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Apes and agriculture
Erik Meijaard
1,2
*, Nabillah Unus
1
, Thina Ariffin
1
, Rona Dennis
1
,
Marc Ancrenaz
1,3
, Serge Wich
4
, Sven Wunder
5,6
,
Chun Sheng Goh
7,8
, Julie Sherman
9
, Matthew C. Ogwu
10
,
Johannes Refisch
11
, Jonathan Ledgard
12
, Douglas Sheil
13
†
and Kimberley Hockings
14
†
1
Borneo Futures, Bandar Seri Begawan, Brunei,
2
Durrell Institute of Conservation and Ecology (DICE),
School of Anthropology and Conservation, University of Kent, Canterbury, United Kingdom,
3
HUTAN-
Kinabatangan Orangutan Conservation Programme (HUTAN –KOCP), Sandakan, Malaysia,
4
School of
Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, United Kingdom,
5
European Forest Institute, Barcelona, Spain,
6
Center for International Forestry Research, Lima, Peru,
7
Jeffrey Sachs Center on Sustainable Development, Sunway University, Kuala Lumpur, Malaysia,
8
Harvard University Asia Center, Cambridge, MA, United States,
9
Wildlife Impact, Portland, OR, United
States,
10
Goodnight Family Sustainable Development Department, Appalachian State University,
Boone, NC, United States,
11
Great Apes Survival Partnership, United Nations Environment Program,
Nairobi, Kenya,
12
Artificial Intelligence Center, Czech Technical University, Prague, Czechia,
13
Forest
Ecology and Forest Management Group, Wageningen University and Research,
Wageningen, Netherlands,
14
Center for Ecology and Conservation, University of Exeter,
Penryn, United Kingdom
Non-human great apes –chimpanzees, gorillas, bonobos, and orangutans –are
threatened by agricultural expansion, particularly from rice, cacao, cassava, maize,
and oil palm cultivation. Agriculture replaces and fragments great ape habitats,
bringingthem closer to humans andoften resulting in conflict. Thoughthe impact of
agriculture on great apes is well-recognized, there is still a need for a more nuanced
understanding of specific contexts and associated negative impacts on habitats and
populations. Herewe review these contexts and theirimplicationsfor great apes. We
estimate that within their African and South-East Asian ranges, there are about 100
people for each great ape. Given that most apes live outside strictly protected areas
and the growing human population and increasing demand for resources in these
landscapes, it will be challenging to balance the needs of both humans and great
apes. Further habitat loss is expected, particularly in Africa, where compromises
must be sought to re-direct agricultural expansion driven by subsistence farmers
with small fields (generally <0.64 ha) away from remaining great ape habitats. To
promote coexistence between humans and great apes, new approaches and
financial models need to be implemented at local scales. Overall, optimized land
use planning and effective implementation, along with strategic investments in
agriculture and wildlife conservation, can improve the synergies between
conservation and food production. Effective governance and conservation
financing are crucial for optimal outcomes in both conservation and food
security. Enforcing forest conservation laws, engaging in trade policy discussions,
and integrating policies on trade, food security, improved agricultural techniques,
and sustainable food systems are vital to prevent further decline in great ape
populations. Saving great apes requires a thorough consideration of specific
agricultural contexts.
KEYWORDS
conservation, conservation finance, crop foraging, food security, food systems, great
apes, poverty, rural development
Frontiers in Conservation Science frontiersin.org01
OPEN ACCESS
EDITED BY
Maria Cristina Duarte,
University of Lisbon, Portugal
REVIEWED BY
Andreia Garces,
University of Tra
´s-os-Montes and Alto
Douro, Portugal
Maria Joana Ferreira Da Silva,
Centro de Investigacao em Biodiversidade
e Recursos Geneticos (CIBIO-InBIO),
Portugal
*CORRESPONDENCE
Erik Meijaard
emeijaard@borneofutures.org
†
These authors have contributed equally to
this work
RECEIVED 20 May 2023
ACCEPTED 09 October 2023
PUBLISHED 09 November 2023
CITATION
Meijaard E, Unus N, AriffinT,Dennis R,
Ancrenaz M, Wich S, Wunder S, Goh CS,
Sherman J, Ogwu MC, Refisch J,
Ledgard J, Sheil D and Hockings K (2023)
Apes and agriculture.
Front. Conserv. Sci. 4:1225911.
doi: 10.3389/fcosc.2023.1225911
COPYRIGHT
© 2023 Meijaard, Unus, Ariffin, Dennis,
Ancrenaz,Wich,Wunder,Goh,Sherman,
Ogwu, Refisch, Ledgard, Sheil and Hockings.
This is an open-access article distributed
under the terms of the Creative Commons
Attribution License (CC BY). The use,
distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Review
PUBLISHED 09 November 2023
DOI 10.3389/fcosc.2023.1225911
1 Introduction
Agricultural expansion is the leading cause of biodiversity loss,
with global cropland estimated at 1,244 Mha in 2019 (Potapov et al.,
2022) and predicted to expand further by 193–317 Mha by 2050,
mainly in Africa (Schmitz et al., 2014). This expansion will reduce
available habitat for 87.7% of the 19,859 terrestrial vertebrate
species recently reviewed by Williams et al. (2021), with 1,280
species losing >25% of their remaining range. Balancing the
demands for crops and conservation is one of the biggest
challenges of the 21
st
century (Dudley and Alexander, 2017),
especially in the tropics, where species diversity is high, and large
natural ecosystems are declining due to human impacts (Cincotta
et al., 2000;Pendrill et al., 2022). The impact of agriculture on non-
human great apes (further referred to as “great apes”) in the Asian
and African tropics is of particular concern, with chimpanzees,
bonobos, Western and Eastern gorillas, and three species of
orangutans all in decline and threatened with extinction within
the coming decades (Figure 1, for scientific names see Table 1). The
distribution and density of these species are primarily determined
by habitat availability, disease, killing for meat and other purposes,
and people’s attitudes to sharing landscapes with great apes. Despite
national legislation legally protecting these species in all 23
countries they occur in, the threat to their survival remains high
(Caldecott and Miles, 2006;Bettinger et al., 2021).
The remaining great apes (750,000-1,250,000, see Figure 1)
share their distribution ranges with around 97 million people (1
great ape per 77-129 people, see Supplementary Materials and
Table 1). In simple terms, one great ape shares resources with 100
humans, mainly in countries with high human population growth
and poverty (i.e., income of less than US$2 per day), and low food
security. For instance, according to World Bank data, the
B
A
FIGURE 1
(A) African great ape subspecies ranges in relation to the distribution of crops expressed as majority crop per 10*10 km grid cell (You et al., 2017).
(B) Asian great ape subspecies. Population estimates from Rainer et al. (2020) and ranges based on IUCN Red List data for individual species.
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org02
Democratic Republic of the Congo (DRC) has a 2.9% annual
population growth rate, which could double the number of people
living alongside great apes in 25 years. Some of the great ape
range countries are also those with the highest levels of
undernourishment: 21% of the Sub-Saharan people were
undernourished in 2020 (The World Bank, 2022a). Thus, there is
an urgent need for increased local food production and more equal
distribution of food to improve food availability, affordability, and
security. Growing human populations and a drive for economic
development, alongside growing international demand, remain key
drivers of deforestation (Busch and Ferretti-Gallon, 2017)and
therefore great ape habitat loss.
The threats to great apes related to agriculture include habitat
loss and fragmentation due to agricultural expansion, the resulting
genetic factors related to small and isolated populations,
agriculture-related diseases, as well as the human-great ape
conflict, and ape killing, capture, and trade (Figure 2). In terms of
agricultural expansion, we focus on crops rather than livestock,
because in the orangutan ranges livestock-related forest loss is rare,
while, in Africa, such losses are concentrated in the drier parts
where great apes generally do not occur (although chimpanzee
habitat in Tanzania, Senegal, and Mali is a local exception). Maize
(Zea mays L.), rice (Oryza spp.), millet (various species), and
cassava (Manihot esculenta Crantz) are the main crops of concern
(for details see Tables S1–S3). These are mostly grown in
smallholder, subsistence agriculture contexts (Table 1), with fields
typically <0.64 ha in size (Lesiv et al., 2019), and further field size
reduction ongoing (Abraham and Pingali, 2020). Rice, maize, and
cassava show the most rapid expansion, while other crops such as
sesame (Sesamum indicum L.), sunflower (Helianthus annuus L.),
cotton (Gossypium L.) and okra (Abelmoschus esculentus (L.)
Moench) have expanded but use up less land (FAOSTAT, 2023).
TABLE 1 Great ape taxa, the number of people within the great ape ranges (Schiavina et al., 2022), the primary drivers of forest cover loss (Laso Bayas
et al., 2022), and main crops in great ape ranges (Meijaard et al., 2021).
Great ape
species or
subspecies
Scientific
name
Estimated number of people
within great ape range in 2020
(predicted annual growth rate in %
2020-2030)
Two main primary driver(s) of
forest cover loss for the period
2008 to 2019 within great ape
ranges
Two main crops
based on largest
area within (sub)
species range
Nigeria-
Cameroon
chimpanzee
Pan t. ellioti 2,411,401 (2.8) Subsistence agriculture and other natural
disturbances Oil palm, cacao
Western
chimpanzee P. t. verus 28,170,665 (2.6) Subsistence agriculture and pasture Rice, cacao
Eastern
chimpanzee
P. t.
schweinfurthii 32,135,959 (2.4) Subsistence agriculture and other natural
disturbances Cassava, maize
Central
chimpanzee
P. t.
troglodytes 14,222,850 (3.2) Subsistence agriculture and other natural
disturbances Cassava, cacao
Bonobo Pan paniscus 3,758,691 (1.5) Subsistence agriculture and other natural
disturbances Cassava, maize
Western
lowland gorilla
Gorilla. g.
gorilla 12,020,627 (3.3) Subsistence agriculture and other natural
disturbances Cassava, cacao
Cross-River
gorilla G. g. diehli 57,798 (2.7) Subsistence agriculture and other natural
disturbances Cassava, vegetables
Grauer’s gorilla G. b. graueri 938,866 (2.4) Subsistence agriculture and other natural
disturbances Beans, maize
Mountain
gorilla G. b. beringei 826 (26.9) No data Beans, potatoes
Northwest
Bornean
orangutan
Pongo p.
pygmaeus 501,084 (1.5) Subsistence agriculture and commercial oil
palm/other plantations Oil palm, tree crops
Southwest
Bornean
orangutan
Pongo p.
wurmbi 1,441,523 (0.9) Subsistence agriculture and commercial oil
palm/other plantations Oil palm, tree crops
Northeast
Bornean
orangutan
Pongo p.
morio 1,080,217 (3.0) Subsistence agriculture and commercial oil
palm/other plantations Oil palm, tree crops
Sumatran
orangutan P. abelii 16,526 (1.7) Subsistence agriculture and commercial oil
palm/other plantations Oil palm, tree crops
Tapanuli
orangutan
P.
tapanuliensis 674 (0.6) Subsistence agriculture, pasture and
commercial oil palm/other plantations Oil palm, tree crops
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org03
African oil palm (Elaeis guineensis Jacq.) is another crop that has
been a driver of deforestation, especially in Southeast Asia’s
orangutan ranges (Table S4), with concerns about its expansion
in Africa and potential impact on great apes (Linder, 2013;Wich
et al., 2014). While the media has extensively covered the effects of
industrial oil palm expansion on great apes, there has been relatively
little scrutiny on the impacts of other crops (Jayathilake et al., 2021).
There is considerable variation in the type of crops grown across
the great ape range (Supplementary Materials). Most African great
apes reside in tropical evergreen forests, but some populations are
also found in deciduous woodland and drier savannah-dominated
habitats interspersed with gallery forests. The crops grown in these
areas are adapted to equatorial fully humid, monsoonal, summer
dry, and winter dry conditions (Kottek et al., 2006). The regions
primarily cultivate annual crops, although there are also perennial
crops such as oil palm, tree crops, and cacao (Table 2). The use of
crop areas by great apes for feeding or dispersal, and the level of
persecution they face for consuming different crops, vary depending
FIGURE 2
Causal transmission chain of (negative) change between human expansion in land use and the fate of the great apes (referred to as “apes”).
TABLE 2 Typology of main crops that occur in great ape ranges and are likely to cause most great ape habitat loss.
Crop Total area
W, C, and
E Africa
and SE
Asia 2021
(ha)
Regional
rate of
expansion
(% increase
2010-2021)
Main
great ape
species
using
these
crops
Type of crop Primary local
crop use
(subsistence
or cash)
Primary
global crop
use
References
Paddy (rice) 60,423,297 2.9% Among
others,
chimpanzees
forage on
paddy
Annual (up to 2-3
crop cycles per year).
In Africa (especially
West) increasingly
used in urban
communities. Staple
in Asia. Important
cash crop.
Food (McLennan and
Hockings, 2014;
Muthayya et al.,
2014;Zenna et al.,
2017)
Maize (corn) 47,035,255 21.3% Chimpanzees,
Western and
Eastern
Gorilla forage
on maize
Annual (5–6-month
crop cycle). Rotated
with other crops
80% used for food
(especially in East
Africa).
56% used for
livestock feed,
remainder for
food, ethanol,
starch, oil,
beverages, glue
(Naughton-Treves
et al., 1998;Ranum
et al., 2014;Hill,
2017;Ekpa et al.,
2019;Erenstein
et al., 2022)
Cassava.
fresh
27,107,655 47.5% Chimpanzees
forage on
cassava
Annual. Long growth
cycle (10-12 months
or more)
80% of global
production from
Africa and Asia.
Food crop and
income. Export crop
in Asia
Livestock feed
and food
(Caccamisi, 2010;
Hockings et al.,
2015;Garriga et al.,
2018)
(Continued)
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org04
on the type of crop cultivated and species ecology (Supplementary
Materials). Soil fertility may also influence great ape presence, with
areas in Borneo that have low soil fertility and are poorly suited to
agriculture, traditionally being used by nomadic hunter-gatherer
people who likely hunted out orangutans in the past (Meijaard,
2017). It remains unclear whether this also applies to Africa,
although the more fertile parts, such as volcanic mountain slopes
(see, e.g., Hengl et al., 2021) seem to retain species such as
mountain gorillas.
Only some areas of the remaining great ape habitat are formally
protected. For example, 83% of chimpanzees in West Africa
(Heinicke et al., 2019) and about 80% of central chimpanzees and
western gorillas in Central Africa reside outside protected areas
(Kormos et al., 2003;Brncic et al., 2015;Tweh et al., 2015;
Strindberg et al., 2018). Additionally, about 50% of orangutans in
Indonesian Borneo reside outside protected areas (Meijaard et al.,
2022b). These unprotected habitats are under particular threat from
agricultural expansion, though even protected areas can be
TABLE 2 Continued
Crop Total area
W, C, and
E Africa
and SE
Asia 2021
(ha)
Regional
rate of
expansion
(% increase
2010-2021)
Main
great ape
species
using
these
crops
Type of crop Primary local
crop use
(subsistence
or cash)
Primary
global crop
use
References
Oil palm
fruit
26,898,747 45.7% Orangutans
and
chimpanzees
feed on fruits
and use crop
for dispersal
Perennial (25-year
cycle)
Cash crop and local
use. Export
commodity in Asia
Food, biofuel,
cosmetics
(Ancrenaz et al.,
2015;Garriga et al.,
2018;Meijaard et al.,
2020)
Sorghum 21,172,564 3.4% No major
crop foraging
by great apes
reported
Perennial plant but
grown in annual
cycles (perennial
tropical grass with a
growing season of 4-5
months)
Mostly local food
subsistence use in
Africa. Not much
used in SE Asia.
Various stover uses
Livestock feed,
biofuel and food
(Mundia et al., 2019)
Groundnuts,
excluding
shelled
16,161,007 22.6% No major
crop foraging
by great apes
reported
Annual (4–5-month
crop cycle). Rotated
with other crops
Local use for food,
oil and feed. Nigeria
and Indonesia major
producers. Cash
crop.
Important source
of oil and protein
(Fletcher and Shi,
2016)
Millet 15,697,663 -19.5% No major
crop foraging
by great apes
reported
Depends on species.
Grown in annual
cycles (4-5 months).
Low fertilizer and
pesticide needs
Mostly local food
subsistence use in
Africa, also livestock
feed. Not much used
in SE Asia.
Increasing global
demand for food.
Drought-resistant
and considered a
“healthy”grain
(Kumar et al., 2018;
Antony Ceasar and
Maharajan, 2022)
Cow peas,
dry
14,556,604 28.2% No major
crop foraging
by great apes
reported
Annual crop of semi-
arid areas.
Intercropped because
of nitrogen-fixation
Mostly grown in
Nigeria and Niger.
Subsistence and cash
crop used for food
and feed.
Increasing
demand from
food & beverages
industry
(Siddiq et al., 2022)
Beans (dry).
Different
species, e.g.,
lentils,
chickpeas
11,777,348 15.2% Western and
Eastern gorilla
forage on
beans
Annuals. Crop cycle
depends on species.
Primarily grown at
higher elevations
Subsistence and cash
crop
Growing demand
because of health
benefits
(Siddiq et al., 2022)
Rubber 11,111,673 39.6% Some bark
stripping and
nesting
reported by
orangutans
Perennial Cash crop. Indonesia
and Malaysia major
producers
Various industrial
uses
(Umar et al., 2011;
Campbell-Smith
et al., 2012)
Cacao 9,444,854 20.0% Chimpanzees
and Western
gorilla feed on
cacao
Perennial Cash crop, mostly for
export
Chocolate
products
(McLennan, 2013)
All crop data (FAOSTAT, 2023).
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org05
vulnerable –depending on management, and the extent to which
community needs are integrated into protected area management.
Overall, understanding the distribution and ecology of great apes is
crucial in understanding the threat posed by agriculture.
The different characteristics of the fourteen great ape species
and subspecies (Table 1,Supplementary Materials), the different
regions of the world in which they occur, and the different
agricultural crops that may threaten their habitats or provide
some ecological opportunities to them (Table 2), result in a
complex picture regarding the relationship between agriculture
and great apes. This is further confounded by the scales at which
crops are produced (e.g., smallholder or industrial scale), growth
types (annual or perennial, monoculture or inter-cropped) or
whether crops are produced for subsistence or cash-income
purposes. Here we review the literature on great apes and
agriculture. Because of the complex nature of the topic and the
often qualitative evidence presented in published sources, we use
literature review with narrative synthesis to generate insights about
the apes and agriculture interface (Grant and Booth, 2009). We
searched the scientificliteratureforpapersongreatapesin
agricultural contexts using species names as search terms,
combined with agriculture-related search terms, but did not
conduct a formal quality assessment. Trends in land use
associated with various crops were determined using data
provided by the United Nations Food and Agriculture
Organization. Our objectives are to 1) assess the dominant crops
and food systems in the ranges of the 14 great ape species and
subspecies; 2) identify antagonistic and synergistic co-occurrences;
3) understand economic and political factors that might influence
future agricultural developments; and 4) provide recommendations
towards improved co-existence between apes and agriculture. We
hope to clarify how future agricultural developments are likely to
affect different great ape taxa, and what can be done to minimize
negative impacts.
2 Key agricultural trends where apes
and crops converge
In Africa, agricultural production mainly serves domestic
consumption with few crops generating export revenues
(Rakotoarisoa et al., 2012). Smallholder farming dominates,
although a transition to business-oriented processes is underway
(Mukasa et al., 2017;Giller, 2020). Farms still struggle to provide
food security or living incomes. Production is expected to increase
(Sanchez, 2002;Pendrill et al., 2022;Potapov et al., 2022), putting
further pressure on land, especially in Ghana, Ivory Coast, Benin,
Nigeria, and Cameroon (Halpern et al., 2022). Infrastructural
development related to extractive industries (Weng et al., 2013)is
linked to agricultural growth corridors (Independent Science and
Partnership Council, 2016), impacting areas of high biodiversity
(Laurance et al., 2015).
Agricultural expansion on Borneo and Sumatra has led to major
forest loss since the 1970s (Wilcove et al., 2013). These tropical
islands are highly suitable for the cultivation of crops such as oil
palm, with rice, rubber (Hevea brasiliensis Müll. Arg.), maize,
coconut (Cocos nucifera L.), and coffee (Coffea arabica L.) also
grown (Table S4). Oil palm agriculture is dominated by large-
holders, but while there is more industrial-scale agriculture
compared to African great ape ranges (Table 1), forest loss has
declined recently due to improved governance of this sector
(Gaveau et al., 2019;Gaveau et al., 2022). Nevertheless, soil
impoverishment and economic factors drive smallholder farmers
to clear forests (Duffy et al., 2021), especially low nutrient peat
swamp forests that are important for orangutans (Meijaard
et al., 2010).
Across Sub-Saharan Africa and South-East Asia, agricultural
expansion is leading to significant changes in land use patterns, with
certain crops showing particularly rapid rates of growth. Cassava,
oil palm, and rubber have been the crops with the greatest regional
expansion rates (Table 2). Meanwhile, land under maize is also
expanding, and if current regional trends continue, it may approach
equivalence with the area under rice within the next decade. Two
other crops, yams (Dioscorea spp.) and plantain (Musa spp.) have
also seen significant increases in area between 2010 and 2021, with
respective growth rates of 87.0% and 55.2% (FAOSTAT, 2023).
There is considerable variation in crop distribution across
different regions. In Central Africa, for instance, which is home to
bonobos, chimpanzees, and Western gorillas, the largest areas are
allocated to cassava, maize, groundnuts (Arachis hypogaea L.),
sorghum (Sorghum bicolor L. Moench), and rice (Table S1).
Meanwhile, in West Africa, which is home to chimpanzees and
Cross-River gorillas, sorghum, maize, and cow peas dominate
(Table S2). While the effects of climate change on crop
distribution are unclear, it is likely that areas with rain-fed
agriculture and limited economic and institutional capacity to
respond to climate variability and change, such as some parts of
West Africa, will be negatively impacted through yield losses
(Sultan and Gaetani, 2016). Such losses could increase pressure
on the remaining forested areas where great apes live. In Borneo,
predicted reductions in rainfall and increases in temperature
(McAlpine et al., 2018) are likely to limit areas suitable for crops
such as oil palm, which is vulnerable to prolonged drought, and
reduce available orangutan habitat (Struebig et al., 2015).
Great apes react differently to reduction in forest habitats and
changing foraging opportunities and threats (see Supplementary
Materials for short species ecology reviews). The species are
primarily adapted to a plant diet –with meat consumption by
chimpanzees being an exception (Fahy et al., 2013)–and may target
crops in fields or fruit and trees in orchards and plantations,
especially when wild foods are scarce, but also because these may
be preferred, since they are highly nutritious and easy to access
(Hockings and Humle, 2009;Hockings et al., 2009;Campbell-Smith
et al., 2011;Hockings and McLennan, 2012;Seiler and Robbins,
2016). Great apes and humans also share the need for water (Box 1).
Preliminary studies indicate that individuals in some great ape
species change their behavior over time to human-dominated
landscapes (Hockings et al., 2015), changing food items as they
learn what is edible and learning to navigate agricultural lands
(McLennan and Hockings, 2014;Ancrenaz et al., 2015;McLennan
et al., 2021). These behaviors are often maladaptive, as the
nutritional benefits can be outweighed by the costs of increased
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org06
mortality through accidental snaring, retaliatory killings, and disease.
As species with low reproductive outputs, retaliatory killings ofapes by
humans in response to crop consumption are unlikely to be
sustainable. Disagreements between different human groups over
how to manage problematic great ape behavior can follow
(Campbell-Smith et al., 2011;Hockings and McLennan, 2012).
3 Reducing antagonistic co-
occurrences between great ape
conservation and agriculture
Great apes can coexist with humans in shared landscapes, but
local attitudes towards them determine whether this is beneficial or
harmful. Coexistence requires humans and wildlife to co-occur
(Harihar et al., 2013), with tolerable risks to both, and should be
sustainable (Carter and Linnell, 2016). Some sites have shown co-
adaptation between chimpanzees and smallholder agriculture
(Halloran, 2016;Bersacola et al., 2021;McLennan et al., 2021),
while orangutans survive in forest fragments in Malaysian oil palm
landscapes because people accept their presence (Ancrenaz et al.,
2021). People in the latter landscape are generally not concerned
about orangutans or crop losses, and orangutans are generally safe,
although it is unclear if these fragmented populations will remain
viable in the long-term (Oram et al., 2022). Conservation planning
for great apes needs to consider whether agricultural expansion is
driven by poverty and if killing of great apes may continue, or if
more stable conditions can be achieved.
Preventing agricultural expansion is the best way to minimize
negative impacts on great apes, but this can be difficult in regions
with undernourishment and poverty (Meijaard et al., 2022a). Areas
of poverty often coincide with relatively good forest protection
(Busch and Ferretti-Gallon, 2017), but transitioning to middle-
income levels may accelerate agricultural development and pose a
threat. Reducing poverty without deforestation requires greater
stakeholder engagement (Garcia et al., 2020), such as involving
communities in forest enterprise (Santika et al., 2019), although the
broader applicability of such models across great ape ranges
remains unclear. Also, even when deforestation rates can be
reduced, reducing poaching ratesischallengingandrequires
long-term financing (Sandker et al., 2009).
Efforts to reduce forest loss and poaching rates whilst alleviating
poverty could help reduce pressures on great ape populations and
habitats as economies develop, i.e., the forest transition (Mather and
Needle, 1998). In Africa, deforestation is thought to be positively
related to real Gross Domestic Product (GDP) per capita until a
turning point around USD 3,000 per capita income, beyond which
deforestation is expected to decline (Ajanaku and Collins, 2021).
African apes are most threatened in areas with low to medium
poverty, growing GDP, expanding agriculture, and growing rural
populations (Tranquilli et al., 2012). Local economic development
that spares forest or development away from forest areas could
reduce population pressure and forest losses. The Sub-Saharan
region is already undergoing rapid urbanization with forecasts
indicating that ca. 58% of its population is going to live in cities
by 2050 compared to ca. 40% now (UNDESA, 2019). Nevertheless,
although overall annual growth rates have declined from 2.4% in
BOX 1 The crucial role of access to water for great apesn.
Apes obtain water from their food and by drinking surface water or water collected in tree holes, sometimes with the use of leaf tools, with some communities of
chimpanzees digging wells (Figure 3). However, agriculture and climate change have reduced the availability of water (Akpabio, 2007), affecting great apes’health,
behavior, and social interactions. For instance, apes in sub-Saharan Africa are facing water scarcity due to increased competition and climate change effects (Vise-Thakor,
2022). Reduced water sources force great apes to drink from fewer shared drinking spots, which increases disease risk (Wright et al., 2022) and the likelihood of aggressive
interactions with people, especially children. The proximity of water sources for agricultural areas can also lead to contamination of water sources with pesticides (Masi
et al., 2012;Shively and Day, 2015;Sharma et al., 2016). Great apes might be able to adapt to these challenges by developing new behaviours or adapting existing ones, such
as well digging (Kalan et al., 2020;Peter et al., 2022), but conservation planning must focus on ensuring safe access to water for great apes as part of forest protection.
FIGURE 3
Adult male chimpanzee at a drinking hole at Cantanhez National Park. Reprinted with permission from Joanna Bessa (Cantanhez Chimpanzee Project).
Meijaard et al. 10.3389/fcosc.2023.1225911
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1980 to 1.7% in 2021 (The World Bank, 2022b), rural population
growth is likely to continue. Resulting migration patterns in Sub-
Saharan Africa are complex, even more so when driven by armed
conflict (Mercandalli et al., 2019). While poverty levels may locally
prevent deforestation, these may not be a good predictor of great
ape survival itself. Ordaz-Nemeth et al. (2021) found a negative
quadratic relationship between African great ape densities and
GDP, with decreasing great ape densities, partially poaching-
related, above a nationwide GDP of $5 billion annually, which
translates into a per capita GDP for these countries between USD
500 and 2,500. The effects of GDP maybe therefore play out
differently on deforestation and poaching, and poverty and
income levels as such may be poor predictors of great ape survival.
The debate on land sharing versus land sparing is relevant to
reducing negative interactions between people and great apes
(Phalan et al., 2011;Law and Wilson, 2015). Land sparing aims to
set aside large tracts of land for exclusive wildlife use while
intensifying agriculture on existing farmland to keep people and
great apes apart. Land sharing seeks coexistence between people and
great apes through small-scale farming and sustainable forest
management in patchworks of low-intensity agriculture.
Empirical evaluations suggest that land sparing results in better
outcomes for wildlife diversity and abundance in the short term
(Phalan et al., 2011;Hulme et al., 2013;Williams et al., 2017), but
others note that isolated protected areas within an agricultural
matrix can increase inbreeding and vulnerability to extinction
(Kremen and Merenlender, 2018). This has been demonstrated in
orangutans (Bruford et al., 2010) and Cross-River gorillas (Bergl
et al., 2008), although such effects will depend on the extent to
which apes use the matrix. The impacts of intensive agriculture,
such as the use of fertilizers, herbicides, fungicides, and pesticides
(Matson and Vitousek, 2006;Dudley and Alexander, 2017), can also
be harmful to great apes (Krief et al., 2017). Research suggests that
intensification does not necessarily reduce the area under
agriculture because high yields drive further agricultural
expansion (Byerlee et al., 2014;Balmford, 2021). The reality for
great apes is likely to remain a mixed sharing and sparing model,
where parts of their remaining range will need to be included in
protected areas while others will need to be shared with farmers
(Meijaard et al., 2022b). Protected land is still necessary in these
shared landscapes due to the low reproductive rates of great apes,
their area requirements, and crop foraging. Therefore, land sparing-
type solutions that safely protect habitat fragments and keep them
connected are required for the synergistic coexistence of people and
great apes (Ancrenaz et al., 2021).
4 Solutions for saving great apes in
secure food systems
The coexistence of great apes and agriculture is challenging and
a win-win situation for both is difficult to achieve. Agricultural
expansion, often associated with people without prior experience of
great ape coexistence moving into great ape areas, is likely to cause
further declines in ape populations. This makes sustainable and
resilient interactions between people and nature difficult to achieve.
If we truly want to save great apes from extinction, then we must
prioritize implementing strict spatial planning and rigorous
enforcement measures, that are ideally co-developed with local
communities. This includes designating no-farming areas,
improving crop productivity and diversification, resolving
human-wildlife conflicts, securing adequate conservation
financing, and clearly defining the roles and responsibilities of
different stakeholders (Table 3). Without a committed and
sustained effort in these areas, the survival of great apes will
remain uncertain, and the consequences of their extinction will be
irreversible. Finding solutions that work for great apes would have
implications for many other threatened species in similar socio-
ecological contexts across the tropics.
Great apes face competition for land and resources with
humans, particularly where crops such as rice, cassava, maize,
cacao, and oil palm are grown within their ranges (Table 3). This
creates trade-offs between reducing poverty, feeding people, and
TABLE 3 Primary food system archetypes for each great ape taxon
based on country profiles by Marshall et al. (2021).
Great ape
species or
subspecies
Primary
food
system
Main crops
concern for
expansion
or foraging
Key strategies
to facilitate
coexistence
Nigeria-
Cameroon
Chimpanzee
Emerging and
Diversifying
Oil palm, rice,
cassava
Produce and
protect, threat
management and
finance, yield
increases
Western
Chimpanzee
Mostly Rural
and
Traditional;
Some Informal
and Expanding
Rice, cacao,
cassava,
groundnut
Produce and
protect, threat
management and
finance, yield
increases
Eastern
Chimpanzee
Mostly Rural
and Traditional
Cassava,
plantain, maize
Produce and
protect, threat
management and
finance, payment
for biodiversity
Central
Chimpanzee
Informal and
Expanding;
Emerging and
Diversifying
Cassava,
plantain, rice
Produce and
protect, threat
management and
finance, payment
for biodiversity
Bonobo Rural and
Traditional
Cassava,
groundnut,
maize
Produce and
protect, threat
management and
finance, payment
for biodiversity
Western
Lowland
Gorilla
Informal and
Expanding;
Emerging and
Diversifying
Plantain
Produce and
protect, threat
management and
finance, payment
for biodiversity
Cross River
Gorilla
Informal and
Expanding Vegetables
Produce and
protect, threat
management and
(Continued)
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conserving the environment. To address this, strategies must tackle
the root causes of the problem, including land use competition. We
suggest a framework for discussion, presented in Figure 5, focused
on three directions. The first is to increase food production
sustainably through agricultural innovations and smarter land use
practices. The second is to modify food consumption patterns and
distribution systems to reduce pressure on land and resources.
Alternative food sources with minimal impact on great apes,
including imported foods, might be effective under specific
conditions. Though such lifestyle changes could raise complex
issues related to food security and trade considerations. The third
direction focuses on generating alternative income.
We emphasize the importance of adopting a landscape and
jurisdictional approach in managing the competition between
humans and great apes (Sayer et al., 2013). Within this
framework, we propose several solutions, including strategies to
increase yield, produce-and-protect practices, and threat
management techniques. Next, we explore potential strategies to
improve alternative income sources for communities, thereby
reducing the need for land exploitation that can trigger
competition with great apes (Figure 4). Finally, we consider the
need to rethink our food systems in the context of the competition
with great apes. We analyze potential solutions on both the
consumption side and the production side, including modifying
local food systems (e.g., by promoting dietary changes among local
communities, such as switching from rice or maize to other crops)
and global food systems (e.g., by reducing waste and rethinking
food versus materials use) (Figure 5).
4.1 Land use planning and
landscape management
To resolve the great ape habitat-agricultural conflict, land use
planning and implementation must consider crop impact on trade,
TABLE 3 Continued
Great ape
species or
subspecies
Primary
food
system
Main crops
concern for
expansion
or foraging
Key strategies
to facilitate
coexistence
finance, yield
increases
Grauer’s
Gorilla
Rural and
Traditional Beans
Yield increases,
produce and
protect, threat
management and
finance
Mountain
Gorilla
Rural and
Traditional
Beans,
vegetables, fruit
Eco-tourism,
payment for
biodiversity,
community
engagement
Northwest
Bornean
orangutan
Informal and
Expanding
Oil palm, tree
crops, rice
Produce and
protect, threat
management and
finance
Southwest
Bornean
orangutan
Informal and
Expanding
Oil palm, tree
crops, rice
Produce and
protect, threat
management and
finance
Northeast
Bornean
orangutan
Modernizing
and
Formalizing
Oil palm
Key stakeholders
and jurisdictional
approach, produce
and protect
Sumatran
Orangutan
Informal and
Expanding Oil palm, rice
Produce and
protect, threat
management and
finance
Tapanuli
Orangutan
Informal and
Expanding Fruit, rice
Produce and
protect, threat
management and
finance
Food systems in Democratic Republic Congo and Central African Republic are assumed to be
Rural and Traditional. For food system description see Table S8.
FIGURE 4
An adult male chimpanzee at Bossou in Guinea crossing a village homestead having foraged on a papaya fruit. Reprinted with permission from
Kimberley Hockings (Cantanhez Chimpanzee Project).
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consumption, and the environment. Plans should respect human
rights and balance agricultural development with conservation in
each priority area. They should assess crops and ecosystems,
production scale and methods (Jansen et al., 2020). Smallholder
agriculture, which dominates much of great ape habitat, can be
challenging to regulate, and new financial models are needed to
facilitate change among smallholders. An effective approach could
focus on food systems rather than crops themselves (Marshall et al.,
2021)(Figure 6) and the transformations these systems are
undergoing (Dornelles et al., 2022). To diversify food systems,
nutrient-rich legumes, pulses, horticulture crops, and livestock
may be introduced. Investing in rural market infrastructure
enables smallholders to commercialize and improve the
availability of perishable products (Abraham and Pingali, 2020).
Different food systems offer different transformation pathways,
either in an agroecological direction based on the redesign and
FIGURE 5
Theory of Change and structure of Discussion.
B
CD
A
FIGURE 6
Example of different primary food systems with great apes. (A) Rural and traditional; smallholder farm area in Sierra Leone near Gola Rainforest
National Park. Google Earth image © 2023 Maxar Technologies and © 2023 CNES/Airbus; (B) Informal and expanding: farm area to the north of
Bwindi Impenetrable Forest, Uganda Google Earth image © 2023 CNES/Airbus and © 2023 Maxar Technologies; (C) Emerging and diversifying; new
oil palm development in Gabon in areas with chimpanzee and western gorilla populations. Google Earth image © Landsat/Copernicus; (D)
Modernizing and formalizing: Lower Kinabatangan area in Sabah, Malaysia where 800 orangutans live in forest fragments surrounded by industrial-
scale oil palm. Google Earth image © 2023 Maxar Technologies and © 2023 CNES/Airbus.
Meijaard et al. 10.3389/fcosc.2023.1225911
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diversification of agroecosystems or following Fourth Industrial
Revolution pathways characterized by new technologies
(Pimbert, 2022).
Government, farmers, industry, financial institutions, scientists,
and civil society must collaborate for food system transformation.
They should identify areas where the costs of agricultural
conversion outweigh the benefits, considering environmental,
social, and economic factors. Evaluating ecosystems’economic,
environmental, and social value before development is crucial.
This includes assessing potential agricultural revenues and socio-
political dynamics. Trade agreements and international finance are
vital policy tools. Great apes play a key role in Performance
Standard 6 of the International Finance Corporation, linking
finance to conservation outcomes and avoiding negative impacts
on apes. Priority great ape areas must be protected, and
conservation organizations should engage stakeholders to
establish “no-go”development zones based on factors such as
food security and the importance of these areas for great ape
populations (Ancrenaz et al., 2016). The World Bank and other
financing entities adhere to these standards, allowing projects in
great ape habitats only in exceptional circumstances.
Planning and implementation at the landscape scale is vital for
great ape survival in human-dominated habitats. Orangutan
populations are maintained in some oil palm concessions in
Indonesia and Malaysia with selected areas of protected forest
from a few hundred to several thousand hectares connected by
forest corridors and riparian areas (Ancrenaz et al., 2015). Similarly,
in Gabon, populations of chimpanzees and Western gorillas are
maintained in areas of forest within an oil palm concession
(Ancrenaz et al., 2016). Preliminary studies indicate that both
orangutans and chimpanzees retain dispersal dynamics in
fragmented landscapes that mirror those in large forests (i.e.,
female dispersal in chimpanzees and male dispersal in
orangutans), as long as they are not hunted (McCarthy et al.,
2018;Ancrenaz et al., 2021), and that the presence of corridors
and small patches in the agricultural matrix likely increases
population viability in orangutans (Seaman et al., 2021;Seaman
et al., 2023).
4.1.1 Yield increases
Increasing productivity on existing agricultural lands can
reduce the need for expansion (Zhang et al., 2021), but closing
yield gaps for food security is challenging, potentially leading to
more land expansion unless local demand is met by imports (van
Ittersum et al., 2016). Boosting productivity through reduced fallow
duration, multiple cropping, early-maturing varieties,
intercropping, catch crops, and enhanced irrigation offers the
largest potential for production increases (Poore and Nemecek,
2018). Furthermore, as productivity increases so do agricultural
land rents, which could create new incentives for agricultural
expansion and deforestation (Phelps et al., 2013). However, rising
productivity in pre-established agricultural areas can attract local
immigration away from vulnerable frontiers, promoting land
sparing and nature conservation (Laurance et al., 2009;Laurance
et al., 2015). Technological advances in established agricultural
lands can help reduce deforestation if increased supply lowers
market prices (Angelsen and Kaimowitz, 2001). This aligns with
the Borlaug hypothesis –i.e., improvements in agricultural
technology will enable farmers to produce more food from a
given piece of land, thereby enabling growth in food supply
without leading to increased deforestation –and the experience of
the Green Revolution (Stevenson et al., 2013). Non-expansion and
abandonment of marginal agricultural lands on the forest frontier
are crucial for ‘forest transition’processes, i.e., the stabilization or
even increase of forest cover at high levels per-capita income
(Mather and Needle, 1998;Meyfroidt and Lambin, 2011).
4.1.2 Produce-and-protect strategies
Another strategy could be to combine both policy tools –i.e., on
the one hand land-use planning of ‘no-go’conservation reserves on
forest land with poor agricultural potential, and on the other
improving agricultural yields on already cultivated land (Zhang
et al., 2021). Such ‘produce-and-protect’type of strategies of
combining land-sparing agriculture with protected areas and
private reserves for the provision of biodiversity services,
indigenous lands and other actively enforced protection strategies
may also be the most promising pathways for meeting the goals of
great ape conservation and food production (Hanson and
Ranganathan, 2022). Their attractive element is above all in their
mutually reinforcing effects. On the one hand, effectively closing the
agricultural frontier hampers land extensification and is inducive to
the adoption of land-saving technologies that can increase producer
incomes. Conversely, protecting land areas from crop expansion is
easier when supply of the same crop is increasing and prices are not,
thus counteracting any ‘leakage’of forest pressures from the newly
protected area to elsewhere (Meyfroidt et al., 2020).
Robust governance and increasing conservation incentives can
help ensure land sparing, but implementation of these strategies
may require tracking future agricultural land rents (Phelps et al.,
2013) and targeting development planning away from core great
ape areas (e.g., avoiding road building into or through priority
habitats). This can stimulate economic growth and draw people
away from frontier areas while increasing the value of natural
ecosystems. Targeting development far from priority great ape
areas makes sense as impacts on biodiversity are most severe in
the earliest stages of agricultural expansion, especially when
conversion occurs in forest interiors (Chaplin-Kramer et al.,
2015). Conservation organizations should collaborate with
governments and industry partners to build consensus about “no-
go”areas for development based on the presence of priority great
ape populations and other high-risk factors.
4.1.3 Food forests, regenerative agriculture
and agroforestry
Improved agricultural methods are needed that reduce soil
degradation and other negative environmental impacts and
provide potential for climate solution (Terasaki Hart et al., 2023).
This includes the increased use of agroforestry systems, which are
thought to be more resilient than monocultures of annual crops
(Mbow et al., 2014) and nitrogen-fixing legumes which increase soil
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fertility and reduce fertilizer needs and run-off (Roupsard et al.,
2020). Agroforestry systems and perennial crops may also increase
great ape dispersal between forest fragments as recorded in
orangutans and chimpanzees. Mixing crops and forest patches
does not necessarily reduce yields, because forests provide
ecological benefits to surrounding agriculture that improves
nearby yields, as demonstrated in Indonesian oil palm (Zemp
et al., 2023). Many food forests are not yet economically viable
but could be if other income could be generated from ecosystem
services (Albrecht and Wiek, 2021).
4.1.4 Threat management and finance
Threat prevention strategies for great ape conservation require
sustained external funding, which can come from various sources
such as nature-based tourism (Maekawa et al., 2013) or funding
from industry (Larson et al., 2021). Increased investment in
patrolling and law enforcement, as well as the presence of civil
society organizations, can help reduce pressure on great ape
populations and habitats. To achieve this, there need to be new
species action plans that call for a significant increase in and
reallocation of conservation funding. Increasing the market value
of biodiversity and allowing this to finance conservation services
from nearby rural communities is one way to close the funding gap,
while ensuring that funds end up where decisions about great apes
are made (Ledgard and Meijaard, 2021;Fergus et al., 2023). The
engagement of the private sector in conservation is another way to
increase investment into biodiversity conservation, such as through
offsetting biodiversity impacts or managing and maintaining species
habitats (Bull and Strange, 2018). For example, palm oil certified
through the Roundtable on Sustainable Palm Oil requires that areas
of high conservation value are protected and values retained (RSPO,
2018). Effective management of great ape populations requires
funding, manpower, and infrastructure which many companies
have access to, but do not necessarily possess the knowledge to
implement evidence-based conservation strategy. Furthermore,
facilitating collaboration between industrial-scale operators and
smallholders, such as has been attempted in the palm oil
industry, can speed up knowledge transfer and increase yields
for smallholders.
Increased funding is not enough. Efficient allocation of funds to
more effective interventions is crucial. One billion USD allocated
over 20 years to orangutan conservation was insufficient to stop
their decline, probably due to inefficient allocation of funds (Santika
et al., 2022). In summary, great ape conservation efforts require
sustained external funding input and efficient allocation of funds to
effective interventions. Increased investment in patrolling and law
enforcement, preferably with the involvement of local communities,
as well as the engagement of the private sector in conservation, can
help achieve conservation goals. However, it is important to ensure
that funds end up where ultimate decisions are made about great
ape survival and that conservation efforts address not only habitat
protection but also the safety of great apes from hunting, poaching,
and disease. Evidence-based conservation is needed to investigate
and determine what solutions will be most effective in different
contexts local situations (Junker et al., 2020).
4.1.5 Key stakeholders and
jurisdictional approach
Respecting human rights and effective engagement and
motivation of communities living in proximity to great apes, in
addition to earlier mentioned financial benefits, is essential for
successful conservation (Chua et al., 2020;Bettinger et al., 2021).
This needs to address the key question of what communities can
gain from participating in conservation programs, and if they
can help guide goals, planning and execution, i.e. “Whose
Conservation”(see, e.g., Kaimowitz and Sheil, 2007;Mace, 2014).
Engaging communities in conservation planning alongside broader
village development planning could ensure that conservation
objectives become integral to these broader plans (Vermeulen and
Sheil, 2007;Meijaard et al., 2022b). Considerable experience exists
in exploring, developing and implementing such initiatives (Lynam
et al., 2007;Margules et al., 2020). The opportunities are generally
greater than is assumed (Padmanaba and Sheil, 2007;Vermeulen
and Sheil, 2007) as local people will often have goals and interests of
their own that overlap with those of conservationists (Sheil et al.,
2006;Chua et al., 2020). Working together to identify and achieve
locally defined goals can be a useful means to build trust, reduce
conflict and build a consensus towards addressing wider
conservation goals (Sayer et al., 2013;Sheil et al., 2017). This
could overcome the current problem that provisions for great ape
conservation are often written by people who have little connection
to or understanding of the livelihood strategies and patterns of
indigenous communities (Chua et al., 2020).
4.2 Alternative income to avoid land
competition with great apes
Achieving direct and immediate benefits for people who are
asked to live side-by-side with great apes, for example through
ecotourism (Robbins, 2021) or payments for conservation services
(Ledgard and Meijaard, 2021;Fergus et al., 2023), could encourage
more positive perceptions regarding apes that are becoming
accustomed to human-dominated landscapes (Chua et al., 2020).
4.2.1 Eco-tourism
Eco-tourism provides a potential solution for achieving poverty
eradication and conservation goals for communities facing
imminent threats of agricultural expansion. The successful
conservation of mountain gorillas has been largely funded by
nature-based tourism (Maekawa et al., 2013), but this has also
resulted in increased negative interactions between habituated
gorillas and local communities (Hill, 2005;Seiler and Robbins,
2015;Robbins, 2021), highlighting the complexity of eco-tourism
contexts. Nevertheless, the value of nature-based tourism to
countries such as Rwanda is high with tourism accounting for
23%of export earnings in 2020 (World Bank and Government of
Rwanda, 2020) and mountain gorillas alone accounting for 2% of
GDP in 2023. In Borneo, eco-tourism businesses also contribute
significantly to regional income (Goh and Potter, 2023), but scaling
up tourism to cover the entire range of Bornean orangutan is
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challenging and may result in lower prices due to increased
competition. While nature-based tourism can benefit great apes
and local communities, it is unlikely to positively influence
significant parts of the great apes’range soon. The pandemic and
the associated travel restrictions and periodic suspension of great
ape visits have revealed the over-dependency on tourism (Ezra et al.,
2021). Alternative financial mechanisms are needed to provide a
safety net for communities when tourism does not bring in the
much-needed resources.
4.2.2 Payment for biodiversity
Often the people who live with great apes see few economic
benefits.Asanexample,aroundBwindiImpenetrableForest
National Park, communities living within 0.5km of the boundaries
are significantly poorer and are more affected by wild crop foraging
animals than those living further away (Twinamatsiko et al., 2014).
Conservation efforts, particularly the management of national parks,
have historically exacerbated rural poverty by restricting access to
forest resources, fining for minor acts and the loss of crops and
livestock to protected wildlife (Blomley et al., 2010). Improved
compensation schemes for conservation are therefore needed to
finance the conservation of great apes and provide financial
benefits to those living alongside them.
Developing payment for ecosystem services (PES) programs
that financially incentivize local communities to conserve critical
forested areas for great ape survival could be a potential approach
(Wunder, 2005). To jumpstart financing for great ape conservation,
compensation schemes for conservation could be combined with
carbon credit schemes. To tackle this issue, a nested approach can
be employed, incorporating carbon credits into a larger
conservation project that encompasses biodiversity preservation
and additional ecosystem services. (Law et al., 2012). The
conservation project can generate carbon credits that can finance
the broader conservation activities (but see West et al., 2023). The
revenue generated can be used to compensate communities living
with great apes or to restore degraded great ape habitat (Darusman
et al., 2021). This approach can ensure that both biodiversity and
carbon sequestration goals are achieved, and local communities
benefit from conservation efforts.
One potential strategy is to establish fair and transparent
compensation mechanisms to offset the costs that communities
incur from living alongside great apes, such as damage to crops and
livestock. Compensation programs can provide financial or material
support to alleviate the economic losses inflicted by great apes, thus
reducing conflicts between humans and wildlife and increasing the
likelihood of coexisting with great apes in the long term. These
programs can be supported by various sources, including
conservation groups, government entities, and concerned private
sector entities. Once such compensation schemes are established,
they may need to remain in place indefinitely, and we acknowledge
that running fair and transparent compensation schemes in many
ape range countries would be a huge challenge.
Biocredits have emerged as an economic instrument to
incentivize conservation in remote areas with great apes (Porras
and Steele, 2020). Similar to carbon credits, they generate revenue
by selling units of biodiversity resulting from improved
conservation actions; how these units will be defined, measured
and verified is yet unclear. Once this is resolved, biocredits can be
purchased by government bodies, philanthropic organizations, and
private companies. German companies have already expressed
interest in purchasing biocredits for conservation through an
online marketplace (Krause and Matzdorf, 2019). These
mechanisms provide direct financial contributions to conservation
organizations and communities, supporting initiatives like citizen
science monitoring and tree planting. The use of biocredits
for direct payments to individuals,communities,andlocal
conservation managers is still limited but shows promise for the
future (Community Conservation Namibia, 2023).
Interspecies Money is a proposed system designed to collect
data on various species, provide them with a unique digital identity
and digital wallets, and allocate based on the importance to
conservation (Ledgard, 2022). Recent technological advancements,
including low-cost sensors, drones, camera traps, bioacoustics,
eDNA sampling, and artificial intelligence, enable data collection
and analysis of population trends in their habitats (Ledgard and
Kharas, 2022). This data-driven approach allows for the
distribution of Interspecies Money based on conservation
outcomes (increased abundance based on human behavior, e.g., a
local farmer not cutting down a tree or not harming a great
ape). This approach aims to simplify conservation finance,
allowing easier upscaling and reducing the reliance on
conservation organizations or governments. However, successful
implementation requires redefining economic rules and piloting
projects in natural settings to assess feasibility and effectiveness
(Ledgard, 2022). The approach is being piloted in Rwanda.
4.3 Rethinking agriculture and
food systems
4.3.1 Modifying global consumption and
local agriculture
To address deforestation and protect great apes, requires
understanding the consumption dynamics and underlying causes
of agricultural expansion. Palm oil, for example, satisfies a
significant portion of global vegetable oil demand (FAOSTAT,
2022), but reducing its use requires a shift in global consumption
patterns (Goh, 2016;Meijaard and Sheil, 2019). Efforts to reduce
reliance on palm oil must also consider potential adverse impacts on
other regions and conservation efforts (Meijaard et al., 2020).
Protecting great apes within the context of modern agriculture
necessitates a comprehensive approach that considers the complex
factors driving agricultural expansion, including internationally
traded cash crops like cocoa, coffee, and oil palm. While a radical
change in global consumption patterns solely for great ape
protection is unlikely, efforts should be tied to larger issues such
as climate change.
Promoting dietary changes within local communities can help
reduce the demand for food production that destroys great ape
habitats (Abraham and Pingali, 2020), as do reductions in food
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org13
losses through improved storage and transportation. However,
balancing conservation efforts with the food security of these
communities presents a major challenge. Subsistence agriculture
is vital for many people living in great ape regions, and altering their
dietary choices and agricultural practices can have significant
economic implications. Cultural and social barriers further
complicate the process, requiring time and effort to implement
changes. Education and capacity building programs can help
transition local food systems to more sustainable practices. Such
interventions must be approached with caution as they involve
changing traditional ways of life.
4.3.2 Consumers’awareness
There is an important role of consumers in putting pressure on
retailers, producers and governments to ensure that the products
they use are not associated with the loss of great apes and their
habitats, or more generally, with the loss of biodiversity in tropical
habitats. Currently, there is some consumer awareness about the
environmental impacts of palm oil production on orangutans (e.g.,
Ostfeld et al., 2019), but much less so about, for example, chocolate
consumption and chimpanzees. Providing consumers with fact-
based and transparent information, e.g., through labelling
processes, about the impact of the production rice, cassava,
peanut, cacao and other crops in great apes’ranges would give
them a more informed choice and an ability to influence markets
and land-use decision-making (Meijaard and Sheil, 2019). The
European Union’s New Deforestation Regulation, although
criticized by tropical producing countries such as Indonesia and
Malaysia, provides a tool for consumers to differentiate products
not on what they contain (e.g., a no-palm oil label) but rather as to
how ingredients were produced (“great ape safe”or “deforestation
free”). Also verified sustainable production practices such as those
certified under the Roundtable on Sustainable Palm Oil can give
consumers a more informed choice.
5 Conclusion
Great apes face significant threats from agriculture driven by
poverty and demand for agricultural resources. Ensuring
coexistence between great apes and people is of paramount
importance, particularly considering that most great apes live
outside protected areas. However, the challenge lies in the fact
that on average each great ape shares its distribution range with
approximately 100 people. Achieving successful coexistence
requires significant incentives and efforts to protect and preserve
these conservation flagships. New financial models are needed that
can more easily be scaled up and attract =more investment.
Optimized land use planning, guided by strategic investments in
agricultural development and wildlife conservation, can maximize
synergies between conservation and food production goals. It is vital
to support effective economic development policies, enforce forest
conservation and environmental laws, engage in trade policy
discussions, and link policies on trade, food security, improved
agricultural techniques, and sustainable food systems with forest
and great ape impact monitoring. The global agenda should focus
on closing crop yield gaps, promoting healthier diets, reducing food
loss and waste, and allocating more research funding to address the
challenges of great ape and human coexistence.
Author contributions
EM, RD, MA, SWi and DS contributed to conception and
design of the study. NU, TA and RD organized the database and
spatial analysis of crop and other data. JS developed the causal
change diagrams. EM wrote the first draft of the manuscript. KH,
SWu, CG, MO, JL, JR, and DS wrote sections of the manuscript. All
authors contributed to manuscript revision, read, and approved the
submitted version.
Funding
Work was supported via a grant from UNEP GRASP (SSFA/
2021/4079) and a grant from UNEP under the GEF funded Congo
Basin Impact Program (PCA/2022/5067) and the Darwin Initiative
(grant number, 26-018) to KH.
Conflict of interest
EM, NU, TA, RD and MA were employed by Borneo Futures.
EM declares that he co-chairs the IUCN Oil Crops Task Force
that studies oil crops. He has received funding from palm oil
producing companies and the Roundtable on Sustainable Palm
Oil, which could be construed as a potential conflict of interest.
The remaining authors declare that the research was conducted
in the absence of any commercial or financial relationships that
could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at:
https://www.frontiersin.org/articles/10.3389/fcosc.2023.1225911/
full#supplementary-material
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org14
References
Abraham, M., and Pingali, P. (2020). “Transforming smallholder agriculture to achieve
the SDGs,”in The Role of Smallholder Farms in Food and Nutrition Security.Eds.S.G.Y.
Paloma, L. Riesgo and K. Louhichi (Cham, Switzerland: Springer), 173–191.
Ajanaku, B. A., and Collins, A. R. (2021). Economic growth and deforestation in
African countries: Is the environmental Kuznets curve hypothesis applicable? For.
Policy Economics 129, 102488. doi: 10.1016/j.forpol.2021.102488
Akpabio, E. M. (2007). Assessing integrated water resources management in Nigeria:
insights and lessons from irrigation projects in the Cross River Basin. Water Policy 9,
149–168. doi: 10.2166/wp.2007.007
Albrecht, S., and Wiek, A. (2021). Food forests: Their services and sustainability.
J. Agriculture Food Systems Community Dev. 10, 91–105. doi: 10.5304/jafscd.2021.103.014
Ancrenaz, M., Meijaard, E., Wich, S. A., and Simery, J. (2016). Palm oil paradox.
Sustainable solutions to save the great apes. (Nairobi, Kenya: UNEP/GRASP).
Ancrenaz, M., Oram, F., Ambu, L., Lackman, I., Ahmad, E., Elahan, H., et al. (2015).
Of pongo, palms, and perceptions –A multidisciplinary assessment of orangutans in an
oil palm context. Oryx 49, 465–472. doi: 10.1017/S0030605313001270
Ancrenaz, M., Oram, F., Nardiyono,, Silmi, M., Jopony, M. E. M., Voigt, M., et al.
(2021). Importance of orangutans in small fragments for maintaining metapopulation
dynamics. Front. Forests Global Change 4, 560944.
Angelsen, A., and Kaimowitz, D. (2001). Agricultural technologies and tropical
deforestation. (Bogor, Indonesia: CIFOR).
Antony Ceasar, S., and Maharajan, T. (2022). The role of millets in attaining United
Nation’s sustainable developmental goals. PLANTS PEOPLE PLANET 4, 345–349. doi:
10.1002/ppp3.10254
Balmford, A. (2021). Concentrating vs. spreading our footprint: how to meet
humanity’s needs at least cost to nature. J. Zoology 315, 79–109. doi: 10.1111/jzo.12920
Bergl,R.A.,Bradley,B.J.,Nsubuga,A.,andVigilant,L.(2008).Effectsofhabitat
fragmentation, population size and demographic history on genetic diversity: the cross river
gorilla in a comparative context. Am.J.Primatology70, 848–859. doi: 10.1002/ajp.20559
Bersacola, E., Hill, C. M., and Hockings, K. J. (2021). Chimpanzees balance resources
and risk in an anthropogenic landscape of fear. Sci. Rep. 11, 4569. doi: 10.1038/s41598-
021-83852-3
Bettinger, T., Cox, D., Kuhar, C., and Leighty, K. (2021). Human engagement and
great ape conservation in Africa. Am. J. Primatology 83, e23216. doi: 10.1002/ajp.23216
Blomley, T., Namara, A., McNeilage, A., Franks, P., Rainer, H., Donaldson, A., et al. (2010 ).
Development AND Gorillas? Assessing fifteen years of integrated conservation and
development in south-western Uganda (London, UK: Natural Resource Issues (23). IIED).
Brncic, T., Amarasekaran, B., McKenna, A., Mundry, R., and Kühl, H. S. (2015).
Large mammal diversity and their conservation in the human-dominated land-use
mosaic of Sierra Leone. Biodiversity Conserv. 24, 2417–2438. doi: 10.1007/s10531-015-
0931-7
Bruford, M. W., Ancrenaz, M., Chikhi, L., Lackman-Ancrenaz, I., Andau, M., Ambu,
L., et al. (2010). Projecting genetic diversity and population viability for the fragmented
orang-utan population in the Kinabatangan floodplain, Sabah, Malaysia. Endangered
Species Res. 12, 249–261. doi: 10.3354/esr00295
Bull, J. W., and Strange, N. (2018). The global extent of biodiversity offset
implementation under no net loss policies . Nat. Sustainability 1, 790 –798. doi:
10.1038/s41893-018-0176-z
Busch, J., and Ferretti-Gallon, K. (2017). What drives deforestation and what stops it?
A meta-analysis. Rev. Environ. Economics Policy 11, 3–23. doi: 10.1093/reep/rew013
Byerlee, D., Stevenson, J., and Villoria, N. (2014). Does intensification slow crop land
expansion or encourage deforestation? Global Food Secur. 3, 92–98. doi: 10.1016/
j.gfs.2014.04.001
Caccamisi, D. S. (2010). Cassava: global production and market trends. Chronica
Hortic. 50, 15–18.
Caldecott, J., and Miles, L. (2006). World Atlas of Great Apes and their Conservation
(Cambridge, UK: UNEP World Conservation Monitoring Centre).
Campbell-Smith, G., Campbell-Smith, M., Singleton, I., and Linkie, M. (2011).
Raiders of the lost bark: orangutan foraging strategies in a degraded landscape.
PloSONE 6, e20962. doi: 10.1371/journal.pone.0020962
Campbell-Smith, G., Sembiring, R., and Linkie, M. (2012). Evaluating the
effectiveness of human-orangutan conflict mitigation strategies in Sumatra. J. Appl.
Ecol. 49, 367–375. doi: 10.1111/j.1365-2664.2012.02109.x
Carter, N. H., and Linnell, J. D. C. (2016). Co-adaptation is key to coexisting with
large carnivores. Trends Ecol. Evol. 31, 575–578. doi: 10.1016/j.tree.2016.05.006
Chaplin-Kramer, R., Sharp, R. P., Mandle, L., Sim, S., Johnson, J., Butnar, I., et al.
(2015). Spatial patterns of agricultural expansion determine impacts on biodiversity
and carbon storage. Proc. Natl. Acad. Sci. 112, 7402–7407. doi: 10.1073/
pnas.1406485112
Chua, L., Harrison, M., Cheyne, S., Fair, H., Milne, S., Palmer, A., et al. (2020).
Conservation and the social sciences: beyond critique and co-optation. A case study
from orangutan conservation. People Nat. 2, 42–60. doi: 10.1002/pan3.10072
Cincotta, R. P., Wisnewski, J., and Engelman, R. (2000). Human population in the
biodiversity hotspots. Nature 404, 990–992. doi: 10.1038/35010105
Community Conservation Namibia (2023) Wildlife Credits, an incentive to conserve.
Available at: https://wildlifecredits.com/how-we-work (Accessed 15 May 2023).
Darusman, T., Lestari, D. P., and Arriyadi, D. (2021). “Management practice and
restoration of the peat swamp forest in Katingan-Mentaya, Indonesia,”in Tropical
Peatland Eco-management. Eds. M. Osaki, N. Tsuji, N. Foead and J. Rieley (Singapore:
Springer Singapore), 381–409.
Dornelles, A. Z., Boonstra, W. J., Delabre, I., Denney, J. M., Nunes, R. J., Jentsch, A.,
et al. (2022). Transformation archetypes in global food systems. Sustainability Sci. 17,
1827–1840. doi: 10.1007/s11625-022-01102-5
Dudley, N., and Alexander, S. (2017). Agriculture and biodiversity: a review.
Biodiversity 18, 45–49. doi: 10.1080/14888386.2017.1351892
Duffy,C.,Toth,G.G.,Hagan,R.P.O.,McKeown,P.C.,Rahman,S.A.,
Widyaningsih, Y., et al. (2021). Agroforestry contributions to smallholder farmer
food security in Indonesia. Agroforestry Syst. 95, 1109–1124. doi: 10.1007/s10457-021-
00632-8
Ekpa, O., Palacios-Rojas, N., Kruseman, G., Fogliano, V., and Linnemann, A. R.
(2019). Sub-saharan african maize-based foods - processing practices, challenges and
opportunities. Food Rev. Int. 35, 609–639. doi: 10.1080/87559129.2019.1588290
Erenstein, O., Jaleta, M., Sonder, K., Mottaleb, K., and Prasanna, B. M. (2022). Global
maize production, consumption and trade: trends and R&D implications. Food
Security. 14, 1295–1319. doi: 10.1007/s12571-022-01288-7
Ezra, P., Kitheka, B., Sabuhoro, E., Riungu, G., Sirima, A., Amani, A., et al. (2021).
Responses and impacts of COVID-19 on east Africa’s tourism industry. Afr. J.
Hospitality Tourism Leisure 10, 1711–1727. doi: 10.46222/ajhtl.19770720.188
Fahy, G. E., Richards, M., Riedel, J., Hublin, J.-J., and Boesch, C. (2013). Stable
isotope evidence of meat eating and hunting specialization in adult male chimpanzees.
Proc. Natl. Acad. Sci. 110, 5829–5833. doi: 10.1073/pnas.1221991110
FAOSTAT (2022). Food and agriculture data (Rome, Italy: The Food and Agriculture
Organization (FAO).
FAOSTAT (2023). Crops and livestock products (Rome, Italy: Food and Agriculture
Organization of the United Nations). Available at: https://www.fao.org/faostat/en/#data/QCL.
Fergus, P., Chalmers, C., Longmore, S., Wich, S., Warmenhove, C., Swart, J., et al.
(2023). Empowering wildlife guardians: an equitable digital stewardship and reward
system for biodiversity conservation using deep learning and 3/4G camera traps.
Remote Sens. 15, 2730. doi: 10.3390/rs15112730
Fletcher, S. M., and Shi, Z. (2016). “Chapter 10 - an overview of world peanut markets,”in
Peanuts.Eds.H.T.StalkerandR.F.Wilson(Cambridge,MA,USA:AOCSPress),267–287.
Garcia, C. A., Savilaakso, S., Verburg, R. W., Gutierrez, V., Wilson, S. J., Krug, C. B.,
et al. (2020). The global forest transition as a human affair. One Earth 2, 417–428. doi:
10.1016/j.oneear.2020.05.002
Garriga, R. M., Marco, I., Casas-Dıaz, E., Amarasekaran, B., and Humle, T. (2018).
Perceptions of challenges to subsistence agriculture, and crop foraging by wildlife and
chimpanzees Pan troglodytes verus in unprotected areas in Sierra Leone. Oryx 52, 761–
774. doi: 10.1017/S0030605316001319
Gaveau, D. L. A., Locatelli, B., Descals, A., Manurung, T., Salim, M. A., Husnayen,,
et al. (2022). Slowing oil palm expansion and deforestation in Indonesia coincide with
low oil prices. PloS One 17, e0266178. doi: 10.1371/journal.pone.0266178
Gaveau, D. L. A., Locatelli, B., Salim, M. A., Yaen, H., Pacheco, P., and Sheil, D.
(2019). Rise and fall of forest loss and industrial plantations in Borneo, (2000–2017).
Conserv. Lett. 12, e12622. doi: 10.1111/conl.12622
Giller, K. E. (2020). The food security conundrum of sub-saharan Africa. Global Food
Secur. 26, 100431. doi: 10.1016/j.gfs.2020.100431
Goh, C. S. (2016). Can we get rid of palm oil? Trends Biotechnol. 34, 948–950.
doi: 10.1016/j.tibtech.2016.08.007
Goh, C. S., and Potter, L. (2023). Transforming Borneo: From Land Exploitation to
Sustainable Development (Singapore: ISEAS–Yusof Ishak Institute Singapore).
Grant, M. J., and Booth, A. (2009). A typology of reviews: an analysis of 14 review
types and associated methodologies. Health Inf. Libraries J. 26, 91–108. doi: 10.1111/
j.1471-1842.2009.00848.x
Halloran, A. R. (2016). “The many facets of human disturbances at the tonkolili
chimpanzee site,”in Ethnoprimatology: Primate Conservation in the 21st Century. Ed.
M. T. Waller (Cham: Springer International Publishing), 273–281.
Halpern, B. S., Frazier, M., Verstaen, J., Rayner, P.-E., Clawson, G., Blanchard, J. L.,
et al. (2022). The environmental footprint of global food production. Nat. Sustainability
5, 1027–1039. doi: 10.1038/s41893-022-00965-x
Hanson, C., and Ranganathan, J. (2022). How to Manage the Global Land
Squeeze? Produce, Protect, Reduce, Restore (Washington DC: World Resources
Institute (WRI).
Harihar, A., Chanchani, P., Sharma, R. K., Vattakaven, J., Gubbi, S., Pandav, B., et al.
(2013). Conflating “co-occurrence”with “coexistence”.Proc. Natl. Acad. Sci. 110, E109–
E109. doi: 10.1073/pnas.1217001110
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org15
Heinicke, S., Mundry, R., Boesch, C., Amarasekaran, B., Barrie, A., Brncic, T., et al.
(2019). Characteristics of positive deviants in western chimpanzee populations. Front.
Ecol. Evol. 7. doi: 10.3389/fevo.2019.00016
Hengl,T.,Miller,M.A.E.,Kriz
an,J.,Shepherd,K.D.,Sila,A.,Kilibarda,M.,etal.(2021).
African soil properties and nutrients mapped at 30 m spatial resolution using two-scale
ensemble machine learning. Sci. Rep. 11, 6130. doi: 10.1038/s41598-021-85639-y
Hill, C. M. (2005). “People, crops and primates: a conflict of interests,”in Primate
commensalism and conflict. Eds. J. D. Paterson and J. Wallis. (American Society of
Primatologists). 41–59.
Hill, C. M. (2017). Primate crop feeding behavior, crop protection, and conservation.
Int. J. Primatology 38, 385–400. doi: 10.1007/s10764-017-9951-3
Hockings, K. J., Anderson, J. R., and Matsuzawa, T. (2009). Use of wild and cultivated
foods by chimpanzees at Bossou, Republic of Guinea: feeding dynamics in a human-
influenced environment. Am. J. Primatology 71, 636–646. doi: 10.1002/ajp.20698
Hockings, K., and Humle, T. (2009). Best Practice Guidelines for the Prevention and
Mitigation of Conflict Between Humans and Great Apes (Gland, Switzerland: IUCN
SSC Primate Specialist Group).
Hockings, K. J., and McLennan, M. R. (2012). From forest to farm: systematic review
of cultivar feeding by chimpanzees –management implications for wildlife in
anthropogenic landscapes. PloS One 7, e33391. doi: 10.1371/journal.pone.0033391
Hockings, K. J., McLennan, M. R., Carvalho, S., Ancrenaz, M., Bobe, R., Byrne, R. W.,
et al. (2015). Apes in the Anthropocene: flexibility and survival. Trends Ecol. Evol. 30,
215–222. doi: 10.1016/j.tree.2015.02.002
Hulme, M. F., Vickery, J. A., Green, R. E., Phalan, B., Chamberlain, D. E., Pomeroy,
D. E., et al. (2013). Conserving the birds of Uganda’s banana-coffee arc: land sparing
and land sharing compared. PloS One 8, e54597. doi: 10.1371/journal.pone.0054597
Independent Science and Parnership Council (2016). Agricultural Growth Corridors.
Mapping potential research gaps on impact, implementation and institutions (Nairobi,
Kenya: CGIAR, Independent Science and Parnership Council and European Centre for
Development Policy Management).
Jansen, M., Guariguata, M. R., Raneri, J. E., Ickowitz, A., Chiriboga-Arroyo, F.,
Quaedvlieg, J., et al. (2020). Food for thought: The underutilized potential of tropical
tree-sourced foods for 21st century sustainable food systems. People Nat. 2, 1006–1020.
doi: 10.1002/pan3.10159
Jayathilake, H. M., Prescott, G. W., Carrasco, L. R., Rao, M., and Symes, W. S. (2021).
Drivers of deforestation and degradation for 28 tropical conservation landscapes.
Ambio 50, 215–228. doi: 10.1007/s13280-020-01325-9
Junker,J.,Petrovan,S.O.,Arroyo-RodrI
guez, V., Boonratana, R., Byler, D.,
Chapman, C. A., et al. (2020). A severe lack of evidence limits effective conservation
of the world’s primates. BioScience 70, 794–803. doi: 10.1093/biosci/biaa082
Kaimowitz, D., and Sheil, D. (2007). Conserving what and for whom? Why
conservation should help meet basic human needs in the tropics. Biotropica 39, 567–
574. doi: 10.1111/j.1744-7429.2007.00332.x
Kalan, A. K., Kulik, L., Arandjelovic, M., Boesch, C., Haas, F., Dieguez, P., et al.
(2020). Environmental variability supports chimpanzee behavioral diversity. Nat.
Commun. 11, 4451. doi: 10.1038/s41467-020-18176-3
Kormos, R., Boesch, C., Bakarr, M. I., and Butynski, T. M. (2003). West African
Chimpanzees: St atus, Survey and Conservation Action Plan (Gland, Switzerland:
International Union for Conservation of Nature (IUCN) World Conservation Union).
Kottek, M., Grieser, J., Beck, C., Rudolf, B., and Rubel, F. (2006). World Map of the
Köppen-Geiger climate classification updated. Meteorologische Z. 15, 259–263. doi:
10.1127/0941-2948/2006/0130
Krause, M. S., and Matzdorf, B. (2019). The intention of companies to invest in
biodiversity and ecosystem services credits through an online-marketplace. Ecosystem
Serv. 40, 101026. doi: 10.1016/j.ecoser.2019.101026
Kremen, C., and Merenlender, A. M. (2018). Landscapes that work for biodiversity
and people. Science 362, eaau6020. doi: 10.1126/science.aau6020
Krief, S., Berny, P., Gumisiriza, F., Gross, R., Demeneix, B., Fini, J. B., et al. (2017).
Agricultural expansion as risk to endangered wildlife: Pesticide exposure in wild
chimpanzees and baboons displaying facial dysplasia. Sci. Total Environ. 598, 647–
656. doi: 10.1016/j.scitotenv.2017.04.113
Kumar, A., Tomer, V., Kaur, A., Kumar, V., and Gupta, K. (2018). Millets: a solution to
agrarian and nutritional challenges. Agric. Food Secur. 7, 31. doi: 10.1186/s40066-018-0183-3
Larson, L. R., Peterson, M. N., Furstenberg, R. V., Vayer, V. R., Lee, K. J., Choi, D. Y.,
et al. (2021). The future of wildlife conservation funding: What options do U.S. college
students support? Conserv. Sci. Pract. 3, e505. doi: 10.1111/csp2.505
Laso Bayas, J. C., See, L., Georgieva, I., Schepaschenko, D., Danylo, O., Dürauer, M.,
et al. (2022). Drivers of tropical forest loss between 2008 and 2019. Sci. Data 9, 146.
doi: 10.1038/s41597-022-01227-3
Laurance, W. F., Goosem, M., and Laurance, S. G. (2009). Impacts of roads and linear
clearings on tropical forests. Trends Ecol. Evol. 24, 659–669. doi: 10.1016/j.tree.2009.06.009
Laurance, W. F., Sloan, S., Weng, L., and Sayer, J. A. (2015). Estimating the
environmental costs of Africa’s massive “Development corridors”.Curr. Biol. 25,
3202–3208. doi: 10.1016/j.cub.2015.10.046
Law, E. A., Thomas, S., Meijaard, E., Dargusch, P. J., and Wilson, K. A. (2012). A
modular framework for management of complexity in international forest-carbon
policy. Nat. Climate Change 2, 155–160. doi: 10.1038/nclimate1376
Law, E. A., and Wilson, K. A. (2015). Providing context for the land-sharing and
land-sparing debate. Conserv. Lett. 8, 404–413. doi: 10.1111/conl.12168
Ledgard, J. (2022). “Interspecies money,”in Breakthrough: The Promise of Frontier
Technologies for Sustainable Development. Eds. H. Kharas, J. W. Mcarthur and I. Ohno
(Washington, D.C: Brookings Institution Press), 77–102.
Ledgard, J., and Kharas, H. (2022) Financing the preservation of diverse life on Earth
in a capitalist system. Available at: https://www.brookings.edu/blog/future-
development/2022/02/15/financing-the-preservation-of-diverse-life-on-earth-in-a-
capitalist-system/ (Accessed 15 May 2023).
Ledgard, J., and Meijaard, E. (2021). Endangered wildlife should pay for its own
protection. (Project Syndicate). Available at: https://www.project-syndicate.org/
commentary/digital-wallets-for-endangered-wild-animals-by-jonathan-ledgard-1-
and-erik-meijaard-2021-2012.
Lesiv, M., Laso Bayas, J. C., See, L., Duerauer, M., Dahlia, D., Durando, N., et al.
(2019). Estimating the global distribution of field size using crowdsourcing. Global
Change Biol. 25, 174–186. doi: 10.1111/gcb.14492
Linder, J. M. (2013). African primate diversity threatened by “New wave”of
industrial oil palm expansion. Afr. Primates 8, 25–38.
Lynam, T., De Jong, W., Sheil, D., Kusumanto, T., and Evans, K. (2007). A review of
tools for incorporating community knowledge, preferences, and values into decision
making in natural resources management. Ecol. Soc. 12. doi: 10.5751/ES-01987-120105
Mace, G. M. (2014). Whose conservation? Science 345, 1558–1560. doi: 10.1126/
science.1254704
Maekawa, M., Lanjouw, A., Rutagarama, E., and Sharp, D. (2013). Mountain gorilla
tourism generating wealth and peace in post-conflict Rwanda. Natural Resour. Forum
37, 127–137. doi: 10.1111/1477-8947.12020
Margules, C., Boedhihartono, A. K., Langston, J. D., Riggs, R. A., Sari, D. A., Sarkar,
S., et al. (2020). Transdisciplinary science for improved conservation outcomes.
Environ. Conserv. 47, 224–233. doi: 10.1017/S0376892920000338
Marshall, Q., Fanzo, J., Barrett, C. B., Jones, A. D., Herforth, A., and McLaren, R.
(2021). Building a global food systems typology: A new tool for reducing complexity in
food systems analysis. Front. Sustain. Food Syst. 5. doi: 10.3389/fsufs.2021.746512
Masi, S., Chauffour, S., Bain, O., Todd, A., Guillot, J., and Krief, S. (2012). Seasonal
effects on great ape health: A case study of wild chimpanzees and western gorillas. PloS
One 7, e49805. doi: 10.1371/journal.pone.0049805
Mather, A. S., and Needle, C. L. (1998). The forest transition: a theoretical basis. Area
30, 117–124. doi: 10.1111/j.1475-4762.1998.tb00055.x
Matson, P. A., and Vitousek, P. M. (2006). Agricultural intensification: will land
spared from farming be land spared for nature? Conserv. Biol. 20, 709–710. doi:
10.1111/j.1523-1739.2006.00442.x
Mbow, C., Van Noordwijk, M., Luedeling, E., Neufeldt, H., Minang, P. A., and
Kowero, G. (2014). Agroforestry solutions to address food security and climate change
challenges in Africa. Curr. Opin. Environ. Sustainability 6, 61–67. doi : 10.1016/
j.cosust.2013.10.014
McAlpine, C. A., Johnson, A., Salazar, A., Syktus, J., Wilson, K., Meijaard, E., et al.
(2018). Forest loss and Borneo’s climate. Environ. Res. Lett. 13, 044009. doi: 10.1088/
1748-9326/aaa4ff
McCarthy, M. S., Lester, J. D., Langergraber, K. E., Stanford, C. B., and Vigilant, L.
(2018). Genetic analysis suggests dispersal among chimpanzees in a fragmented forest
landscape in Uganda. Am. J. Primatology 80, e22902. doi: 10.1002/ajp.22902
McLennan, M. R. (2013). Diet and Feeding Ecology of Chimpanzees (Pan
troglodytes) in Bulindi, Uganda: Foraging Strategies at the Forest–Farm Interface.
Int. J. Primatology 34, 585–614. doi: 10.1007/s10764-013-9683-y
McLennan, M. R., Hintz, B., Kiiza, V., Rohen, J., Lorenti, G. A., and Hockings, K. J.
(2021). Surviving at the extreme: Chimpanzee ranging is not restricted in a deforested
human-dominated landscape in Uganda. Afr. J. Ecol. 59, 17–28. doi: 10.1111/aje.12803
McLennan, M. R., and Hockings, K. J. (2014). Wild chimpanzees show group
differences in selection of agricultural crops. Sci. Rep. 4, 5956. doi: 10.1038/srep05956
Meijaard, E. (2017). “How a mistaken ecological narrative could be undermining
orangutan conservation,”in Effective Conservation Science: Data Not Dogma. Eds. P.
Kareiva, M. Marvier and B. Silliman (Oxford, UK: Oxford University Press), 90–97.
Meijaard, E., Abrams, J. F., Slavin, J. L., and Sheil, D. (2022a). Dietary fats, human nutrition
and the environment: balance and sustainability. Front. Nutr. 9. doi: 10.3389/fnut.2022.878644
Meijaard, E., Ariffin, T., Unus, N., Dennis, R., Wich, S. A., and Ancrenaz, M. (2021).
Great apes and oil palm in a broader agricultural context. Report by Borneo Futures and
the IUCN Oil Crops Task Force for UNEP/GRASP (Bandar Seri Begawan, Brunei
Darussalam: Borneo Futures and the IUCN Oil Crops Task Force).
Meijaard, E., Brooks, T. M., Carlson, K. M., Slade, E. M., Garcia-Ulloa, J., Gaveau, D.
L. A., et al. (2020). The environmental impacts of palm oil in context. Nat. Plants 6,
1418–1426. doi: 10.1038/s41477-020-00813-w
Meijaard, E., and Sheil, D. (2019). The moral minefield of ethical oil palm and
sustainable development. Front. Forests Global Change 2. doi: 10.3389/ffgc.2019.00022
Meijaard, E., Sheil, D., Sherman, J., Chua, L., Ni’matullah, S., Wilson, K., et al.
(2022b). Restoring the orangutan in a Whole- or Half-Earth context. Oryx 566–577.
doi: 10.1017/S003060532200093X
Meijaard, E., Welsh, A., Ancrenaz, M., Wich, S., Nijman, V., and Marshall, A. J.
(2010). Declining orangutan encounter rates from Wallace to the present suggest the
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org16
species was once more abundant. PlosONE 5, e12042. doi: 10.1371/
journal.pone.0012042
Mercandalli, S., Losch, B., Belebema, M. N., Belières, J.-F., Bourgeois, R., Dinbabo, M.
F., et al. (2019). Rural migration in sub–Saharan Africa: Patterns, drivers and relation to
structural transformation (Rome, Italy: FAO and CIRAD).
Meyfroidt, P., Börner, J., Garrett, R., Gardner, T., Godar, J., Kis-Katos, K., et al.
(2020). Focus on leakage and spillovers: informing land-use governance in a tele-
coupled world. Environ. Res. Lett. 15, 090202. doi: 10.1088/1748-9326/ab7397
Meyfroidt, P., and Lambin, E. F. (2011). Global forest transition: prospects for an end
to deforestation. Annu. Rev. Environ. Resour. 36, 343–371. doi: 10.1146/annurev-
environ-090710-143732
Mukasa, A. N., Woldemichael, A. D., Salami, A. O., and Simpasa, A. M. (2017).
Africa’s agricultural transformation: identifying priority areas and overcoming
challenges. Afr. Economic Brief 8, 1–16.
Mundia, C. W., Secchi, S., Akamani, K., and Wang, G. (2019). A regional comparison
of factors affecting global sorghum production: the case of North America, Asia and
Africa’s Sahel. Sustainability 11, 2135. doi: 10.3390/su11072135
Muthayya, S., Sugimoto, J. D., Montgomery, S., and Maberly, G. F. (2014). An
overview of global rice production, supply, trade, and consumption. Ann. New York
Acad. Sci. 1324, 7–14. doi: 10.1111/nyas.12540
Naughton-Treves, L., Treves, A., Chapman, C. A., and Wrangham, R. W. (1998).
Temporal patterns of crop-raiding by primates: linking food availability in croplands
and adjacent forest. J. Appl. Ecol. 35, 596–606. doi: 10.1046/j.1365-2664.1998.3540596.x
Oram, F., Kapar, M. D., Saharon, A. R., Elahan, H., Segaran, P., Poloi, S., et al. (2022).
“Engaging the Enemy”: Orangutan (Pongo pygmaeus morio) Conservation in Human
Modified Environments in the Kinabatangan floodplain of Sabah, Malaysian Borneo.
Int. J. Primatol 43, 1–28. doi: 10.1007/s10764-022-00288-w
Ordaz-Nemeth, I., Sop, T., Amarasekaran, B., Bachmann, M., Boesch, C., Brncic, T.,
et al. (2021). Range-wide indicators of African great ape density distribution. Am. J.
Primatology 83, e23338. doi: 10.1002/ajp.23338
Ostfeld, R., Howarth, D., Reiner, D., and Krasny, P. (2019). Peeling back the label—
exploring sustainable palm oil ecolabelling and consumption in the United Kingdom.
Environ. Res. Lett. 14, 014001. doi: 10.1088/1748-9326/aaf0e4
Padmanaba, M., and Sheil, D. (2007). Finding and promoting a local conservation
consensusin a globally important tropical forest landscape. Biodiversity Conserv. 16,
137–151. doi: 10.1007/s10531-006-9009-x
Pendrill, F., Gardner, T. A., Meyfroidt, P., Persson, U. M., Adams, J., Azevedo, T.,
et al. (2022). Disentangling the numbers behind agriculture-driven tropical
deforestation. Science 377, eabm9267. doi: 10.1126/science.abm9267
Peter, H., Zuberbühler, K., and Hobaiter, C. (2022). Well-digging in a community of
forest-living wild East African chimpanzees (Pan troglodytes schweinfurthii). Primates
63, 355–364. doi: 10.1007/s10329-022-00992-4
Phalan, B., Onial, M., Balmford, A., and Green, R. E. (2011). Reconciling food
production and biodiversity conservation: land sharing and land sparing compared.
Science 333, 1289–1291. doi: 10.1126/science.1208742
Phelps, J., Ca rrasco, L. R., Webb, E. L., Koh, L. P., and Pas cual, U. (2013).
Agricultural intensification escalates future conservation costs. Proc. Natl. Acad. Sci.
110, 7601–7606. doi: 10.1073/pnas.1220070110
Pimbert, M. P. (2022). Transforming food and agriculture: Competing visions and
major controversies. Mondes en developpement 199-200, 361–384. doi: 10.3917/
med.199.0365
Poore, J., and Nemecek, T. (2018). Reducing food’s environmental impacts through
producers and consumers. Science 360, 987–992. doi: 10.1126/science.aaq0216
Porras, I., and Steele, P. (2020). Biocredits. A solution for protecting nature and
tackling poverty Environmental Economics. Issue Paper February 2020 (London: IIED).
Potapov, P., Turubanova, S., Hansen, M. C., Tyukavina, A., Zalles, V., Khan, A., et al.
(2022). Global maps of cropland extent and change show accelerated cropland expansion in
the twenty-first century. Nat. Food 3, 19–28. doi: 10.1038/s43016-021-00429-z
Rainer, H., White, A., and Lanjouw, A. (2020). State of the Apes. Killing, Capture,
Trade and Conservation (Cambridge, UK: Cambridge University Press).
Rakotoarisoa, M. A., Lafrate, M., and Paschali, M. (2012). Why has Africa become a
Net Food Importer? Explaining Africa Agricultural and Food Trade Deficits (Rome,
Italy: Food and Agriculture Organization).
Ranum, P., Peñ a-Rosas, J. P., and Garcia-Casal, M. N. (2014). Global maize
production, utilization, and consumption. Ann. New York Acad. Sci. 1312, 105–112.
doi: 10.1111/nyas.12396
Robbins, M. M. (2021). Assessing attitudes towards gorilla conservation via
employee interviews. Am. J. Primatology 83, e23191. doi: 10.1002/ajp.23191
Roupsard, O., Audebert, A., Ndour, A. P., Clermont-Dauphin, C., Agbohessou, Y.,
Sanou, J., et al. (2020). How far does the tree affect the crop in agroforestry? New spatial
analysis methods in a Faidherbia parkland. Agriculture Ecosyst. Environ. 296, 106928.
doi: 10.1016/j.agee.2020.106928
RSPO (2018). RSPO Principles & Criteria Certification For the Production of
Sustainable Palm Oil. 2018 (Kualu Lumpur, Malaysia: Roundtable on Sustainable
Palm Oil).
Sanchez, P. A. (2002). Soil fertility and hunger in Africa. Science 295, 2019–2020. doi:
10.1126/science.1065256
Sandker, M., Campbell, B. M., Nzooh, Z., Sunderland, T., Amougou, V., Defo, L.,
et al. (2009). Exploring the effectiveness of integrated conservation and development
interventions in a Central African forest landscape. Biodiversity Conserv. 18, 2875–
2892. doi: 10.1007/s10531-009-9613-7
Santika, T., Sherman, J., Voigt, M., Ancrenaz, M., Wich, S. A., Wilson, K. A., et al.
(2022). Effectiveness of 20 years of conservation investments in protecting orangutans.
Curr. Biol. 32, 1754–1763.e1756. doi: 10.1016/j.cub.2022.02.051
Santika, T., Wilson, K. A., Budiharta, S., Kusworo, A., Meijaard, E., Law, E. A., et al.
(2019). Heterogeneous impacts of community forestry on forest conservation and
poverty alleviation: Evidence from Indonesia. People Nat. 1, 204–219. doi: 10.1002/
pan3.25
Sayer, J., Sunderland, T., Ghazoul, J., Pfund, J.-L., Sheil, D., Meijaard, E., et al. (2013).
Ten principles for a landscape approach to reconciling agriculture, conservation, and
other competing land uses. Proc. Natl. Acad. Sci. United States America 110, 8349–
8356. doi: 10.1073/pnas.1210595110
Schiavina, M., Freire, S., and MacManus, K. (2022). GHS-POP R2022A - GHS
population grid multitemporal, (1975-2030) (Ispra, Italy: European Commission, Joint
Research Centre (JRC). Available at: http://data.europa.eu/89h/d6d86a90-4351-4508-
99c1-cb074b022c4a.
Schmitz, C., van Meijl, H., Kyle, P., Nelson, G. C., Fujimori, S., Gurgel, A., et al.
(2014). Land-use change trajectories up to 2050: insights from a global agro-economic
model comparison. Agric. Economics 45, 69–84. doi: 10.1111/agec.12090
Seaman, D. J. I., Voigt, M., Ancrenaz, M., Bocedi, G., Meijaard, E., Oram, F., et al.
(2023). Capacity for recovery in Bornean orangutan populations if forest fragmentation
and offtake is limited. (Authorea). doi: 10.22541/au.169382404.49701088/v1
Seaman, D. J. I., Voigt, M., Bocedi, G., Travis, J. M. J., Palmer, S. C. F., Ancrenaz, M.,
et al. (2021). Orangutan movement and population dynamics across human-modified
landscapes: implications of policy and management. Landscape Ecol. 36, 2957–2975.
doi: 10.1007/s10980-021-01286-8
Seiler, N., and Robbins, M. M. (2015). Ranging on community land and crop-raiding
by Bwindi Gorillas. Gorilla J. 50.
Seiler, N., and Robbins, M. M. (2016). Factors influencing ranging on community
land and crop raiding by mountain gorillas. Anim. Conserv. 19, 176–188. doi: 10.1111/
acv.12232
Sharma, N., Huffman, M. A., Gupta, S., Nautiyal, H., Mendonca, R., Morino, L., et al.
(2016). Watering holes: The use of arboreal sources of drinking water by Old World
monkeys and apes. Behav. Processes 129, 18–26. doi: 10.1016/j.beproc.2016.05.006
Sheil, D., Puri, R., Wan, M., Basuki, I., van Heist, M., Liswanti, N., et al. (2006).
Recognizing local people’s priorities for tropical forest biodiversity. Ambio 35, 17–24.
doi: 10.1579/0044-7447-35.1.17
Sheil, D., Sanz, N., Lewis, R., Mata, J., and Connaughton, C. (2017). “Exploring local
perspectives and preferences in forest landscapes: Towards democratic conservation,”
in Tropical forest conservation: Long-term processes of human evolution, cultural
adaptations and consumption patterns (Mexico City: UNESCO), 262–283.
Shively, C. A., and Day, S. M. (2015). Social inequalities in health in nonhuman
primates. Neurobiol. Stress 1, 156–163. doi: 10.1016/j.ynstr.2014.11.005
Siddiq, M., Uebersax, M. A., and Siddiq, F. (2022). “Global production, trade,
processing and nutritional profile of dry beans and other pulses,”in Dry Beans and
Pulses. Eds. M. Siddiq and M. A. Uebersax. (Chichester, UK: Wiley Blackwell) 1–28.
Stevenson, J. R., Villoria, N., Byerlee, D., Kelley, T., and Maredia, M. (2013). Green
Revolution research saved an estimated 18 to 27 million hectares from being brought
into agricultural production. Proc. Natl. Acad. Sci. 110, 8363–8368. doi: 10.1073/
pnas.1208065110
Strindberg, S., Maisels, F., Williamson, E. A., Blake, S., Stokes, E. J., Aba’a, R., et al.
(2018). Guns, germs, and trees determine density and distribution of gorillas and
chimpanzees in Western Equatorial Africa. Sci. Adv. 4, eaar2964. doi: 10.1126/
sciadv.aar2964
Struebig, M. J., Fischer, M., Gaveau, D. L. A., Meijaard, E., Wich, S. A., Gonner, C.,
et al. (2015). Anticipated climate and land-cover changes reveal refuge areas for
Borneo’s orang-utans. Global Change Biol. 21, 2891–2904. doi: 10.1111/gcb.12814
Sultan, B., and Gaetani, M. (2016). Agriculture in West Africa in the twenty-first
century: climate change and impacts scenarios, and potential for adaptation. Front.
Plant Sci. 7. doi: 10.3389/fpls.2016.01262
Terasaki Hart, D. E., Yeo, S., Almaraz, M., Beillouin, D., Cardinael, R., Garcia, E.,
et al. (2023). Priority science can accelerate agroforestry as a natural climate solution.
Nat. Climate Change. doi: 10.1038/s41558-023-01810-5
The World Bank (2022a) Prevalence of undernourishment (% of population) - Sub-
Saharan Africa. Available at: https://data.worldbank.org/indicator/SN.ITK.DEFC.ZS?
locations=ZG.
The World Bank (2022b) Rural population growth (annual %) - Sub-Saharan Africa.
Available at: https://data.worldbank.org/indicator/SP.RUR.TOTL.ZG?locations=ZG.
Tranquilli, S., Abedi-Lartey, M., Amsini, F., Arranz, L., ASamoah, A., Babafemi, O.,
et al. (2012). Lack of conservation effort rapidly increases African great ape extinction
risk. Conserv. Lett. 5, 48–55. doi: 10.1111/j.1755-263X.2011.00211.x
Tweh, C. G., Lormie, M. M., Kouakou, C. Y., Hillers, A., Kühl, H. S., and Junker, J.
(2015). Conservation status of chimpanzees Pan troglodytes verus and other large
mammals in Liberia: a nationwide survey. Oryx 49, 710–718. doi: 10.1017/
S0030605313001191
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org17
Twinamatsiko, M., Baker, J., Harrison, M., Shirkhorshidi, M., Bitariho, R., Wieland, M.,
et al. (2014). Linking Conservation, Equity and Poverty Alle viation Understanding profiles and
motivations of resource users and local perceptions of governance at Bwindi Impenetrable
National Park, Uganda. (London, UK: International Institute for Environment and
Development)
Umar, H. Y., Giroh, D. Y., Agbonkpolor, N. B., and Mesike, C. S. (2011). An overview
of world natural rubber production and consumption: an implication for economic
empowerment and poverty alleviation in Nigeria. J. Hum. Ecol. 33, 53–59. doi: 10.1080/
09709274.2011.11906350
UNDESA (2019). World Urbanization Prospects: The 2018 revision (New York:
United Nations Department of Economic and Social Affairs).
van Ittersum, M. K., van Bussel, L. G. J., Wolf, J., Grassini, P., van Wart, J., Guilpart,
N., et al. (2016). Can sub-Saharan Africa feed itself? Proc. Natl. Acad. Sci. 113, 14964–
14969. doi: 10.1073/pnas.1610359113
Vermeulen, S., and Sheil, D. (2007). Partnerships for tropical conservation. Oryx 41,
434–440. doi: 10.1017/S0030605307001056
Vise-Thakor, R. (2022)Sanctuaries in Africa face water shortages. In: . Available at:
https://pasa.org/awareness/sanctuaries-in-africa-face-water-shortages/.
Weng, L., Boedhihartono, A. K., Dirks, P. H. G. M., Dixon, J., Lubis, M. I., and Sayer,
J. A. (2013). Mineral industries, growth corridors and agricultural development in
Africa. Global Food Secur. 2, 195–202. doi: 10.1016/j.gfs.2013.07.003
West, T. A. P., Wunder, S., Sills, E. O., Börner, J., Rifai, S. W., Neidermeier, A. N.,
et al. (2023). Action needed to make carbon offsets from forest conservation work for
climate change mitigation. Science 381, 873–877. doi: 10.1126/science.ade3535
Wich, S. A., Garcia-Ulloa, J., Kühl, H. S., Humle, T., Lee, J. S. H., and Koh, L. P.
(2014). Will oil palm’s homecoming spell doom for Africa’s great apes? Curr. Biol. 24,
1659–1663. doi: 10.1016/j.cub.2014.05.077
Wilcove, D. S., Giam, X., Edwards, D. P., Fisher, B., and Koh, L. P. (2013). Navjot’s
nightmare revisited: logging, agriculture, and biodiversity in Southeast Asia. Trends
Ecol. Evol. 28, 531–540. doi: 10.1016/j.tree.2013.04.005
Williams, D. R., Alvarado, F., Green, R. E., Manica, A., Phalan, B., and Balmford, A.
(2017). Land-use strategies to balance livestock production, biodiversity conservation
and carbon storage in Yucatan, Mexico. Glob Chang Biol. 23, 5260–5272. doi: 10.1111/
gcb.13791
Williams, D. R., Clark, M., Buchanan, G. M., Ficetola, G. F., Rondinini, C., and
Tilman, D. (2021). Proactive conservation to prevent habitat losses to agricultural
expansion. Nat. Sustainability 4, 314–322. doi: 10.1038/s41893-020-00656-5
World Bank and Government of Rwanda (2020). Future Drivers of Growth in
Rwanda: Innovation, Integration, Agglomeration, and Competition (Washington, DC:
World Bank).
Wright, E., Eckardt, W., Refisch, J., Bitariho, R., Grueter, C. C., Ganas-Swaray, J.,
et al. (2022). Higher Maximum Temperature Increases the Frequency of Water
Drinking in Mountain Gorillas (Gorilla beringei beringei). Front. Conserv. Sci. 3. doi:
10.3389/fcosc.2022.738820
Wunder, S. (2005). Payments for Environmental Services: Some nuts and bolts. Center
for International Forestry Research Occasional Paper No. 42 (Bogor, Indonesia: Center
for International Forestry Research).
You, L., Wood-Sichra, U., Fritz, S., Guo, Z., See, L., and Koo, J. (2017) Spatial
Production Allocation Model (SPAM) 2005 v3.2. 2017. Available at: http://mapspam.
info.
Zemp, D. C., Guerrero-Ramirez, N., Brambach, F., Darras, K., Grass, I., Potapov, A.,
et al. (2023). Tree islands enhance biodiversity and functioning in oil palm landscapes.
Nature 618, 316–321. doi: 10.1038/s41586-023-06086-5
Zenna, N., Senthilkumar, K., and Sie, M. (2017). “Rice production in Africa,”in Rice
Production Worldwide. Eds. B. S. Chauhan, K. Jabran and G. Mahajan (Cham: Springer
International Publishing), 117–135.
Zhang, Y., Runting, R. K., Webb, E. L., Edwards, D. P., and Carrasco, L. R. (2021).
Coordinated i ntensification to reconcile the ‘zero hunger’and ‘life on land’Sustainable
Development Goals. J. Environ.Manage. 284, 112032.doi: 10.1016/j.jenvman.2021.112032
Meijaard et al. 10.3389/fcosc.2023.1225911
Frontiers in Conservation Science frontiersin.org18
