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https://doi.org/10.1038/s41893-018-0062-8

There are amendments to this paper

Climate-smart sustainable agriculture in low-to-

intermediate shade agroforests
W. J. Blaser 1
*, J. Oppong2, S. P. Hart 3
, J. Landolt1, E. Yeboah2 and J. Six1

Meeting demands for agricultural production while maintaining ecosystem services, mitigating and adapting to climate change
and conserving biodiversity will be a defining challenge of this century. Crop production in agroforests is being widely imple-
mented with the expectation that it can simultaneously meet each of these goals. But trade-offs are inherent to agroforestry
and so unless implemented with levels of canopy cover that optimize these trade-offs, this effort in climate-smart, sustainable
intensification may simply compromise both production and ecosystem services. By combining simultaneous measurements
of production, soil fertility, disease, climate variables, carbon storage and species diversity along a shade-tree cover gradient,
here we show that low-to-intermediate shade cocoa agroforests in West Africa do not compromise production, while creating
benefits for climate adaptation, climate mitigation and biodiversity. As shade-tree cover increases above approximately 30%,
agroforests become increasingly less likely to generate win–win scenarios. Our results demonstrate that agroforests cannot
simultaneously maximize production, climate and sustainability goals but might optimise the trade-off between these goals at
low-to-intermediate levels of cover.

H
ow agriculture is implemented will be one of the strongest
determinants of global human and environmental health
over the coming century, and the challenges are formidable.
Meeting food security needs for the world’s population requires
sustained production, which requires healthy soils, effective control
of pests and disease and adaptation to new climates1–3. Meanwhile,
given agriculture’s particular vulnerability to climate change4,5, and
an already vast global footprint2,6, best-practice agriculture should
mitigate against further, avoidable climate change, while also lim-
iting impacts on biodiversity and other ecosystem services. These
multi-dimensional requirements for the future of agriculture have
recently been summarized by two complementary concepts: sus-
tainable intensification and climate-smart agriculture2,6,7. However,
while the concepts and requirements for the future of agriculture
are clear, easily implemented integrative solutions are rare.
Agroforests—the deliberate inclusion of trees in cropping sys-
tems in some form of spatial arrangement or temporal sequence8—
are an ideal candidate for climate-smart, sustainable agricultural
intensification2,7,9. Agroforests are widely expected to buffer crops
from climate change, improve soil fertility and regulate pests and
pathogens10–15. Moreover, agroforests are believed to contribute
to climate-change mitigation through increased carbon seques-
tration9,16–18, while also maintaining diversity of associated spe-
cies13,19,20. However, although they are widely advocated, and are
currently being implemented across large parts of Africa, Asia and
South America, agroforests generate costs and many of their pre-
sumed benefits, while intuitive, are often untested. For example,
climate-change adaptation has been a major reason to encourage
agroforests but shade trees are likely to have multiple interacting
effects on different climate variables such as temperature and water
availability so that the net effects on crops under climate change
may not always be positive. Furthermore, shade trees reduce crop
production through competition21, and at the same time agrofor-
ests are unlikely to match the diversity and service provisioning of
primary forests20,22,23. Trade-offs are, therefore, inherent to agrofor-
estry. Unless agroforests are implemented in a way that optimizes
these trade-offs, this effort in climate-smart, sustainable intensifica-
tion may simply compromise our ability to meet production, cli-
mate, sustainability and conservation goals.
The contribution of agroforests to the future of agriculture there-
fore requires understanding the balance of their costs and benefits.
First, this requires simultaneous measurements of the multiple
effects of agroforests to identify the trade-offs inherent to their
implementation. And second, it requires understanding how the
costs and benefits accrue with changes in shade-tree cover so that
they can be implemented with shade levels that maximize benefits
while minimizing costs. Here, we quantify the effectiveness of cocoa
agroforests along gradients of shade-tree cover to determine if—and
at what levels of shade-tree cover—agroforests can be both climate-
smart and sustainable (Fig. 1). Over a period of 2 years, including
1 normal and 1 exceptionally dry year, we measured cocoa produc-
tion, losses to disease, soil fertility, temperature, relative humidity,
soil moisture, carbon stocks and biodiversity of multiple taxa in 20
cocoa agroforest plots selected systematically along a gradient of
shade-tree cover in a globally significant cocoa growing region in
Ghana, West Africa (see Methods for further details).
To isolate the effects of shade trees from confounding factors
such as differences in farm management, soil type and local micro-
climate, all plots were compared with paired monoculture plots on
the same farms (Methods). The shade-tree cover and the species
composition of cocoa agroforests often varies over the lifetime of
cocoa, with higher shade requirements in the establishment phase
(0–3 years), which can be provided by food crops in addition to
shade trees, and then a reduction or removal of shade as cocoa trees
mature13. In this context, our study focuses on the effects of shade
trees in mature cocoa farms (15–25 years since establishment) in
which shade levels are less likely to vary over time. We focused our
assessment on cocoa agroforests in Ghana because agriculture in this

Sustainable Agroecosystems Group, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland. 2Council for Scientific and Industrial
1

Research – Soil Research Institute, Kwadaso, Kumasi, Ghana. 3Institute of Integrative Biology, Department of Environmental Systems Science, ETH Zurich,
Zurich, Switzerland. *e-mail: wilma.blaser@usys.ethz.ch

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NAture SustAinABility
10% 30% 50% 70%
1. Agricultural production
Crop yields –3.6%
* iological models30, but are more optimistic than those models about
Soil fertility +0.1%
Pest control * +59%
2. Climate adaptation
Temperature * –0.1%
Water availability * –16%
3. Climate mitigation
Aboveground C * +70%
Soil C –0.8%
4. Biodiversity conservation * +91%
10 20 30 40 50 60 70
Canopy cover (%)
Fig. 1 | The simultaneous costs and benefits of agroforests on production,
climate adaptation, climate mitigation and biodiversity along a gradient
of shade-tree cover (10–80%). The four top panels give a schematic aerial
view of four representative plots along the gradient of increasing shade-
tree cover. Each bar in the lower panels shows the effect of shade trees
on a particular response variable, with blue indicating shade trees confer
a benefit, red indicating shade trees confer a cost and white indicating
no difference, relative to cocoa monocultures. The colour gradients are
quantitative, matching the predicted values for the percentage difference
in each response variable relative to monocultures, and scaled to the
ranges shown in Fig. 2. The actual predicted range over the gradient for
each variable is indicated with minimum and maximum predicted values of
percentage difference (%) at the ends of each bar. Predicted values were
based on significant regression lines (marked with a red asterisk) shown in
Fig. 2, for crop yields (mean annual cocoa yields 2015–2017), pest control
(mean annual total losses to disease 2015–2017), temperature (dry season
maximum temperature 2016), water availability (dry season soil moisture
2016), aboveground C (aboveground carbon stocks in tree biomass)
and biodiversity (bird richness). Predicted values for non-significant
relationships (soil fertility (total soil nitrogen stocks) and soil C (total soil
carbon stocks)) are averages across the shade-tree cover gradient.
region is critically vulnerable to each of the threats that agroforestry
promises to mitigate. For example, while global demand for cocoa
is increasing, current productivity in West Africa (which accounts
for more than 65% of global production) is declining because of
degraded soils and pathogens, and future production is threatened
by climate change24–26. At the same time, agricultural expansion has
led to extensive deforestation in this region, with little remaining
primary forest habitat27, which makes the biodiversity and carbon
storage potential of agroforests critically important.
Results and discussion
Can agricultural production be maintained in agroforests? Our
results suggest that shade trees are unlikely to compromise mean
annual production of cocoa up to levels of ~30% cover (Figs. 1
and 2a). This result provides a pathway to sustainable agricultural
intensification. As shade-tree cover increases beyond ~30%, cocoa
production declines (Fig. 2a, see also19,28,29). These declines can be
significant in magnitude, although shade trees may not necessar-
ily compromise production up to ~50% cover (95% confidence
interval at 50% cover: +​  1.2 to −​33.3). The decrease in yield as cover
increases is likely to occur as a consequence of competition for light
(Supplementary Fig. 1), water (Fig. 2g) and nutrients21,30, which is
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consistent with the smaller size of cocoa trees found under higher
levels of cover (Supplementary Table 1). Yields assessed per cocoa
tree gave similar results (Supplementary Table 1), indicating that
lower yields at higher shade-tree cover were not the effect of lower
planting densities of cocoa trees. Notably, our empirical results take
–73%
a similar functional form to predictions based on mechanistic phys-
+0.1%
the ability of cocoa to sustain yields in agroforests.
+32% It is commonly believed that the negative effects of shade trees on
short-term productivity will be partially offset by positive effects of
–2.4% shade trees on soil fertility13 and disease prevalence14,15, which would
–58% then enable the maintenance of production over longer periods of
time10,13. With respect to disease prevalence, our results support this
+530% contention but only at intermediate levels of cover (Figs. 1 and 2b).
–0.8% While in low- and high-shade agroforests cocoa suffered from dis-
ease more than in monocultures, at around 50% shade-tree cover the
+698% proportion of diseased pods and infestation of cocoa trees by para-
sitic plants (mistletoe) was reduced relative to monocultures (Fig. 2b,
80
Supplementary Table 2). Our results corroborate emerging evidence
that intermediate levels of shade may improve long-term production
by minimizing losses to disease14, although these benefits were insuf-
ficient to increase production to levels above monocultures in our
study (Fig. 2a). Our results, along with others14,28,31–33, do not support
the contention that agroforestry will facilitate long-term production
through increases in soil fertility, at least as currently implemented in
our study area. Shade trees did not increase soil carbon stocks (Fig. 2c)
or other soil fertility parameters, including total soil nitrogen (Fig. 2d)
and phosphorus, resin extractable phosphorus, exchangeable cations
(potassium, calcium, magnesium and sodium) and effective soil cat-
ion exchange capacity (Supplementary Table 3). Whether shade trees
can increase the productive lifetime of cocoa plantations by reduc-
ing premature aging compared to full-sun monocultures remains
to be studied. In sum, agroforests with approximately 30% cover
(and sometimes higher) can have similar production levels to cocoa
monocultures and can reduce pressure from pest and disease (Fig. 1).
Notably, these levels of cover are likely to be higher than is most
commonly implemented in this region34,35.
Do agroforests allow adaptation to climate change? The idea that
agroforests can buffer crops from the worst effects of climate change
is a major reason for their implementation in climate-vulnerable
agricultural sectors and regions11,12. In general, it is most important
for shade trees to buffer climate extremes during the dry season,
when cocoa is most vulnerable to high temperatures and drought
stress30. However, we found that agroforests had both positive and
negative effects on climate-related variables during the dry season.
Increasing shade-tree cover buffered cocoa against temperature
extremes by decreasing daily maximum and daily mean tempera-
tures in the dry season (Figs. 1 and 2e, and Supplementary Table 4).
However, while increasing shade-tree cover increased relative
humidity in the wet season (Supplementary Table 4), evidence that
trees could do so in the dry season was less convincing (Fig. 2f).
Moreover, increasing shade-tree cover also decreased soil moisture
during both the short and long dry seasons (Figs. 1 and 2g, and
Supplementary Table 4; see also36).
Taken together, our results suggest that the effectiveness of
agroforests for climate adaptation will depend on the nature of the
principal climate-related threats to production in a given area (high
temperatures and/or low water availability), and on how agrofor-
ests are implemented in relation to these threats. On the one hand,
a decrease in water availability with increasing shade-tree cover is
expected to exacerbate drought stress, which has long been consid-
ered a major climate-related threat to cocoa production in West Afr
ica24,25,36,37. However, rising temperatures may be an equally or more
important threat to cocoa in this region25,38, suggesting that future cli-
matic suitability for cocoa may depend on the temperature-buffering
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Agricultural production
a Yield b Losses to disease c Soil C d Soil N
100 100 100 100
2 2 2
R = 0.49** R = 0.40* R = 0.08 R 2 = 0.02

Difference relative to
Difference relative to

Difference relative to
Difference relative to

monoculture (%)

monoculture (%)
monoculture (%)
50 50 50 50
monoculture (%)

0 0 0 0

–50 –50 −50 −50

–100 –100 −100 −100

0 30 60 90 0 30 60 90 0 30 60 90 0 30 60 90
Shade-tree cover (%) Shade-tree cover (%) Shade-tree cover (%) Shade-tree cover (%)

Climate adaptation and mitigation

e Temperature f Humidity g Soil moisture h Aboveground C
5.0 2 10 2 100 2 1,000
R = 0.23* R = 0.05 R = 0.28° R 2 = 0.49***

Difference relative to
Difference relative to

Difference relative to
Difference relative to

750

monoculture (%)
monoculture (%)

monoculture (%)
monoculture (%)

2.5 5 50

500
0.0 0 0

250
−2.5 −5 −50
0
−5.0 −10 −100
0 30 60 90 0 30 60 90 0 30 60 90 0 30 60 90
Shade-tree cover (%) Shade-tree cover (%) Shade-tree cover (%) Shade-tree cover (%)

Biodiversity conservation
i Tree richness j Bird richness k Ant richness l Frog richness
1,200 2
1,000 2
100 100
R = 0.37** R = 0.47*
Difference relative to

Difference relative to
Difference relative to

Difference relative to

900 750
monoculture (%)

monoculture (%)
monoculture (%)

monoculture (%)

50 50

600 500
0 0

300 250
−50 −50
0 R 2 = 0.06 R 2 = 0.17
0
−100 −100
0 30 60 90 0 30 60 90 0 30 60 90 0 30 60 90
Shade tree cover (%) Shade tree cover (%) Shade tree cover (%) Shade tree cover (%)

Fig. 2 | The effects of agroforests on agricultural production, climate adaptation, climate mitigation and biodiversity along a gradient of shade-tree
cover. a, Mean annual cocoa production (period 2015–2017) was maintained at low-to-intermediate levels of shade, decreasing relative to monocultures
at levels above ~30% cover. b–d, Shade trees reduced the proportion of cocoa pods lost to disease (period 2015–2017) at medium cover (b) but did not
increase soil fertility (soil carbon (C) and soil nitrogen (N)) relative to monocultures (c,d). e–g, Shade trees buffered maximum air temperatures (e) and
minimum relative air humidity (f) but decreased soil moisture (g) during the long dry season (2016). h, Shade trees significantly increased aboveground
carbon stocks. i–l, The diversity of trees (i) and birds (j) increased with increasing shade-tree cover, but the diversity of ants (k) and frogs (l), while
significantly higher in agroforests than in monocultures, was not related to shade-tree cover. Plots show the percentage difference in each response
variable between agroforests and monocultures along a gradient of increasing shade-tree cover (10–80% cover), where positive values indicate higher
values in agroforests. Solid lines show significant relationships and broken lines indicate non-significant relationships with significance levels: °P =​ 0.06;
*P <​ 0.05; **P <​ 0.01; ***P <​0.001. The dotted horizontal line represents no difference between agroforest and monoculture plots. See Supplementary
Tables 1–5 for analyses, including analyses of additional response variables and in additional seasons.

effects of shade trees that we demonstrate. Importantly, benefits the heavily shaded agroforests represents only 34–39% of the carbon
of shade trees for temperature emerged at lower levels of shade- stored in semideciduous natural forests in Ghana39.
tree cover than did costs for soil moisture (Figs. 1 and 2e–g), It is also clear that the biggest potential for carbon sequestra-
providing a potentially important opportunity to optimize the tion in cocoa agroforests lies in aboveground biomass and not in
trade-offs between climate adaptation benefits and costs in agro- soils, where we found no increases in carbon stocks relative to
forestry systems. monocultures (Fig. 2c and Supplementary Table 4). Soil carbon
sequestration has recently been promoted as a major potential
Can agroforests mitigate future climate change? Increasing shade- climate-change mitigation strategy—especially in agroforestry
tree cover has strong positive effects on aboveground carbon seques- systems40. However, our results and others18,28,31,33 suggest that
tration (Figs. 1 and 2h and Supplementary Table 4). Low-shade in perennial cropping systems, such as cocoa and coffee, add-
( <​ 30%) cocoa agroforests had up to 210% more carbon stored in ing shade trees may not have the same potential for soil car-
aboveground standing biomass than paired monocultures, while bon sequestration as in annual cropping systems. This may be
some of the most heavily shaded plots had more than 660% more car- because the litter produced by shade trees in perennial crop-
bon (62.0 Mg C ha-1 versus 8.1 Mg C ha-1, Fig. 2h and Supplementary ping systems might not significantly increase carbon inputs to
Table 4). While the increase relative to monocultures is substantial, it levels above those of the perennial crops alone, as was the case
is also important to note that the aboveground stored carbon in even in our study (mean difference in litter between agroforests and

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NAture SustAinABility
monocultures −​8.8%, t-test: t =​  −​1.72, P =​  0.95; Supplementary
Methods and Supplementary Table 4).
Taken together, our results suggest that the net carbon sequestra-
tion potential of agroforests will depend strongly on land-use history
before their establishment. For example, the incorporation of shade
trees into annual or degraded systems will most likely result in a net
increase in below- and aboveground carbon stocks18,40,41, whereas
the establishment of new agroforests through the conversion of
natural forests will lead to net carbon losses from both aboveground
biomass (~75% loss) and soils (30–50% loss)22,32,40. Nevertheless, it is
clear that the potential for climate mitigation through aboveground
carbon storage in agroforests is a major advantage of agroforests
over monocultures, and is likely to be particularly important for cli-
mate mitigation in regions where limited primary forest remains16.
Moreover, the strong positive relationship between shade and car-
bon sequestration (Figs. 1 and 2h) suggests that conversion from
high-shade to low-shade agroforests will come at the cost of a sub-
stantial loss of carbon storage capacity, particularly in landscapes
such as those in large parts of West Africa where agroforests have
already replaced large areas of natural forest (see also16).
How effective are agroforests for the conservation of biodiver-
sity? We found that agroforests support higher levels of species
diversity than monocultures (Figs. 1 and 2i–l, and Supplementary
Table 5), a result that is consistent with findings from other cocoa
and oil palm agroforests42–44. However, one of the major questions
surrounding the effectiveness of agroforests is their ability to sup-
port biodiversity without compromising yields19. In this context,
our results suggest that, relative to monocultures, agroforests can
have large benefits for biodiversity that do not strongly compro-
mise yields up to a cover of ~30% (Fig. 1). Beyond these levels,
the positive relationship between shade-tree cover and bird and
tree diversity (Figs. 2i,j) combined with the negative relationship
between cover and yield (Fig. 2a) causes an increasingly strong
trade-off between diversity and yield as cover increases. This result
is contrary to recent studies of cocoa agroforests in Indonesia19, but
consistent with negative biodiversity–yield relationships in temper-
ate systems45,46. In contrast, ants and amphibians showed a posi-
tive effect of shade trees (t-test amphibians: t =​  2.27, P =​  0.02; ants:
t =​  3.7, P =​ 0.003) but no significant relationship with shade-tree
cover (Figs. 2k,l, and Supplementary Table 5), suggesting that in our
study these taxa benefit from the simple inclusion of shade trees,
irrespective of the level of shade-tree cover.
Are the benefits of agroforests for biodiversity worth the cost to
yields at higher levels of shade-tree cover, particularly given that bio-
diversity in cocoa agroforests is already strongly reduced compared
to natural forests? Studies in Ghana, Indonesia and Uganda that have
compared land-sharing practices, such as agroforestry, with land-spar-
ing strategies have found that more tree and bird species were con-
served under land-sparing approaches27,47. Our observations suggest a
similar pattern because we recorded no forest interior bird species in
any of our plots, regardless of the shade-tree cover, as well as relatively
low diversity of trees compared with intact forests. Nevertheless, the
conservation value of agroforests can be considerable and might be
one of few options for conserving biodiversity in human-dominated
landscapes that have little remaining primary habitat48.
Limitations and the potential to maximize agroforest perfor-
mance. To control for confounding factors, we compared mono-
cultures and agroforests on the same farm, which meant that the
size of our study plots was dictated by the approximate size at which
monocultures and agroforests are most commonly implemented in
the study area. One potential implication is that the performance
of these often relatively small monoculture and agroforest patches
may be affected by other nearby patches that may have higher
or lower levels of cover. For example, the diversity of associated
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species in monocultures may be increased by ‘spillover’ from nearby
agroforest patches49. Equally, the performance of agroforests may
be affected by conditions in nearby monocultures, and these effects
could also extend to some disease and climate adaptation variables.
Such effects would be expected to reduce the differences in perfor-
mance between monocultures and agroforests in our study, suggest-
ing our conclusions are likely to be conservative.
While we chose farms that were representative of how agrofor-
ests are most commonly managed in the study region, the extent to
which our results apply to other regions, or to farms that are better
maintained will, at least partly, depend on local conditions. Yields in
our study system were relatively low (mean 551.2 ±​ 25.8 kg ha-1) as
is typical across large parts of West Africa26,35, and improvements in
farm management have been shown to improve yields independent
of shade-tree cover in agroforests elsewhere19. This may suggest that
yields could be improved further in low-input systems such as those
that we studied, while maintaining many of the benefits of agro-
forests that we document. Focussing these management efforts in
agroforests with higher cover (30–50%)—which our data suggests
may still have the potential for yields similar to monocultures in
some farms (Fig. 2a)—would lead to much higher realized benefits
of agroforests for climate (Fig. 2h) and biodiversity (Figs. 2i,j)17,19.
While there were no clear patterns in the distribution of par-
ticular shade-tree species in our plots (Supplementary Fig. 2 and
Supplementary Table 6), there may also be potential to improve the
effectiveness of agroforests through careful (rather than ad hoc)
selection of shade trees with particular functional traits. Soil fertility
benefits, for example, may be more likely to arise with the deliberate
inclusion of nitrogen-fixing species, and deep-rooting trees might
limit competition for water10,13. The overall economic performance of
agroforests can also be improved (beyond benefits to the yield of the
primary crop) by including species that can be harvested for timber,
fruit or other products, something not explicitly considered in our
study (but see Supplementary Table 6). Finally, because shade trees
differ in their crown architecture and size, optimal levels of cover can
either be achieved with a high density of small shade trees or a low
density of large shade trees50 (see Supplementary Fig. 3 for details).
Including tall trees that offer small amounts of shade relative to their
size, for example, could potentially increase biodiversity and carbon
storage relative to monocultures, while also maximizing yields16,17,19.
Agroforestry and the future of climate-smart sustainable agri-
culture. Our study suggests that agroforests have large potential—
across a wide range of production, climate, ecosystem services
and diversity metrics—as a strategy for climate-smart, sustainable
agriculture. Nevertheless, shade levels are critical such that ad hoc
inclusion of trees in cropping systems is likely to generate subopti-
mal outcomes without careful consideration of which production,
climate and sustainability goals will be compromised. While agri-
cultural production is highest in monocultures and agroforests up
to 30% shade-tree cover, the provision of regulating ecosystem ser-
vices and the value for biodiversity conservation is maximized in
heavily shaded systems (Fig. 1). Moreover, the inclusion of shade
trees has conflicting effects on the ability of cocoa production to
adapt to climate change, suggesting trees need to be included at lev-
els that minimize costs by addressing the most important climate-
related threats. Despite these difficulties, our results suggest that
cocoa agroforests up to 30% cover are far superior to monocultures
because they do not strongly compromise production, while at the
same time they provide benefits for disease management, climate
mitigation and adaptation and biodiversity conservation (Fig. 1).
Methods
Study area and sampling design. We did our study in the moist semideciduous
tropical zone of the Ashanti Region in Ghana, West Africa (06°40’ N and 01°57’ W).
Closed semideciduous tropical forest in this region has been replaced by a mosaic
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of rotational fallows, slash-and-burn agricultural systems and perennial cropping
systems. Cocoa is the dominant perennial crop in this region and is grown
under variable shade-tree cover, including full-sun monocultures. Mean annual
precipitation in the study area ranges between 1,700 and 1,850 mm and occurs
across two separate wet seasons (March to mid-July and September to October).
The months between the rains are marked by a short dry season in August and a
long dry season from December to February. Variation in the yield of cocoa trees is
affected more by rainfall than by any other climate variable30. The first year of this
study was exceptionally dry, with only 30 mm of rain during the two driest months
(January and February 2016) compared to an average of 110 ±​ 16 mm over the past
10 years (Kwadaso Agricultural Station, Ghana). This exceptional dry period is
believed to have been caused by a particularly strong El Niño event, and these are,
more generally, known to cause droughts in West Africa36. Because El Niño events
are predicted to increase in intensity as a consequence of climate change51, such dry
periods may become more common in this region in the future.
In 2015, we selected 20 plots in cocoa agroforests along a gradient of shade-tree
cover ranging from low to high shade (14–76% shade-tree cover, see Supplementary
Table 6). Because low-shade agroforests are more common in the study region,
random selection of plots would have resulted in comparisons of the simple presence
versus absence of shade trees, which would not have allowed a comparison of how
the effects of agroforests change at different levels of shade-tree cover. Therefore, we
selected plots systematically to ensure our design could be used to meet our aim of
quantifying changes in the effectiveness of shade trees to meet production, climate
and conservation goals across a gradient of shade-tree cover. This design required
that other systematic differences between plots be controlled for. We therefore paired
each agroforest plot with a nearby monoculture plot on the same farm. The paired
sampling was aimed at controlling for variability between plots due to different soils,
local climate, farm age, cocoa variety and management practices between farms in
order to isolate the effects of shade trees on measured variables. We selected all plots
from relatively well-maintained, low-fertilizer-input, mature cocoa farms (15–25
years since establishment) with no commercial fruit or timber production, and in
which we could locate cocoa growing in monoculture and in agroforests. While
there was a possibility that high-shade plots may have occurred only in inherently
unproductive locations, this possibility was not supported by our soil fertility data
(Fig. 2c,d, and Supplementary Table 3). Plots measured 30 m ×​ 30 m. This plot size
was chosen because it is representative of the size of existing monocultures and
high-shade agroforest patches in the region. Our plots contained between 63 and 195
cocoa trees, with a mean of 108 ±​ 5 cocoa trees per plot.
The percentage of shade-tree canopy cover of each plot was estimated using
high-resolution aerial photographs captured with a quadcopter drone (Green
Copter Tropic-Quadro, Rucon Engineering) equipped with a digital camera
(Canon PowerShot S110). Photographs were analysed using image-processing
software (Agisoft PhotoScan 1.2.3 and Arc GIS 10.4). In each plot, we counted
cocoa and shade trees and calculated their density. We identified each species
of shade tree (Supplementary Table 6). We further recorded diameter at breast
height (DBH) of all cocoa and shade trees (Supplementary Table 6), and the height
of all shade trees. Based on these measurements, we estimated carbon stocks in
aboveground biomass using allometric relationships (Supplementary Methods).
We note that shade-tree density and DBH are strong determinants of shade-tree
cover (multiple regression: F3,16 =​  9.85, R2 =​  0.65, P <​ 0.001), and that similar shade-
tree cover could be achieved with a high density of small trees or a low density of
large trees (see Supplementary Figure 3 for analysis, and for calculations of cover as
a function of different tree-density and tree-size combinations).
Agricultural production, pests and disease. Ripe cocoa pods were harvested
within each plot at fortnightly intervals during the main and minor harvesting
seasons from September 2015 to July 2017. We recorded the number of healthy
and diseased cocoa pods and categorised diseased pods according to whether they
had black pod (Phytophthora sp.) or other diseases (mostly mirid bugs Sahlbergella
singularis and Distantiella theobroma). Wet-bean cocoa weight was measured for
healthy pods. Extracted beans from healthy pods on ten farms were fermented and
dried to determine the wet/dry bean conversion factor. Yields were expressed as dry
bean yield per area, as well as yield per cocoa tree. Disease levels were expressed as
the percentage of harvested pods lost to disease. Infestation with parasitic plants
(mistletoe) was assessed once by counting individual plants in each plot in January
2016. It is also important to note that a visual assessment by an expert in cocoa
swollen shoot virus did not reveal any signs of the disease in our plots.
Soil fertility. We collected 36 soil samples with a gouge auger (diameter 3 cm) in
each plot (0–15 cm depth) in May 2015. Samples were composited at the plot level
and analysed for pH, total carbon, nitrogen and phosphorus content, content of resin
extractable phosphorus and exchangeable cations (potassium, calcium, magnesium
and sodium), effective soil cation exchange capacity and soil texture. Soil bulk density
was determined based on nine additional core samples and used to calculate soil
carbon, nitrogen and phosphorus pools. For details, see Supplementary Methods.
Microclimate. Temperature and relative humidity were measured continuously
with five HOBO data loggers (HOBO Pro v2 U23-001) per agroforest plot,
installed 0.5 m above the cocoa canopy in September 2015. Monoculture plots
238
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NAture SustAinABility
were equipped with one logger in the centre of each plot, after we verified that
this design adequately captured the variability in full-sun monocultures (data not
shown). We calculated average daily mean temperature and relative humidity, daily
maximum temperatures and daily minimum relative humidity for each month.
We present monthly averages for October to represent the conditions at the end of
the wet season when shade trees have their full foliage and monthly averages for
February, which represents the height of the long dry period.
Volumetric water content in topsoils (0–20 cm) was measured at every metre
along six regular transects in each plot (126 measurements per plot) with a time
domain reflectometry sensor (HydroSense II, Campbell Scientific Ltd.), during
the peak of the short dry season (August 2015) and during the long dry season
(February 2016).
Biodiversity. Tree species richness was recorded in all plots with surveys of all trees
with DBH >​ 10 cm. In 10 out of 20 paired plots, we recorded the richness of birds,
ants and litter frogs between October and December 2015. Birds were recorded using
visual and acoustic surveys. Surveys were done on three separate mornings (between
06:00 and 10:00) in each plot, for 20 min each time. Surveys were done from the
centre of each plot, using the fixed-radius point-count method52. All surveys were
done by the same observer (J.L.). During each survey, bird calls were also recorded
continuously using a Tascam DR100 hand-held recorder equipped with a Sennheiser
ME66/K6 microphone, and the time-points of individual observations were recorded
to aid in a posteriori confirmation of bird identification when necessary53. Over
the course of 1 month prior to the survey period, the bird calls of the study area
were systematically recorded to build a reference database53. Species observed only
flying above the canopy were excluded. Litter frogs were surveyed in both the wet
and dry seasons. We conducted an exhaustive search for frogs for 30 min between
09:00 and 17:00 along 30 parallel, 1-m wide transects. After 30 min, all individuals
were identified, photographed and returned to the plot. When necessary, species
identification was confirmed using the photographs. Ground-dwelling ants were
sampled using four pitfall traps (diameter 14.5 cm) in each plot. After installation the
traps were closed for 10 days to avoid a temporary increase in the capture rate due
to the disturbance caused by the installation54. The traps were subsequently opened
and filled with ethanol. Traps were left open for 14 days, and insects were collected
every 7 days. All ants were identified to species or morphospecies level. We note
that our plots appear to be slightly smaller (for birds and trees) or similar (for frogs
and ants) in size compared to those used previously in assessments of biodiversity
in agroforests and other forest landscapes19,29,32,55,56. We further note that they were
of a sufficiently large size and number to detect differences in biodiversity between
monocultures and agroforests in all taxa, and significant positive relationships
between cover and diversity in two of four taxa (trees and birds).
Data analysis. We use the relative percentage difference (d) between monoculture
(m) and agroforest (a) plots according to the following equation for all measured
parameters: d=(a−m)/m×​100. This metric incorporates information from our
paired design, isolating the effects of shade trees from other confounding factors.
Moreover, this metric implicitly uses performance in monoculture as a baseline
to quantify the added advantage/disadvantage (expressed as percent change) of
the inclusion of shade trees on each of our response variables. With this metric,
we used polynomial regression to quantify the relationship between each of our
response variables and shade-tree cover. Models were simplified using partial F
tests, retaining quadratic terms at a significance level of P <​ 0.20 to guard against
type II errors57. Analyses for yield and losses to disease were based on values
averaged over the 2 years. Analyses of microclimate variables were done separately
for both wet and dry seasons in both years. Analyses of soil fertility variables,
carbon stocks and biodiversity were done using the single estimates of each of these
variables collected during the study.
Variables for resin-extractable phosphorus and bulk density were
log(x +​ constant)-transformed to meet model assumptions. When we detected no
effect of increasing shade-tree cover on a response variable, we carried out t-tests to
determine whether the simple presence or absence of trees (that is, agroforest versus
monoculture) caused differences in our response variable, independent of shade-tree
cover. All analyses were performed in R 3.2.4 (R Development Core Team 2016).
Data availability. The data that support the findings of this study are openly
available in figshare at https://doi.org/10.6084/m9.figshare.6118562
Received: 25 November 2017; Accepted: 10 April 2018;
Published online: 15 May 2018
References
1. Palm, C. A. et al. Identifying potential synergies and trade-offs for meeting
food security and climate change objectives in sub-Saharan Africa. Proc. Natl
Acad. Sci. USA 107, 19661–19666 (2010).
2. Lipper, L. et al. Climate-smart agriculture for food security. Nat. Clim.
Change 4, 1068–1072 (2014).
3. Godfray, H. C. J. et al. Food security: The challenge of feeding 9 billion
people. Science 327, 812–818 (2010).
Nature Sustainability | VOL 1 | MAY 2018 | 234–239 | www.nature.com/natsustain
NAture SustAinABility
4. Parry, M., Evans, A., Rosegrant, M. W. & Wheeler, T. Climate Change and
Hunger: Responding to the Challenge (World Food Programme, Rome, 2009).
5. Morton, J. F. The impact of climate change on smallholder and subsistence
agriculture. Proc. Natl Acad. Sci. USA 104, 19680–19685 (2007).
6. Garnett, T. et al. Sustainable intensification in agriculture: premises and
policies. Science 341, 33–34 (2013).
7. Campbell, B. M., Thornton, P., Zougmoré, R., van Asten, P. & Lipper, L.
Sustainable intensification: What is its role in climate smart agriculture?
Curr. Opin. Environ. Sustain. 8, 39–43 (2014).
8. Nair, P. R. An Introduction to Agroforestry (Kluwer Academic Publishers,
Dordrecht, 1993).
9. Harvey, C. A. et al. Climate-smart landscapes: Opportunities and challenges
for integrating adaptation and mitigation in tropical agriculture. Conserv.
Lett. 7, 77–90 (2014).
10. Jose, S. Agroforestry for ecosystem services and environmental benefits: an
overview. Agrofor. Syst. 76, 1–10 (2009).
11. Vaast, P., Harmand, J.-M., Rapidel, B., Jagoret, P. & Deheuvels, O. in Climate
Change and Agriculture Worldwide (ed. Torquebiau, E.) 209–224 (Springer
Netherlands, Dordrecht, 2016).
12. Lin, B. B. Agroforestry management as an adaptive strategy against potential
microclimate extremes in coffee agriculture. Agric. For. Meteorol. 144,
85–94 (2007).
13. Tscharntke, T. et al. Multifunctional shade-tree management in tropical
agroforestry landscapes—a review. J. Appl. Ecol 48, 619–629 (2011).
14. Andres, C. et al. Agroforestry systems can mitigate the severity of cocoa
swollen shoot virus disease. Agric. Ecosyst. Environ. 252, 83–92 (2018).
15. Schroth, G., Krauss, U., Gasparotto, L., Duarte Aguilar, J. A. & Vohland, K.
Pests and diseases in agroforestry systems of the humid tropics. Agrofor. Syst.
50, 199–241 (2000).
16. Schroth, G. et al. Contribution of agroforests to landscape carbon storage.
Mitig. Adapt. Strat. Glob. Change 20, 1175–1190 (2015).
17. Schroth, G. et al. Climate friendliness of cocoa agroforests is compatible with
productivity increase. Mitig. Adapt. Strat. Glob. Change 21, 67–80 (2016).
18. Feliciano, D., Ledo, A., Hillier, J. & Nayak, D. R. Which agroforestry options
give the greatest soil and above ground carbon benefits in different world
regions? Agric. Ecosyst. Environ. 254, 117–129 (2018).
19. Clough, Y. et al. Combining high biodiversity with high yields in tropical
agroforests. Proc. Natl Acad. Sci. USA 108, 8311–8316 (2011).
20. De Beenhouwer, M., Aerts, R. & Honnay, O. A global meta-analysis of the
biodiversity and ecosystem service benefits of coffee and cacao agroforestry.
Agric. Ecosyst. Environ 175, 1–7 (2013).
21. Sanchez, P. A. Science in agroforestry. Agrofor. Syst. 30, 5–55 (1995).
22. Guo, L. B. & Gifford, R. M. Soil carbon stocks and land use change: A meta
analysis. Glob. Change Biol. 8, 345–360 (2002).
23. Gibson, L. et al. Primary forests are irreplaceable for sustaining tropical
biodiversity. Nature 478, 378–381 (2011).
24. Läderach, P., Martinez-Valle, A., Schroth, G. & Castro, N. Predicting the
future climatic suitability for cocoa farming of the world’s leading producer
countries, Ghana and Côte d’Ivoire. Climatic Change 119, 841–854 (2013).
25. Schroth, G., Laderach, P., Martinez-Valle, A. I., Bunn, C. & Jassogne, L.
Vulnerability to climate change of cocoa in West Africa: patterns, opportunities
and limits to adaptation. Sci. Total Environ. 556, 231–241 (2016).
26. Franzen, M. & Borgerhoff Mulder, M. Ecological, economic and social
perspectives on cocoa production worldwide. Biodivers. Conserv. 16,
3835–3849 (2007).
27. Phalan, B., Onial, M., Balmford, A. & Green, R. E. Reconciling food
production and biodiversity conservation: Land sharing and land sparing
compared. Science 333, 1289–1291 (2011).
28. Blaser, W. J., Oppong, J., Yeboah, E. & Six, J. Shade trees have limited benefits
for soil fertility in cocoa agroforests. Agric. Ecosyst. Environ. 243, 83–91 (2017).
29. Bisseleua, D. H. B., Missoup, A. D. & Vidal, S. Biodiversity conservation,
ecosystem functioning, and economic incentives under cocoa agroforestry
intensification. Conserv. Biol. 23, 1176–1184 (2009).
30. Zuidema, P. A., Leffelaar, P. A., Gerritsma, W., Mommer, L. & Anten, N. P. R.
A physiological production model for cocoa (Theobroma cacao): model
presentation, validation and application. Agric. Syst. 84, 195–225 (2005).
31. Jacobi, J. et al. Carbon stocks, tree diversity, and the role of organic
certification in different cocoa production systems in Alto Beni, Bolivia.
Agrofor. Syst. 88, 1117–1132 (2014).
32. Steffan-Dewenter, I. et al. Tradeoffs between income, biodiversity, and
ecosystem functioning during tropical rainforest conversion and agroforestry
intensification. Proc. Natl Acad. Sci. USA 104, 4973–4978 (2007).
33. Wartenberg, A. C. et al. Does shade tree diversity increase soil fertility in
cocoa plantations? Agric. Ecosyst. Environ. 248, 190–199 (2017).
34. Ruf, F. O. The myth of complex cocoa agroforests: The case of Ghana. Hum.
Ecol. 39, 373–388 (2011).
35. Gockowski, J., Afari-Sefa, V., Sarpong, D. B., Osei-Asare, Y. B. & Agyeman, N. F.
Improving the productivity and income of Ghanaian cocoa farmers while
maintaining environmental services: What role for certification? Int. J. Agric.
Sustain. 11, 331–346 (2013).
Nature Sustainability | VOL 1 | MAY 2018 | 234–239 | www.nature.com/natsustain
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Articles
36. Abdulai, I. et al. Cocoa agroforestry is less resilient to sub-optimal and extreme
climate than cocoa in full sun. Glob. Change Biol. 24, 273–286 (2018).
37. Carr, M. K. V. & Lockwood, G. The water relations and irrigation
requirements of cocoa (Theobroma cacao L.): a review. Exp. Agric 47,
653–676 (2011).
38. Schroth, G., Läderach, P., Martinez-Valle, A. I. & Bunn, C. From site-level to
regional adaptation planning for tropical commodities: cocoa in West Africa.
Mitig. Adapt. Strat. Glob. Change 22, 903–927 (2017).
39. Asase, A., Asitoakor, B. K. & Ekpe, P. K. Linkages between tree diversity and
carbon stocks in unlogged and logged West African tropical forests.
Int. J. Biodivers. Sci. Ecosyst. Serv. Manag. 8, 217–230 (2012).
40. Paustian, K. et al. Climate-smart soils. Nature 532, 49–57 (2016).
41. Jagoret, P., Michel-Dounias, I., Snoeck, D., Ngnogue, H. T. & Malezieux, E.
Afforestation of savannah with cocoa agroforestry systems: A small-farmer
innovation in central Cameroon. Agrofor. Syst. 86, 493–504 (2012).
42. Clough, Y., Putra, D. D., Pitopang, R. & Tscharntke, T. Local and landscape
factors determine functional bird diversity in Indonesian cacao agroforestry.
Biol. Conserv. 142, 1032–1041 (2009).
43. Abrahamczyk, S., Kessler, M., Dwi Putra, D., Waltert, M. & Tscharntke, T.
The value of differently managed cacao plantations for forest bird
conservation in Sulawesi, Indonesia. Bird. Conserv. Int. 18, 349–362 (2008).
44. Teuscher, M. et al. Trade-offs between bird diversity and abundance, yields
and revenue in smallholder oil palm plantations in Sumatra, Indonesia. Biol.
Conserv. 186, 306–318 (2015).
45. Kleijn, D. et al. On the relationship between farmland biodiversity
and land-use intensity in Europe. Proc. R. Soc. B Biol. Sci. 276,
903–909 (2009).
46. Nilsson, F. O. L. Biodiversity on Swedish pastures: Estimating biodiversity
production costs. J. Environ. Manag. 90, 131–143 (2009).
47. Hulme, M. F. et al. Conserving the birds of Uganda’s banana-coffee arc: land
sparing and land sharing compared. PloS ONE 8, e54597 (2013).
48. Bhagwat, S. A., Willis, K. J., Birks, H. J. B. & Whittaker, R. J. Agroforestry:
a refuge for tropical biodiversity? Trends Ecol. Evol. 23, 261–267 (2008).
49. Lucey, J. M. & Hill, J. K. Spillover of insects from rain forest into adjacent oil
palm plantations. Biotropica 44, 368–377 (2012).
50. Asare, R. & Ræbild, A. Tree diversity and canopy cover in cocoa systems in
Ghana. New For. 47, 287–302 (2016).
51. Cai, W. et al. Increasing frequency of extreme El Niño eve’nts due to
greenhouse warming. Nat. Clim. Change 4, 111 (2014).
52. Hutto, R. L., Pletschet, S. M. & Hendricks, P. A fixed-radius point
count method for nonbreeding and breeding season use. Auk 103,
593–602 (1986).
53. Parker, T. A. III On the use of tape recorders in avifaunal surveys. Auk 108,
443–444 (1991).
54. Leather, S. R. Insect Sampling in Forest Ecosystems (Blackwell, Oxford, 2005).
55. Ferreira, R. B., Beard, K. H. & Crump, M. L. Breeding guild determines frog
distributions in response to edge effects and habitat conversion in the Brazil’s
Atlantic Forest. PLoS ONE 11, e0156781 (2016).
56. Kraft, N. J. B. et al. Disentangling the drivers of β​diversity along latitudinal
and elevational gradients. Science 333, 1755–1758 (2011).
57. Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for
Biologists (Cambridge Univ. Press, Cambridge, 2002).
Acknowledgements
We thank K. Oppong and D. Oppong for assistance with fieldwork, and farmers in
the study region for allowing access to their farms. We further acknowledge J. O. Fening
for institutional support provided by the Soil Research Institute of Ghana. We thank
B. Jahn-Humphrey, G. Asamoah, B. Studer, G. Quansah, T. Afreh and M. Amponsah for
laboratory assistance. C. Ofori kindly helped us with the identification of frogs. This study was
funded by the Sustainable Agroecosystems Group at ETH Zurich and a grant from the Swiss-
African Research Cooperation (SARECO) funded by the University of Basel, Switzerland.
Author contributions
W.J.B., S.P.H. and J.S. designed the research. W.J.B., J.O., J.L. and E.Y. performed the
research. W.J.B., S.P.H. and J.S. analysed and interpreted the data. W.J.B. wrote the first
draft and S.P.H. and J.S. contributed to revisions.
Competing interests
The authors declare no competing interests.
Additional information
Supplementary information is available for this paper at https://doi.org/10.1038/
s41893-018-0062-8.
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