cocoa cycle often finds growers replanting shade to create an
agroforestrysystem. Diversificationis a response to the falling
cocoa yields and diminished income brought on by continued
shadeless conditions. At this stage of the cocoa cycle, farmers
may shift entirely to the productionof anothercommodity crop
(see ref. 21 for discussion of shifts between cacao and banana
productionin CentralAmerica).
Because of predictablychanging ecological and social conditions, regionalcacao productionis often unstable,moving to agriculturalfrontiers, areas of primarytropical forest. Although
cacao zones of long-termstabilitydo occur (Trinidad,Ecuador),
the overall patternof instability and the search for new lands
predominatesand needs to be addressed. First, the continued
clearing of agriculturalfrontiersis a threatto biodiversityconservation. Second, concentrationof activity at particularfrontier regions makes the global cacao crop vulnerableto the invasion of new diseases or pests. And third, there are few forest
frontierregions left in the world.
litter from trees provides mulch and a supply of organic matter
for the soil. This, in turn,can increase aeration,infiltration,and
drainage,as well as result in a slow and steady release of nutrients into the mineralsoil. The decaying litterprovidesresources
for a greaterdiversity of soil and litter organisms, which may
be critical in nutrientbreakdownand cycling (41). In particular, fungal symbionts such as vesicular-arbuscularmycorrhizae
play a key role in the nutrientbudget of moist forest understory
plants (42) and cacao has long been known to harborsuch fungi
(43). Dependingupon the species involved, shade trees can also
fix atmosphericnitrogenand hold it within the soil layer. However, any shade tree can potentiallycompete with the cacao for
nutrients,and wood or fruit productsremoved from the shade
component representnutrientsleaving the agroforestrysystem
(38).
Young cacao plantsbenefit from the protectionof shadetrees
and the influence shade has on growth form. One study has
shown that shade also promotesgreaterlong-termproductionof
older cacao plants with low levels of fertilization (37). Shade
trees also serve to lessen the winds at or neargroundlevel within
the cacao agroforestrysystem.Perhapsmoreimportantis the protection shade trees can provide from windbornespores of fungal diseases. We have long known that shade reducesthe spread
of coffee leaf rust (Hemileia vastatrix)spores within plots (44).
Evans (45) demonstratedthe benefitsof shadeanddisease spread
in cacao, at least in the cases of Witches Broom (Crinipellis
perniciosa) and Frosty Pod Rot (Moniliophthoraroreri). Much
more work is needed to untanglethe relationshipbetween shade
and disease control.
Economic Value of Shade Trees
In agroforestrysystems, additionalplant species mixed with the
targetcrops can provide an arrayof valuableproducts(46-48).
In COted'Ivoire, cacao producersmake use of some 27 mostly
wild forest species as shade, 13 of which (48%) provide
fuelwood and medicine, 11 of which (41%)offer food products,
and 6 of which (22%) are used in construction(49). Researchers (50) showed that low-inputcacao systems that include commercialfruit productionfare quite well duringtimes of low cocoa prices.The break-evencocoa price for these virtuallychemical-free holdings is just over 50% of the price needed to break
even in cacao withoutfruittrees.
Shade trees themselves may also be valuable as timber (38,
51, 52). These trees have low maintenancecosts (41). Trials in
coffee show that laurel (Cordia alliadora), plantedat a density
of 100 trees ha-', yields up to 6 m3 ha-' yr-1.Earningsfrom timber could compensate for lost coffee yields of 17% when coffee prices are high, of 33% when prices are intermediate,and
up to 100% of any lost productionwhen prices are low; likewise, we assume similarearningscould apply to cocoa.
BENEFITSOF
ENVIRONMENTAL
Carbonsequestrationis a poorly assessed potential value of
SHADEDSYSTEMS
shadetrees, althoughNewmark(53) has been exploringthe posThe impact of cacao cultivation on biodiversity will be mini- sibility of using emissions tradingto providesmall farmerswith
mized if productionis focused on already cleared lands, if ex- additionaleconomic incentives for shade tree establishmentand
isting cacao farms show greaterlong-term stability, and if the protection. Some work (15) found mature (40-year-old) cacao
farmsthemselvessupportgreaterlevels of biodiversity.Improved agroforestrysystems in Cameroonto be fixing carbonat around
shade managementcan addressall three of these problems.The 154 tonnesha-';cacao systems in place for 15 and 25 years show
greatestlong-termincentives for promotingthe managementof averagecarbonamountsof 111 and 132 tonnes,respectively.Ala diverse shade canopy can be found in the ecological and ag- though these sequestrationvalues are less than for primaryforronomic services providedby the shade itself (38). Many of the est (307 tonnes ha-'), they are generally greaterthan for annual
long-termeconomic advantagesof shade alreadyexist and need crops. Based on fallow periods of 7 year and < 3 years. 106 and
greaterrecognition. Some of the potential value to be obtained 87 tonnes ha-' of carbon,respectively,are sequestered.
from shade will requireresearchfocused on shade management
The Role of Shade in Pest and Disease Control
sections.
Agrochemicalsarecommonlyused to controlpests, diseases,and
Shade Trees, Soil Protection, and Crop Health
weeds, in cacao holdings (32). In additionto the health and enShade trees provide protectionfrom the physical impact of pre- vironmentalproblems this may engender, the chemicals themcipitation and hence can reduce soil erosion (39-41). The leaf selves often induce resistance in target species. Capsids
Ambio Vol. 29 No. 3, May 2000
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171
(Miridae),small plant-suckinginsects thatattackcacao pods and
are the vectors of viral disease, developed resistance to aldrin
and lindanein the early 1960s in Ghana.Severalauthoritieshave
suggested thatthe removal of shade and the sprayingof insecticides are two major contributingfactors in the developmentof
pest species in cacao (5, 7).
The use of shade can lessen a farmer'sdependenceon chemicals. Shade usually inhibitsweed growth(38), and has also been
shown to help control outbreaksof at least one of the important
fungal diseases (Witches' Broom, Crinipellisperniciosa). In addition, shade reduces the activity of capsids (54,55). Shade is
thoughtto affect the physiology of the cacao plantand the physical environmentas well, which affects disease and pest organisms. MacVean (56) has suggested that natural predators of
nematodes, which damage plant roots, are dependentupon leaf
litter createdprimarilyby shade trees in coffee farms. The role
that mycorrhizaland endophyticfungi might play in conferring
disease resistance is an active and promising area of research
(Herre,pers. comm.).
A central hypothesis in need of much more investigation is
that organismsare less likely to reach pest or epidemic proportions in the presence of more complex predatorassemblages.
Such research is related to the "enemies hypothesis" (57-59),
which posits thatincreasedvegetationaldiversityof polycultures
supportsa relatively greaterabundanceand diversity of predators and parasitesof herbivorousinsects. This explains why herbivore populationsare often lower in the same species of plant
grown in a polyculturethan in a monoculture.Ratherthan manipulatespecific predator-preyrelationships,as some have done
(60), manipulationof the cacao habitatin orderto retainthe coevolved ecological relationshipscharacteristicof naturalforest
should be the first approachto be taken to prevent disease or
pest problems.
Much more research is needed to address the role of an increasingly diverse predatorycommunityassociated with shade.
Trophicrelationshipsare often complex. Ants, for instance, are
the most abundantarthropodpredatorsin many cacao farmsand
the dominantant species can be importantpredators.But they
also defendhomopterans,e.g. mealybugs,which themselvescan
be pest species. Furthermore,in discussing the role of increased
biological diversity in controlling pest and potential pest
populations,it shouldbe noted thatbufferhabitatsmay also provide resourcesfor pests themselves. In particular,mammalsand
birds, e.g. squirrelsand woodpeckershave been noted to damage cacao pods (61).
SHORT-TERMINCENTIVES
Many of the ecological services providedby shade management
play out over time, yet the decisions must be consideredin light
of short-termprofits for farmers.If there is a short-termcost of
reduced productionassociated with shade management,it may
need to be addressedby additionalmarketand institutionalincentives.
Market Incentives
Recent yearshave seen the developmentof the shadecoffee concept, followed by a numberof efforts to bring such a productto
the market.The goal has been both to rewardproducersthrough
a premium and provide consumers with a product with highly
verifiable standards.Conceivably, a similar programcould be
established for cocoa producers.Among the myriad issues are
who pays for and what institutionsadministerthe certification
program,of course, how large can the marketpremiumbe and
who realizes the increase?
Because no shade certificationfor cacao currentlyexists, and
since the organic standardsfor cacao include a shade component (62), certified organic ("ecological" in Europe) cocoa is
probablythe best surrogatefor marketableshade cacao. Organic
172
certification confers an added value to the product. However,
certifiedorganiccocoa productionis in its infancy and currently
representsa minusculefractionof total world productionof cocoa. Estimates now put total certified organic area at 8000 ha
worldwide,coming mostly from LatinAmerica.Its marketshare
within the United States is less than 1% (USD 15.4 million out
of USD 13 billion in the US). In Europe,organic cocoa weighs
in with about USD 18.2 mill. in sales (Daniels, pers. comm.).
Still, as in the case of coffee, organic cacao is growing rapidly.
Between 1990 and 1996, organicfoods in generalgrew by 20%
a year (63). The organicchocolatemarketgrew by 36% in 1996/
97, with companies like the Organic Commodities Project reporting a doubling in sales within the first six months of 1998
(Daniels, pers. comm.).
Other Financial Incentives
Given thatno developedconsumerdemandnow exists for shade
cocoa, the emergence of a price premiumin the near future is
doubtful. But there are other ways to encourage shade grown
cocoa. Growersproducingcocoa on farmswith shadethatmeets
specific criteria related to biodiversity could receive higher
prices, inexpensive credit, and relevant extension services
through nationally or internationallymanaged environmental
funds. In addition,a tax on agrochemicalscould act as a disinReferences and Notes
1. Greenberg,R., Bichier, P. and Sterling,J. 1997. Bird populationsin rustic and planted
shade coffee plantationsof easternChiapas,Mexico. Biotropica29, 501-514.
2. Perfecto, I. Rice, R.A., Greenberg,R. and van der Voort, M. 1996. Shade coffee as a
refuge for biodiversity.BioScience 46, 598-608.
3. Rice, R.A. and Ward, J. 1996. Coffee, Conservationand Commercein the Western
Hemisphere.SmithsonianMigratoryBird Center/NaturalResourcesDefense Council:
Washington,DC.
4. Moguel, P. and Toledo, V. 1999. Biodiversity conservationin traditionalcoffee systems of Mexico. Conserv.Biol. 13, 1-12.
5. Wood, G.A.R. and Lass, R.A. 1985. Cocoa. Longman,New York.
6. Ruf, F. and Zadi, H. 1998. Cocoa: From Deforestation to Reforestation.Paper presented at the FirstSustainableWorkshopon SustainableCocoa Growing,PanamaCity,
Panama,March30-April 2, 1998.
7. Leston, D. 1970. Entomologyof the cocoa farm.Ann. Rev. Entomol. 15, 273-294.
8. Room, P.M. 1971. The relative abundanceof ant species in Ghana's cocoa farms. J.
Anim.Ecol. 40, 735-751.
9. Estrada,A., Coates-Estrada,R. and Merritt,Jr.,D. 1993. Bat species richnessand abundance in tropical rain forest fragments and in agriculturalhabitats at Las Tuxtlas,
Mexico. Ecography 16, 309-318.
10. Estrada,A., Coates-Estrada,R. and Merritt,Jr.,D. 1994. Non flying mammalsand landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico. Ecography
17, 229-241.
11. Estrada,A., Coates-Estrada,R. and Merritt, Jr.,D. 1997. Anthropogenic landscape
changes and avian diversity at Los Tuxtlas, Mexico. Biodiv. Conserv.6, 19-43.
12. Estrada,A., Coates-Estrada,R.. MerittJr.,D., Montiel, S. and Curiel,D. 1993. Pattern
of frugivorespecies richness and abundancein forest islands and in agriculturalhabitats at Los Tuxtias, Mexico. In: Fleming, T.H. and Estrada,A. (eds): Frugivores and
Seed Dispersal: Ecological and Evolutionarv Aspects. Kluwer Academic Publ.
Dordrecht,The Netherlands,pp. 245-257.
13. Parrish,J., Reitsma,R. and Greenberg,R. 1998. Cacao as Cropand ConservationTool:
Lessonsfrom the TalamancaRegion of Costa Rica. Paperpresentedat the First SustainableWorkshopon SustainableCocoa Growing,PanamaCity, Panama,March30April 2, 1998.
14. Power, A. and Flecker, A.S. 1998. Agroecosystemsand biodiversity.Paperpresented
at the First Sustainable Workshop on Sustainable Cocoa Growing, Panama City,
Panama,March30-April 2, 1998.
15. Gockowski, J., Nkamleu, B. and Wendt, J. 1998. Implicationsof Resource Use Intensificationfor the Environmentand Sustainable TechnologySystemsin the CentralAfrican Rainforest. InternationalInstitute of Tropical Agriculture-Humid Forest Station, Yaound6,Cameroon.
16. Larison,B. and Smith, T.B. 1996. A Surveyof Montaneand LowlandBirdsfrom Three
Sites on the Island of Bioko, Equatorial Guinea. Reportto the governmentof Equatorial Guinea.
17. Room, P.M. 1975. Diversity and organizationof the groundforagingant faunasof forest, grasslandand tree crops in Papua,New Guinea.Aust. J. Zool. 23, 71-89.
18. Andrews, R.M. 1979. Evolution of life histories:A comparisonof Anolis lizardsfrom
matchedisland and mainlandhabitats.Brevoria454, 1-52.
19. Alves, M.C. 1990. The Role of Cocoa Plantations in the Conservationof the Atlantic
Forests of SouthernBahia, Brazil. M.S. Thesis. Univ. of Florida.Gainseville, Florida,
USA.
20. Room, P.M. 1972. The constitutionand naturalhistory of the fauna of the mistletoe
Tapinathusbangwensis (Eng. and Krause)growing on cocoa in Ghana.J. Anim.Ecol.
41, 519-535.
21. Young, A. 1994. The Chocolate Tree. SmithsonianInstitutionPress, Washington,DC,
USA.
22. Majer,J.D. 1993. Comparisonof the arborealant mosaic in Ghana,Brazil, PapuaNew
Guineaand Australia-its structureand influenceon arthropoddiversity.In: Hymenoptera and Biodiversity.LaSalle, J. and Gould, I. (eds). CAB International,Wallingford,
England,pp. 115-141.
23. Greenberg,R., Bichier, P. and Cruz, A. 2000. The impact of bird insectivory on herbivorous arthropodsand leaf damage in some Guatemalancoffee plantations.Animnal
Conserv.(in press).
24. Pacheco, J.F., Whitney, B.M. and Gonzaga. L.P. 1996. A new genus and species of
furnariid(Aves: Furnariidae)from the cocoa-growing region of southeasternBahia,
Brazil. WilsonBull. 108, 397-606.
25. WorldTradeOrganization,1995. World Cocoa Production
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Ambio Vol. 29 No. 3, May 2000
centive toward habitatcontaminationand alleviate worker exposure to toxic chemicals. The taxes, in turn,could go into the
aforementionedenvironmentalfunds that reward growers for
land stewardshipmeeting biodiversity criteria.Finally, the cocoa industryitself could invest more of its researchand development funds to supportsustainablecacao initiatives as a way
of ensuringstable supplies long into the future(64).
versity and act as a more effective refuge for some tropicalforest organisms than alternativelowland tropical crops, particularly annualcrops and cattle pasture.Therefore,the approachto
improvingthe role thatcacao cultivationhas in biodiversityconservationshould be two-pronged.First, in each cacao-growing
region, programsshould be establishedto replantabandonedor
failing cacao holdings using diverse shadethatis useful to farmers and supportswildlife, as well as to protectremainingforest
lands. Second, in regions of new cacao production,farmsshould
CONCLUSIONS
be establishedon alreadydeforestedlands so that cacao would
Cacao cultivation has a complex effect on global biodiversity. provide a mode of reforestation,and particularefforts shouldbe
Because of continued increasing demands for chocolate, the made to incorporatecacao as a buffer zone crop for established
amount of cacao produced has doubled and the area of cacao forest reserves and parks.
If traditionalcacao is to be actively promotedratherthanconcultivationincreasedover 2.5 mill. ha in the past 25 years.Much
of the expansion of cacao productionhas taken place in areas tinuing to be simply the result of laissez-faire neglect, then a
of primaryforest in West Africa and on Borneo and Sulawesi. majorresearchand extension effort is required.A comprehenEven if demand for cacao were constant, cultivation for cacao sive programneeds to be establishedthat will increasethe longwould continue to involve the clearing of new lands because of term productionof small shade-grownfarms in a mannerthat
the dynamic cacao cycles describedearlierin this paper.Cacao protectsbiodiversityand addressesthe needs of small-scale cais one of many crops that form the first step in a naturalpro- cao farmers(65). To ensureadequateand sustainedfunding,such
a programmust receive backing from the diverse stakeholders
gression from forest to agriculturaland degradedlandscapes.
However, cacao cultivation plays a relatively small role in with interestsin cocoa, producergroups,traders,manufacturers,
cacao farms etc., as well as from institutions concerned about global biotropicaldeforestationon a global scale. Furthermore,
with diverse shade have the potentialto supportgreaterlocal di- diversity,ruralcommunities,and sustainableagriculture.
26. FAO. Variousyears. AgricultureProduction Yearbook.United Nations Food and AgricultureOrganization,Rome, Italy.
27. Cacao area from FAO figures; deforestationfigures from Myers, N. 1991. Tropical
forests: presentstatusand futureoutlook ClimateChange 19, 3-32.
28. Ruf, F., Yoddang, J. and Ardhy, W. 1995. The spectacularefficiency of cocoa smallholders in Sulawesi: why? until when? In: Cocoa Cycles: The Economics of Cocoa
Supply.Ruf, F. and Siswoputranto,P.S. (eds). WoodheadPublishing,Ltd. Cambridge,
England,Ch. 17.
29. Clarence-Smith,W.G. 1997. Cocoa plantationsin the Third World, 1870s-1914: the
politicaleconomy of inefficiency.In: TheNew InstitutionalEconomicsand ThirdWorld
Development.Harris,J., Hunter,J. and Lewis, C. (eds). Routledge, London, pp. 157171.
30. Ruf, F. 1993. Comparisonof cocoa productioncosts in seven producingcountries:C6te
d'Ivoire, Ghana,Nigeria,Cameroon,Malaysia,Indonesia,Brazil. ThePlanter 69, 247262.
31. Buttel, F.H. 1990. Social relations and the growth of modern agriculture. In:
Agroecology. Carroll,C.R., Vandermeer,J.H. and Rosset, P.M. (eds). McGraw-Hill,
New York, USA, pp. 113-145.
32. Soule, J., Carre,D. and Jackson, W. 1990. Ecological impact of modem agriculture.
In: Agroecology. Carroll, C.R., Vandermeer,J.H. and Rosset, P.M. (eds). McGrawHill, New York, USA, pp. 165-188.
33. Pimentel, D. and Wen Dazhong 1990. Technological changes in energy use in U.S.
agriculturalproduction.In: Agroecology. Carroll,C.R., Vandermeer,J.H. and Rosset,
P.M. (eds). McGraw-Hill,New York, USA, pp.147-163.
34. Laird,S.A., Obialor,C. and Skinner,E.A. 1996. An IntroductoryHandbookto Cocoa
Certification:A Feasibility Studyand Regional Profile of WestAfrica. RainforestAlliance, New York.
35. Taylor, M. 1998. The WorldCocoa Situation.Paperpresentedat the IntemationalForum in Cocoa, Lima, Peru,28-29 October 1998.
36. Ruf, F. 1995. In: Cocoa Cycles: The Economics of Cocoa Supply. Ruf, F. and
Siswoputranto,P.S. (eds). WoodheadPublishing,Ltd., Cambridge,England,Ch. 1.
37. Ahenkorah,Y. Akrofi, G.S. and Adri, A.K. 1974. The end of the first cocoa shade and
manurialexperiment at the Cocoa Research Instituteof Ghana. J. Horticult. Sci. 49,
43-51.
38. Beer, J. 1987 Advantages, disadvantagesand desirable characteristicsof shade trees
for coffee, cacao and tea. AgroforestrySyst. 5, 3-13.
39. Gligo, N. 1986. Agriculturay Medio Ambienteen AmericaLatina. EDUCA, San Jos6,
Costa Rica. (in Spanish).
40. Rice, R.A. 1990. TransformingAgriculture:The Case of Coffee Leaf Rust and Coffee
Renovation in Southern Nicaragua. Doctoral Dissertation. University of Califomia:
Berkeley, CA, USA.
41. Beer, J., Muschler,R., Kass, D. and Somarriba,E. 1997. Shade managementin coffee
and cacao plantations.AgroforestrySyst. 38, 139-164.
42. Janos, D.P. 1980. Vesicular-arbuscularmycorrhizaeaffect lowland tropicalrain forest
plant growth.Ecology 61, 151-162.
43. Laycock, D.H. 1945. Preliminaryinvestigationsinto the functions of the endotrophic
mycorrhizaof Theobromacacao L. Trop.Agricult. (Trinidad)22, 77-80.
44. Ward,H.M. 1882. On the life-history of Hemileia vastatrix.J. LinneanSoc. London:
Botany 19, 299-335.
45. Evans, H.C. 1998. Disease and Sustainabilityin the Cocoa Agroecosystem.Paperpresented at the FirstSustainableWorkshopon SustainableCocoa Growing,PanamaCity,
Panama,March30-April 2, 1998.
46. Farrell,J.G. 1987. Agroforestrysystems. In: Agroecology: The Scientific Basis of AlternativeAgriculture.Altieri, M.A. (ed.). Westview Press, Boulder, Colorado, USA,
pp. 149-158.
47. Nair, P.K.R. 1990. Agroforestry:an approachto sustainableland use in the tropics.
In: Agroecology and Small Farn Development.Altieri, M.A. and Hecht, S.B. (eds).
CRC Press, Boca Raton, Florida,USA, pp. 121-136.
48. Belsky, J.M. 1993. Household food security, farm trees, and agroforestry:a comparative study in Indonesiaand the Philippines.Human Organiz.52, 130-141.
49. Herzog, F. 1994. Multipurposeshade trees in coffee and cocoa plantationsin C6te
d'Ivoire. AgroforestrySyst. 27, 259-267.
50. Duguma,B., Gockowski,J. and Bakala,J. 1998. Small Cocoa (Theobromacacao Linn.)
Cultivationin AgroforestrySystems of Westand CentralAfrica: Challenges and Opportunities. Paper presentedat the First SustainableWorkshopon SustainableCocoa
Growing. PanamaCity, Panama,March30-April 2, 1998.
Ambio Vol. 29 No. 3, May 2000
51. Heuveldop,J., Fassbender,H.W., Alpizar,L., Enriquez,G. and Fiulster,H. 1988. Modelling agroforestrysystems of cacao (Theobromacacao) with laurel(Cordiaalliodora)
and poro (Erythrinapoeppigiana) in Costa Rica. II: Cacao and wood production,litter
productionand decomposition.AgroforestrySyst. 6, 37-48.
52. Somarriba,E., Beer,J. andBonnemann,A. 1996.Arbolesleguminososy maderablescomo
sombraparacacao:el concepto.SerieTecnica.InformeT6cnicoNo. 274. SerieGeneracionv
Transferencia
de Tecnologka
No. 18.CATTE,
CostaRica.(InSpanish).
Turrialba,
53. Newmark,T. 1998.CarbonSequestration
and Cocoaproduction:FinancingSustainableDeWorkvelopment
byTradingCarbonEmissionCredits.PaperpresentedattheFirstSustainable
shopon SustainableCocoaGrowing,PanamaCity,Panama,March30-April2, 1998.
54. Gerrard,B.M. 1964. Insects associatedwith unshadedTheobromacacao. Ghana.Proc.
Conferenceon Mirids and OtherPests of Cocoa. West African Cocoa ResearchInstitute, Nigeria, pp. 101-1I11.
55. Padi, B. and Owusu, G.K. 1998. Towardsan IntegratedPest Managemenltfor Sustainable Cocoa Production in Ghana. Paperpresentedat the First SustainableWorkshop on SustainableCocoa Growing,PanamaCity, Panama,March30-April 2, 1998.
56. MacVean, C. 1992. Causas y naturalezadel mal de viniasenicafetos de Guatemala.
Institutode Investigaciones,Universidadde Guatemala,Guatemala.(In Spanish).
57. Root, R.B. 1973. Organizationof plant-arthropodassociations in simple and diverse
habitats:the faunaof collards (Brassica oleracea). Ecol. Monogr.43, 95-124.
58. Altieri, M.A. and Smith, L. 1986. The dynamicsof colonizing arthropodcommunities
at the interface of abandoned,organic and commercial apple orchardsand adjacent
woodlands.Agricult.Ecosyst. Environ.16, 29-43.
59. Russell, E.P. 1989. Enemies hypothesis: a review of the effect of vegetationaldiversity on predatoryinsects and parisitoids.Environ.Ecol. 18, 590-599.
60. Khoo, K.C. 1992. The influenceof Dolichoderusthoracicus(Hymenoptera:Formicidae)
on losses due to Helopeltistheivora(Heteroptera:
Miridae),blackpod disease,andmammalianpests of cocoa in Malaysia.Bull. Entom.Res. 82, 485-491.
61. Bhat, S.K., Nair, C.P.R. and Mathew, D.N. 1981. Mammalianpests of cocoa in South
India. TropicalPest Mgmt27, 297-302.
62. IFOAM 1996. Basic Standardsfor Organic Agricultureand Processing and Guidelinesfor Coffee,Cocoa and Tea. IntemationalFederationof OrganicAgriculturalMovements, Thorley-Theley,Germany(FRG).
63. Murphy,K. 1996. Organic food makersreap green yields of revenue. The New York
Times,October26, p. B 1.
64. Yoon, C.K. 1998. Chocoholics take note: beloved bean in peril. The New YorkTimes,
May 4, p. 1.
65. For a comprehensivelist of recommendationsfor such a program,see "The First Intemational Workshopon SustainableCocoa Growing",available in the "Cocoa Corner"of the SmithsonianMigratoryBird Center'swebsite at <www.si.edu/smbc>.
66. We thank the following people for providing us with information for this paper:
Stephanie Daniels, Development Coordinatorat the Organic Commodity Project in
Cambridge,MA.; Alan Herre,researcherat the SmithsonianTropicalResearchInstitute, PanamaCity, Panama;B.K. Matlick, consultantin cacao industry;FranqoisRuf,
researcherat CIRAD, stationedin Cote d'Ivoire;John Lunde, SustainableCocoa Specialist for Mars, Inc.; Ed Ng, CommercialStaff Officer for Mars, Inc. We also appreciate the financial supportprovided by Mars, Inc. during the researchand writing of
this paper, and the help of all participantsin the First SustainableWorkshopon SustainableCocoa Growing,PanamaCity, Panama,March30-April 2, 1998.
67. First submitted25 May 1999. Accepted for publicationafterrevision 13 Jan. 2000.
Robert A. Rice is a geographer and policy researcher at the
Smithsonian MigratoryBird Center (SMBC)in Washington,
DC, USA, where he studies land-use changes related to bird
habitat. E-mail:[email protected]
Russell Greenberg, Directorof SMBC,is an ecologist who
has conducted avian research in the USA, Russia, and
throughout LatinAmerica. E-mail:[email protected]
Their address: Smithsonian MigratoryBird Center, National
Zoological Park,Washington, DC-20008,USA
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