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Opinion

Agroforestry: a refuge for tropical


biodiversity?
Shonil A. Bhagwat1, Katherine J. Willis1, H. John B. Birks2 and Robert J. Whittaker1
1
Biodiversity Research Group, Oxford University Centre for the Environment, University of Oxford, Oxford OX1 3QY, UK
2
Department of Biology, University of Bergen, Allegaten 41, N-5007 Bergen, Norway

As rates of deforestation continue to rise in many parts areas remains seriously under-researched (but see Ref.
of the tropics, the international conservation community [8]).
is faced with the challenge of finding approaches which Here we review evidence from studies across the tropics
can reduce deforestation and provide rural livelihoods in where species richness and composition of agroforestry
addition to conserving biodiversity. Much of modern- systems are compared with that of neighbouring forest
day conservation is motivated by a desire to conserve reserves. We treat this evidence from two perspectives.
pristine nature in protected areas, while there is grow- First, we highlight the changing concept of pristine nature
ing recognition of the long-term human involvement in by arguing that people have played a key role in shaping
forest dynamics and of the importance of conservation many of the so-called pristine forests of today and empha-
outside protected areas. Agroforestry intentional man- sise that future approaches to conservation need to con-
agement of shade trees with agricultural crops has the sider agroforestry. Second, we recognise the so-called
potential for providing habitats outside formally pro- matrix effect on species diversity in landscape mosaics
tected land, connecting nature reserves and alleviating with native tree cover, and suggest that agroforestry sys-
resource-use pressure on conservation areas. Here we tems can provide corridors that connect distant reserves.
examine the role of agroforestry systems in maintaining Based on the evidence from the literature, we ask whether
species diversity and conclude that these systems can agroforestry systems can offer a useful tool for biodiversity
play an important role in biodiversity conservation in conservation and conclude that they can play an important
human-dominated landscapes. role by providing habitat for many species in increasingly
human-dominated landscapes.
Biodiversity conservation in the tropics
In tropical regions, extensive conversion of forests and Conservation in human-dominated landscapes
agricultural intensification are typically identified as the Many landscapes that are considered pristine forests
most prominent drivers of land-use change and biodiversity today have, in fact, been under some form of cultivation
loss [1,2]. Rates of deforestation in some parts of the tropics in the past [9]. Cultivation techniques included not only the
are estimated to have increased since the beginning of the planting of trees but also soil-management strategies. For
21st century compared to those in the 1990s [3]. Moreover, example, evidence has recently emerged that the ancient
land-use pressure is compounded by the fact that some of the Maya manipulated and cultivated the landscape of the
worlds poorest people live in the tropics. It is estimated that Yalahau region in the northeast corner of the Yucatan
up to 86% of the population in some tropical countries lives Peninsula in Mexico using algae from wetlands to enrich
below the poverty line [4]. In addition, the population growth upland garden plots, and cultivated trees within their
rate in these regions is substantially higher than the popu- communities [10]. Similarly, there is substantial evidence
lation growth rate of the world as a whole [5]. Therefore, any to indicate that the fertile Terra Preta soils were developed
approach that aims to mitigate tropical deforestation and by pre-Columbian native populations in central Amazonia
protect biodiversity should address the livelihoods and through the addition of large amounts of charred residues,
needs of local communities. organic waste, excrement and bones [11]. A variety of
Agroforestry intentional management of shade trees agroforestry crops are known to have been cultivated by
with agricultural crops has emerged as one of the most prehistoric populations in the tropics [12,13]. These in-
promising approaches to reducing deforestation in the clude Brazil nut trees Bertholletia excelsa cultivated in
tropics while enhancing rural livelihoods [6]. Further- forest groves by the Kayapo Indians of the Brazilian Ama-
more, it has been suggested that agroforestry systems can zon before European colonisation [14], the cultivation of
alleviate the resource-use pressure on protected areas, Boswellia papyrifera (the tree that yields frankincense)
enhancing habitats for some wild species and increasing over 2500 years ago in Africa [15] and banana cultivation in
the connectivity of landscape components, thereby mak- the heart of the African rain forest at least 3000 years ago
ing conservation more effective [7]. However, the extent [16]. The hunter-gatherer communities in Nkang,
to which agroforestry might provide a viable option for southern Cameroon are also believed to have cultivated
biodiversity management outside formally protected bananas around 3000 years ago in addition to keeping
livestock [17]. Similarly, people inhabiting the lower mon-
Corresponding author: Bhagwat, S.A. (shonil.bhagwat@gmail.com). tane rain forests of the highlands of Papua New Guinea are
0169-5347/$ see front matter 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.01.005 Available online 24 March 2008 261
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Opinion Trends in Ecology and Evolution Vol.23 No.5

believed to have maintained banana plantations around Today, in some humid tropical landscapes, trees have
6500 years ago [17]. such a prominent place in farming systems that the differ-
There is a substantial lobby within modern-day conser- ence between forests, old fallows and extensively managed
vation that promotes protection of the largest possible tree-crop plantations is not always apparent. Coffee plan-
tracts of pristine landscapes [18]. Although large tracts tations in many tropical regions, for example, are grown
of forest habitat are necessary for conservation of, for under shade of native tree species, making these planta-
example, megafauna that have large home ranges, such tions resemble neighbouring forests in their structure [29]
habitats are rarely as pristine as they are typically (Figure 1). Such plantations provide habitat for many
represented [9]. In fact, it has long been known that people species outside protected reserves in otherwise highly
have had a significant influence on landscape development human-dominated landscapes [7]. This role of agroforestry
in tropical regions. There is ample archaeological evidence plantations in biodiversity conservation is often over-
of prehistoric human-induced environmental change, often looked. Much emphasis is placed on fencing in forests
indicating degradation of natural landscapes [1921]. within strictly protected reserves and nature conservation
Recent work in applied palaeoecology is adding to a gra- is largely regarded as being focused almost exclusively on
dual shift in perception that many of todays so-called formally protected areas [30]. Although there is no doubt
natural landscapes were, in fact, shaped by prehistoric that protected areas do contribute hugely to preserving
people [22]. Therefore, many areas conceptualised as pris- large parts of the biodiversity on Earth, such areas often
tine forests might have regenerated from agricultural fail to cover the entire diversity of ecological habitats and
fallows in the recent past. Long-term palaeoecological species and, as crucially, strict protection of such areas is
records provide realistic estimates of the time it takes often resented by local people [31]. In a recent debate over
for a forest to regenerate after abandonment from cultiva- the future of tropical forest species, it has been suggested
tion. For example, evidence of cultivation by humans that although some forest specialists need intact forest
around 700 years ago has been reported from vast habitat, the bulk of tropical species will be forced to persist
stretches of so-called pristine rain forests in southern in degraded and secondary habitats outside forest reserves
Nigeria today [23]. Several other examples have shown in the future (see Ref. [32] and references therein). There-
cycles of use, forest regeneration and re-use of land by fore, the need for biodiversity conservation in human-
humans (see Ref. [24] and references therein). This work dominated landscapes in the tropics is greater today than
emphasises the message that people are part of nature and ever.
that the biodiversity found today is the result of past
human activities, as well as a combination of other eco- Agroforest refuges for biodiversity
logical and climatic processes [25]. A substantial body of Recent research in tropical fragmented landscapes
knowledge suggesting that todays pristine forests might suggests that small, isolated fragments, typically less than
have been yesterdays agricultural fallows is, by necessity, 100 ha in area (much of which is forest edge), are domi-
changing concepts and approaches to biodiversity conser- nated by common and invasive species and are poor in rare
vation [2528]. and endemic species [33]. Agroforests are often very small

Figure 1. An example of a coffee plantation grown under the shade of native trees. In this coffee plantation in Kodagu, Western Ghats, India, a layer of coffee bushes is seen
in the understorey and a canopy of native trees is seen above this layer. Such plantations of shade-grown coffee in many tropical regions have canopy structure similar to
that of secondary forests. The shade of native trees provides habitat for many forest-dwelling species in otherwise highly human-dominated landscapes.

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Opinion Trends in Ecology and Evolution Vol.23 No.5

Figure 2. Countries represented in studies on species richness and composition of agroforestry systems. Twelve agroforestry systems and nine taxa in fourteen countries
across the tropics represent cases where a direct comparison was made between agroforestry systems and neighbouring forest reserves, and where species richness and
similarity in species composition were reported. For each country, A refers to the agroforestry system (As, allspice; Bn, banana; Bz, benzoin; Ca, cardamom; Cc, cocoa-
coffee; Cf, coffee; Co, cocoa; Ft, farm trees; Hg, home gardens; Jr, jungle rubber; Mf, mixed fruit orchard; Rt, rattan) and T refers to the plant or animal taxa (Br, birds; Bt,
bats; Hr, herptiles; In, insects; Mf, macrofungi; Mm, mammals; Pl, plants [lower]; Pn, plants [herbaceous]; Tr, trees).

in size, surrounded by open landscapes and resemble forest munities of bats and of lower plants (including bryophytes
fragments. It has therefore been argued that the species and ferns) are richer (112139%) than in the neighbouring
distinctiveness (presence of rare or endemic species) of forest reserves, the richness values for other taxa are lower
such anthropogenic systems is frequently low, even though (6293%) (Table 1). The mean values of similarity in
their species richness (total number of species) might be species composition are between 25% (herbaceous plants)
equal to or higher than that of neighbouring forests (e.g. and 65% (mammals). Although, in general, mobile taxa
Ref. [34]). Noble and Dirzo [35], for example, suggest that such as bats, other mammals and birds display higher
5080% of species from regional species pools typically similarity values and the values for plants are lower, in
survive in agroforestry systems; however, many endemic certain studies agroforests show high levels of similarity to
species are lost from agroforests [36]. Does this mean that neighbouring forest reserves (e.g. 91% for mammals, 98%
agroforestry systems have rather limited conservation for insects and 100% for trees) (Table 1). The studies also
significance? suggest that agroforestry systems are high in species
Although agroforestry systems might be impoverished richness and more similar to neighbouring forest reserves
in richness of endemic or specialist forest species, and in species composition if (i) the forest land was fairly
distinctive in composition owing to their intensive man- recently converted to agroforestry plantation (e.g. Ref.
agement [35], the other side to this argument is that these [37]); (ii) the management was less intensive (e.g. Ref.
systems conserve biodiversity in habitat remnants in [38]); and (iii) the canopy cover of native trees was high
otherwise open landscapes and provide enhanced potential (e.g. Ref. [39]). Furthermore, the studies reveal three major
for species movements between habitat remnants. In a reasons why agroforestry systems might be valuable for
literature search on the Web of Science database in Decem- biodiversity conservation.
ber 2007 using keywords agroforestry and biodiversity, First, many agroforestry systems are shown to be
we found 185 references. Of these, 36 made a direct com- important for the protection of species and habitats outside
parison between agroforestry systems and neighbouring formally protected areas. For example, Williams-Guillen
forest reserves. In total, 12 types of agroforestry systems and colleagues [40] found that shade coffee plantations in
and 9 taxa were represented in 14 tropical countries Nicaragua can serve as alternative wildlife habitats and as
(Figure 2). Many of these studies sampled multiple taxa corridors between forest fragments for mantled howling
in forest and agroforestry landscapes, providing a total of monkeys Alouatta palliata. Similarly, research on the
69 examples. Based on the published data, we calculated, distribution of birds on Khao Luang Mountain in southern
for each agroforest, the species richness as a percentage of Thailand has shown that 3848% of bird species inhabiting
that found in the neighbouring forest reserve and neighbouring forests are also found in mixed fruit orchards
examined the similarity in species composition between [41]. Tylianakis and colleagues [42] also found a notable
the two system types (summarised in Table 1; see overlap in the Hymenopteran communities of different
Appendix 1 in online Supplementary Material for details). habitat types, including coffee agroforests and native forest
Although there is a wide variation across studies and fragments in Ecuador, indicating that even intensively
taxa, the mean values for richness in agroforestry systems managed land can make a valuable contribution to the
are greater than 60% of the forest values. Whereas com- overall biodiversity of the landscape mosaic.

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Table 1. Animal and plant taxa represented in the agroforestry systems studied and the richness and similarity in species
composition in relation to neighbouring forest reserves (see online Appendix 1 Supplementary Material for details)
Taxa reported Number of Agroforestry systems represented Richness compared to forest Similarity with forest Refs (in online
examples (abbreviated name [number of % (mean [range]) b % (mean [range]) c Supplementary
examples]) a Material)
Bats 3 Bn (1), Co (2) 139 (115186) 61 (5570) [11,15]
Birds 12 As (1), Bn (1), Cf (4), Co (3), Ft (1), Jr 92 (20179) 52 (1979) [3,4,11,15,18,20,23,27,
(1), Mf (1) 28,34,35]
Herptiles 1 As (1) 62 (62) 34 (1538) [18]
Insects 19 Bn (1), Co (10), Cc (1), Cf (6), Jr (1) 86 (44250) 49 (298) [1,5,810,14,26,2832]
Macrofungi 1 Cf (1) 89 (89) 61 (61) [4]
Mammals 3 As (1), Bn (1), Co (1) 93 (67121) 65 (4591) [14,18]
(excluding bats)
Plants (lower) 5 Co (2), Jr (3) 112 (77144) 42 (681) [2,3,30]
Plants 5 Co (2), Cc (1), Cf (1), Hg (1) 64 (25100) 25 (254) [6,22,28,30,36]
(herbaceous)
Trees 20 Bn (2), Bz (2), Ca (1), Co (6), Cc (1), Cf 64 (8213) 39 (5100) [3,4,68,1216,19
(4), Ft (1), Hg (1), Jr (1), Rt (1) 21,24,25,30,33]
a
Agroforestry systems: As, allspice; Bn, banana; Bz, benzoin; Ca, cardamom; Cc, cocoa-coffee; Cf, coffee; Co, cocoa; Ft, farm trees; Hg, home gardens; Jr, jungle rubber; Mf,
mixed fruit orchard; Rt, rattan.
b
Richness: values based on published data reporting species richness in agroforestry systems and neighbouring forest reserves. NB Values greater than 100 suggest
agroforestry system with species richness higher than that of neighbouring forest reserve owing to the presence of non-forest species.
c
Similarity: values based on published data reporting similarity in species composition between agroforestry systems and neighbouring forests. NB Differences in methods
involved between studies mean that the numerical comparisons shown here should be seen as only a rough guide.

Second, agroforestry systems maintain heterogeneity at tropical biodiversity [49]. This is where agroforestry
the habitat and landscape scales. For example, Parikesit systems can play an important role. Although agroforestry
and colleagues [43] identified 12 different plant assem- systems cannot stand alone as conservation areas, they can
blages in Kebon Tatangkalan agroforests of the Upper buffer existing reserves and provide corridors for persist-
Citarum Watershed, West Java, Indonesia. These agrofor- ence and movement of species across landscapes (e.g. Ref.
ests are maintained by small households spread across the [50]). Such systems offer a useful means for combating
watershed and contribute to the highly heterogeneous species loss as a result of tropical forest fragmentation.
species assemblages in the regional flora. Kindt and col-
leagues [44] carried out complete tree inventories on 201 Countryside biogeography
farms from four villages in western Kenya. They found For the last four decades, many approaches to conservation
significant differences in tree species composition between have been rooted in MacArthur and Wilsons equilibrium
farms. The choice of shade trees left on their plantations by theory of island biogeography [51]. This theory set out to
individual farmers contributed to the overall heterogeneity account for the long-established relationship between the
of trees in this agroforestry landscape. A study on Mount number of species and (island) area one of the most
Kilimanjaro has also shown that traditional coffee-banana widely described general properties of ecological systems
plantations, locally called Chagga homegardens, maintain [52]. Consistent with this theory, a loss in the size of
a multilayered vegetation structure similar to tropical habitat is known to result in a proportional loss of species
montane forests [45]. [53]. Conversely, with an increase in the size of available
Third, trees in agroforestry landscapes reduce pressure habitat, there will be a proportional increase in species
on formally protected forest reserves. Murniati and col- number. Thus, an agricultural landscape with high tree
leagues [46] studied the availability of forest resources in cover should support more forest species than a landscape
mixed gardens and village forests in the northern part of without trees. The application of island theory led con-
the Kerinci Seblat National Park, Sumatra, Indonesia. servationists to view nature reserves as islands in a sea of
They found that households that owned mixed gardens ruined habitat, and to focus on what configuration of
depended much less on national park resources than fragments provided the best return with regard to species
households which cultivated wetland rice fields alone. richness [54]. Partly as a result of this focus on island
Similarly, Masozera and Alavalapati [47] found that com- theory, conservation biologists became so focused on
munities which earned a high income from diversified reserves that they have paid insufficient attention to the
agricultural lands were much less dependent on forest significance of the properties of the landscape matrix
resources from the Nyungwe Forest Reserve in Rwanda surrounding reserves [55].
compared to communities which earned a low income from Recent calls have been made, under the headings var-
agriculture. Research on trees outside forests in several iously of countryside biogeography [56], reconciliation
small-island developing states of the Pacific Ocean ecology [57] and conservation biogeography [58], for
suggests that the presence of such trees is valuable for research to establish how to create wildlife-friendly coun-
minimising deforestation, forest degradation and loss of tryside landscapes. One part of this research agenda
biodiversity from reserves [48]. should focus on the role of agroforests of various types,
Although networks of protected areas in the tropics to establish how effective they are as habitats and corridors
might currently provide habitat for many rare and endemic for wildlife within mixed countryside. Many of the worlds
species that prefer old-growth forest, it has been acknowl- agroforests provide a habitat-rich landscape matrix where
edged that these networks are insufficient to protect all native species can survive outside nature reserves (e.g. Ref.

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[59]). Given that conservation decisions are often driven


Box 1. Management of agroforestry systems for
more by political and economic rather than ecological
biodiversity conservation
criteria and that the governance of nature reserves suffers
from high levels of corruption in many tropical countries, It has been recognised that in order for the potential of agroforestry
to be harnessed effectively, farmers need clear incentives to plant
conservation within reserves is constantly under threat
and protect trees [6]. Here we consolidate several recommendations
(e.g. Ref. [60]). Although protected reserves do play crucial that might make agroforestry ecologically and economically viable
roles for conservation of biodiversity, a factor that will in the long term.
contribute significantly to their success in the future is
the quality of the landscape matrix around reserves. Landscape-based management
Although it is essential to maintain and cultivate shade-tree species
Finally, future climate change might put pressure on
that are native to the region in question (instead of monospecific
species of conservation concern to migrate in response [61]. shade), the variety of species cultivated is also of key importance
A landscape matrix surrounding reserves can provide [62]. Similarly, keeping remnants of natural forest within agrofor-
corridors through which species can migrate from one estry plantations and redesigning annual croplands to include
reserve to another: a further reason why constituting wild- features such as hedgerows can contribute to landscape-level
connectivity [63]. To sustain the conservation potential of agrofor-
life-friendly landscapes makes good sense. Therefore, agro- estry systems, a balance between production and protection of
forestry systems have the potential not only to provide natural features in the landscape is necessary.
suitable habitat but also to provide corridors for the
migration of many forest-dwelling species that will face Incentives for conservation
the effects of changing climate in the future. It is important to recognise that farmers often have to forego part of
their income by maintaining forests on farmland. Although it is
essential that regional land-use planning is sensitive to the
Conclusions economic needs of farmers [43], several incentives can be offered
Long-term ecological knowledge that todays pristine for- to repay the cost of maintaining native trees on plantations [64]. Tax
ests might have been yesterdays agricultural fallows relief for planting native shade trees, payment for environmental
services provided by agroforestry farms and soft credits for
should be applied to the concept of naturalness of land-
ecologically beneficial farming practices have been suggested as
scapes and approaches to biodiversity conservation today. ways to make conservation lucrative to farmers [65]. A more direct
The ecological histories of many tropical landscapes cur- way of encouraging conservation in agroforestry systems is to
rently within protected areas suggest that they were promote certification of shade-grown, biodiversity-friendly and
impacted by human activities in the recent past. Although organic produce and to provide a secure market for certified
produce through farmers cooperatives [66]. Rewards for conserva-
the current protected area networks provide an important
tion are more likely to work than severe restrictions on agricultural
conservation apparatus, further expansion of this network land use.
might be limited by competing demands for other land
uses. Therefore, conservationists need also to look beyond Education and training
reserves and consider the importance of the surrounding In many tropical countries the levels of literacy are low. As a result,
communication of new government policies to farmers can be
landscape matrix. challenging, and encouraging farmers to put them into practice
Agroforestry provides a potentially valuable conserva- even more difficult [67]. Although national and regional pro-
tion tool that can be useful for reducing land-use pressure grammes for planting native trees outside forests are essential
and enhancing rural livelihoods in tropical countries (Box 1). [48], community-based training programmes on techniques for
The availability of useful tree species and other non-timber diversifying agroforestry plantations would also be beneficial to
farmers [68]. Furthermore, it would be crucial to educate farmers in
forest products in agroforests can alleviate resource-use self-sufficiency to reduce their dependence on adjacent protected
pressure on conservation areas. Several examples across areas. Self-sufficiency can be encouraged by providing training in
the tropics have shown that a substantial proportion of management and marketing of agroforestry produce [69]. Although
biodiversity of forest reserves is represented in agroforests. education in useful techniques and skills can enhance the benefits to
farmers from their agroforests, it can also alleviate some pressure
The ability of many tree-covered but intensively used land-
from reserves, thereby making protected areas more effective.
scapes to support native species suggests that maintaining
and creating habitats in human-dominated landscapes can
help conserve a large proportion of biodiversity.
The literature reviewed suggests that agroforests with Acknowledgements
less intensive management and high canopy cover have We are grateful to H.H. Birks, C. Garcia, P.K.R. Nair, K. Triantis, W.F.
Laurance and two anonymous referees for comments and helpful
high species richness and are more similar to neighbouring suggestions on this manuscript. S.A.B.s current work at the Oxford
forest reserves than intensively managed agroforests with University Centre for the Environment is funded by the Leverhulme
open canopies. Effective management of agroforestry sys- Trust and a William L. Brown Research Fellowship of the Missouri
tems, therefore, entails several aspects (see Box 1). First, Botanical Garden. Collaboration with H.J.B.B. was initiated while he
we suggest an integrated approach to reserve networks held a Visiting Senior Research Fellowship at Jesus College, Oxford.

that includes agroforestry systems as an important con-


Supplementary data
servation tool. Second, we recommend that farmers who
Supplementary data associated with this article can
maintain agroforests might, in particular circumstances,
be found, in the online version, at doi:10.1016/j.tree.
be offered compensation in the form of various incentives
2008.01.005.
for biodiversity-friendly farming practices. Third, we advo-
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