Agroforestry Systems 61: 155165, 2004. 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Nature vs. nurture: managing relationships between forests, agroforestry and wild biodiversity
J.A. McNeely
The World Conservation Union (IUCN), 1196 Gland, Switzerland; e-mail: jam@iucn.org

Key words: Coffee, Conservation, History, Invasive species Abstract Many agroforestry systems are found in places that otherwise would be appropriate for natural forests, and often have replaced them. Humans have had a profound inuence on forests virtually everywhere they both are found. Thus natural dened as without human inuence is a hypothetical construct, though one that has assumed mythological value among many conservationists. Biodiversity is a forest value that does not carry a market price. It is the foundation, however, upon which productive systems depend. The relationship between agroforestry and the wild biodiversity contained in more natural forests is a complicated one, depending on the composition of the agroforestry system itself and the way it is managed. Complex forest gardens are more supportive of biodiversity than monocrop systems, shade coffee more than sun coffee, and systems using native plants tend to be more biologically diverse. Nonnative plants, especially potentially invasive alien species, threaten biodiversity and need to be avoided. The relationship between forests, agroforestry and wild biodiversity can be made most productive through applying adaptive management approaches that incorporate ongoing research and monitoring in order to feed information back into the management system. Maintaining diversity in approaches to management of agroforestry systems will provide humanity with the widest range of options for adapting to changing conditions. Clear government policy frameworks are needed that support alliances among the many interest groups involved in forest biodiversity.

Introduction This paper addresses the changing perceptions of relationships between people and nature and how this affects forest management. It begins by reviewing some basic concepts, outlining the history of human impacts on forest ecosystems, and discussing the relationship between biodiversity conservation and agroforestry. This leads to the identication of several management issues and a call for closer collaboration between agroforestry and conservation interests. In western culture, nature is often considered to be that which operates independently of people (Hoerr 1993), and a major focus of development has been to bring nature under greater human control. In fact, progress is often measured by technological innovations that have enabled humans to gain a greater share of the planets productivity. Conservation, on the

other hand, has been based on the idea of sequestering the largest possible tracts of nature in a state of imagined innocence as national parks and other kinds of protected areas. Forests that are pristine or virgin or primary are thus given particularly high value for conservation, and considered likely to have high biological diversity (Gomez-Pompa and Kaus 1992). Despite the dominance of this view of nature, work in ecology (Sprugel 1991), paleontology (Martin and Klein, 1984), forestry (Poffenberger 1990), history (Boyden 1992; Ponting 1992; Flannery 2001), archaeology (Audric 1972; Raven-Hart 1981), anthropology (Denevan 1992a; Roosevelt 1994), and ethics (Taylor 1986) is calling into question the separation of people from nature, supporting instead the ageold view of many cultures that people are part of nature and that the biodiversity that is, the variety of genes, species, and ecosystems found in todays

156 forests result from a combination of cyclical ecological and climatic processes and past human action. Evidence is building to support the view that very few of todays forests anywhere in the world can be considered pristine, virgin, or even primary, and that conserving biological diversity requires a far more subtle appreciation of both human and natural inuences. McNeely (1994) drew from recent studies to suggest four basic conclusions about the history of forests and biodiversity: i. Humans have been a dominant force in the evolution of todays forests. ii. As humans develop more sophisticated technology, their impact on forests increases until forests are degraded to the long-term detriment of the overexploiting society. iii. Overexploitation is usually followed by a culture change that may reduce human pressure, after which some forests may return to a highly productive and diverse, albeit altered, condition, and others may be permanently altered to much less productive and diverse conditions. iv. The best approach to conserving forests and their biodiversity is through a variety of management approaches ranging from strict protection through intensive use, with a careful consideration of the distribution of costs and benets of each. Different systems of management may enhance or reduce forest diversity. Completely excluding human intervention from species-rich communities found in hilly, high rainfall areas of the tropics, for example, may reduce genetic and species diversity by changing the mix of successional stages, or it may help to conserve species that are conned to old-growth stages of succession. Further, the sheer number of species is not necessarily a useful measure. Australia, California, Hawaii and New Zealand, for example, have more species now than ever before. Many of these are nonnative and maintained by human action, but some are invasive alien species that threaten the native species (McNeely et al. 2001). The notions of natural vegetation or ecosystem processes, therefore, are still useful goals in forest management, but they should be revised to recognize that a range of ecosystems can legitimately be considered natural (Sprugel 1991), and nearly all of them have been signicantly inuenced by people. Managing agroforestry systems to address biodiversity concerns will both enhance productivity and contribute to conservation objectives. The role of myth in conserving biodiversity The idea that nature exists as something separate from people has become part of the mythology of industrial society. The Oxford Dictionary (Pollard 1994) denes myth as a story arising from an unknown source and containing ideas or beliefs that purport to explain natural events without a basis in fact. It appears that this mythic image of nature is essential to the psychological well being of modern humanity (Campbell 1985; Jung 1964), whose industrial approach to conquering nature can be so destructive. Nonindustrial societies have different myths, often treating what industrial society calls nature as a set of very real threats to human existence. Campbell (1985) suggests that societies that cherish and keep their myths alive will be nourished from the soundest, richest strata of the human spirit, and that myths often contain many elements that ring true to the people who believe them. The myth of the virgin forest and nature untouched by humans is above all a myth of urban-dwelling people who are well separated from the reality of the forest. Those who actually live in the forest are faced with rich diversity that is mostly hidden far above or in the heavy cover of the ground vegetation where various dangers lurk (Campbell 1985). The forest village is a place of safety and stability that is separated from the forest, though elds often are hacked from the forest to bring human order into the chaos of nature. Agroforests or agroforestry systems may bring domestication to the disorder of wild nature. This is supported by various kinds of mythology that help to explain observed phenomena, such as how people rst learned to domesticate plants and animals (see, for example, Suzuki and Knudtson 1992). Rites and rituals are carried out by forest-dwelling peoples to help reinforce the myths, while the myths provide the mental support for rites and rituals, helping to ensure that children are made well aware of the social and natural environment into which they must t in order to become a competent member of society (Campbell 1985). The corresponding rituals of modern urban society in relation to the myth of nature may be watching nature programs on television, giving money to organizations that claim to conserve nature, and visiting protected areas, many of which assume almost a sacred character (Putney et al. 2003). The western mythical vision of an untouched wilderness has permeated global policies and politics in resource management (Gomez-Pompa and Kaus 1992). But this view of forests is based on an out-

157 moded ecological perspective, and on misunderstanding of the historical relationship between people and forests, and the role people have played in maintaining biodiversity in forested habitats. A brief review of certain episodes in the history of people, forests, and biodiversity will show how humans have affected the birth, growth, death, and renewal cycle of forests in a variety of ways, with various outcomes in different parts of the world (Holling 1978). A more sophisticated understanding of the relationship between forests and people will not replace the myth of the pristine forest but may lead to better forest conservation and better agroforestry. cultivation. Mature tropical forests conceal most of their edible products high in the canopy beyond the reach of the terrestrial herbivores, while forest clearings bring the forests productivity down to where it can be reached by hungry browsers. The earlier successional stages are also faster growing, and therefore more productive than the later stages of the cycle as the forest becomes more mature. The conclusion that shifting cultivation has beneted both people and forest depends, however, on the practice being carried out in a sustainable manner, which today is rare. Shifting cultivation can become maladaptive in at least three ways: by an increase in human population that causes old plots to be recultivated too soon; by inept agricultural practices such as cultivating the land for so long that productivity declines and persistent weeds such as Imperata cylindrica become established; and by attempting to cultivate forests that are too dry, so recovery is slow and the danger of cataclysmic re is great (Geertz 1963). Sometimes the three factors work together to destroy wide areas of tropical forest. Most shifting cultivation has taken place in the hills, where vegetation dries out more quickly and updrafts help fan the ames among the cut vegetation. The lowlands, many of which were seasonally ooded or otherwise difcult to burn, remained relatively intact during the early years of agriculture and were used mostly for hunting, shing, and gathering of tubers and other plants. With the development of irrigation and agricultural surpluses, all that changed, and new civilizations ourished in lowlands where wet rice could be grown, often leading to substantial forest clearance. Sumatra, Indonesia, for example, was the centre of the rice-growing Sriwijaya civilization, which spread its inuence from what is now Palembang throughout Southeast Asia. Following the collapse of the Sriwijaya civilization in the 14th century, forests quickly reclaimed much of the landscape that had been transformed by Sriwijaya (Schnitger 1964); parts of these ancient farmlands are now so important for biodiversity that they are included in Indonesias protected area system. Some of Indonesias most remote protected areas are proving to contain important Sriwijanan archaeological sites, as in Kalimantans Kayan Mentarang Nature Reserve, an indication of substantial historical human activity in forests noted today for their high biodiversity. In tropical Asia, precolonial forest management was primarily in the hands of the people who lived

Connections: the history of people, forests, and biodiversity The conclusion that the world has few, if any forests which have not been signicantly inuenced by people is supported by evidence from many parts of the world. Cycles of human activity that have affected biodiversity are evident in tropical Asia, the Western Hemisphere, and Europe and the Mediterranean. Tropical Asia Tropical Asia was one of the heartlands of shifting cultivation (Solheim 1972), a cyclical land use that has had a profound inuence on habitats throughout the region over the past 10 000 years. Spencer (1966), in a detailed study of the impact of shifting cultivation in Asia, concluded that most of the mature forests of the Orient today are not virgin forests in the proper sense, but merely old forests that have reached a fairly stable equilibrium of ecological succession after some earlier clearing by human or natural means. In some areas it is possible that old forests are not secondary forests or even tertiary forests, but forests of some number well above three. Traditional systems of shifting cultivation often include many agroforestry elements. The older elds contain a high proportion of fruit trees, which are attractive to primates, squirrels, hornbills, and a variety of other animals. In addition, large mammals ourish, with elephants, wild cattle, deer, and wild pigs all feeding in the abandoned elds; tigers, leopards, and other predators are in turn attracted by the herbivores. Wharton (1968) has provided convincing evidence that the distribution of the major large mammals of Southeast Asia is highly dependent on shifting

158 in the forests. The colonial era brought forests into the global market system, leading to the nationalization of many forests, the import of forest management technology from Europe, and the loss of traditional resource management practices that maintained biodiversity in forests, though not explicitly designed to do so (Poffenberger 1990). The post-colonial period perhaps has been worse with few forest departments able to control exploitation from concession holders or to work constructively with forest-dwelling people. Poffenberger (1990) points out that conicts between state land management policies and locally operating forest-use systems is a major cause of forestland mismanagement throughout southeast Asia. With both colonial and post-colonial regimes, forest departments in Myanmar (Burma), India, Indonesia, and Sri Lanka, were designed to generate revenue for the state rather than provide direct benets to rural communities that were practicing various forms of agroforestry. He concludes that radical changes in tenure rights and lack of clarity over ownership of tree and forest products are key factors in understanding the speed with which Asian forests have been depleted and why so many species are threatened today. Agroforestry that returns control of at least some forests to local people can help restore sustainable-use management practices that can complement biodiversity conservation in protected areas. The western hemisphere The vast boreal forest-covered wilderness of North America is often considered to be natural. But people have occupied this forest from its very beginnings, as the great ice sheets withdrew northwards at the end of the Pleistocene. New studies have established that Native Americans in northern Alberta regularly and systematically burned habitats to inuence the local distribution and relative abundance of plant and animal resources (Hoffecker et al. 1993). Trees played a crucial role in the initial occupation of the Western Hemisphere. It is now believed that the critical environmental variable that enabled the rst humans to move from Asia into North America was the reappearance of trees in Alaskan river valleys, which provided essential fuel sources as glaciers withdrew at the end of the Pleistocene around 11 00012 000 years ago. As Lewis and Ferguson (1988) show, this pyrotechnology is similar to that reported for hunter-gatherers elsewhere in the world, creating an overall re mosaic that characterizes the northern boreal forests. Crosscultural comparisons of these practices with those in other parts of North America, as well as in several parts of Australia, illustrate functionally parallel strategies in the ways that hunter-gatherers employed habitat res, specically in the maintenance of reyards and re corridors in widely separated and different kinds of biological zones (Flannery 1994; 2001). As they moved further south, the immigrants from Asia continued to modify the American forests. In reviewing the evidence, Denevan (1992b) concluded that pre-Columbian human settlement had modied forest extent and composition, expanded grasslands, and rearranged the local landscape through countless articial earthworks. Agricultural elds, towns, and trails were common, having local impacts on soil, microclimate, hydrology, and wildlife. These early immigrants had a signicant impact on biodiversity as well, with some 34 genera of large mammals becoming extinct around the time of rst human occupation of the continent (Martin and Klein 1984). Agroforestry may well have been one of the earliest vehicles of plant domestication in Central America. For example, Native American populations are known to have cultivated a large number of plants and domesticated them for their starch-rich belowground parts such as rhizomes and tubers. Suggestions that tropical forests, the likely source of many of these crops, were an early and inuential centre of plant husbandry have long been controversial because the organic remains of roots and tubers are poorly preserved in the archaeological sediments from the humid tropics. But Piperno et al. (2000) reported the occurrence of starch grains identiable as manioc (Manihot esculenta), yams (Dioscorea spp.) and arrowroot (Maranta arundinacea) on assemblages of plant milling-stones from preceramic horizons at the Aguadulce shelter, Panama, dated between 7000 and 5000 years before present. The artefacts also contain maize (Zea mays) starch, indicating that early horticultural systems in this region were mixtures of root and seed crops, as well as tree crops, though the evidence for the latter is circumstantial. The data provide the earliest direct evidence for root crop cultivation in the Americas, and an ancient and independent emergence of plant domestication in the lowland Neotropical forest. This serves as another indication that the composition of presumed virgin or untouched tropical forests has been importantly inuenced by people. By A.D. 800, the Maya had modied 75% of the Yucatan forest, and following the collapse of the

159 classical Mayan civilization shortly thereafter, forest recovery in the central lowlands was nearly complete by the time the Spaniards arrived 700 years later (Whitmore et al. 1990). The Aztecs followed a similar cycle. Examining the association between erosion and pre-Columbian population in Central Mexico, Cook (1949) concluded: An important cycle of erosion and deposition accompanied intensive land use by huge primitive populations in central Mexico, and had gone far toward the devastation of the country before the white man arrived. OHara et al. (1993) found three major episodes of erosion in central Mexico during the past 4000 years, correlated to the rst arrival of corn (maize)-farming of steep slopes, and a period of heavy population density, all in pre-colonial times. The current composition of the vegetation in Central America thus is the legacy of past civilizations, the heritage of cultivated elds and managed agroforests abandoned hundreds of years ago (Gomez-Pompa and Kaus 1992) as the pre-European population estimated at 22.8 million people crashed (Denevan 1992). Turner and Butzer (1992) estimate that 76% of the human population was eliminated between 1492 and 1650, primarily because of disease, leaving wide areas to revert to tropical forests which today are often considered pristine or natural. Further south, by about 2000 years ago, fairly complex societies had been established in Amazonia, with large populations, public works, differentiated settlements, elaborate ceremonial art, long-distance trade, and other signs of complex chiefdoms. By the time of rst European contact, these chieftains had large domains, maintained by organized large-scale warfare and diplomacy, elite ranking based on descent from deied human ancestors, and long-distance interregional trade and tribute systems (Roosevelt 1994). Archaeological sites indicate that substantial human populations inhabited Amazonia before Europeans arrived, with some shell middens so extensive that they have been used as commercial lime mines, providing fertilizer and road-building material for more than 200 years. Some Bolivian prehistoric archaeological midden sites have been an important soil resource for commercial agriculture in the Brazilian Amazon since the mid-19th century. Recent ndings from Brazils Upper Xingu, the largest area of Amazonian forest still being managed by indigenous peoples, indicate that the region supported a dense human population that substantially altered both forests and wetlands (Heckenberger et al. 2003). This also supports Denevans (1992) estimate that South America had a pre-colonial population of 24.3 million. As Roosevelt (1994 p. 9) concludes, Historical studies in the oodplains show that the European conquest affected the transition from ancient chiefdoms to indigenous village societies or peasant communities through a long process involving military defeat, decimation, forced migration, enslavement, misogynization, and acculturation. In response to the European invasion, the areas that held the majority of the massive late prehistoric occupations of Amazonia were rapidly emptied of Indians, who now persist in a mosaic with non-Indian communities, mostly at the margins of the basin. Thus the current Amazonian Indians have a way of life that is a complex indigenous adaptation to conquest and nationalization as well as to Amazonian environments, and the virgin Amazonian forests are at least partly an inadvertent legacy of the European invasion of South America. Europe and the Mediterranean The case for Europe is perhaps even more dramatic. The early Holocene of the Mediterranean area was a mixed evergreen and deciduous forest of oaks, beech, pines, and cedars. The forest was eaten away by waves of different civilizations that used the forest and forest lands to further their development objectives, expanding and contracting as the wisdom of their policies was tested. The process of forest clearance was already well underway at the time of Homer in the 9th century B.C., who likened the noise of a battle to the din of wood cutters in the glades of a mountain. Early in the 4th century B.C., Plato, referring to the disappearance of forests in Attica, wrote: What now remains compared with what then existed, is like the skeleton of a sick man, all the fat and soft earth having been wasted away, and only the bare framework of the land being left (quoted in Ponting 1992 p. 76). Civilizations from Bronze Age Crete and Knossos, Mycenaean Greece, Cyprus, Greece, and Rome rose and fell with the forests that supported them (Perlin 1989). Subsequent overgrazing by sheep, cattle, and goats prevented the forests from ever becoming reestablished, though agroforestry is now beginning a comeback. The olive (Olea europaea) can be considered the agship species of the Mediterranean. Developed from a straggly wild relative along the coasts of Syria and Anatolia in the 6th century B.C., it soon became a

160 crop of outstanding economic importance. But it also contributed to signicant deforestation, land degradation, and loss of biodiversity, at least of vertebrates. As the richer valley lands were cleared of forests to plant crops, the poorer soils of the hillsides were being planted with olives. The development of Crete between 2500 and 1500 B.C. was supported by the export of timber and olive oil to Egypt, as forest trees were felled and olive trees were planted. But as a result of deforestation, soil accumulated over millennia was being washed from the hillsides in just a few centuries, and the natural wealth of the country was eroded with the soil. The decline of the Cretan forests was mirrored by the same transformation, following in the wake of the axe, the plough, and the olive in their westward progress through all the civilized states of the Mediterranean (Darlington 1969). As a result, much of the evergreen forest in the Mediterranean region was transformed into the brushwood known as maquis, which today is maintained by re. The loss of native forests through conversion to agriculture also had signicant impact on biodiversity, with some 90% of the endemic mammalian genera of the Mediterranean becoming extinct after the development of agriculture (Sondaar 1977). While little of the remaining forest can be considered natural in any sense, agroforestry may be used as a tool to reclaim land devoted to low-yield annual crops and contribute to ecological diversity in closed forests. It may help to bring back at least some of the biodiversity that formerly characterized the Mediterranean region an area that even now is considered a biodiversity hotspot (Myers et al. 2000). use of nonplanted tree species. Data were collected for 144 tree species in six agroforests and two natural forest patches. The investigators found that the older agroforests had nearly the same proportions of species of different successional stages and modes of dispersal as natural forests, and emphasized the potential of agroforests in conserving tree species. Nonplanted tree species of the agroforests and natural forests have similar human uses, indicating that the management of these agroforests does not signicantly discriminate between species with certain uses. However, regional differentiation between agroforests and natural forest patches was signicant. Late successional species and animal-dispersed species of the agroforests were more widespread geographically than species of the same ecological characteristics found in natural forests. The investigators concluded that although the agroforests are similar to natural forests in terms of numbers of species with different ecological characteristics, the composition of nonplanted tree species in the agroforests is not consistent with natural forests, but over-represents species that are easily dispersed and/or established. Swidden succession Ferguson et al. (2003) compared post-agricultural succession along the range of farming activities practiced in Guatemalas northern lowlands: agroforestry, swidden, ranching, and input-intensive monocultures. Using several characteristics of the vegetation, they found that succession was dramatically faster on agroforestry and swidden sites than on pastures or inputintensive monocultures. Overall recruitment was faster for swiddens than for agroforests, but other response variables did not differ signicantly between the two treatments. The investigators results suggest that the conservation strategy of discouraging swidden agriculture in favor of sedentary, input-intensive agriculture to relieve pressure on old-growth forest may be counterproductive over the long term. Agroforestry may be a more appropriate option for maintaining biodiversity in production landscapes (McNeely and Scherr 2003). Shaded coffee (Coffea spp.) Marjokopri and Ruokolainen (2003) compared agroforests (Tembawang) in West Kalimantan, Indonesia, to patches of primary forest, which may have been old-growth secondary forests, in terms of successional stage, mode of dispersal, and characteristics of human Petit and Petit (2003) examined bird communities associated with 11 natural and human-modied habitats in Panama and assessed the importance of those habitats for species of different vulnerability to disturbance.

The interface between biodiversity conservation and agroforestry Conserving biodiversity where people live is a major challenge, especially in the tropical countries. But a growing body of research shows that agroforestry can make a signicant contribution to conserving biodiversity in a wide range of settings. Complex agroforests

161 Calculating habitat importance scores using both relative habitat preferences and vulnerability indices for all species present, they found that species of moderate and high vulnerability were those categorized principally as forest specialists or forest generalists. As expected, even species-rich nonforest habitats provided little conservation value for the most vulnerable species. Shaded coffee plantations were modied habitats with relatively high conservation value however, as were gallery forest corridors. Sugarcane (Saccharum ofcinarum) elds and Caribbean pine (Pinus caribaea) plantations, important land uses in much of Central America, offered virtually no conservation value for birds. However, agroforestry, especially systems that use native species, can provide substantial biodiversity benets. Benzoin gardens in Sumatra Styrax paralleloneurun is a forest canopy tree species from Sumatra that produces benzoin, an aromatic resin, and is cultivated in a traditional agroforestry management system. Garcia-Fernandez et al. (2003) sought to determine the impact of benzoin garden management on forest structure, species composition, and diversity. They chose 45 gardens for study in two northern Sumatra villages, where data on management practices and ecological structure were gathered. Ecological information was also collected from abandoned benzoin gardens and what they considered primary forest areas for purposes of comparison. Although benzoin management requires that competing vegetation be thinned, these activities are not intensive, allowing species that coppice to remain in the garden and thereby reducing the effects of competitive exclusion mechanisms on species composition. The investigators found that tree species diversity in abandoned gardens was similar to that in primary forest, but endemic species and species characteristic of mature habitats were less common. They concluded that traditional benzoin garden management represents only a low-intensity disturbance and maintains an ecological structure that allows effective accumulation of forest species over the long term. Community-based enterprise An essential element of successful agroforestry is the economic viability of the various enterprises that are involved. If local people can benet nancially from enterprises that depend on the biodiversity of the forest within which they live, then they might reasonably be expected to support the conservation and sustainable use of the forest ecosystem. This attractive idea has been extensively tested across 39 project sites in Asia and the Pacic, involving activities such as ecotourism, distilling essential oils from wild plant roots, producing jams and jellies from forest fruits, collecting other forest products, and sustainably harvesting timber (Salafsky et al. 2001). The conclusion from this study was that a community-based enterprise strategy can indeed lead to conservation, but only under specied conditions that are critically dependent on external factors such as market access. Further, any such enterprise can be sustainable only if it is designed to be adaptable to changing conditions. Because many agroforestry areas are subject to political or economic turmoil, res, droughts, and other external factors, this adaptability of the enterprise is essential to long-term sustainability of the forest. The complexity of factors affecting agroforests also calls for multiple levels for protecting biodiversity, with actions at local, national, and international levels providing the redundancy needed for ensuring that all genes, species, and ecosystems are conserved.

Management systems Adaptive management is the most effective approach to agroforestry, involving careful planning on the basis of available information, implementation, associated research, monitoring systematic of results, and feeding the results of the monitoring back to improved management of the agroforestry enterprise. This approach helps ensure that agroforestry can respond effectively to changing conditions through constant adaptation. Converting the potential benets of forest biodiversity conservation into real and perceived goods and services for society at large, particularly for local people, requires a systems approach to management that includes agroforestry as an essential element that provides economic benets to local people. The approach is comprised of six key components. i. Integrated protected areas encompassing various levels of management and administration, including the national, provincial, and local governments, nongovernmental organizations, local communities and indigenous peoples, the private sector, and other stakeholders (McNeely 1999). ii. Civil society engagement in economic development that includes managing production forests, agro-

162 forests, and protected areas, especially for tourism and the sustainable use of certain natural resources (Szaro and Johnston 1996). iii. Bioregional or ecoregional resource management frameworks, that include farms, agroforests, protected areas, harvested forests, human settlements, and infrastructures as part of a diverse landscape (Miller 1996). iv. Multi-stakeholder cooperation in agroforestry between private landowners, indigenous peoples, other local communities, industry and resource users. v. Economic mechanisms to support agroforestry including nancial incentives, tax arrangements and land exchanges to promote biodiversity conservation. vi. Institutional capacities which encourage local stakeholders, universities, research institutions, and public agencies to harmonize their efforts in agroforestry and biodiversity conservation. Combining these elements can lead to a balanced program for sustainable agroforest management and biodiversity conservation. Enforced governmental regulation should be designed to complement the rights, responsibilities and management activities that are assumed by civil society. Agroforesters who live within or close to protected areas and other forested regions should form alliances with other stakeholders that enable each to assume appropriate roles according to clear government policies and laws. Management issues Agroforestry, biodiversity, and invasive alien species As the global movement of people and products has expanded, so has the movement of plant and animal species. When a tree species is introduced into a new habitat, for example the introduction of the oil palm (Elaeis guineensis) from Africa into Indonesia, eucalypts (Eucalyptus spp.) from Australia into California, or rubber (Hevea brasiliensis) from Brazil into Malaysia, the alien species typically requires human intervention to survive and reproduce. Many of the most popular species of trees used for agroforestry are alien or nonnative species that prosper in their new environments, partly because they no longer face the same competitors, predators and pests that they did at home. Such alien species have been economically important and have enhanced the production of various forest commodities in many parts of the world. But in some cases, introduced species are a signicant problem, becoming established in the wild and spreading at the expense of native species and affecting entire ecosystems. Notorious examples of these invasive alien species that have negative effects on native biodiversity include various species of Northern Hemisphere pines (Pinus spp.) and Australian acacias (Acacia spp.) in southern Africa, and Melaleuca from South America invading Floridas Everglades National Park. These and many other woody plants were introduced intentionally but had unintended consequences. Of the 2000 or so species used in agroforestry, perhaps as many as 10% are invasive (Richardson 1999). While only about 1% are highly so, this includes some popular species such as Casuarina glauca, Leucaena leucocephala, and Pinus radiata. Great care is required to ensure that such species serve the economic purposes for which they were introduced, and do not escape to cause unanticipated negative impacts on native ecosystems and their biodiversity. One management option would be to plant only sterile forms, so reproduction and spread would be impossible. Worse perhaps, are the invasive alien species that are introduced unintentionally, such as disease organisms that can devastate an entire tree species. The Dutch elm disease (Ophiostoma ulmi and O. novaulmi) and the American chestnut blight (Cryphonectria parasitica) in North America are notorious examples. Pests, such as gypsy moths (Lymantria dispar) or longhorned beetles (Anoplophora glabripennis), can have profound economic impacts on native forests or plantations. The economic impact of such pests amounts to several hundred billion dollars per year (Perrings et al. 2000). Much of this economic toll is felt in forested ecosystems, even within well-protected national parks. The 1951 International Plant Protection Convention was established to address some of these issues, and new international programs have been developed to respond to current serious problems. A global strategy has been developed (McNeely et al. 2001) and best practices for prevention and management have been designed (Wittenberg and Cock 2001). But growth in global trade means that the threat of devastating invasive species of insects and pathogens will also grow and could fundamentally alter natural forests and virtually wipe out plantations whose lack of species diversity makes them especially vulnerable. Both conservation of biological diversity and sustainable agroforestry need to be managed to ensure that the issue of invasive alien species is well recognized and addressed.

163 Shade or sun? Siebert (2002) investigated biophysical, soil and biodiversity effects associated with growing methods of coffee and cacao (Theobroma cacao) in Sulawesi, Indonesia, where neither species is native. Canopy height, tree, epiphyte, liana and bird species diversity, vegetation structural complexity, percent ground cover by leaf litter, and soil calcium, nitrate nitrogen, and organic matter levels in the O horizons were all signicantly greater in shaded than in sun-grown farms. In contrast, air and soil temperatures, weed diversity, and percent ground cover by weeds were signicantly greater in sun compared to shade farms. At the landscape level, conversion of shade-grown crops to sun conditions isolates protected areas and remnant old-growth forest fragments. Local cultivators realize the agronomic and socioeconomic risks associated with sun-grown perennial monocultures and some are increasing the density and diversity of fruit tree cultivation in an effort to provide shade and organic matter, and increase and diversify crop yields. A side effect is better conditions for supporting wild biodiversity. While coffee grown in monoculture plantations with full exposure to sun have higher yields, coffee grown in the shade is far more benecial for sustainable agriculture and conserving biodiversity (Siebert 2002). Shade coffee, especially in diverse systems, can support more than twice as many species of birds as sun coffee. The more diverse systems with multiple species of trees providing shade also help support benecial insects, orchids, mammals, and other species. They also protect fragile tropical soils from erosion, providing nutrients, and suppressing weeds, thereby reducing or eliminating the need for chemical herbicides and fertilizers and thus reducing farming costs. Farmers also are able to harvest various species of fruits, rewood, lumber, and medicines from the shade trees. In agroforestry as in other uses of the land, how much biodiversity is conserved depends on the management practices applied. Knowledge limitation To develop effective means of managing biodiversity in forests and in agroforestry systems will require a robust and dynamic knowledge base from which to develop strategies and make decisions. Our present state of knowledge for this purpose is limited, though CIFOR and the World Agroforestry Centre are addressing many of the highest-priority constraints. Priorities for research should be organized around key questions that are consistent with elements of adaptive management systems. i. Landscape Management: What can landscape scale studies teach us about biodiversity management options, and is it worth continuing investment in them? Or is it better to let market forces, local people, and government policies operate without a landscape-scale vision? ii. Landscape ecology: How can diversied landscapes, with numerous different approaches to earning a living from the land, be made conducive to maintaining biodiversity while also producing a wide range of products? iii. Socioeconomics: How can livelihood security be delivered at the community level while still managing forests in the national interest? How can ecosystem service agroforest enterprises be established? What sorts of tenure systems might need to be involved? What new policies are required? How should the benets be distributed? iv. Fundamental research: How can the diversity of soil microorganisms be assessed, and how important is their diversity in terms of ecosystem functions in agroforestry systems? v. The ecology of agroforestry: What are the effects of forest regeneration when crops are grown under trees? How is recruitment affected, and what are the implications of this for biodiversity? vi. Sustainable use: How can we unravel the package of issues around sustainable use, including what are the benchmarks that need to be established for assessing and monitoring sustainable use? What are the synergies, complementarities, and conicts among the provision of the various goods and services that are potentially available from agroforests? How can the output of goods and services at the agroforest level be optimized? What are appropriate silviculture practices for multiple use that can be applied by communities? vii. Native species: How can we make greater use of native species in agroforestry and other rural development efforts, thereby enabling more of the native biodiversity to survive? viii. Invasive alien species: What are the impacts on biodiversity and ecosystem functions of invasive alien species in agroforestry systems?

Conclusions Changing circumstances are bringing about new perceptions and new demands on agroforestry. Deepened

164 understanding of the roles of trees and forests in carbon, other nutrient, climatic and water cycles will stimulate new approaches to forest management, agroforestry management and biodiversity conservation. A challenge inherent in a multiple-use approach is that outputs of forests that can be allocated by markets are relatively easy to quantify and exploit, while those that cannot be given a market value, such as biodiversity, tend to be undervalued and are therefore likely to be degraded over time. Utilitarian values as expressed through agroforestry are often in conict with strongly held romantic and symbolic values that have been referred to as myths. To many urban people today, clearing rare old-growth forests for their commodity values and subsequent conversion to agroforestry is as sensible as melting down the Eiffel Tower and selling the iron to make more automobiles. Any money yielded by such an action would be inconsequential relative to the social value of the national symbol. As nonproduct benets like biodiversity become more important to urban citizens, our social and political systems inevitably will become more prominent in forest management. The issue of whether these measures are symptoms of signicant improvements or of management systems becoming over-connected and more brittle, and therefore approaching senility, remains to be seen. Foresters increasingly are seeking diverse combinations of compatible forest uses. They are nding, for example, that conserving biodiversity and storing carbon for reducing atmospheric carbon dioxide are highly compatible forest services, and that such uses can also allow the production of nontimber forest products, the conservation of soil and water, and provision of recreation and tourism. These uses are incompatible with clear-felling, but may be compatible with well-managed agroforestry. The trend away from single-product forestry is continuing, delivering more diversity and benets for people living in and around the forests. It appears that the best way to maintain biodiversity in forest ecosystems as the 21st century begins is through a combination of strategically selected, strictly protected areas; multiple-use agroforestry areas intensively managed by local people; natural forests extensively managed by forestry professionals for sustainable production of logs and other commodities, and forest plantations intensively managed for other wood products needed by society. This diversity of approaches and uses will provide humanity with the widest range of options the greatest diversity of opportunities for adapting to the cyclical changes that are certain to continue.

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